Initial viral load determines the magnitude of the human CD8 T cell response to yellow fever vaccination

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 10, 2015, Pages 3050-3055

  Akondy, Rama S ^a   Johnson, Philip L F ^b,d   Nakaya, Helder I ^a,c   Edupuganti, Srilatha ^a   Mulligan, Mark J ^a   Lawson, Benton ^b   Miller, Joseph D ^a   Pulendran, Bali ^a   Antia, Rustom ^b   Ahmed, Rafi ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d University of Maryland   (United States)

Author keywords

Effector T cells; Human CD8 T cells; Immune memory; Vaccines; Viral load

Indexed keywords

YELLOW FEVER VACCINE;

ADULT; ARTICLE; BLOOD SAMPLING; CD8+ T LYMPHOCYTE; COHORT ANALYSIS; GENE EXPRESSION; GENOME; HUMAN; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; SINGLE DRUG DOSE; TREATMENT RESPONSE; VACCINATION; VIRUS LOAD; YELLOW FEVER; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; YELLOW FEVER VIRUS;

CD8-POSITIVE T-LYMPHOCYTES; COHORT STUDIES; GENE EXPRESSION PROFILING; HUMANS; VIRAL LOAD; YELLOW FEVER VACCINE; YELLOW FEVER VIRUS;

EID: 84924301515     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1500475112     Document Type: Article

References (50)

1. Harrer T, et al. (1996) Strong cytotoxic T cell and weak neutralizing antibody responses in a subset of persons with stable nonprogressing HIV type 1 infection. AIDS Res Hum Retroviruses 12(7):585-592.
2. Pereyra F, et al. (2008) Genetic and immunologic heterogeneity among persons who control HIV infection in the absence of therapy. J Infect Dis 197(4):563-571.
3. Kiepiela P, et al. (2007) CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 13(1):46-53.
4. Schmidt NW, et al. (2008) Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria. Proc Natl Acad Sci USA 105(37):14017-14022.
5. Chen CY, et al. (2009) A critical role for CD8 T cells in a nonhuman primate model of tuberculosis. PLoS Pathog 5(4):e1000392.
6. Swadling L, Klenerman P, Barnes E (2013) Ever closer to a prophylactic vaccine for HCV. Expert Opin Biol Ther 13(8):1109-1124.
7. Stanley DA, et al. (2014) Chimpanzee adenovirus vaccine generates acute and durable protective immunity against ebolavirus challenge. Nat Med 20(10):1126-1129.
8. Sullivan NJ, et al. (2011) CD8+ cellular immunity mediates rAd5 vaccine protection against Ebola virus infection of nonhuman primates. Nat Med 17(9):1128-1131.
9. Drake CG, Lipson EJ, Brahmer JR (2014) Breathing new life into immunotherapy: review of melanoma, lung and kidney cancer. Nat Rev Clin Oncol 11(1):24-37.
10. Kamphorst AO, Ahmed R (2013) Manipulating the PD-1 pathway to improve immunity. Curr Opin Immunol 25(3):381-388.
11. Murali-Krishna K, et al. (1998) Counting antigen-specific CD8 T cells: A reevaluation of bystander activation during viral infection. Immunity 8(2):177-187.
12. Cui W, Kaech SM (2010) Generation of effector CD8+ T cells and their conversion to memory T cells. Immunol Rev 236:151-166.
13. Asquith B, Bangham CR (2007) Quantifying HTLV-I dynamics. Immunol Cell Biol 85(4):280-286.
14. Betts MR, et al. (2001) Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: Relationship to viral load in untreated HIV infection. J Virol 75(24):11983-11991.
15. Ciuffreda D, et al. (2008) Polyfunctional HCV-specific T-cell responses are associated with effective control of HCV replication. Eur J Immunol 38(10):2665-2677.
16. Davenport MP, Ribeiro RM, Zhang L, Wilson DP, Perelson AS (2007) Understanding the mechanisms and limitations of immune control of HIV. Immunol Rev 216:164-175.
17. Day CL, et al. (2007) Proliferative capacity of epitope-specific CD8 T-cell responses is inversely related to viral load in chronic human immunodeficiency virus type 1 infection. J Virol 81(1):434-438.
18. Elemans M, Seich Al Basatena NK, Asquith B (2012) The efficiency of the human CD8+ T cell response: How should we quantify it, what determines it, and does it matter? PLOS Comput Biol 8(2):e1002381.
19. Novitsky V, et al. (2003) Association between virus-specific T-cell responses and plasma viral load in human immunodeficiency virus type 1 subtype C infection. J Virol 77(2):882-890.
20. Nowak MA, Bangham CR (1996) Population dynamics of immune responses to persistent viruses. Science 272(5258):74-79.
21. Sester M, et al. (2002) Dominance of virus-specific CD8 T cells in human primary cytomegalovirus infection. J Am Soc Nephrol 13(10):2577-2584.
22. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB (1994) Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 68(9):6103-6110.
23. Koup RA, et al. (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 68(7):4650-4655.
24. Matis LA, Glimcher LH, Paul WE, Schwartz RH (1983) Magnitude of response of histocompatibility-restricted T-cell clones is a function of the product of the concentrations of antigen and Ia molecules. Proc Natl Acad Sci USA 80(19):6019-6023.
25. Pantaleo G, et al. (1994) Major expansion of CD8+ T cells with a predominant V beta usage during the primary immune response to HIV. Nature 370(6489):463-467.
26. Davenport MP, Ribeiro RM, Perelson AS (2004) Kinetics of virus-specific CD8 + T cells and the control of human immunodeficiency virus infection. J Virol 78(18):10096-10103.
27. Davenport MP, et al. (2005) High-potency human immunodeficiency virus vaccination leads to delayed and reduced CD8 + T-cell expansion but improved virus control. J Virol 79(15):10059-10062.
28. Poland JD, Calisher CH, Monath TP, Downs WG, Murphy K (1981) Persistence of neutralizing antibody 30-35 years after immunization with 17D yellow fever vaccine. Bull World Health Organ 59(6):895-900.
29. Monath TPG, Staples JE, Barrett ADT (2012) Yellow fever vaccine. Vaccines, eds Plotkin S, Orenstein W, Offit P (Elsevier Saunders, Philadelphia), 6th Ed, pp 870-968.
30. Barnett ED (2007) Yellow fever: Epidemiology and prevention. Clin Infect Dis 44(6):850-856.
31. Pulendran B, Oh JZ, Nakaya HI, Ravindran R, Kazmin DA (2013) Immunity to viruses: Learning from successful human vaccines. Immunol Rev 255(1):243-255.
32. Barba-Spaeth G, Longman RS, Albert ML, Rice CM (2005) Live attenuated yellow fever 17D infects human DCs and allows for presentation of endogenous and recombinant T cell epitopes. J Exp Med 202(9):1179-1184.
33. Gaucher D, et al. (2008) Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. J Exp Med 205(13):3119-3131.
34. James EA, et al. (2013) Yellow fever vaccination elicits broad functional CD4+ T cell responses that recognize structural and nonstructural proteins. J Virol 87(23):12794-12804.
35. Querec TD, et al. (2009) Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol 10(1):116-125.
36. Vratskikh O, et al. (2013) Dissection of antibody specificities induced by yellow fever vaccination. PLoS Pathog 9(6):e1003458.
37. Akondy RS, et al. (2009) The yellow fever virus vaccine induces a broad and poly-functional human memory CD8+ T cell response. J Immunol 183(12):7919-7930.
38. Miller JD, et al. (2008) Human effector and memory CD8+ T cell responses to smallpox and yellow fever vaccines. Immunity 28(5):710-722.
39. Edupuganti S, et al.; YF-Ig Study Team (2013) A randomized, double-blind, controlled trial of the 17D yellow fever virus vaccine given in combination with immune globulin or placebo: Comparative viremia and immunogenicity. Am J Trop Med Hyg 88(1):172-177.
40. Subramanian A, et al. (2005) Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102(43):15545-15550.
41. Pulendran B, et al. (2008) Case of yellow fever vaccine - Associated viscerotropic disease with prolonged viremia, robust adaptive immune responses, and polymorphisms in CCR5 and RANTES genes. J Infect Dis 198(4):500-507.
42. Hansen SG, et al. (2011) Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473(7348):523-527.
43. Hansen SG, et al. (2013) Immune clearance of highly pathogenic SIV infection. Nature 502(7469):100-104.
44. Masopust D, et al. (2010) Dynamic T cell migration program provides resident memory within intestinal epithelium. J Exp Med 207(3):553-564.
45. Kaech SM, Ahmed R (2001) Memory CD8+ T cell differentiation: Initial antigen encounter triggers a developmental program in naïve cells. Nat Immunol 2(5):415-422.
46. van Stipdonk MJ, Lemmens EE, Schoenberger SP (2001) Naïve CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat Immunol 2(5):423-429.
47. Mercado R, et al. (2000) Early programming of T cell populations responding to bacterial infection. J Immunol 165(12):6833-6839.
48. Antia R, Bergstrom CT, Pilyugin SS, Kaech SM, Ahmed R (2003) Models of CD8+ responses: 1. What is the antigen-independent proliferation program. J Theor Biol 221(4):585-598.
49. Buchbinder SP, et al.; Step Study Protocol Team (2008) Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): A double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 372(9653):1881-1893.
50. Rerks-Ngarm S, et al.; MOPH-TAVEG Investigators (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361(23):2209-2220.