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Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Anti-Müllerian hormone receptor type 2 (AMHR2) expression in bovine oviducts and endometria: comparison of AMHR2 mRNA and protein abundance between old Holstein and young and old Wagyu females

Raihana Nasrin Ferdousy A , Onalenna Kereilwe A and Hiroya Kadokawa https://orcid.org/0000-0002-8454-9601 A B
+ Author Affiliations
- Author Affiliations

A Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi-shi, Yamaguchi-ken 1677-1, Japan.

B Corresponding author. Email address: hiroya@yamaguchi-u.ac.jp

Reproduction, Fertility and Development 32(8) 738-747 https://doi.org/10.1071/RD19121
Submitted: 29 March 2019  Accepted: 2 December 2019   Published: 27 April 2020

Abstract

Anti-Müllerian hormone (AMH) is a glycoprotein produced by granulosa cells of preantral and small antral follicles that has multiple important roles in the ovaries. Recent studies have revealed extragonadal AMH regulation of gonadotrophin secretion from bovine gonadotrophs. In this study we investigated whether the primary receptor for AMH, AMH receptor type 2 (AMHR2), is expressed in bovine oviducts and endometria. Reverse transcription–polymerase chain reaction detected expression of AMHR2 mRNA in oviductal and endometrial specimens. Western blotting and immunohistochemistry were performed to analyse AMHR2 protein expression using anti-bovine AMHR2 antibody. Immunohistochemistry revealed robust AMHR2 expression in the tunica mucosa of the ampulla and isthmus, as well as in the glandular and luminal epithelium of the endometrium. AMHR2 mRNA (measured by real-time polymerase chain reaction) and AMHR2 protein expression in these layers did not significantly differ among oestrous phases in adult Wagyu cows (P > 0.1). In addition, AMHR2 mRNA and protein expression in these layers did not differ among old Holsteins (mean (±s.e.m.) age 91.9 ± 6.4 months) and young (26.6 ± 0.8 months) and old (98.8 ± 10.2 months) Wagyu cows. Therefore, AMHR2 is expressed in bovine oviducts and endometria.

Additional keywords: age, breed, extragonadal role, Müllerian-inhibiting substance, ruminant.


References

Arouche, N., Picard, J. Y., Monniaux, D., Jamin, S. P., Vigier, B., Josso, N., Cate, R. L., di Clemente, N., and Taieb, J. (2015). The BOC ELISA, a ruminant-specific AMH immunoassay, improves the determination of plasma AMH concentration and its correlation with embryo production in cattle. Theriogenology 84, 1397–1404.
The BOC ELISA, a ruminant-specific AMH immunoassay, improves the determination of plasma AMH concentration and its correlation with embryo production in cattle.Crossref | GoogleScholarGoogle Scholar | 26298408PubMed |

Besenfelder, U., Havlicek, V., and Brem, G. (2012). Role of the oviduct in early embryo development. Reprod. Domest. Anim. 47, 156–163.
Role of the oviduct in early embryo development.Crossref | GoogleScholarGoogle Scholar | 22827365PubMed |

Bhide, P., and Homburg, R. (2016). Anti-Müllerian hormone and polycystic ovary syndrome. Best Pract. Res. Clin. Obstet. Gynaecol. 37, 38–45.
Anti-Müllerian hormone and polycystic ovary syndrome.Crossref | GoogleScholarGoogle Scholar | 27103234PubMed |

Binelli, M., Gonella-Diaza, A. M., Mesquita, F. S., and Membrive, C. M. B. (2018). Sex steroid-mediated control of oviductal function in cattle. Biology (Basel) 7, 15.
Sex steroid-mediated control of oviductal function in cattle.Crossref | GoogleScholarGoogle Scholar |

Croxatto, H. B. (2002). Physiology of gamete and embryo transport through the Fallopian tube. Reprod. Biomed. Online 4, 160–169.
Physiology of gamete and embryo transport through the Fallopian tube.Crossref | GoogleScholarGoogle Scholar | 12470580PubMed |

Dewailly, D., Andersen, C. Y., Balen, A., Broekmans, F., Dilaver, N., Fanchin, R., Griesinger, G., Kelsey, T. W., La Marca, A., Lambalk, C., Mason, H., Nelson, S. M., Visser, J. A., Wallace, W. H., and Anderson, R. A. (2014). The physiology and clinical utility of anti-Müllerian hormone in women. Hum. Reprod. Update 20, 370–385.
The physiology and clinical utility of anti-Müllerian hormone in women.Crossref | GoogleScholarGoogle Scholar | 24430863PubMed |

El-Sheikh Ali, H., Kitahara, G., Nibe, K., Yamaguchi, R., Horii, Y., Zaabel, S., and Osawa, T. (2013). Plasma anti-Müllerian hormone as a biomarker for bovine granulosa–theca cell tumors: comparison with immunoreactive inhibin and ovarian steroid concentrations. Theriogenology 80, 940–949.
Plasma anti-Müllerian hormone as a biomarker for bovine granulosa–theca cell tumors: comparison with immunoreactive inhibin and ovarian steroid concentrations.Crossref | GoogleScholarGoogle Scholar | 23978493PubMed |

Faure, E., Gouédard, L., Imbeaud, S., Cate, R., Picard, J. Y., Josso, N., and di Clemente, N. (1996). Mutant isoforms of the anti-Müllerian hormone type II receptor are not expressed at the cell membrane. J. Biol. Chem. 271, 30571–30575.
Mutant isoforms of the anti-Müllerian hormone type II receptor are not expressed at the cell membrane.Crossref | GoogleScholarGoogle Scholar | 8940028PubMed |

Garrel, G., Racine, C., L’Hôte, D., Denoyelle, C., Guigon, C. J., di Clemente, N., and Cohen-Tannoudji, J. (2016). Anti-Müllerian hormone: a new actor of sexual dimorphism in pituitary gonadotrope activity before puberty. Sci. Rep. 6, 23790.
Anti-Müllerian hormone: a new actor of sexual dimorphism in pituitary gonadotrope activity before puberty.Crossref | GoogleScholarGoogle Scholar | 27030385PubMed |

Herath, S., Williams, E. J., Lilly, S. T., Gilbert, R. O., Dobson, H., Bryant, C. E., and Sheldon, I. M. (2007). Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction 134, 683–693.
Ovarian follicular cells have innate immune capabilities that modulate their endocrine function.Crossref | GoogleScholarGoogle Scholar | 17965259PubMed |

Hernandez-Medrano, J. H., Campbell, B. K., and Webb, R. (2012). Nutritional influences on folliculogenesis. Reprod. Domest. Anim. 47, 274–282.
Nutritional influences on folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 22827381PubMed |

Hirayama, H., Naito, A., Fujii, T., Sugimoto, M., Takedomi, T., Moriyasu, S., Sakai, H., and Kageyama, S. (2019). Effects of genetic background on responses to superovulation in Japanese Black cattle. J. Vet. Med. Sci. 81, 373–378.
Effects of genetic background on responses to superovulation in Japanese Black cattle.Crossref | GoogleScholarGoogle Scholar | 30643104PubMed |

Hirschhorn, T., di Clemente, N., Amsalem, A. R., Pepinsky, R. B., Picard, J. Y., Smorodinsky, N. I., Cate, R. L., and Ehrlich, M. (2015). Constitutive negative regulation in the processing of the anti-Müllerian hormone receptor II. J. Cell Sci. 128, 1352–1364.
Constitutive negative regulation in the processing of the anti-Müllerian hormone receptor II.Crossref | GoogleScholarGoogle Scholar | 25663701PubMed |

Hugentobler, S. A., Sreenan, J. M., Humpherson, P. G., Leese, H. J., Diskin, M. G., and Morris, D. G. (2010). Effects of changes in the concentration of systemic progesterone on ions, amino acids and energy substrates in cattle oviduct and uterine fluid and blood. Reprod. Fertil. Dev. 22, 684–694.
Effects of changes in the concentration of systemic progesterone on ions, amino acids and energy substrates in cattle oviduct and uterine fluid and blood.Crossref | GoogleScholarGoogle Scholar | 20353728PubMed |

Hunter, R. H. (2005). The Fallopian tubes in domestic mammals: how vital is their physiological activity? Reprod. Nutr. Dev. 45, 281–290.
The Fallopian tubes in domestic mammals: how vital is their physiological activity?Crossref | GoogleScholarGoogle Scholar | 15982454PubMed |

Josso, N. (2019). Anti-Müllerian hormone: a look back and ahead. Reproduction 157, F81–F89.
Anti-Müllerian hormone: a look back and ahead.Crossref | GoogleScholarGoogle Scholar |

Kadokawa, H., and Martin, G. B. (2006). A new perspective on management of reproduction in dairy cows: the need for detailed metabolic information, an improved selection index and extended lactation. J. Reprod. Dev. 52, 161–168.
A new perspective on management of reproduction in dairy cows: the need for detailed metabolic information, an improved selection index and extended lactation.Crossref | GoogleScholarGoogle Scholar | 16538035PubMed |

Kamomae, H. (2012). Reproductive disturbance. In ‘Veterinary Theriogenology’. (Eds T. Nakao, S. Tsumagari, and S. Katagiri.) pp. 283–340. (Buneidou Press: Tokyo, Japan.) [In Japanese]

Kelly, R. W., Carr, G. G., and Critchley, H. O. (1997). A cytokine switch induced by human seminal plasma: an immune modulation with implications for sexually transmitted disease. Hum. Reprod. 12, 677–681.
A cytokine switch induced by human seminal plasma: an immune modulation with implications for sexually transmitted disease.Crossref | GoogleScholarGoogle Scholar | 9159423PubMed |

Kereilwe, O., and Kadokawa, H. (2019). Bovine gonadotrophs express anti-Mullerian hormone (AMH): comparison of AMH mRNA and protein expression levels between old Holsteins and young and old Japanese Black females. Reprod. Fertil. Dev. 31, 810–819.
Bovine gonadotrophs express anti-Mullerian hormone (AMH): comparison of AMH mRNA and protein expression levels between old Holsteins and young and old Japanese Black females.Crossref | GoogleScholarGoogle Scholar | 30554590PubMed |

Kereilwe, O., Pandey, K., Borromeo, V., and Kadokawa, H. (2018). Anti-Müllerian hormone receptor type 2 is expressed in gonadotrophs of postpubertal heifers to control gonadotrophin secretion. Reprod. Fertil. Dev. 30, 1192–1203.
Anti-Müllerian hormone receptor type 2 is expressed in gonadotrophs of postpubertal heifers to control gonadotrophin secretion.Crossref | GoogleScholarGoogle Scholar | 29533759PubMed |

Kim, S. Y., Moon, H. M., Lee, M. K., Chung, Y. J., Song, J. Y., Cho, H. H., Kim, M. R., and Kim, J. H. (2018). The expression of Müllerian inhibiting substance/anti-Müllerian hormone type II receptor in myoma and adenomyosis. Obstet. Gynecol. Sci. 61, 127–134.
The expression of Müllerian inhibiting substance/anti-Müllerian hormone type II receptor in myoma and adenomyosis.Crossref | GoogleScholarGoogle Scholar | 29372159PubMed |

Kim, S. M., Kim, Y. O., Lee, M. K., Chung, Y. J., Jeung, I. C., Kim, M. R., and Kim, J. H. (2019). Müllerian inhibiting substance/anti-Müllerian hormone type II receptor protein and mRNA expression in the healthy and cancerous endometria. Oncol. Lett. 17, 532–538.
Müllerian inhibiting substance/anti-Müllerian hormone type II receptor protein and mRNA expression in the healthy and cancerous endometria.Crossref | GoogleScholarGoogle Scholar | 30655798PubMed |

Koizumi, M., and Kadokawa, H. (2017). Positive correlations of age and parity with plasma anti-Müllerian hormone concentrations in Japanese Black cows. J. Reprod. Dev. 63, 205–209.
Positive correlations of age and parity with plasma anti-Müllerian hormone concentrations in Japanese Black cows.Crossref | GoogleScholarGoogle Scholar | 28132978PubMed |

Lyttle Schumacher, B. M., Jukic, A. M. Z., and Steiner, A. Z. (2018). Antimullerian hormone as a risk factor for miscarriage in naturally conceived pregnancies. Fertil. Steril. 109, 1065–1071.e1.
Antimullerian hormone as a risk factor for miscarriage in naturally conceived pregnancies.Crossref | GoogleScholarGoogle Scholar | 29871793PubMed |

Miyamoto, Y., Skarzynski, D. J., and Okuda, K. (2000). Is tumor necrosis factor α a trigger for the initiation of endometrial prostaglandin F2α release at luteolysis in cattle? Biol. Reprod. 62, 1109–1115.
Is tumor necrosis factor α a trigger for the initiation of endometrial prostaglandin F release at luteolysis in cattle?Crossref | GoogleScholarGoogle Scholar | 10775155PubMed |

Mossa, F., and Ireland, J. J. (2019). Physiology and endocrinology symposium: anti-Mullerian hormone: a biomarker for the ovarian reserve, ovarian function, and fertility in dairy cows. J. Anim. Sci. 97, 1446–1455.
Physiology and endocrinology symposium: anti-Mullerian hormone: a biomarker for the ovarian reserve, ovarian function, and fertility in dairy cows.Crossref | GoogleScholarGoogle Scholar | 30668706PubMed |

Nahar, A., and Kadokawa, H. (2017). Expression of macrophage migration inhibitory factor (MIF) in bovine oviducts is higher in the postovulatory phase than during the oestrus and luteal phase. Reprod. Fertil. Dev. 29, 1521–1529.
Expression of macrophage migration inhibitory factor (MIF) in bovine oviducts is higher in the postovulatory phase than during the oestrus and luteal phase.Crossref | GoogleScholarGoogle Scholar | 27465152PubMed |

Nahar, A., Maki, S., and Kadokawa, H. (2013). Suppressed expression of granulocyte macrophage colony-stimulating factor in oviduct ampullae of obese cows. Anim. Reprod. Sci. 139, 1–8.
Suppressed expression of granulocyte macrophage colony-stimulating factor in oviduct ampullae of obese cows.Crossref | GoogleScholarGoogle Scholar | 23611472PubMed |

Osoro, K., and Wright, I. A. (1992). The effect of body condition, live weight, breed, age, calf performance, and calving date on reproductive performance of spring-calving beef cows. J. Anim. Sci. 70, 1661–1666.
The effect of body condition, live weight, breed, age, calf performance, and calving date on reproductive performance of spring-calving beef cows.Crossref | GoogleScholarGoogle Scholar | 1634389PubMed |

Paradisi, R., Vicenti, R., Macciocca, M., Seracchioli, R., Rossi, S., and Fabbri, R. (2016). High cytokine expression and reduced ovarian reserve in patients with Hodgkin lymphoma or non-Hodgkin lymphoma. Fertil. Steril. 106, 1176–1182.
High cytokine expression and reduced ovarian reserve in patients with Hodgkin lymphoma or non-Hodgkin lymphoma.Crossref | GoogleScholarGoogle Scholar | 27430206PubMed |

Pfeiffer, K. E., Jury, L. J., and Larson, J. E. (2014). Determination of anti-Müllerian hormone at estrus during a synchronized and a natural bovine estrous cycle. Domest. Anim. Endocrinol. 46, 58–64.
Determination of anti-Müllerian hormone at estrus during a synchronized and a natural bovine estrous cycle.Crossref | GoogleScholarGoogle Scholar | 24211073PubMed |

Pohler, K. G., Geary, T. W., Atkins, J. A., Perry, G. A., Jinks, E. M., and Smith, M. F. (2012). Follicular determinants of pregnancy establishment and maintenance. Cell Tissue Res. 349, 649–664.
Follicular determinants of pregnancy establishment and maintenance.Crossref | GoogleScholarGoogle Scholar | 22427068PubMed |

Poole, D. H., Ocón-Grove, O. M., and Johnson, A. L. (2016). Anti-Müllerian hormone (AMH) receptor type II expression and AMH activity in bovine granulosa cells. Theriogenology 86, 1353–1360.
Anti-Müllerian hormone (AMH) receptor type II expression and AMH activity in bovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 27268296PubMed |

Quayle, A. J. (2002). The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells. J. Reprod. Immunol. 57, 61–79.
The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells.Crossref | GoogleScholarGoogle Scholar | 12385834PubMed |

Rekawiecki, R., Rutkowska, J., and Kotwica, J. (2012). Identification of optimal housekeeping genes for examination of gene expression in bovine corpus luteum. Reprod. Biol. 12, 362–367.
Identification of optimal housekeeping genes for examination of gene expression in bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 23229008PubMed |

Rey, R., Lukas-Croisier, C., Lasala, C., and Bedecarras, P. (2003). AMH/MIS: what we know already about the gene, the protein and its regulation. Mol. Cell. Endocrinol. 211, 21–31.
AMH/MIS: what we know already about the gene, the protein and its regulation.Crossref | GoogleScholarGoogle Scholar | 14656472PubMed |

Ribeiro, E. S., Bisinotto, R. S., Lima, F. S., Greco, L. F., Morrison, A., Kumar, A., Thatcher, W. W., and Santos, J. E. (2014). Plasma anti-Müllerian hormone in adult dairy cows and associations with fertility. J. Dairy Sci. 97, 6888–6900.
Plasma anti-Müllerian hormone in adult dairy cows and associations with fertility.Crossref | GoogleScholarGoogle Scholar | 25173464PubMed |

Scheffer, J. A. B., Scheffer, B., Scheffer, R., Florencio, F., Grynberg, M., and Lozano, D. M. (2018). Are age and anti-Müllerian hormone good predictors of ovarian reserve and response in women undergoing IVF? JBRA Assist. Reprod. 22, 215–220.
Are age and anti-Müllerian hormone good predictors of ovarian reserve and response in women undergoing IVF?Crossref | GoogleScholarGoogle Scholar |

Sefrioui, O., Madkour, A., Aboulmaouahib, S., Kaarouch, I., and Louanjli, N. (2019). Women with extreme low AMH values could have in vitro fertilization success. Gynecol. Endocrinol. 35, 170–173.
Women with extreme low AMH values could have in vitro fertilization success.Crossref | GoogleScholarGoogle Scholar | 30324831PubMed |

Seifer, D. B., and Merhi, Z. (2014). Is AMH a regulator of follicular atresia? J. Assist. Reprod. Genet. 31, 1403–1407.
Is AMH a regulator of follicular atresia?Crossref | GoogleScholarGoogle Scholar | 25193290PubMed |

Signorile, P. G., Petraglia, F., and Baldi, A. (2014). Anti-Mullerian hormone is expressed by endometriosis tissues and induces cell cycle arrest and apoptosis in endometriosis cells. J. Exp. Clin. Cancer Res. 33, 46.
Anti-Mullerian hormone is expressed by endometriosis tissues and induces cell cycle arrest and apoptosis in endometriosis cells.Crossref | GoogleScholarGoogle Scholar | 24886254PubMed |

Tang, L., Zhang, H., Lei, L., Gong, S., Zhou, Z., Baseman, J., and Zhong, G. (2013). Oviduct infection and hydrosalpinx in dba1/j mice is induced by intracervical but not intravaginal inoculation with Chlamydia muridarum. PLoS One 8, e71649.
Oviduct infection and hydrosalpinx in dba1/j mice is induced by intracervical but not intravaginal inoculation with Chlamydia muridarum.Crossref | GoogleScholarGoogle Scholar | 24482673PubMed |

Tarasconi, B., Tadros, T., Ayoubi, J. M., Belloc, S., de Ziegler, D., and Fanchin, R. (2017). Serum antimullerian hormone levels are independently related to miscarriage rates after in vitro fertilization–embryo transfer. Fertil. Steril. 108, 518–524.
Serum antimullerian hormone levels are independently related to miscarriage rates after in vitro fertilization–embryo transfer.Crossref | GoogleScholarGoogle Scholar | 28865551PubMed |

Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalisation of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034.1–research0034.11.
Accurate normalisation of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar |

Walker, C. G., Meier, S., Mitchell, M. D., Roche, J. R., and Littlejohn, M. (2009). Evaluation of real-time PCR endogenous control genes for analysis of gene expression in bovine endometrium. BMC Mol. Biol. 10, 100.
Evaluation of real-time PCR endogenous control genes for analysis of gene expression in bovine endometrium.Crossref | GoogleScholarGoogle Scholar | 19878604PubMed |