Scavenger receptor BI and BII expression levels modulate hepatitis C virus infectivity

Journal of Virology

Volumn 81, Issue 7, 2007, Pages 3162-3169

  Grove, Joe ^a   Huby, Thierry ^b   Stamataki, Zania ^a   Vanwolleghem, Thomas ^c   Meuleman, Philip ^c   Farquhar, Michelle ^a   Schwarz, Anne ^a   Moreau, Martine ^b   Owen, James S ^d   Leroux Roels, Geert ^c   Balfe, Peter ^a   McKeating, Jane A ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b INSERM   (France)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

^d ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD81 ANTIGEN; CLATHRIN; GLYCOPROTEIN; LIPOPROTEIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY E2; SCAVENGER RECEPTOR B; SCAVENGER RECEPTOR BI; SCAVENGER RECEPTOR BII; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LINE; CONTROLLED STUDY; DISEASE MODEL; ENDOCYTOSIS; HEPATITIS C; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; MOUSE; NONHUMAN; PLASMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCID MOUSE; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS STRAIN;

ANIMALS; ANTIBODIES; CELL LINE; CRICETINAE; GENE EXPRESSION REGULATION; HEPACIVIRUS; HUMANS; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; PROTEIN BINDING; RECEPTORS, SCAVENGER; SCAVENGER RECEPTORS, CLASS B; SOLUBILITY; VIRAL ENVELOPE PROTEINS;

HEPATITIS C VIRUS; MUS;

EID: 33947365513     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02356-06     Document Type: Article

References (56)

1. Acton, S., A. Rigotti, K. T. Landschulz, S. Xu, H. H. Hobbs, and M. Krieger. 1996. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271:518-520.
2. Andre, P., F. Komurian-Pradel, S. Deforges, M. Perret, J. L. Berland, M. Sodoyer, S. Pol, C. Brechot, G. Paranhos-Baccala, and V. Lotteau. 2002. Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J. Virol. 76:6919-6928.
3. Bannert, N., D. Schenten, S. Craig, and J. Sodroski. 2000. The level of CD4 expression limits infection of primary rhesus monkey macrophages by a T-tropic simian immunodeficiency virus and macrophagetropic human immunodeficiency viruses. J. Virol. 74:10984-10993.
4. Bartosch, B., J. Dubuisson, and F. L. Cosset. 2003. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 197:633-642.
5. Bartosch, B., G. Verney, M. Dreux, P. Donot, Y. Morice, F. Penin, J. M. Pawlotsky, D. Lavillette, and F. L. Cosset. 2005. An interplay between hypervariable region 1 of the hepatitis C virus E2 glycoprotein, the scavenger receptor BI, and high-density lipoprotein promotes both enhancement of infection and protection against neutralizing antibodies. J. Virol. 79:8217-8229.
6. Bartosch, B., A. Vitelli, C. Granier, C. Goujon, J. Dubuisson, S. Pascale, E. Scarselli, R. Cortese, A. Nicosia, and F. L. Cosset. 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.
7. Blanchard, E., S. Belouzard, L. Goueslain, T. Wakita, J. Dubuisson, C. Wychowski, and Y. Rouille. 2006. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J. Virol. 80:6964-6972.
8. Blight, K. J., J. A. McKeating, and C. M. Rice. 2002. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76:13001-13014.
9. Chisholm, J. W., E. R. Burleson, G. S. Shelness, and J. S. Parks. 2002. ApoA-I secretion from HepG2 cells: evidence for the secretion of both lipid-poor apoA-I and intracellularly assembled nascent HDL. J. Lipid Res. 43:36-44.
10. Codran, A., C. Royer, D. Jaeck, M. Bastien-Valle, T. F. Baumert, M. P. Kieny, C. A. Pereira, and J. P. Martin. 2006. Entry of hepatitis C virus pseudotypes into primary human hepatocytes by clathrin-dependent endocytosis. J. Gen. Virol. 87:2583-2593.
11. Domitrovich, A. M., D. J. Felmlee, and A. Siddiqui. 2005. Hepatitis C virus nonstructural proteins inhibit apolipoprotein B100 secretion. J. Biol. Chem. 280:39802-39808.
12. Dreux, M., T. Pietschmann, C. Granier, C. Voisset, S. Ricard-Blum, P. E. Mangeot, Z. Keck, S. Foung, N. Vu-Dac, J. Dubuisson, R. Bartenschlager, D. Lavillette, and F. L. Cosset. 2006. High density lipoprotein inhibits hepatitis C virus neutralising antibodies by stimulating cell entry via activation of the scavenger receptor BI. J. Biol. Chem. 281:18285-18295.
13. Eckhardt, E. R., L. Cai, S. Shetty, Z. Zhao, A. Szanto, N. R. Webb, and D. R. Van der Westhuyzen. 2006. High density lipoprotein endocytosis by scavenger receptor SR-BII is clathrin-dependent and requires a carboxyl-terminal dileucine motif. J. Biol. Chem. 281:4348-4353.
14. Eckhardt, E. R., L. Cai, B. Sun, N. R. Webb, and D. R. van der Westhuyzen. 2004. High density lipoprotein uptake by scavenger receptor SR-BII. J. Biol. Chem. 279:14372-14381.
15. Falkowska, E., R. J. Durso, J. P. Gardner, E. G. Cormier, R. A. Arrigale, R. N. Ogawa, G. P. Donovan, P. J. Maddon, W. C. Olson, and T. Dragic. 2006. L-SIGN (CD209L) isoforms differently mediate trans-infection of hepatoma cells by hepatitis C virus pseudoparticles. J. Gen. Virol. 87:2571-2576.
16. Flint, M., J. M. Thomas, C. M. Maidens, C. Shotton, S. Levy, W. S. Barclay, and J. A. McKeating. 1999. Functional analysis of cell surface-expressed hepatitis C virus E2 glycoprotein. J. Virol. 73:6782-6790.
17. Flint, M., T. von Hahn, J. Zhang, M. Farquhar, C. T. Jones, P. Balfe, C. M. Rice, and J. A. McKeating. 2006. Diverse CD81 proteins support hepatitis C virus infection. J. Virol. 80:11331-11342.
18. Gardner, J. P., R. J. Durso, R. R. Arrigale, G. P. Donovan, P. J. Maddon, T. Dragic, and W. C. Olson. 2003. L-SIGN (CD 209L) is a liver-specific capture receptor for hepatitis C virus. Proc. Natl. Acad. Sci. USA 100:4498-4503.
19. Higashi, Y., H. Itabe, H. Fukase, M. Mori, Y. Fujimoto, and T. Takano. 2003. Transmembrane lipid transfer is crucial for providing neutral lipids during very low density lipoprotein assembly in endoplasmic reticulum. J. Biol. Chem. 278:21450-21458.
20. Hsu, M., J. Zhang, M. Flint, C. Logvinoff, C. Cheng-Mayer, C. M. Rice, and J. A. McKeating. 2003. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. USA 100:7271-7276.
21. Kapadia, S. B., H. Barth, T. Baumert, J. A. McKeating, and F. V. Chisari. 2006. 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.
22. Koutsoudakis, G., A. Kaul, E. Steinmann, S. Kallis, V. Lohmann, T. Pietschmann, and R. Bartenschlager. 2006. Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J. Virol. 80:5308-5320.
23. Krieger, M. 2001. Scavenger receptor class B type I is a multiligand HDL receptor that influences diverse physiologic systems. J. Clin. Investig. 108: 793-797.
24. Lavillette, D., A. W. Tarr, C. Voisset, P. Donot, B. Bartosch, C. Bain, A. H. Patel, J. Dubuisson, J. K. Ball, and F. L. Cosset. 2005. Characterization of host-range and cell entry properties of the major genotypes and subtypes of hepatitis C virus. Hepatology 41:265-274.
25. Lindenbach, B. D., M. J. Evans, A. J. Syder, B. Wolk, T. L. Tellinghuisen, C. C. Liu, T. Maruyama, R. O. Hynes, D. R. Burton, J. A. McKeating, and C. M. Rice. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626.
26. Lindenbach, B. D., P. Meuleman, A. Ploss, T. Vanwolleghem, A. J. Syder, J. A. McKeating, R. E. Lanford, S. M. Feinstone, M. E. Major, G. Leroux-Roels, and C. M. Rice. 2006. Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc. Natl. Acad. Sci. USA 103:3805-3809.
27. Lozach, P. Y., H. Lortat-Jacob, A. de Lacroix de Lavalette, I. Staropoli, S. Foung, A. Amara, C. Houles, F. Fieschi, O. Schwartz, J. L. Virelizier, F. Arenzana-Seisdedos, and R. Altmeyer. 2003. DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2. J. Biol. Chem. 278:20358-20366.
28. Maillard, P., T. Huby, U. Andreo, M. Moreau, J. Chapman, and A. Budkowska. 2006. The interaction of natural hepatitis C virus with human scavenger receptor SR-BI/Cla1 is mediated by ApoB-containing lipoproteins. FASEB J. 20:735-737.
29. McKeating, J. A., L. Q. Zhang, C. Logvinoff, M. Flint, J. Zhang, J. Yu, D. Butera, D. D. Ho, L. B. Dustin, C. M. Rice, and P. Balfe. 2004. Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner. J. Virol. 78:8496-8505.
30. Meertens, L., C. Bertaux, and T. Dragic. 2006. Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles. J. Virol. 80:11571-11578.
31. Mercer, D. F., D. E. Schiller, J. F. Elliott, D. N. Douglas, C. Hao, A. Rinfret, W. R. Addison, K. P. Fischer, T. A. Churchill, J. R. Lakey, D. L. Tyrrell, and N. M. Kneteman. 2001. Hepatitis C virus replication in mice with chimeric human livers. Nat. Med. 7:927-933.
32. Meuleman, P., L. Libbrecht, R. De Vos, B. de Hemptinne, K. Gevaert, J. Vandekerckhove, T. Roskams, and G. Leroux-Roels. 2005. Morphological and biochemical characterization of a human liver in a uPA-SCID mouse chimera. Hepatology 41:847-856.
33. Mulcahy, J. V., D. R. Riddell, and J. S. Owen. 2004. Human scavenger receptor class B type II (SR-BII) and cellular cholesterol efflux. Biochem. J. 377:741-747.
34. Nieland, T. J., M. Ehrlich, M. Krieger, and T. Kirchhausen. 2005. Endocytosis is not required for the selective lipid uptake mediated by murine SR-BI. Biochim. Biophys. Acta 1734:44-51.
35. Nielsen, S. U., M. F. Bassendine, A. D. Burt, C. Martin, W. Pumeechockchai, and G. L. Toms. 2006. Association between hepatitis C virus and very-low-density lipoprotein (VLDL)/LDL analyzed in iodixanol density gradients. J. Virol. 80:2418-2428.
36. Pietschmann, T., A. Kaul, G. Koutsoudakis, A. Shavinskaya, S. Kallis, E. Steinmann, K. Abid, F. Negro, M. Dreux, F. L. Cosset, and R. Bartenschlager. 2006. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. USA 103: 7408-7413.
37. Pileri, P., Y. Uematsu, S. Campagnoli, G. Galli, F. Falugi, R. Petracca, A. J. Weiner, M. Houghton, D. Rosa, G. Grandi, and S. Abrignani. 1998. Binding of hepatitis C virus to CD81. Science 282:938-941.
38. Pitas, R. E., T. L. Innerarity, J. N. Weinstein, and R. W. Mahley. 1981. Acetoacetylated lipoproteins used to distinguish fibroblasts from macrophages in vitro by fluorescence microscopy. Arteriosclerosis 1:177-185.
39. Piatt, E. J., K. Wehrly, S. E. Kuhmann, B. Chesebro, and D. Kabat. 1998. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J. Virol. 72:2855-2864.
40. Pohlmann, S., J. Zhang, F. Baribaud, Z. Chen, G. J. Leslie, G. Lin, A. Granelli-Pipemo, R. W. Doms, C. M. Rice, and J. A. McKeating. 2003. Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR. J. Virol. 77:4070-4080.
41. Reaven, E., Y. Cortez, S. Leers-Sucheta, A. Nomoto, and S. Azhar. 2004. Dimerization of the scavenger receptor class B type I: formation, function, and localization in diverse cells and tissues. J. Lipid Res. 45:513-528.
42. Rhainds, D., and L. Brissette. 2004. The role of scavenger receptor class B type I (SR-BI) in lipid trafficking. Defining the rules for lipid traders. Int. J. Biochem. Cell Biol. 36:39-77.
43. Scarselli, E., H. Ansuini, R. Cerino, R. M. Roccasecca, S. Acali, G. Filocamo, C. Traboni, A. Nicosia, R. Cortese, and A. Vitelli. 2002. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 21:5017-5025.
44. Silver, D. L. 2004. SR-BI and protein-protein interactions in hepatic high density lipoprotein metabolism. Rev. Endocrine Metabolic Disorders 5:327-333.
45. Thomssen, R., S. Bonk, and A. Thiele. 1993. Density heterogeneities of hepatitis C virus in human sera due to the binding of beta-lipoproteins and immunoglobulins. Med. Microbiol. Immunol. 182:329-334.
46. Treguier, M., C. Doucet, M. Moreau, C. Dachet, J. Thillet, M. J. Chapman, and T. Huby. 2004. Transcription factor sterol regulatory element binding protein 2 regulates scavenger receptor Cla-1 gene expression. Arterioscler. Thromb. Vasc. Biol. 24:2358-2364.
47. Tscherne, D. M., C. T. Jones, M. J. Evans, B. D. Lindenbach, J. A. McKeating, and C. M. Rice. 2006. Time- and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. J. Virol. 80:1734-1741.
48. Voisset, C., N. Callens, E. Blanchard, A. Op De Beeck, J. Dubuisson, and N. Vu-Dac. 2005. High density lipoproteins facilitate hepatitis C virus entry through the scavenger receptor class B type I. J. Biol. Chem. 280:7793-7799.
49. Voisset, C., A. O. de Beeck, P. Horellou, M. Dreux, T. Gustot, G. Duverlie, F. L. Cosset, N. Vu-Dac, and J. Dubuisson. 2006. High-density lipoproteins reduce the neutralizing effect of hepatitis C virus (HCV)-infected patient antibodies by promoting HCV entry. J. Gen. Virol. 87:2577-2581.
50. von Hahn, T., B. D. Lindenbach, A. Boullier, O. Quehenberger, M. Paulson, C. M. Rice, and J. A. McKeating. 2006. Oxidized low-density lipoprotein inhibits hepatitis C virus cell entry in human hepatoma cells. Hepatology 43:932-942.
51. Wakita, T., T. Pietschmann, T. Kato, T. Date, M. Miyamoto, Z. Zhao, K. Murthy, A. Habermann, H. G. Krausslich, M. Mizokami, R. Bartenschlager, and T. J. Liang. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-796.
52. Webb, N. R., P. M. Connell, G. A. Graf, E. J. Smart, W. J. de Villiers, F. C. de Beer, and D. R. van der Westhuyzen. 1998. SR-BII, an isoform of the scavenger receptor BI containing an alternate cytoplasmic tail, mediates lipid transfer between high density lipoprotein and cells. J. Biol. Chem. 273: 15241-15248.
53. Zennou, V., C. Serguera, C. Sarkis, P. Colin, E. Perret, J. Mallet, and P. Charneau. 2001. The HIV-1 DNA flap stimulates HIV vector-mediated cell transduction in the brain. Nat. Biotechnol. 19:446-450.
54. Zhang, J., G. Randall, A. Higginbottom, P. Monk, C. M. Rice, and J. A. McKeating. 2004. CD81 is required for hepatitis C virus glycoprotein-mediated viral infection. J. Virol. 78:1448-1455.
55. Zhong, J., P. Gastaminza, G. Cheng, S. Kapadia, T. Kato, D. R. Burton, S. F. Wieland, S. L. Uprichard, T. Wakita, and F. V. Chisari. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. USA 102:9294-9299.
56. Zhong, J., P. Gastaminza, J. Chung, Z. Stamataki, M. Isogawa, G. Cheng, J. A. McKeating, and F. V. Chisari. 2006. Persistent hepatitis C virus infection in vitro: coevolution of virus and host. J. Virol. 80:11082-11093.