Mitochondrial decay is involved in BaP-induced cervical damage

Free Radical Biology and Medicine

Volumn 49, Issue 11, 2010, Pages 1735-1745

  Gao, Meili ^a   Long, Jiangang ^a   Li, Yongfei ^b   Shah, Walayat ^a,c   Fu, Ling ^a   Liu, Jiankang ^a   Wang, Yili ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b XI'AN TECHNOLOGICAL UNIVERSITY   (China)

^c KHYBER MEDICAL UNIVERSITY   (Pakistan)

Author keywords

Antioxidants; Benzo a pyrene; Cervix; Free radicals; Lipid peroxidation; Mitochondria; ROS

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; BENZO[A]PYRENE; BIOLOGICAL MARKER; CATALASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; MALATE DEHYDROGENASE; REACTIVE OXYGEN METABOLITE; RETINOL; SUCCINATE DEHYDROGENASE; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; LIPID PEROXIDATION; MEMBRANE POTENTIAL; METABOLITE; MITOCHONDRION; MORPHOLOGY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SERUM; UTERINE CERVIX DISEASE;

ANIMALS; APOPTOSIS; BENZO(A)PYRENE; CERVIX UTERI; FEMALE; MALONDIALDEHYDE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED ICR; MITOCHONDRIA; MUTAGENS; NECROSIS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; UTERINE CERVICAL DISEASES;

MUS;

EID: 78049405980     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.09.003     Document Type: Article

References (75)

1. Pan L.Q., Ren J., Liu J. Responses of antioxidant systems and LPO level to benzo(a)pyrene and benzo(k)fluoranthene in the haemolymph of the scallop Chlamys ferrari. Environ. Pollut. 2006, 141:443-451.
2. 3) acts by oxidative stress and potentiates benzo[a]pyrene genotoxicity. Mutat. Res. 2004, 563:117-129.
3. Bauer E., Guo Z., Ueng Y.F., Bell L.C., Zeldin D., Guengerich F.P. Oxidation of benzo[a]pyrene by recombinant human cytochrome P450 enzymes. Chem. Res. 1995, 8:136-142.
4. Yun C.H., Shimada T., Guengerich F.P. Role of human liver cytochrome P4502C and 3A enzymes in 3-hydroxylation of benzo[a]pyrene. Cancer Res. 1992, 52:1868-1874.
5. Melikian A.A., Sun P., Prokopczyk B., El-Bayoumy K., Hoffmann D., Wang X., Waggoner S. Identification of benzo[a]pyrene metabolites in cervical mucus and DNA adducts in cervical tissues in humans by gas chromatography mass spectrometry. Cancer Lett. 1999, 146:127-134.
6. Judge S., Jang Y.M., Smith A., Hagen T., Leeuwenburgh C. Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J. 2005, 19:419-421.
7. Korashy H.M., El-Kadi A.O. The role of aryl hydrocarbon receptor and the reactive oxygen species in the modulation of glutathione transferase by heavy metals in murine hepatoma cell lines. Chem. Biol. Interact. 2006, 162:237-248.
8. Cenini G., Sultana R., Memo M., Butterfield D.A. Effects of oxidative and nitrosative stress in brain on p53 proapoptotic protein in amnestic mild cognitive impairment and Alzheimer disease. Free Radic. Biol. Med. 2008, 45:81-85.
9. Vieira L.R., Sousa A., Frascoa M.F., Lima I., Morgado F., Guilhermino L. Acute effects of benzo[a]pyrene, anthracene and a fuel oil on biomarkers of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Sci. Total Environ. 2008, 395:87-100.
10. Kim H.S., Kwack S.J., Lee B.M. Lipid peroxidation, antioxidant enzymes, and benzo[a]pyrene-quinones in the blood of rats treated with benzo[a]pyrene. Chem. Biol. Interact. 2000, 127:139-150.
11. Dasgupta T., Hebbel R.P., Kaul D.K. Protective effect of arginine on oxidative stress in transgenic sickle mouse models. Free Radic. Biol. Med. 2006, 41:1771-1780.
12. Circu M.L., Aw T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 2010, 48:749-762.
13. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552:335-344.
14. MacMillan-Crow L.A., Crow J.P., Thompson J.A. Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 1998, 37:1613-1622.
15. Ballinger S.W., Patterson W.C., Yan C.-N., Doan R., Burow D.L., Young C.G., Yakes F.M., Van Houten B., Ballinger C.A., Freeman B.A., Runge M.S. Hydrogen peroxide and peroxynitrite induced mitochondrial DNA damage and dysfunction in vascular endothelial and smooth muscle cells. Circ. Res. 2000, 86:960-966.
16. Yan L.-J., Sohal R.S. Prevention of flight activity prolongs the life span of the housefly, Musca domestica, and attenuates the age-associated oxidative damage to specific mitochondrial proteins. Free Radic. Biol. Med. 2000, 29:1143-1150.
17. Mier-Cabrera J., Aburto-Soto T., Burrola-Méndez S., Jiménez-Zamudio L., Tolentino M.C., Casanueva E., Hernández-Guerrero C. Women with endometriosis improved their peripheral antioxidant markers after the application of a high antioxidant diet. Reprod. Biol. Endocrinol. 2009, 7:54-61.
18. Le Prell C.G., Hughes L.F., Miller J.M. Free radical scavengers, vitamins A, C, and E, plus magnesium reduces noise trauma. Free Radic. Biol. Med. 2007, 42:1454-1463.
19. Wang C., Liand J., Zhang C., Bi Y., Shi X., Shi Q. Effect of ascorbic acid and thiamine supplementation at different concentrations on lead toxicity in liver. Ann. Occup. Hyg. 2007, 51:563-569.
20. Chang C.K., Huang H.Y., Tseng H.F., Hsuuw Y.D., Tso T.K. Interaction of vitamin E and exercise training on oxidative stress and antioxidant enzyme activities in rat skeletal muscles. J. Nutr. Biochem. 2007, 18:39-45.
21. Bansal A.K., Bansal M., Soni G., Bhatnagar D. Protective role of vitamin E pre-treatment on N-nitrosodiethylamine induced oxidative stress in rat liver. Chem. Biol. Interact. 2005, 156:101-111.
22. Srivastava S., Natu S.M., Gupta A., Pal K.A., Singh U., Agarwal G.G., Singh U., Goel M.M., Srivastava A.N. Lipid peroxidation and antioxidants in different stages of cervical cancer: prognostic significance. Indian J. Cancer 2009, 46:297-302.
23. Sharma A., Rajappa M., Saxena A., Sharma M. Antioxidant status in advanced cervical cancer patients undergoing neoadjuvant chemoradiation. Br. J. Biomed. Sci. 2007, 64:23-27.
24. Amresh G., Rao C.V., Singh P.N. Antioxidant activity of Cissampelos pareira on benzo(a)pyrene-induced mucosal injury in mice. Nutr. Res. 2007, 27:625-632.
25. Knuckles M.E., Inyang F., Ramesh A. Acute and subchronic oral toxicities of benzo[a]pyrene in F-344 rats. Toxicol. Sci. 2001, 61:382-388.
26. Wu Y.Q., Wang C.G., Wang Y., Zhao Y., Chen Y.X., Zuo Z.H. Antioxidant responses to benzo[a]pyrene, tributyltin and their mixture in the spleen of Sebasticus marmoratus. J. Environ. Sci. 2007, 19:1129-1135.
27. Wright J.R., Colby H.D., Miles P.R. Cytosolic factors which affect microsomal lipid peroxidation in lung and liver. Arch. Biochem. Biophys. 1981, 206:296-304.
28. Marklund S., Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 1974, 47:469-474.
29. Aebi H. Catalase in vitro. Methods Enzymol. 1984, 105:121-126.
30. Anderson M.E. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol. 1985, 113:548-555.
31. Rotruck J.T., Pope A.L., Ganther H.E. Selenium: biochemical roles as a component of glutathione peroxidase. Science 1973, 179:588-590.
32. Habig W.H., Jakoby W.B. Assays for differentiation of glutathione S-transferase. Methods Enzymol. 1981, 77:398-405.
33. Nishikimi M., Appaji N., Yagi K. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem. Biophys. Res. Commun. 1972, 46:849-854.
34. 2 production by macrophages and neutrophils with homovanillic acid and horseradish peroxidase. J. Immunol. Methods 1983, 63:347-357.
35. Gutteridge J.M. Thiobarbituric acid-reactivity following iron-dependent free-radical damage to amino acids and carbohydrates. FEBS Lett. 1981, 128:343-346.
36. Bortolotti A., Lucchini G., Barzago M.M., Stellari F., Bonati M. Simultaneous determination of retinol, alpha-tocopherol and retinyl palmitate in plasma of premature newborns by reversed-phase high performance liquid chromatography. J. Chromatogr. 1993, 617:313-317.
37. Cadenas S., Rojas C., Méndez J., Herrero A., Barja G. Vitamin E decreases urine lipid peroxidation products in young healthy human volunteers under normal conditions. Pharmacol. Toxicol. 1996, 79:247-253.
38. Baker H., Frank O., De Angelis B., Feingod S. Plasma tocopherol in man at various times after ingesting free or acetylated tocopherol. Nutr. Rep. Int. 1980, 21:531-536.
39. Guha M., Kumar S., Choubey V., Maity P., Bandyopadhyay U. Apoptosis in liver during malaria: role of oxidative stress and implication of mitochondrial pathway. FASEB J. 2006, 20:1224-1226.
40. Rustin P., Chretien D., Bourgeron T., Gerard B., Rotig A., Saudubray J.M., Munnich A. Biochemical and molecular investigations in respiratory chain deficiencies. Clin. Chim. Acta 1994, 228:35-51.
41. Turner L.V., Manchester K.L. Effects of denervation on the activities of some tricarboxylic acid-cycle-associated dehydrogenases and adenine-metabolizing enzymes in rat diaphragm muscle. Biochem. J. 1972, 128:803-809.
42. Richter C. Oxidative stress, mitochondria, and apoptosis. Restor. Neurol. Neurosci. 1998, 12:59-62.
43. Murata M., Ohta N., Sakurai S. The role of aldose reductase in sugar cataract formation: aldose reductase plays a key role in lens epithelial cell death (apoptosis). Chem. Biol. Interact. 2001, 130-132:617-625.
44. Duzguner V., Kaya S. Effect of zinc on the lipid peroxidation and the antioxidant defense systems of the alloxan-induced diabetic rabbits. Free Radic. Biol. Med. 2007, 42:1481-1486.
45. Wang C., Zhao Y., Zheng R., Ding X., Wei W., Zuo Z., Chen Y. Effects of tributyltin, benzo[a]pyrene, and their mixture on antioxidant defense systems in Sebastiscus marmoratus. Ecotoxicol. Environ. Saf. 2006, 65:381-387.
46. International Agency for Research on Cancer Polynuclear aromatic compounds. Environmental and Experimental Data 1983, vol. 32:33-224. WHO, Geneva.
47. Hasspieler B.M., Behar J.V., Di Giulio R.T. Glutathione dependent defense in channel catfish (Ictalurus punctatus) and brown bullhead (Ameiurus nebulosus). Ecotoxicol. Environ. Saf. 1994, 28:82-90.
48. DeLeve L.D., Wang X., Kuhlenkamp J.F., Kaplowitz N. Toxicity of azathioprine and monocrotaline in murine sinusoidal endothelial cells and hepatocytes: the role of glutathione and relevance to hepatic venoocclusive disease. Hepatology 1996, 23:589-599.
49. Sharma A., Rajappa M., Saxena A., Sharma M. Antioxidant status in advanced cervical cancer patients undergoing neoadjuvant chemoradiation. Br. J. Biomed. Sci. 2007, 64:23-27.
50. Beevi S.S., Rasheed M.H., Geetha A. Evidence of oxidative and nitrosative stress in patients with cervical squamous cell carcinoma. Clin. Chim. Acta 2007, 375:119-123.
51. Chiu H.J., Fischman D.A., Hammerling U. Vitamin A depletion causes oxidative stress, mitochondrial dysfunction, and PARP-1-dependent energy deprivation. FASEB J. 2008, 22:3878-3887.
52. Frei B., Lawson S. Vitamin C and cancer revisited. Proc. Natl Acad. Sci. USA 2008, 105:11037-11038.
53. Kamaraj S., Vinodhkumar R., Anandakumar P., Jagan S., Ramakrishnan G., Devaki T. The effects of quercetin on antioxidant status and tumor markers in the lung and serum of mice treated with benzo(a)pyrene. Biol. Pharm. Bull. 2007, 30:2268-2273.
54. Shvedova A.A., Kisin E.R., Murray A.R., Gorelik O., Arepalli S., Castranova V., Young S.H., Gao F., Tyurina Y.Y., Oury T.D., Kagan V.E. Vitamin E deficiency enhances pulmonary inflammatory response and oxidative stress induced by single walled carbon nanotubes in C57BL/6 mice. Toxicol. Appl. Pharmacol. 2007, 221:339-348.
55. Lim Y., Vasu V.T., Valacchi G., Leonard S., Aung H.H., Schock B.C., Kenyon N.J., Li C.S., Traber M.G., Cross C.E. Severe vitamin E deficiency modulates airway allergic inflammatory responses in the murine asthma model. Free Radic. Res. 2008, 42:387-396.
56. Oommen S., Vasu V.T., Leonard S.W., Traber M.G., Cross C.E., Gohil K. Genome wide responses of murine lungs to dietary α-tocopherol. Free Radic. Res. 2007, 41:98-109.
57. Manju V., Kalaivani Sailaja J., Nalini N. Circulating lipid peroxidation and antioxidant status in cervical cancer patients: a case-control study. Clin. Biochem. 2002, 35:621-625.
58. Logan D.L. The mitochondrial compartment. J. Exp. Bot. 2006, 57:1225-1243.
59. Norberg E., Gogvadze V., Vakifahmetoglu H., Orrenius S., Zhivotovsky B. Oxidative modification sensitizes mitochondrial apoptosis-inducing factor to calpain-mediated processing. Free Radic. Biol. Med. 2010, 48:791-797.
60. Bonnard C., Durand A., Peyrol S., Chanseaume E., Chauvin M.A., Morio B., Vidal H., Rieusset J. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J. Clin. Invest. 2008, 118:789-800.
61. Venkatraman M., Konga D., Peramiyan R., Ganapathy E., Dhanapal S. Reduction of mitochondrial oxidative damage and improved mitochondrial efficiency by administration of crocetin against benzo[a]pyrene induced experimental animals. Biol. Pharm. Bull. 2008, 31:1639-1645.
62. Tatone C., Carbone M.C., Falone S., Aimola P., Giardinelli A., Caserta D., Marci R., Pandolfi A., Ragnelli A.M., Amicarelli F. Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol. Hum. Reprod. 2006, 12:655-660.
63. Kim J.Y., Chung J.Y., Park J.E., Lee S.G., Kim Y.J., Cha M.S., Han M.S., Lee H.J., Yoo Y.H., Kim J.M. Benzo[a]pyrene induces apoptosis in RL95-2 human endometrial cancer cells by cytochrome P450 1A1 activation. Endocrinology 2007, 148:5112-5122.
64. Xiong Y., Singh I.N., Hall E.D. Tempol protection of spinal cord mitochondria from peroxynitrite-induced oxidative damage. Free Radic. Res. 2009, 43:604-612.
65. Kitchin K.T. Recent advances in arsenic carcinogenesis: modes of action, animal model systems, and methylated arsenic metabolites. Toxicol. Appl. Pharmacol. 2001, 172:249-261.
66. Sharma A., Neekhra A., Gramajo A.L., Patil J., Chwa M., Kuppermann B.D., Kenney M.C. Effects of benzo(e)pyrene, a toxic component of cigarette smoke, on human retinal pigment epithelial cells in vitro. Invest. Ophthalmol. Visual Sci. 2008, 49:5111-5117.
67. Kim J.S., He L., Lemasters J.J. Mitochondrial permeability transition: a common pathway to necrosis and apoptosis. Biochem. Biophys. Res. Commun. 2003, 304:463-470.
68. Zamzami N., Kroemer G. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell Biol. 2001, 2:67-71.
69. Nakagawa T., et al. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005, 434:652-658.
70. Iskander K., Gaikwad A., Paquet M., Long D.J., Brayton C., Barrios R., Jaiswal A.K. Lower induction of p53 and decreased apoptosis in NQO1-null mice lead to increased sensitivity to chemical-induced skin carcinogenesis. Cancer Res. 2005, 65:2054-2058.
71. 3) enhances benzo[a]pyrene genotoxicity in endotracheally treated rat, as determined by comet assay. Mutat. Res. 2003, 538:19-29.
72. Alam S., Conway M.J., Chen H.S., Meyers C. The cigarette smoke carcinogen benzo[a]pyrene enhances human papillomavirus synthesis. J. Virol. 2008, 82:1053-1058.
73. Liu H., Weisman D., Ye Y., Cui B., Huang Y., Colón-Carmona A., Wang Z. An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana. Plant Sci. 2009, 176:375-382.
74. Annas A., Brittebo E., Hellman B. Evaluation of benzo(a)pyrene-induced DNA damage in human endothelial cells using alkaline single cell gel electrophoresis. Mutat. Res. 2000, 471:145-155.
75. Garry S., Nesslany F., Aliouat E., Haguenoer J.M., Marzin D. Assessment of genotoxic effect of benzo[a]pyrene in endotracheally treated rat using the comet assay. Mutat. Res. 2003, 534:33-43.