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Effects of Hormones on the Expression of Matrix Metalloproteinases and Their Inhibitors in Bovine Spermatozoa

  • Kim, Sang-Hwan (Institute of Genetic Engineering, Hankyong National University) ;
  • Song, Young-Seon (Graduate School of Bio and Information Technology, Hankyong National University) ;
  • Hwang, Sue-Yun (Graduate School of Bio and Information Technology, Hankyong National University) ;
  • Min, Kwan-Sik (Graduate School of Bio and Information Technology, Hankyong National University) ;
  • Yoon, Jong-Taek (Department of Animal Life Science, Hankyong National University)
  • Received : 2012.10.10
  • Accepted : 2012.12.01
  • Published : 2013.03.01

Abstract

Proteases and protease inhibitors play key roles in most physiological processes, including cell migration, cell signaling, and cell surface and tissue remodeling. Among these, the matrix metalloproteinase (MMPs) pathway is one of the most efficient biosynthetic pathways for controlling the activation of enzymes responsible for protein degradation. This also indicates the association of MMPs with the maturation of spermatozoa. In an attempt to investigate the effect of MMP activation and inhibitors in cultures with various hormones during sperm capacitation, we examined and monitored the localization and expression of MMPs (MMP-2 and MMP-9), tissue inhibitors of metalloproteinases (TIMP-2 and TIMP-3), as well as their expression profiles. Matured spermatozoa were collected from cultures with follicle-stimulating hormone (FSH), luteinizing hormone (LH), and Lutalyse at 1 h, 6 h, 18 h, and 24 h. ELISA detected the expression of MMP-2, MMP-9, TIMP-2, and TIMP-3 in all culture media, regardless of medium type (FSH-supplemented fertilization Brackett-Oliphant medium (FFBO), LH-supplemented FBO (LFBO), or Lutalyse-supplemented FBO (LuFBO)). TIMP-2 and TIMP-3 expression patterns decreased in LFBO and LuFBO. MMP-2 and MMP-9 activity in FBO and FFBO progressively increased from 1 h to 24 h but was not detected in LFBO and LuFBO. The localization and expression of TIMP-2 and TIMP-3 in sperm heads was also measured by immunofluorescence analysis. However, MMPs were not detected in the sperm heads. MMP and TIMP expression patterns differed according to the effect of various hormones. These findings suggest that MMPs have a role in sperm viability during capacitation. In conjunction with hormones, MMPs play a role in maintaining capacitation and fertilization by controlling extracellular matrix inhibitors of sperm.

Keywords

Bovine;Spermatozoa;MMPs;TIMPs;Capacitation

Acknowledgement

Supported by : Rural Development Administration

References

  1. Barrett, A. J., N. D. Rowlings and J. F. Woessner. 1998. Handbook of Proteolytic Enzymes. Academic Press, London, UK.
  2. Brackett, B. G. and G. Oliphant. 1975. Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12:260-274. https://doi.org/10.1095/biolreprod12.2.260
  3. Breitbart, H. 2004. Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Mol. Cell Endocrinol. 187:139-144.
  4. Chang, M. C. 1951. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168:697-698.
  5. Chung, N. P. and C. Y. Cheng. 2001. Is cadmium chloride-induced inter-Sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis. Endocrinology 142:1878-1888. https://doi.org/10.1210/en.142.5.1878
  6. de Leeuw, A. M., J. H. den Daas and H. Woelders. 1991. The fix vital stain method. Simultaneous determination of viability and acrosomal status of bovine spermatozoa. J. Androl. 12:112-118.
  7. Frayne, J., J. A. Jury, H. L. Barker, A. C. Perry, R. Jones and L. Hall. 1998. Macaque MDC family of proteins: sequence analysis, tissue distribution and processing in the male reproductive tract. Mol. Hum. Reprod. 4:429-437. https://doi.org/10.1093/molehr/4.5.429
  8. Gunnarsson, M., I. Lecander and P. A. Abrahamsson. 1999. Factors of the plasminogen activator system in human testis. as demonstrated by in-situ hybridization and immunohistochemistry. Mol. Hum. Reprod. 5:934-940. https://doi.org/10.1093/molehr/5.10.934
  9. Hulboy, D. L., L. A. Rudolph and L. M. Matrisian. 1997. Matrix metalloproteinases as mediators of reproductive function. Mol. Hum. Reprod. 3:27-45. https://doi.org/10.1093/molehr/3.1.27
  10. Kohno, N., K. Yamagata, S. Yamada, S. Kashiwabara, Y. Sakai and T. Baba. 1998. Two novel testicular serine proteases, TESP1 and TESP2, are present in the mouse sperm acrosome. Biochem. Biophys. Res. Commun. 245:658-665. https://doi.org/10.1006/bbrc.1998.8501
  11. Longin, J., P. Guillaumot, M. A. Chauvin, A. M. Morera and B. B. Le Magueresse. 2001. MT1-MMP in rat testicular development and the control of Sertoli cell proMMP-2 activation. J. Cell. Sci. 114:2125-2134.
  12. Longin, J. and B. B. Le Magueressei. 2002. Evidence that MMP-2 and TIMP-2 are at play in the FSH-induced changes in Sertoli cells. Mol. Cell Endocrinol. 189:25-35. https://doi.org/10.1016/S0303-7207(01)00756-0
  13. Siu, M. K. and C. Y. Cheng. 2004. Interactions of proteases, protease inhibitors, and the beta1 integrin/laminin gamma3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol. Reprod. 70:945-964.
  14. Mruk, D. D., M. K. Siu, A. M. Conway, N. P. Lee, A. S. Lau and C. Y. Cheng. 2003. Role of tissue inhibitor of metallo proteases-1 in junction dynamics in the testis. J. Androl. 24:510-523.
  15. Mruk, D., L. J. Zhu, B. Silvestrini, W. M. Lee and C. Y. Cheng. 1997. Interactions of proteases and protease inhibitors in Sertoli-germ cell co-cultures preceding the formation of specialized Sertoli-germ cell junctions in vitro. J. Androl. 18:612-622.
  16. Phelps, B. M., D. E. Koppel, P. Primakoff and D. G. Myles. 1990. Evidence that proteolysis of the surface is an initial step in the mechanism of formation of sperm cell surface domains. J. Cell Biol. 111:1839-1847. https://doi.org/10.1083/jcb.111.5.1839
  17. Ray, J. M. and W. G. Stetler-Stevenson. 1994. The role of matrix metalloproteases and their inhibitors in tumour invasion, metastasis and angiogenesis. Eur. Respir. J. 7:2062-2072.
  18. Robinson, L. L., N. A. Sznajder, S. C. Riley and R. A. Anderson. 2001. Matrix metallo-proteinases and tissue inhibitors of metalloproteinases in human fetal testis and ovary. Mol. Hum. Reprod. 7:641-648. https://doi.org/10.1093/molehr/7.7.641
  19. Salamonsen, L. A. and D. E. Woolley. 1996. Matrix metalloproteinases in normal menstruation. Hum. Reprod. 11:124-133. https://doi.org/10.1093/humrep/11.suppl_2.124
  20. Sang, Q. X., M. Dym, and S. W. Byers. 1990. Secreted metalloproteinases in testicular cell culture. Biol. Reprod. 43:946-955. https://doi.org/10.1095/biolreprod43.6.946
  21. Slongo, M. L., M. Zampieri and M. Onisto. 2002. Expression of matrix metalloproteases (MMP-2, MT1-MMP) and their tissue inhibitor (TIMP-2) by rat Sertoli cells in culture: implications for spermatogenesis. Biol. Chem. 383:235-239.
  22. Suarez, S. S. 2008. Control of hyperactivation in sperm. Hum. Reprod. Update. 14:647-657. https://doi.org/10.1093/humupd/dmn029
  23. Tulsiani, D. R., H. A. Abou, C. R. Loeser and B. M. Pereira. 1998. The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization. Exp. Cell Res. 240:151-164. https://doi.org/10.1006/excr.1998.3943
  24. Xia, J., D. Reigada, C. H. Mitchell and D. Ren. 2007. CATSPER channel mediated $Ca^{2+}$ entry into mouse sperm triggers a tail-to-head propagation. Biol. Reprod. 77:551-559. https://doi.org/10.1095/biolreprod.107.061358
  25. Xia, J. and D. Ren. 2009. Egg-coat proteins activate calcium entry into mouse sperm via CATSPER channels. Biol. Reprod. 80:1092-1098. https://doi.org/10.1095/biolreprod.108.074039
  26. Xu, P., Y. L. Wang, S. J. Zhu, S. Y. Luo, Y. S. Piao and L. Z. Zhuang. 2000. Expression of matrix metalloproteinase-2, -9, and -14, tissue inhibitors of metalloproteinase-1, and matrix proteins in human placenta during the first trimester. Biol. Reprod. 62:988-994. https://doi.org/10.1095/biolreprod62.4.988
  27. Yamagata, K., K. Murayama, M. Okabe, K. Toshimori, T. Nakanishi, S. Kashiwabara and T. Baba. 1998. Acrosin accelerates the dispersal of sperm acrosomal proteins during acrosome reaction. J. Biol. Chem. 273:10470-10474. https://doi.org/10.1074/jbc.273.17.10470
  28. Wong, C. C., S. S. Chung. J. Grima, L. J. Zhu, D. Mruk, W. M. Lee and C. Y. Cheng. 2000. Changes in the expression of junctional and nonjunctional complex component genes when inter-Sertoli tight junctions are formed in vitro. J. Androl. 21:227-237.
  29. Woessner, J. F. Jr. 1994. The family of matrix metalloproteinases. Ann. NY. Acad. Sci. 732:11-21. https://doi.org/10.1111/j.1749-6632.1994.tb24720.x
  30. Yanagimachi, R. 1994. Mammalian Fertilization, In The Physiology of Reproduction. 2nd edition. Edited by E. Knobil, and J. D. Neill. Raven. pp. 189-315.

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