期刊论文详细信息
Gut Pathogens
Animal models to study acute and chronic intestinal inflammation in mammals
Richard REUwiera1  GDouglas Inglis3  Trina CUwiera2  Janelle AJiminez1 
[1] Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada;Department of Surgery, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, AB, Canada;Agriculture and Agri-Food Canada Research Centre, Lethbridge, AB, Canada
关键词: Biological;    Chemical;    Incitants;    Animal models;    Chronic;    Acute;    Inflammation;    Intestine;   
Others  :  1232080
DOI  :  10.1186/s13099-015-0076-y
 received in 2015-09-14, accepted in 2015-10-22,  发布年份 2015
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【 摘 要 】

Acute and chronic inflammatory diseases of the intestine impart a significant and negative impact on the health and well-being of human and non-human mammalian animals. Understanding the underlying mechanisms of inflammatory disease is mandatory to develop effective treatment and prevention strategies. As inflammatory disease etiologies are multifactorial, the use of appropriate animal models and associated metrics of disease are essential. In this regard, animal models used alone or in combination to study acute and chronic inflammatory disease of the mammalian intestine paired with commonly used inflammation-inducing agents are reviewed. This includes both chemical and biological incitants of inflammation, and both non-mammalian (i.e. nematodes, insects, and fish) and mammalian (i.e. rodents, rabbits, pigs, ruminants, dogs, and non-human primates) models of intestinal inflammation including germ-free, gnotobiotic, as well as surgical, and genetically modified animals. Importantly, chemical and biological incitants induce inflammation via a multitude of mechanisms, and intestinal inflammation and injury can vary greatly according to the incitant and animal model used, allowing studies to ascertain both long-term and short-term effects of inflammation. Thus, researchers and clinicians should be aware of the relative strengths and limitations of the various animal models used to study acute and chronic inflammatory diseases of the mammalian intestine, and the scope and relevance of outcomes achievable based on this knowledge. The ability to induce inflammation to mimic common human diseases is an important factor of a successful animal model, however other mechanisms of disease such as the amount of infective agent to induce disease, invasion mechanisms, and the effect various physiologic changes can have on inducing damage are also important features. In many cases, the use of multiple animal models in combination with both chemical and biological incitants is necessary to answer the specific question being addressed regarding intestinal disease. Some incitants can induce acute responses in certain animal models while others can be used to induce chronic responses; this review aims to illustrate the strengths and weaknesses in each animal model and to guide the choice of an appropriate acute or chronic incitant to facilitate intestinal disease.

【 授权许可】

   
2015 Jiminez et al.

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【 参考文献 】
  • [1]Akdis M. Healthy immune response to allergens: T regulatory cells and more. Curr Opin Immunol. 2006; 18(6):738-744.
  • [2]Rubin DC, Shaker A, Levin MS. Chronic intestinal inflammation: inflammatory bowel disease and colitis-associated colon cancer. Front Immunol. 2012; 3:107.
  • [3]Shinoda M, Hatano S, Kawakubo H, Kakefuda T, Omori T, Ishii S. Adult cecoanal intussusception caused by cecum cancer: report of a case. Surg Today. 2007; 37(9):802-805.
  • [4]Dundas SAC, Dutton J, Skipworth P. Reliability of rectal biopsy in distinguishing between chronic inflammatory bowel disease and acute self-limiting colitis. Histopathology. 1997; 31(1):60-66.
  • [5]Kornbluth A, Sachar DB. Ulcerative colitis practice guidelines in adults (update): american college of gastroenterology, practice parameters committee. Am J Gastroenterol. 2004; 99(7):1371-1385.
  • [6]Sanchez MI, Bercik P. Epidemiology and burden of chronic constipation. Can J Gastroenterol. 2011; 25 Suppl B:11B-15B.
  • [7]Hunt R, Quigley E, Abbas Z, Eliakim A, Emmanuel A, Goh KL et al.. Coping with common gastrointestinal symptoms in the community: a global perspective on heartburn, constipation, bloating, and abdominal pain/discomfort May 2013. J Clin Gastroenterol. 2014; 48(7):567-578.
  • [8]World Health Organization. Diarrhoeal disease. In: Fact Sheet Number 330. 2013. http://www.who.int/mediacentre/factsheets/fs330/en/. Accessed 30 July 2015.
  • [9]Glass K, Ford L, Kirk MD. Drivers of uncertainty in estimates of foodborne gastroenteritis incidence. Foodborne Pathog Dis. 2014; 11(12):938-944.
  • [10]Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD et al.. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014; 14(8):725-730.
  • [11]Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE et al.. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet. 2012; 379(9832):2151-2161.
  • [12]Freedman SB, Ali S, Oleszczuk M, Gouin S, Hartling L. Treatment of acute gastroenteritis in children: an overview of systematic reviews of interventions commonly used in developed countries. Evid Based Child Health. 2013; 8(4):1123-1137.
  • [13]Centers for Disease Control and Prevention: Norovirus is now the leading cause of severe gastroenteritis in US children [database on the Internet]. 2013. Available from: http://www.cdc.gov/media/releases/2013/p0321_norovirus_children.html. Accessed 1 Sept 2015.
  • [14]Morton VK, Thomas MK, McEwen SA. Estimated hospitalizations attributed to norovirus and rotavirus infection in Canada, 2006–2010. Epidemiol Infect. 2015; 143(16):3528-3537.
  • [15]Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142(1):46–54 e42; (quiz e30). doi:10.1053/j.gastro.2011.10.001.
  • [16]Ponder A, Long MD. A clinical review of recent findings in the epidemiology of inflammatory bowel disease. Clin Epidemiol. 2013; 5:237-247.
  • [17]Thomas MK, Murray R, Flockhart L, Pintar K, Pollari F, Fazil A et al.. Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog Dis. 2013; 10(7):639-648.
  • [18]Rocchi A, Benchimol EI, Bernstein CN, Bitton A, Feagan B, Panaccione R et al.. Inflammatory bowel disease: a Canadian burden of illness review. Can J Gastroenterol. 2012; 26(11):811-817.
  • [19]Wilson J, Hair C, Knight R, Catto-Smith A, Bell S, Kamm M et al.. High incidence of inflammatory bowel disease in Australia: a prospective population-based Australian incidence study. Inflamm Bowel Dis. 2010; 16(9):1550-1556.
  • [20]Bengtson MB, Solberg C, Aamodt G, Sauar J, Jahnsen J, Moum B et al.. Familial aggregation in Crohn’s disease and ulcerative colitis in a Norwegian population-based cohort followed for 10 years. J Crohns Colitis. 2009; 3(2):92-99.
  • [21]Bercik P, Verdu EF, Foster JA, Macri J, Potter M, Huang X, et al. Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice. Gastroenterology. 2010;139(6):2102–12.e1. doi:10.1053/j.gastro.2010.06.063.
  • [22]Denou E, Lolmede K, Garidou L, Pomie C, Chabo C, Lau TC et al.. Defective NOD2 peptidoglycan sensing promotes diet-induced inflammation, dysbiosis, and insulin resistance. EMBO Mol Med. 2015; 7(3):259-274.
  • [23]Leone V, Chang EB, Devkota S. Diet, microbes, and host genetics: the perfect storm in inflammatory bowel diseases. J Gastroenterol. 2013; 48(3):315-321.
  • [24]Lidar M, Langevitz P, Shoenfeld Y. The role of infection in inflammatory bowel disease: initiation, exacerbation and protection. Isr Med Assoc J. 2009; 11(9):558-563.
  • [25]Tabas I, Glass CK. Anti-inflammatory therapy in chronic disease: challenges and opportunities. Science. 2013; 339(6116):166-172.
  • [26]Wallace KL, Zheng LB, Kanazawa Y, Shih DQ. Immunopathology of inflammatory bowel disease. World J Gastroenterol. 2014; 20(1):6-21.
  • [27]Geremia A, Biancheri P, Allan P, Corazza GR, Di Sabatino A. Innate and adaptive immunity in inflammatory bowel disease. Autoimmun Rev. 2014; 13(1):3-10.
  • [28]Janeway CAJ, Travers P, Walport M, Sclomchik MJ. Immunobiology: the immune system in health and disease. 5th ed. Garland Science, New York; 2001.
  • [29]Mader SS. Human biology. McGraw-Hill Higher Education; 2007.
  • [30]Williams AE. Immunology: mucosal and body surface defences. Wiley; 2011.
  • [31]Turvey SE, Broide DH. Innate immunity. J Allergy Clin Immunol. 2010; 125(2 Suppl 2):S24-S32.
  • [32]Jiang H, Chess L. An integrated view of suppressor T cell subsets in immunoregulation. J Clin Invest. 2004; 114(9):1198-1208.
  • [33]Medzhitov R, Janeway CA. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol. 1997; 9(1):4-9.
  • [34]Bercik P, Collins SM, Verdu EF. Microbes and the gut-brain axis. Neurogastroenterol Motil. 2012; 24(5):405-413.
  • [35]Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012; 489(7415):220-230.
  • [36]Gourbeyre P, Denery S, Bodinier M. Probiotics, prebiotics, and synbiotics: impact on the gut immune system and allergic reactions. J Leukoc Biol. 2011; 89(5):685-695.
  • [37]Cohen M, Varki NM, Jankowski MD, Gagneux P. Using unfixed, frozen tissues to study natural mucin distribution. J Vis Exp. 2012; 67:e3928.
  • [38]Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC et al.. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2007; 2(2):119-129.
  • [39]Lyte M, Vulchanova L, Brown DR. Stress at the intestinal surface: catecholamines and mucosa–bacteria interactions. Cell Tissue Res. 2011; 343(1):23-32.
  • [40]Lee WJ, Hase K. Gut microbiota-generated metabolites in animal health and disease. Nat Chem Biol. 2014; 10(6):416-424.
  • [41]Hawrelak JA, Myers SP. The causes of intestinal dysbiosis: a review. Altern Med Rev. 2004; 9(2):180-197.
  • [42]Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 2007; 104(34):13780-13785.
  • [43]Wilson M. Microbial inhabitants of humans: their ecology and role in health and disease. Cambridge University Press; 2005.
  • [44]Stecher B, Hardt WD. Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol. 2011; 14(1):82-91.
  • [45]Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol. 2010; 10(2):131-144.
  • [46]Mouse Genome Sequencing C, Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF et al.. Initial sequencing and comparative analysis of the mouse genome. Nature. 2002; 420(6915):520-562.
  • [47]Lin J, Hackam DJ. Worms, flies and four-legged friends: the applicability of biological models to the understanding of intestinal inflammatory diseases. Dis Model Mech. 2011; 4(4):447-456.
  • [48]Lam SH, Chua HL, Gong Z, Lam TJ, Sin YM. Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev Comp Immunol. 2004; 28(1):9-28.
  • [49]Walters E, Wolf E, Whyte J, Mao J, Renner S, Nagashima H et al.. Completion of the swine genome will simplify the production of swine as a large animal biomedical model. BMC Med Genom. 2012; 5(1):55.
  • [50]Coors ME, Glover JJ, Juengst ET, Sikela JM. The ethics of using transgenic non-human primates to study what makes us human. Nat Rev Genet. 2010; 11(9):658-662.
  • [51]Ideland M. Different views on ethics: how animal ethics is situated in a committee culture. J Med Ethics. 2009; 35(4):258-261.
  • [52]Robinson AM, Sakkal S, Park A, Jovanovska V, Payne N, Carbone SE et al.. Mesenchymal stem cells and conditioned medium avert enteric neuropathy and colon dysfunction in guinea pig TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol. 2014; 307(11):G1115-G1129.
  • [53]Kathrani A, Lee H, White C, Catchpole B, Murphy A, German A et al.. Association between nucleotide oligomerisation domain two (Nod2) gene polymorphisms and canine inflammatory bowel disease. Vet Immunol Immunopathol. 2014; 161(1–2):32-41.
  • [54]Cerquetella M, Spaterna A, Laus F, Tesei B, Rossi G, Antonelli E et al.. Inflammatory bowel disease in the dog: differences and similarities with humans. World J Gastroenterol. 2010; 16(9):1050-1056.
  • [55]Koleva PT, Valcheva RS, Sun X, Ganzle MG, Dieleman LA. Inulin and fructo-oligosaccharides have divergent effects on colitis and commensal microbiota in HLA-B27 transgenic rats. Br J Nutr. 2012; 108(9):1633-1643.
  • [56]Mizoguchi A. Animal models of inflammatory bowel disease. In: Conn PM, editor. Progress in Molecular Biology and Translational Science. Academic Press; 2012. p. 263–320.
  • [57]Mizoguchi A, Mizoguchi E, Bhan AK. Immune networks in animal models of inflammatory bowel disease. Inflamm Bowel Dis. 2003; 9(4):246-259.
  • [58]Engelman RW, Kerr W. Assessing inflammatory disease at mucosal surfaces in murine genetic models. In: Perl A, editor. Autoimmunity. methods in molecular biology. Humana Press; 2012. p. 433–41.
  • [59]Dieleman Palmen, Akol Bloemena, Pena Meuwissen et al.. Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol. 1998; 114(3):385-391.
  • [60]Eri R, McGuckin MA, Wadley R. T cell transfer model of colitis: a great tool to assess the contribution of T cells in chronic intestinal inflammation. Methods Mol Biol. 2012; 844:261-275.
  • [61]Heylen M, Deleye S, De Man JG, Ruyssers NE, Vermeulen W, Stroobants S et al.. Colonoscopy and microPET/CT are valid techniques to monitor inflammation in the adoptive transfer colitis model in mice. Inflamm Bowel Dis. 2013; 19(5):967-976.
  • [62]Terzić J, Grivennikov S, Karin E, Karin M. Inflammation and colon cancer. Gastroenterology. 2010;138(6):2101–14.e5.
  • [63]Wymore Brand M, Wannemuehler MJ, Phillips GJ, Proctor A, Overstreet AM, Jergens AE et al.. The altered schaedler flora: continued applications of a defined murine microbial community. ILAR J. 2015; 56(2):169-178.
  • [64]Nell S, Suerbaum S, Josenhans C. The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models. Nat Rev Microbiol. 2010; 8(8):564-577.
  • [65]Rongvaux A, Willinger T, Martinek J, Strowig T, Gearty SV, Teichmann LL et al.. Development and function of human innate immune cells in a humanized mouse model. Nat Biotechnol. 2014; 32(4):364-372.
  • [66]Hintze KJ, Cox JE, Rompato G, Benninghoff AD, Ward RE, Broadbent J et al.. Broad scope method for creating humanized animal models for animal health and disease research through antibiotic treatment and human fecal transfer. Gut Microbes. 2014; 5(2):183-191.
  • [67]Bryda EC. The mighty mouse: the impact of rodents on advances in biomedical research. Mo Med. 2013; 110(3):207-211.
  • [68]Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007; 449(7164):811-818.
  • [69]Mestas J, Hughes CCW. Of mice and not men: differences between mouse and human immunology. J Immunol. 2004; 172(5):2731-2738.
  • [70]Nguyen D, Xu T. The expanding role of mouse genetics for understanding human biology and disease. Dis Model Mech. 2008; 1(1):56-66.
  • [71]Smith CM, Finger JH, Hayamizu TF, McCright IJ, Xu J, Berghout J, et al. The mouse Gene Expression Database (GXD): 2014 update. Nucleic Acids Res. 2014;42(Database issue):D818–24. doi:10.1093/nar/gkt954.
  • [72]Low D, Nguyen DD, Mizoguchi E. Animal models of ulcerative colitis and their application in drug research. Drug Des Dev Ther. 2013; 7:1341.
  • [73]Heinz S, Haehnel V, Karaghiosoff M, Schwarzfischer L, Muller M, Krause SW et al.. Species-specific regulation of Toll-like receptor 3 genes in men and mice. J Biol Chem. 2003; 278(24):21502-21509.
  • [74]Muzio M, Bosisio D, Polentarutti N, D’Amico G, Stoppacciaro A, Mancinelli R et al.. Differential expression and regulation of toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J Immunol. 2000; 164(11):5998-6004.
  • [75]Hedrich H. The laboratory mouse. Academic Press; 2004.
  • [76]Helwig BG, Ward JA, Blaha MD, Leon LR. Effect of intraperitoneal radiotelemetry instrumentation on voluntary wheel running and surgical recovery in mice. J Am Assoc Lab Anim Sci JAALAS. 2012; 51(5):600-608.
  • [77]Fujimoto JG. Optical coherence tomography for ultrahigh resolution in vivo imaging. Nat Biotechnol. 2003; 21(11):1361-1367.
  • [78]Geiger BM, Gras-Miralles B, Ziogas DC, Karagiannis AK, Zhen A, Fraenkel P et al.. Intestinal upregulation of melanin-concentrating hormone in TNBS-induced enterocolitis in adult zebrafish. PLoS One. 2013; 8(12):e83194.
  • [79]Fitzpatrick LR, Meirelles K, Small JS, Puleo FJ, Koltun WA, Cooney RN. A new model of chronic hapten-induced colitis in young rats. J Pediatr Gastroenterol Nutr. 2010; 50(3):240-250.
  • [80]Krimi RB, Kotelevets L, Dubuquoy L, Plaisancie P, Walker F, Lehy T et al.. Resistin-like molecule beta regulates intestinal mucous secretion and curtails TNBS-induced colitis in mice. Inflamm Bowel Dis. 2008; 14(7):931-941.
  • [81]Moreau NM, Champ MM, Goupry SM, Le Bizec BJ, Krempf M, Nguyen PG et al.. Resistant starch modulates in vivo colonic butyrate uptake and its oxidation in rats with dextran sulfate sodium-induced colitis. J Nutr. 2004; 134(3):493-500.
  • [82]Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE, Balish E et al.. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Invest. 1996; 98(4):945-953.
  • [83]Hammer RE, Maika SD, Richardson JA, Tang J-P, Taurog JD. Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human β2m: An animal model of HLA-B27-associated human disorders. Cell. 1990; 63(5):1099-1112.
  • [84]Morales W, Pimentel M, Hwang L, Kunkel D, Pokkunuri V, Basseri B et al.. Acute and chronic histological changes of the small bowel secondary to C. jejuni infection in a rat model for post-infectious IBS. Dig Dis Sci. 2011; 56(9):2575-2584.
  • [85]Abnous K, Brooks SP, Kwan J, Matias F, Green-Johnson J, Selinger LB et al.. Diets enriched in oat bran or wheat bran temporally and differentially alter the composition of the fecal community of rats. J Nutr. 2009; 139(11):2024-2031.
  • [86]Kalmokoff M, Zwicker B, O’Hara M, Matias F, Green J, Shastri P et al.. Temporal change in the gut community of rats fed high amylose cornstarch is driven by endogenous urea rather than strictly on carbohydrate availability. J Appl Microbiol. 2013; 114(5):1516-1528.
  • [87]Kalmokoff M, Franklin J, Petronella N, Green J, Brooks SPJ. Phylum level change in the cecal and fecal gut communities of rats fed diets containing different fermentable substrates supports a role for nitrogen as a factor contributing to community structure. Nutrients. 2015; 7(5):3279-3299.
  • [88]Irving AA, Yoshimi K, Hart ML, Parker T, Clipson L, Ford MR et al.. The utility of Apc-mutant rats in modeling human colon cancer. Dis Model Mech. 2014; 7(11):1215-1225.
  • [89]Johnson M. Laboratory mice and rats. Mater Methods. 2012; 2:113.
  • [90]Vandamme TF. Use of rodents as models of human diseases. J Pharm Bioallied Sci. 2014; 6(1):2-9.
  • [91]Zhao S, Shetty J, Hou L, Delcher A, Zhu B, Osoegawa K et al.. Human, mouse, and rat genome large-scale rearrangements: stability versus speciation. Genome Res. 2004; 14(10a):1851-1860.
  • [92]Schulenburg H, Kurz CL, Ewbank JJ. Evolution of the innate immune system: the worm perspective. Immunol Rev. 2004; 198(1):36-58.
  • [93]Pukkila-Worley R, Ausubel FM. Immune defense mechanisms in the Caenorhabditis elegans intestinal epithelium. Curr Opin Immunol. 2012; 24(1):3-9.
  • [94]Felix MA, Duveau F. Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae. BMC Biol. 2012; 10(1):59.
  • [95]Diard M, Baeriswyl S, Clermont O, Gouriou S, Picard B, Taddei F et al.. Caenorhabditis elegans as a simple model to study phenotypic and genetic virulence determinants of extraintestinal pathogenic Escherichia coli. Microbes Infect. 2007; 9(2):214-223.
  • [96]Balla KM, Troemel ER. Caenorhabditis elegans as a model for intracellular pathogen infection. Cell Microbiol. 2013; 15(8):1313-1322.
  • [97]Guha S, Klees M, Wang X, Li J, Dong Y, Cao M. Influence of planktonic and sessile Listeria monocytogenes on Caenorhabditis elegans. Arch Microbiol. 2013; 195(1):19-26.
  • [98]Shaye DD, Greenwald I. OrthoList: a compendium of C. elegans genes with human orthologs. PLoS One. 2011; 6(5):e20085.
  • [99]Bangi E, Pitsouli C, Rahme LG, Cagan R, Apidianakis Y. Immune response to bacteria induces dissemination of Ras-activated Drosophila hindgut cells. EMBO Rep. 2012; 13(6):569-576.
  • [100]Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B. Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe. 2009; 5(2):200-211.
  • [101]Kim SH, Lee WJ. Role of DUOX in gut inflammation: lessons from Drosophila model of gut-microbiota interactions. Front Cell Infect Microbiol. 2014; 3:116.
  • [102]Apidianakis Y, Rahme LG. Drosophila melanogaster as a model for human intestinal infection and pathology. Dis Model Mech. 2011; 4(1):21-30.
  • [103]Zaidman-Remy A, Regan JC, Brandao AS, Jacinto A. The Drosophila larva as a tool to study gut-associated macrophages: PI3K regulates a discrete hemocyte population at the proventriculus. Dev Comp Immunol. 2012; 36(4):638-647.
  • [104]Simonsen KT, Moller-Jensen J, Kristensen AR, Andersen JS, Riddle DL, Kallipolitis BH. Quantitative proteomics identifies ferritin in the innate immune response of C. elegans. Virulence. 2011; 2(2):120-130.
  • [105]Sifri CD, Begun J, Ausubel FM. The worm has turned–microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol. 2005; 13(3):119-127.
  • [106]Gerbaba TK, Gupta P, Rioux K, Hansen D, Buret AG. Giardia duodenalis-induced alterations of commensal bacteria kill Caenorhabditis elegans: a new model to study microbial–microbial interactions in the gut. Am J Physiol Gastrointest Liver Physiol. 2015; 308(6):G550-G561.
  • [107]Chapman RF. The insects: structure and function. Cambridge university press; 1998.
  • [108]Shin JT, Fishman MC. From Zebrafish to human: modular medical models. Annu Rev Genom Hum Genet. 2002; 3:311-340.
  • [109]Pack M, Solnica-Krezel L, Malicki J, Neuhauss SC, Schier AF, Stemple DL et al.. Mutations affecting development of zebrafish digestive organs. Development. 1996; 123(1):321-328.
  • [110]Oehlers SH, Flores MV, Hall CJ, Crosier KE, Crosier PS. Retinoic acid suppresses intestinal mucus production and exacerbates experimental enterocolitis. Dis Model Mech. 2012; 5(4):457-467.
  • [111]He Q, Wang L, Wang F, Li Q. Role of gut microbiota in a zebrafish model with chemically induced enterocolitis involving toll-like receptor signaling pathways. Zebrafish. 2014; 11(3):255-264.
  • [112]Milligan-Myhre K, Charette JR, Phennicie RT, Stephens WZ, Rawls JF, Guillemin K et al. Chapter 4—Study of host–microbe interactions in zebrafish. In: William Detrich HMW, Leonard IZ, editors. Methods in Cell Biology. Academic Press; 2011. p. 87–116.
  • [113]Rawls JF, Mahowald MA, Ley RE, Gordon JI. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell. 2006; 127(2):423-433.
  • [114]Patterson JK, Lei XG, Miller DD. The pig as an experimental model for elucidating the mechanisms governing dietary influence on mineral absorption. Exp Biol Med (Maywood). 2008; 233(6):651-664.
  • [115]Zhang Q, Widmer G, Tzipori S. A pig model of the human gastrointestinal tract. Gut Microbes. 2013; 4(3):193-200.
  • [116]Haverson K, Rehakova Z, Sinkora J, Sver L, Bailey M. Immune development in jejunal mucosa after colonization with selected commensal gut bacteria: a study in germ-free pigs. Vet Immunol Immunopathol. 2007; 119(3–4):243-253.
  • [117]Scharek L, Guth J, Reiter K, Weyrauch KD, Taras D, Schwerk P et al.. Influence of a probiotic Enterococcus faecium strain on development of the immune system of sows and piglets. Vet Immunol Immunopathol. 2005; 105(1–2):151-161.
  • [118]Foster N, Lovell MA, Marston KL, Hulme SD, Frost AJ, Bland P et al.. Rapid protection of gnotobiotic pigs against experimental Salmonellosis following induction of polymorphonuclear leukocytes by avirulent Salmonella enterica. Infect Immun. 2003; 71(4):2182-2191.
  • [119]Bautista EM, Nfon C, Ferman GS, Golde WT. IL-13 replaces IL-4 in development of monocyte derived dendritic cells (MoDC) of swine. Vet Immunol Immunopathol. 2007; 115(1–2):56-67.
  • [120]Lu X, Fu WX, Luo YR, Ding XD, Zhou JP, Liu Y et al.. Genome-wide association study for T lymphocyte subpopulations in swine. BMC Genom. 2012; 13(1):488.
  • [121]Bailey M, Christoforidou Z, Lewis MC. The evolutionary basis for differences between the immune systems of man, mouse, pig and ruminants. Vet Immunol Immunopathol. 2013; 152(1–2):13-19.
  • [122]Zuckermann FA. Extrathymic CD4/CD8 double positive T cells. Vet Immunol Immunopathol. 1999; 72(1–2):55-66.
  • [123]Kazen AR, Adams EJ. Evolution of the V, D, and J gene segments used in the primate gammadelta T-cell receptor reveals a dichotomy of conservation and diversity. Proc Natl Acad Sci USA. 2011; 108(29):E332-E340.
  • [124]Kaser T, Gerner W, Hammer SE, Patzl M, Saalmuller A. Phenotypic and functional characterisation of porcine CD4(+)CD25(high) regulatory T cells. Vet Immunol Immunopathol. 2008; 122(1–2):153-158.
  • [125]Crawley A, Raymond C, Wilkie BN. Control of immunoglobulin isotype production by porcine B-cells cultured with cytokines. Vet Immunol Immunopathol. 2003; 91(2):141-154.
  • [126]The Pig Site. 2013. http://www.thepigsite.com/knowledge/. Accessed 03 Dec 2013.
  • [127]Biggers JD, Curnow RN, Finn CA, McLaren A. Regulation of the gestation period in mice. J Reprod Fertil. 1963; 6(1):125-138.
  • [128]Drickamer LC. Sexual maturation of female house mice: social inhibition. Dev Psychobiol. 1974; 7(3):257-265.
  • [129]Gozalo AS, Cheng LI, St Claire ME, Ward JM, Elkins WR. Pathology of captive moustached tamarins (Saguinus mystax). Comp Med. 2008; 58(2):188-195.
  • [130]Gozalo A, Dagle GE, Montoya E, Weller RE. Spontaneous terminal ileitis resembling Crohn disease in captive tamarins. J Med Primatol. 2002; 31(3):142-146.
  • [131]Gardner MB, Luciw PA. Macaque models of human infectious disease. ILAR J. 2008; 49(2):220-255.
  • [132]Elson CO, Sartor RB, Tennyson GS, Riddell RH. Experimental models of inflammatory bowel disease. Gastroenterology. 1995; 109(4):1344-1367.
  • [133]Hart A, Kamm MA. Review article: mechanisms of initiation and perpetuation of gut inflammation by stress. Aliment Pharmacol Ther. 2002; 16(12):2017-2028.
  • [134]Wood JD, Peck OC, Tefend KS, Stonerook MJ, Caniano DA, Mutabagani KH et al.. Evidence that colitis is initiated by environmental stress and sustained by fecal factors in the Cotton-Top Tamarin (Saguinus oedipus). Dig Dis Sci. 2000; 45(2):385-393.
  • [135]David JM, Dick EJ, Hubbard GB. Spontaneous pathology of the common marmoset (Callithrix jacchus) and tamarins (Saguinus oedipus, Saguinus mystax). J Med Primatol. 2009; 38(5):347-359.
  • [136]Ramesh G, Alvarez X, Borda JT, Aye PP, Lackner AA, Sestak K. Visualizing cytokine-secreting cells in situ in the rhesus macaque model of chronic gut inflammation. Clin Diagn Lab Immunol. 2005; 12(1):192-197.
  • [137]Caplan MS, Hsueh W. Necrotizing enterocolitis: role of platelet activating factor, endotoxin, and tumor necrosis factor. J Pediatr. 1990; 117(1 Pt 2):S47-S51.
  • [138]Yildirim S, Yeoman CJ, Sipos M, Torralba M, Wilson BA, Goldberg TL et al.. Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLoS One. 2010; 5(11):e13963.
  • [139]Nakamura N, Leigh SR, Mackie RI, Gaskins HR. Microbial community analysis of rectal methanogens and sulfate reducing bacteria in two non-human primate species. J Med Primatol. 2009; 38(5):360-370.
  • [140]Russell RG, Blaser MJ, Sarmiento JI, Fox J. Experimental Campylobacter jejuni infection in Macaca nemestrina. Infect Immun. 1989; 57(5):1438-1444.
  • [141]Fox JG, Boutin SR, Handt LK, Taylor NS, Xu S, Rickman B et al.. Isolation and characterization of a novel helicobacter species, “Helicobacter macacae,” from rhesus monkeys with and without chronic idiopathic colitis. J Clin Microbiol. 2007; 45(12):4061-4063.
  • [142]Montiel-Castro AJ, Gonzalez-Cervantes RM, Bravo-Ruiseco G, Pacheco-Lopez G. The microbiota-gut-brain axis: neurobehavioral correlates, health and sociality. Front Integr Neurosci. 2013; 7:70.
  • [143]Ibeakanma C, Ochoa-Cortes F, Miranda-Morales M, McDonald T, Spreadbury I, Cenac N, et al. Brain–gut interactions increase peripheral nociceptive signaling in mice with postinfectious irritable bowel syndrome. Gastroenterology. 2011;141(6):2098–108.e5.
  • [144]Tranquilli S, Abedi-Lartey M, Amsini F, Arranz L, Asamoah A, Babafemi O et al.. Lack of conservation effort rapidly increases African great ape extinction risk. Conserv Lett. 2012; 5(1):48-55.
  • [145]Reinhardt V, Roberts A. Effective feeding enrichment for non-human primates: a brief review. Anim Welf. 1997; 6(3):265-272.
  • [146]Huff JL, Barry PA. B-virus (Cercopithecine herpesvirus 1) infection in humans and macaques: potential for zoonotic disease. Emerg Infect Dis. 2003; 9(2):246-250.
  • [147]Prescott JF, Barker IK, Manninen KI, Miniats OP. Campylobacter jejuni colitis in gnotobiotic dogs. Can J Comp Med. 1981; 45(4):377-383.
  • [148]Jergens AE, Sonea IM, O’Connor AM, Kauffman LK, Grozdanic SD, Ackermann MR et al.. Intestinal cytokine mRNA expression in canine inflammatory bowel disease: a meta-analysis with critical appraisal. Comp Med. 2009; 59(2):153-162.
  • [149]Rossi G, Pengo G, Caldin M, Palumbo Piccionello A, Steiner JM, Cohen ND et al.. Comparison of microbiological, histological, and immunomodulatory parameters in response to treatment with either combination therapy with prednisone and metronidazole or probiotic VSL#3 strains in dogs with idiopathic inflammatory bowel disease. PLoS One. 2014; 9(4):e94699.
  • [150]Hungate RE. The rumen and its microbes. Academic Press Inc, New York; 1966.
  • [151]Wolfs TG, Kallapur SG, Polglase GR, Pillow JJ, Nitsos I, Newnham JP et al.. IL-1alpha mediated chorioamnionitis induces depletion of FoxP3+ cells and ileal inflammation in the ovine fetal gut. PLoS One. 2011; 6(3):e18355.
  • [152]Krebs T, Boettcher M, Schafer H, Eschenburg G, Wenke K, Appl B et al.. Gut inflammation and expression of ICC in a fetal lamb model of fetoscopic intervention for gastroschisis. Surg Endosc. 2014; 28(8):2437-2442.
  • [153]Pierce ES. Ulcerative colitis and Crohn’s disease: is Mycobacterium avium subspecies paratuberculosis the common villain? Gut Pathog. 2010; 2(1):21.
  • [154]Greenstein RJ. Is Crohn’s disease caused by a mycobacterium? Comparisons with leprosy, tuberculosis, and Johne’s disease. Lancet Infect Dis. 2003; 3(8):507-514.
  • [155]Liaskos C, Spyrou V, Roggenbuck D, Athanasiou LV, Orfanidou T, Mavropoulos A et al.. Crohn’s disease-specific pancreatic autoantibodies are specifically present in ruminants with paratuberculosis: implications for the pathogenesis of the human disease. Autoimmunity. 2013; 46(6):388-394.
  • [156]Pesciaroli M, Aloisio F, Ammendola S, Pistoia C, Petrucci P, Tarantino M et al.. An attenuated Salmonella enterica serovar Typhimurium strain lacking the ZnuABC transporter induces protection in a mouse intestinal model of Salmonella infection. Vaccine. 2011; 29(9):1783-1790.
  • [157]Gerdts V, Uwiera RRE, Mutwiri GK, Wilson DJ, Bowersock T, Kidane A et al.. Multiple intestinal ‘loops’ provide an in vivo model to analyse multiple mucosal immune responses. J Immunol Methods. 2001; 256(1–2):19-33.
  • [158]Kuroe K, Haga Y, Funakoshi O, Mizuki I, Kanazawa K, Yoshida Y. Extraintestinal manifestations of granulomatous enterocolitis induced in rabbits by long-term submucosal administration of muramyl dipeptide emulsified with Freund’s incomplete adjuvant. J Gastroenterol. 1996; 31(2):199-206.
  • [159]Bozeman AP, Dassinger MS, Birusingh RJ, Burford JM, Smith SD. An animal model of necrotizing enterocolitis (NEC) in preterm rabbits. Fetal Pediatr Pathol. 2013; 32(2):113-122.
  • [160]Voravuthikunchai SP, Lee A. Cecectomy causes long-term reduction of colonization resistance in the mouse gastrointestinal tract. Infect Immun. 1987; 55(4):995-999.
  • [161]Henriksson A, Khaled AKD, Conway PL. The effect of caecectomy on the faecal concentrations of urobilinogen and active trypsin in mice. Microb Ecol Health Dis. 1996; 9(2):61-65.
  • [162]Winter HS, Hendren RB, Fox CH, Russell GJ, Perez-Atayde A, Bhan AK et al.. Human intestine matures as nude mouse xenograft. Gastroenterology. 1991; 100(1):89-98.
  • [163]Golan L, Gonen E, Yagel S, Rosenshine I, Shpigel NY. Enterohemorrhagic Escherichia coli induce attaching and effacing lesions and hemorrhagic colitis in human and bovine intestinal xenograft models. Dis Model Mech. 2011; 4(1):86-94.
  • [164]Leapman SB, Deutsch AA, Grand RJ, Folkman J. Transplant of fetal intestine: survival and function in a subcutaneous in adult animals. Ann Surg. 1974; 179:109-114.
  • [165]Savidge TC, Morey AL, Ferguson DJ, Fleming KA, Shmakov AN, Phillips AD. Human intestinal development in a severe-combined immunodeficient xenograft model. Differentiation. 1995; 58(5):361-371.
  • [166]Savidge TC, Pan W-H, Newman P, O’Brien M, Anton PM, Pothoulakis C. Clostridium difficile toxin B is an inflammatory enterotoxin in human intestine. Gastroenterology. 2003; 125(2):413-420.
  • [167]Thulin JD, Kuhlenschmidt MS, Rolsma MD, Current WL, Gelberg HB. An intestinal xenograft model for Cryptosporidium parvum infection. Infect Immun. 1994; 62(1):329-331.
  • [168]Laurent F, Eckmann L, Savidge TC, Morgan G, Theodos C, Naciri M et al.. Cryptosporidium parvum infection of human intestinal epithelial cells induces the polarized secretion of C-X-C chemokines. Infect Immun. 1997; 65(12):5067-5073.
  • [169]Seydel KB, Zhang T, Champion GA, Fichtenbaum C, Swanson PE, Tzipori S et al.. Cryptosporidium parvum infection of human intestinal xenografts in SCID mice induces production of human tumor necrosis factor alpha and interleukin-8. Infect Immun. 1998; 66(5):2379-2382.
  • [170]Melendez-Lopez SG, Herdman S, Hirata K, Choi M-H, Choe Y, Craik C et al.. Use of recombinant Entamoeba histolytica cysteine proteinase 1 to identify a potent inhibitor of amebic invasion in a human colonic model. Eukaryot Cell. 2007; 6(7):1130-1136.
  • [171]Seydel KB, Li E, Swanson PE, Stanley SL. Human intestinal epithelial cells produce proinflammatory cytokines in response to infection in a SCID mouse-human intestinal xenograft model of amebiasis. Infect Immun. 1997; 65(5):1631-1639.
  • [172]Seydel KB, Li E, Zhang Z, Stanley SL. Epithelial cell-initiated inflammation plays a crucial role in early tissue damage in amebic infection of human intestine. Gastroenterology. 1998; 115(6):1446-1453.
  • [173]Zhang Z, Mahajan S, Zhang X, Stanley SL. Tumor necrosis factor alpha is a key mediator of gut inflammation seen in amebic colitis in human intestine in the SCID mouse-human intestinal xenograft model of disease. Infect Immun. 2003; 71(9):5355-5359.
  • [174]Thulin JD, Kuhlenschmidt MS, Gelberg HB. Development, characterization, and utilization of an intestinal xenograft model for infectious disease research. Lab Invest. 1991; 65(6):719-731.
  • [175]Lozniewski A, Muhale F, Hatier R, Marais A, Conroy MC, Edert D et al.. Human embryonic gastric xenografts in nude mice: a new model of Helicobacter pylori infection. Infect Immun. 1999; 67(4):1798-1805.
  • [176]Golan L, Livneh-Kol A, Gonen E, Yagel S, Rosenshine I, Shpigel NY. Mycobacterium avium paratuberculosis invades human small-intestinal goblet cells and elicits inflammation. J Infect Dis. 2009; 199(3):350-354.
  • [177]Huang GT, Eckmann L, Savidge TC, Kagnoff MF. Infection of human intestinal epithelial cells with invasive bacteria upregulates apical intercellular adhesion molecule-1 (ICAM)-1) expression and neutrophil adhesion. J Clin Invest. 1996; 98(2):572-583.
  • [178]Eckmann L, Stenson WF, Savidge TC, Lowe DC, Barrett KE, Fierer J et al.. Role of intestinal epithelial cells in the host secretory response to infection by invasive bacteria. Bacterial entry induces epithelial prostaglandin h synthase-2 expression and prostaglandin E2 and F2alpha production. J Clin Invest. 1997; 100(2):296-309.
  • [179]Zhang Z, Jin L, Champion G, Seydel KB, Stanley SL. Shigella infection in a SCID mouse-human intestinal xenograft model: role for neutrophils in containing bacterial dissemination in human intestine. Infect Immun. 2001; 69(5):3240-3247.
  • [180]Laflin SL, Gnad DP. Rumen cannulation: procedure and use of a cannulated bovine. Vet Clin N Am Food A. 2008;24(2):335–40, vii. doi:10.1016/j.cvfa.2008.02.007.
  • [181]Rupp GP, Kreikemeier KK, Perino LJ, Ross GS. Measurement of volatile fatty acid disappearance and fluid flux across the abomasum of cattle, using an improved omasal cannulation technique. Am J Vet Res. 1994; 55(4):522-529.
  • [182]Horigane A, Araki T, Horigane AK, Hashimoto K, Shinoda M, Sasaki I et al.. Technical note: development of a duodenal cannula for sheep. J Anim Sci. 1992; 70(4):1216-1219.
  • [183]Robinson PH, Kennelly JJ. Evaluation of a duodenal cannula for dairy cattle. J Dairy Sci. 1990; 73(11):3146-3157.
  • [184]Aliyev AA. New methods for re-entrant cannulation of the duodenum and ileocaecum. Res Vet Sci. 1982; 32(3):265-269.
  • [185]Ivan M, Johnston DW. Reentrant cannulation of the small intestine in sheep: cannula and surgical method. J Anim Sci. 1981; 52(4):849-856.
  • [186]MacRae JC, Reid CS, Dellow DW, Wyburn RS. Cannulation of the caecum in sheep. Proc Nutr Soc. 1973; 32(1):23A-24A.
  • [187]Allen AJ, Park KT, Barrington GM, Lahmers KK, Hamilton MJ, Davis WC. Development of a bovine ileal cannulation model to study the immune response and mechanisms of pathogenesis of paratuberculosis. Clin Vaccine Immunol. 2009; 16(4):453-463.
  • [188]St Jean G, Rings DM, Schmall LM, Hull BL, Hoffsis GF. Comparison of three intestinal cannulas used to obtain repeated biopsy of the jejunal mucosa in the newborn calf. Cornell Vet. 1989; 79(3):283-293.
  • [189]Gidenne T, Bellier R. In vivo study of cecal fermentation activity in the rabbit. Completion and validation of a new technique for cecal cannulation. Reprod Nutri Dev. 1992; 32(4):365-376.
  • [190]Kunta JR, Perry BA, Sutyak JP, Sinko PJ. Development of a novel intestinal and vascular access port (IVAP) rabbit model to study regiospecific oral absorption pharmacokinetics. Comp Med. 2001; 51(4):349-356.
  • [191]Bellier R, Gidenne T, Vernay M, Colin M. In vivo study of circadian variations of the cecal fermentation pattern in postweaned and adult rabbits. J Anim Sci. 1995; 73(1):128-135.
  • [192]Zysset T, Bieri HU, Probst P, Bircher J. A rabbit model allowing access to portal vein, vena cava, aorta and duodenum without anesthesia. Arzneimittelforschung. 1981; 31(6):965-969.
  • [193]Walker JA, Harmon DL, Gross KL, Collings GF. Evaluation of nutrient utilization in the canine using the ileal cannulation technique. J Nutr. 1994; 124(12 Suppl):2672S-2676S.
  • [194]Defilippi C, Cumsille F. Small-intestine absorption during continuous intraduodenal infusion of nutrients in dogs. Nutrition. 2001; 17(3):254-258.
  • [195]Hill RC, Ellison GW, Burrows CF, Bauer JE, Carbia B. Ileal cannulation and associated complications in dogs. Lab Anim Sci. 1996; 46(1):77-80.
  • [196]Rubinstein A, Li VH, Gruber P, Bass P, Robinson JR. Improved intestinal cannula for drug delivery studies in the dog. J Pharmacol Methods. 1988; 19(3):213-217.
  • [197]Jacobson M, Lindberg JE, Lindberg R, Segerstad CH, Wallgren P, Fellstrom C et al.. Intestinal cannulation: model for study of the midgut of the pig. Comp Med. 2001; 51(2):163-170.
  • [198]Hogberg A, Lindberg JE, Wallgren P. Influence of ileo-caecal cannulation and oxytetracycline on ileo-caecal and rectal coliform populations in pigs. Acta Vet Scand. 2001; 42(4):435-440.
  • [199]Wubben JE, Smiricky MR, Albin DM, Gabert VM. Improved procedure and cannula design for simple-T cannulation at the distal ileum in growing pigs. Contemp Top Lab Anim Sci. 2001; 40(6):27-31.
  • [200]Simmons HA, Ford EJ. Multiple cannulation of the large intestine of the horse. Br Vet J. 1988; 144(5):449-454.
  • [201]Santos RL, Zhang S, Tsolis RM, Baumler AJ, Adams LG. Morphologic and molecular characterization of Salmonella typhimurium infection in neonatal calves. Vet Pathol. 2002; 39(2):200-215.
  • [202]Vidal JE, McClane BA, Saputo J, Parker J, Uzal FA. Effects of Clostridium perfringens beta-toxin on the rabbit small intestine and colon. Infect Immun. 2008; 76(10):4396-4404.
  • [203]Uzzau S, Leori GS, Petruzzi V, Watson PR, Schianchi G, Bacciu D et al.. Salmonella enterica serovar-host specificity does not correlate with the magnitude of intestinal invasion in sheep. Infect Immun. 2001; 69(5):3092-3099.
  • [204]Xue H, Song D, Shi B, Li Y, Li J. Tracking of green fluorescent protein labeled Escherichia coli confirms bacterial translocation in blind loop rat. J Surg Res. 2007; 143(2):206-210.
  • [205]Uwiera RR, Kastelic JP, Inglis GD. Catheterization of intestinal loops in ruminants. J Vis Exp. 2009; 28:1301.
  • [206]Inglis GD, Kastelic JP, Uwiera RRE. Catheterization of intestinal loops in ruminants does not adversely affect loop function. Comp Med. 2010; 60(6):469-478.
  • [207]Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M et al.. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun. 2003; 71(5):2839-2858.
  • [208]Pizarro TT, Arseneau KO, Bamias G, Cominelli F. Mouse models for the study of Crohn’s disease. Trends Mol Med. 2003; 9(5):218-222.
  • [209]Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB et al.. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006; 131(1):117-129.
  • [210]Perse M, Cerar A. Dextran sodium sulphate colitis mouse model: traps and tricks. J Biomed Biotechnol. 2012; 2012:718617.
  • [211]Wirtz S, Neufert C, Weigmann B, Neurath MF. Chemically induced mouse models of intestinal inflammation. Nat Protoc. 2007; 2(3):541-546.
  • [212]Lakhan SE, Kirchgessner A. Neuroinflammation in inflammatory bowel disease. J Neuroinflamm. 2010; 7:37.
  • [213]Kitajima S, Morimoto M, Sagara E, Shimizu C, Ikeda Y. Dextran sodium sulfate-induced colitis in germ-free IQI/Jic mice. Exp Anim. 2001; 50(5):387-395.
  • [214]Kawada M, Arihiro A, Mizoguchi E. Insights from advances in research of chemically induced experimental models of human inflammatory bowel disease. World J Gastroenterol. 2007; 13(42):5581-5593.
  • [215]Yan Y, Kolachala V, Dalmasso G, Nguyen H, Laroui H, Sitaraman SV et al.. Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS One. 2009; 4(6):e6073.
  • [216]Hakansson A, Tormo-Badia N, Baridi A, Xu J, Molin G, Hagslatt ML et al.. Immunological alteration and changes of gut microbiota after dextran sulfate sodium (DSS) administration in mice. Clin Exp Med. 2015; 15:107-120.
  • [217]Oz HS, Chen T, Ebersole JL. A model for chronic mucosal inflammation in IBD and periodontitis. Dig Dis Sci. 2010; 55(8):2194-2202.
  • [218]Young D, Ibuki M, Nakamori T, Fan M, Mine Y. Soy-derived di- and tripeptides alleviate colon and ileum inflammation in pigs with dextran sodium sulfate-induced colitis. J Nutr. 2012; 142(2):363-368.
  • [219]Kim CJ, Kovacs-Nolan JA, Yang C, Archbold T, Fan MZ, Mine Y. l-Tryptophan exhibits therapeutic function in a porcine model of dextran sodium sulfate (DSS)-induced colitis. J Nutr Biochem. 2010; 21(6):468-475.
  • [220]Sussman DA, Santaolalla R, Strobel S, Dheer R, Abreu MT. Cancer in inflammatory bowel disease: lessons from animal models. Curr Opin Gastroenterol. 2012; 28(4):327-333.
  • [221]Venning FA, Claesson MH, Kissow H. The carcinogenic agent azoxymethane (AOM) enhances early inflammation-induced colon crypt pathology. J Cancer Sci Ther. 2013; 5(11):377-383.
  • [222]Chen J, Huang XF. The signal pathways in azoxymethane-induced colon cancer and preventive implications. Cancer Biol Ther. 2009; 8(14):1313-1317.
  • [223]Saleh M, Trinchieri G. Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat Rev Immunol. 2011; 11(1):9-20.
  • [224]Mariman R, Kremer B, van Erk M, Lagerweij T, Koning F, Nagelkerken L. Gene expression profiling identifies mechanisms of protection to recurrent trinitrobenzene sulfonic acid colitis mediated by probiotics. Inflamm Bowel Dis. 2012; 18(8):1424-1433.
  • [225]Pouillart PR, Depeint F, Abdelnour A, Deremaux L, Vincent O, Maziere JC et al.. Nutriose, a prebiotic low-digestible carbohydrate, stimulates gut mucosal immunity and prevents TNBS-induced colitis in piglets. Inflamm Bowel Dis. 2010; 16(5):783-794.
  • [226]Kim HS, Berstad A. Experimental colitis in animal models. Scand J Gastroenterol. 1992; 27(7):529-537.
  • [227]Kremer B, Mariman R, van Erk M, Lagerweij T, Nagelkerken L. Temporal colonic gene expression profiling in the recurrent colitis model identifies early and chronic inflammatory processes. PLoS One. 2012; 7(11):e50388.
  • [228]Fichtner-Feigl S, Fuss IJ, Young CA, Watanabe T, Geissler EK, Schlitt H-J et al.. Induction of IL-13 triggers TGF-β1-dependent tissue fibrosis in chronic 2,4,6-trinitrobenzene sulfonic acid colitis. J Immunol. 2007; 178(9):5859-5870.
  • [229]Uhlig HH, McKenzie BS, Hue S, Thompson C, Joyce-Shaikh B, Stepankova R et al.. Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity. 2006; 25(2):309-318.
  • [230]Alex P, Zachos NC, Nguyen T, Gonzales L, Chen TE, Conklin LS et al.. Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm Bowel Dis. 2009; 15(3):341-352.
  • [231]Neurath MF. IL-23: a master regulator in Crohn disease. Nat Med. 2007; 13(1):26-28.
  • [232]Brenna O, Furnes MW, Drozdov I, van Beelen Granlund A, Flatberg A, Sandvik AK et al.. Relevance of TNBS-colitis in rats: a methodological study with endoscopic, histologic and transcriptomic [corrected] characterization and correlation to IBD. PLoS One. 2013; 8(1):e54543.
  • [233]Neurath M, Fuss I, Strober W. TNBS-colitis. Int Rev Immunol. 2000; 19(1):51-62.
  • [234]Boirivant M, Fuss IJ, Chu A, Strober W. Oxazolone colitis: a murine model of T helper cell type 2 colitis treatable with antibodies to interleukin 4. J Exp Med. 1998; 188(10):1929-1939.
  • [235]Gerlach K, Hwang Y, Nikolaev A, Atreya R, Dornhoff H, Steiner S et al.. TH9 cells that express the transcription factor PU.1 drive T cell-mediated colitis via IL-9 receptor signaling in intestinal epithelial cells. Nat Immunol. 2014; 15(7):676-686.
  • [236]Lombardi VR, Etcheverria I, Carrera I, Cacabelos R, Chacon AR. Prevention of chronic experimental colitis induced by dextran sulphate sodium (DSS) in mice treated with FR91. J Biomed Biotechnol. 2012; 2012:826178.
  • [237]Whittem CG, Williams AD, Williams CS. Murine colitis modeling using dextran sulfate sodium (DSS). J Vis Exp. 2010; 35:1652.
  • [238]Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS et al.. Metagenomic analysis of the human distal gut microbiome. Science. 2006; 312(5778):1355-1359.
  • [239]Hoffmann C, Hill DA, Minkah N, Kirn T, Troy A, Artis D et al.. Community-wide response of the gut microbiota to enteropathogenic Citrobacter rodentium infection revealed by deep sequencing. Infect Immun. 2009; 77(10):4668-4678.
  • [240]Shen XJ, Rawls JF, Randall T, Burcal L, Mpande CN, Jenkins N et al.. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes. 2010; 1(3):138-147.
  • [241]Sherman MA, Kalman D. Initiation and resolution of mucosal inflammation. Immunol Res. 2004; 29(1–3):241-252.
  • [242]Bhinder G, Sham HP, Chan JM, Morampudi V, Jacobson K, Vallance BA. The Citrobacter rodentium mouse model: studying pathogen and host contributions to infectious colitis. J Vis Exp. 2013; 72:e50222.
  • [243]Bergstrom KS, Guttman JA, Rumi M, Ma C, Bouzari S, Khan MA et al.. Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen. Infect Immun. 2008; 76(2):796-811.
  • [244]Rodrigues DM, Sousa AJ, Johnson-Henry KC, Sherman PM, Gareau MG. Probiotics are effective for the prevention and treatment of Citrobacter rodentium-induced colitis in mice. J Infect Dis. 2012; 206(1):99-109.
  • [245]Smith AD, Botero S, Shea-Donohue T, Urban JF. The pathogenicity of an enteric Citrobacter rodentium infection is enhanced by deficiencies in the antioxidants selenium and vitamin E. Infect Immun. 2011; 79(4):1471-1478.
  • [246]Costa E, Uwiera RR, Kastelic JP, Selinger LB, Inglis GD. Non-therapeutic administration of a model antimicrobial growth promoter modulates intestinal immune responses. Gut Pathog. 2011; 3(1):14.
  • [247]Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S. Citrobacter rodentium of mice and man. Cell Microbiol. 2005; 7(12):1697-1706.
  • [248]Mohawk KL, O’Brien AD. Mouse models of Escherichia coli O157:H7 infection and shiga toxin injection. J Biomed Biotechnol. 2011; 2011:258185.
  • [249]Melton-Celsa AR, O’Brien AD. Animal models for STEC-mediated disease. In: Philpott D, Ebel F, editors. E. coli. Humana Press; 2003. p. 291–305.
  • [250]Papamichael K, Konstantopoulos P, Mantzaris GJ. Helicobacter pylori infection and inflammatory bowel disease: is there a link? World J Gastroenterol. 2014; 20(21):6374-6385.
  • [251]Smet A, Flahou B, Mukhopadhya I, Ducatelle R, Pasmans F, Haesebrouck F et al.. The other helicobacters. Helicobacter. 2011; 16 Suppl 1:70-75.
  • [252]Chiba T, Marusawa H, Ushijima T. Inflammation-associated cancer development in digestive organs: mechanisms and roles for genetic and epigenetic modulation. Gastroenterology. 2012; 143(3):550-563.
  • [253]Etou T, Iizuka M, Ohshima A, Yagisawa H, Yamano HO, Ishii T et al.. Ulcerative colitis accompanied by idiopathic thrombocytopenic purpura and Helicobacter pylori infection. Intern Med (Tokyo, Japan). 2013; 52(5):547-549.
  • [254]Roka K, Roubani A, Stefanaki K, Panayotou I, Roma E, Chouliaras G. The prevalence of Helicobacter pylori gastritis in newly diagnosed children with inflammatory bowel disease. Helicobacter. 2014; 19(5):400-405.
  • [255]Zhang S, Moss SF. Rodent models of Helicobacter infection, inflammation, and disease. In: Houghton J, editor. Helicobacter Species. Humana Press; 2012. p. 89–98.
  • [256]Luther J, Dave M, Higgins PD, Kao JY. Association between Helicobacter pylori infection and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Inflamm Bowel Dis. 2010; 16(6):1077-1084.
  • [257]Hansen R, Thomson JM, Fox JG, El-Omar EM, Hold GL. Could Helicobacter organisms cause inflammatory bowel disease? FEMS Immunol Med Microbiol. 2011; 61(1):1-14.
  • [258]Woodworth HL, McCaskey SJ, Duriancik DM, Clinthorne JF, Langohr IM, Gardner EM et al.. Dietary fish oil alters T lymphocyte cell populations and exacerbates disease in a mouse model of inflammatory colitis. Cancer Res. 2010; 70(20):7960-7969.
  • [259]Ericsson AC, Myles M, Davis W, Ma L, Lewis M, Maggio-Price L et al.. Noninvasive detection of inflammation-associated colon cancer in a mouse model. Neoplasia (New York, NY). 2010; 12(12):1054-1065.
  • [260]Fox JG, Dewhirst FE, Tully JG, Paster BJ, Yan L, Taylor NS et al.. Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J Clin Microbiol. 1994; 32(5):1238-1245.
  • [261]Fox JG, Ge Z, Whary MT, Erdman SE, Horwitz BH. Helicobacter hepaticus infection in mice: models for understanding lower bowel inflammation and cancer. Mucosal Immunol. 2011; 4(1):22-30.
  • [262]Ward JM, Fox JG, Anver MR, Haines DC, George CV, Collins MJ et al.. Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J Natl Cancer Inst. 1994; 86(16):1222-1227.
  • [263]Foltz CJ, Fox JG, Cahill R, Murphy JC, Yan L, Shames B et al.. Spontaneous inflammatory bowel disease in multiple mutant mouse lines: association with colonization by Helicobacter hepaticus. Helicobacter. 1998; 3(2):69-78.
  • [264]Wu S, Lu R, Zhang YG, Sun J. Chronic Salmonella infected mouse model. J Vis Exp. 2010; 39:1947.
  • [265]Vishwakarma V, Pati NB, Ray S, Das S, Suar M. TTSS2-deficient hha mutant of Salmonella Typhimurium exhibits significant systemic attenuation in immunocompromised hosts. Virulence. 2014; 5(2):311-320.
  • [266]Lawhon SD, Khare S, Rossetti CA, Everts RE, Galindo CL, Luciano SA et al.. Role of SPI-1 secreted effectors in acute bovine response to Salmonella enterica Serovar Typhimurium: a systems biology analysis approach. PLoS One. 2011; 6(11):e26869.
  • [267]Mastroeni P, Chabalgoity JA, Dunstan SJ, Maskell DJ, Dougan G. Salmonella: immune responses and vaccines. Vet J. 2001; 161(2):132-164.
  • [268]Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, Winter SE et al.. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med. 2008; 14(4):421-428.
  • [269]Elguezabal N, Chamorro S, Molina E, Garrido JM, Izeta A, Rodrigo L et al.. Lactase persistence, NOD2 status and Mycobacterium avium subsp. paratuberculosis infection associations to inflammatory bowel disease. Gut Pathog. 2012; 4(1):6.
  • [270]Mutwiri GK, Kosecka U, Benjamin M, Rosendal S, Perdue M, Butler DG. Mycobacterium avium subspecies paratuberculosis triggers intestinal pathophysiologic changes in beige/scid mice. Comp Med. 2001; 51(6):538-544.
  • [271]Koc A, Bargen I, Suwandi A, Roderfeld M, Tschuschner A, Rath T et al.. Systemic and mucosal immune reactivity upon Mycobacterium avium ssp. paratuberculosis infection in mice. PLoS One. 2014; 9(4):e94624.
  • [272]McClure HM, Chiodini RJ, Anderson DC, Swenson RB, Thayer WR, Coutu JA. Mycobacterium paratuberculosis infection in a colony of stumptail macaques (Macaca arctoides). J Infect Dis. 1987; 155(5):1011-1019.
  • [273]Antignano F, Mullaly SC, Burrows K, Zaph C. Trichuris muris infection: a model of type 2 immunity and inflammation in the gut. J Vis Exp. 2011; 51:2774.
  • [274]Hernandez JL, Leung G, McKay DM. Cestode regulation of inflammation and inflammatory diseases. Int J Parasitol. 2013; 43(3–4):233-243.
  • [275]Cliffe LJ, Grencis RK. The Trichuris muris system: a paradigm of resistance and susceptibility to intestinal nematode infection. Adv Parasitol. 2004; 57:255-307.
  • [276]Owyang AM, Zaph C, Wilson EH, Guild KJ, McClanahan T, Miller HR et al.. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J Exp Med. 2006; 203(4):843-849.
  • [277]Bancroft AJ, Else KJ, Humphreys NE, Grencis RK. The effect of challenge and trickle Trichuris muris infections on the polarisation of the immune response. Int J Parasitol. 2001; 31(14):1627-1637.
  • [278]Hasnain SZ, Thornton DJ, Grencis RK. Changes in the mucosal barrier during acute and chronic Trichuris muris infection. Parasite Immunol. 2011; 33(1):45-55.
  • [279]Artis D, Potten CS, Else KJ, Finkelman FD, Grencis RK. Trichuris muris: host intestinal epithelial cell hyperproliferation during chronic infection is regulated by interferon-gamma. Exp Parasitol. 1999; 92(2):144-153.
  • [280]Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 2011; 474(7351):298-306.
  • [281]Jensen KD, Wang Y, Wojno ED, Shastri AJ, Hu K, Cornel L et al.. Toxoplasma polymorphic effectors determine macrophage polarization and intestinal inflammation. Cell Host Microbe. 2011; 9(6):472-483.
  • [282]Wilson MS, Feng CG, Barber DL, Yarovinsky F, Cheever AW, Sher A et al.. Redundant and pathogenic roles for IL-22 in mycobacterial, protozoan, and helminth infections. J Immunol. 2010; 184(8):4378-4390.
  • [283]Pierdomenico M, Negroni A, Stronati L, Vitali R, Prete E, Bertin J et al.. Necroptosis is active in children with inflammatory bowel disease and contributes to heighten intestinal inflammation. Am J Gastroenterol. 2014; 109(2):279-287.
  • [284]Matsumoto H, Kimura Y, Murao T, Osawa M, Akiyama T, Mannoji K et al.. Severe colitis associated with both Epstein–Barr virus and cytomegalovirus reactivation in a patient with severe aplastic anemia. Case Rep Gastroenterol. 2014; 8(2):240-244.
  • [285]Sim WH, Wagner J, Cameron DJ, Catto-Smith AG, Bishop RF, Kirkwood CD. Expression profile of genes involved in pathogenesis of pediatric Crohn’s disease. J Gastroenterol Hepatol. 2012; 27(6):1083-1093.
  • [286]Lidar M, Langevitz P, Barzilai O, Ram M, Porat-Katz BS, Bizzaro N et al.. Infectious serologies and autoantibodies in inflammatory bowel disease: insinuations at a true pathogenic role. Ann N Y Acad Sci. 2009; 1173(1):640-648.
  • [287]Ekbom A, Daszak P, Kraaz W, Wakefield AJ. Crohn’s disease after in utero measles virus exposure. Lancet. 1996; 348(9026):515-517.
  • [288]Montgomery SM, Morris DL, Pounder RE, Wakefield AJ. Paramyxovirus infections in childhood and subsequent inflammatory bowel disease. Gastroenterology. 1999; 116(4):796-803.
  • [289]Thomas PD, Pollok R, Gazzard BG. Enteric viral infections as a cause of diarrhoea in the acquired immunodeficiency syndrome. HIV Med. 1999; 1(1):19-24.
  • [290]Coban S, Ensari A, Kuzu MA, Yalcin S, Palabiyikoglu M, Ormeci N. Cytomegalovirus infection in a patient with Crohn’s ileocolitis. Can J Gastroenterol. 2005; 19(2):109-111.
  • [291]Hussein K, Hayek T, Yassin K, Fischer D, Vlodavsky E, Kra-Oz Z, et al. Acute cytomegalovirus infection associated with the onset of inflammatory bowel disease. Am J Med Sci. 2006;331(1):40–3. doi:00000441-200601000-00012.
  • [292]Brunson JL, Becker F, Stokes KY. The impact of primary and persistent cytomegalovirus infection on the progression of acute colitis in a murine model. Pathophysiology. 2015; 22(1):31-37.
  • [293]Stoicov C, Whary M, Rogers AB, Lee FS, Klucevsek K, Li H et al.. Coinfection modulates inflammatory responses and clinical outcome of Helicobacter felis and Toxoplasma gondii infections. J Immunol. 2004; 173(5):3329-3336.
  • [294]Neurath MF, Finotto S, Glimcher LH. The role of Th1/Th2 polarization in mucosal immunity. Nat Med. 2002; 8(6):567-573.
  • [295]O’Shea JJ, Paul WE. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science. 2010; 327(5969):1098-1102.
  • [296]Sollid LM, Johansen FE. Animal models of inflammatory bowel disease at the dawn of the new genetics era. PLoS Med. 2008; 5(9):5.
  • [297]Coombes JL, Robinson NJ, Maloy KJ, Uhlig HH, Powrie F. Regulatory T cells and intestinal homeostasis. Immunol Rev. 2005; 204:184-194.
  • [298]Stolfi C, Rizzo A, Franze E, Rotondi A, Fantini MC, Sarra M et al.. Involvement of interleukin-21 in the regulation of colitis-associated colon cancer. J Exp Med. 2011; 208(11):2279-2290.
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