1932

Abstract

The equine intestinal mucosa is intimately involved in maintaining homeostasis both on a systemic level by controlling extracellular fluid movement and at the local level to maintain barrier function. Horses are particularly susceptible to the clinical syndrome of colic, with the most severe cases involving strangulating obstruction that induces ischemia. Because of the mucosal vascular architecture, the mucosal epithelium is particularly susceptible to ischemic injury. The potential for reperfusion injury has been investigated and found to play a minimal role. However, inflammation does affect mucosal repair. Mechanisms of repair, including villus contraction, epithelial restitution, and tight junction closure, are critical to reforming the mucosal barrier. Nonsteroidal anti-inflammatory drugs have an impact on this repair, particularly at the level of the tight junctions. Completion of mucosal regeneration requires proliferation, which is now being actively studied in equine enteroids. All of these aspects of equine mucosal pathobiology are reviewed in depth.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-030117-014748
2018-02-15
2024-04-17
Loading full text...

Full text loading...

/deliver/fulltext/animal/6/1/annurev-animal-030117-014748.html?itemId=/content/journals/10.1146/annurev-animal-030117-014748&mimeType=html&fmt=ahah

Literature Cited

  1. Argenzio R. 1.  1990. Physiology of digestive, secretory, and absorptive processes. The Equine Acute Abdomen NA White 25–35 Philadelphia: Lea & Febiger, 1st ed.. [Google Scholar]
  2. Janis C. 2.  1976. The evolutionary strategy of the Equidae and the origins of rumen and cecal digestion. Evolution 30:757–74 [Google Scholar]
  3. Clarke LL, Roberts MC, Argenzio RA. 3.  1990. Feeding and digestive problems in horses: physiologic responses to a concentrated meal. Vet. Clin. N. Am. Equine Pract. 6:433–50 [Google Scholar]
  4. Krunkosky TM, Jarrett CL, Moore JN. 4.  2017. Gross and microscopic anatomy of the equine gastrointestinal tract. The Equine Acute Abdomen AT Blikslager, NA White, JN Moore, TS Mair 3–18 Hoboken, NJ: Wiley-Blackwell, 3rd ed.. [Google Scholar]
  5. Dabareiner RM, White NA. 5.  1995. Large colon impaction in horses: 147 cases (1985–1991). J. Am. Vet. Med. Assoc. 206:679–85 [Google Scholar]
  6. Ragle CA, Meagher DM, Lacroix CA, Honnas CM. 6.  1989. Surgical treatment of sand colic: results in 40 horses. Vet. Surg. 18:48–51 [Google Scholar]
  7. Hassel DM, Schiffman PS, Snyder JR. 7.  2001. Petrographic and geochemic evaluation of equine enteroliths. Am. J. Vet. Res. 62:350–58 [Google Scholar]
  8. Clarke LL, Argenzio RA. 8.  1990. NaCl transport across equine proximal colon and the effect of endogenous prostanoids. Am. J. Physiol. 259:G62–69 [Google Scholar]
  9. Clarke LL, Argenzio RA, Roberts MC. 9.  1990. Effect of meal feeding on plasma volume and urinary electrolyte clearance in ponies. Am. J. Vet. Res. 51:571–76 [Google Scholar]
  10. Clarke LL, Ganjam VK, Fichtenbaum B, Hatfield D, Garner HE. 10.  1988. Effect of feeding on renin-angiotensin-aldosterone system of the horse. Am. J. Physiol. 254:R524–530 [Google Scholar]
  11. Clarke LL, Roberts MC, Grubb BR, Argenzio RA. 11.  1992. Short-term effect of aldosterone on Na-Cl transport across equine colon. Am. J. Physiol. 262:R939–46 [Google Scholar]
  12. Hackett ES, Embertson RM, Hopper SA, Woodie JB, Ruggles AJ. 12.  2015. Duration of disease influences survival to discharge of Thoroughbred mares with surgically treated large colon volvulus. Equine Vet. J. 47:650–54 [Google Scholar]
  13. Suthers JM, Pinchbeck GL, Proudman CJ, Archer DC. 13.  2013. Risk factors for large colon volvulus in the UK. Equine Vet. J. 45:558–63 [Google Scholar]
  14. Weese JS, Holcombe SJ, Embertson RM, Kurtz KA, Roessner HA. 14.  et al. 2014. Changes in the faecal microbiota of mares precede the development of post partum colic. Equine Vet. J. 47:641–49 [Google Scholar]
  15. Schoster A, Arroyo LG, Staempfli HR, Weese JS. 15.  2013. Comparison of microbial populations in the small intestine, large intestine and feces of healthy horses using terminal restriction fragment length polymorphism. BMC Res. Notes 6:91 [Google Scholar]
  16. Daly K, Proudman CJ, Duncan SH, Flint HJ, Dyer J, Shirazi-Beechey SP. 16.  2012. Alterations in microbiota and fermentation products in equine large intestine in response to dietary variation and intestinal disease. Br. J. Nutr. 107:989–95 [Google Scholar]
  17. Zhang K, Hornef MW, Dupont A. 17.  2015. The intestinal epithelium as guardian of gut barrier integrity. Cell. Microbiol. 17:1561–69 [Google Scholar]
  18. Kararli TT. 18.  1995. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm. Drug Dispos. 16:351–80 [Google Scholar]
  19. Gonzalez LM, Kinnin LA, Blikslager AT. 19.  2015. Characterization of discrete equine intestinal epithelial cell lineages. Am. J. Vet. Res. 76:358–66 [Google Scholar]
  20. Cheng H, Leblond CP. 20.  1974. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian theory of the origin of the four epithelial cell types. Am. J. Anat. 141:537–61 [Google Scholar]
  21. Barker N, Van Es JH, Kuipers J, Kujala P, van den Born M. 21.  et al. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. . Nature 449:1003–7 [Google Scholar]
  22. Yan KS, Chia LA, Li X, Ootani A, Su J. 22.  et al. 2012. The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. PNAS 109:466–71 [Google Scholar]
  23. Clevers HC, Bevins CL. 23.  2013. Paneth cells: maestros of the small intestinal crypts. Annu. Rev. Physiol. 75:289–311 [Google Scholar]
  24. Sankaran-Walters S, Hart R, Dills C. 24.  2017. Guardians of the gut: enteric defensins. Front. Microbiol. 8:647 [Google Scholar]
  25. Markel TA, Crisostomo PR, Lahm T, Novotny NM, Rescorla FJ. 25.  et al. 2008. Stem cells as a potential future treatment of pediatric intestinal disorders. J. Pediatr. Surg. 43:1953–63 [Google Scholar]
  26. Lin SA, Barker N. 26.  2011. Gastrointestinal stem cells in self-renewal and cancer. J. Gastroenterol. 46:1039–55 [Google Scholar]
  27. Smith L, Gonzalez LM, Blikslager AT. 27.  2013. Impact of ischemia on components of the equine stem cell niche as determined by immunofluorescence. Vet. Surg. 42:E108 [Google Scholar]
  28. Gerring Z, Pearson JF, Morrin HR, Robinson BA, Harris GC, Walker LC. 28.  2015. Phosphohistone H3 outperforms Ki67 as a marker of outcome for breast cancer patients. Histopathology 67:538–47 [Google Scholar]
  29. Traub-Dargatz JL, Kopral CA, Seitzinger AH, Garber LP, Forde K, White NA. 29.  2001. Estimate of the national incidence of and operation-level risk factors for colic among horses in the United States, spring 1998 to spring 1999. J. Am. Vet. Med. Assoc. 219:67–71 [Google Scholar]
  30. Proudman CJ. 30.  1992. A two year, prospective survey of equine colic in general practice. Equine Vet. J. 24:90–93 [Google Scholar]
  31. Proudman CJ, Smith JE, Edwards GB, French NP. 31.  2002. Long-term survival of equine surgical colic cases. Part 2: modelling postoperative survival. Equine Vet. J. 34:438–43 [Google Scholar]
  32. Proudman CJ, Smith JE, Edwards GB, French NP. 32.  2002. Long-term survival of equine surgical colic cases. Part 1: patterns of mortality and morbidity. Equine Vet. J. 34:432–37 [Google Scholar]
  33. Allen D Jr., White NA 2nd, Tyler DE. 33.  1988. Morphologic effects of experimental distention of equine small intestine. Vet. Surg. 17:10–14 [Google Scholar]
  34. Dabareiner RM, Sullins KE, Snyder JR, White NA 2nd, Gardner IA. 34.  1993. Evaluation of the microcirculation of the equine small intestine after intraluminal distention and subsequent decompression. Am. J. Vet. Res. 54:1673–82 [Google Scholar]
  35. White NA 2nd. 35.  1981. Intestinal infarction associated with mesenteric vascular thrombotic disease in the horse. J. Am. Vet. Med. Assoc. 178:259–62 [Google Scholar]
  36. Gerard MP, Blikslager AT, Roberts MC, Tate LP Jr., Argenzio RA. 36.  1999. The characteristics of intestinal injury peripheral to strangulating obstruction lesions in the equine small intestine. Equine Vet. J. 31:331–35 [Google Scholar]
  37. Meschter CL, Tyler DE, White NA, Moore J. 37.  1986. Histologic findings in the gastrointestinal tract of horses with colic. Am. J. Vet. Res. 47:598–606 [Google Scholar]
  38. Moore RM, Hardy J, Muir WW. 38.  1995. Mural blood flow distribution in the large colon of horses during low-flow ischemia and reperfusion. Am. J. Vet. Res. 56:812–18 [Google Scholar]
  39. Dabareiner RM, Snyder JR, White NA, Pascoe JR, Harmon FA. 39.  et al. 1995. Microvascular permeability and endothelial cell morphology associated with low-flow ischemia/reperfusion injury in the equine jejunum. Am. J. Vet. Res. 56:639–48 [Google Scholar]
  40. Hilton H, Nieto JE, Moore PF, Harmon FA, Naydan DK, Snyder JR. 40.  2011. Expression of cyclooxygenase genes in the jejunum of horses during low-flow ischemia and reperfusion. Am. J. Vet. Res. 72:681–86 [Google Scholar]
  41. Reeves MJ, Vansteenhouse J, Stashak TS, Yovich JV, Cockerell G. 41.  1990. Failure to demonstrate reperfusion injury following ischaemia of the equine large colon using dimethyl sulphoxide. Equine Vet. J. 22:126–32 [Google Scholar]
  42. Snyder JR, Olander HJ, Pascoe JR, Holland M, Kurpershoek CJ. 42.  1988. Morphologic alterations observed during experimental ischemia of the equine large colon. Am. J. Vet. Res. 49:801–9 [Google Scholar]
  43. Snyder JR, Pascoe JR, Olander HJ, Hinds DM, Young R, Tyler WS. 43.  1990. Vascular injury associated with naturally occurring strangulating obstructions of the equine large colon. Vet. Surg. 19:446–55 [Google Scholar]
  44. Gonzalez LM, Fogle CA, Baker WT, Hughes FE, Law JM. 44.  et al. 2015. Operative factors associated with short-term outcome in horses with large colon volvulus: 47 cases from 2006 to 2013. Equine Vet. J. 47:279–84 [Google Scholar]
  45. Laws EG, Freeman DE. 45.  1995. Significance of reperfusion injury after venous strangulation obstruction of equine jejunum. J. Investig. Surg. 8:263–70 [Google Scholar]
  46. Blikslager AT, Roberts MC, Rhoads JM, Argenzio RA. 46.  1997. Is reperfusion injury an important cause of mucosal damage after porcine intestinal ischemia?. Surgery 121:526–34 [Google Scholar]
  47. Van Hoogmoed L, Snyder JR, Pascoe JR, Olander H. 47.  2000. Use of pelvic flexure biopsies to predict survival after large colon torsion in horses. Vet. Surg. 29:572–77 [Google Scholar]
  48. Freeman DE, Schaeffer DJ, Cleary OB. 48.  2014. Long-term survival in horses with strangulating obstruction of the small intestine managed without resection. Equine Vet. J. 46:711–17 [Google Scholar]
  49. McAnulty JF, Stone WC, Darien BJ. 49.  1997. The effects of ischemia and reperfusion on mucosal respiratory function, adenosine triphosphate, electrolyte, and water content in the ascending colon of ponies. Vet. Surg. 26:172–81 [Google Scholar]
  50. Gonzalez LM, Moeser AJ, Blikslager AT. 50.  2015. Animal models of ischemia-reperfusion-induced intestinal injury: progress and promise for translational research. Am. J. Physiol. Gastrointest. Liver Physiol. 308:G63–G75 [Google Scholar]
  51. Dart AJ, Snyder JR, Julian D, Hinds DM. 51.  1992. Microvascular circulation of the small intestine in horses. Am. J. Vet. Res. 53:995–1000 [Google Scholar]
  52. Chiu CJ, McArdle AH, Brown R, Scott HJ, Gurd FN. 52.  1970. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch. Surg. 101:478–83 [Google Scholar]
  53. Grosche A, Morton AJ, Graham AS, Sanchez LC, Blikslager AT. 53.  et al. 2011. Ultrastructural changes in the equine colonic mucosa after ischaemia and reperfusion. Equine Vet. J. Suppl. 2011:398–15 [Google Scholar]
  54. Graham AS, Grosche A, Morton AJ, Polyak MM, Freeman DE. 54.  2011. In vitro and in vivo responses of mucosa from the large colon of horses to ischemia and reperfusion. Am. J. Vet. Res. 72:982–89 [Google Scholar]
  55. Grosche A, Morton AJ, Graham AS, Polyak MM, Freeman DE. 55.  2013. Effect of large colon ischemia and reperfusion on concentrations of calprotectin and other clinicopathologic variables in jugular and colonic venous blood in horses. Am. J. Vet. Res. 74:1281–90 [Google Scholar]
  56. Blikslager AT, Moeser AJ, Gookin JL, Jones SL, Odle J. 56.  2007. Restoration of barrier function in injured intestinal mucosa. Physiol. Rev. 87:545–64 [Google Scholar]
  57. Moore RM, Muir WW, Granger DN. 57.  1995. Mechanisms of gastrointestinal ischemia-reperfusion injury and potential therapeutic interventions: a review and its implications in the horse. J. Vet. Intern. Med. 9:115–32 [Google Scholar]
  58. Prichard M, Ducharme NG, Wilkins PA, Erb HN, Butt M. 58.  1991. Xanthine oxidase formation during experimental ischemia of the equine small intestine. Can. J. Vet. Res. 55:310–14 [Google Scholar]
  59. Moore RM, Muir WW, Bertone AL, Oliver JL. 59.  1998. Effect of platelet-activating factor antagonist L-691,880 on low-flow ischemia-reperfusion injury of the large colon in horses. Vet. Surg. 27:37–48 [Google Scholar]
  60. Blikslager AT, Roberts MC, Gerard MP, Argenzio RA. 60.  1997. How important is intestinal reperfusion injury in horses?. J. Am. Vet. Med. Assoc. 211:1387–89 [Google Scholar]
  61. Kubes P, Hunter J, Granger DN. 61.  1992. Ischemia/reperfusion-induced feline intestinal dysfunction: importance of granulocyte recruitment. Gastroenterology 103:807–12 [Google Scholar]
  62. Park PO, Haglund U, Bulkley GB, Falt K. 62.  1990. The sequence of development of intestinal tissue injury after strangulation ischemia and reperfusion. Surgery 107:574–80 [Google Scholar]
  63. Rotting AK, Freeman DE, Constable PD, Eurell JA, Wallig MA. 63.  2008. Mucosal distribution of eosinophilic granulocytes within the gastrointestinal tract of horses. Am. J. Vet. Res. 69:874–79 [Google Scholar]
  64. Rotting AK, Freeman DE, Constable PD, Eurell JA, Wallig MA. 64.  2016. Effects of ischemia and reperfusion on eosinophilic accumulation and distribution in mucosa of equine jejunum and colon. Am. J. Vet. Res. 77:534–39 [Google Scholar]
  65. Grosche A, Freeman DE, Morton AJ, Polyak MM, Matyjaszek SA. 65.  2012. Effects of ischemia and reperfusion on production of nitrotyrosine, activation of eosinophils, and apoptosis in the large colonic mucosa of horses. Am. J. Vet. Res. 73:53–61 [Google Scholar]
  66. Moore R, Carlson S, Madara JL. 66.  1989. Villus contraction aids repair of intestinal epithelium after injury. Am. J. Physiol. 257:G274–83 [Google Scholar]
  67. Gookin JL, Rhoads JM, Argenzio RA. 67.  2002. Inducible nitric oxide synthase mediates early epithelial repair of porcine ileum. Am. J. Physiol. Gastrointest. Liver Physiol. 283:G157–68 [Google Scholar]
  68. Erickson RA, Tarnawski A, Dines G, Stachura J. 68.  1990. 16,16-Dimethyl prostaglandin E2 induces villus contraction in rats without affecting intestinal restitution. Gastroenterology 99:708–16 [Google Scholar]
  69. Cook VL, Jones Shults J, McDowell M, Campbell NB, Davis JL, Blikslager AT. 69.  2008. Attenuation of ischaemic injury in the equine jejunum by administration of systemic lidocaine. Equine Vet. J. 40:353–57 [Google Scholar]
  70. Cook VL, Meyer CT, Campbell NB, Blikslager AT. 70.  2009. Effect of firocoxib or flunixin meglumine on recovery of ischemic-injured equine jejunum. Am. J. Vet. Res. 70:992–1000 [Google Scholar]
  71. Little D, Brown SA, Campbell NB, Moeser AJ, Davis JL, Blikslager AT. 71.  2007. Effects of the cyclooxygenase inhibitor meloxicam on recovery of ischemia-injured equine jejunum. Am. J. Vet. Res. 68:614–24 [Google Scholar]
  72. White NA, Moore JN, Trim CM. 72.  1980. Mucosal alterations in experimentally induced small intestinal strangulation obstruction in ponies. Am. J. Vet. Res. 41:193–98 [Google Scholar]
  73. Moore R, Carlson S, Madara JL. 73.  1989. Rapid barrier restitution in an in vitro model of intestinal epithelial injury. Lab. Investig. 60:237–44 [Google Scholar]
  74. Moore R, Madara JL, MacLeod RJ. 74.  1994. Enterocytes adhere preferentially to collagen IV in a differentially regulated divalent cation-dependent manner. Am. J. Physiol. 266:G1099–107 [Google Scholar]
  75. Moore R, Madri J, Carlson S, Madara JL. 75.  1992. Collagens facilitate epithelial migration in restitution of native guinea pig intestinal epithelium. Gastroenterology 102:119–30 [Google Scholar]
  76. McCormack SA, Viar MJ, Johnson LR. 76.  1992. Migration of IEC-6 cells: a model for mucosal healing. Am. J. Physiol. 263:G426–35 [Google Scholar]
  77. Blikslager AT, Roberts MC. 77.  1997. Mechanisms of intestinal mucosal repair. J. Am. Vet. Med. Assoc. 211:1437–41 [Google Scholar]
  78. Podolsky DK. 78.  1999. Mucosal immunity and inflammation. V. Innate mechanisms of mucosal defense and repair: The best offense is a good defense. Am. J. Physiol. 277:G495–99 [Google Scholar]
  79. Wang JY, Johnson LR. 79.  1992. Role of transglutaminase and protein cross-linking in the repair of mucosal stress erosions. Am. J. Physiol. 262:G818–25 [Google Scholar]
  80. Moeser AJ, Haskell MM, Shifflett DE, Little D, Schultz BD, Blikslager AT. 80.  2004. ClC-2 chloride secretion mediates prostaglandin-induced recovery of barrier function in ischemia-injured porcine ileum. Gastroenterology 127:802–15 [Google Scholar]
  81. Nighot PK, Blikslager AT. 81.  2012. Chloride channel ClC-2 modulates tight junction barrier function via intracellular trafficking of occludin. Am. J. Physiol. Cell Physiol. 302:C178–87 [Google Scholar]
  82. Tomlinson J, Blikslager A. 82.  2003. Role of nonsteroidal anti-inflammatory drugs in gastrointestinal tract injury and repair. J. Am. Vet. Med. Assoc. 222:946–51 [Google Scholar]
  83. Morton AJ, Grosche A, Matyjaszek SA, Polyak MM, Freeman DE. 83.  2011. Effects of flunixin meglumine on the recovery of ischaemic equine colonic mucosa in vitro. Equine Vet. J. Suppl. 2011:39112–16 [Google Scholar]
  84. Nighot PK, Leung L, Ma TY. 84.  2017. Chloride channel ClC-2 enhances intestinal epithelial tight junction barrier function via regulation of caveolin-1 and caveolar trafficking of occludin. Exp. Cell Res. 352:113–22 [Google Scholar]
  85. Grisham MB, Hernandez LA, Granger DN. 85.  1986. Xanthine oxidase and neutrophil infiltration in intestinal ischemia. Am. J. Physiol. 251:G567–74 [Google Scholar]
  86. Krieglstein CF, Cerwinka WH, Laroux FS, Salter JW, Russell JM. 86.  et al. 2001. Regulation of murine intestinal inflammation by reactive metabolites of oxygen and nitrogen: divergent roles of superoxide and nitric oxide. J. Exp. Med. 194:1207–18 [Google Scholar]
  87. Kurtel H, Fujimoto K, Zimmerman BJ, Granger DN, Tso P. 87.  1991. Ischemia-reperfusion-induced mucosal dysfunction: role of neutrophils. Am. J. Physiol. 261:G490–96 [Google Scholar]
  88. Gayle J, Jones SL, Argenzio RA, Blikslager AT. 88.  2002. Neutrophils increase paracellular permeability of restituted ischemic-injured porcine ileum. Surgery 132:461–70 [Google Scholar]
  89. Tomlinson JE, Wilder BO, Young KM, Blikslager AT. 89.  2004. Effects of flunixin meglumine or etodolac treatment on mucosal recovery of equine jejunum after ischemia. Am. J. Vet. Res. 65:761–69 [Google Scholar]
  90. Cook VL, Jones Shults J, McDowell MR, Campbell NB, Davis JL. 90.  et al. 2009. Anti-inflammatory effects of intravenously administered lidocaine hydrochloride on ischemia-injured jejunum in horses. Am. J. Vet. Res. 70:1259–68 [Google Scholar]
  91. Blikslager AT. 91.  1999. Do we need cyclooxygenase-2 inhibitors in equine practice?. Comp. Contin. Educ. Pract. Vet. 21:548–50 [Google Scholar]
  92. Marshall JF, Bhatnagar AS, Bowman SG, Howard CM, Morris NN. 92.  et al. 2011. Evaluation of the cyclooxygenase selectivity of robenacoxib and its effect on recovery of ischemia-injured jejunal mucosa in horses. Am. J. Vet. Res. 72:226–32 [Google Scholar]
  93. Tomlinson JE, Blikslager AT. 93.  2004. Effects of ischemia and the cyclooxygenase inhibitor flunixin on in vitro passage of lipopolysaccharide across equine jejunum. Am. J. Vet. Res. 65:1377–83 [Google Scholar]
  94. Tomlinson JE, Blikslager AT. 94.  2005. Effects of cyclooxygenase inhibitors flunixin and deracoxib on permeability of ischaemic-injured equine jejunum. Equine Vet. J. 37:75–80 [Google Scholar]
  95. Marshall JF, Blikslager AT. 95.  2011. The effect of nonsteroidal anti-inflammatory drugs on the equine intestine. Equine Vet. J. Suppl. 43:39140–44 [Google Scholar]
  96. Fogle J, Jacob M, Blikslager A, Edwards A, Wagner B. 96.  et al. 2016. Comparison of lipopolysaccharides and soluble CD14 measurement between clinically endotoxaemic and nonendotoxaemic horses. Equine Vet. J. 49:155–59 [Google Scholar]
  97. Cook VL, Neuder LE, Blikslager AT, Jones SL. 97.  2009. The effect of lidocaine on in vitro adhesion and migration of equine neutrophils. Vet. Immunol. Immunopathol. 129:137–42 [Google Scholar]
  98. Cook VL, Blikslager AT. 98.  2008. Use of systemically administered lidocaine in horses with gastrointestinal tract disease. J. Am. Vet. Med. Assoc. 232:1144–48 [Google Scholar]
  99. Blikslager AT, Rhoads JM, Bristol DG, Roberts MC, Argenzio RA. 99.  1999. Glutamine and transforming growth factor-alpha stimulate extracellular regulated kinases and enhance recovery of villous surface area in porcine ischemic-injured intestine. Surgery 125:186–94 [Google Scholar]
  100. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N. 100.  et al. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:262–65 [Google Scholar]
  101. Gonzalez LM, Williamson I, Piedrahita JA, Blikslager AT, Magness ST. 101.  2013. Cell lineage identification and stem cell culture in a porcine model for the study of intestinal epithelial regeneration. PLOS ONE 8:e66465 [Google Scholar]
  102. Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH. 102.  et al. 2011. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141:1762–72 [Google Scholar]
  103. Jacobs C, Southwood L, Lindborg S. 103.  2014. Development of an in-vitro three-dimensional culture system for equine gastrointestinal crypts Presented at 11th Equine Colic Res. Symp. Dublin, Irel.:
  104. Kretzschmar K, Clevers H. 104.  2016. Organoids: modeling development and the stem cell niche in a dish. Dev. Cell 38:590–600 [Google Scholar]
  105. Yui S, Nakamura T, Sato T, Nemoto Y, Mizutani T. 105.  et al. 2012. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell. Nat. Med. 18:618–23 [Google Scholar]
  106. Powell RH, Behnke MS. 106.  2017. WRN conditioned media is sufficient for in vitro propagation of intestinal organoids from large farm and small companion animals. Biol. Open 6:698–705 [Google Scholar]
/content/journals/10.1146/annurev-animal-030117-014748
Loading
/content/journals/10.1146/annurev-animal-030117-014748
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error