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Endocrine Reviews, doi:10.1210/edrv-9-2-267
Endocrine Reviews 9 (2): 267-293
Copyright © 1988 by The Endocrine Society
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Inhibins, Activins, and Follistatins: Gonadal Proteins Modulating the Secretion of Follicle-Stimulating Hormone

SHAO-YAO YING

Laboratories for Neuroendocrinology, The Salk Institute La Jolla, California 92037

Correspondence: Address requests for reprints to: Shao-Yao Ying, Ph.D., Laboratories for Neuroendocrinology, The Salk Institute, 10010 North Torrey Pines Road, La Jolla, California 92037.

Abstract

I. Introduction: The concept that proteins, in addition to steroid hormones, of gonadal origin could play a role in the inhibition of gonadatropin secretion from the anterior lobe of the pituitary was proposed more than 65 yr ago. Only recently, however, has the elucidation of the chemistry and physiology of these proposed gonadal hormones actually been achieved. Mottram and Cramer (1) reported pituitary hypertrophy as determined by the appearance of so-called castration cells in the anterior lobe of pituitary after treatment of the testes with radium. The removal of the testes leads to the development of highly vacuolated, signet-shaped basophil cells in the pituitary (2), termed castration cells, demonstrating a reciprocal relationship between the pituitary and the gonads and suggesting that a secretion of the testes has an inhibitory effect on the pituitary (3). The pituitary hypertrophy after castration or irradiation of the testes was postulated to be due to a lack of some substance from the seminal epithelium because vasectomy totally prevented the morphological changes, suggesting that the status of the seminiferous tubules might be responsible for the observed changes in the pituitary gland.




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M. W. Elting, J. Kwee, R. Schats, L. T. M. Rekers-Mombarg, and J. Schoemaker
The Rise of Estradiol and Inhibin B after Acute Stimulation with Follicle-Stimulating Hormone Predict the Follicle Cohort Size in Women with Polycystic Ovary Syndrome, Regularly Menstruating Women with Polycystic Ovaries, and Regularly Menstruating Women with Normal Ovaries
J. Clin. Endocrinol. Metab., April 1, 2001; 86(4): 1589 - 1595.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
M. Baratta, L.A. West, A.M. Turzillo, and T.M. Nett
Activin Modulates Differential Effects of Estradiol on Synthesis and Secretion of Follicle-Stimulating Hormone in Ovine Pituitary Cells
Biol Reprod, February 1, 2001; 64(2): 714 - 719.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
F. J. Hayes, S. DeCruz, S. B. Seminara, P. A. Boepple, and W. F. Crowley Jr.
Differential Regulation of Gonadotropin Secretion by Testosterone in the Human Male: Absence of a Negative Feedback Effect of Testosterone on Follicle-Stimulating Hormone Secretion
J. Clin. Endocrinol. Metab., January 1, 2001; 86(1): 53 - 58.
[Abstract] [Full Text]

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 J. Immunol.Home page
K. Ogawa, M. Funaba, L. S. Mathews, and T. Mizutani
Activin A Stimulates Type IV Collagenase (Matrix Metalloproteinase-2) Production in Mouse Peritoneal Macrophages
J. Immunol., September 15, 2000; 165(6): 2997 - 3003.
[Abstract] [Full Text] [PDF]

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 Mol Hum ReprodHome page
F. Debieve, S. Pampfer, and K. Thomas
Inhibin and activin production and subunit expression in human placental cells cultured in vitro
Mol. Hum. Reprod., August 1, 2000; 6(8): 743 - 749.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
C. H. de Koning, C. Popp-Snijders, J. Schoemaker, and C. B. Lambalk
Elevated FSH concentrations in imminent ovarian failure are associated with higher FSH and LH pulse amplitude and response to GnRH
Hum. Reprod., July 1, 2000; 15(7): 1452 - 1456.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
T. Minegishi, T. Kameda, T. Hirakawa, K. Abe, M. Tano, and Y. Ibuki
Expression of Gonadotropin and Activin Receptor Messenger Ribonucleic Acid in Human Ovarian Epithelial Neoplasms
Clin. Cancer Res., July 1, 2000; 6(7): 2764 - 2770.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
T. Wu, H. Patel, S. Mukai, C. Melino, R. Garg, X. Ni, J. Chang, and C. Peng
Activin, Inhibin, and Follistatin in Zebrafish Ovary: Expression and Role in Oocyte Maturation
Biol Reprod, June 1, 2000; 62(6): 1585 - 1592.
[Abstract] [Full Text]

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 Hum ReprodHome page
C. M. Foster, D. J. Phillips, T. Wyman, L. W. Evans, N. P. Groome, and V. Padmanabhan
Changes in serum inhibin, activin and follistatin concentrations during puberty in girls
Hum. Reprod., May 1, 2000; 15(5): 1052 - 1057.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
D. J. Hecht, A. J. Davis, C. F. Brooks, and P. A. Johnson
Molecular Cloning and Expression Analysis of the Complementary Deoxyribonucleic Acid for Chicken Inhibin/Activin {beta}B Subunit
Biol Reprod, May 1, 2000; 62(5): 1128 - 1134.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
X. Ni, S. Luo, T. Minegishi, and C. Peng
Activin A in JEG-3 Cells: Potential Role as an Autocrine Regulator of Steroidogenesis in Humans
Biol Reprod, May 1, 2000; 62(5): 1224 - 1230.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
F. Debieve, S. Beerlandt, C. Hubinont, and K. Thomas
Gonadotropins, Prolactin, Inhibin A, Inhibin B, and Activin A in Human Fetal Serum from Midpregnancy and Term Pregnancy
J. Clin. Endocrinol. Metab., January 1, 2000; 85(1): 270 - 274.
[Abstract] [Full Text]

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 EndocrinologyHome page
M. Tena-Sempere, J. Kero, A. Rannikko, W. Yan, and I. Huhtaniemi
The Pattern of Inhibin/Activin {alpha}- and {beta}B-Subunit Messenger Ribonucleic Acid Expression in Rat Testis after Selective Leydig Cell Destruction by Ethylene Dimethane Sulfonate
Endocrinology, December 1, 1999; 140(12): 5761 - 5770.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
J. D. Veldhuis, A. Iranmanesh, L. M. Demers, and T. Mulligan
Joint Basal and Pulsatile Hypersecretory Mechanisms Drive the Monotropic Follicle-Stimulating Hormone (FSH) Elevation in Healthy Older Men: Concurrent Preservation of the Orderliness of the FSH Release Process: A General Clinical Research Center Study
J. Clin. Endocrinol. Metab., October 1, 1999; 84(10): 3506 - 3514.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
Y. Pang and W. Ge
Activin Stimulation of Zebrafish Oocyte Maturation in Vitro and Its Potential Role in Mediating Gonadotropin-Induced Oocyte Maturation
Biol Reprod, October 1, 1999; 61(4): 987 - 992.
[Abstract] [Full Text]

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 Endocr. Rev.Home page
D. Engler, E. Redei, and I. Kola
The Corticotropin-Release Inhibitory Factor Hypothesis: A Review of the Evidence for the Existence of Inhibitory as Well as Stimulatory Hypophysiotropic Regulation of Adrenocorticotropin Secretion and Biosynthesis
Endocr. Rev., August 1, 1999; 20(4): 460 - 500.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
A. Pappa, K. Seferiadis, T. Fotsis, A. Shevchenko, M. Marselos, O. Tsolas, and I. E.Messinis
Purification of a candidate gonadotrophin surge attenuating factor from human follicular fluid
Hum. Reprod., June 1, 1999; 14(6): 1449 - 1456.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
J.H. Bame, J.C. Dalton, S.D. Degelos, T.E.M. Good, J.L.H. Ireland, F. Jimenez-Krassel, T. Sweeney, R.G. Saacke, and J.J. Ireland
Effect of Long-Term Immunization against Inhibin on Sperm Output in Bulls
Biol Reprod, June 1, 1999; 60(6): 1360 - 1366.
[Abstract] [Full Text]

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 Endocr. Rev.Home page
S. L. Asa and S. Ezzat
The Cytogenesis and Pathogenesis of Pituitary Adenomas
Endocr. Rev., December 1, 1998; 19(6): 798 - 827.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
M. Safi, N. Buys, O.M. Onagbesan, B. Vleugels, and E. Decuypere
Quantification of Inhibin/Activin {alpha} and ßA Subunit Messenger Ribonucleic Acid by Competitive Reverse Transcription-Polymerase Chain Reaction in Chicken Granulosa Cells during Follicular Development
Biol Reprod, November 1, 1998; 59(5): 1047 - 1054.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
N. E. Reame, T. L. Wyman, D. J. Phillips, D. M. de Kretser, and V. Padmanabhan
Net Increase in Stimulatory Input Resulting from a Decrease in Inhibin B and an Increase in Activin A May Contribute in Part to the Rise in Follicular Phase Follicle-Stimulating Hormone of Aging Cycling Women
J. Clin. Endocrinol. Metab., September 1, 1998; 83(9): 3302 - 3307.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
M. E. Wilson and R. J. Handa
Activin Subunit, Follistatin, and Activin Receptor Gene Expression in the Prepubertal Female Rat Pituitary
Biol Reprod, August 1, 1998; 59(2): 278 - 283.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
F. J. Hayes, J. E. Hall, P. A. Boepple, and W. F. Crowley Jr.
Differential Control of Gonadotropin Secretion in the Human: Endocrine Role of Inhibin
J. Clin. Endocrinol. Metab., June 1, 1998; 83(6): 1835 - 1841.
[Full Text]

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 EndocrinologyHome page
A. C. Dalkin, D. J. Haisenleder, J. T. Gilrain, K. Aylor, M. Yasin, and J. C. Marshall
Regulation of Pituitary Follistatin and Inhibin/Activin Subunit Messenger Ribonucleic Acids (mRNAs) in Male and Female Rats: Evidence for Inhibin Regulation of Follistatin mRNA in Females
Endocrinology, June 1, 1998; 139(6): 2818 - 2823.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
M. Szabo, S. M. Kilen, S. Saberi, S. J. Ringstrom, and N. B. Schwartz
Antiprogestins Suppress Basal and Activin-Stimulated Follicle-Stimulating Hormone Secretion in an Estrogen-Dependent Manner
Endocrinology, May 1, 1998; 139(5): 2223 - 2228.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
D. S. McConnell, Q. Wang, P. M. Sluss, N. Bolf, R. H. Khoury, A. L. Schneyer, A. R. Midgley Jr., N. E. Reame, W. F. Crowley Jr., and V. Padmanabhan
A Two-Site Chemiluminescent Assay for Activin-Free Follistatin Reveals That Most Follistatin Circulating in Men and Normal Cycling Women Is in an Activin-Bound State
J. Clin. Endocrinol. Metab., March 1, 1998; 83(3): 851 - 858.
[Abstract] [Full Text]

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 EndocrinologyHome page
N. Di Simone, H. A. Hall, C. Welt, and A. L. Schneyer
Activin Regulates {beta}A-Subunit and Activin Receptor Messenger Ribonucleic Acid and Cellular Proliferation in Activin-Responsive Testicular Tumor Cells
Endocrinology, March 1, 1998; 139(3): 1147 - 1155.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
T. M. Lovell, R. T. Gladwell, F. J. Cunningham, N. P. Groome, and P. G. Knight
Differential Changes in Inhibin A, Activin A, and Total {alpha}-Subunit Levels in Granulosa and Thecal Layers of Developing Preovulatory Follicles in the Chicken
Endocrinology, March 1, 1998; 139(3): 1164 - 1171.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
N. A. Cataldo, V. Y. Fujimoto, and R. B. Jaffe
Interferon-{gamma} and Activin A Promote Insulin-Like Growth Factor-Binding Protein-2 and -4 Accumulation by Human Luteinizing Granulosa Cells, and Interferon-{gamma} Promotes Their Apoptosis
J. Clin. Endocrinol. Metab., January 1, 1998; 83(1): 179 - 186.
[Abstract] [Full Text]

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 J. Histochem. Cytochem.Home page
G. V. Childs and G. Unabia
Cytochemical Studies of the Effects of Activin on Gonadotropin-releasing Hormone (GnRH) Binding by Pituitary Gonadotropes and Growth Hormone Cells
J. Histochem. Cytochem., December 1, 1997; 45(12): 1603 - 1610.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
F. Petraglia, S. Luisi, C. Benedetto, M. Zonca, P. Florio, E. Casarosa, A. Volpe, S. Bernasconi, and A. R. Genazzani
Changes of Dimeric Inhibin B Levels in Maternal Serum Throughout Healthy Gestation and in Women with Gestational Diseases
J. Clin. Endocrinol. Metab., September 1, 1997; 82(9): 2991 - 2995.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
C. K. Welt, K. A. Martin, A. E. Taylor, G. M. Lambert-Messerlian, W. F. Crowley Jr., J. A. Smith, D. A. Schoenfeld, and J. E. Hall
Frequency Modulation of Follicle-Stimulating Hormone (FSH) during the Luteal-Follicular Transition: Evidence for FSH Control of Inhibin B in Normal Women
J. Clin. Endocrinol. Metab., August 1, 1997; 82(8): 2645 - 2652.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
L. M. Besecke, M. J. Guendner, P. A. Sluss, A. G. Polak, T. K. Woodruff, J. L. Jameson, A. C. Bauer-Dantoin, and J. Weiss
Pituitary Follistatin Regulates Activin-Mediated Production of Follicle-Stimulating Hormone during the Rat Estrous Cycle
Endocrinology, July 1, 1997; 138(7): 2841 - 2848.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
S. Mesiano and R. B. Jaffe
Developmental and Functional Biology of the Primate Fetal Adrenal Cortex
Endocr. Rev., June 1, 1997; 18(3): 378 - 403.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
P. Pigny, R. Desailloud, C. Cortet-Rudelli, A. Duhamel, D. Deroubaix-Allard, A. Racadot, and D. Dewailly
Serum {alpha}-Inhibin Levels in Polycystic Ovary Syndrome: Relationship to the Serum Androstenedione Level
J. Clin. Endocrinol. Metab., June 1, 1997; 82(6): 1939 - 1943.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
G. Majdic, A. S. McNeilly, R. M. Sharpe, L. R. Evans, N. P. Groome, and P. T. K. Saunders
Testicular Expression of Inhibin and Activin Subunits and Follistatin in the Rat and Human Fetus and Neonate and During Postnatal Development in the Rat
Endocrinology, May 1, 1997; 138(5): 2136 - 2147.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
J. D. Veldhuis, A. Iranmanesh, E. Samojlik, and R. J. Urban
Differential Sex Steroid Negative Feedback Regulation of Pulsatile Follicle-Stimulating Hormone Secretion in Healthy Older Men: Deconvolution Analysis and Steady- State Sex-Steroid Hormone Infusions in Frequently Sampled Healthy Older Individuals
J. Clin. Endocrinol. Metab., April 1, 1997; 82(4): 1248 - 1254.
[Abstract] [Full Text] [PDF]


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