Occult hepatitis C virus elicits mitochondrial oxidative stress in lymphocytes and triggers PI3-kinase-mediated DNA damage response

Free Radical Biology and Medicine

Volumn 51, Issue 9, 2011, Pages 1806-1814

  Bhargava, Arpit ^a,b   Raghuram, Gorantla V ^a,b   Pathak, Neelam ^a   Varshney, Subodh ^a   Jatawa, Suresh K ^a   Jain, Deepika ^a,b   Mishra, Pradyumna K ^a,b  

^a BHOPAL MEMORIAL HOSPITAL AND RESEARCH CENTRE   (India)

^b TATA MEMORIAL HOSPITAL   (India)

Author keywords

Apoptosis; Circulating nucleosomes; DNA repair; Free radicals; mtDNA; Translational research

Indexed keywords

ATM PROTEIN; ATR PROTEIN; DOUBLE STRANDED DNA; HISTONE H2AX; MITOCHONDRIAL DNA; MRE11 PROTEIN; NIBRIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN P53; RAD50 PROTEIN;

ADULT; APOPTOSIS; ARTICLE; CHROMATID ABERRATION; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME ACTIVITY; FEMALE; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; LYMPHOCYTE; LYMPHOCYTE PROLIFERATION; MAJOR CLINICAL STUDY; MALE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; NUCLEOSOME; OCCULT HEPATITIS C VIRUS INFECTION; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; VIRUS CELL INTERACTION;

ADULT; DNA DAMAGE; DNA, MITOCHONDRIAL; FEMALE; HEPATITIS C; HUMANS; LYMPHOCYTES; MALE; MITOCHONDRIA; OXIDATIVE STRESS; PHOSPHATIDYLINOSITOL 3-KINASES;

HEPATITIS C VIRUS;

EID: 80053614206     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.08.009     Document Type: Article

References (46)

1. L.B. Dustin, and C.M. Rice Flying under the radar: the immunobiology of hepatitis C Annu. Rev. Immunol. 25 2007 71 99 (Pubitemid 46697903)
2. N. Appel, T. Schaller, F. Penin, and R. Bartenschlager From structure to function: new insights into hepatitis C virus RNA replication J. Biol. Chem. 281 2006 9833 9836 (Pubitemid 43864513)
3. F. Penin, V. Brass, N. Appel, S. Ramboarina, R. Montserret, D. Ficheux, H.E. Blum, R. Bartenschlager, and D. Moradpour Structure and function of the membrane anchor domain of hepatitis C virus nonstructural protein 5A J. Biol. Chem. 279 2004 40835 40843 (Pubitemid 39287681)
4. C. Piccoli, R. Scrima, A. D'Aprile, M. Ripoli, L. Lecce, D. Boffoli, and N. Capitanio Mitochondrial dysfunction in hepatitis C virus infection Biochim. Biophys. Acta 1757 2006 1429 1437 (Pubitemid 44442124)
5. K. Machida, K.T. Cheng, C.K. Lai, K.S. Jeng, V.M. Sung, and M.M. Lai Hepatitis C virus triggers mitochondrial permeability transition with production of reactive oxygen species, leading to DNA damage and STAT3 activation J. Virol. 80 2006 7199 7207 (Pubitemid 44025216)
6. L. Deng, T. Adachi, K. Kitayama, Y. Bungyoku, S. Kitazawa, S. Ishido, I. Shoji, and H. Hotta Hepatitis C virus infection induces apoptosis through a Bax-triggered, mitochondrion-mediated, caspase 3-dependent pathway J. Virol. 82 2008 10375 10385 (Pubitemid 352691171)
7. K. Machida, G. McNamara, K.T. Cheng, J. Huang, C.H. Wang, L. Comai, J.H. Ou, and M.M. Lai Hepatitis C virus inhibits DNA damage repair through reactive oxygen and nitrogen species and by interfering with the ATM-NBS1/Mre11/Rad50 DNA repair pathway in monocytes and hepatocytes J. Immunol. 185 2010 6985 6998
8. C. Piccoli, G. Quarato, M. Ripoli, A. D'Aprile, R. Scrima, O. Cela, D. Boffoli, D. Moradpour, and N. Capitanio HCV infection induces mitochondrial bioenergetic unbalance: causes and effects Biochim. Biophys. Acta 1787 2009 539 546
9. T.N. Pham, D. King, S.A. Macparland, J.S. McGrath, S.B. Reddy, F.R. Bursey, and T.I. Michalak Hepatitis C virus replicates in the same immune cell subsets in chronic hepatitis C and occult infection Gastroenterology 134 2008 812 822 (Pubitemid 351312726)
10. V. Carreño Occult hepatitis C virus infection: a new form of hepatitis C World J. Gastroenterol. 12 2006 6922 6925 (Pubitemid 44834880)
11. V. Carreño, J. Bartolomé, I. Castillo, and J.A. Quiroga Does occult hepatitis C virus infection exist? J. Clin. Microbiol. 46 2008 3550
12. Z. Stamataki Hepatitis C infection of B lymphocytes: more tools to address pending questions Expert Rev. Anti Infect. Ther. 8 2010 977 980
13. P.K. Mishra, A. Bhargava, S. Khan, N. Pathak, R.P. Punde, and S. Varshney Prevalence of hepatitis C virus genotypes and impact of T helper cytokines in achieving sustained virological response during combination therapy: a study from central India Indian J. Med. Microbiol. 28 2010 358 362
14. M.W. Welker, and S. Zeuzem Occult hepatitis C: how convincing are the current data? Hepatology 49 2009 665 675
15. A. Bhargava, S. Khan, H. Panwar, N. Pathak, R.P. Punde, S. Varshney, and P.K. Mishra Occult hepatitis B virus infection with low viremia induces DNA damage, apoptosis and oxidative stress in peripheral blood lymphocytes Virus Res. 153 2010 143 150
16. A. Bhargava, R.P. Punde, S. Varshney, N. Pathak, and P.K. Mishra A novel FRET probe based approach for identification, quantification and characterization of occult HCV infections in patients with cryptogenic liver cirrhosis Indian J. Pathol. Microbiol. 54 2011 421 422
17. P.K. Mishra, G.V. Raghuram, H. Panwar, D. Jain, H. Pandey, and K.K. Maudar Mitochondrial oxidative stress elicits chromosomal instability after exposure to isocyanates in human kidney epithelial cells Free Radic. Res. 43 2009 718 728
18. Mishra, P.K.; Raghuram, G.V.; Bhargava, A.; Ahirwar, A.K.; Samarth, R.M.; Upadhyaya, R.; Jain, S.K.; Pathak, N. In vitro and in vivo evaluation of anticarcinogenic and cancer chemopreventive potential of a flavonoid-rich fraction from a traditional Indian herb Selaginella bryopteris. Br. J. Nutr. doi:10.1017/S0007114511001498; 2011.
19. G.V. Raghuram, N. Pathak, D. Jain, H. Panwar, H. Pandey, S.K. Jain, and P.K. Mishra Molecular mechanisms of isocyanate induced oncogenic transformation in ovarian epithelial cells Reprod. Toxicol. 30 2010 377 386
20. P. Rustin, D. Chretien, T. Bourgeron, B. Gérard, A. Rötig, J.M. Saudubray, and A. Munnich Biochemical and molecular investigations in respiratory chain deficiencies Clin. Chim. Acta 228 1994 35 51 (Pubitemid 24231224)
21. J. Xing, M. Chen, C.G. Wood, J. Lin, M.R. Spitz, J. Ma, C.I. Amos, P.G. Shields, N.L. Benowitz, J. Gu, M. de Andrade, G.E. Swan, and X. Wu Mitochondrial DNA content: its genetic heritability and association with renal cell carcinoma J. Natl. Cancer Inst. 100 2008 1104 1112
22. P.K. Mishra, V.R. Gorantla, N. Akhtar, P. Tamrakar, S.K. Jain, and K.K. Maudar Analysis of cellular response to isocyanate using N-succinimidyl N-methylcarbamate exposure in cultured mammalian cells Environ. Mol. Mutat. 50 2009 328 336
23. P.K. Mishra, S. Khan, A. Bhargava, H. Panwar, S. Banerjee, S.K. Jain, and K.K. Maudar Regulation of isocyanate-induced apoptosis, oxidative stress, and inflammation in cultured human neutrophils: isocyanate-induced neutrophils apoptosis Cell Biol. Toxicol. 26 2010 279 291
24. P.K. Mishra, H. Panwar, A. Bhargava, V.R. Gorantla, S.K. Jain, S. Banerjee, and K.K. Maudar Isocyanates induces DNA damage, apoptosis, oxidative stress, and inflammation in cultured human lymphocytes J. Biochem. Mol. Toxicol. 22 2008 429 440
25. D. Jain, N. Pathak, S. Khan, G.V. Raghuram, A. Bhargava, R.M. Samarth, and P.K. Mishra Evaluation of cytotoxicity and anti-carcinogenic potential of Mentha leaf extracts Int. J. Toxicol. 30 2011 225 236
26. A. Bhargava, R.P. Punde, N. Pathak, S. Dabadghao, P. Desikan, A. Jain, K.K. Maudar, and P.K. Mishra Status of inflammatory biomarkers in the population that survived the Bhopal gas tragedy: a study after two decades Ind. Health 48 2010 204 208
27. P.K. Mishra, S. Dabadghao, G.K. Modi, P. Desikan, A. Jain, I. Mittra, D. Gupta, C. Chauhan, S.K. Jain, and K.K. Maudar In utero exposure to methyl isocyanate in the Bhopal gas disaster: evidence of persisting hyperactivation of immune system two decades later Occup. Environ. Med. 66 2009 279
28. D. Mishra, P.K. Mishra, S. Dabadghao, V. Dubey, M. Nahar, and N.K. Jain Comparative evaluation of hepatitis B surface antigen-loaded elastic liposomes and ethosomes for human dendritic cell uptake and immune response Nanomedicine 6 2010 110 118
29. P.K. Mishra, A. Bhargava, G.V. Raghuram, S.K. Jatawa, N. Akhtar, S. Khan, A. Tiwari, and K.K. Maudar Induction of genomic instability in cultured human colon epithelial cells following exposure to isocyanates Cell Biol. Int. 33 2009 675 683
30. G.V. Raghuram, N. Pathak, D. Jain, H. Pandey, H. Panwar, S.K. Jain, S. Banerjee, and P.K. Mishra Molecular characterization of isocyanate-induced male germ-line genomic instability J. Environ. Pathol. Toxicol. Oncol. 29 2010 213 234
31. F. Farinati, R. Cardin, M. Bortolami, M. Guido, and M. Rugge Oxidative damage, pro-inflammatory cytokines, TGF-alpha and c-myc in chronic HCV-related hepatitis and cirrhosis World J. Gastroenterol. 12 2006 2065 2069
32. C.F. Canakci, Y. Cicek, and V. Canacki Reactive oxygen species and human inflammatory periodontal diseases Biochemistry (Moscow) 70 2005 619 628 (Pubitemid 41118160)
33. Y.H. Wei, and H.C. Lee Mitochondrial DNA mutations and oxidative stress in mitochondrial diseases Adv. Clin. Chem. 37 2003 83 128
34. R.W. Taylor, and D.M. Turnbull Mitochondrial DNA mutations in human disease Nat. Rev. Genet. 6 2005 389 402 (Pubitemid 40577182)
35. I. Manoli, S. Alesci, M.R. Blackman, Y.A. Su, O.M. Rennert, and G.P. Chrousos Mitochondria as key components of the stress response Trends Endocrinol. Metab. 18 2007 190 198 (Pubitemid 46970733)
36. R. Cardin, G. Saccoccio, F. Masutti, S. Bellentani, F. Farinati, and C. Tiribelli DNA oxidative damage in leukocytes correlates with the severity of HCV-related liver disease: validation in an open population study J. Hepatol. 34 2001 587 592 (Pubitemid 32328517)
37. C. Bolukbas, F.F. Bolukbas, A. Kocyigit, M. Aslan, S. Selek, M. Bitiren, and M. Ulukanligil Relationship between levels of DNA damage in lymphocytes and histopathological severity of chronic hepatitis C and various clinical forms of hepatitis Braz. J. Gastroenterol. Hepatol. 21 2006 610 616
38. Y. Ariumi, M. Kuroki, H. Dansako, K. Abe, M. Ikeda, T. Wakita, and N. Kato The DNA damage sensors ataxia-telangiectasia mutated kinase and checkpoint kinase 2 are required for hepatitis C virus RNA replication J. Virol. 82 2008 9639 9646
39. F.A. Derheimer, H.M. O'Hagan, H.M. Krueger, S. Hanasoge, M.T. Paulsen, and M. Ljungman RPA and ATR link transcriptional stress to p53 Proc. Natl. Acad. Sci. U. S. A. 104 2007 12778 12783 (Pubitemid 47255231)
40. L.J. Kuo, and L.X. Yang Gamma-H2AX-a novel biomarker for DNA double-strand breaks In Vivo 22 2008 305 309
41. T. Uziel, Y. Lerenthal, L. Moyal, Y. Andegeko, L. Mittelman, and Y. Shiloh Requirement of the MRN complex for ATM activation by DNA damage EMBO J. 22 2003 5612 5621 (Pubitemid 37279970)
42. S. Sarfraz, S. Hamid, S. Ali, W. Jafri, and A.A. Siddiqui Modulations of cell cycle checkpoints during HCV associated disease BMC Infect. Dis. 9 2009 125
43. I. Emerit, F. Serejo, and M. Carneiro de Moura Clastogenic factors in the plasma of patients with hepatitis C: their possible role at the origin of hepatocarcinoma Cancer Genet. Cytogenet. 179 2007 31 35 (Pubitemid 350018901)
44. F.H. Duong, V. Christen, S. Lin, and M.H. Heim Hepatitis C virus-induced up-regulation of protein phosphatase 2A inhibits histone modification and DNA damage repair Hepatology 51 2010 741 751
45. S. Pal, S.J. Polyak, N. Bano, W.C. Qiu, R.L. Carithers, M. Shuhart, D.R. Gretch, and A. Das Hepatitis C virus induces oxidative stress, DNA damage and modulates the DNA repair enzyme NEIL1 J. Gastroenterol. Hepatol. 25 2010 627 634
46. M.V. Ruchko, O.M. Gorodnya, A. Zuleta, V.M. Pastukh, and M.N. Gillespie The DNA glycosylase Ogg1 defends against oxidant-induced mtDNA damage and apoptosis in pulmonary artery endothelial cells Free Radic. Biol. Med. 250 2011 1107 1113