Early but not late administration of glucagon-like peptide-2 following ileo-cecal resection augments putative intestinal stem cell expansion

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 296, Issue 3, 2009, Pages

  Garrison, Aaron P ^a   Dekaney, Christopher M ^a   Von Allmen, Douglas C ^a   Lund, P Kay ^a,b   Henning, Susan J ^a,b   Helmrath, Michael A ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Intestinal adaptation

Indexed keywords

BETA CATENIN; GLUCAGON LIKE PEPTIDE 2; MESSENGER RNA; SERINE; SOMATOMEDIN C; CATNB PROTEIN, MOUSE; PROTEIN; SERIN RICH SPERMATOGENIC PROTEIN 1, RAT; SERIN-RICH SPERMATOGENIC PROTEIN 1, RAT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SELECTION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOPATHOLOGY; ILEUM RESECTION; IMMUNOHISTOCHEMISTRY; INTESTINE CELL; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL EXPANSION; SURVIVAL; WEIGHT GAIN; ANIMAL; C57BL MOUSE; CECUM; CELL DIVISION; CYTOLOGY; DRUG EFFECT; ENTEROPATHY; ILEUM; METABOLISM; PATHOLOGY; POSTOPERATIVE COMPLICATION; STEM CELL; TIME;

ANIMALS; BETA CATENIN; CECUM; CELL DIVISION; GLUCAGON-LIKE PEPTIDE 2; ILEUM; INSULIN-LIKE GROWTH FACTOR I; INTESTINAL DISEASES; MALE; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; POSTOPERATIVE COMPLICATIONS; PROTEINS; STEM CELLS; TIME FACTORS; WEIGHT GAIN;

EID: 65349165236     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90588.2008     Document Type: Article

References (39)

1. Bjerknes M, Cheng H. Modulation of specific intestinal epithelial progenitors by enteric neurons. Proc Natl Acad Sci USA 98: 12497-12502, 2001.
2. Booth C, Booth D, Williamson S, Demchyshyn LL, Potten CS. Teduglutide ([Gly2]GLP-2) protects small intestinal stem cells from radiation damage. Cell Prolif 37: 385-400, 2004.
3. Burrin DG, Stoll B, Jiang R, Petersen Y, Elnif J, Buddington RK, Schmidt M, Holst JJ, Hartmann B, Sangild PT. GLP-2 stimulates intestinal growth in premature TPN-fed pigs by suppressing proteolysis and apoptosis. Am J Physiol Gastrointest Liver Physiol 279: G1249-G1256, 2000.
4. Cummins AG, Catto-Smith AG, Cameron DJ, Couper RT, Davidson GP, Day AS, Hammond PD, Moore DJ, Thompson FM. Crypt fission peaks early during infancy and crypt hyperplasia broadly peaks during infancy and childhood in the small intestine of humans. J Pediatr Gastroenterol Nutr 47: 153-157, 2008.
5. Dahly EM, Guo Z, Ney DM. IGF-I augments resection-induced mucosal hyperplasia by altering enterocyte kinetics. Am J Physiol Regul Integr Comp Physiol 285: R800-R808, 2003.
6. Dekaney CM, Fong JJ, Rigby RJ, Lund PK, Henning SJ, Helmrath MA. Expansion of intestinal stem cells associated with long-term adaptation following ileocecal resection in mice. Am J Physiol Gastrointest Liver Physiol 293: G1013-G1022, 2007.
7. Dekaney CM, Rodriguez JM, Graul MC, Henning SJ. Isolation and characterization of a putative intestinal stem cell fraction from mouse jejunum. Gastroenterology 129: 1567-1580, 2005.
8. Drucker DJ. Biologic actions and therapeutic potential of the proglucagon-derived peptides. Nat Clin Pract Endocrinol Metab 1: 22-31, 2005.
9. Dube PE, Brubaker PL. Frontiers in glucagon-like peptide-2: multiple actions, multiple mediators. Am J Physiol Endocrinol Metab 293: E460-E465, 2007.
10. Dube PE, Forse CL, Bahrami J, Brubaker PL. The essential role of insulin-like growth factor-1 in the intestinal tropic effects of glucagon-like peptide-2 in mice. Gastroenterology 131: 589-605, 2006.
11. Dube PE, Rowland KJ, Brubaker PL. Glucagon-like peptide-2 activates beta-catenin signaling in the mouse intestinal crypt: role of insulin-like growth factor-I. Endocrinology 149: 291-301, 2008.
12. Gillingham MB, Kritsch KR, Murali SG, Lund PK, Ney DM. Resection upregulates the IGF-I system of parenterally fed rats with jejunocolic anastomosis. Am J Physiol Gastrointest Liver Physiol 281: G1158-G1168, 2001.
13. Guan X, Karpen HE, Stephens J, Bukowski JT, Niu S, Zhang G, Stoll B, Finegold MJ, Holst JJ, Hadsell D, Nichols BL, Burrin DG. GLP-2 receptor localizes to enteric neurons and endocrine cells expressing vasoactive peptides and mediates increased blood flow. Gastroenterology 130: 150-164, 2006.
14. Gulati AS, Ochsner SA, Henning SJ. Molecular properties of side population-sorted cells from mouse small intestine. Am J Physiol Gastrointest Liver Physiol 294: G286-G294, 2008.
15. He XC, Yin T, Grindley JC, Tian Q, Sato T, Tao WA, Dirisina R, Porter-Westpfahl KS, Hembree M, Johnson T, Wiedemann LM, Barrett TA, Hood L, Wu H, Li L. PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat Genet 39: 189-198, 2007.
16. Jeppesen PB. Growth factors in short-bowel syndrome patients. Gastroenterol Clin North Am 36: 109-121, 2007.
17. Jeppesen PB, Hartmann B, Thulesen J, Graff J, Lohmann J, Hansen BS, Tofteng F, Poulsen SS, Madsen JL, Holst JJ, Mortensen PB. Glucagon-like peptide 2 improves nutrient absorption and nutritional status in short-bowel patients with no colon. Gastroenterology 120: 806-815, 2001.
18. Jeppesen PB, Sanguinetti EL, Buchman A, Howard L, Scolapio JS, Ziegler TR, Gregory J, Tappenden KA, Holst J, Mortensen PB. Teduglutide (ALX-0600), a dipeptidyl peptidase IV resistant glucagon-like peptide 2 analogue, improves intestinal function in short bowel syndrome patients. Gut 54: 1224-1231, 2005.
19. Koopmann MC, Nelson DW, Murali SG, Liu X, Brownfield MS, Holst JJ, Ney DM. Exogenous glucagon-like peptide-2 (GLP-2) augments GLP-2 receptor mRNA and maintains proglucagon mRNA levels in resected rats. JPEN J Parenter Enteral Nutr 32: 254-265, 2008.
20. Ljungmann K, Hartmann B, Kissmeyer-Nielsen P, Flyvbjerg A, Holst JJ, Laurberg S. Time-dependent intestinal adaptation and GLP-2 alterations after small bowel resection in rats. Am J Physiol Gastrointest Liver Physiol 281: G779-G785, 2001.
21. Loeffler M, Bratke T, Paulus U, Li YQ, Potten CS. Clonality and life cycles of intestinal crypts explained by a state dependent stochastic model of epithelial stem cell organization. J Theor Biol 186: 41-54, 1997.
22. Lund PK. Insulin-like growth factors. In: Gut Peptides: Biochemistry and Physiology, edited by Walsh JH and Dockray GJ. New York: Raven Press, 1994, p. 587-613.
23. Mantell MP, Ziegler TR, Adamson WT, Roth JA, Zhang W, Frankel W, Bain A, Chow JC, Smith RJ, Rombeau JL. Resection-induced colonic adaptation is augmented by IGF-I and associated with upregulation of colonic IGF-I mRNA. Am J Physiol Gastrointest Liver Physiol 269: G974-G980, 1995.
24. Martin GR, Wallace LE, Hartmann B, Holst JJ, Demchyshyn L, Toney K, Sigalet DL. Nutrient-stimulated GLP-2 release and crypt cell proliferation in experimental short bowel syndrome. Am J Physiol Gastrointest Liver Physiol 288: G431-G438, 2005.
25. Munroe DG, Gupta AK, Kooshesh F, Vyas TB, Rizkalla G, Wang H, Demchyshyn L, Yang ZJ, Kamboj RK, Chen H, McCallum K, Sumner-Smith M, Drucker DJ, Crivici A. Prototypic G protein-coupled receptor for the intestinotrophic factor glucagon-like peptide 2. Proc Natl Acad Sci USA 96: 1569-1573, 1999.
26. Nelson DW, Sharp JW, Brownfield MS, Raybould HE, Ney DM. Localization and activation of glucagon-like peptide-2 receptors on vagal afferents in the rat. Endocrinology 148: 1954-1962, 2007.
27. Orskov C, Hartmann B, Poulsen SS, Thulesen J, Hare KJ, Holst JJ. GLP-2 stimulates colonic growth via KGF, released by subepithelial myofibroblasts with GLP-2 receptors. Regul Pept 124: 105-112, 2005.
28. Pereira-Fantini PM, Nagy ES, Thomas SL, Taylor RG, Sourial M, Paris MC, Holst JJ, Fuller PJ, Bines JE. GLP-2 administration results in increased proliferation but paradoxically an adverse outcome in a juvenile piglet model of short bowel syndrome. J Pediatr Gastroenterol Nutr 46: 20-28, 2008.
29. Peterson CA, Gillingham MB, Mohapatra NK, Dahly EM, Adamo ML, Carey HV, Lund PK, Ney DM. Enterotrophic effect of insulin-like growth factor-I but not growth hormone and localized expression of insulin-like growth factor-I, insulin-like growth factor binding protein-3 and -5 mRNAs in jejunum of parenterally fed rats. JPEN J Parenter Enteral Nutr 24: 288-295, 2000.
30. Sangild PT, Tappenden KA, Malo C, Petersen YM, Elnif J, Bartholome AL, Buddington RK. Glucagon-like peptide 2 stimulates intestinal nutrient absorption in parenterally fed newborn pigs. J Pediatr Gastroenterol Nutr 43: 160-167, 2006.
31. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW. Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 285: 194-204, 2000.
32. Scott RB, Kirk D, MacNaughton WK, Meddings JB. GLP-2 augments the adaptive response to massive intestinal resection in rat. Am J Physiol Gastrointest Liver Physiol 275: G911-G921, 1998.
33. Scoville DH, Sato T, He XC, Li L. Current view: intestinal stem cells and signaling. Gastroenterology 134: 849-864, 2008.
34. Williams KL, Fuller CR, Fagin J, Lund PK. Mesenchymal IGF-I overexpression: paracrine effects in the intestine, distinct from endocrine actions. Am J Physiol Gastrointest Liver Physiol 283: G875-G885, 2002.
35. Wright NA. Epithelial stem cell repertoire in the gut: clues to the origin of cell lineages, proliferative units and cancer. Int J Exp Pathol 81: 117-143, 2000.
36. Yang H, Teitelbaum DH. Novel agents in the treatment of intestinal failure: humoral factors. Gastroenterology 130: S117-S121, 2006.
37. Yusta B, Huang L, Munroe D, Wolff G, Fantaske R, Sharma S, Demchyshyn L, Asa SL, Drucker DJ. Enteroendocrine localization of GLP-2 receptor expression in humans and rodents. Gastroenterology 119: 744-755, 2000.
38. Ziegler TR, Fernandez-Estivariz C, Gu LH, Bazargan N, Umeakunne K, Wallace TM, Diaz EE, Rosado KE, Pascal RR, Galloway JR, Wilcox JN, Leader LM. Distribution of the H+/peptide transporter PepT1 in human intestine: up-regulated expression in the colonic mucosa of patients with short-bowel syndrome. Am J Clin Nutr 75: 922-930, 2002.
39. Ziegler TR, Mantell MP, Chow JC, Rombeau JL, Smith RJ. Intestinal adaptation after extensive small bowel resection: differential changes in growth and insulin-like growth factor system messenger ribonucleic acids in jejunum and ileum. Endocrinology 139: 3119-3126, 1998.