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Potential Role of Exosomes in the Male Reproductive System

Year 2024, Volume: 9 Issue: 3, 404 - 416, 31.12.2024

Oya Korkmaz , Mustafa Numan Bucak

https://doi.org/10.51754/cusbed.1572462

Abstract

Infertility is a reproductive disorder that can affect both men and women and has become a global health problem. Approximately 50% of infertile cases are known to be caused by male reproductive disorders. Exosomes are nano-sized membrane vesicles secreted by a wide variety of cells and abundant in biological fluids, including semen. They contain lipids, proteins, microRNAs, and mRNAs and are known to play important roles in intracellular communication. Seminal exosomes mainly contain epididymosomes and prostasomes. Studies show that exosomes play a central role in regulating reproductive processes. The use of exosome therapy has significant potential in the treatment of infertility in patients. The amount of these membrane vesicles in biological fluids can be linked to physiological and pathological conditions. The molecular composition of seminal plasma and seminal exosomes, who regulates vesicle trafficking and fusion with spermatozoa, and what are the exosomal functions in sperm physiology remain unclear. This review focuses on discussing the effects of exosomes on the male reproductive system. By analysing current research findings on this topic, the knowledge on the contribution of exosomes to male reproductive health is highlighted.

Keywords

exosome male infertility spermatogenesis sertoli cell leydig cell

References

  • Aalberts, M., Stout, T. A., & Stoorvogel, W. (2013). Prostasomes: extracellular vesicles from the prostate. Reproduction (Cambridge, England), 147(1), R1–R14. https://doi.org/10.1530/REP-13-0358
  • Aalberts, M., Sostaric, E., Wubbolts, R., Wauben, M. W., Nolte-'t Hoen, E. N., Gadella, B. M., Stout, T. A., & Stoorvogel, W. (2013). Spermatozoa recruit prostasomes in response to capacitation induction. Biochimica et biophysica acta, 1834(11), 2326–2335. https://doi.org/10.1016/j.bbapap.2012.08.008
  • Admyre, C., Johansson, S. M., Qazi, K. R., Filén, J. J., Lahesmaa, R., Norman, M., Neve, E. P., Scheynius, A., & Gabrielsson, S. (2007). Exosomes with immune modulatory features are present in human breast milk. Journal of immunology (Baltimore, Md. : 1950), 179(3), 1969–1978. https://doi.org/10.4049/jimmunol.179.3.1969
  • Agarwal, A., Durairajanayagam, D., Halabi, J., Peng, J., & Vazquez-Levin, M. (2014). Proteomics, oxidative stress and male infertility. Reproductive biomedicine online, 29(1), 32–58. https://doi.org/10.1016/j.rbmo.2014.02.013
  • Ahmed, N., Yufei, H., Yang, P., Muhammad Yasir, W., Zhang, Q., Liu, T., Hong, C., Lisi, H., Xiaoya, C., & Chen, Q. (2016). Cytological study on Sertoli cells and their interactions with germ cells during annual reproductive cycle in turtle. Ecology and evolution, 6(12), 4050–4064. https://doi.org/10.1002/ece3.2193
  • Airola, M. V., & Hannun, Y. A. (2013). Sphingolipid metabolism and neutral sphingomyelinases. Handbook of experimental pharmacology, (215), 57–76. https://doi.org/10.1007/978-3-7091-1368-4_3
  • Alasmari, W., Costello, S., Correia, J., Oxenham, S. K., Morris, J., Fernandes, L., Ramalho-Santos, J., Kirkman-Brown, J., Michelangeli, F., Publicover, S., & Barratt, C. L. (2013). Ca2+ signals generated by CatSper and Ca2+ stores regulate different behaviors in human sperm. The Journal of biological chemistry, 288(9), 6248–6258. https://doi.org/10.1074/jbc.M112.439356
  • Amiri, N., Mohammadi, P., Allahgholi, A., Salek, F., & Amini, E. (2023). The potential of sertoli cells (SCs) derived exosomes and its therapeutic efficacy in male reproductive disorders. Life sciences, 312, 121251. https://doi.org/10.1016/j.lfs.2022.121251
  • Arienti, G., Carlini, E., Nicolucci, A., Cosmi, E. V., Santi, F., & Palmerini, C. A. (1999a). The motility of human spermatozoa as influenced by prostasomes at various pH levels. Biology of the Cell, 91(1), 51-54.
  • Aydos, O. S., Yukselten, Y., Ozkan, T., Ozkavukcu, S., Tuten Erdogan, M., Sunguroglu, A., & Aydos, K. (2023). Co-Culture of Cryopreserved Healthy Sertoli Cells with Testicular Tissue of Non-Obstructive Azoospermia (NOA) Patients in Culture Media Containing Follicle-Stimulating Hormone (FSH)/Testosterone Has No Advantage in Germ Cell Maturation. Journal of Clinical Medicine, 12(3), 1073. https://doi.org/10.3390/jcm12031073
  • Baskaran, S., Selvam, M. K. P., & Agarwal, A. (2020). Exosomes of male reproduction. Advances in clinical chemistry, 95, 149-163. https://doi.org/10.1016/bs.acc.2019.08.004
  • Bechoua, S., Rieu, I., Sion, B., & Grizard, G. (2011). Prostasomes as potential modulators of tyrosine phosphorylation in human spermatozoa. Systems Biology in Reproductive Medicine, 57(3), 139-148. https://doi.org/10.3109/19396368.2010.549538
  • Belleannée, C., Calvo, É., Caballero, J., & Sullivan, R. (2013). Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biology of reproduction, 89(2), 30. https://doi.org/10.1095/biolreprod.113.110486
  • Breitbart, H., Cohen, G., & Rubinstein, S. (2005). Role of actin cytoskeleton in mammalian sperm capacitation and the acrosome reaction. Reproduction (Cambridge, England), 129(3), 263–268. https://doi.org/10.1530/rep.1.00269
  • Brody, I., Ronquist, G., & Gottfries, A. (1983). Ultrastructural localization of the prostasome-an organelle in human seminal plasma. Upsala journal of medical sciences, 88(2), 63-80. https://doi.org/10.3109/03009738309178440
  • Burden, H. P., Holmes, C. H., Persad, R., & Whittington, K. (2006). Prostasomes—their effects on human male reproduction and fertility. Human reproduction update, 12(3), 283-292. https://doi.org/10.1093/humupd/dmi052
  • Caballero, J., Frenette, G., D'Amours, O., Belleannée, C., Lacroix‐Pepin, N., Robert, C., & Sullivan, R. (2012). Bovine sperm raft membrane associated glioma pathogenesis‐related 1‐like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zona pellucida. Journal of cellular physiology, 227(12), 3876-3886. https://doi.org/10.1002/jcp.24099
  • Castro, B. M., Prieto, M., & Silva, L. C. (2014). Ceramide: a simple sphingolipid with unique biophysical properties. Progress in lipid research, 54, 53-67. https://doi.org/10.1016/j.plipres.2014.01.004
  • Chabory, E., Damon, C., Lenoir, A., Kauselmann, G., Kern, H., Zevnik, B., Garrel, C., Saez, F., Cadet, R., Henry-Berger, J., Schoor, M., Gottwald, U., Habenicht, U., Drevet, J. R., & Vernet, P. (2009). Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice. The Journal of clinical investigation, 119(7), 2074–2085. https://doi.org/10.1172/JCI38940
  • Choy, K. H. K., Chan, S. Y., Lam, W., Jin, J., Zheng, T., Law, T. Y. S., Yu, S. S., Wang, W., Li, L., Xie, G., Yim, H. C. H., Chen, H., & Fok, E. K. L. (2022). The repertoire of testicular extracellular vesicle cargoes and their involvement in inter-compartmental communication associated with spermatogenesis. BMC biology, 20(1), 78. https://doi.org/10.1186/s12915-022-01268-5
  • De Lazari, F. L., Sontag, E. R., Schneider, A., Moura, A. A. A., Vasconcelos, F. R., Nagano, C. S., Mattos, R. C., Jobim, M. I. M., & Bustamante-Filho, I. C. (2019). Seminal plasma proteins and their relationship with sperm motility and morphology in boars. Andrologia, 51(4), e13222. https://doi.org/10.1111/and.13222
  • Ding, Y., Ding, N., Zhang, Y., Xie, S., Huang, M., Ding, X., Dong, W., Zhang, Q., & Jiang, L. (2021). MicroRNA-222 Transferred From Semen Extracellular Vesicles Inhibits Sperm Apoptosis by Targeting BCL2L11. Frontiers in cell and developmental biology, 9, 736864. https://doi.org/10.3389/fcell.2021.736864
  • Drabovich, A. P., Saraon, P., Jarvi, K., & Diamandis, E. P. (2014). Seminal plasma as a diagnostic fluid for male reproductive system disorders. Nature reviews. Urology, 11(5), 278–288. https://doi.org/10.1038/nrurol.2014.74
  • Du, J., Shen, J., Wang, Y., Pan, C., Pang, W., Diao, H., & Dong, W. (2016). Boar seminal plasma exosomes maintain sperm function by infiltrating into the sperm membrane. Oncotarget, 7(37), 58832–58847. https://doi.org/10.18632/oncotarget.11315
  • Duan, Y. G., Gong, J., Yeung, W. S. B., Haidl, G., & Allam, J. P. (2020). Natural killer and NKT cells in the male reproductive tract. Journal of reproductive immunology, 142, 103178. https://doi.org/10.1016/j.jri.2020.103178 Eickhoff, R., Baldauf, C., Koyro, H. W., Wennemuth, G., Suga, Y., Seitz, J., Henkel, R., & Meinhardt, A. (2004). Influence of macrophage migration inhibitory factor (MIF) on the zinc content and redox state of protein-bound sulphydryl groups in rat sperm: indications for a new role of MIF in sperm maturation. Molecular human reproduction, 10(8), 605–611. https://doi.org/10.1093/molehr/gah075
  • Esfandyari, S., Elkafas, H., Chugh, R. M., Park, H. S., Navarro, A., & Al-Hendy, A. (2021). Exosomes as biomarkers for female reproductive diseases diagnosis and therapy. International journal of molecular sciences, 22(4), 2165. https://doi.org/10.3390/ijms22042165
  • Fraser L. R. (2010). The "switching on" of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation. Molecular reproduction and development, 77(3), 197–208. https://doi.org/10.1002/mrd.21124
  • Frenette, G., Lessard, C., & Sullivan, R. (2002). Selected proteins of “prostasome-like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biology of reproduction, 67(1), 308-313. https://doi.org/10.1095/biolreprod67.1.308
  • Frenette, G., Légaré, C., Saez, F., & Sullivan, R. (2005). Macrophage migration inhibitory factor in the human epididymis and semen. Molecular human reproduction, 11(8), 575-582. https://doi.org/10.1093/molehr/gah197
  • Frenette, G., Thabet, M., & Sullivan, R. (2006). Polyol pathway in human epididymis and semen. Journal of andrology, 27(2), 233–239. https://doi.org/10.2164/jandrol.05108
  • Fornés, M. W., Barbieri, A., & Cavicchia, J. C. (1995). Morphological and enzymatic study of membrane-bound vesicles from the lumen of the rat epididymis. Andrologia, 27(1), 1–5. https://doi.org/10.1111/j.1439-0272.1995.tb02087.x
  • Gao, H., Cao, H., Li, Z., Li, L., Guo, Y., Chen, Y., Peng, G., Zeng, W., Du, J., Dong, W., & Yang, F. (2023). Exosome-derived Small RNAs in mouse Sertoli cells inhibit spermatogonial apoptosis. Theriogenology, 200, 155–167. https://doi.org/10.1016/j.theriogenology.2023.02.011
  • Gilany K, Minai-Tehrani A, Savadi-Shiraz E, Rezadoost H, Lakpour N. Exploring the human seminal plasma proteome: an unexplored gold mine of biomarker for male infertility and male reproduction disorder. J Reprod Infertil. 2015 Apr-Jun;16(2):61-71.
  • Griffiths, G. S., Miller, K. A., Galileo, D. S., & Martin-DeLeon, P. A. (2008). Murine SPAM1 is secreted by the estrous uterus and oviduct in a form that can bind to sperm during capacitation: acquisition enhances hyaluronic acid-binding ability and cumulus dispersal efficiency. Reproduction (Cambridge, England), 135(3), 293–301. https://doi.org/10.1530/REP-07-0340
  • Girouard, J., Frenette, G., & Sullivan, R. (2011). Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. International journal of andrology, 34(5 Pt 2), e475–e486. https://doi.org/10.1111/j.1365-2605.2011.01203.x
  • Goossens, E., Jahnukainen, K., Mitchell, R. T., van Pelt, A., Pennings, G., Rives, N., Poels, J., Wyns, C., Lane, S., Rodriguez-Wallberg, K. A., Rives, A., Valli-Pulaski, H., Steimer, S., Kliesch, S., Braye, A., Andres, M. M., Medrano, J., Ramos, L., Kristensen, S. G., Andersen, C. Y., … Stukenborg, J. B. (2020). Fertility preservation in boys: recent developments and new insights. Human reproduction open, 2020(3), hoaa016. https://doi.org/10.1093/hropen/hoaa016
  • Gurunathan, S., Kang, M. H., & Kim, J. H. (2021). A Comprehensive Review on Factors Influences Biogenesis, Functions, Therapeutic and Clinical Implications of Exosomes. International journal of nanomedicine, 16, 1281–1312. https://doi.org/10.2147/IJN.S291956
  • Haigler, H. T., & Christmas, P. (1990). Annexin 1 is secreted by the human prostate. Biochemical Society transactions, 18(6), 1104–1106. https://doi.org/10.1042/bst0181104
  • Houali, K., Wang, X., Shimizu, Y., Djennaoui, D., Nicholls, J., Fiorini, S., Bouguermouh, A., & Ooka, T. (2007). A new diagnostic marker for secreted Epstein-Barr virus encoded LMP1 and BARF1 oncoproteins in the serum and saliva of patients with nasopharyngeal carcinoma. Clinical cancer research : an official journal of the American Association for Cancer Research, 13(17), 4993–5000. https://doi.org/10.1158/1078-0432.CCR-06-2945
  • Ibtisham, F., Wu, J., Xiao, M., An, L., Banker, Z., Nawab, A., Zhao, Y., & Li, G. (2017). Progress and future prospect of in vitro spermatogenesis. Oncotarget, 8(39):66709-66727. https://doi.org/10.18632/oncotarget.19640 James, E. R., Carrell, D. T., Aston, K. I., Jenkins, T. G., Yeste, M., & Salas-Huetos, A. (2020). The Role of the Epididymis and the Contribution of Epididymosomes to Mammalian Reproduction. International journal of molecular sciences, 21(15), 5377. https://doi.org/10.3390/ijms21155377
  • Jodar, M., Soler-Ventura, A., Oliva, R., & Molecular Biology of Reproduction and Development Research Group (2017). Semen proteomics and male infertility. Journal of proteomics, 162, 125–134. https://doi.org/10.1016/j.jprot.2016.08.018
  • Johnson, M.H. (2018). Sperm and eggs. In Essential Reproduction, 8th ed.; Wiley Blackwell: Hoboken, NJ, USA, 183, 196.
  • Joshi, C. S., Khan, S. A., & Khole, V. V. (2014). Regulation of acrosome reaction by Liprin α3, LAR and its ligands in mouse spermatozoa. Andrology, 2(2), 165–174. https://doi.org/10.1111/j.2047-2927.2013.00167
  • Keller, S., Rupp, C., Stoeck, A., Runz, S., Fogel, M., Lugert, S., Hager, H. D., Abdel-Bakky, M. S., Gutwein, P., & Altevogt, P. (2007). CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney international, 72(9), 1095–1102. https://doi.org/10.1038/sj.ki.5002486
  • Kelly R. W. (1995). Immunosuppressive mechanisms in semen: implications for contraception. Human reproduction (Oxford, England), 10(7), 1686–1693. https://doi.org/10.1093/oxfordjournals.humrep.a136156 Kharazi, U., & Badalzadeh, R. (2020). A review on the stem cell therapy and an introduction to exosomes as a new tool in reproductive medicine. Reproductive biology, 20(4), 447–459. https://doi.org/10.1016/j.repbio.2020.07.002
  • Kirchhoff, C., & Hale, G. (1996). Cell-to-cell transfer of glycosylphosphatidylinositol-anchored membrane proteins during sperm maturation. Molecular human reproduction, 2(3), 177–184. https://doi.org/10.1093/molehr/2.3.177
  • Kitamura, M., Namiki, M., Matsumiya, K., Tanaka, K., Matsumoto, M., Hara, T., Kiyohara, H., Okabe, M., Okuyama, A., & Seya, T. (1995). Membrane cofactor protein (CD46) in seminal plasma is a prostasome-bound form with complement regulatory activity and measles virus neutralizing activity. Immunology, 84(4), 626–632. Kotaja N. (2014). MicroRNAs and spermatogenesis. Fertility and sterility, 101(6), 1552–1562. https://doi.org/10.1016/j.fertnstert.2014.04.025
  • Kowalczyk, A., Wrzecińska, M., Czerniawska-Piątkowska, E., & Kupczyński, R. (2022). Exosomes - Spectacular role in reproduction. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie, 148, 112752. https://doi.org/10.1016/j.biopha.2022.112752
  • Krapf, D., Ruan, Y.C., Wertheimer, E.V., Battistone, M.A., Pawlak, J.B., Sanjay, A., Pilder, S.H., Cuasnicu, P., Breton, S., & Visconti, P.E. (2012). cSrc is necessary for epididymal development and is incorporated into sperm during epididymal transit. Dev Biol. 369(1):43-53. https://doi.org/10.1016/j.ydbio.2012.06.017
  • Kravets, F. G., Lee, J., Singh, B., Trocchia, A., Pentyala, S. N., & Khan, S. A. (2000). Prostasomes: current concepts. The Prostate, 43(3), 169–174. https://doi.org/10.1002/(sici)1097-0045(20000515)43:3<169::aid-pros2>3.0.co;2-d
  • Kumar, A., Pandita, S., Laxmi, N. A., Bhakat, M., & Mohanty, T. K. (2019). Effects of prostasomes on functional parameters of fresh and cryopreservedthawed spermatozoa of crossbred Karan Fries (KF) bulls. Indian Journal of Animal Research, 53(9), 1167-1171. https://doi.org/10.18805/ijar.B-3665.
  • Lange-Consiglio, A., Capra, E., Monferrini, N., Canesi, S., Bosi, G., Cretich, M., Frigerio, R., Galbiati, V., Bertuzzo, F., Cobalchini, F., Cremonesi, F., & Gasparrini, B. (2022). Extracellular vesicles from seminal plasma to improve fertilizing capacity of bulls. Reproduction & fertility, 3(4), 313–327. Advance online publication. https://doi.org/10.1530/RAF-22-0037
  • Li, Q., Li, H., Liang, J., Mei, J., Cao, Z., Zhang, L., Luo, J., Tang, Y., Huang, R., Xia, H., Zhang, Q., Xiang, Q., Yang, Y., & Huang, Y. (2021). Sertoli cell-derived exosomal MicroRNA-486-5p regulates differentiation of spermatogonial stem cell through PTEN in mice. Journal of cellular and molecular medicine, 25(8), 3950–3962. https://doi.org/10.1111/jcmm.16347
  • Liang, J., Li, H., Mei, J., Cao, Z., Tang, Y., Huang, R., Xia, H., Zhang, Q., Xiang, Q., Yang, Y., & Huang, Y. (2021). Sertoli cell-derived exosome-mediated transfer of miR-145-5p inhibits Leydig cell steroidogenesis by targeting steroidogenic factor 1. Federation of american societies for experimental biology journal, 35(6):e21660. https://doi.org/10.1096/fj.202002589RRRR
  • Lin, Y., Liang, A., He, Y., Li, Z., Li, Z., Wang, G., & Sun, F. (2019). Proteomic analysis of seminal extracellular vesicle proteins involved in asthenozoospermia by iTRAQ. Molecular reproduction and development, 86(9), 1094–1105. https://doi.org/10.1002/mrd.23224
  • Ma, Y., Zhou, Y., Xiao, Q., Zou, S. S., Zhu, Y. C., Ping, P., & Chen, X. F. (2021). Seminal exosomal miR-210-3p as a potential marker of Sertoli cell damage in Varicocele. Andrology, 9(1), 451–459. https://doi.org/10.1111/andr.12913
  • Ma, Y., Zhou, Y., Zou, S. S., Sun, Y., & Chen, X. F. (2022). Exosomes released from Sertoli cells contribute to the survival of Leydig cells through CCL20 in rats Molecular human reproduction, 28(2), gaac002. https://doi.org/10.1093/molehr/gaac002
  • Machtinger, R., Laurent, L. C., & Baccarelli, A. A. (2016). Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Human reproduction update, 22(2), 182–193. https://doi.org/10.1093/humupd/dmv055
  • Martin-DeLeon P. A. (2006). Epididymal SPAM1 and its impact on sperm function. Molecular and cellular endocrinology, 250(1-2), 114–121. https://doi.org/10.1016/j.mce.2005.12.033
  • Mathivanan, S., Fahner, C. J., Reid, G. E., & Simpson, R. J. (2012). ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic acids research, 40(Database issue), D1241–D1244. https://doi.org/10.1093/nar/gkr828
  • Miksa, M., Wu, R., Dong, W., Komura, H., Amin, D., Ji, Y., Wang, Z., Wang, H., Ravikumar, T. S., Tracey, K. J., & Wang, P. (2009). Immature dendritic cell-derived exosomes rescue septic animals via milk fat globule epidermal growth factor-factor VIII [corrected]. Journal of immunology (Baltimore, Md. : 1950), 183(9), 5983–5990. https://doi.org/10.4049/jimmunol.0802994
  • Milardi, D., Grande, G., Vincenzoni, F., Messana, I., Pontecorvi, A., De Marinis, L., Castagnola, M., & Marana, R. (2012). Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertility and sterility, 97(1), 67–73.e1. https://doi.org/10.1016/j.fertnstert.2011.10.013
  • Minelli, A., Allegrucci, C., Liguori, L., & Ronquist, G. (2002). Ecto-diadenosine polyphosphates hydrolase activity on human prostasomes. The Prostate, 51(1), 1–9. https://doi.org/10.1002/pros.10062
  • Murdica, V., Giacomini, E., Alteri, A., Bartolacci, A., Cermisoni, G. C., Zarovni, N., Papaleo, E., Montorsi, F., Salonia, A., Viganò, P., & Vago, R. (2019). Seminal plasma of men with severe asthenozoospermia contain exosomes that affect spermatozoa motility and capacitation. Fertility and sterility, 111(5), 897–908.e2. https://doi.org/10.1016/j.fertnstert.2019.01.030
  • Mobarak, H., Heidarpour, M., Lolicato, F., Nouri, M., Rahbarghazi, R., & Mahdipour, M. (2019). Physiological impact of extracellular vesicles on female reproductive system; highlights to possible restorative effects on female age-related fertility. BioFactors (Oxford, England), 45(3), 293–303. https://doi.org/10.1002/biof.1497
  • Mobarak, H., Heidarpour, M., Rahbarghazi, R., Nouri, M., & Mahdipour, M. (2021). Amniotic fluid-derived exosomes improved spermatogenesis in a rat model of azoospermia. Life sciences, 274, 119336. https://doi.org/10.1016/j.lfs.2021.119336
  • Neto, F. T., Bach, P. V., Najari, B. B., Li, P. S., & Goldstein, M. (2016). Spermatogenesis in humans and its affecting factors. Seminars in cell & developmental biology, 59, 10–26. https://doi.org/10.1016/j.semcdb.2016.04.009
  • Ni, F. D., Hao, S. L., & Yang, W. X. (2019). Multiple signaling pathways in Sertoli cells: recent findings in spermatogenesis. Cell death & disease, 10(8), 541. https://doi.org/10.1038/s41419-019-1782-z
  • Nilsson, J., Skog, J., Nordstrand, A., Baranov, V., Mincheva-Nilsson, L., Breakefield, X. O., & Widmark, A. (2009). Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. British journal of cancer, 100(10), 1603–1607. https://doi.org/10.1038/sj.bjc.6605058
  • Oh, J. S., Han, C., & Cho, C. (2009). ADAM7 is associated with epididymosomes and integrated into sperm plasma membrane. Molecules and cells, 28(5), 441–446. https://doi.org/10.1007/s10059-009-0140-x
  • Oliver, E., & Stukenborg, J. B. (2020). Rebuilding the human testis in vitro. Andrology, 8(4), 825–834. https://doi.org/10.1111/andr.12710
  • Park KH, Kim BJ, Kang J, Nam TS, Lim JM, Kim HT, Park JK, Kim YG, Chae SW, Kim UH. Ca2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal. 2011 May 17;4(173):ra31.
  • Patil, S. M., Sawant, S. S., & Kunda, N. K. (2020). Exosomes as drug delivery systems: A brief overview and progress update. European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V, 154, 259–269. https://doi.org/10.1016/j.ejpb.2020.07.026
  • Paul, N., Talluri, T. R., Nag, P., & Kumaresan, A. (2021). Epididymosomes: A potential male fertility influencer. Andrologia, 53(9), e14155. https://doi.org/10.1111/and.14155
  • Pelzman, D. L., Orwig, K. E., & Hwang, K. (2020). Progress in translational reproductive science: testicular tissue transplantation and in vitro spermatogenesis. Fertility and sterility, 113(3), 500–509. https://doi.org/10.1016/j.fertnstert.2020.01.038
  • Perez-Hernandez, D., Gutiérrez-Vázquez, C., Jorge, I., López-Martín, S., Ursa, A., Sánchez-Madrid, F., Vázquez, J., & Yáñez-Mó, M. (2013). The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes. The Journal of biological chemistry, 288(17), 11649–11661. https://doi.org/10.1074/jbc.M112.445304
  • Raposo, G., Nijman, H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V., Melief, C. J., & Geuze, H. J. (1996). B lymphocytes secrete antigen-presenting vesicles. The Journal of experimental medicine, 183(3), 1161–1172. https://doi.org/10.1084/jem.183.3.1161
  • Rejraji, H., Vernet, P., & Drevet, J. R. (2002). GPX5 is present in the mouse caput and cauda epididymidis lumen at three different locations. Molecular reproduction and development, 63(1), 96–103. https://doi.org/10.1002/mrd.10136
  • Richer, G., Baert, Y., & Goossens, E. (2020). In-vitro spermatogenesis through testis modelling: Toward the generation of testicular organoids. Andrology, 8(4), 879–891. https://doi.org/10.1111/andr.12741
  • Ronquist G. (2012). Prostasomes are mediators of intercellular communication: from basic research to clinical implications. Journal of internal medicine, 271(4), 400–413. https://doi.org/10.1111/j.1365-2796.2011.02487.x
  • Ronquist, K. G., Ek, B., Morrell, J., Stavreus-Evers, A., Ström Holst, B., Humblot, P., Ronquist, G., & Larsson, A. (2013). Prostasomes from four different species are able to produce extracellular adenosine triphosphate (ATP). Biochimica et biophysica acta, 1830(10), 4604–4610. https://doi.org/10.1016/j.bbagen.2013.05.019
  • Ronquist, K. G., Sanchez, C., Dubois, L., Chioureas, D., Fonseca, P., Larsson, A., Ullén, A., Yachnin, J., Ronquist, G., & Panaretakis, T. (2016). Energy-requiring uptake of prostasomes and PC3 cell-derived exosomes into non-malignant and malignant cells. Journal of extracellular vesicles, 5, 29877. https://doi.org/10.3402/jev.v5.29877
  • Rowlison, T., Cleland, T. P., Ottinger, M. A., & Comizzoli, P. (2020). Novel Proteomic Profiling of Epididymal Extracellular Vesicles in the Domestic Cat Reveals Proteins Related to Sequential Sperm Maturation with Differences Observed between Normospermic and Teratospermic Individuals. Molecular & cellular proteomics : MCP, 19(12), 2090–2104. https://doi.org/10.1074/mcp.RA120.002251
  • Salek, F., Baharara, J., Shahrokhabadi, K. N., & Amini, E. (2021). The guardians of germ cells; Sertoli-derived exosomes against electromagnetic field-induced oxidative stress in mouse spermatogonial stem cells. Theriogenology, 173, 112–122. https://doi.org/10.1016/j.theriogenology.2021.08.001
  • Samanta, L., Parida, R., Dias, T. R., & Agarwal, A. (2018). The enigmatic seminal plasma: a proteomics insight from ejaculation to fertilization. Reproductive biology and endocrinology : RB&E, 16(1), 41. https://doi.org/10.1186/s12958-018-0358-6
  • Schlatt, S., & Ehmcke, J. (2014). Regulation of spermatogenesis: an evolutionary biologist's perspective. Seminars in cell & developmental biology, 29, 2–16. https://doi.org/10.1016/j.semcdb.2014.03.007 Sherif, I. O., Sabry, D., Abdel-Aziz, A., & Sarhan, O. M. (2018). The role of mesenchymal stem cells in chemotherapy-induced gonadotoxicity. Stem cell research & therapy, 9(1), 196. https://doi.org/10.1186/s13287-018-0946-6
  • Sinha, D., Roy, S., Saha, P., Chatterjee, N., & Bishayee, A. (2021). Trends in Research on Exosomes in Cancer Progression and Anticancer Therapy. Cancers, 13(2), 326. https://doi.org/10.3390/cancers13020326
  • Skibinski, G., Kelly, R. W., Harkiss, D., & James, K. (1992). Immunosuppression by human seminal plasma--extracellular organelles (prostasomes) modulate activity of phagocytic cells. American journal of reproductive immunology (New York, N.Y. : 1989), 28(2), 97–103. https://doi.org/10.1111/j.1600-0897.1992.tb00767.x
  • Skryabin, G. O., Komelkov, A. V., Savelyeva, E. E., & Tchevkina, E. M. (2020). Lipid Rafts in Exosome Biogenesis. Biochemistry. Biokhimiia, 85(2), 177–191. https://doi.org/10.1134/S0006297920020054
  • Sousa, C., Pereira, I., Santos, A. C., Carbone, C., Kovačević, A. B., Silva, A. M., & Souto, E. B. (2017). Targeting dendritic cells for the treatment of autoimmune disorders. Colloids and surfaces. B, Biointerfaces, 158, 237–248. https://doi.org/10.1016/j.colsurfb.2017.06.050
  • Sullivan R. (2016). Epididymosomes: Role of extracellular microvesicles in sperm maturation. Frontiers in bioscience (Scholar edition), 8(1), 106–114. https://doi.org/10.2741/s450
  • Sullivan, R., & Saez, F. (2013). Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction (Cambridge, England), 146(1), R21–R35. https://doi.org/10.1530/REP-13-0058
  • Sullivan, R., Saez, F., Girouard, J., & Frenette, G. (2005). Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood cells, molecules & diseases, 35(1), 1–10. https://doi.org/10.1016/j.bcmd.2005.03.005
  • Sullivan, R., & Saez, F. (2013). Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction (Cambridge, England), 146(1), R21–R35. https://doi.org/10.1530/REP-13-0058
  • Tamessar, C. T., Trigg, N. A., Nixon, B., Skerrett-Byrne, D. A., Sharkey, D. J., Robertson, S. A., Bromfield, E. G., & Schjenken, J. E. (2021). Roles of male reproductive tract extracellular vesicles in reproduction. American journal of reproductive immunology (New York, N.Y. : 1989), 85(2), e13338. https://doi.org/10.1111/aji.13338
  • Tannetta, D., Dragovic, R., Alyahyaei, Z., & Southcombe, J. (2014). Extracellular vesicles and reproduction-promotion of successful pregnancy. Cellular & molecular immunology, 11(6), 548–563. https://doi.org/10.1038/cmi.2014.42
  • Tarazona, R., Delgado, E., Guarnizo, M. C., Roncero, R. G., Morgado, S., Sánchez-Correa, B., Gordillo, J. J., Dejulián, J., & Casado, J. G. (2011). Human prostasomes express CD48 and interfere with NK cell function. Immunobiology, 216(1-2), 41–46. https://doi.org/10.1016/j.imbio.2010.03.002
  • Thiageswaran, S., Steele, H., Voigt, A. L., & Dobrinski, I. (2022). A Role for Exchange of Extracellular Vesicles in Porcine Spermatogonial Co-Culture. International journal of molecular sciences, 23(9), 4535. https://doi.org/10.3390/ijms23094535
  • Thimon, V., Frenette, G., Saez, F., Thabet, M., & Sullivan, R. (2008). Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. Human reproduction (Oxford, England), 23(8), 1698–1707. https://doi.org/10.1093/humrep/den181
  • Tran, K. T. D., Valli-Pulaski, H., Colvin, A., & Orwig, K. E. (2022). Male fertility preservation and restoration strategies for patients undergoing gonadotoxic therapies†. Biology of reproduction, 107(2), 382–405. https://doi.org/10.1093/biolre/ioac072
  • Utleg, A. G., Yi, E. C., Xie, T., Shannon, P., White, J. T., Goodlett, D. R., Hood, L., & Lin, B. (2003). Proteomic analysis of human prostasomes. The Prostate, 56(2), 150–161. https://doi.org/10.1002/pros.10255
  • Van den Boorn, J. G., Dassler, J., Coch, C., Schlee, M., & Hartmann, G. (2013). Exosomes as nucleic acid nanocarriers. Advanced drug delivery reviews, 65(3), 331–335. https://doi.org/10.1016/j.addr.2012.06.011
  • Vasan S. S. (2011). Semen analysis and sperm function tests: How much to test?. Indian journal of urology : IJU : journal of the Urological Society of India, 27(1), 41–48. https://doi.org/10.4103/0970-1591.78424
  • Vernet, P., Aitken, R. J., & Drevet, J. R. (2004). Antioxidant strategies in the epididymis. Molecular and cellular endocrinology, 216(1-2), 31–39. https://doi.org/10.1016/j.mce.2003.10.069
  • Vickram, A. S., Srikumar, P. S., Srinivasan, S., Jeyanthi, P., Anbarasu, K., Thanigaivel, S., Nibedita, D., Jenila Rani, D., & Rohini, K. (2021). Seminal exosomes - An important biological marker for various disorders and syndrome in human reproduction. Saudi journal of biological sciences, 28(6), 3607–3615. https://doi.org/10.1016/j.sjbs.2021.03.038
  • Vickram, A. S., Anbarasu, K., Gulothungan, G., Thanigaivel, S., Nanmaran, R., & Palanivelu, J. (2022). Characterization of human prostasomes protein Clusterin (macromolecule) - a novel biomarker for male infertility diagnosis and prognosis. Journal of biomolecular structure & dynamics, 40(9), 3979–3988. https://doi.org/10.1080/07391102.2020.1852960
  • Vickram, A. S., Srikumar, P. S., Srinivasan, S., Jeyanthi, P., Anbarasu, K., Thanigaivel, S., Nibedita, D., Jenila Rani, D., & Rohini, K. (2021). Seminal exosomes - An important biological marker for various disorders and syndrome in human reproduction. Saudi journal of biological sciences, 28(6), 3607–3615. https://doi.org/10.1016/j.sjbs.2021.03.038
  • Vivacqua, A., Siciliano, L., Sabato, M., Palma, A., & Carpino, A. (2004). Prostasomes as zinc ligands in human seminal plasma. International journal of andrology, 27(1), 27–31. https://doi.org/10.1111/j.1365-2605.2004.00441.x
  • Wang, G. J., Liu, Y., Qin, A., Shah, S. V., Deng, Z. B., Xiang, X., Cheng, Z., Liu, C., Wang, J., Zhang, L., Grizzle, W. E., & Zhang, H. G. (2008). Thymus exosomes-like particles induce regulatory T cells. Journal of immunology (Baltimore, Md. : 1950), 181(8), 5242–5248. https://doi.org/10.4049/jimmunol.181.8.5242
  • Wang, B., Zhai, C., Li, Y., Ma, B., Li, Z., & Wang, J. (2023). Sertoli cells-derived exosomal miR-30a-5p regulates ubiquitin E3 ligase Zeb2 to affect the spermatogonial stem cells proliferation and differentiation. Reproductive toxicology (Elmsford, N.Y.), 117, 108340. https://doi.org/10.1016/j.reprotox.2023.108340
  • World Health Organization (WHO). WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 4th ed.; Cambridge University Press: New York, NY, USA, 1999. Yellon, D. M., & Davidson, S. M. (2014). Exosomes: nanoparticles involved in cardioprotection?. Circulation research, 114(2), 325–332. https://doi.org/10.1161/CIRCRESAHA.113.300636
  • Zakharova, L., Svetlova, M., & Fomina, A. F. (2007). T cell exosomes induce cholesterol accumulation in human monocytes via phosphatidylserine receptor. Journal of cellular physiology, 212(1), 174–181. https://doi.org/10.1002/jcp.21013
  • Quadri, Z., Elsherbini, A., & Bieberich, E. (2022). Extracellular vesicles in pharmacology: Novel approaches in diagnostics and therapy. Pharmacological research, 175, 105980. https://doi.org/10.1016/j.phrs.2021.105980
  • Yang, C., Guo, W. B., Zhang, W. S., Bian, J., Yang, J. K., Zhou, Q. Z., Chen, M. K., Peng, W., Qi, T., Wang, C. Y., & Liu, C. D. (2017). Comprehensive proteomics analysis of exosomes derived from human seminal plasma. Andrology, 5(5), 1007–1015. https://doi.org/10.1111/andr.12412
  • Yeung, C. H., Cooper, T. G., Schröter, S., Kirchhoff, C., & Nieschlag, E. (1998). Epididymal secretion of CD52 as measured in human seminal plasma by a fluorescence immunoassay. Molecular human reproduction, 4(5), 447–451. https://doi.org/10.1093/molehr/4.5.447
  • Yu, K., Xiao, K., Sun, Q. Q., Liu, R. F., Huang, L. F., Zhang, P. F., Xu, H. Y., Lu, Y. Q., & Fu, Q. (2023). Comparative proteomic analysis of seminal plasma exosomes in buffalo with high and low sperm motility. BMC genomics, 24(1), 8. https://doi.org/10.1186/s12864-022-09106-2
  • Yue, D., Yang, R., Xiong, C., & Yang, R. (2022). Functional prediction and profiling of exosomal circRNAs derived from seminal plasma for the diagnosis and treatment of oligoasthenospermia. Experimental and therapeutic medicine, 24(5), 649. https://doi.org/10.3892/etm.2022.11586

Erkek Üreme Sisteminde Eksozomların Potansiyel Rolü

Year 2024, Volume: 9 Issue: 3, 404 - 416, 31.12.2024

Oya Korkmaz , Mustafa Numan Bucak

https://doi.org/10.51754/cusbed.1572462

Abstract

İnfertilite hem erkekler de hem de kadınlarda görülebilen bir üreme sistemi bozukluğudur ve küresel bir sağlık sorunu haline gelmiştir. İnfertil vakaların yaklaşık %50'sinin erkek üreme bozukluklarından kaynaklandığı bilinmektedir. Eksozomlar, çok çeşitli hücreler tarafından salgılanan ve semen de dahil olmak üzere biyolojik sıvılarda bol miktarda bulunan nano boyutlu membran vezikülleridir. Lipidler, proteinler, mikroRNA'lar ve mRNA'lar içerirler ve hücre içi iletişimde önemli rol oynadıkları bilinmektedir. Seminal eksozomlar esas olarak epididimozomları ve prostasomları içerir. Yapılan çalışmalar, eksozomların üreme süreçlerini düzenlemede merkezi bir rol oynadığını göstermektedir. Eksozom tedavisinin kullanımı, hastalarda infertilite tedavisinde önemli bir potansiyele sahiptir. Bu membran veziküllerin biyolojik sıvılardaki miktarı, fizyolojik ve patolojik durumlarla bağlantılı olabilir. Seminal plazmanın ve seminal eksozomların moleküler bileşimi, vezikül trafiği ve spermatozoa ile füzyonunu kimin düzenlediği ve sperm fizyolojisindeki eksozomal işlevlerin neler olduğu hala belirsizliğini korumaya devam etmektedir. Bu derleme, eksozomların erkek üreme sistemi üzerindeki etkilerini tartışmaya odaklanmaktadır. Bu konudaki güncel araştırma bulguları analiz edilerek, erkek üreme sağlığı üzerindeki eksozomların katkısı hakkındaki bilgiler vurgulanmaktadır.

Keywords

eksozom erkek infertilitesi spermatogenez sertoli hücresi leydig hücresi

Ethical Statement

Bu derleme makalesi etik kurul onayı gerektirmemektedir.

Supporting Institution

Yok.

Thanks

Yok.

References

  • Aalberts, M., Stout, T. A., & Stoorvogel, W. (2013). Prostasomes: extracellular vesicles from the prostate. Reproduction (Cambridge, England), 147(1), R1–R14. https://doi.org/10.1530/REP-13-0358
  • Aalberts, M., Sostaric, E., Wubbolts, R., Wauben, M. W., Nolte-'t Hoen, E. N., Gadella, B. M., Stout, T. A., & Stoorvogel, W. (2013). Spermatozoa recruit prostasomes in response to capacitation induction. Biochimica et biophysica acta, 1834(11), 2326–2335. https://doi.org/10.1016/j.bbapap.2012.08.008
  • Admyre, C., Johansson, S. M., Qazi, K. R., Filén, J. J., Lahesmaa, R., Norman, M., Neve, E. P., Scheynius, A., & Gabrielsson, S. (2007). Exosomes with immune modulatory features are present in human breast milk. Journal of immunology (Baltimore, Md. : 1950), 179(3), 1969–1978. https://doi.org/10.4049/jimmunol.179.3.1969
  • Agarwal, A., Durairajanayagam, D., Halabi, J., Peng, J., & Vazquez-Levin, M. (2014). Proteomics, oxidative stress and male infertility. Reproductive biomedicine online, 29(1), 32–58. https://doi.org/10.1016/j.rbmo.2014.02.013
  • Ahmed, N., Yufei, H., Yang, P., Muhammad Yasir, W., Zhang, Q., Liu, T., Hong, C., Lisi, H., Xiaoya, C., & Chen, Q. (2016). Cytological study on Sertoli cells and their interactions with germ cells during annual reproductive cycle in turtle. Ecology and evolution, 6(12), 4050–4064. https://doi.org/10.1002/ece3.2193
  • Airola, M. V., & Hannun, Y. A. (2013). Sphingolipid metabolism and neutral sphingomyelinases. Handbook of experimental pharmacology, (215), 57–76. https://doi.org/10.1007/978-3-7091-1368-4_3
  • Alasmari, W., Costello, S., Correia, J., Oxenham, S. K., Morris, J., Fernandes, L., Ramalho-Santos, J., Kirkman-Brown, J., Michelangeli, F., Publicover, S., & Barratt, C. L. (2013). Ca2+ signals generated by CatSper and Ca2+ stores regulate different behaviors in human sperm. The Journal of biological chemistry, 288(9), 6248–6258. https://doi.org/10.1074/jbc.M112.439356
  • Amiri, N., Mohammadi, P., Allahgholi, A., Salek, F., & Amini, E. (2023). The potential of sertoli cells (SCs) derived exosomes and its therapeutic efficacy in male reproductive disorders. Life sciences, 312, 121251. https://doi.org/10.1016/j.lfs.2022.121251
  • Arienti, G., Carlini, E., Nicolucci, A., Cosmi, E. V., Santi, F., & Palmerini, C. A. (1999a). The motility of human spermatozoa as influenced by prostasomes at various pH levels. Biology of the Cell, 91(1), 51-54.
  • Aydos, O. S., Yukselten, Y., Ozkan, T., Ozkavukcu, S., Tuten Erdogan, M., Sunguroglu, A., & Aydos, K. (2023). Co-Culture of Cryopreserved Healthy Sertoli Cells with Testicular Tissue of Non-Obstructive Azoospermia (NOA) Patients in Culture Media Containing Follicle-Stimulating Hormone (FSH)/Testosterone Has No Advantage in Germ Cell Maturation. Journal of Clinical Medicine, 12(3), 1073. https://doi.org/10.3390/jcm12031073
  • Baskaran, S., Selvam, M. K. P., & Agarwal, A. (2020). Exosomes of male reproduction. Advances in clinical chemistry, 95, 149-163. https://doi.org/10.1016/bs.acc.2019.08.004
  • Bechoua, S., Rieu, I., Sion, B., & Grizard, G. (2011). Prostasomes as potential modulators of tyrosine phosphorylation in human spermatozoa. Systems Biology in Reproductive Medicine, 57(3), 139-148. https://doi.org/10.3109/19396368.2010.549538
  • Belleannée, C., Calvo, É., Caballero, J., & Sullivan, R. (2013). Epididymosomes convey different repertoires of microRNAs throughout the bovine epididymis. Biology of reproduction, 89(2), 30. https://doi.org/10.1095/biolreprod.113.110486
  • Breitbart, H., Cohen, G., & Rubinstein, S. (2005). Role of actin cytoskeleton in mammalian sperm capacitation and the acrosome reaction. Reproduction (Cambridge, England), 129(3), 263–268. https://doi.org/10.1530/rep.1.00269
  • Brody, I., Ronquist, G., & Gottfries, A. (1983). Ultrastructural localization of the prostasome-an organelle in human seminal plasma. Upsala journal of medical sciences, 88(2), 63-80. https://doi.org/10.3109/03009738309178440
  • Burden, H. P., Holmes, C. H., Persad, R., & Whittington, K. (2006). Prostasomes—their effects on human male reproduction and fertility. Human reproduction update, 12(3), 283-292. https://doi.org/10.1093/humupd/dmi052
  • Caballero, J., Frenette, G., D'Amours, O., Belleannée, C., Lacroix‐Pepin, N., Robert, C., & Sullivan, R. (2012). Bovine sperm raft membrane associated glioma pathogenesis‐related 1‐like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zona pellucida. Journal of cellular physiology, 227(12), 3876-3886. https://doi.org/10.1002/jcp.24099
  • Castro, B. M., Prieto, M., & Silva, L. C. (2014). Ceramide: a simple sphingolipid with unique biophysical properties. Progress in lipid research, 54, 53-67. https://doi.org/10.1016/j.plipres.2014.01.004
  • Chabory, E., Damon, C., Lenoir, A., Kauselmann, G., Kern, H., Zevnik, B., Garrel, C., Saez, F., Cadet, R., Henry-Berger, J., Schoor, M., Gottwald, U., Habenicht, U., Drevet, J. R., & Vernet, P. (2009). Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice. The Journal of clinical investigation, 119(7), 2074–2085. https://doi.org/10.1172/JCI38940
  • Choy, K. H. K., Chan, S. Y., Lam, W., Jin, J., Zheng, T., Law, T. Y. S., Yu, S. S., Wang, W., Li, L., Xie, G., Yim, H. C. H., Chen, H., & Fok, E. K. L. (2022). The repertoire of testicular extracellular vesicle cargoes and their involvement in inter-compartmental communication associated with spermatogenesis. BMC biology, 20(1), 78. https://doi.org/10.1186/s12915-022-01268-5
  • De Lazari, F. L., Sontag, E. R., Schneider, A., Moura, A. A. A., Vasconcelos, F. R., Nagano, C. S., Mattos, R. C., Jobim, M. I. M., & Bustamante-Filho, I. C. (2019). Seminal plasma proteins and their relationship with sperm motility and morphology in boars. Andrologia, 51(4), e13222. https://doi.org/10.1111/and.13222
  • Ding, Y., Ding, N., Zhang, Y., Xie, S., Huang, M., Ding, X., Dong, W., Zhang, Q., & Jiang, L. (2021). MicroRNA-222 Transferred From Semen Extracellular Vesicles Inhibits Sperm Apoptosis by Targeting BCL2L11. Frontiers in cell and developmental biology, 9, 736864. https://doi.org/10.3389/fcell.2021.736864
  • Drabovich, A. P., Saraon, P., Jarvi, K., & Diamandis, E. P. (2014). Seminal plasma as a diagnostic fluid for male reproductive system disorders. Nature reviews. Urology, 11(5), 278–288. https://doi.org/10.1038/nrurol.2014.74
  • Du, J., Shen, J., Wang, Y., Pan, C., Pang, W., Diao, H., & Dong, W. (2016). Boar seminal plasma exosomes maintain sperm function by infiltrating into the sperm membrane. Oncotarget, 7(37), 58832–58847. https://doi.org/10.18632/oncotarget.11315
  • Duan, Y. G., Gong, J., Yeung, W. S. B., Haidl, G., & Allam, J. P. (2020). Natural killer and NKT cells in the male reproductive tract. Journal of reproductive immunology, 142, 103178. https://doi.org/10.1016/j.jri.2020.103178 Eickhoff, R., Baldauf, C., Koyro, H. W., Wennemuth, G., Suga, Y., Seitz, J., Henkel, R., & Meinhardt, A. (2004). Influence of macrophage migration inhibitory factor (MIF) on the zinc content and redox state of protein-bound sulphydryl groups in rat sperm: indications for a new role of MIF in sperm maturation. Molecular human reproduction, 10(8), 605–611. https://doi.org/10.1093/molehr/gah075
  • Esfandyari, S., Elkafas, H., Chugh, R. M., Park, H. S., Navarro, A., & Al-Hendy, A. (2021). Exosomes as biomarkers for female reproductive diseases diagnosis and therapy. International journal of molecular sciences, 22(4), 2165. https://doi.org/10.3390/ijms22042165
  • Fraser L. R. (2010). The "switching on" of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation. Molecular reproduction and development, 77(3), 197–208. https://doi.org/10.1002/mrd.21124
  • Frenette, G., Lessard, C., & Sullivan, R. (2002). Selected proteins of “prostasome-like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biology of reproduction, 67(1), 308-313. https://doi.org/10.1095/biolreprod67.1.308
  • Frenette, G., Légaré, C., Saez, F., & Sullivan, R. (2005). Macrophage migration inhibitory factor in the human epididymis and semen. Molecular human reproduction, 11(8), 575-582. https://doi.org/10.1093/molehr/gah197
  • Frenette, G., Thabet, M., & Sullivan, R. (2006). Polyol pathway in human epididymis and semen. Journal of andrology, 27(2), 233–239. https://doi.org/10.2164/jandrol.05108
  • Fornés, M. W., Barbieri, A., & Cavicchia, J. C. (1995). Morphological and enzymatic study of membrane-bound vesicles from the lumen of the rat epididymis. Andrologia, 27(1), 1–5. https://doi.org/10.1111/j.1439-0272.1995.tb02087.x
  • Gao, H., Cao, H., Li, Z., Li, L., Guo, Y., Chen, Y., Peng, G., Zeng, W., Du, J., Dong, W., & Yang, F. (2023). Exosome-derived Small RNAs in mouse Sertoli cells inhibit spermatogonial apoptosis. Theriogenology, 200, 155–167. https://doi.org/10.1016/j.theriogenology.2023.02.011
  • Gilany K, Minai-Tehrani A, Savadi-Shiraz E, Rezadoost H, Lakpour N. Exploring the human seminal plasma proteome: an unexplored gold mine of biomarker for male infertility and male reproduction disorder. J Reprod Infertil. 2015 Apr-Jun;16(2):61-71.
  • Griffiths, G. S., Miller, K. A., Galileo, D. S., & Martin-DeLeon, P. A. (2008). Murine SPAM1 is secreted by the estrous uterus and oviduct in a form that can bind to sperm during capacitation: acquisition enhances hyaluronic acid-binding ability and cumulus dispersal efficiency. Reproduction (Cambridge, England), 135(3), 293–301. https://doi.org/10.1530/REP-07-0340
  • Girouard, J., Frenette, G., & Sullivan, R. (2011). Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. International journal of andrology, 34(5 Pt 2), e475–e486. https://doi.org/10.1111/j.1365-2605.2011.01203.x
  • Goossens, E., Jahnukainen, K., Mitchell, R. T., van Pelt, A., Pennings, G., Rives, N., Poels, J., Wyns, C., Lane, S., Rodriguez-Wallberg, K. A., Rives, A., Valli-Pulaski, H., Steimer, S., Kliesch, S., Braye, A., Andres, M. M., Medrano, J., Ramos, L., Kristensen, S. G., Andersen, C. Y., … Stukenborg, J. B. (2020). Fertility preservation in boys: recent developments and new insights. Human reproduction open, 2020(3), hoaa016. https://doi.org/10.1093/hropen/hoaa016
  • Gurunathan, S., Kang, M. H., & Kim, J. H. (2021). A Comprehensive Review on Factors Influences Biogenesis, Functions, Therapeutic and Clinical Implications of Exosomes. International journal of nanomedicine, 16, 1281–1312. https://doi.org/10.2147/IJN.S291956
  • Haigler, H. T., & Christmas, P. (1990). Annexin 1 is secreted by the human prostate. Biochemical Society transactions, 18(6), 1104–1106. https://doi.org/10.1042/bst0181104
  • Houali, K., Wang, X., Shimizu, Y., Djennaoui, D., Nicholls, J., Fiorini, S., Bouguermouh, A., & Ooka, T. (2007). A new diagnostic marker for secreted Epstein-Barr virus encoded LMP1 and BARF1 oncoproteins in the serum and saliva of patients with nasopharyngeal carcinoma. Clinical cancer research : an official journal of the American Association for Cancer Research, 13(17), 4993–5000. https://doi.org/10.1158/1078-0432.CCR-06-2945
  • Ibtisham, F., Wu, J., Xiao, M., An, L., Banker, Z., Nawab, A., Zhao, Y., & Li, G. (2017). Progress and future prospect of in vitro spermatogenesis. Oncotarget, 8(39):66709-66727. https://doi.org/10.18632/oncotarget.19640 James, E. R., Carrell, D. T., Aston, K. I., Jenkins, T. G., Yeste, M., & Salas-Huetos, A. (2020). The Role of the Epididymis and the Contribution of Epididymosomes to Mammalian Reproduction. International journal of molecular sciences, 21(15), 5377. https://doi.org/10.3390/ijms21155377
  • Jodar, M., Soler-Ventura, A., Oliva, R., & Molecular Biology of Reproduction and Development Research Group (2017). Semen proteomics and male infertility. Journal of proteomics, 162, 125–134. https://doi.org/10.1016/j.jprot.2016.08.018
  • Johnson, M.H. (2018). Sperm and eggs. In Essential Reproduction, 8th ed.; Wiley Blackwell: Hoboken, NJ, USA, 183, 196.
  • Joshi, C. S., Khan, S. A., & Khole, V. V. (2014). Regulation of acrosome reaction by Liprin α3, LAR and its ligands in mouse spermatozoa. Andrology, 2(2), 165–174. https://doi.org/10.1111/j.2047-2927.2013.00167
  • Keller, S., Rupp, C., Stoeck, A., Runz, S., Fogel, M., Lugert, S., Hager, H. D., Abdel-Bakky, M. S., Gutwein, P., & Altevogt, P. (2007). CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney international, 72(9), 1095–1102. https://doi.org/10.1038/sj.ki.5002486
  • Kelly R. W. (1995). Immunosuppressive mechanisms in semen: implications for contraception. Human reproduction (Oxford, England), 10(7), 1686–1693. https://doi.org/10.1093/oxfordjournals.humrep.a136156 Kharazi, U., & Badalzadeh, R. (2020). A review on the stem cell therapy and an introduction to exosomes as a new tool in reproductive medicine. Reproductive biology, 20(4), 447–459. https://doi.org/10.1016/j.repbio.2020.07.002
  • Kirchhoff, C., & Hale, G. (1996). Cell-to-cell transfer of glycosylphosphatidylinositol-anchored membrane proteins during sperm maturation. Molecular human reproduction, 2(3), 177–184. https://doi.org/10.1093/molehr/2.3.177
  • Kitamura, M., Namiki, M., Matsumiya, K., Tanaka, K., Matsumoto, M., Hara, T., Kiyohara, H., Okabe, M., Okuyama, A., & Seya, T. (1995). Membrane cofactor protein (CD46) in seminal plasma is a prostasome-bound form with complement regulatory activity and measles virus neutralizing activity. Immunology, 84(4), 626–632. Kotaja N. (2014). MicroRNAs and spermatogenesis. Fertility and sterility, 101(6), 1552–1562. https://doi.org/10.1016/j.fertnstert.2014.04.025
  • Kowalczyk, A., Wrzecińska, M., Czerniawska-Piątkowska, E., & Kupczyński, R. (2022). Exosomes - Spectacular role in reproduction. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie, 148, 112752. https://doi.org/10.1016/j.biopha.2022.112752
  • Krapf, D., Ruan, Y.C., Wertheimer, E.V., Battistone, M.A., Pawlak, J.B., Sanjay, A., Pilder, S.H., Cuasnicu, P., Breton, S., & Visconti, P.E. (2012). cSrc is necessary for epididymal development and is incorporated into sperm during epididymal transit. Dev Biol. 369(1):43-53. https://doi.org/10.1016/j.ydbio.2012.06.017
  • Kravets, F. G., Lee, J., Singh, B., Trocchia, A., Pentyala, S. N., & Khan, S. A. (2000). Prostasomes: current concepts. The Prostate, 43(3), 169–174. https://doi.org/10.1002/(sici)1097-0045(20000515)43:3<169::aid-pros2>3.0.co;2-d
  • Kumar, A., Pandita, S., Laxmi, N. A., Bhakat, M., & Mohanty, T. K. (2019). Effects of prostasomes on functional parameters of fresh and cryopreservedthawed spermatozoa of crossbred Karan Fries (KF) bulls. Indian Journal of Animal Research, 53(9), 1167-1171. https://doi.org/10.18805/ijar.B-3665.
  • Lange-Consiglio, A., Capra, E., Monferrini, N., Canesi, S., Bosi, G., Cretich, M., Frigerio, R., Galbiati, V., Bertuzzo, F., Cobalchini, F., Cremonesi, F., & Gasparrini, B. (2022). Extracellular vesicles from seminal plasma to improve fertilizing capacity of bulls. Reproduction & fertility, 3(4), 313–327. Advance online publication. https://doi.org/10.1530/RAF-22-0037
  • Li, Q., Li, H., Liang, J., Mei, J., Cao, Z., Zhang, L., Luo, J., Tang, Y., Huang, R., Xia, H., Zhang, Q., Xiang, Q., Yang, Y., & Huang, Y. (2021). Sertoli cell-derived exosomal MicroRNA-486-5p regulates differentiation of spermatogonial stem cell through PTEN in mice. Journal of cellular and molecular medicine, 25(8), 3950–3962. https://doi.org/10.1111/jcmm.16347
  • Liang, J., Li, H., Mei, J., Cao, Z., Tang, Y., Huang, R., Xia, H., Zhang, Q., Xiang, Q., Yang, Y., & Huang, Y. (2021). Sertoli cell-derived exosome-mediated transfer of miR-145-5p inhibits Leydig cell steroidogenesis by targeting steroidogenic factor 1. Federation of american societies for experimental biology journal, 35(6):e21660. https://doi.org/10.1096/fj.202002589RRRR
  • Lin, Y., Liang, A., He, Y., Li, Z., Li, Z., Wang, G., & Sun, F. (2019). Proteomic analysis of seminal extracellular vesicle proteins involved in asthenozoospermia by iTRAQ. Molecular reproduction and development, 86(9), 1094–1105. https://doi.org/10.1002/mrd.23224
  • Ma, Y., Zhou, Y., Xiao, Q., Zou, S. S., Zhu, Y. C., Ping, P., & Chen, X. F. (2021). Seminal exosomal miR-210-3p as a potential marker of Sertoli cell damage in Varicocele. Andrology, 9(1), 451–459. https://doi.org/10.1111/andr.12913
  • Ma, Y., Zhou, Y., Zou, S. S., Sun, Y., & Chen, X. F. (2022). Exosomes released from Sertoli cells contribute to the survival of Leydig cells through CCL20 in rats Molecular human reproduction, 28(2), gaac002. https://doi.org/10.1093/molehr/gaac002
  • Machtinger, R., Laurent, L. C., & Baccarelli, A. A. (2016). Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation. Human reproduction update, 22(2), 182–193. https://doi.org/10.1093/humupd/dmv055
  • Martin-DeLeon P. A. (2006). Epididymal SPAM1 and its impact on sperm function. Molecular and cellular endocrinology, 250(1-2), 114–121. https://doi.org/10.1016/j.mce.2005.12.033
  • Mathivanan, S., Fahner, C. J., Reid, G. E., & Simpson, R. J. (2012). ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic acids research, 40(Database issue), D1241–D1244. https://doi.org/10.1093/nar/gkr828
  • Miksa, M., Wu, R., Dong, W., Komura, H., Amin, D., Ji, Y., Wang, Z., Wang, H., Ravikumar, T. S., Tracey, K. J., & Wang, P. (2009). Immature dendritic cell-derived exosomes rescue septic animals via milk fat globule epidermal growth factor-factor VIII [corrected]. Journal of immunology (Baltimore, Md. : 1950), 183(9), 5983–5990. https://doi.org/10.4049/jimmunol.0802994
  • Milardi, D., Grande, G., Vincenzoni, F., Messana, I., Pontecorvi, A., De Marinis, L., Castagnola, M., & Marana, R. (2012). Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertility and sterility, 97(1), 67–73.e1. https://doi.org/10.1016/j.fertnstert.2011.10.013
  • Minelli, A., Allegrucci, C., Liguori, L., & Ronquist, G. (2002). Ecto-diadenosine polyphosphates hydrolase activity on human prostasomes. The Prostate, 51(1), 1–9. https://doi.org/10.1002/pros.10062
  • Murdica, V., Giacomini, E., Alteri, A., Bartolacci, A., Cermisoni, G. C., Zarovni, N., Papaleo, E., Montorsi, F., Salonia, A., Viganò, P., & Vago, R. (2019). Seminal plasma of men with severe asthenozoospermia contain exosomes that affect spermatozoa motility and capacitation. Fertility and sterility, 111(5), 897–908.e2. https://doi.org/10.1016/j.fertnstert.2019.01.030
  • Mobarak, H., Heidarpour, M., Lolicato, F., Nouri, M., Rahbarghazi, R., & Mahdipour, M. (2019). Physiological impact of extracellular vesicles on female reproductive system; highlights to possible restorative effects on female age-related fertility. BioFactors (Oxford, England), 45(3), 293–303. https://doi.org/10.1002/biof.1497
  • Mobarak, H., Heidarpour, M., Rahbarghazi, R., Nouri, M., & Mahdipour, M. (2021). Amniotic fluid-derived exosomes improved spermatogenesis in a rat model of azoospermia. Life sciences, 274, 119336. https://doi.org/10.1016/j.lfs.2021.119336
  • Neto, F. T., Bach, P. V., Najari, B. B., Li, P. S., & Goldstein, M. (2016). Spermatogenesis in humans and its affecting factors. Seminars in cell & developmental biology, 59, 10–26. https://doi.org/10.1016/j.semcdb.2016.04.009
  • Ni, F. D., Hao, S. L., & Yang, W. X. (2019). Multiple signaling pathways in Sertoli cells: recent findings in spermatogenesis. Cell death & disease, 10(8), 541. https://doi.org/10.1038/s41419-019-1782-z
  • Nilsson, J., Skog, J., Nordstrand, A., Baranov, V., Mincheva-Nilsson, L., Breakefield, X. O., & Widmark, A. (2009). Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. British journal of cancer, 100(10), 1603–1607. https://doi.org/10.1038/sj.bjc.6605058
  • Oh, J. S., Han, C., & Cho, C. (2009). ADAM7 is associated with epididymosomes and integrated into sperm plasma membrane. Molecules and cells, 28(5), 441–446. https://doi.org/10.1007/s10059-009-0140-x
  • Oliver, E., & Stukenborg, J. B. (2020). Rebuilding the human testis in vitro. Andrology, 8(4), 825–834. https://doi.org/10.1111/andr.12710
  • Park KH, Kim BJ, Kang J, Nam TS, Lim JM, Kim HT, Park JK, Kim YG, Chae SW, Kim UH. Ca2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal. 2011 May 17;4(173):ra31.
  • Patil, S. M., Sawant, S. S., & Kunda, N. K. (2020). Exosomes as drug delivery systems: A brief overview and progress update. European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V, 154, 259–269. https://doi.org/10.1016/j.ejpb.2020.07.026
  • Paul, N., Talluri, T. R., Nag, P., & Kumaresan, A. (2021). Epididymosomes: A potential male fertility influencer. Andrologia, 53(9), e14155. https://doi.org/10.1111/and.14155
  • Pelzman, D. L., Orwig, K. E., & Hwang, K. (2020). Progress in translational reproductive science: testicular tissue transplantation and in vitro spermatogenesis. Fertility and sterility, 113(3), 500–509. https://doi.org/10.1016/j.fertnstert.2020.01.038
  • Perez-Hernandez, D., Gutiérrez-Vázquez, C., Jorge, I., López-Martín, S., Ursa, A., Sánchez-Madrid, F., Vázquez, J., & Yáñez-Mó, M. (2013). The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes. The Journal of biological chemistry, 288(17), 11649–11661. https://doi.org/10.1074/jbc.M112.445304
  • Raposo, G., Nijman, H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V., Melief, C. J., & Geuze, H. J. (1996). B lymphocytes secrete antigen-presenting vesicles. The Journal of experimental medicine, 183(3), 1161–1172. https://doi.org/10.1084/jem.183.3.1161
  • Rejraji, H., Vernet, P., & Drevet, J. R. (2002). GPX5 is present in the mouse caput and cauda epididymidis lumen at three different locations. Molecular reproduction and development, 63(1), 96–103. https://doi.org/10.1002/mrd.10136
  • Richer, G., Baert, Y., & Goossens, E. (2020). In-vitro spermatogenesis through testis modelling: Toward the generation of testicular organoids. Andrology, 8(4), 879–891. https://doi.org/10.1111/andr.12741
  • Ronquist G. (2012). Prostasomes are mediators of intercellular communication: from basic research to clinical implications. Journal of internal medicine, 271(4), 400–413. https://doi.org/10.1111/j.1365-2796.2011.02487.x
  • Ronquist, K. G., Ek, B., Morrell, J., Stavreus-Evers, A., Ström Holst, B., Humblot, P., Ronquist, G., & Larsson, A. (2013). Prostasomes from four different species are able to produce extracellular adenosine triphosphate (ATP). Biochimica et biophysica acta, 1830(10), 4604–4610. https://doi.org/10.1016/j.bbagen.2013.05.019
  • Ronquist, K. G., Sanchez, C., Dubois, L., Chioureas, D., Fonseca, P., Larsson, A., Ullén, A., Yachnin, J., Ronquist, G., & Panaretakis, T. (2016). Energy-requiring uptake of prostasomes and PC3 cell-derived exosomes into non-malignant and malignant cells. Journal of extracellular vesicles, 5, 29877. https://doi.org/10.3402/jev.v5.29877
  • Rowlison, T., Cleland, T. P., Ottinger, M. A., & Comizzoli, P. (2020). Novel Proteomic Profiling of Epididymal Extracellular Vesicles in the Domestic Cat Reveals Proteins Related to Sequential Sperm Maturation with Differences Observed between Normospermic and Teratospermic Individuals. Molecular & cellular proteomics : MCP, 19(12), 2090–2104. https://doi.org/10.1074/mcp.RA120.002251
  • Salek, F., Baharara, J., Shahrokhabadi, K. N., & Amini, E. (2021). The guardians of germ cells; Sertoli-derived exosomes against electromagnetic field-induced oxidative stress in mouse spermatogonial stem cells. Theriogenology, 173, 112–122. https://doi.org/10.1016/j.theriogenology.2021.08.001
  • Samanta, L., Parida, R., Dias, T. R., & Agarwal, A. (2018). The enigmatic seminal plasma: a proteomics insight from ejaculation to fertilization. Reproductive biology and endocrinology : RB&E, 16(1), 41. https://doi.org/10.1186/s12958-018-0358-6
  • Schlatt, S., & Ehmcke, J. (2014). Regulation of spermatogenesis: an evolutionary biologist's perspective. Seminars in cell & developmental biology, 29, 2–16. https://doi.org/10.1016/j.semcdb.2014.03.007 Sherif, I. O., Sabry, D., Abdel-Aziz, A., & Sarhan, O. M. (2018). The role of mesenchymal stem cells in chemotherapy-induced gonadotoxicity. Stem cell research & therapy, 9(1), 196. https://doi.org/10.1186/s13287-018-0946-6
  • Sinha, D., Roy, S., Saha, P., Chatterjee, N., & Bishayee, A. (2021). Trends in Research on Exosomes in Cancer Progression and Anticancer Therapy. Cancers, 13(2), 326. https://doi.org/10.3390/cancers13020326
  • Skibinski, G., Kelly, R. W., Harkiss, D., & James, K. (1992). Immunosuppression by human seminal plasma--extracellular organelles (prostasomes) modulate activity of phagocytic cells. American journal of reproductive immunology (New York, N.Y. : 1989), 28(2), 97–103. https://doi.org/10.1111/j.1600-0897.1992.tb00767.x
  • Skryabin, G. O., Komelkov, A. V., Savelyeva, E. E., & Tchevkina, E. M. (2020). Lipid Rafts in Exosome Biogenesis. Biochemistry. Biokhimiia, 85(2), 177–191. https://doi.org/10.1134/S0006297920020054
  • Sousa, C., Pereira, I., Santos, A. C., Carbone, C., Kovačević, A. B., Silva, A. M., & Souto, E. B. (2017). Targeting dendritic cells for the treatment of autoimmune disorders. Colloids and surfaces. B, Biointerfaces, 158, 237–248. https://doi.org/10.1016/j.colsurfb.2017.06.050
  • Sullivan R. (2016). Epididymosomes: Role of extracellular microvesicles in sperm maturation. Frontiers in bioscience (Scholar edition), 8(1), 106–114. https://doi.org/10.2741/s450
  • Sullivan, R., & Saez, F. (2013). Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction (Cambridge, England), 146(1), R21–R35. https://doi.org/10.1530/REP-13-0058
  • Sullivan, R., Saez, F., Girouard, J., & Frenette, G. (2005). Role of exosomes in sperm maturation during the transit along the male reproductive tract. Blood cells, molecules & diseases, 35(1), 1–10. https://doi.org/10.1016/j.bcmd.2005.03.005
  • Sullivan, R., & Saez, F. (2013). Epididymosomes, prostasomes, and liposomes: their roles in mammalian male reproductive physiology. Reproduction (Cambridge, England), 146(1), R21–R35. https://doi.org/10.1530/REP-13-0058
  • Tamessar, C. T., Trigg, N. A., Nixon, B., Skerrett-Byrne, D. A., Sharkey, D. J., Robertson, S. A., Bromfield, E. G., & Schjenken, J. E. (2021). Roles of male reproductive tract extracellular vesicles in reproduction. American journal of reproductive immunology (New York, N.Y. : 1989), 85(2), e13338. https://doi.org/10.1111/aji.13338
  • Tannetta, D., Dragovic, R., Alyahyaei, Z., & Southcombe, J. (2014). Extracellular vesicles and reproduction-promotion of successful pregnancy. Cellular & molecular immunology, 11(6), 548–563. https://doi.org/10.1038/cmi.2014.42
  • Tarazona, R., Delgado, E., Guarnizo, M. C., Roncero, R. G., Morgado, S., Sánchez-Correa, B., Gordillo, J. J., Dejulián, J., & Casado, J. G. (2011). Human prostasomes express CD48 and interfere with NK cell function. Immunobiology, 216(1-2), 41–46. https://doi.org/10.1016/j.imbio.2010.03.002
  • Thiageswaran, S., Steele, H., Voigt, A. L., & Dobrinski, I. (2022). A Role for Exchange of Extracellular Vesicles in Porcine Spermatogonial Co-Culture. International journal of molecular sciences, 23(9), 4535. https://doi.org/10.3390/ijms23094535
  • Thimon, V., Frenette, G., Saez, F., Thabet, M., & Sullivan, R. (2008). Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. Human reproduction (Oxford, England), 23(8), 1698–1707. https://doi.org/10.1093/humrep/den181
  • Tran, K. T. D., Valli-Pulaski, H., Colvin, A., & Orwig, K. E. (2022). Male fertility preservation and restoration strategies for patients undergoing gonadotoxic therapies†. Biology of reproduction, 107(2), 382–405. https://doi.org/10.1093/biolre/ioac072
  • Utleg, A. G., Yi, E. C., Xie, T., Shannon, P., White, J. T., Goodlett, D. R., Hood, L., & Lin, B. (2003). Proteomic analysis of human prostasomes. The Prostate, 56(2), 150–161. https://doi.org/10.1002/pros.10255
  • Van den Boorn, J. G., Dassler, J., Coch, C., Schlee, M., & Hartmann, G. (2013). Exosomes as nucleic acid nanocarriers. Advanced drug delivery reviews, 65(3), 331–335. https://doi.org/10.1016/j.addr.2012.06.011
  • Vasan S. S. (2011). Semen analysis and sperm function tests: How much to test?. Indian journal of urology : IJU : journal of the Urological Society of India, 27(1), 41–48. https://doi.org/10.4103/0970-1591.78424
  • Vernet, P., Aitken, R. J., & Drevet, J. R. (2004). Antioxidant strategies in the epididymis. Molecular and cellular endocrinology, 216(1-2), 31–39. https://doi.org/10.1016/j.mce.2003.10.069
  • Vickram, A. S., Srikumar, P. S., Srinivasan, S., Jeyanthi, P., Anbarasu, K., Thanigaivel, S., Nibedita, D., Jenila Rani, D., & Rohini, K. (2021). Seminal exosomes - An important biological marker for various disorders and syndrome in human reproduction. Saudi journal of biological sciences, 28(6), 3607–3615. https://doi.org/10.1016/j.sjbs.2021.03.038
  • Vickram, A. S., Anbarasu, K., Gulothungan, G., Thanigaivel, S., Nanmaran, R., & Palanivelu, J. (2022). Characterization of human prostasomes protein Clusterin (macromolecule) - a novel biomarker for male infertility diagnosis and prognosis. Journal of biomolecular structure & dynamics, 40(9), 3979–3988. https://doi.org/10.1080/07391102.2020.1852960
  • Vickram, A. S., Srikumar, P. S., Srinivasan, S., Jeyanthi, P., Anbarasu, K., Thanigaivel, S., Nibedita, D., Jenila Rani, D., & Rohini, K. (2021). Seminal exosomes - An important biological marker for various disorders and syndrome in human reproduction. Saudi journal of biological sciences, 28(6), 3607–3615. https://doi.org/10.1016/j.sjbs.2021.03.038
  • Vivacqua, A., Siciliano, L., Sabato, M., Palma, A., & Carpino, A. (2004). Prostasomes as zinc ligands in human seminal plasma. International journal of andrology, 27(1), 27–31. https://doi.org/10.1111/j.1365-2605.2004.00441.x
  • Wang, G. J., Liu, Y., Qin, A., Shah, S. V., Deng, Z. B., Xiang, X., Cheng, Z., Liu, C., Wang, J., Zhang, L., Grizzle, W. E., & Zhang, H. G. (2008). Thymus exosomes-like particles induce regulatory T cells. Journal of immunology (Baltimore, Md. : 1950), 181(8), 5242–5248. https://doi.org/10.4049/jimmunol.181.8.5242
  • Wang, B., Zhai, C., Li, Y., Ma, B., Li, Z., & Wang, J. (2023). Sertoli cells-derived exosomal miR-30a-5p regulates ubiquitin E3 ligase Zeb2 to affect the spermatogonial stem cells proliferation and differentiation. Reproductive toxicology (Elmsford, N.Y.), 117, 108340. https://doi.org/10.1016/j.reprotox.2023.108340
  • World Health Organization (WHO). WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 4th ed.; Cambridge University Press: New York, NY, USA, 1999. Yellon, D. M., & Davidson, S. M. (2014). Exosomes: nanoparticles involved in cardioprotection?. Circulation research, 114(2), 325–332. https://doi.org/10.1161/CIRCRESAHA.113.300636
  • Zakharova, L., Svetlova, M., & Fomina, A. F. (2007). T cell exosomes induce cholesterol accumulation in human monocytes via phosphatidylserine receptor. Journal of cellular physiology, 212(1), 174–181. https://doi.org/10.1002/jcp.21013
  • Quadri, Z., Elsherbini, A., & Bieberich, E. (2022). Extracellular vesicles in pharmacology: Novel approaches in diagnostics and therapy. Pharmacological research, 175, 105980. https://doi.org/10.1016/j.phrs.2021.105980
  • Yang, C., Guo, W. B., Zhang, W. S., Bian, J., Yang, J. K., Zhou, Q. Z., Chen, M. K., Peng, W., Qi, T., Wang, C. Y., & Liu, C. D. (2017). Comprehensive proteomics analysis of exosomes derived from human seminal plasma. Andrology, 5(5), 1007–1015. https://doi.org/10.1111/andr.12412
  • Yeung, C. H., Cooper, T. G., Schröter, S., Kirchhoff, C., & Nieschlag, E. (1998). Epididymal secretion of CD52 as measured in human seminal plasma by a fluorescence immunoassay. Molecular human reproduction, 4(5), 447–451. https://doi.org/10.1093/molehr/4.5.447
  • Yu, K., Xiao, K., Sun, Q. Q., Liu, R. F., Huang, L. F., Zhang, P. F., Xu, H. Y., Lu, Y. Q., & Fu, Q. (2023). Comparative proteomic analysis of seminal plasma exosomes in buffalo with high and low sperm motility. BMC genomics, 24(1), 8. https://doi.org/10.1186/s12864-022-09106-2
  • Yue, D., Yang, R., Xiong, C., & Yang, R. (2022). Functional prediction and profiling of exosomal circRNAs derived from seminal plasma for the diagnosis and treatment of oligoasthenospermia. Experimental and therapeutic medicine, 24(5), 649. https://doi.org/10.3892/etm.2022.11586
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Details

Primary Language Turkish
Subjects Clinical Sciences (Other)
Journal Section Review
Authors

Oya Korkmaz 0000-0003-2923-5869

Mustafa Numan Bucak 0000-0002-2955-8599

Early Pub Date December 29, 2024
Publication Date December 31, 2024
Submission Date November 10, 2024
Acceptance Date December 12, 2024
Published in Issue Year 2024Volume: 9 Issue: 3

Cite

Vancouver Korkmaz O, Bucak MN. Erkek Üreme Sisteminde Eksozomların Potansiyel Rolü. J Cumhuriyet Univ Health Sci Inst. 2024;9(3):404-16.
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The Journal of Sivas Cumhuriyet University Institute of Health Sciences is an international, peer-reviewed scientific journal published by Sivas Cumhuriyet University, Institute of Health Sciences.