Human Vδ2+ γδ T cells differentially induce maturation, cytokine production, and alloreactive T cell stimulation by dendritic cells and B cells

Frontiers in Immunology

Volumn 5, Issue DEC, 2014, Pages

  Petrasca, Andreea ^a   Doherty, Derek G ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Antibody production; APC; B cells; Cytokines; Dendritic cells; Human T cells; T cell proliferation

Indexed keywords

ALPHA INTERFERON; CD40 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; HLA DR ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 4; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANTIBODY PRODUCTION; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FLOW CYTOMETRY; GAMMA DELTA T LYMPHOCYTE; HUMAN; NORMAL HUMAN; PROTEIN EXPRESSION; TH1 CELL;

EID: 84919488917     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00650     Document Type: Article

References (51)

1. Morita CT, Jin C, Sarikonda G, Wang H. Nonpeptide antigens, presentation, mechanisms and immunological memory of human Vγ2Vδ2 T cells: discriminating friend from foe through the recognition of prenyl pyrophosphate antigens. Immunol Rev (2007) 215:59-76. doi:10.1111/j.1600-065X.2006.00479.x
2. Kabelitz D, He W. The malfunctionality of human Vγ9Vδ2 γδ T cells: clonal plasticity or distinct subsets? Scand J Immunol (2012) 76:213-22. doi:10.1111/j.1365-3083.2012.02727.x
3. Vantourout P, Hayday AC. Six-of-the-best: unique contributions of γδ T cells to immunology. Nat Rev Immunol (2013) 13:88-100. doi:10.1038/nri3384
4. Chien YH, Meyer C, Bonneville M. γδ T cells: first line of defense and beyond. Annu Rev Immunol (2014) 32:121-55. doi:10.1146/annurev-immunol-032713-120216
5. Hara T, Mizuno Y, Takaki K, Takada H, Akeda H, Aoki T, et al. Predominant activation and expansion of Vγ9-bearing γδ T cells in vivo as well as in vitro in Salmonella infection. J Clin Invest (1992) 90:204-10. doi:10.1172/JCI115837
6. Eberl M, Hintz M, Reichenberg A, Kollas AK, Wiesner J, Jomaa H. Microbial isoprenoid biosynthesis and human γδ T cell activation. FEBS Lett (2003) 554:4-10. doi:10.1016/S0014-5793(03)00483-6
7. Harly C, Guillaume Y, Nedellec S, Peigné CM, Mönkkönen J, Li J, et al. Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human γδ T-cell subset. Blood (2012) 120:2269-79. doi:10.1182/blood-2012-05-430470
8. Sandstrom A, Peigné CM, Léger A, Crooks JE, Konczak F, Gesnel MC, et al. The intracellular B30.2 domain of butyrophilin 3A1 binds phosphoantigens to mediate activation of human Vγ9Vδ2 T cells. Immunity (2014) 40:490-500. doi:10.1016/j.immuni.2014.03.003
9. Hintz M, Reichenberg A, Altincicek B, Bahr U, Gschwind RM, Kollas AK, et al. Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human γδ T cells in Escherichia coli. FEBS Lett (2001) 509:317-22. doi:10.1016/S0014-5793(01)03191-X
10. Dunne MR, Madrigal-Estebas L, Tobin LM, Doherty DG. E(H)-4-hydroxy-3-methyl-but-2 enyl pyrophosphate-stimulated Vγ9Vδ2 T cells possess T helper type 1-promoting adjuvant activity for human monocyte-derived dendritic cells. Cancer Immunol Immunother (2010) 59:1109-20. doi:10.1007/s00262-010-0839-8
11. Banchereau J, Briere F, Caux C, Davoust J, Lebcque S, Liu YJ, et al. Immunobiology of dendritic cells. Annu Rev Immunol (2000) 18:767-811. doi:10.1146/annurev.immunol.18.1.767
12. Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell (2001) 106:255-8. doi:10.1016/S0092-8674(01)00449-4
13. Ismaili J, Olislagers V, Poupot R, Fournié JJ, Goldman M. Human γδ T cells induce dendritic cell maturation. Clin Immunol (2002) 103:296-302. doi:10.1006/clim.2002.5218
14. Conti L, Casetti R, Cardone M, Varano B, Martino A, Belardelli F, et al. Reciprocal activating interaction between dendritic cells and pamidronate-stimulated T cells: role of CD86 and inflammatory cytokines. J Immunol (2005) 174:252-60. doi:10.4049/jimmunol.174.1.252
15. Martino A, Casetti R, D'Alessandri A, Sacchi A, Poccia F. Complementary function of gamma delta T-lymphocytes and dendritic cells in the response to isopentenyl-pyrophosphate and lipopolysaccharide antigens. J Clin Immunol (2005) 25:230-7. doi:10.1007/s10875-005-4080-8
16. Shrestha N, Ida JA, Lubinski AS, Pallin M, Kaplan G, Haslett PA. Regulation of acquired immunity by γδ T-cell/dendritic-cell interactions. Ann N Y Acad Sci (2005) 1062:79-94. doi:10.1196/annals.1358.011
17. Devilder MC, Maillet S, Bouyge-Moreau I, Donnadieu E, Bonneville M, Scotet E. Potentiation of antigen-stimulated Vγ9Vδ2 T cell cytokine production by immature dendritic cells (DC) and reciprocal effect on DC maturation. J Immunol (2006) 176:1386-93. doi:10.4049/jimmunol.176.3.1386
18. Kalyan S, Chow AW. Linking innate and adaptive immunity: human Vγ9Vδ2 T cells enhance CD40 expression and HMGB-1 secretion. Mediators Inflamm (2009) 2009:819408. doi:10.1155/2009/819408
19. Eberl M, Roberts GW, Meuter S, Williams JD, Topley N, Moser B. A rapid crosstalk of human γδ T cells and monocytes drives the acute inflammation in bacterial infections. PLoS Pathog (2009) 5:e1000308. doi:10.1371/journal.ppat.1000308
20. Agrati C, Cimini E, Sacchi A, Bordoni V, Gioia C, Casetti R, et al. Activated Vγ9Vδ2 T cells trigger granulocyte functions via MCP-2 release. J Immunol (2009) 182:522-9. doi:10.4049/jimmunol.182.1.522
21. Davey MS, Lin CY, Roberts GW, Heuston S, Brown AC, Chess JA, et al. Human neutrophil clearance of bacterial pathogens triggers anti-microbial γδ T cell responses in early infection. PLoS Pathog (2011) 7:e1002040. doi:10.1371/journal.ppat.1002040
22. Davey MS, Morgan MP, Liuzzi AR, Tyler CJ, Khan MW, Szakmany T, et al. Microbe-specific unconventional T cells induce human neutrophil differentiation into antigen cross-presenting cells. J Immunol (2014) 193:3704-16. doi:10.4049/jimmunol.1401018
23. Rodriguez-Pinto D. B cells as antigen presenting cells. Cell Immunol (2005) 238:67-75. doi:10.1016/j.cellimm.2006.02.005
24. Harris DP, Haynes L, Sayles PC, Duso DK, Eaton SM, Lepak NM, et al. Reciprocal regulation of polarized cytokine production by effector B cells and T cells. Nat Immunol (2000) 1:475-82. doi:10.1038/82717
25. Brandes M, Willimann K, Lang AB, Nam KH, Jin C, Brenner MB, et al. Flexible migration program regulates γδ T-cell involvement in humoral immunity. Blood (2003) 102:3693-701. doi:10.1182/blood-2003-04-1016
26. Caccamo N, Battistini L, Bonneville M, Poccia F, Fournié JJ, Meraviglia S, et al. CXCR5 identifies a subset of Vγ9Vδ2 T cells which secrete IL-4 and IL-10 and help B cells for antibody production. J Immunol (2006) 177:5290-5. doi:10.4049/jimmunol.177.8.5290
27. Bansal RR, Mackay CR, Moser B, Eberl M. IL-21 enhances the potential of human γδ T cells to provide B-cell help. Eur J Immunol (2011) 42:110-9. doi:10.1002/eji.201142017
28. Caccamo N, Todaro M, La Manna MP, Sireci G, Stassi G, Dieli F. IL-21 regulates the differentiation of a human γδ T cell subset equipped with B cell helper activity. PLoS One (2012) 7:e41940. doi:10.1371/journal.pone.0041940
29. Marcu-Malina V, Balbir-Gurman A, Dardik R, Braun-Moscovici Y, Segel MJ, Bank I. A novel prothrombotic pathway in systemic sclerosis patients: possible role of biosphosphonate-activated γδ T cells. Front Immunol (2014) 5:414. doi:10.3389/fimmu.2014.00414
30. Tisch R. Immunogenic versus tolerogenic dendritic cells: a matter of maturation. Int Rev Immunol (2010) 29:111-8. doi:10.3109/08830181003602515
31. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol (2003) 21:685-711. doi:10.1146/annurev.immunol.21.120601.141040
32. Reise Sousa C. Dendritic cells in a mature age. Nat Rev Immunol (2006) 6:476-83. doi:10.1038/nri1845
33. Lutz MB, Schuler G. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol (2002) 23:445-9. doi:10.1016/S1471-4906(02)02281-0
34. Eynon EE, Parker DC. Small B cells as antigen-presenting cells in the induction of tolerance to soluble protein antigen. J Exp Med (1992) 175:131-8. doi:10.1084/jem.175.1.131
35. Fuchs EJ, Matzinger P. B cells turn off virgin but not memory T cells. Science (1992) 258:1156-9. doi:10.1126/science.1439825
36. Kitamura H, Iwakabe K, Yahata T, Nishimura S, Ohta A, Ohmi Y, et al. The natural killer T (NKT) cell ligand alpha-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells. J Exp Med (1999) 189:1121-8. doi:10.1084/jem.189.7.1121
37. Vincent MS, Leslie DS, Gumperz JE, Xiong X, Grant EP, Brenner MB. CD1-dependent dendritic cell instruction. Nat Immunol (2002) 3:1163-8. doi:10.1038/ni851
38. Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM. Activation of natural killer T cells by a-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J Exp Med (2003) 198:267-79. doi:10.1084/jem.20030324
39. Galli G, Nuti S, Tavarini S, Galli-Stampino L, De Lalla C, Casorati G, et al. CD1d-restricted help to B cells by human invariant natural killer T lymphocytes. J Exp Med (2003) 197:1051-7. doi:10.1084/jem.20021616
40. Devera T, Shah H, Lang G, Lang M. Glycolipid-activated NKT cells support the induction of persistent plasma cell responses and antibody titers. Eur J Immunol (2008) 38:1001-11. doi:10.1002/eji.200738000
41. Barral P, Eckl-Dorna J, Harwood NE, De Santo C, Salio M, Illarionov P, et al. B cell receptor-mediated uptake of CD1d-restricted antigen augments antibody responses by recruiting invariant NKT cell help in vivo. Proc Natl Acad Sci USA (2008) 105:8345-50. doi:10.1073/pnas.0802968105
42. Leadbetter E, Brigl M, Illarionov P, Cohen N, Luteran M, Pillai S, et al. NK T cells provide lipid antigen-specific cognate help for B cells. Proc Natl Acad Sci USA (2008) 105:8339-44. doi:10.1073/pnas.0801375105
43. O'Reilly V, Zeng S, Bricard G, Atzberger A, Hogan AE, Jackson J, et al. Distinct and overlapping effector functions of expanded human CD4+, CD8a+ and CD4-CD8a- invariant natural killer T cells. PLoS One (2011) 6:e28648. doi:10.1371/journal.pone.0028648
44. Zeng SG, Ghnewa YG, O'Reilly VP, Lyons VG, Atzberger A, Hogan AE, et al. Human invariant NKT cell subsets differentially promote differentiation, antibody production and T cell stimulation by B cells in vitro. J Immunol (2013) 191:1666-76. doi:10.4049/jimmunol.1202223
45. Leslie DS, Vincent MS, Spada FM, Das H, Sugita M, Morita CT, et al. CD1-mediated γδ T cell maturation of dendritic cells. J Exp Med (2002) 196:1575-84. doi:10.1084/jem.20021515
46. Collins C, Wolfe J, Roessner K, Shi C, Sigal LH, Budd RC. Lyme arthritis synovial γδ T cells instruct dendritic cells via fas ligand. J Immunol (2005) 175:5656-65. doi:10.4049/jimmunol.175.9.5656
47. Mangan BA, Dunne MR, O'Reilly VP, Dunne PJ, Exley MA, Doherty DG. Cutting edge: CD1d restriction and Th1/Th2/Th17 cytokine secretion by human Vd3 T cells. J Immunol (2013) 191:30-4. doi:10.4049/jimmunol.1300121
48. Russano AM, Agea E, Corazzi L, Postle AD, De Libero G, Porcelli S, et al. Recognition of pollen-derived phosphatidyl-ethanolamine by human CD1d-restricted γδ T cells. J Allergy Clin Immunol (2006) 117:1178-84. doi:10.1016/j.jaci.2006.01.001
49. Meraviglia S, Eberl M, Vermijlen D, Todaro M, Buccheri S, Cicero G, et al. In vivo manipulation of Vγ9Vδ2 T cells with zoledronate and low-dose interleukin-2 for immunotherapy of advanced breast cancer patients. Clin Exp Immunol (2010) 161:290-7. doi:10.1111/j.1365-2249.2010.04167.x
50. Kalyan S, Wesch D, Kabelitz D. Aminobisphosphonates and Toll-like receptor ligands: recruiting Vγ9Vδ2 T cells for the treatment of hematologic malignancy. Curr Med Chem (2011) 18:5206-16. doi:10.2174/092986711798184280
51. Santolaria T, Robard M, Léger A, Catros V, Bonneville M, Scotet E. Repeated systemic administrations of both aminobisphosphonates and human Vγ9Vδ2 T cells efficiently control tumor development in vivo. J Immunol (2013) 191:1993-2000. doi:10.4049/jimmunol.1300255