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Differential expression of estrogen receptor α and progesterone receptor in the normal and cryptorchid testis of a dog

Laboratory Animal Research volume 32, pages 128–132 (2016)Cite this article

Abstract

Descending of the testes is an important process for spermatogenesis and cryptorchidism is one of the most relevant genital defects in dogs. In a previous study, we observed abnormal morphology and proliferation of Sertoli cells in a cryptorchid testis. In the present study, we investigated the expression of estrogen and progesterone receptors in the normal and cryptorchid testis of a dog. Elective orchidectomy was performed on the dog’s abdominal right testis (undescended, cryptorchid) and scrotal left testis (descended, normal). In the normal testis, estrogen receptor a immunoreactivity was detected in Leydig cells alone, while estrogen receptor a immunoreactivity in the cryptorchid testis was significantly prominent in the Sertoli cells as well. In addition, progesterone receptor immunoreactivity in the control testis was detected in the spermatids, but was not detected in the cryptorchid testis. This result suggests that unilateral cryptorchidism causes increases of estrogen receptor a expression in Sertoli cells.

References

  1. Yates D, Hayes G, Heffernan M, Beynon R. Incidence of cryptorchidism in dogs and cats. Vet Rec 2003; 152(16): 502–504.

    Article  CAS  PubMed  Google Scholar 

  2. Nef S, Parada LF. Cryptorchidism in mice mutant for Insl3. Nat Genet 1999; 22(3): 295–299.

    Article  CAS  PubMed  Google Scholar 

  3. Zimmermann S, Steding G, Emmen JM, Brinkmann AO, Nayernia K, Holstein AF, Engel W, Adham IM. Targeted disruption of the Insl3 gene causes bilateral cryptorchidism. Mol Endocrinol 1999; 13(5): 681–691.

    Article  CAS  PubMed  Google Scholar 

  4. Hutson JM, Baker M, Terada M, Zhou B, Paxton G. Hormonal control of testicular descent and the cause of cryptorchidism. Reprod Fertil Dev 1994; 6(2): 151–156.

    Article  CAS  PubMed  Google Scholar 

  5. Gill WB, Schumacher GF, Bibbo M, Straus FH 2nd, Schoenberg HW. Association of diethylstilbestrol exposure in utero with cryptorchidism, testicular hypoplasia and semen abnormalities. J Urol 1979; 122(1): 36–39.

    Article  CAS  PubMed  Google Scholar 

  6. Grocock CA, Charlton HM, Pike MC. Role of the fetal pituitary in cryptorchidism induced by exogenous maternal oestrogen during pregnancy in mice. J Reprod Fertil 1988; 83(1): 295–300.

    Article  CAS  PubMed  Google Scholar 

  7. Hadziselimovic F, Girard J. Pathogenesis of cryptorchidism. Horm Res 1977; 8(2): 76–83.

    Article  CAS  PubMed  Google Scholar 

  8. Khan SA, Ball RB, Hendry WJ 3rd. Effects of neonatal administration of diethylstilbestrol in male hamsters: disruption of reproductive function in adults after apparently normal pubertal development. Biol Reprod 1998; 58(1): 137–142.

    Article  CAS  PubMed  Google Scholar 

  9. Akingbemi BT. Estrogen regulation of testicular function. Reprod Biol Endocrinol 2005; 3: 51.

  10. Couse JF, Korach KS. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 1999; 20(3): 358–417.

    CAS  PubMed  Google Scholar 

  11. Walker VR, Korach KS. Estrogen receptor knockout mice as a model for endocrine research. ILAR J 2004; 45(4): 455–461.

    Article  CAS  PubMed  Google Scholar 

  12. Carreau S, Hess RA. Oestrogens and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010; 365(1546): 1517–1535.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Couse JF, Hewitt SC, Bunch DO, Sar M, Walker VR, Davis BJ, Korach KS. Postnatal sex reversal of the ovaries in mice lacking estrogen receptors alpha and beta. Science 1999; 286(5448): 2328–2331.

    Article  CAS  PubMed  Google Scholar 

  14. Antal MC, Krust A, Chambon P, Mark M. Sterility and absence of histopathological defects in nonreproductive organs of a mouse ERbeta-null mutant. Proc Natl Acad Sci U S A 2008; 105(7): 2433–2438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Royer C, Lucas TF, Lazari MF, Porto CS. 17Beta-estradiol signaling and regulation of proliferation and apoptosis of rat Sertoli cells. Biol Reprod 2012; 86(4): 108.

    Article  PubMed  Google Scholar 

  16. Ramesh R, Pearl CA, At-Taras E, Roser JF, Berger T. Ontogeny of androgen and estrogen receptor expression in porcine testis: effect of reducing testicular estrogen synthesis. Anim Reprod Sci 2007; 102(3-4): 286–299.

    Article  CAS  PubMed  Google Scholar 

  17. Cavaco JE, Laurentino SS, Barros A, Sousa M, Socorro S. Estrogen receptors alpha and beta in human testis: both isoforms are expressed. Syst Biol Reprod Med 2009; 55(4): 137–144.

    Article  CAS  PubMed  Google Scholar 

  18. Lucas TF, Pimenta MT, Pisolato R, Lazari MF, Porto CS. 17a-estradiol signaling and regulation of Sertoli cell function. Spermatogenesis. 2011; 1(4): 318–324.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Lucas TF, Siu ER, Esteves CA, Monteiro HP, Oliveira CA, Porto CS, Lazari MF. 17beta-estradiol induces the translocation of the estrogen receptors ESR1 and ESR2 to the cell membrane, MAPK3/1 phosphorylation and proliferation of cultured immature rat Sertoli cells. Biol Reprod 2008; 78(1): 101–114.

    Article  CAS  PubMed  Google Scholar 

  20. Gunawan A, Kaewmala K, Uddin MJ, Cinar MU, Tesfaye D, Phatsara C, Tholen E, Looft C, Schellander K. Association study and expression analysis of porcine ESR1 as a candidate gene for boar fertility and sperm quality. Anim Reprod Sci 2011; 128(1-4): 11–21.

    Article  CAS  PubMed  Google Scholar 

  21. Filipiak E, Suliborska D, Laszczynska M, Walczak-Jedrzejowska R, Oszukowska E, Marchlewska K, Kula K, Slowikowska-Hilczer J. Estrogen receptor alpha localization in the testes of men with normal spermatogenesis. Folia Histochem Cytobiol 2013; 50(3): 340–345.

    Article  PubMed  Google Scholar 

  22. Gonzalez CR, Muscarsel Isla ML, Leopardo NP, Willis MA, Dorfman VB, Vitullo AD. Expression of androgen receptor, estrogen receptors alpha and beta and aromatase in the fetal, perinatal, prepubertal and adult testes of the South American plains Vizcacha, Lagostomus maximus (Mammalia, Rodentia). J Reprod Dev 2012; 58(6): 629–635.

    Article  CAS  PubMed  Google Scholar 

  23. Schoen J, Sharbati S, Ritter J, Jewgenow K. Feline gonads exhibit tissue specific alternative splicing of oestrogen receptor alpha (ESR1). Reprod Domest Anim 2012; 47 Suppl 6: 30–34.

    Article  Google Scholar 

  24. Moon JH, Yoo DY, Jo YK, Kim GA, Jung HY, Choi JH, Hwang IK, Jang G. Unilateral cryptorchidism induces morphological changes of testes and hyperplasia of Sertoli cells in a dog. Lab Anim Res 2014; 30(4): 185–189.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Makinen S, Makela S, Weihua Z, Warner M, Rosenlund B, Salmi S, Hovatta O, Gustafsson JA. Localization of oestrogen receptors alpha and beta in human testis. Mol Hum Reprod 2001; 7(6): 497–503.

    Article  CAS  PubMed  Google Scholar 

  26. Saunders FT, Sharpe RM, Williams K, Macpherson S, Urquart H, Irvine DS, Millar MR. Differential expression of oestrogen receptor alpha and beta proteins in the testes and male reproductive system of human and non-human primates. Mol Hum Reprod 2001; 7(3): 227–236.

    Article  CAS  PubMed  Google Scholar 

  27. Pelletier G, El-Alfy M. Immunocytochemical localization of estrogen receptors alpha and beta in the human reproductive organs. J Clin Endocrinol Metab 2000; 85(12): 4835–4840.

    CAS  PubMed  Google Scholar 

  28. Mizuno K, Kojima Y, Kurokawa S, Kamisawa H, Kohri K, Hayashi Y. Altered expression and localization of estrogen receptors alpha and beta in the testes of a cryptorchid rat model. Urology 2011; 77(1): 251.

    Article  PubMed  Google Scholar 

  29. Hermanowicz A, Matuszczak E, Debek W, Dzienis-Koronkiewicz E, Komarowska M, Oksiuta M, Kowalewska J, Milewski R. Expression of estrogen receptors a and a in paratesticular tissues in boys operated on for unilateral cryptorchidism between the 1st and 4th years of life. Med Sci Monit 2012; 18(10): CR630-CR634.

    Google Scholar 

  30. Hejmej A, Bilihska B. The effects of cryptorchidism on the regulation of steroidogenesis and gap junctional communication in equine testes. Endokrynol Pol 2008; 59(2): 112–118.

    PubMed  Google Scholar 

  31. Robertson JA, Farnell Y, Lindahl LS, Ing NH. Estradiol up-regulates estrogen receptor messenger ribonucleic acid in endometrial carcinoma (Ishikawa) cells by stabilizing the message. J Mol Endocrinol 2002; 29(1): 125–135.

    Article  CAS  PubMed  Google Scholar 

  32. Couse JE, Mahato D, Eddy EM, Korach KS. Molecular mechanism of estrogen action in the male: insights from the estrogen receptor null mice. Reprod Fertil Dev 2001; 13(4): 211–219.

    Article  CAS  PubMed  Google Scholar 

  33. Mahato D, Goulding EH, Korach KS, Eddy EM. Spermatogenic cells do not require estrogen receptor-alpha for development or function. Endocrinology 2000; 141(3): 1273–1276.

    Article  CAS  PubMed  Google Scholar 

  34. Farinola MA, Gown AM, Judson K, Ronnett BM, Barry TS, Movahedi-Lankarani S, Vang R. Estrogen receptor alpha and progesterone receptor expression in ovarian adult granulosa cell tumors and Sertoli-Leydig cell tumors. Int J Gynecol Pathol 2007; 26(4): 375–382.

    Article  PubMed  Google Scholar 

  35. Dube JY, Tremblay RR. Search for progesterone receptors in testes from various animal species. Mol Cell Endocrinol 1979; 16(1): 39–44.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy and Cell Biology, College of Veterinary Medicine, Seoul National University, Seoul, 08826, Korea

    Hyo Young Jung, Dae Young Yoo & In Koo Hwang

  2. Laboratory of Theriogenology and Biotechnology, Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Seoul National University, Seoul, 08826, Korea

    Young Kwang Jo, Geon A. Kim & Goo Jang

  3. Department of Veterinary Internal Medicine and Geriatrics, College of Veterinary Medicine, Kangwon National University, Chuncheon, 24341, Korea

    Jin Young Chung

  4. Department of Anatomy, College of Veterinary Medicine, Kangwon National University, Chuncheon, 24341, Korea

    Jung Hoon Choi

  5. BK21 PLUS Program for Creative Veterinary Science Research, and Research Institute for Veterinary Science, Seoul National University, Seoul, 08826, Korea

    Hyo Young Jung, Dae Young Yoo, Young Kwang Jo, Geon A. Kim, Goo Jang & In Koo Hwang

  6. Institute of Green Bio Science & Technology, Seoul National University, Pyeong Chang Kangwon do, Korea

    Goo Jang

  7. Emergence Center for Food-Medicine Personalized Therapy System, Advanced Institutes of Convergence Technology, Seoul National University, Gyeonggi-do, Korea

    Goo Jang

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  1. Hyo Young Jung
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Jung, H.Y., Yoo, D.Y., Jo, Y.K. et al. Differential expression of estrogen receptor α and progesterone receptor in the normal and cryptorchid testis of a dog. Lab Anim Res 32, 128–132 (2016). https://doi.org/10.5625/lar.2016.32.2.128

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  • DOI: https://doi.org/10.5625/lar.2016.32.2.128

Keywords

Laboratory Animal Research

ISSN: 2233-7660