Cross-talk between intraepithelial γδ T cells and epithelial cells

Journal of Leukocyte Biology

Volumn 94, Issue 1, 2013, Pages 69-76

  Witherden, Deborah A ^a   Havran, Wendy L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Dendritic epidermal T cells; Epithelium; Lymphocytes; Wound repair

Indexed keywords

CHEMOKINE; GLYCOSAMINOGLYCAN; GROWTH FACTOR;

ARTICLE; CELL COMMUNICATION; CELL CONTACT; CELL INTERACTION; CYTOKINE PRODUCTION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GAMMA DELTA T LYMPHOCYTE; HOMEOSTASIS; HUMAN; INFLAMMATION; LYMPHOCYTE FUNCTION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION; TISSUE REPAIR; TUMOR REJECTION; WOUND HEALING;

DENDRITIC EPIDERMAL T CELLS; EPITHELIUM; LYMPHOCYTES; WOUND REPAIR;

ANIMALS; CELL COMMUNICATION; EPITHELIAL CELLS; HUMANS; LYMPHOCYTES; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA;

EID: 84879569338     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0213101     Document Type: Article

References (87)

1. Allison, J. P., Havran, W. L. (1991) The immunobiology of T cells with invariant γδ antigen receptors. Annu. Rev. Immunol. 9, 679-705.
2. Chen, Y., Chou, K., Fuchs, E., Havran, W. L., Boismenu, R. (2002) Protection of the intestinal mucosa by intraepithelial γδ T cells. Proc. Natl. Acad. Sci. USA 99, 14338-14343.
3. Girardi, M., Oppenheim, D. E., Steele, C. R., Lewis, J. M., Glusac, E., Filler, R., Hobby, P., Sutton, B., Tigelaar, R. E., Hayday, A. C. (2001) Regulation of cutaneous malignancy by γδ T cells. Science 294, 605-609.
4. Jameson, J., Ugarte, K., Chen, N., Yachi, P., Fuchs, E., Boismenu, R., Havran, W. L. (2002) A role for skin γδ T cells in wound repair. Science 296, 747-749.
5. King, D. P., Hyde, D. M., Jackson, K. A., Novosad, D. M., Ellis, T. N., Putney, L., Stovall, M. Y., Van Winkle, L. S., Beaman, B. L., Ferrick, D. A. (1999) Cutting edge: protective response to pulmonary injury requires γδ T lymphocytes. J. Immunol. 162, 5033-5036.
6. Sharp, L. L., Jameson, J. M., Cauvi, G., Havran, W. L. (2005) Dendritic epidermal T cells regulate skin homeostasis through local production of insulin-like growth factor 1. Nat. Immunol. 6, 73-79.
7. Boyden, L. M., Lewis, J. M., Barbee, S. D., Bas, A., Girardi, M., Hayday, A. C., Tigelaar, R. E., Lifton, R. P. (2008) Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal γδ T cells. Nat. Genet. 40, 656-662.
8. Garman, R. D., Doherty, P. J., Raulet, D. H. (1986) Diversity, rearrangement, and expression of murine T cell γ genes. Cell 45, 733-742.
9. Lewis, J. M., Girardi, M., Roberts, S. J., Barbee, S. D., Hayday, A. C., Tigelaar, R. E. (2006) Selection of the cutaneous intraepithelial γδ+ T cell repertoire by a thymic stromal determinant. Nat. Immunol. 7, 843-850.
10. Turchinovich, G., Hayday, A. C. (2011) Skint-1 identifies a common molecular mechanism for the development of interferon-γ-secreting versus interleukin-17-secreting γδ T cells. Immunity 35, 59-68.
11. Meyer, C., Zeng, X., Chien, Y. H. (2010) Ligand recognition during thymic development and γδ T cell function specification. Semin. Immunol. 22, 207-213.
12. Haks, M. C., Lefebvre, J. M., Lauritsen, J. P., Carleton, M., Rhodes, M., Miyazaki, T., Kappes, D. J., Wiest, D. L. (2005) Attenuation of γδ TCR signaling efficiently diverts thymocytes to the γδ lineage. Immunity 22, 595-06.
13. Jensen, K. D., Shin, S., Chien, Y. H. (2009) Cutting edge: γδ intraepithelial lymphocytes of the small intestine are not biased toward thymic antigens. J. Immunol. 182, 7348-7351.
14. Leclercq, G., Plum, J., Nandi, D., De Smedt, M., Allison, J. P. (1993) Intrathymic differentiation of Vγ3 T cells. J. Exp. Med. 178, 309-315.
15. Jin, Y., Xia, M., Sun, A., Saylor, C. M., 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.
16. Hu, S., Xiong, N. (2013) Programmed downregulation of CCR6 is important for establishment of epidermal γδT cells by regulating their thymic egress and epidermal location. J. Immunol. 190, 3267-3275.
17. Jameson, J., Havran, W. L. (2007) Skin γδ T-cell functions in homeostasis and wound healing. Immunol. Rev. 215, 114-122.
18. Inagaki-Ohara, K., Chinen, T., Matsuzaki, G., Sasaki, A., Sakamoto, Y., Hiromatsu, K., Nakamura-Uchiyama, F., Nawa, Y., Yoshimura, A. (2004) Mucosal T cells bearing TCRγδ play a protective role in intestinal inflammation. J. Immunol. 173, 1390-1398.
19. Ismail, A. S., Behrendt, C. L., Hooper, L. V. (2009) Reciprocal interactions between commensal bacteria and γδ intraepithelial lymphocytes during mucosal injury. J. Immunol. 182, 3047-3054.
20. Ismail, A. S., Severson, K. M., Vaishnava, S., Behrendt, C. L., Yu, X., Benjamin, J. L., Ruhn, K. A., Hou, B., DeFranco, A. L., Yarovinsky, F., Hooper, L. V. (2011) γδ Intraepithelial lymphocytes are essential mediators of host-microbial homeostasis at the intestinal mucosal surface. Proc. Natl. Acad. Sci. USA 108, 8743-8748.
21. Edelblum, K. L., Shen, L., Weber, C. R., Marchiando, A. M., Clay, B. S., Wang, Y., Prinz, I., Malissen, B., Sperling, A. I., Turner, J. R. (2012) Dynamic migration of γδ intraepithelial lymphocytes requires occludin. Proc. Natl. Acad. Sci. USA 109, 7097-7102.
22. Wands, J. M., Roark, C. L., Aydintug, M. K., Jin, N., Hahn, Y. S., Cook, L., Yin, X., Dal Porto, J., Lahn, M., Hyde, D. M., Gelfand, E. W., Mason, R. J., O'Brien, R. L., Born, W. K. (2005) Distribution and leukocyte contacts of γδ T cells in the lung. J. Leukoc. Biol. 78, 1086-1096.
23. Born, W., Cady, C., Jones-Carson, J., Mukasa, A., Lahn, M., O'Brien, R. (1999) Immunoregulatory functions of γδ T cells. Adv. Immunol. 71, 77-144.
24. Born, W. K., Lahn, M., Takeda, K., Kanehiro, A., O'Brien, R. L., Gelfand, E. W. (2000) Role of γδ T cells in protecting normal airway function. Respir. Res. 1, 151-158.
25. +γδ T cells regulate airway hyperreactivity to methacholine in ovalbumin-sensitized and challenged mice. J. Immunol. 171, 3170-3178.
26. Lahn, M., Kanehiro, A., Takeda, K., Konowal, A., O'Brien, R. L., Gelfand, E. W., Born, W. K. (2001) γδ T cells as regulators of airway hyperresponsiveness. Int. Arch. Allergy Immunol. 125, 203-210.
27. Hayday, A., Theodoridis, E., Ramsburg, E., Shires, J. (2001) Intraepithelial lymphocytes: exploring the third way in immunology. Nat. Immunol. 2, 997-1003.
28. Mallick-Wood, C. A., Lewis, J. M., Richie, L. I., Owen, M. J., Tigelaar, R. E., Hayday, A. C. (1998) Conservation of T cell receptor conformation in epidermal γδ cells with disrupted primary Vγ gene usage. Science 279, 1729-1733.
29. Jameson, J. M., Cauvi, G., Witherden, D. A., Havran, W. L. (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.
30. Komori, H. K., Witherden, D. A., Kelly, R., Sendaydiego, K., Jameson, J. M., Teyton, L., Havran, W. L. (2012) Cutting edge: dendritic epidermal γδ T cell ligands are rapidly and locally expressed by keratinocytes following cutaneous wounding. J. Immunol. 188, 2972-2976.
31. Jameson, J. M., Cauvi, G., Sharp, L. L., Witherden, D. A., Havran, W. L. (2005) γδ T cell-induced hyaluronan production by epithelial cells regulates inflammation. J. Exp. Med. 201, 1269-1279.
32. Karvinen, S., Pasonen-Seppanen, S., Hyttinen, J. M., Pienimaki, J. P., Torronen, K., Jokela, T. A., Tammi, M. I., Tammi, R. (2003) Keratinocyte growth factor stimulates migration and hyaluronan synthesis in the epidermis by activation of keratinocyte hyaluronan synthases 2 and 3. J. Biol. Chem. 278, 49495-49504.
33. Chodaczek, G., Papanna, V., Zal, M. A., Zal, T. (2012) Body-barrier surveillance by epidermal γδ TCRs. Nat. Immunol. 13, 272-282.
34. Hayday, A., Tigelaar, R. (2012) Casting new light on the TCR. Nat. Immunol. 13, 209-211.
35. Moog-Lutz, C., Cave-Riant, F., Guibal, F. C., Breau, M. A., Di Gioia, Y., Couraud, P. O., Cayre, Y. E., Bourdoulous, S., Lutz, P. G. (2003) JAML, a novel protein with characteristics of a junctional adhesion molecule, is induced during differentiation of myeloid leukemia cells. Blood 102, 3371-3378.
36. Luissint, A. C., Lutz, P. G., Calderwood, D. A., Couraud, P. O., Bourdoulous, S. (2008) JAM-L-mediated leukocyte adhesion to endothelial cells is regulated in cis by α4β1 integrin activation. J. Cell Biol. 183, 1159-1173.
37. Zen, K., Liu, Y., McCall, I. C., Wu, T., Lee, W., Babbin, B. A., Nusrat, A., Parkos, C. A. (2005) Neutrophil migration across tight junctions is mediated by adhesive interactions between epithelial coxsackie and adenovirus receptor and a junctional adhesion molecule-like protein on neutrophils. Mol. Biol. Cell 16, 2694-2703.
38. Witherden, D. A., Verdino, P., Rieder, S. E., Garijo, O., Mills, R. E., Teyton, L., Fischer, W. H., Wilson, I. A., Havran, W. L. (2010) The junctional adhesion molecule JAML is a costimulatory receptor for epithelial γδ T cell activation. Science 329, 1205-1210.
39. Bergelson, J. M., Cunningham, J. A., Droguett, G., Kurt-Jones, E. A., Krithivas, A., Hong, J. S., Horwitz, M. S., Crowell, R. L., Finberg, R. W. (1997) Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275, 1320-1323.
40. Verdino, P., Witherden, D. A., Havran, W. L., Wilson, I. A. (2010) The molecular interaction of CAR and JAML recruits the central cell signal transducer PI3K. Science 329, 1210-1214.
41. Rudd, C. E., Schneider, H. (2003) Unifying concepts in CD28, ICOS and CTLA4 co-receptor signalling. Nat. Rev. Immunol. 3, 544-556.
42. Bauer, S., Groh, V., Wu, J., Steinle, A., Phillips, J. H., Lanier, L. L., Spies, T. (1999) Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285, 727-729.
43. Jamieson, A. M., Diefenbach, A., McMahon, C. W., Xiong, N., Carlyle, J. R., Raulet, D. H. (2002) The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17, 19-29.
44. Raulet, D. H. (2003) Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3, 781-790.
45. Zafirova, B., Wensveen, F. M., Gulin, M., Polic, B. (2011) Regulation of immune cell function and differentiation by the NKG2D receptor. Cell. Mol. Life Sci. 68, 3519-3529.
46. Coudert, J. D., Held, W. (2006) The role of the NKG2D receptor for tumor immunity. Semin. Cancer Biol. 16, 333-343.
47. Lodoen, M. B., Lanier, L. L. (2006) Natural killer cells as an initial defense against pathogens. Curr. Opin. Immunol. 18, 391-398.
48. Champsaur, M., Lanier, L. L. (2010) Effect of NKG2D ligand expression on host immune responses. Immunol. Rev. 235, 267-285.
49. Eagle, R. A., Trowsdale, J. (2007) Promiscuity and the single receptor: NKG2D. Nat. Rev. Immunol. 7, 737-744.
50. Whang, M. I., Guerra, N., Raulet, D. H. (2009) Costimulation of dendritic epidermal γδ T cells by a new NKG2D ligand expressed specifically in the skin. J. Immunol. 182, 4557-4564.
51. Yoshida, S., Mohamed, R. H., Kajikawa, M., Koizumi, J., Tanaka, M., Fugo, K., Otsuka, N., Maenaka, K., Yagita, H., Chiba, H., Kasahara, M. (2012) Involvement of an NKG2D ligand H60c in epidermal dendritic T cell-mediated wound repair. J. Immunol. 188, 3972-3979.
52. 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.
53. Strid, J., Roberts, S. J., Filler, R. B., Lewis, J. M., Kwong, B. Y., Schpero, W., Kaplan, D. H., Hayday, A. C., Girardi, M. (2008) Acute upregulation of an NKG2D ligand promotes rapid reorganization of a local immune compartment with pleiotropic effects on carcinogenesis. Nat. Immunol. 9, 146-154.
54. Das, H., Groh, V., Kuijl, C., Sugita, M., Morita, C. T., Spies, T., Bukowski, J. F. (2001) MICA engagement by human Vγ2Vδ2 T cells enhances their antigen-dependent effector function. Immunity 15, 83-93.
55. Groh, V., Rhinehart, R., Secrist, H., Bauer, S., Grabstein, K. H., Spies, T. (1999) Broad tumor-associated expression and recognition by tumorderived γδ T cells of MICA and MICB. Proc. Natl. Acad. Sci. USA 96, 6879-6884.
56. Groh, V., Steinle, A., Bauer, S., Spies, T. (1998) Recognition of stressinduced MHC molecules by intestinal epithelial γδ T cells. Science 279, 1737-1740.
57. Xu, B., Pizarro, J. C., Holmes, M. A., McBeth, C., Groh, V., Spies, T., Strong, R. K. (2011) Crystal structure of a γδ T-cell receptor specific for the human MHC class I homolog MICA. Proc. Natl. Acad. Sci. USA 108, 2414-2419.
58. Hall, K. T., Boumsell, L., Schultze, J. L., Boussiotis, V. A., Dorfman, D. M., Cardoso, A. A., Bensussan, A., Nadler, L. M., Freeman, G. J. (1996) Human CD100, a novel leukocyte semaphorin that promotes Bcell aggregation and differentiation. Proc. Natl. Acad. Sci. USA 93, 11780-11785.
59. Kumanogoh, A., Watanabe, C., Lee, I., Wang, X., Shi, W., Araki, H., Hirata, H., Iwahori, K., Uchida, J., Yasui, T., Matsumoto, M., Yoshida, K., Yakura, H., Pan, C., Parnes, J. R., Kikutani, H. (2000) Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling. Immunity 13, 621-631.
60. Masuda, K., Furuyama, T., Takahara, M., Fujioka, S., Kurinami, H., Inagaki, S. (2004) Sema4D stimulates axonal outgrowth of embryonic DRG sensory neurones. Genes Cells 9, 821-829.
61. Tamagnone, L., Artigiani, S., Chen, H., He, Z., Ming, G. I., Song, H., Chedotal, A., Winberg, M. L., Goodman, C. S., Poo, M., Tessier-Lavigne, M., Comoglio, P. M. (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99, 71-80.
62. Kruger, R. P., Aurandt, J., Guan, K. L. (2005) Semaphorins command cells to move. Nat. Rev. Mol. Cell. Biol. 6, 789-800.
63. Kumanogoh, A., Kikutani, H. (2004) Biological functions and signaling of a transmembrane semaphorin, CD100/Sema4D. Cell. Mol. Life Sci. 61, 292-300.
64. Bougeret, C., Mansur, I. G., Dastot, H., Schmid, M., Mahouy, G., Bensussan, A., Boumsell, L. (1992) Increased surface expression of a newly identified 150-kDa dimer early after human T lymphocyte activation. J. Immunol. 148, 318-323.
65. Shi, W., Kumanogoh, A., Watanabe, C., Uchida, J., Wang, X., Yasui, T., Yukawa, K., Ikawa, M., Okabe, M., Parnes, J. R., Yoshida, K., Kikutani, H. (2000) The class IV semaphorin CD100 plays nonredundant roles in the immune system: defective B and T cell activation in CD100-deficient mice. Immunity 13, 633-642.
66. Witherden, D. A., Watanabe, M., Garijo, O., Rieder, S. E., Sarkisyan, G., Cronin, S. J., Verdino, P., Wilson, I. A., Kumanogoh, A., Kikutani, H., Teyton, L., Fischer, W. H., Havran, W. L. (2012) The CD100 receptor interacts with its plexin B2 ligand to regulate epidermal γδ T cell function. Immunity 37, 314-325.
67. Esser, C., Rannug, A., Stockinger, B. (2009) The aryl hydrocarbon receptor in immunity. Trends Immunol. 30, 447-454.
68. Fernandez-Salguero, P., Pineau, T., Hilbert, D. M., McPhail, T., Lee, S. S., Kimura, S., Nebert, D. W., Rudikoff, S., Ward, J. M., Gonzalez, F. J. (1995) Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268, 722-726.
69. Kadow, S., Jux, B., Zahner, S. P., Wingerath, B., Chmill, S., Clausen, B. E., Hengstler, J., Esser, C. (2011) Aryl hydrocarbon receptor is critical for homeostasis of invariant γδ T cells in the murine epidermis. J. Immunol. 187, 3104-3110.
70. Li, Y., Innocentin, S., Withers, D. R., Roberts, N. A., Gallagher, A. R., Grigorieva, E. F., Wilhelm, C., Veldhoen, M. (2011) Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation. Cell 147, 629-640.
71. Boulter, E., Estrach, S., Errante, A., Pons, C., Cailleteau, L., Tissot, F., Meneguzzi, G., Feral, C. C. (2013) CD98hc (SLC3A2) regulation of skin homeostasis wanes with age. J. Exp. Med. 210, 173-190.
72. Shires, J., Theodoridis, E., Hayday, A. C. (2001) Biological insights into TCRγδ+ and TCRαβ+ intraepithelial lymphocytes provided by serial analysis of gene expression (SAGE). Immunity 15, 419-434.
73. Girardi, M., Sherling, M. A., Filler, R. B., Shires, J., Theodoridis, E., Hayday, A. C., Tigelaar, R. E. (2003) Anti-inflammatory effects in the skin of thymosin-β4 splice-variants. Immunology 109, 1-7.
74. Malinda, K. M., Sidhu, G. S., Mani, H., Banaudha, K., Maheshwari, R. K., Goldstein, A. L., Kleinman, H. K. (1999) Thymosin β4 accelerates wound healing. J. Invest. Dermatol. 113, 364-368.
75. Uchida, Y., Kawai, K., Ibusuki, A., Kanekura, T. (2011) Role for E-cadherin as an inhibitory receptor on epidermal γδ T cells. J. Immunol. 186, 6945-6954.
76. Boismenu, R., Feng, L., Xia, Y. Y., Chang, J. C., Havran, W. L. (1996) Chemokine expression by intraepithelial γδ T cells. Implications for the recruitment of inflammatory cells to damaged epithelia. J. Immunol. 157, 985-992.
77. Matsue, H., Cruz P. D., Jr., Bergstresser, P. R., Takashima, A. (1993) Profiles of cytokine mRNA expressed by dendritic epidermal T cells in mice. J. Invest. Dermatol. 101, 537-542.
78. Taylor, K. R., Mills, R. E., Costanzo, A. E., Jameson, J. M. (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, e11422.
79. Cai, Y., Shen, X., Ding, C., Qi, C., Li, K., Li, X., Jala, V. R., Zhang, H. G., Wang, T., Zheng, J., Yan, J. (2011) Pivotal role of dermal IL-17-producing γδ T cells in skin inflammation. Immunity 35, 596-610.
80. Gray, E. E., Suzuki, K., Cyster, J. G. (2011) Cutting edge: identification of a motile IL-17-producing γδ T cell population in the dermis. J. Immunol. 186, 6091-6095.
81. 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.
82. 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.
83. Cho, J. S., Pietras, E. M., Garcia, N. C., Ramos, R. I., Farzam, D. M., Monroe, H. R., Magorien, J. E., Blauvelt, A., Kolls, J. K., Cheung, A. L., Cheng, G., Modlin, R. L., Miller, L. S. (2010) IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J. Clin. Invest. 120, 1762-1773.
84. Sumaria, N., Roediger, B., Ng, L. G., Qin, J., Pinto, R., Cavanagh, L. L., Shklovskaya, E., Fazekas de St Groth, B., Triccas, J. A., Weninger, W. (2011) Cutaneous immunosurveillance by self-renewing dermal γδ T cells. J. Exp. Med. 208, 505-518.
85. Yang, H., Antony, P. A., Wildhaber, B. E., Teitelbaum, D. H. (2004) Intestinal intraepithelial lymphocyte γδ-T cell-derived keratinocyte growth factor modulates epithelial growth in the mouse. J. Immunol. 172, 4151-4158.
86. Fahrer, A. M., Konigshofer, Y., Kerr, E. M., Ghandour, G., Mack, D. H., Davis, M. M., Chien, Y. H. (2001) Attributes of γδ intraepithelial lymphocytes as suggested by their transcriptional profile. Proc. Natl. Acad. Sci. USA 98, 10261-10266.
87. Gallo, R. L., Hooper, L. V. (2012) Epithelial antimicrobial defence of the skin and intestine. Nat. Rev. Immunol. 12, 503-516.