Skin immune surveillance by T cells-A new order?

Seminars in Immunology

Volumn 21, Issue 3, 2009, Pages 110-120

  Strid, Jessica ^a   Tigelaar, Robert E ^b   Hayday, Adrian C ^a  

^a GUY S HOSPITAL   (United Kingdom)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Immunosurveillance; Intraepithelial lymphocytes; Keratinocytes; NKG2D; T cells

Indexed keywords

ADAPTIVE IMMUNITY; BODY SURFACE; DENDRITIC CELL; EPITHELIUM CELL; HUMAN; IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOLOGY; IMMUNOREGULATION; IMMUNOSTIMULATION; IMMUNOSURVEILLANCE; INFECTION; INNATE IMMUNITY; KERATINOCYTE; LANGERHANS CELL; LYMPHOCYTE; MOLECULAR RECOGNITION; PROTEIN TARGETING; REVIEW; STRESS; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; AUTOANTIGENS; CELL COMMUNICATION; CELL MOVEMENT; CYTOKINES; HUMANS; IMMUNOLOGIC SURVEILLANCE; KERATINOCYTES; LANGERHANS CELLS; LYMPHOCYTE ACTIVATION; SKIN; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTES;

EID: 65749108613     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2009.03.002     Document Type: Review

References (108)

1. Elias P.M. The skin barrier as an innate immune element. Semin Immunopathol 29 April (1) (2007) 3-14
2. Janeway C.A. Janeway's immunobiology. 7th ed. (2007), Taylor & Francis, Inc.
3. Leung D.Y., Boguniewicz M., Howell M.D., Nomura I., and Hamid Q.A. New insights into atopic dermatitis. J Clin Invest 113 March (5) (2004) 651-657
4. van Beelen A.J., Teunissen M.B., Kapsenberg M.L., and de Jong E.C. Interleukin-17 in inflammatory skin disorders. Curr Opin Allergy Clin Immunol 7 October (5) (2007) 374-381
5. Ghoreschi K., Weigert C., and Rocken M. Immunopathogenesis and role of T cells in psoriasis. Clin Dermatol 25 November-December (6) (2007) 574-580
6. Elias P.M., and Menon G.K. Structural and lipid biochemical correlates of the epidermal permeability barrier. Adv Lipid Res 24 (1991) 1-26
7. Roop D. Defects in the barrier. Science 267 January (5197) (1995) 474-475
8. Elias P.M., Crumrine D., Rassner U., et al. Basis for abnormal desquamation and permeability barrier dysfunction in RXLI. J Invest Dermatol 122 February (2) (2004) 314-319
9. Harding C.R. The stratum corneum: structure and function in health and disease. Dermatol Ther 17 Suppl. 1 (2004) 6-15
10. Mihai S., and Sitaru C. Immunopathology and molecular diagnosis of autoimmune bullous diseases. J Cell Mol Med 11 May-June (3) (2007) 462-481
11. McGrath J.A., and Eady R.A. Recent advances in the molecular basis of inherited skin diseases. Adv Genet 43 (2001) 1-32
12. O'Regan G.M., Sandilands A., McLean W.H., and Irvine A.D. Filaggrin in atopic dermatitis. J Allergy Clin Immunol 122 October (4) (2008) 689-693
13. Veal C.D., Capon F., Allen M.H., et al. Family-based analysis using a dense single-nucleotide polymorphism-based map defines genetic variation at PSORS1, the major psoriasis-susceptibility locus. Am J Hum Genet 71 September (3) (2002) 554-564
14. Clark R.A., Chong B., Mirchandani N., et al. The vast majority of CLA+ T cells are resident in normal skin. J Immunol 176 April (7) (2006) 4431-4439
15. Wood L.C., Elias P.M., Calhoun C., Tsai J.C., Grunfeld C., and Feingold K.R. Barrier disruption stimulates interleukin-1 alpha expression and release from a pre-formed pool in murine epidermis. J Invest Dermatol 106 March (3) (1996) 397-403
16. Lamkanfi M., Kanneganti T.D., Franchi L., and Nunez G. Caspase-1 inflammasomes in infection and inflammation. J Leukoc Biol 82 August (2) (2007) 220-225
17. Nishijima T., Tokura Y., Imokawa G., Seo N., Furukawa F., and Takigawa M. Altered permeability and disordered cutaneous immunoregulatory function in mice with acute barrier disruption. J Invest Dermatol 109 August (2) (1997) 175-182
18. Nickoloff B.J., and Naidu Y. Perturbation of epidermal barrier function correlates with initiation of cytokine cascade in human skin. J Am Acad Dermatol 30 April (4) (1994) 535-546
19. Wood L.C., Jackson S.M., Elias P.M., Grunfeld C., and Feingold K.R. Cutaneous barrier perturbation stimulates cytokine production in the epidermis of mice. J Clin Invest 90 August (2) (1992) 482-487
20. Strid J., Hourihane J., Kimber I., Callard R., and Strobel S. Disruption of the stratum corneum allows potent epicutaneous immunization with protein antigens resulting in a dominant systemic Th2 response. Eur J Immunol 34 August (8) (2004) 2100-2109
21. Tokura Y., Kobayashi M., and Kabashima K. Epidermal chemokines and modulation by antihistamines, antibiotics and antifungals. Exp Dermatol 17 February (2) (2008) 81-90
22. Ruckert R., Asadullah K., Seifert M., et al. Inhibition of keratinocyte apoptosis by IL-15: a new parameter in the pathogenesis of psoriasis?. J Immunol 165 August (4) (2000) 2240-2250
23. Imamichi H., Sereti I., and Lane H.C. IL-15 acts as a potent inducer of CD4(+)CD25(hi) cells expressing FOXP3. Eur J Immunol 38 June (6) (2008) 1621-1630
24. Michalek M., Gelhaus C., Hecht O., et al. The human antimicrobial protein psoriasin acts by permeabilization of bacterial membranes. Dev Comp Immunol 33 June (6) (2009) 740-746
25. Chavanas S., Bodemer C., Rochat A., et al. Mutations in SPINK5, encoding a serine protease inhibitor, cause Netherton syndrome. Nat Genet 25 June (2) (2000) 141-142
26. Walley A.J., Chavanas S., Moffatt M.F., et al. Gene polymorphism in Netherton and common atopic disease. Nat Genet 29 October (2) (2001) 175-178
27. Rast J.P., Smith L.C., Loza-Coll M., Hibino T., and Litman G.W. Genomic insights into the immune system of the sea urchin. Science 314 November (5801) (2006) 952-956
28. Hampe J., Cuthbert A., Croucher P.J., et al. Association between insertion mutation in NOD2 gene and Crohn's disease in German and British populations. Lancet 357 June (9272) (2001) 1925-1928
29. Raulet D.H. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 3 10 (2003 Oct) 781-790
30. Cerwenka A., and Lanier L.L. NKG2D ligands: unconventional MHC class I-like molecules exploited by viruses and cancer. Tissue Antigens 61 May (5) (2003) 335-343
31. Bahram S., Bresnahan M., Geraghty D.E., and Spies T. A second lineage of mammalian major histocompatibility complex class I genes. Proc Natl Acad Sci USA 91 July (14) (1994) 6259-6263
32. Gasser S., Orsulic S., Brown E.J., and Raulet D.H. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436 August (7054) (2005) 1186-1190
33. Dunn C., Chalupny N.J., Sutherland C.L., et al. Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J Exp Med 197 June (11) (2003) 1427-1439
34. Stern-Ginossar N., Gur C., Biton M., et al. Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol 9 September (9) (2008) 1065-1073
35. Girardi M., Oppenheim D.E., Steele C.R., et al. Regulation of cutaneous malignancy by gammadelta T cells. Science 294 October (5542) (2001) 605-609
36. Strid J., Roberts S.J., Filler R.B., et al. Acute upregulation of an NKG2D ligand promotes rapid reorganization of a local immune compartment with pleiotropic effects on carcinogenesis. Nat Immunol 9 February (2) (2008) 146-154
37. Groh V., Rhinehart R., Secrist H., Bauer S., Grabstein K.H., and Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci USA 96 June (12) (1999) 6879-6884
38. Vetter C.S., Groh V., thor Straten P., Spies T., Brocker E.B., and Becker J.C. Expression of stress-induced MHC class I related chain molecules on human melanoma. J Invest Dermatol 118 April (4) (2002) 600-605
39. Takada A., Yoshida S., Kajikawa M., et al. Two novel NKG2D ligands of the mouse H60 family with differential expression patterns and binding affinities to NKG2D. J Immunol 180 February (3) (2008) 1678-1685
40. Elias P.M., and Steinhoff M. Outside-to-inside" (and now back to "outside") pathogenic mechanisms in atopic dermatitis. J Invest Dermatol 128 May (5) (2008) 1067-1070
41. Maurer D., and Stingl G. Langerhans cells. In: Lotze M.T., and Thomson A.W. (Eds). Dendritic cells (2001), Academic Press 35-50
42. Bollrath J., Phesse T.J., von Burstin V.A., et al. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis. Cancer Cell 15 February (2) (2009) 91-102
43. Banchereau J., and Steinman R.M. Dendritic cells and the control of immunity. Nature 392 March (6673) (1998) 245-252
44. Cumberbatch M., Dearman R.J., Griffiths C.E., and Kimber I. Langerhans cell migration. Clin Exp Dermatol 25 July (5) (2000) 413-418
45. Merad M., Manz M.G., Karsunky H., et al. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat Immunol 3 Dec 12 (2002) 1135-1141
46. Tripp C.H., Chang-Rodriguez S., Stoitzner P., et al. Ontogeny of Langerin/CD207 expression in the epidermis of mice. J Invest Dermatol 122 March (3) (2004) 670-672
47. Borkowski T.A., Letterio J.J., Farr A.G., and Udey M.C. A role for endogenous transforming growth factor beta 1 in Langerhans cell biology: the skin of transforming growth factor beta 1 null mice is devoid of epidermal Langerhans cells. J Exp Med 184 6 (1996 Dec 1) 2417-2422
48. Bursch L.S., Wang L., Igyarto B., et al. Identification of a novel population of Langerin + dendritic cells. J Exp Med 204 December (13) (2007) 3147-3156
49. Ginhoux F., Collin M.P., Bogunovic M., et al. Blood-derived dermal langerin + dendritic cells survey the skin in the steady state. J Exp Med 204 December (13) (2007) 3133-3146
50. Poulin L.F., Henri S., de Bovis B., Devilard E., Kissenpfennig A., and Malissen B. The dermis contains langerin + dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med 204 December (13) (2007) 3119-3131
51. Kaplan D.H., Jenison M.C., Saeland S., Shlomchik W.D., and Shlomchik M.J. Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23 6 (2005 Dec) 611-620
52. Kissenpfennig A., Henri S., Dubois B., et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22 May (5) (2005) 643-654
53. Bennett C.L., van Rijn E., Jung S., et al. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J Cell Biol 169 May (4) (2005) 569-576
54. Wang L., Bursch L.S., Kissenpfennig A., Malissen B., Jameson S.C., and Hogquist K.A. Langerin expressing cells promote skin immune responses under defined conditions. J Immunol 180 April (7) (2008) 4722-4727
55. Obhrai J.S., Oberbarnscheidt M., Zhang N., et al. Langerhans cells are not required for efficient skin graft rejection. J Invest Dermatol 128 August (8) (2008) 1950-1955
56. Huang F.P., Platt N., Wykes M., et al. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J Exp Med 191 February (3) (2000) 435-444
57. Waithman J., Allan R.S., Kosaka H., et al. Skin-derived dendritic cells can mediate deletional tolerance of class I-restricted self-reactive T cells. J Immunol 179 October (7) (2007) 4535-4541
58. Kondo H., Ichikawa Y., and Imokawa G. Percutaneous sensitization with allergens through barrier-disrupted skin elicits a Th2-dominant cytokine response. Eur J Immunol 28 March (3) (1998) 769-779
59. Herrick C.A., MacLeod H., Glusac E., Tigelaar R.E., and Bottomly K. Th2 responses induced by epicutaneous or inhalational protein exposure are differentially dependent on IL-4. J Clin Invest 105 March (6) (2000) 765-775
60. Wang L.F., Lin J.Y., Hsieh K.H., and Lin R.H. Epicutaneous exposure of protein antigen induces a predominant Th2-like response with high IgE production in mice. J Immunol 156 June (11) (1996) 4077-4082
61. Nickoloff B.J., Fivenson D.P., Kunkel S.L., Strieter R.M., and Turka L.A. Keratinocyte interleukin-10 expression is upregulated in tape-stripped skin, poison ivy dermatitis, and Sezary syndrome, but not in psoriatic plaques. Clin Immunol Immunopathol 73 October (1) (1994) 63-68
62. Herrick C.A., Xu L., McKenzie A.N., Tigelaar R.E., and Bottomly K. IL-13 is necessary, not simply sufficient, for epicutaneously induced Th2 responses to soluble protein antigen. J Immunol 170 March (5) (2003) 2488-2495
63. Matsui K., and Nishikawa A. Lipoteichoic acid from Staphylococcus aureus induces Th2-prone dermatitis in mice sensitized percutaneously with an allergen. Clin Exp Allergy 32 5 (2002 May) 783-788
64. Sigmundsdottir H., Pan J., Debes G.F., et al. DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27. Nat Immunol 8 March (3) (2007) 285-293
65. Liu P.T., Stenger S., Li H., et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311 March (5768) (2006) 1770-1773
66. Krutzik S.R., Hewison M., Liu P.T., et al. IL-15 links TLR2/1-induced macrophage differentiation to the vitamin D-dependent antimicrobial pathway. J Immunol 181 November (10) (2008) 7115-7120
67. Clark R.A., Chong B.F., Mirchandani N., et al. A novel method for the isolation of skin resident T cells from normal and diseased human skin. J Invest Dermatol 126 May (5) (2006) 1059-1070
68. Boyman O., Hefti H.P., Conrad C., Nickoloff B.J., Suter M., and Nestle F.O. Spontaneous development of psoriasis in a new animal model shows an essential role for resident T cells and tumor necrosis factor-alpha. J Exp Med 199 March (5) (2004) 731-736
69. Nestle F.O., Conrad C., Tun-Kyi A., et al. Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J Exp Med 202 July (1) (2005) 135-143
70. Galon J., Costes A., Sanchez-Cabo F., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313 September (5795) (2006) 1960-1964
71. Piersma S.J., Jordanova E.S., van Poelgeest M.I., et al. High number of intraepithelial CD8+ tumor-infiltrating lymphocytes is associated with the absence of lymph node metastases in patients with large early-stage cervical cancer. Cancer Res 67 January (1) (2007) 354-361
72. Sato E., Olson S.H., Ahn J., et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci USA 102 December (51) (2005) 18538-18543
73. Pennington D.J., Vermijlen D., Wise E.L., Clarke S.L., Tigelaar R.E., and Hayday A.C. The integration of conventional and unconventional T cells that characterizes cell-mediated responses. Adv Immunol 87 (2005) 27-59
74. Asarnow D.M., Goodman T., LeFrancois L., and Allison J.P. Distinct antigen receptor repertoires of two classes of murine epithelium-associated T cells. Nature 341 September (6237) (1989) 60-62
75. Tigelaar R.E., Lewis J.M., and Bergstresser P.R. TCR gamma/delta + dendritic epidermal T cells as constituents of skin-associated lymphoid tissue. J Invest Dermatol 94 June (6, Suppl.) (1990) 58S-63S
76. Hayday A., Theodoridis E., Ramsburg E., and Shires J. Intraepithelial lymphocytes: exploring the Third Way in immunology. Nat Immunol 2 November (11) (2001) 997-1003
77. Havran W.L., Chien Y.H., and Allison J.P. Recognition of self antigens by skin-derived T cells with invariant gamma delta antigen receptors. Science 252 June (5011) (1991) 1430-1432
78. Tigelaar R.E., and Lewis J.M. Immunobiology of mouse dendritic epidermal T cells: a decade later, some answers, but still more questions. J Invest Dermatol 105 July (1, Suppl.) (1995) 43S-49S
79. Bonish B., Jullien D., Dutronc Y., et al. Overexpression of CD1d by keratinocytes in psoriasis and CD1d-dependent IFN-gamma production by NK-T cells. J Immunol 165 October (7) (2000) 4076-4085
80. Cameron A.L., Kirby B., Fei W., and Griffiths C.E. Natural killer and natural killer-T cells in psoriasis. Arch Dermatol Res 294 November (8) (2002) 363-369
81. Michel M.L., Mendes-da-Cruz D., Keller A.C., et al. Critical role of ROR-gammat in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc Natl Acad Sci USA 105 December (50) (2008) 19845-19850
82. Ribot J.C., deBarros A., Pang D.J., et al. CD27 is a thymic determinant of the balance between interferon-γ- and interleukin-17-producing gamma delta T cell subsets. Nat Immunol 10 April (4) (2009) 427-436
83. Holtmeier W., Pfander M., Hennemann A., Zollner T.M., Kaufmann R., and Caspary W.F. The TCR-delta repertoire in normal human skin is restricted and distinct from the TCR-delta repertoire in the peripheral blood. J Invest Dermatol 116 February (2) (2001) 275-280
84. Ebert L.M., Meuter S., and Moser B. Homing and function of human skin gammadelta T cells and NK cells: relevance for tumor surveillance. J Immunol 176 April (7) (2006) 4331-4336
85. Groh V., Wu J., Yee C., and Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419 October (6908) (2002) 734-738
86. Kaiser B.K., Yim D., Chow I.T., et al. Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature 447 May (7143) (2007) 482-486
87. Oppenheim D.E., Roberts S.J., Clarke S.L., et al. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 6 September (9) (2005) 928-937
88. Jinushi M., Hodi F.S., and Dranoff G. Therapy-induced antibodies to MHC class I chain-related protein A antagonize immune suppression and stimulate antitumor cytotoxicity. Proc Natl Acad Sci USA 103 June (24) (2006) 9190-9195
89. Gao Y., Yang W., Pan M., et al. Gamma delta T cells provide an early source of interferon gamma in tumor immunity. J Exp Med 198 August (3) (2003) 433-442
90. Boismenu R., and Havran W.L. Modulation of epithelial cell growth by intraepithelial gamma delta T cells. Science 266 November (5188) (1994) 1253-1255
91. Sharp L.L., Jameson J.M., Cauvi G., and Havran W.L. Dendritic epidermal T cells regulate skin homeostasis through local production of insulin-like growth factor 1. Nat Immunol 6 January (1) (2005) 73-79
92. Cao X., Cai S.F., Fehniger T.A., et al. Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity 27 October (4) (2007) 635-646
93. Zaiss D.M., Yang L., Shah P.R., Kobie J.J., Urban J.F., and Mosmann T.R. Amphiregulin, a TH2 cytokine enhancing resistance to nematodes. Science 314 December (5806) (2006) 1746
94. Jameson J., Ugarte K., Chen N., et al. A role for skin gammadelta T cells in wound repair. Science 296 April (5568) (2002) 747-749
95. Girardi M., Lewis J., Glusac E., et al. Resident skin-specific gammadelta T cells provide local, nonredundant regulation of cutaneous inflammation. J Exp Med 195 April (7) (2002) 855-867
96. Girardi M., Sherling M.A., Filler R.B., et al. Anti-inflammatory effects in the skin of thymosin-beta4 splice-variants. Immunology 109 May (1) (2003) 1-7
97. Poussier P., Ning T., Banerjee D., and Julius M. A unique subset of self-specific intraintestinal T cells maintains gut integrity. J Exp Med 195 June (11) (2002) 1491-1497
98. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., and Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118 July (2) (2004) 229-241
99. Satoh-Takayama N., Vosshenrich C.A., Lesjean-Pottier S., et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29 December (6) (2008) 958-970
100. Girardi M., Lewis J.M., Filler R.B., Hayday A.C., and Tigelaar R.E. Environmentally responsive and reversible regulation of epidermal barrier function by gammadelta T cells. J Invest Dermatol 126 April (4) (2006) 808-814
101. Lewis J.M., Girardi M., Roberts S.J., Barbee S.D., Hayday A.C., and Tigelaar R.E. Selection of the cutaneous intraepithelial gammadelta+ T cell repertoire by a thymic stromal determinant. Nat Immunol 7 August (8) (2006) 843-850
102. Boyden L.M., Lewis J.M., Barbee S.D., et al. Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal gammadelta T cells. Nat Genet 40 May (5) (2008) 656-662
103. Arnett H.A., Escobar S.S., Gonzalez-Suarez E., et al. BTNL2, a butyrophilin/B7-like molecule, is a negative costimulatory molecule modulated in intestinal inflammation. J Immunol 178 February (3) (2007) 1523-1533
104. Valentonyte R., Hampe J., Huse K., et al. Sarcoidosis is associated with a truncating splice site mutation in BTNL2. Nat Genet 37 April (4) (2005) 357-364
105. Zou Y., Stastny P., Susal C., Dohler B., and Opelz G. Antibodies against MICA antigens and kidney-transplant rejection. N Engl J Med 357 September (13) (2007) 1293-1300
106. Gibbons D.L., Haque S.F., Copestake S.L., et al. Suppression of airway inflammation by a natural acute infection of the intestinal epithelium. Mucosal Immunol December (2008)
107. Strid J., Hourihane J., Kimber I., Callard R., and Strobel S. Epicutaneous exposure to peanut protein prevents oral tolerance and enhances allergic sensitization. Clin Exp Allergy 35 June (6) (2005) 757-766
108. Shiohara T., Mizukawa Y., and Teraki Y. Pathophysiology of fixed drug eruption: the role of skin-resident T cells. Curr Opin Allergy Clin Immunol 2 August (4) (2002) 317-323