Activation of the ER stress gene gadd153 by hepatitis C virus sensitizes cells to oxidant injury

Virus Research

Volumn 126, Issue 1-2, 2007, Pages 128-138

  Ciccaglione, A R ^a   Marcantonio, C ^a   Tritarelli, E ^a   Equestre, M ^a   Vendittelli, F ^a   Costantino, A ^a   Geraci, A ^a   Rapicetta, M ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

ER; Gadd153; HCV; Oxidative stress; Replicon

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HYDROGEN PEROXIDE; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL DAMAGE; CELL DEATH; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE ACTIVATION; GENE EXPRESSION; GENE TARGETING; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; VIRUS REPLICATION;

CELL LINE; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENOME, VIRAL; HEAT-SHOCK PROTEINS; HEPACIVIRUS; HEPATITIS C; HUMANS; HYDROGEN PEROXIDE; MOLECULAR CHAPERONES; OXIDATIVE STRESS; PROMOTER REGIONS (GENETICS); REPLICON; TRANSCRIPTION FACTOR CHOP;

HEPATITIS C VIRUS;

EID: 34248209510     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2007.02.006     Document Type: Article

References (63)

1. Abdalla M.Y., Britigan B.E., Wen F., Icardi M., McCormick M.L., LaBrecque D.R., Voigt M., Brown K.E., and Schmidt W.N. Down-regulation of heme oxygenase-1 by hepatitis C virus infection in vivo and by the in vitro expression of hepatitis C core protein. J. Infect. Dis. 190 (2004) 1109-1118
2. Benali-Furet N.L., Chami M., Houel L., De Giorgi F., Vernejoul F., Lagorce D., Buscail L., Bartenschlager R., Ichas F., Rizzuto R., and Paterlini-Brechot P. Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion. Oncogene 24 (2005) 4921-4933
3. Boyce M., and Yuan J. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ. 13 (2006) 363-373
4. Browning J.D., and Horton J.D. Molecular mediators of hepatic steatosis and liver injury. J. Clin. Invest. 114 (2004) 147-152
5. Bruhat A., Jousse C., Carraro V., Reimold A.M., Ferrara M., and Fafournoux P. Amino acids control mammalian gene transcription: activating transcription factor 2 is essential for the amino acid responsiveness of the CHOP promoter. Mol. Cell. Biol. 20 (2000) 7192-7204
6. Chan S.W., and Egan P.A. Hepatitis C virus envelope proteins regulate CHOP via induction of the unfolded protein response. FASEB J. 19 (2005) 1510-1512
7. Ciccaglione A.R., Costantino A., Tritarelli E., Marcantonio C., Equestre M., Marziliano N., and Rapicetta M. Activation of endoplasmic reticulum stress response by hepatitis C virus proteins. Arch. Virol. 150 (2005) 1339-1356
8. De Franceschi L., Fattovich G., Turrini F., Ayi K., Brugnara C., Manzato F., Noventa F., Stanzial A.M., Solero P., and Corrocher R. Hemolytic anemia induced by ribavirin therapy in patients with chronic hepatitis C virus infection: role of membrane oxidative damage. Hepatology 31 (2000) 997-1004
9. De Maria N., Colantoni A., Fagiuoli S., Liu G.J., Rogers B.K., Farinati F., Van Thiel D.H., and Floyd R.A. Association between reactive oxygen species and disease activity in chronic hepatitis C. Free Radic. Biol. Med. 21 (1996) 291-295
10. Di Bisceglie A.M. Hepatitis C and hepatocellular carcinoma. Hepatology 26 (1997) 34S-38S
11. Dubuisson J., and Rice C.M. Hepatitis C virus glycoprotein folding: disulfide bond formation and association with calnexin. J. Virol. 70 (1996) 778-786
12. Eymin B., Dubrez L., Allouche M., and Solary E. Increased gadd153 messenger RNA level is associated with apoptosis in human leukemic cells treated with etoposide. Cancer Res. 57 (1997) 686-695
13. Farinati F., Cardin R., Degan P., De Maria N., Floyd R.A., Van Thiel D.H., and Naccarato R. Oxidative DNA damage in circulating leukocytes occurs as an early event in chronic HCV infection. Free Radic. Biol. Med. 27 (1999) 1284-1291
14. Finkel T. Oxygen radicals and signalling. Curr. Opin. Cell. Biol. 10 (1998) 248-253
15. Friedman A.D. GADD153/CHOP, a DNA damage-inducible protein, reduced CAAT/enhancer binding protein activities and increased apoptosis in 32D c13 myeloid cells. Cancer Res. 56 (1996) 3250-3256
16. Gale Jr. M. Effector genes of interferon action against hepatitis C virus. Hepatology 37 (2003) 975-978
17. Grakoui A., Wychowski C., Lin C., Feinstone S.M., and Rice C.M. Expression and identification of hepatitis C virus polyprotein cleavage products. J. Virol. 67 (1993) 1385-1395
18. Guyton K.Z., Xu Q., and Holbrook N.J. Induction of the mammalian stress response gene GADD153 by oxidative stress: role of AP-1 element. Biochem. J. 314 (1996) 547-554
19. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., and Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6 (2000) 1099-1108
20. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., Stojdl D.F., Bell J.C., Hettmann T., Leiden J.M., and Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11 (2003) 619-633
21. Hijikata M., Kato N., Ootsuyama Y., Nakagawa M., and Shimotohno K. Gene mapping of the putative structural region of the hepatitis C virus genome by in vitro processing analysis. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 5547-5551
22. Holbrook N.J., and Ikeyama S. Age-related decline in cellular response to oxidative stress: links to growth factor signalling pathways with common defects. Biochem. Pharmacol. 64 (2002) 999-1005
23. Hoofnagle J.H. Hepatitis C: the clinical spectrum of disease. Hepatology 26 (1997) 15S-20S
24. Hourigan L.F., Macdonald G.A., Purdie D., Whitehall V.H., Shorthouse C., Clouston A., and Powell E.E. Fibrosis in chronic hepatitis C correlates significantly with body mass index and steatosis. Hepatology 29 (1999) 1215-1219
25. Ikeda M., Yi M., Li K., and Lemon S.M. Selectable subgenomic and genome-length dicistronic RNAs derived from an infectious molecular clone of the HCV-N strain of hepatitis C virus replicate efficiently in cultured Huh7 cells. J. Virol. 76 (2002) 2997-3006
26. Ikeyama S., Kokkonen G., Martindale J.L., Wang X.T., Gorospe M., and Holbrook N.J. Effects of aging and calorie restriction of Fischer 344 rats on hepatocellular response to proliferative signals. Exp. Gerontol. 38 (2003) 431-439
27. Ikeyama S., Wang X.T., Li J., Podlutsky A., Martindale J.L., Kokkonen G., van Huizen R., Gorospe M., and Holbrook N.J. Expression of the pro-apoptotic gene gadd153/chop is elevated in liver with aging and sensitizes cells to oxidant injury. J. Biol. Chem. 278 (2003) 16726-16731
28. Kapadia S.B., and Chisari F.V. Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 2561-2566
29. Katze M.G., He Y., and Gale Jr. M. Viruses and interferon: a fight for supremacy. Nat. Rev. Immunol. 2 (2002) 675-687
30. Kaufman R.J. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13 (1999) 1211-1233
31. Larrea E., Beloqui O., Munoz-Navas M.A., Civeira M.P., and Prieto J. Superoxide dismutase in patients with chronic hepatitis C virus infection. Free Radic. Biol. Med. 24 (1998) 1235-1241
32. Li J., and Holbrook N.J. Elevated gadd153/chop expression and enhanced c-Jun N-terminal protein kinase activation sensitizes aged cells to ER stress. Exp. Gerontol. 39 (2004) 735-744
33. Liberman E., Fong Y.L., Selby M.J., Choo Q.L., Cousens L., Houghton M., and Yen T.S. Activation of the grp78 and grp94 promoters by hepatitis C virus E2 envelope protein. J. Virol. 73 (1999) 3718-3722
34. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
35. Lohmann V., Korner F., Koch J., Herian U., Theilmann L., and Bartenschlager R. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285 (1999) 110-113
36. Lonardo A., Adinolfi L.E., Loria P., Carulli N., Ruggiero G., and Day C.P. Steatosis and hepatitis C virus: mechanisms and significance for hepatic and extrahepatic disease. Gastroenterology 126 (2004) 586-597
37. Ma Y., Brewer J.W., Diehl J.A., and Hendershot L.M. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318 (2002) 1351-1365
38. Marshall A., Rushbrook S., Davies S.E., Morris L.S., Scott I.S., Vowler S.L., Coleman N., and Alexander G. Relation between hepatocyte G1 arrest, impaired hepatic regeneration, and fibrosis in chronic hepatitis C virus infection. Gastroenterology 128 (2005) 33-42
39. Martindale J.L., and Holbrook N.J. Cellular response to oxidative stress: signaling for suicide and survival. J. Cell. Physiol. 192 (2002) 1-15
40. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., and Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21 (2001) 1249-1259
41. Morbitzer M., and Herget T. Expression of gastrointestinal glutathione peroxidase is inversely correlated to the presence of hepatitis C virus subgenomic RNA in human liver cells. J. Biol. Chem. 280 (2005) 8831-8841
42. Morris J.A., Dorner A.J., Edwards C.A., Hendershot L.M., and Kaufman R.J. Immunoglobulin binding protein (BiP) function is required to protect cells from endoplasmic reticulum stress but is not required for the secretion of selective proteins. J. Biol. Chem. 272 (1997) 4327-4334
43. Mutlu-Turkoglu U., Ademoglu E., Turkoglu S., Badur S., Uysal M., and Toker G. The effects of interferon-alpha on serum lipid peroxidation and total thiol content in patients with chronic active hepatitis-C. Res. Commun. Mol. Pathol. Pharmacol. 96 (1997) 357-361
44. Okada T., Yoshida H., Akazawa R., Negishi M., and Mori K. Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem. J. 366 (2002) 585-594
45. Ong J.P., Younossi Z.M., Speer C., Olano A., Gramlich T., and Boparai N. Chronic hepatitis C and superimposed nonalcoholic fatty liver disease. Liver 21 (2001) 266-271
46. Pietschmann T., Lohmann V., Kaul A., Krieger N., Rinck G., Rutter G., Strand D., and Bartenschlager R. Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J. Virol. 76 (2002) 4008-4021
47. Pietschmann T., Lohmann V., Rutter G., Kurpanek K., and Bartenschlager R. Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J. Virol. 75 (2001) 1252-1264
48. Powell E.E., Jonsson J.R., and Cluston A.D. Steatosis: co-factor in other liver diseases. Hepatology 42 (2005) 5-13
49. Poynard T., Bedossa P., and Opolon P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet 349 (1997) 825-832
50. Qadri I., Iwahashi M., Capasso J.M., Hopken M.W., Flores S., Schaack J., and Simon F.R. Induced oxidative stress and activated expression of manganese superoxide dismutase during hepatitis C virus replication: role of JNK, p38 MAPK and AP-1. Biochem. J. 378 (2004) 919-928
51. Reed K.E., and Rice C.M. Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr. Top. Microbiol. Immunol. 242 (2000) 55-84
52. Ron D., and Habener J.F. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 6 (1992) 439-453
53. Scheuner D., Song B., McEwen E., Liu C., Laybutt R., Gillespie P., Saunders T., Bonner-Weir S., and Kaufman R.J. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7 (2001) 1165-1176
54. Scholle F., Li K., Bodola F., Ikeda M., Luxon B.A., and Lemon S.M. Virus-host cell interactions during hepatitis C virus RNA replication: impact of polyprotein expression on the cellular transcriptome and cell cycle association with viral RNA synthesis. J. Virol. 78 (2004) 1513-1524
55. Schwarz K.B. Oxidative stress during viral infection: a review. Free Radic. Biol. Med. 21 (1996) 641-649
56. Shen J., Chen X., Hendershot L., and Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3 (2002) 99-111
57. Stehbens W.E. Oxidative stress in viral hepatitis and AIDS. Exp. Mol. Pathol. 77 (2004) 121-132
58. Tardif K.D., Mori K., Kaufman R.J., and Siddiqui A. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J. Biol. Chem. 279 (2004) 17158-17164
59. Tardif K.D., Mori K., and Siddiqui A. Hepatitis C virus subgenomic replicons induces endoplasmic reticulum stress activating an intracellular signaling pathway. J. Virol. 76 (2002) 7453-7459
60. Tardif K.D., Waris G., and Siddiqui A. Hepatitis C virus, ER stress, and oxidative stress. Trends Microbiol. 13 (2005) 159-163
61. Ubeda M., Wang X.Z., Zinszner H., Wu I., Habener J.F., and Ron D. Stress-induced binding of the transcriptional factor CHOP to a novel DNA control element. Mol. Cell. Biol. 16 (1996) 1479-1489
62. Wang X.Z., Lawson B., Brewer J.W., Zinszner H., Sanjay A., Mi L.J., Boorstein R., Kreibich G., Hendershot L.M., and Ron D. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell. Biol. 16 (1996) 4273-4280
63. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., Stevens J.L., and Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12 (1998) 982-995