Functional characterization of nuclear localization and export signals in hepatitis C virus proteins and their role in the membranous web

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Levin, Aviad ^a,b   Neufeldt, Christopher J ^b   Pang, Daniel ^a   Wilson, Kristen ^a   Loewen Dobler, Darci ^a   Joyce, Michael A ^a   Wozniak, Richard W ^b   Tyrrell, D Lorne J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; HEPATITIS C VIRUS PROTEIN; IMPORTIN ALPHA5; IMPORTIN BETA3; KARYOPHERIN ALPHA; KARYOPHERIN BETA; UNCLASSIFIED DRUG; VIRUS PROTEIN; CORE PROTEIN; HEPATITIS C ANTIGEN; MESSENGER RNA; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; NUCLEOPORIN; PEPTIDE FRAGMENT;

ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; HEPATITIS C; HEPATITIS C VIRUS; IN VITRO STUDY; LIFE CYCLE STAGE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; VIRUS IDENTIFICATION; VIRUS MORPHOLOGY; VIRUS REPLICATION; ACTIVE TRANSPORT; AMINO ACID SEQUENCE; CELL CULTURE; CELL MEMBRANE; CELL NUCLEUS; CELL PROLIFERATION; CYTOPLASM; GENETICS; HEPACIVIRUS; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY; WESTERN BLOTTING;

HEPATITIS C VIRUS;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; BLOTTING, WESTERN; CELL MEMBRANE; CELL NUCLEUS; CELL PROLIFERATION; CELLS, CULTURED; CYTOPLASM; HEPACIVIRUS; HEPATITIS C; HEPATITIS C ANTIGENS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR EXPORT SIGNALS; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PORE COMPLEX PROTEINS; PEPTIDE FRAGMENTS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VIRAL CORE PROTEINS; VIRUS REPLICATION;

EID: 84915748288     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114629     Document Type: Article

References (81)

1. Alter MJ, Margolis HS, Krawczynski K, Judson FN, Mares A, et al. (1992) The natural history of community-acquired hepatitis C in the United States. The Sentinel Counties Chronic non-A, non-B Hepatitis Study Team. N Engl J Med 327: 1899-1905.
2. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, et al. (1989) Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244: 359-362.
3. Alter HJ, Seeff LB (2000) Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcome. Semin Liver Dis 20: 17-35.
4. Shepard CW, Finelli L, Alter MJ (2005) Global epidemiology of hepatitis C virus infection. Lancet Infect Dis 5: 558-567.
5. Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, et al. (2002) Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J Med Virol 68: 206-215.
6. Owen DM, Huang H, Ye J, Gale M, Jr. (2009) Apolipoprotein E on hepatitis C virion facilitates infection through interaction with low-density lipoprotein receptor. Virology 394: 99-108.
7. Agnello V, Abel G, Elfahal M, Knight GB, Zhang QX (1999) Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. Proc Natl Acad Sci U S A 96: 12766-12771.
8. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, et al. (1998) Binding of hepatitis C virus to CD81. Science 282: 938-941.
9. Cormier EG, Tsamis F, Kajumo F, Durso RJ, Gardner JP, et al. (2004) CD81 is an entry coreceptor for hepatitis C virus. Proc Natl Acad Sci U S A 101: 7270-7274.
10. Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S, et al. (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. Timpe JM, Stamataki Z, Jennings A, Hu K, Farquhar MJ, et al. (2008) Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies. Hepatology 47: 17-24.
12. Ploss A, Evans MJ, Gaysinskaya VA, Panis M, You H, et al. (2009) Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457: 882-886.
13. Blanchard E, Belouzard S, Goueslain L, Wakita T, Dubuisson J, et al. (2006) Hepatitis C virus entry depends on clathrin-mediated endocytosis. J Virol 80: 6964-6972.
14. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, et al. (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446: 801-805.
15. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, et al. (2011) EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 17: 589-595.
16. Lavillette D, Pecheur EI, Donot P, Fresquet J, Molle J, et al. (2007) Characterization of fusion determinants points to the involvement of three discrete regions of both E1 and E2 glycoproteins in the membrane fusion process of hepatitis C virus. J Virol 81: 8752-8765.
17. Egger D, Wolk B, Gosert R, Bianchi L, Blum HE, et al. (2002) Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J Virol 76: 5974-5984.
18. Paul D, Hoppe S, Saher G, Krijnse-Locker J, Bartenschlager R (2013) Morphological and biochemical characterization of the membranous hepatitis C virus replication compartment. J Virol 87: 10612-10627.
19. Ferraris P, Beaumont E, Uzbekov R, Brand D, Gaillard J, et al. (2013) Sequential biogenesis of host cell membrane rearrangements induced by hepatitis C virus infection. Cell Mol Life Sci 70: 1297-1306.
20. Romero-Brey I, Merz A, Chiramel A, Lee JY, Chlanda P, et al. (2012) Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog 8: e1003056.
21. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, et al. (2007) The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol 9: 1089-1097.
22. Joyce MA, Tyrrell DL (2010) The cell biology of hepatitis C virus. Microbes Infect 12: 263-271.
23. Gastaminza P, Cheng G, Wieland S, Zhong J, LiaoW, et al. (2008) Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J Virol 82: 2120-2129.
24. Chang SJ, Hou MF, Tsai SM, Wu SH, Hou LA, et al. (2007) The association between lipid profiles and breast cancer among Taiwanese women. Clin Chem Lab Med 45: 1219-1223.
25. Huang H, Sun F, Owen DM, Li W, Chen Y, et al. (2007) Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins. Proc Natl Acad Sci U S A 104: 5848-5853.
26. den Boon JA, Ahlquist P (2010) Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol 64: 241-256.
27. Diaz A, Wang X, Ahlquist P (2010) Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. Proc Natl Acad Sci U S A 107: 16291-16296.
28. Miller DJ, Schwartz MD, Dye BT, Ahlquist P (2003) Engineered retargeting of viral RNA replication complexes to an alternative intracellular membrane. J Virol 77: 12193-12202.
29. Miyanari Y, Hijikata M, Yamaji M, Hosaka M, Takahashi H, et al. (2003) Hepatitis C virus non-structural proteins in the probable membranous compartment function in viral genome replication. The Journal of biological chemistry 278: 50301-50308.
30. Quinkert D, Bartenschlager R, Lohmann V (2005) Quantitative analysis of the hepatitis C virus replication complex. J Virol 79: 13594-13605.
31. Hsu NY, Ilnytska O, Belov G, Santiana M, Chen YH, et al. (2010) Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141: 799-811.
32. Neufeldt CJ, Joyce MA, Levin A, Steenbergen RH, Pang D, 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.
33. Overby AK, Weber F (2011) Hiding from intracellular pattern recognition receptors, a passive strategy of flavivirus immune evasion. Virulence 2: 238-240.
34. Marfori M, Mynott A, Ellis JJ, Mehdi AM, Saunders NF, et al. (2011) Molecular basis for specificity of nuclear import and prediction of nuclear localization. Biochim Biophys Acta 1813: 1562-1577.
35. Rodriguez MS, Dargemont C, Stutz F (2004) Nuclear export of RNA. Biol Cell 96: 639-655.
36. Kau TR, Way JC, Silver PA (2004) Nuclear transport and cancer: from mechanism to intervention. Nat Rev Cancer 4: 106-117.
37. Uchil PD, Kumar AV, Satchidanandam V (2006) Nuclear localization of flavivirus RNA synthesis in infected cells. J Virol 80: 5451-5464.
38. Mori Y, Okabayashi T, Yamashita T, Zhao Z, Wakita T, et al. (2005) Nuclear localization of Japanese encephalitis virus core protein enhances viral replication. J Virol 79: 3448-3458.
39. Cerutti A, Maillard P, Minisini R, Vidalain PO, Roohvand F, et al. (2011) Identification of a functional, CRM-1-dependent nuclear export signal in hepatitis C virus core protein. PLoS One 6: e25854.
40. Ide Y, Zhang L, Chen M, Inchauspe G, Bahl C, et al. (1996) Characterization of the nuclear localization signal and subcellular distribution of hepatitis C virus nonstructural protein NS5A. Gene 182: 203-211.
41. Suzuki R, Matsuura Y, Suzuki T, Ando A, Chiba J, et al. (1995) Nuclear localization of the truncated hepatitis C virus core protein with its hydrophobic C terminus deleted. J Gen Virol 76 ( Pt 1): 53-61.
42. Satterly N, Tsai PL, van Deursen J, Nussenzveig DR, Wang Y, et al. (2007) Influenza virus targets the mRNA export machinery and the nuclear pore complex. Proc Natl Acad Sci U S A 104: 1853-1858.
43. Schmitz A, Schwarz A, Foss M, Zhou L, Rabe B, et al. (2010) Nucleoporin 153 arrests the nuclear import of hepatitis B virus capsids in the nuclear basket. PLoS Pathog 6: e1000741.
44. Gustin KE, Sarnow P (2001) Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J 20: 240-249.
45. Enninga J, Levy DE, Blobel G, Fontoura BM (2002) Role of nucleoporin induction in releasing an mRNA nuclear export block. Science 295: 1523-1525.
46. Khadka S, Vangeloff AD, Zhang C, Siddavatam P, Heaton NS, et al. (2011) A physical interaction network of dengue virus and human proteins. Mol Cell Proteomics 10: M111 012187.
47. Huang YP, Zhang SL, Cheng J, Wang L, Guo J, et al. (2005) Screening of genes of proteins interacting with p7 protein of hepatitis C virus from human liver cDNA library by yeast two-hybrid system. World J Gastroenterol 11: 4709-4714.
48. Suzuki R, Sakamoto S, Tsutsumi T, Rikimaru A, Tanaka K, et al. (2005) Molecular determinants for subcellular localization of hepatitis C virus core protein. J Virol 79: 1271-1281.
49. Maqbool MA, Imache MR, Higgs MR, Carmouse S, Pawlotsky JM, et al. (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.
50. Song J, Nagano-Fujii M, Wang F, Florese R, Fujita T, et al. (2000) Nuclear localization and intramolecular cleavage of N-terminally deleted NS5A protein of hepatitis C virus. Virus Res 69: 109-117.
51. Muramatsu S, Ishido S, Fujita T, Itoh M, Hotta H (1997) Nuclear localization of the NS3 protein of hepatitis C virus and factors affecting the localization. J Virol 71: 4954-4961.
52. Germain MA, Chatel-Chaix L, Gagne B, Bonneil E, Thibault P, et al. (2014) Elucidating Novel Hepatitis C Virus/Host Interactions Using Combined Mass Spectrometry and Functional Genomics Approaches. Mol Cell Proteomics 13: 184-203.
53. Chung KM, Lee J, Kim JE, Song OK, Cho S, et al. (2000) Nonstructural protein 5A of hepatitis C virus inhibits the function of karyopherin beta3. J Virol 74: 5233-5241.
54. Chang SC, Yen JH, Kang HY, Jang MH, Chang MF (1994) Nuclear localization signals in the core protein of hepatitis C virus. Biochem Biophys Res Commun 205: 1284-1290.
55. Derossi D, Chassaing G, Prochiantz A (1998) Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol 8: 84-87.
56. Guttler T, Madl T, Neumann P, Deichsel D, Corsini L, et al. (2010) NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nat Struct Mol Biol 17: 1367-1376.
57. Leung SW, Harreman MT, Hodel MR, Hodel AE, Corbett AH (2003) Dissection of the karyopherin alpha nuclear localization signal (NLS)-binding groove: functional requirements for NLS binding. J Biol Chem 278: 41947-41953.
58. Hu CD, Kerppola TK (2003) Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat Biotechnol 21: 539-545.
59. Hu CD, Chinenov Y, Kerppola TK (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 9: 789-798.
60. Hanoulle X, Verdegem D, Badillo A, Wieruszeski JM, Penin F, et al. (2009) Domain 3 of non-structural protein 5A from hepatitis C virus is natively unfolded. Biochem Biophys Res Commun 381: 634-638.
61. Penin F, Dubuisson J, Rey FA, Moradpour D, Pawlotsky JM (2004) Structural biology of hepatitis C virus. Hepatology 39: 5-19.
62. Kalderon D, Roberts BL, Richardson WD, Smith AE (1984) A short amino acid sequence able to specify nuclear location. Cell 39: 499-509.
63. Levin A, Hayouka Z, Friedler A, Loyter A (2010) Over-expression of the HIV-1 Rev promotes death of nondividing eukaryotic cells. Virus Genes 40: 341-346.
64. Sainz B, Jr., Barretto N, Martin DN, Hiraga N, Imamura M, et al. (2012) Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat Med 18: 281-285.
65. Herker E, Harris C, Hernandez C, Carpentier A, Kaehlcke K, et al. (2010) Efficient hepatitis C virus particle formation requires diacylglycerol acyltransferase-1. Nat Med 16: 1295-1298.
66. de Chassey B, Navratil V, Tafforeau L, Hiet MS, Aublin-Gex A, et al. (2008) Hepatitis C virus infection protein network. Mol Syst Biol 4: 230.
67. Levin A, Hayouka Z, Friedler A, Loyter A (2010) Transportin 3 and importin alpha are required for effective nuclear import of HIV-1 integrase in virus-infected cells. Nucleus 1: 422-431.
68. Ashfaq UA, Javed T, Rehman S, Nawaz Z, Riazuddin S (2011) An overview of HCV molecular biology, replication and immune responses. Virol J 8: 161.
69. Hughes M, Griffin S, Harris M (2009) Domain III of NS5A contributes to both RNA replication and assembly of hepatitis C virus particles. J Gen Virol 90: 1329-1334.
70. Santolini E, Migliaccio G, La Monica N (1994) Biosynthesis and biochemical properties of the hepatitis C virus core protein. J Virol 68: 3631-3641.
71. Bird G, O'Donnell M, Moroianu J, Garcea RL (2008) Possible role for cellular karyopherins in regulating polyomavirus and papillomavirus capsid assembly. J Virol 82: 9848-9857.
72. Katta SS, Smoyer CJ, Jaspersen SL (2014) Destination: inner nuclear membrane. Trends Cell Biol 24: 221-229.
73. Strawn LA, Shen T, Shulga N, Goldfarb DS, Wente SR (2004) Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat Cell Biol 6: 197-206.
74. Makhnevych T, Lusk CP, Anderson AM, Aitchison JD, Wozniak RW (2003) Cell cycle regulated transport controlled by alterations in the nuclear pore complex. Cell 115: 813-823.
75. Jakel S, Mingot JM, Schwarzmaier P, Hartmann E, Gorlich D (2002) Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains. EMBO J 21: 377-386.
76. Walther TC, Askjaer P, Gentzel M, Habermann A, Griffiths G, et al. (2003) RanGTP mediates nuclear pore complex assembly. Nature 424: 689-694.
77. Lusk CP, Makhnevych T, Marelli M, Aitchison JD, Wozniak RW (2002) Karyopherins in nuclear pore biogenesis: a role for Kap121p in the assembly of Nup53p into nuclear pore complexes. J Cell Biol 159: 267-278.
78. Blight KJ, McKeating JA, Rice CM (2002) Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 76: 13001-13014.
79. Vrolijk JM, Kaul A, Hansen BE, Lohmann V, Haagmans BL, et al. (2003) A replicon-based bioassay for the measurement of interferons in patients with chronic hepatitis C. J Virol Methods 110: 201-209.
80. Rosenbluh J, Hayouka Z, Loya S, Levin A, Armon-Omer A, et al. (2007) Interaction between HIV-1 Rev and integrase proteins: a basis for the development of anti-HIV peptides. J Biol Chem 282: 15743-15753.
81. Levin A, Hayouka Z, Helfer M, Brack-Werner R, Friedler A, et al. (2009) Peptides derived from HIV-1 integrase that bind Rev stimulate viral genome integration. PLoS One 4: e4155.