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Endocrine Reviews, doi:10.1210/edrv-15-6-707
Endocrine Reviews 15 (6): 707-724
Copyright © 1994 by The Endocrine Society
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Ovarian Follicle Atresia: A Hormonally Controlled Apoptotic Process*

AARON J. W. HSUEH, HÅKAN BILLIG and ALEX TSAFRIRI

Division of Reproductive Biology, Department of Gynecology/Obstetrics, Stanford University School of Medicine Stanford, California 94305-5317

Correspondence: Address requests for reprints to: Aaron J. W. Hsueh, Ph.D., Division of Reproductive Biology, Department of Gynecology and Obstetrics, Stanford University Medical Center, 300 Pasteur Drive, Stanford, California 94305-5317.

Abstract

GREATER THAN 99% of ovarian follicles undergo a degenerative process called atresia during reproductive life. Extending earlier morphological analysis, recent studies have demonstrated that apoptotic cell death is the molecular mechanism underlying follicle atresia. The use of DNA 3'-end-labeling methods allows quantitation and identification of internucleosomal degradation of DNA after gel fractionation as well as in situ analysis of specific cell types undergoing DNA fragmentation in histological sections. Using rats as the experimental model, gonadotropins, epidermal growth factor (EGF)/transforming growth factor-{alpha} (TGF{alpha}), basic fibroblast growth factor (bFGF), insulin-like growth factor-I (IGF-I), and estrogens have been identified as follicle survival factors capable of suppressing apoptotic DNA fragmentation, whereas androgens, interleukin-6 (IL-6), and GnRH are potential atretogenic factors. This review summarizes the historical background of studies on follicle atresia and selection as well as recent advances in the intraovarian hormonal mechanisms that control follicle apoptosis. It is suggested that during the penultimate stage of follicle development, exposure to a survival factor (probably FSH) is responsible for follicle selection.

Footnotes

* This work was supported by NIH Grant HD-31566.




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J.J. Peluso, G. Fernandez, A. Pappalardo, and B.A. White
Characterization of a Putative Membrane Receptor for Progesterone in Rat Granulosa Cells
Biol Reprod, July 1, 2001; 65(1): 94 - 101.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
S.-Y. Chun, H.-W. Bae, W.-J. Kim, J.-H. Park, S. Y. Hsu, and A. J. W. Hsueh
Expression of Messenger Ribonucleic Acid for the Antiapoptosis Gene P11 in the Rat Ovary: Gonadotropin Stimulation in Granulosa Cells of Preovulatory Follicles
Endocrinology, June 1, 2001; 142(6): 2311 - 2317.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
J.J. Peluso, A. Pappalardo, and G. Fernandez
E-Cadherin-Mediated Cell Contact Prevents Apoptosis of Spontaneously Immortalized Granulosa Cells by Regulating Akt Kinase Activity
Biol Reprod, April 1, 2001; 64(4): 1183 - 1190.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
A.-C. Hägglund, P. Basset, and T. Ny
Stromelysin-3 Is Induced in Mouse Ovarian Follicles Undergoing Hormonally Controlled Apoptosis, but This Metalloproteinase Is Not Required for Follicular Atresia
Biol Reprod, February 1, 2001; 64(2): 457 - 463.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
A. W. Wood and G. J. Van Der Kraak
Apoptosis and Ovarian Function: Novel Perspectives from the Teleosts
Biol Reprod, January 1, 2001; 64(1): 264 - 271.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
K. M. Vaknin, S. Lazar, M. Popliker, and A. Tsafriri
Role of Meiosis-Activating Sterols in Rat Oocyte Maturation: Effects of Specific Inhibitors and Changes in the Expression of Lanosterol 14{{alpha}}-Demethylase During the Preovulatory Period
Biol Reprod, January 1, 2001; 64(1): 299 - 309.
[Abstract] [Full Text]

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 EndocrinologyHome page
K. Lynch, G. Fernandez, A. Pappalardo, and J. J. Peluso
Basic Fibroblast Growth Factor Inhibits Apoptosis of Spontaneously Immortalized Granulosa Cells by Regulating Intracellular Free Calcium Levels through a Protein Kinase C{delta}-Dependent Pathway
Endocrinology, November 1, 2000; 141(11): 4209 - 4217.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
P.J. Devine, C.M. Payne, M.K. McCuskey, and P.B. Hoyer
Ultrastructural Evaluation of Oocytes During Atresia in Rat Ovarian Follicles
Biol Reprod, November 1, 2000; 63(5): 1245 - 1252.
[Abstract] [Full Text]

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 EndocrinologyHome page
U. A. Vitt, E. A. McGee, M. Hayashi, and A. J. W. Hsueh
In Vivo Treatment with GDF-9 Stimulates Primordial and Primary Follicle Progression and Theca Cell Marker CYP17 in Ovaries of Immature Rats
Endocrinology, October 1, 2000; 141(10): 3814 - 3820.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
N. A. Cataldo, D. A. Dumesic, P. C. Goldsmith, and R. B. Jaffe
Immunolocalization of Fas and Fas ligand in the ovaries of women with polycystic ovary syndrome: relationship to apoptosis
Hum. Reprod., September 1, 2000; 15(9): 1889 - 1897.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
H. Matsumi, T. Yano, Y. Osuga, K. Kugu, X. Tang, J. P. Xu, N. Yano, Y. Kurashima, T. Ogura, O. Tsutsumi, et al.
Regulation of Nitric Oxide Synthase to Promote Cytostasis in Ovarian Follicular Development
Biol Reprod, July 1, 2000; 63(1): 141 - 146.
[Abstract] [Full Text]

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 J. Histochem. Cytochem.Home page
R. M. Zucker, A. P. Keshaviah, O. T. Price, and J. M. Goldman
Confocal Laser Scanning Microscopy of Rat Follicle Development
J. Histochem. Cytochem., June 1, 2000; 48(6): 781 - 792.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
M. Y. Yang and R. Rajamahendran
Morphological and Biochemical Identification of Apoptosis in Small, Medium, and Large Bovine Follicles and the Effects of Follicle-Stimulating Hormone and Insulin-Like Growth Factor-I on Spontaneous Apoptosis in Cultured Bovine Granulosa Cells
Biol Reprod, May 1, 2000; 62(5): 1209 - 1217.
[Abstract] [Full Text]

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 Endocr. Rev.Home page
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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 DevelopmentHome page
S Allard, P Adin, L Gouedard, N di Clemente, N Josso, M. Orgebin-Crist, J. Picard, and F Xavier
Molecular mechanisms of hormone-mediated Mullerian duct regression: involvement of beta-catenin
Development, January 8, 2000; 127(15): 3349 - 3360.
[Abstract] [PDF]

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 Biol. Reprod.Home page
N. A. Danilovich, A. Bartke, and T. A. Winters
Ovarian Follicle Apoptosis in Bovine Growth Hormone Transgenic Mice
Biol Reprod, January 1, 2000; 62(1): 103 - 107.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
D. L. Russell and J. S. Richards
Differentiation-Dependent Prolactin Responsiveness and Stat (Signal Transducers and Activators of Transcription) Signaling in Rat Ovarian Cells
Mol. Endocrinol., December 1, 1999; 13(12): 2049 - 2064.
[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.M. Fraser, S.F. Lunn, D.J. Harrison, and J.B. Kerr
Luteal Regression in the Primate: Different Forms of Cell Death During Naturaland Gonadotropin-Releasing Hormone Antagonist or Prostaglandin Analogue-Induced Luteolysis
Biol Reprod, December 1, 1999; 61(6): 1468 - 1479.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
J. L. Spearow, P. A. Nutson, W. S. Mailliard, M. Porter, and M. Barkley
Mapping Genes That Control Hormone-Induced Ovulation Rate in Mice
Biol Reprod, October 1, 1999; 61(4): 857 - 872.
[Abstract] [Full Text]

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 Endocr. Rev.Home page
L. Poretsky, N. A. Cataldo, Z. Rosenwaks, and L. C. Giudice
The Insulin-Related Ovarian Regulatory System in Health and Disease
Endocr. Rev., August 1, 1999; 20(4): 535 - 582.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
J. F. Couse and K. S. Korach
Estrogen Receptor Null Mice: What Have We Learned and Where Will They Lead Us?
Endocr. Rev., June 1, 1999; 20(3): 358 - 417.
[Abstract] [Full Text]

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 EndocrinologyHome page
P.-A. Svensson, M. S. C. Johnson, C. Ling, L. M. S. Carlsson, H. Billig, and B. Carlsson
Scavenger Receptor Class B Type I in the Rat Ovary: Possible Role in High Density Lipoprotein Cholesterol Uptake and in the Recognition of Apoptotic Granulosa Cells
Endocrinology, June 1, 1999; 140(6): 2494 - 2500.
[Abstract] [Full Text]

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 EndocrinologyHome page
R. J. Mann, R. A. Keri, and J. H. Nilson
Transgenic Mice with Chronically Elevated Luteinizing Hormone Are Infertile Due to Anovulation, Defects in Uterine Receptivity, and Midgestation Pregnancy Failure
Endocrinology, June 1, 1999; 140(6): 2592 - 2601.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
K. R. von Schalburg, C. M. Warby, and N. M. Sherwood
Evidence for Gonadotropin-Releasing Hormone Peptides in the Ovary and Testis of Rainbow Trout
Biol Reprod, June 1, 1999; 60(6): 1338 - 1344.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
N. Walther, A. Einspanier, and M. Jansen
Expression of Granulosa Cell-Specific Genes and Induction of Apoptosis in Conditionally Immortalized Granulosa Cell Lines Established from H-2Kb-tsA58 Transgenic Mice
Biol Reprod, May 1, 1999; 60(5): 1078 - 1086.
[Abstract] [Full Text]

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 Physiol. Rev.Home page
J. A. McCracken, E. E. Custer, and J. C. Lamsa
Luteolysis: A Neuroendocrine-Mediated Event
Physiol Rev, April 1, 1999; 79(2): 263 - 323.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
P. Melamed, G. Gur, H. Rosenfeld, A. Elizur, and Z. Yaron
Possible Interactions between Gonadotrophs and Somatotrophs in the Pituitary of Tilapia: Apparent Roles for Insulin-Like Growth Factor I and Estradiol
Endocrinology, March 1, 1999; 140(3): 1183 - 1191.
[Abstract] [Full Text]

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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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 J. Biol. Chem.Home page
M. G. Mahon, K. A. Lindstedt, M. Hermann, J. Nimpf, and W. J. Schneider
Multiple Involvement of Clusterin in Chicken Ovarian Follicle Development. BINDING TO TWO OOCYTE-SPECIFIC MEMBERS OF THE LOW DENSITY LIPOPROTEIN RECEPTOR GENE FAMILY
J. Biol. Chem., February 12, 1999; 274(7): 4036 - 4044.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. Lee, H.-J. Park, H.-S. Choi, H.-B. Kwon, A. Arimura, B.-J. Lee, W.-S. Choi, and S.-Y. Chun
Gonadotropin Stimulation of Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) Messenger Ribonucleic Acid in the Rat Ovary and the Role of PACAP as a Follicle Survival Factor
Endocrinology, February 1, 1999; 140(2): 818 - 826.
[Abstract] [Full Text]

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 EndocrinologyHome page
M. Sar and F. Welsch
Differential Expression of Estrogen Receptor-{beta} and Estrogen Receptor-{alpha} in the Rat Ovary
Endocrinology, February 1, 1999; 140(2): 963 - 971.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
J.J. Peluso and A. Pappalardo
Progesterone Maintains Large Rat Granulosa Cell Viability Indirectly by Stimulating Small Granulosa Cells to Synthesize Basic Fibroblast Growth Factor
Biol Reprod, February 1, 1999; 60(2): 290 - 296.
[Abstract] [Full Text] [PDF]

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H. Mizunuma, X. Liu, K. Andoh, Y. Abe, J. Kobayashi, K. Yamada, H. Yokota, Y. Ibuki, and Y. Hasegawa
Activin from Secondary Follicles Causes Small Preantral Follicles to Remain Dormant at the Resting Stage
Endocrinology, January 1, 1999; 140(1): 37 - 42.
[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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K. Hosokawa, D. Aharoni, A. Dantes, E. Shaulian, C. Schere-Levy, R. Atzmon, F. Kotsuji, M. Oren, I. Vlodavsky, and A. Amsterdam
Modulation of Mdm2 Expression and p53-Induced Apoptosis in Immortalized Human Ovarian Granulosa Cells
Endocrinology, November 1, 1998; 139(11): 4688 - 4700.
[Abstract] [Full Text] [PDF]


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