Anti-Müllerian Hormone Expression in the Ovarian Follicles and Factors Related to Serum Anti-Müllerian Hormone Concentrations in the Domestic Queens

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Publiée : Απρ 20, 2024
DOI : https://doi.org/10.12681/jhvms.33352
A Gözer
Hatay Mustafa Kemal University, Faculty of Veterinary Medicine, Department of Obstetrics and Gynaecology, Hatay, Turkey
G Dogruer
Hatay Mustafa Kemal University, Faculty of Veterinary Medicine, Department of Obstetrics and Gynaecology, Hatay, Turkey
I Gokcek
Hatay Mustafa Kemal University, Faculty of Veterinary Medicine, Department of Physiology, Hatay, Turkey
T Kutlu
Hatay Mustafa Kemal University, Faculty of Veterinary Medicine, Department of Pathology, Hatay, Turkey
O Bahan
Yozgat Bozok University, Faculty of Veterinary Medicine, Department of Obstetrics and Gynaecology, Yozgat, Turkey
I Pır Yagcı
Kırıkkale University, Faculty of Veterinary Medicine, Department of Obstetrics and Gynaecology, Kırıkkale, Turkey
Résumé

Antimüllerian Hormone (AMH) is a glycoprotein with 140 kDa molecular weight secreted by the granulosa cells, belonging to the transforming growth factor-β family. Antimüllerian Hormone plays a crucial role in folliculogenesis. The present study aimed to reveal (1) the relationship between age, body weight, sexual cycle, and ovariohysterectomy with the serum antimüllerian hormone concentrations and (2) ovarian expressions of the AMH in the ovarian follicles. Serum AMH concentrations were determined by the commercial ELISA (Beckman Coulter Gen II) immunoassay. The immunohistochemical method determined ovarian expressions of the AMH in the granulosa cells. Twenty cats admitted to Hatay Mustafa Kemal University Veterinary Faculty of Obstetrics and Gynaecology Clinics were included in the current study. Cats were allocated to three groups according to the period of the sexual cycle, age, and body weight. The sexual cycle was determined by the estradiol 17-ß and progesterone measurement. Blood samples were collected into tubes without anticoagulant to determine serum AMH concentration at preoperative (Day 0), postoperative 3rd and 10th days. There was a decrease in the third postoperative days of AMH levels compared to the preoperative level (0th) (p<0.001). No statistical differences were found between postpartum 3rd and 10th days (p>0.05). It was observed that the period of the sexual cycle, age, and body weight did not affect the AMH level (p>0.05). In immunohistochemical analyses, it was observed that a mild AMH expression was first observed in granulosa cells of the primary follicles. Moderate AMH expressions were observed in the granulosa cells of the secondary follicles. While strong AMH expression was observed in the cumulus cells of the antral follicles, mild AMH expressions were in the mural granulosa cells of the antral follicles. In conclusion, ovariohysterectomy was the only determinant of serum AMH concentration, and AMH expression in the ovarian follicles shows the stage-dependent characteristic in domestic cats.

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Références
Alkan-Karakaş K, Ceylan A, Alkan H, Özen D, Bayraktaroğlu AG, Kaymaz M (2019) Immunohistochemical and qPCR determination of the expression and serum level of antimüllerian Hormone in pre-pubertal, intact and ovarian remnant syndrome detected bitches. Reprod Domest Anim 54: 979-986.
Almeida J, Ball BA, Conley AJ, Place NJ, Liu IKM, Scholtz EL, Moeller BC (2011) Biological and clinical significance of anti-Müllerian hormone determination in blood serum of the mare. Theriogenology 76(8): 1393-1403.
Almeida FR, Costermans NG, Soede NM, Bunschoten A, Keijer J, Kemp B, Teerds KJ (2018) Presence of anti-Müllerian hormone (AMH) during follicular development in the porcine ovary. PLoS One, 13(7), e0197894.
Anadol E, Gultiken N, Yarim GF, Karaca E, Kanca H, Yarim M (2020) Investigation of diagnostic use of serum anti-Müllerian hormone concentration in dioestrus and anoestrus bitches before and after ovariohysterectomy and the relationship with ovarian follicle numbers. Pol J Vet Sci 23(3).
Axnér E, Holst BS (2015) Concentrations of anti-Müllerian hormone in the domestic cat. Relation with spay or neuter status and serum estradiol. Theriogenology83(5): 817-821.
Baarends WM, Uilenbroek JT, Kramer PIET, Hoogerbrugge JW, Van Leeuwen EC, Themmen AP, Groootegoed JA (1995) Anti-müllerian Hormone and anti-müllerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinol136(11): 4951-4962.
Ball BA, Ali HES, Scoggin KE, Riddle WT, Schnobrich M, Bradekamp E, Troedsson MHT (2019) Relationship between anti-Müllerian hormone and fertility in the mare. Theriogenology125: 335-341.
Bezard J, Vigier B, Tran D, Mauleon P, Josso N (1987) Immunocytochemical study of anti-Müllerian Hormone in sheep ovarian follicles during fetal and post-natal development. Reprod80(2): 509-516.
Böhmer F, Erber K, Ewringmann A, Klein R, Reese S, Böhmer C, Walter B (2022) Anti‐Müllerian hormone concentrations in female rabbits and its relation to spay status, pseudopregnancy, and ovarian follicle numbers. Reprod Domest Anim 57(12): 1636-1643.
Bristol-Gould S, Woodruff TK (2006) Folliculogenesis in the domestic cat (Felis catus). Theriogenology66(1): 5-13.
Cate RL, Mattaliano RJ, Hession C, Tizard R, Farber NM, Cheung A, Donahoe PK (1986) Isolation of the bovine and human genes for Müllerian inhibiting substance and expression of the human gene in animal cells. Cell 45(5): 685-698.
Convissar S, Armouti M, Fierro MA, Winston NJ, Scoccia H, Zamah AM, Stocco C (2017) Regulation of AMH by oocyte-specific growth factors in human primary cumulus cells. Reprod 154(6): 745-753.
Durlinger ALL, Visser JA, Themmen APN (2002) Regulation of ovarian function: The role of anti-Müllerian Hormone. Reprod 124: 601-609.
Ferré-Dolcet L, Ferro S, Contiero B, Fontaine C, Badon T, Gelli D, Romagnoli S (2022) Clinical use of Anti-Müllerian Hormone to monitor resumption of ovarian activity following removal of a 4.7 mg deslorelin implant in queens. Vet Res Commun 1-8.
Flock U, Fischer S, Weeger J, Reese S, Walter B (2022a) Anti-Müllerian hormone as a diagnostic tool to identify queens with ovarian remnant syndrome. J Fel Med Surg 1098612X221099195.
Flock U, Reese S, Otzdorff C, Klein R, Walter B (2022b) Anti-Müllerian hormone concentrations in queens throughout the estrous cycle. Domest Anim Endocrinol81: 106749.
Fujihara M, Comizzoli P, Keefer CL, Wildt DE, Songsasen N (2014) Epidermal growth factor (EGF) sustains in vitro primordial follicle viability by enhancing stromal cell proliferation via MAPK and PI3K pathways in the prepubertal, but not adult, cat ovary. Biol Reprod90(4): 86-1.
Grøndahl ML, Nielsen ME, Dal Canto MB, Fadini R, Rasmussen IA, Westergaard LG, Andersen CY (2011) Anti-Müllerian hormone remains highly expressed in human cumulus cells during the final stages of folliculogenesis. Reprod Biomed Online 22(4): 389-398.
Gozer A, Bahan O, Dogruer G, Kutlu T (2023) Serum antimüllerian hormone concentrations in female cats. Relation with ovarian remnant syndrome, ovarian cysts and gonadectomy status. Theriogenology 200: 106-113.
Gültiken N, Yarim M, Aslan S, Gürler H, Yarim GF, Tuncay M, Schafer-Somi S (2022). Expression of Anti-Müllerian Hormone and Its Type 2 Receptor in the Ovary of Pregnant and Cyclic Domestic Cats. Animals12(7): 877.
Hamouzova P, Cizek P, Novotny R, Bartoskova A, Tichy F (2017) Distribution of mast cells in the feline ovary in various phases of the oestrous cycle. Reprod Domes Anim52(3): 483-486.
Heaps LA, Scudder CJ, Lipscomb VJ, Steinbach SM, Priestnall SL, Martineau H, Garden OA (2017) Serum anti-Müllerian hormone concentrations before and after treatment of an ovarian granulosa cell tumour in a cat. J Felin Med Surg Open Rep3(2): 2055116917722701.
Hehenkamp WJ, Looman CW, Themmen AP, De Jong FH, Te Velde ER, Broekman FJ (2006) Anti-Mullerian hormone levels in the spontaneous menstrual cycle do not show substantial fluctuation. J Clin Endocrinol Metab91(10): 4057-4063.
Hu R, Wang FM, Yu L, Luo Y, Wu X, Li J, Bocca S (2014) Antimüllerian Hormone regulates stem cell factor expression in human granulosa cells. Fertil Steril102(6): 1742-1750.
Ireland JLH, Scheetz D, Jimenez-Krassel F, Themmen APN, Ward F, Lonergan P, Ireland JJ (2008) Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol Reprod, 79(6): 1219-1225.
Jost, A (1953) Problems of fetal endocrinology: the gonadal and hypophyseal hormones. Recent Progr Hormon Res8: 379-413.
Kehoe S, Jewgenow K, Johnston PR, Mbedi S, Braun BC (2021) Signalling pathways and mechanistic cues highlighted by transcriptomic analysis of primordial, primary, and secondary ovarian follicles in domestic cat. Sci Rep 11(1): 1-17.
Kevenaar ME, Meerasahib MF, Kramer P, van de Lang-Born BM, de Jong FH, Groome NP, Visser JA (2006) Serum anti-mullerian hormone levels reflect the size of the primordial follicle pool in mice. Endocrinol 147(7): 3228-3234.
Kitiyanant Y, Saikhun J, Pavasuthipaisit K (2003) Somatic cell nuclear transfer in domestic cat oocytes treated with IGF-I for in vitro maturation. Theriogenology59(8): 1775-1786.
Lahoz B, Alabart JL, Cocero MJ, Monniaux D, Echegoyen E, Snchhez P, Folch J (2014) Anti-Müllerian hormone concentration in sheep and its dependence of age and independence of BMP15 genotype: an endocrine predictor to select the best donors for embryo biotechnologies. Theriogenology81(2): 347-357.
Lapuente C, Faya M, Blanco PG, Grisolia-Romero M, Marchetti C, Gobello C (2023) Anti-Müllerian Hormone in queens: Serum concentrations and total ovarian follicle population. Theriogenology 119: 111-115.
Lebbe M, Woodruff TK (2013) Involvement of androgens in ovarian health and disease. Mol Hum Reprod19(12): 828-837.
McNatty KP, Smith P, Moore LG, Reader K, Lun S, Hanrahan JP, Juengel JL (2005) Oocyte-expressed genes affecting ovulation rate. Mol Cell Endocrinol234(1-2): 57-66.
Monniaux D, Baril G, Laine AL, Jarrier P, Poulin N, Cognie J, Fabre S (2011) Anti-Müllerian hormone as a predictive endocrine marker for embryo production in the goat. Reprod142(6): 845-854.
Monniaux D, Drouilhet L, Rico C, Estienne A, Jarrier P, Touze JL, Fabre S (2012) Regulation of anti-Müllerian hormone production in domestic animals. Reprod Fertil Dev25(1): 1-16.
Moy V, Jindal S, Lieman H, Buyuk E (2015) Obesity adversely affects serum anti-müllerian hormone (AMH) levels in Caucasian women. J Assist Reprod Genet32(9): 1305-1311.
Munsterberg A, Lovell-Badge R (1991) Expression of the mouse anti-mullerian hormone gene suggests a role in both male and female sexual differentiation. Development 113(2): 613-624.
Nilsson E, Rogers N, Skinner MK (2007) Actions of anti-Mullerian Hormone on the ovarian transcriptome to inhibit rimordial to primary follicle transition. Reprod 134(2): 209-221.
Ottosson M. (2017) Anti-Müllerian hormone in canine pyometra.Perego MC, Bellitto N, Maylem ERS, Caloni F, Spicer LJ (2021) Effects of selected hormones and their combination on progesterone and estradiol production and proliferation of feline granulosa cells cultured in vitro. Theriogenology168: 1-12.
Phillips DJ, Woodruff TK (2004) Inhibin: actions and signalling. Growth factors2(1): 13-18.
Pir Yağcı İ, Polat İM, Pekcan M (2016) Evaluation of Age Releated Anti-Müllerian Hormone Variations in Domestic Cat. Kafkas Univ Vet Fak Derg22(5): 729-732.
Place NJ, Hansen BS, Cheraskin JL, Cudney SE, Flanders JA, Newmark AD, Scarlett JM (2011) Measurement of serum anti-Müllerian hormone concentration in female dogs and cats before and after ovariohysterectomy. J Vet Diagn23(3): 524-527.
Rico C, Médigue C, Fabre S, Jarrier P, Bontoux M, Clement F, Monniaux D (2011). Regulation of anti-Müllerian hormone production in the cow: a multiscale study at endocrine, ovarian, follicular, and granulosa cell levels. Biol Reprod84(3): 560-571.
Sahmay S, Usta T, Erel CT, İmamoğlu M, Küçük M, Atakul N, Seyisoğlu H (2012) Is there any correlation between AMH and obesity in premenopausal women? Arch Gynecol Obstet286(3): 661-665.
Saint-Dizier M, Malandain E, Thoumire S, Remy B, Chastant-Maillard S (2007) Expression of Follicle Stimulating Hormone and Luteinizing Hormone Receptors During Follicular Growth in the Domestic Cat Ovary. Mol Reprod Dev 74: 989-996.
Salmon NA, Handyside AH, Joyce IM (2004) Oocyte regulation of anti-Müllerian hormone expression in granulosa cells during ovarian follicle development in mice. Dev Biol266(1): 201-208.
Santos LC, dos Anjos Cordeiro JM, da Silva Santana L, Barbosa EM, Santos BR, da Silva TQM, Silva J. F (2022) Expression profile of the Kisspeptin/Kiss1r system and angiogenic and immunological mediators in the ovary of cyclic and pregnant cats. Domest Anim Endocrinol 78: 106650.
Schäfer-Somi S (2017) Effect of melatonin on the reproductive cycle in female cats: a review of clinical experiences and previous studies. J Feline Med Surg19(1): 5-12.
Skałba P, Cygal A, Madej P, Dąbkowska-Huć A, Sikora J, Martirosian G, Olszancka-Glinianowicz M (2011) Is the plasma anti-Müllerian hormone (AMH) level associated with body weight and metabolic, and hormonal disturbances in women with and without polycystic ovary syndrome? Eur J Obstet Gynecol158(2): 254-259.
Snoeck F, Sarrazin S, Wydooghe E, Van Soom A (2017) Age and anti‐Müllerian hormone levels predict the success of in vitro maturation of cat oocytes. Reprod Domest Anim52: 98-102.
Teh APP, Izzati UZ, Mori K, Fuke N, Hirai T, Kitahara G, Yamaguchi R (2018) Histological and immunohistochemical evaluation of granulosa cells during different stages of folliculogenesis in bovine ovaries. Reprod Domest Anim 53(3): 569-581.
Weenen C, Laven JS, Von Bergh AR, Cranfield M, Groome NP, Visser JA, Themmen AP (2004) Anti‐Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. MHR: Basic science of reproductive medicine10(2): 77-83.
Yıldırım K, Vural MR, Küplülü Ş, Özcan Z, Polat IM (2014) The effects of EGF and IGF-1 on FSH-mediated in vitro maturation of domestic cat oocytes derived from follicular and luteal stages. Reprod Biol14(2): 122-127.
Zhao Z, Guo F, Sun X, He Q, Dai Z, Chen X, Wang J (2018) BMP15 regulates AMH expression via the p38 MAPK pathway in granulosa cells from goat. Theriogenology 118: 72-79
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