Immune exhaustion and immune senescence: Two distinct pathways for HBV vaccine failure during HCV and/or HIV infection

Archivum Immunologiae et Therapiae Experimentalis

Volumn 61, Issue 3, 2013, Pages 193-201

  Yao, Zhi Q ^a,b   Moorman, Jonathan P ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b East Tennessee State University   (United States)

Author keywords

HBV vaccine response; HCV; HIV; Immune exhaustion; Immune senescence

Indexed keywords

AGATOLIMOD; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HBVAXPRO40; HEPATITIS A HEPATITIS B VACCINE; HEPATITIS B VACCINE; HEPATOCYTE NUCLEAR FACTOR 3; LEVAMISOLE; NEF PROTEIN; PROGRAMMED DEATH 1 RECEPTOR; RECOMBINANT HEPATITIS B VACCINE; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN PRESENTING CELL; CARCINOGENESIS; CD4 LYMPHOCYTE COUNT; CELL FUNCTION; DRUG EFFICACY; DRUG SAFETY; ENZYME ACTIVATION; EXHAUSTION; GENETIC POLYMORPHISM; HEPATITIS B; HEPATITIS C; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNE STATUS; IMMUNOREGULATION; MIXED INFECTION; MOLECULAR DYNAMICS; MORBIDITY; MORTALITY; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; REVIEW; RISK FACTOR; SENESCENCE; SEROCONVERSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VACCINATION; VACCINE FAILURE; VIRUS TRANSMISSION;

COINFECTION; HEPATITIS B ANTIBODIES; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VACCINES; HEPATITIS B, CHRONIC; HEPATITIS C, CHRONIC; HIV INFECTIONS; HUMANS; IMMUNOCOMPROMISED HOST; RISK FACTORS; SUPERINFECTION; TREATMENT FAILURE;

EID: 84878020722     PISSN: 0004069X     EISSN: 16614917     Source Type: Journal    
DOI: 10.1007/s00005-013-0219-0     Document Type: Review

References (92)

1. Albarran B, Goncalves B, Salmen B et al (2005) Profiles of NK, NKT cell activation and cytokine production following vaccination against hepatitis B. APMIS 113:526-535
2. Alexander WS (2002) Suppressors of cytokine signaling (SOCS) in the immune system. Nat Rev Immunol 2:410-416
3. Allain JP, Canotti D (2012) Hepatitis B virus in transfusion medicine: still a problem? Biologicals 40:180-186
4. Appay V, Almeida JR, Sauce D et al (2007) Accelerated immune senescence and HIV-1 infection. Exp Gerontol 42:432-437
5. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506
6. Barber DL, Wherry EJ, Asopust DM et al (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439:682-687
7. Bauer T, Jilg W (2006) Hepatitis B surface antigen-specific T and B cell memory in individuals who had lost protective antibodies after hepatitis B vaccination. Vaccine 24:572-577
8. Bauer T, Gunther M, Bienzie I et al (2007) Vaccination against hepatitis B in liver transplant receipients: pilot analysis of cellular immune response shows evidence of HBsAg-specific regulatory T cells. Liver Transpl 13:434-442
9. Biggar R, Goedert J, Hoofnagle J (1987) Accelerated loss of antibody to hepatitis B surface antigen among immunodeficient homosexual men infected with HIV. N Engl J Med 316:630-631
10. Bodsworth N, Donovan B, Nightingale B (1989) The effect of concurrent human immunodeficiency virus infection on chronic hepatitis B. a study of 150 homosexual men. J Infect Dis 160:577-582
11. Bodsworth NJ, Cooper DA, Donovan B (1991) The influence of human immunodeficiency virus type 1 infection on the development of the hepatitis B virus carrier state. J Infect Dis 163:1138-1140
12. Boni C, Fisicaro P, Valdatta C et al (2007) Charaterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J Virol 81:4215-4225
13. Brown EJ, Baltimore D (2003) Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev 17:615-628
14. Bruguera M, Cremades M, Salinas R et al (1992) Impaired response to recombinant hepatitis B vaccine in HIV-infected persons. J Clin Gastroenterol 14:27-30
15. Chen L (2004) Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol 4:336-347
16. Cheruvu S, Marks K, Talal AH (2007) Understanding and management of hepatitis B/HIV and hepatitis B/hepatitis C virus coinfection. Clin Liver Dis 11:917-943
17. Chong MM, Metcalf D, Jamieson E et al (2005) Suppressor of cytokine signaling-1 in T cells and macrophages is critical for preventing lethal inflammation. Blood 106:1668-1675
18. Collier A, Corey L, Murphy V et al (1988) Antibody to human immunodeficiency virus (HIV) and suboptimal response to hepatitis B vaccination. Ann Intern Med 109:101-105
19. D'Souza M, Fontenot AP, Mack DG et al (2007) Programmed death 1 expression on HIV-specific CD4+ T cells is driven by viral replication and associated with T cell dysfunction. J Immunol 179:1979-1987
20. De Silvestri A, Pasi A, Martinetti M et al (2001) Family study of non-responsiveness to hepatitis B vaccine confirms the importance of HLA class III C4A locus. Genes Immun 2:367-372
21. Desombere I, Hauser P, Rossau R et al (1995) Non responders to hepatitis B vaccine can present evelope particles to T lymphocytes. J Immunol 154(15):520-529
22. Desombere I, Cao P, Gijbels Y et al (2005) Non-responsiveness to hepatitis B surface antigen vaccines is not caused by defective antigen presentation or a lack of B7 co-stimulation. Clin Exp Immunol 140:126-137
23. Dong H, Strome SE, Salomao DR et al (2002) Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 8:793-800
24. Duberg AS, Torner A, Daviosdottir L et al (2008) Cause of death in individuals with chronic HBV and/or HCV infection, a nationwide community-based register study. J Viral Hepat 15:538-550
25. Effros RB, Fletcher CV, Gebo K et al (2008) Aging and infectious diseases: workshop on HIV infection and aging: what is known and future research directions. Clin Infect Dis 47:542-553
26. Egan PJ, Lawlor KE, Alexander WS et al (2003) Suppressor of cytokine signaling-1 regulates acute inflammatory arthritis and T cell activation. J Clin Invest 111:915-924
27. Eskild A, Magnus P, Petersen G et al (1992) Hepatitis B antibodies in HIV-infected homosexual men are associated with more rapid progression to AIDS. AIDS 6:571-574
28. Ferrando-Martínez S, Ruiz-Mateos E, Romero-Sánchez MC et al (2011) HIV infection-related premature immunosenescence: high rates of immune exhaustion after short time infection. Curr HIV Res 9:289-294
29. Filippini P, Coppola N, Pisapia R et al (2007) Virological and clinical aspects of HBV-HCV coinfection in HIV positive patients. J Med Virol 79:1679-1685
30. Fisman DN, Agrawal D, Leder K (2002) The effect of age on immunologic response to recombinant hepatitis B vaccine: a meta-analysis. Clin Infect Dis 35:1368-1375
31. Frazier AD, Zhang CL, Ni L et al (2010) Program death-1 pathway affects suppressor of cytokine signaling-1 expression in T cells during hepatitis C infection. Viral Immunol 23:487-495
32. Gilson RJ, Hawkins AE, Beecham MR et al (1997) Interactions between HIV and hepatitis B virus in homosexual men: effects on the natural history of infection. AIDS 11:597-606
33. Godkin A, Davenport M, Hill AV (2005) Molecular analysis of HLA class II associations with hepatitis B virus clearance and vaccine nonresponsiveness. Hepatology 41:1383-1390
34. Golden-Mason L, Palmer B, Klarquist J et al (2007) Upregulation of PD-1 expression on circulating and intrahepatic hepatitis C virus-specific CD8+ T cells associated with reversible immune dysfunction. J Virol 81:9249-9258
35. Goncalves L, Albarran B, Salmen S et al (2004) The nonresponse to hepatitis B vaccination is associated with impaired lymphocyte activation. Virology 326:20-28
36. Hafler DA, Kuchroo V (2008) TIMs: central regulators of immune responses. J Exp Med 205:2699-2701
37. Hohler T, Stradmann-Bellinghausen B, Starke R et al (2002) C4A deficiency and nonresponse to hepatitis B vaccination. J Hepatol 37:387-392
38. Horvath J, Raffanti S (1994) Clinical aspects of the interactions between human immunodeficiency virus and the hepatotropic viruses. Clin Infect Dis 18:339-410
39. Iwai Y, Terawaya S, Ikegawa M et al (2003) PD-1 inhibits antiviral immunity at the effector phase in the liver. J Exp Med 198:39-50
40. Jacques P, Moens G, Desombere I et al (2002) The immunogenicity and reacogenicity profile of a candidate hepatitis B vaccine in an adult vaccine non-responder population. Vaccine 20:3644-3649
41. Jin HT, Anderson AC, Tan WG et al (2010) Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc Natl Acad Sci USA 107:14733-14738
42. Jones RB, Ndhlovu LC, Barbour JD et al (2008) Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J Exp Med 205:2763-2779
43. Kao JH, Chen DS (2002) Global control of hepatitis B virus infection. Lancet Infect Dis 2:395-403
44. Keeffe EB (2005) Acute hepatitis A and B in patients with chronic liver disease: prevention through vaccination. Am J Med 118((Suppl 10A)):21S-27S
45. Kellerman SE, Hanson DL, McNaghten AD et al (2003) Prevalence of chronic hepatitis B and incidence of acute hepatitis B infection in human immunodeficiency virus-infected subjects. J Infect Dis 188:571-577
46. Khoury SJ, Sayegh MH (2004) The role of the new negative T cell costimulatory pathways in regulating autoimmunity. Immunity 20:529-538
47. Kim MJ, Nafziger AN, Harro CD et al (2003) Revaccination of healthy nonreasponders with hepatitis B vaccine and prediction of seroprotection response. Vaccine 21:1174-1179
48. Klein SL (2012) Sex influences immune responses to viruses, and efficacy of prophylaxis and treatments for viral diseases. Bio Essays 34:1050-1059
49. Klein SL, Jedlicka A, Pekosz A (2010) The Xs and Y of immune responses to viral vaccines. Lancet Infect Dis 10:338-349
50. Kramer ES, Hofmann C, Smith PG et al (2009) Response to hepatitis A and B vaccine alone or in combination in patients with chronic hepatitis C virus and advanced fibrosis. Dig Dis Sci 54:2016-2025
51. Kuchroo VK, Umetsu DT, DeKruyff RH et al (2003) The TIM gene family: emerging roles in immunity and disease. Nat Rev Immunol 3:454-462
52. Lango-Warensjo A, Cardell K, Lindblom B (1998) Haplotypes comprising subtypes of the DQB1*06 allele direct the antibody response with hepatitis B surface antigen. Tissue Antigens 52:374-380
53. Lazizi Y, Grangeot-Keros L, Delfraissy J et al (1988) Reappearance of hepatitis B virus in immune patients infected with the human immunodeficiency virus type 1. J Infect Dis 158:666-667
54. Le Saux S, Weyand CM, Goronzy JJ (2012) Mechanisms of immune senescence: lessons from models of accelerated immune aging. Ann NY Acad Sci 1247:69-82
55. Ma CJ, Ni L, Zhang Y et al (2011) PD-1 negatively regulates IL-12 expression by limiting STAT-1 phosphorylation in monocytes/macrophages during chronic hepatitis C infection. Immunology 132:421-431
56. Macedo LC, Isolani AP, Visentainer JE et al (2010) Association of cytokine genetic polymorphrisms with the humoral immune response to recombinant vaccine against HBV in infants. J Med Virol 82:929-933
57. Malaspina A, Moir S, Orsega SM et al (2005) Compromised B cell responses to influenza vaccination in HIV-infected individuals. J Infect Dis 191:1442-1450
58. + HCV-specific human CTLs is associated with viral persistence, and its blockade restores hepatocyte-directed in vitro cytotoxicity. J Clin Invest 120:4546-4557
59. Moorman JP, Dong ZP, Ni L et al (2009) Abnormal B lymphocyte activation associated with TALL-1 overexpression and SOCS-1 deregulation in chronic HCV infection. Immunology 128:227-235
60. Moorman JP, Zhang CL, Ni L et al (2011) Impaired hepatitis B vaccine responses during chronic hepatitis C infection: involvement of the PD-1 pathway in regulating CD4+ T cell responses. Vaccine 29:3169-3176
61. Moorman JP, Wang JM, Zhang Y et al (2012) Tim-3 controls regulatory and effector T cell balance during HCV Infection. J Immunol 189:755-766
62. Morita Y, Naka T, Kawazoe Y et al (2000) Signals transducers and activators of transcription (STAT)-indueced STAT inhibitor (SS-1)/suppressor of cytokine signaling-1 (SOCS-1) suppreses tumor necrosis factor α-induced cell death in fibroblasts. Proc Natl Acad Sci USA 97:5405-5410
63. Ni L, Ma CJ, Zhang Y et al (2010) PD-1 modulates Regulatory T cells and suppresses T cell responses in HCV-associated Lymphoma. Immunol Cell Biol 89:535-539
64. Nishimura H, Honjo T (2001) PD-1: an inhibitory immunoreceptor involved in peripheral tolerance. Trends Immunol 22:265-268
65. Nystrom J, Cardell K, Bjornsdottir TB et al (2008) Improved cell mediated immune responses after successful re-vaccination of non-responders to the hepatitis B virus surface antigen (HBsAg) vaccine using the combined hepatitis A and B vaccine. Vaccine 26:5967-5972
66. Okazaki T, Honjo T (2007) PD-1 and PD-1 ligands: from discovery to clinical application. Int Immunol 19:813-824
67. Rahman F, Dahmen A, Herzog-Hauff S et al (2000) Cellular and humoral immune responses induced by intradermal or intramuscular vaccination with a major hepatitis B surface antigen. Hepatology 31:521-527
68. Ramon JM, Bou R, Oromi J (1996) Low-dose intramuscular revaccination against hepatitis B. Vaccine 14:1647-1650
69. Rodriguez-Barradas MC, Alexandraki I, Nazir T et al (2003) Response of human immunodeficiency virus-infected patients receiving highly active antiretroviral therapy to vaccination with 23-valent pneumococcal polysaccharide vaccine. Clin Infect Dis 37:438-447
70. Rossi C, Shrier I, Marshall L et al (2012) Seroprevalence of chronic hepatitis B virus infection and prior immunity in immigrants and refugees: a systematic review and meta-analysis. PLoS One 7:e44611
71. Ryckman KK, Fielding K, Hill AV et al (2010) Host genetic factors and vaccine-induced immunity to HBV infection: haplotype analysis. PLoS One 5:e12273
72. Salazar M, Deulofeut H, Granja C et al (1995) Normal HBsAg presentation and T cell defect in the immune response of nonresponders. Immunogenetics 41:366-374
73. Sancar A, Lindsey-Boltz LA, Unsal-Kaçmaz K et al (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73:39-85
74. Shafran SD, Mashinter LD, Lindemulder A et al (2007) Poor efficacy of intradermal administration of recombinant hepatitis B virus immunization in HIV-infected individuals who fail to respond to intramuscular administration of hepatitis B virus vaccine. HIV Med 8:295-299
75. Sharpe AH, Freeman GJ (2002) The B7-CD28 superfamily. Nat Rev Immunol 2:116-126
76. Stramer SL, Wend U, Candotti D et al (2011) Nucleic acid testing to detect HBV infection in blood donors. N Engl J Med 364:236-247
77. Thio CL, Seaberg EC, Skolasky RJ et al (2002) HIV-1, hepatitis B virus, and risk for liver-related mortality in the Multicenter Cohort Study (MACS). Lancet 360:1921-1926
78. Torbenson M, Kannangai R, Astemborski J et al (2004) High prevalence of occult hepatitis B in Baltimore injection drug users. Hepatology 39:51-57
79. Tsai IJ, Chang MH, Chen HL et al (2000) Immunogenicity and reactogenicity of the combined hepatitis A and B vaccine in young adults. Vaccine 19:437-441
80. Vali B, Jones RB, Sakhdari A et al (2010) HCV-specific T cells in HCV/HIV co-infection show elevated frequencies of dual Tim-3/PD-1 expression that correlate with liver disease progression. Eur J Immunol 40:2493-2505
81. Verkade MA, van Druningen CJ, de Op Hoek CT et al (2007) Decreased antigen-specific T cell proliferation by moDC among hepatitis B vaccine non-responders on haemodialysis. Clin Exp Med 7:65-71
82. Voehringer D, Blaser C, Brawand P et al (2001) Viral infections induce abundant numbers of senescent CD8 T cells. J Immunol 167:4838-4843
83. Weber R, Sabin CA, Friis-Moller N et al (2006) Liver-related deaths in persons infected with the human immunodeficiency virus: the D:A:D Study. Arch Intern Med 166:1632-1641
84. Yao ZQ, Eisen-Vandervelde A, Ray S et al (2003) HCV core/gC1qR interaction arrests T cell cycle progression through stabilization of the cell cycle inhibitor p27kip1. Virology 314:271-282
85. Yao ZQ, King E, Prayther D et al (2007) T cell dysfunction by hepatitis C virus core protein involves PD-1/PDL-1 signaling. Viral Immunol 20:276-287
86. Yao ZQ, Prayther D, Trabu C et al (2008) Differential regulation of SOCS-1 signaling in T and B lymphocytes by HCV core protein. Immunology 125:197-207
87. Yao ZQ, Ni L, Zhang Y et al (2010) Differential regulation of T and B lymphocytes by PD-1 and SOCS-1 signaling in hepatitis C virus-associated non-Hodgkin's lymphoma. Immunol Invest 40:243-264
88. Zarski JP, Bohn B, Bastie A et al (1998) Characteristics of patients with dual infection by hepatitis B and C viruses. J Hepatol 28:27-33
89. Zhang Y, Ma CJ, Ni L et al (2011a) Crosstalk between PD-1 and SOCS-1 in HCV core-mediated IL-12 suppression. J Immunol 186:3093-3103
90. Zhang Y, Ma CJ, Wu XY et al (2011b) Tim-3 negatively regulates IL-12 production by monocytes in HCV infection. PLoS One 6:e19664
91. Zhang Y, Cheng J, Ma CJ et al (2012) Tim-3 regulates pro- and anti-inflammatory cytokine expression in human CD14+ monocytes. J Leukoc Biol 91:189-196
92. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548