Hepatitis C virus and host cell nuclear transport machinery: A clandestine affair

Frontiers in Microbiology

Volumn 6, Issue JUN, 2015, Pages

  Bonamassa, Barbara ^a   Ciccarese, Francesco ^b   Di Antonio, Veronica ^a   Contarini, Andrea ^a   Palù, Giorgio ^a   Alvisi, Gualtiero ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

Author keywords

Caspase; Exportin; Importin; NPC; Nuclear import; Nucleoporin; Ran; Replication factories

Indexed keywords

CASPASE; NONSTRUCTURAL PROTEIN 5A; NUCLEOPORIN; PROTEIN BAX; PROTEIN BCL 2; VIRUS RNA;

CELL NUCLEUS; CELL STRESS; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; ENDOPLASMIC RETICULUM MEMBRANE; GENE AMPLIFICATION; GENE EXPRESSION; GENETIC REGULATION; HEPATITIS C; HEPATITIS C VIRUS; HOST CELL; IMMUNE RESPONSE; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; SHORT SURVEY; VIRUS CELL INTERACTION; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 84936993283     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00619     Document Type: Short Survey

References (75)

1. Ahola, T., Lampio, A., Auvinen, P., and Kaariainen, L. (1999). Semliki Forest virus mRNA capping enzyme requires association with anionic membrane phospholipids for activity. EMBO J. 18, 3164-3172. doi: 10.1093/emboj/18.11.3164
2. Alvisi, G., and Jans, D. A. (2015). Basis of cargo recognition by importin as: the power of structure. Structure 23, 251-252. doi: 10.1016/j.str.2015.01.005
3. Alvisi, G., Jans, D. A., Camozzi, D., Avanzi, S., Loregian, A., Ripalti, A., et al. (2013). Regulated transport into the nucleus of herpesviridae DNA replication core proteins. Viruses 5, 2210-2234. doi: 10.3390/v5092210
4. Alvisi, G., Madan, V., and Bartenschlager, R. (2011a). Hepatitis C virus and host cell lipids: an intimate connection. RNA Biol. 8, 258-269. doi: 10.4161/rna.8.2.15011
5. Alvisi, G., Marin, O., Pari, G., Mancini, M., Avanzi, S., Loregian, A., et al. (2011b). Multiple phosphorylation sites at the C-terminus regulate nuclear import of HCMV DNA polymerase processivity factor ppUL44. Virology 417, 259-267. doi: 10.1016/j.virol.2011.06.015
6. Alvisi, G., Rawlinson, S. M., Ghildyal, R., Ripalti, A., and Jans, D. A. (2008). Regulated nucleocytoplasmic trafficking of viral gene products: a therapeutic target? Biochim. Biophys. Acta 1784, 213-227. doi: 10.1016/j.bbapap.2007.08.021
7. Appel, N., Zayas, M., Miller, S., Krijnse-Locker, J., Schaller, T., Friebe, P., et al. (2008). Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly. PLoS Pathog. 4:e1000035. doi: 10.1371/journal.ppat.1000035
8. Berger, C., Romero-Brey, I., Radujkovic, D., Terreux, R., Zayas, M., Paul, D., et al. (2014). Daclatasvir-like inhibitors of NS5A block early biogenesis of hepatitis C virus-induced membranous replication factories, independent of RNA replication. Gastroenterology 147, 1094-1105.e25. doi: 10.1053/j.gastro.2014.07.019
9. Bianco, A., Reghellin, V., Donnici, L., Fenu, S., Alvarez, R., Baruffa, C., et al. (2012). Metabolism of phosphatidylinositol 4-kinase IIIa-dependent PI4P Is subverted by HCV and is targeted by a 4-anilino quinazoline with antiviral activity. PLoS Pathog. 8:e1002576. doi: 10.1371/journal.ppat.1002576
10. Camus-Bouclainville, C., Fiette, L., Bouchiha, S., Pignolet, B., Counor, D., Filipe, C., et al. (2004). A virulence factor of myxoma virus colocalizes with NF-κB in the nucleus and interferes with inflammation. J. Virol. 78, 2510-2516. doi: 10.1128/JVI.78.5.2510-2516.2004
11. Cansizoglu, A. E., Lee, B. J., Zhang, Z. C., Fontoura, B. M., and Chook, Y. M. (2007). Structure-based design of a pathway-specific nuclear import inhibitor. Nat. Struct. Mol. Biol. 14, 452-454. doi: 10.1038/nsmb1229
12. Cerutti, A., Maillard, P., Minisini, R., Vidalain, P. O., Roohvand, F., Pecheur, E. I., et al. (2011). Identification of a functional, CRM-1-dependent nuclear export signal in hepatitis C virus core protein. PLoS ONE 6:e25854. doi: 10.1371/journal.pone.0025854
13. Chang, S. C., Yen, J. H., Kang, H. Y., Jang, M. H., and Chang, M. F. (1994). Nuclear localization signals in the core protein of hepatitis C virus. Biochem. Biophys. Res. Commun. 205, 1284-1290. doi: 10.1006/bbrc.1994.2804
14. Chook, Y. M., and Suel, K. E. (2011). Nuclear import by karyopherin-ßs: recognition and inhibition. Biochim. Biophys. Acta 1813, 1593-1606. doi: 10.1016/j.bbamcr.2010.10.014
15. Chung, K. M., Lee, J., Kim, J. E., Song, O. K., Cho, S., Lim, J., et al. (2000). Nonstructural protein 5A of hepatitis C virus inhibits the function of karyopherin ß3. J. Virol. 74, 5233-5241. doi: 10.1128/JVI.74.11.5233-5241.2000
16. Chung, Y. L., Sheu, M. L., and Yen, S. H. (2003). Hepatitis C virus NS5A as a potential viral Bcl-2 homologue interacts with Bax and inhibits apoptosis in hepatocellular carcinoma. Int. J. Cancer 107, 65-73. doi: 10.1002/ijc.11303
17. Eberle, C. A., Zayas, M., Stukalov, A., Pichlmair, A., Alvisi, G., Muller, A. C., et al. (2014). The lysine methyltransferase SMYD3 interacts with hepatitis C virus NS5A and is a negative regulator of viral particle production. Virology 462-463, 34-41. doi: 10.1016/j.virol.2014.05.016
18. Elazar, M., Cheong, K. H., Liu, P., Greenberg, H. B., Rice, C. M., and Glenn, J. S. (2003). Amphipathic helix-dependent localization of NS5A mediates hepatitis C virus RNA replication. J. Virol. 77, 6055-6061. doi: 10.1128/JVI.77.10.6055-6061.2003
19. Fontes, M. R., Teh, T., and Kobe, B. (2000). Structural basis of recognition of monopartite and bipartite nuclear localization sequences by mammalian importin-a. J. Mol. Biol. 297, 1183-1194. doi: 10.1006/jmbi.2000.3642
20. 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. doi: 10.1128/JVI.02053-07
21. Germain, M. A., Chatel-Chaix, L., Gagne, B., Bonneil, E., Thibault, P., Pradezynski, F., et al. (2014). Elucidating novel hepatitis C virus-host interactions using combined mass spectrometry and functional genomics approaches. Mol. Cell. Proteomics 13, 184-203. doi: 10.1074/mcp.M113.030155
22. Ghosh, A. K., Steele, R., Meyer, K., Ray, R., and Ray, R. B. (1999). Hepatitis C virus NS5A protein modulates cell cycle regulatory genes and promotes cell growth. J. Gen. Virol. 80, 1179-1183.
23. Haybaeck, J., Zeller, N., Wolf, M. J., Weber, A., Wagner, U., Kurrer, M. O., et al. (2009). A lymphotoxin-driven pathway to hepatocellular carcinoma. Cancer Cell 16, 295-308. doi: 10.1016/j.ccr.2009.08.021
24. Hope, R. G., Mcelwee, M. J., and Mclauchlan, J. (2006). Efficient cleavage by signal peptide peptidase requires residues within the signal peptide between the core and E1 proteins of hepatitis C virus strain J1. J. Gen. Virol. 87, 623-627. doi: 10.1099/vir.0.81371-0
25. Hsu, N. Y., Ilnytska, O., Belov, G., Santiana, M., Chen, Y. H., Takvorian, P. M., et al. (2010). Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141, 799-811. doi: 10.1016/j.cell.2010.03.050
26. Ide, Y., Zhang, L., Chen, M., Inchauspe, G., Bahl, C., Sasaguri, Y., et al. (1996). Characterization of the nuclear localization signal and subcellular distribution of hepatitis C virus nonstructural protein NS5A. Gene 182, 203-211. doi: 10.1016/S0378-1119(96)00555-0
27. Imasaki, T., Shimizu, T., Hashimoto, H., Hidaka, Y., Kose, S., Imamoto, N., et al. (2007). Structural basis for substrate recognition and dissociation by human transportin 1. Mol. Cell 28, 57-67. doi: 10.1016/j.molcel.2007.08.006
28. Jakel, S., and Gorlich, D. (1998). Importin ß, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 17, 4491-4502. doi: 10.1093/emboj/17.15.4491
29. Jones, C. T., Murray, C. L., Eastman, D. K., Tassello, J., and Rice, C. M. (2007). Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus. J. Virol. 81, 8374-8383. doi: 10.1128/JVI.00690-07
30. Kalderon, D., Roberts, B. L., Richardson, W. D., and Smith, A. E. (1984). A short amino acid sequence able to specify nuclear location. Cell 39, 499-509. doi: 10.1016/0092-8674(84)90457-4
31. Kao, C. F., Chen, S. Y., and Lee, Y. H. (2004). Activation of RNA polymerase I transcription by hepatitis C virus core protein. J. Biomed. Sci. 11, 72-94. doi: 10.1159/000075291
32. Kato, N. (2000). Genome of human hepatitis C virus (HCV): gene organization, sequence diversity, and variation. Microb. Comp. Genomics 5, 129-151. doi: 10.1089/mcg.2000.5.129
33. Khabar, K. S., Al-Zoghaibi, F., Al-Ahdal, M. N., Murayama, T., Dhalla, M., Mukaida, N., et al. (1997). The a chemokine, interleukin 8, inhibits the antiviral action of interferon a. J. Exp. Med. 186, 1077-1085. doi: 10.1084/jem.186.7.1077
34. Legembre, P., Schickel, R., Barnhart, B. C., and Peter, M. E. (2004). Identification of SNF1/AMP kinase-related kinase as an NF-κB-regulated anti-apoptotic kinase involved in CD95-induced motility and invasiveness. J. Biol. Chem. 279, 46742-46747. doi: 10.1074/jbc.M404334200
35. Levin, A., Neufeldt, C. J., Pang, D., Wilson, K., Loewen-Dobler, D., Joyce, M. A., et al. (2014). Functional characterization of nuclear localization and export signals in hepatitis C virus proteins and their role in the membranous web. PLoS ONE 9:e114629. doi: 10.1371/journal.pone.0114629
36. Lindenboim, L., Sasson, T., Worman, H. J., Borner, C., and Stein, R. (2014). Cellular stress induces Bax-regulated nuclear bubble budding and rupture followed by nuclear protein release. Nucleus 5, 527-541. doi: 10.4161/19491034.2014.970105
37. Lohmann, V., Korner, F., Koch, J., Herian, U., Theilmann, L., and Bartenschlager, R. (1999). Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285, 110-113. doi: 10.1126/science.285.5424.110
38. Lyle, J. M., Bullitt, E., Bienz, K., and Kirkegaard, K. (2002). Visualization and functional analysis of RNA-dependent RNA polymerase lattices. Science 296, 2218-2222. doi: 10.1126/science.1070585
39. Mai, R. T., Yeh, T. S., Kao, C. F., Sun, S. K., Huang, H. H., and Wu Lee, Y. H. (2006). Hepatitis C virus core protein recruits nucleolar phosphoprotein B23 and coactivator p300 to relieve the repression effect of transcriptional factor YY1 on B23 gene expression. Oncogene 25, 448-462. doi: 10.1038/sj.onc.1209052
40. Majumder, M., Ghosh, A. K., Steele, R., Ray, R., and Ray, R. B. (2001). Hepatitis C virus NS5A physically associates with p53 and regulates p21/waf1 gene expression in a p53-dependent manner. J. Virol. 75, 1401-1407. doi: 10.1128/JVI.75.3.1401-1407.2001
41. Maqbool, M. A., Imache, M. R., Higgs, M. R., Carmouse, S., Pawlotsky, J. M., and Lerat, H. (2013). Regulation of hepatitis C virus replication by nuclear translocation of nonstructural 5A protein and transcriptional activation of host genes. J. Virol. 87, 5523-5539. doi: 10.1128/JVI.00585-12
42. Marshall, J. A., Borg, J., Coulepis, A. G., and Anderson, D. A. (1996). Annulate lamellae and lytic HAV infection in vitro. Tissue Cell 28, 205-214. doi: 10.1016/S0040-8166(96)80008-5
43. Masaki, T., Suzuki, R., Murakami, K., Aizaki, H., Ishii, K., Murayama, A., et al. (2008). Interaction of hepatitis C virus nonstructural protein 5A with core protein is critical for the production of infectious virus particles. J. Virol. 82, 7964-7976. doi: 10.1128/JVI.00826-08
44. Merisko, E. M. (1989). Annulate lamellae: an organelle in search of a function. Tissue Cell 21, 343-354. doi: 10.1016/0040-8166(89)90049-9
45. Miyanari, Y., Atsuzawa, K., Usuda, N., Watashi, K., Hishiki, T., Zayas, M., et al. (2007). The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 9, 1089-1097. doi: 10.1038/ncb1631
46. Miyanari, Y., Hijikata, M., Yamaji, M., Hosaka, M., Takahashi, H., and Shimotohno, K. (2003). Hepatitis C virus non-structural proteins in the probable membranous compartment function in viral genome replication. J. Biol. Chem. 278, 50301-50308. doi: 10.1074/jbc.M305684200
47. Moriishi, K., Okabayashi, T., Nakai, K., Moriya, K., Koike, K., Murata, S., et al. (2003). Proteasome activator PA28γ-dependent nuclear retention and degradation of hepatitis C virus core protein. J. Virol. 77, 10237-10249. doi: 10.1128/JVI.77.19.10237-10249.2003
48. Moriishi, K., Shoji, I., Mori, Y., Suzuki, R., Suzuki, T., Kataoka, C., et al. (2010). Involvement of PA28γ in the propagation of hepatitis C virus. Hepatology 52, 411-420. doi: 10.1002/hep.23680
49. Moriya, K., Fujie, H., Yotsuyanagi, H., Shintani, Y., Tsutsumi, T., Matsuura, Y., et al. (1997). Subcellular localization of hepatitis C virus structural proteins in the liver of transgenic mice. Jpn. J. Med. Sci. Biol. 50, 169-177. doi: 10.7883/yoken1952.50.169
50. Neufeldt, C. J., Joyce, M. A., Levin, A., Steenbergen, R. H., Pang, D., Shields, J., et al. (2013). Hepatitis C virus-induced cytoplasmic organelles use the nuclear transport machinery to establish an environment conducive to virus replication. PLoS Pathog. 9:e1003744. doi: 10.1371/journal.ppat.1003744
51. Ogino, T., Fukuda, H., Imajoh-Ohmi, S., Kohara, M., and Nomoto, A. (2004). Membrane binding properties and terminal residues of the mature hepatitis C virus capsid protein in insect cells. J. Virol. 78, 11766-11777. doi: 10.1128/JVI.78.21.11766-11777.2004
52. Okamoto, K., Mori, Y., Komoda, Y., Okamoto, T., Okochi, M., Takeda, M., et al. (2008). Intramembrane processing by signal peptide peptidase regulates the membrane localization of hepatitis C virus core protein and viral propagation. J. Virol. 82, 8349-8361. doi: 10.1128/JVI.00306-08
53. Overby, A. K., Popov, V. L., Niedrig, M., and Weber, F. (2010). Tick-borne encephalitis virus delays interferon induction and hides its double-stranded RNA in intracellular membrane vesicles. J. Virol. 84, 8470-8483. doi: 10.1128/JVI.00176-10
54. Paul, D., and Bartenschlager, R. (2013). Architecture and biogenesis of plus-strand RNA virus replication factories. World J. Virol. 2, 32-48. doi: 10.5501/wjv.v2.i2.32
55. Paul, D., Hoppe, S., Saher, G., Krijnse-Locker, J., and Bartenschlager, R. (2013). Morphological and biochemical characterization of the membranous hepatitis C virus replication compartment. J. Virol. 87, 10612-10627. doi: 10.1128/JVI.01370-13
56. Pichlmair, A., Kandasamy, K., Alvisi, G., Mulhern, O., Sacco, R., Habjan, M., et al. (2012). Viral immune modulators perturb the human molecular network by common and unique strategies. Nature 487, 486-490. doi: 10.1038/nature11289
57. Reiss, S., Rebhan, I., Backes, P., Romero-Brey, I., Erfle, H., Matula, P., et al. (2011). Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe 9, 32-45. doi: 10.1016/j.chom.2010.12.002
58. Romero-Brey, I., Merz, A., Chiramel, A., Lee, J. Y., Chlanda, P., Haselman, U., et al. (2012). Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog. 8:e1003056. doi: 10.1371/journal.ppat.1003056
59. Ruggieri, A., Dazert, E., Metz, P., Hofmann, S., Bergeest, J. P., Mazur, J., et al. (2012). Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 12, 71-85. doi: 10.1016/j.chom.2012.05.013
60. Sacco, R., Tsutsumi, T., Suzuki, R., Otsuka, M., Aizaki, H., Sakamoto, S., et al. (2003). Antiapoptotic regulation by hepatitis C virus core protein through up-regulation of inhibitor of caspase-activated DNase. Virology 317, 24-35. doi: 10.1016/j.virol.2003.08.028
61. Satoh, S., Hirota, M., Noguchi, T., Hijikata, M., Handa, H., and Shimotohno, K. (2000). Cleavage of hepatitis C virus nonstructural protein 5A by a caspase-like protease(s) in mammalian cells. Virology 270, 476-487. doi: 10.1006/viro.2000.0287
62. Sauter, D., Himmelsbach, K., Kriegs, M., Carvajal Yepes, M., and Hildt, E. (2009). Localization determines function: N-terminally truncated NS5A fragments accumulate in the nucleus and impair HCV replication. J. Hepatol. 50, 861-871. doi: 10.1016/j.jhep.2008.11.024
63. Shimakami, T., Hijikata, M., Luo, H., Ma, Y. Y., Kaneko, S., Shimotohno, K., et al. (2004). Effect of interaction between hepatitis C virus NS5A and NS5B on hepatitis C virus RNA replication with the hepatitis C virus replicon. J. Virol. 78, 2738-2748. doi: 10.1128/JVI.78.6.2738-2748.2004
64. Shoji, I. (2012). Roles of the two distinct proteasome pathways in hepatitis C virus infection. World J. Virol. 1, 44-50. doi: 10.5501/wjv.v1.i2.44
65. Stapleford, K. A., and Lindenbach, B. D. (2011). Hepatitis C virus NS2 coordinates virus particle assembly through physical interactions with the E1-E2 glycoprotein and NS3-NS4A enzyme complexes. J. Virol. 85, 1706-1717. doi: 10.1128/JVI.02268-10
66. Steinmann, E., Penin, F., Kallis, S., Patel, A. H., Bartenschlager, R., and Pietschmann, T. (2007). Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions. PLoS Pathog. 3:e103. doi: 10.1371/journal.ppat.0030103
67. Suzuki, R., Moriishi, K., Fukuda, K., Shirakura, M., Ishii, K., Shoji, I., et al. (2009). Proteasomal turnover of hepatitis C virus core protein is regulated by two distinct mechanisms: a ubiquitin-dependent mechanism and a ubiquitin-independent but PA28γ-dependent mechanism. J. Virol. 83, 2389-2392. doi: 10.1128/JVI.01690-08
68. Tran, E. J., Bolger, T. A., and Wente, S. R. (2007). SnapShot: nuclear transport. Cell 131, 420. doi: 10.1016/j.cell.2007.10.015
69. Truant, R., and Cullen, B. R. (1999). The arginine-rich domains present in human immunodeficiency virus type 1 Tat and Rev function as direct importin ß-dependent nuclear localization signals. Mol. Cell. Biol. 19, 1210-1217.
70. Wang, J. J., Liao, C. L., Chiou, Y. W., Chiou, C. T., Huang, Y. L., and Chen, L. K. (1997). Ultrastructure and localization of E proteins in cultured neuron cells infected with Japanese encephalitis virus. Virology 238, 30-39. doi: 10.1006/viro.1997.8791
71. Wang, T., Yu, B., Lin, L., Zhai, X., Han, Y., Qin, Y., et al. (2012). A functional nuclear localization sequence in the VP1 capsid protein of coxsackievirus B3. Virology 433, 513-521. doi: 10.1016/j.virol.2012.08.040
72. Yamane, D., Mcgivern, D. R., Wauthier, E., Yi, M., Madden, V. J., Welsch, C., et al. (2014). Regulation of the hepatitis C virus RNA replicase by endogenous lipid peroxidation. Nat. Med. 20, 927-935. doi: 10.1038/nm.3610
73. Yarbrough, M. L., Mata, M. A., Sakthivel, R., and Fontoura, B. M. (2014). Viral subversion of nucleocytoplasmic trafficking. Traffic 15, 127-140. doi: 10.1111/tra.12137
74. Zhang, Q., Gong, R., Qu, J., Zhou, Y., Liu, W., Chen, M., et al. (2012). Activation of the Ras/Raf/MEK pathway facilitates hepatitis C virus replication via attenuation of the interferon-JAK-STAT pathway. J. Virol. 86, 1544-1554. doi: 10.1128/JVI.00688-11
75. Zhang, X., Wu, K., Wang, D., Yue, X., Song, D., Zhu, Y., et al. (2007). Nucleocapsid protein of SARS-CoV activates interleukin-6 expression through cellular transcription factor NF-κB. Virology 365, 324-335. doi: 10.1016/j.virol.2007.04.009