Temporal dynamics of the primary human T cell response to yellow fever virus 17D as it matures from an effector- to a memory-type response

Journal of Immunology

Volumn 190, Issue 5, 2013, Pages 2150-2158

  Blom, Kim ^a   Braun, Monika ^a   Ivarsson, Martin A ^a   Gonzalez, Veronica D ^a   Falconer, Karolin ^a   Moll, Markus ^a   Ljunggren, Hans Gustaf ^a   Michaëlsson, Jakob ^a   Sandberg, Johan K ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; CD45RA ANTIGEN; CHEMOKINE RECEPTOR CCR7; EPITOPE; HLA A2 ANTIGEN; HLA B7 ANTIGEN; PROGRAMMED DEATH 1 RECEPTOR; YELLOW FEVER VACCINE;

ADULT; ARTICLE; CD45RA+CCR72PD-12CD27LOW MEMORY CELL; CD8+ T LYMPHOCYTE; CELL COMPOSITION; CELL KINETICS; CELL MATURATION; CELL SPECIFICITY; CELLULAR IMMUNITY; CONTROLLED STUDY; DYNAMICS; EFFECTOR CELL; HUMAN; HUMAN CELL; LYMPHOCYTE FUNCTION; MEMORY T LYMPHOCYTE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA VIRUS INFECTION; SINGLE DRUG DOSE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; VIRUS CELL INTERACTION; YELLOW FEVER FLAVIVIRUS; YELLOW FEVER FLAVIVIRUS INFECTION; YELLOW FEVER VIRUS 17D;

ADOLESCENT; ADULT; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; HISTOCOMPATIBILITY TESTING; HLA ANTIGENS; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; MIDDLE AGED; TIME FACTORS; VACCINES, ATTENUATED; YELLOW FEVER; YELLOW FEVER VACCINE; YELLOW FEVER VIRUS;

EID: 84874244299     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202234     Document Type: Article

References (44)

1. Douek, D. C., M. Roederer, and R. A. Koup. 2009. Emerging concepts in the immunopathogenesis of AIDS. Annu. Rev. Med. 60: 471-484.
2. Rehermann, B. 2009. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J. Clin. Invest. 119: 1745-1754.
3. Gonzalez, V. D., A. L. Landay, and J. K. Sandberg. 2010. Innate immunity and chronic immune activation in HCV/HIV-1 co-infection. Clin. Immunol. 135: 12-25.
4. Murphy, B. R., and S. S. Whitehead. 2011. Immune response to dengue virus and prospects for a vaccine. Annu. Rev. Immunol. 29: 587-619.
5. Staples, J. E., M. Gershman, and M. Fischer; Centers for Disease Control and Prevention (CDC). 2010. Yellow fever vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm. Rep. 59 (RR-7): 1-27.
6. Lloyd, W., M. Theiler, and N. I. Ricci. 1936. Modifications of the virulence of yellow fever virus by cultivation in tissues in vitro. Trans. R. Soc. Trop. Med. Hyg. 29: 481-529.
7. Pulendran, B. 2009. Learning immunology from the yellow fever vaccine: innate immunity to systems vaccinology. Nat. Rev. Immunol. 9: 741-747.
8. Ahmed, R., and R. S. Akondy. 2011. Insights into human CD8(+) T-cell memory using the yellow fever and smallpox vaccines. Immunol. Cell Biol. 89: 340-345.
9. Miller, J. D., R. G. van der Most, R. S. Akondy, J. T. Glidewell, S. Albott, D. Masopust, K. Murali-Krishna, P. L. Mahar, S. Edupuganti, S. Lalor, et al. 2008. Human effector and memory CD8+ T cell responses to smallpox and yellow fever vaccines. Immunity 28: 710-722.
10. Butz, E. A., and M. J. Bevan. 1998. Massive expansion of antigen-specific CD8+ T cells during an acute virus infection. Immunity 8: 167-175.
11. Murali-Krishna, K., J. D. Altman, M. Suresh, D. J. Sourdive, A. J. Zajac, J. D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8: 177-187.
12. Yewdell, J. W. 2006. Confronting complexity: real-world immunodominance in antiviral CD8+ T cell responses. Immunity 25: 533-543.
13. Akram, A., and R. D. Inman. 2012. Immunodominance: a pivotal principle in host response to viral infections. Clin. Immunol. 143: 99-115.
14. Appay, V., P. R. Dunbar, M. Callan, P. Klenerman, G. M. Gillespie, L. Papagno, G. S. Ogg, A. King, F. Lechner, C. A. Spina, et al. 2002. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8: 379-385.
15. Callan, M. F., L. Tan, N. Annels, G. S. Ogg, J. D. Wilson, C. A. O'Callaghan, N. Steven, A. J. McMichael, and A. B. Rickinson. 1998. Direct visualization of antigen-specific CD8+ T cells during the primary immune response to Epstein- Barr virus In vivo. J. Exp. Med. 187: 1395-1402.
16. Roos, M. T., R. A. van Lier, D. Hamann, G. J. Knol, I. Verhoofstad, D. van Baarle, F. Miedema, and P. T. Schellekens. 2000. Changes in the composition of circulating CD8+ T cell subsets during acute epstein-barr and human immunodeficiency virus infections in humans. J. Infect. Dis. 182: 451-458.
17. Lauer, G. M., K. Ouchi, R. T. Chung, T. N. Nguyen, C. L. Day, D. R. Purkis, M. Reiser, A. Y. Kim, M. Lucas, P. Klenerman, and B. D. Walker. 2002. Comprehensive analysis of CD8(+)-T-cell responses against hepatitis C virus reveals multiple unpredicted specificities. J. Virol. 76: 6104-6113.
18. Sandberg, J. K., N. M. Fast, and D. F. Nixon. 2001. Functional heterogeneity of cytokines and cytolytic effector molecules in human CD8+ T lymphocytes. J. Immunol. 167: 181-187.
19. Urbani, S., C. Boni, G. Missale, G. Elia, C. Cavallo, M. Massari, G. Raimondo, and C. Ferrari. 2002. Virus-specific CD8+ lymphocytes share the same effectormemory phenotype but exhibit functional differences in acute hepatitis B and C. J. Virol. 76: 12423-12434.
20. Appay, V., and S. L. Rowland-Jones. 2004. Lessons from the study of T-cell differentiation in persistent human virus infection. Semin. Immunol. 16: 205-212.
21. Sallusto, F., D. Lenig, R. Förster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
22. Champagne, P., G. S. Ogg, A. S. King, C. Knabenhans, K. Ellefsen, M. Nobile, V. Appay, G. P. Rizzardi, S. Fleury, M. Lipp, et al. 2001. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410: 106-111.
23. Akondy, R. S., N. D. Monson, J. D. Miller, S. Edupuganti, D. Teuwen, H. Wu, F. Quyyumi, S. Garg, J. D. Altman, C. Del Rio, et al. 2009. The yellow fever virus vaccine induces a broad and polyfunctional human memory CD8+ T cell response. J. Immunol. 183: 7919-7930.
24. Larsen, M. V., C. Lundegaard, K. Lamberth, S. Buus, O. Lund, and M. Nielsen. 2007. Large-scale validation of methods for cytotoxic T-lymphocyte epitope prediction. BMC Bioinformatics 8: 424.
25. Larsen, M. V., C. Lundegaard, K. Lamberth, S. Buus, S. Brunak, O. Lund, and M. Nielsen. 2005. An integrative approach to CTL epitope prediction: a combined algorithm integrating MHC class I binding, TAP transport efficiency, and proteasomal cleavage predictions. Eur. J. Immunol. 35: 2295-2303.
26. Gonzalez, V. D., N. K. Björkström, K. J. Malmberg, M. Moll, C. Kuylenstierna, J. Michaëlsson, H. G. Ljunggren, and J. K. Sandberg. 2008. Application of ninecolor flow cytometry for detailed studies of the phenotypic complexity and functional heterogeneity of human lymphocyte subsets. J. Immunol. Methods 330: 64-74.
27. Lindgren, T., C. Ahlm, N. Mohamed, M. Evander, H. G. Ljunggren, and N. K. Björkström. 2011. Longitudinal analysis of the human T cell response during acute hantavirus infection. J. Virol. 85: 10252-10260.
28. Martins, M. A., M. L. Silva, A. P. Marciano, V. Peruhype-Magalhães, S. M. Eloi- Santos, G. Ribeiro, R. Correa-Oliveira, A. Homma, E. G. Kroon, A. Teixeira- Carvalho, and O. A. Martins-Filho. 2007. Activation/modulation of adaptive immunity emerges simultaneously after 17DD yellow fever first-time vaccination: is this the key to prevent severe adverse reactions following immunization? Clin. Exp. Immunol. 148: 90-100.
29. Gaucher, D., R. Therrien, N. Kettaf, B. R. Angermann, G. Boucher, A. Filali- Mouhim, J. M. Moser, R. S. Mehta, D. R. Drake, III, E. Castro, et al. 2008. Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. J. Exp. Med. 205: 3119-3131.
30. Han, Q., N. Bagheri, E. M. Bradshaw, D. A. Hafler, D. A. Lauffenburger, and J. C. Love. 2012. Polyfunctional responses by human T cells result from sequential release of cytokines. Proc. Natl. Acad. Sci. USA 109: 1607-1612.
31. Ma, C., R. Fan, H. Ahmad, Q. Shi, B. Comin-Anduix, T. Chodon, R. C. Koya, C. C. Liu, G. A. Kwong, C. G. Radu, et al. 2011. A clinical microchip for evaluation of single immune cells reveals high functional heterogeneity in phenotypically similar T cells. Nat. Med. 17: 738-743.
32. Newell, E. W., N. Sigal, S. C. Bendall, G. P. Nolan, and M. M. Davis. 2012. Cytometry by time-of-flight shows combinatorial cytokine expression and virusspecific cell niches within a continuum of CD8+ T cell phenotypes. Immunity 36: 142-152.
33. Zimmerli, S. C., A. Harari, C. Cellerai, F. Vallelian, P. A. Bart, and G. Pantaleo. 2005. HIV-1-specific IFN-gamma/IL-2-secreting CD8 T cells support CD4- independent proliferation of HIV-1-specific CD8 T cells. Proc. Natl. Acad. Sci. USA 102: 7239-7244.
34. Betts, M. R., M. C. Nason, S. M. West, S. C. De Rosa, S. A. Migueles, J. Abraham, M. M. Lederman, J. M. Benito, P. A. Goepfert, M. Connors, et al. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107: 4781-4789.
35. Ferrari, G., B. Korber, N. Goonetilleke, M. K. Liu, E. L. Turnbull, J. F. Salazar- Gonzalez, N. Hawkins, S. Self, S. Watson, M. R. Betts, et al. 2011. Relationship between functional profile of HIV-1 specific CD8 T cells and epitope variability with the selection of escape mutants in acute HIV-1 infection. PLoS Pathog. 7: e1001273.
36. Kim, T. K., L. S. St John, E. D. Wieder, J. Khalili, Q. Ma, and K. V. Komanduri. 2009. Human late memory CD8+ T cells have a distinct cytokine signature characterized by CC chemokine production without IL-2 production. J. Immunol. 183: 6167-6174.
37. Eller, M. A., L. A. Eller, S. Ratto-Kim, B. J. Ouma, V. Lo, M. de Souza, D. Guwatudde, B. Nails, N. L. Michael, F. Wabwire-Mangen, et al. 2012. Singlecell level response of HIV-specific and cytomegalovirus-specific CD4 T cells correlate with viral control in chronic HIV-1 subtype A infection. J. Acquir. Immune Defic. Syndr. 61: 9-18.
38. Hess, C., M. Altfeld, S. Y. Thomas, M. M. Addo, E. S. Rosenberg, T. M. Allen, R. Draenert, R. L. Eldrige, J. van Lunzen, H. J. Stellbrink, et al. 2004. HIV-1 specific CD8+ T cells with an effector phenotype and control of viral replication. Lancet 363: 863-866.
39. Northfield, J. W., C. P. Loo, J. D. Barbour, G. Spotts, F. M. Hecht, P. Klenerman, D. F. Nixon, and J. Michaëlsson. 2007. Human immunodeficiency virus type 1 (HIV-1)-specific CD8+ T(EMRA) cells in early infection are linked to control of HIV-1 viremia and predict the subsequent viral load set point. J. Virol. 81: 5759-5765.
40. Kohler, S., N. Bethke, M. Böthe, S. Sommerick, M. Frentsch, C. Romagnani, M. Niedrig, and A. Thiel. 2012. The early cellular signatures of protective immunity induced by live viral vaccination. Eur. J. Immunol. 42: 2363-2373.
41. Barba-Spaeth, G., R. S. Longman, M. L. Albert, and C. M. Rice. 2005. Live attenuated yellow fever 17D infects human DCs and allows for presentation of endogenous and recombinant T cell epitopes. J. Exp. Med. 202: 1179-1184.
42. Querec, T., S. Bennouna, S. Alkan, Y. Laouar, K. Gorden, R. Flavell, S. Akira, R. Ahmed, and B. Pulendran. 2006. Yellow fever vaccine YF-17D activates multiple dendritic cell subsets via TLR2, 7, 8, and 9 to stimulate polyvalent immunity. J. Exp. Med. 203: 413-424.
43. Mason, R. A., N. M. Tauraso, R. O. Spertzel, and R. K. Ginn. 1973. Yellow fever vaccine: direct challenge of monkeys given graded doses of 17D vaccine. Appl. Microbiol. 25: 539-544.
44. Pace, L., A. Tempez, C. Arnold-Schrauf, F. Lemaitre, P. Bousso, L. Fetler, T. Sparwasser, and S. Amigorena. 2012. Regulatory T cells increase the avidity of primary CD8+ T cell responses and promote memory. Science 338: 532-536.