Maturation of the mucosal immune system underlies colitis susceptibility in interleukin-10-deficient (IL-10-/-) mice

Journal of Leukocyte Biology

Volumn 82, Issue 2, 2007, Pages 311-319

  Etling, Michele R ^a   Davies, Sarah ^a   Campbell, Melanie ^a   Redline, Raymond W ^a   Fu, Pingfu ^a   Levine, Alan D ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Cytokine; Inflammation

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 23; INTERLEUKIN 4; PROBIOTIC AGENT; PROTEIN P40;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CELL MATURATION; COLITIS; CONTROLLED STUDY; DIARRHEA; DISEASE COURSE; DISEASE PREDISPOSITION; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOPATHOLOGY; IMMUNE SYSTEM; MOUSE; MUCOSA; NONHUMAN; PRIORITY JOURNAL; WEIGHT REDUCTION;

AGING; ANIMALS; CELLS, CULTURED; COLITIS; DISEASE SUSCEPTIBILITY; ENZYME-LINKED IMMUNOSORBENT ASSAY; INFLAMMATION; INTERFERON TYPE II; INTERLEUKIN-10; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; MUCOUS MEMBRANE;

ANIMALIA; MUS;

EID: 34547775237     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0606396     Document Type: Article

References (51)

1. Podolsky, D. K. (2002) Inflammatory bowel disease. N. Engl. J. Med. 347, 417-429.
2. Fiocchi, C. (1997) Intestinal inflammation: a complex interplay of immune and nonimmune cell interactions. Am. J. Physiol. 273, G769-G775.
3. Strober, W., Fuss, I. J., Blumberg, R. S. (2002) The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20, 495-549.
4. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K., Muller, W. (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274.
5. Davidson, N. J., Leach, M. W., Fort, M. M., Thompson-Snipes, L., Kuhn, R., Muller, W., Berg, D. J., Rennick, D. M. (1996) T helper cell 1-type CD4+ T cells, but not B cells, mediate colitis in interleukin 10-deficient mice. J. Exp. Med. 184, 241-251.
6. Davidson, N. J., Hudak, S. A., Lesley, R. E., Menon, S., Leach, M. W., Rennick, D. M. (1998) IL-12, but not IFN-γ, plays a major role in sustaining the chronic phase of colitis in IL-10-deficient mice. J. Immunol. 161, 3143-3149.
7. Yen, D., Cheung, J., Scheerens, H., Poulet, F., McClanahan, T., Mckenzie, B., Kleinschek, M. A., Owyang, A., Mattson, J., Blumenschein, W., Murphy, E., Sathe, M., Cua, D. J., Kastelein, R. A., Rennick, D. (2006) IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 116, 1310-1316.
8. Hue, S., Ahern, P., Buonocore, S., Kullberg, M. C., Cua, D. J., McKenzie, B. S., Powrie, F., Maloy, K. J. (2006) Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203, 2473-2483.
9. Kullberg, M. C., Jankovic, D., Feng, C. G., Hue, S., Gorelick, P. L., McKenzie, B. S., Cua, D. J., Powrie, F., Cheever, A. W., Maloy, K. J., Sher, A. (2006) IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J. Exp. Med. 203, 2485-2494.
10. Sellon, R. K., Tonkonogy, S., Schultz, M., Dieleman, L. A., Grenther, W., Balish, E., Rennick, D. M., Sartor, R. B. (1998) Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect. Immun. 66, 5224-5231.
11. Berg, D. J., Davidson, N., Kuhn, R., Muller, W., Menon, S., Holland, G., Thompson-Snipes, L., Leach, M. W., Rennick, D. (1996) Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J. Clin. Invest. 98, 1010-1020.
12. Spencer, D. M., Veldman, G. M., Banerjee, S., Willis, J., Levine, A. D. (2002) Distinct inflammatory mechanisms mediate early versus late colitis in mice. Gastroenterology 122, 94-105.
13. Castle, S., Uyemura, K., Wong, W., Modlin, R., Effros, R. (1997) Evidence of enhanced type 2 immune response and impaired upregulation of a type 1 response in frail elderly nursing home residents. Mech. Ageing Dev. 94, 7-16.
14. Shearer, G. M. (1997) Th1/Th2 changes in aging. Mech. Ageing Dev. 94, 1-5.
15. Frasca, D., Pucci, S., Goso, C., Barattini, P., Barile, S., Pioli, C., Doria, G. (1997) Regulation of cytokine production in aging: use of recombinant cytokines to upregulate mitogen-stimulated spleen cells. Mech. Ageing Dev. 93, 157-169.
16. Kubo, M., Cinader, B. (1990) Polymorphism of age-related changes in interleukin (IL) production: differential changes of T helper subpopulations, synthesizing IL 2, IL 3 and IL 4. Eur. J. Immunol. 20, 1289-1296.
17. Sandmand, M., Bruunsgaard, H., Kemp, K., Andersen-Ranberg, K., Pedersen, A., Skinhoj, P., Pedersen, B. (2002) Is ageing associated with a shift in the balance between Type 1 and Type 2 cytokines in humans? Clin. Exp. Immunol. 127, 107-114.
18. Ginaldi, L., Loreto, M. F., Corsi, M. P., Modesti, M., De Martinis, M. (2001) Immunosenescence and infectious diseases. Microbes Infect. 3, 851-857.
19. Ramos-Casals, M., A García-Carrasco, M., Brito, M. P., López-Soto, A., Font, J. (2003) Autoimmunity and geriatrics: clinical significance of autoimmune manifestations in the elderly. Lupus 12, 341-355.
20. Calkins, B. (1994) Inflammatory bowel diseases. In Digestive Diseases in the United States: Epidemiology and Impact (J. E. Everhart, U.S. National Digestive Diseases Data Working Group, U. S. National Institute of Diabetes and Digestive and Kidney Diseases, eds.), U.S. Department of Health and Human Services, Public Health Service, National Institutes of Health, Bethesda, MD, USA, 511-546.
21. Gazzinelli, R. T., Wysocka, M., Hieny, S., Scharton-Kersten, T., Cheever, A., Kuhn, R., Muller, W., Trinchieri, G., Sher, A. (1996) In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-γ and TNF-α. J. Immunol. 157, 798-805.
22. Cleveland, W. S. (1979) Robust locally weighted regression and smoothing scatterplots. J. Am. Stat. Assoc. 74, 829-836.
23. Diggle, P., Liang, K-Y., Zeger, S. L. (1994) Analysis of Longitudinal Data, Oxford, UK, Oxford University Press.
24. Bibiloni, R., Fedorak, R. N., Tannock, G. W., Madsen, K. L., Gionchetti, P., Campieri, M., De Simone, C., Sartor, R. B. (2005) VSL#3 probioticmixture induces remission in patients with active ulcerative colitis. Am. J. Gastroenterol. 100, 1539-1546.
25. Gionchetti, P., Rizzello, F., Helwig, U., Venturi, A., Lammers, K. M., Brigidi, P., Vitali, B., Poggioli, G., Miglioli, M., Campieri, M. (2003) Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology 124, 1202-1209.
26. Madsen, K., Cornish, A., Soper, P., McKaigney, C., Jijon, H., Yachimec, C., Doyle, J., Jewell, L., De Simone, C. (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121, 580-591.
27. Madsen, K. L., Doyle, J. S., Jewell, L. D., Tavernini, M. M., Fedorak, R. N. (1999) Lactobacillus species prevents colitis in interleukin 10 genedeficient mice. Gastroenterology 116, 1107-1114.
28. Jump, R. L., Levine, A. D. (2002) Murine Peyer's patches favor development of an IL-10-secreting, regulatory T cell population. J. Immunol. 168, 6113-6119.
29. Spencer, D. M., Levine, A. D. (2003) Neutralizing IL-4 or IL-13 alters mucosal immunity in late phase colitis of IL-10-/- mice. FASEB J. 17, C-230.
30. Rennick, D. M., Fort, M. M. (2000) Lessons from genetically engineered animal models. XII. IL-10-deficient (IL-10(-/-)) mice and intestinal inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 278, G829-G833.
31. Bamias, G., Martin, C., Mishina, M., Ross, W. G., Rivera-Nieves, J., Marini, M., Cominelli, F. (2005) Proinflammatory effects of TH2 cytokines in a murine model of chronic small intestinal inflammation. Gastroenterology 128, 654-666.
32. Farrell, R. J., Peppercorn, M. A. (2002) Ulcerative colitis. Lancet 359, 331-340.
33. Loftus, E. V., Schoenfeld, P., Sandborn, W. J. (2002) The epidemiology and natural history of Crohn's disease in population-based patient cohorts from North America: a systematic review. Aliment. Pharmacol. Ther. 16, 51-60.
34. Farmer, R. G., Easley, K., Rankin, G. (1993) Clinical patterns, natural history, and progression of ulcerative colitis. A long-term follow-up of 1116 patients. Dig. Dis. Sci. 38, 1137-1146.
35. Langholz, E., Munkholm, P., Davidsen, M., Nielsen, O., Binder, V. (1996) Changes in extent of ulcerative colitis: a study on the course and prognostic factors. Scand. J. Gastroenterol. 31, 260-266.
36. Hyams, J. S., Davis, P., Grancher, K., Lerer, T., Justinich, C., Markowitz, J. (1996) Clinical outcome of ulcerative colitis in children. J. Pediatr. 129, 81-88.
37. Kugathasan, S., Dubinsky, M. C., Keljo, D., Moyer, M. S., Rufo, P. A., Wyllie, R., Zachos, M., Hyams, J. (2005) Severe colitis in children. J. Pediatr. Gastroenterol. Nutr. 41, 375-385.
38. Kugathasan, S., Itoh, J., Kou, D., Boyle, J. T., Levine, A. D., Fiocchi, C. (1998) IL-12 receptor β2 chain upregulation in mucosal T-cells in early but not late Crohn's disease (CD): implications for variable IFN-γ production during disease progression. Gastroenterology 114, A-1015.
39. Miller, R. A. (1996) The aging immune system: primer and prospectus. Science 273, 70-74.
40. Segal, R., Bermas, B., Dayan, M., Kalush, F., Shearer, G., Mozes, E. (1997) Kinetics of cytokine production in experimental systemic lupus erythematosus: involvement of T helper cell 1/T helper cell 2-type cytokines in disease. J. Immunol. 158, 3009-3016.
41. Segal, R., Dayan, M., Globerson, A., Habut, B., Shearer, G. M., Mozes, E. (1997) Effect of aging on cytokine production in normal and experimental systemic lupus erythematosus afflicted mice. Mech. Ageing Dev. 96, 47-58.
42. Dayan, M., Segal, R., Globerson, A., Habut, B., Shearer, G. M., Mozes, E. (2000) Effect of aging on cytokine production in normal and experimental systemic lupus erythematosus-afflicted mice. Exp. Gerontol. 35, 225-236.
43. Veltkamp, C., Tonkonogy, S. L., De Jong, Y. P., Albright, C., Grenther, W. B., Balish, E., Terhorst, C., Sartor, R. B. (2001) Continuous stimulation by normal luminal bacteria is essential for the development and perpetuation of colitis in Tg(ε26) mice. Gastroenterology 120, 900-913.
44. Aranda, R., Sydora, B., McAllister, P., Binder, S., Yang, H., Targan, S., Kronenberg, M. (1997) Analysis of intestinal lymphocytes in mouse colitis mediated by transfer of CD4+, CD45RBhigh T cells to SCID recipients. J. Immunol. 158, 3464-3473.
45. Rath, H. C., Herfarth, H. H., Ikeda, J. S., Grenther, W. B., Hamm Jr., T. E., Balish, E., Taurog, J. D., Hammer, R. E., Wilson, K. H., Sartor, R. B. (1996) Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human β2 microglobulin transgenic rats. J. Clin. Invest. 98, 945-953.
46. Falk, P. G., Hooper, L. V., Midtvedt, T., Gordon, J. I. (1998) Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol. Mol. Biol. Rev. 62, 1157-1170.
47. Madsen, K. L., Doyle, J. S., Tavernini, M. M., Jewell, L. D., Rennie, R. P., Fedorak, R. N. (2000) Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice. Gastroenterology 118, 1094-1105.
48. Sartor, R. B. (1997) The influence of normal microbial flora on the development of chronic mucosal inflammation. Res. Immunol. 148, 567-576.
49. Kullberg, M. C., Jankovic, D., Gorelick, P. L., Caspar, P., Letterio, J. J., Cheever, A. W., Sher, A. (2002) Bacteria-triggered CD4+ T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196, 505-515.
50. Kullberg, M. C., Ward, J. M., Gorelick, P. L., Caspar, P., Hieny, S., Cheever, A., Jankovic, D., Sher, A. (1998) Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and γ interferon-dependent mechanism. Infect. Immun. 66, 5157-5166.
51. Kim, S. C., Tonkonogy, S. L., Albright, C. A., Tsang, J., Balish, E. J., Braun, J., Huycke, M. M., Sartor, R. B. (2005) Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology 128, 891-906.