Worms, flies and four-legged friends: The applicability of biological models to the understanding of intestinal inflammatory diseases

DMM Disease Models and Mechanisms

Volumn 4, Issue 4, 2011, Pages 447-456

  Lin, Joyce ^a,b   Hackam, David J ^a,b  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BLEOMYCIN; DEXTRAN SULFATE; ENDOTOXIN; GAMMA INTERFERON; IMMUNOSUPPRESSIVE AGENT; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1; INTERLEUKIN 20; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; NERVE CELL ADHESION MOLECULE; OXAZOLONE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SERINE PROTEINASE INHIBITOR; STAT PROTEIN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; TOLL LIKE RECEPTOR 4; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR ALPHA;

ABDOMINAL INFECTION; ABDOMINAL PAIN; APOPTOSIS; BACTERIUM; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; CD4+ T LYMPHOCYTE; CELL DAMAGE; CELL DEATH; CELL PROLIFERATION; CELL REGENERATION; CELLS AND CELL COMPONENTS; CHICKEN; COST; CROHN DISEASE; DIET THERAPY; DISEASE COURSE; DISEASE PREDISPOSITION; DISEASE SEVERITY; DNA POLYMORPHISM; DROSOPHILA MELANOGASTER; ENDOTHELIUM CELL; ENTERITIS; ENTEROCOLITIS; ENTEROENDOCRINE CELL; EPITHELIUM CELL; EXPERIMENTAL RABBIT; FLUID RESUSCITATION; FLY; GASTROINTESTINAL SURGERY; GENE SILENCING; GENOME; GOBLET CELL; GRANULOMA; GROUPS BY AGE; HOMEOSTASIS; HOUSING; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; INFLAMMATION; INNATE IMMUNITY; INTENSIVE CARE UNIT; INTESTINE; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE INJURY; INTESTINE NECROSIS; INTESTINE PERFORATION; LAPAROTOMY; LEUKOCYTE; LIFESPAN; MAMMAL; MEMBRANE DAMAGE; MEMBRANE PERMEABILITY; MESENCHYME CELL; MICROBIOME; MICROVASCULATURE; MORBIDITY; MOUSE STRAIN; NECROSIS; NECROTIZING ENTEROCOLITIS; NEMATODE; NEWBORN MORBIDITY; NONHUMAN; NOTE; NUTRITIONAL INTOLERANCE; ONSET AGE; ORGANISMAL INTERACTION; OVERALL SURVIVAL; PANETH CELL; PATHOGENESIS; PHASE CONTRAST MICROSCOPE; PIGLET; PREMATURITY; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUALITY OF LIFE; RECTUM HEMORRHAGE; REGENERATION; RODENT; SEPSIS; SEQUENCE HOMOLOGY; SHEEP; SIGNAL TRANSDUCTION; SKIN DEFECT; TH2 CELL; ULCERATIVE COLITIS; VEIN THROMBOSIS; VERTEBRATE; WORM;

ANIMALS; DIPTERA; DISEASE MODELS, ANIMAL; HELMINTHS; INFLAMMATORY BOWEL DISEASES; MODELS, BIOLOGICAL; VERTEBRATES;

ANIMALIA; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; INVERTEBRATA; MAMMALIA; MUS; RATTUS; VERTEBRATA;

EID: 79959635045     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.007252     Document Type: Note

References (130)

1. Aboobaker, A. A. and Blaxter, M. L. (2000). Medical significance of Caenorhabditis elegans. Ann. Med. 32, 23-30.
2. Abreu, M. T., Vora, P., Faure, E., Thomas, L. S., Arnold, E. T. and Arditi, M. (2001). Decreased expression of Toll-Like Receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J. Immunol. 167, 1609-1616. (Pubitemid 32703162)
3. Abreu, M. T., Arnold, E. T., Thomas, L. S., Gonsky, R., Zhou, Y., Hu, B. and Arditi, M. (2002). TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J. Biol. Chem. 277, 20431-20437.
4. Achilleos, A., Wehman, A. M. and Nance, J. (2010). PAR-3 mediates the initial clustering and apical localization of junction and polarity proteins during C. elegans intestinal epithelial cell polarization. Development 137, 1833-1842.
5. Afrazi, A., Sodhi, C. P., Richardson, W., Neal, M., Good, M., Siggers, R. and Hackam, D. J. (2010). New insights into the pathogenesis and treatment of necrotizing enterocolitis: Toll-like receptors and beyond. Pediatr. Res. 69, 183-188.
6. Alper, S. (2010). Model systems to the rescue: the relationship between aging and innate immunity. Commun. Integr. Biol. 3, 409-414.
7. Amcheslavsky, A., Jiang, J. and Ip, Y. T. (2009). Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 4, 49-61.
8. Anand, R. J., Leaphart, C. L., Mollen, K. P. and Hackam, D. J. (2007). The role of the intestinal barrier in the pathogenesis of necrotizing enterocolitis. Shock 27, 124-133. (Pubitemid 46105827)
9. Apidianakis, Y., Pitsouli, C., Perrimon, N. and Rahme, L. (2009). Synergy between bacterial infection and genetic predisposition in intestinal dysplasia. Proc. Natl. Acad. Sci. USA 106, 20883-20888.
10. Araki, Y., Mukaisyo, K., Sugihara, H., Fujiyama, Y. and Hattori, T. (2010). Increased apoptosis and decreased proliferation of colonic epithelium in dextran sulfate sodium-induced colitis in mice. Oncol. Rep. 24, 869-874.
11. Arrieta, M. C., Bistritz, L. and Meddings, J. B. (2006). Alterations in intestinal permeability. Gut 55, 1512-1520.
12. Baregamian, N., Song, J., Bailey, C. E., Papaconstantinou, J., Evers, B. M. and Chung, D. H. (2009). Tumor necrosis factor-alpha and apoptosis signal-regulating kinase 1 control reactive oxygen species release, mitochondrial autophagy, and c-Jun N-terminal kinase/p38 phosphorylation during necrotizing enterocolitis. Oxid. Med. Cell. Longev. 2, 297-306.
13. Biteau, B., Hochmuth, C. E. and Jasper, H. (2008). JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 3, 442-455.
14. Blakely, M. L., Lally, K. P., McDonald, S., Brown, R. L., Barnhart, D. C., Ricketts, R. R., Thompson, W. R., Scherer, L. R., Klein, M. D., Letton, R. W. et al. (2005). Postoperative outcomes of extremely low birth-weight infants with necrotizing enterocolitis or isolated intestinal perforation: a prospective cohort study by the NICHD Neonatal Research Network. Ann. Surg. 241, 984-989; discussion 989-994.
15. Boismenu, R. and Chen, Y. (2000). Insights from mouse models of colitis. J. Leukoc. Biol. 67, 267-278.
16. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
17. Bruewer, M., Samarin, S. and Nusrat, A. (2006). Inflammatory bowel disease and the apical junctional complex. Ann. N. Y. Acad. Sci. 1072, 242-252.
18. Buchon, N., Broderick, N. A., Poidevin, M., Pradervand, S. and Lemaitre, B. (2009). Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5, 200-211.
19. Calvert, R. and Pothier, P. (1990). Migration of fetal intestinal intervillous cells in neonatal mice. Anat. Rec. 227, 199-206.
20. Caplan, M. S. (2008). Neonatal necrotizing enterocolitis. Introduction. Semin. Perinatol. 32, 69.
21. Cetin, S., Ford, H. R., Sysko, L. R., Agarwal, C., Wang, J., Neal, M. D., Baty, C., Apodaca, G. and Hackam, D. J. (2004). Endotoxin inhibits intestinal epithelial restitution through activation of Rho-GTPase and increased focal adhesions. J. Biol. Chem. 279, 24592-24600.
22. Cetin, S., Leaphart, C. L., Li, J., Ischenko, I., Hayman, M., Upperman, J., Zamora, R., Watkins, S., Ford, H. R., Wang, J. et al. (2007). Nitric oxide inhibits enterocyte migration through activation of RhoA-GTPase in a SHP-2-dependent manner. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1347-G1358.
23. Chinnadurai, G., Vijayalingam, S. and Gibson, S. B. (2008). BNIP3 subfamily BH3-only proteins: mitochondrial stress sensors in normal and pathological functions. Oncogene 27 Suppl. 1, S114-S127.
24. Choi, Y. H., Kim, I. O., Cheon, J. E., Kim, J. E., Kim, E. K., Kim, W. S. and Yeon, K. M. (2010). Doppler sonographic findings in an experimental rabbit model of necrotizing enterocolitis. J. Ultrasound Med. 29, 379-386.
25. Claud, E. C. and Walker, W. A. (2008). Bacterial colonization, probiotics, and necrotizing enterocolitis. J. Clin. Gastroenterol. 42 Suppl. 2, S46-S52.
26. Clayburgh, D. R., Rosen, S., Witkowski, E. D., Wang, F., Blair, S., Dudek, S., Garcia, J. G. N., Alverdy, J. C. and Turner, J. R. (2004). A differentiation-dependent splice variant of Myosin Light Chain Kinase, MLCK1, regulates epithelial tight junction permeability. J. Biol. Chem. 279, 55506-55513.
27. Dai, S., Sodhi, C. P., Cetin, S., Richardson, W., Branca, M., Neal, M. D., Prindle, T., Ma, C., Shapiro, R. A., Li, B. et al. (2010). Extracellular high mobility group box1 (HMGB1) inhibits enterocyte migration via activation of toll like receptor 4 and increased cell-matrix adhesiveness. J. Biol. Chem. 285, 4995-5002.
28. Darby, C. (2005). Interactions with microbial pathogens. WormBook (ed. The C. elegans Research Community, Wormbook), pp. 1-15. http://www.workbook.org.
29. Feng, J. and Besner, G. E. (2007). Heparin-binding epidermal growth factor-like growth factor promotes enterocyte migration and proliferation in neonatal rats with necrotizing enterocolitis. J. Pediatr. Surg. 42, 214-220.
30. Fort, M. M., Mozaffarian, A., Stöver, A. G., Correia, J. S., Johnson, D. A., Crane, R. T., Ulevitch, R. J., Persing, D. H., Bielefeldt-Ohmann, H., Probst, P. et al. (2005). A synthetic TLR4 antagonist has anti-inflammatory effects in two murine models of inflammatory bowel disease. J. Immunol. 174, 6416-6423. (Pubitemid 40663835)
31. Friswell, M., Campbell, B. and Rhodes, J. (2010). The role of bacteria in the pathogenesis of inflammatory bowel disease. Gut Liver 4, 295-306.
32. Frost, B. L., Jilling, T. and Caplan, M. S. (2008). The importance of pro-inflammatory signaling in neonatal necrotizing enterocolitis. Semin. Perinatol. 32, 100-106.
33. Fukata, M., Michelsen, K. S., Eri, R., Thomas, L. S., Hu, B., Lukasek, K., Nast, C. C., Lechago, J., Xu, R., Naiki, Y. et al. (2005). 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. 288, G1055-G1065.
34. Fukata, M., Chen, A., Klepper, A., Krishnareddy, S., Vamadevan, A. S., Thomas, L. S., Xu, R., Inoue, H., Arditi, M., Dannenberg, A. J. et al. (2006). Cox-2 is regulated by Toll-like receptor-4 (TLR4) signaling: role in proliferation and apoptosis in the intestine. Gastroenterology 131, 862-877. (Pubitemid 44316821)
35. Garthright, W. E., Archer, D. L. and Kvenberg, J. E. (1988). Estimates of incidence and costs of intestinal infectious diseases in the United States. Public Health Rep. 103, 107-115.
36. Gosai, S. J., Kwak, J. H., Luke, C. J., Long, O. S., King, D. E., Kovatch, K. J., Johnston, P. A., Shun, T. Y., Lazo, J. S., Perlmutter, D. H. et al. (2010). Automated high-content live animal drug screening using C. elegans expressing the aggregation prone serpin alpha1-antitrypsin Z. PLoS ONE 5, e15460.
37. Grave, G. D., Nelson, S. A., Walker, W. A., Moss, R. L., Dvorak, B., Hamilton, F. A., Higgins, R. and Raju, T. N. (2007). New therapies and preventive approaches for necrotizing enterocolitis: report of a research planning workshop. Pediatr. Res. 62, 510-514.
38. Gribar, S. C., Anand, R., Sodhi, C. P. and Hackam, D. J. (2008). The role of epithelial Toll-like receptor signaling in the pathogenesis of intestinal inflammation. J. Leukoc. Biol. 83, 493-498.
39. Gribar, S. C., Sodhi, C. P., Richardson, W. M., Anand, R. J., Gittes, G. K., Branca, M. F., Jakub, A., Shi, X. H., Shah, S., Ozolek, J. A. et al. (2009). Reciprocal expression and signaling of TLR4 and TLR9 in the pathogenesis and treatment of necrotizing enterocolitis. J. Immunol. 182, 636-646.
40. Ha, C. and Kornbluth, A. (2010). Mucosal healing in inflammatory bowel disease: where do we stand? Curr. Gastroenterol. Rep. 12, 471-478.
41. Hackam, D. J., Upperman, J. S., Grishin, A. and Ford, H. R. (2005). Disordered enterocyte signaling and intestinal barrier dysfunction in the pathogenesis of necrotizing enterocolitis. Semin. Pediatr. Surg. 14, 49-57.
42. Haerty, W., Artieri, C., Khezri, N., Singh, R. S. and Gupta, B. P. (2008). Comparative analysis of function and interaction of transcription factors in nematodes: extensive conservation of orthology coupled to rapid sequence evolution. BMC Genomics 9, 399.
43. Hall, P. A., Coates, P. J., Ansari, B. and Hopwood, D. (1994). Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J. Cell Sci. 107, 3569-3577.
44. Halpern, M. D. and Dvorak, B. (2008). Does abnormal bile acid metabolism contribute to NEC? Semin. Perinatol. 32, 114-121. (Pubitemid 351381167)
45. Hermiston, M. L. and Gordon, J. I. (1995). Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 270, 1203-1207.
46. Holman, R., Stehr-Green, J. and Zelasky, M. (1989). Necrotizing enterocolitis mortality in the United States. Am. J. Public Health 79, 987-989. (Pubitemid 19207429)
47. Holman, R. C., Stoll, B. J., Clarke, M. J. and Glass, R. I. (1997). The epidemiology of necrotizing enterocolitis infant mortality in the United States. Am. J. Public Health 87, 2026-2031. (Pubitemid 28055926)
48. Holman, R. C., Stoll, B. J., Curns, A. T., Yorita, K. L., Steiner, C. A. and Schonberger, L. B. (2006). Necrotising enterocolitis hospitalisations among neonates in the United States. Paediatr. Perinat. Epidemiol. 20, 498-506.
49. Hou, S. X. (2010). Intestinal stem cell asymmetric division in the Drosophila posterior midgut. J. Cell. Physiol. 224, 581-584.
50. Iwasaki, A. and Medzhitov, R. (2010). Regulation of adaptive immunity by the innate immune system. Science 327, 291-295.
51. Jiang, H., Patel, P. H., Kohlmaier, A., Grenley, M. O., McEwen, D. G. and Edgar, B. A. (2009). Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137, 1343-1355.
52. Jilling, T., Simon, D., Lu, J., Meng, F. J., Li, D., Schy, R., Thomson, R. B., Soliman, A., Arditi, M. and Caplan, M. S. (2006). The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J. Immunol. 177, 3273-3282. (Pubitemid 44277847)
53. Kang, C. and Avery, L. (2010). Death-associated protein kinase (DAPK) and signal transduction: fine-tuning of autophagy in Caenorhabditis elegans homeostasis. FEBS J. 277, 66-73.
54. Kappelman, M. D., Rifas-Shiman, S. L., Porter, C. Q., Ollendorf, D. A., Sandler, R. S., Galanko, J. A. and Finkelstein, J. A. (2008). Direct health care costs of Crohn's disease and ulcerative colitis in US children and adults. Gastroenterology 135, 1907-1913.
55. Khailova, L., Mount Patrick, S. K., Arganbright, K. M., Halpern, M. D., Kinouchi, T. and Dvorak, B. (2010). Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 299, G1118-G1127.
56. Kim, C. J., Kovacs-Nolan, J., Yang, C., Archbold, T., Fan, M. Z. and Mine, Y. (2009). L-cysteine supplementation attenuates local inflammation and restores gut homeostasis in a porcine model of colitis. Biochim. Biophys. Acta 1790, 1161-1169.
57. Koon, H. W., Zhao, D., Zhan, Y., Rhee, S. H., Moyer, M. P. and Pothoulakis, C. (2006). Substance P stimulates cyclooxygenase-2 and prostaglandin E2 expression through JAK-STAT activation in human colonic epithelial cells. J. Immunol. 176, 5050-5059.
58. Kormish, J. D., Gaudet, J. and McGhee, J. D. (2010). Development of the C. elegans digestive tract. Curr. Opin. Genet. Dev. 20, 346-354.
59. Krauter, E. M., Strong, D. S., Brooks, E. M., Linden, D. R., Sharkey, K. A. and Mawe, G. M. (2007). Changes in colonic motility and the electrophysiological properties of myenteric neurons persist following recovery from trinitrobenzene sulfonic acid colitis in the guinea pig. Neurogastroenterol. Motil. 19, 990-1000.
60. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K. and Muller, W. (1993). Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274. (Pubitemid 23320290)
61. Leach, M. W., Bean, A. G., Mauze, S., Coffman, R. L. and Powrie, F. (1996). Inflammatory bowel disease in C.B-17 scid mice reconstituted with the CD45RBhigh subset of CD4+ T cells. Am. J. Pathol. 148, 1503-1515.
62. Leaphart, C. L., Cavallo, J. C., Gribar, S. C., Cetin, S., Li, J., Branca, M. F., Dubowski, T. D., Sodhi, C. P. and Hackam, D. J. (2007a). A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J. Immunol. 179, 4808-4820.
63. Leaphart, C. L., Qureshi, F., Cetin, S., Li, J., Dubowski, T., Batey, C., Beer-Stolz, D., Guo, F., Murray, S. A. and Hackam, D. J. (2007b). Interferon-[gamma] inhibits intestinal restitution by preventing gap junction communication between enterocytes. Gastroenterology 132, 2395-2411. (Pubitemid 46890858)
64. Lee, E. G., Boone, D. L., Chai, S., Libby, S. L., Chien, M., Lodolce, J. P. and Ma, A. (2000). Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 289, 2350-2354.
65. Lee, G., Goretsky, T., Managlia, E., Dirisina, R., Singh, A. P., Brown, J. B., May, R., Yang, G. Y., Ragheb, J. W., Evers, B. M. et al. (2010). Phosphoinositide 3-kinase signaling mediates beta-catenin activation in intestinal epithelial stem and progenitor cells in colitis. Gastroenterology 139, 869-881.e9.
66. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. M. and Hoffmann, J. A. (1996). The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973-983.
67. Lindquist, R. A., Ottina, K. A., Wheeler, D. B., Hsu, P. P., Thoreen, C. C., Guertin, D. A., Ali, S. M., Sengupta, S., Shaul, Y. D., Lamprecht, M. R. et al. (2011). Genome-scale RNAi on living-cell microarrays identifies novel regulators of Drosophila melanogaster TORC1-S6K pathway signaling. Genome Res. 21, 433-446.
68. Liu, W., Singh, S. R. and Hou, S. X. (2010). JAK-STAT is restrained by Notch to control cell proliferation of the Drosophila intestinal stem cells. J. Cell. Biochem. 109, 992-999.
69. Liu, Y., Zhang, Z., Wang, L., Li, J., Dong, L., Yue, W., Chen, J., Sun, X., Zhong, L. and Sun, D. (2010). TLR4 monoclonal antibody blockade suppresses dextran-sulfate-sodium-induced colitis in mice. J. Gastroenterol. Hepatol. 25, 209-214.
70. Llanos, A. R., Moss, M. E., Pinzon, M. C., Dye, T., Sinkin, R. A. and Kendig, J. W. (2002). Epidemiology of neonatal necrotising enterocolitis: a population-based study. Paediatr. Perinat. Epidemiol. 16, 342-349.
71. Lu, J., Jilling, T., Li, D. and Caplan, M. S. (2007). Polyunsaturated fatty acid supplementation alters proinflammatory gene expression and reduces the incidence of necrotizing enterocolitis in a neonatal rat model. Pediatr. Res. 61, 427-432.
72. Lu, N., Yu, X., He, X. and Zhou, Z. (2009). Detecting apoptotic cells and monitoring their clearance in the nematode Caenorhabditis elegans. Methods Mol. Biol. 559, 357-370.
73. Luke, C. J., Pak, S. C., Askew, Y. S., Naviglia, T. L., Askew, D. J., Nobar, S. M., Vetica, A. C., Long, O. S., Watkins, S. C., Stolz, D. B. et al. (2007). An intracellular serpin regulates necrosis by inhibiting the induction and sequelae of lysosomal injury. Cell 130, 1108-1119. (Pubitemid 47422305)
74. MacDonald, T. T. and Monteleone, G. (2006). Overview of role of the immune system in the pathogenesis of inflammatory bowel disease. Adv. Exp. Med. Biol. 579, 98-107.
75. Madara, J. L. (1990). Warner-Lambert/Parke-Davis Award lecture. Pathobiology of the intestinal epithelial barrier. Am. J. Pathol. 137, 1273-1281.
76. Mannoia, K., Boskovic, D. S., Slater, L., Plank, M. S., Angeles, D. M. and Gollin, G. (2011). Necrotizing enterocolitis is associated with neonatal intestinal injury. J. Pediatr. Surg. 46, 81-85.
77. Marchiando, A. M., Graham, W. V. and Turner, J. R. (2010). Epithelial barriers in homeostasis and disease. Annu. Rev. Pathol. 5, 119-144.
78. Markaki, M. and Tavernarakis, N. (2010). Modeling human diseases in Caenorhabditis elegans. Biotechnol. J. 5, 1261-1276.
79. Matsumoto, S., Okabe, Y., Setoyama, H., Takayama, K., Ohtsuka, J., Funahashi, H., Imaoka, A., Okada, Y. and Umesaki, Y. (1998). Inflammatory bowel disease-like enteritis and caecitis in a senescence accelerated mouse P1/Yit strain. Gut 43, 71-78. (Pubitemid 28335492)
80. McGhee, J. D. (2007). The C. elegans intestine, WormBook (ed. The C. elegans Research Community, Wormbook), pp. 1-36, http://www.wormbook.org.
81. Melmed, G., Thomas, L. S., Lee, N., Tesfay, S. Y., Lukasek, K., Michelsen, K. S., Zhou, Y., Hu, B., Arditi, M. and Abreu, M. T. (2003). Human intestinal epithelial cells are broadly unresponsive to Toll-Like Receptor 2-Dependent bacterial ligands: implications for host-microbial interactions in the gut J. Immunol. 170, 1406-1415.
82. Micchelli, C. A. and Perrimon, N. (2006). Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439, 475-479. (Pubitemid 43152838)
83. Mizoguchi, A. and Mizoguchi, E. (2010). Animal models of IBD: linkage to human disease. Curr. Opin. Pharmacol. 10, 578-587.
84. Mizrahi, A., Barlow, O., Berdon, W., Blanc, W. A. and Silverman, W. A. (1965). Necrotizing enterocolitis in premature infants. J. Pediatr. 66, 697-705.
85. Mokrowiecka, A., Kumor, A., Jakubczyk, E., Pietruczuk, M. and Malecka-Panas, E. (2010). The application of montreal classification in different clinical and serological IBD subtypes. Hepatogastroenterology 57, 787-793.
86. Mombaerts, P., Mizoguchi, E., Grusby, M. J., Glimcher, L. H., Bhan, A. K. and Tonegawa, S. (1993). Spontaneous development of inflammatory bowel disease in T cell receptor mutant mice. Cell 75, 274-282.
87. Nadler, E. P., Dickinson, E., Knisely, A., Zhang, X. R., Boyle, P., Beer-Stolz, D., Watkins, S. C. and Ford, H. R. (2000). Expression of inducible nitric oxide synthase and interleukin-12 in experimental necrotizing enterocolitis. J. Surg. Res. 92, 71-77.
88. Neal, M. D., Leaphart, C., Levy, R., Prince, J., Billiar, T. R., Watkins, S., Li, J., Cetin, S., Ford, H., Schreiber, A. et al. (2006). Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J. Immunol. 176, 3070-3079.
89. Neisch, A. L., Speck, O., Stronach, B. and Fehon, R. G. (2010). Rho1 regulates apoptosis via activation of the JNK signaling pathway at the plasma membrane. J. Cell Biol. 189, 311-323.
90. Neu, J. and Walker, W. A. (2011). Necrotizing enterocolitis. N. Engl. J. Med. 363, 255-264.
91. Odashima, M., Bamias, G., Rivera-Nieves, J., Linden, J., Nast, C. C., Moskaluk, C. A., Marini, M., Sugawara, K., Kozaiwa, K., Otaka, M. et al. (2005). Activation of A2A adenosine receptor attenuates intestinal inflammation in animal models of inflammatory bowel disease. Gastroenterology 129, 26-33. (Pubitemid 41002039)
92. Ohlstein, B. and Spradling, A. (2006). The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439, 470-474. (Pubitemid 43152837)
93. Onderdonk, A. B. (1985). Experimental models for ulcerative colitis. Dig. Dis. Sci. 30, 40S-44S.
94. Panwala, C. M., Jones, J. C. and Viney, J. L. (1998). A novel model of inflammatory bowel disease: mice deficient for the multiple drug resistance gene, mdr1a, spontaneously develop colitis. J. Immunol. 161, 5733-5744.
95. Park, J.-S., Kim, Y.-S. and Yoo, M.-A. (2009). The role of p38b MAPK in age-related modulation of intestinal stem cell proliferation and differentiation in Drosophila. Aging 1, 637-651.
96. Park, K. T. and Bass, D. (2010). Inflammatory bowel disease-attributable costs and cost-effective strategies in the United States: a review. Inflamm. Bowel Dis. (Epub ahead of print).
97. Park, S. S., Lillehoj, H. S., Allen, P. C., Park, D. W., FitzCoy, S., Bautista, D. A. and Lillehoje, E. P. (2008). Immunopathology and cytokine responses in broiler chickens coinfected with Eimeria maxima and Clostridium perfringens with the use of an animal model of necrotic enteritis. Avian Dis. 52, 14-22. (Pubitemid 351497476)
98. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C. et al. (1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088. (Pubitemid 29001265)
99. Pujol, N., Link, E. M., Liu, L. X., Kurz, C. L., Alloing, G., Tan, M. W., Ray, K. P., Solari, R., Johnson, C. D. and Ewbank, J. J. (2001). A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr. Biol. 11, 809-821.
100. Radulescu, A., Zhang, H. Y., Yu, X., Olson, J. K., Darbyshire, A. K., Chen, Y. and Besner, G. E. (2010). Heparin-binding epidermal growth factor-like growth factor overexpression in transgenic mice increases resistance to necrotizing enterocolitis. J. Pediatr. Surg. 45, 1933-1939.
101. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. and Medzhitov, R. (2004). Recognition of commensal microflora by Toll-Like receptors is required for intestinal homeostasis. Cell 118, 229-241. (Pubitemid 38962578)
102. Reinshagen, M., Patel, A., Sottili, M., Nast, C., Davis, W., Mueller, K. and Eysselein, V. (1994). Protective function of extrinsic sensory neurons in acute rabbit experimental colitis. Gastroenterology 106, 1208-1214. (Pubitemid 24129236)
103. Richardson, W. M., Sodhi, C. P., Russo, A., Siggers, R. H., Afrazi, A., Gribar, S. C., Neal, M. D., Dai, S., Prindle, T. J., Branca, M. et al. (2010). Nucleotide-binding oligomerization Domain-2 inhibits Toll Like Receptor-4 signaling in the intestinal epithelium. Gastroenterology 139, 904-917.
104. Rowlands, B. J., Soong, C. V. and Gardiner, K. R. (1999). The gastrointestinal tract as a barrier in sepsis. Br. Med. Bull. 55, 196-211.
105. Sangild, P. T., Siggers, R. H., Schmidt, M., Elnif, J., Bjornvad, C. R., Thymann, T., Grondahl, M. L., Hansen, A. K., Jensen, S. K. and Boye, M. (2006). Diet- and colonization-dependent intestinal dysfunction predisposes to necrotizing enterocolitis in preterm pigs. Gastroenterology 130, 1776-1792. (Pubitemid 43668865)
106. Schmidt, G. H., Winton, D. J. and Ponder, B. A. (1988). Development of the pattern of cell renewal in the crypt-villus unit of chimaeric mouse small intestine. Development 103, 785-790.
107. Schnabl, K. L., Van Aerde, J. E., Thomson, A. B. and Clandinin, M. T. (2008). Necrotizing enterocolitis: a multifactorial disease with no cure. World J. Gastroenterol. 14, 2142-2161.
108. Schwab, M., Schaeffeler, E., Marx, C., Fromm, M. F., Kaskas, B., Metzler, J., Stange, E., Herfarth, H., Schoelmerich, J., Gregor, M. et al. (2003). Association between the C3435T MDR1 gene polymorphism and susceptibility for ulcerative colitis. Gastroenterology 124, 26-33. (Pubitemid 36055335)
109. Segain, J. P., Raingeard de la Bletiere, D., Sauzeau, V., Bourreille, A., Hilaret, G., Cario-Toumaniantz, C., Pacaud, P., Galmiche, J. P. and Loirand, G. (2003). Rho kinase blockade prevents inflammation via nuclear factor kappa B inhibition: evidence in Crohn's disease and experimental colitis. Gastroenterology 124, 1180-1187. (Pubitemid 36531793)
110. Shibata, Y., Taruishi, M. and Ashida, T. (1993). Experimental ileitis in dogs and colitis in rats with trinitrobenzene sulfonic acid-colonoscopic and histopathologic studies. Gastroenterol. Jpn. 28, 518-527.
111. Shkoda, A., Werner, T., Daniel, H., Gunckel, M., Rogler, G. and Haller, D. (2007). Differential protein expression profile in the intestinal epithelium from patients with inflammatory bowel disease. J. Proteome Res. 6, 1114-1125. (Pubitemid 46480475)
112. Silverman, G. A., Luke, C. J., Bhatia, S. R., Long, O. S., Vetica, A. C., Perlmutter, D. H. and Pak, S. C. (2009). Modeling molecular and cellular aspects of human disease using the nematode Caenorhabditis elegans. Pediatr. Res. 65, 10-18.
113. Sodhi, C., Richardson, W., Gribar, S. C. and Hackam, D. J. (2008). The development of animal models for the study of necrotizing enterocolitis. Dis. Model. Mech. 1, 94-98.
114. Sodhi, C. P., Shi, X. H., Richardson, W. M., Grant, Z. S., Shapiro, R. A., Prindle, T. J., Branca, M., Russo, A., Gribar, S. C., Ma, C. et al. (2010). Toll-like Receptor-4 inhibits enterocyte proliferation via impaired beta-catenin signaling in necrotizing enterocolitis. Gastroenterology 138, 185-196.
115. Stein, L. D., Bao, Z., Blasiar, D., Blumenthal, T., Brent, M. R., Chen, N., Chinwalla, A., Clarke, L., Clee, C., Coghlan, A. et al. (2003). The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol. 1, E45.
116. Steinbrecher, K. A., Harmel-Laws, E., Sitcheran, R. and Baldwin, A. S. (2008). Loss of epithelial RelA results in deregulated intestinal proliferative/apoptotic homeostasis and susceptibility to inflammation. J. Immunol. 180, 2588-2599.
117. Suzuki, A., Hanada, T., Mitsuyama, K., Yoshida, T., Kamizono, S., Hoshino, T., Kubo, M., Yamashita, A., Okabe, M., Takeda, K. et al. (2001). CIS3/SOCS3/SSI3 plays a negative regulatory role in STAT3 activation and intestinal inflammation. J. Exp. Med. 193, 471-481.
118. Takeda, K., Clausen, B. E., Kaisho, T., Tsujimura, T., Terada, N., Forster, I. and Akira, S. (1999). Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10, 39-49. (Pubitemid 29077382)
119. Terhzaz, S., Finlayson, A. J., Stirrat, L., Yang, J., Tricoire, H., Woods, D. J., Dow, J. A. and Davies, S. A. (2010). Cell-specific inositol 1,4,5 trisphosphate 3-kinase mediates epithelial cell apoptosis in response to oxidative stress in Drosophila. Cell. Signal. 22, 737-748.
120. Turner, J. R. (2009). Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809.
121. Uhlig, H. H. and Powrie, F. (2009). Mouse models of intestinal inflammation as tools to understand the pathogenesis of inflammatory bowel disease. Eur J. Immunol. 39, 2021-2026.
122. Ungaro, R., Fukata, M., Hsu, D., Hernandez, Y., Breglio, K., Chen, A., Xu, R., Sotolongo, J., Espana, C., Zaias, J. et al. (2009). A novel Toll-like receptor 4 antagonist antibody ameliorates inflammation but impairs mucosal healing in murine colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G1167-G1179.
123. Van den Brande, J. M., Koehler, T. C., Zelinkova, Z., Bennink, R. J., te Velde, A. A., ten Cate, F. J., van Deventer, S. J., Peppelenbosch, M. P. and Hommes, D. W. (2007). Prediction of antitumour necrosis factor clinical efficacy by real-time visualisation of apoptosis in patients with Crohn's disease. Gut 56, 509-517.
124. Vucelic, B. (2009). Inflammatory bowel diseases: controversies in the use of diagnostic procedures. Dig. Dis. 27, 269-277.
125. Wei, J. and Feng, J. (2010). Signaling pathways associated with inflammatory bowel disease. Recent Pat. Inflamm. Allergy Drug Discov. 4, 105-117.
126. Wirtz, S., Neufert, C., Weigmann, B. and Neurath, M. F. (2007). Chemically induced mouse models of intestinal inflammation. Nature protocols 2, 541-546.
127. Wolfs, T. G., Buurman, W. A., Zoer, B., Moonen, R. M., Derikx, J. P., Thuijls, G., Villamor, E., Gantert, M., Garnier, Y., Zimmermann, L. J. et al. (2009). Endotoxin induced chorioamnionitis prevents intestinal development during gestation in fetal sheep. PLoS ONE 4, e5837.
128. Xavier, R. J. and Podolsky, D. K. (2007). Unravelling the pathogenesis of inflammatory bowel disease. Nature 448, 427-434.
129. Yamamoto, M. T. (2010). Drosophila genetic resource and stock center; The National BioResource Project. Exp. Anim. 59, 125-138.
130. You, Y., Fu, J. J., Meng, J., Huang, G. D. and Liu, Y. H. (2009). Effect of N-acetylcysteine on the murine model of colitis induced by dextran sodium sulfate through up-regulating PON1 activity. Dig. Dis. Sci. 54, 1643-1650.