Transient activation of the PI3K-AKT pathway by hepatitis C virusto enhance viral entry

Journal of Biological Chemistry

Volumn 287, Issue 50, 2012, Pages 41922-41930

  Liu, Zhe ^a   Tian, Yongjun ^a   Machida, Keigo ^a   Lai, Michael M C ^a   Luo, Guangxiang ^b   Foung, Steven K H ^c   Ou, Jing Hsiung James ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR PATHWAY; CLASS B; CLAUDIN; CONSTITUTIVELY ACTIVES; CORECEPTORS; ECTODOMAIN; ENVELOPE PROTEINS; HEPATITIS C; HEPATITIS C VIRUS; OCCLUDIN; SCAVENGER RECEPTOR; SIGNALING PATHWAYS;

VIRUSES;

ANTIBODIES;

CD81 ANTIGEN; CLAUDIN 1; OCCLUDIN;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MYRISTYLATION; PI3K AKT SIGNALING PATHWAY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA SYNTHESIS; SIGNAL TRANSDUCTION; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS REPLICATION;

ANTIGENS, CD81; CELL LINE; ENZYME ACTIVATION; HEPACIVIRUS; HEPATITIS C; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; ULTRAVIOLET RAYS; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION; VIRUS REPLICATION;

HEPATITIS C VIRUS; VESICULAR STOMATITIS VIRUS;

EID: 84871280686     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.414789     Document Type: Article

References (55)

1. Shepard, C. W., Finelli, L., and Alter, M. J. (2005) Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 5, 558-567 (Pubitemid 41196755)
2. Bartenschlager, R., Frese, M., and Pietschmann, T. (2004) Novel insights into hepatitis C virus replication and persistence. Adv. Virus Res. 63, 71-180 (Pubitemid 39752303)
3. Bartenschlager, R., and Sparacio, S. (2007) Hepatitis C virus molecular clones and their replication capacity in vivo and in cell culture. Virus Res. 127, 195-207 (Pubitemid 47058197)
4. Brass, V., Moradpour, D., and Blum, H. E. (2006) Molecular virology of hepatitis C virus (HCV). 2006 update. Int. J. Med. Sci. 3, 29-34
5. Penin, F., Brass, V., Appel, N., Ramboarina, S., Montserret, R., Ficheux, D., Blum, H. E., Bartenschlager, R., and Moradpour, D. (2004) Structure and function of the membrane anchor domain of hepatitis C virus nonstructural protein 5A. J. Biol. Chem. 279, 40835-40843 (Pubitemid 39287681)
6. Gastaminza, P., Cheng, G., Wieland, S., Zhong, J., Liao, W., and Chisari, F. V. (2008) Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J. Virol. 82, 2120-2129 (Pubitemid 351293514)
7. Ye, J. (2007) Reliance of host cholesterol metabolic pathways for the life cycle of hepatitis C virus. PLoS Pathog. 3, e108
8. Jiang, J., Cun, W., Wu, X., Shi, Q., Tang, H., and Luo, G. (2012) Hepatitis C virus attachment mediated by apolipoprotein E binding to cell surface heparan sulfate. J. Virol. 86, 7256-7267
9. Pileri, P., Uematsu, Y., Campagnoli, S., Galli, G., Falugi, F., Petracca, R., Weiner, A. J., Houghton, M., Rosa, D., Grandi, G., and Abrignani, S. (1998) Binding of hepatitis C virus to CD81. Science 282, 938-941 (Pubitemid 28507525)
10. Scarselli, E., Ansuini, H., Cerino, R., Roccasecca, R. M., Acali, S., Filocamo, G., Traboni, C., Nicosia, A., Cortese, R., and Vitelli, A. (2002) The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 21, 5017-5025
11. Evans, M. J., von Hahn, T., Tscherne, D. M., Syder, A. J., Panis, M., Wölk, B., Hatziioannou, T., McKeating, J. A., Bieniasz, P. D., and Rice, C. M. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446, 801-805 (Pubitemid 46582027)
12. Liu, S., Yang, W., Shen, L., Turner, J. R., Coyne, C. B., and Wang, T. (2009) Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection. J. Virol. 83, 2011-2014
13. Ploss, A., Evans, M. J., Gaysinskaya, V. A., Panis, M., You, H., de Jong, Y. P., and Rice, C. M. (2009) Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457, 882-886
14. Benedicto, I., Molina-Jiménez, F., Bartosch, B., Cosset, F. L., Lavillette, D., Prieto, J., Moreno-Otero, R., Valenzuela-Fernández, A., Aldabe, R., López- Cabrera, M., and Majano, P. L. (2009) The tight junction-associated protein occludin is required for a postbinding step in hepatitis C virus entry and infection. J. Virol. 83, 8012-8020
15. Rigotti, A., Edelman, E. R., Seifert, P., Iqbal, S. N., DeMattos, R. B., Temel, R. E., Krieger, M., and Williams, D. L. (1996) Regulation by adrenocorticotropic hormone of the in vivo expression of scavenger receptor class B type I (SR-BI), a high density lipoprotein receptor, in steroidogenic cells of the murine adrenal gland. J. Biol. Chem. 271, 33545-33549
16. Reaven, E., Nomoto, A., Leers-Sucheta, S., Temel, R., Williams, D. L., and Azhar, S. (1998) Expression and microvillar localization of scavenger receptor, class B, type I (a high density lipoprotein receptor) in luteinized and hormone-desensitized rat ovarian models. Endocrinology 139, 2847-2856 (Pubitemid 28512395)
17. Reaven, E., Zhan, L., Nomoto, A., Leers-Sucheta, S., and Azhar, S. (2000) Expression and microvillar localization of scavenger receptor class B, type I (SR-BI) and selective cholesteryl ester uptake in Leydig cells from rat testis. J. Lipid Res. 41, 343-356 (Pubitemid 30183617)
18. Reaven, E., Leers-Sucheta, S., Nomoto, A., and Azhar, S. (2001) Expression of scavenger receptor class B type 1 (SR-BI) promotes microvillar channel formation and selective cholesteryl ester transport in a heterologous reconstituted system. Proc. Natl. Acad. Sci. U.S.A. 98, 1613-1618 (Pubitemid 32165547)
19. Kellner-Weibel, G., de La Llera-Moya, M., Connelly, M. A., Stoudt, G., Christian, A. E., Haynes, M. P., Williams, D. L., and Rothblat, G. H. (2000) Expression of scavenger receptor BI in COS-7 cells alters cholesterol content and distribution. Biochemistry 39, 221-229 (Pubitemid 30033337)
20. Williams, D. L., Wong, J. S., and Hamilton, R. L. (2002) SR-BI is required for microvillar channel formation and the localization of HDL particles to the surface of adrenocortical cells in vivo. J. Lipid Res. 43, 544-549
21. Huang, Z. H., Gu, D., Lange, Y., and Mazzone, T. (2003) Expression of scavenger receptor BI facilitates sterol movement between the plasma membrane and the endoplasmic reticulum in macrophages. Biochemistry 42, 3949-3955 (Pubitemid 36402688)
22. Peng, Y., Akmentin, W., Connelly, M. A., Lund-Katz, S., Phillips, M. C., and Williams, D. L. (2004) Scavenger receptor BI (SR-BI) clustered on microvillar extensions suggests that this plasma membrane domain is a way station for cholesterol trafficking between cells and high-density lipoprotein. Mol. Biol. Cell 15, 384-396 (Pubitemid 38044971)
23. Bertaux, C., and Dragic, T. (2006) Different domains of CD81 mediate distinct stages of hepatitis C virus pseudoparticle entry. J. Virol. 80, 4940-4948
24. Harris, H. J., Davis, C., Mullins, J. G., Hu, K., Goodall, M., Farquhar, M. J., Mee, C. J., McCaffrey, K., Young, S., Drummer, H., Balfe, P., and McKeating, J. A. (2010) Claudin association with CD81 defines hepatitis C virus entry. J. Biol. Chem. 285, 21092-21102
25. Flint, M., von Hahn, T., Zhang, J., Farquhar, M., Jones, C. T., Balfe, P., Rice, C. M., and McKeating, J. A. (2006) Diverse CD81 proteins support hepatitis C virus infection. J. Virol. 80, 11331-11342 (Pubitemid 44706573)
26. Kohaar, I., Ploss, A., Korol, E., Mu, K., Schoggins, J. W., O'Brien, T. R., Rice, C. M., and Prokunina-Olsson, L. (2010) Splicing diversity of the human OCLN gene and its biological significance for hepatitis C virus entry. J. Virol. 84, 6987-6994
27. Toker, A., and Cantley, L. C. (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387, 673-676 (Pubitemid 27270600)
28. Wullschleger, S., Loewith, R., and Hall, M. N. (2006) TOR signaling in growth and metabolism. Cell 124, 471-484 (Pubitemid 43199434)
29. Gingras, A. C., Kennedy, S. G., O'Leary, M. A., Sonenberg, N., and Hay, N. (1998) 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev. 12, 502-513 (Pubitemid 28101013)
30. Juntilla, M. M., Patil, V. D., Calamito, M., Joshi, R. P., Birnbaum, M. J., and Koretzky, G. A. (2010) AKT1 and AKT2 maintain hematopoietic stem cell function by regulating reactive oxygen species. Blood 115, 4030-4038
31. Cooray, S. (2007) Apoptosis, Cell Signaling, and Human Diseases: Molecular Mechanisms, pp. 57-80 Humana Press Inc., Totowa, NJ
32. Shin, Y. K., Liu, Q., Tikoo, S. K., Babiuk, L. A., and Zhou, Y. (2007) Effect of the phosphatidylinositol 3-kinase/Akt pathway on influenzaAvirus propagation. J. Gen. Virol. 88, 942-950 (Pubitemid 46359565)
33. Feng, S. Z., Cao, W. S., and Liao, M. (2011) The PI3K/Akt pathway is involved in early infection of some exogenous avian leukosis viruses. J. Gen. Virol. 92, 1688-1697
34. Saeed, M. F., Kolokoltsov, A. A., Freiberg, A. N., Holbrook, M. R., and Davey, R. A. (2008) Phosphoinositide-3 kinase-Akt pathway controls cellular entry of Ebola virus. PLoS Pathog. 4, e1000141
35. Patel, R. K., and Hardy, R. W. (2012) Role for the phosphatidylinositol 3-kinase-Akt-TOR pathway during sindbis virus replication in arthropods. J. Virol. 86, 3595-3604
36. Urata, S., Ngo, N., and de la Torre, J. C. (2012) The PI3K/Akt pathway contributes to arenavirus budding. J. Virol. 86, 4578-4585
37. Yu, Y., and Alwine, J. C. (2002) Human cytomegalovirus major immedi-ate- early proteins and simian virus 40 largeTantigen can inhibit apoptosis through activation of the phosphatidylinositide 3′-OH kinase pathway and the cellular kinase Akt. J. Virol. 76, 3731-3738 (Pubitemid 34250537)
38. Esfandiarei, M., Luo, H., Yanagawa, B., Suarez, A., Dabiri, D., Zhang, J., and McManus, B. M. (2004) Protein kinase B/Akt regulates coxsackievirus B3 replication through a mechanism which is not caspase dependent. J. Virol. 78, 4289-4298 (Pubitemid 38437232)
39. Rahaus, M., Desloges, N., and Wolff, M. H. (2007) Varicella-zoster virus requires a functional PI3K/Akt/GSK-3α/β signaling cascade for efficient replication. Cell. Signal. 19, 312-320 (Pubitemid 44969980)
40. Guo, H., Zhou, T., Jiang, D., Cuconati, A., Xiao, G. H., Block, T. M., and Guo, J. T. (2007) Regulation of hepatitis B virus replication by the phosphatidylinositol 3-kinase-Akt signal transduction pathway. J. Virol. 81, 10072-10080 (Pubitemid 350067711)
41. Street, A., Macdonald, A., McCormick, C., and Harris, M. (2005) Hepatitis C virus NS5A-mediated activation of phosphoinositide 3-kinase results in stabilization of cellular β-catenin and stimulation of β-catenin- responsive transcription. J. Virol. 79, 5006-5016 (Pubitemid 40464251)
42. Street, A., Macdonald, A., Crowder, K., and Harris, M. (2004) The hepatitis C virus NS5A protein activates a phosphoinositide 3-kinase-dependent survival signaling cascade. J. Biol. Chem. 279, 12232-12241 (Pubitemid 38445788)
43. Banerjee, S., Saito, K., Ait-Goughoulte, M., Meyer, K., Ray, R. B., and Ray, R. (2008) Hepatitis C virus core protein upregulates serine phosphorylation of insulin receptor substrate-1 and impairs the downstream Akt/protein kinase B signaling pathway for insulin resistance. J. Virol. 82, 2606-2612 (Pubitemid 351329151)
44. Bose, S. K., Shrivastava, S., Meyer, K., Ray, R. B., and Ray, R. (2012) Hepatitis C virus activates the mTOR/S6K1 signaling pathway in inhibiting IRS-1 function for insulin resistance. J. Virol. 86, 6315-6322
45. Jiang, J., and Luo, G. (2012) Cell culture-adaptive mutations promote viral protein-protein interactions and morphogenesis of infectious hepatitis C virus. J. Virol. 86, 8987-8997
46. Lo, S. Y., Masiarz, F., Hwang, S. B., Lai, M. M., and Ou, J. H. (1995) Differential subcellular localization of hepatitis C virus core gene products. Virology 213, 455-461
47. Keck, Z. Y., Xia, J., Cai, Z., Li, T. K., Owsianka, A. M., Patel, A. H., Luo, G., and Foung, S. K. (2007) Immunogenic and functional organization of hepatitis C virus (HCV) glycoprotein E2 on infectious HCV virions. J. Virol. 81, 1043-1047 (Pubitemid 46067930)
48. Keck, Z. Y., Saha, A., Xia, J., Wang, Y., Lau, P., Krey, T., Rey, F. A., and Foung, S. K. (2011) Mapping a region of hepatitisCvirus E2 that is responsible for escape from neutralizing antibodies and a core CD81-binding region that does not tolerate neutralization escape mutations. J. Virol. 85, 10451-10463
49. Zhang, C., Comai, L., and Johnson, D. L. (2005) PTEN represses RNA polymerase I transcription by disrupting the SL1 complex. Mol. Cell Biol. 25, 6899-6911 (Pubitemid 41105891)
50. Singh, A. B., Sharma, A., Smith, J. J., Krishnan, M., Chen, X., Eschrich, S., Washington, M. K., Yeatman, T. J., Beauchamp, R. D., and Dhawan, P. (2011) Claudin-1 up-regulates the repressor ZEB-1 to inhibit E-cadherin expression in colon cancer cells. Gastroenterology 141, 2140-2153
51. Zeisel, M. B., Fofana, I., Fafi-Kremer, S., and Baumert, T. F. (2011) Hepatitis C virus entry into hepatocytes. Molecular mechanisms and targets for antiviral therapies. J. Hepatol. 54, 566-576
52. Lin, K. K., Rossi, L., Boles, N. C., Hall, B. E., George, T. C., and Goodell, M. A. (2011) CD81 is essential for the re-entry of hematopoietic stem cells to quiescence following stress-induced proliferation via deactivation of the Akt pathway. PLoS Biol. 9, e1001148
53. Sánchez, E. G., Quintas, A., Pérez-Núñez, D., Nogal, M., Barroso, S., Carrascosa, A.Ĺ., and Revilla, Y. (2012) African Swine Fever virus uses macropinocytosis to enter host cells. PLoS Pathog. 8, e1002754
54. Agarwal, V., and Hammerschmidt, S. (2009) Cdc42 and the phosphatidylinositol 3-kinase-Akt pathway are essential for PspC-mediated internalization of pneumococci by respiratory epithelial cells. J. Biol. Chem. 284, 19427-19436
55. Farquhar, M. J., Harris, H. J., Diskar, M., Jones, S., Mee, C. J., Nielsen, S. U., Brimacombe, C. L., Molina, S., Toms, G. L., Maurel, P., Howl, J., Herberg, F. W., van Ijzendoorn, S. C., Balfe, P., and McKeating, J. A. (2008) Protein kinase A-dependent step(s) in hepatitis C virus entry and infectivity. J. Virol. 82, 8797-8811