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Expression of Neurotrophin 4 and Its Receptor Tyrosine Kinase B in Reproductive Tissues during the Follicular and Luteal Phases in Cows

  • Sun, Yongfeng (College of Animal Science and Veterinary Medicine, Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University) ;
  • Li, Chunjin (College of Animal Science and Veterinary Medicine, Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University) ;
  • Sun, Yanling (College of Animal Science and Veterinary Medicine, Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University) ;
  • Chen, Lu (College of Animal Science and Veterinary Medicine, Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University) ;
  • Liu, Zhuo (College of Animal Science and Veterinary Medicine, Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University) ;
  • Ma, Yonghe (College of Animal Science and Veterinary Medicine, Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University) ;
  • Wang, Chunqiang (College of Animal Science and Veterinary Medicine, Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University) ;
  • Zhang, Wei (College of Animal Science and Veterinary Medicine, Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University) ;
  • Zhou, Xu (College of Animal Science and Veterinary Medicine, Jilin Provincial Key Laboratory of Animal Embryo Engineering, Jilin University)
  • 투고 : 2010.07.07
  • 심사 : 2010.12.31
  • 발행 : 2011.03.01

초록

The neurotrophins, required for the survival and differentiation of the nervous system, are known to be important for the development of the reproductive tissues. However, the signals initiating the growth of follicles, gamete development, and transport and the development of zygote in the reproductive system of cows remain ambiguous. The purpose of the present study was to identify the transcripts and proteins of Neurotrophin 4 (NT4) and its receptor tyrosine kinase B (TrkB) in bovine reproductive tissues. The transcripts and immunoreactivity of NT4 and TrkB proteins were detected by reverse transcription polymerase chain reaction and western blot analysis. Using immunohistochemistry, the specific immunoreactivity of NT4 and TrkB were detected in the oocytes of primordial follicles and in the growing primary follicles. The NT4 and TrkB immunoreactivity was predominantly observed in granulosa cells, cumulus granulosa cells, cumulus oocyte complexes, theca cells of mature follicles, as well as in the oviduct epithelial cells, uterine gland cell, and epithelium cells of the uterus during the follicular and luteal phases in cows. Expressions of NT4 and TrkB mRNAs were not significantly different among the ovary, oviduct, and uterus of the follicular phase. For the luteal phase, the expression of NT4 mRNA in the ovary was significantly higher than that in the oviduct and uterus, and the expression of TrkB mRNA in the oviduct was significantly higher than that in the ovary and uterus, as determined by fluorescence quantitative reverse transcription polymerase chain reaction. The expression of NT4 mRNA was significantly higher than that of TrkB mRNA in the ovary and uterus, whereas NT4 mRNA expression was lower than that of TrkB mRNA in the oviduct during the luteal phase. The present study hypothesizes that NT4 participates in the regulation of both gonads and extra-gonadal reproductive tissues in cows.

키워드

참고문헌

  1. Anderson, R. A., L. L. Robinson, J. Brooks and N. Spears. 2002. Neurotropins and their receptors are expressed in the human fetal ovary. J. Clin. Endocrinol. Metab. 87:890-897. https://doi.org/10.1210/jc.87.2.890
  2. Betancourt-Alonso, M. A., F. I. Flores-Perez, C. Rosas-Velasco and M. Perez-Martinez. 2006. Role of cytokines in embryo implantation in domestic mammals. Vet. Mex. 37:335-350.
  3. Bjorling, D. E., M. Beckman, M. K. Clayton and Z. Y. Wang. 2002. Modulation of nerve growth factor in peripheral organs by estrogen and progesterone. Neuroscience 110:155-167. https://doi.org/10.1016/S0306-4522(01)00568-1
  4. Buratini, J. Jr., M. G. Pinto, A. C. Castilho, R. L. Amorim, I. C. Giometti, V. M. Portela, E. S. Nicola and C. A. Price. 2007. Expression and function of fibroblast growth factor 10 and its receptor, fibroblast growth factor receptor 2B, in bovine follicles. Biol. Reprod. 77:743-750. https://doi.org/10.1095/biolreprod.107.062273
  5. Byskov, A. G. 1986. Differentiation of mammalian embryonic gonad. Physiol. Rev. 66:71-117. https://doi.org/10.1016/0034-5687(86)90140-4
  6. De Sousa, P. A., S. J. da Silva and R. A. Anderson. 2004. Neurotrophin signaling in oocyte survival and developmental competence: a paradigm for cellular toti-potency. Cloning Stem Cells 6:375-385. https://doi.org/10.1089/clo.2004.6.375
  7. Dissen, G. A., A. N. Hirshfield, S. Malamed and S. R. Ojeda. 1995. Expression of neurotropins and their receptors in the mammalian ovary is developmentally regulated: changes at the time of folliculogensis. Endocrinology 136:4681-4692. https://doi.org/10.1210/en.136.10.4681
  8. Dissen, G. A., J. A. Parrott, M. K. Skinner, D. F. Hill, M. E. Costa and S. R. Ojeda. 2000. Direct effects of nerve growth factor on thecal cells from antral ovarian follicles. Endocrinology 141:4736-4750. https://doi.org/10.1210/en.141.12.4736
  9. Dissen, G. A., C. Romero, A. N. Hirshfield and S. R. Ojeda. 2001. Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 142:2078-2086. https://doi.org/10.1210/en.142.5.2078
  10. Donovan, M. J., R. C. Miranda, R. Kraemer, T. A. McCaffrey, L. Tessarollo, D. Mahadeo, S. Sharif, D. R. Kaplan, P. Tsorflas, L. Parada, C. D. Toran-Allerand, D. P. Hajjar and B. L. Hempstead. 1995. Neurotrophin and neurotrophin receptors in vascular smooth muscle cells. Regulation of expression in response to injury. Am. J. Pathol. 147:309-324.
  11. Fridman, W. J. and L. A. Greene. 1999. Neurotrophin signaling via Trks and p75. Exp. Cell Res. 253:131-142. https://doi.org/10.1006/excr.1999.4705
  12. Gandolfi, F., S. Modina, T. A. Brevini, L.Passoni, P. Artini, F. Petraglia and A. Lauria. 1995. Activin beta A subunit is expressed in bovine oviduct. Mol. Reprod. 40:286-291. https://doi.org/10.1002/mrd.1080400304
  13. Gupta, A., F. W. Bazer and L. A. Jaeger. 1997. Immunolocalization of acidic and basic fibroblast growth factors in porcine uterine and concept us tissues. Biol. Reprod. 56:1527-1536. https://doi.org/10.1095/biolreprod56.6.1527
  14. Hong, S. G., G. Jang, H. J. Oh, O. J. Koo, J. E. Park, H. J. Park, S. K. Kang and B. Lee. 2009. The effects of brain-derived neurotrophic factor and metformin on in vitro developmental competence of bovine oocytes. Zygote 17:187-193. https://doi.org/10.1017/S0967199409005255
  15. Ibanez, C. F. 1995. Neurotrophin factors: from structure-function studies to designing effective therapeutics. Trends Biotechnol. 13:217-227. https://doi.org/10.1016/S0167-7799(00)88949-0
  16. Kawamura, K., N. Kawamura, J. Fukuda, J. Kumagai, A. Hsueh and T. Tanaka. 2007. Regulation of preimplantation embryo development by brain-derived neurotrophic factor. Dev. Biol. 311:147-158. https://doi.org/10.1016/j.ydbio.2007.08.026
  17. Kawamura, K., N. Kawamura, S. M. Mulders, M. D. Sollewijn Gelpke and A. J. Hsueh. 2005. Ovarian brain-derived neurotrophic factor (BDNF) promotes the development of oocytes into preimplantation embryos. Proc. Natl. Acad. Sci. USA 102: 9206-9211. https://doi.org/10.1073/pnas.0502442102
  18. Krizsan-Agbas, D., T. Pedchenko, W. Hasan and P. G. Smith. 2003. Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus. Eur. J. Neurosci.18:2760-2768. https://doi.org/10.1111/j.1460-9568.2003.03029.x
  19. Levanti, M. B., A. Germana, F. Abbate, G. Montalbano, J. A. Vega and G. Germana. 2005. TrkA and p75NTR in the ovary of adult cow and pig. J. Anat. 207:93-96. https://doi.org/10.1111/j.1469-7580.2005.00423.x
  20. Li, C. J., L. W. Zheng, C. Q. Wang and X. Zhou. 2010. Absence of nerve growth factor and comparison of tyrosine kinase receptor A levels in mature spermatozoa from oligoasthenozoospermic, asthenozoospermic and fertile men. Clin. Chim. Acta. 411:1482-1486. https://doi.org/10.1016/j.cca.2010.06.002
  21. Martins, da Silva, S. J., J. O. Gardner, J. E. Taylor, A. Springbett, P. A. De Sousa and R. A. Anderson. 2005. Brain-derived neurotrophic factor promotes bovine oocyte cytoplasmic competence for embryo development. Reproduction 129:423-434. https://doi.org/10.1530/rep.1.00471
  22. Mattioli, M., B. Barboni, L. Gioia and P. Lucidi. 1999. Nerve growth factor production in sheep antral follicles. Domest. Anim. Endocrinol. 17:361-371. https://doi.org/10.1016/S0739-7240(99)00056-9
  23. Mayerhofer, A., G. A. Dissen, J. A. Parrott, D. F. Hill, D. Mayerhofer, R. E. Garfield, M. E. Costa, M. K. Skinner and S. R. Ojeda. 1996. Involvement of nerve growth factor in the ovulatory cascade: trkA receptor activation inhibits gap junctional communication between thecal cells. Endocrinology 137:5662-5670. https://doi.org/10.1210/en.137.12.5662
  24. McLaren, A. 1991. Development of the mammalian gonad: the fate of the supporting cell lineage. BioEssays 13:151-156. https://doi.org/10.1002/bies.950130402
  25. Munoz, M., A. Rodriguez, C. Diez, J. N. Caamano, M. T. Fernandez-Sanchez, A. Perez-Gomez, C. De Frutos, N. Facal and E. Gomez. 2009. Tyrosine kinase A, C and fibroblast growth factor-2 receptors in bovine embryos cultured in vitro. Theriogenology 71:1005-1010. https://doi.org/10.1016/j.theriogenology.2008.11.008
  26. Paredes, A., C. Romero, G. A. Dissen, T. M. DeChiara, L. Reichardt, A. Cornea, S. R. Ojeda and B. Xu. 2004. TrkB receptors are required for follicular growth and oocyte survival in the mammalian ovary. Dev. Biol. 267:430-449. https://doi.org/10.1016/j.ydbio.2003.12.001
  27. Ren, L., M. S. Medan, Q. Weng, W. Jin, C. Li, G. Watanabe and K. Taya. 2005. Immunolocalization of nerve growth factor (NGF) and its receptors (TrkA and p75LNGFR) in the reproductive organs of Shiba goats. J. Reprod. Dev. 51:399-404. https://doi.org/10.1262/jrd.16082
  28. Schell, D. L., P. A. Mavrogianis, A. T. Fazleabas and H. G. Verhage. 1994. Epidermal growth factor, transforming growth factor-alpha, and epidermal growth factor receptor localization in the banboon (Papio anubis) oviduct during steroid treatment and the meastrual cycle. J. Soc. Gynecol. Investig. 1:269-276.
  29. Shimizu, K., W. Jin, C. Kojima, Z. Shi, M. Kondo, M. Itoh, G. Watanabe and K. Taya. 2002. Cellular localization of nerve growth factor (NGF) and its receptors TrkA and p75LNGFR in the ovary of the Japanese monkey (Macaca fuscata fuscata). J. Reprod. Dev. 48:377-381. https://doi.org/10.1262/jrd.48.377
  30. Shi, Z., K. Y. Arai, W. Jin, Q. Weng, G. Watanabe, A. K. Suzuki and K. Taya. 2006. Expression of nerve growth factor and its receptors NTRK1 and TNFRSF1B is regulated by estrogen and progesterone in the uteri of golden hamsters. Biol. Reprod.74:850-856. https://doi.org/10.1095/biolreprod.105.044917
  31. Spears, N., M. D. Molinek, L. L. Robinson, N. Fulton, H. Cameron, K. Shimoda, E. E. Telfer, R. A. Anderson and D. J. Price. 2003. The role of neurotrophin receptors in female germ-cell survival in mouse and human. Development 130:5481-5491. https://doi.org/10.1242/dev.00707
  32. Witschi, E. 1948. Migration of the germ cells of human embryos from the yolksac to the primitive gonadal fold. Contrib. Embryol. 32:67-80.
  33. Yeh, J. and R. Osathanondh. 1993. Expression of messenger ribonucleic acids encoding for basic fibroblast growth factor (FGF) and alternatively spliced FGF receptor in human fetal ovary and uterus. J. Clin. Endocrinol. Metab. 77:1367-1371. https://doi.org/10.1210/jc.77.5.1367
  34. Zettler, C., R. J. Head and R. A. Rush. 1991. Chronic nerve growth factor treatment of normotensive rats. Brain. Res. 538:251-262. https://doi.org/10.1016/0006-8993(91)90437-Z

피인용 문헌

  1. Detection of Neurotrophin-4 (NT-4) in Ejaculated Bull Spermatozoa and its Effect on Spermatozoa Mitochondrial Activity vol.48, pp.1, 2012, https://doi.org/10.1111/j.1439-0531.2012.02048.x