Acute infection with a single hepatitis C virus strain in dialysis patients: Analysis of adaptive immune response and viral variability

Journal of Hepatology

Volumn 50, Issue 4, 2009, Pages 693-704

  Weseslindtner, Lukas ^a   Neumann Haefelin, Christoph ^b   Viazov, Sergei ^c   Haberstroh, Anita ^b   Kletzmayr, Josef ^d   Aberle, Judith H ^a   Timm, Joerg ^c   Ross, Stefan R ^c   Klauser Braun, Renate ^d   Baumert, Thomas F ^b,e   Roggendorf, Michael ^c   Thimme, Robert ^b   Holzmann, Heidemarie ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

^d DANUBE HOSPITAL   (Austria)

^e INSERM   (France)

Author keywords

Acute hepatitis C; CD4; CD8; Dialysis; Hepatitis C virus; Immune response; Neutralizing antibodies; T cells; Viral variability; Virus host interaction

Indexed keywords

NEUTRALIZING ANTIBODY;

ADAPTIVE IMMUNITY; ADULT; ARTICLE; CASE REPORT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE COURSE; ENVELOPE GENE; FEMALE; GENETIC STABILITY; GENETIC VARIABILITY; HEMODIALYSIS PATIENT; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INFECTION CONTROL; MALE; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROSPECTIVE STUDY; VIREMIA; VIRUS GENOME; VIRUS STRAIN;

ADULT; BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CROSS INFECTION; CYTOKINES; FEMALE; GENOTYPE; HEPACIVIRUS; HEPATITIS C; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; RENAL DIALYSIS; RNA, VIRAL; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS; TRANSAMINASES; VIRAL LOAD;

EID: 61749094559     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2008.11.023     Document Type: Article

References (50)

1. Thomas D.L., and Seeff L.B. Natural history of hepatitis C. Clin Liver Dis 9 (2005) 383-398
2. Thimme R., Oldach D., Chang K.M., Steiger C., Ray S.C., and Chisari F.V. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 194 (2001) 1395-1406
3. Tester I., Smyk-Pearson S., Wang P., Wertheimer A., Yao E., Lewinsohn D.M., et al. Immune evasion versus recovery after acute hepatitis C virus infection from a shared source. J Exp Med 201 (2005) 1725-1731
4. Rosen H.R., Miner C., Sasaki A.W., Lewinsohn D.M., Conrad A.J., Bakke A., et al. Frequencies of HCV-specific effector CD4+ T cells by flow cytometry: correlation with clinical disease stages. Hepatology 35 (2002) 190-198
5. Lauer G.M., Barnes E., Lucas M., Timm J., Ouchi K., Kim A.Y., et al. High resolution analysis of cellular immune responses in resolved and persistent hepatitis C virus infection. Gastroenterology 127 (2004) 924-936
6. Folgori A., Spada E., Pezzanera M., Ruggeri L., Mele A., Garbuglia A.R., et al. Early impairment of hepatitis C virus specific T cell proliferation during acute infection leads to failure of viral clearance. Gut 55 (2006) 1012-1019
7. Thimme R., Bukh J., Spangenberg H.C., Wieland S., Pemberton J., Steiger C., et al. Viral and immunological determinants of hepatitis C virus clearance, persistence, and disease. Proc Natl Acad Sci USA 99 (2002) 15661-15668
8. Urbani S., Amadei B., Fisicaro P., Tola D., Orlandini A., Sacchelli L., et al. Outcome of acute hepatitis C is related to virus-specific CD4 function and maturation of antiviral memory CD8 responses. Hepatology 44 (2006) 126-139
9. Gerlach J.T., Diepolder H.M., Jung M.C., Gruener N.H., Schraut W.W., Zachoval R., et al. Recurrence of hepatitis C virus after loss of virus-specific CD4(+) T-cell response in acute hepatitis C. Gastroenterology 117 (1999) 933-941
10. Ulsenheimer A., Lucas M., Seth N.P., Gerlach J.T., Gruener N.H., Loughry A., et al. Transient immunological control during acute hepatitis C virus infection: ex vivo analysis of helper T-cell responses. J Viral Hepat 13 (2006) 708-714
11. Aberle J.H., Formann E., Steindl-Munda P., Weseslindtner L., Gurguta C., Perstinger G., et al. Prospective study of viral clearance and CD4(+) T-cell response in acute hepatitis C primary infection and reinfection. J Clin Virol 36 (2006) 24-31
12. Kaplan D.E., Sugimoto K., Newton K., Valiga M.E., Ikeda F., Aytaman A., et al. Discordant role of CD4 T-cell response relative to neutralizing antibody and CD8 T-cell responses in acute hepatitis C. Gastroenterology 132 (2007) 654-666
13. Zibert A., Meisel H., Kraas W., Schulz A., Jung G., and Roggendorf M. Early antibody response against hypervariable region 1 is associated with acute self-limiting infections of hepatitis C virus. Hepatology 25 (1997) 1245-1249
14. Pestka J.M., Zeisel M.B., Bläser E., Schürmann P., Bartosch B., Cosset F.L., et al. Rapid induction of virus-neutralizing antibodies and viral clearance in a single-source outbreak of hepatitis C. Proc Natl Acad Sci USA 104 (2007) 6025-6030
15. Timm J., Lauer G.M., Kavanagh D.G., Sheridan I., Kim A.Y., Lucas M., et al. CD8 epitope escape and reversion in acute HCV infection. J Exp Med 200 (2004) 1593-1604
16. Neumann-Haefelin C., McKiernan S., Ward S., Viazov S., Spangenberg H.C., Killinger T., et al. Dominant influence of an HLA-B27 restricted CD8+ T cell response in mediating HCV clearance and evolution. Hepatology 43 (2006) 563-572
17. Cox A.L., Mosbruger T., Mao Q., Liu Z., Wang X.H., Yang H.C., et al. Cellular immune selection with hepatitis C virus persistence in humans. J Exp Med 201 (2005) 1741-1752
18. Grakoui A., Shoukry N.H., Woollard D.J., Han J.H., Hanson H.L., Ghrayeb J., et al. HCV persistence and immune evasion in the absence of memory T cell help. Science 302 (2003) 659-662
19. von Hahn T., Yoon J.C., Alter H., Rice C.M., Rehermann B., Balfe P., et al. Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 132 (2007) 667-678
20. Farci P., Shimoda A., Coiana A., Diaz G., Peddis G., Melpolder J.C., et al. The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288 (2000) 339-344
21. Ray S.C., Wang Y.M., Laeyendecker O., Ticehurst J.R., Villano S.A., and Thomas D.L. Acute hepatitis C virus structural gene sequences as predictors of persistent viremia: hypervariable region 1 as a decoy. J Virol 73 (1999) 2938-2946
22. Sheridan I., Pybus O.G., Holmes E.C., and Klenerman P. High-resolution phylogenetic analysis of hepatitis C virus adaptation and its relationship to disease progression. J Virol 78 (2004) 3447-3454
23. Fabrizi F., Lunghi G., Ganeshan S.V., Martin P., and Messa P. Hepatitis C virus infection and the dialysis patient. Semin Dial 20 (2007) 416-422
24. Eleftheriadis T., Antoniadi G., Liakopoulos V., Kartsios C., and Stefanidis I. Disturbances of acquired immunity in hemodialysis patients. Semin Dial 20 (2007) 440-451
25. Ankersmit H.J., Deicher R., Moser B., Teufel I., Roth G., Gerlitz S., et al. Impaired T cell proliferation, increased soluble death-inducing receptors and activation-induced T cell death in patients undergoing haemodialysis. Clin Exp Immunol 125 (2001) 142-148
26. Stachowski J., Pollok M., Burrichter H., Spithaler C., and Baldamus C.A. Signalling via the TCR/CD3 antigen receptor complex in uremia is limited by the receptors number. Nephron 64 (1993) 369-375
27. Stevens C.E., Alter H.J., Taylor P.E., Zang E.A., Harley E.J., and Szmuness W. Hepatitis B vaccine in patients receiving hemodialysis. Immunogenicity and efficacy. N Engl J Med 311 (1984) 496-501
28. Rautenberg P., Teifke I., Schlegelberger T., and Ullmann U. Influenza subtype-specific IgA, IgM and IgG responses in patients on hemodialysis after influenza vaccination. Infection 16 (1988) 323-328
29. Kwok S., and Higuchi R. Avoiding false positives with PCR. Nature 339 (1989) 237-238
30. Mizokami M., and Lau J.Y.N. Molecular evolutionary analysis. Its application in the study of hepatitis C virus. In: Lau J.Y.N. (Ed). Hepatitis C protocols (1998), Humana Press, Totowa 147-158
31. Felsenstein J. PHYLIP (Phylogenetic Inference Package). Available from: http://evolution.gs.washington.edu/phylip.html. Accessed November 2006.
32. Neumann-Haefelin C., Timm J., Spangenberg H.C., Wischniowski N., Nazarova N., Kersting N., et al. Virological and immunological determinants of intrahepatic virus-specific CD8+ T-cell failure in chronic hepatitis C virus infection. Hepatology 47 (2008) 1824-1836
33. Barth H., Schnober E.K., Zhang F., Linhardt R.J., Depla E., Boson B., et al. Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. J Virol 80 (2006) 10579-10590
34. Sarobe P., Huarte E., Lasarte J.J., López-Di{dotless}́az de Cerio A., Garci{dotless}́a N., Borrás-Cuesta F., et al. Characterization of an immunologically conserved epitope from hepatitis C virus E2 glycoprotein recognized by HLA-A2 restricted cytotoxic T lymphocytes. J Hepatol 34 (2001) 321-329
35. Wong D.K., Dudley D.D., Afdhal N.H., Dienstag J., Rice C.M., Wang L., et al. Liver-derived CTL in hepatitis C virus infection: breadth and specificity of responses in a cohort of persons with chronic infection. J Immunol 160 (1998) 1479-1488
36. Wong D.K., Dudley D.D., Dohrenwend P.B., Lauer G.M., Chung R.T., Thomas D.L., et al. Detection of diverse hepatitis C virus (HCV)-specific cytotoxic T lymphocytes in peripheral blood of infected persons by screening for responses to all translated proteins of HCV. J Virol 75 (2001) 1229-1235
37. Koziel M.J., Wong D.K., Dudley D., Houghton M., and Walker B.D. Hepatitis C virus-specific cytolytic T lymphocyte and T helper cell responses in seronegative persons. J Infect Dis 176 (1997) 859-866
38. Koziel M.J., Dudley D., Afdhal N., Grakoui A., Rice C.M., Choo Q.L., et al. HLA class I-restricted cytotoxic T lymphocytes specific for hepatitis C virus. Identification of multiple epitopes and characterization of patterns of cytokine release. J Clin Invest 96 (1995) 2311-2321
39. Scognamiglio P., Accapezzato D., Casciaro M.A., Cacciani A., Artini M., Bruno G., et al. Presence of effector CD8+ T cells in hepatitis C virus-exposed healthy seronegative donors. J Immunol 162 (1999) 6681-6689
40. Prezzi C., Casciaro M.A., Francavilla V., Schiaffella E., Finocchi L., Chircu L.V., et al. Virus-specific CD8(+) T cells with type 1 or type 2 cytokine profile are related to different disease activity in chronic hepatitis C virus infection. Eur J Immunol 31 (2001) 894-906
41. Rehermann B., Chang K.M., McHutchinson J., Kokka R., Houghton M., Rice C.M., et al. Differential cytotoxic T-lymphocyte responsiveness to the hepatitis B and C viruses in chronically infected patients. J Virol 70 (1996) 7092-7102
42. Rehermann B., Chang K.M., McHutchison J.G., Kokka R., Houghton M., and Chisari F.V. Quantitative analysis of the peripheral blood cytotoxic T lymphocyte response in patients with chronic hepatitis C virus infection. J Clin Invest 98 (1996) 1432-1440
43. Takaki A., Wiese M., Maertens G., Depla E., Seifert U., Liebetrau A., et al. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat Med 6 (2000) 578-582
44. Sarobe P., Jauregui J.I., Lasarte J.J., Garci{dotless}́a N., Civeira M.P., Borrás-Cuesta F., et al. Production of interleukin-2 in response to synthetic peptides from hepatitis C virus E1 protein in patients with chronic hepatitis C: relationship with the response to interferon treatment. J Hepatol 25 (1996) 1-9
45. McKiernan S.M., Hagan R., Curry M., McDonald G.S., Kelly A., Nolan N., et al. Distinct MHC class I and II alleles are associated with hepatitis C viral clearance, originating from a single source. Hepatology 40 (2004) 108-114
46. Somsouk M., Lauer G.M., Casson D., Terella A., Day C.L., Walker B.D., et al. Spontaneous resolution of chronic hepatitis C virus disease after withdrawal of immunosuppression. Gastroenterology 124 (2003) 1946-1949
47. Lavillette D., Morice Y., Germanidis G., Donot P., Soulier A., Pagkalos E., 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 79 (2005) 6023-6034
48. Girndt M. Humoral immune responses in uremia and the role of IL-10. Blood Purif 20 (2002) 485-488
49. Booth J.C., Kumar U., Webster D., Monjardino J., and Thomas H.C. 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 27 (1998) 223-227
50. Wertheimer A.M., Miner C., Lewinsohn D.M., Sasaki A.W., Kaufman E., and Rosen H.R. Novel CD4+ and CD8+ T-cell determinants within the NS3 protein in subjects with spontaneously resolved HCV infection. Hepatology 37 (2003) 577-589