Large Animal Models: The Key to Translational Discovery in Digestive Disease Research

Amanda Ziegler1, Liara Gonzalez1, Anthony Blikslager1
1Center for Gastrointestinal Biology and Disease, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina

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Peery, 2012, Burden of gastrointestinal disease in the United States: 2012 update, Gastroenterology, 143, 1179, 10.1053/j.gastro.2012.08.002 Low, 2012, Mouse models in gastroenterology research, Gastroenterology, 143, 1410, 10.1053/j.gastro.2012.10.011 Chung, 1997, Mouse models for human diseases, Hong Kong Med J, 3, 201 Wagner, 2013, Semisynthetic diet ameliorates Crohn's disease-like ileitis in TNFDeltaARE/WT mice through antigen-independent mechanisms of gluten, Inflamm Bowel Dis, 19, 1285, 10.1097/MIB.0b013e318281f573 Pizarro, 2011, SAMP1/YitFc mouse strain: a spontaneous model of Crohn's disease-like ileitis, Inflamm Bowel Dis, 17, 2566, 10.1002/ibd.21638 Boivin, 2003, Pathology of mouse models of intestinal cancer: consensus report and recommendations, Gastroenterology, 124, 762, 10.1053/gast.2003.50094 Flisikowska, 2012, A porcine model of familial adenomatous polyposis, Gastroenterology, 143, 1173, 10.1053/j.gastro.2012.07.110 US Department of Health and Human Services. Opportunities and Challenges in Digestive Diseases Research: Recommendations of the National Commission on Digestive Diseases. March 2009; NIH Publication No. 08-6514. Cibelli, 2013, Strategies for improving animal models for regenerative medicine, Cell Stem Cell, 12, 271, 10.1016/j.stem.2013.01.004 Patterson, 2008, The pig as an experimental model for elucidating the mechanisms governing dietary influence on mineral absorption, Exp Biol Med (Maywood), 233, 651, 10.3181/0709-MR-262 Kararli, 1995, Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals, Biopharm Drug Dispos, 16, 351, 10.1002/bdd.2510160502 Kirk, 2003, Crossing the bridge: large animal models in translational transplantation research, Immunol Rev, 196, 176, 10.1046/j.1600-065X.2003.00081.x Block, 2011, Altered mRNA expression due to acute mesenteric ischaemia in a porcine model, Eur J Vasc Endovasc Surg, 41, 281, 10.1016/j.ejvs.2010.09.012 Yandza, 2012, The pig as a preclinical model for intestinal ischemia-reperfusion and transplantation studies, J Surg Res, 178, 807, 10.1016/j.jss.2012.07.025 Elfenbein, 2013, Novel determinants of intestinal colonization of Salmonella enterica serotype typhimurium identified in bovine enteric infection, Infect Immun, 81, 4311, 10.1128/IAI.00874-13 Swindle, 2012, Swine as models in biomedical research and toxicology testing, Vet Pathol, 49, 344, 10.1177/0300985811402846 Roura, 2016, Critical review evaluating the pig as a model for human nutritional physiology, Nutr Res Rev, 29, 60, 10.1017/S0954422416000020 Rothkotter, 2002, The pig as a model of developmental immunology, Hum Exp Toxicol, 21, 533, 10.1191/0960327102ht293oa Bendixen, 2010, Advances in porcine genomics and proteomics–a toolbox for developing the pig as a model organism for molecular biomedical research, Brief Funct Genomics, 9, 208, 10.1093/bfgp/elq004 Lunney, 2007, Advances in swine biomedical model genomics, Int J Biol Sci, 3, 179, 10.7150/ijbs.3.179 Hart, 2007, Lessons learned from the initial sequencing of the pig genome: comparative analysis of an 8 Mb region of pig chromosome 17, Genome Biol, 8, R168, 10.1186/gb-2007-8-8-r168 Ibrahim, 2006, Selected physiologic compatibilities and incompatibilities between human and porcine organ systems, Xenotransplantation, 13, 488, 10.1111/j.1399-3089.2006.00346.x Gonzalez, 2015, Porcine models of digestive disease: the future of large animal translational research, Transl Res, 166, 12, 10.1016/j.trsl.2015.01.004 Garman, 2012, Review: experimental models for Barrett's esophagus and esophageal adenocarcinoma, Am J Physiol Gastrointest Liver Physiol, 302, G1231, 10.1152/ajpgi.00509.2011 Ranjay Chakraborty, 2014, Contribution of body length on axial length during normal eye development in C57BL/6J and 129S1/SvJ wild-type mouse strains, Invest Ophthalmol Vis Sci, 55, 3614 Casteleyn, 2010, Surface area assessment of the murine intestinal tract as a prerequisite for oral dose translation from mouse to man, Lab Anim, 44, 176, 10.1258/la.2009.009112 Gonzalez, 2013, Cell lineage identification and stem cell culture in a porcine model for the study of intestinal epithelial regeneration, PLoS One, 8, e66465, 10.1371/journal.pone.0066465 Chen, 2003, Changes of microvascular architecture, ultrastructure and permeability of rat jejunal villi at different ages, World J Gastroenterol, 9, 795, 10.3748/wjg.v9.i4.795 Barker, 2012, Identifying the stem cell of the intestinal crypt: strategies and pitfalls, Cell Stem Cell, 11, 452, 10.1016/j.stem.2012.09.009 Graham, 1987, The pig as a model in dietary fibre digestion studies, Scand J Gastroenterol Suppl, 129, 55, 10.3109/00365528709095851 Nguyen, 2015, How informative is the mouse for human gut microbiota research?, Dis Model Mech, 8, 1, 10.1242/dmm.017400 Miller, 1987, The pig as a model for human nutrition, Annu Rev Nutr, 7, 361, 10.1146/annurev.nu.07.070187.002045 Pang, 2007, Inter-species transplantation of gut microbiota from human to pigs, ISME J, 1, 156, 10.1038/ismej.2007.23 Ley, 2005, Obesity alters gut microbial ecology, Proc Natl Acad Sci U S A, 102, 11070, 10.1073/pnas.0504978102 Abdulnour-Nakhoul, 2007, Characterization of esophageal submucosal glands in pig tissue and cultures, Dig Dis Sci, 52, 3054, 10.1007/s10620-006-9739-3 Long, 1999, Esophageal submucosal glands: structure and function, Am J Gastroenterol, 94, 2818, 10.1111/j.1572-0241.1999.1422_b.x Kawaura, 2001, Immunohistochemical study of p53, c-erbB-2, and PCNA in Barrett's esophagus with dysplasia and adenocarcinoma arising from experimental acid or alkaline reflux model, J Gastroenterol, 36, 595, 10.1007/s005350170042 Kapoor, 2015, Animal models of Barrett's esophagus and esophageal adenocarcinoma-past, present, and future, Clin Transl Sci, 8, 841, 10.1111/cts.12304 Tian, 2010, Characterization of a necrotizing enterocolitis model in newborn mice, Int J Clin Exp Med, 3, 293 Azcarate-Peril, 2011, Acute necrotizing enterocolitis of preterm piglets is characterized by dysbiosis of ileal mucosa-associated bacteria, Gut Microbes, 2, 234, 10.4161/gmic.2.4.16332 Sangild, 2006, Diet- and colonization-dependent intestinal dysfunction predisposes to necrotizing enterocolitis in preterm pigs, Gastroenterology, 130, 1776, 10.1053/j.gastro.2006.02.026 Weixiong, 1994, Quantification of tissue damage in the feline small intestine during ischaemia-reperfusion: the importance of free radicals, Acta Physiol Scand, 150, 241, 10.1111/j.1748-1716.1994.tb09683.x Granger, 1986, Xanthine oxidase inhibitors attenuate ischemia-induced vascular permeability changes in the cat intestine, Gastroenterology, 90, 80, 10.1016/0016-5085(86)90078-8 Cook, 2008, Attenuation of ischaemic injury in the equine jejunum by administration of systemic lidocaine, Equine Vet J, 40, 353, 10.2746/042516408X293574 Filez, 1990, Influences of ischemia and reperfusion on the feline small-intestinal mucosa, J Surg Res, 49, 157, 10.1016/0022-4804(90)90255-Z Arakawa, 2005, Bradykinin B2 receptor antagonist FR173657 ameliorates small bowel ischemia-reperfusion injury in dogs, Dig Dis Sci, 50, 27, 10.1007/s10620-005-1273-1 Moeser, 2007, Recovery of mucosal barrier function in ischemic porcine ileum and colon is stimulated by a novel agonist of the ClC-2 chloride channel, lubiprostone, Am J Physiol Gastrointest Liver Physiol, 292, G647, 10.1152/ajpgi.00183.2006 Gonzalez, 2015, Animal models of ischemia-reperfusion-induced intestinal injury: progress and promise for translational research, Am J Physiol Gastrointest Liver Physiol, 308, G63, 10.1152/ajpgi.00112.2013 Blikslager, 1997, Is reperfusion injury an important cause of mucosal damage after porcine intestinal ischemia?, Surgery, 121, 526, 10.1016/S0039-6060(97)90107-0 Blikslager, 2007, Restoration of barrier function in injured intestinal mucosa, Physiol Rev, 87, 545, 10.1152/physrev.00012.2006 Moore, 1989, Rapid barrier restitution in an in vitro model of intestinal epithelial injury, Lab Invest, 60, 237 Moeser, 2008, Mice lacking the Na+/H+ exchanger 2 have impaired recovery of intestinal barrier function, Am J Physiol Gastrointest Liver Physiol, 295, G791, 10.1152/ajpgi.00538.2007 Nighot, 2012, Chloride channel ClC-2 modulates tight junction barrier function via intracellular trafficking of occludin, Am J Physiol Cell Physiol, 302, C178, 10.1152/ajpcell.00072.2011 Blikslager, 1999, Glutamine and transforming growth factor-alpha stimulate extracellular regulated kinases and enhance recovery of villous surface area in porcine ischemic-injured intestine, Surgery, 125, 186, 10.1016/S0039-6060(99)70264-3 Ahdieh, 1998, L-glutamine and transforming growth factor-alpha enhance recovery of monoacylglycerol acyltransferase and diacylglycerol acyltransferase activity in porcine postischemic ileum, Pediatr Res, 43, 227, 10.1203/00006450-199802000-00012 Moore, 1989, Villus contraction aids repair of intestinal epithelium after injury, Am J Physiol, 257, G274 Joyce, 1987, Morphologic and biochemical evidence for a contractile cell network within the rat intestinal mucosa, Gastroenterology, 92, 68, 10.1016/0016-5085(87)90841-9 Gookin, 2002, Inducible nitric oxide synthase mediates early epithelial repair of porcine ileum, Am J Physiol Gastrointest Liver Physiol, 283, G157, 10.1152/ajpgi.00005.2001 Dignass, 1994, Trefoil peptides promote epithelial migration through a transforming growth factor beta-independent pathway, J Clin Invest, 94, 376, 10.1172/JCI117332 Albers, 1995, Fate of polarized membrane components and evidence for microvillus disassembly on migrating enterocytes during repair of native intestinal epithelium, Lab Invest, 73, 139 Blikslager, 1999, Prostaglandin-induced recovery of barrier function in porcine ileum is triggered by chloride secretion, Am J Physiol, 276, G28 Little, 2003, PI3K signaling is required for prostaglandin-induced mucosal recovery in ischemia-injured porcine ileum, Am J Physiol Gastrointest Liver Physiol, 284, G46, 10.1152/ajpgi.00121.2002 Gayle, 2002, Neutrophils increase paracellular permeability of restituted ischemic-injured porcine ileum, Surgery, 132, 461, 10.1067/msy.2002.125320 Kubes, 1992, Ischemia/reperfusion-induced feline intestinal dysfunction: importance of granulocyte recruitment, Gastroenterology, 103, 807, 10.1016/0016-5085(92)90010-V Mallick, 2004, Ischemia-reperfusion injury of the intestine and protective strategies against injury, Dig Dis Sci, 49, 1359, 10.1023/B:DDAS.0000042232.98927.91 Pucilowska, 2000, Fibrogenesis. IV. Fibrosis and inflammatory bowel disease: cellular mediators and animal models, Am J Physiol Gastrointest Liver Physiol, 279, G653, 10.1152/ajpgi.2000.279.4.G653 Sala, 2009, Tissue-engineered small intestine and stomach from autologous tissue in a preclinical large animal model, J Surg Res, 156, 205, 10.1016/j.jss.2009.03.062 Khalil, 2016, A novel culture system for adult porcine intestinal crypts, Cell Tissue Res, 365, 123, 10.1007/s00441-016-2367-0 Silke, 2013, Improved cell line IPEC-J2, characterized as a model for porcine jejunal epithelium, PLoS One, 8, e79643, 10.1371/journal.pone.0079643 Nossol, 2015, Comparing two intestinal porcine epithelial cell lines (IPECs): morphological differentiation, function and metabolism, PLoS One, 10, e0132323, 10.1371/journal.pone.0132323 Brosnahan, 2012, Porcine IPEC-J2 intestinal epithelial cells in microbiological investigations, Vet Microbiol, 156, 229, 10.1016/j.vetmic.2011.10.017 Saaby, 2016, IPEC-J2 MDR1, a novel high-resistance cell line with functional expression of human P-glycoprotein (ABCB1) for drug screening studies, Mol Pharm, 13, 640, 10.1021/acs.molpharmaceut.5b00874 Rogers, 2008, Production of CFTR-null and CFTR-DeltaF508 heterozygous pigs by adeno-associated virus-mediated gene targeting and somatic cell nuclear transfer, J Clin Invest, 118, 1571, 10.1172/JCI34773 Keiser, 2011, New animal models of cystic fibrosis: what are they teaching us?, Curr Opin Pulm Med, 17, 478, 10.1097/MCP.0b013e32834b14c9 Smith, 2010, Early weaning stress impairs development of mucosal barrier function in the porcine intestine, Am J Physiol Gastrointest Liver Physiol, 298, G352, 10.1152/ajpgi.00081.2009 Moeser, 2007, Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs, Am J Physiol Gastrointest Liver Physiol, 293, G413, 10.1152/ajpgi.00304.2006 Moeser, 2007, Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig, Am J Physiol Gastrointest Liver Physiol, 292, G173, 10.1152/ajpgi.00197.2006 Overman, 2012, CRF induces intestinal epithelial barrier injury via the release of mast cell proteases and TNF-alpha, PLoS One, 7, e39935, 10.1371/journal.pone.0039935 Schreiber, 2005, Adrenocorticotrophic hormone modulates Escherichia coli O157:H7 adherence to porcine colonic mucosa, Stress, 8, 185, 10.1080/10253890500188732 Chen, 2006, Mucosally-directed adrenergic nerves and sympathomimetic drugs enhance non-intimate adherence of Escherichia coli O157:H7 to porcine cecum and colon, Eur J Pharmacol, 539, 116, 10.1016/j.ejphar.2006.03.081 Schmidt, 2007, Autonomic neurotransmitters modulate immunoglobulin A secretion in porcine colonic mucosa, J Neuroimmunol, 185, 20, 10.1016/j.jneuroim.2006.10.028 Tang, 2010, Acute mesenteric ischemia induced by ligation of porcine superior mesenteric vein: multidetector CT evaluations, Acad Radiol, 17, 1146, 10.1016/j.acra.2010.04.014 Bruhn, 2013, Early detection of acute mesenteric ischemia using diffusion-weighted 3.0-T magnetic resonance imaging in a porcine model, Invest Radiol, 48, 231, 10.1097/RLI.0b013e3182809143 Klein, 1996, CT and MRI of experimentally induced mesenteric ischemia in a porcine model, J Comput Assist Tomogr, 20, 254, 10.1097/00004728-199603000-00016 Jacobi, 2012, Dietary long-chain PUFA enhance acute repair of ischemia-injured intestine of suckling pigs, J Nutr, 142, 1266 Acosta, 2007, L-lactate after embolization of the superior mesenteric artery, J Surg Res, 143, 320, 10.1016/j.jss.2007.02.003 Gookin, 2003, PG-mediated closure of paracellular pathway and not restitution is the primary determinant of barrier recovery in acutely injured porcine ileum, Am J Physiol Gastrointest Liver Physiol, 285, G967, 10.1152/ajpgi.00532.2002 Thymann, 2009, Carbohydrate maldigestion induces necrotizing enterocolitis in preterm pigs, Am J Physiol Gastrointest Liver Physiol, 297, G1115, 10.1152/ajpgi.00261.2009 Van Haver, 2009, Diet-dependent mucosal colonization and interleukin-1beta responses in preterm pigs susceptible to necrotizing enterocolitis, J Pediatr Gastroenterol Nutr, 49, 90, 10.1097/MPG.0b013e31818de393 Siggers, 2008, Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs, J Nutr, 138, 1437 Sangild, 2002, Preterm birth affects the intestinal response to parenteral and enteral nutrition in newborn pigs, J Nutr, 132, 3786 Pereira-Fantini, 2011, Short- and long-term effects of small bowel resection: a unique histological study in a piglet model of short bowel syndrome, Histochem Cell Biol, 135, 195, 10.1007/s00418-011-0778-2 Vegge, 2013, Glucagon-like peptide-2 induces rapid digestive adaptation following intestinal resection in preterm neonates, Am J Physiol Gastrointest Liver Physiol, 305, G277, 10.1152/ajpgi.00064.2013 Aigner, 2010, Transgenic pigs as models for translational biomedical research, J Mol Med (Berl), 88, 653, 10.1007/s00109-010-0610-9 Fan, 2013, Genetically modified pig models for human diseases, J Genet Genomics, 40, 67, 10.1016/j.jgg.2012.07.014 Whyte, 2011, Genetic modifications of pigs for medicine and agriculture, Mol Reprod Dev, 78, 879, 10.1002/mrd.21333 Fisher, 2011, Comparative biology of cystic fibrosis animal models, Methods Mol Biol, 742, 311, 10.1007/978-1-61779-120-8_19 Grussner, 1993, Streptozotocin-induced diabetes mellitus in pigs, Horm Metab Res, 25, 199, 10.1055/s-2007-1002076 Barb, 1992, Growth hormone secretion, serum, and cerebral spinal fluid insulin and insulin-like growth factor-I concentrations in pigs with streptozotocin-induced diabetes mellitus, Proc Soc Exp Biol Med, 201, 223, 10.3181/00379727-201-43503