1887

Abstract

Hepatitis C virus (HCV) exists as a complex swarm of genetically related viruses known as a quasispecies. Recent work has shown that quasispecies complexity and evolutionary rates are associated with the outcome of acute infection. Knowledge of how the virus population evolves at different stages of chronic infection is less clear. We have studied rates of evolution of the first hypervariable region (HVR1) of the E2 envelope protein in six individuals with disparate liver disease severity. These data show that virus populations present in individuals with mild non-progressive liver disease evolve in a typical Darwinian fashion, with a consistent accumulation of non-synonymous (amino acid-changing) substitutions. By contrast, the virus population remains relatively static in individuals with severe progressive liver disease. Possible mechanisms for this disparity are discussed.

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2002-01-01
2020-07-10
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References

  1. Alter M. J., Margolis H. S., Krawczynski K., Judson F. N., Mares A., Alexander W. J., Hu P. Y., Miller J. K., Gerber M. A., Sampliner R. E., Meeks E., Beech M. J.. 1992; The natural history of community-acquired hepatitis C in the United States. New England Journal of Medicine327:1899–1905
    [Google Scholar]
  2. Ball J. K., Holmes E. C., Whitwell H., Desselberger U.. 1994; Genomic variation of human immunodeficiency virus type 1 (HIV-1): molecular analyses of HIV-1 in sequential blood samples and various organs obtained at autopsy. Journal of General Virology75:67–79
    [Google Scholar]
  3. Berger E. A., Doms R. W., Fenyo E. M., Korber B. T., Littman D. R., Moore J. P., Sattentau Q. J., Schuitemaker H., Sodroski J., Weiss R. A.. 1998; A new classification for HIV-1. Nature391:240
    [Google Scholar]
  4. Booth J. C., Kumar L., Webster D., Monjardino J., Thomas H. C.. 1998; Comparison of the rate of sequence variation in the hypervariable region (HVR) of the E2/NS1 region of hepatitis C virus in normal and hypogammaglobulinaemic patients. Hepatology27:223–227
    [Google Scholar]
  5. Cabot B., Martell M., Esteban J. I., Sauleda S., Otero T., Esteban R., Guardia J., Gomez J.. 2000; Nucleotide and amino acid complexity of hepatitis C virus quasispecies in serum and liver. Journal of Virology74:805–811
    [Google Scholar]
  6. Chang K. M., Rehermann B., McHutchison J. G., Pasquellini C., Southwood S., Sette A., Chisari F. V.. 1997; Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. Journal of Clinical Investigation100:2376–2385
    [Google Scholar]
  7. Chomczynski P., Saachi N.. 1987; Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry162:156–159
    [Google Scholar]
  8. Choo Q. L., Richman K. H., Han J. H., Berger K., Lee C., Dong C., Gallegos C., Coit D., Medina-Selby R., Barr P. J.. 1991; Genetic organization and diversity of the hepatitis C virus. Proceedings of the National Academy of Sciences, USA88:2451–2455
    [Google Scholar]
  9. Cronin T. M., Raymo M. E.. 1997; Orbital forcing of deep-sea benthic species diversity. Nature385:624–627
    [Google Scholar]
  10. Fanning L. E., Kenny-Walsh J., Levis K. R., Choudury B., Cannon M., Sheenan M., Whelton M., Shanahan F.. 2000; Natural fluctuations of hepatitis C viral load in a homogeneous patient population: a prospective study. Hepatology31:225–229
    [Google Scholar]
  11. Farci P., Shimoda A., Wong D., Cabezon T., de Gioannis D., Strazzera A., Shimizu Y., Shapiro M., Alter H. J., Purceli R. H.. 1996; Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proceedings of the National Academy of Sciences, USA93:15394–15399
    [Google Scholar]
  12. Farci P., Shimoda A., Coiana A., Diaz G., Peddis G., Melpolder J. C., Strazzera A., Chien D. Y., Munoz S. J., Balestrieri A., Purcell R. H., Alter H. J.. 2000; The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science288:339–344
    [Google Scholar]
  13. Felsenstein J.. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution39:783–791
    [Google Scholar]
  14. Fouchier R. A. M., Groenink M., Kootstra N. A., Tersmette M., Huisman H. G., Meidema F., Scuitemaker H.. 1992; Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. Journal of Virology66:3183–3187
    [Google Scholar]
  15. Frasca L., Del Porto P., Tuosto L., Marinari B., Scotta C., Carbonari M., Nicosia A., Piccolella E.. 1999; Hypervariable region 1 variants act as TCR antagonists for hepatitis C virus-specific CD4+ T cells. Journal of Immunology162:650–658
    [Google Scholar]
  16. Fukumoto T., Berg T., Ku Y., Bechstein W. O., Knoop M., Lemmens H.-P., Lobeck H., Hopf U., Neuhaus P.. 1996; Viral dynamics of hepatitis C early after orthoptic liver transplantation: evidence for rapid turnover of serum virions. Hepatology24:1351–1354
    [Google Scholar]
  17. Gonzalez-Peralta R. P., Qian K., She J. Y., Davis G. L., Ohno T., Mizokami M., Lau J. Y. N.. 1996; Clinical implications of viral quasispecies heterogeneity in chronic hepatitis C. Journal of Medical Virology49:242–247
    [Google Scholar]
  18. Gretch D. R., Polyak S. J., Wilson J. J., Carithers R. L. Jr, Perkins J. D., Corey L.. 1996; Tracking hepatitis C virus quasispecies major and minor variants in symptomatic and asymptomatic liver transplant recipients. Journal of Virology70:7622–7631
    [Google Scholar]
  19. Hayashi J., Kishihara Y., Yamaji K., Furusyo N., Yamamoto T., Pae Y., Etoh Y., Ikematsu H., Kashiwagi S.. 1997; Hepatitis C viral quasispecies and liver damage in patients with chronic hepatitis C virus infection. Hepatology25:697–701
    [Google Scholar]
  20. Hollingsworth R. C., Sillekens P., Van Deurson P., Neal K. R., Irving W. L.. 1996; Serum HCV RNA levels assessed by quantitative NASBA™: stability of viral load over time and lack of correlation with liver disease. Journal of Hepatology25:301–306
    [Google Scholar]
  21. Holzmann H., Kundi M., Stiasny K., Clement J., McKenna P., Kunz C., Heinz F. X.. 1996; Correlation between ELISA, hemagglutination inhibition, and neutralization tests after vaccination against tick-borne encephalitis. Journal of Medical Virology48:102–107
    [Google Scholar]
  22. Honda M., Kaneko S., Sakai A., Unoura M., Murakami S., Kobayashi K.. 1994; Degree of diversity of hepatitis C virus quasispecies and progression of liver disease. Hepatology20:1144–1151
    [Google Scholar]
  23. Ishak K., Baptista A., Bianchi L., Callea F., De Groote J., Gudat F., Denk H., Desmet V., Korb G., MacSween R. N.. 1995; Histological grading and staging of chronic hepatitis. Journal of Hepatology22:696–699
    [Google Scholar]
  24. Kimura M.. 1980; A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. Journal of Molecular Evolution16:111–120
    [Google Scholar]
  25. Klenerman P., Zinkernagel R. M.. 1998; Original antigenic sin impairs cytotoxic T lymphocyte responses to viruses bearing variant epitopes. Nature394:482–485
    [Google Scholar]
  26. Knodell R. G., Ishak K. G., Black W. C.. 1981; Formulation and application of a numerical scoring system for assessing histological activity in asymptomatic chronic active hepatitis. Hepatology1:431–435
    [Google Scholar]
  27. Korber B., Myers G.. 1992; Signature pattern analysis: a method for assessing viral sequence relatedness. AIDS Research and Human Retroviruses8:1549–1560
    [Google Scholar]
  28. Kumar U., Monjardino J., Thomas H. C.. 1994; Hypervariable region of hepatitis C virus envelope glycoprotein (E2/NS1) in an agammaglobulinaemic patient. Gastroenterology106:1072–1075
    [Google Scholar]
  29. Laskus T., Radkowski M., Wang L.-F., Nowicki M., Rakela J.. 2000; Uneven distribution of hepatitis C virus quasispecies in tissues from subjects with end-stage liver disease: confounding effect of viral adsorption and mounting evidence for the presence of extra-hepatic replication. Journal of Virology74:1014–1017
    [Google Scholar]
  30. Lawal Z., Petrik J., Wong V.-S., Alexander G. J. M., Allain J.-P.. 1997; Hepatitis C virus genomic variability in untreated and immunosuppressed patients. Virology228:107–111
    [Google Scholar]
  31. Li W. H.. 1993; Unbiased estimation of the rates of synonymous and non-synonymous substitution. Journal of Molecular Evolution36:96–99
    [Google Scholar]
  32. Lopez-Labrador F. X., Ampurdanes S., Gimenez-Barcons M., Guilera M., Costa J., Jimenez de Anta M. T., Sanchez-Tapies J. M., Rodes J., Saiz J. C.. 1999; Relationship of the genomic complexity of hepatitis C virus with liver disease severity and response to interferon in patients with chronic HCV genotype 1b interferon. Hepatology29:897–903
    [Google Scholar]
  33. McAllister J., Casino C., Davidson F., Power J., Lawlor E., Yap P. L., Simmonds P., Smith D. B.. 1998; Long-term evolution of the hypervariable region of hepatitis C virus in a common-source-infected cohort. Journal of Virology72:4893–4905
    [Google Scholar]
  34. Majid A., Jackson P., Lawal Z., Pearson G. M. J., Parker H., Alexander G. M. J., Allain J.-P., Petrik J.. 1999; Ontogeny of hepatitis C virus (HCV) hypervariable region 1 (HVR1) heterogeneity and HVR1 antibody responses over a 3 year period in a patient infected with HCV type 2b. Journal of General Virology80:317–325
    [Google Scholar]
  35. Makris M., Preston F. E., Rosendaal F. R., Underwood J. C. E., Rice K. M., Triger D. R.. 1996; The natural history of chronic hepatitis C in haemophiliacs. British Journal of Haematology94:746–752
    [Google Scholar]
  36. Manzin A., Solforosi L., Debiaggi M., Zara F., Tanzi E., Romano L., Zanetti A. R., Clementi M.. 2000; Dominant role of host selective pressure in driving hepatitis C virus evolution in perinatal infection. Journal of Virology74:4327–4334
    [Google Scholar]
  37. Martell M., Esteban J. J., Quer J., Genesca J., Weiner A., Esteban R., Guardia J., Gomez J.. 1992; Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: quasispecies nature of HCV genome distribution. Journal of Virology66:3225–3229
    [Google Scholar]
  38. Messier W., Stewart C.-B.. 1997; Episodic adaptive evolution of primate lysozymes. Nature385:151–154
    [Google Scholar]
  39. Meyerhans A., Vartanian J.-P., Wain-Hobson S.. 1990; DNA recombination during PCR. Nucleic Acids Research18:1687–1691
    [Google Scholar]
  40. Mohsen A.. The Trent Hepatitis C Virus Study Group 2001; The epidemiology of hepatitis C in a UK Health Regional population of 5·12 million. Gut48:707–713
    [Google Scholar]
  41. Mondelli M. U., Cerino A., Lisa A., Brambilla S., Segagni L., Cividini A., Bissolati M., Missale M., Bellati G., Meola A., Bruniercole B., Nicosia A., Galfre G., Silini E.. 1999; Antibody responses to hepatitis C virus hypervariable region 1: evidence for cross-reactivity and immune-mediated sequence variation. Hepatology30:537–545
    [Google Scholar]
  42. Naito M., Hayashi N., Moribe T., Hagiwara H., Mita E., Kanazawa Y., Kasahara A., Fusamoto H., Kamada T.. 1995; Hepatitis C viral quasispecies in hepatitis C virus carriers with normal liver enzymes and patients with type C chronic liver disease. Hepatology22:407–412
    [Google Scholar]
  43. Natali A., Valcavi P., Chezzi C.. 1996; Antigenic variation in influenza viruses. Microbiologia Medica11:21–25
    [Google Scholar]
  44. Navas S., Martin J., Quiroga J. A., Castillo I., Carreno V.. 1998; Genetic diversity and tissue compartmentalization of the hepatitis C virus genome in blood mononuclear cells, liver, and serum from chronic hepatitis C patients. Journal of Virology72:1640–1646
    [Google Scholar]
  45. Neumann A. U., Lam N. P., Dahari H., Gretch D. R., Wiley T. E., Layden T. J., Perelson A. S.. 1998; Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon alpha therapy. Science282:103–107
    [Google Scholar]
  46. Okamoto H., Kojima M., Okada S., Yoshizawa H., Iizuka H., Tanaka T., Muchmore E. E., Peterson D. A., Ito Y., Mishiro S.. 1992; Genetic drift of hepatitis C virus during an 8·2 year infection in a chimpanzee: variability and stability. Virology190:894–899
    [Google Scholar]
  47. Puoti C., Magrini A., Stati T., Rigato P., Montagnese F., Rossi P., Aldegheri L., Resta S.. 1997; Clinical, histological and virological features of hepatitis C virus carriers with persistently normal and abnormal alanine transaminase levels. Hepatology26:1393–1398
    [Google Scholar]
  48. Ramratnam B., Bonhoeffer S., Binley J., Hurley A., Zhang L., Mittler J. E., Markowitz M., Moore J. P., Perelson A. S., Ho D. D.. 1999; Rapid production and clearance of HIV-1 and hepatitis C virus assessed by large volume plasma apheresis. Lancet354:1782–1785
    [Google Scholar]
  49. Ray S. C., Wang Y. M., Laeyendecker O., Ticehurst J. R., Villano S. A., Thomas D. L.. 1999; Acute hepatitis C virus structural gene sequences as predictors of persistent viremia: hypervariable region 1 as a decoy. Journal of Virology73:2938–2946
    [Google Scholar]
  50. Rosa D., Campagnoli S., Moretto C., Guenzi E., Cousens L., Chin M., Dong C., Weiner A. J., Lau J. Y. N., Choo Q. L., Chien D., Pileri P., Houghton M., Abrignani S.. 1996; A quantitative test to estimate neutralizing antibodies to the hepatitis C virus: cytofluorimetric assessment of envelope glycoprotein 2 binding to target cells. Proceedings of the National Academy of Sciences, USA93:1759–1763
    [Google Scholar]
  51. Saitou N., Nei M.. 1987; The neighbor-joining method: a new method for reconstructing evolutionary trees. Molecular Biology and Evolution4:406–425
    [Google Scholar]
  52. Schuitemaker H., Koot M., Kootstra N. A., Dercksen M. W., de Goede R. E. Y., van Steenwijk R. P., Lange J. M. A., Eeftink Schattenkerk J. K. M., Meidema F., Tersmette M.. 1992; Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from moncytotropic to T-cell tropic virus populations. Journal of Virology66:1354–1360
    [Google Scholar]
  53. Sekiya H., Kato N., Ootsuyama Y., Nakazawa T., Yamauchi K., Shimotohno K.. 1994; Genetic alterations of the putative envelope proteins encoding region of the hepatitis C virus in the progression to relapsed phase from acute hepatitis: humoral immune response to hypervariable region 1. International Journal of Cancer57:664–670
    [Google Scholar]
  54. Simmonds P., Balfe P., Peutherer J. F., Ludlam C. A., Bishop J. O., Leigh Brown A. J.. 1990; Human immunodeficiency virus-infected individuals contain provirus in small numbers of peripheral blood mononuclear cells and at low copy number. Journal of Virology64:864–872
    [Google Scholar]
  55. Swofford D. L.. 1998; PAUP*. Phylogenetic analysis using parsimony (*and other methods. Version4: Sinnauer Associates, Sunderland, Massachusetts:
    [Google Scholar]
  56. Taylor R. R., Egan A., McGuinness D., Jepson A., Adair R., Drakely C., Riley E.. 1996; Selective recognition of malaria antigens by human serum antibodies is not genetically determined but demonstrates some features of clonal imprinting. International Journal of Immunology8:905–915
    [Google Scholar]
  57. Thompson J. D., Higgins D. G., Gibson T. J.. 1994; CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research22:673–4680
    [Google Scholar]
  58. Wang H., Eckels D. D.. 1999; Mutations in immunodominant T cell epitopes derived from the non-structural 3 protein of hepatitis C virus have the potential for generating escape variants that may have important consequences for T cell recognition. Journal of Immunology162:4177–4183
    [Google Scholar]
  59. Weiner A. J., Geyson H. M., Christopherson C., Hall J. E., Mason T. J., Saracco G., Bonino F., Crawford K., Marion C. D., Crawford K. A.. 1992; Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: potential role in chronic HCV infections. Proceedings of the National Academy of Sciences, USA89:3468–3472
    [Google Scholar]
  60. Yuki N., Hayashi N., Moribe T., Matsushita Y., Tabata T., Inoue T., Kanazawa Y., Ohkawa K., Kasahara A., Fusamoto H., Kamada T.. 1997; Relation of disease activity during chronic hepatitis C infection to complexity of hypervariable region 1 quasispecies. Hepatology25:439–444
    [Google Scholar]
  61. Zhang L. Q., Diaz R. S., Ho D. D., Mosley J. W., Busch M. P., Mayer A.. 1997; Host-specific driving force in human immunodeficiency virus type 1 evolution in vivo. Journal of Virology71:2555–2561
    [Google Scholar]
  62. Zibert A., Kraas W., Meisel H., Jung G., Roggendorf M.. 1997; Epitope mapping of antibodies directed against hypervariable region 1 in acute self-limiting and chronic infections due to hepatitis C virus. Journal of Virology71:4123–4127
    [Google Scholar]
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