Proteasome- and ethanol-dependent regulation of HCV-infection pathogenesis

Biomolecules

Volumn 4, Issue 4, 2014, Pages 885-896

  Osna, Natalia A ^a,b   Ganesan, Murali ^a,b   Donohue, Terrence M ^a,b  

^a VA NEBRASKA WESTERN IOWA HEALTH CARE SYSTEM   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Antigen presentation; Ethanol; Hepatitis C virus; Interferon sensitive genes; PA28; Proteasome; Ubiquitylation

Indexed keywords

PROTEASOME; SOFOSBUVIR; ALCOHOL; HLA ANTIGEN CLASS 1; INTERFERON; VIRUS PROTEIN;

ENZYME ACTIVITY; GENE EXPRESSION; HEPATITIS C; HUMAN; IMMUNE RESPONSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UBIQUITINATION; VIRAL CLEARANCE; VIRUS ENTRY; VIRUS REPLICATION; ADAPTIVE IMMUNITY; ALCOHOLISM; ANTIGEN PRESENTING CELL; DRUG EFFECTS; GENETICS; HEPACIVIRUS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; LIVER CELL; METABOLISM; PATHOGENICITY; PHYSIOLOGY;

ADAPTIVE IMMUNITY; ALCOHOLISM; ANTIGEN-PRESENTING CELLS; ETHANOL; HEPACIVIRUS; HEPATOCYTES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERONS; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; VIRAL PROTEINS;

EID: 84964313835     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom4040885     Document Type: Review

References (67)

1. Armstrong, G.L.; Wasley, A.; Simard, E.P.; McQuillan, G.M.; Kuhnert, W.L.; Alter, M.J. The prevalence of hepatitis C virus infection in the united states, 1999 through 2002. Ann. Intern. Med. 2006, 144, 705-714.
2. Mohd Hanafiah, K.; Groeger, J.; Flaxman, A.D.; Wiersma, S.T. Global epidemiology of hepatitis C virus infection: New estimates of age-specific antibody to HCV seroprevalence. Hepatology 2013, 57, 1333-1342.
3. Gastaminza, P.; Cheng, G.; Wieland, S.; Zhong, J.; Liao, W.; Chisari, F.V. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J. Virol. 2008, 82, 2120-2129.
4. Bartenschlager, R.; Lohmann, V.; Penin, F. The molecular and structural basis of advanced antiviral therapy for hepatitis C virus infection. Nat. Rev. Microbiol. 2013, 11, 482-496.
5. Otani, K.; Korenaga, M.; Beard, M.R.; Li, K.; Qian, T.; Showalter, L.A.; Singh, A.K.; Wang, T.; Weinman, S.A. Hepatitis C virus core protein, cytochrome P450 2E1, and alcohol produce combined mitochondrial injury and cytotoxicity in hepatoma cells. Gastroenterology 2005, 128, 96-107.
6. Seronello, S.; Sheikh, M.Y.; Choi, J. Redox regulation of hepatitis C in nonalcoholic and alcoholic liver. Free Radic. Biol. Med. 2007, 43, 869-882.
7. Osna, N.; McVicker, B.; Poluektova, L.; Ganesan, M.; Kharbanda, K. Mode of oral ethanol feeding affects liver oxidative stress levels and methylation status: Study on NS5A-transgenic mice. Int. J. Biochem. Res. Rev. 2014, 4, 344-357.
8. Hohn, T.J.; Grune, T. The proteasome and the degradation of oxidized proteins: Part III-redox regulation of the proteasomal system. Redox Biol. 2014, 2, 388-394.
9. Niforou, K.; Cheimonidou, C.; Trougakos, I.P. Molecular chaperones and proteostasis regulation during redox imbalance. Redox Biol. 2014, 2, 323-332.
10. Nishizawa-Yokoi, A.; Tainaka, H.; Yoshida, E.; Tamoi, M.; Yabuta, Y.; Shigeoka, S. The 26S proteasome function and Hsp90 activity involved in the regulation of HsfA2 expression in response to oxidative stress. Plant Cell Physiol. 2010, 51, 486-496.
11. Breusing, N.; Grune, T. Regulation of proteasome-mediated protein degradation during oxidative stress and aging. Biol. Chem. 2008, 389, 203-209.
12. Osna, N.A.; Bardag-Gorce, F.; White, R.L.; Weinman, S.A.; Donohue, T.M., Jr.; Kharbanda, K.K. Ethanol and hepatitis C virus suppress peptide-MHC class I presentation in hepatocytes by altering proteasome function. Alcohol. Clin. Exp. Res. 2012, 36, 2028-2035.
13. Osna, N.A.; Haorah, J.; Krutik, V.M.; Donohue, T.M., Jr. Peroxynitrite alters the catalytic activity of rodent liver proteasome in vitro and in vivo. Hepatology 2004, 40, 574-582.
14. Groettrup, M.; Standera, S.; Stohwasser, R.; Kloetzel, P.M. The subunits MECL-1 and LMP2 are mutually required for incorporation into the 20S proteasome. Proc. Natl. Acad. Sci. USA 1997, 94, 8970-8975.
15. Heink, S.; Ludwig, D.; Kloetzel, P.M.; Kruger, E. IFN-gamma-induced immune adaptation of the proteasome system is an accelerated and transient response. Proc. Natl. Acad. Sci. USA 2005, 102, 9241-9246.
16. Seifert, U.; Kruger, E. Remodelling of the ubiquitin-proteasome system in response to interferons. Biochem. Soc. Trans. 2008, 36, 879-884.
17. Guillaume, B.; Chapiro, J.; Stroobant, V.; Colau, D.; van Holle, B.; Parvizi, G.; Bousquet-Dubouch, M.P.; Theate, I.; Parmentier, N.; van den Eynde, B.J. Two abundant proteasome subtypes that uniquely process some antigens presented by HLA class I molecules. Proc. Natl. Acad. Sci. USA 2010, 107, 18599-18604.
18. Osna, N.A.; Clemens, D.L.; Donohue, T.M., Jr. Interferon gamma enhances proteasome activity in recombinant Hep G2 cells that express cytochrome P4502E1: Modulation by ethanol. Biochem. Pharmacol. 2003, 66, 697-710.
19. Pickering, A.M.; Davies, K.J. Differential roles of proteasome and immunoproteasome regulators Pa28alphabeta, Pa28gamma and Pa200 in the degradation of oxidized proteins. Arch. Biochem. Biophys. 2012, 523, 181-190.
20. Pickering, A.M.; Vojtovich, L.; Tower, J.; Davies, K.J.A. Oxidative stress adaptation with acute, chronic, and repeated stress. Free Radic. Biol. Med. 2013, 55, 109-118.
21. Korenaga, M.; Okuda, M.; Otani, K.; Wang, T.; Li, Y.; Weinman, S.A. Mitochondrial dysfunction in hepatitis C. J. Clin. Gastroenterol. 2005, 39, S162-S166.
22. Fujinaga, H.; Tsutsumi, T.; Yotsuyanagi, H.; Moriya, K.; Koike, K. Hepatocarcinogenesis in hepatitis C: HCV shrewdly exacerbates oxidative stress by modulating both production and scavenging of reactive oxygen species. Oncology 2011, 81, 11-17.
23. Paracha, U.Z.; Fatima, K.; Alqahtani, M.; Chaudhary, A.; Abuzenadah, A.; Damanhouri, G.; Qadri, I. Oxidative stress and hepatitis C virus. Virol. J. 2013, 10, 251.
24. Burdette, D.; Olivarez, M.; Waris, G. Activation of transcription factor Nrf2 by hepatitis C virus induces the cell-survival pathway. J. Gen. Virol. 2010, 91, 681-690.
25. Osna, N.A.; White, R.L.; Krutik, V.M.; Wang, T.; Weinman, S.A.; Donohue, T.M., Jr. Proteasome activation by hepatitis C core protein is reversed by ethanol-induced oxidative stress. Gastroenterology 2008, 134, 2144-2152.
26. Pavio, N.; Taylor, D.R.; Lai, M.M. Detection of a novel unglycosylated form of hepatitis C virus E2 envelope protein that is located in the cytosol and interacts with PKR. J. Virol. 2002, 76, 1265-1272.
27. Franck, N.; le Seyec, J.; Guguen-Guillouzo, C.; Erdtmann, L. Hepatitis C virus NS2 protein is phosphorylated by the protein kinase CK2 and targeted for degradation to the proteasome. J. Virol. 2005, 79, 2700-2708.
28. Gao, L.; Tu, H.; Shi, S.T.; Lee, K.J.; Asanaka, M.; Hwang, S.B.; Lai, M.M. Interaction with a ubiquitin-like protein enhances the ubiquitination and degradation of hepatitis C virus RNA-dependent RNA polymerase. J. Virol. 2003, 77, 4149-4159.
29. Hou, W.; Tian, Q.; Zheng, J.; Bonkovsky, H.L. Zinc mesoporphyrin induces rapid proteasomal degradation of hepatitis C nonstructural 5A protein in human hepatoma cells. Gastroenterology 2010, 138, 1909-1919.
30. Kim, M.J.; Yoo, J.Y. Inhibition of hepatitis C virus replication by IFN-mediated isgylation of HCV-NS5A. J. Immunol. 2010, 185, 4311-4318.
31. Haqshenas, G. The P7 protein of hepatitis C virus is degraded via the proteasome-dependent pathway. Virus Res. 2013, 176, 211-215.
32. Hundt, J.; Li, Z.; Liu, Q. Post-translational modifications of hepatitis C viral proteins and their biological significance. World J. Gastroenterol. 2013, 19, 8929-8939.
33. Nitahara-Kasahara, Y.; Fukasawa, M.; Shinkai-Ouchi, F.; Sato, S.; Suzuki, T.; Murakami, K.; Wakita, T.; Hanada, K.; Miyamura, T.; Nishijima, M. Cellular vimentin content regulates the protein level of hepatitis C virus core protein and the hepatitis C virus production in cultured cells. Virology 2009, 383, 319-327.
34. Tripathi, L.P.; Kambara, H.; Moriishi, K.; Morita, E.; Abe, T.; Mori, Y.; Chen, Y.A.; Matsuura, Y.; Mizuguchi, K. Proteomic analysis of hepatitis C virus (HCV) core protein transfection and host regulator Pa28gamma knockout in HCV pathogenesis: A network-based study. J. Proteome Res. 2012, 11, 3664-3679.
35. Shoji, I. Roles of the two distinct proteasome pathways in hepatitis C virus infection. World J. Virol. 2012, 1, 44-50.
36. Shirakura, M.; Murakami, K.; Ichimura, T.; Suzuki, R.; Shimoji, T.; Fukuda, K.; Abe, K.; Sato, S.; Fukasawa, M.; Yamakawa, Y.; et al. E6AP ubiquitin ligase mediates ubiquitylation and degradation of hepatitis C virus core protein. J. Virol. 2007, 81, 1174-1185.
37. Suzuki, R.; Tamura, K.; Li, J.; Ishii, K.; Matsuura, Y.; Miyamura, T.; Suzuki, T. Ubiquitin-mediated degradation of hepatitis C virus core protein is regulated by processing at its carboxyl terminus. Virology 2001, 280, 301-309.
38. Moriishi, K.; Shoji, I.; Mori, Y.; Suzuki, R.; Suzuki, T.; Kataoka, C.; Matsuura, Y. Involvement of Pa28gamma in the propagation of hepatitis C virus. Hepatology 2010, 52, 411-420.
39. Moriishi, K.; Mochizuki, R.; Moriya, K.; Miyamoto, H.; Mori, Y.; Abe, T.; Murata, S.; Tanaka, K.; Miyamura, T.; Suzuki, T.; et al. Critical role of Pa28gamma in hepatitis C virus-associated steatogenesis and hepatocarcinogenesis. Proc. Natl. Acad. Sci. USA 2007, 104, 1661-1666.
40. Moriishi, K.; Okabayashi, T.; Nakai, K.; Moriya, K.; Koike, K.; Murata, S.; Chiba, T.; Tanaka, K.; Suzuki, R.; Suzuki, T.; et al. Proteasome activator Pa28gamma-dependent nuclear retention and degradation of hepatitis C virus core protein. J. Virol. 2003, 77, 10237-10249.
41. Kondo, M.; Moriishi, K.; Wada, H.; Noda, T.; Marubashi, S.; Wakasa, K.; Matsuura, Y.; Doki, Y.; Mori, M.; Nagano, H. Upregulation of nuclear Pa28gamma expression in cirrhosis and hepatocellular carcinoma. Exp. Ther. Med. 2012, 3, 379-385.
42. Gale, M., Jr.; Foy, E.M. Evasion of intracellular host defence by hepatitis C virus. Nature 2005, 436, 939-945.
43. Castanier, C.; Zemirli, N.; Portier, A.; Garcin, D.; Bidere, N.; Vazquez, A.; Arnoult, D. Mavs ubiquitination by the E3 ligase TRIM25 and degradation by the proteasome is involved in type I interferon production after activation of the antiviral RIG-I-like receptors. BMC Biol. 2012, 10, 44.
44. Jia, Y.; Song, T.; Wei, C.; Ni, C.; Zheng, Z.; Xu, Q.; Ma, H.; Li, L.; Zhang, Y.; He, X.; et al. Negative regulation of mavs-mediated innate immune response by PSMA7. J. Immunol. 2009, 183, 4241-4248.
45. Oshiumi, H.; Miyashita, M.; Matsumoto, M.; Seya, T. A distinct role of riplet-mediated K63-linked polyubiquitination of the RIG-I repressor domain in human antiviral innate immune responses. PLoS Pathog. 2013, 9, e1003533.
46. Arnaud, N.; Dabo, S.; Akazawa, D.; Fukasawa, M.; Shinkai-Ouchi, F.; Hugon, J.; Wakita, T.; Meurs, E.F. Hepatitis C virus reveals a novel early control in acute immune response. PLoS Pathog. 2011, 7, e1002289.
47. Horner, S.M.; Park, H.S.; Gale, M., Jr. Control of innate immune signaling and membrane targeting by the hepatitis C virus NS3/4A protease are governed by the NS3 helix alpha0. J. Virol. 2012, 86, 3112-3120.
48. Lin, W.; Kim, S.S.; Yeung, E.; Kamegaya, Y.; Blackard, J.T.; Kim, K.A.; Holtzman, M.J.; Chung, R.T. Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J. Virol. 2006, 80, 9226-9235.
49. Stevenson, N.J.; Bourke, N.M.; Ryan, E.J.; Binder, M.; Fanning, L.; Johnston, J.A.; Hegarty, J.E.; Long, A.; O’Farrelly, C. Hepatitis C virus targets the interferon-alpha JAK/STAT pathway by promoting proteasomal degradation in immune cells and hepatocytes. FEBS Lett. 2013, 587, 1571-1578.
50. Duong, F.H.; Christen, V.; Filipowicz, M.; Heim, M.H. S-adenosylmethionine and betaine correct hepatitis C virus induced inhibition of interferon signaling in vitro. Hepatology 2006, 43, 796-806.
51. Duong, F.H.; Christen, V.; Lin, S.; Heim, M.H. Hepatitis C virus-induced up-regulation of protein phosphatase 2A inhibits histone modification and DNA damage repair. Hepatology 2010, 51, 741-751.
52. Duong, F.H.; Filipowicz, M.; Tripodi, M.; la Monica, N.; Heim, M.H. Hepatitis C virus inhibits interferon signaling through up-regulation of protein phosphatase 2A. Gastroenterology 2004, 126, 263-277.
53. Shin, E.C.; Seifert, U.; Kato, T.; Rice, C.M.; Feinstone, S.M.; Kloetzel, P.M.; Rehermann, B. Virus-induced type I IFN stimulates generation of immunoproteasomes at the site of infection. J. Clin. Invest. 2006, 116, 3006-3014.
54. Shin, E.C.; Seifert, U.; Urban, S.; Truong, K.T.; Feinstone, S.M.; Rice, C.M.; Kloetzel, P.M.; Rehermann, B. Proteasome activator and antigen-processing aminopeptidases are regulated by virus-induced type I interferon in the hepatitis C virus-infected liver. J. Interferon Cytokine Res. 2007, 27, 985-990.
55. Leone, P.; di Tacchio, M.; Berardi, S.; Santantonio, T.; Fasano, M.; Ferrone, S.; Vacca, A.; Dammacco, F.; Racanelli, V. Dendritic cell maturation in HCV infection: Altered regulation of MHC class I antigen processing-presenting machinery. J. Hepatol. 2014, 61, 242-251.
56. Kimura, Y.; Gushima, T.; Rawale, S.; Kaumaya, P.; Walker, C.M. Escape mutations alter proteasome processing of major histocompatibility complex class I-restricted epitopes in persistent hepatitis C virus infection. J. Virol. 2005, 79, 4870-4876.
57. Seifert, U.; Liermann, H.; Racanelli, V.; Halenius, A.; Wiese, M.; Wedemeyer, H.; Ruppert, T.; Rispeter, K.; Henklein, P.; Sijts, A.; et al. Hepatitis C virus mutation affects proteasomal epitope processing. J. Clin. Invest. 2004, 114, 250-259.
58. Khu, Y.L.; Tan, Y.J.; Lim, S.G.; Hong, W.; Goh, P.Y. Hepatitis C virus non-structural protein NS3 interacts with LMP7, a component of the immunoproteasome, and affects its proteasome activity. Biochem. J. 2004, 384, 401-409.
59. Kuzushita, N.; Sugimoto, Y.; Sasaki, Y.; Hayashi, N. Involvement of TAP2 and LMP7 gene polymorphisms in HCV infection. Nihon Rinsho 2001, 59, 1248-1253.
60. Osna, N.A.; White, R.L.; Thiele, G.M.; Donohue, T.M., Jr. Ethanol metabolism alters major histocompatibility complex class I-restricted antigen presentation in liver cells. Hepatology 2009, 49, 1308-1315.
61. Osna, N.A.; White, R.L.; Donohue, T.M., Jr.; Beard, M.R.; Tuma, D.J.; Kharbanda, K.K. Impaired methylation as a novel mechanism for proteasome suppression in liver cells. Biochem. Biophys. Res. Commun. 2010, 391, 1291-1296.
62. Bardag-Gorce, F. Effects of ethanol on the proteasome interacting proteins. World J. Gastroenterol. 2010, 16, 1349-1357.
63. Bousquet-Dubouch, M.P.; Nguen, S.; Bouyssie, D.; Burlet-Schiltz, O.; French, S.W.; Monsarrat, B.; Bardag-Gorce, F. Chronic ethanol feeding affects proteasome-interacting proteins. Proteomics 2009, 9, 3609-3622.
64. Kleijnen, M.F.; Roelofs, J.; Park, S.; Hathaway, N.A.; Glickman, M.; King, R.W.; Finley, D. Stability of the proteasome can be regulated allosterically through engagement of its proteolytic active sites. Nat. Struct. Mol. Biol. 2007, 14, 1180-1188.
65. Singal, A.K.; Anand, B.S. Mechanisms of synergy between alcohol and hepatitis C virus. J. Clin. Gastroenterol. 2007, 41, 761-772.
66. Szabo, G.; Wands, J.R.; Eken, A.; Osna, N.A.; Weinman, S.A.; Machida, K.; Joe Wang, H. Alcohol and hepatitis C virus-interactions in immune dysfunctions and liver damage. Alcohol. Clin. Exp. Res. 2010, 34, 1675-1686.
67. Muir, A.J. The rapid evolution of treatment strategies for hepatitis C. Am. J. Gastroenterol. 2014, 109, 628-635.