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Complementary Function of γδ T-Lymphocytes and Dendritic Cells in the Response to Isopentenyl-Pyrophosphate and Lipopolysaccharide Antigens

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Abstract

Dendritic cells and γδ T-lymphocytes play a crucial role in the early response to microbial infections. Since both dendritic cells and γδ T-lymphocytes may be activated by specific microbial products, we analyzed their interplay in the presence of such respective ligands: lipopolysaccharide and isopentenyl-pyrophosphate. Activated γδ T-cells increased the maturational state of dendritic cells induced by lipopolysaccharide, increasing the expression of co-stimulatory and MHC class I and II molecules. IL-12 production by dendritic cells was strongly amplified in the presence of activated γδ T-cells and the Th1 polarization of naïve CD4+ T-lymphocytes was significantly increased. On the other hand, dendritic cells enhanced γδ T-cell functions induced by isopentenyl-pyrophosphate and promote their IL-2 independent proliferation through CD86 contact. Altogether, dendritic cells and γδ T-cells exert a complementary function promoting an optimal immune response to non peptidic microbial antigens.

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References

  1. Banchereau J, Steinman RM: Dendritic cells and the control of the immunity. Nature 392:245–252, 1998

    CAS  PubMed  Google Scholar 

  2. Banchereau J, Briere F, Caux C, Davoust J, Lebeque Liu YJ, Pulendram B, Palucka K: Immunobiology of dendritic cells. Annu Rev Immunol 18:767–811, 2000

    Article  CAS  PubMed  Google Scholar 

  3. Steinman RM, Inaba K, Turley S, Pierre P, Mellman I: Antigen capture, processing, and presentation by dendritic cells: RecenT-cell biological studies. Hum Immunol 60(7):562–567, 1999

    Article  CAS  PubMed  Google Scholar 

  4. Qi H, Denning TL, Soong L: Differential induction of interleukin-10 and interleukin-12 in dendritic cells by microbial toll-like receptor activators and skewing of T-cell cytokine profiles. Infect Immun 71(6):3337–3342, 2003

    Article  CAS  PubMed  Google Scholar 

  5. Ramirez-Pineda JR, Frohlich A, Berberich C, Moll H: Dendritic cells (DC) activated by CpG DNA ex vivo are potent inducers of host resistance to an intracellular pathogen that is independent of IL-12 derived from the immunizing DC. J Immunol 172(10):6281–6289, 2004

    CAS  PubMed  Google Scholar 

  6. Aksoy E, Zouain C, Vanhoutte F, Fontaine J, Pavelka N, Thieblemont N, Willems F, Ricciardi-Castagnoli P, Goldman M, Capron M, Ryffel B, Trottein F: Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J Biol Chem 280(1):277–283, 2005

    CAS  PubMed  Google Scholar 

  7. Lanzavecchia A, Sallusto F: Regulation of T-cell immunity by dendritic cells. Cell 106(3):263–266, 2001

    CAS  PubMed  Google Scholar 

  8. Levin D, Constant S, Pasqualini T, Flavell R, Bottomly K: Role of dendritic cells in the priming of CD4+ T-lymphocytes to peptide antigen in vivo. Immunol 151(12):6742–6750, 1993

    CAS  Google Scholar 

  9. Lanzavecchia A, Sallusto F: The instructive role of dendritic cells on T-cell responses: Lineages, plasticity and kinetics. Curr Opin Immunol 13(3):291–298, 2001

    Article  CAS  PubMed  Google Scholar 

  10. Lanzavecchia A: Dendritic cell maturation and generation of immune responses. Haematologica 84(suppl EHA-4):23–25, 1999

    PubMed  Google Scholar 

  11. Shreedhar V, Moodycliffe AM, Ullrich SE, Bucana C, Kripke ML, Flores-Romo L: Dendritic cells require T-cells for functional maturation in vivo. Immunity 11(5):625–636, 1999

    Article  CAS  PubMed  Google Scholar 

  12. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G: Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med 195(3):327–333, 2002

    Article  CAS  PubMed  Google Scholar 

  13. Reis e Sousa C: Activation of dendritic cells translating innate into adaptive immunity. Curr Opin Immunol 16(1):21–25, 2004

    Article  PubMed  Google Scholar 

  14. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, Sallusto F: Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 5(12):1260–1265, 2004

    Article  CAS  PubMed  Google Scholar 

  15. Tanaka Y, Sano S, Nieves E, De Libero G, Rosa D, Modlin RL, Brenner MB, Bloom BR, Morita CT: Nonpeptide ligands for human gamma delta T-cells. Proc Natl Acad Sci USA 91(17):8175–8179, 1994

    CAS  PubMed  Google Scholar 

  16. Wilhelm M, Tony HP: An in vitro model for the expansion of V gamma 9 delta 2 T-lymphocytes during development. Scand J Immunol 40(5):521–528, 1994

    CAS  PubMed  Google Scholar 

  17. Constant P, Davodeau F, Peyrat MA, Poquet Y, Puzo G, Bonneville M, Fournie JJ: Stimulation of human gamma delta T-cells by nonpeptidic mycobacterial ligands. Science 264(5156):267–270, 1994

    CAS  PubMed  Google Scholar 

  18. Tanaka Y, Morita CT, Tanaka Y, Nieves E, Brenner MB, Bloom BR: Natural and synthetic non-peptide antigens recognized by human gamma delta T-cells. Nature 375(6527):155–158, 1995

    Article  CAS  PubMed  Google Scholar 

  19. Morita CT, Beckman EM, Bukowski JF, Tanaka Y, Band H, Bloom BR, Golan DE, Brenner MB: Direct presentation of nonpeptide prenyl pyrophosphate antigens to human gamma delta T-cells. Immunity 3(4):495–507, 1995

    Article  CAS  PubMed  Google Scholar 

  20. Lang F, Peyrat MA, Constant P, Devodeau F, David-Ameline J, Poquet Y, Vie H, Fournie JJ, Bonneville M: Early activation of human V gamma 9V delta 2 T-cell broad cytotoxicity and TNF production by nonpeptidic mycobacterial ligands. J Immunol 154(11):5986–5994, 1995

    CAS  PubMed  Google Scholar 

  21. Poccia F, Gougeon ML, Bonneville M, Lopez-Botet M, Moretta A, Battistini L, Wallace M, Colizzi V, Malkovsky M: Innate T-cell immunity to nonpeptidic antigens. Immunol Today 19(6):253–256, 1998

    Article  CAS  PubMed  Google Scholar 

  22. Ferrarini M, Ferrero E, Dagna L, Poggi A, Zocchi MR: Human gammadelta T-cells: A nonredundant system in the immune-surveillance against cancer. Trends Immunol 23(1):14–18, 2002

    Article  CAS  PubMed  Google Scholar 

  23. Ismaili J, Olislagers V, Poupot R, Fournie JJ, Goldman M: Human gamma delta T-cells induce dendritic cell maturation. Clin Immunol 103:296–302, 2002

    Article  CAS  PubMed  Google Scholar 

  24. Leslie DS, Vincent MS, Spada FM, Das H, Sugita M, Morita CT, Brenner MB: CD1-mediated gamma/delta T-cell maturation of dendritic cells. J Exp Med 196(12):1575–1584, 2002.

    Article  CAS  PubMed  Google Scholar 

  25. Poccia F, Cipriani B, Vendetti S, Colizzi V, Poquet Y, Battistini L, Lopez-Botet M, Fournie JJ, Gougeon ML: CD94/NKG2 inhibitory receptor complex modulates both anti-viral and anti-tumoral responses of polyclonal phosphoantigen-reactive V gamma 9V delta 2 T-lymphocytes. J Immunol 159(12):6009–6017, 1997

    CAS  PubMed  Google Scholar 

  26. Battistini L, Borsellino G, Sawicki G, Poccia F, Salvetti M, Ristori G, Brosnan CF: Phenotypic and cytokine analysis of human peripheral blood gamma delta T-cells expressing NK cell receptors. J Immunol 159(8):3723–3730, 1997

    CAS  PubMed  Google Scholar 

  27. Sporri R, Reis e Sousa C: Newly activated T-cells promote maturation of bystander dendritic cells but not IL-12 production. J Immunol 171(12):6406–6413, 2003

    PubMed  Google Scholar 

  28. Mailliard RB, Egawa S, Cai Q, Kalinska A, Bykowskaya SN, Lotze MT, Kapsenberg ML, Storkus WJ, Kalinski P: Complementary dendritic cell-activating function of CD8+ and CD4+ T-cells: Helper role of CD8+ T-cells in the development of T helper type 1 responses. J Exp Med 195(4):473–483, 2002

    Article  CAS  PubMed  Google Scholar 

  29. Reudl C, Kopf M, Bachmann MF: CD8(+) T-cells mediate CD40-independent maturation of dendritic cells in vivo. J Exp Med 189(12):1875–1884, 1999

    Article  PubMed  Google Scholar 

  30. Gober HJ, Kistowska M, Angman L, Jeno P, Mori L, De Libero G: Human T-cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 197(2):163–168, 2003

    Article  CAS  PubMed  Google Scholar 

  31. Rohmer M, Knani M, Simonin P, Sutter B, Sahm H: Isoprenoid biosynthesis in bacteria: A novel pathway for the early steps leading to isopentenyl diphosphate. Biochem J 295:517–524, 1993

    CAS  PubMed  Google Scholar 

  32. Poggi A, Zocchi MR, Costa P, Ferrero E, Borsellino G, Placido R, Galgani S, Salvetti M, Gasperini C, Ristori G, Brosnan CF, Battistini L: IL-12-mediated NKRP1A up-regulation and consequent enhancement of endothelial transmigration of V delta 2+ TCR gamma delta + T-lymphocytes from healthy donors and multiple sclerosis patients. J Immunol 162(7):4349–4354, 1999

    CAS  PubMed  Google Scholar 

  33. Schulz O, Edwards AD, Schito M, Aliberti J, Manickasingham S, Sher A, Reis e Sousa C: CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity 13(4):453–462, 2000

    Article  CAS  PubMed  Google Scholar 

  34. Miyagawa F, Tanaka Y, Yamashita S, Minato N: Essential requirement of antigen presentation by monocyte lineage cells for the activation of primary human gamma delta T-cells by aminobisphosphonate antigen. J Immunol 166(9):5508–5514, 2001

    CAS  PubMed  Google Scholar 

  35. Kato Y, Tanaka Y, Tanaka H, Yamashita S, Minato N: Requirement of species-specific interactions for the activation of human gamma delta T-cells by pamidronate. J Immunol. 170(7):3608–3613, 2003

    CAS  PubMed  Google Scholar 

  36. Fikri Y, Pastoret PP, Nyabenda J: Costimulatory molecule requirement for bovine WC1+ gammadelta T-cells’ proliferative response to bacterial superantigens. Scand J Immunol 55(4):373–381, 2002

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Unit of Cellular Immunology, National Institute for Infectious Diseases “Lazzaro Spallanzani” – IRCCS, Rome, Italy

    Angelo Martino, Rita Casetti, Alessandra D’Alessandri, Alessandra Sacchi & Fabrizio Poccia

  2. Unit of Cellular Immunology, “Padiglione Del Vecchio” National Institute for Infectious Diseases “L. Spallanzani” – IRCCS, Via Portuense 292, 00149, Rome, Italy

    Angelo Martino & Rita Casetti

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  1. Angelo Martino
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  2. Rita Casetti
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  3. Alessandra D’Alessandri
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  4. Alessandra Sacchi
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  5. Fabrizio Poccia
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Correspondence to Angelo Martino.

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These authors contributed equally to the work.

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Martino, A., Casetti, R., D’Alessandri, A. et al. Complementary Function of γδ T-Lymphocytes and Dendritic Cells in the Response to Isopentenyl-Pyrophosphate and Lipopolysaccharide Antigens. J Clin Immunol 25, 230–237 (2005). https://doi.org/10.1007/s10875-005-4080-8

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  • DOI: https://doi.org/10.1007/s10875-005-4080-8

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