Immunopathogenesis of hepatitis e virus infection

Seminars in Liver Disease

Volumn 33, Issue 1, 2013, Pages 71-78

  Wedemeyer, Heiner ^a   Rybczynska, Jolanta ^b,c   Pischke, Sven ^a   Krawczynski, Kris ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c MEDICAL UNIVERSITY OF WARSAW   (Poland)

Author keywords

animal models; hepatitis E virus; HEV; humoral immunity; T cell responses

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; PROGESTERONE RECEPTOR;

ADAPTIVE IMMUNITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; GENE MUTATION; GENOTYPE; HEPATITIS E; HUMAN; HUMORAL IMMUNITY; IMMUNOPATHOGENESIS; INNATE IMMUNITY; LIVER FAILURE; MATERNAL MORTALITY; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; VACCINATION; VIRAL CLEARANCE; VIRUS TRANSMISSION;

HEPATITIS E; HEPATITIS E VIRUS; HUMANS;

EID: 84875986813     PISSN: 02728087     EISSN: 10988971     Source Type: Journal    
DOI: 10.1055/s-0033-1338118     Document Type: Article

References (81)

1. Kamar N., Bendall R., Legrand-Abravanel F., et al. Hepatitis E. Lancet: 2012; 379 9835 2477 2488
2. Wedemeyer H., Pischke S., Manns M. P. Pathogenesis and treatment of hepatitis e virus infection. Gastroenterology: 2012; 142 6 1388 1397, e1
3. Aggarwal R., Jameel S. Hepatitis E. Hepatology: 2011; 54 6 2218 2226
4. Mahtab M. A., Rahman S., Khan M., Karim M. F. Hepatitis E virus is a leading cause of acute-on-chronic liver disease: experience from a tertiary centre in Bangladesh. Hepatobiliary Pancreat Dis Int: 2009; 8 1 50 52
5. Péron J. M., Bureau C., Poirson H., et al. Fulminant liver failure from acute autochthonous hepatitis E in France: description of seven patients with acute hepatitis E and encephalopathy. J Viral Hepat: 2007; 14 5 298 303
6. Kamar N., Selves J., Mansuy J. M., et al. Hepatitis E virus and chronic hepatitis in organ-transplant recipients. N Engl J Med: 2008; 358 8 811 817
7. Haagsma E. B., Niesters H. G., van den Berg A. P., et al. Prevalence of hepatitis E virus infection in liver transplant recipients. Liver Transpl: 2009; 15 10 1225 1228
8. Pischke S., Suneetha P. V., Baechlein C., et al. Hepatitis E virus infection as a cause of graft hepatitis in liver transplant recipients. Liver Transpl: 2010; 16 1 74 82
9. Kamar N., Garrouste C., Haagsma E. B., et al. Factors associated with chronic hepatitis in patients with hepatitis E virus infection who have received solid organ transplants. Gastroenterology: 2011; 140 5 1481 1489
10. Pischke S., Stiefel P., Franz B., et al. Chronic hepatitis e in heart transplant recipients. Am J Transplant: 2012; 12 11 3128 3133
11. Bhatia V., Singhal A., Panda S. K., Acharya S. K. A 20-year single-center experience with acute liver failure during pregnancy: is the prognosis really worse? Hepatology: 2008; 48 5 1577 1585
12. Bose P. D., Das B. C., Kumar A., Gondal R., Kumar D., Kar P. High viral load and deregulation of the progesterone receptor signaling pathway: association with hepatitis E-related poor pregnancy outcome. J Hepatol: 2011; 54 6 1107 1113
13. Divizia M., Gabrieli R., Degener A. M., et al. Evidence of hepatitis E virus replication on cell cultures. New Microbiol: 1999; 22 2 77 83
14. Zhang H. Y., Chen D. S., Wu Y. Q., He Q. G., Chen H. C., Liu Z. F. Both swine and human cells are capable to support the replication of swine hepatitis E virus type 4 in vitro. Virus Res: 2011; 158 1-2 289 293
15. Thomson A. W., Knolle P. A. Antigen-presenting cell function in the tolerogenic liver environment. Nat Rev Immunol: 2010; 10 11 753 766
16. Protzer U., Maini M. K., Knolle P. A. Living in the liver: hepatic infections. Nat Rev Immunol: 2012; 12 3 201 213
17. Lunemann S., Schlaphoff V., Cornberg M., Wedemeyer H. NK cells in hepatitis C: role in disease susceptibility and therapy. Dig Dis: 2012; 30 01 48 54
18. Stegmann K. A., Björkström N. K., Veber H., et al. Interferon-alpha-induced TRAIL on natural killer cells is associated with control of hepatitis C virus infection. Gastroenterology: 2010; 138 5 1885 1897
19. Stegmann K. A., Björkström N. K., Ciesek S., et al. Interferon α-stimulated natural killer cells from patients with acute hepatitis C virus (HCV) infection recognize HCV-infected and uninfected hepatoma cells via DNAX accessory molecule-1. J Infect Dis: 2012; 205 9 1351 1362
20. Peppa D., Gill U. S., Reynolds G., et al. Up-regulation of a death receptor renders antiviral T cells susceptible to NK cell-mediated deletion. J Exp Med: 2013; 210 1 99 114
21. Waggoner S. N., Cornberg M., Selin L. K., Welsh R. M. Natural killer cells act as rheostats modulating antiviral T cells. Nature: 2012; 481 7381 394 398
22. Guidotti L. G., Rochford R., Chung J., Shapiro M., Purcell R., Chisari F. V. Viral clearance without destruction of infected cells during acute HBV infection. Science: 1999; 284 5415 825 829
23. Guidotti L. G., Borrow P., Brown A., McClary H., Koch R., Chisari F. V. Noncytopathic clearance of lymphocytic choriomeningitis virus from the hepatocyte. J Exp Med: 1999; 189 10 1555 1564
24. Guidotti L. G., Chisari F. V. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol: 2001; 19 65 91
25. Rehermann B. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J Clin Invest: 2009; 119 7 1745 1754
26. Klenerman P., Thimme R. T cell responses in hepatitis C: the good, the bad and the unconventional. Gut: 2012; 61 8 1226 1234
27. Krawczynski K., Meng X. J., Rybczynska J. Pathogenetic elements of hepatitis E and animal models of HEV infection. Virus Res: 2011; 161 1 78 83
28. Tsarev S. A., Tsareva T. S., Emerson S. U., et al. Successful passive and active immunization of cynomolgus monkeys against hepatitis E. Proc Natl Acad Sci U S A: 1994; 91 21 10198 10202
29. Shata M. T., Daef E. A., Zaki M. E., et al. Protective role of humoral immune responses during an outbreak of hepatitis E in Egypt. Trans R Soc Trop Med Hyg: 2012; 106 10 613 618
30. Zhang J., Gu Y., Ge S. X., et al. Analysis of hepatitis E virus neutralization sites using monoclonal antibodies directed against a virus capsid protein. Vaccine: 2005; 23 22 2881 2892
31. Schofield D. J., Glamann J., Emerson S. U., Purcell R. H. Identification by phage display and characterization of two neutralizing chimpanzee monoclonal antibodies to the hepatitis E virus capsid protein. J Virol: 2000; 74 12 5548 5555
32. Engle R. E., Yu C., Emerson S. U., Meng X. J., Purcell R. H. Hepatitis E virus (HEV) capsid antigens derived from viruses of human and swine origin are equally efficient for detecting anti-HEV by enzyme immunoassay. J Clin Microbiol: 2002; 40 12 4576 4580
33. Zhang J., Li S. W., Wu T., Zhao Q., Ng M. H., Xia N. S. Hepatitis E virus: neutralizing sites, diagnosis, and protective immunity. Rev Med Virol: 2012; 22 5 339 349
34. Shrestha M. P., Scott R. M., Joshi D. M., et al. Safety and efficacy of a recombinant hepatitis E vaccine. N Engl J Med: 2007; 356 9 895 903
35. Zhu F. C., Zhang J., Zhang X. F., et al. Efficacy and safety of a recombinant hepatitis E vaccine in healthy adults: a large-scale, randomised, double-blind placebo-controlled, phase 3 trial. Lancet: 2010; 376 9744 895 902
36. Arankalle V. A., Favorov M. O., Chadha M. S., Phule D. M., Banerjee K. Rhesus monkeys infected with hepatitis E virus (HEV) from the former USSR are immune to subsequent challenge with an Indian strain of HEV. Acta Virol: 1993; 37 6 515 518
37. Torresi J., Johnson D., Wedemeyer H. Progress in the development of preventive and therapeutic vaccines for hepatitis C virus. J Hepatol: 2011; 54 6 1273 1285
38. Aggarwal R., Shukla R., Jameel S., et al. T-cell epitope mapping of ORF2 and ORF3 proteins of human hepatitis E virus. J Viral Hepat: 2007; 14 4 283 292
39. Wu T., Zhang J., Su Z. J., et al. Specific cellular immune response in hepatitis E patients. Intervirology: 2008; 51 5 322 327
40. Husain M. M., Aggarwal R., Kumar D., Jameel S., Naik S. Effector T cells immune reactivity among patients with acute hepatitis E. J Viral Hepat: 2011; 18 10 e603 e608
41. Tripathy A. S., Das R., Rathod S. B., Arankalle V. A. Cytokine profiles, CTL response and T cell frequencies in the peripheral blood of acute patients and individuals recovered from hepatitis E infection. PLoS ONE: 2012; 7 2 e31822
42. Srivastava R., Aggarwal R., Sachdeva S., Alam M. I., Jameel S., Naik S. Adaptive immune responses during acute uncomplicated and fulminant hepatitis E. J Gastroenterol Hepatol: 2011; 26 2 306 311
43. Lhomme S., Abravanel F., Dubois M., et al. Hepatitis E virus quasispecies and the outcome of acute hepatitis E in solid-organ transplant patients. J Virol: 2012; 86 18 10006 10014
44. Suneetha P. V., Pischke S., Schlaphoff V., et al. Hepatitis E virus (HEV)-specific T-cell responses are associated with control of HEV infection. Hepatology: 2012; 55 3 695 708
45. Timm J., Li B., Daniels M. G., et al. Human leukocyte antigen-associated sequence polymorphisms in hepatitis C virus reveal reproducible immune responses and constraints on viral evolution. Hepatology: 2007; 46 2 339 349
46. TrehanPati N., Kotillil S., Hissar S. S., et al. Circulating Tregs correlate with viral load reduction in chronic HBV-treated patients with tenofovir disoproxil fumarate. J Clin Immunol: 2011; 31 3 509 520
47. Dunn C., Brunetto M., Reynolds G., et al. Cytokines induced during chronic hepatitis B virus infection promote a pathway for NK cell-mediated liver damage. J Exp Med: 2007; 204 3 667 680
48. Srivastava R., Aggarwal R., Bhagat M. R., Chowdhury A., Naik S. Alterations in natural killer cells and natural killer T cells during acute viral hepatitis E. J Viral Hepat: 2008; 15 12 910 916
49. Tripathy A. S., Das R., Rathod S. B., Gurav Y. K., Arankalle V. A. Peripheral T regulatory cells and cytokines in hepatitis E infection. Eur J Clin Microbiol Infect Dis: 2012; 31 2 179 184
50. Yu C., Boon D., McDonald S. L., et al. Pathogenesis of hepatitis E virus and hepatitis C virus in chimpanzees: similarities and differences. J Virol: 2010; 84 21 11264 11278
51. Dong C., Zafrullah M., Mixson-Hayden T., et al. Suppression of interferon-α signaling by hepatitis E virus. Hepatology: 2012; 55 5 1324 1332
52. Emerson S. U., Purcell R. H. Recombinant vaccines for hepatitis E. Trends Mol Med: 2001; 7 10 462 466
53. Purcell R. H., Emerson S. U. Hepatitis E: an emerging awareness of an old disease. J Hepatol: 2008; 48 3 494 503
54. McCaustland K. A., Krawczynski K., Ebert J. W., et al. Hepatitis E virus infection in chimpanzees: a retrospective analysis. Arch Virol: 2000; 145 9 1909 1918
55. Meng X. J., Purcell R. H., Halbur P. G., et al. A novel virus in swine is closely related to the human hepatitis E virus. Proc Natl Acad Sci U S A: 1997; 94 18 9860 9865
56. Halbur P. G., Kasorndorkbua C., Gilbert C., et al. Comparative pathogenesis of infection of pigs with hepatitis E viruses recovered from a pig and a human. J Clin Microbiol: 2001; 39 3 918 923
57. Feagins A. R., Opriessnig T., Huang Y. W., Halbur P. G., Meng X. J. Cross-species infection of specific-pathogen-free pigs by a genotype 4 strain of human hepatitis E virus. J Med Virol: 2008; 80 8 1379 1386
58. Huang F., Hua X., Yang S., Yuan C., Zhang W. Effective inhibition of hepatitis E virus replication in A549 cells and piglets by RNA interference (RNAi) targeting RNA-dependent RNA polymerase. Antiviral Res: 2009; 83 3 274 281
59. Maneerat Y., Clayson E. T., Myint K. S., Young G. D., Innis B. L. Experimental infection of the laboratory rat with the hepatitis E virus. J Med Virol: 1996; 48 2 121 128
60. Zhao C., Ma Z., Harrison T. J., et al. A novel genotype of hepatitis E virus prevalent among farmed rabbits in China. J Med Virol: 2009; 81 8 1371 1379
61. Aggarwal R., Kamili S., Spelbring J., Krawczynski K. Experimental studies on subclinical hepatitis E virus infection in cynomolgus macaques. J Infect Dis: 2001; 184 11 1380 1385
62. Bradley D. W., Balayan M. S. Virus of enterically transmitted non-A, non-B hepatitis. Lancet: 1988; 1 8589 819
63. Arankalle V., Banerjee K. Viruses of enterically transmitted non-A, non-B hepatitis. Lancet: 1988; 2 8603 160
64. Krawczynski K., Bradley D. W. Enterically transmitted non-A, non-B hepatitis: identification of virus-associated antigen in experimentally infected cynomolgus macaques. J Infect Dis: 1989; 159 6 1042 1049
65. Ticehurst J., Rhodes L. L. Jr, Krawczynski K., et al. Infection of owl monkeys (Aotus trivirgatus) and cynomolgus monkeys (Macaca fascicularis) with hepatitis E virus from Mexico. J Infect Dis: 1992; 165 5 835 845
66. Shata M. T., Barrett A., Shire N. J., et al. Characterization of hepatitis E-specific cell-mediated immune response using IFN-gamma ELISPOT assay. J Immunol Methods: 2007; 328 1-2 152 161
67. Soe S., Uchida T., Suzuki K., et al. Enterically transmitted non-A, non-B hepatitis in cynomolgus monkeys: morphology and probable mechanism of hepatocellular necrosis. Liver: 1989; 9 3 135 145
68. Peron J. M., Danjoux M., Kamar N., et al. Liver histology in patients with sporadic acute hepatitis E: a study of 11 patients from South-West France. Virchows Arch: 2007; 450 4 405 410
69. Malcolm P., Dalton H., Hussaini H. S., Mathew J. The histology of acute autochthonous hepatitis E virus infection. Histopathology: 2007; 51 2 190 194
70. Wendum D., Nachury M., Yver M., et al. Acute hepatitis E: a cause of lymphocytic destructive cholangitis. Hum Pathol: 2005; 36 4 436 438
71. Agrawal V., Goel A., Rawat A., Naik S., Aggarwal R. Histological and immunohistochemical features in fatal acute fulminant hepatitis E. Indian J Pathol Microbiol: 2012; 55 1 22 27
72. Prabhu S. B., Gupta P., Durgapal H., et al. Study of cellular immune response against hepatitis E virus (HEV). J Viral Hepat: 2011; 18 8 587 594
73. Kar P., Jilani N., Husain S. A., et al. Does hepatitis E viral load and genotypes influence the final outcome of acute liver failure during pregnancy? Am J Gastroenterol: 2008; 103 10 2495 2501
74. Jilani N., Das B. C., Husain S. A., et al. Hepatitis E virus infection and fulminant hepatic failure during pregnancy. J Gastroenterol Hepatol: 2007; 22 5 676 682
75. Mishra N., Arankalle V. A. Association of polymorphisms in the promoter regions of TNF- with susceptibility to hepatitis E virus and TNF-α (-1031) and IFN-y (+874) genes with clinical outcome of hepatitis E in India. J Hepatol: 2011; 55 1227 1234
76. Wu T., Zhu F. C., Huang S. J., et al. Safety of the hepatitis E vaccine for pregnant women: a preliminary analysis. Hepatology: 2012; 55 6 2038
77. Kamar N., Weclawiak H., Guilbeau-Frugier C., et al. Hepatitis E virus and the kidney in solid-organ transplant patients. Transplantation: 2012; 93 6 617 623
78. Kamar N., Bendall R. P., Peron J. M., et al. Hepatitis E virus and neurologic disorders. Emerg Infect Dis: 2011; 17 2 173 179
79. Kammer A. R., van der Burg S. H., Grabscheid B., et al. Molecular mimicry of human cytochrome P450 by hepatitis C virus at the level of cytotoxic T cell recognition. J Exp Med: 1999; 190 2 169 176
80. Pischke S., Hardtke S., Bode U., et al. Ribavirin treatment of acute and chronic hepatitis E: a single center experience. Liver International: 2013;; in press
81. Moal V., Textoris J., Ben Amara A., et al. Chronic hepatitis E virus infection is specifically associatd with an interferon-related transcriptional program. J Infect Dis: 2013; 207 1 125 132