Intestinal-Specific TNFα Overexpression Induces Crohn's-Like Ileitis in Mice

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Bamias, Giorgos ^a   Dahman, Mohamed I ^b   Arseneau, Kristen O ^c   Guanzon, Mitchell ^c   Gruska, Dennis ^c   Pizarro, Theresa T ^c   Cominelli, Fabio ^c  

^a UNIVERSITY OF ATHENS   (Greece)

^b Mercy Health System   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD69 ANTIGEN; CYTOKINE; FAS LIGAND; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 5; L SELECTIN; TUMOR NECROSIS FACTOR ALPHA; BIOLOGICAL MARKER;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CHRONIC INFLAMMATION; CROHN DISEASE; CYTOKINE PRODUCTION; DISEASE SEVERITY; GENE OVEREXPRESSION; HISTOPATHOLOGY; HOMOZYGOSITY; ILEITIS; IMMUNOPATHOGENESIS; IMMUNOPHENOTYPING; INTESTINE EPITHELIUM; INTESTINE MUCOSA; INTESTINE VILLUS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SUBPOPULATION; MESENTERY LYMPH NODE; MOUSE; MOUSE MUTANT; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHENOTYPE; SEVERE COMBINED IMMUNODEFICIENCY; TH1 CELL; TH2 CELL; WILD TYPE; ANIMAL; ANTIBODY SPECIFICITY; APOPTOSIS; CD4 LYMPHOCYTE COUNT; DISEASE MODEL; GENETICS; HUMAN; IMMUNOCOMPROMISED PATIENT; IMMUNOLOGY; INTESTINE; LYMPH NODE; METABOLISM; MUTATION; PATHOLOGY; SCID MOUSE;

ADOPTIVE TRANSFER; ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; CD4 LYMPHOCYTE COUNT; CROHN DISEASE; DISEASE MODELS, ANIMAL; HUMANS; ILEITIS; IMMUNOCOMPROMISED HOST; INTESTINAL MUCOSA; INTESTINES; LYMPH NODES; MICE, SCID; MUTATION; ORGAN SPECIFICITY; TH1 CELLS; TH2 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84882609582     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072594     Document Type: Article

References (33)

1. Bamias G, Nyce MR, De La Rue SA, Cominelli F, American College of P, et al. (2005) New concepts in the pathophysiology of inflammatory bowel disease. Ann Intern Med 143: 895-904.
2. Papadakis KA, Targan SR, (2000) Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu Rev Med 51: 289-298. doi:10.1146/annurev.med.51.1.289. PubMed: 10774465.
3. Locksley RM, Killeen N, Lenardo MJ, (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104: 487-501. doi:10.1016/S0092-8674(01)00237-9. PubMed: 11239407.
4. Matsuda R, Koide T, Tokoro C, Yamamoto T, Godai T, et al. (2009) Quantitative cytokine mRNA expression profiles in the colonic mucosa of patients with steroid naive ulcerative colitis during active and quiescent disease. Inflamm Bowel Dis 15: 328-334. doi:10.1002/ibd.20759. PubMed: 18942752.
5. Raddatz D, Bockemühl M, Ramadori G, (2005) Quantitative measurement of cytokine mRNA in inflammatory bowel disease: relation to clinical and endoscopic activity and outcome. Eur J Gastroenterol Hepatol 17: 547-557. doi:10.1097/00042737-200505000-00012. PubMed: 15827446.
6. Neurath MF, Fuss I, Pasparakis M, Alexopoulou L, Haralambous S, et al. (1997) Predominant pathogenic role of tumor necrosis factor in experimental colitis in mice. Eur J Immunol 27: 1743-1750. doi:10.1002/eji.1830270722. PubMed: 9247586.
7. Kontoyiannis D, Pasparakis M, Pizarro TT, Cominelli F, Kollias G, (1999) Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 10: 387-398. doi:10.1016/S1074-7613(00)80038-2. PubMed: 10204494.
8. Marini M, Bamias G, Rivera-Nieves J, Moskaluk CA, Hoang SB, et al. (2003) TNF-alpha neutralization ameliorates the severity of murine Crohn's-like ileitis by abrogation of intestinal epithelial cell apoptosis. Proc Natl Acad Sci U S A 100: 8366-8371. doi:10.1073/pnas.1432897100. PubMed: 12832622.
9. Colombel JF, Schwartz DA, Sandborn WJ, Kamm MA, D'Haens G, et al. (2009) Adalimumab for the treatment of fistulas in patients with Crohn's disease. Gut 58: 940-948. doi:10.1136/gut.2008.159251. PubMed: 19201775.
10. Rutgeerts P, Sandborn WJ, Feagan BG, Reinisch W, Olson A, et al. (2005) Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med 353: 2462-2476. doi:10.1056/NEJMoa050516. PubMed: 16339095.
11. Sandborn WJ, Colombel JF, Enns R, Feagan BG, Hanauer SB, et al. (2005) Natalizumab induction and maintenance therapy for Crohn's disease. N Engl J Med 353: 1912-1925. doi:10.1056/NEJMoa043335. PubMed: 16267322.
12. Sandborn WJ, Hanauer SB, Rutgeerts P, Fedorak RN, Lukas M, et al. (2007) Adalimumab for maintenance treatment of Crohn's disease: results of the CLASSIC II trial. Gut 56: 1232-1239. doi:10.1136/gut.2006.106781. PubMed: 17299059.
13. Targan SR, Hanauer SB, van Deventer SJ, Mayer L, Present DH, et al. (1997) A short-term study of chimeric monoclonal antibody cA2 to tumor necrosis factor alpha for Crohn's disease. Crohn's Disease cA2 Study Group. N Engl J Med 337: 1029-1035. doi:10.1056/NEJM199710093371502. PubMed: 9321530.
14. Chen CY, Shyu AB, (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20: 465-470. doi:10.1016/S0968-0004(00)89102-1. PubMed: 8578590.
15. Kruys V, Marinx O, Shaw G, Deschamps J, Huez G, (1989) Translational blockade imposed by cytokine-derived UA-rich sequences. Science 245: 852-855. doi:10.1126/science.2672333. PubMed: 2672333.
16. Saam JR, Gordon JI, (1999) Inducible gene knockouts in the small intestinal and colonic epithelium. J Biol Chem 274: 38071-38082. doi:10.1074/jbc.274.53.38071. PubMed: 10608876.
17. Kosiewicz MM, Nast CC, Krishnan A, Rivera-Nieves J, Moskaluk CA, et al. (2001) Th1-type responses mediate spontaneous ileitis in a novel murine model of Crohn's disease. J Clin Invest 107: 695-702. doi:10.1172/JCI10956. PubMed: 11254669.
18. Olson TS, Reuter BK, Scott KG, Morris MA, Wang XM, et al. (2006) The primary defect in experimental ileitis originates from a nonhematopoietic source. J Exp Med 203: 541-552. doi:10.1084/jem.20050407. PubMed: 16505137.
19. Jung HC, Eckmann L, Yang SK, Panja A, Fierer J, et al. (1995) A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 95: 55-65. doi:10.1172/JCI117676. PubMed: 7814646.
20. Tan X, Hsueh W, Gonzalez-Crussi F, (1993) Cellular localization of tumor necrosis factor (TNF)-alpha transcripts in normal bowel and in necrotizing enterocolitis. TNF gene expression by Paneth cells, intestinal eosinophils, and macrophages. Am J Pathol 142: 1858-1865. PubMed: 8506954.
21. Roulis M, Armaka M, Manoloukos M, Apostolaki M, Kollias G, (2011) Intestinal epithelial cells as producers but not targets of chronic TNF suffice to cause murine Crohn-like pathology. Proc Natl Acad Sci U S A 108: 5396-5401. doi:10.1073/pnas.1007811108. PubMed: 21402942.
22. Kajino-Sakamoto R, Inagaki M, Lippert E, Akira S, Robine S, et al. (2008) Enterocyte-derived TAK1 signaling prevents epithelium apoptosis and the development of ileitis and colitis. J Immunol 181: 1143-1152. PubMed: 18606667.
23. Nenci A, Becker C, Wullaert A, Gareus R, van Loo G, et al. (2007) Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446: 557-561. doi:10.1038/nature05698. PubMed: 17361131.
24. Zeissig S, Bojarski C, Buergel N, Mankertz J, Zeitz M, et al. (2004) Downregulation of epithelial apoptosis and barrier repair in active Crohn's disease by tumour necrosis factor alpha antibody treatment. Gut 53: 1295-1302. doi:10.1136/gut.2003.036632. PubMed: 15306588.
25. Dotan I, Allez M, Nakazawa A, Brimnes J, Schulder-Katz M, et al. (2007) Intestinal epithelial cells from inflammatory bowel disease patients preferentially stimulate CD4+ T cells to proliferate and secrete interferon-gamma. Am J Physiol Gastrointest Liver Physiol 292: G1630-G1640. doi:10.1152/ajpgi.00294.2006. PubMed: 17347451.
26. Bamias G, Martin C, Mishina M, Ross WG, Rivera-Nieves J, et al. (2005) Proinflammatory effects of TH2 cytokines in a murine model of chronic small intestinal inflammation. Gastroenterology 128: 654-666. doi:10.1053/j.gastro.2004.11.053. PubMed: 15765401.
27. Spencer DM, Veldman GM, Banerjee S, Willis J, Levine AD, (2002) Distinct inflammatory mechanisms mediate early versus late colitis in mice. Gastroenterology 122: 94-105. doi:10.1053/gast.2002.30308. PubMed: 11781285.
28. Mizoguchi E, Hachiya Y, Kawada M, Nagatani K, Ogawa A, et al. (2008) TNF receptor type I-dependent activation of innate responses to reduce intestinal damage-associated mortality. Gastroenterology 134: 470-480. doi:10.1053/j.gastro.2007.11.055. PubMed: 18242213.
29. Naito Y, Takagi T, Handa O, Ishikawa T, Nakagawa S, et al. (2003) Enhanced intestinal inflammation induced by dextran sulfate sodium in tumor necrosis factor-alpha deficient mice. J Gastroenterol Hepatol 18: 560-569. doi:10.1046/j.1440-1746.2003.03034.x. PubMed: 12702049.
30. Pagnini C, Saeed R, Bamias G, Arseneau KO, Pizarro TT, et al. (2010) Probiotics promote gut health through stimulation of epithelial innate immunity. Proc Natl Acad Sci U S A 107: 454-459. doi:10.1073/pnas.0910307107. PubMed: 20018654.
31. Glocker EO, Kotlarz D, Boztug K, Gertz EM, Schäffer AA, et al. (2009) Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N Engl J Med 361: 2033-2045. doi:10.1056/NEJMoa0907206. PubMed: 19890111.
32. Rivera-Nieves J, Bamias G, Vidrich A, Marini M, Pizarro TT, et al. (2003) Emergence of perianal fistulizing disease in the SAMP1/YitFc mouse, a spontaneous model of chronic ileitis. Gastroenterology 124: 972-982. doi:10.1053/gast.2003.50148. PubMed: 12671894.
33. Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE Jr., et al. (1996) Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Invest 98: 945-953. doi:10.1172/JCI118878. PubMed: 8770866.