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      Inhibitory Actions of Anti-Müllerian Hormone (AMH) on Ovarian Primordial Follicle Assembly

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          Abstract

          The current study was designed to investigate the actions of Anti-Müllerian Hormone (AMH) on primordial follicle assembly. Ovarian primordial follicles develop from the breakdown of oocyte nests during fetal development for the human and immediately after birth in rodents. AMH was found to inhibit primordial follicle assembly and decrease the initial primordial follicle pool size in a rat ovarian organ culture. The AMH expression was found to be primarily in the stromal tissue of the ovaries at this period of development, suggesting a stromal-epithelial cell interaction for primordial follicle assembly. AMH was found to promote alterations in the ovarian transcriptome during primordial follicle assembly with over 200 genes with altered expression. A gene network was identified suggesting a potential central role for the Fgf2/Nudt6 antisense transcript in the follicle assembly process. A number of signal transduction pathways are regulated by AMH actions on the ovarian transcriptome, in particular the transforming growth factor – beta (TGFß) signaling process. AMH is the first hormone/protein shown to have an inhibitory action on primordial follicle assembly. Due to the critical role of the primordial follicle pool size for female reproduction, elucidation of factors, such as AMH, that regulate the assembly process will provide insights into potential therapeutics to manipulate the pool size and female reproduction.

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          Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary.

          A. Durlinger, P. KRAMER, B Karels … (1999)
          The dimeric glycoprotein anti-Müllerian hormone (AMH) is a member of the transforming growth factor-beta superfamily of growth and differentiation factors. During male fetal sex differentiation, AMH is produced by Sertoli cells and induces degeneration of the Müllerian ducts, which form the anlagen of part of the internal female genital system. In females, AMH is produced by the ovary, but only postnatally. The function of AMH in the ovary is, however, still unknown. Female AMH null mice were reported to be fertile, with normal litter size, but this does not exclude a more subtle function for ovarian AMH. To investigate the function of AMH in the ovary, the complete follicle population was determined in AMH null mice, in mice heterozygous for the AMH null mutation, and in wild-type mice of different ages: 25 days, 4 months, and 13 months. In the present study we found that ovaries of 25-day- and 4-month-old AMH null females, compared to those of wild-type females, contain more preantral and small antral follicles. In addition, in 4- and 13-month-old AMH null females, smaller numbers of primordial follicles were found. Actually, in 13-month-old AMH null females, almost no primordial follicles could be detected, coinciding with a reduced number of preantral and small antral follicles in these females. In almost all females heterozygous for the AMH null mutation the number of follicles fell in between the numbers found in wild-type and AMH null females. In 4-month-old AMH null females serum inhibin levels were higher and FSH levels were lower compared to those in wild-type females. In contrast, inhibin levels were lower in 13-month-old AMH null females, and FSH levels were unchanged compared to those in wild-type females. Furthermore, the weight of the ovaries was twice as high in the 4-month-old AMH null females as in age-matched wild-type females. We conclude that AMH plays an important role in primordial follicle recruitment, such that more primordial follicles are recruited in AMH null mice than in wild-type mice; the mice heterozygous for the AMH null mutation take an in-between position. Consequently, the ovaries of AMH null females and those of females heterozygous for the AMH null mutation will show a relatively early depletion of their stock of primordial follicles. The female AMH null mouse may thus provide a useful model to study regulation of primordial follicle recruitment and the relation between follicular dynamics and ovarian aging.
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            Regulation of ovarian function: the role of anti-Müllerian hormone.

            Axel P N Themmen, Jenny Visser, Alexandra Durlinger (2002)
            Anti-Müllerian hormone (AMH), also known as Müllerian inhibiting substance, is a member of the transforming growth factor beta superfamily of growth and differentiation factors. In contrast to other members of the family, which exert a broad range of functions in multiple tissues, the principal function of AMH is to induce regression of the Müllerian ducts during male sex differentiation. However, the patterns of expression of AMH and its type II receptor in the postnatal ovary indicate that AMH may play an important role in ovarian folliculogenesis. This review describes several in vivo and in vitro studies showing that AMH participates in two critical selection points of follicle development: it inhibits the recruitment of primordial follicles into the pool of growing follicles and also decreases the responsiveness of growing follicles to FSH.
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              Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary.

              J Anton Grootegoed, Jan Th J Uilenbroek, Alexandra L L Durlinger … (2002)
              Recruitment of primordial follicles is essential for female fertility; however, the exact mechanisms regulating this process are largely unknown. Earlier studies using anti-Müllerian hormone (AMH)-deficient mice suggested that AMH is involved in the regulation of primordial follicle recruitment. We tested this hypothesis in a neonatal ovary culture system, in which ovaries from 2-d-old C57Bl/6J mice were cultured for 2 or 4 d in the absence or presence of AMH. Ovaries from 2-d-old mice contain multiple primordial follicles, some naked oocytes, and no follicles at later stages of development. We observed that in the cultured ovaries, either nontreated or AMH-treated, follicular development progressed to the same extent as in in vivo ovaries of comparable age, confirming the validity of our culture system. However, in the presence of AMH, cultured ovaries contained 40% fewer growing follicles compared with control ovaries. A similar reduction was found after 4 d of culture. Consistent with these findings, we noted lower inhibin alpha-subunit expression in AMH-treated ovaries compared with untreated ovaries. In contrast, expression of AMH ligand type II receptor and the expression of oocyte markers growth and differentiation factor 9 and zona pellucida protein 3 were not influenced by AMH. Based on the results, we suggest that AMH inhibits initiation of primordial follicle growth and therefore functions as an inhibitory growth factor in the ovary during these early stages of folliculogenesis.
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                Author and article information

                Contributors
                : Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2011
                Publication date (Electronic): 27 May 2011
                Volume: 6
                Issue: 5
                Electronic Location Identifier: e20087
                Affiliations
                [1]Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, Washington, United States of America
                State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, China
                Author notes

                Conceived and designed the experiments: MKS EEN. Performed the experiments: EEN RS MS. Analyzed the data: EEN RS MS. Wrote the paper: EEN MKS. Reviewed and edited the manuscript: EEN RS MS MKS.

                [¤]

                Current address: Biotechnology Program, San Jose State University, San Jose, California, United States of America

                Article
                Publisher ID: PONE-D-11-01955
                DOI: 10.1371/journal.pone.0020087
                PMC ID: 3103528
                PubMed ID: 21637711
                SO-VID: 7b1481a9-b31e-483b-99e2-b98b31fef198
                Copyright © Nilsson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                Date received : 26 January 2011
                Date accepted : 17 April 2011
                Page count
                Pages: 10
                Categories
                Subject: Research Article
                Subject: Biology
                Subject: Anatomy and Physiology
                Subject: Reproductive System
                Subject: Reproductive Physiology
                Subject: Sexual Reproduction
                Subject: Computational Biology
                Subject: Genomics
                Subject: Developmental Biology
                Subject: Molecular Development
                Subject: Morphogens
                Subject: Cell Differentiation
                Subject: Morphogenesis
                Subject: Genetics
                Subject: Gene Networks
                Subject: Genomics
                Subject: Model Organisms
                Subject: Animal Models
                Subject: Rat

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