Apoptosis in the ovary: molecular mechanisms.

Cell death was first described in rabbit ovaries (Graaffian follicles), the phenomenon being called 'chromatolysis' rather than apoptosis. In humans, the ovarian endowment of primordial follicles is established during fetal life. Apoptotic cell death depletes this endowment by at least two-thirds before birth, executed with the help of several players and pathways conserved from worms to humans. To date, apoptosis has been reported to be involved in oogenesis, folliculogenesis, oocyte loss/selection and atresia. Several pro-survival and pro-apoptotic molecules are involved in ovarian apoptosis with the delicate balance between them being the determinant for the final destiny of the follicular cells. This review critically analyses the current knowledge about the biological roles of these molecules and their relevance to the dynamics of follicle development. It also presents the existing literature and assesses the gaps in our knowledge.

[1]  R. Wieser The transforming growth factor-beta signaling pathway in tumorigenesis. , 2001, Current opinion in oncology.

[2]  J C Reed,et al.  IAP family proteins--suppressors of apoptosis. , 1999, Genes & development.

[3]  [Transforming growth factor-beta signaling and cancer]. , 2000, Human cell.

[4]  Martin M Matzuk,et al.  NOBOX Deficiency Disrupts Early Folliculogenesis and Oocyte-Specific Gene Expression , 2004, Science.

[5]  D. Orlicky,et al.  Immunohistochemical localization of PGF2α receptor in the rat ovary , 1992 .

[6]  A. Johnson,et al.  Expression of members of the bcl-2 gene family in the immature rat ovary: equine chorionic gonadotropin-mediated inhibition of granulosa cell apoptosis is associated with decreased bax and constitutive bcl-2 and bcl-xlong messenger ribonucleic acid levels. , 1995, Endocrinology.

[7]  C. Thompson,et al.  4-1BB and Ox40 Are Members of a Tumor Necrosis Factor (TNF)-Nerve Growth Factor Receptor Subfamily That Bind TNF Receptor-Associated Factors and Activate Nuclear Factor κB , 1998, Molecular and Cellular Biology.

[8]  J. Tilly,et al.  The aryl hydrocarbon receptor, a basic helix-loop-helix transcription factor of the PAS gene family, is required for normal ovarian germ cell dynamics in the mouse. , 2000, Endocrinology.

[9]  Y. Taketani,et al.  Fas/APO-1/CD95 system as a mediator of granulosa cell apoptosis in ovarian follicle atresia. , 1996, Endocrinology.

[10]  N. Inoue,et al.  Roles of tumor necrosis factor-related apoptosis-inducing ligand signaling pathway in granulosa cell apoptosis during atresia in pig ovaries. , 2003, The Journal of reproduction and development.

[11]  J. Eberle,et al.  Resistance to CD95/Fas‐induced and ceramide‐mediated apoptosis of human melanoma cells is caused by a defective mitochondrial cytochrome c release , 2000, FEBS letters.

[12]  B. Christopher,et al.  Immunolocalization of transforming growth factor-beta1 during follicular development and atresia in the mouse ovary. , 2000, Endocrine journal.

[13]  M. Marone,et al.  bcl-2, bax, bcl-XL, and bcl-XS expression in normal and neoplastic ovarian tissues. , 1998, Clinical cancer research : an official journal of the American Association for Cancer Research.

[14]  S. Porter Current status of clinical trials with anti-TNF. , 1997, Chest.

[15]  J. M. Kim,et al.  Expression of inhibitor of apoptosis proteins (IAPs) in rat granulosa cells during ovarian follicular development and atresia. , 1998, Endocrinology.

[16]  M. De Felici Regulation of primordial germ cell development in the mouse. , 2000, The International journal of developmental biology.

[17]  John Calvin Reed,et al.  Cloning and sequencing of a cDNA encoding the rat Bcl-2 protein. , 1994, Gene.

[18]  C. Young,et al.  Tumor-promoting phorbol ester-induced cell death and gene expression in a human prostate adenocarcinoma cell line. , 1994, Oncology research.

[19]  K. Mayo,et al.  Characterization of prohibitin in a newly established rat ovarian granulosa cell line. , 2001, Endocrinology.

[20]  T. Mori,et al.  Integrin alpha 6 is a differentiation antigen of human granulosa cells. , 1995, The Journal of clinical endocrinology and metabolism.

[21]  P. Leung,et al.  Multi-factorial role of GnRH-I and GnRH-II in the human ovary , 2003, Molecular and Cellular Endocrinology.

[22]  A. Hsueh,et al.  Bok is a pro-apoptotic Bcl-2 protein with restricted expression in reproductive tissues and heterodimerizes with selective anti-apoptotic Bcl-2 family members. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[23]  G. Rune,et al.  Expression of integrins in marmoset (Callithrix jacchus) ovary during folliculogenesis. , 1996, Tissue & cell.

[24]  T. Vaskivuo,et al.  Survival of human ovarian follicles from fetal to adult life: apoptosis, apoptosis-related proteins, and transcription factor GATA-4. , 2001, The Journal of clinical endocrinology and metabolism.

[25]  C P Leo,et al.  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. , 1999, Endocrinology.

[26]  I. Zwain,et al.  cAMP-INDUCED APOPTOSIS IN GRANULOSA CELLS IS ASSOCIATED WITH UP-REGULATION OF P53 AND BAX AND DOWN-REGULATION OF CLUSTERIN , 2001, Endocrine research.

[27]  J. Bobe,et al.  Molecular cloning and expression of a TNF receptor and two TNF ligands in the fish ovary. , 2001, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[28]  H. Imura,et al.  Endothelins inhibit luteinization of cultured porcine granulosa cells. , 1991, Endocrinology.

[29]  N. Dhanasekaran,et al.  Apoptosis of ovarian granulosa cells: Correlation with the reduced activity of ERK‐signaling module , 1999, Journal of cellular biochemistry.

[30]  John Calvin Reed,et al.  Endogenous Inhibitors of Caspases , 1999, Journal of Clinical Immunology.

[31]  M. Pesce,et al.  Bcl-2 and Bax regulation of apoptosis in germ cells during prenatal oogenesis in the mouse embryo , 1999, Cell Death and Differentiation.

[32]  C. Jongeneel,et al.  Efficient adenoviral transfer of NF‐κB inhibitor sensitizes melanoma to tumor necrosis factor‐mediated apoptosis , 1999, International journal of cancer.

[33]  A. Roberts,et al.  Suppressor and oncogenic roles of transforming growth factor-beta and its signaling pathways in tumorigenesis. , 2001, Advances in cancer research.

[34]  S. Chun,et al.  Gonadal cell apoptosis. , 1996, Recent progress in hormone research.

[35]  N. Manabe,et al.  Abnormal structural luteolysis in ovaries of the senescence accelerated mouse (SAM): expression of Fas ligand/Fas-mediated apoptosis signaling molecules in luteal cells. , 2003, The Journal of reproduction and development.

[36]  N. Zachos,et al.  Up-Regulation of α-Inhibin Expression in the Fetal Ovary of Estrogen-Suppressed Baboons Is Associated with Impaired Fetal Ovarian Folliculogenesis1 , 2003, Biology of reproduction.

[37]  J. M. Kim,et al.  Involvement of the Fas/fas Ligand System in P53- Mediated Granulosa Cell Apoptosis during Follicular Development and Atresia* , 2022 .

[38]  N. Manabe,et al.  Soluble Fas (FasB) regulates luteal cell apoptosis during luteolysis in murine ovaries , 2003, Molecular reproduction and development.

[39]  A. Wyllie,et al.  Apoptosis: A Basic Biological Phenomenon with Wide-ranging Implications in Tissue Kinetics , 1972, British Journal of Cancer.

[40]  A. Johnson,et al.  Expression and Regulation of Fas Antigen and Tumor Necrosis Factor Receptor Type I in Hen Granulosa Cells1 , 2001, Biology of reproduction.

[41]  Tilly Jl The molecular basis of ovarian cell death during germ cell attrition, follicular atresia, and luteolysis. , 1996 .

[42]  J. Tilly Apoptosis and the ovary: a fashionable trend or food for thought? , 1997, Fertility and sterility.

[43]  P. Hersey,et al.  Immunologically-mediated tumour cell apoptosis: the role of TRAIL in T cell and cytokine-mediated responses to melanoma. , 2000, Forum.

[44]  P. Hoyer,et al.  Ultrastructural Evaluation of Oocytes During Atresia in Rat Ovarian Follicles1 , 2000, Biology of reproduction.

[45]  M. Skinner,et al.  Bone Morphogenetic Protein-4 Acts as an Ovarian Follicle Survival Factor and Promotes Primordial Follicle Development1 , 2003, Biology of reproduction.

[46]  D. Wallach,et al.  MAP3K-related kinase involved in NF-KB induction by TNF, CD95 and IL-1 , 1997, Nature.

[47]  B. Tsang,et al.  Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. , 1998, Biology of reproduction.

[48]  A. Hsueh,et al.  Expression and function of a proapoptotic Bcl-2 family member Bcl-XL/Bcl-2-associated death promoter (BAD) in rat ovary. , 1997, Endocrinology.

[49]  N. Williams,et al.  Immunohistochemical Analysis of the Proapoptotic Protein Par-4 in Normal Rat Tissues1 Strange, And , 1997 .

[50]  F. Gaytán,et al.  Selective Apoptosis of Luteal Endothelial Cells in Dexamethasone-Treated Rats Leads to Ischemic Necrosis of Luteal Tissue1 , 2002, Biology of reproduction.

[51]  B. Fisch,et al.  Preliminary studies on apoptosis in human fetal ovaries. , 2002, Fertility and sterility.

[52]  M. Nishihara,et al.  Fas/Fas ligand system in prolactin-induced apoptosis in rat corpus luteum: possible role of luteal immune cells. , 1999, Biochemical and biophysical research communications.

[53]  M. Laiho,et al.  Human melanoma cell line UV responses show independency of p53 function. , 1999, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[54]  B. Berisha,et al.  Real‐time changes of the local vasoactive peptide systems (angiotensin, endothelin) in the bovine corpus luteum after induced luteal regression , 2003, Molecular reproduction and development.

[55]  S. Shimasaki,et al.  Reproductive Biology and Endocrinology Open Access the Spatiotemporal Expression Pattern of the Bone Morphogenetic Protein Family in Rat Ovary Cell Types during the Estrous Cycle , 2022 .

[56]  J. Flaws,et al.  Interleukin-1 beta-converting enzyme-related proteases (IRPs) and mammalian cell death: dissociation of IRP-induced oligonucleosomal endonuclease activity from morphological apoptosis in granulosa cells of the ovarian follicle. , 1995, Endocrinology.

[57]  J. E. Fortune,et al.  The primordial to primary follicle transition , 2000, Molecular and Cellular Endocrinology.

[58]  F. Kotsuji,et al.  Steroid Regulation during Apoptosis of Ovarian Follicular Cells , 1998, Steroids.

[59]  S. Chun,et al.  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 Ovary1. , 1999, Endocrinology.

[60]  F. Hughes,et al.  Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. , 1991, Endocrinology.

[61]  Nicole C Johnson,et al.  BRCA1 185delAG mutation inhibits Akt-dependent, IAP-mediated caspase 3 inactivation in human ovarian surface epithelial cells. , 2004, Experimental cell research.

[62]  John Calvin Reed,et al.  Analysis of apoptosis and expression of bcl-2 gene family members in the human and baboon ovary , 1998, Cell Death and Differentiation.

[63]  H. Yoon,et al.  Participation of Bir1p, a member of the inhibitor of apoptosis family, in yeast chromosome segregation events. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[64]  R. Cortvrindt,et al.  Roles of KIT and KIT LIGAND in ovarian function. , 2000, Reviews of reproduction.

[65]  S. Amae,et al.  The functional roles of porcine CD80 molecule and its ability to stimulate and regulate human anti-pig cellular response1 , 2003, Transplantation.

[66]  A. Amsterdam,et al.  Cross-talk between cAMP and p53-generated signals in induction of differentiation and apoptosis in steroidogenic granulosa cells , 1996, Steroids.

[67]  K. Doi,et al.  Possible involvement of DNA methylation in 5-azacytidine-induced neuronal cell apoptosis. , 1999, Histology and histopathology.

[68]  S. Ojeda,et al.  TrkB receptors are required for follicular growth and oocyte survival in the mammalian ovary. , 2004, Developmental biology.

[69]  S. Shimasaki,et al.  Analysis of spatial and temporal expression patterns of bone morphogenetic protein family members in the rat uterus over the estrous cycle. , 2004, The Journal of endocrinology.

[70]  A. Pardee,et al.  Release of Mitochondrial Cytochrome C in Both Apoptosis and Necrosis Induced by β-Lapachone in Human Carcinoma Cells , 1999, Molecular medicine.

[71]  S. Korsmeyer,et al.  Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency , 1999, Nature Genetics.

[72]  J. Cidlowski,et al.  Identification of Potassium-Dependent and -Independent Components of the Apoptotic Machinery in Mouse Ovarian Germ Cells and Granulosa Cells1 , 2000, Biology of reproduction.

[73]  A. Hsueh,et al.  Initial and cyclic recruitment of ovarian follicles. , 2000, Endocrine reviews.

[74]  G. Rune,et al.  Proliferation and apoptosis in follicles of the marmoset monkey (Callithrix jacchus) ovary. , 1997, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[75]  R. Harman,et al.  Apoptosis of Bovine Granulosa Cells After Serum Withdrawal Is Mediated by Fas Antigen (CD95) and Fas Ligand1 , 2001, Biology of reproduction.

[76]  H. Fraser,et al.  Ubiquitin and apoptosis in the corpus luteum of the marmoset monkey (Callithrix jacchus). , 1998, Journal of reproduction and fertility.

[77]  D. Wilson,et al.  Transcription factors GATA-4 and GATA-6 and a GATA family cofactor, FOG-2, are expressed in human ovary and sex cord-derived ovarian tumors. , 2000, The Journal of clinical endocrinology and metabolism.

[78]  D. Wilson,et al.  Expression and hormonal regulation of transcription factors GATA-4 and GATA-6 in the mouse ovary. , 1997, Endocrinology.

[79]  Gong Yang,et al.  Activation of Antioxidant Pathways in Ras-Mediated Oncogenic Transformation of Human Surface Ovarian Epithelial Cells Revealed by Functional Proteomics and Mass Spectrometry , 2004, Cancer Research.

[80]  P. Hersey,et al.  The Role of NF-κB in TNF-Related Apoptosis-Inducing Ligand (TRAIL)-Induced Apoptosis of Melanoma Cells1 , 2001, The Journal of Immunology.

[81]  J. Ikeda,et al.  Neuronal apoptosis inhibitory protein (NAIP) may enhance the survival of granulosa cells thus indirectly affecting oocyte survival , 1999, Molecular reproduction and development.

[82]  M. Betenbaugh,et al.  Inhibiting apoptosis in mammalian cell culture using the caspase inhibitor XIAP and deletion mutants. , 2002, Biotechnology and bioengineering.

[83]  R. Viger,et al.  Transcription factor GATA-4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the Müllerian inhibiting substance promoter. , 1998, Development.

[84]  R. Berkowitz,et al.  Bcl-2 and p53 protein expression, apoptosis, and p53 mutation in human epithelial ovarian cancers. , 2000, The American journal of pathology.

[85]  B. Tsang,et al.  Nuclear factor-kappaB-mediated X-linked inhibitor of apoptosis protein expression prevents rat granulosa cells from tumor necrosis factor alpha-induced apoptosis. , 2001, Endocrinology.

[86]  Jiarui Wu,et al.  c-Myc degradation induced by DNA damage results in apoptosis of CHO cells , 2003, Oncogene.

[87]  E. Shaulian,et al.  Modulation of Mdm2 expression and p53-induced apoptosis in immortalized human ovarian granulosa cells. , 1998, Endocrinology.

[88]  L. Zon,et al.  Activation of the SAPK pathway by the human STE20 homologue germinal centre kinase , 1995, Nature.

[89]  C. Hack,et al.  The Granzyme B Inhibitor, Protease Inhibitor 9, Is Mainly Expressed by Dendritic Cells and at Immune-Privileged Sites1 , 2001, The Journal of Immunology.

[90]  C. Deng,et al.  Smad 3 May Regulate Follicular Growth in the Mouse Ovary1 , 2002, Biology of reproduction.

[91]  R. Dubose,et al.  Cloning and Characterization of TRAIL-R3, a Novel Member of the Emerging TRAIL Receptor Family , 1997, The Journal of experimental medicine.

[92]  T. Woodruff,et al.  Follicle-Restricted Compartmentalization of Transforming Growth Factor β Superfamily Ligands in the Feline Ovary1 , 2004, Biology of reproduction.

[93]  M. Matzuk,et al.  Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. , 1999, Molecular endocrinology.

[94]  B. Tsang,et al.  Nuclear Factor-k B-Mediated X-Linked Inhibitor of Apoptosis Protein Expression Prevents Rat Granulosa Cells from Tumor Necrosis Factor a-Induced Apoptosis , 2000 .

[95]  A. Johnson,et al.  Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. , 1991, Endocrinology.

[96]  J. Tilly,et al.  The molecular basis of ovarian cell death during germ cell attrition, follicular atresia, and luteolysis. , 1996, Frontiers in bioscience : a journal and virtual library.

[97]  B. Sonntag,et al.  The Ovarian Life Cycle: A Contemporary View , 2004, Reviews in Endocrine and Metabolic Disorders.

[98]  D. Busso,et al.  Morphologic and functional determinants of primordial and primary follicles in the monkey ovary , 2000, Molecular and Cellular Endocrinology.

[99]  T. Vaskivuo,et al.  Apoptosis in the human ovary. , 2003, Reproductive biomedicine online.

[100]  I. Herr,et al.  The CD95 (APO-1/Fas) system mediates drug-induced apoptosis in neuroblastoma cells. , 1997, Cancer research.

[101]  D. Monniaux Apoptose ovocytaire et volution de la rserve ovarienne , 2002 .

[102]  N. Dhanasekaran,et al.  Apoptosis of granulosa cells: a review on the role of MAPK-signalling modules. , 2003, Reproduction in domestic animals = Zuchthygiene.

[103]  J. Bridgham,et al.  Caspase-mediated apoptosis in the vertebrate ovary. , 2002, Reproduction.

[104]  A. Forabosco,et al.  Apoptosis in different stages of human oogenesis. , 1998, Anticancer research.

[105]  F. Harrisson,et al.  Distribution of apoptosis-related proteins in the quail ovary during folliculogenesis: BCL-2, BAX and CPP32. , 1999, Acta histochemica.

[106]  A. Gougeon Regulation of ovarian follicular development in primates: facts and hypotheses. , 1996, Endocrine reviews.

[107]  Y. Dor,et al.  Alternative pathways of ovarian apoptosis: death for life. , 2003, Biochemical pharmacology.

[108]  S. Isom,et al.  Regulation of Prohibitin Expression During Follicular Development and Atresia in the Mammalian Ovary1 , 2004, Biology of reproduction.

[109]  E. Borden,et al.  Preferential Induction of Apoptosis by Interferon (IFN)-β Compared with IFN-α2 , 2001 .

[110]  C. Smith,et al.  The novel receptor TRAIL-R4 induces NF-kappaB and protects against TRAIL-mediated apoptosis, yet retains an incomplete death domain. , 1997, Immunity.

[111]  Z. Ronai,et al.  Role of TRAF2/GCK in melanoma sensitivity to UV-induced apoptosis , 2000, Oncogene.

[112]  T. Nandedkar,et al.  Expression of bcl(xs) and c-myc in atretic follicles of mouse ovary. , 2001, Reproductive biomedicine online.

[113]  R. J. Lai,et al.  Targeted overexpression of Bcl-2 in ovaries of transgenic mice leads to decreased follicle apoptosis, enhanced folliculogenesis, and increased germ cell tumorigenesis. , 1996, Endocrinology.

[114]  M. Fenwick,et al.  Immunohistochemical localization of active caspase-3 in the mouse ovary: growth and atresia of small follicles. , 2002, Reproduction.

[115]  V. Dixit,et al.  Boo, a novel negative regulator of cell death, interacts with Apaf‐1 , 1999, The EMBO journal.

[116]  李晓燕,et al.  Detection of c-myc gene expression in nasopharyngeal carcinoma by nonradioactive in situ hybridization and immunohistochemistry , 1997 .

[117]  E. Rimon,et al.  Steroidogenesis and apoptosis in the mammalian ovary , 2003, Steroids.

[118]  X-linked inhibitor of apoptosis protein activates the phosphatidylinositol 3-kinase/Akt pathway in rat granulosa cells during follicular development. , 2001, Endocrinology.

[119]  J. Tilly Commuting the death sentence: how oocytes strive to survive , 2001, Nature Reviews Molecular Cell Biology.

[120]  J. Flaws,et al.  Smad 3 regulates proliferation of the mouse ovarian surface epithelium. , 2003, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[121]  A. Sandler,et al.  Survivin mRNA is down‐regulated during early Xenopus laevis embryogenesis , 2002, Developmental dynamics : an official publication of the American Association of Anatomists.

[122]  R. Wieser The transforming growth factor-β signaling pathway in tumorigenesis , 2001 .

[123]  G. Rune,et al.  Relationship between expression of integrins and granulosa cell apoptosis in ovarian follicles of the marmoset (Callithrix jacchus). , 1997, Tissue & cell.

[124]  J. McCRACKEN,et al.  Luteolysis: a neuroendocrine-mediated event. , 1999, Physiological reviews.

[125]  J. M. Boyd,et al.  Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. , 1995, Oncogene.

[126]  N. Sugino,et al.  Expression of Bcl-2 and Bax in the human corpus luteum during the menstrual cycle and in early pregnancy: regulation by human chorionic gonadotropin. , 2000, The Journal of clinical endocrinology and metabolism.

[127]  B. Tsang,et al.  Involvement of Transforming Growth Factor α in the Regulation of Rat Ovarian X-Linked Inhibitor of Apoptosis Protein Expression and Follicular Growth by Follicle-Stimulating Hormone1 , 2002, Biology of reproduction.

[128]  G. Wood,et al.  Apoptosis and melanoma: molecular mechanisms , 2003, The Journal of pathology.

[129]  C. Sorenson,et al.  Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. , 1995, Endocrinology.

[130]  V. Dixit,et al.  Apoptosis control by death and decoy receptors. , 1999, Current opinion in cell biology.

[131]  G. Wood,et al.  p53-related pathways and the molecular pathogenesis of melanoma , 2003, European journal of cancer prevention : the official journal of the European Cancer Prevention Organisation.

[132]  K. Imakawa,et al.  Prostaglandin F2alpha-induced functional regression of the corpus luteum and apoptosis in rodents. , 2003, Journal of pharmacological sciences.

[133]  P. Navarra,et al.  Endothelins enhance prostaglandin (PGE(2) and PGF(2alpha)) biosynthesis and release by human luteal cells: evidence of a new paracrine/autocrine regulation of luteal function. , 2001, The Journal of clinical endocrinology and metabolism.

[134]  A. Wyllie,et al.  Apoptosis (the 1992 Frank Rose Memorial Lecture). , 1993, British Journal of Cancer.

[135]  J. A. Whittaker,et al.  Immunolocalization and expression of prohibitin, a mitochondrial associated protein within the rat ovaries , 1999, The Anatomical record.

[136]  Changning Yan,et al.  Nobox is a homeobox-encoding gene preferentially expressed in primordial and growing oocytes , 2002, Mechanisms of Development.

[137]  J. Tilly,et al.  Oocyte apoptosis: like sand through an hourglass. , 1999, Developmental biology.

[138]  J. Tilly,et al.  Localization, Regulation and Possible Consequences of Apoptotic Protease-Activating Factor-1 (Apaf-1) Expression in Granulosa Cells of the Mouse Ovary. , 1999, Endocrinology.

[139]  S. Levison,et al.  Expression of mouse ovarian insulin growth factor system components during follicular development and atresia. , 1998, Endocrinology.

[140]  A. Hsueh,et al.  BOD (Bcl-2-related ovarian death gene) is an ovarian BH3 domain-containing proapoptotic Bcl-2 protein capable of dimerization with diverse antiapoptotic Bcl-2 members. , 1998, Molecular endocrinology.

[141]  J. Tilly,et al.  Apoptosis in atretic ovarian follicles is associated with selective decreases in messenger ribonucleic acid transcripts for gonadotropin receptors and cytochrome P450 aromatase. , 1992, Endocrinology.

[142]  J. Bridgham,et al.  Avian TVB (DR5-like) death receptor expression in hen ovarian follicles. , 2002, Biochemical and biophysical research communications.