Differential effects of α4β7 and GPR15 on homing of effector and regulatory T cells from patients with UC to the inflamed gut in vivo

Gut

Volumn 65, Issue 10, 2016, Pages 1642-1664

  Fischer, Anika ^a   Zundler, Sebastian ^a   Atreya, Raja ^a   Rath, Timo ^a   Voskens, Caroline ^a   Hirschmann, Simon ^a   López Posadas, Rocío ^a   Watson, Alastair ^b   Becker, Christoph ^a   Schuler, Gerold ^a   Neufert, Clemens ^a   Atreya, Imke ^a   Neurath, Markus F ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA4 BETA7 INTEGRIN; CD4 ANTIGEN; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 15; INTEGRIN; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 7 RECEPTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VEDOLIZUMAB; CELL SURFACE RECEPTOR; GASTROINTESTINAL AGENT; GPR15 PROTEIN, MOUSE; HOMING RECEPTOR; INTEGRIN ALPHA4BETA7; MONOCLONAL ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL HOMING; CELL MIGRATION; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CROHN DISEASE; EFFECTOR CELL; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LAMINA PROPRIA; MONONUCLEAR CELL; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; ULCERATIVE COLITIS; ANIMAL; BLOOD; DRUG EFFECTS; IMMUNOLOGY; INTESTINE MUCOSA; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; COLITIS, ULCERATIVE; CROHN DISEASE; GASTROINTESTINAL AGENTS; HUMANS; INTEGRINS; INTESTINAL MUCOSA; MICE; MODELS, ANIMAL; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, LYMPHOCYTE HOMING; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 84938099850     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2015-310022     Document Type: Article

References (52)

1. Thomas S, Baumgart DC. Targeting leukocyte migration and adhesion in Crohn's disease and ulcerative colitis. Inflammopharmacology 2012;20:1-18.
2. Ley K, Laudanna C, Cybulsky MI, et al. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007;7:678-89.
3. Danese S. New therapies for inflammatory bowel disease: from the bench to the bedside. Gut 2012;61:918-32.
4. Strober W, Fuss I, Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest 2007;117:514-21.
5. Baumgart DC, Sandborn WJ. Crohn's disease. Lancet 2012;380:1590-605.
6. Macdonald TT, Monteleone G. Immunity, inflammation, and allergy in the gut. Science 2005;307:1920-5.
7. Dustin ML, Bromley SK, Kan Z, et al. Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc Natl Acad Sci USA 1997;94:3909-13.
8. Egawa G, Honda T, Tanizaki H, et al. In vivo imaging of T-cell motility in the elicitation phase of contact hypersensitivity using two-photon microscopy. J Invest Dermatol 2011;131:977-9.
9. Weninger W, Biro M, Jain R. Leukocyte migration in the interstitial space of non-lymphoid organs. Nat Rev Immunol 2014;14:232-46.
10. Nourshargh S, Hordijk PL, Sixt M. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat Rev Mol Cell Biol 2010;11:366-78.
11. Haddad W, Cooper CJ, Zhang Z, et al. P-selectin and P-selectin glycoprotein ligand 1 are major determinants for Th1 cell recruitment to nonlymphoid effector sites in the intestinal lamina propria. J Exp Med 2003;198:369-77.
12. Kempster SL, Kaser A. alpha4beta7 integrin: beyond T cell trafficking. Gut 2014;63:1377-9.
13. Agace WW. Tissue-tropic effector T cells: generation and targeting opportunities. Nat Rev Immunol 2006;6:682-92.
14. Villablanca EJ, De Calisto J, Torregrosa Paredes P, et al. beta7 integrins are required to give rise to intestinal mononuclear phagocytes with tolerogenic potential. Gut 2014;63:1431-40.
15. Hamann A, Andrew DP, Jablonski-Westrich D, et al. Role of alpha 4-integrins in lymphocyte homing to mucosal tissues in vivo. J Immunol 1994;152:3282-93.
16. Podolsky DK, Lobb R, King N, et al. Attenuation of colitis in the cotton-top tamarin by anti-alpha 4 integrin monoclonal antibody. J Clin Invest 1993;92:372-80.
17. Picarella D, Hurlbut P, Rottman J, et al. Monoclonal antibodies specific for beta 7 integrin and mucosal addressin cell adhesion molecule-1 (MAdCAM-1) reduce inflammation in the colon of scid mice reconstituted with CD45RBhigh CD4+ T cells. J Immunol 1997;158:2099-106.
18. 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;111:1373-80.
19. 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.
20. Sandborn WJ, Colombel JF, Enns R, et al. Natalizumab induction and maintenance therapy for Crohn's disease. N Engl J Med 2005;353:1912-25.
21. Ghosh S, Goldin E, Gordon FH, et al. Natalizumab for active Crohn's disease. N Engl J Med 2003;348:24-32.
22. Van Assche G, Van Ranst M, Sciot R, et al. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn's disease. N Engl J Med 2005;353:362-8.
23. Feagan BG, Rutgeerts P, Sands BE, et al. Vedolizumab as induction and maintenance therapy for ulcerative colitis. N Engl J Med 2013;369:699-710.
24. Sandborn WJ, Feagan BG, Rutgeerts P, et al. Vedolizumab as induction and maintenance therapy for Crohn's disease. N Engl J Med 2013;369:711-21.
25. Wyant T, Yang L, Fedyk E. In vitro assessment of the effects of vedolizumab binding on peripheral blood lymphocytes. MAbs 2013;5:842-50.
26. Wyant T, Leach T, Sankoh S, et al. Vedolizumab affects antibody responses to immunisation selectively in the gastrointestinal tract: randomised controlled trial results. Gut 2015;64:77-83.
27. Rutgeerts PJ, Fedorak RN, Hommes DW, et al. A randomised phase I study of etrolizumab (rhuMAb beta7) in moderate to severe ulcerative colitis. Gut 2013;62:1122-30.
28. Vermeire S, O'Byrne S, Keir M, et al. Etrolizumab as induction therapy for ulcerative colitis: a randomised, controlled, phase 2 trial. Lancet 2014;384:309-18.
29. Maul J, Loddenkemper C, Mundt P, et al. Peripheral and intestinal regulatory CD4+ CD25(high) T cells in inflammatory bowel disease. Gastroenterology 2005;128:1868-78.
30. Li Z, Arijs I, De Hertogh G, et al. Reciprocal changes of Foxp3 expression in blood and intestinal mucosa in IBD patients responding to infliximab. Inflamm Bowel Dis 2010;16:1299-310.
31. Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol 2014;14:329-42.
32. Desreumaux P, Foussat A, Allez M, et al. Safety and efficacy of antigen-specific regulatory T-cell therapy for patients with refractory Crohn's disease. Gastroenterology 2012;143:1207-17 e1-2.
33. Kim SV, Xiang WV, Kwak C, et al. GPR15-mediated homing controls immune homeostasis in the large intestine mucosa. Science 2013;340:1456-9.
34. Gerlach K, Hwang Y, Nikolaev A, et al. TH9 cells that express the transcription factor PU.1 drive T cell-mediated colitis via IL-9 receptor signaling in intestinal epithelial cells. Nat Immunol 2014;15:676-86.
35. Atreya R, Mudter J, Finotto S, et al. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in crohn disease and experimental colitis in vivo. Nat Med 2000;6: 583-8.
36. Tidswell M, Pachynski R, Wu SW, et al. Structure-function analysis of the integrin beta 7 subunit: identification of domains involved in adhesion to MAdCAM-1. J Immunol 1997;159:1497-505.
37. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translational biomedical research. Nat Rev Immunol 2007;7:118-30.
38. Wirtz S, Neufert C, Weigmann B, et al. Chemically induced mouse models of intestinal inflammation. Nat Protoc 2007;2:541-6.
39. Wang Y, Liu XP, Zhao ZB, et al. Expression of CD4+ forkhead box P3 (FOXP3)+ regulatory T cells in inflammatory bowel disease. J Dig Dis 2011;12:286-94.
40. Jovani M, Danese S. Vedolizumab for the treatment of IBD: a selective therapeutic approach targeting pathogenic a4b7 cells. Curr Drug Targets 2013;14:1433-43.
41. Oki M, Ohtani H, Kinouchi Y, et al. Accumulation of CCR5+ T cells around RANTES+ granulomas in Crohn's disease: a pivotal site of Th1-shifted immune response? Lab Invest 2005;85:137-45.
42. Papadakis KA, Prehn J, Moreno ST, et al. CCR9-positive lymphocytes and thymus-expressed chemokine distinguish small bowel from colonic Crohn's disease. Gastroenterology 2001;121:246-54.
43. Pryde SE, Duncan SH, Hold GL, et al. The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 2002;217:133-9.
44. Fuss IJ, Strober W. The role of IL-13 and NK T cells in experimental and human ulcerative colitis. Mucosal immunol 2008;1(Suppl 1):S31-3.
45. Kanai T, Nemoto Y, Kamada N, et al. Homeostatic (IL-7) and effector (IL-17) cytokines as distinct but complementary target for an optimal therapeutic strategy in inflammatory bowel disease. Curr Opin Gastroenterol 2009;25:306-13.
46. Rott LS, Briskin MJ, Andrew DP, et al. A fundamental subdivision of circulating lymphocytes defined by adhesion to mucosal addressin cell adhesion molecule-1. Comparison with vascular cell adhesion molecule-1 and correlation with beta 7 integrins and memory differentiation. J Immunol 1996;156:3727-36.
47. Hoshino H, Kobayashi M, Mitoma J, et al. An integrin alpha4beta7∗IgG heterodimeric chimera binds to MAdCAM-1 on high endothelial venules in gut-associated lymphoid tissue. J Histochem Cytochem 2011;59:572-83.
48. Neurath MF. New targets for mucosal healing and therapy in inflammatory bowel diseases. Mucosal Immunol 2014;7:6-19.
49. Babyatsky MW, Rossiter G, Podolsky DK. Expression of transforming growth factors alpha and beta in colonic mucosa in inflammatory bowel disease. Gastroenterology 1996;110:975-84.
50. Canavan JB, Scotta C, Vossenkamper A, et al. Developing in vitro expanded CD45RA+ regulatory T cells as an adoptive cell therapy for Crohn's disease. Gut Published Online First: 24 Feb 2015. http://dx.doi.org/10.1136/gutjnl-2014-306919
51. Fantini MC, Becker C, Tubbe I, et al. Transforming growth factor beta induced FoxP3+ regulatory T cells suppress Th1 mediated experimental colitis. Gut 2006;55:671-80.
52. Nguyen LP, Pan J, Dinh TT, et al. Role and species-specific expression of colon T cell homing receptor GPR15 in colitis. Nat Immunol 2015;16:207-13.