Hepatitis C virus genotype-3a core protein enhances sterol regulatory element-binding protein-1 activity through the phosphoinositide 3-kinase-Akt-2 pathway

Journal of General Virology

Volumn 91, Issue 6, 2010, Pages 1388-1395

  Jackel Cram, Candice ^a   Qiao, Ling ^a   Xiang, Zhongua ^a   Brownlie, Robert ^a   Zhou, Yan ^a   Babiuk, Lorne ^a,b   Liu, Qiang ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CHIMERIC PROTEIN; FATTY ACID SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B BETA; SHORT HAIRPIN RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FATTY LIVER; GENOTYPE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIPOGENESIS; MODULATION; NONHUMAN; PHOSPHORYLATION; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; REPLICON; TRANSIENT EXPRESSION; UPREGULATION; VIRUS GENOME; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; BLOTTING, WESTERN; CELL LINE; CHROMONES; ENZYME INHIBITORS; GENE KNOCKDOWN TECHNIQUES; GENOTYPE; HEPACIVIRUS; HEPATOCYTES; HUMANS; MORPHOLINES; PROTO-ONCOGENE PROTEINS C-AKT; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; VIRAL CORE PROTEINS;

HEPATITIS C VIRUS; HEPATITIS C VIRUS GENOTYPE 3;

EID: 77952737082     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.017418-0     Document Type: Article

References (48)

1. Abid, K., Pazienza, V., de Gottardi, A., Rubbia-Brandt, L., Conne, B., Pugnale, P., Rossi, C., Mangia, A. & Negro, F. (2005). An in vitro model of hepatitis C virus genotype 3a-associated triglycerides accumulation. J Hepatol 42, 744-751.
2. Amemiya-Kudo, M., Shimano, H., Hasty, A. H., Yahagi, N., Yoshikawa, T., Matsuzaka, T., Okazaki, H., Tamura, Y., Iizuka, Y. & other authors (2002). Transcriptional activities of nuclear SREBP-1a, -1c, and -2 to different target promoters of lipogenic and cholesterogenic genes. J Lipid Res 43, 1220-1235.
3. Amoroso, P., Rapicetta, M., Tosti, M. E., Mele, A., Spada, E., Buonocore, S., Lettieri, G., Pierri, P., Chionne, P. & other authors (1998). Correlation between virus genotype and chronicity rate in acute hepatitis C. J Hepatol 28, 939-944.
4. Bengoechea-Alonso, M. T. & Ericsson, J. (2007). SREBP in signal transduction: cholesterol metabolism and beyond. Curr Opin Cell Biol 19, 215-222.
5. Bengoechea-Alonso, M. T. & Ericsson, J. (2009). A phosphorylation cascade controls the degradation of active SREBP1. J Biol Chem 284, 5885-5895.
6. Brazil, D. P., Yang, Z. Z. & Hemmings, B. A. (2004). Advances in protein kinase B signalling: AKTion on multiple fronts. Trends Biochem Sci 29, 233-242.
7. Brown, M. S., Ye, J., Rawson, R. B. & Goldstein, J. L. (2000). Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100, 391-398.
8. Brownlie, R., Zhu, J., Allan, B., Mutwiri, G. K., Babiuk, L. A., Potter, A. & Griebel, P. (2009). Chicken TLR21 acts as a functional homologue to mammalian TLR9 in the recognition of CpG oligodeoxynucleotides. Mol Immunol 46, 3163-3170.
9. Castera, L., Hezode, C., Roudot-Thoraval, F., Lonjon, I., Zafrani, E. S., Pawlotsky, J. M. & Dhumeaux, D. (2004). Effect of antiviral treatment on evolution of liver steatosis in patients with chronic hepatitis C: indirect evidence of a role of hepatitis C virus genotype 3 in steatosis. Gut 53, 420-424.
10. Cho, H., Mu, J., Kim, J. K., Thorvaldsen, J. L., Chu, Q., Crenshaw, E. B., III, Kaestner, K. H., Bartolomei, M. S., Shulman, G. I. & Birnbaum, M. J. (2001). Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKBβ). Science 292, 1728-1731.
11. Du, X., Kristiana, I., Wong, J. & Brown, A. J. (2006). Involvement of Akt in ER-to-Golgi transport of SCAP/SREBP: a link between a key cell proliferative pathway and membrane synthesis. Mol Biol Cell 17, 2735-2745.
12. Engelman, J. A. (2009). Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 9, 550-562.
13. Engelman, J. A., Luo, J. & Cantley, L. C. (2006). The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7, 606-619.
14. Fang, G., Weiser, B., Visosky, A., Moran, T. & Burger, H. (1999). PCR-mediated recombination: a general method applied to construct chimeric infectious molecular clones of plasma-derived HIV-1 RNA. Nat Med 5, 239-242.
15. Gottwein, J. M., Scheel, T. K., Hoegh, A. M., Lademann, J. B., Eugen-Olsen, J., Lisby, G. & Bukh, J. (2007). Robust hepatitis C genotype 3a cell culture releasing adapted intergenotypic 3a/2a (S52/JFH1) viruses. Gastroenterology 133, 1614-1626.
16. Graham, F. L. & van der Eb, A. J. (1973). A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52, 456-467.
17. Hawkins, J. L., Robbins, M. D., Warren, L. C., Xia, D., Petras, S. F., Valentine, J. J., Varghese, A. H., Wang, I. K., Subashi, T. A. & other authors (2008). Pharmacologic inhibition of site 1 protease activity inhibits sterol regulatory element-binding protein processing and reduces lipogenic enzyme gene expression and lipid synthesis in cultured cells and experimental animals. J Pharmacol Exp Ther 326, 801-808.
18. Horton, J. D., Goldstein, J. L. & Brown, M. S. (2002). SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 109, 1125-1131.
19. Hourioux, C., Patient, R., Morin, A., Blanchard, E., Moreau, A., Trassard, S., Giraudeau, B. & Roingeard, P. (2007). The genotype 3-specific hepatitis C virus core protein residue phenylalanine 164 increases steatosis in an in vitro cellular model. Gut 56, 1302-1308.
20. Ikeda, M., Yi, M., Li, K. & Lemon, S. M. (2002). 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, 2997-3006.
21. Jackel-Cram, C., Babiuk, L. A. & Liu, Q. (2007). Up-regulation of fatty acid synthase promoter by hepatitis C virus core protein: genotype-3a core has a stronger effect than genotype-1b core. J Hepatol 46, 999-1008.
22. Kotzka, J., Muller-Wieland, D., Koponen, A., Njamen, D., Kremer, L., Roth, G., Munck, M., Knebel, B. & Krone, W. (1998). ADD1/SREBP-1c mediates insulin-induced gene expression linked to the MAP kinase pathway. Biochem Biophys Res Commun 249, 375-379.
23. Kumar, D., Farrell, G. C., Fung, C. & George, J. (2002). Hepatitis C virus genotype 3 is cytopathic to hepatocytes: reversal of hepatic steatosis after sustained therapeutic response. Hepatology 36, 1266-1272.
24. Latasa, M. J., Moon, Y. S., Kim, K. H. & Sul, H. S. (2000). Nutritional regulation of the fatty acid synthase promoter in vivo: sterol regulatory element binding protein functions through an upstream region containing a sterol regulatory element. Proc Natl Acad Sci U S A 97, 10619-10624.
25. Lohmann, V., Hoffmann, S., Herian, U., Penin, F. & Bartenschlager, R. (2003). Viral and cellular determinants of hepatitis C virus RNA replication in cell culture. J Virol 77, 3007-3019. (Pubitemid 36228086)
26. Lu, M. & Shyy, J. Y. (2006). Sterol regulatory element-binding protein 1 is negatively modulated by PKA phosphorylation. Am J Physiol Cell Physiol 290, C1477-C1486. (Pubitemid 43830787)
27. Mannova, P. & Beretta, L. (2005). Activation of the N-Ras-PI3K-Akt-mTOR pathway by hepatitis C virus: control of cell survival and viral replication. J Virol 79, 8742-8749. (Pubitemid 40934785)
28. Negro, F. (2006). Mechanisms and significance of liver steatosis in hepatitis C virus infection. World J Gastroenterol 12, 6756-6765. (Pubitemid 44811395)
29. Oem, J. K., Jackel-Cram, C., Li, Y. P., Zhou, Y., Zhong, J., Shimano, H., Babiuk, L. A. & Liu, Q. (2008). Activation of sterol regulatory element-binding protein 1c and fatty acid synthase transcription by hepatitis C virus non-structural protein 2. J Gen Virol 89, 1225-1230.
30. Park, C. Y., Jun, H. J., Wakita, T., Cheong, J. H. & Hwang, S. B. (2009). Hepatitis C virus nonstructural 4B protein modulates sterol regulatory element-binding protein signaling via the AKT pathway. J Biol Chem 284, 9237-9246.
31. Patton, H. M., Patel, K., Behling, C., Bylund, D., Blatt, L. M., Vallee, M., Heaton, S., Conrad, A., Pockros, P. J. & McHutchison, J. G. (2004). The impact of steatosis on disease progression and early and sustained treatment response in chronic hepatitis C patients. J Hepatol 40, 484-490.
32. Pazienza, V., Clement, S., Pugnale, P., Conzelmann, S., Pascarella, S., Mangia, A. & Negro, F. (2009). Gene expression profile of Huh-7 cells expressing hepatitis C virus genotype 1b or 3a core proteins. Liver Int 29, 661-669.
33. Pietschmann, T., Lohmann, V., Kaul, A., Krieger, N., Rinck, G., Rutter, G., Strand, D. & Bartenschlager, R. (2002). Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J Virol 76, 4008-4021.
34. Pietschmann, T., Kaul, A., Koutsoudakis, G., Shavinskaya, A., Kallis, S., Steinmann, E., Abid, K., Negro, F., Dreux, M. & other authors (2006). Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci U S A 103, 7408-7413.
35. Piodi, A., Chouteau, P., Lerat, H., Hezode, C. & Pawlotsky, J. M. (2008). Morphological changes in intracellular lipid droplets induced by different hepatitis C virus genotype core sequences and relationship with steatosis. Hepatology 48, 16-27.
36. Porstmann, T., Griffiths, B., Chung, Y. L., Delpuech, O., Griffiths, J. R., Downward, J. & Schulze, A. (2005). PKB/Akt induces transcription of enzymes involved in cholesterol and fatty acid biosynthesis via activation of SREBP. Oncogene 24, 6465-6481.
37. Poynard, T., Ratziu, V., McHutchison, J., Manns, M., Goodman, Z., Zeuzem, S., Younossi, Z. & Albrecht, J. (2003a). Effect of treatment with peginterferon or interferon alfa-2b and ribavirin on steatosis in patients infected with hepatitis C. Hepatology 38, 75-85. (Pubitemid 36775798)
38. Poynard, T., Yuen, M. F., Ratziu, V. & Lai, C. L. (2003b). Viral hepatitis C. Lancet 362, 2095-2100.
39. Punga, T., Bengoechea-Alonso, M. T. & Ericsson, J. (2006). Phosphorylation and ubiquitination of the transcription factor sterol regulatory element-binding protein-1 in response to DNA binding. J Biol Chem 281, 25278-25286. (Pubitemid 44401915)
40. Raghow, R., Yellaturu, C., Deng, X., Park, E. A. & Elam, M. B. (2008). SREBPs: the crossroads of physiological and pathological lipid homeostasis. Trends Endocrinol Metab 19, 65-73. (Pubitemid 351317897)
41. Roth, G., Kotzka, J., Kremer, L., Lehr, S., Lohaus, C., Meyer, H. E., Krone, W. & Muller-Wieland, D. (2000). MAP kinases Erk1/2 phosphorylate sterol regulatory element-binding protein (SREBP)-1a at serine 117 in vitro. J Biol Chem 275, 33302-33307.
42. Rubbia-Brandt, L., Quadri, R., Abid, K., Giostra, E., Male, P. J., Mentha, G., Spahr, L., Zarski, J. P., Borisch, B. & other authors (2000). Hepatocyte steatosis is a cytopathic effect of hepatitis C virus genotype 3. J Hepatol 33, 106-115.
43. Sheikh, M. Y., Choi, J., Qadri, I., Friedman, J. E. & Sanyal, A. J. (2008). Hepatitis C virus infection: molecular pathways to metabolic syndrome. Hepatology 47, 2127-2133. (Pubitemid 351945577)
44. Shimano, H., Horton, J. D., Shimomura, I., Hammer, R. E., Brown, M. S. & Goldstein, J. L. (1997). Isoform 1c of sterol regulatory element binding protein is less active than isoform 1a in livers of transgenic mice and in cultured cells. J Clin Invest 99, 846-854.
45. Street, A., Macdonald, A., Crowder, K. & Harris, M. (2004). The hepatitis C virus NS5A protein activates a phosphoinositide 3-kinase dependent survival signalling cascade. J Biol Chem 279, 12232-12241. (Pubitemid 38445788)
46. Taniguchi, C. M., Kondo, T., Sajan, M., Luo, J., Bronson, R., Asano, T., Farese, R., Cantley, L. C. & Kahn, C. R. (2006). Divergent regulation of hepatic glucose and lipid metabolism by phosphoinositide 3-kinase via Akt and PKCλ/ζ. Cell Metab 3, 343-353.
47. Waris, G., Felmlee, D. J., Negro, F. & Siddiqui, A. (2007). Hepatitis C virus induces proteolytic cleavage of sterol regulatory element binding proteins and stimulates their phosphorylation via oxidative stress. J Virol 81, 8122-8130. (Pubitemid 47101498)
48. Yap, T. A., Garrett, M. D., Walton, M. I., Raynaud, F., de Bono, J. S. & Workman, P. (2008). Targeting the PI3K-AKT-mTOR pathway: progress, pitfalls, and promises. Curr Opin Pharmacol 8, 393-412.