Skeletal Muscle Insulin Resistance Associated with Cholesterol-Induced Activation of Macrophages Is Prevented by High Density Lipoprotein

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Carey, Andrew L ^a   Siebel, Andrew L ^a   Reddy Luthmoodoo, Medini ^a   Natoli, Alaina K ^a   D'Souza, Wilissa ^a   Meikle, Peter J ^a   Sviridov, Dmitri ^a   Drew, Brian G ^b   Kingwell, Bronwyn A ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH DENSITY LIPOPROTEIN; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE RELEASE; ENZYME PHOSPHORYLATION; FAT CONTENT; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; INSULIN RESISTANCE; INSULIN SENSITIVITY; MACROPHAGE ACTIVATION; MUSCLE BIOPSY; PROTEIN FUNCTION; SKELETAL MUSCLE;

ADIPOSITY; ADULT; CELLS, CULTURED; CHOLESTEROL; DIABETES MELLITUS, TYPE 2; GLUCOSE; HUMANS; INSULIN; INSULIN RESISTANCE; LIPOPROTEINS, HDL; MACROPHAGES; MIDDLE AGED; MUSCLE, SKELETAL; OBESITY; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84874310072     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056601     Document Type: Article

References (36)

1. Barter PJ, Rye KA, Tardif JC, Waters DD, Boekholdt SM, et al. (2011) Effect of torcetrapib on glucose, insulin, and hemoglobin A1c in subjects in the Investigation of Lipid Level Management to Understand its Impact in Atherosclerotic Events (ILLUMINATE) trial. Circulation 124: 555-562.
2. Drew BG, Duffy SJ, Formosa MF, Natoli AK, Henstridge DC, et al. (2009) High-density lipoprotein modulates glucose metabolism in patients with type 2 diabetes mellitus. Circulation 119: 2103-2111.
3. Drew BG, Rye KA, Duffy SJ, Barter P, Kingwell BA, (2012) The emerging role of HDL in glucose metabolism. Nat Rev Endocrinol 8: 237-245.
4. Fryirs MA, Barter PJ, Appavoo M, Tuch BE, Tabet F, et al. (2010) Effects of high-density lipoproteins on pancreatic beta-cell insulin secretion. Arterioscler Thromb Vasc Biol 30: 1642-1648.
5. Brunham LR, Kruit JK, Pape TD, Timmins JM, Reuwer AQ, et al. (2007) Beta-cell ABCA1 influences insulin secretion, glucose homeostasis and response to thiazolidinedione treatment. Nat Med 13: 340-347.
6. Kruit JK, Kremer PH, Dai L, Tang R, Ruddle P, et al. (2010) Cholesterol efflux via ATP-binding cassette transporter A1 (ABCA1) and cholesterol uptake via the LDL receptor influences cholesterol-induced impairment of beta cell function in mice. Diabetologia 53: 1110-1119.
7. Kruit JK, Wijesekara N, Fox JE, Dai XQ, Brunham LR, et al. (2011) Islet cholesterol accumulation due to loss of ABCA1 leads to impaired exocytosis of insulin granules. Diabetes 60: 3186-3196.
8. Vergeer M, Brunham LR, Koetsveld J, Kruit JK, Verchere CB, et al. (2010) Carriers of loss-of-function mutations in ABCA1 display pancreatic beta-cell dysfunction. Diabetes Care 33: 869-874.
9. Murphy AJ, Woollard KJ, Hoang A, Mukhamedova N, Stirzaker RA, et al. (2008) High-density lipoprotein reduces the human monocyte inflammatory response. Arterioscler Thromb Vasc Biol 28: 2071-2077.
10. Yvan-Charvet L, Pagler T, Gautier EL, Avagyan S, Siry RL, et al. (2010) ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science 328: 1689-1693.
11. Patel S, Drew BG, Nakhla S, Duffy SJ, Murphy AJ, et al. (2009) Reconstituted high-density lipoprotein increases plasma high-density lipoprotein anti-inflammatory properties and cholesterol efflux capacity in patients with type 2 diabetes. J Am Coll Cardiol 53: 962-971.
12. Terasaka N, Wang N, Yvan-Charvet L, Tall AR, (2007) High-density lipoprotein protects macrophages from oxidized low-density lipoprotein-induced apoptosis by promoting efflux of 7-ketocholesterol via ABCG1. Proc Natl Acad Sci U S A 104: 15093-15098.
13. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808.
14. Hotamisligil GS, (2006) Inflammation and metabolic disorders. Nature 444: 860-867.
15. Hotamisligil GS, Shargill NS, Spiegelman BM, (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87-91.
16. Ford ES, Giles WH, Dietz WH, (2002) Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey. JAMA 287: 356-359.
17. Hoang A, Drew BG, Low H, Remaley AT, Nestel P, et al. (2007) Mechanism of cholesterol efflux in humans after infusion of reconstituted high-density lipoprotein. Eur Heart J 33: 657-665.
18. Thiebaud D, Jacot E, DeFronzo RA, Maeder E, Jequier E, et al. (1982) The effect of graded doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man. Diabetes 31: 957-963.
19. Chen MB, McAinch AJ, Macaulay SL, Castelli LA, O'Brien P E, et al. (2005) Impaired activation of AMP-kinase and fatty acid oxidation by globular adiponectin in cultured human skeletal muscle of obese type 2 diabetics. J Clin Endocrinol Metab 90: 3665-3672.
20. Huang R, Silva RA, Jerome WG, Kontush A, Chapman MJ, et al. (2011) Apolipoprotein A-I structural organization in high-density lipoproteins isolated from human plasma. Nat Struct Mol Biol 18: 416-422.
21. Carey AL, Steinberg GR, Macaulay SL, Thomas WG, Holmes AG, et al. (2006) Interleukin-6 increases insulin-stimulated glucose disposal in humans and glucose uptake and fatty acid oxidation in vitro via AMP-activated protein kinase. Diabetes 55: 2688-2697.
22. Gregor MF, Hotamisligil GS, (2011) Inflammatory mechanisms in obesity. Annu Rev Immunol 29: 415-445.
23. Hevener AL, Olefsky JM, Reichart D, Nguyen MT, Bandyopadyhay G, et al. (2007) Macrophage PPAR gamma is required for normal skeletal muscle and hepatic insulin sensitivity and full antidiabetic effects of thiazolidinediones. J Clin Invest 117: 1658-1669.
24. Solinas G, Vilcu C, Neels JG, Bandyopadhyay GK, Luo JL, et al. (2007) JNK1 in hematopoietically derived cells contributes to diet-induced inflammation and insulin resistance without affecting obesity. Cell Metab 6: 386-397.
25. Varma V, Yao-Borengasser A, Rasouli N, Nolen GT, Phanavanh B, et al. (2009) Muscle inflammatory response and insulin resistance: synergistic interaction between macrophages and fatty acids leads to impaired insulin action. Am J Physiol Endocrinol Metab 296: E1300-1310.
26. Hotamisligil GS, Murray DL, Choy LN, Spiegelman BM, (1994) Tumor necrosis factor alpha inhibits signaling from the insulin receptor. Proc Natl Acad Sci U S A 91: 4854-4858.
27. Steinberg GR, Michell BJ, van Denderen BJ, Watt MJ, Carey AL, et al. (2006) Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab 4: 465-474.
28. Goldfine AB, Fonseca V, Jablonski KA, Pyle L, Staten MA, et al. (2010) The effects of salsalate on glycemic control in patients with type 2 diabetes: a randomized trial. Ann Intern Med 152: 346-357.
29. Goldfine AB, Silver R, Aldhahi W, Cai D, Tatro E, et al. (2008) Use of salsalate to target inflammation in the treatment of insulin resistance and type 2 diabetes. Clin Transl Sci 1: 36-43.
30. Devries-Seimon T, Li Y, Yao PM, Stone E, Wang Y, et al. (2005) Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J Cell Biol 171: 61-73.
31. Singh I, Carey AL, Watson N, Febbraio MA, Hawley JA, (2008) Oxidative stress-induced insulin resistance in skeletal muscle cells is ameliorated by gamma-tocopherol treatment. Eur J Nutr 47: 387-392.
32. Elmendorf JS, (2004) Fluidity of insulin action. Mol Biotechnol 27: 127-138.
33. Hoffman NJ, Elmendorf JS, (2011) Signaling, cytoskeletal and membrane mechanisms regulating GLUT4 exocytosis. Trends Endocrinol Metab 22: 110-116.
34. Quehenberger O, Dennis EA, (2011) The human plasma lipidome. N Engl J Med 365: 1812-1823.
35. Cao H, Gerhold K, Mayers JR, Wiest MM, Watkins SM, et al. (2008) Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 134: 933-944.
36. Meikle PJ, Wong G, Tsorotes D, Barlow CK, Weir JM, et al. (2011) Plasma lipidomic analysis of stable and unstable coronary artery disease. Arterioscler Thromb Vasc Biol 31: 2723-2732.