Important Lessons Derived from Animal Models of Celiac Disease

REFERENCES

• Hourigan CS. The molecular basis of coeliac disease. Clin Exp Med. 2006;6(2):53–59.
   PubMed Web of Science ®Google Scholar
• Batt RM, McLean L, Carter MW. Sequential morphologic and biochemical studies of naturally occurring wheat-sensitive enteropathy in Irish setter dogs. Dig Dis Sci. 1987;32(2):184–194.
   Web of Science ®Google Scholar
• Batt RM, Carter MW, McLean L. Wheat-sensitive enteropathy in Irish setter dogs: possible age-related brush border abnormalities. Res Vet Sci. 1985;39(1):80–83.
   Web of Science ®Google Scholar
• Hall EJ, Batt RM. Delayed introduction of dietary cereal may modulate the development of gluten-sensitive enteropathy in Irish setter dogs. J Nutr. 1991;121(11 Suppl):S152–S153.
   Web of Science ®Google Scholar
• Hall EJ, Batt RM. Abnormal intestinal permeability could play a role in the development of gluten-sensitive enteropathy in Irish setter dogs. J Nutr. 1991;121(11 Suppl):S150–S151.
   Web of Science ®Google Scholar
• Hall EJ, Batt RM. Differential sugar absorption for the assessment of canine intestinal permeability: the cellobiose/mannitol test in gluten-sensitive enteropathy of Irish setters. Res Vet Sci. 1991;51(1):83–87.
   Web of Science ®Google Scholar
• Hall EJ, Batt RM. Abnormal permeability precedes the development of a gluten sensitive enteropathy in Irish setter dogs. Gut. 1991;32(7):749–753. PMCID: 1378989.
   PubMed Web of Science ®Google Scholar
• Polvi A, Garden OA, Houlston RS, Maki M, Batt RM, Partanen J. Genetic susceptibility to gluten sensitive enteropathy in Irish setter dogs is not linked to the major histocompatibility complex. Tissue Antigens. 1998;52(6):543–549.
   Google Scholar
• Bethune MT, Borda JT, Ribka E, A non-human primate model for gluten sensitivity. PLoS One. 2008;3(2):e1614. PMCID: 2229647.
   PubMed Web of Science ®Google Scholar
• Mazumdar K, Alvarez X, Borda JT, Visualization of transepithelial passage of the immunogenic 33-residue peptide from alpha-2 gliadin in gluten-sensitive macaques. PLoS One. 2010;5(4):e10228. PMCID: 2856682.
   Web of Science ®Google Scholar
• Bethune MT, Ribka E, Khosla C, Sestak K. Transepithelial transport and enzymatic detoxification of gluten in gluten-sensitive rhesus macaques. PLoS One. 2008;3(3):e1857. PMCID: 2267209.
   PubMed Web of Science ®Google Scholar
• Stepankova R, Tlaskalova-Hogenova H, Sinkora J, Jodl J, Fric P. Changes in jejunal mucosa after long-term feeding of germfree rats with gluten. Scand J Gastroenterol. 1996;31(6):551–557.
   Web of Science ®Google Scholar
• Cinova J, De Palma G, Stepankova R, Role of intestinal bacteria in gliadin-induced changes in intestinal mucosa: study in germ-free rats. PLoS One. 2011;6(1):e16169. PMCID: 3020961.
   PubMed Web of Science ®Google Scholar
• Maurano F, Mazzarella G, Luongo D, Small intestinal enteropathy in non-obese diabetic mice fed a diet containing wheat. Diabetologia. 2005;48(5):931–937.
   Web of Science ®Google Scholar
• Sblattero D, Maurano F, Mazzarella G, Characterization of the anti-tissue transglutaminase antibody response in nonobese diabetic mice. J Immunol. 2005;174(9):5830–5836.
   Web of Science ®Google Scholar
• Freitag TL, Rietdijk S, Junker Y, Gliadin-primed CD4+CD45RBlowCD25- T cells drive gluten-dependent small intestinal damage after adoptive transfer into lymphopenic mice. Gut. 2009;58(12):1597–1605.
   Web of Science ®Google Scholar
• Sollid LM. Molecular basis of celiac disease. Annu Rev Immunol. 2000;18:53–81.
   PubMed Web of Science ®Google Scholar
• Black KE, Murray JA, David CS. HLA-DQ determines the response to exogenous wheat proteins: a model of gluten sensitivity in transgenic knockout mice. J Immunol. 2002;169(10):5595–5600.
   Web of Science ®Google Scholar
• Verdu EF, Huang X, Natividad J, Gliadin-dependent neuromuscular and epithelial secretory responses in gluten-sensitive HLA-DQ8 transgenic mice. Am J Physiol Gastrointest Liver Physiol. 2008;294(1):G217–G225.
   Web of Science ®Google Scholar
• Hovhannisyan Z, Weiss A, Martin A, The role of HLA-DQ8 beta57 polymorphism in the anti-gluten T-cell response in coeliac disease. Nature. 2008;456(7221):534–538.
   Web of Science ®Google Scholar
• Fehniger TA, Suzuki K, Ponnappan A, Fatal leukemia in interleukin 15 transgenic mice follows early expansions in natural killer and memory phenotype CD8+ T cells. J Exp Med. 2001;193(2):219–231. PMCID: 2193336.
   PubMed Web of Science ®Google Scholar
• Mention JJ, Ben Ahmed M, Begue B, Interleukin 15: a key to disrupted intraepithelial lymphocyte homeostasis and lymphomagenesis in celiac disease. Gastroenterology. 2003;125(3):730–745.
   Web of Science ®Google Scholar
• DePaolo RW, Abadie V, Tang F, Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens. Nature. 2011;471(7337):220–224. PMCID: 3076739.
   PubMed Web of Science ®Google Scholar
• Chen Z, Dudek N, Wijburg O, A 320-kilobase artificial chromosome encoding the human HLA DR3-DQ2 MHC haplotype confers HLA restriction in transgenic mice. J Immunol. 2002;168(6):3050–3056.
   Web of Science ®Google Scholar
• Chen D, Ueda R, Harding F, Characterization of HLA DR3/DQ2 transgenic mice: a potential humanized animal model for autoimmune disease studies. Eur J Immunol. 2003;33(1):172–182.
   Web of Science ®Google Scholar
• de Kauwe AL, Chen Z, Anderson RP, Resistance to celiac disease in humanized HLA-DR3-DQ2-transgenic mice expressing specific anti-gliadin CD4+ T cells. J Immunol. 2009;182(12): 7440–7450.
   Web of Science ®Google Scholar
• Marietta E, Black K, Camilleri M, A new model for dermatitis herpetiformis that uses HLA-DQ8 transgenic NOD mice. J Clin Invest. 2004;114(8):1090–1097. PMCID: 522239.
   PubMed Web of Science ®Google Scholar
• Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009;1(6):6ra14. PMCID: 2894525.
   PubMed Web of Science ®Google Scholar
• Collado MC, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease. J Clin Pathol. 2009;62(3):264–269.
   Web of Science ®Google Scholar
• Natividad JM, Huang X, Slack E, Host responses to intestinal microbial antigens in gluten-sensitive mice. PLoS One. 2009;4(7):e6472. PMCID: 2715133.
   PubMed Web of Science ®Google Scholar
• Pinier M, Verdu EF, Nasser-Eddine M, Polymeric binders suppress gliadin-induced toxicity in the intestinal epithelium. Gastroenterology. 2009;136(1):288–298.
   Web of Science ®Google Scholar
• Senger S, Luongo D, Maurano F, Intranasal administration of a recombinant alpha-gliadin down-regulates the immune response to wheat gliadin in DQ8 transgenic mice. Immunol Lett. 2003;88(2):127–134.
   Web of Science ®Google Scholar
• Huibregtse IL, Marietta EV, Rashtak S, Induction of antigen-specific tolerance by oral administration of Lactococcus lactis delivered immunodominant DQ8-restricted gliadin peptide in sensitized nonobese diabetic Abo Dq8 transgenic mice. J Immunol. 2009;183(4):2390–2396.
   PubMed Web of Science ®Google Scholar
• Mazzarella G, Maglio M, Paparo F, An immunodominant DQ8 restricted gliadin peptide activates small intestinal immune response in in vitro cultured mucosa from HLA-DQ8 positive but not HLA-DQ8 negative coeliac patients. Gut. 2003;52(1):57–62. PMCID: 1773526.
   PubMed Web of Science ®Google Scholar
• Keech CL, Dromey J, Chen ZJ, Anderson RP, McCluskey J. Immune tolerance induced by peptide immunotherapy in an HLA Dq2-dependent mouse model of gluten immunity. Gastroenterology. 2009;136(5):A57–A57.
   Web of Science ®Google Scholar
• Lammers KM, Lu R, Brownley J, Gliadin induces an increase in intestinal permeability and zonulin release by binding to the chemokine receptor CXCR3. Gastroenterology. 2008;135(1):194–204 e3. PMCID: 2653457.
   PubMed Web of Science ®Google Scholar
• Tripathi A, Lammers KM, Goldblum S, Identification of human zonulin, a physiological modulator of tight junctions, as prehaptoglobin-2. Proc Natl Acad Sci U S A. 2009;106(39):16799–16804. PMCID: 2744629.
   PubMed Web of Science ®Google Scholar
• Batt RM, Carter MW, McLean L. Morphological and biochemical studies of a naturally occurring enteropathy in the Irish setter dog: a comparison with coeliac disease in man. Res Vet Sci. 1984;37(3):339–346.
   Web of Science ®Google Scholar
• Bevan S, Popat S, Braegger CP, Contribution of the MHC region to the familial risk of coeliac disease. J Med Genet. 1999;36(9):687–690. PMCID: 1734425.
   PubMed Web of Science ®Google Scholar
• Sollid LM, Jabri B. Is celiac disease an autoimmune disorder? Curr Opin Immunol. 2005;17(6):595–600.
   PubMed Web of Science ®Google Scholar
• Marzari R, Sblattero D, Florian F, Molecular dissection of the tissue transglutaminase autoantibody response in celiac disease. J Immunol. 2001;166(6):4170–4176.
   Web of Science ®Google Scholar
• Korponay-Szabo IR, Halttunen T, Szalai Z, In vivo targeting of intestinal and extraintestinal transglutaminase 2 by coeliac autoantibodies. Gut. 2004;53(5):641–648. PMCID: 1774023.
   PubMed Web of Science ®Google Scholar
• Maglio M, Tosco A, Auricchio R, Intestinal deposits of anti-tissue transglutaminase IgA in childhood celiac disease. Dig Liver Dis. 2011; doi:10.1016/j.did.2011.01.015.
   PubMedGoogle Scholar
• Stene LC, Honeyman MC, Hoffenberg EJ, Rotavirus infection frequency and risk of celiac disease autoimmunity in early childhood: a longitudinal study. Am J Gastroenterol. 2006;101(10):2333–2340.
   PubMed Web of Science ®Google Scholar
• Zanoni G, Navone R, Lunardi C, In celiac disease, a subset of autoantibodies against transglutaminase binds toll-like receptor 4 and induces activation of monocytes. PLoS Med. 2006;3(9):e358. PMCID: 1569884.
   PubMed Web of Science ®Google Scholar
• Norris JM, Barriga K, Hoffenberg EJ, Risk of celiac disease autoimmunity and timing of gluten introduction in the diet of infants at increased risk of disease. JAMA. 2005;293(19):2343–2351.
   PubMed Web of Science ®Google Scholar
• D'Amico MA, Holmes J, Stavropoulos SN, Presentation of pediatric celiac disease in the United States: prominent effect of breastfeeding. Clin Pediatr (Phila). 2005;44(3):249–258.
   PubMed Web of Science ®Google Scholar
• Akobeng AK, Ramanan AV, Buchan I, Heller RF. Effect of breast feeding on risk of coeliac disease: a systematic review and meta-analysis of observational studies. Arch Dis Child. 2006;91(1):39–43. PMCID: 2083075.
   PubMed Web of Science ®Google Scholar
• Ostanin DV, Brown CM, Gray L, Bharwani S, Grisham MB. Evaluation of the immunoregulatory activity of intraepithelial lymphocytes in a mouse model of chronic intestinal inflammation. Int Immunol. 2010;22(12):927–939. PMCID: 3031346.
   PubMed Web of Science ®Google Scholar