Hepatitis c virus envelope glycoprotein signatures are associated with treatment failure and modulation of viral entry and neutralization

Journal of Infectious Diseases

Volumn 207, Issue 8, 2013, Pages 1306-1315

  Schvoerer, Evelyne ^a,b,c   Moenne Loccoz, Rémy ^a,b   Murray, John M ^e,f   Velay, Aurélie ^a,b   Turek, Marine ^a,b   Fofana, Isabel ^a,b   Fafi Kremer, Samira ^a,b,c   Erba, Anne Claire ^a,b   Habersetzer, François ^a,b,d   Doffoël, Michel ^a,b,d   Gut, Jean Pierre ^a,b,c   Donlin, Maureen J ^g,h   Tavis, John E ^g,h   Zeisel, Mirjam B ^a,b   Stoll Keller, Françoise ^a,b,c   Baumert, Thomas F ^a,b,d  

^a INSERM   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c CHU NANCY BRABOIS   (France)

^d UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^e School of Mathematics and Statistics and   (Australia)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

^g Department of Molecular Microbiology and Immunology ^*  (United States)

^h SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

interferon alfa; outcome; resistance; ribavirin; therapy

Indexed keywords

ALANINE AMINOTRANSFERASE; ANTIVIRUS AGENT; GLYCOPROTEIN E1; GLYCOPROTEIN E2; PEGINTERFERON ALPHA PLUS RIBAVIRIN; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS RNA;

ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANTIGENICITY; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; ETHNICITY; FEMALE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA ANALYSIS; TREATMENT FAILURE; TREATMENT RESPONSE; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION; VIRUS TRANSMISSION;

ADULT; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIVIRAL AGENTS; COMPUTATIONAL BIOLOGY; FEMALE; GENOTYPE; HEK293 CELLS; HEPACIVIRUS; HEPATITIS C; HUMANS; IMMUNE EVASION; MALE; MIDDLE AGED; MUTAGENESIS, SITE-DIRECTED; MUTATION; NEUTRALIZATION TESTS; RIBAVIRIN; STRUCTURE-ACTIVITY RELATIONSHIP; TREATMENT FAILURE; VIRAL ENVELOPE PROTEINS; VIRUS INTERNALIZATION;

EID: 84875578673     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jit032     Document Type: Article

References (42)

1. Schaefer EAK, Chung RT. Anti-hepatitis C virus drugs in development. Gastroenterology 2012; 142:1340-50.
2. Pawlotsky J-M. Treatment failure and resistance with direct-acting antiviral drugs against hepatitis C virus. Hepatology 2011; 53:1742-51.
3. Sarrazin C, Hézode C, Zeuzem S, Pawlotsky J-M. Antiviral strategies in hepatitis C virus infection. J Hepatol 2012; 56 (Suppl 1):S88-100.
4. Fried MW, Hadziyannis SJ, Shiffman ML, Messinger D, Zeuzem S. Rapid virological response is the most important predictor of sustained virological response across genotypes in patients with chronic hepatitis C virus infection. J Hepatol 2011; 55:69-75.
5. Asselah T, Estrabaud E, Bieche I, et al. Hepatitis C: viral and host factors associated with non-response to pegylated interferon plus ribavirin. Liver Int 2010; 30:1259-69.
6. Ge D, Fellay J, Thompson AJ, et al. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 2009; 461:399-401.
7. Zeisel MB, Fofana I, Fafi-Kremer S, Baumert TF. Hepatitis C virus entry into hepatocytes: molecular mechanisms and targets for antiviral therapies. J Hepatol 2011; 54:566-76.
8. 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; 132:667-78.
9. Fafi-Kremer S, Fofana I, Soulier E, et al. Viral entry and escape from antibody-mediated neutralization influence hepatitis C virus reinfection in liver transplantation. J Exp Med 2010; 207:2019-31.
10. Fofana I, Fafi-Kremer S, Carolla P, et al. Mutations that alter use of hepatitis C virus cell entry factors mediate escape from neutralizing antibodies. Gastroenterology 2012; 143:223-33.
11. Di Liberto G, Roque-Afonso A-M, Kara R, et al. Clinical and therapeutic implications of hepatitis C virus compartmentalization. Gastroenterology 2006; 131:76-84.
12. Schramm F, Soulier E, Royer C, et al. Frequent compartmentalization of hepatitis C virus with leukocyte-related amino acids in the setting of liver transplantation. J Infect Dis 2008; 198:1656-66.
13. Stamataki Z, Shannon-Lowe C, Shaw J, et al. Hepatitis C virus association with peripheral blood B lymphocytes potentiates viral infection of liver-derived hepatoma cells. Blood 2009; 113:585-93.
14. Baumert TF, Wellnitz S, Aono S, et al. Antibodies against hepatitis C virus-like particles and viral clearance in acute and chronic hepatitis C. Hepatology 2000; 32:610-7.
15. Hamed MRB, Tarr AW, McClure CP, Ball JK, Hickling TP, Irving WL. Association of antibodies to hepatitis C virus glycoproteins 1 and 2 (anti-E1E2) with HCV disease. J Viral Hepat 2008; 15:339-45.
16. Gaudy C, Moreau A, Veillon P, Temoin S, Lunel F, Goudeau A. Significance of pretreatment analysis of hepatitis C virus genotype 1b hypervariable region 1 sequences to predict antiviral outcome. J Clin Microbiol 2003; 41:3615-22.
17. Barth H, Schafer C, Adah MI, et al. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 2003; 278:41003-12.
18. Pileri P, Uematsu Y, Campagnoli S, et al. Binding of hepatitis C virus to CD81. Science 1998; 282:938-41.
19. 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; 21:5017-25.
20. Zeisel MB, Koutsoudakis G, Schnober EK, et al. 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 2007; 46:1722-31.
21. Evans MJ, von Hahn T, Tscherne DM, et al. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007; 446:801-5.
22. Krieger SE, Zeisel MB, Davis C, et al. Inhibition of hepatitis C virus infection by anti-claudin-1 antibodies is mediated by neutralization of E2-CD81-claudin-1 associations. Hepatology 2010; 51:1144-57.
23. Ploss A, Evans MJ, Gaysinskaya VA, et al. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009; 457:882-6.
24. Lupberger J, Zeisel MB, Xiao F, et al. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 2011; 17:589-95.
25. 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; 79:8217-29.
26. Liu L, Fisher BE, Thomas DL, Cox AL, Ray SC. Spontaneous clearance of primary acute hepatitis C virus infection correlated with high initial viral RNA level and rapid HVR1 evolution. Hepatology 2012; 55:1684-91.
27. Chambers TJ, Fan X, Droll DA, et al. Quasispecies heterogeneity within the E1/E2 region as a pretreatment variable during pegylated interferon therapy of chronic hepatitis C virus infection. J Virol 2005; 79:3071-83.
28. Aurora R, Donlin MJ, Cannon NA, Tavis JE. Genome-wide hepatitis C virus amino acid covariance networks can predict response to antiviral therapy in humans. J Clin Invest 2009; 119:225-36.
29. Donlin MJ, Cannon NA, Aurora R, et al. Contribution of genomewide HCV genetic differences to outcome of interferon-based therapy in Caucasian American and African American patients. PloS One 2010; 5:e9032.
30. Sheehy P, Scallan M, Kenny-Walsh E, Shanahan F, Fanning LJ. A strategy for obtaining near full-length HCV cDNA clones (assemblicons) by assembly PCR. J Virol Methods 2005; 123:115-24.
31. Parker JM, Guo D, Hodges RS. New hydrophilicity scale derived from high-performance liquid chromatography peptide retention data: correlation of predicted surface residues with antigenicity and X-rayderived accessible sites. Biochemistry 1986; 25:5425-32.
32. Pestka JM, Zeisel MB, Bläser 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; 104:6025-30.
33. Haberstroh A, Schnober EK, Zeisel MB, et al. Neutralizing host responses in hepatitis C virus infection target viral entry at postbinding steps and membrane fusion. Gastroenterology 2008; 135: 1719-28.
34. Bartosch B, Dubuisson J, Cosset F-L. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med 2003; 197:633-42.
35. Helle F, Goffard A, Morel V, et al. The neutralizing activity of antihepatitis C virus antibodies is modulated by specific glycans on the E2 envelope protein. J Virol 2007; 81:8101-11.
36. Krey T, d'Alayer J, Kikuti CM, et al. The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathog 2010; 6:e1000762.
37. Keck Z-Y, Olson O, Gal-Tanamy M, et al. A point mutation leading to hepatitis C virus escape from neutralization by a monoclonal antibody to a conserved conformational epitope. J Virol 2008; 82:6067-72.
38. Maurin G, Fresquet J, Granio O, Wychowski C, Cosset F-L, Lavillette D. Identification of interactions in the E1E2 heterodimer of hepatitis C virus important for cell entry. J Biol Chem 2011; 286:23865-76.
39. Grove J, Nielsen S, Zhong J, et al. 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 2008; 82:12020-9.
40. Keck Z-Y, Li SH, Xia J, et al. Mutations in hepatitis C virus E2 located outside the CD81 binding sites lead to escape from broadly neutralizing antibodies but compromise virus infectivity. J Virol 2009; 83: 6149-60.
41. Gal-Tanamy M, Keck Z-Y, Yi M, et al. In vitro selection of a neutralization- resistant hepatitis C virus escape mutant. Proc Natl Acad Sci U S A 2008; 105:19450-5.
42. Habersetzer F, Honnet G, Bain C, et al. A poxvirus vaccine is safe, induces T-cell responses, and decreases viral load in patients with chronic hepatitis C. Gastroenterology 2011; 14:890-9.