Ovarian activity regulation by anti-Müllerian hormone in early stages of human female life, an overview

Authors

  • Małgorzata Jusiakowska-Piputa Department of Human Biological Development, Institute of Anthropology, Faculty of Biology, Adam Mickiewicz University, Poznań, Poland
  • Maria Kaczmarek Department of Human Biological Development, Institute of Anthropology, Faculty of Biology, Adam Mickiewicz University, Poznań, Poland

DOI:

https://doi.org/10.2478/anre-2018-0026

Keywords:

AMH, sex determination, gonad differentitation, folliculogenesis, in vitro fertilization, androgens

Abstract

The present study aimed at describing the anti-Müllerian hormone (AMH), with special focus on molecular background for ovarian activity, in particular the role AMH plays in sex determination and gonadogenesis process in early stages of prenatal life and folliculogenesis in postnatal life. It is a review of the literature currently indexed and abstracted in MEDLINE, SCOPUS and Google Scholars. The process of sex determination and gonad differentiation occurring during embryogenesis was discussed along with underlying molecular mechanisms. In the postnatal life the impact of AMH on the process of folliculogenesis was described. Clinical use of recent findings was shown as well. Genetic studies and molecular analyses have demonstrated that AMH is highly conservative, indicating its significance in reproductive process on the background of evolutionary processes.

Downloads

Download data is not yet available.

References

Al-Asaad I, Chardard D, di Clemente N, Picard JY, Dumond H, Chesnel A, et al. 2013. Mullerian inhibiting substance in the caudate amphibian Pleurodeles waltl. Endocrinology 154(10):3931-36.
View in Google Scholar

Alvaro Mercadal B, Imbert R, Demeestere I, Gervy C, De Leener A, Englert Y et al. 2015. AMH mutations with reduced in vitro bioactivity are related to premature ovarian insufficiency. Hum Reprod 30(5):1196-202.
View in Google Scholar

Baarends WM, van Helmond MJ, Post M, van der Schoot PJ, Hoogerbrugge JW, de Winter JP, et al. 1994. A novel member of the transmembrane serine/threonine kinase receptor family is specifically expressed in the gonads and in mesenchymal cells adjacent to the mullerian duct. Development 120(1):189-197.
View in Google Scholar

Barrionuevo F. 2005. Homozygous Inactivation of Sox9 Causes Complete XY Sex Reversal in Mice. Biol Reprod 74(1):195-201.
View in Google Scholar

Behringer RR, Cate RL, Froelick GJ, Palmiter RD, Brinster RL. 1990. Abnormal sexual development in transgenic mice chronically expressing Müllerian inhibiting substance. Nature 345:167-170.
View in Google Scholar

Biason-Lauber A, Chaboissier MC. 2015. Ovarian development and disease: The known and the unexpected. Semin Cell Dev Biol 45:59-67.
View in Google Scholar

Birk OS, Casiano DE, Wassif CA, Cogliati T, Zhao L, Zhao Y, Grinberg A, Huang S, Kreidberg JA, Parker KL, Porter FD, Westphal H. 2000. The LIM homeobo Xgene Lhx9 is essential for mouse gonad formation. Nature. 24;403(6772):909-13.
View in Google Scholar

Carré-Eusèbe D, di Clemente N, Rey R, Pieau C, Vigier B, Josso N, et al. 1996. Cloning and expression of the chick anti-Mullerian hormone gene. J Biol Chem 271(9):4798-804.
View in Google Scholar

Cate RL, Mattaliano RJ, Hession C, Tizard R, Farber NM, Cheung A, et al. 1986. Isolation of the bovine and human genes for Mullerian inhibiting substance and expression of the human gene in animal cells. Cell 45(5):685-98.
View in Google Scholar

Chaboissier MC, Kobayashi A, Vidal VIP, Lützkendorf S, van Kant HJG, Wegner M, et al. 2004. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131(9):1891-901.
View in Google Scholar

Cohen-Haguenauer O, Picard JY, Mattei MG, Serero S, Nguyen VC, de Tand MF, et al. 1987. Mapping of the gene for anti-Mullerian hormone to the short arm of human chromosome 19. Cytogenet Cell Genet 44(1):2-6.
View in Google Scholar

De Falco T, Capel B. 2009. Gonad morphogenesis in vertebrates: divergent means to a convergent end. Annu Rev Cell Dev Biol 25:457–82.
View in Google Scholar

Dennis NA, Houghton LA, Jones GT, Van Ry AM, Morgan K, Mc Lenna IS. The level of serum anti-mullerian hormone correlates with vitamin D status in men and women but not in boys. J Clin Endocrinol Metab. 2012;97:2450–5.
View in Google Scholar

di Clemente N, Goxe B, Remy JJ, Cate RL, Josso N, Vigier B, et al. 1994. Inhibitory effect of AMH upon the expression of aromatase and LH receptors by cultured granulosa cells of rat and porcine immature ovaries. Endocrine 2:553–58.
View in Google Scholar

di Clemente N, Jamin SP, Lugovskoy A, Carmillo P, Ehrenfels C, Picard JY, et al. 2010. Processing of Anti-Mullerian Hormone Regulates Receptor Activation by a Mechanism Distinct from TGF-β. Mol Endocrinol 24(11):2193-206.
View in Google Scholar

Di Pasquale E, Beck-Peccoz P, Persani L. 2004. Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein- 15 (BMP15) gene. Am J Hum Genet 75(1):106-111.
View in Google Scholar

Dewailly D, Robin,G, Peigne M, Decanter C, Pigny P, Catteau-Jonard S. 2016. Interactions between androgens, FSH, anti-Mullerian hormone and estradiol during folliculogenesis in the human normal and polycystic ovary. Hum Reprod Update 22(6):709-24.
View in Google Scholar

Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. 1996. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383:531-35.
View in Google Scholar

Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, Grootegoed JA, et al. 1999. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology 140(12):5789-96.
View in Google Scholar

Durlinger AL, Visser JA, Themmen AP. 2002. Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 124(5):601-09.
View in Google Scholar

Fowler PA, Flannigan S, Mathers A, Gillanders K, Lea RG, Wood MJ et al. 2009. Gene expression analysis of human fetal ovarian primordial follicle formation. J Clin Endocrinol Metab 94(4):1427-35
View in Google Scholar

Gassner D, Jung R. 2014. First fully automated immunoassay for anti-Mullerian hormone. Clin Chem Lab Med. 52(8):1143–52.
View in Google Scholar

Grinspon RP, Rey RA. 2010. Anti-mullerian hormone and Sertoli cell function in paediatric male hypogonadism. Horm Res Paediatr 73(2):81-92.
View in Google Scholar

Grossman M, Nakaji S, Fallat M, Yong S. 2008. Mullerian inhibiting substance inhibits cytochrome P450 aromataze activity in human granulosa lutein cell culture. Fertil Steril 89(5):1364–70.
View in Google Scholar

Gustafson ML, Lee MM, Scully RE, Moncure AC, Hirakawa T, Goodman A, et al. 1992. Mullerian inhibiting substance as a marker for ovarian sex-cord tumor. N Engl J Med 326(7):466-71.
View in Google Scholar

Halm S, Rocha A, Miura T, Prat F, Zanuy S. 2007. Anti-Mullerian hormone (AMH/ AMH) in the European sea bass: Its gene structure, regulatory elements, and the expression of alternatively-spliced isoforms. Gene 388(1):148-58.
View in Google Scholar

Han X, McShane M, Sahertian R, White C, Ledger W. 2014. Pre-mixing serum samples with assay buffer is a prerequisite for reproducible anti-Mullerian hormone measurement using the Beckman Coulter Gen II assay. Hum Reprod 29(5):1042-1048.
View in Google Scholar

Hoshiya Y, Gupta V, Segev DL, Hoshiya M, Carey JL, Sasur LM, et al. 2003. Mullerian inhibiting substance induces NF kappa B signaling in breast and prostate cancer cells. Mol Cell Endocrinol 211(1-2):43–49.
View in Google Scholar

Josso N, Rey R, Picard JY. 2012. Testicular anti- Mullerian hormone: clinical applications in DSD. Semin Reprod Med 30(5):364-73.
View in Google Scholar

Juula A, Hagena CP, Aksglaedea L, Sřrensena K, Mouritsena A, Frederiksena H, et al. 2012. Endocrine evaluation of reproductive function in girls during infancy, childhood and adolescence. Endocr Dev Basel 22:24–39.
View in Google Scholar

Kuiri-Hanninen T, Kallio S, Seuri R, Tyrvainen E, Liakka A, Tapanainen J, et al. 2011. Postnatal developmental changes in the pituitary-ovarian axis in preterm and term infant girls. J Clin Endocrinol Metab 96(11):3432-39.
View in Google Scholar

La Marca A, Grisendi V, Griesinger G. 2013. How much does AMH really vary in normal women? [pdf] International Journal of Endocrinology. Available at https://www.hindawi.com/journals/ije/2013/959487/cta/ [Accessed 6 July 2018]
View in Google Scholar

La Marca A, Sunkara SK. 2014. Individualization of controlled ovarian stimulation in IVF using ovarian reserve markers: from theory to practice. Hum Reprod Update 20(1):124–140.
View in Google Scholar

Lebbe M, Woodruff TK. 2013. Involvement of androgens in ovarian health and disease. Mol Hum Reprod 19(12):828-37.
View in Google Scholar

Laitinen M, Vuojolainen K, Jaatinen R, Ketola I, Aaltonen J, Lehtonen E, et al. 1998. A novel growth differentiation factor-9 (GDF-9) relat d factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech Dev 78(1-2):135-40.
View in Google Scholar

Lasala C, Carre-Eusebe D, Picard JY, Rey R. 2004. Subcellular and molecular mechanisms regulating anti-Mullerian hormon gene expression in mammalian and nonmammalian species. DNA Cell Biol 23(9):572-85.
View in Google Scholar

Lasala C, Schteingart HF, Arouche N, Bedecarrás P, Grinspon RP, Picard JY, et al. 2011. SOX9 and SF1 are involved in cyclic AMP-mediated upregulation of anti-Mullerian gene expression in the testicular prepubertal Sertoli cell line SMAT1. Am J Physiol Endocrinol Metab 301(3):E539-47.
View in Google Scholar

Li HWR, Ng EHY, Wong BPC, Anderson RA, Ho PC, Yeung WSB. 2012. Correlation between three assay systems for anti-Mullerian hormone (AMH) determination. J Assist Reprod Genet 29(12):1443-46.
View in Google Scholar

Lin YT, Capel B. 2015. Cell fate commitment during mammalian sex determination. Curr Opin Genet Dev 32:144-52.
View in Google Scholar

Long WQ, Ranchin V, Pautier P, Belville C, Denizot P, Cailla H, et al. 2000. Detection of minimal levels of serum anti-Mullerian hormone during follow-up of patients with ovarian granulosa cell tumor by means of a highly sensitive enzyme-linked immunosorbent assay. J Clin Endocrinol Metab 85(2):540-44.
View in Google Scholar

Lukas-Croisier C, Lasala C, Nicaud J, Bedecarrás P, Kumar TR, Dutertre M, et al. 2003. Follicle-stimulating hormone increases testicular Anti-Mullerian hormone (AMH) production through Sertoli cell proliferation and a nonclassical cyclic adenosine 5’monophosphate-mediated activation of the AMH gene. Mol Endocrinol 17(4):550-61.
View in Google Scholar

Massagué J. 1996. TGF beta signaling: Receptors, transducers, and Mad proteins. Cell 85(7):947–50.
View in Google Scholar

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): 613-24.
View in Google Scholar

Neeper M, Lowe R, Galuska S, Hofmann KJ, Smith RG, Elbrecht A. 1996. Molecular cloning of an avian anti-Mullerian hormone homologue. Gene 176(1):203-9.
View in Google Scholar

Nussey S, Whitehead S. 2001. Schematic overview of the differentiation of the internal male and female reproductive tracts from the Wolffian and Mullerian ducts. Box 6.3 Endocrinology: An Integrated Approach. Oxford: BIOS Scientific Publishers. NCBI Bookshelf. A service of the National Library of Medicine, National Institutes of Health.
View in Google Scholar

Oreal E, Mazaud S, Picard JY, Magre S, Carre-Eusebe D. 2002. Different patterns of anti-Mullerian hormone expression, as related to DMRT1, SF-1, WT1, GATA-4, Wnt-4 and Lhx9 expression, in the chick differentiating gonads. Dev Dyn 225(3):221-32.
View in Google Scholar

Pala I, Kluver N, Thorsteinsdottir S, Schartl M, Coelho MM. 2008. Expression pattern of anti-Mullerian hormone (amh) in the hybrid fish complex of Squalius alburnoides. Gene 410(2):249-58.
View in Google Scholar

Pearson K, Long M, Prasad J, Wu YY, Bonifacio M. 2016. Assessment of the Access AMH assay as an automated, high-performance replacement for the AMH Generation II manual ELISA. Reprod Biol Endocrinol 14(1):8.
View in Google Scholar

Pfennig F, Standke A, Gutzeit HO. 2015. The role of Amh signaling in teleost fish-Multiple functions not restricted to the gonads. Gen Comp Endocrinol 223:87-107..
View in Google Scholar

Racine C, Rey R, Forest MG, Louis F, Ferré A, Huhtaniemi I et al. 1998. Receptors for anti-mullerian hormone on Leydig cells are responsible for its effects on steroidogenesis and cell differentiation. Proc Natl Acad Sci USA 95:594-99.
View in Google Scholar

Renaud EJ, MacLaughlin DT, Oliva E, Rueda BR and Donahoe PK. 2005. Endometrial cancer is a receptor-mediated target for Mullerian Inhibiting Substance. Proc Natl Acad Sci USA 102(1):111–116.
View in Google Scholar

Rey RA, Grinspon RP, Gottlieb S, Pasqualini T, Knoblovits P, Aszpis S, et al. 2013. Male hypogonadism: an extended classification based on a developmental, endocrine physiology-based approach. Andrology 1(1):3-16.
View in Google Scholar

Rey RA, Grinspon RP. 2011. Normal male sexual differentiation and aetiology of disorders of sex development. Best Pract Res Clin Endocrinol Metab 25(2):221-38.
View in Google Scholar

Rey RA, Venara M, Coutant R, Trabut JB, Rouleau S, Lahlou N, et al. 2006. Unexpected mosaicism of R201H-GNAS1 mutant-bearing cells in the testes underlie macro-orchidism without sexual precocity in Mc-Cune-Albright syndrome. Hum Mol Genet 15(24):3538-43.
View in Google Scholar

Reynaud K, Cortvrindt R, Verlinde F, De Schepper J, Bourgain C, Smitz J. 2004. Number of ovarian follicles in human fetuses with the 45, X karyotype. Fertil Steril 81(4):1112-19.
View in Google Scholar

Roberts SC, Seav SM, McDade TW, Dominick SA, Gorman JR, Whitcomb BW, et al. 2016. Self-collected dried blood spots as a tool for measuring ovarian reserve in young female cancer survivors. Hum Reprod 31(7):1570-78.
View in Google Scholar

Rodriguez-Mari A, Yan YL, BreMiller RA, Wilsson C, Canestro C, Postlethwait JH. 2005. Characterization and expression pat tern of zebrafish anti-Mullerian hormone (amh) relative to sox9a, sox9b and cyp19a1a, during gonad development. Gene Expression Patterns 5(5):655–67.
View in Google Scholar

Rohayem J, Nieschlag E, Kliesch S, Zitzmann M. 2015. Inhibin B, AMH, but not INSL3, IGF1 or DHEAS support differentiation between constitutional delay of growth and puberty and hypogonadotropic hypogonadism. Andrology 3(5):882-87.
View in Google Scholar

Shi Y, Massagué J. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113(6):685-700.
View in Google Scholar

Smith U, Blader P, Adam J, Ingham PW. 1994. A Simple and efficient procedure for non-isotopick in situ hybridization to sectioned material. Trends Genet 10(3):75-76.
View in Google Scholar

Soyal SM, Amleh A, Dean J. 2000. FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development 127(21):4645-54.
View in Google Scholar

Su HI, Sammel MD, Homer MV, Bu K, Haunschild C, Stanczyk FZ. 2014. Comparability of anti-mullerian hormone levels among commercially available immunoassays. Fertil Steril 101(6):1766–72.
View in Google Scholar

Svingen T, Koopman P.2013. Building the mammalian testis: origins, differentiation, and assembly of the component cell populations. Genes Dev 27(22):2409-26.
View in Google Scholar

Tanaka SS, Nishinakamura R. 2014. Regulation of male sex determination: genital ridge formation and Sry activation in mice. Cell Mol Life Sci 71(24):4781-802.
View in Google Scholar

te Velde ER, Pearson PL. 2002. The variability of female reproductive ageing. Hum Reprod Update 8(2):141–54.
View in Google Scholar

Tehrani FR, Solaymani-Dodaran M, Tohidi M, Gohari MR, Azizi F. 2013. Modeling age at menopause using serum concentration of anti-mullerian hormone. J Clin Endocrinol Metab 98(2):729-35.
View in Google Scholar

Tevosian SG. 2013. Genetic control of ovarian development. Sex Dev 7(1-3):33-45.
View in Google Scholar

van Disseldorp J, Lambalk CB, Kwee J, Looman CW, Eijkemans MJ, Fauser BC, et al. 2010. Comparison of inter- and intra-cycle variability of anti-Mullerian hormone and antral follicle counts. Hum Reprod 25(1):221-27.
View in Google Scholar

van Rooij IAJ, Broekmans FJ, Scheffer GJ, Looman CW, Habbema JD, de Jong FH, et al. 2005. Serum antimullerian hormone levels best reflect the reproductive decline with age in normal women with proven fertility: a longitudinal study. Fertil Steril 83(4):979-87.
View in Google Scholar

van Rooij IAJ, Broekmans FJM, te Velde ER, Fauser BCJM, Bancsi LFJM, Jong FH, et al. 2002. Serum anti-Mullerian hormone levels: a novel measure of ovarian reserve. Hum Reprod 17(12):3065-71.
View in Google Scholar

Vidal VP, Chaboissier MC, de Rooij DG, Schedl A. 2001. Sox9 induces testis development in XX transgenic mice. Nat Genet 28(3):216.
View in Google Scholar

Visser JA, de Jong FH, Laven JSE, Themmen APN. 2006. Anti-Mullerian hormone: a new marker for ovarian function. Reproduction 131(1):1-9.
View in Google Scholar

Visser JA, Themmen AP. 2005. Anti-Mullerian hormone and folliculogenesis. Mol Cell Endocrinol 234(1-2):81-86.
View in Google Scholar

Wallace AM, Faye SA, Fleming R, Nelson SM. 2011. A multicentre evaluation of the new Beckman Coulter anti-Mullerian hormone immunoassay (AMH Gen II). Ann Clin Biochem 48(4):370–73.
View in Google Scholar

Western PS, Harry JL, Graves JA, Sinclair AH. 1999. Temperature-dependent sex determination: upregulation of SOX9 expression after commitment to male development. Dev Dyn 214(3):171-77.
View in Google Scholar

Western PS, Harry JL, Graves JA, Sinclair AH. 1999. Temperature-dependent se Xdetermination in the American alligator: AMH precedes SOX9 expression. Dev Dyn 216(4-5):411-19.
View in Google Scholar

Yigong S, Massagué J. 2003. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113(6):685-700.
View in Google Scholar

Downloads

Published

2018-09-30

How to Cite

Jusiakowska-Piputa, M., & Kaczmarek, M. (2018). Ovarian activity regulation by anti-Müllerian hormone in early stages of human female life, an overview. Anthropological Review, 81(3), 325–340. https://doi.org/10.2478/anre-2018-0026

Issue

Section

Articles

Most read articles by the same author(s)

1 2 3 > >> 

Similar Articles

<< < 1 2 3 4 5 6 7 8 9 10 > >> 

You may also start an advanced similarity search for this article.