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2005, Number 1

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Vet Mex 2005; 36 (1)

Apoptosis and follicular atresia: an essential binomial for ovarian development

Flores-Pérez FI, Rosas-Velasco C, Romano PMC, Pérez-Martínez M

Language: English/Spanish
References: 150
Page: 87-103
PDF size: 1391.64 Kb.


ABSTRACT

This study presents current information concerning cellular death through apoptosis, a systematic and genetically programmed form of cell death. Furthermore, the importance of this process in ovarian follicular atresia in various species is discussed, considering it to be an essential reproductive cellular event upon which ovarian function largely depends.


REFERENCES

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  2. 2.Flores-Pérez F.I ¿Es la Muerte importante para la vida? Vet.Mex 2002; 33:161-171.

  3. 3.Hsu SY, Hsueh AJ. Intracellular mechanisms of ovarian cell apoptosis. Mol Cell Endocrinol 1998;145: 21-25.

  4. 4.Zachary J, Xue D. Functional genomic analysis of apoptotic DNA degradation in C. elegans. Mol Cell 2003;11:987-996.

  5. 5.Hacker G. The morphology of apoptosis. Cell Tissue Res 2000;301:5-17.

  6. 6.Coultas L, Pellegrin M,Visvader JE, Lindeman GJ,Chen L, Adams JM, et al. Bfk: a novel weakly proaptotic member of Bcl-2 protein family with a Bh3 and Bh2 region. Cell Death Diffr 2003; 10:185-192.

  7. 7.Johnson AL, Bridgham JT. Caspase-mediated apoptosis in the vertebrate ovary. Reproduction 2002;124:19-27.

  8. 8.Johnson AL. Intracellular mechanisms regulating cell survival in ovarian follicles. Anim Reprod Sci 2003;78:185-201.

  9. 9.Markstrom E, Svensson E Ch, Shao R, Svanderg B,Billig H. Survival factors regulating ovarian apoptosisdependence on follicle differentiation. Reproduction

  10. 2002 ;123:23-30.

  11. 10.Henson PM, Bratton DL,Fadok V. Apoptotic cell removal. Curr Biol 2001;11:795-805.

  12. 11.Hsueh AJ, Billing H, Tsafriri A. Ovarian follicule atresia: a hormonally controlled apoptotic process. Endocrinol. Rev 1994; 6:707-724.

  13. 12.Shiota M, Sugai N,Tamura M, Yamaguchi R, Fukushima N, Miyano T, et al. Correlation of mitogen-activated protein kinase activities with cells survival and apoptosis in porcine granulose cells. Zoolog Sci 2003;20:193-201.

  14. 13.Rosales-Torres AM, Avalos-Rodriguez A, Vergara-Onofre M,Hernandez-Perez O, Ballesteros LM, Garcia-Macedo R, et al. Multiparametric study of atresia in ewe antral follicles: histology, fl owcytometry,internucleosomal DNA fragmentation, and lysosmal

  15. enzyme activities in granulosa cells and follicular fl uid.Mol Reprod Dev 2000;55:270-281.

  16. 14.Maillet G, Bréard E, Benhaim A, Leymarie P, Féra L.Hormonal regulation of apoptosis in rabbit granulosa cells in vitro : evaluation by fl ow cytometric detection of

  17. plasma membrane phosphatidylserine externalization.Reproduction 2002;123:243-251.

  18. 15.Porter DA , Harman RM, Cowan RG, Quirk SM.Relationship of fas ligand expression and atresia during bovine follicle development. Reproduction 2001; 121:561-566.

  19. 16.Asdell SA. Patterns of mammalian reproduction 2nd ed. New York. Cornell: University Press, 1964.

  20. 17.Rosales TA, Atresia folicular. En : Velazques MJ editor.Biología de la reproducción. México D.F. Universidad Autónoma Metropolitana. 1998:223-261.

  21. 18.Sang-Young C, Hsueh JWA. Paracrine mechanisms of ovarian follicle apoptosis. J Reprod Immunol 1998;32:63-75.

  22. 19.Rosado A, Rosales AM, Maduración folicular en el mamífero. Ciencia 1991; 42:81-97.

  23. 20.Kaipia A , Hsueh AJ. Regulation of ovarian follicule atresia. Annu Rev Physiol 1997:59;349-363.

  24. 21.Reynaund K, Driancourt MA. Oocyte attrition. Mol Cell Endocrinol 2000:163;101-108.

  25. 22.Tilly J. Apoptosis and ovarian function. Rev Reprod 1996;1:162-172.

  26. 23.Mc Gee EA , Hsu S, Kaipia A, Hsueh AJ. Cell death and survival during ovarian follicle development. Mol Cell Endocrinol 1998;140:15-18.

  27. 24.Mikkelsen AL, Hopstand E, Lindenber G. Incidence of apoptosis in granulosa cells from immature human follicles. Reproduction 2001; 122:481-486.

  28. 25.Richards JS. Hormonal control of gene expression in the ovary. Endocrinol Rev 1994 ;6:725-751.

  29. 26.McGee EA, Chun SY, Lai S, He Y, Hsueh AJ.Keratinocyte growth factor promotes the survival,growth and diffentiation of prenatal ovarian follicles.Fertil Steroid 1999; 71:732-738.

  30. 27.Dunkel L, Tilly JL, Shikone T, Nishimori K, Hsueh AJ. Follicle-stimulating hormone receptor expression in the rat ovary: increases during prepubertal development and regulation by the opposing actions of transforming growth factors beta and alpha. Biol

  31. Reprod 1994;50:940-948.

  32. 28.Ranikki AS, Zang FP, Huhtaniemi IT. Ontogeny of follicle stimulating hormone receptor gene expression in the rat testis and ovary. Molec Cell Endocr 1995;107:199-208.

  33. 29.Billing h, Furuta I, Huseh AJ. Estrogens inhibit and androgens enhance ovarian granulose cell apoptosis.Endocrinology 1993;133:2204-2212.

  34. 30.Murray AA, Molinek MD, Baker SJ, Kojima FN, Smith MF, Hillier SG, et al. Role of ascorbic acid in promoting follicle integrity and survival in intact mouse ovarian

  35. follicles in vitro. Reproduction 2001;121:89-96.

  36. 31.Chun SY, Billing H, Tilly JL, Furuta I, Tsafriri A,Hsueh AJ. Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor. Endocrinology 1994;135:1845-1853.

  37. 32.Chun Sy, Hsueh AJW. Paracrinre Mechanisms of ovarian follicle apoptosis, J Reprod Immunol 1998;39:63-75.

  38. 33.Weeb R, Nicholas B, Gong JG, Campbell BK, Gutierrez CG, Garverik HA, et al. Mechanisms regulating follicular development and selection of the dominant

  39. follicle. Reproduction suppl 2003;61:71-79.

  40. 34.Tilly L,Billing H, Kowalski Kl , Hsueh AJ. Epidermal growth factor and basic fi broblast growth factor suppress the spontaneous onset of apoptosis in cultured rat ovarian granulose cells and follicles by atyrosine kinase-dependent mechanism. Mol

  41. Endocrinol 1992;6:1942-1950.

  42. 35.Svensson EC, Markstrom E, Andersson M, Billing H. Progesterone receptor-mediated inhibition of apoptosis in granulose cells insolated from rats treated with human chorionic gonadotropin. Biol Reprod 2000;63:1457-1464.

  43. 36.Markigiannakis A, Coukos G, Christofi dou-Solamidou M, Montas S, C. Progesterone is an autocrine/paracrine regulator of human granulose cell survival in vitro. Ann N Y Acad Sci 2000;900: 16-25.

  44. 37.Ronghao Li, Phillips MD, Morre A, Mather J. Folliclestimulating hormone induces terminal differentiation in apredifferentiated rat granulose cell line (ROG).

  45. Endcorinology 1997;138:2648-2657.

  46. 38.Asselin E, Xia CW, Wong FE, Tsang BK. Mammalian folicular development and atresia: role of apoptosis.Biol Signals Recept 2000;9: 874-895.

  47. 39.Zeuner A, Muller K,Reguszynski K, Jewgenow K.Apoptosis within bovine follicular cells and its effect on oocyte development during in vitro maturation.

  48. Theriogenology 2003;59,1421-1433.

  49. 40.FenwicK MA, Hurst P.R. Immunohistochmical localization of active caspase-3 in the mouse ovary: growth and atresia of small follicles. Reproduction

  50. 2002;124:659-665.

  51. 41.Hsueh AJW, McGee EA, Hayasi M,Hsu S.Y. Hormonal regulation of early follicle development in the rat ovary. Mol Cell Endocrinol. 2000;163:95-100.

  52. 42.Maillet G, BenhaÏm A,Mittre H, Féral C. Involvement of theca cells and steroids in the regulation of granulose cells apoptosis in rabbit preovulatory

  53. follicles. Reproduction 2003;125:709-716.

  54. 43.Bobes RJ, Perez-Martinez M, Gomez Y, Romano MC. Metabolism of progesterone to estrogens and androgens by individual follicles of the goat ovary.Small Rum Res 2003;47:233-242.

  55. 44.Yu Y, Li W, Han Z, Lou M, Chang Z, Tan J. The effect of follicle-stimulating hormone on follicular development, granulose cell apoptosis and steroidogenesis and its mediation by insulin-like growth factor-I in the goat ovary. Theriogenology

  56. 2003;60:1691-1704.

  57. 45.Pedersen HG,Watson ED, Telfer E. Analysis of atresia in equine follicles using histology, fresh granulosa cell morphology, and detection of DNA fragmentation.

  58. Reproduction 2003;125:417-423.

  59. 46.Iway T, Fujii S, Nabuy Y, Nonogak H, Konishi I, Mori T, et al. Effect of human chorionic gonadotropin on the expression of progesterone receptor and estrogen

  60. receptor in rabbit ovarian granulosa cells and the uterus. Endocrinology 1991;129:1840-1848.

  61. 47.Byers M, Kiuper GG, Gustafsson JA, Park -Sarge OK.Estrogen-receptor- b mRNA expression in rat ovary:down regulation by gonadotropins. Mol Endocrinol

  62. 1997;11:172-182.

  63. 48.Makrigianna A, Coukos G, Blaschuk O, Coutifaris C.Follicular atresia and luteolysis. Evidence of a role for N-cadherin. Ann N Y Acad Sci 2000;900:46-55.

  64. 49.Arowsmith CH. Structure and function in the p53 family. Cell Death Differ 1999;94:514-519.

  65. 50.Bendi A, Mookerje B. Biological significance and molecular mechanisms of p-53 inducedapoptosis.Apoptosis1988;3:224-237.

  66. 51.Burns Ft, El -Deiry WS. The p53 pathway and apoptosis.J Cell Phys 1999; 181:231-239

  100. Kaufmann HS. Apoptosis: pharmacological implications and therapeutic opportunities. San Diego: Academic Press, 1997.

  101. Flores-Pérez F.I ¿Es la Muerte importante para la vida? Vet.Mex 2002; 33:161-171.

  102. Hsu SY, Hsueh AJ. Intracellular mechanisms of ovarian cell apoptosis. Mol Cell Endocrinol 1998;145: 21-25.

  103. Zachary J, Xue D. Functional genomic analysis of apoptotic DNA degradation in C. elegans. Mol Cell 2003;11:987-996.

  104. Hacker G. The morphology of apoptosis. Cell Tissue Res 2000;301:5-17.

  105. Coultas L, Pellegrin M, Visvader JE, Lindeman GJ,Chen L, Adams JM, et al. Bfk: a novel weakly proaptotic member of Bcl-2 protein family with a Bh3 and Bh2 region. Cell Death Diffr 2003; 10:185-192.

  106. Johnson AL, Bridgham JT. Caspase-mediated apoptosis in the vertebrate ovary. Reproduction 2002;124:19-27.

  107. Johnson AL. Intracellular mechanisms regulating cell survival in ovarian follicles. Anim Reprod Sci 2003;78:185-201.

  108. Markstrom E, Svensson E Ch, Shao R, Svanderg B,Billig H. Survival factors regulating ovarian apoptosisdependence on follicle differentiation. Reproduction 2002 ;123:23-30.

  109. Henson PM, Bratton DL, Fadok V. Apoptotic cell removal. Curr Biol 2001;11:795-805.

  110. Hsueh AJ, Billing H, Tsafriri A. Ovarian follicule atresia: a hormonally controlled apoptotic process. Endocrinol. Rev 1994; 6:707-724.

  111. Shiota M, Sugai N,Tamura M, Yamaguchi R, Fukushima N, Miyano T, et al. Correlation of mitogen-activated protein kinase activities with cells survival and apoptosis in porcine granulose cells. Zoolog Sci 2003;20:193-201.

  112. Rosales-Torres AM, Avalos-Rodriguez A, Vergara-Onofre M, Hernandez-Perez O, Ballesteros LM, Garcia-Macedo R, et al. Multiparametric study of atresia in ewe antral follicles: histology, flowcytometry,internucleosomal DNA fragmentation, and lysosmal enzyme activities in granulosa cells and follicular fluid. Mol Reprod Dev 2000;55:270-281.

  113. Maillet G, Bréard E, Benhaim A, Leymarie P, Féra L.Hormonal regulation of apoptosis in rabbit granulosa cells in vitro: evaluation by fl ow cytometric detection of plasma membrane phosphatidylserine externalization. Reproduction 2002;123:243-251.

  114. Porter DA , Harman RM, Cowan RG, Quirk SM. Relationship of fas ligand expression and atresia during bovine follicle development. Reproduction 2001; 121:561-566.

  115. Asdell SA. Patterns of mammalian reproduction 2nd ed. New York. Cornell: University Press, 1964.

  116. Rosales TA, Atresia folicular. En: Velazques MJ editor.Biología de la reproducción. México D.F. Universidad Autónoma Metropolitana. 1998:223-261.

  117. Sang-Young C, Hsueh JWA. Paracrine mechanisms of ovarian follicle apoptosis. J Reprod Immunol 1998;32:63-75.

  118. Rosado A, Rosales AM, Maduración folicular en el mamífero. Ciencia 1991; 42:81-97.

  119. Kaipia A , Hsueh AJ. Regulation of ovarian follicule atresia. Annu Rev Physiol 1997:59;349-363.

  120. Reynaund K, Driancourt MA. Oocyte attrition. Mol Cell Endocrinol 2000:163;101-108.

  121. Tilly J. Apoptosis and ovarian function. Rev Reprod 1996;1:162-172.

  122. Mc Gee EA , Hsu S, Kaipia A, Hsueh AJ. Cell death and survival during ovarian follicle development. Mol Cell Endocrinol 1998;140:15-18.

  123. Mikkelsen AL, Hopstand E, Lindenber G. Incidence of apoptosis in granulosa cells from immature human follicles. Reproduction 2001; 122:481-486.

  124. Richards JS. Hormonal control of gene expression in the ovary. Endocrinol Rev 1994 ;6:725-751.

  125. McGee EA, Chun SY, Lai S, He Y, Hsueh AJ.Keratinocyte growth factor promotes the survival,growth and diffentiation of prenatal ovarian follicles.Fertil Steroid 1999; 71:732-738.

  126. Dunkel L, Tilly JL, Shikone T, Nishimori K, Hsueh AJ. Follicle-stimulating hormone receptor expression in the rat ovary: increases during prepubertal development and regulation by the opposing actions of transforming growth factors beta and alpha. Biol Reprod 1994;50:940-948.

  127. Ranikki AS, Zang FP, Huhtaniemi IT. Ontogeny of follicle stimulating hormone receptor gene expression in the rat testis and ovary. Molec Cell Endocr 1995;107:199-208.

  128. Billing h, Furuta I, Huseh AJ. Estrogens inhibit and androgens enhance ovarian granulose cell apoptosis.Endocrinology 1993;133:2204-2212.

  129. Murray AA, Molinek MD, Baker SJ, Kojima FN, Smith MF, Hillier SG, et al. Role of ascorbic acid in promoting follicle integrity and survival in intact mouse ovarian follicles in vitro. Reproduction 2001;121:89-96.

  130. Chun SY, Billing H, Tilly JL, Furuta I, Tsafriri A, Hsueh AJ. Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor. Endocrinology 1994;135:1845-1853.

  131. Chun Sy, Hsueh AJW. Paracrinre Mechanisms of ovarian follicle apoptosis, J Reprod Immunol 1998;39:63-75.

  132. Weeb R, Nicholas B, Gong JG, Campbell BK, Gutierrez CG, Garverik HA, et al. Mechanisms regulating follicular development and selection of the dominant follicle. Reproduction suppl 2003;61:71-79.

  133. Tilly L, Billing H, Kowalski Kl, Hsueh AJ. Epidermal growth factor and basic fibroblast growth factor suppress the spontaneous onset of apoptosis in cultured rat ovarian granulose cells and follicles by atyrosine kinase-dependent mechanism. Mol Endocrinol 1992;6:1942-1950.

  134. Svensson EC, Markstrom E, Andersson M, Billing H. Progesterone receptor-mediated inhibition of apoptosis in granulose cells insolated from rats treated with human chorionic gonadotropin. Biol Reprod 2000;63:1457-1464.

  135. Markigiannakis A, Coukos G, Christofidou-Solamidou M, Montas S, C. Progesterone is an autocrine/paracrine regulator of human granulose cell survival in vitro. Ann N Y Acad Sci 2000;900: 16-25.

  136. Ronghao Li, Phillips MD, Morre A, Mather J. Folliclestimulating hormone induces terminal differentiation in apredifferentiated rat granulose cell line (ROG). Endcorinology 1997;138:2648-2657.

  137. Asselin E, Xia CW, Wong FE, Tsang BK. Mammalian folicular development and atresia: role of apoptosis.Biol Signals Recept 2000;9: 874-895.

  138. Zeuner A, Muller K, Reguszynski K, Jewgenow K. Apoptosis within bovine follicular cells and its effect on oocyte development during in vitro maturation. Theriogenology 2003;59,1421-1433.

  139. FenwicK MA, Hurst P.R. Immunohistochmical localization of active caspase-3 in the mouse ovary: growth and atresia of small follicles. Reproduction 2002;124:659-665.

  140. Hsueh AJW, McGee EA, Hayasi M, Hsu S.Y. Hormonal regulation of early follicle development in the rat ovary. Mol Cell Endocrinol. 2000;163:95-100.

  141. Maillet G, BenhaÏm A, Mittre H, Féral C. Involvement of theca cells and steroids in the regulation of granulose cells apoptosis in rabbit preovulatory follicles. Reproduction 2003;125:709-716.

  142. Bobes RJ, Perez-Martinez M, Gomez Y, Romano MC. Metabolism of progesterone to estrogens and androgens by individual follicles of the goat ovary. Small Rum Res 2003;47:233-242.

  143. Yu Y, Li W, Han Z, Lou M, Chang Z, Tan J. The effect of follicle-stimulating hormone on follicular development, granulose cell apoptosis and steroidogenesis and its mediation by insulin-like growth factor-I in the goat ovary. Theriogenology 2003;60:1691-1704.

  144. Pedersen HG,Watson ED, Telfer E. Analysis of atresia in equine follicles using histology, fresh granulosa cell morphology, and detection of DNA fragmentation. Reproduction 2003;125:417-423.

  145. Iway T, Fujii S, Nabuy Y, Nonogak H, Konishi I, Mori T, et al. Effect of human chorionic gonadotropin on the expression of progesterone receptor and estrogen receptor in rabbit ovarian granulosa cells and the uterus. Endocrinology 1991;129:1840-1848.

  146. Byers M, Kiuper GG, Gustafsson JA, Park-Sarge OK.Estrogen-receptor-b mRNA expression in rat ovary: down regulation by gonadotropins. Mol Endocrinol 1997;11:172-182.

  147. Makrigianna A, Coukos G, Blaschuk O, Coutifaris C. Follicular atresia and luteolysis. Evidence of a role for N-cadherin. Ann N Y Acad Sci 2000;900:46-55.

  148. Arowsmith CH. Structure and function in the p53 family. Cell Death Differ 1999;94:514-519.

  149. Bendi A, Mookerje B. Biological significance and molecular mechanisms of p-53 inducedapoptosis. Apoptosis1988;3:224-237.

  150. Burns Ft, El-Deiry WS. The p53 pathway and apoptosis.J Cell Phys 1999; 181:231-239




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