Jejunal Proteins Secreted by db/db Mice or Insulin-Resistant Humans Impair the Insulin Signaling and Determine Insulin Resistance

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Salinari, Serenella ^a   Debard, Cyrille ^b   Bertuzzi, Alessandro ^c   Durand, Christine ^b   Zimmet, Paul ^d   Vidal, Hubert ^b   Mingrone, Geltrude ^e  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITÉ LYON 1   (France)

^c CNR   (Italy)

^d BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^e CATHOLIC UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN; JEJUNAL PROTEIN; PROTEIN; PROTEIN SERINE THREONINE KINASE; RAPAMYCIN; THREONINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DUODENUM; FEMALE; GLUCOSE TRANSPORT; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; JEJUNUM; MALE; MOUSE; MUSCLE FIBRIL; MYOBLAST; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN SECRETION; SOLEUS MUSCLE;

ADULT; ANIMALS; CELL DIFFERENTIATION; CULTURE MEDIA, CONDITIONED; DEOXYGLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INSULIN; INSULIN RESISTANCE; JEJUNUM; MICE; MICE, INBRED C57BL; MUSCLE FIBERS, SKELETAL; PHOSPHORYLATION; PHOSPHOSERINE; PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION;

EID: 84874244844     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056258     Document Type: Article

References (50)

1. DeFronzo RA, (2004) Pathogenesis of type 2 diabetes mellitus. Med Clin N Am 88: 787-835.
2. Kasuga M, (2006) Insulin resistance and pancreatic β cell failure. J Clin Invest 116: 1756-1760.
3. Prentki M, Nolan CJ, (2006) Islet β cell failure in type 2 diabetes. J Clin Invest 116: 1802-1812.
4. Guidone C, Manco M, Valera Mora E, Iaconelli A, Gniuli D, et al. (2006) Mechanisms of recovery from type 2 diabetes after malabsorptive bariatric surgery. Diabetes 55: 2025-2031.
5. Mingrone G, Panunzi S, De Gaetano A, Guidone C, Iaconelli A, et al. (2012) Bariatric surgery vs. conventional medical therapy for type 2 diabetes. New Engl J Med 336: 1577-1585.
6. Mari A, Manco M, Guidone C, Nanni G, Castagneto M, et al. (2006) Restoration of normal glucose tolerance in severely obese patients after bilio-pancreatic diversion: role of insulin sensitivity and beta cell function. Diabetologia 49: 2136-2143.
7. Salinari S, Bertuzzi A, Asnaghi S, Guidone C, Manco M, et al. (2009) First-phase insulin secretion restoration and differential response to glucose load depending on the route of administration in type 2 diabetic subjects after bariatric surgery. Diabetes Care 32: 375-380.
8. Rubino F, Marescaux J, (2004) Effect of duodenal-jejunal exclusion in a non-obese animal model of type 2 diabetes: a new perspective for an old disease. Ann Surg 239: 1-11.
9. Rubino F, Forgione A, Cummings DE, Vix M, Gnuli D, et al. (2006) The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg 244: 741-749.
10. Breen DM, Rasmussen BA, Kokorovic A, Wang R, Cheung GW, et al. (2012) Jejunal nutrient sensing is required for duodenal-jejunal bypass surgery to rapidly lower glucose concentrations in uncontrolled diabetes. Nature Med 18: 950-955.
11. Hummel KP, Dickie MM, Coleman DL, (1966) Diabetes, a new mutation in the mouse. Science 153: 1127-1128.
12. Kodama H, Fujita M, Yamaguchi I, (1994) Development of hyperglycaemia and insulin resistance in conscious genetically diabetic (C57BL/KsJ-db/db) mice. Diabetologia 37: 739-744.
13. Brozinick JT Jr, McCoid SC, Reynolds TH, Nardone NA, Hargrove DM, et al. (2001) GLUT4 over-expression in db/db mice dose-dependently ameliorates diabetes but is not a lifelong cure. Diabetes 50: 593-600.
14. Russell MS, Bailey J, Duffy SJ, Vogels CM, Broderick TL, et al. (2006) Gut transport of a molybdenum/ascorbic acid complex. Drugs R D 7: 111-117.
15. Bergman RN, Ider YZ, Bowden CR, Cobelli C, (1979) Quantitative estimation of insulin sensitivity. Am J Physiol 236: E667-E677.
16. Pacini G, Thomaseth K, Ahrén B, (2001) Contribution to glucose tolerance of insulin-independent vs. insulin-dependent mechanisms in mice. Am J Physiol Endocrinol Metab 281: E693-E703.
17. Sheiner LB, Beal SL, (1980) Evaluation of methods for estimating population pharmacokinetics parameters. I. Michaelis-Menten model: routine clinical pharmacokinetic data. J Pharmacokinet Biopharm 8: 553-571.
18. Burcelin R, Crivelli V, Dacosta A, Roy-Tirelli A, Thorens B, (2002) Heterogeneous metabolic adaptation of C57BL/6J mice to high-fat diet. Am J Physiol Endocrinol Metab 282: E834-E842.
19. Ueyama A, Yaworsky KL, Wang Q, Ebina Y, Klip A, (1999) GLUT-4myc ectopic expression in L6 myoblasts generates a GLUT-4-specific pool conferring insulin sensitivity. Am J Physiol Endocrinol Metab 277: E572-E578.
20. Koivisto UM, Martinez-Valdez H, Bilan PJ, Burdett E, Ramlal P, et al. (1991) Differential regulation of the GLUT-1 and GLUT-4 glucose transport systems by glucose and insulin in L6 muscle cells in culture. J Biol Chem 266: 2615-2621.
21. Cozzone D, Fröjdö S, Disse E, Debard C, Laville M, et al. (2008) Isoform-specific defects of insulin stimulation of Akt/protein kinase B (PKB) in skeletal muscle cells from type 2 diabetic patients. Diabetologia 51: 512-521.
22. DeFronzo RA, Tobin JD, Andres R, (1979) Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol 237: E214-E223.
23. Bouzakri K, Roques M, Gual P, Espinosa S, Guebre-Egziabher F, et al. (2003) Reduced activation of phosphatidylinositol-3 kinase and increased serine 636 phosphorylation of insulin receptor substrate-1 in primary culture of skeletal muscle cells from patients with type 2 diabetes. Diabetes 52: 1319-1325.
24. Montori-Grau M, Guitart M, Lerin C, Andreu AL, Newgard CB, et al. (2007) Expression and glycogenic effect of glycogen-targeting protein phosphatase I regulatory subunit GL in cultured human muscle. Biochem J 405: 107-113.
25. Schauer PR, Kashyap SR, Wolski K, Brethauer SA, Kirwan JP, et al. (2012) Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med 366: 1567-1576.
26. Capristo E, Mingrone G, Addolorato G, Greco AV, Gasbarrini G, (1998) Metabolic features of inflammatory bowel disease in a remission phase of the disease activity. J Intern Med 243: 339-347.
27. Sarbassov DD, Ali SM, Sabatini D M, (2005) Growing roles for the mTOR pathway. Curr Opin Cell Biol 17: 596-603.
28. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, et al. (1997) Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol 7: 261-269.
29. Stephens L, Anderson K, Stokoe D, Erdjument-Bromage H, Painter GF, et al. (1998) Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science. 279: 710-714.
30. Fraenkel M, Ketzinel-Gilad M, Ariav Y, Pappo O, Karaca M, et al. (2008) mTOR inhibition by rapamycin prevents beta-cell adaptation to hyperglycemia and exacerbates the metabolic state in type 2 diabetes. Diabetes 57: 945-957.
31. Li J, DeFea K, Roth RA, (1999) Modulation of insulin receptor substrate-1 tyrosine phosphorylation by an Akt/phosphatidylinositol 3-kinase pathway. J Biol Chem 274: 9351-9356.
32. Frame S, Cohen P, (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359: 1-16.
33. Goñi-Oliver P, Lucas JJ, Avila J, Hernandez F, (2007) N-terminal cleavage of GSK-3 by calpain. A new form of GSK-3 regulation. J Biol Chem 282: 22406-22413.
34. Cross DAE, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA, (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature. 378: 785-789.
35. McManus EJ, Sakamoto K, Armit LJ, Ronaldson L, Shapiro N, et al. (2005) Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knockin analysis. EMBO J 24: 1571-1583.
36. Eldar-Finkelman H, Krebs EG, (1997) Phosphorylation of insulin receptor substrate 1 by glycogen synthase kinase 3 impairs insulin action. Proc Natl Acad Sci U S A 94: 9660-9664.
37. Liberman Z, Eldar-Finkelman H, (2005) Serine 332 phosphorylation of insulin receptor substrate-1 by glycogen synthase kinase-3 attenuates insulin signaling. J Biol Chem 280: 4422-4428.
38. Wang QM, Fiol CJ, DePaoli RAA, Roach PJ, (1994) Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J Biol Chem 269: 14566-14574.
39. Eldar-Finkelman H, Schreyer SA, Shinohara MM, LeBoeuf RC, Krebs EG, (1999) Increased glycogen synthase kinase-3 activity in diabetes- and obesity-prone C57BL/6J mice. Diabetes 48: 1662-1666.
40. Dokken BB, Sloniger JA, Henriksen EJ, (2005) Acute selective glycogen synthase kinase-3 inhibition enhances insulin signaling in pre-diabetic insulin-resistant rat skeletal muscle. Am J Physiol Endocrinol Metab 288: E1188-E1194.
41. Wente SR, Villalba M, Schramm VL, Rosen OM, (1990) Mn2(+)-binding properties of a recombinant protein-tyrosine kinase derived from the human insulin receptor. Proc Natl Acad Sci U S A 87: 2805-2809.
42. Ciaraldi TP, Nikoulina SE, Bandukwala SA, Carter L, Henry RR, (2007) Role of glycogen synthase kinase-3 alpha in insulin action in cultured human skeletal muscle cells. Endocrinology 148: 4393-4399.
43. Ring DB, Johnson KW, Henriksen EJ, Nuss JM, Goff D, et al. (2003) Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 52: 588-595.
44. Mora A, Sakamoto K, McManus EJ, Alessi DR, (2005) Role of the PDK1-PKB-GSK3 pathway in regulating glycogen synthase and glucose uptake in the heart. FEBS Lett 579: 3632-3638.
45. Hay N, Sonenberg N, (2004) Upstream and downstream of mTOR. Genes Dev 18: 1926-1945.
46. Feldman ME, Apsel B, Uotila A, Loewith R, Knight ZA, et al. (2009) Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol 7(2): e38.
47. Huang J, Dibble CC, Matsuzaki M, Manning BD, (2008) The TSC1-TSC2 complex is required for proper activation of mTOR complex 2. Mol Cell Biol 28: 4104-4115.
48. Huang J, Manning BD, (2009) A complex interplay between Akt, TSC2 and the two mTOR complexes. Biochem Soc Trans 37: 217-222.
49. Cybulski N, Hall MN, (2009) TOR complex 2: a signaling pathway of its own. Trends Biochem Sci 34: 620-627.
50. Dixon JB, le Roux CW, Rubino F, Zimmet P, (2012) Bariatric surgery for type 2 diabetes. Lancet 379: 2300-2311.