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Endocrine Reviews, doi:10.1210/edrv-5-1-76
Endocrine Reviews 5 (1): 76-127
Copyright © 1984 by The Endocrine Society
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Hormonal Regulation of the Differentiation of Cultured Ovarian Granulosa Cells*

AARON J. W. HSUEH{dagger}, E. Y. ADASHI{ddagger}, PHILLIP B. C. JONES§ and THOMAS H. WELSH, JR

Department of Reproductive Medicine, School of Medicine, M-025, University of California San Diego, La Jolla, California 92093

Correspondence: {dagger} To whom correspondence should be addressed. A.J.W.H. is the recipient of Research Career Development Award HD-00375.

Abstract

1. Cell Culture Approach to the Study of Granulosa Cells: In 1672, Regnier de Graaf first described the differentiation of ovarian follicles into the corpus luteum. He stated that "age and coitus cause very great changes in eggs (follicles). In young animals, they are very small and in more developed ones they are larger. After coitus, they (the follicles) so alter as to resemble the globules (the corpora lutea) ..., being one or more according as the animal will produce one or more fetuses." (1)

Follicles as the functional unit: Ovarian follicles have since been shown to be the basic functional unit of the ovary and consist of an outer layer of theca interna cells which encircle inner layers of granulosa cells. Granulosa cells, in turn, surround the innermost oocyte-cumulus cell complex. The maturation of ovarian follicles and their transformation into corpora lutea is regulated by a specific set of hormones and has been a major research area for ovarian physiologists for several hundred years.

Footnotes

* Research performed by the authors' laboratory is supported by NIH grants HD14084 and HD-12303.

{ddagger} Present address: Department of Obstetrics and Gynecology, University of Maryland School of Medicine, Baltimore, Maryland 21201.

§ Present address: Department of Pharmacology, Stanford University School of Medicine, Stanford, California 94305.

Present address: Department of Animal Science, Physiology of Reproduction Section, Kleberg Center, Texas A&M University, College Station, Texas 77843. T.H.W. was the recipient of a Bank of America-Giannini Foundation Fellowship.




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S. Chen, X. Liu, and D. L. Segaloff
A Novel Cyclic Adenosine 3',5'-Monophosphate-Responsive Element Involved In the Transcriptional Regulation of the Lutropin Receptor Gene in Granulosa Cells
Mol. Endocrinol., September 1, 2000; 14(9): 1498 - 1508.
[Abstract] [Full Text]

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 Arch NeurolHome page
J. I. T. Isojarvi and J. S. Tapanainen
Valproate, Hyperandrogenism, and Polycystic Ovaries: A Report of 3 Cases
Arch Neurol, July 1, 2000; 57(7): 1064 - 1068.
[Abstract] [Full Text] [PDF]

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J. Dor, D. Bider, A. Shulman, J. Levron, S. Shine, S. Mashiach, and J. Rabinovici
Effects of gonadotrophin-releasing hormone agonists on human ovarian steroid secretion in vivo and in vitro--results of a prospective, randomized in-vitro fertilization study
Hum. Reprod., June 1, 2000; 15(6): 1225 - 1230.
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E. A. McGee and A. J. W. Hsueh
Initial and Cyclic Recruitment of Ovarian Follicles
Endocr. Rev., April 1, 2000; 21(2): 200 - 214.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
U.A. Vitt, M. Hayashi, C. Klein, and A.J.W. Hsueh
Growth Differentiation Factor-9 Stimulates Proliferation but Suppresses the Follicle-Stimulating Hormone-Induced Differentiation of Cultured Granulosa Cells from Small Antral and Preovulatory Rat Follicles
Biol Reprod, February 1, 2000; 62(2): 370 - 377.
[Abstract] [Full Text]

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 EndocrinologyHome page
C. P. Leo, S. Y. Hsu, S.-Y. Chun, H.-W. Bae, and A. J. W. Hsueh
Characterization of the Antiapoptotic Bcl-2 Family Member Myeloid Cell Leukemia-1 (Mcl-1) and the Stimulation of Its Message by Gonadotropins in the Rat Ovary
Endocrinology, December 1, 1999; 140(12): 5469 - 5477.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
H. Yada, K. Hosokawa, K. Tajima, Y. Hasegawa, and F. Kotsuji
Role of Ovarian Theca and Granulosa Cell Interaction in Hormone Productionand Cell Growth During the Bovine Follicular Maturation Process
Biol Reprod, December 1, 1999; 61(6): 1480 - 1486.
[Abstract] [Full Text]

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 EndocrinologyHome page
A. Ny, G. Leonardsson, A.-C. Hägglund, P. Hägglöf, V. A. Ploplis, P. Carmeliet, and T. Ny
Ovulation in Plasminogen-Deficient Mice
Endocrinology, November 1, 1999; 140(11): 5030 - 5035.
[Abstract] [Full Text]

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 EndocrinologyHome page
C. Ko, Y.-H. In, and O.-K. Park-Sarge
Role of Progesterone Receptor Activation in Pituitary Adenylate Cyclase Activating Polypeptide Gene Expression in Rat Ovary
Endocrinology, November 1, 1999; 140(11): 5185 - 5194.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
H. Kishi and G. S. Greenwald
In Vitro Steroidogenesis by Dissociated Rat Follicles, Primary to Antral, Before and After Injection of Equine Chorionic Gonadotropin
Biol Reprod, November 1, 1999; 61(5): 1177 - 1183.
[Abstract] [Full Text]

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 EndocrinologyHome page
T. Hirakawa, T. Minegishi, M. Tano, T. Kameda, H. Kishi, Y. Ibuki, T. Mizutani, and K. Miyamoto
Effect of Prolactin on the Expression of Luteinizing Hormone Receptors during Cell Differentiation in Cultured Rat Granulosa Cells
Endocrinology, August 1, 1999; 140(8): 3444 - 3451.
[Abstract] [Full Text]

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 EndocrinologyHome page
S. L. Fitzpatrick, J. M. Funkhouser, D. M. Sindoni, P. E. Stevis, D. C. Deecher, A. R. Bapat, I. Merchenthaler, and D. E. Frail
Expression of Estrogen Receptor-{beta} Protein in Rodent Ovary
Endocrinology, June 1, 1999; 140(6): 2581 - 2591.
[Abstract] [Full Text]

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 EndocrinologyHome page
S. Chen, H. Shi, X. Liu, and D. L. Segaloff
Multiple Elements and Protein Factors Coordinate the Basal and Cyclic Adenosine 3',5'-Monophosphate-Induced Transcription of the Lutropin Receptor Gene in Rat Granulosa Cells
Endocrinology, May 1, 1999; 140(5): 2100 - 2109.
[Abstract] [Full Text]

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 EndocrinologyHome page
M. Hayashi, E. A. McGee, G. Min, C. Klein, U. M. Rose, M. v. Duin, and A. J. W. Hsueh
Recombinant Growth Differentiation Factor-9 (GDF-9) Enhances Growth and Differentiation of Cultured Early Ovarian Follicles
Endocrinology, March 1, 1999; 140(3): 1236 - 1244.
[Abstract] [Full Text]

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 Mol Hum ReprodHome page
A. Misajon, P. Hutchinson, N. Lolatgis, A. O. Trounson, and G. Almahbobi
The mechanism of action of epidermal growth factor and transforming growth factor {alpha} on aromatase activity in granulosa cells from polycystic ovaries
Mol. Hum. Reprod., February 1, 1999; 5(2): 96 - 103.
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 Mol. Endocrinol.Home page
D. A. DeManno, J. E. Cottom, M. P. Kline, C. A. Peters, E. T. Maizels, and M. Hunzicker-Dunn
Follicle-Stimulating Hormone Promotes Histone H3 Phosphorylation on Serine-10
Mol. Endocrinol., January 1, 1999; 13(1): 91 - 105.
[Abstract] [Full Text]

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 Am. J. Physiol. Endocrinol. Metab.Home page
E. Kotani, M. Sugimoto, H. Kamata, N. Fujii, M. Saitoh, S. Usuki, T. Kubo, K. Song, M. Miyazaki, K. Murakami, et al.
Biological roles of angiotensin II via its type 2 receptor during rat follicle atresia
Am J Physiol Endocrinol Metab, January 1, 1999; 276(1): E25 - E33.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
T. W. Sandhoff, D. B. Hales, K. H. Hales, and M. P. McLean
Transcriptional Regulation of the Rat Steroidogenic Acute Regulatory Protein Gene by Steroidogenic Factor 1
Endocrinology, December 1, 1998; 139(12): 4820 - 4831.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
K. Hosokawa, A. Dantes, C. Schere-Levy, A. Barash, Y. Yoshida, F. Kotsuji, I. Vlodavsky, and A. Amsterdam
Induction of Ad4BP/SF-1, Steroidogenic Acute Regulatory Protein, and Cytochrome P450scc Enzyme System Expression in Newly Established Human Granulosa Cell Lines
Endocrinology, November 1, 1998; 139(11): 4679 - 4687.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
T. Ronen-Fuhrmann, R. Timberg, S. R. King, K. H. Hales, D. B. Hales, D. M. Stocco, and J. Orly
Spatio-Temporal Expression Patterns of Steroidogenic Acute Regulatory Protein (StAR) During Follicular Development in the Rat Ovary
Endocrinology, January 1, 1998; 139(1): 303 - 315.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
H. Yokota, K. Yamada, X. Liu, J. Kobayashi, Y. Abe, H. Mizunuma, and Y. Ibuki
Paradoxical Action of Activin A on Folliculogenesis in Immature and Adult Mice
Endocrinology, November 1, 1997; 138(11): 4572 - 4576.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
E. Y. Adashi, C. E. Resnick, D. W. Payne, R. G. Rosenfeld, T. Matsumoto, M. K. Hunter, S. E. Gargosky, J. Zhou, and C. A. Bondy
The Mouse Intraovarian Insulin-Like Growth Factor I System: Departures from the Rat Paradigm
Endocrinology, September 1, 1997; 138(9): 3881 - 3890.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
A. Amsterdam and N. Selvaraj
Control of Differentiation, Transformation, and Apoptosis in Granulosa Cells by Oncogenes, Oncoviruses, and Tumor Suppressor Genes
Endocr. Rev., August 1, 1997; 18(4): 435 - 461.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
A. Mayerhofer, G. A. Dissen, M. E. Costa, and S. R. Ojeda
A Role for Neurotransmitters in Early Follicular Development: Induction of Functional Follicle-Stimulating Hormone Receptors in Newly Formed Follicles of the Rat Ovary
Endocrinology, August 1, 1997; 138(8): 3320 - 3329.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
I. Schipper, F. F. G. Rommerts, P. M. ten Hacken, and B. C. J. M. Fauser
Low Levels of Follicle-Stimulating Hormone Receptor-Activation Inhibitors in Serum and Follicular Fluid from Normal Controls and Anovulatory Patients with or without Polycystic Ovary Syndrome
J. Clin. Endocrinol. Metab., May 1, 1997; 82(5): 1325 - 1331.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
B. C. J. M. Fauser and A. M. van Heusden
Manipulation of Human Ovarian Function: Physiological Concepts and Clinical Consequences
Endocr. Rev., February 1, 1997; 18(1): 71 - 106.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
M. Byers, G. G. J. M. Kuiper, J.-A. Gustafsson, and O.-K. Park-Sarge
Estrogen Receptor-{beta} mRNA Expression in Rat Ovary: Down-Regulation by Gonadotropins
Mol. Endocrinol., February 1, 1997; 11(2): 172 - 182.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
G. Hosseini, J. Liu, and A. I.d. Agostini
Characterization and Hormonal Modulation of Anticoagulant Heparan Sulfate Proteoglycans Synthesized by Rat Ovarian Granulosa Cells
J. Biol. Chem., September 6, 1996; 271(36): 22090 - 22099.
[Abstract] [Full Text] [PDF]

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 Reproductive SciencesHome page
A. Hurwitz, K. Ruutiainen-Altman, L. Marzella, L. Botero, M. Dushnik, and E. Y. Adashi
Follicular Atresia as an Apoptotic Process: Atresia-Associated Increase in the Ovarian Expression of the Putative Apoptotic Marker Sulfated Glycoprotein-2
Reproductive Sciences, July 1, 1996; 3(4): 199 - 208.
[Abstract] [PDF]

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 Toxicol Ind HealthHome page
W. G. Foster, J. F. Jarrell, E. V. Younglai, M. G. Wade, D. L. Arnold, and S. Jordan
An Overview of Some Reproductive Toxicology Studies Conducted At Health Canada
Toxicology and Industrial Health, May 1, 1996; 12(3-4): 447 - 459.
[PDF]

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 ANN INTERN MEDHome page
R. Barnes and R. L. Rosenfield
The Polycystic Ovary Syndrome: Pathogenesis and Treatment
Ann Intern Med, March 1, 1989; 110(5): 386 - 399.
[Abstract] [PDF]

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 ScienceHome page
T. Woodruff, J D'Agostino, N. Schwartz, and K. Mayo
Dynamic changes in inhibin messenger RNAs in rat ovarian follicles during the reproductive cycle
Science, March 11, 1988; 239(4845): 1296 - 1299.
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 J. Biol. Chem.Home page
S. Mukherjee, J. E. Casanova, and M. Hunzicker-Dunn
Desensitization of the Luteinizing Hormone/Choriogonadotropin Receptor in Ovarian Follicular Membranes Is Inhibited by Catalytically Inactive ARNO+
J. Biol. Chem., February 23, 2001; 276(9): 6524 - 6528.
[Abstract] [Full Text] [PDF]


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