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• W1965297895 abstract "The objectives of this study were to identify whether there is a decline in Müllerian inhibiting substance (MIS) in the female rat during chronological aging, and to define the physiological basis of aging-related changes in MIS. The results demonstrate that there is an exponential decline in both serum and ovarian levels of MIS with increasing female age, and that the histologic origin for the reduction in serum levels of MIS is a decline in the number of small ovarian follicles expressing MIS. The objectives of this study were to identify whether there is a decline in Müllerian inhibiting substance (MIS) in the female rat during chronological aging, and to define the physiological basis of aging-related changes in MIS. The results demonstrate that there is an exponential decline in both serum and ovarian levels of MIS with increasing female age, and that the histologic origin for the reduction in serum levels of MIS is a decline in the number of small ovarian follicles expressing MIS. Müllerian inhibiting substance (MIS; also known as anti-Müllerian hormone) is a member of the transforming growth factor-β superfamily (1Lee M.M. Donahoe P.K. Müllerian inhibiting substance: a gonadal hormone with multiple functions.Endocr Rev. 1993; 14: 152-164PubMed Google Scholar). It was localized in preantral and small antral follicles (2Bezard J. Vigier B. Tran D. Mauleon P. Josso N. Immunocytochemical study of anti-Müllerian hormone in sheep ovarian follicles during fetal and post-natal development.J Reprod Fertil. 1987; 80: 509-516Crossref PubMed Scopus (101) Google Scholar, 3Ueno S. Kuroda T. Maclaughlin D.T. Ragin R.C. Manganaro T.F. Donahoe P.K. Müllerian inhibiting substance in the adult rat ovary during various stages of the estrous cycle.Endocrinology. 1989; 125: 1060-1066Crossref PubMed Scopus (118) Google Scholar, 4Ueno S. Takahashi M. Manganaro T.F. Ragin R.C. Donahoe P.K. Cellular localization of Müllerian inhibiting substance in the developing rat ovary.Endocrinology. 1989; 124: 1000-1006Crossref PubMed Scopus (95) Google Scholar, 5Baarends W.M. Uilenbroek J.T. Kramer P. Hoogerbrugge J.W. van Leeuwen E.C. Themmen A.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: 4951-4962Crossref PubMed Google Scholar, 6Hirobe S. He W.W. Gustafson M.L. MacLaughlin D.T. Donahoe P.K. Müllerian inhibiting substance gene expression in the cycling rat ovary correlates with recruited or Graafian follicle selection.Biol Reprod. 1994; 50: 1238-1243Crossref PubMed Scopus (56) Google Scholar, 7Weenen C. Laven J.S. Von Bergh A.R. Cranfield M. Groome N.P. Visser J.A. et al.Anti-Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment.Mol Hum Reprod. 2004; 10: 77-83Crossref PubMed Scopus (979) Google Scholar, 8Stubbs S.A. Hardy K. Da Silva-Buttkus P. Stark J. Webber L.J. Flanagan A.M. et al.Anti-Müllerian hormone protein expression is reduced during the initial stages of follicle development in human polycystic ovaries.J Clin Endocrinol Metab. 2005; 90: 5536-5543Crossref PubMed Scopus (127) Google Scholar, 9Themmen A.P. Anti-Müllerian hormone: its role in follicular growth initiation and survival and as an ovarian reserve marker.J Natl Cancer Inst Monogr. 2005; 34: 18-21Crossref PubMed Scopus (80) Google Scholar, 10Visser J.A. Themmen A.P. Anti-Müllerian hormone and folliculogenesis.Mol Cell Endocrinol. 2005; 234: 81-86Crossref PubMed Scopus (329) Google Scholar). In experiments using MIS knockout mice, the null females had more preantral and small antral follicles at 25 days and 4 months, but at 13 months, the null females had almost no primordial follicles, which suggested that they had an early depletion of primordial follicles (11Durlinger A.L. Kramer P. Karels B. de Jong F.H. Uilenbroek J.T. Grootegoed J.A. et al.Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary.Endocrinology. 1999; 140: 5789-5796Crossref PubMed Scopus (569) Google Scholar). Further data indicated that MIS regulates the development of early follicles in two ways: [1] as a negative stimulator of follicular maturation, and [2] as an inhibitor of FSH sensitivity of growing follicles, which serves to negatively modulate the FSH-dependent selection of dominant follicles (12Durlinger A.L. Gruijters M.J. Kramer P. Karels B. Ingraham H.A. Nachtigal M.W. et al.Anti-Müllerian hormone inhibits initiation of primordial follicle growth in the mouse ovary.Endocrinology. 2002; 143: 1076-1084Crossref PubMed Scopus (476) Google Scholar, 13Durlinger A.L. Gruijters M.J. Kramer P. Karels B. Kumar T.R. Matzuk M.M. et al.Anti-Müllerian hormone attenuates the effects of FSH on follicle development in the mouse ovary.Endocrinology. 2001; 142: 4891-4899Crossref PubMed Scopus (430) Google Scholar, 14Durlinger A.L. Visser J.A. Themmen A.P. Regulation of ovarian function: the role of anti-Müllerian hormone.Reproduction. 2002; 124: 601-609Crossref PubMed Scopus (588) Google Scholar). Ovarian reserve is a term used to denote the potential for reproduction (15Arroyo A. Yeh J. Understanding the menopausal transition, and managing its clinical challenges.Sex Reprod Menopause. 2005; 3: 12-17Crossref Scopus (11) Google Scholar, 16Practice Committee of the American Society for Reproductive MedicineAging and infertility in women.Fertil Steril. 2004; 82: S102-S106PubMed Google Scholar). A number of investigators presented data to support the hypothesis that MIS could be used as a biomarker of ovarian age and ovarian reserve in humans (17de Vet A. Laven J.S. de Jong F.H. Themmen A.P. Fauser B.C. Anti-Müllerian hormone serum levels: a putative marker for ovarian aging.Fertil Steril. 2002; 77: 357-362Abstract Full Text Full Text PDF PubMed Scopus (721) Google Scholar, 18van Rooij I.A. Broekmans F.J. te Velde E.R. Fauser B.C. Bancsi L.F. de Jong F.H. Themmen A.P. Serum anti-Müllerian hormone levels: a novel measure of ovarian reserve.Hum Reprod. 2002; 17: 3065-3071Crossref PubMed Scopus (815) Google Scholar, 19Fanchin R. Schonauer L.M. Righini C. Guibourdenche J. Frydman R. Taieb J. Serum anti-Müllerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3.Hum Reprod. 2003; 18: 323-327Crossref PubMed Scopus (532) Google Scholar, 20Hazout A. Bouchard P. Seifer D.B. Aussage P. Junca A.M. Cohen-Bacrie P. Serum anti-Müllerian hormone/Müllerian-inhibiting substance appears to be a more discriminatory marker of assisted reproductive technology outcome than follicle-stimulating hormone, inhibin B, or estradiol.Fertil Steril. 2004; 82: 1323-1329Abstract Full Text Full Text PDF PubMed Scopus (268) Google Scholar, 21van Rooij I.A. Tonkelaar I. Broekmans F.J. Looman C.W. Scheffer G.J. de Jong F.H. et al.Anti-Müllerian hormone is a promising predictor for the occurrence of the menopausal transition.Menopause. 2004; 11: 601-606Crossref PubMed Scopus (243) Google Scholar, 22Fanchin R. Taieb J. Lozano D.H. Ducot B. Frydman R. Bouyer J. High reproducibility of serum anti-Müllerian hormone measurements suggests a multi-staged follicular secretion and strengthens its role in the assessment of ovarian follicular status.Hum Reprod. 2005; 20: 923-927Crossref PubMed Scopus (249) Google Scholar, 23Pastor C.L. Vanderhoof V.H. Lim L.C.L. Calis K.A. Premkumar A. Guerrero N.T. et al.Pilot study investigating the age-related decline in ovarian function of regularly menstruating normal women.Fertil Steril. 2005; 84: 1462-1469Abstract Full Text Full Text PDF PubMed Scopus (19) Google Scholar, 24Tremellen K.P. Kolo M. Gilmore A. Lekamge D.N. Anti-Müllerian hormone as a marker of ovarian reserve.Aust N Z J Obstet Gynaecol. 2005; 45: 20-24Crossref PubMed Scopus (166) Google Scholar, 25van Rooij I.A. Broekmans F.J. Scheffer G.J. Looman C.W. Habbema J.D. de Jong F.H. et al.Serum anti-Müllerian hormone levels best reflect the reproductive decline with age in normal women with proven fertility: a longitudinal study.Fertil Steril. 2005; 83: 979-987Abstract Full Text Full Text PDF PubMed Scopus (456) Google Scholar, 26Fanchin R. Louafi N. Lozano D.H. Frydman N. Frydman R. Taieb J. Per-follicle measurements indicate that anti-Müllerian hormone secretion is modulated by the extent of follicular development and luteinization and may reflect qualitatively the ovarian follicular status.Fertil Steril. 2005; 84: 167-173Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 27Muttukrishna S. McGarrigle H. Wakim R. Khadum I. Ranieri D.M. Serhal P. Antral follicle count, anti-Mullerian hormone and inhibin B: predictors of ovarian response in assisted reproductive technology?.Br J Obstet Gynaecol. 2005; 112: 1384-1390Crossref Scopus (242) Google Scholar). In humans, findings showed [1] that serum MIS levels decline with increasing reproductive age, [2] that after oophorectomy there is a precipitate drop in levels of MIS, [3] that after gonadotropin stimulation for assisted reproductive technologies, the levels of MIS decline, and [4] that the follicular-fluid MIS levels differ between younger patients and older patients (17de Vet A. Laven J.S. de Jong F.H. Themmen A.P. Fauser B.C. Anti-Müllerian hormone serum levels: a putative marker for ovarian aging.Fertil Steril. 2002; 77: 357-362Abstract Full Text Full Text PDF PubMed Scopus (721) Google Scholar, 18van Rooij I.A. Broekmans F.J. te Velde E.R. Fauser B.C. Bancsi L.F. de Jong F.H. Themmen A.P. Serum anti-Müllerian hormone levels: a novel measure of ovarian reserve.Hum Reprod. 2002; 17: 3065-3071Crossref PubMed Scopus (815) Google Scholar, 19Fanchin R. Schonauer L.M. Righini C. Guibourdenche J. Frydman R. Taieb J. Serum anti-Müllerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3.Hum Reprod. 2003; 18: 323-327Crossref PubMed Scopus (532) Google Scholar, 20Hazout A. Bouchard P. Seifer D.B. Aussage P. Junca A.M. Cohen-Bacrie P. Serum anti-Müllerian hormone/Müllerian-inhibiting substance appears to be a more discriminatory marker of assisted reproductive technology outcome than follicle-stimulating hormone, inhibin B, or estradiol.Fertil Steril. 2004; 82: 1323-1329Abstract Full Text Full Text PDF PubMed Scopus (268) Google Scholar, 21van Rooij I.A. Tonkelaar I. Broekmans F.J. Looman C.W. Scheffer G.J. de Jong F.H. et al.Anti-Müllerian hormone is a promising predictor for the occurrence of the menopausal transition.Menopause. 2004; 11: 601-606Crossref PubMed Scopus (243) Google Scholar, 22Fanchin R. Taieb J. Lozano D.H. Ducot B. Frydman R. Bouyer J. High reproducibility of serum anti-Müllerian hormone measurements suggests a multi-staged follicular secretion and strengthens its role in the assessment of ovarian follicular status.Hum Reprod. 2005; 20: 923-927Crossref PubMed Scopus (249) Google Scholar, 23Pastor C.L. Vanderhoof V.H. Lim L.C.L. Calis K.A. Premkumar A. Guerrero N.T. et al.Pilot study investigating the age-related decline in ovarian function of regularly menstruating normal women.Fertil Steril. 2005; 84: 1462-1469Abstract Full Text Full Text PDF PubMed Scopus (19) Google Scholar, 24Tremellen K.P. Kolo M. Gilmore A. Lekamge D.N. Anti-Müllerian hormone as a marker of ovarian reserve.Aust N Z J Obstet Gynaecol. 2005; 45: 20-24Crossref PubMed Scopus (166) Google Scholar, 25van Rooij I.A. Broekmans F.J. Scheffer G.J. Looman C.W. Habbema J.D. de Jong F.H. et al.Serum anti-Müllerian hormone levels best reflect the reproductive decline with age in normal women with proven fertility: a longitudinal study.Fertil Steril. 2005; 83: 979-987Abstract Full Text Full Text PDF PubMed Scopus (456) Google Scholar, 26Fanchin R. Louafi N. Lozano D.H. Frydman N. Frydman R. Taieb J. Per-follicle measurements indicate that anti-Müllerian hormone secretion is modulated by the extent of follicular development and luteinization and may reflect qualitatively the ovarian follicular status.Fertil Steril. 2005; 84: 167-173Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 27Muttukrishna S. McGarrigle H. Wakim R. Khadum I. Ranieri D.M. Serhal P. Antral follicle count, anti-Mullerian hormone and inhibin B: predictors of ovarian response in assisted reproductive technology?.Br J Obstet Gynaecol. 2005; 112: 1384-1390Crossref Scopus (242) Google Scholar, 28La Marca A. De Leo V. Giulini S. Orvieto R. Giannella L. Volpe A. Anti-Müllerian hormone in premenopausal women and after spontaneous or surgically induced menopause.J Soc Gynecol Invest. 2005; 12: 545-548Crossref PubMed Scopus (96) Google Scholar). Kevenaar et al. measured serum MIS in mice, and the decline in MIS levels found in aging mice is consistent with the results obtained in humans (29Kevenaar M.E. Meerasahib M.F. Kramer P. van de Lang-Born B.M.N. de Jong F.H. Groome N.P. et al.Serum anti-Müllerian hormone levels reflect the size of the primordial follicle pool in mice.Endocrinology. 2006; 147: 3228-3234Crossref PubMed Scopus (309) Google Scholar). It was hypothesized in this study that the physiological basis of the age-dependent decline in serum MIS is because of a decrease in the number of ovarian follicles expressing MIS. We sought to determine how the levels of MIS in the rat might change during ovarian chronological aging, and we looked for specific histologic features leading to MIS changes in aging. Female Sprague-Dawley rats were used (Harlan, Indianapolis, IN) (30Palumbo A. Yeh J. In situ localization of apoptosis in the rat ovary during follicular atresia.Biol Reprod. 1994; 51: 888-895Crossref PubMed Scopus (156) Google Scholar). The animals studied were immature (26 days old; “young”) females, adult (65–75 days old; “adult”) females, and retired breeders (8–9 months old; “reproductive aging;” retired breeders have smaller litter sizes or increased estrous-cycle irregularity). This study was approved by the Institutional Animal Care and Use Committee of the University at Buffalo (protocol GYN07042N). The adult and reproductive-aging animals were studied both as estrous-cycle staged and as estrous-cycle nonstaged (31Marcondes F.K. Bianchi F.J. Tanno A.P. Determination of the estrous cycle phases of rats: some helpful considerations.Braz J Biol. 2002; 62: 609-614Crossref PubMed Scopus (989) Google Scholar). The females of the three age groups were examined at baseline, and were given an ovarian challenge with pregnant mare serum gonadotropin (PMSG) to replicate preovulatory conditions, so as to further distinguish the differences in the three age groups. Therefore, the rats were sacrificed at 0 hours and at 54 hours, after an injection of PMSG (1 IU/g body weight; Sigma, St. Louis, MO) (32Soodak L.K. Behrman H.R. Mitochondria mediate amplification of luteinizing hormone action by adenosine in luteal cells.Endocrinology. 1988; 122: 1308-1313Crossref PubMed Scopus (6) Google Scholar). Blood was collected via terminal cardiac puncture. The ovaries were collected, with one ovary snap-frozen and then stored at −80°C, and the other ovary fixed in 10% formalin for paraffin sectioning. For measurement of serum MIS, the DSL-10-14400 MIS ELISA kit was used (DSL, Webster, TX). We used this commercial kit because it was the intent of this study to understand the relative changes of rat MIS levels in different conditions. Whole ovaries were used for the MIS protein analysis, as prepared by the protocol of Yeh et al. (33Yeh J. Kim B. Liang Y.J. Peresie J. Müllerian inhibiting substance as a novel biomarker of cisplatin-induced ovarian damage.Biochem Biophys Res Commun. 2006; 348: 337-344Crossref PubMed Scopus (39) Google Scholar). Quantitative analysis of MIS levels in ovarian lysates was performed with the DSL-10-14400 MIS ELISA kit, as described. The final results were normalized to “ng/mg total protein,” to allow comparisons of MIS concentrations between the three age groups. The Western blot method followed a previously described method (33Yeh J. Kim B. Liang Y.J. Peresie J. Müllerian inhibiting substance as a novel biomarker of cisplatin-induced ovarian damage.Biochem Biophys Res Commun. 2006; 348: 337-344Crossref PubMed Scopus (39) Google Scholar, 34Khan S.M. Oliver R.H. Yeh J. Epidermal growth factor receptor inhibition by tyrphostin 51 induces apoptosis in luteinized granulosa cells.J Clin Endocrinol Metab. 2005; 90: 469-473Crossref PubMed Scopus (15) Google Scholar). Reducing conditions were used to optimize the visualization of MIS proteins. The membranes were incubated with goat anti-MIS antibody (1:200, C-20:sc-6886; Santa Cruz Biotechnology, Santa Cruz, CA). Membranes were reprobed for actin for normalization. Immunofluorescence studies were performed with the use of previously described methods (33Yeh J. Kim B. Liang Y.J. Peresie J. Müllerian inhibiting substance as a novel biomarker of cisplatin-induced ovarian damage.Biochem Biophys Res Commun. 2006; 348: 337-344Crossref PubMed Scopus (39) Google Scholar), with goat anti-MIS as primary antibody (1:100 dilution; C-20: sc-6886; Santa Cruz Biotechnology). For the negative control experiments, preimmune serum was applied. To quantify the number of positive MIS follicles, each ovarian follicle was evaluated by the criteria of Liao et al. (35Liao Y. Abel U. Grobholz R. Hermani A. Trojan L. Angel P. et al.Up-regulation of insulin-like growth factor axis components in human primary prostate cancer correlates with tumor grade.Hum Pathol. 2005; 36: 1186Abstract Full Text Full Text PDF PubMed Scopus (88) Google Scholar) and Yeh et al. (33Yeh J. Kim B. Liang Y.J. Peresie J. Müllerian inhibiting substance as a novel biomarker of cisplatin-induced ovarian damage.Biochem Biophys Res Commun. 2006; 348: 337-344Crossref PubMed Scopus (39) Google Scholar) to obtain a final immunofluorescent score. Two independent observers reviewed the ovarian sections. To obtain a relative ovarian follicle count, a count was obtained in the ovarian sections of each age group. The results are presented as mean ± SEM. The experiments were repeated 3–6 times. Analysis of variance (ANOVA), followed by Scheffé’s post hoc analysis, was used for comparison of different groups, when appropriate. P<.05 was considered significant. The serum MIS results show that basal serum MIS levels spontaneously declined in the rat with increasing chronological age. After the animals were challenged with PMSG, a decline in the serum levels of MIS for the young and adult rats was found (0 hours versus 54 hours, P<.05; Fig. 1A). However, after stimulation with PMSG, there was no change in serum MIS levels in the reproductive-aging animals (P=NS). In addition, when comparing the relative MIS levels at 54 hours for the young, adult, and reproductive-aging females, there was still a comparative stepwise fall in MIS serum levels with rising chronological age after PMSG challenge (P<.01). The serum levels of MIS in all stages of the estrous cycle showed that the serum MIS measurement distinguishes between adult and reproductive-aging females at every stage of the estrous cycle and that, after PMSG stimulation, serum MIS levels continued to be able to differentiate between the adult and reproductive-aging females. The ovaries were analyzed by two different methods to quantify MIS protein levels. First, ovarian lysates were measured for MIS levels by using ELISA. At baseline (0 hours), there was a reduction with increasing chronological age (P<.05). Furthermore, for the young and adult females, there was a decline from 0-hour levels in the ovarian lysates 54 hours after stimulation with PMSG (P<.05). No decline in the ovarian lysate MIS level was found in reproductive-aging females after stimulation with PMSG (P=NS). Western blot analysis showed that at 0 hours, there was a stepwise drop in the 65-kDa MIS protein level with increasing chronological age (P<.05). In addition, the 0-hour results of the MIS ELISA and Western blot analysis matched the serum results in which the young, adult, and reproductive-aging ovaries had progressively diminishing levels of MIS (Fig. 1B). Immunofluorescence showed that for all three age groups studied, the primary follicles and small antral follicles had the most intense staining for MIS. After PMSG ovarian stimulation, the primary follicles and small antral follicles continued to have the most intense staining for MIS. The number of the MIS positively stained follicles decreased with increasing chronological age at 0 hours (P<.001; Fig. 1C). In contrast, the percentage of positive staining follicles for MIS was relatively constant at 50%–60% for all three age groups at 0 hours (P=NS). Furthermore, after stimulation with PMSG, the percentage of immunoreactive follicles declined to the range of 20%–30% for all three age groups (P<.05 for 0 hours versus 54 hours, by ANOVA). The decline in number of MIS-positive small follicles mirrored the stepwise decrease found in serum MIS levels with increasing chronological age. To our knowledge, the results presented here are the first in the rat to show that serum and ovarian MIS levels decline with increasing chronological age. Importantly, the results described here confirm that the physiological basis for the decline in serum MIS found in aging is likely due to a decrease in the total number of MIS-positive small follicles, and not because of a loss in the percentage of MIS-positive follicles. This is in agreement with the results found in mice by Kevenaar et al. (29Kevenaar M.E. Meerasahib M.F. Kramer P. van de Lang-Born B.M.N. de Jong F.H. Groome N.P. et al.Serum anti-Müllerian hormone levels reflect the size of the primordial follicle pool in mice.Endocrinology. 2006; 147: 3228-3234Crossref PubMed Scopus (309) Google Scholar). Their work showed a clear association between serum MIS levels and the number of small follicles in the aging process. The decline in levels of serum MIS was highly correlated with the decline in number of primordial and growing follicles in aging mice up to 18 months of age. Building on the work of Kevenaar et al. (29Kevenaar M.E. Meerasahib M.F. Kramer P. van de Lang-Born B.M.N. de Jong F.H. Groome N.P. et al.Serum anti-Müllerian hormone levels reflect the size of the primordial follicle pool in mice.Endocrinology. 2006; 147: 3228-3234Crossref PubMed Scopus (309) Google Scholar), our work extends the understanding of the decline of serum MIS in aging in three respects. First, we showed by quantitative MIS Western blot analysis that ovarian MIS protein declined in parallel to the serum MIS changes. Second, we demonstrated that gonadotropin stimulation of the ovaries resulted in a decline in serum MIS levels after ovarian stimulation only in the younger reproductive age groups. Third, we showed that the number of MIS-positive follicles in aging, as demonstrated by immunohistochemistry, paralleled the serum MIS decline in aging. Thus, our work supports the findings of Kevenaar et al. (29Kevenaar M.E. Meerasahib M.F. Kramer P. van de Lang-Born B.M.N. de Jong F.H. Groome N.P. et al.Serum anti-Müllerian hormone levels reflect the size of the primordial follicle pool in mice.Endocrinology. 2006; 147: 3228-3234Crossref PubMed Scopus (309) Google Scholar), and extends the association between serum levels of MIS and aging-associated changes found in the ovary. From the rat data generated in this study, the mathematical curves in chronological aging for both serum MIS levels and total ovarian MIS levels could be calculated. Modeling of the decline in MIS with increasing age revealed that both calculated curves are exponential decay curves. Our extrapolation is in agreement with the conclusions of de Vet et al. (17de Vet A. Laven J.S. de Jong F.H. Themmen A.P. Fauser B.C. Anti-Müllerian hormone serum levels: a putative marker for ovarian aging.Fertil Steril. 2002; 77: 357-362Abstract Full Text Full Text PDF PubMed Scopus (721) Google Scholar) and Visser et al. (36Visser J.A. de Jong F.H. Laven J.S.E. Themmen A.P.N. Anti-Müllerian hormone: a new marker for ovarian function.Reproduction. 2006; 131: 1-9Crossref PubMed Scopus (600) Google Scholar), that MIS is an early marker of ovarian aging, and that MIS may indicate ovarian aging earlier than FSH. The histological basis of the decline in serum MIS in chronological aging had not been characterized until this study. In human studies by de Vet et al. (17de Vet A. Laven J.S. de Jong F.H. Themmen A.P. Fauser B.C. Anti-Müllerian hormone serum levels: a putative marker for ovarian aging.Fertil Steril. 2002; 77: 357-362Abstract Full Text Full Text PDF PubMed Scopus (721) Google Scholar) and Fanchin et al. (19Fanchin R. Schonauer L.M. Righini C. Guibourdenche J. Frydman R. Taieb J. Serum anti-Müllerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3.Hum Reprod. 2003; 18: 323-327Crossref PubMed Scopus (532) Google Scholar), as subsequently reviewed by Visser et al. (36Visser J.A. de Jong F.H. Laven J.S.E. Themmen A.P.N. Anti-Müllerian hormone: a new marker for ovarian function.Reproduction. 2006; 131: 1-9Crossref PubMed Scopus (600) Google Scholar), a correlation was observed between serum MIS levels and the antral follicle count as determined by ultrasonography. Further, Fanchin et al. (26Fanchin R. Louafi N. Lozano D.H. Frydman N. Frydman R. Taieb J. Per-follicle measurements indicate that anti-Müllerian hormone secretion is modulated by the extent of follicular development and luteinization and may reflect qualitatively the ovarian follicular status.Fertil Steril. 2005; 84: 167-173Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar) showed a correlation between the ultrasonographically defined small follicle count and the serum MIS level, and concluded that the serum MIS level may reflect per-follicle MIS follicle production. The findings reported in this study extend the previous studies, and show histologically that it is the total number of small follicles that are MIS-positive that is related to the serum MIS level. Moreover, the present data demonstrate that even after ovarian stimulation, MIS level reflects the number of MIS-positive small follicles." @default.
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• W1965297895 title "Serum and ovarian Müllerian inhibiting substance, and their decline in reproductive aging" @default.
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• W1965297895 doi "https://doi.org/10.1016/j.fertnstert.2006.11.011" @default.
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