Integrin αeβ7: Molecular features and functional significance in the immune system

Advances in Experimental Medicine and Biology

Volumn 819, Issue , 2014, Pages 97-110

  Hadley, Gregg A ^a   Higgins, Jonathan M G ^b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Dendritic cells; Integrins; Intraepithelial T cells; Mast cells; Regulatory T cells; TGF

Indexed keywords

ALPHAEBETA7 INTEGRIN; INTEGRIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; ALPHA INTEGRIN; ALPHAE BETA7 INTEGRIN; BETA7 INTEGRIN; ISOPROTEIN; LIGAND;

ADAPTIVE IMMUNITY; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ARTICLE; CELLULAR DISTRIBUTION; DENDRITIC CELL; EFFECTOR CELL; GENE LOCUS; GENE STRUCTURE; GRAFT REJECTION; GRAFT VERSUS HOST REACTION; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNE SYSTEM; IMMUNOREGULATION; INNATE IMMUNITY; LIGAND BINDING; MAST CELL; MEMORY T LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TISSUE DISTRIBUTION; TUMOR IMMUNITY; ALLOGRAFT; EPITHELIUM CELL; IMMUNE RESPONSE; LEUKOCYTE; MOUSE; PROTEIN DOMAIN; PROTEIN INTERACTION; TUMOR IMMUNOLOGY;

ANIMALS; DENDRITIC CELLS; HUMANS; IMMUNOLOGIC MEMORY; INTEGRINS; NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; TRANSPLANTATION, HOMOLOGOUS;

EID: 84934439357     PISSN: 00652598     EISSN: 22148019     Source Type: Book Series    
DOI: 10.1007/978-94-17-9153-3_7     Document Type: Article

References (118)

1. Allez M, Brimnes J, Dotan I, Mayer L (2002) Expansion of CD8+ T cells with regulatory function after interaction with intestinal epithelial cells. Gastroenterology 123:1516-1526
2. Andrew DP, Rott LS, Kilshaw PJ, Butcher EC (1996) Distribution of alpha 4 beta 7 and alpha E beta 7 integrins on thymocytes, intestinal epithelial lymphocytes and peripheral lymphocytes. Eur J Immunol 26:897-905
3. Annacker O, Coombes JL, Malmstrom V, Uhlig HH, Bourne T, Johansson-Lindbom B et al (2005) Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J Exp Med 202:1051-1061
4. Annunziato F, Cosmi L, Liotta F, Lazzeri E, Romagnani P, Angeli R et al (2006) CXCR3 and alpha E beta 7 integrin identify a subset of CD8+ mature thymocytes that share phenotypic and functional properties with CD8+ gut intraepithelial lymphocytes. Gut 55:961-968
5. Baker E, Sutherland GR, Jiang WM, Yuan Q, Leung E, Watson JD et al (1992) Mapping of the human integrin beta 7 gene (ITG beta 7) to 12q13.13 by non-isotopic in situ hybridization. Mamm Genome 2:272-273
6. Bedoui S, Whitney PG, Waithman J, Eidsmo L, Wakim L, Caminschi I et al (2009) Crosspresentation of viral and self antigens by skinderived CD103+ dendritic cells. Nat Immunol 10:488-495
7. Brenan M, Puklavec M (1992) The MRC OX-62 antigen: a useful marker in the purification of rat veiled cells with the biochemical properties of an integrin. J Exp Med 175:1457-1465
8. Brenan M, Rees DJ (1997) Sequence analysis of rat integrin alpha E1 and alpha E2 subunits: tissue expression reveals phenotypic similarities between intraepithelial lymphocytes and dendritic cells in lymph. Eur J Immunol 27:3070-3079
9. Brew R, West DC, Burthem J, Christmas SE (1995) Expression of the human mucosal lymphocyte antigen, HML-1, by T cells activated with mitogen or specific antigen in vitro. Scand J Immunol 41:553-562
10. Brown DW, Furness J, Speight PM, Thomas GJ, Li J, Thornhill MH et al (1999) Mechanisms of binding of cutaneous lymphocyte-associated antigenpositive and alphaebeta7-positive lymphocytes to oral and skin keratinocytes. Immunology 98:9-15
11. Butcher EC, Williams M, Youngman K, Rott L, Briskin M (1999) Lymphocyte trafficking and regional immunity. Adv Immunol 72:209-253
12. Cepek KL, Parker CM, Madara JL, Brenner MB (1993) Integrin alpha E beta 7 mediates adhesion of T lymphocytes to epithelial cells. J Immunol 150:3459-3470
13. Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL et al (1994) Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 372:190-193
14. Cerf-Bensussan N, Begue B, Gagnon J, Meo T (1992) The human intraepithelial lymphocyte marker HML-1 is an integrin consisting of a beta 7 subunit associated with a distinctive alpha chain. Eur J Immunol 22:885
15. Cerf-Bensussan N, Guy-Grand D, Lisowska- Grospierre B, Griscelli C, Bhan AK (1986) A monoclonal antibody specific for rat intestinal lymphocytes. J Immunol 136:76-82
16. Cerf-Bensussan N, Jarry A, Brousse N, Lisowska- Grospierre B, Guy-Grand D, Griscelli C (1987) A monoclonal antibody (HML-1) defining a novel membrane molecule present on human intestinal lymphocytes. Eur J Immunol 17:1279-1285
17. Chatenoud L, Salomon B, Bluestone JA (2001) Suppressor T cells-they're back and critical for regulation of autoimmunity! Immunol Rev 182:149-163
18. Choi JH, Cheong C, Dandamudi DB, Park CG, Rodriguez A, Mehandru S et al (2011) Flt3 signaling-dependent dendritic cells protect against atherosclerosis. Immunity 35:819-831
19. Collazo MM, Wood D, Paraiso KH, Lund E, Engelman RW, Le CT et al (2009) SHIP limits immunoregulatory capacity in the T-cell compartment. Blood 113:2934-2944
20. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, Belkaid Y et al (2007) A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 204:1757-1764
21. Corbi AL, Garcia-Aguilar J, Springer TA (1990) Genomic structure of an integrin alpha subunit, the leukocyte p150,95 molecule. J Biol Chem 265:2782-2788
22. Cresswell J, Robertson H, Neal DE, Griffiths TR, Kirby JA (2001) Distribution of lymphocytes of the alpha(E)beta(7) phenotype and E-cadherin in normal human urothelium and bladder carcinomas. Clin Exp Immunol 126:397-402
23. Csencsits KL, Walters N, Pascual DW (2001) Cutting edge: dichotomy of homing receptor dependence by mucosal effector B cells: alpha(E) versus L-selectin. J Immunol 167:2441-2445
24. El-Asady R, Yuan R, Liu K, Wang D, Gress RE, Lucas PJ et al (2005) TGF-{beta}-dependent CD103 expression by CD8(+) T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease. J Exp Med 201:1647-1657
25. Farstad IN, Halstensen TS, Lien B, Kilshaw PJ, Lazarovits AI, Brandtzaeg P (1996) Distribution of beta 7 integrins in human intestinal mucosa and organized gut-associated lymphoid tissue. Immunology 89:227-237
26. Feng Y, Wang D, Yuan R, Parker CM, Farber DL, Hadley GA (2002) CD103 expression is required for destruction of pancreatic islet allografts by CD8(+) T cells. J Exp Med 196:877-886
27. Fleming JC, Pahl HL, Gonzalez DA, Smith TF, Tenen DG (1993) Structural analysis of the CD11b gene and phylogenetic analysis of the alpha-integrin gene family demonstrate remarkable conservation of genomic organization and suggest early diversification during evolution. J Immunol 150:480-490
28. Flores-Langarica A, Marshall JL, Hitchcock J, Cook C, Jobanputra J, Bobat S et al (2012) Systemic flagellin immunization stimulates mucosal CD103+ dendritic cells and drives Foxp3+ regulatory T cell and IgA responses in the mesenteric lymph node. J Immunol 189:5745-5754
29. Franciszkiewicz K, Le Floc'h A, Boutet M, Vergnon I, Schmitt A, Mami-Chouaib F (2013) CD103 or LFA-1 engagement at the immune synapse between cytotoxic T cells and tumor cells promotes maturation and regulates T-cell effector functions. Cancer Res 73:617-628
30. Franciszkiewicz K, Le Floc'h A, Jalil A, Vigant F, Robert T, Vergnon I et al (2009) Intratumoral induction of CD103 triggers tumor-specific CTL function and CCR5-dependent T-cell retention. Cancer Res 69:6249-6255
31. Gabor MJ, Sedgwick JD, Lemckert FA, Godfrey DI, Korner H (2001) Lymphotoxin controls alphaEbeta7-integrin expression by peripheral CD8+ T cells. Immunol Cell Biol 79:323-331
32. Gavin MA, Clarke SR, Negrou E, Gallegos A, Rudensky A (2002) Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat Immunol 3:33-41
33. Grueter B, Petter M, Egawa T, Laule-Kilian K, Aldrian CJ, Wuerch A et al (2005) Runx3 regulates integrin alpha E/CD103 and CD4 expression during development of CD4-/CD8+ T cells. J Immunol 175:1694-1705
34. Hadley GA, Bartlett ST, Via CS, Rostapshova EA, Moainie S (1997) The epithelial cell-specific integrin, CD103 (alpha E integrin), defines a novel subset of alloreactive CD8 + CTL. J Immunol 159:3748-3756
35. Hadley GA, Charandee C, Weir MR, Wang D, Bartlett ST, Drachenberg CB (2001) CD103+ CTL accumulate within the graft epithelium during clinical renal allograft rejection. Transplantation 72:1548-1555
36. Hadley GA, Rostapshova EA, Gomolka DM, Taylor BM, Bartlett ST, Drachenberg CI et al (1999) Regulation of the epithelial cell-specific integrin, CD103, by human CD8+ cytolytic T lymphocytes. Transplantation 67:1418-1425
37. Higgins JM (2001) The Haspin gene: location in an intron of the integrin alphaE gene, associated transcription of an integrin alphaE-derived RNA and expression in diploid as well as haploid cells. Gene 267:55-69
38. Higgins JM, Cernadas M, Tan K, Irie A, Wang J, Takada Y et al (2000) The role of alpha and beta chains in ligand recognition by beta 7 integrins. J Biol Chem 275:25652-25664
39. Higgins JM, Mandlebrot DA, Shaw SK, Russell GJ, Murphy EA, Chen YT et al (1998) Direct and regulated interaction of integrin alphaEbeta7 with E-cadherin. J Cell Biol 140:197-210
40. Hoffkes HG, Schmidtke G, Uppenkamp M, Schmucker U (1996) Multiparametric immunophenotyping of B cells in peripheral blood of healthy adults by flow cytometry. Clin Diagn Lab Immunol 3:30-36
41. Jenkinson SE, Whawell SA, Swales BM, Corps EM, Kilshaw PJ, Farthing PM (2011) The alphaE(CD103)beta7 integrin interacts with oral and skin keratinocytes in an E-cadherinindependent manner. Immunology 132:188-196
42. Jiang WM, Jenkins D, Yuan Q, Leung E, Choo KH, Watson JD et al (1992) The gene organization of the human beta 7 subunit, the common beta subunit of the leukocyte integrins HML-1 and LPAM-1. Int Immunol 4:1031-1040
43. Johansson-Lindbom B, Svensson M, Pabst O, Palmqvist C, Marquez G, Forster R et al (2005) Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med 202:1063-1073
44. Karecla PI, Bowden SJ, Green SJ, Kilshaw PJ (1995) Recognition of E-cadherin on epithelial cells by the mucosal T cell integrin alpha M290 beta 7 (alpha E beta 7). Eur J Immunol 25:852-856
45. Karecla PI, Green SJ, Bowden SJ, Coadwell J, Kilshaw PJ (1996) Identification of a binding site for integrin alphaEbeta7 in the N-terminal domain of E-cadherin. J Biol Chem 271:30909-30915
46. Kilshaw PJ (1993) Expression of the mucosal T cell integrin alpha M290 beta 7 by a major subpopulation of dendritic cells in mice. Eur J Immunol 23:3365-3368
47. Kilshaw PJ, Baker KC (1988) A unique surface antigen on intraepithelial lymphocytes in the mouse. Immunol Lett 18:149-154
48. Kilshaw PJ, Higgins JM (2002) Alpha E: no more rejection? J Exp Med 196:873-875
49. Kilshaw PJ, Murant SJ (1991) Expression and regulation of beta 7(beta p) integrins on mouse lymphocytes: relevance to the mucosal immune system. Eur J Immunol 21:2591-2597
50. Kilshaw PJ, Murant SJ (1990) A new surface antigen on intraepithelial lymphocytes in the intestine. Eur J Immunol 20:2201-2207
51. Kim SK, Schluns KS, Lefrancois L (1999) Induction and visualization of mucosal memory CD8 T cells following systemic virus infection. J Immunol 163:4125-4132
52. Kinnebrew MA, Buffie CG, Diehl GE, Zenewicz LA, Leiner I, Hohl TM et al (2012) Interleukin 23 production by intestinal CD103(+)CD11b(+) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity 36:276-287
53. Klebanoff CA, Spencer SP, Torabi-Parizi P, Grainger JR, Roychoudhuri R, Ji Y et al (2013) Retinoic acid controls the homeostasis of pre-cDCderived splenic and intestinal dendritic cells. J Exp Med 210:1961-1976
54. Krissansen GW, Print CG, Prestidge RL, Hollander D, Yuan Q, Jiang WM et al (1992) Immunologic and structural relatedness of the integrin beta 7 complex and the human intraepithelial lymphocyte antigen HML-1. FEBS Lett 296:25-28
55. Kunisawa J, Kurashima Y, Higuchi M, Gohda M, Ishikawa I, Ogahara I et al (2007) Sphingosine 1- phosphate dependence in the regulation of lymphocyte trafficking to the gut epithelium. J Exp Med 204:2335-2348
56. Kutlesa S, Wessels JT, Speiser A, Steiert I, Muller CA, Klein G (2002) E-cadherin-mediated interactions of thymic epithelial cells with CD103 + thymocytes lead to enhanced thymocyte cell proliferation. J Cell Sci 115:4505-4515
57. Le Floc'h A, Jalil A, Franciszkiewicz K, Validire P, Vergnon I, Mami-Chouaib F (2011) Minimal engagement of CD103 on cytotoxic T lymphocytes with an E-cadherin-Fc molecule triggers lytic granule polarization via a phospholipase Cgamma-dependent pathway. Cancer Res 71:328-338
58. Le Floc'h A, Jalil A, Vergnon I, Le Maux Chansac B, Lazar V, Bismuth G et al (2007) Alpha E beta 7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis. J Exp Med 204:559-570
59. Lefrancois L, Barrett TA, Havran WL, Puddington L (1994) Developmental expression of the alpha IEL beta 7 integrin on T cell receptor gamma delta and T cell receptor alpha beta T cells. Eur J Immunol 24:635-640
60. Lehmann J, Huehn J, de la Rosa M, Maszyna F, Kretschmer U, Krenn V 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 USA 99:13031-13036
61. Li N, Chen Y, He W, Yi T, Zhao D, Zhang C et al (2009) Anti-CD3 preconditioning separates GVL from GVHD via modulating host dendritic cell and donor T-cell migration in recipients conditioned with TBI. Blood 113:953-962
62. Liu K, Anthony BA, Yearsly MM, Hamadani M, Gaughan A, Wang JJ et al (2011) CD103 deficiency prevents graft-versus-host disease but spares graftversus- tumor effects mediated by alloreactive CD8 T cells. PLoS ONE 6:e21968
63. Mackay LK, Stock AT, Ma JZ, Jones CM, Kent SJ, Mueller SN et al (2012) Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc Natl Acad Sci USA 109:7037-7042
64. Maloy KJ, Powrie F (2001) Regulatory T cells in the control of immune pathology. Nat Immunol 2:816-822
65. Maric I, Holt PG, Perdue MH, Bienenstock J (1996) Class II MHC antigen (Ia)-bearing dendritic cells in the epithelium of the rat intestine. J Immunol 156:1408-1414
66. McCarthy NE, Bashir Z, Vossenkamper A, Hedin CR, Giles EM, Bhattacharjee S et al (2013) Proinflammatory Vdelta2+ T cells populate the human intestinal mucosa and enhance IFN-gamma production by colonic alphabeta T cells. J Immunol 191:2752-2763
67. McFarland RD, Douek DC, Koup RA, Picker LJ (2000) Identification of a human recent thymic emigrant phenotype. Proc Natl Acad Sci USA 97:4215-4220
68. McHugh RS, Whitters MJ, Piccirillo CA, Young DA, Shevach EM, Collins M et al (2002) CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 16:311-323
69. McLellan AD, Kapp M, Eggert A, Linden C, Bommhardt U, Brocker EB et al (2002) Anatomic location and T-cell stimulatory functions of mouse dendritic cell subsets defined by CD4 and CD8 expression. Blood 99:2084-2093
70. Micklem KJ, Dong Y, Willis A, Pulford KA, Visser L, Durkop H et al (1991) HML-1 antigen on mucosa-associated T cells, activated cells, and hairy leukemic cells is a new integrin containing the beta 7 subunit. Am J Pathol 139:1297-1301
71. Moldenhauer G, Mielke B, Dorken B, Schwartz- Albiez R, Moller P (1990) Identity of HML-1 antigen on intestinal intraepithelial T cells and of Bly7 antigen on hairy cell leukaemia. Scand J Immunol 32:77-82
72. Moller P, Mielke B, Moldenhauer G (1990) Monoclonal antibody HML-1, a marker for intraepithelial T cells and lymphomas derived thereof, also recognizes hairy cell leukemia and some B-cell lymphomas. Am J Pathol 136:509-512
73. Nelson DJ, McMenamin C, McWilliam AS, Brenan M, Holt PG (1994) Development of the airway intraepithelial dendritic cell network in the rat from class II major histocompatibility (Ia)-negative precursors: differential regulation of Ia expression at different levels of the respiratory tract. J Exp Med 179:203-212
74. Noti JD, Gordon M, Hall RE (1992) Human p150,95 alpha-subunit: genomic organization and analysis of the 5'-flanking region. DNA Cell Biol 11:123-138
75. Nunes-Cabaco H, Caramalho I, Sepulveda N, Sousa AE (2011) Differentiation of human thymic regulatory T cells at the double positive stage. Eur J Immunol 41:3604-3614
76. Parker CM, Cepek KL, Russell GJ, Shaw SK, Posnett DN, Schwarting R et al (1992) A family of beta 7 integrins on human mucosal lymphocytes. Proc Natl Acad Sci USA 89:1924-1928
77. Quayle AJ, Pudney J, Munoz DE, Anderson DJ (1994) Characterization of T lymphocytes and antigen-presenting cells in the murine male urethra. Biol Reprod 51:809-820
78. Ribi E, Granger DL, Milner KC, Yamamoto K, Strain SM, Parker R et al (1982) Induction of resistance to tuberculosis in mice with defined components of mycobacteria and with some unrelated materials. Immunology 46:297-305
79. Riedl E, Stockl J, Majdic O, Scheinecker C, Rappersberger K, Knapp W et al (2000) Functional involvement of E-cadherin in TGF-beta 1-induced cell cluster formation of in vitro developing human Langerhans-type dendritic cells. J Immunol 165:1381-1386
80. Rihs S, Walker C, Virchow JC Jr, Boer C, Kroegel C, Giri SN et al (1996) Differential expression of alpha E beta 7 integrins on bronchoalveolar lavage T lymphocyte subsets: regulation by alpha 4 beta 1- integrin crosslinking and TGF-beta. Am J Respir Cell Mol Biol 15:600-610
81. Roberts AI, O'Connell SM, Ebert EC (1993) Intestinal intraepithelial lymphocytes bind to colon cancer cells by HML-1 and CD11a. Cancer Res 53:1608-1611
82. Roberts K, Kilshaw PJ (1993) The mucosal T cell integrin alpha M290 beta 7 recognizes a ligand on mucosal epithelial cell lines. Eur J Immunol 23:1630-1635
83. Robertson H, Wong WK, Burt AD, Mohamed MA, Talbot D, Kirby JA (2001) Relationship between TGFbeta(1), intratubular CD103 positive T cells and acute renal allograft rejection. Transplant Proc 33:1159
84. Robertson H, Wong WK, Talbot D, Burt AD, Kirby JA (2001) Tubulitis after renal transplantation: demonstration of an association between CD103+ T cells, transforming growth factor beta1 expression and rejection grade. Transplantation 71:306-313
85. Robinson PW, Green SJ, Carter C, Coadwell J, Kilshaw PJ (2001) Studies on transcriptional regulation of the mucosal T-cell integrin alphaEbeta7 (CD103). Immunology 103:146-154
86. Rostapshova EA, Burns JM, Bartlett ST, Hadley GA (1998) Integrin-mediated interactions influence the tissue specificity of CD8+ cytolytic T lymphocytes. Eur J Immunol 28:3031-3039
87. Schieferdecker HL, Ullrich R, Weiss-Breckwoldt AN, Schwarting R, Stein H, Riecken EO et al (1990) The HML-1 antigen of intestinal lymphocytes is an activation antigen. J Immunol 144:2541-2549
88. Schon MP, Arya A, Murphy EA, Adams CM, Strauch UG, Agace WW et al (1999) Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J Immunol 162:6641-6649
89. Shaw SK, Cepek KL, Murphy EA, Russell GJ, Brenner MB, Parker CM (1994) Molecular cloning of the human mucosal lymphocyte integrin alpha E subunit. Unusual structure and restricted RNA distribution. J Biol Chem 269:6016-6025
90. Shibahara T, Si-Tahar M, Shaw SK, Madara JL (2000) Adhesion molecules expressed on homing lymphocytes in model intestinal epithelia. Gastroenterology 118:289-298
91. Siddiqui KR, Laffont S, Powrie F (2010) E-cadherin marks a subset of inflammatory dendritic cells that promote T cell-mediated colitis. Immunity 32:557-567
92. Smith TJ, Ducharme LA, Shaw SK, Parker CM, Brenner MB, Kilshaw PJ et al (1994) Murine M290 integrin expression modulated by mast cell activation. Immunity 1:393-403
93. Strauch UG, Mueller RC, Li XY, Cernadas M, Higgins JM, Binion DG et al (2001) Integrin alpha E(CD103)beta 7 mediates adhesion to intestinal microvascular endothelial cell lines via an Ecadherin- independent interaction. J Immunol 166:3506-3514
94. Suffia I, Reckling SK, Salay G, Belkaid Y (2005) A role for CD103 in the retention of CD4+ CD25+ Treg and control of Leishmania major infection. J Immunol 174:5444-5455
95. Suvas PK, Dech HM, Sambira F, Zeng J, Onami TM (2007) Systemic and mucosal infection program protective memory CD8 T cells in the vaginal mucosa. J Immunol 179:8122-8127
96. Suzuki R, Nakao A, Kanamaru Y, Okumura K, Ogawa H, Ra C (2002) Localization of intestinal intraepithelial T lymphocytes involves regulation of alphaEbeta7 expression by transforming growth factor-beta. Int Immunol 14:339-345
97. Takeichi M (1993) Cadherins in cancer: implications for invasion and metastasis. Curr Opin Cell Biol 5:806-811
98. Taraszka KS, Higgins JM, Tan K, Mandelbrot DA, Wang JH, Brenner MB (2000) Molecular basis for leukocyte integrin alpha(E)beta(7) adhesion to epithelial (E)-cadherin. J Exp Med 191:1555-1567
99. Teraki Y, Shiohara T (2002) Preferential expression of alphaEbeta7 integrin (CD103) on CD8+ T cells in the psoriatic epidermis: regulation by interleukins 4 and 12 and transforming growth factor-beta. Br J Dermatol 147:1118-1126
100. Tiisala S, Paavonen T, Renkonen R (1995) Alpha E beta 7 and alpha 4 beta 7 integrins associated with intraepithelial and mucosal homing, are expressed on macrophages. Eur J Immunol 25:411-417
101. Trinite B, Chauvin C, Peche H, Voisine C, Heslan M, Josien R (2005) Immature CD4-CD103+ rat dendritic cells induce rapid caspase-independent apoptosis-like cell death in various tumor and nontumor cells and phagocytose their victims. J Immunol 175:2408-2417
102. Uchida Y, Kawai K, Ibusuki A, Kanekura T (2011) Role for E-cadherin as an inhibitory receptor on epidermal gammadelta T cells. J Immunol 186:6945-6954
103. Uss E, Rowshani AT, Hooibrink B, Lardy NM, van Lier RA, ten Berge IJ (2006) CD103 is a marker for alloantigen-induced regulatory CD8+ T cells. J Immunol 177:2775-2783
104. Van den Bossche J, Bogaert P, van Hengel J, Guerin CJ, Berx G, Movahedi K et al (2009) Alternatively activated macrophages engage in homotypic and heterotypic interactions through IL-4 and polyamine-induced E-cadherin/catenin complexes. Blood 114:4664-4674
105. Van den Bossche J, Malissen B, Mantovani A, De Baetselier P, Van Ginderachter JA (2012) Regulation and function of the E-cadherin/catenin complex in cells of the monocyte-macrophage lineage and DCs. Blood 119:1623-1633
106. Van VQ, Darwiche J, Raymond M, Lesage S, Bouguermouh S, Rubio M et al (2008) Cutting edge: CD47 controls the in vivo proliferation and homeostasis of peripheral CD4 + CD25 + Foxp3 + regulatory T cells that express CD103. J Immunol 181:5204-5208
107. Wakim LM, Woodward-Davis A, Bevan MJ (2010) Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc Natl Acad Sci USA 107:17872-17879
108. Watchmaker PB, Lahl K, Lee M, Baumjohann D, Morton J, Kim SJ et al (2014) Comparative transcriptional and functional profiling defines conserved programs of intestinal DC differentiation in humans and mice. Nat Immunol
109. Weiner HL, da Cunha AP, Quintana F, Wu H (2011) Oral tolerance. Immunol Rev 241:241-259
110. Wong DA, Davis EM, LeBeau M, Springer TA (1996) Cloning and chromosomal localization of a novel gene-encoding a human beta 2-integrin alpha subunit. Gene 171:291-294
111. Wright SH, Brown J, Knight PA, Thornton EM, Kilshaw PJ, Miller HR (2002) Transforming growth factor-beta1 mediates coexpression of the integrin subunit alphaE and the chymase mouse mast cell protease-1 during the early differentiation of bone marrow-derived mucosal mast cell homologues. Clin Exp Allergy 32:315-324
112. Yarmus M, Woolf E, Bernstein Y, Fainaru O, Negreanu V, Levanon D et al (2006) Groucho/ transducin-like Enhancer-of-split (TLE)-dependent and -independent transcriptional regulation by Runx3. Proc Natl Acad Sci USA 103:7384-7389
113. Yu CI, Becker C, Wang Y, Marches F, Helft J, Leboeuf M et al (2013) Human CD1c+ dendritic cells drive the differentiation of CD103 + CD8 + mucosal effector T cells via the cytokine TGF-beta. Immunity 38:818-830
114. Yuan J, Zhang G, Yang X, Liu K, Wang F (2013) Transplantation of allograft transforming growth factor-beta1 transfected CD103(+) lamina propria dendritic cells could effectively induce antigenspecific regulatory T cells in vivo. Transplant Proc 45:3408-3413
115. Yuan Q, Jiang WM, Hollander D, Leung E, Watson JD, Krissansen GW (1991) Identity between the novel integrin beta 7 subunit and an antigen found highly expressed on intraepithelial lymphocytes in the small intestine. Biochem Biophys Res Commun 176:1443-1449
116. Yuan Q, Kozak CA, Jiang WM, Hollander D, Watson JD, Krissansen GW (1992) Genetic mapping of the gene coding for the integrin beta 7 subunit to the distal part of mouse chromosome 15. Immunogenetics 35:403-407
117. Zelenika D, Adams E, Humm S, Graca L, Thompson S, Cobbold SP et al (2002) Regulatory T cells overexpress a subset of Th2 gene transcripts. J Immunol 168:1069-1079
118. Zhou S, Ueta H, Xu XD, Shi C, Matsuno K (2008) Predominant donor CD103 + CD8 + T cell infiltration into the gut epithelium during acute GvHD: a role of gut lymph nodes. Int Immunol 20:385-394