Structural basis for broad neutralization of hepatitis c virus quasispecies

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Lapierre, Pascal ^a   Troesch, Myriam ^a,b   Alvarez, Fernando ^a,b   Soudeyns, Hugo ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AR3B HUMAN MONOCLONAL ANTIBODY; GLYCOPROTEIN E2; HUMAN MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; GLYCOPROTEIN E2, HEPATITIS C VIRUS; HEPATITIS C ANTIBODY; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CLINICAL ARTICLE; GENETIC VARIABILITY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN STRUCTURE; SPECIES; STRUCTURAL HOMOLOGY; TICK BORNE ENCEPHALITIS FLAVIVIRUS; VIRUS MORPHOLOGY; VIRUS NEUTRALIZATION; VIRUS QUASISPECIES; CHEMISTRY; EPITOPE MAPPING; IMMUNOLOGY; MOLECULAR GENETICS; PROTEIN CONFORMATION;

HEPATITIS C VIRUS; TICK-BORNE ENCEPHALITIS VIRUS;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ENCEPHALITIS VIRUSES, TICK-BORNE; EPITOPE MAPPING; GENETIC VARIATION; HEPACIVIRUS; HEPATITIS C ANTIBODIES; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; VIRAL ENVELOPE PROTEINS;

EID: 80055043200     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026981     Document Type: Article

References (58)

1. Shepard CW, Finelli L, Alter MJ, (2005) Global epidemiology of hepatitis C virus infection. Lancet Infect Dis 5: 558-567.
2. No authors listed (2002) NIH Consensus Statement on Management of Hepatitis C: 2002. NIH Consens State Sci Statements 19: 1-46.
3. Simmonds P, Bukh J, Combet C, Deleage G, Enomoto N, et al. (2005) Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42: 962-973.
4. Steinhauser DA, Holland JJ, (1987) Rapid evolution of RNA viruses. Ann Rev Microbiol 41: 409-433.
5. Martell M, Esteban JI, Quer J, Genesca J, Weiner A, et al. (1992) Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: quasispecies nature of HCV genome distribution. J Virol 66: 3225-3229.
6. Bukh J, Miller RH, Purcell RH, (1995) Genetic heterogeneity of Hepatitis C virus: quasispecies and genotypes. Sem Liv Dis 15: 41-63.
7. Weiner AJ, Brauer MJ, Rosenblatt J, Richman KH, Tung J, et al. (1991) Variable and hypervariable domains are found in the regions of HCV corresponding to the flavivirus envelope and NS1 proteins and the pestivirus envelope glycoproteins. Virology 180: 842-848.
8. Kato N, Ootsuyama Y, Tanaka T, Nakagawa M, Nakazawa T, et al. (1992) Marked sequence diversity in the putative envelope proteins of hepatitis C viruses. Virus Res 22: 107-123.
9. Kato N, Ootsuyama Y, Ohkoshi S, Nakazawa T, Sekiya H, et al. (1992) Characterization of hypervariable regions in the putative envelope protein of hepatitis C virus. Biochem Biophys Res Commun 189: 119-127.
10. Troesch M, Meunier I, Lapierre P, Alvarez F, Boucher M, et al. (2006) Study of a novel hypervariable region in hepatitis C virus (HCV) E2 envelope glycoprotein. Virology 352: 357-367.
11. McCaffrey K, Boo I, Poumbourios P, Drummer HE, (2007) Expression and characterization of a minimal hepatitis C virus glycoprotein E2 core domain that retains CD81 binding. J Virol 81: 9584-9590.
12. Cuevas JM, Torres-Puente M, Jimenez-Hernandez N, Bracho MA, García-Robles I, et al. (2008) Refined analysis of genetic variability parameters in hepatitis C virus and the ability to predict antiviral treatment response. J Viral Hepat 15: 578-590.
13. Torres-Puente M, Cuevas JM, Jimenez-Hernandez N, Bracho MA, Garcia-Robles I, et al. (2008) Using evolutionary tools to refine the new hypervariable region 3 within the envelope 2 protein of hepatitis C virus. Infect Genet Evol 8: 74-82.
14. Law M, Maruyama T, Lewis J, Giang E, Tarr AW, et al. (2008) Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat Med 14: 25-27.
15. Penin F, Combet C, Germanidis G, Frainais PO, Deleage G, et al. (2001) 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 75: 5703-5710.
16. Weiner AJ, Geysen HM, Christopherson C, Hall JE, Mason TJ, et al. (1992) Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: potential role in chronic HCV infections. Proc Natl Acad Sci U S A 89: 3468-3472.
17. Kato N, Sekiya H, Ootsuyama Y, Nakazawa T, Hijikata M, et al. (1993) Humoral immune response to hypervariable region 1 of the putative envelope glycoprotein (gp70) of hepatitis C virus. J Virol 67: 3923-3930.
18. Farci P, Alter HJ, Govindarajan S, Wong DC, Engle R, et al. (1992) Lack of protective immunity against reinfection with hepatitis C virus. Science 258: 135-140.
19. Beld M, Penning M, van Putten M, Lukashov V, van den Hoek A, et al. (1999) Quantitative antibody responses to structural (core) and nonstructural (NS3, NS4, and NS5) hepatitis C virus proteins among seroconverting injecting drug users: impact of epitope variation and relationship to detection of HCV RNA in blood. Hepatology 29: 1288-1298.
20. Adams G, Kuntz S, Rabelais G, Bratcher D, Tamburro CH, et al. (1997) Natural recovery from acute hepatitis C virus infection by agammaglobulinemic twin children. Pediatr Infect Dis J 16: 533-534.
21. Meunier JC, Russell RS, Goossens V, Priem S, Walter H, et al. (2008) Isolation and characterization of broadly neutralizing human monoclonal antibodies to the E1 glycoprotein of hepatitis C virus. J Virol 82: 966-973.
22. Grove J, Nielsen S, Zhong J, Bassendine MF, Drummer HE, et al. (2008) Identification of a residue in hepatitis C virus E2 glycoprotein that determines scavenger receptor BI and CD81 receptor dependency and sensitivity to neutralizing antibodies. J Virol 82: 12020-12029.
23. Gal-Tanamy M, Keck ZY, Yi M, McKeating JA, Patel AH, et al. (2008) In vitro selection of a neutralization-resistant hepatitis C virus escape mutant. Proc Natl Acad Sci U S A 105: 19450-19455.
24. Keck ZY, Li TK, Xia J, Gal-Tanamy M, Olson O, et al. (2008) Definition of a conserved immunodominant domain on hepatitis C virus E2 glycoprotein by neutralizing human monoclonal antibodies. J Virol 82: 6061-6066.
25. Keck ZY, Olson O, Gal-Tanamy M, Xia J, Patel AH, et al. (2008) A point mutation leading to hepatitis C virus escape from neutralization by a monoclonal antibody to a conserved conformational epitope. J Virol 82: 6067-6072.
26. Flint M, Maidens C, Loomis-Price LD, Shotton C, Dubuisson J, et al. (1999) Characterization of hepatitis C virus E2 glycoprotein interaction with a putative cellular receptor, CD81. J Virol 73: 6235-6244.
27. Von Hahn T, Yoon JC, Alter H, Rice CM, Rehermann B, et al. (2007) Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterol 132: 667-678.
28. Johansson DX, Voisset C, Tarr AW, Aung M, Ball JK, et al. (2007) Human combinatorial libraries yield rare antibodies that broadly neutralize hepatitis C virus. Proc Natl Acad Sci U S A 104: 16269-16274.
29. Keck ZY, Li SH, Xia J, von Hahn T, Balfe P, et al. (2009) Mutations in HCV E2 located outside the CD81 binding sites lead to escape from broadly neutralizing antibodies but compromise virus infectivity. J Virol 83: 6149-6160.
30. Keck ZY, Saha A, Xia J, Wang Y, Lau P, et al. (2011) Mapping a region of HCV E2 that is responsible for escape from neutralizing antibodies and a core CD81-binding region that does not tolerate neutralization escape mutations. J Virol [Epub ahead of print].
31. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, et al. (1998) Binding of hepatitis C virus to CD81. Science 282: 938-941.
32. 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.
33. Mercer DF, Schiller DE, Elliott JF, Douglas DN, Hao C, et al. (2001) Hepatitis C virus replication in mice with chimeric human livers. Nat Med 7: 927-933.
34. Yagnik AT, Lahm A, Meola A, Roccasecca RM, Ercole BB, et al. (2000) A model for the hepatitis C virus envelope glycoprotein E2. Proteins 40: 355-366.
35. Rey FA, Heinz FX, Mandl C, Kunz C, Harrison SC, (1995) The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature 375: 291-298.
36. Kuiken C, Yusim K, Boykin L, Richardson R, (2005) The Los Alamos hepatitis C sequence database. Bioinformatics 21: 379-384.
37. Krissinel E, Henrick K, (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60: 2256-2268.
38. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
39. Dazert E, Neumann-Haefelin C, Bressanelli S, Fitzmaurice K, Kort J, et al. (2009) Loss of viral fitness and cross-recognition by CD8+ T cells limit HCV escape from a protective HLA-B27-restricted human immune response. J Clin Invest 119: 376-386.
40. Stamataki Z, Grove J, Balfe P, McKeating JA, (2008) Hepatitis C virus entry and neutralization. Clin Liver Dis 12: 693-712.
41. Davies DR, Cohen GH, (1996) Interactions of protein antigens with antibodies. Proc Natl Acad Sci U S A 93: 7-12.
42. Shoukry NH, Cawthon AG, Walker CM, (2004) Cell-mediated immunity and the outcome of hepatitis C virus infection. Ann Rev Immunol 58: 391-424.
43. Krey T, d'Alayer J, Kikuti CM, Saulnier A, Damier-Piolle L, et al. (2010) The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathog 6 (2): e1000762.
44. Albecka A, Montserret R, Krey T, Tarr AW, Diesis E, et al. (2011) Identification of new functional regions in hepatitis C virus envelope glycoprotein E2. J Virol 85: 1777-1792.
45. Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J, et al. (2002) Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108: 717-725.
46. Kiermayr S, Stiasny K, Heinz FX, (2009) Impact of quaternary organization on the antigenic structure of the tick-borne encephalitis virus envelope glycoprotein E. J Virol 83: 8482-8491.
47. Marceau G, Lapierre P, Beland K, Soudeyns H, Alvarez F, (2005) LKM1 autoantibodies in chronic hepatitis C infection: a case of molecular mimicry? Hepatology 42: 675-682.
48. O'Leary JG, Lepe R, Davis GL, (2008) Indications for liver transplantation. Gastroenterology 134: 1764-1776.
49. Ofek G, Guenaga FJ, Schief WR, Skinner J, Baker D, et al. (2010) Elicitation of structure-specific antibodies by epitope scaffolds. Proc Natl Acad Sci U S A 107: 17880-17887.
50. Troesch M, Jalbert E, Canobio S, Routy JP, Bernard N, et al. (2005) Characterization of humoral and cell-mediated immune responses directed against hepatitis C virus F protein in patients coinfected with hepatitis C virus and HIV-1. AIDS 19: 775-784.
51. Murphy D, Willems B, Delage G, (1994) Use of the 5′ noncoding region for genotyping hepatitis C virus. J Infect Dis 169: 473-475.
52. Farci P, Shimoda A, Coiana A, Diaz G, Peddis G, et al. (2000) The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288: 339-344.
53. Polyak SJ, Sullivan DG, Austin MA, Dai JY, Shunhart MC, et al. (2005) Comparison of amplification enzymes for hepatitis C virus quasispecies analysis. Virol J 2: 41.
54. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24: 1596-1599.
55. Sali A, Blundell TL, (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
56. Dauber-Osguthorpe P, Roberts VA, Osguthorpe DJ, Wolff J, Genest M, et al. (1988) Structure and energetics of ligand binding to proteins: Escherichia coli dihydrofolate reductase-trimethoprim, a drug-receptor system. Proteins 4: 31-47.
57. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
58. Korber BTM, Kunstman KJ, Patterson BK, Furtado M, McEvilly MM, et al. (1994) Genetic differences between blood- and brain-derived viral sequences from human immunodeficiency virus type 1-infected patients: evidence of conserved elements in the V3 region of the envelope protein of brain-derived sequences. J Virol 68: 7467-7481.