RNA interference and single particle tracking analysis of hepatitis C virus endocytosis

PLoS Pathogens

Volumn 5, Issue 12, 2009, Pages

  Coller, Kelly E ^a   Berger, Kristi L ^a   Heaton, Nicholas S ^a   Cooper, Jacob D ^a   Yoon, Rosa ^a   Randall, Glenn ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CBL PROTEIN; CD81 ANTIGEN; CLATHRIN LIGHT CHAIN; CLAUDIN 1; RAB PROTEIN; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE E3; RNA; VIRUS PROTEIN;

ACTIN POLYMERIZATION; ANALYTIC METHOD; ARTICLE; CELL CULTURE; CELL MEMBRANE; CELL MIGRATION; CYTOSKELETON; ENDOCYTOSIS; ENDOSOME; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INTERNALIZATION; NONHUMAN; PROTEIN INTERACTION; RNA INTERFERENCE; SINGLE PARTICLE TRACKING ANALYSIS; TIGHT JUNCTION; VIRUS GENE; VIRUS PARTICLE; ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; GENE LIBRARY; GENETICS; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; VIRUS ATTACHMENT; VIRUS ENTRY;

HEPATITIS C VIRUS;

ANIMALS; ENDOCYTOSIS; FLUORESCENT ANTIBODY TECHNIQUE; GENE LIBRARY; GENES, VIRAL; HEPACIVIRUS; HUMANS; POLYMERASE CHAIN REACTION; RNA; RNA INTERFERENCE; VIRAL PROTEINS; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 74549150609     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000702     Document Type: Article

References (74)

1. Lemon SM, Walker C, Alter MJ, Yi M (2007) Hepatitis C virus. In: Knipe DM, Howley PM, eds. Fields virology. Philadelphia: Lippincott Williams & Wilkins. pp 1253-1304.
2. Bartosch B, Vitelli A, Granier C, Goujon C, Dubuisson J, et al. (2003) Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 278: 41624-41630.
3. 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.
4. Grove J, Huby T, Stamataki Z, Vanwolleghem T, Meuleman P, et al. (2007) Scavenger receptor BI and BII expression levels modulate hepatitis C virus infectivity. J Virol 81: 3162-3169.
5. Hsu M, Zhang J, Flint M, Logvinoff C, Cheng-Mayer C, et al. (2003) Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc Natl Acad Sci U S A 100: 7271-7276.
6. Kapadia SB, Barth H, Baumert T, McKeating JA, Chisari FV (2007) Initiation of hepatitis C virus infection is dependent on cholesterol and cooperativity between CD81 and scavenger receptor B type I. J Virol 81: 374-383.
7. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, et al. (2005) Complete replication of hepatitis C virus in cell culture. Science 309: 623-626.
8. Molina S, Castet V, Fournier-Wirth C, Pichard-Garcia L, Avner R, et al. (2007) The low-density lipoprotein receptor plays a role in the infection of primary human hepatocytes by hepatitis C virus. J Hepatol 46: 411-419.
9. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, et al. (1998) Binding of hepatitis C virus to CD81. Science 282: 938-941.
10. 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.
11. 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.
12. Drummer HE, Maerz A, Poumbourios P (2003) Cell surface expression of functional hepatitis C virus E1 and E2 glycoproteins. FEBS Lett 546: 385-390.
13. Zhang J, Randall G, Higginbottom A, Monk P, Rice CM, et al. (2004) CD81 is required for hepatitis C virus glycoprotein-mediated viral infection. J Virol 78: 1448-1455.
14. McKeating JA, Zhang LQ, Logvinoff C, Flint M, Zhang J, et al. (2004) Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner. J Virol 78: 8496-8505.
15. Andre P, Komurian-Pradel F, Deforges S, Perret M, Berland JL, et al. (2002) Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J Virol 76: 6919-6928.
16. Diaz O, Delers F, Maynard M, Demignot S, Zoulim F, et al. (2006) Preferential association of Hepatitis C virus with apolipoprotein B48-containing lipoproteins. J Gen Virol 87: 2983-2991.
17. Nielsen SU, Bassendine MF, Burt AD, Martin C, Pumeechockchai W, et al. (2006) Association between hepatitis C virus and very-low-density lipoprotein (VLDL)/LDL analyzed in iodixanol density gradients. J Virol 80: 2418-2428.
18. Thomssen R, Bonk S, Propfe C, Heermann KH, Kochel HG, et al. (1992) Association of hepatitis C virus in human sera with beta-lipoprotein. Med Microbiol Immunol 181: 293-300.
19. Gastaminza P, Kapadia SB, Chisari FV (2006) Differential biophysical properties of infectious intracellular and secreted hepatitis C virus particles. J Virol 80: 11074-11081.
20. Agnello V, Abel G (1997) Localization of hepatitis C virus in cutaneous vasculitic lesions in patients with type II cryoglobulinemia. Arthritis Rheum 40: 2007-2015.
21. Monazahian M, Bohme I, Bonk S, Koch A, Scholz C, et al. (1999) Low density lipoprotein receptor as a candidate receptor for hepatitis C virus. J Med Virol 57: 223-229.
22. Zeisel MB, Koutsoudakis G, Schnober EK, Haberstroh A, Blum HE, et al. (2007) Scavenger receptor class B type I is a key host factor for hepatitis C virus infection required for an entry step closely linked to CD81. Hepatology 46: 1722-1731.
23. Dreux M, Dao Thi VL, Fresquet J, Guerin M, Julia Z, et al. (2009) Receptor complementation and mutagenesis reveal SR-BI as an essential HCV entry factor and functionally imply its intra- and extra-cellular domains. PLoS Pathog 5: e1000310. doi:10.1371/journal.ppat.1000310.
24. Liu S, Yang W, Shen L, Turner JR, Coyne CB, et al. (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.
25. Meertens L, Bertaux C, Cukierman L, Cormier E, Lavillette D, et al. (2008) The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. J Virol 82: 3555-3560.
26. Zheng A, Yuan F, Li Y, Zhu F, Hou P, et al. (2007) Claudin-6 and claudin-9 function as additional coreceptors for hepatitis C virus. J Virol 81: 12465-12471.
27. Brazzoli M, Bianchi A, Filippini S, Weiner A, Zhu Q, et al. (2008) CD81 is a central regulator of cellular events required for hepatitis C virus infection of human hepatocytes. J Virol 82: 8316-8329.
28. 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.
29. Meertens L, Bertaux C, Dragic T (2006) Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrincoated vesicles. J Virol 80: 11571-11578.
30. Koutsoudakis G, Kaul A, Steinmann E, Kallis S, Lohmann V, et al. (2006) Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol 80: 5308-5320.
31. Tscherne DM, Jones CT, Evans MJ, Lindenbach BD, McKeating JA, et al. (2006) Time- and temperature-dependent activation of hepatitis C virus for lowpH-triggered entry. J Virol 80: 1734-1741.
32. Moradpour D, Penin F, Rice CM (2007) Replication of hepatitis C virus. Nat Rev Microbiol 5: 453-463.
33. Berger KL, Cooper JD, Heaton NS, Yoon R, Oakland TE, et al. (2009) Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication. Proc Natl Acad Sci U S A 106: 7577-7582.
34. Ng TI, Mo H, Pilot-Matias T, He Y, Koev G, et al. (2007) Identification of host genes involved in hepatitis C virus replication by small interfering RNA technology. Hepatology 45: 1413-1421.
35. Randall G, Panis M, Cooper JD, Tellinghuisen TL, Sukhodolets KE, et al. (2007) Cellular cofactors affecting hepatitis C virus infection and replication. Proc Natl Acad Sci U S A 104: 12884-12889.
36. Supekova L, Supek F, Lee J, Chen S, Gray N, et al. (2008) Identification of human kinases involved in hepatitis C virus replication by small interference RNA library screening. J Biol Chem 283: 29-36.
37. Tai AW, Benita Y, Peng LF, Kim SS, Sakamoto N, et al. (2009) A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host Microbe 5: 298-307.
38. Vaillancourt FH, Pilote L, Cartier M, Lippens J, Liuzzi M, et al. (2009) Identification of a lipid kinase as a host factor involved in hepatitis C virus RNA replication. Virology 387: 5-10.
39. van der Schaar HM, Rust MJ, Waarts BL, van der Ende-Metselaar H, Kuhn RJ, et al. (2007) Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking. J Virol 81: 12019-12028.
40. Musch MW, Arvans DL, Walsh-Reitz MM, Uchiyama K, Fukuda M, et al. (2007) Synaptotagmin I binds intestinal epithelial NHE3 and mediates cAMPand Ca2+-induced endocytosis by recruitment of AP2 and clathrin. Am J Physiol Gastrointest Liver Physiol 292: G1549-1558.
41. Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, et al. (2002) Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108: 261-269.
42. van der Schaar HM, Rust MJ, Chen C, van der Ende-Metselaar H, Wilschut J, et al. (2008) Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog 4: e1000244. doi:10.1371/journal. ppat.1000244.
43. Brandenburg B, Lee LY, Lakadamyali M, Rust MJ, Zhuang X, et al. (2007) Imaging Poliovirus Entry in Live Cells. PLoS Biol 5: e183. doi:10.1371/ journal.pbio.0050183.
44. Lakadamyali M, Rust MJ, Babcock HP, Zhuang X (2003) Visualizing infection of individual influenza viruses. Proc Natl Acad Sci U S A 100: 9280-9285.
45. Hijikata M, Shimizu YK, Kato H, Iwamoto A, Shih JW, et al. (1993) Equilibrium centrifugation studies of hepatitis C virus: evidence for circulating immune complexes. J Virol 67: 1953-1958.
46. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, et al. (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11: 791-796.
47. Hadlock KG, Lanford RE, Perkins S, Rowe J, Yang Q, et al. (2000) Human monoclonal antibodies that inhibit binding of hepatitis C virus E2 protein to CD81 and recognize conserved conformational epitopes. J Virol 74: 10407-10416.
48. Huang CY, Lu TY, Bair CH, Chang YS, Jwo JK, et al. (2008) A novel cellular protein, VPEF, facilitates vaccinia virus penetration into HeLa cells through fluid phase endocytosis. J Virol 82: 7988-7999.
49. Lehmann MJ, Sherer NM, Marks CB, Pypaert M, Mothes W (2005) Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J Cell Biol 170: 317-325.
50. Schelhaas M, Ewers H, Rajamaki ML, Day PM, Schiller JT, et al. (2008) Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions. PLoS Pathog 4: e1000148. doi:10.1371/journal. ppat.1000148.
51. Tiwari V, Oh MJ, Kovacs M, Shukla SY, Valyi-Nagy T, et al. (2008) Role for nectin-1 in herpes simplex virus 1 entry and spread in human retinal pigment epithelial cells. Febs J 275: 5272-5285.
52. Shen L, Turner JR (2005) Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell 16: 3919-3936.
53. Merrifield CJ, Feldman ME, Wan L, Almers W (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4: 691-698.
54. Yarar D, Waterman-Storer CM, Schmid SL (2005) A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16: 964-975.
55. Schwarz AK, Grove J, Hu K, Mee CJ, Balfe P, et al. (2009) Hepatoma cell density promotes Claudin-1 and scavenger receptor BI expression and hepatitis C virus internalization. J Virol.
56. Joazeiro CA, Wing SS, Huang H, Leverson JD, Hunter T, et al. (1999) The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 286: 309-312.
57. Pelkmans L, Puntener D, Helenius A (2002) Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296: 535-539.
58. Van Minnebruggen G, Van de Walle GR, Favoreel HW, Nauwynck HJ, Pensaert MB (2002) Temporary disturbance of actin stress fibers in swine kidney cells during pseudorabies virus infection. Vet Microbiol 86: 89-94.
59. Chan YG, Cardwell MM, Hermanas TM, Uchiyama T, Martinez JJ (2009) Rickettsial outer-membrane protein B (rOmpB) mediates bacterial invasion through Ku70 in an actin, c-Cbl, clathrin and caveolin 2-dependent manner. Cell Microbiol 11: 629-644.
60. Veiga E, Cossart P (2005) Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nat Cell Biol 7: 894-900.
61. Krishnan MN, Ng A, Sukumaran B, Gilfoy FD, Uchil PD, et al. (2008) RNA interference screen for human genes associated with West Nile virus infection. Nature 455: 242-245.
62. Mee CJ, Grove J, Harris HJ, Hu K, Balfe P, et al. (2008) Effect of cell polarization on hepatitis C virus entry. J Virol 82: 461-470.
63. Mee CJ, Harris HJ, Farquhar MJ, Wilson G, Reynolds G, et al. (2009) Polarization restricts hepatitis C virus entry into HepG2 hepatoma cells. J Virol 83: 6211-6221.
64. Reynolds GM, Harris HJ, Jennings A, Hu K, Grove J, et al. (2008) Hepatitis C virus receptor expression in normal and diseased liver tissue. Hepatology 47: 418-427.
65. 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.
66. Witteveldt J, Evans MJ, Bitzegeio J, Koutsoudakis G, Owsianka AM, et al. (2009) CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells. J Gen Virol 90: 48-58.
67. 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.
68. Mateu G, Donis RO, Wakita T, Bukh J, Grakoui A (2008) Intragenotypic JFH1 based recombinant hepatitis C virus produces high levels of infectious particles but causes increased cell death. Virology 376: 397-407.
69. Randall G, Chen L, Panis M, Fischer AK, Lindenbach BD, et al. (2006) Silencing of USP18 potentiates the antiviral activity of interferon against hepatitis C virus infection. Gastroenterology 131: 1584-1591.
70. Zennou V, Petit C, Guetard D, Nerhbass U, Montagnier L, et al. (2000) HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 101: 173-185.
71. Philippe S, Sarkis C, Barkats M, Mammeri H, Ladroue C, et al. (2006) Lentiviral vectors with a defective integrase allow efficient and sustained transgene expression in vitro and in vivo. Proc Natl Acad Sci U S A 103: 17684-17689.
72. Randall G, Grakoui A, Rice CM (2003) Clearance of replicating hepatitis C virus replicon RNAs in cell culture by small interfering RNAs. Proc Natl Acad Sci U S A 100: 235-240.
73. Sage D, Neumann FR, Hediger F, Gasser SM, Unser M (2005) Automatic tracking of individual fluorescence particles: application to the study of chromosome dynamics. IEEE Trans Image Process 14: 1372-1383.
74. Levi V, Gratton E (2007) Exploring dynamics in living cells by tracking single particles. Cell Biochem Biophys 48: 1-15.