Diethyl maleate-induced oxidative stress leads to testicular germ cell apoptosis involving Bax and Bcl-2

Journal of Biochemical and Molecular Toxicology

Volumn 22, Issue 6, 2008, Pages 371-381

  Kalia, Sumiti ^a   Bansal, M P ^a  

^a PANJAB UNIVERSITY   (India)

Author keywords

Apoptosis; Bax; Diethyl maleate; Oxidative stress; Testis

Indexed keywords

BIOLOGICAL MARKER; BIOTIN; DNA NUCLEOTIDYLEXOTRANSFERASE; GLUTATHIONE; MALEIC ACID DIETHYL ESTER; MESSENGER RNA; PROTEIN BAX; PROTEIN BCL 2; URIDINE TRIPHOSPHATE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BAGG ALBINO MOUSE; CELL COUNT; CELL LOSS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GERM CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PREVALENCE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TESTIS CELL;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL SHAPE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MALE; MALEATES; MICE; MICE, INBRED BALB C; OXIDATIVE STRESS; RNA, MESSENGER; SPERMATOZOA; TESTIS;

ANIMALIA; MUS;

EID: 58149269440     PISSN: 10956670     EISSN: 10990461     Source Type: Journal    
DOI: 10.1002/jbt.20252     Document Type: Article

References (64)

1. Allan D J, Harmon B V, Roberts S A. Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat. Cell Prolif 1992; 25: 241-250.
2. Bartke A. Apoptosis of male germ cells, a generalized or a cell type-specific phenomenon. Endocrinology 1995; 136: 3-4.
3. Billig H, Furuta I, Rivier C, Tapanainen J, Parvinen M, Hseuh A J. Apoptosis in testis germ cells: Developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology 1995; 136: 5-12.
4. Shaha C. Modulators of spermatogenic cell survival. Soc Reprod Fertil 2007; 63: 173-186.
5. Blanchard K T, Allard E K, Boekelheide K. Fate of germ cells in 2, 5-hexanedione-induced testicular injury. Toxicol Appl Pharmacol 1996; 137: 141-148.
6. Richburg J H, Boekelheide K. Mono-(2-ethylhexyl)phthalate rapidly alters both Sertoli cell vimentin filaments and germ cell apoptosis in young rat testes. Toxicol Appl Pharmacol 1996; 137: 42-50.
7. Yoshinaga K, Nishikawa S, Ogawa M, Hayashi S, Kunisada T, Fujimoto T, Nishikawa S. Role of c-kit in mouse spermatogenesis: Identification of spermatogonia as a specific site of c-kit expression and function. Development 1991; 113: 689-699.
8. Russell L D, Alger L E, Nequin L G. Hormonal control of pubertal spermatogenesis. Endocrinology 1987; 120: 1615-1632.
9. Sinha Hikim A P, Wang C, Leung A, Swerdloff R S. Involvement of apoptosis in the induction of germ cell degeneration in adult rats after gonadotropin-releasing hormone antagonist treatment. Endocrinology 1995; 136: 2770-2775.
10. Miraglia S M, Hayashi H. Histomorphometry of immature rat testis after heating. J Morphol 1993; 217: 65-74.
11. Meistrich M L. Effects of chemotherapy and radiotherapy on spermatogenesis. Eur Urol 1993; 23: 136-141.
12. Nunez G, Clarke M F. The Bcl-2 family of proteins: Regulators of cell death and survival. Trends Cell Biol 1994; 4: 399-403.
13. Oltvai Z N, Milliman C L, Korsmeyer S J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74: 609-619.
14. Khaled A R, Kim K, Hofmeister R, Muegge K, Durum S K. Withdrawal of IL-7 induces Bax translocation from cytosol to mitochondria through a rise in intracellular pH. Proc Natl Acad Sci USA 1999; 96: 14476-14481.
15. Yamamoto C M, Sinha A P, Huynh P N, Shapiro B, Lue Y, Salameh W A, Wang C, Swerdloff R S. Redistribution of Bax is an early Step in an apoptotic pathway leading to germ cell death in rats, triggered by mild testicular hyperthermia. Biol Reprod 2000; 63: 1683-1690.
16. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: The calcium-apoptosis. Nat Rev Mol Cell Biol 2003; 4: 552-565.
17. Samanta L, Chainy G B. Comparison of hexachlorocyclohexane-induced oxidative stress in the testis of immature and adults rats. Comp Biochem Physiol C 1998; 118: 319-327.
18. Lucesoli F, Fraga C G. Oxidative stress in testes of rats subjected to chronic ion intoxication and γ-tocopherol supplementation. Toxicology 1999; 132: 179-186.
19. Pasqualotto F F, Sharma R K, Potts J M, Nelson D R, Thomas A J, Agarwal A. Seminal oxidative stress in patients with chronic prostatitis. Urology 2000; 55; 881-885.
20. Wellejus A, Bornholdt J, Vogel U B, Risom L, Wiger R, Loft S. Cell-specific oxidative DNA damage induced by estrogen in rat testicular cells in vitro. Toxicol Lett 2004; 150: 317-323.
21. Kaur P, Kalia S, Bansal M P. Effect of diethyl maleate induced oxidative stress on male reproductive activity in mice: Redox active enzymes and transcription factors expression. Mol Cell Biochem 2006; 291: 55-61.
22. Hissin P J, Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 1976; 74(1): 214-226.
23. Driver A S, Rao P, Kodavanti S, Mundy W R. Age-related changes in the reactive oxygen species production in rat brain homogenates. Neurotoxicol Teratol 2000; 22: 175-181.
24. Wills E D. Mechanisms of lipid peroxide formation in animal tissues. Biochem J 1966; 99(3): 667-676.
25. Leblond C P, Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann NY Acad Sci 1952; 55: 548-573.
26. Chew B P, Brown C M, Park J S, Mixter P F. Dietary lutein inhibits mouse mammary tumor growth by regulating angiogenesis and apoptosis. Anticancer Res 2003; 23(4): 3333-3339.
27. Levine B, Huang Q, Isaacs J T, Reed J C, Griffin D E, Hardwick J M. Conversion of lytic to persistent alpha virus infection by the Bcl-2 cellular oncogene. Nature 1993; 61: 739-742.
28. Yamada K, Takane-Gyotoku N, Yuan X, Ichikawa F, Inada C, Nonaka K. Mouse islet cell lysis mediated by interleukin-1-induced Fas. Diabetologia 1996; 39: 1306-1312.
29. Oakland E. A description of spermatogenesis in the mouse and its use in analysis of the cycle of seminiferous epithelium and germ cell renewal. Am J Anat 1956; 99: 391-413.
30. Johnson L, Petty C S, Neaves W B. Further quantification of human spermatogenesis: Germ cell loss during post-prophase of meiosis and its relationship to daily sperm production. Biol Reprod 1983; 29: 207-215.
31. Huckins C. The morphology and kinetics of spermatogonial degeneration in normal adult rats: An analysis using a simplified classification of the germinal epithelium. Anat Rec 1978; 190: 905-926.
32. Lee J, Richburg J H, Younkin S C, Boekelheide K. The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 1997; 138: 2081-2088.
33. Woolveridge I, Boer-Brouwer M, Taylor M F, Teerds K J, Wu FCW, Morris I D. Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: Changes in apoptosis-related genes. Biol Reprod 1999; 60: 461-470.
34. Nandi S, Banerjee P P, Zirkin B R. Germ cell apoptosis in the testes of Sprague Dawley rats following testosterone withdrawal by ethane 1, 2-dimethanesulfonate administration: Relationship to Fas? Biol Reprod 1999; 61: 70-75.
35. Dunkel L, Taskinen S, Hovatta O, Tilly J L, Wikstrom S. Germ cell apoptosis after treatment of cryptorchidism with human chorionic gonadotropin is associated with impaired reproductive function in the adult. J Clin Invest 1997; 100: 2341-2346.
36. Dunkel L, Hirvonen V, Erkkilä K. Clinical aspects of male germ cell apoptosis during testis development and spermatogenesis. Cell Death Differ 1997; 4: 171-179.
37. Knudson C M, Tung K S K, Tourtellotte W G, Brown GAJ, Korsmeyer S J. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 1995; 270: 96-99.
38. Print C G, Loveland K L, Gibson L, Meehan T, Stylianou A, Wreford N, Dekretser D, Metcalf D, Kontgen F, Adams J M, Cory S. Apoptosis regulator Bcl-W is essential for spermatogenesis but appears otherwise redundant. Proc Natl Acad Sci USA 1998; 95: 12424-12431.
39. Furuchi T, Masuko K, Nishimune Y, Obinata M, Matsui Y. Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia. Development 1996; 122: 1703-1709.
40. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P. An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J 1997; 16: 2262-2270.
41. Deneke S M, Fanburg B L. Regulation of cellular glutathione. Am J Physiol 1989; 257: L163-L173.
42. Klatt P, Lamas S. Regulation of protein function by S-glutathionylation in response to oxidative and nitrosative stress. Eur J Biochem 2000; 267: 4928-4944.
43. Turrens J F. Mitochondrial formation of reactive oxygen species. J Physiol (London) 2003; 552: 335-344.
44. Griffith O W. Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic Biol Med 1999; 27: 922-935.
45. Oldereid N B, Angelis P D, Wiger R, Clausen OPF. Expression of Bcl-2 family proteins and spontaneous apoptosis in normal human testis. Mol Hum Reprod 2001; 7: 403-408.
46. Celli A, Que F G, Gores G J, LaRusso N F. Glutathione depletion is associated with decreased Bcl-2 expression and increased apoptosis in cholangiocytes. Am J Physiol 1998; 275: G749-G757.
47. Merad-Boudia M, Nicole A, Santiard-Baron D, Saillé C, Ceballos-Picot I. Mitochondrial impairment as an early event in the process of apoptosis induced by glutathione depletion in neuronal cells: Relevance to Parkinson's disease. Biochem Pharmacol 1998; 56: 645-655.
48. Higuchi Y, Matsukawa S. Glutathione depletion induces giant DNA and high-molecular-weight DNA fragmentation associated with apoptosis through lipid peroxidation and protein kinase C activation in C6 glioma cells. Arch Biochem Biophys 1999; 363: 33-42.
49. Anderson C P, Tsai J M, Meek W E, Liu R M, Tang Y, Forman H J, Reynolds C P. Depletion of glutathione by buthionine sulfoximine is cytotoxic for human neuroblastoma cell lines via apoptosis. Exp Cell Res 1999; 246: 183-192.
50. Wright S C, Wang H, Wei Q S, Kinder D H, Larrick J W. Bcl-2-mediated resistance to apoptosis is associated with glutathione-induced inhibition of AP24 activation of nuclear DNA fragmentation. Cancer Res 1998; 58: 5570-5576.
51. Schnelldorfer T, Gansauge S, Gansauge F, Schlosser S, Beger H G, Nussler A K. Glutathione depletion causes cell growth inhibition and enhanced apoptosis in pancreatic cancer cells. Cancer 2000; 89: 1440-1447.
52. Ekshyyan O, Aw T Y. Decreased susceptibility of differentiated PC12 cells to oxidative challenge: Relationship to cellular redox status and expression of apoptotic protease activating factor-1. Cell Death Differ 2005; 12: 1066-1077.
53. Xia S, Rosen E M, Laterra J. Sensitization of glioma cells to Fas-dependent apoptosis by chemotherapy-induced oxidative stress. Cancer Res 2005; 65: 5248-5255.
54. Chandra J, Samali A, Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 2000; 29: 323-333.
55. Haidara K, Morel I, Abaléa V, Barré G, Denizeau F. Mechanism of tert-butylhydroperoxide induced apoptosis in rat hepatocytes: Involvement of mitochondria and endoplasmic reticulum. Biochim Biophys Acta 2002; 1542: 173-185.
56. Jungas T, Motta I, Duffieux F, Fanen P, Stoven V, Ojcius D M. Glutathione levels and BAX activation during apoptosis due to oxidative stress in cells expressing wild-type and mutant cystic fibrosis transmembrane conductance regulator. J Biol Chem 2002; 277: 27912-27913.
57. Ran Q, Liang H, Gu M, Qi W, Walter CA, Roberts L J, Herman B, Richardson A, Van Remmen H. Transgenic mice overexpressing glutathione peroxidase 4 are protected against oxidative stress-induced apoptosis. J Biol Chem 2004; 279: 55137-55146.
58. Higuchi Y, Matsukawa S. Glutathione depletion induces giant DNA and high-molecular-weight DNA fragmentation associated with apoptosis through lipid peroxidation and protein kinase C activation in C6 glioma cells. Arch Biochem Biophys 1999; 363: 33-42.
59. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 1997; 3(6): 614-620.
60. Lysiak J J, Nguyen Q A, Turner T T. Fluctuations in rat testicular interstitial oxygen tensions are linked to testicular vasomotion: Persistence after repair of torsion. Biol Reprod 2000; 63(5): 1383-1389.
61. Gross A, Yin X M, Wang K, Wei M C, Jockel J, Milliman C, Erdjument- Bromage H, Tempst P, Korsmeyer S J. Caspase cleaved bid targets mitochondria and is required for cytochrome c release, while bcl-xl prevents this release but not tumor necrosis factor-r1/fas death. J Biol Chem 1999; 274: 1156-1163.
62. Eskes R, Desagher S, Antonsson B, Martinou J C. Bid and induces the oligomerization and insertion of bax into the outer mitochondrial membrane. Mol Cell Biol 2000; 20: 929-935.
63. Edmund B, Rucker III Dierisseau P, Wagner KU, Garrett L, Boris AW, Flaws JA, Hennighausen L. Bcl-x and Bax regulate mouse primordial germ cell survival apoptosis during embryogenesis. Mol Endocrinol 200; 14(7): 1038.
64. Pawlowski J, Andrew S. Bax-induced apoptotic cell death. PNAS 2000; 97: 529-531.