Mice with a selective deletion of the CC chemokine receptors 5 or 2 are protected from dextran sodium sulfate-mediated colitis: Lack of CC chemokine receptor 5 expression results in a NK1.1+ lymphocyte-associated Th2-type immune response in the intestine

Journal of Immunology

Volumn 164, Issue 12, 2000, Pages 6303-6312

  Andres, Pietro G ^a   Beck, Paul L ^a   Mizoguchi, Emiko ^b   Mizoguchi, Atsushi ^b   Bhan, Atul K ^b   Dawson, Tracey ^c   Kuziel, William A ^d   Maeda, Nobuyo ^c   MacDermott, Richard P ^a,e   Podolsky, Daniel K ^a   Reinecker, Hans Christian ^a,b  

^a Center for Inflammatory Bowel Disease   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^e ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR5; DEXTRAN SULFATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLITIS; FEMALE; IMMUNE RESPONSE; LYMPHOCYTIC INFILTRATION; MACROPHAGE MIGRATION; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION; TH2 CELL;

EID: 0034659767     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.164.12.6303     Document Type: Article

References (66)

1. Kim, C. H., and H. E. Broxmeyer. 1999. Chemokines: signal lamps for trafficking of T and B cells for development and effector function. J. Leukocyte Biol. 65:6.
2. Lukacs, N. W., R. M. Strieter, S. W. Chensue, and S. L. Kunkel. 1996. Activation and regulation of chemokines in allergic airway inflammation. J. Leukocyte Biol. 59:13.
3. Taub, D. D., S. M. Turcovski-Corrales, M. L. Key, D. L. Longo, and W. J. Murphy. 1996. Chemokines and T lymphocyte activation. 1. β Chemokines costimulale human T lymphocyte activation in vitro. J. Immunol. 156:2095.
4. MacDermott, R. P., I. R. Sanderson, and H. C. Reinecker. 1998. The central role of chemokines (chemotactic cytokines) in the immunopathogenesis of ulcerative colitis and Crohn's disease. Inflamm. Bowel Dis. 4:54.
5. Premack, B. A., and T. J. Schall. 1996. Chemokine receptors: gateways to inflammation and infection. Nat. Med. 2:1174.
6. Charo, I. F., S. J. Myers, A. Herman, C. Franci, A. J. Connolly, and S. R. Coughlin. 1994. Molecular cloning and functional expression of two monoeyte chemoattractant protein I receptors reveals alternative splicing of the carboxyl-terminal tails. Proc. Natl. Acad. Sci. USA 91:2752.
7. Connor, R. I., K. E. Sheridan, D. Ceradini, S. Choc, and N. R. Landau. 1997. Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J. Exp. Med. 185:621.
8. Doranz, B. J., J. Rucker, Y. Yi, R. J. Smyth, M. Samson, S. C. Peiper, M. Parmentier, R. G. Collman, and R. W. Doms. 1996. A dual-tropic primary HIV-1 isolate that uses fusin and the β-chemokine receptors CKR-5, CKR-3, and CKR-2h as fusion cofactors. Cell 85:1149.
9. Reinecker, H. C., E. Y. Loh, D. J. Ringler, A. Mehta, J. L. Rombeau, and R. P. MacDermott. 1995. Monocyte-chemoattractant protein 1 gene expression in intestinal epithelial cells and inflammatory bowel disease mucosa. Gastroenterology 108:40.
10. Wedemeyer, J., A. Lorentz, M. Goke, P. N. Meier, P. Flemming, C. A. Dahinden, M. P. Manns, and S. C. Bischoff. 1999. Enhanced production of monocyte chemotactic protein 3 in inflammatory bowel disease mucosa. Gut 44:629.
11. Yoshimura, T., E. A. Robinson, S. Tanaka, E. Appella, J. Kuratsu, and E. J. Leonard. 1989. Purification and amino acid analysis of two human glioma-derived monocyte chemoattractants. J. Exp. Med. 169:1449.
12. Matsushima, K., C. G. Larsen, G. C. DuBois, and J. J. Oppenheim. 1989. Purification and characterization of a novel monocyte chemotactic and activating factor produced by a human myelomonocytic cell line. J. Exp. Med. 169:1485.
13. Allavena, P., G. Bianchi, D. Zhou, J. van Damme, P. Jilek, S. Sozzani, and A. Mantovani. 1994. Induction of natural killer cell migration by monocyte chemotactic protein-1, -2 and -3. Eur. J. Immunol. 24:3233.
14. Carr, M. W., S. J. Roth, E. Luther, S. S. Rose, and T. A. Springer. 1994. Monocyte chemoattractant protein I acts as a T-lymphocyte chemoattractant. Proc. Natl. Acad. Sci. USA 91:3652.
15. Proost, P., A. Wuyts, and J. Van Damme. 1996. Human monocyte chemotactic proteins-2 and -3: structural and functional comparison with MCP-I. J. Leukocyte Biol. 59:67.
16. Sica, A., A. Saccani, A. Borsatti, C. A. Power, T. N. Wells, W. Luini, N. Polentarulti, S. Sozzani, and A. Mantovani. 1997. Bacterial lipopolysaccharide rapidly inhibits expression of C-C chemokine receptors in human monocytes. J. Exp. Med 185:969.
17. Denholm, E. M., and G. P. Stankus. 1995. Changes in the expression of MCP-1 receptors on monocytic THP-1 cells following differentiation to macrophages with phorbol myristate acetate. Cytokine 7:436.
18. Tangirala, R. K., K. Murao, and O. Quehenberger. 1997. Regulation of expression of the human monocyte chemotactic protein-1 receptor (hCCR2) by cytokines. J. Biol. Chem. 272:8050.
19. Loetscher, P., M. Seitz, M. Baggiolini, and B. Moser. 1996. Interleukin-2 regulates CC chemokine receptor expression and chemotactic responsiveness in T lymphocytes. J. Exp. Med. 184:569.
20. Raport, C. J., J. Gosling, V. L. Schweickart, P. W. Gray, and I. F. Charo. 1996. Molecular cloning and functional characterization of a novel human CC chemokine receptor (CCR5) for RANTES. MIP-1β. and MIP-lα. J. Biol. Chem. 271: 17161.
21. Kolios, G., K. L. Wright, N. J. Jordan, J. B. Leithead, D. A. Robertson, and J. Westwick. 1999. C-X-C and C-C chemokine expression and secretion by the human colonic epithelial cell line. HT-29: differential effect of T lymphocyte-derived cytokines. Eur. J. Immunol. 29:530.
22. Yang, S. K., L. Eckmann, A. Panja, and M. F. Kagnoff. 1997. Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 113:1214.
23. Mazzucchelli, L., C. Hauser, K. Zgraggen, H. E. Wagner, M. W. Hess, J. A. Laissue, and C. Mueller. 1996. Differential in situ expression of the genes encoding the chemokines MCP-1 and RANTES in human inflammatory bowel disease. J. Pathol. 178:201.
24. Berrebi, D., A. Banerjee, R. Paris, F. Potet, Y. Aigrain, D. Emilie, J. P. Cezard, J. P. Hugot, J. Navarro, and M. Peuchmaur. 1997. In situ Rantes and interferon-γ gene expression in pediatric small bowel Crohn's disease. J. Pediatr. Gastroenterol. Nutr. 25:371.
25. Vainer, B., O. H. Nielsen, and T. Horn. 1998. Expression of E-selectin, sialyl Lewis X, and macrophage inflammatory protein-1α by colonic epithelial cells in ulcerativc colitis. Dig. Dis. Sci. 43:596
26. Schrum, S., P. Probst, B. Fleischer, and P. F. Zipfel. 1996. Synthesis of the CC-chemokines MIP-1α, MIP-1β, and RANTES is associated with a type 1 immune response. J. Immunol. 157:3598.
27. Schall, T. J., K. Bacon, R. D. Camp, J. W. Kaspari, and D. V. Goeddel. 1993. Human macrophage inflammatory protein α (MIP-lα) and MIP-1β chemokines attract distinct populations of lymphocytes. J. Exp. Med. 177:1821.
28. + T cells in response to MIP-1α and MIP-1β. Science 260:355.
29. Qin, S., J. B. Rottman, P. Myers, N. Kassam, M. Weinblatt, M. Loetscher, A. E. Koch, B. Moser, and C. R. Mackay. 1998. The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J. Clin. Invest. 101:746.
30. Kuziel, W. A., S. J. Morgan, T. C. Dawson, S. Griffin, O. Smithies, K. Ley, and N. Maeda. 1997. Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc. Natl. Acad. Sci. USA 94:12053.
31. Mashimo, H., D. C. Wu, D. K, Podolsky, and M. C. Fishman. 1996. Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science 274:262.
32. Okayasu, I., S. Hatakeyama, M. Yamada, T. Ohkusa, Y. Inagaki, and R. Nakaya. 1990. A novel method in the induction of reliable experimental acute and chronic ulcerativc colitis in mice. Gastroenterology 98:694.
33. Mahler, M., I. J. Bristol, E. H. Leiter, A. E. Workman, E. H. Birkenmeier, C. O. Elson, and J. P. Sundberg. 1998. Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis. Am. J. Physiol. 274:G544.
34. Bradley, P. P., D. A. Priebat, R. D. Christensen, and G. Rothstein. 1982. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J. Invest. Dermatol. 78:206.
35. Mombaerts, P., E. Mizoguchi, M. J. Grusby, L. H. Glimcher, A. K. Bhan, and S. Tonegawa. 1993. Spontaneous development of inflammatory bowel disease in T cell receptor mutant mice. Cell 75:274.
36. Mizoguchi, A., E. Mizoguchi, C. Chiba, G. M. Spiekermann, S. Tonegawa, C. Nagler-Anderson, and A. K. Bhan. 1996. Cytokine imbalance and autoantibody production in T cell receptor-α mutant mice with inflammatory bowel disease. J. Exp. Med. 183:847.
37. Rollins, B. J. 1997. Chemokines. Blood 90:909.
38. Cacalano, G., J. Lee, K. Kikly, A. M. Ryan, S. Pitts-Meek, B. Hultgren, W. I. Wood, and M. W. Moore. 1994. Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. [Published erratum appears in 1995 Science 270:365.] Science 265:682.
39. Gao, J. L., T. A. Wynn, Y. Chang, E. J. Lee, H. E. Broxmeyer, S. Cooper, H. L. Tiffany, H. Westphal, J. Kwon-Chung, and P. M. Murphy. 1997. Impaired host defense, hematopoiesis, granulomatous inflammation and type 1-type 2 cytokine balance in mice lacking CC chemokine receptor I. J. Exp. Med. 185:1959.
40. Rothenberg, M. E., J. A. MacLean, E. Pearlman, A. D. Luster, and P. Leder. 1997. Targeted disruption of the chemokine eotaxin partially reduces antigen-induced tissue eosinophilia. J. Exp. Med. 185:785.
41. Nagasawa, T., S. Hirota, K. Tachibana, N. Takakura, S. Nishikawa, Y. Kitamura, N. Yoshida, H. Kikutani, and T. Kishimoto. 1996. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/ SDF-1. Nature 382:635.
42. Cook, D. N., M. A. Beck, T. M. Coffman, S. L. Kirby, J. F. Sheridan, I. B. Pragnell, and O. Smithies. 1995. Requirement of MIP-1α for an inflammatory response to viral infection. Science 269:1583.
43. Elson, C. O., R. B. Sartor, G. S. Tennyson, and R. H. Riddell. 1995. Experimental models of inflammatory bowel disease. Gastroenterology 109:1344.
44. + T cells produce large amounts of IL-4 and IFN-γ upon activation by anti-CD3 or CDI. J. Immunol. 159:2240.
45. +) T cells established from murine tumor-infiltrating lymphocytes. J. Immunol. 158:4846.
46. + T cells in a transfer model of colitis. J. Immunol. 161:3256.
47. Chizzolini, C., R. Chicheportiche, D. Burger, and J. M. Dayer. 1997. Human Th1 cells preferentially induce interleukin (1L)-1β while Th2 cells induce IL-1 receptor antagonist production upon cell/cell contact with monocytes. Eur. J. Immunol. 27:171.
48. Siveke, J. T., and A. Hamann. 1998. T helper 1 and T helper 2 cells respond differentially to chemokines. J. Immunol. 160:550.
49. Loetscher, P., M. Uguccioni, L. Bordoli, M. Baggiolini, B. Moser, C. Chizzolini, and J. M. Dayer. 1998. CCR5 is characteristic of Th1 lymphocytes. Nature 391: 344.
50. Ward, S. G., and J. Westwick. 1998. Chemokines: understanding their role in T-lymphocyte biology. Biochem. J. 333:457.
51. Sallusto, F., C. R. Mackay, and A. Lanzavecchia. 1997. Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science 277:2005.
52. Bonecchi, R., G. Blanchi, P. P. Bordignon, D. D'Ambrosio, R. Lang, A. Borsatti, S. Sozzani, P. Allavena, P. A. Gray, A. Mantovani, and F. Sinigaglia. 1998. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med. 187:129.
53. Gerber, B. O., M. P. Zanni, M. Uguccioni, M. Loetscher, C. R. Mackay, W. J. Pichler, N. Yawalkar, M. Baggiolini, and B. Moser. 1997. Functional expression of the eotaxin receptor CCR3 in T lymphocytes co-localizing with eosinophils. Curr. Biol. 7:836.
54. Abbas, A. K., K. M. Murphy, and A. Sher. 1996. Functional diversity of helper T lymphocytes. Nature 383:787.
55. Strober, W., B. R. Ludviksson, and I. J. Fuss. 1998. The pathogenesis of mucosal inflammation in murine models of inflammatory bowel disease and Crohn disease. Ann. Intern. Med. 128:848.
56. Obermeier, F., G. Kojouharoff, W. Hans, J. Scholmerich, V. Gross, and W. Falk, 1999. Interferon-γ (lFN-γ)- and tumour necrosis factor (TNF)-induced nitric oxide as toxic effector molecule in chronic dextran sulphate sodium (DSS)-induced colitis in mice. Clin. Exp. Immunol. 116:238.
57. Guler, M. L., J. D. Gorham, C. S. Hsieh, A. J. Mackey, R. G. Steen, W. F. Dietrich, and K. M. Murphy. 1996. Genetic susceptibility to Leishmania: IL-12 responsiveness in TH1 cell development. Science 271:984.
58. Zhou, Y., T. Kurihara, R. P. Ryseck, Y. Yang, C. Ryan, J. Loy, G. Warr, and R. Bravo. 1998. Impaired macrophage function and enhanced T cell-dependent immune response in mice lacking CCR5, the mouse homologue of the major HIV-1 coreceptor. J. Immunol. 160:4018.
59. Mizoguchi, A., E. Mizoguchi, R. N. Smith, F. I. Prefer, and A. K. Bhan. 1997. Suppressive role of B cells in chronic colitis of T cell receptor mutant mice. J. Exp. Med. 186:1749.
60. Boring, L., J. Gosling, S. W. Chensue, S. L. Kunkel, R. V. Farese, Jr., H. E. Broxmeyer, and I. F. Charo. 1997. Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J. Clin. Invest. 100:2552.
61. Warmington, K. S., L. Boring, J. H. Ruth, J. Sonstein, C. M. Hogaboam, J. L. Curtis, S. L. Kunkel, I. R. Charo, and S. W. Chensue. 1999. Effect of C-C chemokine receptor 2 (CCR2) knockout on type-2 (schistosomal antigen-elicited) pulmonary granuloma formation: analysis of cellular recruitment and cytokine responses. Am. J. Pathol. 154:1407.
62. Kurihara, T., G. Warr, J. Loy, and R. Bravo. 1997. Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor. J. Exp. Med. 186:1757.
63. Brynskov, J., O. H. Nielsen, I. Ahnfelt-Ronne, and K. Bendtzen. 1994. Cytokines (immunoinflammatory hormones) and their natural regulation in inflammatory bowel disease (Crohn's disease and ulcerative colitis): a review. Dig. Dis. 12:290.
64. Lentsch, A. B., T. P. Shanley, V. Sarma, and P. A. Ward. 1997. In vivo suppression of NF-κB and preservation of IκBα by interleukin-10 and interleukin-13. J. Clin. Invest. 100:2443.
65. Kuhn, R., J. Lohler, D. Rennick, K. Rajewsky, and W. Muller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75:263.
66. + TH1-like responses. J. Clin. Invest. 98:1010.