HCV NS4B induces apoptosis through the mitochondrial death pathway

Virus Research

Volumn 169, Issue 1, 2012, Pages 1-7

  Zhao, Peng ^a   Han, Tao ^a   Guo, Jin Jing ^a   Zhu, Sheng Li ^a   Wang, Jun ^a   Ao, Fang ^a   Jing, Ming Zhen ^a   She, Ying Long ^a   Wu, Zheng Hui ^a   Ye, Lin Bai ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Apoptosis; Cytochrome c; Hepatitis C virus; Mitochondrial death pathway; NS4B

Indexed keywords

4 [5 (4 METHYL 1 PIPERAZINYL)[2,5' BI 1H BENZIMIDAZOL] 2' YL]PHENOL; ACTIN; BETA ACTIN; CASPASE 3; CASPASE 7; CASPASE 9; CYTOCHROME C; DNA FRAGMENT; GLUCOSE REGULATED PROTEIN 78; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GREEN FLUORESCENT PROTEIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; LIPOCORTIN 5; MESSENGER RNA; MITOCHONDRIAL PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NONSTRUCTURAL PROTEIN 4B; PROTEIN TIM23; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME RELEASE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MITOCHONDRIAL DEATH PATHWAY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; RNA REPLICATION; RNA SPLICING; STAINING;

APOPTOSIS; CASPASE 3; CASPASE 7; CASPASE 9; CELL LINE; CYTOCHROMES C; HEPACIVIRUS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; POLY(ADP-RIBOSE) POLYMERASES; PROTEOLYSIS; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE FACTORS;

HEPATITIS C VIRUS;

EID: 84867201509     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2012.04.006     Document Type: Article

References (46)

1. Bantel H., Lugering A., Poremba C., Lugering N., Held J., Domschke W., Schulze-Osthoff K. Caspase activation correlates with the degree of inflammatory liver injury in chronic hepatitis C virus infection. Hepatology 2001, 34(4 Pt 1):758-767.
2. Bantel H., Schulze-Osthoff K. Apoptosis in hepatitis C virus infection. Cell Death and Differentiation 2003, 10(Suppl. 1):S48-S58.
3. Berg C.P., Schlosser S.F., Neukirchen D.K., Papadakis C., Gregor M., Wesselborg S., Stein G.M. Hepatitis C virus core protein induces apoptosis-like caspase independent cell death. Virology Journal 2009, 6:213.
4. Chayama K., Hayes C.N. Hepatitis C virus: how genetic variability affects pathobiology of disease. Journal of Gastroenterology and Hepatology 2011, 26(Suppl. 1):83-95.
5. Chiou H.-L., Hsieh Y.-S., Hsieh M.-R., Chen T.-Y. HCV E2 may induce apoptosis of Huh-7 cells via a mitochondrial-related caspase pathway. Biochemical and Biophysical Research Communications 2006, 345(1):453-458.
6. Chou A.H., Tsai H.F., Wu Y.Y., Hu C.Y., Hwang L.H., Hsu P.I., Hsu P.N. Hepatitis C virus core protein modulates TRAIL-mediated apoptosis by enhancing Bid cleavage and activation of mitochondria apoptosis signaling pathway. Journal of Immunology 2005, 174(4):2160-2166.
7. Chung Y.L., Sheu M.L., Yen S.H. Hepatitis C virus NS5A as a potential viral Bcl-2 homologue interacts with Bax and inhibits apoptosis in hepatocellular carcinoma. International Journal of Cancer 2003, 107(1):65-73.
8. Ciccaglione A.R., Marcantonio C., Costantino A., Equestre M., Rapicetta M. Expression of HCV E1 protein in baculovirus-infected cells: effects on cell viability and apoptosis induction. Intervirology 2003, 46(2):121-126.
9. Ciccaglione A.R., Marcantonio C., Tritarelli E., Equestre M., Magurano F., Costantino A., Nicoletti L., Rapicetta M. The transmembrane domain of hepatitis C virus E1 glycoprotein induces cell death. Virus Research 2004, 104(1):1-9.
10. Deng L., Adachi T., Kitayama K., Bungyoku Y., Kitazawa S., Ishido S., Shoji I., Hotta H. Hepatitis C virus infection induces apoptosis through a Bax-triggered, mitochondrion-mediated, caspase 3-dependent pathway. Journal of Virology 2008, 82(21):10375-10385.
11. Elazar M., Liu P., Rice C.M., Glenn J.S. An N-terminal amphipathic helix in hepatitis C virus (HCV) NS4B mediates membrane association, correct localization of replication complex proteins, and HCV RNA replication. Journal of Virology 2004, 78(20):11393-11400.
12. Erdtmann L., Franck N., Lerat H., Le Seyec J., Gilot D., Cannie I., Gripon P., Hibner U., Guguen-Guillouzo C. The hepatitis C virus NS2 protein is an inhibitor of CIDE-B-induced apoptosis. Journal of Biological Chemistry 2003, 278(20):18256-18264.
13. Fischer R., Baumert T., Blum H.E. Hepatitis C virus infection and apoptosis. World Journal of Gastroenterology 2007, 13(36):4865-4872.
14. Hügle T. The hepatitis C virus nonstructural protein 4B is an integral endoplasmic reticulum membrane protein. Virology 2001, 284(1):70-81.
15. Hayashi T., Rizzuto R., Hajnoczky G., Su T.-P. MAM: more than just a housekeeper. Trends in Cell Biology 2009, 19(2):81-88.
16. Jones D.M., Patel A.H., Targett-Adams P., McLauchlan J. The hepatitis C virus NS4B protein can trans-complement viral RNA replication and modulates production of infectious virus. Journal of Virology 2009, 83(5):2163-2177.
17. Kountouras J., Zavos C., Chatzopoulos D. Apoptosis in hepatitis C. Journal of Viral Hepatitis 2003, 10(5):335-342.
18. Kumar S. Caspase function in programmed cell death. Cell Death and Differentiation 2007, 14(1):32-43.
19. Lan K.H., Sheu M.L., Hwang S.J., Yen S.H., Chen S.Y., Wu J.C., Wang Y.J., Kato N., Omata M., Chang F.Y., Lee S.D. HCV NS5A interacts with p53 and inhibits p53-mediated apoptosis. Oncogene 2002, 21(31):4801-4811.
20. Lee S.K., Park S.O., Joe C.O., Kim Y.S. Interaction of HCV core protein with 14-3-3epsilon protein releases Bax to activate apoptosis. Biochemical and Biophysical Research Communications 2007, 352(3):756-762.
21. Lindenbach B.D., Rice C.M. Unravelling hepatitis C virus replication from genome to function. Nature 2005, 436(7053):933-938.
22. Lundin M., Monne M., Widell A., Von Heijne G., Persson M.A. Topology of the membrane-associated hepatitis C virus protein NS4B. Journal of Virology 2003, 77(9):5428-5438.
23. Marusawa H., Hijikata M., Chiba T., Shimotohno K. Hepatitis C virus core protein inhibits Fas- and tumor necrosis factor alpha-mediated apoptosis via NF-kappaB activation. Journal of Virology 1999, 73(6):4713-4720.
24. McConkey D.J., Zhivotovsky B., Orrenius S. Apoptosis-molecular mechanisms and biomedical implications. Molecular Aspects of Medicine 1996, 17(1):1-110.
25. Nomura-Takigawa Y., Nagano-Fujii M., Deng L., Kitazawa S., Ishido S., Sada K., Hotta H. Non-structural protein 4A of Hepatitis C virus accumulates on mitochondria and renders the cells prone to undergoing mitochondria-mediated apoptosis. Journal of General Virology 2006, 87(Pt 7):1935-1945.
26. Okada M., Smith N.I., Palonpon A.F., Endo H., Kawata S., Sodeoka M., Fujita K. Label-free Raman observation of cytochrome c dynamics during apoptosis. Proceedings of the National Academy of Sciences of the United States of America 2012, 109(1):28-32.
27. Ploss A., Rice C.M. Towards a small animal model for hepatitis C. EMBO Reports 2009, 10(11):1220-1227.
28. Prikhod'ko E.A., Prikhod'ko G.G., Siegel R.M., Thompson P., Major M.E., Cohen J.I. The NS3 protein of hepatitis C virus induces caspase-8-mediated apoptosis independent of its protease or helicase activities. Virology 2004, 329(1):53-67.
29. Ray R.B., Meyer K., Steele R., Shrivastava A., Aggarwal B.B., Ray R. Inhibition of tumor necrosis factor (TNF-alpha)-mediated apoptosis by hepatitis C virus core protein. Journal of Biological Chemistry 1998, 273(4):2256-2259.
30. Raynal P., Pollard H.B. Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochimica et Biophysica Acta 1994, 1197(1):63-93.
31. Saito K., Meyer K., Warner R., Basu A., Ray R.B., Ray R. Hepatitis C virus core protein inhibits tumor necrosis factor alpha-mediated apoptosis by a protective effect involving cellular FLICE inhibitory protein. Journal of Virology 2006, 80(9):4372-4379.
32. Sheridan C., Martin S.J. Mitochondrial fission/fusion dynamics and apoptosis. Mitochondrion 2010, 10(6):640-648.
33. Siavoshian S., Abraham J.D., Thumann C., Kieny M.P., Schuster C. Hepatitis C virus core, NS3, NS5A, NS5B proteins induce apoptosis in mature dendritic cells. Journal of Medical Virology 2005, 75(3):402-411.
34. Suzuki T., Aizaki H., Murakami K., Shoji I., Wakita T. Molecular biology of hepatitis C virus. Journal of Gastroenterology 2007, 42(6):411-423.
35. Tait S.W., Green D.R. Mitochondria and cell death: outer membrane permeabilization and beyond. Nature Reviews Molecular Cell Biology 2010, 11(9):621-632.
36. Tanaka M., Nagano-Fujii M., Deng L., Ishido S., Sada K., Hotta H. Single-point mutations of hepatitis C virus NS3 that impair p53 interaction and anti-apoptotic activity of NS3. Biochemical and Biophysical Research Communications 2006, 340(3):792-799.
37. Tardif K.D., Mori K., Kaufman R.J., Siddiqui A. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. Journal of Biological Chemistry 2004, 279(17):17158-17164.
38. Tewari M., Quan L.T., O'Rourke K., Desnoyers S., Zeng Z., Beidler D.R., Poirier G.G., Salvesen G.S., Dixit V.M. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly (ADP-ribose) polymerase. Cell 1995, 81(5):801-809.
39. Thoren F., Romero A., Lindh M., Dahlgren C., Hellstrand K. A hepatitis C virus-encoded, nonstructural protein (NS3) triggers dysfunction and apoptosis in lymphocytes: role of NADPH oxidase-derived oxygen radicals. Journal of Leukocyte Biology 2004, 76(6):1180-1186.
40. Valva P., De Matteo E., Galoppo M.C., Gismondi M.I., Preciado M.V. Apoptosis markers related to pathogenesis of pediatric chronic hepatitis C virus infection: M30 mirrors the severity of steatosis. Journal of Medical Virology 2010, 82(6):949-957.
41. Verfaillie T., Garg A.D., Agostinis P. Targeting ER stress induced apoptosis and inflammation in cancer. Cancer Letters 2010.
42. Wang J., Tong W., Zhang X., Chen L., Yi Z., Pan T., Hu Y., Xiang L., Yuan Z. Hepatitis C virus non-structural protein NS5A interacts with FKBP38 and inhibits apoptosis in Huh7 hepatoma cells. FEBS Letters 2006, 580(18):4392-4400.
43. Yoshida H., Matsui T., Yamamoto A., Okada T., Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001, 107(7):881-891.
44. Yoshida H., Okada T., Haze K., Yanagi H., Yura T., Negishi M., Mori K. Endoplasmic reticulum stress-induced formation of transcription factor complex ERSF including NF-Y (CBF) and activating transcription factors 6alpha and 6beta that activates the mammalian unfolded protein response. Molecular and Cellular Biology 2001, 21(4):1239-1248.
45. Zekri A.R., Bahnassy A.A., Hafez M.M., Hassan Z.K., Kamel M., Loutfy S.A., Sherif G.M., El-Zayadi A.R., Daoud S.S. Characterization of chronic HCV infection-induced apoptosis. Comparative Hepatology 2011, 10(1):4.
46. Zhu N., Khoshnan A., Schneider R., Matsumoto M., Dennert G., Ware C., Lai M.M. Hepatitis C virus core protein binds to the cytoplasmic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis. Journal of Virology 1998, 72(5):3691-3697.