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• W2023407302 abstract "Neurotropins and their receptors play an essential role in the differentiation and survival of neurons in the central and peripheral nervous systems. Their actions, however, do not appear to be limited to the nervous system. At least four of the five known neurotropins, including nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF), neurotropin-3 (NT-3), and neurotropin-4/5 (NT-4/5), as well as their receptors (p75 NFR, trkA, trkB, and trk C) are present in the developing ovary. Studies using mice carrying null mutations of the genes encoding neurotropins NGF, NT-4/5, and BDNF have suggested that neurotropins are required for the growth of primordial follicles (1Ojeda S.R. Romero C.R. Tapia V. Disson G.A. Neurotrophic and cell-cell dependent control of early follicular development.Mol Cell Endocrinol. 2000; 163: 67-71Crossref PubMed Scopus (96) Google Scholar). In previous studies, we have demonstrated that BDNF and NT-4/5, but not NT-3, accelerate first polar body extrusion by mouse oocytes in vitro, suggesting involvement of trkB receptor binding in oocyte nuclear maturation (2Seifer DB, Feng B, Shelden RM, Chen S, Dreyfus CF. Brain-derived neurotrophic factor: a novel human ovarian follicular protein. J Clin Endocrinol Metab 2002;87:87:655–9Google Scholar, 3Seifer D.B. Feng B. Shelden R.M. Chen S. Dreyfus C.F. Neurotrophin-4/5 and neurotrophin-3 are present within the human ovarian follicle but appear to have different paracrine/autocrine functions.J Clin Endocrinol Metab. 2002; 87: 4569-4571Crossref PubMed Scopus (38) Google Scholar). We previously have demonstrated that human preovulatory cumulus granulosa cells secrete BDNF and that BDNF secretion is enhanced by cAMP in vitro. Our investigation of cAMP stimulation of BDNF production by human cumulus cells directed us to perform a series of experiments to determine whether FSH, LH, or hCG may influence BDNF production by cumulus granulosa cells. Eighteen women aged <42 years and undergoing oocyte retrieval for IVF were enrolled in the study. All had received leuprolide acetate (Lupron, TAP Pharmaceuticals, Inc., North Chicago, IL) for pituitary desensitization. Two to eight ampules of gonadotropins were given daily in divided doses between morning and evening as described elsewhere (4Seifer D.B. Gardiner A.C. Lambert-Messerlian G. Schneyer A.L. Differential secretion of dimeric inhibin in cultured luteinized granulosa cells as a function of ovarian reserve.J Clin Endocrinol Metab. 1996; 81: 736-739Crossref PubMed Scopus (64) Google Scholar). Transvaginal follicular aspiration was performed under sedation 36 hours after 5,000 or 10,000 IU hCG injection. Approval of this study was obtained from the institutional review board of UMDNJ—Robert Wood Johnson Medical School. Cumulus cells removed from oocytes in preparation for IVF–intracytoplasmic sperm injection were incubated with hyaluronidase (100 IU/mL, Sigma, St. Louis, MO) then washed twice with Hanks’ balanced salt solution (Sigma). In each experiment, cumulus granulosa cells from two or three patients were pooled, then plated at 1.5 × 105 cells in 0.3 mL of medium in a 24-well plate. Cumulus cells were cultured in Ham’s F-10 medium supplemented with 10% fetal bovine serum at 37°C, 5% CO2 in air. To study the regulation of BDNF secretion by human gonadotropins, cells were cultured for 24 hours, then rinsed two times with Ham’s F-10. Fresh Ham’s F-10 was added, with or without human recombinant FSH (Serono Laboratories, Randolph, MA), human menopausal urinary gonadotropin (Ferring Pharmaceuticals, Tarrytown, NJ), human pituitary LH, or hCG (both from Sigma, St. Louis, MO). Culture media were collected 24 hours later and stored at −80°C for assay of BDNF. BDNF levels were determined using the commercially available BDNF Emax immunoassay system (Promega, Madison, WI). The ELISAs were performed according to the manufacturer’s protocol. Granulosa cell culture media were diluted 1:2 (vol/vol) with sample buffer provided by manufacturer. All samples were assayed in duplicate. Each result was repeated at least twice. The BDNF assay demonstrated <3% cross-reactivity with related neurotrophic factors (NGF, NT-3, and NT-4) at 100 ng/mL. Assay sensitivity was 15.6 pg/mL, with a mean intra-assay coefficient of variance of 6.3%. The interassay coefficient of variance was 8.0%. Negative assay controls included the following: [1] absence of the reporting antibody specific to BDNF and [2] absence of reporting antibody and the ligand. Negative controls were included in each assay and demonstrated the absence of nonspecific binding. Statistical analysis of data was performed using a two-tailed t test. Statistical significance was assumed at P<.05. Figure 1 summarizes data demonstrating that BDNF secretion was enhanced up to fourfold (P<.03) by LH (50 ng/mL) in cumulus cell culture. When cumulus cells were exposed to hCG, BDNF secretion was increased 14-fold (P<.02) at hCG concentrations of 100 ng/mL (Fig. 1). Stimulation of BDNF secretion by hCG was demonstrated to be dose dependent (data not shown). Human menopausal urinary gonadotropin (10 mIU/mL), a mixture of approximately equal FSH and LH bioactivity, stimulated BDNF secretion by cumulus cells approximately twofold (P=.02). However, rFSH failed to stimulate BDNF secretion by cultured cumulus cells at concentrations of 0.1, 1, or 10 mIU/mL (data not shown). This study is a continuation of previous work, which demonstrated the presence of BDNF in human follicular fluid, its secretion by cumulus granulosa cells, and its increase in vitro secretion by cAMP (2Seifer DB, Feng B, Shelden RM, Chen S, Dreyfus CF. Brain-derived neurotrophic factor: a novel human ovarian follicular protein. J Clin Endocrinol Metab 2002;87:87:655–9Google Scholar). Because cAMP stimulation is the initial response to gonadotropin binding to appropriate receptors in the ovary, we investigated the response of BDNF secretion to gonadotropin stimulation of follicular cumulus granulosa cells. These data demonstrated that BDNF secretion by cumulus cells was enhanced by LH and hCG in vitro but was unchanged by was unchanged by rFSH treatment. It is speculated that the inability of FSH to elicit an increase in BDNF by cumulus cells in vitro may result from an absence of FSH receptors on mature cumulus cells, from FSH receptor saturation, or from the presence of an FSH receptor inhibitor (5Alouf C.A. Reichert L.E. Kellom T.A. Lee D.W. Cultured human granulosa cells secrete a follicle stimulating hormone receptor-binding inhibitor.Hum Reprod. 1997; 12: 2735-2740Crossref PubMed Scopus (2) Google Scholar). Although our data do not clearly support one of these possibilities over another, the differential response of granulosa cells to gonadotropins observed in these experiments is similar to that described by McAllister et al. (6McAllister J.M. Manson J.I. Byrd W. Trant J.M. Waterman M.R. Simpson E.R. Proliferating human granulosa-lutein cells in long term monolayer culture expression of aromatase, cholesterol side-chain cleavage, and 3β-hydroxysteroid dehydrogenase.J Clin Endocrinol Metab. 1990; 71: 26-33Crossref PubMed Scopus (52) Google Scholar) from studies employing primary cultures of granulosa cells. In their study, LH and hCG produced a dose-dependent increase in aromatase activity. However, aromatase activity was not significantly changed in response to FSH treatment. Furthermore, our present findings are consistent with other observations that BDNF levels in human follicular fluid are significantly higher in ART cycles (with hCG administration) than in natural cycles (without hCG administration) (7Seifer D.B. Lambert-Messerlian G. Schneyer A.L. Ovarian brain-derived neurotrophic factor (BDNF) is present in follicular fluid from normally cycling women.Fertil Steril. 2003; 79: 451-452Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar). Thus, these findings suggest that cumulus cells produce and secrete into follicular fluid an elevated concentration of BDNF after hCG administration. BDNF expression has been shown to be regulated by cAMP in neuronal and vascular endothelial as well as in ovarian granulosa cumulus cells. Results from the current experiments demonstrate that the gonadotropin LH serves as an active regulator of BDNF, possibly through the cAMP signaling pathway. At the present time, little is known regarding ovarian BDNF influence upon the female reproductive system. Results from this study provide the first evidence that LH signaling leads to alteration in synthesis and secretion of BDNF by cumulus cells. On the basis of these data and those from our previous studies, indicating that BDNF accelerates first polar body extrusion by mouse oocytes in vitro, BDNF may play important intraovarian roles in mediating LH actions in promoting late–follicular phase oocyte meiotic maturation. The authors are grateful to Amy Baker, B.S., and John Beloni, B.S., at the University Center for Reproductive Endocrinology and Fertility, UMDNJ—Robert Wood Johnson University Hospital, for their help with granulosa cell collection." @default.
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• W2023407302 title "Effect of gonadotropins on brain-derived neurotrophic factor secretion by human follicular cumulus cells" @default.
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