The unique surface molecules on intestinal intraepithelial lymphocytes: From tethering to recognizing

Digestive Diseases and Sciences

Volumn 59, Issue 3, 2014, Pages 520-529

  Qiu, Yuan ^a   Yang, Yang ^a   Yang, Hua ^a  

^a Xinqiao Hospital   (China)

Author keywords

Intestinal epithelial cells; Intraepithelial lymphocytes; Recognition; Surface molecules

Indexed keywords

CD2 ANTIGEN; CD28 ANTIGEN; CD5 ANTIGEN; CD8 T CELL RECEPTOR ALPHAALPHA; CHEMOKINE RECEPTOR CCR9; EPITHELIAL CELL ADHESION MOLECULE; INTEGRIN; INTEGRIN ALPHAEBETA7; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; NATURAL KILLER CELL RECEPTOR NKG2A; NATURAL KILLER CELL RECEPTOR NKG2D; OCCLUDIN; T CELL RECEPTOR ALPHABETA; T CELL RECEPTOR GAMMADELTA; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DNA RESPONSIVE ELEMENT; EXTRACELLULAR MATRIX; HUMAN; INTESTINE EPITHELIUM; INTESTINE LYMPHATIC TISSUE; INTRAEPITHELIAL LYMPHOCYTE; LYMPHOCYTE; LYMPHOCYTE MIGRATION; LYMPHOID TISSUE; NONHUMAN; PRIORITY JOURNAL; REVIEW; WNT SIGNALING PATHWAY;

BIOLOGICAL MARKERS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELL COMMUNICATION; CELL MOVEMENT; HUMANS; INTESTINAL MUCOSA; PHENOTYPE; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS;

EID: 84896726196     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-013-2933-1     Document Type: Review

References (86)

1. Zufferey C, Erhart D, Saurer L, Mueller C. Production of interferon-gamma by activated T-cell receptor-alphabeta CD8alphabeta intestinal intraepithelial lymphocytes is required and sufficient for disruption of the intestinal barrier integrity. Immunology. 2009;128:351-359.
2. Beagley KW, Fujihashi K, Lagoo AS, et al. Differences in intraepithelial lymphocyte T cell subsets isolated from murine small versus large intestine. J Immunol. 1995;154:5611-5619.
3. Yamagata T, Mathis D, Benoist C. Self-reactivity in thymic double-positive cells commits cells to a CD8 alpha alpha lineage with characteristics of innate immune cells. Nat Immunol. 2004;5:597-605.
4. Suzuki H. Differences in intraepithelial lymphocytes in the proximal, middle, distal parts of small intestine, cecum, and colon of mice. Immunol Invest. 2009;38:780-796.
5. Lundqvist C, Baranov V, Hammarstrom S, Athlin L, Hammarstrom ML. Intra-epithelial lymphocytes. Evidence for regional specialization and extrathymic T cell maturation in the human gut epithelium. Int Immunol. 1995;7:1473-1487.
6. Hayday A, Theodoridis E, Ramsburg E, Shires J. Intraepithelial lymphocytes: Exploring the Third Way in immunology. Nat Immunol. 2001;2:997-1003.
7. Cheroutre H, Lambolez F, Mucida D. The light and dark sides of intestinal intraepithelial lymphocytes. Nat Rev Immunol. 2011;11: 445-456.
8. Wang R, Wang-Zhu Y, Grey H. Interactions between double positive thymocytes and high affinity ligands presented by cortical epithelial cells generate double negative thymocytes with T cell regulatory activity. Proc Natl Acad Sci USA. 2002;99:2181-2186.
9. Arstila T, Arstila TP, Calbo S, et al. Identical T cell clones are located within the mouse gut epithelium and lamina propia and circulate in the thoracic duct lymph. J Exp Med. 2000;191:823-834.
10. Manzano M, Abadia-Molina AC, Garcia-Olivares E, Gil A, Rueda R. Absolute counts and distribution of lymphocyte subsets in small intestine of BALB/c mice change during weaning. J Nutr. 2002;132:2757-2762.
11. Umesaki Y, Setoyama H, Matsumoto S, Okada Y. Expansion of alpha beta T-cell receptor-bearing intestinal intraepithelial lymphocytes after microbial colonization in germ-free mice and its independence from thymus. Immunology. 1993;79:32-37.
12. Cheroutre H. Starting at the beginning: New perspectives on the biology of mucosal T cells. Annu Rev Immunol. 2004;22:217-246.
13. Lepage AC, Buzoni-Gatel D, Bout DT, Kasper LH. Gut-derived intraepithelial lymphocytes induce long term immunity against Toxoplasma gondii. J Immunol. 1998;161:4902-4908.
14. Shires J, Theodoridis E, Hayday AC. Biological insights into TCRgammadelta? and TCRalphabeta? intraepithelial lymphocytes provided by serial analysis of gene expression (SAGE). Immunity. 2001;15:419-434.
15. Lefrancois L. Phenotypic complexity of intraepithelial lymphocytes of the small intestine. J Immunol. 1991;147:1746-1751.
16. Cawthon AG, Lu H, Alexander-Miller MA. Peptide requirement for CTL activation reflects the sensitivity to CD3 engagement: Correlation with CD8alphabeta versus CD8alphaalpha expression. J Immunol. 2001;167:2577-2584.
17. Van Houten N, Mixter PF, Wolfe J, Budd RC. CD2 expression on murine intestinal intraepithelial lymphocytes is bimodal and defines proliferative capacity. Int Immunol. 1993;5:665-672.
18. Ohteki T, MacDonald HR. Expression of the CD28 costimulatory molecule on subsets of murine intestinal intraepithelial lymphocytes correlates with lineage and responsiveness. Eur J Immunol. 1993;23:1251-1255.
19. Agace WW. T-cell recruitment to the intestinal mucosa. Trends Immunol. 2008;29:514-522.
20. Lambolez F, Kronenberg M, Cheroutre H. Thymic differentiation of TCR alpha beta(+) CD8 alpha alpha(+) IELs. Immunol Rev. 2007;215:178-188.
21. Gangadharan D, Lambolez F, Attinger A, Wang-Zhu Y, Sullivan BA, Cheroutre H. Identification of pre-and postselection TCRalphabeta ? intraepithelial lymphocyte precursors in the thymus. Immunity. 2006;25:631-641.
22. AbadieV,DiscepoloV, Jabri B. Intraepithelial lymphocytes in celiac disease immunopathology. Semin Immunopathol. 2012;34:551-566.
23. Laky K, Lefrancois L, Lingenheld EG, et al. Enterocyte expression of interleukin 7 induces development of gammadelta T cells and Peyer's patches. J Exp Med. 2000;191:1569-1580.
24. Park SG, Mathur R, Long M, et al. T regulatory cells maintain intestinal homeostasis by suppressing gammadelta T cells. Immunity. 2010;33:791-803.
25. Kunisawa J, Takahashi I, Kiyono H. Intraepithelial lymphocytes: Their shared and divergent immunological behaviors in the small and large intestine. Immunol Rev. 2007;215:136-153.
26. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol. 2007;25:619-647.
27. Askari JA, Buckley PA, Mould AP, Humphries MJ. Linking integrin conformation to function. J Cell Sci. 2009;122:165-170.
28. Agace WW, Higgins JM, Sadasivan B, Brenner MB, Parker CM. T-lymphocyte-epithelial-cell interactions: Integrin alpha(E)(CD103) beta(7), LEEP-CAM and chemokines. Curr Opin Cell Biol. 2000;12:563-568.
29. Gorfu G, Rivera-Nieves J, Ley K. Role of beta7 integrins in intestinal lymphocyte homing and retention. Curr Mol Med. 2009;9:836-850.
30. Lim SP, Leung E, Krissansen GW. The beta7 integrin gene (Itgb-7) promoter is responsive to TGF-beta1: Defining control regions. Immunogenetics. 1998;48:184-195.
31. Ericsson A, Svensson M, Arya A, Agace WW. CCL25/CCR9 promotes the induction and function of CD103 on intestinal intraepithelial lymphocytes. Eur J Immunol. 2004;34:2720-2729.
32. Schon MP, Arya A, Murphy EA, et al. Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J Immunol. 1999;162:6641-6649.
33. Wagner N, Lohler J, Kunkel EJ, et al. Critical role for beta7 integrins in formation of the gut-associated lymphoid tissue. Nature. 1996;382:366-370.
34. Tian X, Liu Z, Niu B, et al. E-cadherin/beta-catenin complex and the epithelial barrier. J Biomed Biotechnol. 2011;2011:567305.
35. Shapiro L, Weis WI. Structure and biochemistry of cadherins and catenins. Cold Spring Harb Perspect Biol. 2009;1:a003053.
36. Nagar B, Overduin M, Ikura M, Rini JM. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature. 1996;380:360-364.
37. Higgins JM, Mandlebrot DA, Shaw SK, et al. Direct and regulated interaction of integrin alphaEbeta7 with E-cadherin. J Cell Biol. 1998;140:197-210.
38. Sarnacki S, Begue B, Buc H, Le Deist F, Cerf-Bensussan N. Enhancement of CD3-induced activation of human intestinal intraepithelial lymphocytes by stimulation of the beta 7-containing integrin defined by HML-1 monoclonal antibody. Eur J Immunol. 1992;22:2887-2892.
39. Lefrancois L, Barrett TA, Havran WL, Puddington L. 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. 1994;24:635-640.
40. Le Floc'h A, Jalil A, Vergnon I, et al. Alpha E beta 7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis. J Exp Med. 2007;204:559-570.
41. El-Asady R, Yuan R, Liu K, et al. 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. 2005;201:1647-1657.
42. Trzpis M, McLaughlin PM, de Leij LM, Harmsen MC. Epithelial cell adhesion molecule: More than a carcinoma marker and adhesion molecule. Am J Pathol. 2007;171:386-395.
43. Balzar M, Winter MJ, de Boer CJ, Litvinov SV. The biology of the 17-1A antigen (Ep-CAM). J Mol Med (Berl). 1999;77: 699-712.
44. Nelson AJ, Dunn RJ, Peach R, Aruffo A, Farr AG. The murine homolog of human Ep-CAM, a homotypic adhesion molecule, is expressed by thymocytes and thymic epithelial cells. Eur J Immunol. 1996;26:401-408.
45. Nochi T, Yuki Y, Terahara K, et al. Biological role of Ep-CAM in the physical interaction between epithelial cells and lymphocytes in intestinal epithelium. Clin Immunol. 2004;113:326-339.
46. Winter MJ, Nagelkerken B, Mertens AE, Rees-Bakker HA, Briaire-de Bruijn IH, Litvinov SV. Expression of Ep-CAM shifts the state of cadherin-mediated adhesions from strong to weak. Exp Cell Res. 2003;285:50-58.
47. Rao R. Occludin phosphorylation in regulation of epithelial tight junctions. Ann N Y Acad Sci. 2009;1165:62-68.
48. Cummins PM. Occludin: One protein, many forms. Mol Cell Biol. 2012;32:242-250.
49. Seth A, Sheth P, Elias BC, Rao R. Protein phosphatases 2A and 1 interact with occludin and negatively regulate the assembly of tight junctions in the CACO-2 cell monolayer. J Biol Chem. 2007;282:11487-11498.
50. Inagaki-Ohara K, Sawaguchi A, Suganuma T, Matsuzaki G, Nawa Y. Intraepithelial lymphocytes express junctional molecules in murine small intestine. Biochem Biophys Res Commun. 2005;331:977-983.
51. Edelblum KL, Shen L, Weber CR, et al. Dynamic migration of gammadelta intraepithelial lymphocytes requires occludin. Proc Natl Acad Sci USA. 2012;109:7097-7102.
52. Dalton JE, Cruickshank SM, Egan CE, et al. Intraepithelial gammadelta ? lymphocytes maintain the integrity of intestinal epithelial tight junctions in response to infection. Gastroenterology. 2006;131:818-829.
53. Inagaki-Ohara K, Dewi FN, Hisaeda H, et al. Intestinal intraepithelial lymphocytes sustain the epithelial barrier function against Eimeria vermiformis infection. Infect Immun. 2006;74:5292-5301.
54. Guy-Grand D, Cuenod-Jabri B, Malassis-Seris M, Selz F, Vassalli P. Complexity of the mouse gut T cell immune system: Identification of two distinct natural killer T cell intraepithelial lineages. Eur J Immunol. 1996;26:2248-2256.
55. Meresse B, Curran SA, Ciszewski C, et al. Reprogramming of CTLs into natural killer-like cells in celiac disease. J Exp Med. 2006;203:1343-1355.
56. Bhagat G, Naiyer AJ, Shah JG, et al. Small intestinal CD8 + TCRgammadelta + NKG2A + intraepithelial lymphocytes have attributes of regulatory cells in patients with celiac disease. J Clin Invest. 2008;118:281-293.
57. Diefenbach A, Tomasello E, Lucas M, et al. Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat Immunol. 2002;3:1142-1149.
58. Eagle RA, Trowsdale J. Promiscuity and the single receptor: NKG2D. Nat Rev Immunol. 2007;7:737-744.
59. Hansen CH, Holm TL, Krych L, et al. Gut microbiota regulates NKG2D ligand expression on intestinal epithelial cells. Eur J Immunol. 2013;43:447-457.
60. Li J, Cui L, He W. Distinct pattern of human Vdelta1 gammadelta T cells recognizing MICA. Cell Mol Immunol. 2005;2:253-258.
61. Hue S, Mention JJ, Monteiro RC, et al. A direct role for NKG2D/MICA interaction in villous atrophy during celiac disease. Immunity. 2004;21:367-377.
62. Meresse B, Chen Z, Ciszewski C, et al. Coordinated induction by IL15 of a TCR-independent NKG2D signaling pathway converts CTL into lymphokine-activated killer cells in celiac disease. Immunity. 2004;21:357-366.
63. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR, Spies T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol. 2001;2:255-260.
64. Bridgeman JS, Sewell AK, Miles JJ, Price DA, Cole DK. Structural and biophysical determinants of alphabeta T-cell antigen recognition. Immunology. 2012;135:9-18.
65. Rudolph MG, Stanfield RL, Wilson IA. How TCRs bind MHCs, peptides, and coreceptors. Annu Rev Immunol. 2006;24:419-466.
66. Kane LP, Lin J, Weiss A. Signal transduction by the TCR for antigen. Curr Opin Immunol. 2000;12:242-249.
67. Kim SK, Reed DS, Olson S, et al. Generation of mucosal cytotoxic T cells against soluble protein by tissue-specific environmental and costimulatory signals. Proc Natl Acad Sci USA. 1998;95:10814-10819.
68. Masopust D, Vezys V, Wherry EJ, Barber DL, Ahmed R. Cutting edge: Gut microenvironment promotes differentiation of a unique memory CD8 T cell population. J Immunol. 2006;176: 2079-2083.
69. Huleatt JW, Pilip I, Kerksiek K, Pamer EG. Intestinal and splenic T cell responses to enteric Listeria monocytogenes infection: Distinct repertoires of responding CD8 T lymphocytes. J Immunol. 2001;166:4065-4073.
70. Muller S, Buhler-Jungo M, Mueller C. Intestinal intraepithelial lymphocytes exert potent protective cytotoxic activity during an acute virus infection. J Immunol. 2000;164:1986-1994.
71. Nancey S, Holvoet S, Graber I, et al. CD8 + cytotoxic T cells induce relapsing colitis in normal mice. Gastroenterology. 2006; 131:485-496.
72. McVay LD, Carding SR. Generation of human gammadelta T-cell repertoires. Crit Rev Immunol. 1999;19:431-460.
73. Champagne E. Gammadelta T cell receptor ligands and modes of antigen recognition. Arch Immunol Ther Exp (Warsz). 2011;59: 117-137.
74. Fahrer AM, Konigshofer Y, Kerr EM, et al. Attributes of gammadelta intraepithelial lymphocytes as suggested by their transcriptional profile. Proc Natl Acad Sci USA. 2001;98: 10261-10266.
75. Deusch K, Luling F, Reich K, Classen M, Wagner H, Pfeffer K. A major fraction of human intraepithelial lymphocytes simultaneously expresses the gamma/delta T cell receptor, the CD8 accessory molecule and preferentially uses the V delta 1 gene segment. Eur J Immunol. 1991;21:1053-1059.
76. Ness-Schwickerath KJ, Morita CT. Regulation and function of IL-17A-and IL-22-producing gammadelta T cells. Cell Mol Life Sci. 2011;68:2371-2390.
77. Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci USA. 1996;93:12445-12450.
78. Xu B, Pizarro JC, Holmes MA, et al. Crystal structure of a gammadelta T-cell receptor specific for the human MHC class I homolog MICA. Proc Natl Acad Sci USA. 2011;108:2414-2419.
79. Montufar-Solis D, Garza T, Klein Jr. T-cell activation in the intestinal mucosa. Immunol Rev. 2007;215:189-201.
80. Leishman AJ, Naidenko OV, Attinger A, et al. T cell responses modulated through interaction between CD8alphaalpha and the nonclassical MHC class I molecule, TL. Science. 2001;294: 1936-1939.
81. Flaherty L, Elliott E, Tine JA, Walsh AC, Waters JB. Immunogenetics of the Q and TL regions of the mouse. Crit Rev Immunol. 1990;10:131-175.
82. Liu Y, Xiong Y, Naidenko OV, et al. The crystal structure of a TL/CD8alphaalpha complex at 2.1 A resolution: Implications for modulation of T cell activation and memory. Immunity. 2003; 18:205-215.
83. Pardigon N, Darche S, Kelsall B, Bennink JR, Yewdell JW. The TL MHC class Ib molecule has only marginal effects on the activation, survival and trafficking of mouse small intestinal intraepithelial lymphocytes. Int Immunol. 2004;16: 1305-1313.
84. Pardigon N, Takeda K, Saunier B, et al. CD8 alpha alpha-mediated intraepithelial lymphocyte snatching of thymic leukemia MHC class Ib molecules in vitro and in vivo. J Immunol. 2006;177:1590-1598.
85. Olivares-Villagomez D, Mendez-Fernandez YV, Parekh VV, et al. Thymus leukemia antigen controls intraepithelial lymphocyte function and inflammatory bowel disease. Proc Natl Acad Sci USA. 2008;105:17931-17936.
86. Olivares-Villagomez D, Algood HM, Singh K, et al. Intestinal epithelial cells modulate CD4 T cell responses via the thymus leukemia antigen. J Immunol. 2011;187:4051-4060.