Leydig cell apoptosis in the rat testes after administration of the cytotoxin ethane dimethanesulphonate: Role of the Bcl-2 family members

Journal of Endocrinology

Volumn 157, Issue 2, 1998, Pages 317-326

  Taylor, M F ^a   Woolveridge, I ^a   Metcalfe, A D ^a   Streuli, C H ^a   Hickman, J A ^a   Morris, I D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIN; ETHYLENE GLYCOL DIMESYLATE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL DEGENERATION; CELL SURVIVAL; CHROMATIN; CYTOTOXICITY; IMMUNOHISTOCHEMISTRY; LEYDIG CELL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN FAMILY; RAT; SEMINIFEROUS TUBULE; TESTIS FUNCTION; TUMOR SUPPRESSOR GENE;

EID: 0031809904     PISSN: 00220795     EISSN: None     Source Type: Journal    
DOI: 10.1677/joe.0.1570317     Document Type: Article

References (69)

1. Almon E, Goldfinger N, Kapon A, Schwartz D, Levine AJ & Rotter V 1993 Testicular tissue-specific expression of the p53 suppresser gene. Developmental Biology 156 107-116.
2. Arends MJ, Morris RJ & Wyllie AH 1990 Apoptosis: the role of the endonuclease. American Journal of Pathology 136 593-608.
3. Bakhshi A, Jensen JP, Goldman P, Wright JJ, McBride OW, Epstein AL & Korsmeyer SJ 1985 Cloning the chromosomal break point of the t(14:18) human lymphomas: clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell 41 889-906.
4. Beaver JP & Waring P 1995 A decrease in intracellular glutathione concentration precedes the onset ot apoptosis in murine thymocytes. European Journal of Cell Biology 68 47-54.
5. Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, Mao X, Nunez G & Thompson C 1993 Bcl-x, a bcl-2 related gene that functions as a dominant regulator of apoptotic death. Cell 74 597-608.
6. Bradford MM 1976 A rapid and sensitive method for the quantification of microgram quantities of protein using the principal of protein dye binding. Analytical Biochemistry 72 248-254.
7. Brown DG, Sun XM & Cohen GM 1993 Dexamethasone-induced apoptosis involves cleavage of DNA to large fragments prior to internucleosomal fragmentation. Journal of Biological Chemistry 268 3037-3039.
8. Caelles C, Helmberg A & Karin M 1994 p53-dependent apoptosis in the absence of transcriptional activation of p53 target genes. Nature 370 646-649.
9. Chittenden T, Harrington EA, O'Conor R, Flemington C, Lutz RJ, Evan GI & Guild BC 1995 Induction of apoptosis by the Bcl-2 homologue Bak. Nature 374 733-736.
10. Cleary ML, Smith SD & Sklar J 1986 Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the t(14:18) translocation. Cell 47 19-28.
11. Cohen JJ & Duke RC 1984 Glucocorticoid activation of a calcium dependent endonuclease in thymocyte nuclei leads to cell death. Journal of Immunology 132 38-42.
12. Corcoran GB, Fix L, Jones DP, Molsen MT, Nicotera P, Oberhammer FA & Buttyan R 1994 Apoptosis: molecular control point in toxicity. Toxicology and Applied Pharmacology 128 169-181.
13. 4 isomerase (3βHSD) in rat testis as studied by immunocytochemistry. Anatomy and Embryology 187 583-589.
14. Earnshaw WC 1995 Nuclear changes in apoptosis. Current Opinions in Cell Biology 7 337-343.
15. Farrow SN, White JHM, Martinou I, Raven T, Pun KT, Grinham CJ, Martinou JC & Brown R 1995 Cloning of a bcl-2 homologue by interaction with adenovirus E1B19K. Nature 374 731-733.
16. Gavrieli Y, Sherman Y & Ben-Sasson SA 1992 Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. Journal of Cell Biology 119 493-501.
17. Gold R, Schmied M, Giegerich G, Breitschopf H, Hartung HP, Toyka KV & Lassmann 1994 Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Laboratory Investigations 71 219-225.
18. Gorczyca W, Gong J & Darzynkiewicz Z 1993 Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Research 53 1945-1951.
19. Henriksen K, Hakovirta H & Parvinen M 1995 Testosterone inhibits and induces apoptosis in rat seminiferous tubules in a stage-specific manner: in situ quantification in squash preparations after administration of ethane dimethanesulphonate. Endocrinology 136 3285-3291.
20. Hockenbery DM, Nunez G, Milliman C, Schreiber RD & Korsmeyer SJ 1990 Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348 334-336.
21. Hockenbery DM, Zutter M, Hickey W, Nahm M & Korsemeyer SJ 1991 Bcl-2 protein is topographically restricted in tissues characterised by apoptotic death. Proceedings of the National Academy of Sciences of the USA 88 6961-6965.
22. Jackson AE, O'Leary PC, Ayres MM & de Kretser DM 1986a The effects of ethane dimethanesulphonate (EDS) on rat Leydig cells: evidence to support a connective tissue origin of Leydig cells. Biology of Reproduction 35 425-427.
23. Jackson CM & Jackson H 1984 Comparative protective actions of gonadotrophins and testosterone against the antispermatogenic action of ethane dimethanesulphonate. Journal of Reproduction and Fertility 71 393-401.
24. 125I-labelled hCG, light and electron microscopy of the repopulation of rat Leydig cells after destruction due to administration of ethylene-1,2-dimethanesulphonate. Journal of Reproduction and Fertility 76 1-10.
25. Kamada S, Shinto AA, Tsujimura Y, Takahashi T, Noda T, Kitamura Y, Kondoh H & Tsuijmoto Y 1995 Bcl-2 deficiency in mice leads to pleiotropic abnormalities: accelerated lymphoid cell death in the thymus and spleen, polycystic kidney, hair hypopigmentation, and distorted small intestine. Cancer Research 4 359.
26. Kelce WR 1994 Buthionine sultoximine protects the viability of adult rat Leydig cells exposed to ethane dimethanesulphonate. Toxicology and Applied Pharmacology 125 237-246.
27. Kelce WR & Zirkin BR 1993 Mechanism by which ethane dimethanesulphonate kills adult rat Leydig cells: involvement of intracellular glutathione. Toxicology and Applied Pharmacology 120 80-88.
28. Kerr JB, Donachie K & Rommerts FFG 1985 Selective destruction and regeneration of rat Leydig cells in vivo. Cell and Tissue Research 242 145-156.
29. Kerr JB, Bartlett JMS & Donachie K 1986 Acute response of testicular interstitial tissue in rats to the cytotoxic drug ethane dimethanesulphonate. An ultrastructural and hormonal study. Cell and Tissue Research 243 405-414.
30. Kerr JB, Bartlett JMS, Donnachie K & Sharpe RM 1987 Origin of regenerating Leydig cells in the testis ot the adult rat. An ultrastructural, morphometric and hormonal assay study. Cell and Tissue Research 249 367-377.
31. Kiefer MC, Brauer MJ, Powers VC, Wu JJ, Umansky SR, Tomei LD & Barr PJ 1995 Modulation of apoptosis by the widely distributed Bcl-2 homologue Bak. Nature 374 736-739.
32. Knudson CM, Tung KSK, Tourtellotte WG, Brown GAJ & Korsmeyer SJ 1995 Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270 96-99.
33. Krajewski S, Krajewska M, Shabaik A, Wang HG, Irie S, Fong L & Reed JC 1994 Immunohistochemical analysis of in vivo patterns of Bcl-x expression. Cancer Research 54 5501-5507.
34. Krajewski S, Bodrug S, Krajewski M, Shabaik A, Gascoyne R, Berean K & Reed J 1995 Immunohistochemical analysis of Mcl-1 protein in human tissues. American Journal of Pathology 146 1309-1319.
35. Krajewski S, Krajewski M & Reed JC 1996 Immunohistochemical analysis of in vivo patterns of Bak expression, a proapoptotic member of the Bcl-2 protein family. Cancer Research 56 2849-2855.
36. Kroemer G, Petit P, Zamami N, Vayssiere JL & Mignotte B 1995 The biochemistry of programmed cell death. FASEB Journal 9 1277-1287.
37. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680-685.
38. Lin T, Calkins JH, Morris PL, Vale W & Bardin CW 1989 Regulation of Leydig cell function in primary culture by inhibin and activin. Endocrinology 125 2134-2140.
39. Miyashita T & Reed JC 1995 Tumour suppresser p53 is a direct transcriptional activator of the human bax gene. Cell 80 293-299.
40. Molenaar R, de Rooij DG, Rommerts FF, Reuvers PJ & van der Molen HJ 1985 Specific destruction of Leydig cells in mature rats after in vivo administration of ethane dimethylsulphonate. Biology of Reproduction 33 1213-1222.
41. Moore A & Morris ID 1993 The involvement of insulin-like growth factor-I in local control of steroidogenesis and DNA synthesis of Leydig and non-Leydig cells in the rat testicular interstitium. Journal of Endocrinology 138 107-114.
42. Morris ID 1996 Leydig cell toxicology. In The Leydig Cell, pp 573-596. Eds AH Payne, MP Hardy & LD Russell. Vienna, II: Cache River Press.
43. Morris ID, Phillips DM & Bardwin CW 1986 Ethane dimethanesulphonate destroys Leydig cells in the rat testis. Endocrinology 118 709-719.
44. Morris AJ, Taylor MF & Morris ID 1997 Leydig cell apoptosis in response to ethane dimethanesulphonate after both in vivo and in vitro treatment. Journal of Andrology 18 274-280.
45. Motoyama N, Wang F, Roth KA, Sawa H, Nakayama K, Nakayama K, Negishi I, Senju S, Zhang Q, Fujii S & Loh D 1995 Massive cell death of immature hematopoetic cells in neurons in bcl-x-deficient mice. Science 267 1506-1510.
46. Nakayama KI, Nakayama K, Negishi I, Kuida K, Shinkai Y, Louie MC, Fields LE, Lucas PI, Stewart V, Alt FW & Loh DY 1993 Disappearance of the lymphoid system in bcl-2 homozygous mutant chimeric mice. Science 261 1584-1588.
47. Nakayama KI, Nakayama K, Negishi I, Kuida K, Sawa H & Loh DY 1994 Targeted disruption of bcl-2 alpha beta in mice: occurrence of grey hair, polycystic kidney disease and lymphocytopenia. Proceeding of the National Academy of Sciences of the USA 91 3700-3704.
48. Novak DV & Korsmeyer SJ 1994 Bcl-2 expression during murnie development. American Journal of Pathology 145 61-73.
49. Oltavi ZN, Millman CL & Korsmeyer SJ 1993 Bcl-2 heterodimers in vivo with a conserved homologue, Bax, that accelerates programmed cell death. Cell 74 609-619.
50. O'Shaughnessy PJ & Murphy L 1991 Steroidogenic enzyme activity in the rat testis following Leydig cell destruction by ethylene-1,2-dimethanesulphonate and during subsequent Leydig cell regeneration. Journal of Endocrinology 131 451-457.
51. Pullan S, wilson J, Metcalfe A, Edwards GM, Goberdhan N, Tilly J, Hickman JA, Dive C & Streuli CH 1996 Requirement of basement membrane for the suppression of programmed cell death in mammary epithelium. Journal of Cell Science 109 631-642.
52. Reynolds JE, Yang T, Qian T, Jenkinson JD, Zhou P, Eastman A & Craig RW 1994 Mcl-1, a member of the Bcl-2 family, delays apoptosis induced by c-Myc overexpression in Chinese hamster ovary cells. Cancer Research 54 6348-6352.
53. Sabbatini P, Chiou SK, Roa L & White E 1995 Modulation of p53-mediated transcriptional repression and apoptosis by the adenovirus E1B 19 kD protein. Molecular and Cellular Biology 15 1060-1070.
54. Schwartz D, Goldfinger N & Rotter V 1993 Expression of p53 protein in spermatogenesis is confined to the tetraploid pachytene spermatocytes. Oncogene 8 1487-1494.
55. Shen Y & Shenk T 1994 Relief of p53-mediated transcriptional repression by the adenovirus E1B 10 kD protein or the cellular Bcl-2 protein. Proceedings of the National Academy of Sciences of the USA 91 8940-8944.
56. Sjoblom T & Lahdetie J 1996 Expression of p53 in normal and γ-irradiated rat testis suggests a role for p53 in meiotic recombination and repair. Oncogene 12 2499-2505.
57. Stephan H, Polzar B, Rauch F, Zanotti S, Ulke C & Mannherz HG 1996 Distribution of deoxyribonudease I (Dnase I) and p53 in rat testis and their correlation with apoptosis. Histochemistry and Cell Biology 106 383-393.
58. Sugimoto C, Matsukawa S, Fujieda S, Noda I, Tanaka N, Tsuzuki H & Saito H 1996 Involvement of intracellular glutathione in induction of apoptosis by cisplatin in a human pharyngeal carcinoma cell line. Anticancer Research 16 675-680.
59. Tapanainen JS, Tilly JL, Vihko KK & Hsueh AJW 1993 Hormonal control of apoptotic cell death in the testis: gonadotrophins and androgens as testicular cell survival factors. Molecular Endocrinology 7 643-650.
60. Teerds KJ 1996 Regeneration of Leydig cells after depletion by EDS: a model for postnatal Leydig cell renewal. In The Leydig Cell, pp 203-220. Eds AH Payne, MP Hardy & LD Russell. Vienna, II: Cache River Press.
61. Vaux DL, Cory S & Adams TM 1988 Bcl-2 promotes the survival of haemopoietic cells and co-operates with c-myc to immortalise pre-B cells. Nature 335 440-442.
62. waf1/cip 1. Genes and Development 8 2817-2830.
63. Weibe JP 1976 Steroidogenesis in rat Leydig cells: changes in activity of 5-ane and 5-ene 3 beta-hydroxysteroid dehydrogenase during sexual maturation. Endocrinology 98 505-513.
64. Wyllie AH 1980 Glucocorticoid induced thyniocyte apoptosis is associated with endogenous endonuclease activation. Nature 284 555-556.
65. Xiao-Ming Y, Oltvai ZN & Korsmyer SJ 1994 BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerisation with Bax. Nature 369 321-323.
66. Yin C, Knudson CM, Korsmeyer SJ & Van Dyke T 1997 Bax suppresses tumorigenesis and stimulates apoptosis in vivo. Nature 385 637-640.
67. Zhan QM, Alamo I, Yu K, Boise LH, Cherney B, Tosato G, O'Conor PM & Fornace AJ 1996 The apoptosis associated gamma-ray response of Bcl-x(L) depends on normal p53 function. Oncogene 13 2287-2293.
68. Zhang XH, Li L, Choe J, Krajewski S, Reed JC, Thompson C & Choi YS 1996 Up-regulation of Bcl-x(1) expression protects CD40-activated human B cells from Fas-mediated apoptosis. Cellular Immunology 173 149-154.
69. 5-3β-hydroxysteroid-dehydrogenase during the foetal and neonatal development of rat Leydig cells. Andrologia 15 392-397.