Insulin resistance: An adaptive mechanism becomes maladaptive in the current environment - An evolutionary perspective

Metabolism: Clinical and Experimental

Volumn 62, Issue 5, 2013, Pages 622-633

  Tsatsoulis, Agathocles ^a   Mantzaris, Michalis D ^b   Bellou, Sofia ^c   Andrikoula, Maria ^a  

^a UNIVERSITY OF IOANNINA   (Greece)

^b UNIVERSITY OF IOANNINA   (Greece)

^c INSTITUTE OF COMPUTER SCIENCE   (Greece)

Author keywords

Central obesity; Low grade inflammation; Metabolic syndrome; Selfish brain; Type 2 diabetes

Indexed keywords

CYTOKINE; STRESS HORMONE;

ADIPOSE TISSUE; BODY FAT DISTRIBUTION; CALORIC INTAKE; CHRONIC STRESS; HUMAN; IMMUNE RESPONSE; INFLAMMATION; INSULIN RESISTANCE; LIPID STORAGE; METABOLIC SYNDROME X; MUSCLE CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN METABOLISM; REVIEW; TARGET ORGAN;

ADAPTATION, PHYSIOLOGICAL; ADIPOSE TISSUE; ANIMALS; BIOLOGICAL EVOLUTION; ENVIRONMENT; GENE-ENVIRONMENT INTERACTION; HUMANS; INSULIN RESISTANCE; MODELS, BIOLOGICAL; STRESS, PHYSIOLOGICAL;

EID: 84876673360     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2012.11.004     Document Type: Review

References (113)

1. J.P. Despres, I. Lemieux, and J. Bergeron Abdominal obesity and the metabolic syndrome: contribution to global cardiometabolic risk Arterioscler Thromb Vasc Biol 28 6 2008 1039 1049
2. G.M. Reaven The metabolic syndrome: time to get off the merry-go-round? J Intern Med 269 2 2011 127 136
3. C.H. Mandavia, L. Pulakat, and V. Demarco Over-nutrition and metabolic cardiomyopathy Metabolism 61 9 2012 1205 1210
4. E.A. Gale The myth of the metabolic syndrome Diabetologia 48 9 2005 1679 1683 (Pubitemid 41317820)
5. R. Kahn, J. Buse, and E. Ferrannini The metabolic syndrome: time for a critical appraisal: joint statement from the American Diabetes Association and the European Association for the Study of Diabetes Diabetes Care 28 9 2005 2289 2304 (Pubitemid 41242486)
6. R.K. Simmons, K.G. Alberti, and E.A. Gale The metabolic syndrome: useful concept or clinical tool? Report of a WHO Expert Consultation Diabetologia 53 4 2010 600 605
7. S.M. Grundy Metabolic syndrome: connecting and reconciling cardiovascular and diabetes worlds J Am Coll Cardiol 47 6 2006 1093 1100
8. R.H. Unger, and P.E. Scherer Gluttony, sloth and the metabolic syndrome: A roadmap to lipotoxicity Trends Endocrinol Metab 21 6 2010 345 352
9. J.P. Despres, and I. Lemieux Abdominal obesity and metabolic syndrome Nature 444 7121 2006 881 887 (Pubitemid 46024995)
10. B.S. McEwen Protective and damaging effects of stress mediators N Engl J Med 338 3 1998 171 179
11. G.F. Cahill Jr., and O.E. Owen Starvation and survival Trans Am Clin Climatol Assoc 79 13-20 1968
12. B.R. Levin, M. Lipsitch, and S. Bonhoeffer Population biology, evolution, and infectious disease: convergence and synthesis Science 283 5403 1999 806 809
13. E. Esteve, W. Ricart, and J.M. Fernandez-Real Dyslipidemia and inflammation: An evolutionary conserved mechanism Clin Nutr 24 1 2005 16 31
14. M.G. Ziegler, H. Elayan, and M. Milic Epinephrine and the metabolic syndrome Curr Hypertens Rep 14 1 2012 1 7
15. E. Barth, G. Albuszies, and K. Baumgart Glucose metabolism and catecholamines Crit Care Med 35 Suppl. 9 2007 S508 S518
16. A.R. Saltiel, and C.R. Kahn Insulin signalling and the regulation of glucose and lipid metabolism Nature 414 6865 2001 799 806 (Pubitemid 34000783)
17. G.J. Taborsky Jr. The physiology of glucagon J Diabetes Sci Technol 4 6 2010 1338 1344
18. J.M. Fernandez-Real, and J.C. Pickup Innate immunity, insulin resistance and type 2 diabetes Diabetologia 55 2 2012 273 278
19. A.R. Saltiel, and J.E. Pessin Insulin signaling pathways in time and space Trends Cell Biol 12 2 2002 65 71 (Pubitemid 34146521)
20. C.M. Taniguchi, B. Emanuelli, and C.R. Kahn Critical nodes in signalling pathways: Insights into insulin action Nat Rev Mol Cell Biol 7 2 2006 85 96 (Pubitemid 43278292)
21. K.N. Aronis, and C.S. Mantzoros A brief history of insulin resistance: from the first insulin radioimmunoassay to selectively targeting protein kinase C pathways Metabolism 61 4 2012 445 449
22. S. Schenk, M. Saberi, and J.M. Olefsky Insulin sensitivity: modulation by nutrients and inflammation J Clin Invest 118 9 2008 2992 3002
23. R.H. Medema, A.M. de Vries-Smits, and G.C. van der Zon Ras activation by insulin and epidermal growth factor through enhanced exchange of guanine nucleotides on p21ras Mol Cell Biol 13 1 1993 155 162 (Pubitemid 23006893)
24. M. Goalstone, K. Carel, and J.W. Leitner Insulin stimulates the phosphorylation and activity of farnesyltransferase via the Ras-mitogen- activated protein kinase pathway Endocrinology 138 12 1997 5119 5124 (Pubitemid 27509668)
25. M.H. Vendelbo, B.F. Clasen, and J.T. Treebak Insulin resistance after a 72-h fast is associated with impaired AS160 phosphorylation and accumulation of lipid and glycogen in human skeletal muscle Am J Physiol Endocrinol Metab 302 2 2012 E190 E200
26. A.H. Mulder, C.J. Tack, and A.J. Olthaar Adrenergic receptor stimulation attenuates insulin-stimulated glucose uptake in 3T3-L1 adipocytes by inhibiting GLUT4 translocation Am J Physiol Endocrinol Metab 289 4 2005 E627 E633
27. D. Haig Genetic conflicts in human pregnancy Q Rev Biol 68 4 1993 495 532 (Pubitemid 2031412)
28. A.R. Saltiel Putting the brakes on insulin signaling N Engl J Med 349 26 2003 2560 2562 (Pubitemid 38010085)
29. P. Gual, Y. Le Marchand-Brustel, and J.F. Tanti Positive and negative regulation of insulin signaling through IRS-1 phosphorylation Biochimie 87 1 2005 99 109 (Pubitemid 40298772)
30. M.F. Gregor, and G.S. Hotamisligil Inflammatory mechanisms in obesity Annu Rev Immunol 29 2011 415 445
31. L. Pirola, A.M. Johnston, and E. Van Obberghen Modulation of insulin action Diabetologia 47 2 2004 170 184 (Pubitemid 38315353)
32. Y. Zick Ser/Thr phosphorylation of IRS proteins: A molecular basis for insulin resistance Sci STKE 268 2005 e4
33. M.A. Cornier, D.H. Bessesen, and I. Gurevich Nutritional upregulation of p85alpha expression is an early molecular manifestation of insulin resistance Diabetologia 49 4 2006 748 754 (Pubitemid 43357550)
34. B. Draznin Mitogenic action of insulin: friend, foe or 'frenemy'? Diabetologia 53 2 2010 229 233
35. E. Armstrong Relative brain size and metabolism in mammals Science 220 4603 1983 1302 1304 (Pubitemid 13104196)
36. A. Peters, U. Schweiger, and L. Pellerin The selfish brain: competition for energy resources Neurosci Biobehav Rev 28 2 2004 143 180 (Pubitemid 38692362)
37. P.L. Madsen, S.G. Hasselbalch, and L.P. Hagemann Persistent resetting of the cerebral oxygen/glucose uptake ratio by brain activation: evidence obtained with the Kety-Schmidt technique J Cereb Blood Flow Metab 15 3 1995 485 491
38. A. Peters The selfish brain: competition for energy resources Am J Hum Biol 23 1 2011 29 34
39. B. Thorens, and M. Mueckler Glucose transporters in the 21st Century Am J Physiol Endocrinol Metab 298 2 2010 E141 E145
40. W.R. Leonard, M.L. Robertson, and J.J. Snodgrass Metabolic correlates of hominid brain evolution Comp Biochem Physiol A Mol Integr Physiol 136 1 2003 5 15 (Pubitemid 37289402)
41. A. Peters, B. Kubera, and C. Hubold The selfish brain: stress and eating behavior Front Neurosci 5 2011 74
42. B. Thorens Brain glucose sensing and neural regulation of insulin and glucagon secretion Diabetes Obes Metab 13 Suppl 1 2011 82 88
43. J.V. Neel The thrifty genotype in 1998 Nutr Rev 57 5 Pt 2 1999 S2 S9
44. P. Trayhurn Endocrine and signalling role of adipose tissue: new perspectives on fat Acta Physiol Scand 184 4 2005 285 293 (Pubitemid 41039735)
45. K.N. Frayn, F. Karpe, and B.A. Fielding Integrative physiology of human adipose tissue Int J Obes Relat Metab Disord 27 8 2003 875 888 (Pubitemid 36918608)
46. R.S. Ahima, and J.S. Flier Adipose tissue as an endocrine organ Trends Endocrinol Metab 11 8 2000 327 332
47. P.J. Havel Update on adipocyte hormones: regulation of energy balance and carbohydrate/lipid metabolism Diabetes 53 Suppl 1 2004 S143 S151
48. Y.H. Lee, F. Magkos, and C.S. Mantzoros Effects of leptin and adiponectin on pancreatic beta-cell function Metabolism 60 12 2011 1664 1672
49. L. Gautron, and J.K. Elmquist Sixteen years and counting: An update on leptin in energy balance J Clin Invest 121 6 2011 2087 2093
50. J.E. Schaffer Lipotoxicity: when tissues overeat Curr Opin Lipidol 14 3 2003 281 287 (Pubitemid 36688207)
51. E.A. Sims, E. Danforth Jr., and E.S. Horton Endocrine and metabolic effects of experimental obesity in man Recent Prog Horm Res 29 1973 457 496
52. A. Garg, and A. Misra Lipodystrophies: rare disorders causing metabolic syndrome Endocrinol Metab Clin North Am 33 2 2004 305 331 (Pubitemid 38680632)
53. D.E. Moller, and K.D. Kaufman Metabolic syndrome: A clinical and molecular perspective Annu Rev Med 56 2005 45 62 (Pubitemid 40299773)
54. L.K. Heilbronn, S.K. Gan, and N. Turner Markers of mitochondrial biogenesis and metabolism are lower in overweight and obese insulin-resistant subjects J Clin Endocrinol Metab 92 4 2007 1467 1473 (Pubitemid 46556427)
55. B.M. Kaess, A. Pedley, and J.M. Massaro The ratio of visceral to subcutaneous fat, a metric of body fat distribution, is a unique correlate of cardiometabolic risk Diabetologia 55 10 2012 2622 2630
56. B.L. Wajchenberg, M. Nery, and M.R. Cunha Adipose tissue at the crossroads in the development of the metabolic syndrome, inflammation and atherosclerosis Arq Bras Endocrinol Metabol 53 2 2009 145 150
57. A.M. Goss, and B.A. Gower Insulin sensitivity is associated with thigh adipose tissue distribution in healthy postmenopausal women Metabolism 2012 10.1016/j.metabol.2012.05.016
58. A. Tchernof Sex differences in energy balance, body composition and body fat distribution A. Tsatsoulis, J. Wyckoff, F.M. Brown, Diabetes in women: pathophysiology and therapy 2009 Human Press New York 1 24
59. C.T. Montague, and S. O'Rahilly The perils of portliness: causes and consequences of visceral adiposity Diabetes 49 6 2000 883 888 (Pubitemid 30349408)
60. P. Mauriege, M. Brochu, and D. Prud'homme Is visceral adiposity a significant correlate of subcutaneous adipose cell lipolysis in men? J Clin Endocrinol Metab 84 2 1999 736 742 (Pubitemid 29075714)
61. M. Bluher Adipose tissue dysfunction in obesity Exp Clin Endocrinol Diabetes 117 6 2009 241 250
62. T. Skurk, C. Alberti-Huber, and C. Herder Relationship between adipocyte size and adipokine expression and secretion J Clin Endocrinol Metab 92 3 2007 1023 1033 (Pubitemid 46465679)
63. C.N. Lumeng, J.L. Bodzin, and A.R. Saltiel Obesity induces a phenotypic switch in adipose tissue macrophage polarization J Clin Invest 117 1 2007 175 184 (Pubitemid 46048464)
64. P. Trayhurn Adipose tissue in obesity - an inflammatory issue Endocrinology 146 3 2005 1003 1005 (Pubitemid 40289287)
65. S. Virtue, and A. Vidal-Puig It's not how fat you are, it's what you do with it that counts PLoS Biol 6 9 2008 E237
66. D.G. Hardie, and D.A. Pan Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase Biochem Soc Trans 30 Pt 6 2002 1064 1070 (Pubitemid 36002407)
67. J.A. Chavez, and S.A. Summers Lipid oversupply, selective insulin resistance, and lipotoxicity: molecular mechanisms Biochim Biophys Acta 1801 3 2010 252 265
68. S.I. Itani, N.B. Ruderman, and F. Schmieder Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha Diabetes 51 7 2002 2005 2011 (Pubitemid 34729001)
69. D.B. Savage, K.F. Petersen, and G.I. Shulman Disordered lipid metabolism and the pathogenesis of insulin resistance Physiol Rev 87 2 2007 507 520 (Pubitemid 47084679)
70. R.H. Unger, G.O. Clark, and P.E. Scherer Lipid homeostasis, lipotoxicity and the metabolic syndrome Biochim Biophys Acta 1801 3 2010 209 214
71. J. Szendroedi, and M. Roden Ectopic lipids and organ function Curr Opin Lipidol 20 1 2009 50 56
72. J. Machann, H. Haring, and F. Schick Intramyocellular lipids and insulin resistance Diabetes Obes Metab 6 4 2004 239 248 (Pubitemid 38807797)
73. A.P. Russell Lipotoxicity: The obese and endurance-trained paradox Int J Obes Relat Metab Disord 28 Suppl 4 2004 S66 S71
74. L. Liu, Y. Zhang, and N. Chen Upregulation of myocellular DGAT1 augments triglyceride synthesis in skeletal muscle and protects against fat-induced insulin resistance J Clin Invest 117 6 2007 1679 1689 (Pubitemid 46871352)
75. D.M. Muoio Revisiting the connection between intramyocellular lipids and insulin resistance: A long and winding road Diabetologia 55 10 2012 2551 2554
76. D.M. Muoio, and C.B. Newgard Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes Nat Rev Mol Cell Biol 9 3 2008 193 205 (Pubitemid 351301824)
77. L. Heilbronn, S.R. Smith, and E. Ravussin Failure of fat cell proliferation, mitochondrial function and fat oxidation results in ectopic fat storage, insulin resistance and type II diabetes mellitus Int J Obes Relat Metab Disord 28 Suppl 4 2004 S12 S21
78. S.P. Weisberg, D. McCann, and M. Desai Obesity is associated with macrophage accumulation in adipose tissue J Clin Invest 112 12 2003 1796 1808 (Pubitemid 38063703)
79. H. Xu, G.T. Barnes, and Q. Yang Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance J Clin Invest 112 12 2003 1821 1830 (Pubitemid 38063705)
80. J.M. Olefsky, and C.K. Glass Macrophages, inflammation, and insulin resistance Annu Rev Physiol 72 2010 219 246
81. N. Hosogai, A. Fukuhara, and K. Oshima Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation Diabetes 56 4 2007 901 911 (Pubitemid 46525054)
82. T. Christiansen, B. Richelsen, and J.M. Bruun Monocyte chemoattractant protein-1 is produced in isolated adipocytes, associated with adiposity and reduced after weight loss in morbid obese subjects Int J Obes (Lond) 29 1 2005 146 150 (Pubitemid 40065478)
83. A. Chatzigeorgiou, K.P. Karalis, and S.R. Bornstein Lymphocytes in obesity-related adipose tissue inflammation Diabetologia 55 10 2012 2583 2592
84. P. Trayhurn, and I.S. Wood Adipokines: Inflammation and the pleiotropic role of white adipose tissue Br J Nutr 92 3 2004 347 355 (Pubitemid 40277057)
85. T. Suganami, J. Nishida, and Y. Ogawa A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: role of free fatty acids and tumor necrosis factor alpha Arterioscler Thromb Vasc Biol 25 10 2005 2062 2068 (Pubitemid 41416301)
86. D. Cai, M. Yuan, and D.F. Frantz Local and systemic insulin resistance resulting from hepatic activation of IKK-beta and NF-kappaB Nat Med 11 2 2005 183 190 (Pubitemid 40321354)
87. O. Osborn, and J.M. Olefsky The cellular and signaling networks linking the immune system and metabolism in disease Nat Med 18 3 2012 363 374
88. G.S. Hotamisligil Inflammation and metabolic disorders Nature 444 7121 2006 860 867 (Pubitemid 46024993)
89. E. Charmandari, C. Tsigos, and G. Chrousos Endocrinology of the stress response Annu Rev Physiol 67 2005 259 284 (Pubitemid 40409509)
90. A.J. Peckett, D.C. Wright, and M.C. Riddell The effects of glucocorticoids on adipose tissue lipid metabolism Metabolism 60 11 2011 1500 1510
91. P. Bjorntorp Visceral fat accumulation: The missing link between psychosocial factors and cardiovascular disease? J Intern Med 230 3 1991 195 201
92. A.M. Strack, R.J. Sebastian, and M.W. Schwartz Glucocorticoids and insulin: reciprocal signals for energy balance Am J Physiol 268 1 Pt 2 1995 R142 R149
93. K.E. Zakrzewska, I. Cusin, and A. Sainsbury Glucocorticoids as counterregulatory hormones of leptin: toward an understanding of leptin resistance Diabetes 46 4 1997 717 719 (Pubitemid 27143393)
94. P.A. Tataranni, D.E. Larson, and S. Snitker Effects of glucocorticoids on energy metabolism and food intake in humans Am J Physiol 271 2 Pt 1 1996 E317 E325
95. J.L. Leahy Pathogenesis of type 2 diabetes mellitus Arch Med Res 36 3 2005 197 209 (Pubitemid 40755133)
96. D. Scheuner, and R.J. Kaufman The unfolded protein response: A pathway that links insulin demand with beta-cell failure and diabetes Endocr Rev 29 3 2008 317 333 (Pubitemid 351679702)
97. S.E. Kahn, R.L. Hull, and K.M. Utzschneider Mechanisms linking obesity to insulin resistance and type 2 diabetes Nature 444 7121 2006 840 846 (Pubitemid 46024990)
98. K.E. Wellen, and G.S. Hotamisligil Inflammation, stress, and diabetes J Clin Invest 115 5 2005 1111 1119 (Pubitemid 40629025)
99. J.R. Perry, and T.M. Frayling New gene variants alter type 2 diabetes risk predominantly through reduced beta-cell function Curr Opin Clin Nutr Metab Care 11 4 2008 371 377
100. S.F. Grant, G. Thorleifsson, and I. Reynisdottir Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes Nat Genet 38 3 2006 320 323
101. J.C. Florez The new type 2 diabetes gene TCF7L2 Curr Opin Clin Nutr Metab Care 10 4 2007 391 396 (Pubitemid 46934105)
102. V. Lyssenko, R. Lupi, and P. Marchetti Mechanisms by which common variants in the TCF7L2 gene increase risk of type 2 diabetes J Clin Invest 117 8 2007 2155 2163 (Pubitemid 47219560)
103. H.J. Welters, and R.N. Kulkarni Wnt signaling: relevance to beta-cell biology and diabetes Trends Endocrinol Metab 19 10 2008 349 355
104. A. Lev-Ran Human obesity: An evolutionary approach to understanding our bulging waistline Diabetes Metab Res Rev 17 5 2001 347 362 (Pubitemid 33040308)
105. H. Kolb, and T. Mandrup-Poulsen The global diabetes epidemic as a consequence of lifestyle-induced low-grade inflammation Diabetologia 53 1 2010 10 20
106. A.V. Nunn, J.D. Bell, and G.W. Guy Lifestyle-induced metabolic inflexibility and accelerated ageing syndrome: Insulin resistance, friend or foe? Nutr Metab (Lond) 6 2009 16
107. E.L. Lim, K.G. Hollingsworth, and B.S. Aribisala Reversal of type 2 diabetes: normalisation of beta cell function in association with decreased pancreas and liver triacylglycerol Diabetologia 54 10 2011 2506 2514
108. E. Phielix, R. Meex, and D.M. Ouwens High oxidative capacity due to chronic exercise training attenuates lipid-induced insulin resistance Diabetes 61 10 2012 2472 2478
109. P. Bostrom, J. Wu, and M.P. Jedrychowski A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis Nature 481 7382 2012 463 468
110. M. Stumvoll, B.J. Goldstein, and T.W. van Haeften Type 2 diabetes: principles of pathogenesis and therapy Lancet 365 9467 2005 1333 1346
111. X. Yang, and U. Smith Adipose tissue distribution and risk of metabolic disease: does thiazolidinedione-induced adipose tissue redistribution provide a clue to the answer? Diabetologia 50 6 2007 1127 1139 (Pubitemid 46701551)
112. C.E. Hagberg, A. Falkevall, and X. Wang Vascular endothelial growth factor B controls endothelial fatty acid uptake Nature 464 7290 2010 917 921
113. C.E. Hagberg, A. Mehlem, and A. Falkevall Targeting VEGF-B as a novel treatment for insulin resistance and type 2 diabetes Nature 490 7420 2012 426 430