Dominance of the CD4+ T helper cell response during acute resolving hepatitis a virus infection

Journal of Experimental Medicine

Volumn 209, Issue 8, 2012, Pages 1481-1492

  Zhou, Yan ^a   Callendret, Benoît ^a   Xu, Dan ^a   Brasky, Kathleen M ^b   Feng, Zongdi ^c,d   Hensley, Lucinda L ^c,d   Guedj, Jeremie ^e,f   Perelson, Alan S ^e   Lemon, Stanley M ^c,d   Lanford, Robert E ^b,g   Walker, Christopher M ^a,h  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b SOUTHWEST NATIONAL PRIMATE RESEARCH CENTER   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

^e LOS ALAMOS NATIONAL LABORATORY   (United States)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g SOUTHWEST FOUNDATION FOR BIOMEDICAL RESEARCH   (United States)

^h THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 7 RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PROGRAMMED DEATH 1 RECEPTOR; TUMOR NECROSIS FACTOR; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHIMPANZEE; CYTOKINE PRODUCTION; FEMALE; HEPATITIS A; HEPATITIS A VIRUS; INFECTION RISK; LIVER CELL DAMAGE; LYMPHOCYTE FUNCTION; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RELAPSE; SYMPTOM; VIREMIA; VIRUS GENOME; VIRUS REPLICATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HEPATITIS A; HEPATITIS A VIRUS; INTERFERON-GAMMA; LIVER; MALE; PAN TROGLODYTES; T-LYMPHOCYTES, HELPER-INDUCER; VIRUS REPLICATION;

EID: 84866449909     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20111906     Document Type: Article

References (55)

1. Aichele, P., H. Unsoeld, M. Koschella, O. Schweier, U. Kalinke, and S. Vucikuja. 2006. CD8 T cells specific for lymphocytic choriomeningitis virus require type I IFN receptor for clonal expansion. J. Immunol. 176:4525-4529.
2. Badovinac, V.P., B.B. Porter, and J.T. Harty. 2002. Programmed contraction of CD8(+) T cells after infection. Nat. Immunol. 3: 619-626. http://dx.doi.org/10.1038/nrm880
3. Bigger, C.B., K.M. Brasky, and R.E. Lanford. 2001. DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J. Virol. 75: 7059-7066. http://dx.doi.org/10.1128/JVI.75.15.7059-7066.2001
4. Bontrop, R.E. 2006. Comparative genetics of MHC polymorphisms in different primate species: duplications and deletions. Hum. Immunol. 67: 388-397. http://dx.doi.org/10.1016/j.humimm.2006.03.007
5. Bowen, D.G., and C.M. Walker. 2005. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature. 436: 946-952. http://dx.doi.org/10.1038/nature04079
6. Brown, K.E., G.J. Freeman, E.J. Wherry, and A.H. Sharpe. 2010. Role of PD-1 in regulating acute infections. Curr. Opin. Immunol. 22: 397-401. http://dx.doi.org/10.1016/j.coi.2010.03.007
7. Chisari, F.V., M. Isogawa, and S.F. Wieland. 2010. Pathogenesis of hepatitis B virus infection. Pathol. Biol. (Paris). 58: 258-266. http://dx.doi.org/10.1016/j.patbio.2009.11.001
8. Cox, M.A., L.E. Harrington, and A.J. Zajac. 2011. Cytokines and the inception of CD8 T cell responses. Trends Immunol. 32: 180-186. http://dx.doi.org/10.1016/j.it.2011.01.004
9. Curtsinger, J.M., and M.F. Mescher. 2010. Inflammatory cytokines as a third signal for T cell activation. Curr. Opin. Immunol. 22: 333-340. http://dx.doi.org/10.1016/j.coi.2010.02.013
10. Curtsinger, J.M., J.O. Valenzuela, P. Agarwal, D. Lins, and M.F. Mescher. 2005. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J. Immunol. 174:4465-4469.
11. Cuthbert, J.A. 2001. Hepatitis A: old and new. Clin. Microbiol. Rev. 14:3858. http://dx.doi.org/10.1128/CMR.14.1.38-58.2001
12. Darrah, P.A., D.T. Patel, P.M. De Luca, R.W. Lindsay, D.F. Davey, B.J. Flynn, S.T. Hoff, P. Andersen, S.G. Reed, S.L. Morris, et al. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13: 843-850. http://dx.doi.org/10.1038/nm1592
13. de Groot, N.G., C.M. Heijmans, N. de Groot, G.G. Doxiadis, N. Otting, and R.E. Bontrop. 2009. The chimpanzee Mhc-DRB region revisited: gene content, polymorphism, pseudogenes, and transcripts. Mol. Immunol. 47: 381-389. http://dx.doi.org/10.1016/j.molimm.2009.09.003
14. Elkington, R., N.H. Shoukry, S. Walker, T. Crough, C. Fazou, A. Kaur, C.M. Walker, and R. Khanna. 2004. Cross-reactive recognition of human and primate cytomegalovirus sequences by human CD4 cytotoxic T lymphocytes specific for glycoprotein B and H. Eur. J. Immunol. 34: 3216-3226. http://dx.doi.org/10.1002/eji.200425203
15. Erickson, A.L., Y. Kimura, S. Igarashi, J. Eichelberger, M. Houghton, J. Sidney, D. McKinney, A. Sette, A.L. Hughes, and C.M. Walker. 2001. The outcome of hepatitis C virus infection is predicted by escape mutations in epitopes targeted by cytotoxic T lymphocytes. Immunity. 15: 883-895. http://dx.doi.org/10.1016/S1074-7613(01)00245-X
16. Foy, E., K. Li, C. Wang, R. Sumpter Jr., M. Ikeda, S.M. Lemon, and M. Gale Jr. 2003. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science. 300: 1145-1148. http://dx.doi.org/10.1126/science.1082604
17. Glikson, M., E. Galun, R. Oren, R. Tur-Kaspa, and D. Shouval. 1992. Relapsing hepatitis A. Review of 14 cases and literature survey. Medicine (Baltimore). 71:14-23.
18. Guidotti, L.G., and F.V. Chisari. 2001. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu. Rev. Immunol. 19: 65-91. http://dx.doi.org/10.1146/annurev.immunol.19.1.65
19. Ha, S.J., E.E. West, K. Araki, K.A. Smith, and R. Ahmed. 2008. Manipulating both the inhibitory and stimulatory immune system towards the success of therapeutic vaccination against chronic viral infections. Immunol. Rev. 223: 317-333. http://dx.doi.org/10.1111/j.1600-065X.2008.00638.x
20. Homann, D., L. Teyton, and M.B. Oldstone. 2001. Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat. Med. 7: 913-919. http://dx.doi.org/10.1038/90950
21. Jacobsen, K.H., and S.T. Wiersma. 2010. Hepatitis A virus seroprevalence by age and world region, 1990 and 2005. Vaccine. 28: 6653-6657. http://dx.doi.org/10.1016/j.vaccine.2010.08.037
22. Kaech, S.M., J.T. Tan, E.J. Wherry, B.T. Konieczny, C.D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4: 1191-1198. http://dx.doi.org/10.1038/ni1009
23. Klenerman, P., and R. Thimme. 2011. T cell responses in hepatitis C: the good, the bad and the unconventional. Gut. In press.
24. Kolumam, G.A., S. Thomas, L.J. Thompson, J. Sprent, and K. MuraliKrishna. 2005. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 202: 637-650. http://dx.doi.org/10.1084/jem.20050821
25. Lanford, R.E., Z. Feng, D. Chavez, B. Guerra, K.M. Brasky, Y. Zhou, D. Yamane, A.S. Perelson, C.M. Walker, and S.M. Lemon. 2011. Acute hepatitis A virus infection is associated with a limited type I interferon response and persistence of intrahepatic viral RNA. Proc. Natl. Acad. Sci. USA. 108: 11223-11228. http://dx.doi.org/10.1073/pnas.1101939108
26. Lechner, F., D.K. Wong, P.R. Dunbar, R. Chapman, R.T. Chung, P. Dohrenwend, G. Robbins, R. Phillips, P. Klenerman, and B.D. Walker. 2000. Analysis of successful immune responses in persons infected with hepatitis C virus. J. Exp. Med. 191: 1499-1512. http://dx.doi.org/10.1084/jem.191.9.1499
27. Lemon, S.M., and L.N. Binn. 1983. Serum neutralizing antibody response to hepatitis A virus. J. Infect. Dis. 148: 1033-1039. http://dx.doi.org/10.1093/infdis/148.6.1033
28. Lemon, S.M., P.C. Murphy, P.J. Provost, I. Chalikonda, J.P. Davide, T.L. Schofield, D.R. Nalin, and J.A. Lewis. 1997. Immunoprecipitation and virus neutralization assays demonstrate qualitative differences between protective antibody responses to inactivated hepatitis A vaccine and passive immunization with immune globulin. J. Infect. Dis. 176: 9-19. http://dx.doi.org/10.1086/514044
29. Li, K., E. Foy, J.C. Ferreon, M. Nakamura, A.C. Ferreon, M. Ikeda, S.C. Ray, M. Gale Jr., and S.M. Lemon. 2005. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. USA. 102: 2992-2997. http://dx.doi.org/10.1073/pnas.0408824102
30. Maier, K., P. Gabriel, E. Koscielniak, Y.D. Stierhof, K.H. Wiedmann, B. Flehmig, and A. Vallbracht. 1988. Human gamma interferon production by cytotoxic T lymphocytes sensitized during hepatitis A virus infection. J. Virol. 62:3756-3763.
31. Manangeeswaran, M., J. Jacques, C. Tami, K. Konduru, N. Amharref, O. Perrella, J.M. Casasnovas, D.T. Umetsu, R.H. Dekruyff, G.J. Freeman, et al. 2012. Binding of hepatitis a virus to its cellular receptor 1 inhibits T-regulatory cell functions in humans. Gastroenterology. 142:1516-1525: e3. http://dx.doi.org/10.1053/j.gastro.2012.02.039
32. Martin, A., and S.M. Lemon. 2006. Hepatitis A virus: from discovery to vaccines. Hepatology. 43:S164-S172. http://dx.doi.org/10.1002/hep.21052
33. Obar, J.J., and L. Lefranáois. 2010. Memory CD8+ T cell differentiation. Ann. N. Y. Acad. Sci. 1183: 251-266. http://dx.doi.org/10.1111/j.17496632.2009.05126.x
34. Pepper, M., J.L. Linehan, A.J. Pagán, T. Zell, T. Dileepan, P.P. Cleary, and M.K. Jenkins. 2010. Different routes of bacterial infection induce longlived TH1 memory cells and short-lived TH17 cells. Nat. Immunol. 11: 83-89. http://dx.doi.org/10.1038/ni.1826
35. Ramos, H.J., A.M. Davis, A.G. Cole, J.D. Schatzle, J. Forman, and J.D. Farrar. 2009. Reciprocal responsiveness to interleukin-12 and interferon-alpha specifies human CD8+ effector versus central memory T-cell fates. Blood. 113: 5516-5525. http://dx.doi.org/10.1182/blood2008-11-188458
36. Rehermann, B. 2009. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J. Clin. Invest. 119: 1745-1754. http://dx.doi.org/10.1172/JCI39133
37. Roederer, M., J.L. Nozzi, and M.C. Nason. 2011. SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A. 79:167-174.
38. Schulte, I., T. Hitziger, S. Giugliano, J. Timm, H. Gold, F.M. Heinemann, Y. Khudyakov, M. Strasser, C. König, E. Castermans, et al. 2011. Characterization of CD8+ T-cell response in acute and resolved hepatitis A virus infection. J. Hepatol. 54: 201-208. http://dx.doi.org/10.1016/j.jhep.2010.07.010
39. + T cell responses are primed during acute hepatitis C infection, but rapidly disappear from human blood with viral persistence. J. Exp. Med. 209: 61-75. http://dx.doi.org/10.1084/jem.20100388
40. Seder, R.A., P.A. Darrah, and M. Roederer. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8: 247-258. http://dx.doi.org/10.1038/nri2274
41. Semmo, N., and P. Klenerman. 2007. CD4+ T cell responses in hepatitis C virus infection. World J. Gastroenterol. 13:4831-4838.
42. + T cells are required for protection from persistent hepatitis C virus infection. J. Exp. Med. 197: 1645-1655. http://dx.doi.org/10.1084/jem.20030239
43. Shoukry, N.H., J. Sidney, A. Sette, and C.M. Walker. 2004. Conserved hierarchy of helper T cell responses in a chimpanzee during primary and secondary hepatitis C virus infections. J. Immunol. 172:483-492.
44. Thimme, R., D. Oldach, K.M. Chang, C. Steiger, S.C. Ray, and F.V. Chisari. 2001. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J. Exp. Med. 194: 1395-1406. http://dx.doi.org/10.1084/jem.194.10.1395
45. Thimme, R., S. Wieland, C. Steiger, J. Ghrayeb, K.A. Reimann, R.H. Purcell, and F.V. Chisari. 2003. CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J. Virol. 77: 68-76. http://dx.doi.org/10.1128/JVI.77.1.68-76.2003
46. Thompson, L.J., G.A. Kolumam, S. Thomas, and K. Murali-Krishna. 2006. Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J. Immunol. 177:1746-1754.
47. Vallbracht, A., K. Maier, Y.D. Stierhof, K.H. Wiedmann, B. Flehmig, and B. Fleischer. 1989. Liver-derived cytotoxic T cells in hepatitis A virus infection. J. Infect. Dis. 160: 209-217. http://dx.doi.org/10.1093/infdis/160.2.209
48. Van Damme, P., J. Banatvala, O. Fay, S. Iwarson, B. McMahon, K. Van Herck, D. Shouval, P. Bonanni, B. Connor, G. Cooksley, et al; International Consensus Group on Hepatitis A Virus Immunity. 2003. Hepatitis A booster vaccination: is there a need? Lancet. 362:1065-1071. http://dx.doi.org/10.1016/S0140-6736(03)14418-2
49. Walker, C.M. 2010. Adaptive immunity to the hepatitis C virus. Adv. Virus Res. 78: 43-86. http://dx.doi.org/10.1016/B978-0-12-385032-4.00002-1
50. Wherry, E.J. 2011. T cell exhaustion. Nat. Immunol. 12: 492-499. http://dx.doi.org/10.1038/ni.2035
51. Wieland, S., R. Thimme, R.H. Purcell, and F.V. Chisari. 2004. Genomic analysis of the host response to hepatitis B virus infection. Proc. Natl. Acad. Sci. USA. 101: 6669-6674. http://dx.doi.org/10.1073/pnas.0401771101
52. Wu, C.Y., J.R. Kirman, M.J. Rotte, D.F. Davey, S.P. Perfetto, E.G. Rhee, B.L. Freidag, B.J. Hill, D.C. Douek, and R.A. Seder. 2002. Distinct lineages of T(H)1 cells have differential capacities for memory cell generation in vivo. Nat. Immunol. 3: 852-858. http://dx.doi.org/10.1038/ni832
53. Xiao, Z., K.A. Casey, S.C. Jameson, J.M. Curtsinger, and M.F. Mescher. 2009. Programming for CD8 T cell memory development requires IL-12 or type I IFN. J. Immunol. 182: 2786-2794. http://dx.doi.org/10.4049/jimmunol.0803484
54. +) T cells in malaria infection. J. Exp. Med. 195: 881-892. http://dx.doi.org/10.1084/jem.20011174
55. Yang, Y., Y. Liang, L. Qu, Z. Chen, M. Yi, K. Li, and S.M. Lemon. 2007. Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc. Natl. Acad. Sci. USA. 104:72537258. http://dx.doi.org/10.1073/pnas.0611506104