Mechanism of granulosa cell death during follicular atresia depends on follicular size

Theriogenology

Volumn 60, Issue 6, 2003, Pages 1071-1081

  Alonso Pozos, Israel ^a   Rosales Torres, Ana Maria ^a   Ávalos Rodríguez, Alejandro ^a   Vergara Onofre, Marcela ^a   Rosado García, Adolfo ^b  

^a DEPARTAMENTO DE SISTEMAS BIOLÓGICOS   (Mexico)

^b DEPARTAMENTO DE QUÍMICA   (Mexico)

Author keywords

Apoptosis; Follicular atresia; Lysosome; Mitochondria; Necrosis

Indexed keywords

EID: 0041783167     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0093-691X(03)00123-7     Document Type: Article

References (50)

1. Driancourt MA. Follicular dynamics in sheep and cattle. Theriogenology 1991;35:55-79.
2. 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.
3. Tilly JL, Kowalski KI, Shomberg DW, Hsueh AJW. Apoptosis in atretic ovarian follicles is associated with selective decrease in messenger ribonucleic acid transcripts for gonadotropin receptors and cytochrome P450 aromatase. Endocrinology 1992;131:1670-6.
4. Blodin P, Dufour M, Sirard MA. Analysis of atresia in bovine follicles using different methods: flow cytometry, enzyme-linked immnunosorbent assay, and classical histology. Biol Reprod 1996;54:631-7.
5. Gaytan F, Morales C, Bellido C, Aguilar E, Sánchez-Criado JE. Ovarian follicles macrophages: is follicular atresia in the immature rat a macrophage mediated event? Biol Reprod 1998;58:52-9.
6. Adhered K, De-Prest B, Roels F. Subtypes of active cell death in the granulosa of ovarian atretic follicles in the quail (Coturnix coturnix japonica). Reprod Nutr Dev 1996;36:1775-89.
7. Van Wezel IL, Dharmarajan AM, Lavreanos TC, Rodgers RJ. Evidence for alternative pathways of granulose cell death in healthy and slightly atretic bovine antral follicles. Endocrinology 1999;140:2602-12.
8. Rosales-Torres AM, Ávalos-Rodríguez A, Vergara-Onofre M, Hernández-Pérez O, Ballesteros LM, García-Macedo R, et al. Multiparametric study of atresia in ewe antral follicles: histology, flow cytometry, internucleosomal DNA fragmentation, and lysosomal enzyme activities in granulosa cells and follicular fluid. Mol Reprod Dev 2000;55:270-81.
9. Rosales AM, Hernández-Pérez O. Domínguez R, Mercado E, Rosado A. Proteolitic and antiproteolitic activities in goat antral follicles. Anim Reprod Sci 1990;23:213-22.
10. Ballesteros LM, Rosales AM, Rosado A, Hernández-Pérez O. Activity, compartmentation, and subcellular distribution of lysosomal enzymes during follicular maturation in the goat. Anim Reprod Sci 1992;27:129-39.
11. Isahara K, Ohsawa Y, Kanamori S, Shibata M, Waguri S, Sato N, et al. Regulation of novel pathway for cell death by lysosomal aspartic and cysteine proteinases. Neuroscience 1999;91:233-49.
12. Li W, Yuan XM, Nordgren G, Dalen H, Dubowchik GM, Firestone RA, et al. Induction of cell death by lysosomotropic detergent MSDH. FEBS Lett 2000;470:35-9.
13. Lemasters JJ, Nieminen AL, Qian T, Trost LC, Elmore SP, Nishimura Y, et al. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis, and autophagy. Biochem Biophys Acta 1998;1366:177-96.
14. Adrian C, Martin SJ. The mitochondrial apoptosome: a killer unleashed by the cytochrome seas. Trends Biochem Sci 2001;26:390-7.
15. deDuve C, deBarsy T, Trouet A, Tulkens R, Van Hoof F. Commentary. Lysosomotropic agents. Biochem Pharmacol 1974;23:2495-531.
16. Traganos F, Darzynkiewicz Z. Lysosomal proton pump activity: supravital cell staining with Acridine Orange differentiates leukocyte subpopulations. Methods Cell Biol 1994;41:185-94.
17. Rundquist I, Olsson M, Brunk U. Cytofluorometric quantitation of Acridine Orange uptake by cultured cells. Acta Pathol Microbiol Immunol Scand 1984;92:303-10.
18. Brunk UT, Zhang H, Roberg K, Öllinger K. Lethal hydrogen peroxide toxicity involves lysosomal iron-catalyzed reaction with membrane damage. Redox Report 1995;1:267-77.
19. Johnson LV, Walsh ML, Chen LB. Localization of mitochondria in living cells with Rhodamine 123. Proc Natl Acad Sci USA 1980;77:990-4.
20. Darzynkiewicz Z, Traganos F, Staiano-Coico L, Kapuscinski J, Melamed MR. Interaction of Rhodamine 123 with living cells studied by flow cytometry. Cancer Res 1982;42:799-806.
21. Shapiro M, Zeri Y, Zeiri Y. Semiempirical potential surfaces for the alkali hydrogenhalide reactions. J Chem Phys 1979;70:5264-70.
22. García R, Ballesteros LM, Hernández-Pérez O, Rosales AM, Espinosa R, Soto H, et al. Metalloproteinase activity during growth, maturation and atresia in the ovarian follicles of the goat. Anim Reprod Sci 1997;47:211-28.
23. Hirshfield AN. Size-frequency analysis of atresia in cycling rats. Biol Reprod 1988;38:1181-8.
24. Guthrie HD, Welch GR, Couper BS, Zakaria AD, Johnson LA. Flow cytometric determination of degraded deoxyribonucleic acid in granulosa cells to identify atretic follicles during preovulatory maturation in the pig. Biol Reprod 1994;50:1303-11.
25. Darzynkiewicz Z, Li X, Gong J. Assay of cell viability: discrimination of cells dying by apoptosis. Methods Cell Biol 1994;41:15-38.
26. Sokal RR, Rohll FJ. Biometry. San Francisco: W.H. Freeman & Co.; 1969. p. 299-342.
27. Wyllie AH, Kerr JFR, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980;68:251-306.
28. Shimizu S, Eguchi Y, Kamiike W, Itoh Y, Hasegawa J, Yamabe K, et al. Induction of apoptosis as well as necrosis by hypoxia and predominant prevention of apoptosis by Bcl-2 and Bcl-xL. Cancer Res 1996;56:2161-6.
29. Renvoizé, C, Biola A, Pallardy M, Bréard J. Apoptosis: identification of dying cells. Cell Biol Toxicol 1998;14:111-20.
30. Columbano A. Cell death: current difficulties in discriminating apoptosis from necrosis in the context of pathological processes in vivo. J Cell Biochem 1995;58:181-90.
31. Zamzami N, Hirsch T, Dallaporta B, Petit PX, Kroemer G. Mitochondrial implications in accidental and programmed cell death: apoptosis and necrosis. J Bioenergy Biomembr 1997;29:185-93.
32. Zamai I, Falcieri E, Marhefka G, Vitale M. Supravital exposure to propidium iodide identifies apoptotic cells in the absence of internucleosomal DNA fragmentation. Cytometry 1996;23:303-11.
33. Liu XJ, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996;86:147-57.
34. Anjum R, Khar A. Caspased-mediated apoptosis in AK-5 tumor cells: a cell-free study using peptide inhibitors and antisense strategy. Exp Cell Res 1997;236:371-7.
35. Besnard N, Pisselet C, Monniaux D, Monget P. Proteolytic activity is involved in changes in intrafollicular insulin-like growth factors-binding protein-2,-3,-4 and 5 in healthy growing and atretic follicles in the pig ovary. Biol Reprod 1997;56:1050-8.
36. Dhanasekaran N, Moudgal NR. Studies on follicle atresia: Role of gonadotropins and gonadal steroids in regulating cathepsin D activity of preovulatory follicles in the rat. Endocrinology 1989;63:133-42.
37. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Nat Acad Sci USA 1995;92:7162-76.
38. Dypbukt JM, Ankarcrona M, Burkitt M, Sjoeholm A, Ström K, Orrenius S, et al. Different prooxidant levels stimulate growth, trigger apoptosis, or produce necrosis of insulin-secreting RINm5F cells. The role of intracellular polyamines. J Biol Chem 1994;269:30553-60.
39. Vayssiere JL, Petit PX, Risler Y, Mignotte B. Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cells conditionally immortalized with simian virus 40. Proc Natl Acad Sci USA 1994;91:11752-6.
40. Zanzami N, Marchetti P, Castedo M, Zanin C, Vayssiére JL, Petit PX, et al. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocytes death in vivo. J Exp Med 1995;181:1661-72.
41. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, et al. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995;15:961-73.
42. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a swith in the decision between apoptosis and necrosis. J Exp Med 1997;185:1481-6.
43. Darzynkiewicz Z, Juan G, Xun L, Gorczyca W, Murakami T, Traganos F. Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 1997;27:1-20.
44. Cossarizza A, Baccarani-Contri M, Kalashnikova G, Franceschi C. A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′ -tetrachloro-1,1′,3,3′-tetraethylbenzimidazolcarbocyanine iodide JC-1. Biochem Biophys Res Commun 1993;197:40.
45. Murdoch WJ. Comparative morphometry and steroidogenic function of antral ovine follicles destined for ovulation or atresia. Dom Anim Endocrinol 1992;9:219-24.
46. Hirshfield AN. Development of follicles in the mammalian ovary. Int Rev Cytol 1991;124:43-101.
47. Richter C, Schweizer M, Cossarizza A, Franceschi C. Control of apoptosis by cellular ATP level. FEBS Lett 1996;378:107-10.
48. Tsujimoto Y. Apoptosis and necrosis: intracellular ATP levels as a determinant for cell death modes. Cell Death Differ 1997;4:429-39.
49. Bukosky A, Presl J, Zidovsky J. Migration of lymphoid cells into the granulosa of rat ovarian follicles. IRCS Med Sci 1979;7:603-4.
50. Leist M, Gantner F, Bohlinger I, Tiegs G, Germann PG, Wendel A. Tumor necrosis factor-induced hepatocyte apoptosis precedes liver failure in experimental murin shock models. Am J Pathol 1995;146:1220-34.