Pharmacological intervention studies using mouse models of the inflammatory bowel diseases: Translating preclinical data into new drug therapies

Inflammatory Bowel Diseases

Volumn 17, Issue 5, 2011, Pages 1229-1245

  Koboziev, Iurii ^a   Karlsson, Fridrik ^a   Zhang, Songlin ^a   Grisham, Matthew B ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

biologics; blood flow; cell based therapy; cytokines; regulatory T cells; small molecules; T cells; therapeutics

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR9; DEXTRAN SULFATE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCLONAL ANTIBODY; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR ALPHA;

ANTIINFLAMMATORY ACTIVITY; BASEMENT MEMBRANE; C57BL 6 MOUSE; DELAYED HYPERSENSITIVITY; DRUG BIOAVAILABILITY; DRUG EFFECT; DRUG STABILITY; ENTERITIS; HISTOPATHOLOGY; HUMAN; IMMUNE SYSTEM; INNATE IMMUNITY; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROPHYLAXIS; REGULATORY T LYMPHOCYTE; REVIEW; STUDY DESIGN; T LYMPHOCYTE;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; INFLAMMATORY BOWEL DISEASES; MICE;

EID: 79953873761     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.21557     Document Type: Review

References (107)

1. Kuhn R, Lohler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993; 75: 263-274. (Pubitemid 23320290)
2. Mombaerts P, Mizoguchi E, Grusby MJ, et al. Spontaneous development of inflammatory bowel disease in T cell receptor mutant mice. Cell. 1993; 75: 274-282.
3. Sadlack B, Merz H, Schorle H, et al. Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell. 1993; 75: 253-261. (Pubitemid 23320289)
4. Powrie F, Leach MW, Mauze S, et al. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol. 1993; 5: 1461-1471. (Pubitemid 23325202)
5. Kirsner JB, Elchlepp J., The production of an experimental ulcerative colitis in rabbits. Trans Assoc Am Physicians. 1957; 70: 102-119.
6. Kirsner JB, Elchlepp JG, Goldgraber MB, et al. Production of an experimental ulcerative "colitis" in rabbits. Arch Pathol. 1959; 68: 392-408.
7. Kraft SC, Fitch FW, Kirsner JB., Histologic and immunohistochemical features of the Auer "colitis" in rabbits. Am J Pathol. 1963; 43: 913-927.
8. Elson CO, Cong Y, McCracken VJ, et al. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol Rev. 2005; 206: 260-276. (Pubitemid 41105175)
9. Maxwell JR, Viney JL., Overview of mouse models of inflammatory bowel disease and their use in drug discovery. Curr Protoc Pharmacol. 2009; 47: 5.57.1-5.57.19.
10. Strober W, Fuss IJ, Blumberg RS., The immunology of mucosal models of inflammation. Annu Rev Immunol. 2002; 20: 495-549. (Pubitemid 34293433)
11. Strober W, Fuss I, Mannon P., The fundamental basis of inflammatory bowel disease. J Clin Invest. 2007; 117: 514-521. (Pubitemid 46348505)
12. Uhlig HH, Powrie F., Mouse models of intestinal inflammation as tools to understand the pathogenesis of inflammatory bowel disease. Eur J Immunol. 2009; 39: 2021-2026.
13. Cho JH, Weaver CT., The genetics of inflammatory bowel disease. Gastroenterology. 2007; 133: 1327-1339. (Pubitemid 47494470)
14. Xavier RJ, Podolsky DK., Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007; 448: 427-434. (Pubitemid 47123518)
15. Chidlow JH Jr, Langston W, Greer JJ, et al. Differential angiogenic regulation of experimental colitis. Am J Pathol. 2006; 169: 2014-2030. (Pubitemid 351181962)
16. Siegmund B, Lehr HA, Fantuzzi G., Leptin: a pivotal mediator of intestinal inflammation in mice. Gastroenterology. 2002; 122: 2011-2025. (Pubitemid 34651443)
17. Siegmund B, Sennello JA, Lehr HA, et al. Development of intestinal inflammation in double IL-10- and leptin-deficient mice. J Leukoc Biol. 2004; 76: 782-786. (Pubitemid 39313713)
18. Te Velde AA, de KF, Sterrenburg E, et al. Comparative analysis of colonic gene expression of three experimental colitis models mimicking inflammatory bowel disease. Inflamm Bowel Dis. 2007; 13: 325-330. (Pubitemid 46465914)
19. Vowinkel T, Anthoni C, Wood KC, et al. CD40-CD40 ligand mediates the recruitment of leukocytes and platelets in the inflamed murine colon. Gastroenterology. 2007; 132: 955-965. (Pubitemid 46440860)
20. Hawkey CJ, Dube LM, Rountree LV, et al. A trial of zileuton versus mesalazine or placebo in the maintenance of remission of ulcerative colitis. The European Zileuton Study Group For Ulcerative Colitis. Gastroenterology. 1997; 112: 718-724. (Pubitemid 27113796)
21. Roberts WG, Simon TJ, Berlin RG, et al. Leukotrienes in ulcerative colitis: results of a multicenter trial of a leukotriene biosynthesis inhibitor, MK-591. Gastroenterology. 1997; 112: 725-732. (Pubitemid 27113797)
22. Sandborn WJ., Strategies for targeting tumour necrosis factor in IBD. Best Pract Res Clin Gastroenterol. 2003; 17: 105-117.
23. STAIR. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke. 1999; 30: 2752-2758.
24. Fisher M, Feuerstein G, Howells DW, et al. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke. 2009; 40: 2244-2250.
25. Mahler M, Bristol IJ, Leiter EH, et al. Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis. Am J Physiol. 1998; 274: G544-G551.
26. Morris GP, Beck PL, Herridge MS, et al. Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology. 1989; 96: 795-803. (Pubitemid 19057602)
27. Wirtz S, Neufert C, Weigmann B, et al. Chemically induced mouse models of intestinal inflammation. Nat Protoc. 2007; 2: 541-546. (Pubitemid 47040018)
28. Yamada Y, Marshall S, Specian RD, et al. A comparative analysis of two models of colitis in rats. Gastroenterology. 1992; 102: 1524-1534.
29. Okayasu I, Hatakeyama S, Yamada M, et al. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 1990; 98: 694-702. (Pubitemid 20069706)
30. Fukata M, Michelsen KS, Eri R, et al. Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis. Am J Physiol Gastrointest Liver Physiol. 2005; 288: G1055-G1065. (Pubitemid 40563149)
31. Hans W, Scholmerich J, Gross V, et al. The role of the resident intestinal flora in acute and chronic dextran sulfate sodium-induced colitis in mice. Eur J Gastroenterol Hepatol. 2000; 12: 267-273. (Pubitemid 30168579)
32. Kitajima S, Morimoto M, Sagara E, et al. Dextran sodium sulfate-induced colitis in germ-free IQI/Jic mice. Exp Anim. 2001; 50: 387-395. (Pubitemid 33692774)
33. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004; 118: 229-241. (Pubitemid 38962578)
34. Kitajima S, Takuma S, Morimoto M., Histological analysis of murine colitis induced by dextran sulfate sodium of different molecular weights. Exp Anim. 2000; 49: 9-15.
35. Dieleman LA, Ridwan BU, Tennyson GS, et al. Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology. 1994; 107: 1643-1652. (Pubitemid 24357616)
36. Krieglstein CF, Cerwinka WH, Sprague AG, et al. Collagen-binding integrin alpha1beta1 regulates intestinal inflammation in experimental colitis. J Clin Invest. 2002; 110: 1773-1782. (Pubitemid 36076484)
37. Seno H, Miyoshi H, Brown SL, et al. Efficient colonic mucosal wound repair requires Trem2 signaling. Proc Natl Acad Sci U S A. 2009; 106: 256-261.
38. Te Velde AA, Verstege MI, Hommes DW., Critical appraisal of the current practice in murine TNBS-induced colitis. Inflamm Bowel Dis. 2006; 12: 995-999. (Pubitemid 44498288)
39. Grisham MB, Volkmer C, Tso P, et al. Metabolism of trinitrobenzene sulfonic acid by the rat colon produces reactive oxygen species. Gastroenterology. 1991; 101: 540-547.
40. Neurath MF, Fuss I, Kelsall BL, et al. Experimental granulomatous colitis in mice is abrogated by induction of TGF-beta-mediated oral tolerance. J Exp Med. 1996; 183: 2605-2616. (Pubitemid 26192369)
41. Han X, Ren X, Jurickova I, et al. Regulation of intestinal barrier function by signal transducer and activator of transcription 5b. Gut. 2009; 58: 49-58.
42. Pereira-Fantini PM, Judd LM, Kalantzis A, et al. A33 antigen-deficient mice have defective colonic mucosal repair. Inflamm Bowel Dis. 2010; 16: 604-612.
43. Robinson A, Keely S, Karhausen J, et al. Mucosal protection by hypoxia-inducible factor prolyl hydroxylase inhibition. Gastroenterology. 2008; 134: 145-155. (Pubitemid 350309309)
44. Cario E, Gerken G, Podolsky DK., Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology. 2007; 132: 1359-1374. (Pubitemid 46627595)
45. Edelblum KL, Washington MK, Koyama T, et al. Raf protects against colitis by promoting mouse colon epithelial cell survival through NF-kappaB. Gastroenterology. 2008; 135: 539-551.
46. Frey MR, Edelblum KL, Mullane MT, et al. The ErbB4 growth factor receptor is required for colon epithelial cell survival in the presence of TNF. Gastroenterology. 2009; 136: 217-226.
47. Cario E, Gerken G, Podolsky DK., Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology. 2007; 132: 1359-1374. (Pubitemid 46627595)
48. Neurath MF, Fuss I, Kelsall BL, et al. Antibodies to interleukin 12 abrogate established experimental colitis in mice. J Exp Med. 1995; 182: 1281-1290.
49. Fiorucci S, Mencarelli A, Palazzetti B, et al. Importance of innate immunity and collagen binding integrin alpha1beta1 in TNBS-induced colitis. Immunity. 2002; 17: 769-780. (Pubitemid 35477796)
50. van Lierop PP, de HC, Lindenbergh-Kortleve DJ, et al. T-cell regulation of neutrophil infiltrate at the early stages of a murine colitis model. Inflamm Bowel Dis. 2010; 16: 442-451.
51. Uhlig HH, McKenzie BS, Hue S, et al. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity. 2006; 25: 309-318.
52. Feng T, Wang L, Schoeb TR, et al. Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis. J Exp Med. 2010; 207: 1321-1332.
53. Powrie F., T cells in inflammatory bowel disease: protective and pathogenic roles. Immunity. 1995; 3: 171-174.
54. Powrie F, Read S, Mottet C, et al. Control of immune pathology by regulatory T cells. Novartis Found Symp. 2003; 252: 92-98.
55. 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.
56. 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.
57. Kanai T, Kawamura T, Dohi T, et al. TH1/TH2-mediated colitis induced by adoptive transfer of CD4+CD45RBhigh T lymphocytes into nude mice. Inflamm Bowel Dis. 2006; 12: 89-99.
58. Mizoguchi A, Mizoguchi E, Takedatsu H, et al. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity. 2002; 16: 219-230. (Pubitemid 34211962)
59. Mizoguchi E, Mizoguchi A, Preffer FI, et al. Regulatory role of mature B cells in a murine model of inflammatory bowel disease. Int Immunol. 2000; 12: 597-605. (Pubitemid 30248892)
60. Hirano D, Kudo S., Usefulness of CD4+CD45RBhigh. J Pharmacol Sci. 2009; 110: 169-181.
61. Dan N, Kanai T, Totsuka T, et al. Ameliorating effect of anti-Fas ligand MAb on wasting disease in murine model of chronic colitis. Am J Physiol Gastrointest Liver Physiol. 2003; 285: G754-G760. (Pubitemid 37151237)
62. Fujii R, Kanai T, Nemoto Y, et al. FTY720 suppresses CD4+ CD44highC. Am J Physiol Gastrointest Liver Physiol. 2006; 291: G267-G274.
63. Kanai T, Totsuka T, Uraushihara K, et al. Blockade of B7-H1 suppresses the development of chronic intestinal inflammation. J Immunol. 2003; 171: 4156-4163. (Pubitemid 37238692)
64. Leon F, Contractor N, Fuss I, et al. Antibodies to complement receptor 3 treat established inflammation in murine models of colitis and a novel model of psoriasiform dermatitis. J Immunol. 2006; 177: 6974-6982. (Pubitemid 44715063)
65. Liu Z, Geboes K, Colpaert S, et al. Prevention of experimental colitis in SCID mice reconstituted with CD45RBhigh CD4+ T cells by blocking the CD40-CD154 interactions. J Immunol. 2000; 164: 6005-6014. (Pubitemid 30389849)
66. Manocha M, Rietdijk S, Laouar A, et al. Blocking CD27-CD70 costimulatory pathway suppresses experimental colitis. J Immunol. 2009; 183: 270-276.
67. Totsuka T, Kanai T, Uraushihara K, et al. Therapeutic effect of anti-OX40L and anti-TNF-alpha MAbs in a murine model of chronic colitis. Am J Physiol Gastrointest Liver Physiol. 2003; 284: G595-G603. (Pubitemid 36343209)
68. Barnes MJ, Powrie F., Regulatory T cells reinforce intestinal homeostasis. Immunity. 2009; 31: 401-411.
69. Izcue A, Coombes JL, Powrie F., Regulatory lymphocytes and intestinal inflammation. Annu Rev Immunol. 2009; 27: 313-338.
70. Dohi T, Fujihashi K, Koga T, et al. T helper type-2 cells induce ileal villus atrophy, goblet cell metaplasia, and wasting disease in T cell-deficient mice. Gastroenterology. 2003; 124: 672-682. (Pubitemid 36268486)
71. Dohi T, Fujihashi K, Koga T, et al. CD4+CD45RBHi interleukin-4 defective T cells elicit antral gastritis and duodenitis. Am J Pathol. 2004; 165: 1257-1268. (Pubitemid 39297731)
72. Zhang S, Ostanin DV, Gray L, et al. Chronic lung and liver inflammation in a mouse model of Crohn's colitis. Gastroenterology (Abstract). 2010; S-272.
73. Berg DJ, Davidson N, Kuhn R, et al. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4 (+) TH1-like responses. J Clin Invest. 1996; 98: 1010-1020. (Pubitemid 26293320)
74. Wilk JN, Bilsborough J, Viney JL., The mdr1a-/- mouse model of spontaneous colitis: a relevant and appropriate animal model to study inflammatory bowel disease. Immunol Res. 2005; 31: 151-159. (Pubitemid 40631385)
75. Panwala CM, Jones JC, Viney JL., A novel model of inflammatory bowel disease: mice deficient for the multiple drug resistance gene, mdr1a, spontaneously develop colitis. J Immunol. 1998; 161: 5733-5744. (Pubitemid 28519142)
76. Garrett WS, Lord GM, Punit S, et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell. 2007; 131: 33-45. (Pubitemid 47505255)
77. Maloy KJ, Salaun L, Cahill R, et al. CD4+CD25+ T (R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med. 2003; 197: 111-119. (Pubitemid 36110262)
78. Hue S, Ahern P, Buonocore S, et al. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med. 2006; 203: 2473-2483. (Pubitemid 44664617)
79. Asquith MJ, Boulard O, Powrie F, et al. Pathogenic and protective roles of MyD88 in leukocytes and epithelial cells in mouse models of inflammatory bowel disease. Gastroenterology. 2010; 139: 519-529.
80. Boulard O, Asquith MJ, Powrie F, et al. TLR2-independent induction and regulation of chronic intestinal inflammation. Eur J Immunol. 2010; 40: 516-524.
81. Kullberg MC, Jankovic D, Feng CG, et al. IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J Exp Med. 2006; 203: 2485-2494. (Pubitemid 44664618)
82. Kontoyiannis D, Pasparakis M, Pizarro TT, et al. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity. 1999; 10: 387-398. (Pubitemid 29165293)
83. Matsumoto S, Okabe Y, Setoyama H, et al. Inflammatory bowel disease-like enteritis and caecitis in a senescence accelerated mouse P1/Yit strain. Gut. 1998; 43: 71-78. (Pubitemid 28335492)
84. Kosiewicz MM, Nast CC, Krishnan A, et al. Th1-type responses mediate spontaneous ileitis in a novel murine model of Crohn's disease. J Clin Invest. 2001; 107: 695-702. (Pubitemid 32225355)
85. Rivera-Nieves J, Bamias G, Vidrich A, et al. Emergence of perianal fistulizing disease in the SAMP1/YitFc mouse, a spontaneous model of chronic ileitis. Gastroenterology. 2003; 124: 972-982. (Pubitemid 36389800)
86. Gooman-Gilman A,. Pharmacokinetics: the dynamics of drug absorption, distribution and elimination. In:, Hardman J, Limbird L, editors. Goodman and Gilman's the pharmacological basis of therapeutics. New York: Mcgraw Hill; 2001: 3-29.
87. Vowinkel T, Kalogeris TJ, Mori M, et al. Impact of dextran sulfate sodium load on the severity of inflammation in experimental colitis. Dig Dis Sci. 2004; 49: 556-564. (Pubitemid 38992541)
88. Pavlick KP, Laroux FS, Fuseler J, et al. Role of reactive metabolites of oxygen and nitrogen in inflammatory bowel disease. Free Radic Biol Med. 2002; 33: 311-322. (Pubitemid 34786271)
89. Conner EM, Aiko S, Fernandez M, et al. Duration of the hemodynamic effects of N (G)-nitro-L-arginine methyl ester in vivo. Nitric Oxide. 2000; 4: 85-93. (Pubitemid 30318298)
90. Napoli C, Ignarro LJ., Nitric oxide and pathogenic mechanisms involved in the development of vascular diseases. Arch Pharm Res. 2009; 32: 1103-1108.
91. Sartor RB,. Animal models of intestinal inflammation. In:, Sartor RB, Sandborn WJ, editors. Kirsner's inflammatory bowel disease. Edinburgh: Saunders; 2004: 120-137.
92. Lindsay J, Van MC, Brennan F, et al. IL-10 gene therapy prevents TNBS-induced colitis. Gene Ther. 2002; 9: 1715-1721. (Pubitemid 36104616)
93. Lindsay JO, Sandison A, Cohen P, et al. IL-10 gene therapy is therapeutic for dextran sodium sulfate-induced murine colitis. Dig Dis Sci. 2004; 49: 1327-1334. (Pubitemid 39178107)
94. Davidson NJ, Leach MW, Fort MM, et al. T helper cell 1-type CD4+ T cells, but not B cells, mediate colitis in interleukin 10-deficient mice. J Exp Med. 1996; 184: 241-251. (Pubitemid 26247233)
95. Herfarth HH, Mohanty SP, Rath HC, et al. Interleukin 10 suppresses experimental chronic, granulomatous inflammation induced by bacterial cell wall polymers. Gut. 1996; 39: 836-845. (Pubitemid 27049087)
96. Herfarth HH, Bocker U, Janardhanam R, et al. Subtherapeutic corticosteroids potentiate the ability of interleukin 10 to prevent chronic inflammation in rats. Gastroenterology. 1998; 115: 856-865. (Pubitemid 28452933)
97. Bickston SJ, Cominelli F., Recombinant interleukin 10 for the treatment of active Crohn's disease: lessons in biologic therapy. Gastroenterology. 2000; 119: 1781-1783. (Pubitemid 32198705)
98. Fedorak RN, Gangl A, Elson CO, et al. Recombinant human interleukin 10 in the treatment of patients with mild to moderately active Crohn's disease. The Interleukin 10 Inflammatory Bowel Disease Cooperative Study Group. Gastroenterology. 2000; 119: 1473-1482. (Pubitemid 32198672)
99. Schreiber S, Fedorak RN, Nielsen OH, et al. Safety and efficacy of recombinant human interleukin 10 in chronic active Crohn's disease. Crohn's Disease IL-10 Cooperative Study Group. Gastroenterology. 2000; 119: 1461-1472. (Pubitemid 32198671)
100. O'Collins VE, Macleod MR, Donnan GA, et al. 1,026 experimental treatments in acute stroke. Ann Neurol. 2006; 59: 467-477. (Pubitemid 43358067)
101. Sena E, van der Worp HB, Howells D, et al. How can we improve the pre-clinical development of drugs for stroke? Trends Neurosci. 2007; 30: 433-439. (Pubitemid 47374833)
102. Crossley NA, Sena E, Goehler J, et al. Empirical evidence of bias in the design of experimental stroke studies: a metaepidemiologic approach. Stroke. 2008; 39: 929-934. (Pubitemid 351619572)
103. Macleod MR, van der Worp HB, Sena ES, et al. Evidence for the efficacy of NXY-059 in experimental focal cerebral ischaemia is confounded by study quality. Stroke. 2008; 39: 2824-2829.
104. Sena ES, van der Worp HB, Bath PM, et al. Publication bias in reports of animal stroke studies leads to major overstatement of efficacy. PLoS Biol. 2010; 8:e1000344.
105. Rosenthal R., Psychological Bulletin. 1979; 86: 638-641.
106. van der Worp HB, Howells DW, Sena ES, et al. Can animal models of disease reliably inform human studies? PLoS Med. 2010; 7: e1000245.
107. Hackam DG, Redelmeier DA., Translation of research evidence from animals to humans. JAMA. 2006; 296: 1731-1732. (Pubitemid 44547792)