Mucosal T lymphocytes - Peacekeepers and warriors

Springer Seminars in Immunopathology

Volumn 27, Issue 2, 2005, Pages 147-165

  Cheroutre, Hilde ^a   Kronenberg, Mitchell ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Effector T cells; Epithelium; Immune regulation; Inflammation; Memory T cells; Tolerance

Indexed keywords

ARTICLE; CELL INTERACTION; CELL MIGRATION; DENDRITIC CELL; EFFECTOR CELL; HOST RESISTANCE; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE MUCOSA; LAMINA PROPRIA; MEMORY CELL; MESENTERY LYMPH NODE; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; DENDRITIC CELLS; HUMANS; INTESTINAL MUCOSA; MUCOUS MEMBRANE; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 24744464148     PISSN: 03444325     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00281-005-0205-7     Document Type: Article

References (120)

1. Mowat AM (2003) Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol 3(4):331-341
2. Cheroutre H (2004) Starting at the beginning: new perspectives on the biology of mucosal T cells. Annu Rev Immunol 22:217-246
3. Cheroutre H, Madakamutil L (2004) Acquired and natural memory T cells join forces at the mucosal front line. Nat Rev Immunol 4(4):290-300
4. Ferguson A (1977) Intraepithelial lymphocytes of the small intestine. Gut 18(11):921-937
5. Mysorekar IU, Lorenz RG, Gordon JI (2002) A gnotobiotic transgenic mouse model for studying interactions between small intestinal enterocytes and intraepithelial lymphocytes. J Biol Chem 277(40):37811-37819
6. Hayday A, Theodoridis E, Ramsburg E et al (2001) Intraepithelial lymphocytes: exploring the Third Way in immunology. Nat Immunol 2(11):997-1003
7. Blumberg RS, Yockey CE, Gross GG et al (1993) Human intestinal intraepithelial lymphocytes are derived from a limited number of T cell clones that utilize multiple V beta T cell receptor genes. J Immunol 150(11):5144-5153
8. Arstila T, Arstila TP, Calbo S et al (2000) Identical T cell clones are located within the mouse gut epithelium and lamina propia and circulate in the thoracic duct lymph. J Exp Med 191(5):823-834
9. Kerneis S, Bogdanova A, Kraehenbuhl JP et al (1997) Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277(5328):949-952
10. Kelsall BL, Strober W (1996) Distinct populations of dendritic cells are present in the subepithelial dome and T cell regions of the murine Peyer's patch. J Exp Med 183(1):237-247
11. Zimmer KP, Buning J, Weber P et al (2000) Modulation of antigen trafficking to MHC class II-positive late endosomes of enterocytes. Gastroenterology 118(1):128-137
12. Rescigno M, Urbano M, Valzasina B et al (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2(4):361-367
13. Niess JH, Brand S, Gu X et al (2005) CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307(5707):254-258
14. Masopust D, Vezys V, Marzo AL et al (2001) Preferential localization of effector memory cells in nonlymphoid tissue. Science 291(5512):2413-2417
15. Reinhardt RL, Khoruts A, Merica R et al (2001) Visualizing the generation of memory CD4 T cells in the whole body. Nature 410(6824):101-105
16. Masopust D, Vezys V, Usherwood EJ et al (2004) Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J Immunol 172(8):4875-4882
17. Sprent J, Miller JF (1976) Fate of H2-activated T lymphocytes in syngeneic hosts. III. Differentiation into long-lived recirculating memory cells. Cell Immunol 21(2):314-326
18. Kim SK, Reed DS, Heath WR et al (1997) Activation and migration of CD8 T cells in the intestinal mucosa. J Immunol 159(9):4295-4306
19. Kim SK, Schluns KS, Lefrancois L (1999) Induction and visualization of mucosal memory CD8 T cells following systemic virus infection. J Immunol 163(8):4125-4132
20. Stagg AJ, Kamm MA, Knight SC (2002) Intestinal dendritic cells increase T cell expression of alpha4beta7 integrin. Eur J Immunol 32(5):1445-1454
21. Johansson-Lindbom B, Svensson M, Wurbel MA et al (2003) Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J Exp Med 198(6):963-969
22. Mora JR, Bono MR, Manjunath N et al (2003) Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424(6944):88-93
23. Sydora BC, Wagner N, Lohler J et al (2002) beta7 Integrin expression is not required for the localization of T cells to the intestine and colitis pathogenesis. Clin Exp Immunol 129(1):35-42
24. Kuklin NA, Rott L, Darling J et al (2000) alpha(4)beta(7) independent pathway for CD8(+) T cell-mediated intestinal immunity to rotavirus. J Clin Invest 106(12):1541-1552
25. Svensson M, Marsal J, Ericsson A et al (2002) CCL25 mediates the localization of recently activated CD8alphabeta(+) lymphocytes to the small-intestinal mucosa. J Clin Invest 110(8):1113-1121
26. Kunkel EJ, Campbell JJ, Haraldsen G et al (2000) Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J Exp Med 192(5):761-768
27. Kunkel EJ, Campbell DJ, Butcher EC (2003) Chemokines in lymphocyte trafficking and intestinal immunity. Microcirculation 10(3-4):313-323
28. Agace WW, Roberts AI, Wu L et al (2000) Human intestinal lamina propria and intraepithelial lymphocytes express receptors specific for chemokines induced by inflammation. Eur J Immunol 30(3):819-826
29. Pan J, Kunkel EJ, Gosslar U et al (2000) A novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J Immunol 165(6):2943-2949
30. Muehlhoefer A, Saubermann LJ, Gu X et al (2000) Fractalkine is an epithelial and endothelial cell-derived chemoattractant for intraepithelial lymphocytes in the small intestinal mucosa. J Immunol 164(6):3368-3376
31. Iwata M, Hirakiyama A, Eshima Y et al (2004) Retinoic acid imprints gut-homing specificity on T cells. Immunity 21(4):527-538
32. Rose JR, Williams MB, Rott LS et al (1998) Expression of the mucosal homing receptor alpha4beta7 correlates with the ability of CD8+ memory T cells to clear rotavirus infection. J Virol 72(1):726-730
33. Dharakul T, Rott L, Greenberg HB (1990) Recovery from chronic rotavirus infection in mice with severe combined immunodeficiency: virus clearance mediated by adoptive transfer of immune CD8+ T lymphocytes. J Virol 64(9):4375-4382
34. Masopust D, Jiang J, Shen H et al (2001) Direct analysis of the dynamics of the intestinal mucosa CD8 T cell response to systemic virus infection. J Immunol 166(4):2348-2356
35. Muller S, Buhler-Jungo M, Mueller C (2000) Intestinal intraepithelial lymphocytes exert potent protective cytotoxic activity during an acute virus infection. J Immunol 164(4):1986-1994
36. Pope C, Kim SK, Marzo A et al (2001) Organ-specific regulation of the CD8 T cell response to Listeria monocytogenes infection. J Immunol 166(5):3402-3409
37. Lepage AC, Buzoni-Gatel D, Bout DT et al (1998) Gut-derived intraepithelial lymphocytes induce long term immunity against Toxoplasma gondii. J Immunol 161(9):4902-4908
38. Campbell JJ, Murphy KE, Kunkel EJ et al (2001) CCR7 expression and memory T cell diversity in humans. J Immunol 166(2):877-884
39. Fuss IJ, Neurath M, Boirivant M et al (1996) Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J Immunol 157(3):1261-1270
40. Russell RK, Nimmo ER, Satsangi J (2004) Molecular genetics of Crohn's disease. Curr Opin Genet Dev 14(3):264-270
41. Netea MG, Kullberg BJ, de Jong DJ et al (2004) NOD2 mediates anti-inflammatory signals induced by TLR2 ligands: implications for Crohn's disease. Eur J Immunol 34(7):2052-2059
42. Strober W, Ludviksson BR, Fuss IJ (1998) The pathogenesis of mucosal inflammation in murine models of inflammatory bowel disease and Crohn disease. Ann Intern Med 128(10):848-856
43. Rengarajan J, Szabo SJ, Glimcher LH (2000) Transcriptional regulation of Th1/Th2 polarization. Immunol Today 21(10):479-483
44. O'Shea JJ (1997) Jaks, STATs, cytokine signal transduction, and immunoregulation: are we there yet? Immunity 7(1):1-11
45. Neurath MF, Fuss I, Kelsall B et al (1996) Effect of IL-12 and antibodies to IL-12 on established granulomatous colitis in mice. Ann N Y Acad Sci 795:368-370
46. Wirtz S, Finotto S, Kanzler S et al (1999) Cutting edge: chronic intestinal inflammation in STAT-4 transgenic mice: characterization of disease and adoptive transfer by TNF- plus IFN-gamma-producing CD4+ T cells that respond to bacterial antigens. J Immunol 162(4):1884-1888
47. Neurath MF, Weigmann B, Finotto S et al (2002) The transcription factor T-bet regulates mucosal T cell activation in experimental colitis and Crohn's disease. J Exp Med 195(9):1129-1143
48. Simpson SJ, Shah S, Comiskey M et al (1998) T cell-mediated pathology in two models of experimental colitis depends predominantly on the interleukin 12/Signal transducer and activator of transcription (Stat)-4 pathway, but is not conditional on interferon gamma expression by T cells. J Exp Med 187(8):1225-1234
49. Fuss IJ, Boirivant M, Lacy B et al (2002) The interrelated roles of TGF-beta and IL-10 in the regulation of experimental colitis. J Immunol 168(2):900-908
50. Strober W, Fuss IJ, Ehrhardt RO et al (1998) Mucosal immunoregulation and inflammatory bowel disease: new insights from murine models of inflammation. Scand J Immunol 48(5):453-458
51. Powrie F, Correa-Oliveira R, Mauze S et al (1994) Regulatory interactions between CD45RBhigh and CD45RBlow CD4+ T cells are important for the balance between protective and pathogenic cell-mediated immunity. J Exp Med 179(2):589-600
52. Powrie F, Leach MW, Mauze S et al (1994) Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity 1(7):553-562
53. Mottet C, Uhlig HH, Powrie F (2003) Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells. J Immunol 170(8):3939-3943
54. Lehmann J, Huehn J, de la Rosa M et al (2002) Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25-regulatory T cells. Proc Natl Acad Sci U S A 99(20):13031-13036
55. Huehn J, Siegmund K, Lehmann JC et al (2004) Developmental stage, phenotype, and migration distinguish naive- and effector/memory-like CD4+ regulatory T cells. J Exp Med 199(3):303-313
56. Das G, Augustine MM, Das J et al (2003) An important regulatory role for CD4+CD8 alpha alpha T cells in the intestinal epithelial layer in the prevention of inflammatory bowel disease. Proc Natl Acad Sci U S A 100(9):5324-5329
57. Iqbal N, Oliver JR, Wagner FH et al (2002) T helper 1 and T helper 2 cells are pathogenic in an antigen-specific model of colitis. J Exp Med 195(1):71-84
58. Groux H, O'Garra A, Bigler M et al (1997) A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389(6652):737-742
59. Kuhn R, Lohler J, Rennick D et al (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75(2):263-274
60. Annacker O, Pimenta-Araujo R, Burlen-Defranoux O et al (2001) CD25+ CD4+ T cells regulate the expansion of peripheral CD4 T cells through the production of IL-10. J Immunol 166(5):3008-3018
61. Asseman C, Mauze S, Leach MW et al (1999) An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 190(7):995-1004
62. Hagenbaugh A, Sharma S, Dubinett SM et al (1997) Altered immune responses in interleukin 10 transgenic mice. J Exp Med 185(12):2101-2110
63. Nakamura K, Kitani A, Fuss I et al (2004) TGF-beta 1 plays an important role in the mechanism of CD4+CD25+ regulatory T cell activity in both humans and mice. J Immunol 172(2):834-842
64. Bilsborough J, George TC, Norment A et al (2003) Mucosal CD8alpha+ DC, with a plasmacytoid phenotype, induce differentiation and support function of T cells with regulatory properties. Immunology 108(4):481-492
65. O'Keeffe M, Hochrein H, Vremec D et al (2002) Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J Exp Med 196(10):1307-1319
66. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F et al (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118(2):229-241
67. Maloy KJ, Mowat AM, Zamoyska R et al (1991) Phenotypic heterogeneity of intraepithelial T lymphocytes from mouse small intestine. Immunology 72(4):555-562
68. Havran WL, Allison JP (1988) Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature 335(6189):443-445
69. Faure F, Jitsukawa S, Triebel F et al (1988) Characterization of human peripheral lymphocytes expressing the CD3-gamma/delta complex with anti-receptor monoclonal antibodies. J Immunol 141(10):3357-3360
70. Spencer J, Isaacson PG, MacDonald TT et al (1991) Gamma/delta T cells and the diagnosis of coeliac disease. Clin Exp Immunol 85(1):109-113
71. Leishman AJ, Naidenko OV, Attinger A et al (2001) T cell responses modulated through interaction between CD8alphaalpha and the nonclassical MHC class I molecule, TL. Science 294(5548):1936-1939
72. Hershberg R, Eghtesady P, Sydora B et al (1990) Expression of the thymus leukemia antigen in mouse intestinal epithelium. Proc Natl Acad Sci U S A 87(24):9727-9731
73. Leishman AJ, Gapin L, Capone M et al (2002) Precursors of functional MHC class I- or class II-restricted CD8alphaalpha(+) T cells are positively selected in the thymus by agonist self-peptides. Immunity 16(3):355-364
74. Liu Y, Xiong Y, Naidenko OV et al (2003) The crystal structure of a TL/CD8alphaalpha complex at 2.1 A resolution: implications for modulation of T cell activation and memory. Immunity 18(2):205-215
75. Madakamutil LT, Christen U, Lena CJ et al (2004) CD8alphaalpha-mediated survival and differentiation of CD8 memory T cell precursors. Science 304(5670):590-593
76. Guy-Grand D, Cuenod-Jabri B, Malassis-Seris M et al (1996) Complexity of the mouse gut T cell immune system: identification of two distinct natural killer T cell intraepithelial lineages. Eur J Immunol 26(9):2248-2256
77. Treiner E (2003) MAIT lymphocytes, regulators of intestinal immunity? Presse Med 32(35):1636-1637
78. Klein JR (1986) Ontogeny of the Thy-1-, Lyt-2+ murine intestinal intraepithelial lymphocyte. Characterization of a unique population of thymus-independent cytotoxic effector cells in the intestinal mucosa. J Exp Med 164(1):309-314
79. Ohteki T, MacDonald HR (1993) Expression of the CD28 costimulatory molecule on subsets of murine intestinal intraepithelial lymphocytes correlates with lineage and responsiveness. Eur J Immunol 23 (6):1251-1255
80. Van Houten N, Mixter PF, Wolfe J et al (1993) CD2 expression on murine intestinal intraepithelial lymphocytes is bimodal and defines proliferative capacity. Int Immunol 5(6):665-672
81. Guy-Grand D, Rocha B, Mintz P et al (1994) Different use of T cell receptor transducing modules in two populations of gut intraepithelial lymphocytes are related to distinct pathways of T cell differentiation. J Exp Med 180(2):673-679
82. Park SY, Arase H, Wakizaka K et al (1995) Differential contribution of the FcR gamma chain to the surface expression of the T cell receptor among T cells localized in epithelia: analysis of FcR gamma-deficient mice. Eur J Immunol 25(7):2107-2110
83. Regnault A, Cumano A, Vassalli P et al (1994) Oligoclonal repertoire of the CD8 alpha alpha and the CD8 alpha beta TCR-alpha/beta murine intestinal intraepithelial T lymphocytes: evidence for the random emergence of T cells. J Exp Med 180(4):1345-1358
84. Rocha B, Vassalli P, Guy-Grand D (1991) The V beta repertoire of mouse gut homodimeric alpha CD8+ intraepithelial T cell receptor alpha/beta + lymphocytes reveals a major extrathymic pathway of T cell differentiation. J Exp Med 173(2):483-486
85. Schild H, Mavaddat N, Litzenberger C et al (1994) The nature of major histocompatibility complex recognition by gamma delta T cells. Cell 76(1):29-37
86. Crowley MP, Fahrer AM, Baumgarth N et al (2000) A population of murine gammadelta T cells that recognize an inducible MHC class Ib molecule. Science 287(5451):314-316
87. Chien YH, Jores R, Crowley MP (1996) Recognition by gamma/delta T cells. Annu Rev Immunol 14:511-532
88. Groh V, Steinle A, Bauer S et al (1998) Recognition of stress-induced MHC molecules by intestinal epithelial gammadelta T cells. Science 279(5357):1737-1740
89. Steinle A, Groh V, Spies T (1998) Diversification, expression, and gamma delta T cell recognition of evolutionarily distant members of the MIC family of major histocompatibility complex class I-related molecules. Proc Natl Acad Sci U S A 95(21):12510-12515
90. Groh V, Bahram S, Bauer S et al (1996) Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A 93(22):12445-12450
91. Groh V, Rhinehart R, Secrist H et al (1999) Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci U S A 96(12):6879-6884
92. Vetter CS, Groh V, thor Straten P et al (2002) Expression of stress-induced MHC class I related chain molecules on human melanoma. J Invest Dermatol 118(5):600-605
93. Meresse B, Chen Z, Ciszewski C et al (2004) Coordinated induction by IL15 of a TCR-independent NKG2D signaling pathway converts CTL into lymphokine-activated killer cells in celiac disease. Immunity 21(3):357-366
94. Hue S, Mention JJ, Monteiro RC et al (2004) A direct role for NKG2D/MICA interaction in villous atrophy during celiac disease. Immunity 21(3):367-377
95. Bauer S, Groh V, Wu J et al (1999) Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285(5428):727-729
96. Cerwenka A, Bakker AB, McClanahan T et al (2000) Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 12(6):721-727
97. Diefenbach A, Jamieson AM, Liu SD et al (2000) Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 1(2):119-126
98. Guehler SR, Bluestone JA, Barrett TA (1996) Immune deviation of 2C transgenic intraepithelial lymphocytes in antigen-bearing hosts. J Exp Med 184(2):493-503
99. Levelt CN, de Jong YP, Mizoguchi E et al (1999) High- and low-affinity single-peptide/MHC ligands have distinct effects on the development of mucosal CD8alphaalpha and CD8alphabeta T lymphocytes. Proc Natl Acad Sci U S A 96(10):5628-5633
100. Saurer L, Seibold I, Rihs S et al (2004) Virus-induced activation of self-specific TCR alpha beta CD8 alpha alpha intraepithelial lymphocytes does not abolish their self-tolerance in the intestine. J Immunol 172(7):4176-4183
101. Guy-Grand D, Pardigon N, Darche S et al (2001) Contribution of double-negative thymic precursors to CD8alpha alpha (+) intraepithelial lymphocytes of the gut in mice bearing TCR transgenes. Eur J Immunol 31(9):2593-2602
102. Sydora BC, Brossay L, Hagenbaugh A et al (1996) TAP-independent selection of CD8+ intestinal intraepithelial lymphocytes. J Immunol 156(11):4209-4216
103. Neuhaus O, Emoto M, Blum C et al (1995) Control of thymus-independent intestinal intraepithelial lymphocytes by beta 2-microglobulin. Eur J Immunol 25(8):2332-2339
104. Fujiura Y, Kawaguchi M, Kondo Y et al (1996) Development of CD8 alpha alpha+ intestinal intraepithelial T cells in beta 2-microglobulin- and/or TAP1-deficient mice. J Immunol 156(8):2710-2715
105. Holcombe HR, Castano AR, Cheroutre H et al (1995) Nonclassical behavior of the thymus leukemia antigen: peptide transporter-independent expression of a nonclassical class I molecule. J Exp Med 181(4):1433-1443
106. Rodgers JR, Mehta V, Cook RG (1995) Surface expression of beta 2-microglobulin-associated thymus-leukemia antigen is independent of TAP2. Eur J Immunol 25(4):1001-1007
107. Gapin L, Cheroutre H, Kronenberg M (1999) Cutting edge: TCR alpha beta+ CD8 alpha alpha+ T cells are found in intestinal intraepithelial lymphocytes of mice that lack classical MHC class I molecules. J Immunol 163(8):4100-4104
108. Park SH, Guy-Grand D, Lemonnier FA et al (1999) Selection and expansion of CD8alpha/alpha(1) T cell receptor alpha/beta(1) intestinal intraepithelial lymphocytes in the absence of both classical major histocompatibility complex class I and nonclassical CD1 molecules. J Exp Med 190(6):885-890
109. Das G, Janeway CA Jr (1999) Development of CD8alpha/alpha and CD8alpha/beta T cells in major histocompatibility complex class I-deficient mice. J Exp Med 190(6):881-884
110. Das G, Gould DS, Augustine MM et al (2000) Qa-2-dependent selection of CD8alpha/alpha T cell receptor alpha/beta(+) cells in murine intestinal intraepithelial lymphocytes. J Exp Med 192(10):1521-1528
111. Shires J, Theodoridis E, Hayday AC (2001) Biological insights into TCRgammadelta+ and TCRalphabeta+ intraepithelial lymphocytes provided by serial analysis of gene expression (SAGE). Immunity 15(3):419-434
112. Janeway CA Jr, Jones B, Hayday A (1988) Specificity and function of T cells bearing gamma delta receptors. Immunol Today 9(3):73-76
113. Fujihashi K, Taguchi T, McGhee JR et al (1990) Regulatory function for murine intraepithelial lymphocytes. Two subsets of CD3+, T cell receptor-1+ intraepithelial lymphocyte T cells abrogate oral tolerance. J Immunol 145(7):2010-2019
114. Roberts SJ, Smith AL, West AB et al (1996) T-cell alpha beta + and gamma delta + deficient mice display abnormal but distinct phenotypes toward a natural, widespread infection of the intestinal epithelium. Proc Natl Acad Sci U S A 93(21):11774-11779
115. Ke Y, Pearce K, Lake JP et al (1997) Gamma delta T lymphocytes regulate the induction and maintenance of oral tolerance. J Immunol 158(8):3610-3618
116. Boismenu R, Havran WL (1994) Modulation of epithelial cell growth by intraepithelial gamma delta T cells. Science 266(5188):1253-1255
117. Hayday AC (2000) [gamma][delta] cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 18:975-1026
118. Born W, Cady C, Jones-Carson J et al (1999) Immunoregulatory functions of gamma delta T cells. Adv Immunol 71:77-144
119. Cruz D, Sydora BC, Hetzel K et al (1998) An opposite pattern of selection of a single T cell antigen receptor in the thymus and among intraepithelial lymphocytes. J Exp Med 188(2):255-265
120. Poussier P, Ning T, Banerjee D et al (2002) A unique subset of self-specific intraintestinal T cells maintains gut integrity. J Exp Med 195(11):1491-1497