Il-23r and TCR signaling drives the generation of neonatal vγ 9v2δ t cells expressing high levels of cytotoxic mediators and producing ifn-γ and il-17

Journal of Leukocyte Biology

Volumn 89, Issue 5, 2011, Pages 743-752

  Moens, Emmanuelle ^a   Brouwer, Margreet ^a   Dimova, Tanya ^a   Goldman, Michel ^a   Willems, Fabienne ^a   Vermijlen, David ^b  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

; Human; Il 23; Newborn

Indexed keywords

GAMMA INTERFERON; GRANULYSIN; GRANZYME; INTERLEUKIN 17; INTERLEUKIN 23; PERFORIN; T LYMPHOCYTE RECEPTOR; ZOLEDRONIC ACID;

ARTICLE; CELL POPULATION; LEUKOCYTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ADULT; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CELL PROLIFERATION; CELLS, CULTURED; DENDRITIC CELLS; DIPHOSPHONATES; FLOW CYTOMETRY; GENES, T-CELL RECEPTOR; GRANZYMES; HUMANS; IMIDAZOLES; INFANT, NEWBORN; INTERFERON-GAMMA; INTERLEUKIN-17; PERFORIN; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, INTERLEUKIN; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS;

EID: 79955794248     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0910501     Document Type: Article

References (71)

1. Marchant, A., Goldman, M. (2005) T cell-mediated immune responses in human newborns: ready to learn? Clin. Exp. Immunol. 141, 10-18.
2. Lewis, D. B., Wilson, C. B. (2001) Developmental immunology and role of host defenses in fetal and neonatal susceptibility to infection. In Infectious Diseases of the Fetus and Newborn Infant. Philadelphia, PA, USA, W. B. Saunders Co., 25-138.
3. White, G. P., Watt, P. M., Holt, B. J., Holt, P. G. (2002) Differential patterns of methylation of the IFN-γ promoter at CpG and non-CpG sites underlie differences in FN-γ gene expression between human neonatal nd adult CD45RO- T cells. J. Immunol. 168, 2820-2827.
4. Levy, O. (2007) Innate immunity of the newborn: basic mechanisms and linical correlates. Nat. Rev. Immunol. 7, 379-390.
5. Zaghouani, H., Hoeman, C. M., Adkins, B. (2009) Neonatal immunity: aulty T-helpers nd the shortcomings of dendritic cells. Trends Immunol. 0, 585-591.
6. Willems, F., Vollstedt, S., Suter, M. (2009) Phenotype and function of eonatal DC. Eur. J. Immunol. 39, 26-35.
7. Goriely, S., Van Lint, C., Dadkhah, R., Libin, M., De Wit, D., Demonté, Willems, F., Goldman, M. (2004) A defect in nucleosome remodeling revents IL-12(p35) gene ranscription in neonatal dendritic cells. J. Exp. ed. 199, 1011-1016.
8. Kollmann, T. R., Crabtree, J., Rein-Weston, A., Blimkie, D., Thommai, F., ang, X. Y., avoie, P. M., Furlong, J., Fortuno, I. I. I. E. S., Hajjar, M., Hawkins, N. R., Self, S. G., ilson, C. B. (2009) Neonatal innate LR-mediated responses are distinct from those of dults. J. Immunol. 83, 7150-7160.
9. Vanden Eijnden, S., Goriely, S., De Wit, D., Goldman, M., Willems, F. 2006) Preferential production of the IL-12(p40)/IL-23(p19) heterodimer y dendritic cells from uman newborns. Eur. J. Immunol. 36, 1-26.
10. Hayday, A. C. (2000) γδ Cells: a right time and a right place for a conserved hird way of protection. Annu. Rev. Immunol. 18, 975-1026.
11. Holtmeier, W., Kabelitz, D. (2005) γδ T cells link innate and adaptive mmune esponses. Chem. Immunol. Allergy 86, 151-183.
12. Wang, L., Kamath, A., Das, H., Li, L., Bukowski, J. F. (2001) Antibacterial ffect of uman V2Vγδ2 T cells in vivo. J. Clin. Invest. 108, 1349-1357.
13. Pennington, D. J., Vermijlen, D., Wise, E. L., Clarke, S. L., Tigelaar, R. E., ayday, A. C. (2005) The integration of conventional and unconventional cells that characterizes cell-mediated responses. Adv. Immunol. 7, 27-59.
14. Toulon, A., Breton, L., Taylor, K. R., Tenenhaus, M., Bhavsar, D., Lanigan, Rudolph, R., Jameson, J., Havran, W. L. (2009) A role for humanskin-resident T cells in wound healing. J. Exp. Med. 206, 743-750.
15. Eberl, M., Hintz, M., Reichenberg, A., Kollas, A. K., Wiesner, J., Jomaa (2003) Microbial isoprenoid biosynthesis and human γδ T cell activation. EBS Lett. 544, 4-10.
16. Dieli, F., Vermijlen, D., Fulfaro, F., Caccamo, N., Meraviglia, S., Cicero, Roberts, Buccheri, S., D'Asaro, M., Gebbia, N., Salerno, A., Eberl, M., Hayday, A. C. (2007) Targeting human γδ T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res. 67, 7450-7457.
17. Body, J. J. (2006) Bisphosphonates for malignancy-related bone disease: current status, future developments. Support. Care Cancer 14, 408-418.
18. Li, J., Herold, M. J., Kimmel, B., Muller, I., Rincon-Orozco, B., Kunzmann, V., Herrmann, T. (2009) Reduced expression of the mevalonate pathway enzyme farnesyl pyrophosphate synthase unveils recognition of tumor cells by Vγ9Vδ2 T cells. J. Immunol. 182, 8118-8124.
19. Kistowska, M., Rossy, E., Sansano, S., Gober, H. J., Landmann, R., Mori, L., De Libero, G. (2008) Dysregulation of the host mevalonate pathway during early bacterial infection activates human TCR γδ cells. Eur. J. Immunol. 38, 2200-2209.
20. Vermijlen, D., Ellis, P., Langford, C., Klein, A., Engel, R., Willimann, K., Jomaa, H., Hayday, A. C., Eberl, M. (2007) Distinct cytokine-driven responses of activated blood γδ T cells: insights into unconventional T cell pleiotropy. J. Immunol. 178, 4304-4314.
21. Ramsburg, E., Tigelaar, R., Craft, J., Hayday, A. (2003) Age-dependent requirement for γδ T cells in the primary but not secondary protective immune response against an intestinal parasite. J. Exp. Med. 198, 1403-1414.
22. De Rosa, S. C., Andrus, J. P., Perfetto, S. P., Mantovani, J. J., Herzenberg, L. A., Herzenberg, L. A., Roederer, M. (2004) Ontogeny of γδ T cells in humans. J. Immunol. 172, 1637-1645.
23. Gibbons, D. L., Haque, S. F., Silberzahn, T., Hamilton, K., Langford, C., Ellis, P., Carr, R., Hayday, A. C. (2009) Neonates harbor highly active γδ T cells with selective impairments in preterm infants. Eur. J. Immunol. 39, 1794-1806.
24. Morita, C. T., Parker, C. M., Brenner, M. B., Band, H. (1994) TCR usage and functional capabilities of human γδ T cells at birth. J. Immunol. 153, 3979-3988.
25. Cairo, C., Mancino, G., Cappelli, G., Pauza, C. D., Galli, E., Brunetti, E., Colizzi, V. (2008) Vγδ2 T-lymphocyte responses in cord blood samples from Italy and Cote d'Ivoire. Immunology 124, 380-387.
26. Vermijlen, D., Brouwer, M., Donner, C., Liesnard, C., Tackoen, M., Van Rysselberge, M., Twite, N., Goldman, M., Marchant, A., Willems, F. (2010) Human cytomegalovirus elicits fetal γδ T cell responses in utero. J. Exp. Med. 207, 807-821.
27. Berthou, C., Legros-Maida, S., Soulie, A., Wargnier, A., Guillet, J., Rabian, C., Gluckman, E., Sasportes, M. (1995) Cord blood T lymphocytes lack constitutive perforin expression in contrast to adult peripheral blood T lymphocytes. Blood 85, 1540-1546.
28. Engelmann, I., Moeller, U., Santamaria, A., Kremsner, P. G., Luty, A. J. (2006) Differing activation status and immune effector molecule expression profiles of neonatal and maternal lymphocytes in an African population. Immunology 119, 515-521.
29. Vanhecke, D., Verhasselt, B., Debacker, V., Leclercq, G., Plum, J., Vandekerckhove, B. (1995) Differentiation to T helper cells in the thymus. Gradual acquisition of T helper cell function by CD3CD4 cells. J. Immunol. 155, 4711-4718.
30. Parker, C. M., Groh, V., Band, H., Porcelli, S. A., Morita, C., Fabbi, M., Glass, D., Strominger, J. L., Brenner, M. B. (1990) Evidence for extrathymic changes in the T cell receptor γδ repertoire. J. Exp. Med. 171, 1597-1612.
31. Gioia, C., Agrati, C., Casetti, R., Cairo, C., Borsellino, G., Battistini, L., Mancino, G., Goletti, D., Colizzi, V., Pucillo, L. P., Poccia, F. (2002) Lack of CD27-CD45RA V9Vγδ2 T cell effectors in immunocompromised hosts and during active pulmonary tuberculosis. J. Immunol. 168, 1484-1489.
32. Dieli, F., Poccia, F., Lipp, M., Sireci, G., Caccamo, N., Di, S. C., Salerno, A. (2003) Differentiation of effector/memory Vγδ2 T cells and migratory routes in lymph nodes or inflammatory sites. J. Exp. Med. 198, 391-397.
33. Sato, K., Kimura, S., Segawa, H., Yokota, A., Matsumoto, S., Kuroda, J., Nogawa, M., Yuasa, T., Kiyono, Y., Wada, H., Maekawa, T. (2005) Cytotoxic effects of γδ T cells expanded ex vivo by a third generation bisphosphonate for cancer immunotherapy. Int. J. Cancer 116, 94-99.
34. Ness-Schwickerath, K. J., Jin, C., Morita, C. T. (2010) Cytokine requirements for the differentiation and expansion of IL-17A- and IL-22-producing human V2Vγδ2 T cells. J. Immunol. 184, 7268-7280.
35. Yin, Z., Chen, C., Szabo, S. J., Glimcher, L. H., Ray, A., Craft, J. (2002) T-bet expression and failure of GATA-3 cross-regulation lead to default production of IFN- by γδ T cells. J. Immunol. 168, 1566-1571.
36. Umemura, M., Kawabe, T., Shudo, K., Kidoya, H., Fukui, M., Asano, M., Iwakura, Y., Matsuzaki, G., Imamura, R., Suda, T. (2004) Involvement of IL-17 in Fas ligand-induced inflammation. Int. Immunol. 16, 1099-1108.
37. Stark, M. A., Huo, Y., Burcin, T. L., Morris, M. A., Olson, T. S., Ley, K. (2005) Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22, 285-294.
38. O'Brien, R. L., Roark, C. L., Born, W. K. (2009) IL-17-producing γδ T cells. Eur. J. Immunol. 39, 662-666.
39. Deknuydt, F., Scotet, E., Bonneville, M. (2009) Modulation of inflammation through IL-17 production by γδ T cells: mandatory in the mouse, dispensable in humans? Immunol. Lett. 127, 8-12.
40. Peng, M. Y., Wang, Z. H., Yao, C. Y., Jiang, L. N., Jin, Q. L., Wang, J., Li, B. Q. (2008) Interleukin 17-producing γδ T cells increased in patients with active pulmonary tuberculosis. Cell. Mol. Immunol. 5, 203-208.
41. Fenoglio, D., Poggi, A., Catellani, S., Battaglia, F., Ferrera, A., Setti, M., Murdaca, G., Zocchi, M. R. (2009) Vγδ1 T lymphocytes producing IFN- and IL-17 are expanded in HIV-1-infected patients and respond to Candida albicans. Blood 113, 6611-6618.
42. Annunziato, F., Cosmi, L., Liotta, F., Maggi, E., Romagnani, S. (2008) The phenotype of human Th17 cells and their precursors, the cytokines that mediate their differentiation and the role of Th17 cells in inflammation. Int. Immunol. 20, 1361-1368.
43. Kabelitz, D., Wesch, D., He, W. (2007) Perspectives of γδ T cells in tumor immunology. Cancer Res. 67, 5-8.
44. Bukowski, J. F., Morita, C. T., Brenner, M. B. (1994) Recognition and destruction of virus-infected cells by human γδ CTL. J. Immunol. 153, 5133-5140.
45. Dieli, F., Troye-Blomberg, M., Ivanyi, J., Fournie, J. J., Krensky, A. M., Bonneville, M., Peyrat, M. A., Caccamo, N., Sireci, G., Salerno, A. (2001) Granulysin-dependent killing of intracellular and extracellular Mycobacterium tuberculosis by V9/Vγδ2 T lymphocytes. J. Infect. Dis. 184, 1082-1085.
46. Gober, H. J., Kistowska, M., Angman, L., Jeno, P., Mori, L., De Libero, G. (2003) Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells. J. Exp. Med. 197, 163-168.
47. Sarikonda, G., Wang, H., Puan, K. J., Liu, X. H., Lee, H. K., Song, Y., Distefano, M. D., Oldfield, E., Prestwich, G. D., Morita, C. T. (2008) Photoaffinity antigens for human γδ T cells. J. Immunol. 181, 7738-7750.
48. Scotet, E., Martinez, L. O., Grant, E., Barbaras, R., Jeno, P., Guiraud, M., Monsarrat, B., Saulquin, X., Maillet, S., Esteve, J. P., Lopez, F., Perret, B., Collet, X., Bonneville, M., Champagne, E. (2005) Tumor recognition fol-lowing V9Vγδ2 T cell receptor interactions with a surface F1-ATPase-related structure and apolipoprotein A-I. Immunity 22, 71-80.
49. Hayday, A. C. (2009) γδ T cells and the lymphoid stress-surveillance response. Immunity 31, 184-196.
50. Goriely, S., Neurath, M. F., Goldman, M. (2008) How microorganisms tip the balance between interleukin-12 family members. Nat. Rev. Immunol. 8, 81-86.
51. Oppmann, B., Lesley, R., Blom, B., Timans, J. C., Xu, Y., Hunte, B., Vega, F., Yu, N., Wang, J., Singh, K., Zonin, F., Vaisberg, E., Churakova, T., Liu, M., Gorman, D., Wagner, J., Zurawski, S., Liu, Y., Abrams, J. S., Moore, K. W., Rennick, D., de Waal-Malefyt, R., Hannum, C., Bazan, J. F., Kastelein, R. A. (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13, 715-725.
52. Ahern, P. P., Schiering, C., Buonocore, S., McGeachy, M. J., Cua, D. J., Maloy, K. J., Powrie, F. (2010) Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 33, 279-288.
53. Bettelli, E., Korn, T., Oukka, M., Kuchroo, V. K. (2008) Induction and effector functions of T(H)17 cells. Nature 453, 1051-1057.
54. Rachitskaya, A. V., Hansen, A. M., Horai, R., Li, Z., Villasmil, R., Luger, D., Nussenblatt, R. B., Caspi, R. R. (2008) Cutting edge: NKT cells constitutively express IL-23 receptor and RORt and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J. Immunol. 180, 5167-5171.
55. Ghoreschi, K., Laurence, A., Yang, X. P., Tato, C. M., McGeachy, M. J., Konkel, J. E., Ramos, H. L., Wei, L., Davidson, T. S., Bouladoux, N., Grainger, J. R., Chen, Q., Kanno, Y., Watford, W. T., Sun, H. W., Eberl, G., Shevach, E. M., Belkaid, Y., Cua, D. J., Chen, W., O'Shea, J. J. (2010) Generation of pathogenic T(H)17 cells in the absence of TGF-β signaling. Nature 467, 967-971.
56. Lockhart, E., Green, A. M., Flynn, J. L. (2006) IL-17 production is dominated by γδ T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J. Immunol. 177, 4662-4669.
57. Sutton, C. E., Lalor, S. J., Sweeney, C. M., Brereton, C. F., Lavelle, E. C., Mills, K. H. (2009) Interleukin-1 and IL-23 induce innate IL-17 production from γδ T cells, amplifying Th17 responses and autoimmunity. Immunity 31, 331-341.
58. Martin, B., Hirota, K., Cua, D. J., Stockinger, B., Veldhoen, M. (2009) Interleukin-17-producing γδ T cells selectively expand in response to pathogen products and environmental signals. Immunity 31, 321-330.
59. Haas, J. D., Gonzalez, F. H., Schmitz, S., Chennupati, V., Fohse, L., Kremmer, E., Forster, R., Prinz, I. (2009) CCR6 and NK1.1 distinguish between IL-17A and IFN--producing γδ effector T cells. Eur. J. Immunol. 39, 3488-3497.
60. Shibata, K., Yamada, H., Nakamura, R., Sun, X., Itsumi, M., Yoshikai, Y. (2008) Identification of CD25 γδ T cells as fetal thymus-derived naturally occurring IL-17 producers. J. Immunol. 181, 5940-5947.
61. Klein, J. O., Remington, J. S. (2001) Current concepts of infections of the fetus and newborn infant. In Infectious Diseases of the Fetus and Newborn Infant. Philadelphia, PA, USA, W. B. Saunders Co., 1-23.
62. Schaub, B., Liu, J., Schleich, I., Hoppler, S., Sattler, C., von Mutius, E. (2008) Impairment of T helper and T regulatory cell responses at birth. Allergy 63, 1438-1447.
63. Chowdhury, D., Lieberman, J. (2008) Death by a thousand cuts: granzyme pathways of programmed cell death. Annu. Rev. Immunol. 26, 389-420.
64. Ooi, J. (2009) Cord blood transplantation in adults. Bone Marrow Transplant. 44, 661-666.
65. Godder, K. T., Henslee-Downey, P. J., Mehta, J., Park, B. S., Chiang, K. Y., Abhyankar, S., Lamb, L. S. (2007) Long term disease-free survival in acute leukemia patients recovering with increased γδ T cells after partially mismatched related donor bone marrow transplantation. Bone Marrow Transplant. 39, 751-757.
66. Farouk, S. E., Mincheva-Nilsson, L., Krensky, A. M., Dieli, F., Troye- Blomberg, M. (2004) γδ T cells inhibit in vitro growth of the asexual blood stages of Plasmodium falciparum by a granule exocytosis-dependent cytotoxic pathway that requires granulysin. Eur. J. Immunol. 34, 2248-2256.
67. Dieli, F., Sireci, G., Caccamo, N., Di, S. C., Titone, L., Romano, A., Di, C. P., Barera, A., Accardo-Palumbo, A., Krensky, A. M., Salerno, A. (2002) Selective depression of interferon-and granulysin production with increase of proliferative response by V9/Vγδ2 T cells in children with tuberculosis. J. Infect. Dis. 186, 1835-1839.
68. Gerosa, F., Baldani-Guerra, B., Lyakh, L. A., Batoni, G., Esin, S., Winkler- ickett, R. T., Consolaro, M. R., De, M. M., Giachino, D., Robbiano, A., Astegiano, M., Sambataro, A., Kastelein, R. A., Carra, G., Trinchieri, G. 2008) Differential regulation of interleukin 12 and interleukin 23 production n human dendritic cells. J. Exp. Med. 205, 1447-1461.
69. Ribot, J. C., Debarros, A., Pang, D. J., Neves, J. F., Peperzak, V., Roberts,. J., Girardi, M., Borst, J., Hayday, A. C., Pennington, D. J., Silva-Santos,. (2009) CD27 is a thymic determinant of the balance between interferon-and interleukin 17-producing γδ T cell subsets. Nat. Immunol. 10,427-436.
70. Jensen, K. D., Su, X., Shin, S., Li, L., Youssef, S., Yamasaki, S., Steinman, L., Saito, T., Locksley, R. M., Davis, M. M., Baumgarth, N., Chien, Y. H.(2008) Thymic selection determines γδ T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon. Immunity 29, 90-100.
71. Glimcher, L. H., Townsend, M. J., Sullivan, B. M., Lord, G. M. (2004) Recent developments in the transcriptional regulation of cytolytic effector cells. Nat. Rev. Immunol. 4, 900-911.