Potential role of skeletal muscle glucose metabolism on the regulation of insulin secretion

Obesity Reviews

Volumn 15, Issue 7, 2014, Pages 587-597

  Mizgier, M L ^a   Casas, M ^b   Contreras Ferrat, A ^b   Llanos, P ^b   Galgani, J E ^a,c  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Beta cell; Glucose flux; Insulin resistance; Myokines

Indexed keywords

FATTY ACID; GLUCOSE; INCRETIN; INSULIN; MUSCLE PROTEIN;

ARTICLE; GLUCOSE METABOLISM; HUMAN; IN VITRO STUDY; INSULIN RELEASE; INSULIN SENSITIVITY; MUSCLE METABOLISM; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN SECRETION; SKELETAL MUSCLE; INSULIN RESISTANCE; METABOLISM; OBESITY; PANCREAS; SECRETION (PROCESS); SIGNAL TRANSDUCTION;

GLUCOSE; HUMANS; INCRETINS; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MUSCLE, SKELETAL; OBESITY; PANCREAS; RECEPTOR CROSS-TALK;

EID: 84903182770     PISSN: 14677881     EISSN: 1467789X     Source Type: Journal    
DOI: 10.1111/obr.12166     Document Type: Article

References (88)

1. Sachdeva MM, Stoffers DA. Minireview: meeting the demand for insulin: molecular mechanisms of adaptive postnatal beta-cell mass expansion. Mol Endocrinol 2009; 23: 747-758.
2. Schaefer JH. The normal weight of the pancreas in the adult human being: a biometric study. Anat Rec 1926; 32: 119-132.
3. Rorsman P, Braun M. Regulation of insulin secretion in human pancreatic islets. Annu Rev Physiol 2013; 75: 155-179.
4. Weyer C, Bogardus C, Mott DM, Pratley RE. The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus. J Clin Invest 1999; 104: 787-794.
5. Duttaroy A, Zimliki CL, Gautam D, Cui Y, Mears D, Wess J. Muscarinic stimulation of pancreatic insulin and glucagon release is abolished in m3 muscarinic acetylcholine receptor-deficient mice. Diabetes 2004; 53: 1714-1720.
6. Winzell MS, Ahrén B. Role of VIP and PACAP in islet function. Peptides 2007; 28: 1805-1813.
7. Hatazawa J, Brooks RA, Di Chiro G, Bacharach SL. Glucose utilization rate versus brain size in humans. Neurology 1987; 37: 583-588.
8. Kolb H, Mandrup-Poulsen T. An immune origin of type 2 diabetes? Diabetologia 2005; 48: 1038-1050.
9. Lin HV, Accili D. Hormonal regulation of hepatic glucose production in health and disease. Cell Metab 2011; 14: 9-19.
10. Porte D Jr. Sympathetic regulation of insulin secretion: its relation to diabetes mellitus. Arch Intern Med 1969; 123: 252-260.
11. Kim J, Wang Z, Heymsfield SB, Baumgartner RN, Gallagher D. Total-body skeletal muscle mass: estimation by a new dual-energy X-ray absorptiometry method. Am J Clin Nutr 2002; 76: 378-383.
12. Baron AD, Brechtel G, Wallace P, Edelman SV. Rates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humans. Am J Physiol 1988; 255: E769-E774.
13. Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006; 444: 840-846.
14. Halperin F, Lopez X, Manning R, Kahn CR, Kulkarni RN, Goldfine AB. Insulin augmentation of glucose-stimulated insulin secretion is impaired in insulin-resistant humans. Diabetes 2012; 61: 301-309.
15. Mari A, Tura A, Natali A etal. Influence of hyperinsulinemia and insulin resistance on in vivo beta-cell function: their role in human beta-cell dysfunction. Diabetes 2011; 60: 3141-3147.
16. De Vos A, Heimberg H, Quartier E etal. Human and rat beta cells differ in glucose transporter but not in glucokinase gene expression. J Clin Invest 1995; 96: 2489-2495.
17. Lynedjian PB, Mobius G, Seitz HJ, Wollheim CB, Renold AE. Tissue-specific expression of glucokinase: identification of the gene product in liver and pancreatic islets. Proc Natl Acad Sci USA 1986; 83: 1998-2001.
18. Matschinsky FM, Glaser B, Magnuson MA. Pancreatic beta-cell glucokinase: closing the gap between theoretical concepts and experimental realities. Diabetes 1998; 47: 307-315.
19. Detimary P, Gilon P, Henquin JC. Interplay between cytoplasmic Ca2+and the ATP/ADP ratio: a feedback control mechanism in mouse pancreatic islets. Biochem J 1998; 333(Pt 2): 269-274.
20. Ashcroft FM, Harrison DE, Ashcroft SJ. Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature 1984; 312: 446-448.
21. Cook DL, Hales CN. Intracellular ATP directly blocks K+ channels in pancreatic B-cells. Nature 1984; 311: 271-273.
22. Deeney JT, Prentki M, Corkey BE. Metabolic control of β-cell function. Semin Cell Dev Biol 2000; 11: 267-275.
23. Gonzalez A, Merino B, Marroquí L etal. Insulin hypersecretion in islets from diet-induced hyperinsulinemic obese female mice is associated with several functional adaptations in individual β-cells. Endocrinology 2013; 154: 3515-3524.
24. Mari A, Ferrannini E. β-Cell function assessment from modelling of oral tests: an effective approach. Diabetes Obes Metab 2008; 10: 77-87.
25. Itoh Y, Kawamata Y, Harada M etal. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 2003; 422: 173-176.
26. Stein DT, Stevenson BE, Chester MW etal. The insulinotropic potency of fatty acids is influenced profoundly by their chain length and degree of saturation. J Clin Invest 1997; 100: 398-403.
27. Nagasumi K, Esaki R, Iwachidow K etal. Overexpression of GPR40 in pancreatic beta-cells augments glucose-stimulated insulin secretion and improves glucose tolerance in normal and diabetic mice. Diabetes 2009; 58: 1067-1076.
28. Karpe F, Dickmann JR, Frayn KN. Fatty acids, obesity, and insulin resistance: time for a reevaluation. Diabetes 2011; 60: 2441-2449.
29. Kelley DE, Williams KV, Price JC, McKolanis TM, Goodpaster BH, Thaete FL. Plasma fatty acids, adiposity, and variance of skeletal muscle insulin resistance in type 2 diabetes mellitus. J Clin Endocrinol Metab 2001; 86: 5412-5419.
30. Poynten AM, Gan SK, Kriketos AD, Campbell LV, Chisholm DJ. Circulating fatty acids, non-high density lipoprotein cholesterol, and insulin-infused fat oxidation acutely influence whole body insulin sensitivity in nondiabetic men. The J Clin Endocrinol Metab 2005; 90: 1035-1040.
31. Galgani JE, Heilbronn LK, Azuma K etal. Metabolic flexibility in response to glucose is not impaired in people with type 2 diabetes after controlling for glucose disposal rate. Diabetes 2008; 57: 841-845.
32. McQuaid SE, Hodson L, Neville MJ etal. Downregulation of adipose tissue fatty acid trafficking in obesity: a driver for ectopic fat deposition? Diabetes 2011; 60: 47-55.
33. Drucker DJ. Incretin action in the pancreas: potential promise, possible perils, and pathological pitfalls. Diabetes 2013; 62: 3316-3323.
34. Tillil H, Shapiro ET, Miller MA etal. Dose-dependent effects of oral and intravenous glucose on insulin secretion and clearance in normal humans. Am J Physiol 1988; 254: E349-E357.
35. McCullough AJ, Miller LJ, Service FJ, Go VLW. Effect of graded intraduodenal glucose infusions on the release and physiological action of gastric inhibitory polypeptide. J Clin Endocrinol Metab 1983; 56: 234-241.
36. Verdich C, Toubro S, Buemann B, Lysgard Madsen J, Juul Holst J, Astrup A. The role of postprandial releases of insulin and incretin hormones in meal-induced satiety - effect of obesity and weight reduction. Int J Obes Relat Metab Disord 2001; 25: 1206-1214.
37. Nauck MA, Vardarli I, Deacon CF, Holst JJ, Meier JJ. Secretion of glucagon-like peptide-1 (GLP-1) in type 2 diabetes: what is up, what is down? Diabetologia 2011; 54: 10-18.
38. Muscelli E, Mari A, Casolaro A etal. Separate impact of obesity and glucose tolerance on the incretin effect in normal subjects and type 2 diabetic patients. Diabetes 2008; 57: 1340-1348.
39. Bouche C, Lopez X, Fleischman A etal. Insulin enhances glucose-stimulated insulin secretion in healthy humans. Proc Natl Acad Sci USA 2010; 107: 4770-4775.
40. Borelli MI, Francini F, Gagliardino JJ. Autocrine regulation of glucose metabolism in pancreatic islets. Am J Physiol Endocrinol Metab 2003; 286: E111-E115.
41. Aspinwall CA, Lakey JR, Kennedy RT. Insulin-stimulated insulin secretion in single pancreatic beta cells. J Biol Chem 1999; 274: 6360-6365.
42. Kulkarni RN, Brüning JC, Winnay JN, Postic C, Magnuson MA, Kahn CR. Tissue-specific knockout of the insulin receptor in pancreatic beta cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell 1999; 96: 329-339.
43. Gunton JE, Kulkarni RN, Yim S etal. Loss of ARNT/HIF1beta mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes. Cell 2005; 122: 337-349.
44. Rhodes CJ, White MF, Leahy JL, Kahn SE. Direct autocrine action of insulin on β-cells: does it make physiological sense? Diabetes 2013; 62: 2157-2163.
45. Trayhurn P, Drevon CA, Eckel J. Secreted proteins from adipose tissue and skeletal muscle - adipokines, myokines and adipose/muscle cross-talk. Arch Physiol Biochem 2011; 117: 47-56.
46. Pedersen BK. Muscle as a secretory organ. Compr Physiol 2013; 3: 1337-1362.
47. Galgani JE, de Jonge L, Rood JC, Smith SR, Young AA, Ravussin E. Urinary C-peptide excretion: a novel alternate measure of insulin sensitivity in physiological conditions. Obesity (Silver Spring) 2010; 18: 1852-1857.
48. Galgani JE, Moro C, Ravussin E. Metabolic flexibility and insulin resistance. Am J Physiol Endocrinol Metab 2008; 295: E1009-E1017.
49. Galgani JE, Ravussin E. Postprandial whole-body glycolysis is similar in insulin-resistant and insulin-sensitive non-diabetic humans. Diabetologia 2012; 55: 737-742.
50. Stull AJ, Galgani JE, Johnson WD, Cefalu WT. The contribution of race and diabetes status to metabolic flexibility in humans. Metabolism 2010; 59: 1358-1364.
51. Kelley DE, Mandarino LJ. Fuel selection in human skeletal muscle in insulin resistance: a reexamination. Diabetes 2000; 49: 677-683.
52. Ferrannini E, Bjorkman O, Reichard GA Jr etal. The disposal of an oral glucose load in healthy subjects. A quantitative study. Diabetes 1985; 34: 580-588.
53. Hartwig S, Raschke S, Knebel B etal. Secretome profiling of primary human skeletal muscle cells. Biochim Biophys Acta 2013; doi: 10.1016/j.bbapap.2013.08.004.
54. Lee SJ. Regulation of muscle mass by myostatin. Annu Rev Cell Dev Biol 2004; 20: 61-86.
55. Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 2008; 88: 1379-1406.
56. Huang Z, Chen X, Chen D. Myostatin: a novel insight into its role in metabolism, signal pathways, and expression regulation. Cell Signal 2011; 23: 1441-1446.
57. Carey AL, Steinberg GR, Macaulay SL etal. Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes 2006; 55: 2688-2697.
58. Bortoluzzi S, Scannapieco P, Cestaro A, Danieli GA, Schiaffino S. Computational reconstruction of the human skeletal muscle secretome. Proteins 2006; 62: 776-792.
59. Bostrom P, Wu J, Jedrychowski MP etal. A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 2012; 481: 463-468.
60. Bouzakri K, Plomgaard P, Berney T, Donath MY, Pedersen BK, Halban PA. Bimodal effect on pancreatic beta-cells of secretory products from normal or insulin-resistant human skeletal muscle. Diabetes 2011; 60: 1111-1121.
61. Ellingsgaard H, Hauselmann I, Schuler B etal. Interleukin-6 enhances insulin secretion by increasing glucagon-like peptide-1 secretion from L cells and alpha cells. Nat Med 2011; 17: 1481-1489.
62. Handschin C, Choi CS, Chin S etal. Abnormal glucose homeostasis in skeletal muscle-specific PGC-1alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk. J Clin Invest 2007; 117: 3463-3474.
63. Andreozzi F, Laratta E, Cardellini M etal. Plasma interleukin-6 levels are independently associated with insulin secretion in a cohort of Italian-Caucasian nondiabetic subjects. Diabetes 2006; 55: 2021-2024.
64. Kim HJ, Higashimori T, Park SY etal. Differential effects of interleukin-6 and -10 on skeletal muscle and liver insulin action in vivo. Diabetes 2004; 53: 1060-1067.
65. Tsigos C, Papanicolaou DA, Kyrou I, Defensor R, Mitsiadis CS, Chrousos GP. Dose-dependent effects of recombinant human interleukin-6 on glucose regulation. J Clin Endocrinol Metab 1997; 82: 4167-4170.
66. van Hall G, Steensberg A, Sacchetti M etal. Interleukin-6 stimulates lipolysis and fat oxidation in humans. J Clin Endocrinol Metab 2003; 88: 3005-3010.
67. Ellingsgaard H, Ehses JA, Hammar EB etal. Interleukin-6 regulates pancreatic alpha-cell mass expansion. Proc Natl Acad Sci USA 2008; 105: 13163-13168.
68. Franckhauser S, Elias I, Rotter Sopasakis V etal. Overexpression of Il6 leads to hyperinsulinaemia, liver inflammation and reduced body weight in mice. Diabetologia 2008; 51: 1306-1316.
69. Eizirik DL, Sandler S, Welsh N etal. Cytokines suppress human islet function irrespective of their effects on nitric oxide generation. J Clin Invest 1994; 93: 1968-1974.
70. Sandler S, Bendtzen K, Eizirik DL, Welsh M. Interleukin-6 affects insulin secretion and glucose metabolism of rat pancreatic islets in vitro. Endocrinology 1990; 126: 1288-1294.
71. Southern C, Schulster D, Green IC. Inhibition of insulin secretion from rat islets of Langerhans by interleukin-6. An effect distinct from that of interleukin-1. Biochem J 1990; 272: 243-245.
72. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol 1979; 237: E214-E223.
73. Woerle HJ, Szoke E, Meyer C etal. Mechanisms for abnormal postprandial glucose metabolism in type 2 diabetes. Am J Physiol Endocrinol Metab 2005; 290: E67-E77.
74. Hirner S, Krohne C, Schuster A etal. MuRF1-dependent regulation of systemic carbohydrate metabolism as revealed from transgenic mouse studies. J Mol Biol 2008; 379: 666-677.
75. Kim JK, Michael MD, Previs SF etal. Redistribution of substrates to adipose tissue promotes obesity in mice with selective insulin resistance in muscle. J Clin Invest 2000; 105: 1791-1797.
76. Brüning JC, Michael MD, Winnay JN etal. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 1998; 2: 559-569.
77. Mauvais-Jarvis F, Virkamaki A, Michael MD etal. A model to explore the interaction between muscle insulin resistance and beta-cell dysfunction in the development of type 2 diabetes. Diabetes 2000; 49: 2126-2134.
78. Tsuchiya M, Manabe Y, Yamada K, Furuichi Y, Hosaka M, Fujii NL. Chronic exercise enhances insulin secretion ability of pancreatic islets without change in insulin content in non-diabetic rats. Biochem Biophys Res Commun 2013; 430: 676-682.
79. de Carvalho Leite N, Ferreira TR, Rickli S etal. Glycolytic and mitochondrial metabolism in pancreatic islets from MSG-treated obese rats subjected to swimming training. Cell Physiol Biochem 2013; 31: 242-256.
80. Gomes RM, Tófolo LP, Rinaldi W etal. Moderate exercise restores pancreatic beta-cell function and autonomic nervous system activity in obese rats induced by high-fat diet. Cell Physiol Biochem 2013; 32: 310-321.
81. Almeida FN, Proença ARG, Chimin P, Marçal AC, Bessa-Lima F, Carvalho CRO. Physical exercise and pancreatic islets: acute and chronic actions on insulin secretion. Islets 2012; 4: 296-301.
82. Oliveira CA, Paiva MF, Mota CA etal. Exercise at anaerobic threshold intensity and insulin secretion by isolated pancreatic islets of rats. Islets 2010; 2: 240-246.
83. Anderwald C, Tura A, Grassi A etal. Insulin infusion during normoglycemia modulates insulin secretion according to whole-body insulin sensitivity. Diabetes Care 2011; 34: 437-441.
84. Francini F, Gagliardino JJ, Borelli MI. Decreased islet sensitivity to insulin in hamsters with dietary-induced insulin resistance. Life Sci 2008; 82: 817-822.
85. Dela F, von Linstow ME, Mikines KJ, Galbo H. Physical training may enhance β-cell function in type 2 diabetes. Am J Physiol Endocrinol Metab 2004; 287: E1024-E1031.
86. Malin SK, Solomon TPJ, Blaszczak A, Finnegan S, Filion J, Kirwan JP. Pancreatic β-cell function increases in a linear dose-response manner following exercise training in adults with prediabetes. Am J Physiol Endocrinol Metab 2013; 305: E1248-E1254.
87. Herman MA, Kahn BB. Glucose transport and sensing in the maintenance of glucose homeostasis and metabolic harmony. J Clin Invest 2006; 116: 1767-1775.
88. Bonuccelli S, Muscelli E, Gastaldelli A etal. Improved tolerance to sequential glucose loading (Staub-Traugott effect): size and mechanisms. Am J Physiol Endocrinol Metab 2009; 297: E532-E537.