TLR4 ligands augment antigen-specific CD8+ T lymphocyte responses elicited by a viral vaccine vector

Journal of Virology

Volumn 84, Issue 19, 2010, Pages 10413-10419

  Rhee, Elizabeth G ^a,b   Kelley, R Phelps ^a   Agarwal, Isha ^a   Lynch, Diana M ^a   La Porte, Annalena ^a   Simmons, Nathaniel L ^a   Clark, Sarah L ^a   Barouch, Dan H ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYMETHYLCELLULOSE POLYCYTIDYLIC POLYINOSINIC ACID POLYLYSINE; GAG PROTEIN; GAMMA INTERFERON; INTERLEUKIN 2; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHORYL LIPID A; SIMIAN IMMUNODEFICIENCY VIRUS VACCINE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; VIRUS VECTOR; IMMUNOLOGICAL ADJUVANT; LIGAND; POLYINOSINIC POLYCYTIDYLIC ACID; RECOMBINANT VACCINE; TLR4 PROTEIN, MOUSE; VIRUS VACCINE;

ADENOVIRUS; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; ADENOVIRIDAE; ANIMAL; C57BL MOUSE; GENE VECTOR; GENETICS; IMMUNOLOGY; METABOLISM; STRUCTURAL GENE;

ADENOVIRIDAE; MUS; SIMIAN IMMUNODEFICIENCY VIRUS;

ADENOVIRIDAE; ADJUVANTS, IMMUNOLOGIC; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; GENES, GAG; GENETIC VECTORS; LIGANDS; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; POLY I-C; SIMIAN IMMUNODEFICIENCY VIRUS; TOLL-LIKE RECEPTOR 4; VACCINES, SYNTHETIC; VIRAL VACCINES;

EID: 77956828437     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00928-10     Document Type: Article

References (42)

1. Abbink, P., A. A. Lemckert, B. A. Ewald, D. M. Lynch, M. Denholtz, S. Smits, L. Holterman, I. Damen, R. Vogels, A. R. Thorner, K. L. O'Brien, A. Carville, K. G. Mansfield, J. Goudsmit, M. J. Havenga, and D. H. Barouch. 2007. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J. Virol. 81:4654-4663.
2. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
3. Altman, J. D., P. A. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274:94-96.
4. Appledorn, D. M., Y. A. Aldhamen, W. Depas, S. S. Seregin, C. J. Liu, N. Schuldt, D. Quach, D. Quiroga, S. Godbehere, I. Zlatkin, S. Kim, J. J. McCormick, and A. Amalfitano. 2010. A new adenovirus based vaccine vector expressing an Eimeria tenella derived TLR agonist improves cellular immune responses to an antigenic target. PLoS One 5:e9579.
5. Bargieri, D. Y., D. S. Rosa, C. J. Braga, B. O. Carvalho, F. T. Costa, N. M. Espindola, A. J. Vaz, I. S. Soares, L. C. Ferreira, and M. M. Rodrigues. 2008. New malaria vaccine candidates based on the Plasmodium vivax merozoite surface protein-1 and the TLR-5 agonist Salmonella Typhimurium FliC flagellin. Vaccine 26:6132-6142.
6. Barouch, D. H., M. G. Pau, J. H. Custers, W. Koudstaal, S. Kostense, M. J. Havenga, D. M. Truitt, S. M. Sumida, M. G. Kishko, J. C. Arthur, B. Korioth-Schmitz, M. H. Newberg, D. A. Gorgone, M. A. Lifton, D. L. Panicali, G. J. Nabel, N. L. Letvin, and J. Goudsmit. 2004. Immunogenicity of recombinant adenovirus serotype 35 vaccine in the presence of pre-existing anti-Ad5 immunity. J. Immunol. 172:6290-6297.
7. Belyakov, I. M., D. Isakov, Q. Zhu, A. Dzutsev, D. Klinman, and J. A. Berzofsky. 2006. Enhancement of CD8+ T cell immunity in the lung by CpG oligodeoxynucleotides increases protective efficacy of a modified vaccinia Ankara vaccine against lethal poxvirus infection even in a CD4-deficient host. J. Immunol. 177:6336-6343.
8. Braga, C. J., L. M. Massis, M. E. Sbrogio-Almeida, B. C. Alencar, D. Y. Bargieri, S. B. Boscardin, M. M. Rodrigues, and L. C. Ferreira. 2010. CD8+ T cell adjuvant effects of Salmonella FliCd flagellin in live vaccine vectors or as purified protein. Vaccine 28:1373-1382.
9. Buwitt-Beckmann, U., H. Heine, K. H. Wiesmuller, G. Jung, R. Brock, S. Akira, and A. J. Ulmer. 2005. Toll-like receptor 6-independent signaling by diacylated lipopeptides. Eur. J. Immunol. 35:282-289.
10. Draper, S. J., and J. L. Heeney. 2010. Viruses as vaccine vectors for infectious diseases and cancer. Nat. Rev. Microbiol. 8:62-73.
11. Geurtsen, J., F. Fransen, R. J. Vandebriel, E. R. Gremmer, L. J. de la Fonteyne-Blankestijn, B. Kuipers, J. Tommassen, and P. van der Ley. 2008. Supplementation of whole-cell pertussis vaccines with lipopolysaccharide analogs: modification of vaccine-induced immune responses. Vaccine 26:899-906.
12. Kanneganti, T. D., N. Ozoren, M. Body-Malapel, A. Amer, J. H. Park, L. Franchi, J. Whitfield, W. Barchet, M. Colonna, P. Vandenabeele, J. Bertin, A. Coyle, E. P. Grant, S. Akira, and G. Nunez. 2006. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 440:233-236.
13. Karan, D., A. M. Krieg, and D. M. Lubaroff. 2007. Paradoxical enhancement of CD8 T cell-dependent anti-tumor protection despite reduced CD8 T cell responses with addition of a TLR9 agonist to a tumor vaccine. Int. J. Cancer. 121:1520-1528.
14. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, O. Yamaguchi, K. Otsu, T. Tsujimura, C. S. Koh, C. Reis e Sousa, Y. Matsuura, T. Fujita, and S. Akira. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105.
15. + T-lymphocytes. J. Virol. 84:5986-5996.
16. Kumar, H., S. Koyama, K. J. Ishii, T. Kawai, and S. Akira. 2008. Cutting edge: cooperation of IPS-1- and TRIF-dependent pathways in poly IC-enhanced antibody production and cytotoxic T cell responses. J. Immunol. 180:683-687.
17. Manicassamy, S., and B. Pulendran. 2009. Modulation of adaptive immunity with Toll-like receptors. Semin. Immunol. 21:185-193.
18. Mata-Haro, V., C. Cekic, M. Martin, P. M. Chilton, C. R. Casella, and T. C. Mitchell. 2007. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 316:1628-1632.
19. Morefield, G. L., L. D. Hawkins, S. T. Ishizaka, T. L. Kissner, and R. G. Ulrich. 2007. Synthetic Toll-like receptor 4 agonist enhances vaccine efficacy in an experimental model of toxic shock syndrome. Clin. Vaccine Immunol. 14:1499-1504.
20. Nakao, Y., K. Funami, S. Kikkawa, M. Taniguchi, M. Nishiguchi, Y. Fukumori, T. Seya, and M. Matsumoto. 2005. Surface-expressed TLR6 participates in the recognition of diacylated lipopeptide and peptidoglycan in human cells. J. Immunol. 174:1566-1573.
21. Nanda, A., D. M. Lynch, J. Goudsmit, A. A. Lemckert, B. A. Ewald, S. M. Sumida, D. M. Truitt, P. Abbink, M. G. Kishko, D. A. Gorgone, M. A. Lifton, L. Shen, A. Carville, K. G. Mansfield, M. J. Havenga, and D. H. Barouch. 2005. Immunogenicity of recombinant fiber-chimeric adenovirus serotype 35 vector-based vaccines in mice and rhesus monkeys. J. Virol. 79:14161-14168.
22. Ngoi, S. M., M. G. Tovey, and A. T. Vella. 2008. Targeting poly(I:C) to the TLR3-independent pathway boosts effector CD8 T cell differentiation through IFN-alpha/beta. J. Immunol. 181:7670-7680.
23. Okemoto, K., K. Kawasaki, K. Hanada, M. Miura, and M. Nishijima. 2006. A potent adjuvant monophosphoryl lipid A triggers various immune responses, but not secretion of IL-1beta or activation of caspase-1. J. Immunol. 176:1203-1208.
24. Ophorst, O. J., K. Radosevic, J. M. Klap, J. Sijtsma, G. Gillissen, R. Mintardjo, M. J. van Ooij, L. Holterman, A. Companjen, J. Goudsmit, and M. J. Havenga. 2007. Increased immunogenicity of recombinant Ad35-based malaria vaccine through formulation with aluminum phosphate adjuvant. Vaccine 25:6501-6510.
25. Ozinsky, A., D. M. Underhill, J. D. Fontenot, A. M. Hajjar, K. D. Smith, C. B. Wilson, L. Schroeder, and A. Aderem. 2000. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc. Natl. Acad. Sci. U. S. A. 97:13766-13771.
26. Perkins, S. D., A. J. Williams, L. M. O'Brien, T. R. Laws, and R. J. Phillpotts. 2008. CpG used as an adjuvant for an adenovirus-based Venezuelan equine encephalitis virus vaccine increases the immune response to the vector, but not to the transgene product. Viral Immunol. 21:451-457.
27. Persing, D. H., R. N. Coler, M. J. Lacy, D. A. Johnson, J. R. Baldridge, R. M. Hershberg, and S. G. Reed. 2002. Taking toll: lipid A mimetics as adjuvants and immunomodulators. Trends Microbiol. 10:S32-S37.
28. Pétrilli, V., C. Dostert, D. A. Muruve, and J. Tschopp. 2007. The inflammasome: a danger sensing complex triggering innate immunity. Curr. Opin. Immunol. 19:615-622.
29. Pulendran, B. 2009. Learning immunology from the yellow fever vaccine: innate immunity to systems vaccinology. Nat. Rev. Immunol. 9:741-747.
30. 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.
31. Quintilio, W., F. S. Kubrusly, D. Iourtov, C. Miyaki, M. A. Sakauchi, F. Lucio, C. Dias Sde, C. S. Takata, E. N. Miyaji, H. G. Higashi, L. C. Leite, and I. Raw. 2009. Bordetella pertussis monophosphoryl lipid A as adjuvant for inactivated split virion influenza vaccine in mice. Vaccine 27:4219-4224.
32. Roberts, D. M., A. Nanda, M. J. Havenga, P. Abbink, D. M. Lynch, B. A. Ewald, J. Liu, A. R. Thorner, P. E. Swanson, D. A. Gorgone, M. A. Lifton, A. A. Lemckert, L. Holterman, B. Chen, A. Dilraj, A. Carville, K. G. Mansfield, J. Goudsmit, and D. H. Barouch. 2006. Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nature 441:239-243.
33. Salem, M. L., S. A. El-Naggar, A. Kadima, W. E. Gillanders, and D. J. Cole. 2006. The adjuvant effects of the toll-like receptor 3 ligand polyinosinic-cytidylic acid poly(I:C) on antigen-specific CD8+ T cell responses are partially dependent on NK cells with the induction of a beneficial cytokine milieu. Vaccine 24:5119-5132.
34. Schulz, O., S. S. Diebold, M. Chen, T. I. Naslund, M. A. Nolte, L. Alexopoulou, Y. T. Azuma, R. A. Flavell, P. Liljestrom, and C. Reis e Sousa. 2005. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 433:887-892.
35. Schwarz, K., T. Storni, V. Manolova, A. Didierlaurent, J. C. Sirard, P. Rothlisberger, and M. F. Bachmann. 2003. Role of Toll-like receptors in costimulating cytotoxic T cell responses. Eur. J. Immunol. 33:1465-1470.
36. Sel, S., M. Wegmann, S. Sel, S. Bauer, H. Garn, G. Alber, and H. Renz. 2007. Immunomodulatory effects of viral TLR ligands on experimental asthma depend on the additive effects of IL-12 and IL-10. J. Immunol. 178:7805-7813.
37. Stahl-Hennig, C., M. Eisenblatter, E. Jasny, T. Rzehak, K. Tenner-Racz, C. Trumpfheller, A. M. Salazar, K. Uberla, K. Nieto, J. Kleinschmidt, R. Schulte, L. Gissmann, M. Muller, A. Sacher, P. Racz, R. M. Steinman, M. Uguccioni, and R. Ignatius. 2009. Synthetic double-stranded RNAs are adjuvants for the induction of T helper 1 and humoral immune responses to human papillomavirus in rhesus macaques. PLoS Pathog. 5:e1000373.
38. Takeuchi, O., and S. Akira. 2009. Innate immunity to virus infection. Immunol. Rev. 227:75-86.
39. Wang, Y., M. Cella, S. Gilfillan, and M. Colonna. 2010. Cutting edge: polyinosinic:polycytidylic acid boosts the generation of memory CD8 T cells through melanoma differentiation-associated protein 5 expressed in stromal cells. J. Immunol. 184:2751-2755.
40. Wille-Reece, U., B. J. Flynn, K. Lore, R. A. Koup, R. M. Kedl, J. J. Mattapallil, W. R. Weiss, M. Roederer, and R. A. Seder. 2005. HIV Gag protein conjugated to a Toll-like receptor 7/8 agonist improves the magnitude and quality of Th1 and CD8+ T cell responses in nonhuman primates. Proc. Natl. Acad. Sci. U. S. A. 102:15190-15194.
41. Wille-Reece, U., C. Y. Wu, B. J. Flynn, R. M. Kedl, and R. A. Seder. 2005. Immunization with HIV-1 Gag protein conjugated to a TLR7/8 agonist results in the generation of HIV-1 Gag-specific Th1 and CD8+ T cell responses. J. Immunol. 174:7676-7683.
42. Zhu, Q., C. Egelston, S. Gagnon, Y. Sui, I. M. Belyakov, D. M. Klinman, and J. A. Berzofsky. 2010. Using 3 TLR ligands as a combination adjuvant induces qualitative changes in T cell responses needed for antiviral protection in mice. J. Clin. Invest. 120:607-616.