The scavenger receptor BI and its ligand, HDL: Partners in crime against HCV neutralizing antibodies

Journal of Viral Hepatitis

Volumn 14, Issue SUPPL. 1, 2007, Pages 68-76

  Dreux, M ^a,b,c   Cosset, F L ^a,b,c  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

Author keywords

HDL; HVC; HVR1; Immune escape; Neutralization; SR BI

Indexed keywords

GLYCOPROTEIN E2; HIGH DENSITY LIPOPROTEIN; LIGAND; LOW DENSITY LIPOPROTEIN; NEUTRALIZING ANTIBODY; SCAVENGER RECEPTOR BI;

ANTIBODY RESPONSE; ATTENUATION; CONFERENCE PAPER; HEPATITIS C VIRUS; HUMAN; HUMORAL IMMUNITY; IN VIVO STUDY; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN INTERACTION; VIRUS INFECTION;

ANIMALS; HEPATITIS C; HEPATITIS C ANTIBODIES; HUMANS; LIGANDS; LIPOPROTEINS, HDL; SCAVENGER RECEPTORS, CLASS B;

EID: 35448947907     PISSN: 13520504     EISSN: 13652893     Source Type: Journal    
DOI: 10.1111/j.1365-2893.2007.00919.x     Document Type: Conference Paper

References (95)

1. Pawlotsky JM. Hepatitis C virus genetic variability: pathogenic and clinical implications. Clin Liver Dis 2003 7: 45 66.
2. Cucchiarini M, Kammer AR, Grabscheid B et al. Vigorous peripheral blood cytotoxic T cell response during the acute phase of hepatitis C virus infection. Cell Immunol 2000 203: 111 123.
3. Diepolder HM, Zachoval R, Hoffmann RM et al. Possible mechanism involving T-lymphocyte response to non-structural protein 3 in viral clearance in acute hepatitis C virus infection. Lancet 1995 346: 1006 1007.
4. Thimme R, Oldach D, Chang KM, Steiger C, Ray SC, Chisari FV. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 2001 194: 1395 1406.
5. Takaki A, Wiese M, Maertens G et al. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat Med 2000 6: 578 582.
6. Cooper S EA, Adams EJ, Kansopon J et al. Analysis of a successful immune response against hepatitis C virus. Immunity 1999 10: 439 449.
7. Ishii K, Rosa D, Watanabe Y et al. High titers of antibodies inhibiting the binding of envelope to human cells correlate with natural resolution of chronic hepatitis C. Hepatology 1998 28: 1117 1120.
8. Racanelli V, Rehermann B. Hepatitis C virus infection: when silence is deception. Trends Immunol 2003 24: 456 464.
9. Bartosch B, Dubuisson J, Cosset FL. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 2003 197: 633 642.
10. Hsu M, Zhang J, Flint M et al. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc Natl Acad Sci U S A 2003 100: 7271 7276.
11. Lindenbach BD, Evans MJ, Syder AJ et al. Complete replication of hepatitis C virus in cell culture. Science 2005 309: 623 626.
12. Wakita T, Pietschmann T, Kato T et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 2005 11: 791 796.
13. Zhong J, Gastaminza P, Cheng G et al. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 2005 102: 9294 9299.
14. Prince AM, Brotman B, Lee DH, Ren L, Moore BS, Scheffel JW. Significance of the anti-E2 response in self-limited and chronic hepatitis C virus infections in chimpanzees and in humans. J Infect Dis 1999 180: 987 991.
15. Bassett SE, Thomas DL, Brasky KM, Lanford RE. Viral persistence, antibody to E1 and E2, and hypervariable region 1 sequence stability in hepatitis C virus-inoculated chimpanzees. J Virol 1999 73: 1118 1126.
16. Hadlock KG, Gish R, Rowe J et al. Cross-reactivity and clinical impact of the antibody response to hepatitis C virus second envelope glycoprotein (E2). J Med Virol 2001 65: 23 29.
17. Logvinoff C, Major ME, Oldach D et al. Neutralizing antibody response during acute and chronic hepatitis C virus infection. Proc Natl Acad Sci U S A 2004 101: 10149 10154.
18. Meunier JC, Engle RE, Faulk K et al. Evidence for cross-genotype neutralization of hepatitis C virus pseudo-particles and enhancement of infectivity by apolipoprotein C1. Proc Natl Acad Sci U S A 2005 102: 4560 4565.
19. Lavillette D, Tarr AW, Voisset C et al. Characterization of host-range and cell entry properties of hepatitis C virus of major genotypes and subtypes. Hepatology 2005 41: 265 274.
20. Pestka JM, Zeisel MB, Blaser E et al. Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc Natl Acad Sci U S A 2007 104: 6025 6030.
21. Farci P, Alter HJ, Wong DC et al. Prevention of hepatitis C virus infection in chimpanzees after antibody-mediated in vitro neutralization. Proc Natl Acad Sci U S A 1994 91: 7792 7796.
22. Farci P, Shimoda A, Wong D et al. Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proc Natl Acad Sci U S A 1996 93: 15394 15399.
23. Krawczynski K, Alter MJ, Tankersley DL et al. Effect of immune globulin on the prevention of experimental hepatitis C virus infection. J Infect Dis 1996 173: 822 828.
24. Feray C, Gigou M, Samuel D et al. Incidence of hepatitis C in patients receiving different preparations of hepatitis B immunoglobulins after liver transplantation. Ann Intern Med 1998 128: 810 816.
25. Yu MY, Bartosch B, Zhang P et al. Neutralizing antibodies to hepatitis C virus (HCV) in immune globulins derived from anti-HCV-positive plasma. Proc Natl Acad Sci U S A 2004 101: 7705 7710.
26. Christie JM, Healey CJ, Watson J et al. Clinical outcome of hypogammaglobulinaemic patients following outbreak of acute hepatitis C: 2 year follow up. Clin Exp Immunol 1997 110: 4 8.
27. Chapel HM, Christie JM, Peach V, Chapman RW. Five-year follow-up of patients with primary antibody deficiencies following an outbreak of acute hepatitis C. Clin Immunol 2001 99: 320 324.
28. Steinmann D, Barth H, Gissler B et al. Inhibition of hepatitis C virus-like particle binding to target cells by antiviral antibodies in acute and chronic hepatitis C. J Virol 2004 78: 9030 9040.
29. Bartosch B, Bukh J, Meunier JC et al. In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc Natl Acad Sci U S A 2003 100: 14199 14204.
30. Netski DM, Mosbruger T, Depla E et al. Humoral immune response in acute hepatitis C virus infection. Clin Infect Dis 2005 41: 667 675.
31. Lavillette D, Morice Y, Germanidis G et al. Human serum facilitates hepatitis C virus infection, and neutralizing responses inversely correlate with viral replication kinetics at the acute phase of hepatitis C virus infection. J Virol 2005 79: 6023 6034.
32. Dittmann S, Roggendorf M, Durkop J, Wiese M, Lorbeer B, Deinhardt F. Long-term persistence of hepatitis C virus antibodies in a single source outbreak. J Hepatol 1991 13: 323 327.
33. Rispeter K, Lu M, Behrens SE, Fumiko C, Yoshida T, Roggendorf M. Hepatitis C virus variability: sequence analysis of an isolate after 10 years of chronic infection. Virus Genes 2000 21: 179 188.
34. Bartosch B, Verney G, Dreux M et al. 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 2005 79: 8217 8229.
35. Andre P, Komurian-Pradel F, Deforges S et al. Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J Virol 2002 76: 6919 6928.
36. Hijikata M, Shimizu YK, Kato H et al. Equilibrium centrifugation studies of hepatitis C virus: evidence for circulating immune complexes. J Virol 1993 67: 1953 1958.
37. Miyamoto H, Okamoto H, Sato K, Tanaka T, Mishiro S. Extraordinarily low density of hepatitis C virus estimated by sucrose density gradient centrifugation and the polymerase chain reaction. J Gen Virol 1992 73: 715 718.
38. Nielsen SU, Bassendine MF, Burt AD, Martin C, Pumeechockchai W, Toms GL. Association between hepatitis C virus and very-low-density lipoprotein (VLDL)/LDL analyzed in iodixanol density gradients. J Virol 2006 80: 2418 2428.
39. Thomssen R, Bonk S, Propfe C, Heermann KH, Kochel HG, Uy A. Association of hepatitis C virus in human sera with beta-lipoprotein. Med Microbiol Immunol 1992 181: 293 300.
40. Thomssen R, Bonk S, Thiele A. Density heterogeneities of hepatitis C virus in human sera due to the binding of beta-lipoproteins and immunoglobulins. Med Microbiol Immunol 1993 182: 329 334.
41. Schettler V, Monazahian M, Wieland E et al. Reduction of hepatitis C virus load by H.E.L.P.-LDL apheresis. Eur J Clin Invest 2001 31: 154 155.
42. Agnello V, Abel G, Elfahal M, Knight GB, Zhang QX. Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. Proc Natl Acad Sci U S A 1999 96: 12766 12771.
43. Maillard P, Huby T, Andreo U, Moreau M, Chapman J, Budkowska A. The interaction of natural hepatitis C virus with human scavenger receptor SR-BI/Cla1 is mediated by ApoB-containing lipoproteins. FASEB J 2006 20: 735 737.
44. Monazahian M, Kippenberger S, Muller A et al. Binding of human lipoproteins (low, very low, high density lipoproteins) to recombinant envelope proteins of hepatitis C virus. Med Microbiol Immunol (Berl) 2000 188: 177 184.
45. Kanto T, Hayashi N, Takehara T et al. Density analysis of hepatitis C virus particle population in the circulation of infected hosts: implications for virus neutralization or persistence. J Hepatol 1995 22: 440 448.
46. Prince AM, Huima-Byron T, Parker TS, Levine DM. Visualization of hepatitis C virions and putative defective interfering particles isolated from low-density lipoproteins. J Viral Hepat 1996 3: 11 17.
47. Catanese MT, Graziani R, Von Hahn T et al. High avidity monoclonal antibodies against human scavenger receptor class B type I efficiently block hepatitis C virus infection in the presence of HDL. J Virol 2007 81: 8063 8071.
48. Dreux M, Pietschmann T, Granier C et al. High density lipoprotein inhibits hepatitis C virus neutralising antibodies by stimulating cell entry via activation of the scavenger receptor BI. J Biol Chem 2006 281: 18285 18295.
49. Voisset C, Callens N, Blanchard E, Op De Beeck A, Dubuisson J, Vu-Dac N. High density lipoproteins facilitate hepatitis C virus entry through the scavenger receptor class B type I. J Biol Chem 2005 280: 7793 7799.
50. Fust G. Enhancing antibodies in HIV infection. Parasitology 1997 115: S127 S140.
51. Halstead SB. Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 2003 60: 421 467.
52. Takada A, Feldmann H, Ksiazek TG, Kawaoka Y. Antibody-dependent enhancement of Ebola virus infection. J Virol 2003 77: 7539 7544.
53. Parathath S, Connelly MA, Rieger RA et al. Changes in plasma membrane properties and phosphatidylcholine subspecies of insect Sf9 cells due to expression of scavenger receptor class B, type I, and CD36. J Biol Chem 2004 279: 41310 41318.
54. Kellner-Weibel G, De La Llera-Moya M, Connelly MA et al. Expression of scavenger receptor BI in COS-7 cells alters cholesterol content and distribution. Biochemistry 2000 39: 221 229.
55. Krieger M. Scavenger receptor class B type I is a multiligand HDL receptor that influences diverse physiologic systems. J Clin Invest 2001 108: 793 797.
56. Bartosch B, Vitelli A, Granier C et al. 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 2003 278: 41624 41630.
57. Scarselli E, Ansuini H, Cerino R et al. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 2002 21: 5017 5025.
58. Voisset C, Op de Beeck A, Horellou P et al. High-density lipoproteins reduce the neutralizing effect of hepatitis C virus (HCV)-infected patient antibodies by promoting HCV entry. J Gen Virol 2006 87: 2577 2581.
59. Charrin S, Manie S, Thiele C et al. A physical and functional link between cholesterol and tetraspanins. Eur J Immunol 2003 33: 2479 2489.
60. Shimizu YK, Igarashi H, Kiyohara T et al. A hyperimmune serum against a synthetic peptide corresponding to the hypervariable region 1 of hepatitis C virus can prevent viral infection in cell cultures. Virology 1996 223: 409 412.
61. Von Hahn T, Yoon JC, Alter H et al. Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 2007 132: 667 678.
62. Kato N, Ootsuyama Y, Sekiya H et al. Genetic drift in hypervariable region 1 of the viral genome in persistent hepatitis C virus infection. J Virol 1994 68: 4776 4784.
63. Kato N, Sekiya H, Ootsuyama Y et al. Humoral immune response to hypervariable region 1 of the putative envelope glycoprotein (gp70) of hepatitis C virus. J Virol 1993 67: 3923 3930.
64. Farci P, Shimoda A, Coiana A et al. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 2000 288: 339 344.
65. Farci P, Strazzera R, Alter HJ et al. Early changes in hepatitis C viral quasispecies during interferon therapy predict the therapeutic outcome. Proc Natl Acad Sci U S A 2002 99: 3081 3086.
66. Van Doorn LJ, Capriles I, Maertens G et al. Sequence evolution of the hypervariable region in the putative envelope region E2/NS1 of hepatitis C virus is correlated with specific humoral immune responses. J Virol 1995 69: 773 778.
67. Booth JC, Kumar U, Webster D, Monjardino J, Thomas HC. Comparison of the rate of sequence variation in the hypervariable region of E2/NS1 region of hepatitis C virus in normal and hypogammaglobulinemic patients. Hepatology 1998 27: 223 227.
68. Kumar U, Monjardino J, Thomas HC. Hypervariable region of hepatitis C virus envelope glycoprotein (E2/NS1) in an agammaglobulinemic patient. Gastroenterology 1994 106: 1072 1075.
69. Ray SC, Wang YM, Laeyendecker O, Ticehurst JR, Villano SA, Thomas DL. Acute hepatitis C virus structural gene sequences as predictors of persistent viremia: hypervariable region 1 as a decoy. J Virol 1999 73: 2938 2946.
70. Mondelli MU, Cerino A, Segagni L et al. Hypervariable region 1 of hepatitis C virus: immunological decoy or biologically relevant domain? Antiviral Res 2001 52: 153 159.
71. Dreux M, Boson B, Ricard-Blum S et al. The exchangeable apolipoprotein ApoC-I promotes membrane fusion of hepatitis C virus 2007 J Biol Chem, in press.
72. Keck ZY, Op De Beeck A, Hadlock KG et al. Hepatitis C virus E2 has three immunogenic domains containing conformational epitopes with distinct properties and biological functions. J Virol 2004 78: 9224 9232.
73. Owsianka A, Tarr AW, Juttla VS et al. Monoclonal antibody AP33 defines a broadly neutralizing epitope on the hepatitis C virus E2 envelope glycoprotein. J Virol 2005 79: 11095 11104.
74. Schofield DJ, Bartosch B, Shimizu YK et al. Human monoclonal antibodies react with the E2 glycoprotein of as many as five major hepatitis C virus (HCV) genotypes and possess neutralizing activity. Hepatology 2005 42: 1055 1062.
75. Tarr AW, Owsianka AM, Timms JM et al. Characterization of the hepatitis C virus E2 epitope defined by the broadly neutralizing monoclonal antibody AP33. Hepatology 2006 43: 592 601.
76. Penin F, Combet C, Germanidis G, Frainais PO, Deleage G, Pawlotsky JM. Conservation of the conformation and positive charges of hepatitis C virus E2 envelope glycoprotein hypervariable region 1 points to a role in cell attachment. J Virol 2001 75: 5703 5710.
77. Garcia KC, Teyton L, Wilson IA. Structural basis of T cell recognition. Annu Rev Immunol 1999 17: 369 397.
78. Forns X, Thimme R, Govindarajan S et al. Hepatitis C virus lacking the hypervariable region 1 of the second envelope protein is infectious and causes acute resolving or persistent infection in chimpanzees. Proc Natl Acad Sci U S A 2000 97: 13318 13323.
79. Burton DR. Antibodies, viruses and vaccines. Nat Rev Immunol 2002 2: 706 713.
80. Eren R, Landstein D, Terkieltaub D et al. Preclinical evaluation of two neutralizing human monoclonal antibodies against hepatitis C virus (HCV): a potential treatment to prevent HCV reinfection in liver transplant patients. J Virol 2006 80: 2654 2664.
81. Keck ZY, Xia J, Cai Z et al. Immunogenic and functional organization of hepatitis C virus (HCV) glycoprotein E2 on infectious HCV virions. J Virol 2007 81: 1043 1047.
82. Keck ZY, Li TK, Xia J et al. Analysis of a highly flexible conformational immunogenic domain a in hepatitis C virus E2. J Virol 2005 79: 13199 13208.
83. Falkowska E, Kajumo F, Garcia E, Reinus J, Dragic T. Hepatitis C virus envelope glycoprotein E2 glycans modulate entry, CD81 binding and neutralization. J Virol 2007 81: 8072 8079.
84. Helle F, Goffard A, Morel V et al. The neutralizing activity of anti-HCV antibodies is modulated by specific glycans on the E2 envelope protein. J Virol 2007 81: 8101 8111.
85. Zhang P, Wu CG, Mihalik K et al. Hepatitis C virus epitope-specific neutralizing antibodies in Igs prepared from human plasma. Proc Natl Acad Sci U S A 2007 104: 8449 8454.
86. Pietschmann T, Kaul A, Koutsoudakis G et al. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci U S A 2006 103: 7408 7413.
87. Drummer HE, Boo I, Poumbourios P. Mutagenesis of a conserved fusion peptide-like motif and membrane-proximal heptad-repeat region of hepatitis C virus glycoprotein E1. J Virol 2007 88: 1144 1148.
88. Flint M, Thomas JM, Maidens CM et al. Functional analysis of cell surface-expressed hepatitis C virus E2 glycoprotein. J Virol 1999 73: 6782 6790.
89. Garry RF, Dash S. Proteomics computational analyses suggest that hepatitis C virus E1 and pestivirus E2 envelope glycoproteins are truncated class II fusion proteins. Virology 2003 307: 255 265.
90. Lavillette D, Pécheur E-I, Donot P et al. 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 2007 81: 8752 8765.
91. Zucchelli S, Roccasecca R, Meola A et al. Mimotopes of the hepatitis C virus hypervariable region 1, but not the natural sequences, induce cross-reactive antibody response by genetic immunization. Hepatology 2001 33: 692 703.
92. Ralston R, Thudium K, Berger K et al. Characterization of hepatitis C virus envelope glycoprotein complexes expressed by recombinant vaccinia viruses. J Virol 1993 67: 6753 6761.
93. Drummer HE, Boo I, Maerz AL, Poumbourios P. A conserved Gly436-Trp-Leu-Ala-Gly-Leu-Phe-Tyr motif in hepatitis C virus glycoprotein E2 is a determinant of CD81 binding and viral entry. J Virol 2006 80: 7844 7853.
94. Owsianka AM, Timms JM, Tarr AW et al. Identification of conserved residues in the E2 envelope glycoprotein of the hepatitis C virus that are critical for CD81 binding. J Virol 2006 80: 8695 8704.
95. Evans MJ, von Hahn T, Tscherne DM, Syder AJ et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007 446: 801 805.