Multiparametric study of atresia in ewe antral follicles: Histology, flow cytometry, internucleosomal DNA fragmentation, and lysosomal enzyme activities in granulosa cells and follicular fluid

Molecular Reproduction and Development

Volumn 55, Issue 3, 2000, Pages 270-281

  Rosales Torres, Ana María ^a   Avalos Rodríguez, Alejandro ^a   Vergara Onofre, Marcela ^a   Hernández Pérez, Omar ^b   Ballesteros, Luz María ^b   García Macedo, Rebeca ^c   Ortíz Navarrete, Vianney ^c   Rosado, Adolfo ^b  

^a DEPARTAMENTO DE SISTEMAS BIOLÓGICOS   (Mexico)

^b DEPARTAMENTO DE QUÍMICA   (Mexico)

^c INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

Author keywords

Apoptosis; Atresia; Follicular growth; Lysosomal enzymes; Necrosis

Indexed keywords

DNA FRAGMENT;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MATURATION; ENZYME ACTIVITY; FLOW CYTOMETRY; FOLLICLE FLUID; GRANULOSA CELL; HISTOLOGY; LYSOSOME MEMBRANE; MEMBRANE BINDING; NONHUMAN; NUCLEOSOME; OVARY FOLLICLE ATRESIA; PRIORITY JOURNAL; SHEEP;

ACID PHOSPHATASE; ANIMALS; ANNEXIN A5; APOPTOSIS; CELL CYCLE; DNA FRAGMENTATION; ELECTROPHORESIS, AGAR GEL; ESTRADIOL; FEMALE; FLOW CYTOMETRY; FOLLICULAR ATRESIA; FOLLICULAR FLUID; GRANULOSA CELLS; HEXOSAMINIDASES; LYSOSOMES; NECROSIS; NUCLEOSOMES; PROGESTERONE; SHEEP;

ANIMALIA; OVIS ARIES;

EID: 0342632814     PISSN: 1040452X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2795(200003)55:3<270::AID-MRD5>3.0.CO;2-H     Document Type: Article

References (71)

1. Amsterdan A, Dantes A, Husokawa K, Schere-Levy CP, Kotsuji F, Aharoni D. 1998. Steroid regulation during apoptosis of ovarian follicular cells. Steroids 63:314-318.
2. Anjum R, Khar A. 1997. Caspase-mediated apoptosis in AK-5 tumor cells: A cell-free study using peptide inhibitors and antisense strategy. Exp Cell Res 236:371-377.
3. Ballesteros LM, Rosales AM, Rosado A, Hernández-Pérez O. 1992. Activity, compartmentation, and subcellular distribution of lysosomal enzymes during follicular maturation in the goat. Anim Reprod Sci 27:129-139.
4. Besnard N, Pisselet C, Zapf J, Hornebeck W, Monniaux D, Monget P. 1996. Proteolytic activity is involved in changes in intrafollicular insulin like growth factors binding protein levels during growth and atresia of ovine ovarian follicles. Endocrinology 137:1599-1607.
5. Besnard N, Pisselet C, Monniaux D, Monget P. 1997. Proteolytic activity is involved in changes in intrafollicular insulin-like growth factor-binding protein-2, -3, -4 and -5 in healthy growing and atretic follicles in the pig ovary. Biol Reprod 56:1050-1058.
6. Blondin P, Dufour M, Sirard M.A. 1996. Analysis of atresia in bovine follicles using different methods: flow cytometry, enzyme-linked immnunosorbent assay, and classical histology. Biol Reprod 54:631-637.
7. Braw RH, Tsafriri A. 1980. Effect of PMSG on follicular atresia in the rat ovary. J Reprod Fertil 59:267-272.
8. Bukovsky A, Presl J, Zidovsky J. 1979: Migration of lymphoid cells into the granulosa of rat ovarian follicles. IRCS Med Sci 7:603-604.
9. Chandrasekher YA, Clark CR, Faessen GH, Giudice LC. 1995. Role of insulin-like growth factor binding protein-4. (IGFBP-4) and IGFBP-4 protease in human granulosa cell function. In: Program of the 77th annual meeting of the Endocrine Society, Annaheim, CA. Abstract 102.
10. Collins RJ, Harmon BV, Gobe GC, Kerr JFR. 1992. Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. Int J Radiat Biol 61:451-453.
11. Columbano A. 1995. Cell death: current difficulties in discriminating apoptosis from necrosis in the context of pathological processes in vivo. J Cell Biochem 58:181-190.
12. Crosby WH, Furth FW. 1956. A modification of the benzidine method for measurement of hemoglobin in plasma and urine. Blood 11:380-385.
13. D'Herde K, De Prest B, Roels F. 1996. Subtypes of active cell death in the granulosa of ovarian atretic follicles in the quail (Coturnix coturnixjaponica). Reprod Nutr Dev 36:175-189.
14. Darzynkiewicz Z, Juan G, Xun Li, Gorczyca W, Murakami T, Traganos F. 1997. Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 27:1-20.
15. Dhanasekaran N, Moudgal NR. 1989. Studies on follicle atresia: role of gonadotropins and gonadal steroids in regulating cathepsin-D activity of preovulatory follicles in the rat. Endocrinology 63:133-142.
16. Dougherty JJ, Puri RK, Toft DO. 1982. Phosphorylation in vivo of chicken oviduct progesterone receptors. J Biol Chem 257:14226-14235.
17. Driancoura M. 1991. Follicular dynamics in sheep and cattle. Theriogenology 35:55-79.
18. Dyson JED, Simmons DM, Daniel J, McLaughin JM, Quirke P, Bird CC. 1986. Cell Tissue Kinet 19:311-324.
19. Fernandez PA, Rotello RJ, Rangini Z, Doupe A, Drexler HCA, Yuan J. 1994. Expression of a specific marker of avian programmed cell death in both apoptosis and necrosis. Proc Natl Acad Sci (USA) 91:8641-8645.
20. García R, Ballesteros LM, Hernández-Pérez O, Rosales AM, Espinosa R, Soto H, Díaz de León L, Rosado A. 1997. Metalloproteinase activity during growth, maturation and atresia in the ovarian follicles of the goat. Anim Reprod Sci 47:211-228.
21. Gaytan F, Morales C, Bellido C, Aguilar E., Sánchez-Criado JE. 1998. Ovarian follicle macrophages: Is follicular atresia in the immature rat a macrophage mediated event. Biol Reprod 58:52-59.
22. Gilbert AB, Perry ME, Walker MA, Waddington D. 1985. Identification of atresia in small ovarian follicles of the domestic hen (Gallus domesticus). IRCS Med Sci 13:723-733.
23. Gong J, Traganos F, Darzynkiewicz Z. 1994. A selective procedure for DNA extraction from apoptotic cells applicable to gel electrophoresis and flow cytometry. Anal Biochem 218:314-319.
24. Greenwald GS. 1989. Temporal and topographic changes in DNA synthesis after induced follicular atresia. Biol Reprod 41:175-181.
25. Greenwald GS, Roy SK. 1994. Follicular development and its control. In: Knobil E, Neill J, editors. The physiology of reproduction. New York: Raven Press. p 629-724.
26. Guthrie HI, Welch GR, Couper BS, Zacaria AD, Johnson LA. 1994. Flow cytometric determination of degraded deoxyribonucleic acid in granulosa cells to identify atretic follicles during preovulatory maturation in the pig. Biol Reprod 50:1303-1311.
27. Hamabata T, Okimura H, Yokoyama N, Takahashi, T, Takahashi, K. 1994. Purification, characterization and localization of follipsin, a novel serine proteinase from the fluid of porcine ovarian follicles. J Biol Chem 269:17899-17904.
28. Hirshfield AN. 1991. Development of follicles in the mammalian ovary. Inter Rev Cytol 124:43-101.
29. Hirshfield AN, Flickinger GL, Ben-Rafael Z. 1988. Flow cytometric analysis of granulosa cell proliferation in the rat. J Reprod Fertil 84:231-238.
30. Hsueh AJW, Billing H, Tsafriri A. 1994. Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr Rev 15:707-724.
31. Hubbard CJ, Greenwald GS. 1985. Morphological changes in atretic Graafian follicles during induced atresia in the hamster. Anat Rec 212:353-357.
32. Hughes FM, Gorospe WC. 1991. Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 129:2415-2422.
33. Huschtscha LI, Jeitner TM, Andersson CE, Bartier WA, Tattersall MHN. 1994. Identification of apoptotic and necrotic human leukemic cells by flow cytometry. Exp Cell Res 212:161-165.
34. Jolly PD, Tisdall DJ, Heath DA, Lun S, MaNatty KP. 1994. 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 51:934-944.
35. Jolly PD, Smith PR, Heath DA, Hudson NL, Lun S, Still LA, Watts CH, MaNatty KP. 1997. Morphological evidence of apoptosis and the prevalence of apoptotoc versus mitotic cells in the membrane granulosa of ovarian follicles during spontaneous and induced atresia. Biol Reprod 56:837-846.
36. Kerr JFR, Searle J, Harmon BM, Bishop CJ. 1987. Perspectives on mammalian cell death. In: Bowen CS, editor. New York: Oxford University Press. p 93-127.
37. Kim JM, Boone DL, Auyeung A, Tsang BK. 1998. Granulosa cell apoptosis induced at the penultimate stage of follicular development is associated with increased levels of Fas and Fas Ligand in the rat ovary. Biol Reprod 58:1170-1176.
38. Kornfeld S. 1987. Trafficking of lysosomal enzymes. FASEB J 1:462-468.
39. Kovacs J, Forgo V, Peczely P. 1992. The fine structure of the follicular cells in growing and atretic ovarian follicles of the domestic goose. Cell Tissue Res 267:561-569.
40. Leist M, Single B Castoldi AF, Kuhnle S, Nicotera P. 1997. Intracellular adenosine triphosphate (ATP) concentration: a seitch in the decision between apoptosis and necrosis. J Exp Med 185:1481-1486.
41. Lemasters JJ, Nieminen AL, Qian T, Trost LC, Elmore SP, Nishimura Y, Crowe RA, Cascio WE, Bradham CA, Brenner DA, Herman B. 1998. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis, and autophagy. Biochim Biophys Acta 1366:177-196.
42. Levin S. 1995. Commentary: a toxicologic pathologist's view of apoptosis or I used to call it necrobiosis, but now I am singing the apoptosis blues. Toxicol Pathol 23:533-539.
43. Li J, Kim JM, Liston P, Li M, Miyazaki T, Mackenzie AE, Korneluk RG, Tsang BK. 1998. Expression of the inhibitor of apoptosis proteins (IAPs) in rat granulosa cells during ovarian follicular development and atresia. Endocrinology 139:1321-1328.
44. Liu XJ, Malkowski M, Guo Y, Erickson G, Shimasaki S, Ling NC. 1993. Development of specific antibodies to rat insulin-like growth factor-binding proteins (IGFBP-2 to 6): analysis of IGFBP production by rat granulosa cells. Endocrinology 132:1176-1183.
45. Liu XJ, Kim CN, Yang J, Jemmerson R, Wang X. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86:147-157.
46. Lowry OH, Rosebrough NJ, Fara AL, Randall RJ. 1951. Protein measurement with the folinphenol reagent. J Biol Chem 193:265-275.
47. Luciano AM, Pappalardo A, Ray C, Peluso JJ. 1994. Epidermal growth factor inhibits large granulosa cells apoptosis by stimulating progesterone synthesis and regulating the distribution of intracellular free calcium. Biol Reprod 51:646-654.
48. Majno G, Joris I. 1995. Apoptosis, oncosis and necrosis: an overview of cell death. Am J Pathol 146:3-16.
49. Moor RM, Mary FH, Dott HM, Cran DJ. 1978. Macroscopic identification and steroidogenic function of atretic follicles in sheep. J Endocrinol 77:309-318.
50. Murdoch WJ. 1992. Comparative morphometry and steroidogenic function of antral ovine follicles destined for ovulation or atresia. Domestic Animal Endocrinol 9:219-224.
51. Narimoto K, Okamura H, Mori T, Sakai M, Espey LL, Ogawa K. 1985. Cytochemical localization of acid phosphatase in the rabbit ovarian follicle. Acta Histochem Cytochem 18:525-537.
52. Palumbo A, Yeh J. 1994. In situ localization of apoptosis in the rat ovary during follicular atresia. Biol Reprod 51: 888-895.
53. Peluso JJ, Charlesworth J, England-Charlesworth C. 1981. Role of estrogen and androgen in maintaining the preovulatory follicle. Cell Tissue Res 216:614-624.
54. Renvoizé C, Biola A, Pallardy M, Bréard J. 1998. Apoptosis: identification of dying cells. Cell Biol Toxicol 14:111-120.
55. Richter CM, Schweizer A, Cossarizza C, Franceschi. 1996. Control of apoptosis by the cellular ATP level. FEBS Lett 378:107-110
56. Rosado A, Mercado E, Gallegos AJ, Wens MA, Aznar R. 1977. Subcellular distribution of lysosomal enzymes in the human endometrium: I. Normal menstrual cycle. Contraception 16:287-297.
57. Rosales AM, Hernández-Pérez O, Domínguez R, Mercado E, Rosado A. 1990. Proteolytic and antiproteolytic activities in goat antral follicles. Anim Reprod Sci 23:213-222.
58. Schwartzman RA, Cidlowski JA. 1993. Apoptosis: the biochemistry and molecular biology of cell death. Endocr Rev 14:133-151
59. Shimizu S, Eguchi Y, Kamiike W, Waguri S, Uchiyama Y, Matzuda H, Tsujimoto Y. 1996. Bcl-2 blocks loss of mitochondrial transmembrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13:21-29.
60. Sokal RR, Rohll FJ. 1969. Biometry. San Francisco: WH Freeman & Co. p 299-342.
61. Thompson C B. 1995. Apoptosis in the pathogenesis and treatment of disease. Science 267:1456-1462.
62. Tilly JL, Kowalski KI, Johnson AL, Hsue AJW. 1991. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129:2799-2801.
63. Tilly JL, Kowalski KI, Shomberg DW, Hsueh AJW. 1992. Apoptosis in atretic ovarian follicles in associated with selective decrease in messenger ribonucleic acid transcripts for gonadotropin receptors and cytochrome P450 aromatase. Endocrinology 131:1670-1676.
64. Traganos F, Darzynkiewicz Z. 1994. Lysosomal proton pump activity: supravital staining with acridine orange differentiates leukocyte subpopulation. Methods Cell Biol 41:185-195.
65. Tsujimoto Y, Shimizu S, Eguchi Y, Kamiike W, Matsuda H. 1997. Bcl-2 and Bcl-xL block apoptosis as well as necrosis: possible involvement of common mediators in apoptotic and necrotic signal transduction pathways. Leukemia 11 (Suppl 3):380-2
66. Vermes I, Haancen C, Steffens-Nakken H, Reuteligsperger Ch. 1995. A novel assay for apoptosis flow cytometric detection of phosphatidyl-serine expression on early apoptotic cell using fluorescein labeled annexin V. J Immunol Methods 184:39-51.
67. Wise T. 1987. Biochemical analysis of bovine follicular fluid: albumin, total protein, lysosomal enzymes, ion, steroids and ascorbic acid content in relation with follicular size, rank, atresia classification and day of estrous cycle. J Anim Sci 64:1153-1169.
68. Woessner JF Jr, Morioka N, Zhu Ch, Mucaida T, Butler T, LeMaire WJ. 1989. Connective tissue breakdown in ovulation. Steroid 54:491-499.
69. Wyllie AH. 1992. Apoptosis and the regulation of cell numbers in normal and neoplastic tissues: an overview. Cancer Metastasis Rev 11:95-103.
70. Zamai I, Falcieri E, Marhefka G, Vitale M. 1996. Supravital exposure to propidium iodide identifies apoptotic cells in the absence of internucleosomal DNA fragmentation. Cytometry 23:303-311.
71. Zanzami N, Hirsch T, Dallaporta B, Petit PX, Kroemer G. 1997. Mitochondrial implications in accidental and programmed cell death: apoptosis and necrosis. J Bioenerg Biomembr 29:185-193.