Adult zebrafish intestine resection: A novel model of short bowel syndrome, adaptation, and intestinal stem cell regeneration

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 309, Issue 3, 2015, Pages G135-G145

  Schall, K A ^a   Holoyda, K A ^a   Grant, C N ^a   Levin, D E ^a   Torres, E R ^a   Maxwell, A ^a   Pollack, H A ^a   Moats, R A ^a   Frey, M R ^a   Darehzereshki, A ^a   Al Alam, D ^a   Lien, C ^a   Grikscheit, T C ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Adaptation; Egf receptor; Igf; Intestinal failure; Intestinal stem cell; Short bowel syndrome

Indexed keywords

BETACELLULIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; SOMATOMEDIN RECEPTOR; ANTIMETABOLITE; BROXURIDINE; IGF1RA PROTEIN, ZEBRAFISH; SOMATOMEDIN C; ZEBRAFISH PROTEIN;

ADAPTATION; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; EXPERIMENTAL MODEL; INTESTINAL STEM CELL; INTESTINE RESECTION; MALE; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; SHORT BOWEL SYNDROME; UPREGULATION; ZEBRA FISH; ABDOMINAL SURGERY; ANIMAL; DISEASE MODEL; HUMAN; INTESTINE; INTESTINE MUCOSA; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; STEM CELL; SURGERY; WEIGHT REDUCTION;

ADAPTATION, BIOLOGICAL; ANIMALS; ANTIMETABOLITES; BROMODEOXYURIDINE; CELL PROLIFERATION; DIGESTIVE SYSTEM SURGICAL PROCEDURES; DISEASE MODELS, ANIMAL; HUMANS; INSULIN-LIKE GROWTH FACTOR I; INTESTINAL MUCOSA; INTESTINES; MALE; SHORT BOWEL SYNDROME; STEM CELLS; WEIGHT LOSS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84938585583     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00311.2014     Document Type: Article

References (58)

1. Akimenko MA, Johnson SL, Westerfield M, Ekker M. Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish. Development 121: 347–357, 1995.
2. Amaral IP, Johnston IA. Insulin-like growth factor (IGF) signalling and genome-wide transcriptional regulation in fast muscle of zebrafish following a single-satiating meal. J Exp Biol 214: 2125–2139, 2011.
3. Andersson H, Bosaeus I, Brummer RJ, Fasth S, Hultén L, Magnusson O, Strauss B. Nutritional and metabolic consequences of extensive bowel resection. Dig Dis 4: 193–202, 1986.
4. Bahrami J, Yusta B, Drucker DJ. ErbB activity links the glucagon-like peptide-2 receptor to refeeding-induced adaptation in the murine small bowel. Gastroenterology 138: 2447–2456, 2010.
5. Benhamou PH, Canarelli JP, Richard S, Cordonnier C, Postel JP, Grenier E, Leke A, Dupont C. Human recombinant growth hormone increases small bowel lengthening after massive small bowel resection in piglets. J Pediatr Surg 32: 1332–1336, 1997.
6. Chaet MS, Arya G, Ziegler MM, Warner BW. Epidermal growth factor enhances intestinal adaptation after massive small bowel resection. J Pediatr Surg 29: 1035–1039, 1994.
7. Diep CQ, Davidson AJ. Transplantation of cells directly into the kidney of adult zebrafish. J Vis Exp 51: 2725, 2011.
8. Erwin CR, Helmrath MA, Shin CE, Falcone RA Jr, Stern LE, Warner BW. Intestinal overexpression of EGF in transgenic mice enhances adaptation after small bowel resection. Am J Physiol Gastrointest Liver Physiol 277: G533–G540, 1999.
9. Frey MR, Goloyin A, Polk B. Epidermal growth factor-stimulated intestinal cell migration requires Src family kinase-dependent p38 MAPK signaling. J Biol Chem 279: 44513–44521, 2004.
10. García-Echeverría C, Pearson MA, Marti A, Meyer T, Mestan J, Zimmermann J, Gao J, Brueggen J, Capraro HG, Cozens R, Evans DB, Fabbro D, Furet P, Porta DG, Liebetanz J, Martiny-Baron G, Ruetz S, Hofmann F. In vivo antitumor activity of NVP-AEW541—A novel, potent, and selective inhibitor of the IGF-IR kinase. Cancer Cell 5: 231–239, 2004.
11. Gómez de Segura IA, Aguilera MJ, Codesal J, Codoceo R, De-Miguel E. Comparative effects of growth hormone in large and small bowel resection in the rat. J Surg Res 62: 5–10, 1996.
12. Gregorieff A, Stange DE, Kujala P, Begthel H, van den Born M, Korving J, Peters PJ, Clevers H. The Ets-domain transcription factor Spdef promotes maturation of goblet and Paneth cells in the intestinal epithelium. Gastroenterology 137: 1333–1345.e1–e3, 2009.
13. Hanson WR, Osborne JW, Sharp JG. Compensation by the residual intestine after intestinal resection in the rat. II. Influence of postoperative time interval. Gastroenterology 72: 701–705, 1977.
14. Health Resources and Services Administration. Scientific Registry of Transplant Recipients: 2011 Annual Data Report. Minneapolis, MN: Scientific Registry of Transplant Recipients, 2011.
15. Heemskerk VH, van Heurn LW, Farla P, Buurman WA, Piersma F, ter Riet G, Heineman E. A successful short-bowel syndrome model in neonatal piglets. J Pediatr Gastroenterol Nutr 29: 457–461, 1999.
16. Helmrath MA, Erwin CR, Warner BW. A defective EGF-receptor in waved-2 mice attenuates intestinal adaptation. J Surg Res 69: 76–80, 1997.
17. Helmrath MA, Fong JJ, Dekaney CM, Henning SJ. Rapid expansion of intestinal secretory lineages following a massive small bowel resection in mice. Am J Physiol Gastrointest Liver Physiol 292: G215–G222, 2007.
18. Herington AC. Insulin-like growth factors: biochemistry and physiology. Baillieres Clin Endocrinol Metab 5: 531–551, 1991.
19. Kamei H, Ding Y, Kajimura S, Wells M, Chiang P, Duan C. Role of IGF signaling in catch-up growth and accelerated temporal development in zebrafish embryos in response to oxygen availability. Development 138: 777–786, 2011.
20. Kato T, Tzakis AG, Selvaggi G, Gaynor JJ, David AI, Bussotti A, Moon JI, Ueno T, DeFaria W, Santiago S, Levi DM, Nishida S, Velasco ML, McLaughlin G, Hernandez E, Thompson JF, Cantwell P, Holliday N, Livingstone AS, Ruiz P. Intestinal and multivisceral transplantation in children. Ann Surg 243: 756–764; discussion 764–766, 2006.
21. Kazanjian A, Shroyer NF. NOTCH signaling and ATOH1 in colorectal cancers. Curr Colorectal Cancer Rep 7: 121–127, 2011.
22. Knudsen SLJ, Mac ASW, Henriksen L, van Deurs B, Grovdal LM. EGFR signaling patterns are regulated by its different ligands. Growth Factors 32: 155–163, 2014.
23. Lemmey AB, Martin AA, Read LC, Tomas FM, Owens PC, Ballard FJ. IGF-I and the truncated analogue des-(1–3)IGF-I enhance growth in rats after gut resection. Am J Physiol Endocrinol Metab 260: E213–E219, 1991.
24. Longshore SW, Wakeman D, McMellen M, Warner BW. Bowel resection induced intestinal adaptation: progress from bench to bedside. Minerva Pediatr 61: 239–251, 2009.
25. Lykins TC, Stockwell J. Comprehensive modified diet simplifies nutrition management of adults with short-bowel syndrome. J Am Diet Assoc 98: 309–315, 1998.
26. Martin GR, Wallace LE, Sigalet DL. Glucagon-like peptide-2 induces intestinal adaptation in parenterally fed rats with short bowel syndrome. Am J Physiol Gastrointest Liver Physiol 286: G964–G972, 2004.
27. McMellen ME, Wakeman D, Longshore SW, McDuffie LA, Warner BW. Growth factors: possible roles for clinical management of the short bowel syndrome. Semin Pediatr Surg 19: 35–43, 2010.
28. Moss JB, Koustubhan P, Greenman M, Parsons MJ, Walter I, Moss LG. Regeneration of the pancreas in adult zebrafish. Diabetes 58: 1844–1851, 2009.
29. Ng AN, de Jong-Curtain TA, Mawdsley DJ, White SJ, Shin J, Appel B, Dong PD, Stainier DY, Heath JK. Formation of the digestive system in zebrafish: III. Intestinal epithelium morphogenesis. Dev Biol 286: 114–135, 2005.
30. O’Loughlin E, Winter M, Shun A, Hardin JA, Gall DG. Structural and functional adaptation following jejunal resection in rabbits: effect of epidermal growth factor. Gastroenterology 107: 87–93, 1994.
31. O’Louglin E, Winter M, Sun A, Hardin J, Gall DG. Structural and functional adaptatio following jejunal resection in rabbits: effect of epidermal growth factor. Gastroenterology 107: 87–93, 1994.
32. Okawada M, Holst JJ, Teitelbaum DH. Administration of a dipeptidyl peptidase IV inhibitor enhances the intestinal adaptation in a mouse model of short bowel syndrome. Surgery 150: 217–223, 2011.
33. Pereira-Fantini PM, Thomas SL, Wilson G, Taylor RG, Sourial M, Bines JE. 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: 195–202, 2011.
34. Peyret B, Collardeau S, Touzet S, Loras-Duclaux I, Yantren H, Michalski MC, Chaix J, Restier-Miron L, Bouvier R, Lachaux A, Peretti N. Prevalence of liver complications in children receiving longterm parenteral nutrition. Eur J Clin Nutr 65: 743–749, 2011.
35. Pozios KC, Ding J, Degger B, Upton Z, Duan C. IGFs stimulate zebrafish cell proliferation by activating MAP kinase and PI3-kinasesignaling pathways. Am J Physiol Regul Integr Comp Physiol 280: R1230–R1239, 2001.
36. Pruyot B, Cure Y, Dijotsa J, Voncken A, Muller M. Developmental defects in zebrafish for classification of EGF pathway inhibitors. Toxicol Appl Pharmacol 274: 339–349, 2014.
37. Pugach EK, Li P, White R, Zon L. Retro-orbital injection in adult zebrafish. J Vis Exp 34: 1645, 2009.
38. Reinecke M, Björnsson BT, Dickhoff WW, McCormick SD, Navarro I, Power DM, Gutiérrez J. Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen Comp Endocrinol 142: 20–24, 2005.
39. Rowland KJ, Brubaker PL. The “cryptic” mechanism of action of glucagon-like peptide-2. Am J Physiol Gastrointest Liver Physiol 301: G1–G8, 2011.
40. Schalamon J, Mayr JM, Hollwarth ME. Mortality and economics in short bowel syndrome. Best Pract Res Clin Gastroenterol 17: 931–942, 2003.
41. Schwartz MZ, Maeda K. Short bowel syndrome in infants and children. Pediatr Clin North Am 32: 1265–1279, 1985.
42. Scott RB, Sheehan A, Chin BC, Tan DT. Hyperplasia of the muscularis propria in response to massive intestinal resection in rat. J Pediatr Gastroenterol Nutr 21: 399–409, 1995.
43. Shulman DI, Hu CS, Duckett G, Lavallee-Grey M. Effects of shortterm growth hormone therapy in rats undergoing 75% small intestinal resection. J Pediatr Gastroenterol Nutr 14: 3–11, 1992.
44. Stollman NH, Neustater BR, Rogers AI. Short-bowel syndrome. Gastroenterologist 4: 118–128, 1996.
45. Taylor JA, Martin CA, Nair R, Guo J, Erwin CR, Warner BW. Lessons learned: optimization of a murine small bowel resection model. J Pediatr Surg 43: 1018–1024, 2008.
46. Van Landeghem L, Santoro MA, Mah AT, Krebs AE, Dehmer JJ, McNaughton KK, Helmrath MA, Magness ST, Lund PK. IGF1 stimulates crypt expansion via differential activation of 2 intestinal stem cell populations. FASEB J 29: 1–15, 2015.
47. Vanderhoof JA, McCusker RH, Clark R, Mohammadpour H, Blackwood DJ, Harty RF, Park JH. Truncated and native insulinlike growth factor I enhance mucosal adaptation after jejunoileal resection. Gastroenterology 102: 1949–1956, 1992.
48. Wales PW, Christison-Lagay ER. Short bowel syndrome: epidemiology and etiology. Semin Pediatr Surg 19: 3–9, 2010.
49. Wallace KN, Akhter S, Smith EM, Lorent K, Pack M. Intestinal growth and differentiation in zebrafish. Mech Dev 122: 157–173, 2005.
50. Wallis K, Walters JR, Gabe S. Short bowel syndrome: the role of GLP-2 on improving outcome. Curr Opin Clin Nutr Metab Care 12: 526–532, 2009.
51. Wang Z, Du J, Lam SH, Mathavan S, Matsudaira P, Gong Z. Morphological and molecular evidence for functional organization along the rostrocaudal axis of the adult zebrafish intestine. BMC Genomics 11: 392, 2010.
52. Weih S, Nickkholgh A, Kessler M, Frongia G, Hafezi M, Golriz M, Fard N, Holland-Cunz S, Mehrabi A. Models of short bowel syndrome in pigs: a technical review. Eur Surg Res 51: 66–78, 2013.
53. Welters CF, Dejong CH, Deutz NE, Heineman E. Intestinal adaptation in short bowel syndrome. ANZ J Surg 72: 229–236, 2002.
54. Wheeler EE, Challacombe DN. The trophic action of growth hormone, insulin-like growth factor-I, and insulin on human duodenal mucosa cultured in vitro. Gut 40: 57–60, 1997.
55. Williamson RC. Intestinal adaptation (second of two parts). Mechanisms of control. N Engl J Med 298: 1444–1450, 1978.
56. Wolvekamp MC, Heineman E, Taylor RG, Fuller PJ. Towards understanding the process of intestinal adaptation. Dig Dis 14: 59–72, 1996.
57. Zou S, Kamei H, Modi Z, Duan C. Zebrafish IGF genes: gene duplication, conservation and divergence, and novel roles in midline and notochord development. PLoS One 4: e7026, 2009.
58. Zu Y, Tong X, Wang Z, Liu D, Pan R, Li Z, Hu Y, Luo Z, Huang P, Wu Q, Zhu Z, Zhang B, Lin S. TALEN-mediated precise genome modification by homologous recombination in zebrafish. Nat Methods 10: 329–331, 2013.