Balanced approach of γδ T cells to type 2 immunity

Immunology and Cell Biology

Volumn 88, Issue 3, 2010, Pages 269-274

  Born, Willi K ^a,b   Yafei, Huang ^a,b   Jin, Niyun ^a,b   Hua, Huang ^a,b   O'Brien, Rebecca L ^a,b  

^a DEPARTMENT OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; ALUMINUM HYDROXIDE; CD4 ANTIGEN; CD40 LIGAND; CD8 ANTIGEN; CHEMOKINE RECEPTOR CXCR5; CXCL13 CHEMOKINE; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 4; METHACHOLINE; T LYMPHOCYTE RECEPTOR; BRONCHOCONSTRICTING AGENT; LYMPHOCYTE ANTIGEN RECEPTOR; METHACHOLINE CHLORIDE;

AIRWAY; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL FUNCTION; CELL POLARITY; CELL TRANSFER; CELLULAR IMMUNITY; DENDRITIC CELL; EOSINOPHIL; EXPOSURE; HELPER CELL; HUMAN; HYPERSENSITIVITY REACTION; IMMUNE RESPONSE; IMMUNIZATION; INHALATION; MEAN CORPUSCULAR HEMOGLOBIN; NATURAL KILLER T CELL; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SPLEEN; SUPPRESSOR CELL; T DELTA CELL; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TARGET CELL; TH17 CELL; TH2 CELL; ANIMAL; DISEASE MODEL; DRUG EFFECT; HYPERSENSITIVITY; IMMUNOLOGY; MOUSE;

ALLERGENS; ANIMALS; BRONCHOCONSTRICTOR AGENTS; DISEASE MODELS, ANIMAL; HUMANS; HYPERSENSITIVITY; IMMUNITY, CELLULAR; IMMUNOGLOBULIN E; METHACHOLINE CHLORIDE; MICE; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; TH2 CELLS;

EID: 77949875787     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2009.105     Document Type: Review

References (78)

1. Haas W, Pereira P, Tonegawa S. Gamma/delta T cells. Annu Rev Immunol 1993; 11: 637-685.
2. Born W, Cady C, Jones-Carson J, Mukasa A, Lahn M, O'Brien R. Immunoregulatory functions of gd T cells. Adv Immunol 1999; 71: 77-144.
3. Hayday A, Tigelaar R. Immunoregulation in the tissues by gd T cells. Nat Rev Immunol 2003; 3: 233-242.
4. Cheng L, Cui Y, Shao H, Han G, Zhu L, Huang Y et al. Mouse gammadelta T cells are capable of expressing MHC class II molecules, and of functioning as antigen-presenting cells. J Neuroimmunol 2008; 203: 3-11.
5. Brandes M, Willimann K, Moser B. Professional antigen-presenting function by human gamma delta T cells. Science 2005; 309: 264-268.
6. Collins RA, Werling D, Duggan SE, Bland AP, Parsons KR, Howard CJ. gd T cells present antigen to CD4+ ab T cells. J Leukoc Biol 1998; 63: 707-714.
7. Rock EP, Sibbald PR, Davis MM, Chien YH. CDR3 length in antigen-specific immune receptors. J Exp Med 1994; 179: 323-328.
8. Chien Y-H, Jores R, Crowley MP. Recognition by g/d T cells. Annu Rev Immunol 1996; 14: 511-532.
9. Cook L, Miyahara N, Jin N, Wands JM, Taube C, Roark CL et al. Evidence that CD8+ dendritic cells enable the development of gammadelta T cells that modulate airway hyperresponsiveness. J Immunol 2008; 181: 309-319.
10. Wen L, Roberts SJ, Viney JL, Wong FS, Mallick C, Findly RC et al. Immunoglobulin synthesis and generalized autoimmunity in mice congenitally deficient in ab(+) T cells. Nature 1994; 369: 654-658.
11. Wen L, Pao W, Wong FS, Peng Q, Craft J, Zheng B et al. Germinal center formation immunoglobulin class switching and autoantibody production driven by 'non a/b' T cells. J Exp Med 1996; 183: 2271-2282.
12. Pao W, Wen L, Smith AL, Gulbranson-Judge A, Zheng B, Kelsoe G et al. Tcell help of B cells is induced by repeated parasitic infection, in the absence of other T cells. Curr Biol 1996; 6: 1317-1325.
13. Huber SA, Graveline D, Newell MK, Born WK, O'Brien RL. Vg1+ T cells suppress and Vg4+ T cells promote susceptibility to coxsackievirus B3-induced myocarditis in mice. J Immunology 2000; 165: 4174-4181.
14. Hahn YS, Taube C, Jin N, Sharp L, Wands JM, Aydintug MK et al. Different potentials of gd T cell subsets in regulating airway responsiveness: Vg1+ cells, but not Vg4+ cells, promote airway hyperreactivity, TH2 cytokines, and airway inflammation. J Immunol 2004; 172: 2894-2902.
15. Huang Y, Jin N, Roark CL, Aydintug MK, Wands JM, Huang H et al. The influence of IgE-enhancing and IgE-suppressive gammadelta T cells changes with exposure to inhaled ovalbumin. J Immunol 2009; 183: 849-855.
16. O'Brien RL, Roark CL, Jin N, Aydintug MK, French JD, Chain JL et al. gd T cell receptors: functional correlations. Immunol Rev 2007; 215: 77-88.
17. Maizels RM, Pearce EJ, Artis D, Yazdanbakhsh M, Wynn TA. Meeting review regulation of pathogenesis and immunity in helminth infections. J Exp Med 2009; 206: 2059-2066.
18. Sandor M, Sperling AI, Cook GA, Weinstock JV, Lynch RG, Bluestone JA. Two waves of gd T cells expressing different Vd genes are recruited into schistosome-induced liver granuloma. J Immunol 1995; 155: 275-284.
19. Tsuji M, Mombaerts P, Lefrancois L, Nussenzweig RS, Zavala F, Tonegawa S. gd T cells contribute to immunity against the liver stages of malaria in ab T-cell-deficient mice. Proc Natl Acad Sci USA 1994; 91: 345-349.
20. Findly RC, Roberts SJ, Hayday AC. Dynamic response of murine gut intraepithelial T cells after infection by the coccidian parasite Eimeria. Eur J Immunol 1993; 23: 2557-2564.
21. Ferrick DA, Schrenzel MD, Mulvania T, Hsieh B, Ferlin WG, Lepper H. Differential production of interferon-g and interleukin-4 in response to Th1-and Th2-stimulating pathogens by gd T cells in vivo. Nature 1995; 373: 255-257.
22. Arck PC, Ferrick DA, Steele-Norwood D, Croitoru K, Clark DA. Murine T cell determination of pregnancy outcome. I. Effects of strain, ab T cell receptor, gd T cell receptor, and gd T cell subsets. Am J Reprod Immunol 1997; 37: 492.
23. Nagaeva O, Jonsson L, Mincheva-Nilsson L. Dominant IL-10 and TGF-beta mRNA expression in gammadelta T cells of human early pregnancy decidua suggests immunoregulatory potential. Am J Reprod Immunol 2002; 48: 9-17.
24. Krug N, Erpenbeck VJ, Balke K, Petschallies J, Tschernig T, Hohlfeld JM et al. Cytokine profile of bronchoalveolar lavage-derived CD4(+), CD8(+), and gammadelta T cells in people with asthma after segmental allergen challenge. Am J Respir Cell Mol Biol 2001; 25: 125-131.
25. Zuany-Amorim C, Ruffie C, Haile S, Vargaftig BB, Pereira P, Pretolani M. Requirement for gd T cells in allergic airway inflammation. Science 1998; 280: 1265-1267.
26. Svenson L, Lilliehook B, Larsson R, Bucht A. gd T cells contribute to the systemic immunoglobulin E response and local B-cell reactivity in allergic eosinophilic airway inflammation. Immunology 2003; 108: 98-108.
27. Russano AM, Agea E, Corazzi L, Postle AD, De Libero G, Porcelli SA et al. Recognition of pollen-derived phosphatidyl-ethanolamine by human CD1d-restricted gamma delta T cells. J Allergy Clin Immunol 2006; 117: 1178-1184.
28. Yamashita T, Miyata H, Miyaji C, Watanabe H, Abo T, Kobayakawa T et al. CD4+ and/or gammadelta+ T cells in the liver spontaneously produce IL-4 in vitro during the early phase of Leishmania major infection in susceptible BALB/c mice. Acta Trop 1999; 73: 109-119.
29. Seo N, Tokura Y, Furukawa F, Takigawa M. Down-regulation of tumoricidal NK and NK T cell activities by MHC Kb molecules expressed on Th2-type gammadelta T and alphabeta T cells coinfiltrating in early B16 melanoma lesions. J Immunol 1998; 161: 4138-4145.
30. McKee AS, Munks MW, MacLeod MK, Fleenor CJ, Van Rooijen N, Kappler JW et al. Alum induces innate immune responses through macrophage and mast cell sensors, but these sensors are not required for alum to act as an adjuvant for specific immunity. J Immunol 2009; 183: 4403-4414.
31. McMenamin C, Pimm C, McKersey M, Holt PG. Regulation of IgE responses to inhaled antigen in mice by antigen-specific gd T cells. Science 1994; 265: 1869-1871.
32. Azuara V, Levraud JP, Lembezat MP, Pereira P. A novel subset of adult gamma delta thymocytes that secretes a distinct pattern of cytokines and expresses a very restricted T cell receptor repertoire. Eur J Immunol 1997; 27: 544-553.
33. Vicari AP, Mocci S, Openshaw P, O'Garra A, Zlotnik A. Mouse gd TCR+NK1.1+ thymocytes specifically produce interleukin-4, are major histocompatibility complex class I independent, and are developmentally related to ab TCR+NK1.1+ thymocytes. Eur J Immunol 1996; 26: 1424-1429.
34. Felices M, Yin CC, Kosaka Y, Kang J, Berg LJ. Tec kinase Itk in gammadelta T cells is pivotal for controlling IgE production in vivo. Proc Natl Acad Sci USA 2009; 106: 8308-8313.
35. Spinozzi F, Agea E, Bistoni O, Forenza N, Bertotto A. gd T cells, allergen recognition and airway inflammation. Immunol Today 1998; 19: 22-26.
36. Hamelmann E, Oshiba A, Paluh J, Bradley K, Loader J, Potter TA et al. Requirement for CD8+ T cells in the development of airway hyperresponsiveness in a murine model of airway sensitization. J Exp Med 1996; 183: 1719-1729.
37. Miyahara N, Swanson BJ, Takeda K, Taube C, Miyahara S, Kodama T et al. Effector CD8+ T cells mediate inflammation and airway hyper-responsiveness. Nat Med 2004; 10: 865-869.
38. Akbari O, Stock P, Meyer E, Kronenberg M, Sidobre S, Nakayama T et al. Essential role of NKT cells producing IL-4 and IL-13 in the development of allergen-induced airway hyperreactivity. Nat Med 2003; 9: 582-588.
39. Schramm CM, Puddington L, Yiamouyiannis CA, Lingenheld EG, Whiteley HE, Wolyniec WW et al. Proinflammatory roles of T-cell receptor (TCR)gd and TCRab lymphocytes in a murine model of asthma. Am J Respir Cell Mol Biol 2000; 22: 218-225.
40. Lahn M, Kanehiro A, Takeda K, Joetham A, Schwarze J, Koehler G et al. Negative regulation of airway responsiveness that is dependent on gd T cells and independent of ab T cells. Nat Med 1999; 5: 1150-1156.
41. Isogai S, Rubin A, Maghni K, Ramos-Barbon D, Taha R, Yoshizawa Y et al. The effects of CD8+ gammadelta T cells on late allergic airway responses and airway inflammation in rats. J Allergy Clin Immunol 2003; 112: 547-555.
42. Jin N, Miyahara N, Roark CL, French JD, Aydintug MK, Matsuda JL et al. Airway hyperresponsiveness through synergy of gd T cells and NKT cells. J Immunol 2007; 179: 2961-2968.
43. Matsubara S, Takeda K, Jin N, Okamoto M, Matsuda H, Shiraishi Y et al. Vgamma1+ T cells and tumor necrosis factor-alpha in ozone-induced airway hyperresponsiveness. Am J Respir Cell Mol Biol 2009; 40: 454-463.
44. Hahn YS, Ji XY, Woo SI, Choi YK, Song MS, Shin KS et al. Vgamma1(+) gammadelta T cells reduce IL-10-producing CD4(+)CD25(+) T cells in the lung of ovalbuminsensitized and challenged mice. Immunol Lett 2008; 121: 87-92.
45. Jin N, Roark CL, Miyahara N, Taube C, Aydintug MK, Wands JM et al. Allergic airway hyperresponsiveness-enhancing gammadelta T cells develop in normal untreated mice and fail to produce IL-4/13, unlike Th2 and NKT cells. J Immunol 2009; 182: 2002-2010.
46. Matsuda JL, Gapin L. Developmental program of mouse Va14i NKT cells. Curr Opin Immunol 2005; 17: 122-130.
47. King C, Tangye SG, Mackay CR. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu Rev Immunol 2008; 26: 741-766.
48. Annunziato F, Cosmi L, Santarlasci V, Maggi L, Liotta F, Mazzinghi B et al. Phenotypic and functional features of human Th17 cells. J Exp Med 2007; 204: 1849-1861.
49. Caccamo N, Battistini L, Bonneville M, Poccia F, Fournié JJ, Meraviglia S et al. CXCR5 identifies a subset of Vgamma9Vdelta2T cells which secrete IL-4 and IL-10 and help B cells for antibody production. J Immunol 2006; 177: 5290-5295.
50. Qi Q, Xia M, Hu J, Hicks E, Iyer A, Xiong N et al. Enhanced development of CD4+ gammadelta T cells in the absence of Itk results in elevated IgE production. Blood 2009; 114: 564-571.
51. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 2009; 31: 331-341.
52. Aydintug MK, Roark CL, Chain JL, Born WK, O'Brien RL. Macrophages express multiple ligands for gammadelta TCRs. Mol Immunol 2008; 45: 3253-3263.
53. Wands JM, Roark CL, Aydintug MK, Jin N, Hahn Y-S, Cook L et al. Distribution and leukocyte contacts of gd T cells in the lung. J Leukoc Biol 2005; 78: 1086-1096.
54. Eberl M, Moser B. Monocytes and gammadelta T cells: close encounters in microbial infection. Trends Immunol 2009; 30: 562-568.
55. Sokol CL, Barton GM, Farr AG, Medzitov R. A mechanism for the initiation of allergeninduced T helper type 2 responses. Nat Immunol 2008; 9: 310-318.
56. Ohmori K, Luo Y, Jia Y, Nishida J, Wang Z, Bunting KD et al. IL-3 induces basophil expansion in vivo by directing granulocyte-monocyte progenitors to differentiate into basophil lineage-restricted progenitors in the bone marrow and by increasing the number of basophil/mast cell progenitors in the spleen. J Immunol 2009; 182: 2835-2841.
57. Yin Z, Chen C, Szabo SJ, Glimcher LH, Ray A, Craft J. T-bet expression and failure of GATA-3 cross-regulation lead to default production of IFN-g by gd T cells. J Immunol 2002; 168: 1566-1571.
58. O'Brien RL, Roark CL, Born WK. IL-17-producing gammadelta T cells. Eur J Immunol 2009; 39: 662-666.
59. Hahn YS, Taube C, Jin N, Takeda K, Park JW, Wands JM et al. Vg4+ T cells regulate airway hyperreactivity to methacholine in ovalbumin-sensitized and challenged mice. J Immunol 2003; 171: 3170-3178.
60. Cui ZH, Joetham A, Aydintug MK, Hahn YS, Born WK, Gelfand EW. Reversal of established allergic airway hyperreactivity by long-term allergen challenge depends on g/d T cells. Am J Respir Crit Care Med 2003; 168: 1324-1332.
61. Lahn M, Kanehiro A, Takeda K, Terry J, Hahn Y-S, Aydintug MK et al. MHC class I-dependent Vg4+ pulmonary T cells regulate ab T cell-independent airway responsiveness. Proc Natl Acad Sci USA 2002; 99: 8850-8855.
62. Jin N, Taube C, Sharp L, Hahn Y-S, Yin X, Wands JM et al. Mismatched antigen prepares gdT cells for suppression of airway hyperresponsiveness. J Immunol 2005; 174: 2671-2679.
63. Lahn M, Kanehiro A, Hahn Y-S, Wands JM, Aydintug MK, O'Brien RL et al. Aerosolized anti-T-cell-receptor antibodies are effective against airway inflammation and hyperreactivity. Int Arch Allergy Immunol 2004; 134: 49-55.
64. McMenamin C, McKersey M, Kühnlein P, Hü nig T, Holt PG. gd T cells down-regulate primary IgE responses in rats to inhaled soluble protein antigens. J Immunol 1995; 154: 4390-4394.
65. Rammensee H-G, Bevan MJ, Fink PJ. Antigen specific suppression of T-cell responses-the veto concept. Immunol Today 1985; 6: 41-43.
66. McCoy KD, Harris NL, Diener P, Hatak S, Odermatt B, Hangartner L et al. Natural IgE production in the absence of MHC class II cognate help. Immunity 2006; 24: 329-339.
67. Bryce PJ, Miller ML, Miyajima I, Tsai M, Galli SJ, Oettgen HC. Immune sensitization in the skin is enhanced by antigen-independent effects of IgE. Immunity 2004; 20: 381-392.
68. Asai K, Kitaura J, Kawakami Y, Yamagata N, Tsai M, Carbone DP et al. Regulation of mast cell survival by IgE. Immunity 2001; 14: 791-800.
69. Kalesnikoff J, Huber M, Lam V, Damen JE, Zhang J, Siraganian RP et al. Monomeric IgE stimulates signaling pathways in mast cells that lead to cytokine production and cell survival. Immunity 2001; 14: 801-811.
70. Kang HS, Blink SE, Chin RK, Lee Y, Kim O, Weinstock J et al. Lymphotoxin is required for maintaining physiological levels of serum IgE that minimizes Th1-mediated airway inflammation. J Exp Med 2003; 198: 1643-1652.
71. Buckley RH. Primary immunodeficiency diseases: dissection of the immune system. Immunol Rev 2002; 185: 206-219.
72. Villa A, Santagata S, Bozzi F, Giliani S, Frattini A, Imberti L et al. Partial V(D)J recombination activity leads to Omenn syndrome. Cell 1998; 93: 885-896.
73. Ochs HD. The Wiscott-Aldrich syndrome. Clin Rev Allergy Immunol 2001; 20: 61-86.
74. Buckley RH. The hyper-IgE syndrome. Clin Rev Allergy Immunol 2001; 20: 139-154.
75. Ito K, Ogita T, Suko M, Mori M, Kudo K, Hayakawa T et al. IgE levels in nude mice. Int Arch Allergy Appl Immunol 1979; 58: 474-476.
76. Savelkoul HF, van den Akker TW, Soeting PW, van Oudenaren A, Benner R. Modulation of total IgE levels in serum of normal and athymic nude BALB/c mice by T cells and exogenous antigenic stimulation. Int Arch Allergy Appl Immunol 1989; 89: 113-119.
77. Aguado E, Richelme S, Nunez-Cruz S, Miazek A, Mura AM, Richelme M et al. Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science 2002; 296: 2036-2040.
78. Parravicini V, Field AC, Tomlinson PD, Basson MA, Zamoyska R. Itch-/-alphabeta and gammadelta T cells independently contribute to autoimmunity in Itchy mice. Blood 2008; 111: 4273-4282.