Aroclor 1254 induced oxidative stress and mitochondria mediated apoptosis in adult rat sperm in vitro

Environmental Toxicology and Pharmacology

Volumn 36, Issue 2, 2013, Pages 274-283

  Aly, Hamdy A A ^a,b  

^a KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^b Al Azhar University   (Egypt)

Author keywords

Apoptosis; Aroclor 1254; Oxidative stress; Sperm

Indexed keywords

ADENOSINE TRIPHOSPHATE; AROCLOR 1254; CARBONYL DERIVATIVE; CASPASE 3; CATALASE; CYTOCHROME C; DNA; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; SUPEROXIDE DISMUTASE;

ACROSOME REACTION; ADULT ANIMAL; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DNA INTEGRITY; ENZYME ACTIVATION; GENETIC PARAMETERS; IN VITRO STUDY; LIPID PEROXIDATION; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; SPERMATOZOON MOTILITY; TOXICITY TESTING;

APOPTOSIS; AROCLOR 1254; OXIDATIVE STRESS; SPERM;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; CASPASE 3; CATALASE; CELL SURVIVAL; CHLORODIPHENYL (54% CHLORINE); CYTOCHROMES C; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; LIPID PEROXIDATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OXIDATIVE STRESS; PROTEIN CARBONYLATION; RATS; RATS, WISTAR; SPERM MOTILITY; SPERMATOZOA; SUPEROXIDE DISMUTASE; TIME FACTORS;

EID: 84878150668     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2013.04.006     Document Type: Article

References (95)

1. Agarwal A., Said T.M. Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum. Reprod. Update 2003, 9:331-345.
2. Aly H.A., Domènech O. Cytotoxicity and mitochondrial dysfunction of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in isolated rat hepatocytes. Toxicol. Lett. 2009, 191:79-87.
3. Aly H.A., Domènech O., Abdel-Naim A.B. Aroclor 1254 impairs spermatogenesis and induces oxidative stress in rat testicular mitochondria. Food Chem. Toxicol. 2009, 47:1733-1738.
4. Antonsson B. Bax and other pro-apoptotic Bcl-2 family "killer-proteins" and their victim, the mitochondrion. Cell Tissue Res. 2001, 306:347-361.
5. Auger J., Mesbah M., Huber C., Dadoune J.P. Aniline blue staining as a marker of sperm chromatin defects associated with different semen characteristics discriminates between proven fertile and suspected infertile men. Int. J. Androl. 1990, 13:452-462.
6. Bai J.P., Shi Y.L. Inhibition of Ca(2+) channels in mouse spermatogenic cells by male antifertility compounds from Tripterygium wilfordii Hook. f. Contraception 2002, 65:441-445.
7. Baumber J., Ball B.A., Gravance C.G., Medina V., Davies-Morel M.C. The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity, mitochondrial membrane potential, and membrane lipid peroxidation. J. Androl. 2000, 21:895-902.
8. Bedford J.M. Significance of the need for sperm capacitation before fertilization in eutherian mammals. Biol. Rep. 1983, 28:108-120.
9. Ben Abdallah F., Fetoui H., Zribi N., Fakfakh F., Ammar-Keskes L. Antioxidant supplementations in vitro improve ratsperm parameters and enhance antioxidant enzyme activities against dimethoate-induced sperm damages. Andrologia 2012, 44:272-279.
10. Berlett B.S., Stadtman E.R. Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 1997, 272:20313-20316.
11. 2+-induced inhibition of substrate oxidation. Biochim. Biophys. Acta 1999, 1453:41-48.
12. Bray T.M., Taylor C.G. Tissue glutathione, nutrition, and oxidative stress. Can. J. Physiol. Pharmacol. 1993, 71:746-751.
13. Brevini T.A., Zanetto S.B., Cillo F. Effects of endocrine disruptors on developmental and reproductive functions. Curr. Drug Targets Immune Endocr. Metabol. Disord. 2005, 5:1-10.
14. Bustamante-Marín X., Quiroga C., Lavandero S., Reyes J.G., Moreno R.D. Apoptosis, necrosis and autophagy are influenced by metabolic energy sources in cultured rat spermatocytes. Apoptosis 2012, 17:539-550.
15. Carlberg I., Mannervik B.J. Purification and characterization of the flavo enzyme glutathione reductase from rat liver. J. Biochem. 1985, 250:5474-5480.
16. Chakraborti T., Das S., Mondal M., Roychoudhury S., Chakraborti S. Oxidant, mitochondria and calcium: an overview. Cell. Signal. 1999, 11:77-85.
17. Chandrappa S., Kavitha C.V., Shahabuddin M.S., Vinaya K., Ananda Kumar C.S., Ranganatha S.R., Raghavan S.C., Rangappa K.S. Synthesis of 2-(5-((5-(4- chlorophenyl)furan-2-yl)methylene)-4-oxo-2-thioxothiazoli-din-3-yl) acetic acid derivatives and evaluation of their cytotoxicity and induction of apoptosis in human leukemia cells. Bioorg. Med. Chem. 2009, 17:2576-2584.
18. Chen H., Cangello D., Benson S., Folmer J., Zhu H., Trush M.A., Zirkin B.R. Age-related increase in mitochondrial superoxide generation in the testosterone producing cells of Brown Norway rat testes: relationship to reduced steroidogenic function?. Exp. Gerontol. 2001, 36:1361-1373.
19. Cheng L., Kellogg E.W., Packer L. Photoin activation of catalase. Photochem. Photobiol. 1981, 34:125-129.
20. Claiborne A. Catalase activity. CRC Handbook of Methods For Oxygen Radical Research 1985, 283-284. CRC Press, Boca Raton, FL. R. Greenwald (Ed.).
21. Cocuzza M., Sikka S.C., Athayde K.S., Agarwal A. Clinical relevance of oxidative stress and sperm chromatin damage in male infertility: an evidence based analysis. Int. Braz. J. Urol. 2007, 33:603-621.
22. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 1999, 341(Pt 2):233-249.
23. Darszon A., Beltran C., Felix R., Nishigaki T., Trevino C.L. Ion transport in sperm signaling. Dev. Biol. 2001, 240:1-14.
24. Das J., Ghosh J., Manna P., Sinha M., Sil P.C. Taurine protects rat testes against NaAsO(2)-induced oxidative stress and apoptosis via mitochondrial dependent and independent pathways. Toxicol. Lett. 2009, 187:201-210.
25. de Catalfo G.E., Gomez Dumm I.N. Lipid dismetabolism in Leydig and Sertoli cells isolated from streptozotocin-diabetic rats. Int. J. Biochem. Cell Biol. 1998, 30:1001-1010.
26. de Lamirande E., Gagnon C. Reactive oxygen species and human spermatozoa. II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. J. Androl. 1992, 13:379-386.
27. de Lamirande E., Jiang H., Zini A., Kodama H., Gagnon C. Reactive oxygen species and sperm physiology. Rev. Reprod. 1997, 2:48-54.
28. Earnshaw W.C., Martins L.M., Kaufmann S.H. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 1999, 68:383-424.
29. Eliasson R. Supravital staining of human spermatozoa. Fertil. Steril. 1977, 28:1257.
30. Erenpreiss J., Bars J., Lipatnikova V., Erenpreisa J., Zalkalns J. Comprative study of cytochemical tests for sperm chromatin integrity. J. Androl. 2001, 22:45-53.
31. Erenpreiss J., Spano M., Erenpreisa J., Bungum M., Giwercman A. Sperm chromatin structure and male fertility: biological and clinical aspects. Asian J. Androl. 2006, 8:11-29.
32. Erickson M.D. Analytical Chemistry of PCBs 1997, 35-59. Lewis Publisher, Boca Raton. second ed.
33. 2+ flux inhibitors on acrosome reaction of hamster spermatozoa. J. Androl. 2007, 28:561-564.
34. Gangadharan B., Murugan M.A., Mathur P.P. Effect of methoxychlor on antioxidant system of goat epididymal sperm in vitro. Asian J. Androl. 2001, 3:285-288.
35. Gao H.B., Tong M.H., Hu Y.Q., You H.Y., Guo Q.S., Ge R.S., Hardy M.P. Mechanisms of glucocorticoid-induced Leydig cell apoptosis. Mol. Cell. Endocrinol. 2003, 199:153-163.
36. + ATPase in primary cortical cultures. Neurosci. Res. 2004, 50:299-306.
37. Halliwell B., Gutterige J.M.C. Free Radicals in Biology and Medicine 2001, Oxford University Press, New York.
38. Hong H., Liu G.Q. Protection against hydrogen peroxide-induced cytotoxicity in PC12 cells by scutellarin. Life Sci. 2004, 74:2959-2973.
39. Hong Z.F., Lin J.M., Zhong X.Y., Li Y., Zhou J.H., Xu W., Peng J. Qianliening capsule () inhibits human prostate cell growth via induction of mitochondrion-dependent cell apoptosis. Chinese J. Integr. Med. 2012, 18:824-830.
40. Isabella D.D., Rossi R., Giustarini D., Milzani A., Colombo R. Protein carbonyl group as biomarkersof oxidative stress. Clin. Chem. Acta 2003, 329:23-38.
41. Jorgensen N., Andersen A.G., Eustache F., Irvine D.S., Suominen J., Petersen J.H., Andersen A.N., Auger J., Cawood E.H., Horte A., Jensen T.K., Jouannet P., Keiding N., Vierula M., Toppari J., Skakkebaek N.E. Regional differences in semen quality in Europe. Hum. Reprod. 2001, 16:1012-1019.
42. Jung K., Henke W. Developmental changes of antioxidant enzymes in kidney and liver from rats. Free Radic. Biol. Med. 1996, 20:613-617.
43. Kao S.H., Chao H.T., Chen H.W., Hwang T.I., Liao T.L., Wei Y.H. Increase of oxidative stress in human sperm with lower motility. Fertil. Steril. 2008, 89:1183-1190.
44. Kasahara E., Sato E.F., Miyoshi M., Konaka R., Hiramoto K., Sasaki J., Tokuda M., Nakano Y., Inoue M. Role of oxidative stress in germ cell apoptosis induced by di(2-ethylhexyl)phthalate. Biochem. J. 2002, 365:456-849.
45. Kasahara E., Sato E.F., Miyoshi M., Konaka R., Hiramoto K., Sasaki J., Tokuda M., Nakano Y., Inoue M. Role of oxidative stress in germ cell apoptosisinduced by di(2-ethylhexyl)phthalate. Biochem. J. 2002, 365:849-856.
46. Kheradmand A., Dezfoulian O., Alirezaei M., Rasoulian B. Ghrelin modulates testicular germ cells apoptosis and proliferation in adult normal rats. Biochem. Biophys. Res. Commun. 2012, 419:299-304.
47. Kimbrough R.D. Polychlorinated biphenyls (PCBs) and human health: an update. Crit. Rev. Toxicol. 1995, 25:133-163.
48. Krishnamoorthy G., Murugesan P., Muthuvel R., Gunadharini D.N., Vijayababu M.R., Arunkumar A., Venkataraman P., Aruldhas M.M., Arunakaran J. Effect of Aroclor 1254 on Sertoli cellular antioxidant system, androgen binding protein and lactate in adult rat in vitro. Toxicology 2005, 212:195-205.
49. Krishnamoorthy G., Venkataraman P., Arunkumar A., Vignesh R.C., Aruldhas M., Arunakaran M.J. Ameliorative effect of vitamins (alpha-tocopherol and ascorbic acid) on PCB (Aroclor 1254) induced oxidative stress in rat epididymal sperm. Reprod. Toxicol. 2007, 23:239-245.
50. Lakpour N., Kharrazi H., Akhondi M.A., et al. The relationship between oxidative stress and sperm damage in normozoospermic men and men with abnormal sperm parameters. TUMJ 2008, 65:11-19.
51. Levine R.L., Garland D., Oliver C.N., Amici A., Climent I., Lenz A.G., Ahn B.W., Shaltiel S., Stadtman E.R. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990, 186:464-478.
52. Li S.F., Liu H.X., Zhang Y.B., Yan Y.C., Li Y.P. The protective effects of alpha-ketoacids against oxidative stress on ratspermatozoain vitro. Asian J. Androl. 2010, 12:247-256.
53. Li S.F., Liu H.X., Zhang Y.B., Yan Y.C., Li Y.P. The protective effects of α-ketoacids against oxidative stress on rat spermatozoa in vitro. Asian J. Androl. 2010, 12:247-256.
54. Linder R.E., Strader L.F., McElroy W.K. Measurement of epididymal sperm motility as a test variable in the rat. Bull. Environ. Contam. Toxicol. 1986, 36:317-324.
55. Lolis D., Georgiou I., Syrrou M., Zikopoulos K., Konstantelli M., Messinis I. Chromomycin A3-staining as an indicator of protamine deficiency and fertilization. Int. J. Androl. 1996, 19:23-27.
56. Marklund S., Marklund G. Involvement of superoxide anion radical in antioxidation of pyrogallol and a constituent assay for superoxide dismutase. Eur. J. Biochem. 1974, 47:469-474.
57. 2 or ultraviolet B light. Arch. Dermatol. Res. 1998, 290:113-118.
58. Mohamad N., Gutiérrez A., Núñez M., Cocca C., Martín G., Cricco G., Medina V., Rivera E., Bergoc R. Mitochondrial apoptotic pathways. Biocell 2005, 29:149-161.
59. Mohandas J., Marshall J.J., Duggin G.G., Horvath J.S., Tiller D.J. Low activities of glutathione-related enzymes as factors in the genesis of urinary bladder. Cancer Res. 1984, 44:5086-5091.
60. Moron M.S., Depierre J.W., Mannervik B. Levels of GSH, GR and GST activities in rat lung and liver. Biochim. Biophys. Acta 1979, 582:67-78.
61. Murugesan P., Balaganesh M., Balasubramanian K., Arunakaran J. Effects of polychlorinated biphenyl (Aroclor 1254) on steroidogenesis and antioxidant system in cultured adult rat Leydig cells. J. Endocrinol. 2007, 192:325-338.
62. Murugesan P., Kanagaraj P., Yuvaraj S., Balasubramanian K., Aruldhas M.M., Arunakaran J. The inhibitory effects of polychlorinated biphenyl (Aroclor 1254) on Leydig cell LH receptors, steroidogenic enzymes, and antioxidant enzymes in adult rats. Reprod. Toxicol. 2005, 20:117-126.
63. Murugesan P., Muthusamy T., Balasubramanian K., Arunakaran J. Polychlorinated biphenyl (Aroclor 1254) inhibits testosterone biosynthesis and antioxidant enzymes in cultured rat Leydig cells. Reprod. Toxicol. 2008, 25:447-454.
64. Murugesan P., Senthil kumar J., Balasubramanian K., Aruldhas M.M., Arunakaran J. Impact of polychlorinated biphenyl Aroclor 1254 on testicular antioxidant system in adult rats. Hum. Exp. Toxicol. 2005, 24:61-66.
65. Nessel C.S., Gallo M.A. Dioxins and Related Compounds. Environmental Toxicants: Human Exposure and their Health Effects 1994, 163-182. Van Nostrand-Reinhold, New York. M. Lippmann (Ed.).
66. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
67. Paoli D., Gallo M., Rizzo F., Baldi E., Francavilla S., Lenzi A., Lombardo F., Gandini L. Mitochondrial membrane potential profile and its correlation with increasing sperm motility. Fertil. Steril. 2011, 95:2315-2319.
68. Pflieger-Bruss S., Schuppe H.C., Schill W.B. The male reproductive system and its susceptibility to endocrine disrupting chemicals. Andrologia 2004, 36:337-345.
69. 2 production by chemically elicited peritoneal macrophages-induced by multiple nonphagocytic stimuli. Cell. Immunol. 1981, 59:301-318.
70. Purohit S.B., Laloraya M., Kumar G.P. Acrosome reaction inducers impose alterations in repulsive strain and hydration barrier in human sperm membranes. Biochem. Mol. Biol. Int. 1998, 45:227-235.
71. Qiang H., Jiang M.S., Lin J.Y., He W.M. Influence of enterococci on human sperm membrane in vitro. Asian J. Androl. 2007, 9:77-81.
72. Rao M.V., Gangadharan B. Antioxidative potential of melatonin against mercury induced intoxication in spermatozoain vitro. Toxicol. In Vitro 2008, 22:935-942.
73. Rigobello M.P., Scutari G., Friso A., Barzon E., Artusi S., Bindoli A. Mitochondrial permeability transition and release of cytochrome c induced by retinoic acids. Biochem. Pharmacol. 1999, 58:665-670.
74. Robertson J.D., Orrenius S. Molecular mechanisms of apoptosis induced bycytotoxic chemicals. Crit. Rev. Toxicol. 2000, 30:609-627.
75. Safe S.H. Polychlorinated biphenyls (PCBs). Environmental impact, biochemical and toxic responses and implications for risk assessment. Crit. Rev. Toxicol. 1994, 24:87-149.
76. Said T.M., Agarwal A., Sharma R.K., Thomas A.J., Sikka S.C. Impact of sperm morphology on DNA damage caused by oxidative stress induced by betanicotinamide adenine dinucleotide phosphate. Fertil. Steril. 2005, 83:95-103.
77. Sheweita S.A., Tilmisany A.M., Al-Sawaf H. Mechanisms ofmale infertility: role of antioxidants. Curr. Drug Metab. 2005, 6:495-501.
78. Shi Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol. Cell 2002, 9:459-470.
79. Shi Y., Song Y., Wang Y., Wang Y., Liang X., Hu Y., Yu H., Guan X., Cheng J., Yang K. β-Benzene hexachloride induces apoptosis of rat Sertoli cells through generation of reactive oxygen species and activation of JNKs and FasL. Environ. Toxicol. 2011, 26:124-135.
80. Shrilatha B., Muralidhara Occurrence of oxidative impairments, response of antioxidant defences and associated biochemical perturbations in male reproductive milieu in the Streptozotocin-diabetic rat. Int. J. Androl. 2007, 30:508-518.
81. Sies H. Glutathione and its role in cellular functions. Free Radic. Biol. Med. 1999, 27:916-921.
82. Talebi A.R., Khalili M.A., Hossaini A. Assessment of nuclear DNA integrity of epididymal spermatozoa following experimental chronic spinal cord injury in the rat. Int. J. Androl. 2007, 30:163-169.
83. Tang X.L., Yang X.Y., Jung H.J., Kim S.Y., Jung S.Y., Choi D.Y., Park W.C., Park H. Asiatic acid induces colon cancer cell growth inhibition and apoptosisthrough mitochondrial death cascade. Biol. Pharm. Bull. 2009, 32:1399-1405.
84. Tremellon K. Oxidative stress and male infertility - a clinical perspective. Hum. Reprod. Update 2008, 14:243-258.
85. Tso W.W., Lee C.S. Effect of Gossypol on boar spermatozoa in vitro. Arch Androl. 1981, 7:85-88.
86. Uguz C., Varisli O., Agca C., Agca Y. Effects of nonylphenol on motility and subcellular elements of epididymal rat sperm. Reprod. Toxicol. 2009, 28:542-549.
87. Vidaeff A.C., Sever L.E. In utero exposure to environmental estrogens and male reproductive health: a systematic review of biological and epidemiologic evidence. Reprod. Toxicol. 2005, 20:5-20.
88. Wassarman P.M. Contribution of mouse egg zona pellucida glycoproteins to gamete recognition during fertilization. J. Cell. Physiol. 2005, 204:388-391.
89. Wu J.H., Sun Z.Y., Cao L. In vitro effects of epristeride on sperm in rats, dogs and man. Arch. Androl. 2006, 52:191-195.
90. Wyrobek A.J., Gordon L.A., Burkhart J.G., Francis M.W., Kapp R.W., Letz G., Malling H.V., Topham J.C., Whorton M.D. An evaluation of the mouse sperm morphology test and other sperm tests in nonhuman mammals. A report of the U.S. Environmental Protection Agency Gene-Tox Program. Mutat. Res. 1983, 115:1-72.
91. Yan Y., Bian J.C., Zhong L.X., Zhang Y., Sun Y., Liu Z.P. Oxidative stress and apoptotic changes of rat cerebral cortical neurons exposed to cadmium in vitro. Biomed. Environ. Sci. 2012, 25:172-181.
92. Yanagimachi R. Mammalian fertilization. The Physiology of Reproduction 2004, 189-317. Raven Press, New York. E. Knobill, J.D. Neill (Eds.).
93. Yao B., Yi N., Zhou S., Ouyang W., Xu H., Ge Y., Cui Y., Xia X. The effect of induced anti-follicle-stimulating hormone autoantibody on serum hormone level and apoptosis in rattestis. Life Sci. 2012, 91:83-88.
94. Zhang S., Zhang Y., Zhuang Y., Wang J., Ye J., Zhang S., Wu J., Yu K., Han Y. Matrine induces apoptosis in human acute myeloid leukemia cells via the mitochondrial pathway and Akt inactivation. PLoS ONE 2012, 7:e46853.
95. Zhao Q., Cao X.H., Zeng B., Wang C.L., Yan L., Xu C.J. Musca domestica larvalectin induces apoptosis in BEL-7402 cells through a mitochondria-mediated reactive oxygen species way. Biol. Pharm. Bull. 2010, 33:1274-1278.