Mechanism of action of glucagon-like peptide-2 to increase IGF-I mRNA in intestinal subepithelial fibroblasts

Endocrinology

Volumn 152, Issue 2, 2011, Pages 436-446

  Leen, Jason L S ^a   Izzo, Angelo ^a   Upadhyay, Chandani ^a   Rowland, Katherine J ^a   Dubé, Philip E ^a   Gu, Steven ^a   Heximer, Scott P ^a   Rhodes, Christopher J ^b   Storm, Daniel R ^c   Lund, P Kay ^d   Brubaker, Patricia L ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b University of Chicago ^*  (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA GALACTOSIDASE; CALCIUM; CYCLIC AMP; EPIDERMAL GROWTH FACTOR; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; TEDUGLUTIDE; VIMENTIN; WORTMANNIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL CULTURE; CONTROLLED STUDY; FEMALE; FIBROBLAST; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; INTESTINE CELL; JEJUNUM; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANDROSTADIENES; ANIMALS; CHROMONES; CYCLIC AMP; FEMALE; FIBROBLASTS; GLUCAGON-LIKE PEPTIDE 2; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR I; INTESTINES; MALE; MICE; MORPHOLINES; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, GLUCAGON; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 79951666823     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0822     Document Type: Article

References (67)

1. Dubé PE, Brubaker PL 2007 Frontiers in glucagon-like peptide-2: multiple actions, multiple mediators. Am J Physiol Endocrinol Metab 293:E460-E465 (Pubitemid 47205088)
2. Shin ED, Estall JL, Izzo A, Drucker DJ, Brubaker PL 2005 Mucosal adaptation to enteral nutrients is dependent on the physiologic actions of glucagon-like peptide-2 in mice. Gastroenterology 128: 1340-1353 (Pubitemid 40712184)
3. Nelson DW, Murali SG, Liu X, Koopmann MC, Holst JJ, Ney DM 2008 Insulin-like growth factor I and glucagon-like peptide-2 responses to fasting followed by controlled or ad libitum refeeding in rats. Am J Physiol Regul Integr Comp Physiol 294:R1175-R1184 (Pubitemid 351490636)
4. Bahrami J, Yusta B, Drucker DJ 2010 ErbB activity links the glucagon-like peptide-2 receptor to refeeding-induced adaptation in the murine small bowel. Gastroenterology 138:2447-2456
5. Drucker DJ, Erlich P, Asa SL, Brubaker PL 1996 Induction of intestinal epithelial proliferation by glucagon-like peptide 2. Proc Natl Acad Sci USA 93:7911-7916 (Pubitemid 26277138)
6. Brubaker PL, Izzo A, Hill M, Drucker DJ 1997 Intestinal function in mice with small bowel growth induced by glucagon-like peptide- 2. Am J Physiol Endocrinol Metab 272:E1050-E1058
7. Benjamin MA, McKay DM, Yang PC, Cameron H, Perdue MH 2000 Glucagon-like peptide-2 enhances intestinal epithelial barrier function of both transcellular and paracellular pathways in the mouse. Gut 47:112-119 (Pubitemid 30430419)
8. Scott RB, Kirk D, MacNaughton WK, Meddings JB 1998 GLP-2 augments the adaptive response to massive intestinal resection in rats. Am J Physiol Gastrointest Liver Physiol 275:G911-G921
9. Koopmann MC, Nelson DW, Murali SG, Liu X, Brownfield MS, Holst JJ, Ney DM 2008 Exogenous glucagon-like peptide-2 (GLP-2) augments GLP-2 receptor mRNA and maintains proglucagon mRNA levels in resected rats. J Parenter Enteral Nutr 32:254-265 (Pubitemid 351571264)
10. Yusta B, Holland D, Koehler JA, Maziarz M, Estall JL, Higgins R, Drucker DJ 2009 ErbB signaling is required for the proliferative actions of GLP-2 in the murine gut. Gastroenterology 137:986-996
11. Dubé PE, Forse CL, Bahrami J, Brubaker PL 2006 Essential role of insulin-like growth factor-1 in the intestinal tropic effects of glucagon-like peptide-2 in mice. Gastroenterology 131:589-605 (Pubitemid 44142460)
12. Jeppesen PB, Sanguinetti EL, Buchman A, Howard L, Scolapio JS, Ziegler TR, Gregory J, Tappenden KA, Holst J, Mortensen PB 2005 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 (Pubitemid 41192479)
13. Jeppesen PB, Lund P, Gottschalck IB, Nielsen HB, Holst JJ, Mortensen J, Poulsen SS, Quistorff B, Mortensen PB 2009 Short bowel patients treated for two years with glucagon-like peptide 2 (GLP-2): compliance, safety, and effects on quality of life. Gastroenterol Res Pract 2009:425759:1-425759:9
14. Jeppesen PB, Lund P, Gottschalck IB, Nielsen HB, Holst JJ, Mortensen J, Poulsen SS, Quistorff B, Mortensen PB 2009 Short bowel patients treated for two years with glucagon-like peptide 2: effects on intestinal morphology and absorption, renal function, bone and body composition, and muscle function. Gastroenterol Res Pract 2009:616054:1-616054:12
15. Boushey RP, Yusta B, Drucker DJ 1999 Glucagon-like peptide 2 decreases mortality and reduces the severity of indomethacin-induced murine enteritis. Am J Physiol Endocrinol Metab 277:E937-E947
16. L'Heureux M-C, Brubaker PL 2003 Glucagon-like peptide-2 and common therapeutics in a murine model of ulcerative colitis. J Pharm Exp Ther 306:347-354 (Pubitemid 36734391)
17. Sigalet DL, Wallace LE, Holst JJ, Martin GR, Kaji T, Tanaka H, Sharkey KA 2007 Enteric neural pathways mediate the anti-inflammatory actions of glucagon-like peptide 2. Am J Physiol Gastrointest Liver Physiol 293:G211-G221 (Pubitemid 47105173)
18. Buchman AL, Katz S, Fang JC, Bernstein CN, Abou-Assi SG 2010 Teduglutide, a novel mucosally active analog of glucagon-like peptide- 2 (GLP-2) for the treatment of moderate to severe Crohn's disease. Inflamm Bowel Dis 16:962-973
19. 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 1999 Prototypic G protein-coupled receptor for the intestinotrophic factor glucagon-like peptide 2. Proc Natl Acad Sci USA 96:1569-1573 (Pubitemid 29098492)
20. Yusta B, Huang L, Munroe D, Wolff G, Fantaske R, Sharma S, Demchyshyn L, Asa SL, Drucker DJ 2000 Enteroendocrine localization of GLP-2 receptor expression in humans and rodents. Gastroenterology 119:744-755
21. Bjerknes M, Cheng H 2001 Modulation of specific intestinal epithelial progenitors by enteric neurons. Proc Natl Acad Sci USA 98: 12497-12502 (Pubitemid 33019974)
22. Ramsanahie A, Duxbury MS, Grikscheit TC, Perez A, Rhoads DB, Gardner-Thorpe J, Ogilvie J, Ashley SW, Vacanti JP, Whang EE 2003 Effect of GLP-2 on mucosal morphology and SGLT1 expression in tissue-engineered neointestine. Am J Physiol Gastrointest Liver Physiol 285:G1345-G1352 (Pubitemid 37449023)
23. Ørskov C, Hartmann B, Poulsen SS, Thulesen J, Hare KJ, Holst JJ 2005 GLP-2 stimulates colonic growth via KGF, released by subepithelial myofibroblasts with GLP-2 receptors. Regul Pept 124: 105-112
24. Guan X, Karpen HE, Stephens J, Bukowski JT, Niu S, Zhang G, Stoll B, Finegold MJ, Holst JJ, Hadsell DL, Nichols BL, Burrin DG 2006 GLP-2 receptor localizes to enteric neurons and endocrine cells expressing vasoactive peptides and mediates increased blood flow. Gastroenterology 130:150-164 (Pubitemid 43049845)
25. Nelson DW, Sharp JW, Brownfield MS, Raybould HE, Ney DM 2007 Localization and activation of glucagon-like peptide-2 receptors on vagal afferents in the rat. Endocrinology 148:1954-1962 (Pubitemid 46997024)
26. Dubé PE, Rowland KJ, Brubaker PL 2008 Glucagon-like peptide-2 activates beta-catenin signaling in the mouse intestinal crypt: role of insulin-like growth factor-I. Endocrinology 149:291-301
27. Powell DW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, West AB 1999 Myofibroblasts. I. Paracrine cells important in health and disease. Am J Physiol 277:C1-C9
28. Powell DW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, West AB 1999 Myofibroblasts. II. Intestinal subepithelial myofibroblasts. Am J Physiol 277:C183-C201 (Pubitemid 29415032)
29. Simmons JG, Pucilowska JB, Lund PK 1999 Autocrine and paracrine actions of intestinal fibroblast-derived insulin-like growth factors. Am J Physiol Gastrointest Liver Physiol 276:G817-G827 (Pubitemid 29214093)
30. Fruchtman S, Simmons JG, Michaylira CZ, Miller ME, Greenhalgh CJ, Ney DM, Lund PK 2005 Suppressor of cytokine signaling-2 modulates the fibrogenic actions of GH and IGF-I in intestinal mesenchymal cells. Am J Physiol Gastrointest Liver Physiol 289:G342-G350 (Pubitemid 41022761)
31. Liu X, Murali SG, Holst JJ, Ney DM 2008 Enteral nutrients potentiate the intestinotrophic action of glucagon-like peptide-2 in association with increased insulin-like growth factor-I responses in rats. Am J Physiol Regul Integr Comp Physiol 295:R1794-R1802
32. Garrison AP, Dekaney CM, von Allmen DC, Lund PK, Henning SJ, Helmrath MA 2009 Early but not late administration of glucagon-like peptide-2 following ileo-cecal resection augments putative intestinal stem cell expansion. Am J Physiol Gastrointest Liver Physiol 296:G643-G650
33. Jobson TM, Billington CK, Hall IP 1998 Regulation of proliferation of human colonic subepithelial myofibroblasts by mediators important in intestinal inflammation. J Clin Invest 101:2650-2657 (Pubitemid 28294573)
34. Theiss AL, Simmons JG, Jobin C, Lund PK 2005 Tumor necrosis factor (TNF) alpha increases collagen accumulation and proliferation in intestinal myofibroblasts via TNF receptor 2. J Biol Chem 280:36099-36109 (Pubitemid 41633881)
35. Impey S, Mark M, Villacres EC, Poser S, Chavkin C, Storm DR 1996 Induction of CRE-mediated gene expression by stimuli that generate long-lasting LTP in area CA1 of the hippocampus. Neuron 16:973-982
36. Dhanvantari S, Seidah NG, Brubaker PL 1996 Role of prohormone convertases in the tissue-specific processing of proglucagon. Mol Endocrinol 10:342-355 (Pubitemid 26112399)
37. Walsh NA, Yusta B, DaCambra MP, Anini Y, Drucker DJ, Brubaker PL 2003 Glucagon-like peptide-2 receptor activation in the rat intestinal mucosa. Endocrinology 144:4385-4392 (Pubitemid 37204837)
38. Dickson LM, Lingohr MK, McCuaig J, Hugl SR, Snow L, Kahn BB, Myers Jr MG, Rhodes CJ 2001 Differential activation of protein kinase B and p70(S6)K by glucose and insulin-like growth factor 1 in pancreatic beta-cells (INS-1). J Biol Chem 276:21110-21120
39. Hoyt EC, Van Wyk JJ, Lund PK 1988 Tissue and development specific regulation of a complex family of rat insulin-like growth factor I messenger ribonucleic acids. Mol Endocrinol 2:1077-1086 (Pubitemid 18262265)
40. Pfaffl MW 2001 A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
41. Gu S, He J, Ho WT, Ramineni S, Thal DM, Natesh R, Tesmer JJ, Hepler JR, Heximer SP 2007 Unique hydrophobic extension of the RGS2 amphipathic helix domain imparts increased plasma membrane binding and function relative to other RGS R4/B subfamily members. J Biol Chem 282:33064-33075 (Pubitemid 350159325)
42. Adegboyega PA, Mifflin RC, DiMari JF, Saada JI, Powell DW 2002 Immunohistochemical study of myofibroblasts in normal colonic mucosa, hyperplastic polyps, and adenomatous colorectal polyps. Arch Pathol Lab Med 126:829-836 (Pubitemid 34761641)
43. Iakoubov R, Izzo A, Yeung A, Whiteside CI, Brubaker PL 2007 Essential role of protein kinase Czeta in oleic acid-induced secretion of glucagon-like peptide-1. Endocrinology 148:1089-1098
44. Thulesen J, Knudsen LB, Hartmann B, Hastrup S, Kissow H, Jeppesen PB, Orskov C, Holst JJ, Poulsen SS 2002 The truncated metabolite GLP-2 (3-33) interacts with the GLP-2 receptor as a partial agonist. Reg Pep 103:9-15 (Pubitemid 34001631)
45. Koehler JA, Yusta B, Drucker DJ 2005 The HeLa cell glucagon-like peptide-2 receptor is coupled to regulation of apoptosis and ERK1/2 activation through divergent signaling pathways. Mol Endocrinol 19:459-473 (Pubitemid 40223469)
46. Estall JL, Yusta B, Drucker DJ 2004 Lipid raft-dependent glucagon-like peptide-2 receptor trafficking occurs independently of agonistinduced desensitization. Mol Biol Cell 15:3673-3687 (Pubitemid 38989705)
47. Estall JL, Koehler JA, Yusta B, Drucker DJ 2005 The glucagon-like peptide-2 receptor C terminus modulates beta-arrestin-2 association but is dispensable for ligand-induced desensitization, endocytosis, and G-protein-dependent effector activation. J Biol Chem280: 22124-22134 (Pubitemid 40827868)
48. Böni-Schnetzler M, Schmid C, Meier PJ, Froesch ER 1991 Insulin regulates insulin-like growth factor I mRNA in rat hepatocytes. Am J Physiol 260:E846-E851
49. Frost RA, Nystrom GJ, Lang CH 2002 Regulation of IGF-I mRNA and signal transducers and activators of transcription-3 and -5 (Stat-3 and -5) by GH in C2C12 myoblasts. Endocrinology 143: 492-503 (Pubitemid 34107202)
50. Lee D, Pearsall RS, Das S, Dey SK, Godfrey VL, Threadgill DW 2004 Epiregulin is not essential for development of intestinal tumors but is required for protection from intestinal damage. Mol Cell Biol 24:8907-8916 (Pubitemid 39313896)
51. Nakamura Y, Handa K, Iwamoto R, Tsukamoto T, Takahasi M, Mekada E 2001 Immunohistochemical distribution of CD9, heparin binding epidermal growth factor-like growth factor, and integrin alpha3beta1 in normal human tissues. J Histochem Cytochem 49: 439-444 (Pubitemid 32295165)
52. Yusta B, Somwar R, Wang F, Munroe D, Grinstein S, Klip A, Drucker DJ 1999 Identification of glucagon-like peptide-2 (GLP- 2)-activated signaling pathways in baby hamster kidney fibroblasts expressing the rat GLP-2 receptor. J Biol Chem 274:30459-30467
53. Burrin DG, Stoll B, Guan X, Cui L, Chang X, Hadsell D 2007 GLP-2 rapidly activates divergent intracellular signaling pathways involved in intestinal cell survival and proliferation in neonatal piglets. Am J Physiol Endocrinol Metab 292:E281-E291
54. Yusta B, Boushey RP, Drucker DJ 2000 The glucagon-like peptide-2 receptor mediates direct inhibition of cellular apoptosis via a cAMP-dependent protein kinase-independent pathway. J Biol Chem 275: 35345-35352
55. Yusta B, Estall J, Drucker DJ 2002 Glucagon-like peptide-2 receptor activation engages Bad and glucagon synthase kinase-3 in a protein kinase A-dependent manner and prevents apoptosis following inhibition of phosphatidylinositol 3-kinase. J Biol Chem 277:24896-24906 (Pubitemid 34951791)
56. Thomas MJ, Umayahara Y, Shu H, Centrella M, Rotwein P, McCarthy TL 1996 Identification of the cAMP response element that controls transcriptional activation of the insulin-like growth factor-I gene by prostaglandin E2 in osteoblasts. J Biol Chem 271: 21835-21841 (Pubitemid 26303803)
57. Du K, Montminy M 1998 CREB is a regulatory target for the protein kinase Akt/PKB. J Biol Chem 273:32377-32379 (Pubitemid 28557606)
58. Nolten LA, van Schaik FM, Steenbergh PH, Sussenbach JS 1994 Expression of the insulin-like growth factor I gene is stimulated by the liver-enriched transcription factors C/EBP alpha and LAP. Mol Endocrinol 8:1636-1645
59. Nolten LA, Steenbergh PH, Sussenbach JS 1995 Hepatocyte nuclear factor 1 alpha activates promoter 1 of the human insulin-like growth factor I gene via two distinct binding sites. Mol Endocrinol 9:1488-1499
60. Goya L, de la Puente A, Ramos S, Martin MA, Escrivá F, Alvarez C, Pascual-Leone AM 2001 Regulation of IGF-I and -II by insulin in primary cultures of fetal rat hepatocytes. Endocrinology 142:5089-5096 (Pubitemid 33131934)
61. Yu XY, Song YH, Geng YJ, Lin QX, Shan ZX, Lin SG, Li Y 2008 Glucose induces apoptosis of cardiomyocytes via microRNA-1 and IGF-1. Biochem Biophys Res Commun 376:548-552
62. Trotman LC, Alimonti A, Scaglioni PP, Koutcher JA, Cordon- Cardo C, Pandolfi PP 2006 Identification of a tumour suppressor network opposing nuclear Akt function. Nature 441:523-527 (Pubitemid 44050155)
63. Wang R, Brattain MG 2006 AKT can be activated in the nucleus. Cell Signal 18:1722-1731 (Pubitemid 44216128)
64. Xiao Q, Boushey R, Drucker DJ, Brubaker PL 1999 Secretion of the intestinotropic hormone glucagon-like peptide-2 is differentially regulated by nutrients in humans. Gastroenterology 117:99-105 (Pubitemid 29297625)
65. Marier JF, Beliveau M, Mouksassi MS, Shaw P, Cyran J, Kesavan J, Wallens J, Zahir H, Wells D, Caminis J 2008 Pharmacokinetics, safety, and tolerability of teduglutide, a glucagon-like peptide-2 (GLP-2) analog, following multiple ascending subcutaneous administrations in healthy subjects. J Clin Pharmacol 48:1289-1299
66. Lund PK 1994 Insulin-like growth factors. In: Walsh JH, Dockray GJ, eds. Gut peptides: biochemistry and physiology. New York: Raven Press; 587-614
67. Lund PK, Ulshen MH, Rountree DB, Selub SE, Buchan AM 1990 Molecular biology of gastrointestinal peptides and growth factors: relevance to intestinal adaptation. Digestion 46(Suppl 2):66-73 (Pubitemid 20298699)