Therapeutic vaccines against hepatitis C virus

Infection, Genetics and Evolution

Volumn 22, Issue , 2014, Pages 120-129

  Xue, Jihua ^a   Zhu, Haihong ^a   Chen, Zhi ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Epitope; Hepatitis C virus; Immunity; T cells; Therapeutic vaccine

Indexed keywords

ADENOVIRUS VECTOR; ANTIVIRUS AGENT; ASUNAPREVIR; BMS 791325; BOCEPREVIR; CHONVAC C; DACLATASVIR; DENDRITIC CELL VACCINE; DNA VACCINE; EPITOPE; HEPATITIS C ANTIBODY; HEPATITIS C ANTIGEN; HEPATITIS C VACCINE; ISOMATRIX; NEUTRALIZING ANTIBODY; NONSTRUCTURAL PROTEIN 5B; PEGINTERFERON ALPHA; PEPTIDE VACCINE; POXVIRUS VECTOR; RECOMBINANT HEPATITIS C VACCINE; RIBAVIRIN; TELAPREVIR; UNCLASSIFIED DRUG; BECLABUVIR; HEPATITIS C VACCINE CIGB 230; HEPATITIS C VACCINE E1E2MF59C; HEPATITIS C VACCINE GI 5005; HEPATITIS C VACCINE IC41; HEPATITIS C VACCINE ISCOMATRIX; HEPATITIS C VACCINE TG4040; INTERFERON; PEGINTERFERON ALPHA2A PLUS RIBAVIRIN; PEGINTERFERON ALPHA2B PLUS RIBAVIRIN;

ANEMIA; ANTIBODY RESPONSE; ANTIGEN RECOGNITION; ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CROSS REACTION; DRUG COST; DRUG EFFICACY; DRUG SAFETY; ELECTROPORATION; HEPATITIS C; HEPATITIS C VIRUS GENOTYPE 1; HUMAN; INFECTION PREVENTION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; RASH; REVIEW; SPECIES DIVERSITY; VACCINATION; VACCINE PRODUCTION; ANTIBODY TITER; ANTIGEN DETECTION; DRUG TOLERABILITY; GENETIC VARIABILITY; HEPATITIS C VIRUS; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOREACTIVITY; MORBIDITY; MORTALITY; PROTEIN BINDING; PROTEIN PURIFICATION; VIRAL CLEARANCE; VIRUS NEUTRALIZATION;

EPITOPE; HEPATITIS C VIRUS; IMMUNITY; T CELLS; THERAPEUTIC VACCINE;

CD8-POSITIVE T-LYMPHOCYTES; HEPACIVIRUS; HEPATITIS C; HUMANS; VIRAL HEPATITIS VACCINES;

EID: 84896739014     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2014.01.008     Document Type: Review

References (117)

1. Afdhal N.H. The natural history of hepatitis C. Semin. Liver Dis. 2004, 24(Suppl. 2):3-8.
2. Agnello V., Abel G., Elfahal M., Knight G.B., Zhang Q.X. Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. Proc. Nat. Acad. Sci. U.S.A. 1999, 96:12766-12771.
3. Alvarez-Lajonchere L., Shoukry N.H., Gra B., Amador-Canizares Y., Helle F., Bedard N., Guerra I., Drouin C., Dubuisson J., Gonzalez-Horta E.E., Martinez G., Marante J., Cinza Z., Castellanos M., Duenas-Carrera S. Immunogenicity of CIGB-230, a therapeutic DNA vaccine preparation, in HCV-chronically infected individuals in a Phase I clinical trial. J. Viral Hepat. 2009, 16:156-167.
4. Ascione A., Tartaglione T., Di Costanzo G.G. Natural history of chronic hepatitis C virus infection. Digest. Liver Dis. 2007, 39(Suppl. 1):S4-S7.
5. Bacon B.R., Gordon S.C., Lawitz E., Marcellin P., Vierling J.M., Zeuzem S. HCV RESPOND-2 final results: high sustained virologic response among genotype 1 previous nonresponders and relapsers to peginterferon/ribavirin when retreated with boceprevir plus PegIntron/ribavirin. Hepatology 2010, 52:430A.
6. Bacon B.R., Gordon S.C., Lawitz E., Marcellin P., Vierling J.M., Zeuzem S., Poordad F., Goodman Z.D., Sings H.L., Boparai N., Burroughs M., Brass C.A., Albrecht J.K., Esteban R. Boceprevir for previously treated chronic HCV genotype 1 infection. New Engl. J. Med. 2011, 364:1207-1217.
7. Banchereau J., Schuler-Thurner B., Palucka A.K., Schuler G. Dendritic cells as vectors for therapy. Cell 2001, 106:271-274.
8. Barnes E., Salio M., Cerundolo V., Francesco L., Pardoll D., Klenerman P., Cox A. Monocyte derived dendritic cells retain their functional capacity in patients following infection with hepatitis C virus. J. Viral Hepat. 2008, 15:219-228.
9. Barth H., Schafer C., Adah M.I., Zhang F., Linhardt R.J., Toyoda H., Kinoshita-Toyoda A., Toida T., Van Kuppevelt T.H., Depla E., Von Weizsacker F., Blum H.E., Baumert T.F. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J. Biol. Chem. 2003, 278:41003-41012.
10. Bartosch B., Bukh J., Meunier J.C., Granier C., Engle R.E., Blackwelder W.C., Emerson S.U., Cosset F.L., Purcell R.H. In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc. Nat. Acad. Sci. U.S.A. 2003, 100:14199-14204.
11. Bassett S.E., Guerra B., Brasky K., Miskovsky E., Houghton M., Klimpel G.R., Lanford R.E. Protective immune response to hepatitis C virus in chimpanzees rechallenged following clearance of primary infection. Hepatology 2001, 33:1479-1487.
12. Battegay M., Fikes J., Di Bisceglie A.M., Wentworth P.A., Sette A., Celis E., Ching W.M., Grakoui A., Rice C.M., Kurokohchi K., et al. Patients with chronic hepatitis C have circulating cytotoxic T cells which recognize hepatitis C virus-encoded peptides binding to HLA-A2.1 molecules. J. Virol. 1995, 69:2462-2470.
13. Beckebaum S., Cicinnati V.R., Gerken G. DNA-based immunotherapy: potential for treatment of chronic viral hepatitis?. Rev. Med. Virol. 2002, 12:297-319.
14. Benedicto I., Molina-Jimenez F., Bartosch B., Cosset F.L., Lavillette D., Prieto J., Moreno-Otero R., Valenzuela-Fernandez A., Aldabe R., Lopez-Cabrera M., Majano P.L. The tight junction-associated protein occludin is required for a postbinding step in hepatitis C virus entry and infection. J. Virol. 2009, 83:8012-8020.
15. Bettauer R.H. Chimpanzees in hepatitis C virus research: 1998-2007. J. Med. Primatol. 2010, 39:9-23.
16. Bian Y., Zhao S., Zhu S., Zeng J., Li T., Fu Y., Wang Y., Zheng X., Zhang L., Wang W., Yang B., Zhou Y., Allain J.P., Li C. Significance of monoclonal antibodies against the conserved epitopes within non-structural protein 3 helicase of hepatitis C virus. PLoS One 2013, 8:e70214.
17. Cerundolo V., Hermans I.F., Salio M. Dendritic cells: a journey from laboratory to clinic. Nat. Immunol. 2004, 5:7-10.
18. Chang K.M., Gruener N.H., Southwood S., Sidney J., Pape G.R., Chisari F.V., Sette A. Identification of HLA-A3 and -B7-restricted CTL response to hepatitis C virus in patients with acute and chronic hepatitis C. J. Immunol. 1999, 162:1156-1164.
19. Cooper S., Erickson A.L., Adams E.J., Kansopon J., Weiner A.J., Chien D.Y., Houghton M., Parham P., Walker C.M. Analysis of a successful immune response against hepatitis C virus. Immunity 1999, 10:439-449.
20. Cucchiarini M., Kammer A.R., Grabscheid B., Diepolder H.M., Gerlach T.J., Gruner N., Santantonio T., Reichen J., Pape G.R., Cerny A. Vigorous peripheral blood cytotoxic T cell response during the acute phase of hepatitis C virus infection. Cell. Immunol. 2000, 203:111-123.
21. Dazert E., Neumann-Haefelin C., Bressanelli S., Fitzmaurice K., Kort J., Timm J., McKiernan S., Kelleher D., Gruener N., Tavis J.E., Rosen H.R., Shaw J., Bowness P., Blum H.E., Klenerman P., Bartenschlager R., Thimme R. 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. 2009, 119:376-386.
22. Doi H., Hiroishi K., Shimazaki T., Eguchi J., Baba T., Ito T., Matsumura T., Nozawa H., Morikawa K., Ishii S., Hiraide A., Sakaki M., Imawari M. Magnitude of CD8 T-cell responses against hepatitis C virus and severity of hepatitis do not necessarily determine outcomes in acute hepatitis C virus infection. Hepatol. Res. 2009, 39:256-265.
23. Dorner M., Horwitz J.A., Robbins J.B., Barry W.T., Feng Q., Mu K., Jones C.T., Schoggins J.W., Catanese M.T., Burton D.R., Law M., Rice C.M., Ploss A. A genetically humanized mouse model for hepatitis C virus infection. Nature 2011, 474:208-211.
24. Drane D., Maraskovsky E., Gibson R., Mitchell S., Barnden M., Moskwa A., Shaw D., Gervase B., Coates S., Houghton M., Basser R. Priming of CD4+ and CD8+ T cell responses using a HCV core ISCOMATRIX vaccine: a phase I study in healthy volunteers. Hum. Vaccines 2009, 5:151-157.
25. Duan L., Lei P., Yumei X., Xiaoping X., Futao Z., Li M., Xin W., Jiuping W., Xuefan B., Zhansheng J. Prediction and identification-based prediction of Chinese hepatitis C viral-specific cytotoxic T lymphocyte epitopes. J. Med. Virol. 2011, 83:1315-1320.
26. Echeverria I., Zabaleta A., Silva L., Diaz-Valdes N., Riezu-Boj J.I., Lasarte J.J., Borras-Cuesta F., Civeira M.P., Prieto J., Sarobe P. Monocyte-derived dendritic cells from HCV-infected patients transduced with an adenovirus expressing NS3 are functional when stimulated with the TLR3 ligand poly(I:C). J. Viral Hepat. 2008, 15:782-789.
27. El-Awady, M.K., El Gendy, M., Waked, I., Tabll, A.A., El Abd, Y., Bader El Din, N., El Shenawy, R., Allam, A., Abdelhafez, T.H., Dawood, R.M., 2013. Immunogenicity and safety of HCV E1E2 peptide vaccine in chronically HCV-infected patients who did not respond to interferon based therapy. Vaccine, in press.
28. EASL Clinical Practice and Guidelines: management of hepatitis C virus infection. J. Hepatol. 2011, 55:245-264. European Association for the Study of the Liver.
29. Evans M.J., von Hahn T., Tscherne D.M., Syder A.J., Panis M., Wolk B., Hatziioannou T., McKeating J.A., Bieniasz P.D., Rice C.M. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007, 446:801-805.
30. Everson G.T., Sims K.D., Rodriguez-Torres M., Hezode C., Lawitz E., Bourliere M., Loustaud-Ratti V., Rustgi V., Schwartz H., Tatum H., Marcellin P., Pol S., Thuluvath P.J., Eley T., Wang X., Huang S.P., McPhee F., Wind-Rotolo M., Chung E., Pasquinelli C., Grasela D.M., Gardiner D.F. Efficacy of an interferon- and ribavirin-free regimen of daclatasvir, asunaprevir, and BMS-791325 in treatment-naive patients with HCV genotype 1 infection. Gastroenterology 2013, 146:420-429.
31. Forns X., Bukh J., Purcell R.H. The challenge of developing a vaccine against hepatitis C virus. J. Hepatol. 2002, 37:684-695.
32. Fournillier A., Gerossier E., Evlashev A., Schmitt D., Simon B., Chatel L., Martin P., Silvestre N., Balloul J.M., Barry R., Inchauspe G. An accelerated vaccine schedule with a poly-antigenic hepatitis C virus MVA-based candidate vaccine induces potent, long lasting and in vivo cross-reactive T cell responses. Vaccine 2007, 25:7339-7353.
33. Frey S.E., Houghton M., Coates S., Abrignani S., Chien D., Rosa D., Pileri P., Ray R., Di Bisceglie A.M., Rinella P., Hill H., Wolff M.C., Schultze V., Han J.H., Scharschmidt B., Belshe R.B. Safety and immunogenicity of HCV E1E2 vaccine adjuvanted with MF59 administered to healthy adults. Vaccine 2010, 28:6367-6373.
34. Fried M.W., Shiffman M.L., Reddy K.R., Smith C., Marinos G., Goncales F.L., Haussinger D., Diago M., Carosi G., Dhumeaux D., Craxi A., Lin A., Hoffman J., Yu J. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N. Engl. J. Med. 2002, 347:975-982.
35. Ge D., Fellay J., Thompson A.J., Simon J.S., Shianna K.V., Urban T.J., Heinzen E.L., Qiu P., Bertelsen A.H., Muir A.J., Sulkowski M., McHutchison J.G., Goldstein D.B. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 2009, 461:399-401.
36. Gelderblom H.C., Nijhuis L.E., de Jong E.C., te Velde A.A., Pajkrt D., Reesink H.W., Beld M.G., van Deventer S.J., Jansen P.L. Monocyte-derived dendritic cells from chronic HCV patients are not infected but show an immature phenotype and aberrant cytokine profile. Liver Int. 2007, 27:944-953.
37. Germi R., Crance J.M., Garin D., Guimet J., Lortat-Jacob H., Ruigrok R.W., Zarski J.P., Drouet E. Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J. Med. Virol. 2002, 68:206-215.
38. Ghany M.G., Nelson D.R., Strader D.B., Thomas D.L., Seeff L.B. An update on treatment of genotype 1 chronic hepatitis C virus infection: 2011 practice guideline by the American Association for the Study of Liver Diseases. Hepatology 2011, 54:1433-1444.
39. Giannini S.L., Hanon E., Moris P., Van Mechelen M., Morel S., Dessy F., Fourneau M.A., Colau B., Suzich J., Losonksy G., Martin M.T., Dubin G., Wettendorff M.A. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine 2006, 24:5937-5949.
40. Gowans E.J., Roberts S., Jones K., Dinatale I., Latour P.A., Chua B., Eriksson E.M., Chin R., Li S., Wall D.M., Sparrow R.L., Moloney J., Loudovaris M., Ffrench R., Prince H.M., Hart D., Zeng W., Torresi J., Brown L.E., Jackson D.C. A phase I clinical trial of dendritic cell immunotherapy in HCV-infected individuals. J. Hepatol. 2010, 53:599-607.
41. Grakoui A., Wychowski C., Lin C., Feinstone S.M., Rice C.M. Expression and identification of hepatitis C virus polyprotein cleavage products. J. Virol. 1993, 67:1385-1395.
42. Grakoui A., Shoukry N.H., Woollard D.J., Han J.H., Hanson H.L., Ghrayeb J., Murthy K.K., Rice C.M., Walker C.M. HCV persistence and immune evasion in the absence of memory T cell help. Science 2003, 302:659-662.
43. Guglietta S., Garbuglia A.R., Salichos L., Ruggeri L., Folgori A., Perrone M.P., Camperio C., Mellace V., Maio G., Maio P., Capobianchi M.R., Spada E., Gargano N., Scotta C., Piccolella E., Del Porto P. Impact of viral selected mutations on T cell mediated immunity in chronically evolving and self limiting acute HCV infection. Virology 2009, 386:398-406.
44. Hadziyannis S.J., Sette H., Morgan T.R., Balan V., Diago M., Marcellin P., Ramadori G., Bodenheimer H., Bernstein D., Rizzetto M., Zeuzem S., Pockros P.J., Lin A., Ackrill A.M. Peginterferon-alpha2a and ribavirin combination therapy in chronic hepatitis C: a randomized study of treatment duration and ribavirin dose. Ann. Intern. Med. 2004, 140:346-355.
45. Helle F., Goffard A., Morel V., Duverlie G., McKeating J., Keck Z.Y., Foung S., Penin F., Dubuisson J., Voisset C. The neutralizing activity of anti-hepatitis C virus antibodies is modulated by specific glycans on the E2 envelope protein. J. Virol. 2007, 81:8101-8111.
46. Hilleman M.R. Overview of the pathogenesis, prophylaxis and therapeusis of viral hepatitis B, with focus on reduction to practical applications. Vaccine 2001, 19:1837-1848.
47. Hiroishi K., Kita H., Kojima M., Okamoto H., Moriyama T., Kaneko T., Ishikawa T., Ohnishi S., Aikawa T., Tanaka N., Yazaki Y., Mitamura K., Imawari M. Cytotoxic T lymphocyte response and viral load in hepatitis C virus infection. Hepatology 1997, 25:705-712.
48. Houghton M., Abrignani S. Prospects for a vaccine against the hepatitis C virus. Nature 2005, 436:961-966.
49. Huang X.J., Lu X., Lei Y.F., Yang J., Yao M., Lan H.Y., Zhang J.M., Jia Z.S., Yin W., Xu Z.K. Cellular immunogenicity of a multi-epitope peptide vaccine candidate based on hepatitis C virus NS5A, NS4B and core proteins in HHD-2 mice. J. Virol. Methods 2013, 189:47-52.
50. Jacobson I.M., McHutchison J.G., Dusheiko G.M., Di Bisceglie A.M., Reddy R., Bzowej N.H. Telaprevir in combination with peginterferon and ribavirin in genotype 1 HCV treatment-naive patients: final results of Phase 3 ADVANCE study. Hepatology 2010, 52:427A.
51. Jacobson I.M., McHutchison J.G., Dusheiko G., Di Bisceglie A.M., Reddy K.R., Bzowej N.H., Marcellin P., Muir A.J., Ferenci P., Flisiak R., George J., Rizzetto M., Shouval D., Sola R., Terg R.A., Yoshida E.M., Adda N., Bengtsson L., Sankoh A.J., Kieffer T.L., George S., Kauffman R.S., Zeuzem S. Telaprevir for previously untreated chronic hepatitis C virus infection. N. Engl. J. Med. 2011, 364:2405-2416.
52. Jolivet-Reynaud C., Adida A., Michel S., Deleage G., Paranhos-Baccala G., Gonin V., Battail-Poirot N., Lacoux X., Rolland D. Characterization of mimotopes mimicking an immunodominant conformational epitope on the hepatitis C virus NS3 helicase. J. Med. Virol. 2004, 72:385-395.
53. Kachko A., Kochneva G., Sivolobova G., Grazhdantseva A., Lupan T., Zubkova I., Wells F., Merchlinsky M., Williams O., Watanabe H., Ivanova A., Shvalov A., Loktev V., Netesov S., Major M.E. New neutralizing antibody epitopes in hepatitis C virus envelope glycoproteins are revealed by dissecting peptide recognition profiles. Vaccine 2011, 30:69-77.
54. Kao J.H., Chen D.S. Global control of hepatitis B virus infection. Lancet Infect. Dis. 2002, 2:395-403.
55. Klade C.S., Wedemeyer H., Berg T., Hinrichsen H., Cholewinska G., Zeuzem S., Blum H., Buschle M., Jelovcan S., Buerger V., Tauber E., Frisch J., Manns M.P. Therapeutic vaccination of chronic hepatitis C nonresponder patients with the peptide vaccine IC41. Gastroenterology 2008, 134:1385-1395.
56. Kurokohchi K., Arima K., Nishioka M. A novel cytotoxic T-cell epitope presented by HLA-A24 molecule in hepatitis C virus infection. J. Hepatol. 2001, 34:930-935.
57. Kwo P.Y., Lawitz E.J., McCone J., Schiff E.R., Vierling J.M., Pound D., Davis M.N., Galati J.S., Gordon S.C., Ravendhran N., Rossaro L., Anderson F.H., Jacobson I.M., Rubin R., Koury K., Pedicone L.D., Brass C.A., Chaudhri E., Albrecht J.K. Efficacy of boceprevir, an NS3 protease inhibitor, in combination with peginterferon alfa-2b and ribavirin in treatment-naive patients with genotype 1 hepatitis C infection (SPRINT-1): an open-label, randomised, multicentre phase 2 trial. Lancet 2010, 376:705-716.
58. Lagging L.M., Meyer K., Westin J., Wejstal R., Norkrans G., Lindh M., Ray R. Neutralization of pseudotyped vesicular stomatitis virus expressing hepatitis C virus envelope glycoprotein 1 or 2 by serum from patients. J. Infect. Dis. 2002, 185:1165-1169.
59. Lauer G.M., Walker B.D. Hepatitis C virus infection. N. Engl. J. Med. 2001, 345:41-52.
60. Lauer G.M., Barnes E., Lucas M., Timm J., Ouchi K., Kim A.Y., Day C.L., Robbins G.K., Casson D.R., Reiser M., Dusheiko G., Allen T.M., Chung R.T., Walker B.D., Klenerman P. High resolution analysis of cellular immune responses in resolved and persistent hepatitis C virus infection. Gastroenterology 2004, 127:924-936.
61. Lavanchy D. The global burden of hepatitis C. Liver Int. 2009, 29(Suppl. 1):74-81.
62. Law M., Maruyama T., Lewis J., Giang E., Tarr A.W., Stamataki Z., Gastaminza P., Chisari F.V., Jones I.M., Fox R.I., Ball J.K., McKeating J.A., Kneteman N.M., Burton D.R. Broadly neutralizing antibodies protect against hepatitis C virus quasispecies challenge. Nat. Med. 2008, 14:25-27.
63. Law J.L., Chen C., Wong J., Hockman D., Santer D.M., Frey S.E., Belshe R.B., Wakita T., Bukh J., Jones C.T., Rice C.M., Abrignani S., Tyrrell D.L., Houghton M. A hepatitis C virus (HCV) vaccine comprising envelope glycoproteins gpE1/gpE2 derived from a single isolate elicits broad cross-genotype neutralizing antibodies in humans. PLoS One 2013, 8:e59776.
64. Lechner F., Wong D.K., Dunbar P.R., Chapman R., Chung R.T., Dohrenwend P., Robbins G., Phillips R., Klenerman P., Walker B.D. Analysis of successful immune responses in persons infected with hepatitis C virus. J. Exp. Med. 2000, 191:1499-1512.
65. Lindenbach B.D., Evans M.J., Syder A.J., Wolk B., Tellinghuisen T.L., Liu C.C., Maruyama T., Hynes R.O., Burton D.R., McKeating J.A., Rice C.M. Complete replication of hepatitis C virus in cell culture. Science 2005, 309:623-626.
66. Liu S., Yang W., Shen L., Turner J.R., Coyne C.B., Wang T. Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection. J. Virol. 2009, 83:2011-2014.
67. 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.
68. Manns M.P., McHutchison J.G., Gordon S.C., Rustgi V.K., Shiffman M., Reindollar R., Goodman Z.D., Koury K., Ling M., Albrecht J.K. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet 2001, 358:958-965.
69. Manns M.P., Wedemeyer H., Cornberg M. Treating viral hepatitis C: efficacy, side effects, and complications. Gut 2006, 55:1350-1359.
70. McHutchison J.G., Manns M.P., Muir A.J., Terrault N.A., Jacobson I.M., Afdhal N.H., Heathcote E.J., Zeuzem S., Reesink H.W., Garg J., Bsharat M., George S., Kauffman R.S., Adda N., Di Bisceglie A.M. Telaprevir for previously treated chronic HCV infection. N. Engl. J. Med. 2010, 362:1292-1303.
71. Mehta S.H., Cox A., Hoover D.R., Wang X.H., Mao Q., Ray S., Strathdee S.A., Vlahov D., Thomas D.L. Protection against persistence of hepatitis C. Lancet 2002, 359:1478-1483.
72. Meuleman P., Bukh J., Verhoye L., Farhoudi A., Vanwolleghem T., Wang R.Y., Desombere I., Alter H., Purcell R.H., Leroux-Roels G. In vivo evaluation of the cross-genotype neutralizing activity of polyclonal antibodies against hepatitis C virus. Hepatology 2011, 53:755-762.
73. Meunier J.C., Gottwein J.M., Houghton M., Russell R.S., Emerson S.U., Bukh J., Purcell R.H. Vaccine-induced cross-genotype reactive neutralizing antibodies against hepatitis C virus. J. Infect. Dis. 2011, 204:1186-1190.
74. Meyer K., Basu A., Przysiecki C.T., Lagging L.M., Di Bisceglie A.M., Conley A.J., Ray R. Complement-mediated enhancement of antibody function for neutralization of pseudotype virus containing hepatitis C virus E2 chimeric glycoprotein. J. Virol. 2002, 76:2150-2158.
75. Missale G., Bertoni R., Lamonaca V., Valli A., Massari M., Mori C., Rumi M.G., Houghton M., Fiaccadori F., Ferrari C. Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. J. Clin. Invest. 1996, 98:706-714.
76. Molina S., Castet V., Fournier-Wirth C., Pichard-Garcia L., Avner R., Harats D., Roitelman J., Barbaras R., Graber P., Ghersa P., Smolarsky M., Funaro A., Malavasi F., Larrey D., Coste J., Fabre J.M., Sa-Cunha A., Maurel P. The low-density lipoprotein receptor plays a role in the infection of primary human hepatocytes by hepatitis C virus. J. Hepatol. 2007, 46:411-419.
77. Nascimbeni M., Mizukoshi E., Bosmann M., Major M.E., Mihalik K., Rice C.M., Feinstone S.M., Rehermann B. Kinetics of CD4+ and CD8+ memory T-cell responses during hepatitis C virus rechallenge of previously recovered chimpanzees. J. Virol. 2003, 77:4781-4793.
78. Neumann-Haefelin C., McKiernan S., Ward S., Viazov S., Spangenberg H.C., Killinger T., Baumert T.F., Nazarova N., Sheridan I., Pybus O., von Weizsacker F., Roggendorf M., Kelleher D., Klenerman P., Blum H.E., Thimme R. Dominant influence of an HLA-B27 restricted CD8+ T cell response in mediating HCV clearance and evolution. Hepatology 2006, 43:563-572.
79. Omata M., Kanda T., Yu M.L., Yokosuka O., Lim S.G., Jafri W., Tateishi R., Hamid S.S., Chuang W.L., Chutaputti A., Wei L., Sollano J., Sarin S.K., Kao J.H., McCaughan G.W. APASL consensus statements and management algorithms for hepatitis C virus infection. Hepatol. Int. 2012, 6:409-435.
80. Osburn W.O., Fisher B.E., Dowd K.A., Urban G., Liu L., Ray S.C., Thomas D.L., Cox A.L. Spontaneous control of primary hepatitis C virus infection and immunity against persistent reinfection. Gastroenterology 2010, 138:315-324.
81. Pedersen J., Carlsen T.H., Prentoe J., Ramirez S., Jensen T.B., Forns X., Alter H., Foung S.K., Law M., Gottwein J., Weis N., Bukh J. Neutralization resistance of hepatitis C virus can be overcome by recombinant human monoclonal antibodies. Hepatology 2013, 58:1587-1597.
82. Pestka J.M., Zeisel M.B., Blaser E., Schurmann P., Bartosch B., Cosset F.L., Patel A.H., Meisel H., Baumert J., Viazov S., Rispeter K., Blum H.E., Roggendorf M., Baumert T.F. Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc. Nat. Acad. Sci. U.S.A. 2007, 104:6025-6030.
83. Pileri P., Uematsu Y., Campagnoli S., Galli G., Falugi F., Petracca R., Weiner A.J., Houghton M., Rosa D., Grandi G., Abrignani S. Binding of hepatitis C virus to CD81. Science 1998, 282:938-941.
84. Ploss A., Evans M.J., Gaysinskaya V.A., Panis M., You H., de Jong Y.P., Rice C.M. Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 2009, 457:882-886.
85. Poordad F., McCone J., Bacon B.R., Bruno S., Manns M.P., Sulkowski M.S. Boceprevir (BOC) combined with peginterferon alfa-2b/ribavirin (P/R) for treatment-naive patients with hepatitis C (HCV) genotype 1: SPRINT-2 final results. Hepatology 2010, 52:402A.
86. Poordad F., McCone J., Bacon B.R., Bruno S., Manns M.P., Sulkowski M.S., Jacobson I.M., Reddy K.R., Goodman Z.D., Boparai N., DiNubile M.J., Sniukiene V., Brass C.A., Albrecht J.K., Bronowicki J.P. Boceprevir for untreated chronic HCV genotype 1 infection. N. Engl. J. Med. 2011, 364:1195-1206.
87. Qiu F., Bi S., Wang Y., Guo M., Yi Y., Chen S., Guo Y., Shen L., Jia Z. Hepatitis C virus-specific cellular and humoral immune responses following immunization with a multi-epitope fusion protein. Int. J. Mol. Med. 2012, 29:12-17.
88. Raghuraman S., Park H., Osburn W.O., Winkelstein E., Edlin B.R., Rehermann B. Spontaneous clearance of chronic hepatitis C virus infection is associated with appearance of neutralizing antibodies and reversal of T-cell exhaustion. J. Infect. Dis. 2012, 205:763-771.
89. Ray R., Meyer K., Banerjee A., Basu A., Coates S., Abrignani S., Houghton M., Frey S.E., Belshe R.B. Characterization of antibodies induced by vaccination with hepatitis C virus envelope glycoproteins. J. Infect. Dis. 2010, 202:862-866.
90. Reed K.E., Rice C.M. Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr. Top. Microbiol. Immunol. 2000, 242:55-84.
91. Sainz B., Barretto N., Martin D.N., Hiraga N., Imamura M., Hussain S., Marsh K.A., Yu X., Chayama K., Alrefai W.A., Uprichard S.L. Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat. Med. 2012, 18:281-285.
92. Salmon-Ceron D., Lewden C., Morlat P., Bevilacqua S., Jougla E., Bonnet F., Heripret L., Costagliola D., May T., Chene G. Liver disease as a major cause of death among HIV infected patients: role of hepatitis C and B viruses and alcohol. J. Hepatol. 2005, 42:799-805.
93. Scarselli E., Ansuini H., Cerino R., Roccasecca R.M., Acali S., Filocamo G., Traboni C., Nicosia A., Cortese R., Vitelli A. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 2002, 21:5017-5025.
94. Schulze zur Wiesch J., Lauer G.M., Day C.L., Kim A.Y., Ouchi K., Duncan J.E., Wurcel A.G., Timm J., Jones A.M., Mothe B., Allen T.M., McGovern B., Lewis-Ximenez L., Sidney J., Sette A., Chung R.T., Walker B.D. Broad repertoire of the CD4+ Th cell response in spontaneously controlled hepatitis C virus infection includes dominant and highly promiscuous epitopes. J. Immunol. 2005, 175:3603-3613.
95. Shepard C.W., Finelli L., Alter M.J. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 2005, 5:558-567.
96. Sherman K.E., Flamm S.L., Afdhal N.H., Nelson D.R., Sulkowski M.S., Everson G.T. Telaprevir in combination with peginterferon alfa2b and ribavirin for 24 or 48 weeks in treatment-naive genotype 1 HCV patients who achieved an extended rapid viral response: final results of Phase 3 ILLUMINATE study. Hepatology 2010, 52:401A.
97. Simmonds P., Bukh J., Combet C., Deleage G., Enomoto N., Feinstone S., Halfon P., Inchauspe G., Kuiken C., Maertens G., Mizokami M., Murphy D.G., Okamoto H., Pawlotsky J.M., Penin F., Sablon E., Shin I.T., Stuyver L.J., Thiel H.J., Viazov S., Weiner A.J., Widell A. Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 2005, 42:962-973.
98. Stamataki Z., Coates S., Evans M.J., Wininger M., Crawford K., Dong C., Fong Y.L., Chien D., Abrignani S., Balfe P., Rice C.M., McKeating J.A., Houghton M. Hepatitis C virus envelope glycoprotein immunization of rodents elicits cross-reactive neutralizing antibodies. Vaccine 2007, 25:7773-7784.
99. Stamataki Z., Grove J., Balfe P., McKeating J.A. Hepatitis C virus entry and neutralization. Clin. Liver Dis. 2008, 12:693-712. x.
100. Strickland G.T., El-Kamary S.S., Klenerman P., Nicosia A. Hepatitis C vaccine: supply and demand. Lancet Infect. Dis. 2008, 8:379-386.
101. Suppiah V., Moldovan M., Ahlenstiel G., Berg T., Weltman M., Abate M.L., Bassendine M., Spengler U., Dore G.J., Powell E., Riordan S., Sheridan D., Smedile A., Fragomeli V., Muller T., Bahlo M., Stewart G.J., Booth D.R., George J. IL28B is associated with response to chronic hepatitis C interferon-alpha and ribavirin therapy. Nat. Genet. 2009, 41:1100-1104.
102. Tanaka Y., Nishida N., Sugiyama M., Kurosaki M., Matsuura K., Sakamoto N., Nakagawa M., Korenaga M., Hino K., Hige S., Ito Y., Mita E., Tanaka E., Mochida S., Murawaki Y., Honda M., Sakai A., Hiasa Y., Nishiguchi S., Koike A., Sakaida I., Imamura M., Ito K., Yano K., Masaki N., Sugauchi F., Izumi N., Tokunaga K., Mizokami M. Genome-wide association of IL28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C. Nat. Genet. 2009, 41:1105-1109.
103. Tang H., Grise H. Cellular and molecular biology of HCV infection and hepatitis. Clin. Sci. (London) 2009, 117:49-65.
104. Thimme R., Oldach D., Chang K.M., Steiger C., Ray S.C., Chisari F.V. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J. Exp. Med. 2001, 194:1395-1406.
105. Thomas D.L., Thio C.L., Martin M.P., Qi Y., Ge D., O'Huigin C., Kidd J., Kidd K., Khakoo S.I., Alexander G., Goedert J.J., Kirk G.D., Donfield S.M., Rosen H.R., Tobler L.H., Busch M.P., McHutchison J.G., Goldstein D.B., Carrington M. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 2009, 461:798-801.
106. Torresi J., Bharadwaj M., Jackson D.C., Gowans E.J. Neutralising antibody, CTL and dendritic cell responses to hepatitis C virus: a preventative vaccine strategy. Curr. Drug Targets 2004, 5:41-56.
107. Urbani S., Uggeri J., Matsuura Y., Miyamura T., Penna A., Boni C., Ferrari C. Identification of immunodominant hepatitis C virus (HCV)-specific cytotoxic T-cell epitopes by stimulation with endogenously synthesized HCV antigens. Hepatology 2001, 33:1533-1543.
108. Vertuani S., Bazzaro M., Gualandi G., Micheletti F., Marastoni M., Fortini C., Canella A., Marino M., Tomatis R., Traniello S., Gavioli R. Effect of interferon-alpha therapy on epitope-specific cytotoxic T lymphocyte responses in hepatitis C virus-infected individuals. Eur. J. Immunol. 2002, 32:144-154.
109. von Hahn T., Yoon J.C., Alter H., Rice C.M., Rehermann B., Balfe P., McKeating J.A. Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 2007, 132:667-678.
110. Wahid A., Dubuisson J. Virus-neutralizing antibodies to hepatitis C virus. J. Viral Hepat. 2013, 20:369-376.
111. Wedemeyer H., He X.S., Nascimbeni M., Davis A.R., Greenberg H.B., Hoofnagle J.H., Liang T.J., Alter H., Rehermann B. Impaired effector function of hepatitis C virus-specific CD8+ T cells in chronic hepatitis C virus infection. J. Immunol. 2002, 169:3447-3458.
112. Wertheimer A.M., Miner C., Lewinsohn D.M., Sasaki A.W., Kaufman E., Rosen H.R. Novel CD4+ and CD8+ T-cell determinants within the NS3 protein in subjects with spontaneously resolved HCV infection. Hepatology 2003, 37:577-589.
113. Yutani S., Komatsu N., Shichijo S., Yoshida K., Takedatsu H., Itou M., Kuromatu R., Ide T., Tanaka M., Sata M., Yamada A., Itoh K. Phase I clinical study of a peptide vaccination for hepatitis C virus-infected patients with different human leukocyte antigen-class I-A alleles. Cancer Sci. 2009, 100:1935-1942.
114. Zeng R., Li G., Ling S., Zhang H., Yao Z., Xiu B., He F., Huang R., Wei L. A novel combined vaccine candidate containing epitopes of HCV NS3, core and E1 proteins induces multi-specific immune responses in BALB/c mice. Antiviral Res. 2009, 84:23-30.
115. Zhang Z.X., Lazdina U., Chen M., Peterson D.L., Sallberg M. Characterization of a monoclonal antibody and its single-chain antibody fragment recognizing the nucleoside Triphosphatase/Helicase domain of the hepatitis C virus nonstructural 3 protein. Clin. Diagn. Lab. Immunol. 2000, 7:58-63.
116. Zhang P., Zhong L., Struble E.B., Watanabe H., Kachko A., Mihalik K., Virata-Theimer M.L., Alter H.J., Feinstone S., Major M. Depletion of interfering antibodies in chronic hepatitis C patients and vaccinated chimpanzees reveals broad cross-genotype neutralizing activity. Proc. Nat. Acad. Sci. U.S.A. 2009, 106:7537-7541.
117. Zhou Y., Zhao F., Chen L., Ma L., Wang Y., He Y., Ma Z., Liu H., Guo Y., Zhang Y., Yao Z., Hao C., Jia Z. Development of a dendritic cell vaccine encoding multiple cytotoxic T lymphocyte epitopes targeting hepatitis C virus. Int. J. Mol. Med. 2013, 32:901-909.