Combatting type 2 diabetes by turning up the heat

Diabetologia

Volumn 59, Issue 11, 2016, Pages 2269-2279

  Schrauwen, Patrick ^a   van Marken Lichtenbelt, Wouter D ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Brown adipose tissue; Cold induced thermogenesis; Diabetes; Energy turnover; Review

Indexed keywords

ATHLETE; BROWN ADIPOSE TISSUE; COLD EXPOSURE; ENERGY BALANCE; ENERGY METABOLISM; EXERCISE; HEAT; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; INTERVENTION STUDY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NONSHIVERING THERMOGENESIS; OBESITY; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PRIORITY JOURNAL; REVIEW; THERMOGENESIS; THERMOREGULATION; TURNOVER TIME; ANIMAL; DIABETES MELLITUS, TYPE 2; METABOLISM; PHYSIOLOGY;

ADIPOSE TISSUE, BROWN; ANIMALS; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; HUMANS; THERMOGENESIS;

EID: 84984907972     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-016-4068-3     Document Type: Review

References (116)

1. Krssak M, Falk Petersen K, Dresner A et al (1999) Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 42:113–116
2. Perseghin G, Scifo P, De Cobelli F et al (1999) Intramyocellular triglyceride content is a determinant of in vivo insulin resistance in humans: a 1H-13C nuclear magnetic resonance spectroscopy assessment in offspring of type 2 diabetic parents. Diabetes 48:1600–1606
3. Slentz CA, Duscha BD, Johnson JL et al (2004) Effects of the amount of exercise on body weight, body composition, and measures of central obesity: STRRIDE--a randomized controlled study. Arch Intern Med 164:31–39
4. Tuomilehto J, Lindstrom J, Eriksson JG et al (2001) Prevention of type 2 diabetes mellitus by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 344:1343–1350
5. Manson JE, Greenland P, LaCroix AZ et al (2002) Walking compared with vigorous exercise for the prevention of cardiovascular events in women. N Engl J Med 347:716–725
6. Hahn V, Halle M, Schmidt-Trucksass A, Rathmann W, Meisinger C, Mielck A (2009) Physical activity and the metabolic syndrome in elderly German men and women: results from the population-based KORA survey. Diabetes Care 32:511–513
7. Friedenreich CM, Neilson HK, Lynch BM (2010) State of the epidemiological evidence on physical activity and cancer prevention. Eur J Cancer 46:2593–2604
8. Dunstan DW, Salmon J, Healy GN et al (2007) Association of television viewing with fasting and 2-h postchallenge plasma glucose levels in adults without diagnosed diabetes. Diabetes Care 30:516–522
9. Healy GN, Dunstan DW, Salmon J et al (2008) Breaks in sedentary time: beneficial associations with metabolic risk. Diabetes Care 31:661–666
10. Thorp AA, Healy GN, Owen N et al (2010) Deleterious associations of sitting time and television viewing time with cardiometabolic risk biomarkers: Australian Diabetes, Obesity and Lifestyle (AusDiab) study 2004-2005. Diabetes Care 33:327–334
11. Duvivier BM, Schaper NC, Bremers MA et al (2013) Minimal intensity physical activity (standing and walking) of longer duration improves insulin action and plasma lipids more than shorter periods of moderate to vigorous exercise (cycling) in sedentary subjects when energy expenditure is comparable. PLoS One 8, e55542
12. Ford ES, Li C, Zhao G, Pearson WS, Tsai J, Churilla JR (2010) Sedentary behavior, physical activity, and concentrations of insulin among US adults. Metabolism 59:1268–1275
13. Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758
14. Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C (1986) Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Investig 78:1568–1578
15. Gissane C, Corrigan DL, White JA (1991) Gross efficiency responses to exercise conditioning in adult males of various ages. J Sports Sci 9:383–391
16. Butte NF, Ekelund U, Westerterp KR (2012) Assessing physical activity using wearable monitors: measures of physical activity. Med Sci Sports Exerc 44:S5–S12
17. Kingma B, Frijns A, van Marken Lichtenbelt W (2012) The thermoneutral zone: implications for metabolic studies. Front Biosci (Elite Ed) 4:1975–1985
18. Mitchell P (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev Camb Philos Soc 41:445–502
19. Benzinger TH (1969) Heat regulation: homeostasis of central temperature in man. Physiol Rev 49:671–759
20. Vosselman MJ, Vijgen GH, Kingma BR, Brans B, van Marken Lichtenbelt WD (2014) Frequent extreme cold exposure and brown fat and cold-induced thermogenesis: a study in a monozygotic twin. PLoS One 9, e101653
21. Dauncey MJ (1981) Influence of mild cold on 24 h energy expenditure, resting metabolism and diet-induced thermogenesis. Br J Nutr 45:257–267
22. Warwick PM, Busby R (1990) Influence of mild cold on 24 h energy expenditure in ʻnormallyʼ clothed adults. Br J Nutr 63:481–488
23. van Ooijen AMJ, van Marken Lichtenbelt WD, van Steenhoven AA, Westerterp K (2004) Seasonal changes in metabolic and temperature responses to cold air in humans. Physiol Behav 82:545–553
24. Wijers SL, Saris WH, van Marken Lichtenbelt WD (2009) Recent advances in adaptive thermogenesis: potential implications for the treatment of obesity. Obes Rev 10:218–226
25. Ravussin E, Lillioja S, Knowler WC et al (1988) Reduced rate of energy expenditure as a risk factor for body-weight gain. N Engl J Med 318:467–472
26. Clapham JC, Arch JR, Chapman H et al (2000) Mice overexpressing human uncoupling protein-3 in skeletal muscle are hyperphagic and lean. Nature 406:415–418
27. Li B, Nolte LA, Ju JS et al (2000) Skeletal muscle respiratory uncoupling prevents diet-induced obesity and insulin resistance in mice. Nat Med 6:1115–1120
28. Huppertz C, Fischer BM, Kim YB et al (2001) Uncoupling protein 3 (UCP3) stimulates glucose uptake in muscle cells through a phosphoinositide 3-kinase-dependent mechanism. J Biol Chem 276:12520–12529
29. Perry RJ, Kim T, Zhang XM et al (2013) Reversal of hypertriglyceridemia, fatty liver disease, and insulin resistance by a liver-targeted mitochondrial uncoupler. Cell Metab 18:740–748
30. Perry RJ, Zhang D, Zhang XM, Boyer JL, Shulman GI (2015) Controlled-release mitochondrial protonophore reverses diabetes and steatohepatitis in rats. Science 347:1253–1256
31. Befroy DE, Petersen KF, Dufour S, Mason GF, Rothman DL, Shulman GI (2008) Increased substrate oxidation and mitochondrial uncoupling in skeletal muscle of endurance-trained individuals. Proc Natl Acad Sci U S A 105:16701–16706
32. Andreyev A, Bondareva TO, Dedukhova VI et al (1989) The ATP/ADP-antiporter is involved in the uncoupling effect of fatty acids on mitochondria. Eur J Biochem 182:585–592
33. Skulachev VP (1991) Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation. FEBS Lett 294:158–162
34. Sparks LM, Gemmink A, Phielix E et al (2016) ANT1-mediated fatty acid-induced uncoupling as a target for improving myocellular insulin sensitivity. Diabetologia 59:1030–1039
35. Lebon V, Dufour S, Petersen KF et al (2001) Effect of triiodothyronine on mitochondrial energy coupling in human skeletal muscle. J Clin Invest 108:733–737
36. Goodpaster BH, He J, Watkins S, Kelley DE (2001) Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 86:5755–5761
37. Shulman GI (2000) Cellular mechanisms of insulin resistance. J Clin Invest 106:171–176
38. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:664–671
39. Amati F, Dube JJ, Alvarez-Carnero E et al (2011) Skeletal muscle triglycerides, diacylglycerols, and ceramides in insulin resistance: another paradox in endurance-trained athletes? Diabetes 60:2588–2597
40. Timmers S, de Vogel-van den Bosch J, Hesselink MK et al (2011) Paradoxical increase in TAG and DAG content parallel the insulin sensitizing effect of unilateral DGAT1 overexpression in rat skeletal muscle. PLoS One 6, e14503
41. Choi CS, Befroy DE, Codella R et al (2008) Paradoxical effects of increased expression of PGC-1alpha on muscle mitochondrial function and insulin-stimulated muscle glucose metabolism. Proc Natl Acad Sci U S A 105:19926–19931
42. Summermatter S, Shui G, Maag D, Santos G, Wenk MR, Handschin C (2013) PGC-1alpha improves glucose homeostasis in skeletal muscle in an activity-dependent manner. Diabetes 62:85–95
43. Koves TR, Sparks LM, Kovalik JP et al (2013) PPARgamma coactivator-1alpha contributes to exercise-induced regulation of intramuscular lipid droplet programming in mice and humans. J Lipid Res 54:522–534
44. Bosma M, Hesselink MK, Sparks LM et al (2012) Perilipin 2 improves insulin sensitivity in skeletal muscle despite elevated intramuscular lipid levels. Diabetes 61:2679–2690
45. Bosma M, Minnaard R, Sparks LM et al (2012) The lipid droplet coat protein perilipin 5 also localizes to muscle mitochondria. Histochem Cell Biol 137:205–216
46. Bosma M, Sparks LM, Hooiveld GJ et al (2013) Overexpression of PLIN5 in skeletal muscle promotes oxidative gene expression and intramyocellular lipid content without compromising insulin sensitivity. Biochim Biophys Acta 1831:844–852
47. Listenberger LL, Han X, Lewis SE et al (2003) Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci U S A 100:3077–3082
48. Perreault L, Bergman BC, Hunerdosse DM, Playdon MC, Eckel RH (2010) Inflexibility in intramuscular triglyceride fractional synthesis distinguishes prediabetes from obesity in humans. Obesity (Silver Spring) 18:1524–1531
49. Perreault L, Bergman BC, Hunerdosse DM, Eckel RH (2010) Altered intramuscular lipid metabolism relates to diminished insulin action in men, but not women, in progression to diabetes. Obesity (Silver Spring) 18:2093–2100
50. Ravussin E, Smith SR (2002) Increased fat intake, impaired fat oxidation, and failure of fat cell proliferation result in ectopic fat storage, insulin resistance, and type 2 diabetes mellitus. Ann N Y Acad Sci 967:363–378
51. Adiels M, Taskinen MR, Boren J (2008) Fatty liver, insulin resistance, and dyslipidemia. Curr Diab Rep 8:60–64
52. Hardie DG (2014) AMPK--sensing energy while talking to other signaling pathways. Cell Metab 20:939–952
53. Hardie DG (2015) AMPK: positive and negative regulation, and its role in whole-body energy homeostasis. Curr Opin Cell Biol 33:1–7
54. Hardie DG (2014) AMP-activated protein kinase: maintaining energy homeostasis at the cellular and whole-body levels. Annu Rev Nutr 34:31–55
55. Michan S, Sinclair D (2007) Sirtuins in mammals: insights into their biological function. Biochem J 404:1–13
56. Chang HC, Guarente L (2014) SIRT1 and other sirtuins in metabolism. Trends Endocrinol Metab 25:138–145
57. Ruderman NB, Carling D, Prentki M, Cacicedo JM (2013) AMPK, insulin resistance, and the metabolic syndrome. J Clin Invest 123:2764–2772
58. Houtkooper RH, Pirinen E, Auwerx J (2012) Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 13:225–238
59. Foretz M, Guigas B, Bertrand L, Pollak M, Viollet B (2014) Metformin: from mechanisms of action to therapies. Cell Metab 20:953–966
60. Rena G, Pearson ER, Sakamoto K (2013) Molecular mechanism of action of metformin: old or new insights? Diabetologia 56:1898–1906
61. McCreight LJ, Bailey CJ, Pearson ER (2016) Metformin and the gastrointestinal tract. Diabetologia 59:426–435
62. Goodyear LJ (2000) AMP-activated protein kinase: a critical signaling intermediary for exercise-stimulated glucose transport? Exerc Sport Sci Rev 28:113–116
63. Schenk S, Horowitz JF (2007) Acute exercise increases triglyceride synthesis in skeletal muscle and prevents fatty acid-induced insulin resistance. J Clin Invest 117:1690–1698
64. Marcinko K, Steinberg GR (2014) The role of AMPK in controlling metabolism and mitochondrial biogenesis during exercise. Exp Physiol 99:1581–1585
65. Friedrichsen M, Mortensen B, Pehmoller C, Birk JB, Wojtaszewski JF (2013) Exercise-induced AMPK activity in skeletal muscle: role in glucose uptake and insulin sensitivity. Mol Cell Endocrinol 366:204–214
66. Fujii N, Jessen N, Goodyear LJ (2006) AMP-activated protein kinase and the regulation of glucose transport. Am J Physiol Endocrinol Metab 291:E867–E877
67. McGee SL, Hargreaves M (2006) Exercise and skeletal muscle glucose transporter 4 expression: molecular mechanisms. Clin Exp Pharmacol Physiol 33:395–399
68. Meex RC, Schrauwen-Hinderling VB, Moonen-Kornips E et al (2010) Restoration of muscle mitochondrial function and metabolic flexibility in type 2 diabetes by exercise training is paralleled by increased myocellular fat storage and improved insulin sensitivity. Diabetes 59:572–579
69. Phielix E, Meex R, Moonen-Kornips E, Hesselink MK, Schrauwen P (2010) Exercise training increases mitochondrial content and ex vivo mitochondrial function similarly in patients with type 2 diabetes and in control individuals. Diabetologia 53:1714–1721
70. Goodpaster BH, Katsiaras A, Kelley DE (2003) Enhanced fat oxidation through physical activity is associated with improvements in insulin sensitivity in obesity. Diabetes 52:2191–2197
71. Coen PM, Menshikova EV, Distefano G et al (2015) Exercise and weight loss improve muscle mitochondrial respiration, lipid partitioning, and insulin sensitivity after gastric bypass surgery. Diabetes 64:3737–3750
72. 2 emissions in obese women are restored to a lean phenotype with aerobic exercise training. Diabetes 64:2104–2115
73. Hey-Mogensen M, Hojlund K, Vind BF et al (2010) Effect of physical training on mitochondrial respiration and reactive oxygen species release in skeletal muscle in patients with obesity and type 2 diabetes. Diabetologia 53:1976–1985
74. Bergman BC, Perreault L, Hunerdosse DM, Koehler MC, Samek AM, Eckel RH (2010) Increased intramuscular lipid synthesis and low saturation relate to insulin sensitivity in endurance-trained athletes. J Appl Physiol (1985) 108:1134–1141
75. Balducci S, Sacchetti M, Haxhi J et al (2015) The Italian Diabetes and Exercise Study 2 (IDES-2): a long-term behavioral intervention for adoption and maintenance of a physically active lifestyle. Trials 16:569
76. Hallsworth K, Thoma C, Hollingsworth KG et al (2015) Modified high-intensity interval training reduces liver fat and improves cardiac function in non-alcoholic fatty liver disease: a randomized controlled trial. Clin Sci (Lond) 129:1097–1105
77. Bacchi E, Negri C, Targher G et al (2013) Both resistance training and aerobic training reduce hepatic fat content in type 2 diabetic subjects with nonalcoholic fatty liver disease (the RAED2 Randomized Trial). Hepatology 58:1287–1295
78. Keating SE, Hackett DA, George J, Johnson NA (2012) Exercise and non-alcoholic fatty liver disease: a systematic review and meta-analysis. J Hepatol 57:157–166
79. Szendroedi J, Chmelik M, Schmid AI et al (2009) Abnormal hepatic energy homeostasis in type 2 diabetes. Hepatology 50:1079–1086
80. Roberts LD, Bostrom P, OʼSullivan JF et al (2014) β-Aminoisobutyric acid induces browning of white fat and hepatic β-oxidation and is inversely correlated with cardiometabolic risk factors. Cell Metab 19:96–108
81. Rao RR, Long JZ, White JP et al (2014) Meteorin-like is a hormone that regulates immune-adipose interactions to increase beige fat thermogenesis. Cell 157:1279–1291
82. Bostrom P, Wu J, Jedrychowski MP et al (2012) A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481:463–468
83. Catoire M, Alex S, Paraskevopulos N et al (2014) Fatty acid-inducible ANGPTL4 governs lipid metabolic response to exercise. Proc Natl Acad Sci U S A 111:E1043–E1052
84. de Ligt M, Timmers S, Schrauwen P (2015) Resveratrol and obesity: can resveratrol relieve metabolic disturbances? Biochim Biophys Acta 1852:1137–1144
85. Timmers S, Konings E, Bilet L et al (2011) Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab 14:612–622
86. Himms-Hagen J (1972) Lipid metabolism during cold-exposure and during cold-acclimation. Lipids 7:310–323
87. Martineau L, Jacobs I (1991) Effects of muscle glycogen and plasma FFA availability on human metabolic responses in cold water. J Appl Physiol (1985) 71:1331–1339
88. Vallerand AL, Zamecnik J, Jacobs I (1995) Plasma glucose turnover during cold stress in humans. J Appl Physiol (1985) 78:1296–1302
89. Wijers SL, Saris W, van Marken Lichtenbelt WD (2010) Cold induced adaptive thermogenesis in lean and obese. J Proteome Res 18:1092–1099
90. Vijgen GH, Bouvy ND, Teule GJ et al (2012) Increase in brown adipose tissue activity after weight loss in morbidly obese subjects. J Clin Endocrinol Metab 97:E1229–E1233
91. Hanssen MJ, Hoeks J, Brans B et al (2015) Short-term cold acclimation improves insulin sensitivity in patients with type 2 diabetes mellitus. Nat Med 21:863–865
92. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359
93. Virtanen KA, Lidell ME, Orava J et al (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518–1525
94. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM et al (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500–1508
95. Saito M, Okamatsu-Ogura Y, Matsushita M et al (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58:1526–1531
96. Cypess AM, Lehman S, Williams G et al (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360:1509–1517
97. Nedergaard J, Bengtsson T, Cannon B (2007) Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 293:E444–E452
98. Hanssen MJ, Wierts R, Hoeks J et al (2015) Glucose uptake in human brown adipose tissue is impaired upon fasting-induced insulin resistance. Diabetologia 58:586–595
99. van der Lans AA, Wierts R, Vosselman MJ, Schrauwen P, Brans B, van Marken Lichtenbelt WD (2014) Cold-activated brown adipose tissue in human adults: methodological issues. Am J Physiol Regul Integr Comp Physiol 307:R103–R113
100. Vijgen GH, Bouvy ND, Teule GJ, Brans B, Schrauwen P, van Marken Lichtenbelt WD (2011) Brown adipose tissue in morbidly obese subjects. PLoS ONE 6, e17247
101. Yoneshiro T, Aita S, Matsushita M et al (2011) Age-related decrease in cold-activated brown adipose tissue and accumulation of body fat in healthy humans. J Proteome Res 19:1755–1760
102. Blondin DP, Labbe SM, Tingelstad HC et al (2014) Increased brown adipose tissue oxidative capacity in cold-acclimated humans. J Clin Endocrinol Metab 99:E438–E446
103. van der Lans AA, Hoeks J, Brans B et al (2013) Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest 123:3395–3403
104. Yoneshiro T, Aita S, Matsushita M et al (2013) Recruited brown adipose tissue as an antiobesity agent in humans. J Clin Invest 123:3404–3408
105. Ma SW, Foster DO (1986) Uptake of glucose and release of fatty acids and glycerol by rat brown adipose tissue in vivo. Can J Physiol Pharmacol 64:609–614
106. Isler D, Hill HP, Meier MK (1987) Glucose metabolism in isolated brown adipocytes under β-adrenergic stimulation. Quantitative contribution of glucose to total thermogenesis. Biochem J 245:789–793
107. Festuccia WT, Blanchard PG, Deshaies Y (2011) Control of brown adipose tissue glucose and lipid metabolism by PPARγ. Front Endocrinol 2:84
108. Stanford KI, Middelbeek RJ, Townsend KL et al (2013) Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest 123:215–223
109. Ouellet V, Routhier-Labadie A, Bellemare W et al (2011) Outdoor temperature, age, sex, body mass index, and diabetic status determine the prevalence, mass, and glucose-uptake activity of 18F-FDG-detected BAT in humans. J Clin Endocrinol Metab 96:192–199
110. Orava J, Nuutila P, Lidell ME et al (2011) Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab 14:272–279
111. Ouellet V, Labbe SM, Blondin DP et al (2012) Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest 122:545–552
112. Orava J, Nuutila P, Noponen T et al (2013) Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans. Obesity (Silver Spring) 21:2279–2287
113. Chondronikola M, Volpi E, Borsheim E et al (2014) Brown adipose tissue improves whole-body glucose homeostasis and insulin sensitivity in humans. Diabetes 63:4089–4099
114. Lee P, Smith S, Linderman J et al (2014) Temperature-acclimated brown adipose tissue modulates insulin sensitivity in humans. Diabetes 63:3686–3698
115. Gasparetti AL, de Souza CT, Pereira-da-Silva M et al (2003) Cold exposure induces tissue-specific modulation of the insulin-signalling pathway in Rattus norvegicus. J Physiol 552:149–162
116. Hanssen MJ, van der Lans AA, Brans B et al (2016) Short-term cold acclimation recruits brown adipose tissue in obese humans. Diabetes 65:1179–1189