355
Views
12
CrossRef citations to date
0
Altmetric
Review

Comparing the role of anti-Müllerian hormone as a marker of FSH action in male and female fertility

, ORCID Icon & ORCID Icon
Pages 203-214 | Received 11 Dec 2018, Accepted 01 Mar 2019, Published online: 18 Mar 2019

References

  • Josso N. Professor Alfred Jost: the builder of modern sex differentiation. Sex Dev. 2008;2(2):55–63.
  • Picard JY, Cate RL, Racine C, et al. The persistent mullerian duct syndrome: an update based upon a personal experience of 157 cases. Sex Dev. 2017;11:109–125.
  • Cate RL, Mattaliano RJ, Hession C, et al. Isolation of the bovine and human genes for Müllerian inhibiting substance and expression of the human gene in animal cells. Cell. 1986;45(5):685–698.
  • Josso N, Lamarre I, Picard JY, et al. Anti-Müllerian hormone in early human development. Early Hum Dev. 1993;33(2):91–99.
  • Edelsztein NY, Racine C, Di Clemente N, et al. Androgens downregulate anti-Mullerian hormone promoter activity in the Sertoli cell through the androgen receptor and intact SF1 sites. Biol Reprod. 2018;99:1303–1312.
  • Lee MM, Donahoe PK, Silverman BL, et al. Measurements of serum Müllerian inhibiting substance in the evaluation of children with nonpalpable gonads. N Engl J Med. 1997;336(21):1480–1486.
  • Lee MM, Misra M, Donahoe PK, et al. MIS/AMH in the assessment of cryptorchidism and intersex conditions. Mol Cell Endocrinol. 2003;211:91–98.
  • Ahmed SF, Keir L, McNeilly J, et al. The concordance between serum anti-Mullerian hormone and testosterone concentrations depends on duration of hCG stimulation in boys undergoing investigation of gonadal function. Clin Endocrinol (Oxf). 2010;72(6):814–819.
  • Grinspon RP, Rey RA. Anti-mullerian hormone and Sertoli cell function in paediatric male hypogonadism. Horm Res Paediatr. 2010;73(2):81–92.
  • Grinspon RP, Bedecarrás P, Ballerini MG, et al. Early onset of primary hypogonadism revealed by serum anti-Müllerian hormone determination during infancy and childhood in trisomy 21. Int J Androl. 2011;34(5pt2):e487–e498.
  • Grinspon RP, Andreone L, Bedecarrás P, et al. Male Central Precocious Puberty: Serum Profile of Anti-Mullerian Hormone and Inhibin B before, during, and after Treatment with GnRH Analogue. Int J Endocrinol. 2013;823064:2013.
  • Josso N, Rey RA, Picard JY. Anti-müllerian hormone: a valuable addition to the toolbox of the pediatric endocrinologist. Int J Endocrinol. 2013;674105:2013.
  • Grinspon RP, Habib C, Bedecarrás P, et al. Compensatory function of the remaining testis is dissociated in boys and adolescents with monorchidism. Eur J Endocrinol. 2016;174(3):399–407.
  • Lindhardt Johansen M, Hagen CP, Johannsen TH, et al. Anti-mullerian hormone and its clinical use in pediatrics with special emphasis on disorders of sex development. Int J Endocrinol. 2013;198698:2013.
  • Grinspon RP, Gottlieb S, Bedecarras P, et al. Anti-Müllerian hormone and testicular function in prepubertal boys with cryptorchidism. Front Endocrinol (Lausanne). 2018;9:182.
  • Bézard J, Vigier B, Tran D, et al. Immunocytochemical study of anti-Müllerian hormone in sheep ovarian follicles during fetal and post-natal development. J Reprod Fertil. 1987;80(2):509–516.
  • Ueno S, Takahashi M, Manganaro TF, et al. Cellular localization of mullerian inhibiting substance in the developing rat ovary. Endocrinology. 1989;124(2):1000–1006.
  • Rajpert-De Meyts E, Jørgensen N, Græm N, et al. Expression of anti-Müllerian hormone during normal and pathological gonadal development: association with differentiation of Sertoli and granulosa cells. J Clin Endocrinol Metab. 1999;84(10):3836–3844.
  • Rey R, Sabourin JC, Venara M, et al. Anti-Mullerian hormone is a specific marker of sertoli- and granulosa-cell origin in gonadal tumors. Hum Pathol. 2000;31(10):1202–1208.
  • Dutertre M, Gouédard L, Xavier F, et al. Ovarian granulosa cell tumors express a functional membrane receptor for anti-Mullerian hormone in transgenic mice. Endocrinology. 2001;142(9):4040–4046.
  • Kuiri-Hänninen T, Kallio S, Seuri R, et al. Postnatal developmental changes in the pituitary-ovarian axis in preterm and term infant girls. J Clin Endocrinol Metab. 2011;96(11):3432–3439.
  • Vigier B, Picard JY, Tran D, et al. Production of anti-Müllerian hormone: another homology between Sertoli and granulosa cells. Endocrinology. 1984;114(4):1315–1320.
  • Jeppesen JV, Anderson RA, Kelsey TW, et al. Which follicles make the most anti-Mullerian hormone in humans? Evidence for an abrupt decline in AMH production at the time of follicle selection. Mol Hum Reprod. 2013;19(8):519–527.
  • Baarends WM, Uilenbroek JT, Kramer P, et al. Anti-mullerian hormone and anti-mullerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology. 1995;136(11):4951–4962.
  • Ueno S, Kuroda T, MacLaughlin DT, et al. Mullerian inhibiting substance in the adult rat ovary during various stages of the estrous cycle. Endocrinology. 1989;125(2):1060–1066.
  • Weenen C, Laven JSE, vonBergh ARM, et al. Anti-Mullerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol.Hum.Reprod. 2004;10(2):77–83.
  • Rey RA, Lhommé C, Marcillac I, et al. Antimüllerian hormone as a serum marker of granulosa cell tumors of the ovary: comparative study with serum alpha-inhibin and estradiol. Am J Obstet Gynecol. 1996;174(3):958–965.
  • Long WQ, Ranchin V, Pautier P, et al. Detection of minimal levels of serum anti-Müllerian 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. 2000;85(2):540–544.
  • Hagen CP, Aksglæde L, Sorensen K, et al. Serum levels of anti-Mullerian hormone as a marker of ovarian function in 926 healthy females from birth to adulthood and in 172 Turner syndrome patients. J Clin Endocrinol Metab. 2010;95(11):5003–5010.
  • Broer SL, Eijkemans MJ, Scheffer GJ, et al. Anti-mullerian hormone predicts menopause: a long-term follow-up study in normoovulatory women. J Clin Endocrinol Metab. 2011;96(8):2532–2539.
  • Lie Fong S, Visser JA, Welt CK, et al. Serum anti-mullerian hormone levels in healthy females: a nomogram ranging from infancy to adulthood. J Clin Endocrinol Metab. 2012;97(12):4650–4655.
  • Elchuri SV, Patterson BC, Brown M, et al. Low anti-mullerian hormone in pediatric cancer survivors in the early years after gonadotoxic therapy. J Pediatr Adolesc Gynecol. 2016;29(4):393–399.
  • Wedrychowicz A, Wojtys J, Starzyk J. Anti-Muellerian hormone (AMH) as only possible marker in the assessment of ovarian function and reserve after hematopoietic stem cell transplantation (HSCT) in prepubertal girls, young females with composed hypogonadism and females receiving hormonal replacement therapy. Bone Marrow Transplant. 2017;52(2):313–316.
  • Broer SL, Broekmans FJ, Laven JS, et al. Anti-Mullerian hormone: ovarian reserve testing and its potential clinical implications. Hum Reprod Update. 2014;20(5):688–701.
  • Iliodromiti S, Anderson RA, Nelson SM. Technical and performance characteristics of anti-Mullerian hormone and antral follicle count as biomarkers of ovarian response. Hum Reprod Update. 2015;21(6):698–710.
  • Kumar TR. Fshb knockout mouse model, two decades later and into the future. Endocrinology. 2018;159(5):1941–1949.
  • Siegel ET, Kim HG, Nishimoto HK, et al. The molecular basis of impaired follicle-stimulating hormone action: evidence from human mutations and mouse models. Reprod Sci. 2013;20(3):211–233.
  • Jonas KC, Oduwole OO, Peltoketo H, et al. Mouse models of altered gonadotrophin action: insight into male reproductive disorders. Reproduction. 2014;148(4):R63–70.
  • Grinspon RP, Urrutia M, Rey RA. Male central hypogonadism in paediatrics – the relevance of follicle-stimulating hormone and sertoli cell markers. Eur Endocrinol. 2018;14:67–71.
  • Arango NA, Lovell-Badge R, Behringer RR. Targeted mutagenesis of the endogenous mouse Mis gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell. 1999;99(4):409–419.
  • Lasala C, Carré-Eusèbe D, Picard JY, et al. Subcellular and molecular mechanisms regulating anti-Müllerian hormone gene expression in mammalian and nonmammalian species. DNA Cell Biol. 2004;23(9):572–585.
  • Salmon NA, Handyside AH, Joyce IM. Expression of Sox8, Sf1, Gata4, Wt1, Dax1, and Fog2 in the mouse ovarian follicle: implications for the regulation of Amh expression. Mol Reprod Dev. 2005;70(3):271–277.
  • Pelusi C, Ikeda Y, Zubair M, et al. Impaired follicle development and infertility in female mice lacking steroidogenic factor 1 in ovarian granulosa cells. Biol Reprod. 2008;79(6):1074–1083.
  • França LR, Hess RA, Dufour JM, et al. The Sertoli cell: one hundred fifty years of beauty and plasticity. Andrology. 2016;4(2):189–212.
  • Chemes HE. Infancy is not a quiescent period of testicular development. Int.J.Androl. 2001;24(1):2–7.
  • McLean DJ, Friel PJ, Pouchnik D, et al. Oligonucleotide microarray analysis of gene expression in follicle-stimulating hormone-treated rat Sertoli cells. Mol Endocrinol. 2002;16(12):2780–2792.
  • Orth JM, Gunsalus GL, Lamperti AA. Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology. 1988;122(3):787–794.
  • Kumar TR, Wang Y, Lu N, et al. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet. 1997;15(2):201–204.
  • Dierich A, Ram Sairam M, Monaco L, et al. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci USA. 1998;95(23):13612–13617.
  • Braslavsky D, Grinspon RP, Ballerini MG, et al. Hypogonadotropic hypogonadism in infants with congenital hypopituitarism: a challenge to diagnose at an early stage. Horm Res Paediatr. 2015;84(5):289–297.
  • Lambert AS, Bougnères P. Growth and descent of the testes in infants with hypogonadotropic hypogonadism receiving subcutaneous gonadotropin infusion. Int J Pediatr Endocrinol. 2016;13:2016.
  • Vizeneux A, Hilfiger A, Bouligand J, et al. Congenital hypogonadotropic hypogonadism during childhood: presentation and genetic analyses in 46 boys. PLoS One. 2013;8(10):e77827.
  • Raivio T, Toppari J, Perheentupa A, et al. Treatment of prepubertal gonadotrophin-deficient boys with recombinant human follicle-stimulating hormone. Lancet. 1997;350(9073):263–264.
  • Main KM, Schmidt IM, Toppari J, et al. Early postnatal treatment of hypogonadotropic hypogonadism with recombinant human FSH and LH. Eur J Endocrinol. 2002;146(1):75–79.
  • Young J, Chanson P, Salenave S, et al. Testicular anti-mullerian hormone secretion is stimulated by recombinant human FSH in patients with congenital hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2005;90(2):724–728.
  • Sykiotis GP, Hoang XH, Avbelj M, et al. Congenital idiopathic hypogonadotropic hypogonadism: evidence of defects in the hypothalamus, pituitary, and testes. J Clin Endocrinol Metab. 2010;95(6):3019–3027.
  • Dwyer AA, Sykiotis GP, Hayes FJ, et al. Trial of recombinant follicle-stimulating hormone pretreatment for GnRH-induced fertility in patients with congenital hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 2013;98(11):E1790–1795.
  • Rohayem J, Hauffa BP, Zacharin M, et al. German adolescent hypogonadotropic hypogonadism study G. Testicular growth and spermatogenesis: new goals for pubertal hormone replacement in boys with hypogonadotropic hypogonadism? -a multicentre prospective study of hCG/rFSH treatment outcomes during adolescence. Clin Endocrinol (Oxf). 2017;86(1):75–87.
  • Stoupa A, Samara-Boustani D, Flechtner I, et al. Efficacy and safety of continuous subcutaneous infusion of recombinant human gonadotropins for congenital micropenis during early infancy. Horm Res Paediatr. 2017;87(2):103–110.
  • Rohayem J, Nieschlag E, Kliesch S, et al. Inhibin B, AMH, but not INSL3, IGF1 or DHEAS support differentiation between constitutional delay of growth and puberty and hypogonadotropic hypogonadism. Andrology. 2015;3(5):882–887.
  • Kohva E, Huopio H, Hero M, et al. Recombinant human FSH treatment outcomes in five boys with severe congenital hypogonadotropic hypogonadism. J Endocr Soc. 2018;2(12):1345–1356.
  • Edelsztein NY, Grinspon RP, Schteingart HF, et al. Anti-Müllerian hormone as a marker of steroid and gonadotropin action in the testis of children and adolescents with disorders of the gonadal axis. Int J Pediatr Endocrinol. 2016;20:2016.
  • Chemes HE, Rey RA, Nistal M, et al. Physiological androgen insensitivity of the fetal, neonatal, and early infantile testis is explained by the ontogeny of the androgen receptor expression in Sertoli cells. J Clin Endocrinol Metab. 2008;93(11):4408–4412.
  • Rey RA, Belville C, Nihoul-Fékété C, et al. Evaluation of gonadal function in 107 intersex patients by means of serum antimüllerian hormone measurement. J Clin Endocrinol Metab. 1999;84(2):627–631.
  • Rey R, Josso N, Racine C. Sexual differentiation. In: De Groot LJ, Beck-Peccoz P, Chrousos G, et al., editors. Endotext [Internet]. South Dartmouth (MA): MDText.com, Inc.;2000–2016 June 1. Available from: http://www.endotext.org/chapter/sexual-differentiation/.
  • Lukas-Croisier C, Lasala C, Nicaud J, et al. Follicle-stimulating hormone increases testicular Anti-Müllerian hormone (AMH) production through sertoli cell proliferation and a nonclassical cyclic adenosine 5ʹ-monophosphate-mediated activation of the AMH gene. Mol Endocrinol. 2003;17(4):550–561.
  • Dutertre M, Rey R, Porteu A, et al. A mouse Sertoli cell line expressing anti-Müllerian hormone and its type II receptor. Mol Cell Endocrinol. 1997;136(1):57–65.
  • Al-Attar L, Noël K, Dutertre M, et al. Hormonal and cellular regulation of Sertoli cell anti-Müllerian hormone production in the postnatal mouse. J Clin Invest. 1997;100(6):1335–1343.
  • Lasala C, Schteingart HF, Arouche N, et al. 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. 2011;301(3):E539–547.
  • Rey RA, Venara M, Coutant R, et al. Unexpected mosaicism of R201H-GNAS1 mutant-bearing cells in the testes underlie macro-orchidism without sexual precocity in McCune-Albright syndrome. Hum Mol Genet. 2006;15(24):3538–3543.
  • Hsueh AJ, Kawamura K, Cheng Y, et al. Intraovarian control of early folliculogenesis. Endocr Rev. 2015;36(1):1–24.
  • Dewailly D, Robin G, Peigne M, et al. Interactions between androgens, FSH, anti-Mullerian hormone and estradiol during folliculogenesis in the human normal and polycystic ovary. Hum Reprod Update. 2016;22(6):709–724.
  • Taieb J, Grynberg M, Pierre A, et al. FSH and its second messenger cAMP stimulate the transcription of human anti-Mullerian hormone in cultured granulosa cells. Mol Endocrinol. 2011;25(4):645–655.
  • Bry-Gauillard H, Larrat-Ledoux F, Levaillant JM, et al. Anti-Mullerian hormone and ovarian morphology in women with isolated hypogonadotropic hypogonadism/Kallmann syndrome. Effects of recombinant human FSH. J Clin Endocrinol Metab. 2017;102:1102–1111.
  • Durlinger AL, Visser JA, Themmen AP. Regulation of ovarian function: the role of anti-Müllerian hormone. Reproduction. 2002;124(5):601–609.
  • Muttukrishna S, Yussoff H, Naidu M, et al. Serum anti-Mullerian hormone and inhibin B in disorders of spermatogenesis. Fertil.Steril. 2007;88(2):516–518.
  • Plotton I, Garby L, Morel Y, et al. Decrease of anti-Mullerian hormone in genetic spermatogenic failure. Andrologia. 2012;44(5):349–354.
  • Fénichel P, Rey R, Poggioli S, et al. Anti-Müllerian hormone as a seminal marker for spermatogenesis in non-obstructive azoospermia. Hum Reprod. 1999;14(8):2020–2024.
  • Rey RA, Grinspon RP, Gottlieb S, et al. Male hypogonadism: an extended classification based on a developmental, endocrine physiology-based approach. Andrology. 2013;1(1):3–16.
  • Bastida MG, Rey RA, Bergadá I, et al. Establishment of testicular endocrine function impairment during childhood and puberty in boys with Klinefelter syndrome. Clin Endocrinol (Oxf). 2007;67(6):863–870.
  • Pacenza N, Pasqualini T, Gottlieb S, et al. Clinical Presentation of Klinefelter’s Syndrome: Differences According to Age. Int J Endocrinol. 2012;324835:2012.
  • Cortes D, Clasen-Linde E, Hutson JM, et al. The Sertoli cell hormones inhibin-B and anti Mullerian hormone have different patterns of secretion in prepubertal cryptorchid boys. J Pediatr Surg. 2016;51(3):475–480.
  • Moniez S, Pienkowski C, Lepage B, et al. Noonan syndrome males display Sertoli cell-specific primary testicular insufficiency. Eur J Endocrinol. 2018;179(6):409–418.
  • Levi M, Hasky N, Stemmer SM, et al. Anti-Mullerian Hormone is a marker for chemotherapy-induced testicular toxicity. Endocrinology. 2015;156(10):3818–3827.
  • Jain M, Kalsi AK, Srivastava A, et al. High serum estradiol and heavy metals responsible for human spermiation defect-a pilot study. J Clin Diagn Res. 2016;10(12):RC09–RC13.
  • Goulis DG, Tsametis C, Iliadou PK, et al. Serum inhibin B and anti-Mullerian hormone are not superior to follicle-stimulating hormone as predictors of the presence of sperm in testicular fine-needle aspiration in men with azoospermia. Fertil Steril. 2009;91(4):1279–1284.
  • Toulis KA, Iliadou PK, Venetis CA, et al. Inhibin B and anti-Mullerian hormone as markers of persistent spermatogenesis in men with non-obstructive azoospermia: a meta-analysis of diagnostic accuracy studies. Hum Reprod Update. 2010;16(6):713–724.
  • Xu HY, Zhang HX, Xiao Z, et al. Regulation of anti-Mullerian hormone (AMH) in males and the associations of serum AMH with the disorders of male fertility. Asian J Androl. 2019;21(2):109-114.
  • Aksglaede L, Olesen IA, Carlsen E, et al. Serum concentration of anti-Mullerian hormone is not associated with semen quality. Andrology. 2018;6(2):286–292.
  • Raivio T, Wikström AM, Dunkel L. Treatment of gonadotropin-deficient boys with recombinant human FSH: long-term observation and outcome. Eur J Endocrinol. 2007;156(1):105–111.
  • Young J, Rey R, Couzinet B, et al. Antimüllerian hormone in patients with hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 1999;84(8):2696–2699.
  • Sinisi AA, Esposito D, Maione L, et al. Seminal anti-Mullerian hormone level is a marker of spermatogenic response during long-term gonadotropin therapy in male hypogonadotropic hypogonadism. Hum.Reprod. 2008;23(5):1029–1034.
  • Caprio F, De Franciscis P, Trotta C, et al. Seminal anti-Mullerian hormone levels during recombinant human follicle-stimulating hormone treatment in men with idiopathic infertility undergoing assisted reproduction cycles. Andrology. 2015;3(5):843–847.
  • Guercio G, Rey RA. Fertility issues in the management of patients with disorders of sex development. Endocr Dev. 2014;27:87–98.
  • Alfano M, Ventimiglia E, Locatelli I, et al. Anti-Mullerian Hormone-to-testosterone ratio is predictive of positive sperm retrieval in men with idiopathic non-obstructive azoospermia. Sci Rep. 2017;7(1):17638.
  • Huhtaniemi I, Hovatta O, La Marca A, et al. Advances in the molecular pathophysiology, genetics, and treatment of primary ovarian insufficiency. Trends Endocrinol Metab. 2018;29(6):400-419.
  • Lew R. Natural history of ovarian function including assessment of ovarian reserve and premature ovarian failure. Best Pract Res Clin Obstet Gynaecol. 2019;55:2-13.
  • Sönmezer M, Özmen B, Atabekoglu CS, et al. Serum anti-Mullerian hormone levels correlate with ovarian response in idiopathic hypogonadotropic hypogonadism. J Assist Reprod Genet. 2012;29(7):597–602.
  • Chan C, Liu K. Clinical pregnancy in a woman with idiopathic hypogonadotropic hypogonadism and low AMH: utility of ovarian reserve markers in IHH. J Assist Reprod Genet. 2014;31(10):1317–1321.
  • Deubzer B, Weber K, Lawrenz B, et al. Anti-mullerian hormone deficiency in girls with congenital multiple pituitary hormone deficiency. J Clin Endocrinol Metab. 2014;99(6):E1045–1049.
  • Medicine PCotASfR. Prevention and treatment of moderate and severe ovarian hyperstimulation syndrome: a guideline. Fertil Steril. 2016;106(7):1634–1647.
  • Catteau-Jonard S, Jamin SP, Leclerc A, et al. Anti-Mullerian hormone, its receptor, FSH receptor, and androgen receptor genes are overexpressed by granulosa cells from stimulated follicles in women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2008;93(11):4456–4461.
  • Adan L, Lechevalier P, Couto-Silva AC, et al. Plasma inhibin B and antimullerian hormone concentrations in boys: Discriminating between congenital hypogonadotropic hypogonadism and constitutional pubertal delay. Med SciMonit. 2010;16(11):CR511–CR517.
  • Coutant R, Biette-Demeneix E, Bouvattier C, et al. Baseline inhibin B and anti-mullerian hormone measurements for diagnosis of hypogonadotropic hypogonadism (HH) in boys with delayed puberty. J Clin Endocrinol Metab. 2010;95(12):5225–5232.
  • Bougnères P, François M, Pantalone L, et al. Effects of an early postnatal treatment of hypogonadotropic hypogonadism with a continuous subcutaneous infusion of recombinant follicle-stimulating hormone and luteinizing hormone. J Clin Endocrinol Metab. 2008;93(6):2202–2205.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.