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WT1 influences apoptosis and proliferation of immature mice granular cells through regulation of the wnt/β-catenin signal pathway
Corresponding Author(s) : Caiping Mao
Cellular and Molecular Biology,
Vol. 65 No. 7: Issue 7
Abstract
Keywords
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- Hughes FM, Gorospe WC. Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 1991; 129: 2415-22.
- Rajakoski E. The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical, end left-right variations. Acta Endocrinol Suppl (Copenh) 1960; 34: 1-68.
- Liu ZH, Yue KZ, Ma SF, Sun XS, Tan JH. Effects of pregnant mare serum gonadotropin (eCG) on follicle development and granulosa-cell apoptosis in the pig. Theriogenology 2003; 59: 775-85.
- Murdoch WJ. Programmed cell death in preovulatory ovine follicles. Biol Reprod 1995; 53: 8-12.
- Jolly PD, Tisdall DJ, Heath DA, Lun S, McNatty KP. Apoptosis in bovine granulosa cells in relation to steroid synthesis, cyclic adenosine 3',5'-monophosphate response to follicle-stimulating hormone and luteinizing hormone, and follicular atresia. Biol Reprod 1994; 51: 934-944.
- Jiang JY, Cheung CK, Wang Y, Tsang BK. Regulation of cell death and cell survival gene expression during ovarian follicular development and atresia. Front Biosci 2003; 8: 222-237.
- Manabe N, Goto Y, Matsuda-Minehata F, Inoue N, Maeda A, Sakamaki K, et al. Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J Reprod Dev 2004; 50: 493-514.
- Matsuda-Minehata F, Inoue N, Goto Y, Manabe N. The regulation of ovarian granulosa cell death by pro- and anti-apoptotic molecules. J Reprod Dev 2006; 52: 695-705.
- Hastie ND. Wilms' tumour 1 (WT1) in development, homeostasis and disease. Development 2017; 144: 2862-2872.
- Scharnhorst V, van der Eb AJ, Jochemsen AG. WT1 proteins: functions in growth and differentiation. Gene 2001; 273: 141-161.
- Rivera MN, Haber DA. Wilms' tumour: connecting tumorigenesis and organ development in the kidney. Nat Rev Cancer 2005; 5: 699-712.
- Hashimoto H, Zhang X, Zheng Y, Wilson GG, Cheng X. Denys-Drash syndrome associated WT1 glutamine 369 mutants have altered sequence-preferences and altered responses to epigenetic modifications. Nucleic Acids Res 2016; 44: 10165-10176.
- Rao MK, Pham J, Imam JS, MacLean JA, Murali D, Furuta Y, et al. Tissue-specific RNAi reveals that WT1 expression in nurse cells controls germ cell survival and spermatogenesis. Genes Dev 2006; 20: 147-152.
- Gao F, Zhang J, Wang X, Yang J, Chen D, Huff V, et al. Wt1 functions in ovarian follicle development by regulating granulosa cell differentiation. Hum Mol Genet 2014; 23: 333-341.
- Wang H, Li G, Zhang J, Gao F, Li W, Qin Y, et al. Novel WT1 Missense Mutations in Han Chinese Women with Premature Ovarian Failure. Sci Rep 2015; 5: 13983.
- Kempisty B, ZióÅ‚kowska A, CiesióÅ‚ka S, Piotrowska H, Antosik P, Bukowska D, et al. Association between the expression of LHR, FSHR and CYP19 genes, cellular distribution of encoded proteins and proliferation of porcine granulosa cells in real-time. J Biol Regul Homeost Agents 2014; 28: 419-431.
- Sanchez AM, Giorgione V, Viganò P, Papaleo E, Candiani M, Mangili G, et al. Treatment with anticancer agents induces dysregulation of specific Wnt signaling pathways in human ovarian luteinized granulosa cells in vitro. Toxicol Sci 2013; 136: 183-192.
- Gupta PS, Folger JK, Rajput SK, Lv L, Yao J, Ireland JJ, et al. Regulation and regulatory role of WNT signaling in potentiating FSH action during bovine dominant follicle selection. PLoS One 2014; 9: 100201.
- Shao H, Ma J, Guo T, Hu R. Triptolide induces apoptosis of breast cancer cells via a mechanism associated with the Wnt/β-catenin signaling pathway. Exp Ther Med 2014; 8: 505-508.
- Kim MK, McGarry TJ, O BP, Flatow JM, Golden AA, Licht JD. An integrated genome screen identifies the Wnt signaling pathway as a major target of WT1. Proc Natl Acad Sci U S A 2009; 106: 11154-11159.
- Sanchez AM, Viganò P, Quattrone F, Pagliardini L, Papaleo E, Candiani M, et al. The WNT/β-catenin signaling pathway and expression of survival promoting genes in luteinized granulosa cells: endometriosis as a paradigm for a dysregulated apoptosis pathway. Fertil Steril 2014; 101: 1688-1696.
- Vainio S, Heikkilä M, Kispert A, Chin N, McMahon AP. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999; 397: 405-409.
- Niksic M, Slight J, Sanford JR, Caceres JF, Hastie ND. The Wilms' tumour protein (WT1) shuttles between nucleus and cytoplasm and is present in functional polysomes. Hum Mol Genet 2004; 13: 463-471.
- Markström E, ECh S, Shao R, Svanberg B, Billig H. Survival factors regulating ovarian apoptosis -- dependence on follicle differentiation. Reproduction 2002; 123: 23-30.
- Hirshfield AN. Development of follicles in the mammalian ovary. Int Rev Cytol 1991; 124: 43-101.
- McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000; 21: 200-214.
- Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 1997; 15: 201-204.
- Ma X, Dong Y, Matzuk MM, Kumar TR. Targeted disruption of luteinizing hormone beta-subunit leads to hypogonadism, defects in gonadal steroidogenesis, and infertility. Proc Natl Acad Sci U S A 2004; 101: 17294-17299.
- Simoni M, Gromoll J, Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr Rev 1997; 18: 739-773.
- Pelletier J, Schalling M, Buckler AJ, Rogers A, Haber DA, Housman D. Expression of the Wilms' tumor gene WT1 in the murine urogenital system. Genes Dev 1991; 5: 1345-1356.
- Sharma PM, Yang X, Bowman M, Roberts V, Sukumar S. Molecular cloning of rat Wilms' tumor complementary DNA and a study of messenger RNA expression in the urogenital system and the brain. Cancer Res 1992; 52: 6407-6412.
- Rauscher FJ. The WT1 Wilms tumor gene product: a developmentally regulated transcription factor in the kidney that functions as a tumor suppressor. FASEB J 1993; 7: 896-903.
- Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, et al. WT-1 is required for early kidney development. Cell 1993; 74: 679-691.
- Makrigiannakis A, Amin K, Coukos G, Tilly JL, Coutifaris C. Regulated expression and potential roles of p53 and Wilms' tumor suppressor gene (WT1) during follicular development in the human ovary. J Clin Endocrinol Metab 2000; 85: 449-459.
- Logan KA, McNatty KP, Juengel JL. Expression of wilms' tumor gene and protein localization during ovarian formation and follicular development in sheep. Biol Reprod 2003; 68: 635-643.
- Garner TP, Lopez A, Reyna DE, Spitz AZ, Gavathiotis E. Progress in targeting the BCL-2 family of proteins. Curr Opin Chem Biol 2017; 39: 133-142.
- Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74: 609-619.
- Perez GI, Robles R, Knudson CM, Flaws JA, Korsmeyer SJ, Tilly JL. Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency. Nat Genet 1999; 21: 200-203.
- Kugu K, Ratts VS, Piquette GN, Tilly KI, Tao XJ, Martimbeau S, et al. Analysis of apoptosis and expression of bcl-2 gene family members in the human and baboon ovary. Cell Death Differ 1998; 5: 67-76.
- Ratts VS, Flaws JA, Kolp R, Sorenson CM, Tilly JL. Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 1995; 136: 3665-3668.
- Hsu SY, Lai RJ, Finegold M, Hsueh AJ. Targeted overexpression of Bcl-2 in ovaries of transgenic mice leads to decreased follicle apoptosis, enhanced folliculogenesis, and increased germ cell tumorigenesis. Endocrinology 1996; 137: 4837-4843.
- Morita Y, Tilly JL. Oocyte apoptosis: like sand through an hourglass. Dev Biol 1999; 213: 1-17.
- Park M, Choi Y, Choi H, Roh J. Wilms' tumor suppressor gene (WT1) suppresses apoptosis by transcriptionally downregulating BAX expression in immature rat granulosa cells. J Ovarian Res 2014; 7: 118.
- Boyer A, Lapointe E, Zheng X, Cowan RG, Li H, Quirk SM, et al. WNT4 is required for normal ovarian follicle development and female fertility. FASEB J 2010; 24: 3010-3025.
- Prunskaite-Hyyryläinen R, Shan J, Railo A, Heinonen KM, Miinalainen I, Yan W, et al. Wnt4, a pleiotropic signal for controlling cell polarity, basement membrane integrity, and antimüllerian hormone expression during oocyte maturation in the female follicle. FASEB J 2014; 28: 1568-1581.
- Sim EU, Smith A, Szilagi E, Rae F, Ioannou P, Lindsay MH, et al. Wnt-4 regulation by the Wilms' tumour suppressor gene, WT1. Oncogene 2002; 21: 2948-2960.
- Ricken A, Lochhead P, Kontogiannea M, Farookhi R. Wnt signaling in the ovary: identification and compartmentalized expression of wnt-2, wnt-2b, and frizzled-4 mRNAs. Endocrinology 2002; 143: 2741-2749.
- Monkley SJ, Delaney SJ, Pennisi DJ, Christiansen JH, Wainwright BJ. Targeted disruption of the Wnt2 gene results in placentation defects. Development 1996; 122: 3343-3353.
- Wang HX, Li TY, Kidder GM. WNT2 regulates DNA synthesis in mouse granulosa cells through beta-catenin. Biol Reprod 2010; 82: 865-875.
- Harwood BN, Cross SK, Radford EE, Haac BE, De Vries WN. Members of the WNT signaling pathways are widely expressed in mouse ovaries, oocytes, and cleavage stage embryos. Dev Dyn 2008; 237: 1099-1111.
- Kenigsberg S, Bentov Y, Chalifa-Caspi V, Potashnik G, Ofir R, Birk OS. Gene expression microarray profiles of cumulus cells in lean and overweight-obese polycystic ovary syndrome patients. Mol Hum Reprod 2009; 15: 89-103.
- Abedini A, Zamberlam G, Lapointe E, Tourigny C, Boyer A, Paquet M, et al. WNT5a is required for normal ovarian follicle development and antagonizes gonadotropin responsiveness in granulosa cells by suppressing canonical WNT signaling. FASEB J 2016. 30: 1534-1547.
References
Hughes FM, Gorospe WC. Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 1991; 129: 2415-22.
Rajakoski E. The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical, end left-right variations. Acta Endocrinol Suppl (Copenh) 1960; 34: 1-68.
Liu ZH, Yue KZ, Ma SF, Sun XS, Tan JH. Effects of pregnant mare serum gonadotropin (eCG) on follicle development and granulosa-cell apoptosis in the pig. Theriogenology 2003; 59: 775-85.
Murdoch WJ. Programmed cell death in preovulatory ovine follicles. Biol Reprod 1995; 53: 8-12.
Jolly PD, Tisdall DJ, Heath DA, Lun S, McNatty KP. Apoptosis in bovine granulosa cells in relation to steroid synthesis, cyclic adenosine 3',5'-monophosphate response to follicle-stimulating hormone and luteinizing hormone, and follicular atresia. Biol Reprod 1994; 51: 934-944.
Jiang JY, Cheung CK, Wang Y, Tsang BK. Regulation of cell death and cell survival gene expression during ovarian follicular development and atresia. Front Biosci 2003; 8: 222-237.
Manabe N, Goto Y, Matsuda-Minehata F, Inoue N, Maeda A, Sakamaki K, et al. Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J Reprod Dev 2004; 50: 493-514.
Matsuda-Minehata F, Inoue N, Goto Y, Manabe N. The regulation of ovarian granulosa cell death by pro- and anti-apoptotic molecules. J Reprod Dev 2006; 52: 695-705.
Hastie ND. Wilms' tumour 1 (WT1) in development, homeostasis and disease. Development 2017; 144: 2862-2872.
Scharnhorst V, van der Eb AJ, Jochemsen AG. WT1 proteins: functions in growth and differentiation. Gene 2001; 273: 141-161.
Rivera MN, Haber DA. Wilms' tumour: connecting tumorigenesis and organ development in the kidney. Nat Rev Cancer 2005; 5: 699-712.
Hashimoto H, Zhang X, Zheng Y, Wilson GG, Cheng X. Denys-Drash syndrome associated WT1 glutamine 369 mutants have altered sequence-preferences and altered responses to epigenetic modifications. Nucleic Acids Res 2016; 44: 10165-10176.
Rao MK, Pham J, Imam JS, MacLean JA, Murali D, Furuta Y, et al. Tissue-specific RNAi reveals that WT1 expression in nurse cells controls germ cell survival and spermatogenesis. Genes Dev 2006; 20: 147-152.
Gao F, Zhang J, Wang X, Yang J, Chen D, Huff V, et al. Wt1 functions in ovarian follicle development by regulating granulosa cell differentiation. Hum Mol Genet 2014; 23: 333-341.
Wang H, Li G, Zhang J, Gao F, Li W, Qin Y, et al. Novel WT1 Missense Mutations in Han Chinese Women with Premature Ovarian Failure. Sci Rep 2015; 5: 13983.
Kempisty B, ZióÅ‚kowska A, CiesióÅ‚ka S, Piotrowska H, Antosik P, Bukowska D, et al. Association between the expression of LHR, FSHR and CYP19 genes, cellular distribution of encoded proteins and proliferation of porcine granulosa cells in real-time. J Biol Regul Homeost Agents 2014; 28: 419-431.
Sanchez AM, Giorgione V, Viganò P, Papaleo E, Candiani M, Mangili G, et al. Treatment with anticancer agents induces dysregulation of specific Wnt signaling pathways in human ovarian luteinized granulosa cells in vitro. Toxicol Sci 2013; 136: 183-192.
Gupta PS, Folger JK, Rajput SK, Lv L, Yao J, Ireland JJ, et al. Regulation and regulatory role of WNT signaling in potentiating FSH action during bovine dominant follicle selection. PLoS One 2014; 9: 100201.
Shao H, Ma J, Guo T, Hu R. Triptolide induces apoptosis of breast cancer cells via a mechanism associated with the Wnt/β-catenin signaling pathway. Exp Ther Med 2014; 8: 505-508.
Kim MK, McGarry TJ, O BP, Flatow JM, Golden AA, Licht JD. An integrated genome screen identifies the Wnt signaling pathway as a major target of WT1. Proc Natl Acad Sci U S A 2009; 106: 11154-11159.
Sanchez AM, Viganò P, Quattrone F, Pagliardini L, Papaleo E, Candiani M, et al. The WNT/β-catenin signaling pathway and expression of survival promoting genes in luteinized granulosa cells: endometriosis as a paradigm for a dysregulated apoptosis pathway. Fertil Steril 2014; 101: 1688-1696.
Vainio S, Heikkilä M, Kispert A, Chin N, McMahon AP. Female development in mammals is regulated by Wnt-4 signalling. Nature 1999; 397: 405-409.
Niksic M, Slight J, Sanford JR, Caceres JF, Hastie ND. The Wilms' tumour protein (WT1) shuttles between nucleus and cytoplasm and is present in functional polysomes. Hum Mol Genet 2004; 13: 463-471.
Markström E, ECh S, Shao R, Svanberg B, Billig H. Survival factors regulating ovarian apoptosis -- dependence on follicle differentiation. Reproduction 2002; 123: 23-30.
Hirshfield AN. Development of follicles in the mammalian ovary. Int Rev Cytol 1991; 124: 43-101.
McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000; 21: 200-214.
Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 1997; 15: 201-204.
Ma X, Dong Y, Matzuk MM, Kumar TR. Targeted disruption of luteinizing hormone beta-subunit leads to hypogonadism, defects in gonadal steroidogenesis, and infertility. Proc Natl Acad Sci U S A 2004; 101: 17294-17299.
Simoni M, Gromoll J, Nieschlag E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr Rev 1997; 18: 739-773.
Pelletier J, Schalling M, Buckler AJ, Rogers A, Haber DA, Housman D. Expression of the Wilms' tumor gene WT1 in the murine urogenital system. Genes Dev 1991; 5: 1345-1356.
Sharma PM, Yang X, Bowman M, Roberts V, Sukumar S. Molecular cloning of rat Wilms' tumor complementary DNA and a study of messenger RNA expression in the urogenital system and the brain. Cancer Res 1992; 52: 6407-6412.
Rauscher FJ. The WT1 Wilms tumor gene product: a developmentally regulated transcription factor in the kidney that functions as a tumor suppressor. FASEB J 1993; 7: 896-903.
Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, et al. WT-1 is required for early kidney development. Cell 1993; 74: 679-691.
Makrigiannakis A, Amin K, Coukos G, Tilly JL, Coutifaris C. Regulated expression and potential roles of p53 and Wilms' tumor suppressor gene (WT1) during follicular development in the human ovary. J Clin Endocrinol Metab 2000; 85: 449-459.
Logan KA, McNatty KP, Juengel JL. Expression of wilms' tumor gene and protein localization during ovarian formation and follicular development in sheep. Biol Reprod 2003; 68: 635-643.
Garner TP, Lopez A, Reyna DE, Spitz AZ, Gavathiotis E. Progress in targeting the BCL-2 family of proteins. Curr Opin Chem Biol 2017; 39: 133-142.
Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74: 609-619.
Perez GI, Robles R, Knudson CM, Flaws JA, Korsmeyer SJ, Tilly JL. Prolongation of ovarian lifespan into advanced chronological age by Bax-deficiency. Nat Genet 1999; 21: 200-203.
Kugu K, Ratts VS, Piquette GN, Tilly KI, Tao XJ, Martimbeau S, et al. Analysis of apoptosis and expression of bcl-2 gene family members in the human and baboon ovary. Cell Death Differ 1998; 5: 67-76.
Ratts VS, Flaws JA, Kolp R, Sorenson CM, Tilly JL. Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 1995; 136: 3665-3668.
Hsu SY, Lai RJ, Finegold M, Hsueh AJ. Targeted overexpression of Bcl-2 in ovaries of transgenic mice leads to decreased follicle apoptosis, enhanced folliculogenesis, and increased germ cell tumorigenesis. Endocrinology 1996; 137: 4837-4843.
Morita Y, Tilly JL. Oocyte apoptosis: like sand through an hourglass. Dev Biol 1999; 213: 1-17.
Park M, Choi Y, Choi H, Roh J. Wilms' tumor suppressor gene (WT1) suppresses apoptosis by transcriptionally downregulating BAX expression in immature rat granulosa cells. J Ovarian Res 2014; 7: 118.
Boyer A, Lapointe E, Zheng X, Cowan RG, Li H, Quirk SM, et al. WNT4 is required for normal ovarian follicle development and female fertility. FASEB J 2010; 24: 3010-3025.
Prunskaite-Hyyryläinen R, Shan J, Railo A, Heinonen KM, Miinalainen I, Yan W, et al. Wnt4, a pleiotropic signal for controlling cell polarity, basement membrane integrity, and antimüllerian hormone expression during oocyte maturation in the female follicle. FASEB J 2014; 28: 1568-1581.
Sim EU, Smith A, Szilagi E, Rae F, Ioannou P, Lindsay MH, et al. Wnt-4 regulation by the Wilms' tumour suppressor gene, WT1. Oncogene 2002; 21: 2948-2960.
Ricken A, Lochhead P, Kontogiannea M, Farookhi R. Wnt signaling in the ovary: identification and compartmentalized expression of wnt-2, wnt-2b, and frizzled-4 mRNAs. Endocrinology 2002; 143: 2741-2749.
Monkley SJ, Delaney SJ, Pennisi DJ, Christiansen JH, Wainwright BJ. Targeted disruption of the Wnt2 gene results in placentation defects. Development 1996; 122: 3343-3353.
Wang HX, Li TY, Kidder GM. WNT2 regulates DNA synthesis in mouse granulosa cells through beta-catenin. Biol Reprod 2010; 82: 865-875.
Harwood BN, Cross SK, Radford EE, Haac BE, De Vries WN. Members of the WNT signaling pathways are widely expressed in mouse ovaries, oocytes, and cleavage stage embryos. Dev Dyn 2008; 237: 1099-1111.
Kenigsberg S, Bentov Y, Chalifa-Caspi V, Potashnik G, Ofir R, Birk OS. Gene expression microarray profiles of cumulus cells in lean and overweight-obese polycystic ovary syndrome patients. Mol Hum Reprod 2009; 15: 89-103.
Abedini A, Zamberlam G, Lapointe E, Tourigny C, Boyer A, Paquet M, et al. WNT5a is required for normal ovarian follicle development and antagonizes gonadotropin responsiveness in granulosa cells by suppressing canonical WNT signaling. FASEB J 2016. 30: 1534-1547.