High-density lipoprotein maintains skeletal muscle function by modulating cellular respiration in mice

Circulation

Volumn 128, Issue 22, 2013, Pages 2364-2371

  Lehti, Maarit ^a,b,c   Donelan, Elizabeth ^b   Abplanalp, William ^b   Al Massadi, Omar ^b   Habegger, Kirk M ^b   Weber, Jon ^b   Ress, Chandler ^b   Mansfeld, Johannes ^b,d   Somvanshi, Sonal ^b   Trivedi, Chitrang ^b,e   Keuper, Michaela ^a   Ograjsek, Teja ^a   Striese, Cynthia ^a   Cucuruz, Sebastian ⁱ   Pfluger, Paul T ^a   Krishna, Radhakrishna ^b   Gordon, Scott M ^b   Silva, R A Gangani D ^b   Luquet, Serge ^f,g   Castel, Julien ^f,g   Martinez, Sarah ^f,g   D'Alessio, David ^b   Davidson, W Sean ^b   Hofmann, Susanna M ^a,b,h   more..

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c LIKES RESEARCH CENTER FOR SPORT AND HEALTH SCIENCES   (Finland)

^d ETH ZURICH   (Switzerland)

^e ZYDUS RESEARCH CENTRE   (India)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g CNRS   (France)

^h LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

ⁱ NONE

Author keywords

Cellular respiration; Cholesterol, HDL; Exercise; Obesity

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOLIPOPROTEIN A1; FATTY ACID; FIBROBLAST GROWTH FACTOR 21; GLUCOSE; HIGH DENSITY LIPOPROTEIN; LACTIC ACID; FIBROBLAST GROWTH FACTOR; GLUCOSE BLOOD LEVEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOENERGY; CELL RESPIRATION; CONTROLLED STUDY; DIET RESTRICTION; ENDURANCE TRAINING; ENZYME SYNTHESIS; EXHAUSTION; FAT MASS; GASTROCNEMIUS MUSCLE; GLUCOSE HOMEOSTASIS; GLUCOSE OXIDATION; GLUCOSE TOLERANCE TEST; GLUCOSE UTILIZATION; GLYCOLYSIS; HYPERGLYCEMIA; IMPAIRED GLUCOSE TOLERANCE; KNOCKOUT MOUSE; LIPID DIET; LIPOLYSIS; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE CELL; MUSCLE FUNCTION; MUSCLE LEVEL; MUSCLE METABOLISM; MUSCLE MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY CHAIN; SKELETAL MUSCLE; TRANSGENIC MOUSE; WHITE ADIPOSE TISSUE; WILD TYPE; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; ENDURANCE; GENETICS; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; HOMEOSTASIS; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PHYSIOLOGY;

ANIMALS; APOLIPOPROTEIN A-I; BLOOD GLUCOSE; CELL RESPIRATION; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; FATTY ACIDS, NONESTERIFIED; FIBROBLAST GROWTH FACTORS; GLUCOSE INTOLERANCE; HOMEOSTASIS; HYPERGLYCEMIA; LIPOPROTEINS, HDL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, MUSCLE; MUSCLE, SKELETAL; PHYSICAL ENDURANCE;

EID: 84888645949     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.001551     Document Type: Article

References (45)

1. Samper-Ternent R, Snih Al S. Obesity in Older Adults: Epidemiology and Implications for Disability and Disease. Rev Clin Gerontol. 2012; 22:10-34
2. Rees K, Dyakova M, Ward K, Thorogood M, Brunner E. Dietary advice for reducing cardiovascular risk. Cochrane Database Syst Rev. 2013;3:CD002128
3. Frohlich J, Al-Sarraf A. Cardiovascular risk and atherosclerosis prevention. Cardiovasc Pathol. 2013;22:16-18
4. Hooper L, Summerbell CD, Thompson R, Sills D, Roberts FG, Moore HJ, Davey Smith G. Reduced or modified dietary fat for preventing cardiovascular disease. Cochrane Database Syst Rev. 2012;5:CD002137
5. Ooi EM, Ng TW, Watts GF, Barrett PH. Dietary fatty acids and lipoprotein metabolism: New insights and updates. Curr Opin Lipidol. 2013;24:192-197
6. Howard BV, Taskinen MR. CVD in women. Nutr Metab Cardiovasc Dis. 2010;20:377-378
7. Boden WE. High-density lipoprotein cholesterol as an independent risk factor in cardiovascular disease: Assessing the data from Framingham to the Veterans Affairs High-Density Lipoprotein Intervention Trial. Am J Cardiol. 2000;86(12A):19L-22L
8. McNeill AM, Katz R, Girman CJ, Rosamond WD, Wagenknecht LE, Barzilay JI, Tracy RP, Savage PJ, Jackson SA. Metabolic syndrome and cardiovascular disease in older people: The cardiovascular health study. J Am Geriatr Soc. 2006;54:1317-1324
9. Gordon SM, Hofmann S, Askew DS, Davidson WS. High density lipoprotein: It's not just about lipid transport anymore. Trends Endocrinol Metab. 2011;22:9-15
10. Rader DJ, Tall AR. The not-so-simple HDL story: Is it time to revise the HDL cholesterol hypothesis? Nat Med. 2012;18:1344-1346
11. Lewis GF, Rader DJ. New insights into the regulation of HDL metabolism and reverse cholesterol transport. Circ Res. 2005;96:1221-1232
12. Larach DB, deGoma EM, Rader DJ. Targeting high density lipoproteins in the prevention of cardiovascular disease? Curr Cardiol Rep. 2012;14:684-691
13. ACCORD (Action to Control Cardiovascular Risk in Diabetes) Study Group, Ginsberg HN, Elam MB, Lovato LC, Crouse JR 3rd, Leiter LA, Linz P, Friedewald WT, Buse JB, Gerstein HC, Probstfield J, Grimm RH, Ismail-Beigi F, Bigger JT, Goff DC Jr, Cushman WC, Simons-Morton DG, Byington RP. Effects of combination lipid therapy in type 2 diabetes mellitus.N Engl J Med. 2010;362:1563-1574
14. Drew BG, Duffy SJ, Formosa MF, Natoli AK, Henstridge DC, Penfold SA, Thomas WG, Mukhamedova N, de Courten B, Forbes JM, Yap FY, Kaye DM, van Hall G, Febbraio MA, Kemp BE, Sviridov D, Steinberg GR, Kingwell BA. High-density lipoprotein modulates glucose metabolism in patients with type 2 diabetes mellitus. Circulation. 2009;119:2103-2111
15. Fryirs MA, Barter PJ, Appavoo M, Tuch BE, Tabet F, Heather AK, Rye KA. Effects of high-density lipoproteins on pancreatic beta-cell insulin secretion. Arterioscler Thromb Vasc Biol. 2010;30:1642-1648
16. Han R, Lai R, Ding Q, Wang Z, Luo X, Zhang Y, Cui G, He J, Liu W, Chen Y. Apolipoprotein A-I stimulates AMP-Activated protein kinase and improves glucose metabolism. Diabetologia. 2007;50:1960-1968
17. McArdle WD, Katch FI, Katch VL. Exercise physiology: Nutrition, energy, and human performance. Wolters Kluwer Health, 2009
18. Sivitz WI, Yorek MA. Mitochondrial dysfunction in diabetes: From molecular mechanisms to functional significance and therapeutic opportunities. Antioxid Redox Signal. 2010;12:537-577
19. Shulman GI, Rothman DL, Jue T, Stein P, DeFronzo RA, Shulman RG. Quantitation of muscle glycogen synthesis in normal subjects and subjects with non-insulin-dependent diabetes by 13C nuclear magnetic resonance spectroscopy. N Engl J Med. 1990;322:223-228
20. LeRoith D, Olefsky JM, Taylor SI. Diabetes Mellitus: A Fundamental and Clinical Text-3rd Ed. Baltimore, MD: Lippincott, Williams & Wilkins; 2003
21. Coen PM, Goodpaster BH. Role of intramyocelluar lipids in human health. Trends Endocrinol Metab. 2012;23:391-398
22. Messer JI, Jackman MR, Willis WT. Pyruvate and citric acid cycle carbon requirements in isolated skeletal muscle mitochondria. Am J Physiol, Cell Physiol. 2004;286:C565-C572
23. Costanzo-Garvey DL, Pfluger PT, Dougherty MK, Stock JL, Boehm M, Chaika O, Fernandez MR, Fisher K, Kortum RL, Hong EG, Jun JY, Ko HJ, Schreiner A, Volle DJ, Treece T, Swift AL, Winer M, Chen D, Wu M, Leon LR, Shaw AS, McNeish J, Kim JK, Morrison DK, Tschöp MH, Lewis RE. KSR2 is an essential regulator of AMP kinase, energy expenditure, and insulin sensitivity. Cell Metab. 2009;10:366-378
24. Kern M, Wells JA, Stephens JM, Elton CW, Friedman JE, Tapscott EB, Pekala PH, Dohm GL. Insulin responsiveness in skeletal muscle is determined by glucose transporter (Glut4) protein level. Biochem J. 1990;270:397-400
25. James DE, Jenkins AB, Kraegen EW. Heterogeneity of insulin action in individual muscles in vivo: Euglycemic clamp studies in rats. Am J Physiol. 1985;248(5 Pt 1):E567-E574
26. Shortreed KE, Krause MP, Huang JH, Dhanani D, Moradi J, Ceddia RB, Hawke TJ. Muscle-specific adaptations, impaired oxidative capacity and maintenance of contractile function characterize diet-induced obese mouse skeletal muscle. PLoS ONE. 2009;4:e7293
27. Pederson BA, Cope CR, Schroeder JM, Smith MW, Irimia JM, Thurberg BL, DePaoli-Roach AA, Roach PJ. Exercise capacity of mice genetically lacking muscle glycogen synthase: In mice, muscle glycogen is not essential for exercise. J Biol Chem. 2005;280:17260-17265
28. Terjung RL, Baldwin KM, Molé PA, Klinkerfuss GH, Holloszy JO. Effect of running to exhaustion on skeletal muscle mitochondria: A biochemical study. Am J Physiol. 1972;223:549-554
29. Baldwin KM, Reitman JS, Terjung RL, Winder WW, Holloszy JO. Substrate depletion in different types of muscle and in liver during prolonged running. Am J Physiol. 1973;225:1045-1050
30. Reitman J, Baldwin KM, Holloszy JO. Intramuscular triglyceride utilization by red, white, and intermediate skeletal muscle and heart during exhausting exercise. Proc Soc Exp Biol Med. 1973;142:628-631
31. Suomalainen A, Elo JM, Pietiläinen KH, Hakonen AH, Sevastianova K, Korpela M, Isohanni P, Marjavaara SK, Tyni T, Kiuru-Enari S, Pihko H, Darin N, Õunap K, Kluijtmans LA, Paetau A, Buzkova J, Bindoff LA, Annunen-Rasila J, Uusimaa J, Rissanen A, Yki-Järvinen H, Hirano M, Tulinius M, Smeitink J, Tyynismaa H. FGF-21 as a biomarker for musclemanifesting mitochondrial respiratory chain deficiencies: A diagnostic study. Lancet Neurol. 2011;10:806-818
32. Hojman P, Pedersen M, Nielsen AR, Krogh-Madsen R, Yfanti C, Akerstrom T, Nielsen S, Pedersen BK. Fibroblast growth factor-21 is induced in human skeletal muscles by hyperinsulinemia. Diabetes. 2009;58:2797-2801
33. Kharitonenkov A, Wroblewski VJ, Koester A, Chen YF, Clutinger CK, Tigno XT, Hansen BC, Shanafelt AB, Etgen GJ. The metabolic state of diabetic monkeys is regulated by fibroblast growth factor-21. Endocrinology. 2007;148:774-781
34. Arner P, Pettersson A, Mitchell PJ, Dunbar JD, Kharitonenkov A, Rydén M. FGF21 attenuates lipolysis in human adipocytes-A possible link to improved insulin sensitivity. FEBS Lett. 2008;582:1725-1730
35. Hotta Y, Nakamura H, Konishi M, Murata Y, Takagi H, Matsumura S, Inoue K, Fushiki T, Itoh N. Fibroblast growth factor 21 regulates lipolysis in white adipose tissue but is not required for ketogenesis and triglyceride clearance in liver. Endocrinology. 2009;150:4625-4633
36. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13:423-433
37. Zhang H, Wang Y, Li J, Yu J, Pu J, Li L, Zhang H, Zhang S, Peng G, Yang F, Liu P. Proteome of skeletal muscle lipid droplet reveals association with mitochondria and apolipoprotein a-I. J Proteome Res. 2011;10:4757-4768
38. Zhang Q, Zhang Y, Feng H, Guo R, Jin L, Wan R, Wang L, Chen C, Li S. High density lipoprotein (HDL) promotes glucose uptake in adipocytes and glycogen synthesis in muscle cells. PLoS ONE. 2011;6:e23556
39. Thacker SV, Nickel M, DiGirolamo M. Effects of food restriction on lactate production from glucose by rat adipocytes. Am J Physiol. 1987;253(4 Pt 1):E336-E342
40. Ruan X, Li Z, Zhang Y, Yang L, Pan Y, Wang Z, Feng GS, Chen Y. Apolipoprotein A-I possesses an anti-obesity effect associated with increase of energy expenditure and up-regulation of UCP1 in brown fat. J Cell Mol Med. 2011;15:763-772
41. Li X, Ge H, Weiszmann J, Hecht R, Li YS, Véniant MM, Xu J, Wu X, Lindberg R, Li Y. Inhibition of lipolysis may contribute to the acute regulation of plasma FFA and glucose by FGF21 in ob/ob mice. FEBS Lett. 2009;583:3230-3234
42. Nestel PJ, Podkolinski M, Fidge NH. Marked increase in high density lipoproteins in mountaineers. Atherosclerosis. 1979;34:193-196
43. Olchawa B, Kingwell BA, Hoang A, Schneider L, Miyazaki O, Nestel P, Sviridov D. Physical fitness and reverse cholesterol transport. Arterioscler Thromb Vasc Biol. 2004;24:1087-1091
44. Sviridov D, Kingwell B, Hoang A, Dart A, Nestel P. Single session exercise stimulates formation of pre beta 1-HDL in leg muscle. J Lipid Res. 2003;44:522-526
45. Kujala UM, Mäkinen VP, Heinonen I, Soininen P, Kangas AJ, Leskinen TH, Rahkila P, Würtz P, Kovanen V, Cheng S, Sipilä S, Hirvensalo M, Telama R, Tammelin T, Savolainen MJ, Pouta A, O'Reilly PF, Mäntyselkä P, Viikari J, Kähönen M, Lehtimäki T, Elliott P, Vanhala MJ, Raitakari OT, Järvelin MR, Kaprio J, Kainulainen H, Ala-Korpela M. Long-Term leisure-Time physical activity and serum metabolome. Circulation. 2013;127:340-348