Functions of skin-resident γδ T cells

Cellular and Molecular Life Sciences

Volumn 68, Issue 14, 2011, Pages 2399-2408

  MacLeod, Amanda S ^a   Havran, Wendy L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

T cells; DETC; Homeostasis; Inflammation; Skin tumors; Wound healing

Indexed keywords

ADAPTOR PROTEIN; FIBROBLAST GROWTH FACTOR 10; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 1ALPHA; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 7; KERATINOCYTE GROWTH FACTOR; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; LYMPHOTACTIN; LYMPHOTOXIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; PROTEIN DAP10; RANTES; SOMATOMEDIN C; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; APOPTOSIS; CELL COMMUNICATION; CELL INTERACTION; CELL MATURATION; CELL SURVIVAL; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DELAYED HYPERSENSITIVITY; DENDRITIC CELL; DENDRITIC EPIDERMAL T LYMPHOCYTE; DOWN REGULATION; EPIDERMIS; GAMMA DELTA T LYMPHOCYTE; GRAFT VERSUS HOST REACTION; HOMEOSTASIS; HUMAN; KERATINOCYTE; LANGERHANS CELL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MELANOMA; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; REVIEW; SKIN CANCER; SKIN INFLAMMATION; SKIN TUMOR; SQUAMOUS CELL CARCINOMA; STAPHYLOCOCCUS INFECTION; TISSUE DISTRIBUTION; TUMOR IMMUNITY; UPREGULATION; WOUND HEALING;

ANIMALS; CELL COMMUNICATION; HOMEOSTASIS; KERATINOCYTES; LANGERHANS CELLS; MICE; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SKIN; T-LYMPHOCYTES;

ANIMALIA; MURINAE;

EID: 79960933117     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0702-x     Document Type: Review

References (83)

1. Asarnow DM, Goodman T, LeFrancois L, Allison JP (1989) Distinct antigen receptor repertoires of two classes of murine epithelium-associated T cells. Nature 341:60-62 (Pubitemid 19220657)
2. Havran WL, Grell S, Duwe G, Kimura J, Wilson A, Kruisbeek AM, O'Brien RL, Born W, Tigelaar RE, Allison JP (1989) Limited diversity of T-cell receptor γ-chain expression of murine Thy-1+ dendritic epidermal cells revealed by Vγ3-specific monoclonal antibody. Proc Natl Acad Sci USA 86:4185-4189 (Pubitemid 19154759)
3. Asarnow DM, Kuziel WA, Bonyhadi M, Tigelaar RE, Tucker PW, Allison JP (1988) Limited diversity of γδ antigen receptor genes of Thy-1+ dendritic epidermal cells. Cell 55:837-847
4. Havran WL, Allison JP (1988) Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature 335:443-445
5. Itohara S, Farr AG, Lafaille JJ, Bonneville M, Takagaki Y, Haas W, Tonegawa S (1990) Homing of a γδ thymocyte subset with homogeneous T-cell receptors to mucosal epithelia. Nature 343:754-757
6. Xiong N, Baker JE, Kang C, Raulet DH (2004) The genomic arrangement of T cell receptor variable genes is a determinant of the developmental rearrangement pattern. Proc Natl Acad Sci USA 101:260-265 (Pubitemid 38084238)
7. Uche UN, Huber CR, Raulet DH, Xiong N (2009) Recombination signal sequence-associated restriction on TCRd gene rearrangement affects the development of tissue-specific γδ T cells. J Immunol 183:4931-4939
8. Xiong N, Raulet DH (2007) Development and selection of γδ T cells. Immunol Rev 215:15-31
9. Xiong N, Zhang L, Kang C, Raulet DH (2008) Gene placement and competition control T cell receptor γ variable region gene rearrangement. J Exp Med 205:929-938 (Pubitemid 351549888)
10. Leclercq G, Plum J, Nandi D, De Smedt M, Allison JP (1993) Intrathymic differentiation of Vγ3 T cells. J Exp Med 178:309-315
11. Xiong N, Kang C, Raulet DH (2004) Positive selection of dendritic epidermal γδ T cell precursors in the fetal thymus determines expression of skin-homing receptors. Immunity 21:121-131
12. Boyden LM, Lewis JM, Barbee SD, Bas A, Girardi M, Hayday AC, Tigelaar RE, Lifton RP (2008) Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal γδ T cells. Nat Genet 40:656-662 (Pubitemid 351601202)
13. Sharp LL, Jameson JM, Witherden DA, Komori HK, Havran WL (2005) Dendritic epidermal T-cell activation. Crit Rev Immunol 25:1-18
14. Ye SK, Maki K, Lee HC, Ito A, Kawai K, Suzuki H, Mak TW, Chien Y, Honjo T, Ikuta K (2001) Differential roles of cytokine receptors in the development of epidermal γδ T cells. J Immunol 167:1929-1934 (Pubitemid 32747497)
15. Ye SK, Agata Y, Lee HC, Kurooka H, Kitamura T, Shimizu A, Honjo T, Ikuta K (2001) The IL-7 receptor controls the accessibility of the TCRγ locus by Stat5 and histone acetylation. Immunity 15:813-823 (Pubitemid 34008508)
16. Kang J, DiBenedetto B, Narayan K, Zhao H, Der SD, Chambers CA (2004) STAT5 is required for thymopoiesis in a development stage-specific manner. J Immunol 173:2307-2314
17. Jiang X, Campbell JJ, Kupper TS (2010) Embryonic trafficking of γδ T cells to skin is dependent on E/P selectin ligands and CCR4. Proc Natl Acad Sci USA 107:7443-7448
18. Jin Y, Xia M, Sun A, Saylor CM, Xiong N (2010) CCR10 is important for the development of skin-specific γδ T cells by regulating their migration and location. J Immunol 185:5723-5731
19. Lee P, Lee DJ, Chan C, Chen SW, Ch'en I, Jamora C (2009) Dynamic expression of epidermal caspase 8 simulates a wound healing response. Nature 458:519-523
20. Jameson JM, Sharp LL, Witherden DA, Havran WL (2004) Regulation of skin cell homeostasis by γδ T cells. Front Biosci 9:2640-2651
21. Sharp LL, Jameson JM, Cauvi G, Havran WL (2005) Dendritic epidermal T cells regulate skin homeostasis through local production of insulin-like growth factor 1. Nat Immunol 6:73-79 (Pubitemid 40136698)
22. Edmondson SR, Thumiger SP, Werther GA, Wraight CJ (2003) Epidermal homeostasis: the role of the growth hormone and insulin-like growth factor systems. Endocr Rev 24:737-764 (Pubitemid 38067697)
23. Su HY, Cheng WT, Chen SC, Lin CT, Lien YY, Liu HJ, Gilmour RS (2004) Mouse keratinocytes express c98, a novel gene homologous to bcl-2, that is stimulated by insulin-like growth factor 1 and prevents dexamethasone-induced apoptosis. Biochim Biophys Acta 1676:127-137 (Pubitemid 38121463)
24. Matsue H, Cruz PD Jr, Bergstresser PR, Takashima A (1993) Profiles of cytokine mRNA expressed by dendritic epidermal T cells in mice. J Invest Dermatol 101:537-542 (Pubitemid 23285849)
25. Boismenu R, Feng L, Xia YY, Chang JC, Havran WL (1996) Chemokine expression by intraepithelial γδ T cells. Implications for the recruitment of inflammatory cells to damaged epithelia. J Immunol 157:985-992
26. Jameson JM, Cauvi G, Sharp LL, Witherden DA, Havran WL (2005) γδ T cell-induced hyaluronan production by epithelial cells regulates inflammation. J Exp Med 201:1269-1279 (Pubitemid 40629070)
27. Taylor KR, Mills RE, Costanzo AE, Jameson JM (2010) γδ T cells are reduced and rendered unresponsive by hyperglycemia and chronic TNFα in mouse models of obesity and metabolic disease. PLoS One 5(7):e11422
28. Wang T, Scully E, Yin Z, Kim JH, Wang S, Yan J, Mamula M, Anderson JF, Craft J, Fikrig E (2003) IFN-c-producing γδ T cells help control murine West Nile virus infection. J Immunol 171:2524-2531 (Pubitemid 37025562)
29. Shibata K, Yamada H, Hara H, Kishihara K, Yoshikai Y (2007) Resident Vd1? γδ T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J Immunol 178:4466-4472 (Pubitemid 46492398)
30. Gao Y, Yang W, Pan M, Scully E, Girardi M, Augenlicht LH, Craft J, Yin Z (2003) γδ T cells provide an early source of interferon γ in tumor immunity. J Exp Med 198:433-442 (Pubitemid 36976054)
31. Cho JS, Pietras EM, Garcia NC, Ramos RI, Farzam DM, Monroe HR, Magorien JE, Blauvelt A, Kolls JK, Cheung AL, Cheng G, Modlin RL, Miller LS (2010) IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J Clin Invest 120(5):1762-1773
32. Molne L, Corthay A, Holmdahl R, Tarkowski A (2003) Role of γδ T cell receptor-expressing lymphocytes in cutaneous infection caused by Staphylococcus aureus. Clin Exp Immunol 132:209-215
33. Leclercq G, Plum J (1995) Stimulation of TCR Vγ3 cells by gram-negative bacteria. J Immunol 154:5313-5319
34. Martin B, Hirota K, Cua DJ, 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
35. Shimura H, Nitahara A, Ito A, Tomiyama K, Ito M, Kawai K (2005) Up-regulation of cell surface Toll-like receptor 4-MD2 expression on dendritic epidermal T cells after the emigration from epidermis during cutaneous inflammation. J Dermatol Sci 37:101-110 (Pubitemid 40126828)
36. Ptak W, Askenase PW (1992) γδ T cells assist αβ T cells in adoptive transfer of contact sensitivity. J Immunol 149:3503-3508
37. Szczepanik M, Lewis J, Geba GP, Ptak W, Askenase PW (1998) Positive regulatory γδ T cells in contact sensitivity: augmented responses by in vivo treatment with anti-γδ monoclonal antibody, or anti-Vγ5 or Vd4. Immunol Invest 27:1-15 (Pubitemid 28193280)
38. Szczepanik M, Nowak B, Askenase PW, Ptak W (1998) Crosstalk between γδ T lymphocytes and immune cells in humoral response. Immunology 95:612-617
39. Ushio H, Tsuji RF, Szczepanik M, Kawamoto K, Matsuda H, Askenase PW (1998) IL-12 reverses established antigen-specific tolerance of contact sensitivity by affecting costimulatory molecules B7-1 (CD80) and B7-2 (CD86). J Immunol 160:2080-2088 (Pubitemid 28119885)
40. Dieli F, Asherson GL, Sireci G, Dominici R, Gervasi F, Vendetti S, Colizzi V, Salerno A (1997) γδ cells involved in contact sensitivity preferentially rearrange the Vc3 region and require interleukin-7. Eur J Immunol 27:206-214 (Pubitemid 27046080)
41. Dieli F, Ptak W, Sireci G, Romano GC, Potestio M, Salerno A, Asherson GL (1998) Cross-talk between Vβ8+ and γδ+ T lymphocytes in contact sensitivity. Immunology 93:469-477
42. Girardi M, Lewis J, Glusac E, Filler RB, Geng L, Hayday AC, Tigelaar RE (2002) Resident skin-specific γδ T cells provide local, nonredundant regulation of cutaneous inflammation. J Exp Med 195:855-867 (Pubitemid 34286757)
43. Lewis JM, Girardi M, Roberts SJ, Barbee SD, Hayday AC, Tigelaar RE (2006) Selection of the cutaneous intraepithelial γδ+ T cell repertoire by a thymic stromal determinant. Nat Immunol 7:843-850 (Pubitemid 44084091)
44. Marcinkiewicz J, Bereta M, Malinowski J, Ptak W (1984) The induction of oxazolone-specific T suppressor afferent cells in mice by hapten-modified isologous IgG. Eur J Immunol 14:759-762 (Pubitemid 14064146)
45. Rosenstein RW, Murray JH, Cone RE, Ptak W, Iverson GM, Gershon RK (1981) Isolation and partial characterization of an antigen-specific T-cell factor associated with the suppression of delayed type hypersensitivity. Proc Natl Acad Sci USA 78:5821-5825 (Pubitemid 12204452)
46. Szczepanik M, Anderson LR, Ushio H, Ptak W, Owen MJ, Hayday AC, Askenase PW (1996) γδ T cells from tolerized αβ T cell receptor (TCR)-deficient mice inhibit contact sensitivity-effector T cells in vivo, and their interferon-c production in vitro. J Exp Med 184:2129-2139
47. McMenamin C, Pimm C, McKersey M, Holt PG (1994) Regulation of IgE responses to inhaled antigen in mice by antigen-specific γδ T cells. Science 265:1869-1871 (Pubitemid 24324243)
48. Shiohara T, Moriya N, Gotoh C, Hayakawa J, Nagashima M, Saizawa K, Ishikawa H (1990) Loss of epidermal integrity by T cell-mediated attack induces long-term local resistance to subsequent attack. I. Induction of resistance correlates with increases in Thy-1+ epidermal cell numbers. J Exp Med 171:1027-1041 (Pubitemid 20120131)
49. Shiohara T, Moriya N, Hayakawa J, Itohara S, Ishikawa H (1996) Resistance to cutaneous graft-vs.-host disease is not induced in T cell receptor δ gene-mutant mice. J Exp Med 183:1483-1489 (Pubitemid 26134291)
50. Kaminski MJ, Cruz PD Jr, Bergstresser PR, Takashima A (1993) Killing of skin-derived tumor cells by mouse dendritic epidermal T-cells. Cancer Res 53:4014-4019 (Pubitemid 23267704)
51. Girardi M, Oppenheim DE, Steele CR, Lewis JM, Glusac E, Filler R, Hobby P, Sutton B, Tigelaar RE, Hayday AC (2001) Regulation of cutaneous malignancy by γδ T cells. Science 294:605-609
52. Oppenheim DE, Roberts SJ, Clarke SL, Filler R, Lewis JM, Tigelaar RE, Girardi M, Hayday AC (2005) Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 6:928-937 (Pubitemid 43090448)
53. Champsaur M, Lanier LL (2010) Effect of NKG2D ligand expression on host immune responses. Immunol Rev 235:267-285
54. Whang MI, Guerra N, Raulet DH (2009) Costimulation of dendritic epidermal γδ T cells by a new NKG2D ligand expressed specifically in the skin. J Immunol 182:4557-4564
55. Nitahara A, Shimura H, Ito A, Tomiyama K, Ito M, Kawai K (2006) NKG2D ligation without T cell receptor engagement triggers both cytotoxicity and cytokine production in dendritic epidermal T cells. J Invest Dermatol 126:1052-1058
56. Diefenbach A, Tomasello E, Lucas M, Jamieson AM, Hsia JK, Vivier E, Raulet DH (2002) Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat Immunol 3:1142-1149 (Pubitemid 35469698)
57. Gilfillan S, Ho EL, Cella M, Yokoyama WM, Colonna M (2002) NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat Immunol 3:1150-1155 (Pubitemid 35469699)
58. Rosen DB, Araki M, Hamerman JA, Chen T, Yamamura T, Lanier LL (2004) A structural basis for the association of DAP12 with mouse, but not human, NKG2D. J Immunol 173:2470-2478 (Pubitemid 39063104)
59. Zompi S, Hamerman JA, Ogasawara K, Schweighoffer E, Tybulewicz VL, Di Santo JP, Lanier LL, Colucci F (2003) NKG2D triggers cytotoxicity in mouse NK cells lacking DAP12 or Syk family kinases. Nat Immunol 4:565-572 (Pubitemid 36701340)
60. Shojaei H, Oberg HH, Juricke M, Marischen L, Kunz M, Mundhenke C, Gieseler F, Kabelitz D, Wesch D (2009) Toll-like receptors 3 and 7 agonists enhance tumor cell lysis by human γδ T cells. Cancer Res 69:8710-8717
61. Krahenbuhl O, Gattesco S, Tschopp J (1992) Murine Thy-1+ dendritic epidermal T cell lines express granule-associated perforin and a family of granzyme molecules. Immunobiology 184:392-401
62. Atkins MB (2006) Cytokine-based therapy and biochemotherapy for advanced melanoma. Clin Cancer Res 12:2353s-2358s
63. Bonmort M, Ullrich E, Mignot G, Jacobs B, Chaput N, Zitvogel L (2007) Interferon-c is produced by another player of innate immune responses: the interferon-producing killer dendritic cell (IKDC). Biochimie 89:872-877 (Pubitemid 47001644)
64. Murugaiyan G, Saha B (2009) Protumor vs. antitumor functions of IL-17. J Immunol 183:4169-4175
65. Baum CL, Arpey CJ (2005) Normal cutaneous wound healing: clinical correlation with cellular and molecular events. Dermatol Surg 31, 674-86 (discussion 686)
66. Gailit J, Clark RA (1994) Wound repair in the context of extracellular matrix. Curr Opin Cell Biol 6:717-725 (Pubitemid 24295306)
67. Strecker-McGraw MK, Jones TR, Baer DG (2007) Soft tissue wounds and principles of healing. Emerg Med Clin North Am 25:1-22 (Pubitemid 46505320)
68. Diegelmann RF, Evans MC (2004) Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci 9:283-289 (Pubitemid 38925460)
69. Izadi K, Ganchi P (2005) Chronic wounds. Clin Plast Surg 32:209-222 (Pubitemid 40462276)
70. Phillips TJ (1994) Chronic cutaneous ulcers: etiology and epidemiology. J Invest Dermatol 102:38S-41S
71. Wolfe RA, Roi LD, Flora JD, Feller I, Cornell RG (1983) Mortality differences and speed of wound closure among specialized burn care facilities. JAMA 250:763-766 (Pubitemid 13039566)
72. Rubin JS, Osada H, Finch PW, Taylor WG, Rudikoff S, Aaronson SA (1989) Purification and characterization of a newly identified growth factor specific for epithelial cells. Proc Natl Acad Sci USA 86:802-806 (Pubitemid 19056244)
73. Werner S, Peters KG, Longaker MT, Fuller-Pace F, Banda MJ, Williams LT (1992) Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc Natl Acad Sci USA 89:6896-6900
74. Finch PW, Rubin JS, Miki T, Ron D, Aaronson SA (1989) Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science 245:752-755 (Pubitemid 19214010)
75. Staiano-Coico L, Krueger JG, Rubin JS, D'Limi S, Vallat VP, Valentino L, Fahey T 3rd, Hawes A, Kingston G, Madden MR et al (1993) Human keratinocyte growth factor effects in a porcine model of epidermal wound healing. J Exp Med 178:865-878 (Pubitemid 23260424)
76. Jameson J, Ugarte K, Chen N, Yachi P, Fuchs E, Boismenu R, Havran WL (2002) A role for skin γδ T cells in wound repair. Science 296:747-749
77. Jameson JM, Cauvi G, Witherden DA, Havran WL (2004) A keratinocyte-responsive γδ TCR is necessary for dendritic epidermal T cell activation by damaged keratinocytes and maintenance in the epidermis. J Immunol 172:3573-3579 (Pubitemid 38337938)
78. Havran WL, Chien YH, Allison JP (1991) Recognition of self antigens by skin-derived T cells with invariant γδ antigen receptors. Science 252:1430-1432 (Pubitemid 21917062)
79. Witherden DA, Verdino P, Rieder SE, Garijo O, Mills RE, Teyton L, Fischer WH, Wilson IA, Havran WL (2010) The junctional adhesion molecule JAML is a costimulatory receptor for epithelial γδ T cell activation. Science 329:1205-1210
80. Verdino P, Witherden DA, Havran WL, Wilson IA (2010) The molecular interaction of CAR and JAML recruits the central cell signal transducer PI3 K. Science 329(5996):1210-1214
81. Morita CT, Parker CM, Brenner MB, Band H (1994) TCR usage and functional capabilities of human γδ T cells at birth. J Immunol 153:3979-3988 (Pubitemid 24322565)
82. Trejdosiewicz LK, Smart CJ, Oakes DJ, Howdle PD, Malizia G, Campana D, Boylston AW (1989) Expression of T-cell receptors TcR1 (γδ) and TcR2 (αβ) in the human intestinal mucosa. Immunology 68:7-12 (Pubitemid 19236061)
83. Toulon A, Breton L, Taylor KR, Tenenhaus M, Bhavsar D, Lanigan C, Rudolph R, Jameson J, Havran WL (2009) A role for human skin-resident T cells in wound healing. J Exp Med 206:743-750