Roles of T cell-associated L-selectin and β7 integrins during induction and regulation of chronic colitis

Inflammatory Bowel Diseases

Volumn 19, Issue 12, 2013, Pages 2547-2559

  Kurmaeva, Elvira ^a   Boktor, Moheb ^a   Zhang, Songling ^a   Bao, Richard ^a   Berney, Seth ^a   Ostanin, Dmitry V ^a  

^a Louisiana State University School of Medicine Shreveport   (United States)

Author keywords

Adhesion molecules; Effector T cell; Inflammation; Inflammatory bowel disease; Leukocyte trafficking

Indexed keywords

BETA7 INTEGRIN; CELL ADHESION MOLECULE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2; L SELECTIN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL HOMING; CELL MIGRATION; CELL PROLIFERATION; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DISEASE SEVERITY; EFFECTOR CELL; FLOW CYTOMETRY; GENOTYPE; HISTOPATHOLOGY; IN VITRO STUDY; INTESTINE; INTESTINE MUCOSA; LAMINA PROPRIA; LYMPHOID TISSUE; MESENTERY LYMPH NODE; MONONUCLEAR CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; SMALL INTESTINE; SURFACE PROPERTY; T LYMPHOCYTE; WILD TYPE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CHRONIC DISEASE; COLITIS; CYTOKINES; FEMALE; FLOW CYTOMETRY; GASTROINTESTINAL TRACT; HOMEODOMAIN PROTEINS; INTEGRIN BETA CHAINS; L-SELECTIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84888367141     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0b013e3182a8df0a     Document Type: Article

References (79)

1. Powrie F, Leach MW. Genetic and spontaneous models of inflammatory bowel disease in rodents: evidence for abnormalities in mucosal immune regulation. Ther Immunol. 1995;2:115-123.
2. Ostanin DV, Pavlick KP, Bharwani S, et al. T cell-induced inflammation of the small and large intestine in immunodeficient mice. Am J Physiol Gastrointest Liver Physiol. 2006;290:G109-G119.
3. Mora JR, Bono MR, Manjunath N, et al. Selective imprinting of guthoming T cells by Peyer's patch dendritic cells. Nature. 2003;424: 88-93.
4. Johansson-Lindbom B, Svensson M, Pabst O, et al. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med. 2005;202:1063-1073.
5. Luster AD, Alon R, von Andrian UH. Immune cell migration in inflammation: present and future therapeutic targets. Nat Immunol. 2005;6: 1182-1190.
6. Villablanca EJ, Cassani B, von Andrian UH, et al. Blocking lymphocyte localization to the gastrointestinal mucosa as a therapeutic strategy for inflammatory bowel diseases. Gastroenterology. 2011;140:1776-1784.
7. Kogan AN, von Andrian UH. Adhesion and communication between lymphocytes and endothelial cells. In: Schmid-Schonbein GW, Granger DN, eds. Molecular Basis for Microcirculatory Disorders. Paris, France: Springer; 2004:101-137.
8. von Andrian UH, Mempel TR. Homing and cellular traffic in lymph nodes. Nat Rev Immunol. 2003;3:867-878.
9. Steeber DA, Tang ML, Zhang XQ, et al. Efficient lymphocyte migration across high endothelial venules of mouse Peyer's patches requires overlapping expression of L-selectin and beta7 integrin. J Immunol. 1998;161: 6638-6647.
10. Wagner N, Lohler J, Tedder TF, et al. L-selectin and beta7 integrin synergistically mediate lymphocyte migration to mesenteric lymph nodes. Eur J Immunol. 1998;28:3832-3839.
11. Berlin C, Berg EL, Briskin MJ, et al. Alpha 4 beta 7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell. 1993;74:185-195.
12. Hu MC, Crowe DT, Weissman IL, et al. Cloning and expression of mouse integrin beta p(beta 7): a functional role in Peyer's patch-specific lymphocyte homing. Proc Natl Acad Sci U S A. 1992;89:8254-8258.
13. Holzmann B, McIntyre BW, Weissman IL. Identification of a murine Peyer's patch - specific lymphocyte homing receptor as an integrin molecule with an alpha chain homologous to human VLA-4 alpha. Cell. 1989; 56:37-46.
14. Ostanin DV, Furr KL, Pavlick KP, et al. T cell-associated CD18 but not CD62L, ICAM-1, or PSGL-1 is required for the induction of chronic colitis. Am J Physiol Gastrointest Liver Physiol. 2007;292:G1706-G1714.
15. Agace WW. T-cell recruitment to the intestinal mucosa. Trends Immunol. 2008;29:514-522.
16. Mora JR, von Andrian UH. T-cell homing specificity and plasticity: new concepts and future challenges. Trends Immunol. 2006;27:235-243.
17. 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.
18. Gorfu G, Rivera-Nieves J, Hoang S, et al. Beta7 integrin deficiency suppresses B cell homing and attenuates chronic ileitis in SAMP1/YitFc mice. J Immunol. 2010;185:5561-5568.
19. Apostolaki M, Manoloukos M, Roulis M, et al. Role of beta7 integrin and the chemokine/chemokine receptor pair CCL25/CCR9 in modeled TNF-dependent Crohn's disease. Gastroenterology. 2008;134:2025-2035.
20. Wang C, Kang SG, HogenEsch H, et al. Retinoic acid determines the precise tissue tropism of inflammatory Th17 cells in the intestine. J Immunol. 2010;184:5519-5526.
21. Gorfu G, Rivera-Nieves J, Ley K. Role of beta7 integrins in intestinal lymphocyte homing and retention. Curr Mol Med. 2009;9:836-850.
22. Park EJ, Mora JR, Carman CV, et al. Aberrant activation of integrin alpha4beta7 suppresses lymphocyte migration to the gut. J Clin Invest. 2007;117:2526-2538.
23. Sydora BC, Wagner N, Lohler J, et al. beta7 Integrin expression is not required for the localization of T cells to the intestine and colitis pathogenesis. Clin Exp Immunol. 2002;129:35-42.
24. Rivera-Nieves J, Olson T, Bamias G, et al. L-selectin, alpha 4 beta 1, and alpha 4 beta 7 integrins participate in CD4+ T cell recruitment to chronically inflamed small intestine. J Immunol. 2005;174:2343-2352.
25. Gordon FH, Hamilton MI, Donoghue S, et al. A pilot study of treatment of active ulcerative colitis with natalizumab, a humanized monoclonal antibody to alpha-4 integrin. Aliment Pharmacol Ther. 2002;16:699-705.
26. Sandborn WJ, Colombel JF, Enns R, et al. Natalizumab induction and maintenance therapy for Crohn's disease. N Engl J Med. 2005;353:1912-1925.
27. Targan SR, Feagan BG, Fedorak RN, et al. Natalizumab for the treatment of active Crohn's disease: results of the ENCORE Trial. Gastroenterology. 2007;132:1672-1683.
28. Major EO. Progressive multifocal leukoencephalopathy in patients on immunomodulatory therapies. Annu Rev Med. 2010;61:35-47.
29. Feagan BG, Greenberg GR, Wild G, et al. Treatment of active Crohn's disease with MLN0002, a humanized antibody to the alpha4beta7 integrin. Clin Gastroenterol Hepatol. 2008;6:1370-1377.
30. Parikh A, Leach T, Wyant T, et al. Vedolizumab for the treatment of active ulcerative colitis: a randomized controlled phase 2 dose-ranging study. Inflamm Bowel Dis. 2012;18:1470-1479.
31. Vermeire S, Ghosh S, Panes J, et al. The mucosal addressin cell adhesion molecule antibody PF-00547,659 in ulcerative colitis: a randomised study. Gut. 2011;60:1068-1075.
32. Eksteen B, Adams DH. GSK-1605786, a selective small-molecule antagonist of the CCR9 chemokine receptor for the treatment of Crohn's disease. IDrugs. 2010;13:472-781.
33. Walters MJ, Wang Y, Lai N, et al. Characterization of CCX282-B, an orally bioavailable antagonist of the CCR9 chemokine receptor, for treatment of inflammatory bowel disease. J Pharmacol Exp Ther. 2010;335: 61-69.
34. Hesterberg PE, Winsor-Hines D, Briskin MJ, et al. Rapid resolution of chronic colitis in the cotton-top tamarin with an antibody to a gut-homing integrin alpha 4 beta 7. Gastroenterology. 1996;111:1373-1380.
35. Podolsky DK, Lobb R, King N, et al. Attenuation of colitis in the cottontop tamarin by anti-alpha 4 integrin monoclonal antibody. J Clin Invest. 1993;92:372-380.
36. Picarella D, Hurlbut P, Rottman J, et al. Monoclonal antibodies specific for beta 7 integrin and mucosal addressin cell adhesion molecule-1 (MAd-CAM-1) reduce inflammation in the colon of scid mice reconstituted with CD45RBhigh CD4+ T cells. J Immunol. 1997;158:2099-2106.
37. Pinola M, Saksela E, Tiisala S, et al. Human NK cells expressing alpha 4 beta 1/beta 7 adhere to VCAM-1 without preactivation. Scand J Immunol. 1994;39:131-136.
38. Soler D, Chapman T, Yang LL, et al. The binding specificity and selective antagonism of vedolizumab, an anti-a4b7 integrin therapeutic antibody in development for inflammatory bowel diseases. J Pharmacol Exp Ther. 2009;330:864-875.
39. Tiisala S, Paavonen T, Renkonen R. Alpha E beta 7 and alpha 4 beta 7 integrins associated with intraepithelial and mucosal homing, are expressed on macrophages. Eur J Immunol. 1995;25:411-417.
40. Mottet C, Uhlig HH, Powrie F. Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells. J Immunol. 2003;170:3939-3943.
41. Liu H, Hu B, Xu D, et al. CD4+CD25+ regulatory T cells cure murine colitis: the role of IL-10, TGF-beta, and CTLA4. J Immunol. 2003;171: 5012-5017.
42. Martin B, Banz A, Bienvenu B, et al. Suppression of CD4+ T lymphocyte effector functions by CD4+CD25+ cells in vivo. J Immunol. 2004;172: 3391-3398.
43. Denning TL, Kim G, Kronenberg M. Cutting edge: CD4+CD25+ regulatory T cells impaired for intestinal homing can prevent colitis. J Immunol. 2005;174:7487-7491.
44. Makita S, Kanai T, Nemoto Y, et al. Intestinal lamina propria retaining CD4+CD25+ regulatory T cells is a suppressive site of intestinal inflammation. J Immunol. 2007;178:4937-4946.
45. Arbones ML, Ord DC, Ley K, et al. Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity. 1994;1:247-260.
46. Ostanin DV, Bao J, Koboziev I, et al. T cell transfer model of chronic colitis: concepts, considerations, and tricks of the trade. Am J Physiol Gastrointest Liver Physiol. 2009;296:G135-G146.
47. Villablanca EJ, Mora JR. Competitive homing assays to study gut-tropic t cell migration. J Vis Exp. 2011.
48. Iwata M, Hirakiyama A, Eshima Y, et al. Retinoic acid imprints guthoming specificity on T cells. Immunity. 2004;21:527-538.
49. Pavlick KP, Ostanin DV, Furr KL, et al. Role of T-cell-associated lymphocyte function-associated antigen-1 in the pathogenesis of experimental colitis. Int Immunol. 2006;18:389-398.
50. Takebayashi K, Koboziev I, Ostanin DV, et al. Role of the gut-associated and secondary lymphoid tissue in the induction of chronic colitis. Inflamm Bowel Dis. 2011;17:268-278.
51. Leach MW, Bean AG, Mauze S, et al. Inflammatory bowel disease in C. B-17 scid mice reconstituted with the CD45RBhigh subset of CD4+ T cells. Am J Pathol. 1996;148:1503-1515.
52. Kandula S, Abraham C. LFA-1 on CD4+ T cells is required for optimal antigen-dependent activation in vivo. J Immunol. 2004;173:4443-4451.
53. Marski M, Ye AL, Abraham C. CD18 is required for intestinal T cell responses at multiple immune checkpoints. J Immunol. 2007;178: 2104-2112.
54. Perez OD, Mitchell D, Jager GC, et al. Leukocyte functional antigen 1 lowers T cell activation thresholds and signaling through cytohesin-1 and Jun-activating binding protein 1. Nat Immunol. 2003;4: 1083-1092.
55. Graf B, Bushnell T, Miller J. LFA-1-mediated T cell costimulation through increased localization of TCR/class II complexes to the central supramolecular activation cluster and exclusion of CD45 from the immunological synapse. J Immunol. 2007;179:1616-1624.
56. Wang C, Kang SG, Lee J, et al. The roles of CCR6 in migration of Th17 cells and regulation of effector T-cell balance in the gut. Mucosal Immunol. 2009;2:173-183.
57. Monks CR, Freiberg BA, Kupfer H, et al. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature. 1998;395:82-86.
58. Salomon B, Bluestone JA. LFA-1 interaction with ICAM-1 and ICAM-2 regulates Th2 cytokine production. J Immunol. 1998;161:5138-5142.
59. Marski M, Kandula S, Turner JR, et al. CD18 is required for optimal development and function of CD4+CD25+ T regulatory cells. J Immunol. 2005;175:7889-7897.
60. von Andrian UH, Mackay CR. T-cell function and migration. Two sides of the same coin. N Engl J Med. 2000;343:1020-1034.
61. Catalina MD, Carroll MC, Arizpe H, et al. The route of antigen entry determines the requirement for L-selectin during immune responses. J Exp Med. 1996;184:2341-2351.
62. Szanto S, Gal I, Gonda A, et al. Expression of L-selectin, but not CD44, is required for early neutrophil extravasation in antigen-induced arthritis. J Immunol. 2004;172:6723-6734.
63. Mora C, Grewal IS, Wong FS, et al. Role of L-selectin in the development of autoimmune diabetes in non-obese diabetic mice. Int Immunol. 2004; 16:257-264.
64. Annacker O, Coombes JL, Malmstrom V, et al. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J Exp Med. 2005; 202:1051-1061.
65. Andrew DP, Rott LS, Kilshaw PJ, et al. Distribution of alpha 4 beta 7 and alpha E beta 7 integrins on thymocytes, intestinal epithelial lymphocytes and peripheral lymphocytes. Eur J Immunol. 1996;26:897-905.
66. Dutt S, Ermann J, Tseng D, et al. L-selectin and beta7 integrin on donor CD4 T cells are required for the early migration to host mesenteric lymph nodes and acute colitis of graft-versus-host disease. Blood. 2005;106:4009-4015.
67. Wang Y, Li D, Nurieva R, et al. LFA-1 affinity regulation is necessary for the activation and proliferation of naive T cells. J Biol Chem. 2009;284: 12645-12653.
68. Kunkel EJ, Ramos CL, Steeber DA, et al. The roles of L-selectin, beta 7 integrins, and P-selectin in leukocyte rolling and adhesion in high endothelial venules of Peyer's patches. J Immunol. 1998;161:2449-2456.
69. Kawachi S, Morise Z, Jennings SR, et al. Cytokine and adhesion molecule expression in SCID mice reconstituted with CD4+ T cells. Inflamm Bowel Dis. 2000;6:171-180.
70. Kawachi S, Jennings S, Panes J, et al. Cytokine and endothelial cell adhesion molecule expression in interleukin-10-deficient mice. Am J Physiol Gastrointest Liver Physiol. 2000;278:G734-G743.
71. Sans M, Panes J, Ardite E, et al. VCAM-1 and ICAM-1 mediate leukocyteendothelial cell adhesion in rat experimental colitis. Gastroenterology. 1999; 116:874-883.
72. Shigematsu T, Specian RD, Wolf RE, et al. MAdCAM mediates lymphocyte-endothelial cell adhesion in a murine model of chronic colitis. Am J Physiol Gastrointest Liver Physiol. 2001;281:G1309-G1315.
73. Burns RC, Rivera-Nieves J, Moskaluk CA, et al. Antibody blockade of ICAM-1 and VCAM-1 ameliorates inflammation in the SAMP-1/Yit adoptive transfer model of Crohn's disease in mice. Gastroenterology. 2001;121:1428-1436.
74. Matsuzaki K, Tsuzuki Y, Matsunaga H, et al. In vivo demonstration of T lymphocyte migration and amelioration of ileitis in intestinal mucosa of SAMP1/Yit mice by the inhibition of MAdCAM-1. Clin Exp Immunol. 2005;140:22-31.
75. Soriano A, Salas A, Salas A, et al. VCAM-1, but not ICAM-1 or MAd-CAM-1, immunoblockade ameliorates DSS-induced colitis in mice. Lab Invest. 2000;80:1541-1551.
76. Gulubova MV, Manolova IM, Vlaykova TI, et al. Adhesion molecules in chronic ulcerative colitis. Int J Colorectal Dis. 2007;22:581-589.
77. Jones SC, Banks RE, Haidar A, et al. Adhesion molecules in inflammatory bowel disease. Gut. 1995;36:724-730.
78. Littman DR, Rudensky AY. Th17 and regulatory T cells in mediating and restraining inflammation. Cell. 2010;140:845-858.
79. Nemoto Y, Kanai T, Makita S, et al. Bone marrow retaining colitogenic CD4+ T cells may be a pathogenic reservoir for chronic colitis. Gastroenterology. 2007;132:176-189.