Elucidating the biological roles of insulin and its receptor in murine intestinal growth and function

Endocrinology

Volumn 158, Issue 8, 2017, Pages 2453-2469

  Jensen, Stina Rikke ^a,b   Wheeler, Sarah E ^a   Hvid, Henning ^b   Ahnfelt Rønne, Jonas ^b   Hansen, Bo Falck ^b   Nishimura, Erica ^b   Olsen, Grith Skytte ^b   Brubaker, Patricia L ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b NOVO NORDISK A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; COMPLEMENTARY DNA; GLUCAGON LIKE PEPTIDE 2; GLUCOSE; GLUCOSE TRANSPORTER 2; INSULIN; INSULIN RECEPTOR; PROTEIN KINASE B; PROTEOME; RECOMBINANT HUMAN INSULIN; RNA; SOMATOMEDIN C RECEPTOR; TRIACYLGLYCEROL; GLUCOSE BLOOD LEVEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; C57BL 6 MOUSE; CHOLESTEROL BLOOD LEVEL; COLON; CONTROLLED STUDY; DIET RESTRICTION; DRUG MEGADOSE; DUODENUM; ENZYME ACTIVATION; FEMALE; FOOD INTAKE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HISTOLOGY; HORMONE ACTION; IMMUNOFLUORESCENCE; INSULIN BLOOD LEVEL; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; JEJUNUM; KNOCKOUT MOUSE; MALE; METABOLIC REGULATION; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SMALL INTESTINE; TRIACYLGLYCEROL BLOOD LEVEL; WESTERN DIET; ANIMAL; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GLUCOSE TOLERANCE TEST; GROWTH, DEVELOPMENT AND AGING; INTESTINE; METABOLISM; MOUSE; PHOSPHORYLATION; TRANSGENIC MOUSE;

ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION REGULATION; GENOTYPE; GLUCOSE TOLERANCE TEST; INSULIN; INTESTINES; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, INSULIN;

EID: 85026650576     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2017-00195     Document Type: Article

References (43)

1. Huang S, Czech MP. The GLUT4 glucose transporter. Cell Metab. 2007;5(4):237-252.
2. Tobin V, Le Gall M, Fioramonti X, Stolarczyk E, Blazquez AG, Klein C, Prigent M, Serradas P, Cuif MH, Magnan C, Leturque A, Brot-Laroche E. Insulin internalizes GLUT2 in the enterocytes of healthy but not insulin-resistant mice. Diabetes. 2008;57(3): 555-562.
3. Nguyen NQ, Debreceni TL, Bambrick JE, Chia B, Wishart J, Deane AM, Rayner CK, Horowitz M, Young RL. Accelerated intestinal glucose absorption in morbidly obese humans: Relationship to glucose transporters, incretin hormones, and glycemia. J Clin Endocrinol Metab. 2015;100(3):968-976.
4. Federico LM, Naples M, Taylor D, Adeli K. Intestinal insulin resistance and aberrant production of apolipoprotein B48 lipoproteins in an animal model of insulin resistance and metabolic dyslipidemia: Evidence for activation of protein tyrosine phosphatase-1B, extracellular signal-related kinase, and sterol regulatory elementbinding protein-1c in the fructose-fed hamster intestine. Diabetes. 2006;55(5):1316-1326.
5. Pavlic M, Xiao C, Szeto L, Patterson BW, Lewis GF. Insulin acutely inhibits intestinal lipoprotein secretion in humans in part by suppressing plasma free fatty acids. Diabetes. 2010;59(3):580-587.
6. Veilleux A, Grenier E, Marceau P, Carpentier AC, Richard D, Levy E. Intestinal lipid handling: Evidence and implication of insulin signaling abnormalities in human obese subjects. Arterioscler Thromb Vasc Biol. 2014;34(3):644-653.
7. Belfiore A, Frasca F, Pandini G, Sciacca L, Vigneri R. Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease. Endocr Rev. 2009; 30(6):586-623.
8. Aliaga JC, Deschênes C, Beaulieu JF, Calvo EL, Rivard N. Requirement of the MAP kinase cascade for cell cycle progression and differentiation of human intestinal cells. Am J Physiol. 1999; 277(3 Pt 1):G631-G641.
9. Ussar S, Haering MF, Fujisaka S, Lutter D, Lee KY, Li N, Gerber GK, Bry L, Kahn CR. Regulation of glucose uptake and enteroendocrine function by the intestinal epithelial insulin receptor. Diabetes. 2017;66(4):886-896.
10. Andres SF, Santoro MA, Mah AT, Keku JA, Bortvedt AE, Blue RE, Lund PK. Deletion of intestinal epithelial insulin receptor attenuates high-fat diet-induced elevations in cholesterol and stem, enteroendocrine, and Paneth cell mRNAs. Am J Physiol Gastrointest Liver Physiol. 2015;308(2):G100-G111.
11. Santoro MA, Blue RE, Andres SF, Mah AT, Van Landeghem L, Lund PK. Obesity and intestinal epithelial deletion of the insulin receptor, but not the IGF 1 receptor, affect radiation-induced apoptosis in colon. Am J Physiol Gastrointest Liver Physiol. 2015; 309(7):G578-G589.
12. Lee JY, Ristow M, Lin X, White MF, Magnuson MA, Hennighausen L. RIP-Cre revisited, evidence for impairments of pancreatic beta-cell function. J Biol Chem. 2006;281(5):2649-2653.
13. Gofflot F, Wendling O, Chartoire N, BirlingMC, Warot X, Auwerx J. Characterization and validation of Cre-driver mouse lines. Curr Protoc Mouse Biol. 2011;1(1):1-15.
14. Dubé 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. 2006;131(2): 589-605.
15. RowlandKJ, Trivedi S, LeeD, WanK, Kulkarni RN, HolzenbergerM, Brubaker PL. Loss of glucagon-like peptide-2-induced proliferation following intestinal epithelial insulin-like growth factor-1-receptor deletion. Gastroenterology. 2011;141(6):2166-2175.
16. Dong CX, Zhao W, Solomon C, Rowland KJ, Ackerley C, Robine S, Holzenberger M, Gonska T, Brubaker PL. The intestinal epithelial insulin-like growth factor-1 receptor links glucagon-like peptide-2 action to gut barrier function. Endocrinology. 2014; 155(2):370-379.
17. Brubaker PL, Izzo A, Hill M, Drucker DJ. Intestinal function in mice with small bowel growth induced by glucagon-like peptide-2. Am J Physiol. 1997;272(6 Pt 1):E1050-E1058.
18. Lundby C, Nordsborg N, Kusuhara K, Kristensen KM, Neufer PD, Pilegaard H. Gene expression in human skeletal muscle: Alternative normalization method and effect of repeated biopsies. Eur J Appl Physiol. 2005;95(4):351-360.
19. Rhinn H, Marchand-Leroux C, Croci N, Plotkine M, Scherman D, Escriou V. Housekeeping while brain's storming validation of normalizing factors for gene expression studies in a murine model of traumatic brain injury. BMC Mol Biol. 2008;9:62.
20. Lenth RV. Least-square means: TheRpackage lsmeans. J Stat Softw. 2016;69(1):1-33.
21. Peña EA, Slate EH. Global validation of linear model assumptions. J Am Stat Assoc. 2006;101(473):341.
22. Jensen SR, Wheeler SE, Hvid H, Schoof EM, Ahnfelt-Ronne J, Kislinger T, Hansen BF, Nishimura E, Olsen GS, Brubaker PL. Quantitative proteomics of mouse intestinal mucosa lacking insulin receptors. Endocrinology. 2017;158(8):2470-2485.
23. Forgue-Lafitte ME, Marescot MR, Chamblier MC, Rosselin G. Evidence for the presence of insulin binding sites in isolated rat intestinal epithelial cells. Diabetologia. 1980;19(4):373-378.
24. Gingerich RL, Gilbert WR, Comens PG, Gavin JR III. Identification and characterization of insulin receptors in basolateral membranes of dog intestinal mucosa. Diabetes. 1987;36(10): 1124-1129.
25. Buts JP, De Keyser N, Marandi S, Maernoudt AS, Sokal EM, Rahier J, Hermans D. Expression of insulin receptors and of 60-kDa receptor substrate in rat mature and immature enterocytes. Am J Physiol. 1997;273(1 Pt 1):G217-G226.
26. Drew JE, Farquharson AJ, Padidar S, Duthie GG, Mercer JG, Arthur JR, Morrice PC, Barrera LN. Insulin, leptin, and adiponectin receptors in colon: Regulation relative to differing body adiposity independent of diet and in response to dimethylhydrazine. Am J Physiol Gastrointest Liver Physiol. 2007;293(4):G682-G691.
27. Ontsouka EC, Philipona C, Hammon HM, Blum JW. Abundance of mRNA encoding for components of the somatotropic axis and insulin receptor in different layers of the jejunum and ileum of neonatal calves. J Anim Sci. 2004;82(11):3181-3188.
28. Pillion DJ, Ganapathy V, Leibach FH. Identification of insulin receptors on the mucosal surface of colon epithelial cells. J Biol Chem. 1985;260(9):5244-5247.
29. Serhan MF, Kreydiyyeh SI. Insulin down-regulates the Na+/K+ ATPase in enterocytes but increases intestinal glucose absorption. Gen Comp Endocrinol. 2010;167(2):228-233.
30. Mäkinen J, Hannukainen JC, Karmi A, Immonen HM, Soinio M, Nelimarkka L, Savisto N, HelmiöM, Ovaska J, Salminen P, Iozzo P, Nuutila P. Obesity-associated intestinal insulin resistance is ameliorated after bariatric surgery. Diabetologia. 2015;58(5): 1055-1062.
31. Honka H, Mäkinen J, Hannukainen JC, Tarkia M, Oikonen V, Teräs M, Fagerholm V, Ishizu T, Saraste A, Stark C, Vähäsilta T, Salminen P, Kirjavainen A, Soinio M, Gastaldelli A, Knuuti J, Iozzo P, Nuutila P. Validation of [18F]fluorodeoxyglucose and positron emission tomography (PET) for the measurement of intestinal metabolism in pigs, and evidence of intestinal insulin resistance in patients with morbid obesity. Diabetologia. 2013;56(4):893-900.
32. Stahl A, Evans JG, Pattel S, Hirsch D, Lodish HF. Insulin causes fatty acid transport protein translocation and enhanced fatty acid uptake in adipocytes. Dev Cell. 2002;2(4):477-488.
33. Stahl A, Hirsch DJ, Gimeno RE, Punreddy S, Ge P, Watson N, Patel S, Kotler M, Raimondi A, Tartaglia LA, Lodish HF. Identification of the major intestinal fatty acid transport protein. Mol Cell. 1999; 4(3):299-308.
34. Shim J, Moulson CL, Newberry EP, Lin MH, Xie Y, Kennedy SM, Miner JH, Davidson NO. Fatty acid transport protein 4 is dispensable for intestinal lipid absorption in mice. J Lipid Res. 2009; 50(3):491-500.
35. Ahn DH, Crawley SC, Hokari R, Kato S, Yang SC, Li JD, Kim YS. TNF-alpha activates MUC2 transcription via NF-kappaB but inhibits via JNK activation. Cell Physiol Biochem. 2005;15(1-4): 29-40.
36. He XC, Zhang J, Tong WG, Tawfik O, Ross J, Scoville DH, Tian Q, Zeng X, He X, Wiedemann LM, Mishina Y, Li L. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet. 2004;36(10):1117-1121.
37. Djiogue S, Nwabo Kamdje AH, Vecchio L, Kipanyula MJ, Farahna M, Aldebasi Y, Seke Etet PF. Insulin resistance and cancer: The role of insulin and IGFs. Endocr Relat Cancer. 2013;20(1):R1-R17.
38. Vigneri PG, Tirrò E, Pennisi MS, Massimino M, Stella S, Romano C, Manzella L. The insulin/IGF system in colorectal cancer development and resistance to therapy. Front Oncol. 2015;5:230.
39. Seely BL, Reichart DR, Takata Y, Yip C, Olefsky JM. A functional assessment of insulin/insulin-like growth factor-I hybrid receptors. Endocrinology. 1995;136(4):1635-1641.
40. Slaaby R. Specific insulin/IGF1 hybrid receptor activation assay reveals IGF1 as a more potent ligand than insulin. Sci Rep. 2015;5: 7911.
41. Brierley GV, Macaulay SL, Forbes BE, Wallace JC, Cosgrove LJ, Macaulay VM. Silencing of the insulin receptor isoform A favors formation of type 1 insulin-like growth factor receptor (IGF-IR) homodimers and enhances ligand-induced IGF-IR activation and viability of human colon carcinoma cells. Endocrinology. 2010; 151(4):1418-1427.
42. Chassaing B, Miles-Brown J, Pellizzon M, Ulman E, Ricci M, Zhang L, Patterson AD, Vijay-Kumar M, Gewirtz AT. Lack of soluble fiber drives diet-induced adiposity in mice. Am J Physiol Gastrointest Liver Physiol. 2015;309(7):G528-G541.
43. Madison BB, Dunbar L, Qiao XT, Braunstein K, Braunstein E, Gumucio DL. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem. 2002;277(36): 33275-33283.