Subscribe to RSS
Please copy the URL and add it into your RSS Feed Reader.
https://www.thieme-connect.de/rss/thieme/en/10.1055-s-00000072.xml
Download PDF
Semin Reprod Med 2024; 42(01): 005-014
DOI: 10.1055/s-0044-1787687
DOI: 10.1055/s-0044-1787687
Review Article
Role of Anti-Müllerian Hormone in Male Reproduction and Sperm Motility
Funding This review did not receive any specific grants from any funding agency in the public, commercial, or nonprofit sectors.
Abstract
Anti-Müllerian hormone (AMH) is secreted by Sertoli cells and is responsible for the regression of Müllerian ducts in the male fetus as part of the sexual differentiation process. Serum AMH concentrations are at their lowest levels in the first days after birth but increase after the first week, likely reflecting active Sertoli cell proliferation. AMH rises rapidly in concentration in boys during the first month, reaching a peak level at ∼6 months of age, and it remains high during childhood, then they will slowly decline during puberty, falling to low levels in adulthood. Serum AMH measurement is used by pediatric endocrinologist as a specific marker of immature Sertoli cell number and function during childhood. After puberty, AMH is released especially by the apical pole of the Sertoli cells toward the lumen of the seminiferous tubules, resulting in higher levels in the seminal plasma than in the serum. Recently, AMH has received increasing attention in research on male fertility–related disorders. This article reviews and summarizes the potential contribution of serum AMH measurement in different male fertility–related disorders.
Authors' Contributions
I confirm that all authors participated in writing the manuscript and have seen and approved the submitted version.
Publication History
Article published online:
24 June 2024
© 2024. Thieme. All rights reserved.
Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA
-
References
- 1 Benderradji H, Barbotin AL, Leroy-Billiard M. et al. Defining reference ranges for serum anti-Müllerian hormone on a large cohort of normozoospermic adult men highlights new potential physiological functions of AMH on FSH secretion and sperm motility. J Clin Endocrinol Metab 2022; 107 (07) 1878-1887
- 2 Aksglaede L, Sørensen K, Boas M. et al. Changes in anti-Müllerian hormone (AMH) throughout the life span: a population-based study of 1027 healthy males from birth (cord blood) to the age of 69 years. J Clin Endocrinol Metab 2010; 95 (12) 5357-5364
- 3 di Clemente N, Wilson C, Faure E. et al. Cloning, expression, and alternative splicing of the receptor for anti-Müllerian hormone. Mol Endocrinol 1994; 8 (08) 1006-1020
- 4 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 (05) 685-698
- 5 Barbotin AL, Peigné M, Malone SA, Giacobini P. Emerging roles of anti-Müllerian hormone in hypothalamic-pituitary function. Neuroendocrinology 2019; 109 (03) 218-229
- 6 Cohen-Haguenauer O, Picard JY, Mattéi MG. et al. Mapping of the gene for anti-Müllerian hormone to the short arm of human chromosome 19. Cytogenet Cell Genet 1987; 44 (01) 2-6
- 7 Baarends WM, Uilenbroek JT, Kramer P. et al. 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. Endocrinology 1995; 136 (11) 4951-4962
- 8 Mishina Y, Rey R, Finegold MJ. et al. Genetic analysis of the Müllerian-inhibiting substance signal transduction pathway in mammalian sexual differentiation. Genes Dev 1996; 10 (20) 2577-2587
- 9 Shi Y, Massagué J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 2003; 113 (06) 685-700
- 10 Josso N, Clemente Nd. Transduction pathway of anti-Müllerian hormone, a sex-specific member of the TGF-β family. Trends Endocrinol Metab 2003; 14 (02) 91-97
- 11 Moses MM, Behringer RR. A gene regulatory network for Müllerian duct regression. Environ Epigenet 2019; 5 (03) dvz017
- 12 Rey R, Lukas-Croisier C, Lasala C, Bedecarrás P. AMH/MIS: what we know already about the gene, the protein and its regulation. Mol Cell Endocrinol 2003; 211 (1-2): 21-31
- 13 Rey RA, Grinspon RP. Normal male sexual differentiation and aetiology of disorders of sex development. Best Pract Res Clin Endocrinol Metab 2011; 25 (02) 221-238
- 14 Renault CH, Aksglaede L, Wøjdemann D, Hansen AB, Jensen RB, Juul A. Minipuberty of human infancy - a window of opportunity to evaluate hypogonadism and differences of sex development?. Ann Pediatr Endocrinol Metab 2020; 25 (02) 84-91
- 15 Bergadá I, Milani C, Bedecarrás P. et al. Time course of the serum gonadotropin surge, inhibins, and anti-Müllerian hormone in normal newborn males during the first month of life. J Clin Endocrinol Metab 2006; 91 (10) 4092-4098
- 16 Lukas-Croisier C, Lasala C, Nicaud J. et al. 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 2003; 17 (04) 550-561
- 17 Grumbach MM. A window of opportunity: the diagnosis of gonadotropin deficiency in the male infant. J Clin Endocrinol Metab 2005; 90 (05) 3122-3127
- 18 Müller J, Skakkebaek NE. Quantification of germ cells and seminiferous tubules by stereological examination of testicles from 50 boys who suffered from sudden death. Int J Androl 1983; 6 (02) 143-156
- 19 Nistal M, Abaurrea MA, Paniagua R. Morphological and histometric study on the human Sertoli cell from birth to the onset of puberty. J Anat 1982; 134 (Pt 2): 351-363
- 20 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
- 21 Boukari K, Meduri G, Brailly-Tabard S. et al. Lack of androgen receptor expression in Sertoli cells accounts for the absence of anti-Mullerian hormone repression during early human testis development. J Clin Endocrinol Metab 2009; 94 (05) 1818-1825
- 22 Rey R. Endocrine, paracrine and cellular regulation of postnatal anti-Müllerian hormone secretion by Sertoli cells. Trends Endocrinol Metab 1998; 9 (07) 271-276
- 23 Rey R, al-Attar L, Louis F. et al. Testicular dysgenesis does not affect expression of anti-Müllerian hormone by Sertoli cells in premeiotic seminiferous tubules. Am J Pathol 1996; 148 (05) 1689-1698
- 24 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 (06) 1335-1343
- 25 Rey R, Lordereau-Richard I, Carel JC. et al. Anti-Müllerian hormone and testosterone serum levels are inversely during normal and precocious pubertal development. J Clin Endocrinol Metab 1993; 77 (05) 1220-1226
- 26 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 (02) 724-728
- 27 Teixeira J, Maheswaran S, Donahoe PK. Müllerian inhibiting substance: an instructive developmental hormone with diagnostic and possible therapeutic applications. Endocr Rev 2001; 22 (05) 657-674
- 28 Gustafson ML, Lee MM, Asmundson L, MacLaughlin DT, Donahoe PK. Müllerian inhibiting substance in the diagnosis and management of intersex and gonadal abnormalities. J Pediatr Surg 1993; 28 (03) 439-444
- 29 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 (02) 540-544
- 30 Wang PY, Protheroe A, Clarkson AN, Imhoff F, Koishi K, McLennan IS. Müllerian inhibiting substance contributes to sex-linked biases in the brain and behavior. Proc Natl Acad Sci U S A 2009; 106 (17) 7203-7208
- 31 Cimino I, Casoni F, Liu X. et al. Novel role for anti-Müllerian hormone in the regulation of GnRH neuron excitability and hormone secretion. Nat Commun 2016; 7 (01) 10055
- 32 Josso N, Rey RA, Pask A. Editorial: fetal testicular hormones. Front Endocrinol (Lausanne) 2022; 13: 1090088
- 33 Picard JY, Cate RL, Racine C, Josso N. The persistent Müllerian duct syndrome: an update based upon a personal experience of 157 cases. Sex Dev 2017; 11 (03) 109-125
- 34 Josso N, Rey RA. What does AMH tell us in pediatric disorders of sex development?. Front Endocrinol (Lausanne) 2020; 11: 619
- 35 Virtanen HE, Bjerknes R, Cortes D. et al. Cryptorchidism: classification, prevalence and long-term consequences. Acta Paediatr 2007; 96 (05) 611-616
- 36 Grinspon RP, Rey RA. Anti-Müllerian hormone and Sertoli cell function in paediatric male hypogonadism. Horm Res Paediatr 2010; 73 (02) 81-92
- 37 Albescú JZ, Bergadá C, Cullen M. Male fertility in patients treated for cryptorchidism before puberty. Fertil Steril 1971; 22 (12) 829-833
- 38 Pettersson A, Richiardi L, Nordenskjold A, Kaijser M, Akre O. Age at surgery for undescended testis and risk of testicular cancer. N Engl J Med 2007; 356 (18) 1835-1841
- 39 Engeler DS, Hösli PO, John H. et al. Early orchiopexy: prepubertal intratubular germ cell neoplasia and fertility outcome. Urology 2000; 56 (01) 144-148
- 40 Thorup J, McLachlan R, Cortes D. et al. What is new in cryptorchidism and hypospadias–a critical review on the testicular dysgenesis hypothesis. J Pediatr Surg 2010; 45 (10) 2074-2086
- 41 Matuszczak E, Hermanowicz A, Debek W, Oksiuta M, Dzienis-Koronkiewicz E, Zelazowska-Rutkowska B. Serum AMH concentration as a marker evaluating gonadal function in boys operated on for unilateral cryptorchidism between 1st and 4th year of life. Endocrine 2012; 41 (02) 334-337
- 42 Demircan M, Akinci A, Mutus M. The effects of orchiopexy on serum anti-Müllerian hormone levels in unilateral cryptorchid infants. Pediatr Surg Int 2006; 22 (03) 271-273
- 43 Guibourdenche J, Lucidarme N, Chevenne D. et al. Anti-Müllerian hormone levels in serum from human foetuses and children: pattern and clinical interest. Mol Cell Endocrinol 2003; 211 (1-2): 55-63
- 44 Tüttelmann F, Dykstra N, Themmen APN, Visser JA, Nieschlag E, Simoni M. Anti-Müllerian hormone in men with normal and reduced sperm concentration and men with maldescended testes. Fertil Steril 2009; 91 (05) 1812-1819
- 45 Kumar S, Tomar V, Yadav SS, Priyadarshi S, Vyas N, Agarwal N. Fertility potential in adult hypospadias. J Clin Diagn Res 2016; 10 (08) PC01-PC05
- 46 Asklund C, Jensen TK, Main KM, Sobotka T, Skakkebaek NE, Jørgensen N. Semen quality, reproductive hormones and fertility of men operated for hypospadias. Int J Androl 2010; 33 (01) 80-87
- 47 Hero M, Tommiska J, Vaaralahti K. et al. Circulating antimüllerian hormone levels in boys decline during early puberty and correlate with inhibin B. Fertil Steril 2012; 97 (05) 1242-1247
- 48 Rey RA, Grinspon RP, Gottlieb S. et al. Male hypogonadism: an extended classification based on a developmental, endocrine physiology-based approach. Andrology 2013; 1 (01) 3-16
- 49 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
- 50 Gravholt CH, Chang S, Wallentin M, Fedder J, Moore P, Skakkebæk A. Klinefelter syndrome: integrating genetics, neuropsychology, and endocrinology. Endocr Rev 2018; 39 (04) 389-423
- 51 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 (06) 863-870
- 52 Lahlou N, Fennoy I, Carel JC, Roger M. Inhibin B and anti-Müllerian hormone, but not testosterone levels, are normal in infants with nonmosaic Klinefelter syndrome. J Clin Endocrinol Metab 2004; 89 (04) 1864-1868
- 53 Renault L, Labrune E, Giscard d'Estaing S. et al. Delaying testicular sperm extraction in 47,XXY Klinefelter patients does not impair the sperm retrieval rate, and AMH levels are higher when TESE is positive. Hum Reprod 2022; 37 (11) 2518-2531
- 54 Benderradji H, Prasivoravong J, Marcelli F. et al. Contribution of serum anti-Müllerian hormone in the management of azoospermia and the prediction of testicular sperm retrieval outcomes: a study of 155 adult men. Basic Clin Androl 2021; 31 (01) 15
- 55 Romeo C, Santoro G. Varicocele and infertility: why a prevention?. J Endocrinol Invest 2009; 32 (06) 559-561
- 56 Bellastella G, Carotenuto R, Caiazzo F. et al. Varicocele: an endocrinological perspective. Front Reprod Health 2022; 4: 863695
- 57 Trigo RV, Bergadá I, Rey R. et al. Altered serum profile of inhibin B, pro-alphaC and anti-Müllerian hormone in prepubertal and pubertal boys with varicocele. Clin Endocrinol (Oxf) 2004; 60 (06) 758-764
- 58 Goulis DCh, Mintziori G, Koliakos N. et al. Inhibin B and anti-Müllerian hormone in spermatic vein of subfertile men with varicocele. Reprod Sci 2011; 18 (06) 551-555
- 59 Goulis DG, Iliadou PK, Tsametis C. et al. Serum anti-Müllerian hormone levels differentiate control from subfertile men but not men with different causes of subfertility. Gynecol Endocrinol 2008; 24 (03) 158-160
- 60 Schwartz CL. ed. Survivors of childhood and adolescent cancer: a multidisciplinary approach. In: Pediatric oncology. 2nd ed.. Berlin: Springer; 2005: 348
- 61 Leroy C, Cortet-Rudelli C, Desailloud R. [Endocrine consequences in young adult survivors of childhood cancer treatment]. Ann Endocrinol (Paris) 2015; 76 (6, Suppl 1): S29-S38
- 62 Cuny A, Trivin C, Brailly-Tabard S. et al. Inhibin B and anti-Müllerian hormone as markers of gonadal function after treatment for medulloblastoma or posterior fossa ependymoma during childhood. J Pediatr 2011; 158 (06) 1016-1022.e1
- 63 Laporte S, Couto-Silva AC, Trabado S. et al. Inhibin B and anti-Müllerian hormone as markers of gonadal function after hematopoietic cell transplantation during childhood. BMC Pediatr 2011; 11 (01) 20
- 64 Muttukrishna S, Yussoff H, Naidu M. et al. Serum anti-Müllerian hormone and inhibin B in disorders of spermatogenesis. Fertil Steril 2007; 88 (02) 516-518
- 65 Xiong Z, Ye Z, Tu J, Meng TQ, Ren N. [Serum anti-Müllerian hormone level for differential diagnosis of obstructive and non-obstructive azoospermia]. Zhonghua Nan Ke Xue 2019; 25 (09) 823-827
- 66 Shu J. Serum anti – Mullerian hormone in azoospermia approach. Farmacia 2023; 71 (02) 280-287
- 67 Peng LP, Shao Y, Wang CC. et al. [Correlation of serum anti-Müllerian hormone with semen parameters]. Zhonghua Nan Ke Xue 2017; 23 (06) 531-535
- 68 Aksglaede L, Olesen IA, Carlsen E, Petersen JH, Juul A, Jørgensen N. Serum concentration of anti-Müllerian hormone is not associated with semen quality. Andrology 2018; 6 (02) 286-292
- 69 Kucera R, Ulcova-Gallova Z, Windrichova J, Losan P, Topolcan O. Anti-Müllerian hormone in serum and seminal plasma in comparison with other male fertility parameters. Syst Biol Reprod Med 2016; 62 (03) 223-226
- 70 El-Halawaty S, Azab H, Said T. et al. Assessment of male serum anti-Mullerian hormone as a marker of spermatogenesis and ICSI outcome. Gynecol Endocrinol 2011; 27 (06) 401-405
- 71 Rashad M, Azab M. Assessment of semen parameters and anti-Müllerian hormone level in patients with chronic kidney disease on hemodialysis: a case control study. JOMH 2021; 17 (04) 72-77
- 72 Domain G, Buczkowska J, Kalak P. et al. Serum anti-Müllerian hormone: a potential semen quality biomarker in stud dogs?. Animals (Basel) 2022; 12 (03) 323
- 73 Andersen JM, Herning H, Witczak O, Haugen TB. Anti-Müllerian hormone in seminal plasma and serum: association with sperm count and sperm motility. Hum Reprod 2016; 31 (08) 1662-1667
- 74 Mostafa T, Amer MK, Abdel-Malak G. et al. Seminal plasma anti-Müllerian hormone level correlates with semen parameters but does not predict success of testicular sperm extraction (TESE). Asian J Androl 2007; 9 (02) 265-270
- 75 Turhan G, Çil N, Kabukçu C, Turan T, Fenkçi İV, Abban Mete G. Relationship of seminal plasma anti-Müllerian hormone concentration with sperm morphology and sperm DNA damage. J Urol Surg 2022; 9 (04) 272-280
- 76 Holst BS, Panzani D, Camillo F, Svensson A, Rota A. Anti-Müllerian hormone (AMH) concentrations are maximal at puberty in male donkeys and secretion is redirected from the blood stream to seminal plasma. Anim Reprod Sci 2020; 218: 106484
- 77 Fénichel P, Rey R, Poggioli S, Donzeau M, Chevallier D, Pointis G. Anti-Müllerian hormone as a seminal marker for spermatogenesis in non-obstructive azoospermia. Hum Reprod 1999; 14 (08) 2020-2024
- 78 Siow Y, Fallat ME, Amin FA, Belker AM. Müllerian inhibiting substance improves longevity of motility and viability of fresh and cryopreserved sperm. J Androl 1998; 19 (05) 568-572
- 79 Nery SF, Vieira MAF, Dela Cruz C. et al. Seminal plasma concentrations of anti-Müllerian hormone and inhibin B predict motile sperm recovery from cryopreserved semen in asthenozoospermic men: a prospective cohort study. Andrology 2014; 2 (06) 918-923
- 80 Dong S, Chen C, Zhang J, Gao Y, Zeng X, Zhang X. Testicular aging, male fertility and beyond. Front Endocrinol (Lausanne) 2022; 13: 1012119
- 81 Chong YH, Dennis NA, Connolly MJ. et al. Elderly men have low levels of anti-Müllerian hormone and inhibin B, but with high interpersonal variation: a cross-sectional study of the Sertoli cell hormones in 615 community-dwelling men. PLoS One 2013; 8 (08) e70967
- 82 Ramezani Tehrani F, Mansournia MA, Solaymani-Dodaran M, Minooee S, Azizi F. Serum variations of anti-Mullerian hormone and total testosterone with aging in healthy adult Iranian men: a population-based study. PLoS One 2017; 12 (07) e0179634