Insulin resistance aggravates atherosclerosis by reducing vascular smoothmuscle cell survival and increasing CX3CL1/CX3CR1 axis

Cardiovascular Research

Volumn 103, Issue 2, 2014, Pages 324-336

  Martínez Hervás, Sergio ^a,b,c,d   Vinué, Ángela ^b   Núñez, Laura ^b   Andrés Blasco, Irene ^b   Piqueras, Laura ^b   TomásReal, José ^a,b,c,d   Ascaso, Juan Francisco ^a,b,c,d   Burks, Deborah Jane ^d,e   Sanz, María Jesús ^b,c   González Navarro, Herminia ^b,d  

^a HOSPITAL CLÍNICO UNIVERSITARIO   (Spain)

^b Instituto Universitario IVI INCLIVA   (Spain)

^c UNIVERSITY OF VALENCIA   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

^e CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

Atherosclerosis; Inflammation; Insulin resistance; Unstable plaque; Vascular smooth muscle cell

Indexed keywords

APOLIPOPROTEIN E; CHEMOKINE RECEPTOR CX3CR1; FRACTALKINE; INSULIN; INSULIN RECEPTOR SUBSTRATE 2; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; ORAL ANTIDIABETIC AGENT; PROTEIN KINASE B; CHEMOKINE RECEPTOR; CX3CL1 PROTEIN, HUMAN; CX3CL1 PROTEIN, MOUSE; CX3CR1 PROTEIN, HUMAN; CX3CR1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; CAROTID ATHEROSCLEROSIS; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; INSULIN RESISTANCE; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; MONOCYTE; MOUSE; MOUSE MODEL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR SMOOTH MUSCLE; ANIMAL; ATHEROSCLEROSIS; C57BL MOUSE; CELL CULTURE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELL SURVIVAL; CELLS, CULTURED; CHEMOKINE CX3CL1; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN RESISTANCE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; RECEPTORS, CHEMOKINE; SIGNAL TRANSDUCTION;

EID: 84904365676     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu115     Document Type: Article

References (44)

1. Hossain P, Kawar B, El Nahas M. Obesity and diabetes in the developing world-A growing challenge. N Engl J Med 2007;356:213-215 (Pubitemid 46143224)
2. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr. Harmonizing the metabolic syndrome: A joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009;120:1640-1645
3. Semenkovich CF. Insulin resistance and atherosclerosis. J Clin Invest 2006;116: 1813-1822 (Pubitemid 44033301)
4. Reaven G. Why syndrome X? From Harold Himsworth to the insulin resistance syndrome. Cell Metab 2005;1:9-14 (Pubitemid 43960585)
5. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004;27:1047-1053 (Pubitemid 38579764)
6. Pirro M, Mauriege P, Tchernof A, Cantin B, Dagenais GR, Despres JP, Lamarche B. Plasma free fatty acid levels and the risk of ischemic heart disease in men: prospective results from the Quebec Cardiovascular Study. Atherosclerosis 2002;160:377-384 (Pubitemid 34159331)
7. DeFronzo RA. Insulin resistance, lipotoxicity, type 2 diabetes and atherosclerosis: the missing links. The Claude Bernard Lecture 2009. Diabetologia 2010;53:1270-1287
8. Dickson BC, Gotlieb AI. Towards understanding acute destabilization of vulnerable atherosclerotic plaques. Cardiovasc Pathol 2003;12:237-248 (Pubitemid 37162706)
9. Glass CK, Witztum JL. Atherosclerosis: the road ahead. Cell 2001;104:503-516 (Pubitemid 32201946)
10. Steinberg D. Atherogenesis in perspective: hypercholesterolemia and inflammation as partners in crime. Nat Med 2002;8:1211-1217 (Pubitemid 35373551)
11. Clarke MC, Littlewood TD, Figg N, Maguire JJ, Davenport AP, Goddard M, Bennett MR. Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res 2008;102: 1529-1538
12. Wang JC, Bennett M. Aging and atherosclerosis: mechanisms, functional consequences, and potential therapeutics for cellular senescence. Circ Res 2012;111: 245-259
13. Tsukano H, Gotoh T, Endo M, Miyata K, Tazume H, Kadomatsu T, Yano M, Iwawaki T, Kohno K, Araki K, Mizuta H, Oike Y. The endoplasmic reticulum stress-C/EBP homologous protein pathway-mediated apoptosis in macrophages contributes to the instability of atherosclerotic plaques. Arterioscler Thromb Vasc Biol 2010;30:1925-1932
14. Bornfeldt KE, Tabas I. Insulin resistance, hyperglycemia, and atherosclerosis. Cell Metab 2011;14:575-585
15. Wang ZH, Shang YY, Zhang S, Zhong M,Wang XP, Deng JT, Pan J, Zhang Y, ZhangW. Silence of TRIB3 suppresses atherosclerosis and stabilizes plaques in diabetic ApoE-/-/LDL receptor-/- mice. Diabetes 2012;61:463-473
16. Tabas I, Tall A, Accili D. The impact of macrophage insulin resistance on advanced atherosclerotic plaque progression. Circ Res 2010;106:58-67
17. Nakazawa T, Chiba T, Kaneko E, Yui K, Yoshida M, Shimokado K. Insulin signaling in arteries prevents smooth muscle apoptosis. Arterioscler Thromb Vasc Biol 2005;25: 760-765 (Pubitemid 40463866)
18. Engberding N, San Martin A, Martin-Garrido A, Koga M, Pounkova L, Lyons E, Lassegue B, Griendling KK. Insulin-like growth factor-1 receptor expression masks the antiinflammatory and glucose uptake capacity of insulin in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2009;29:408-415
19. Apostolakis S, Krambovitis E, Vlata Z, Kochiadakis GE, Baritaki S, Spandidos DA. CX3CR1 receptor is up-regulated in monocytes of coronary artery diseased patients: impact of pre-inflammatory stimuli and renin-angiotensin system modulators. Thromb Res 2007;121:387-395
20. Cheng C, Tempel D, van Haperen R, de Boer HC, Segers D, Huisman M, van Zonneveld AJ, Leenen PJ, van der Steen A, Serruys PW, de Crom R, Krams R. Shear stress-induced changes in atherosclerotic plaque composition are modulated by chemokines. J Clin Invest 2007;117:616-626 (Pubitemid 46348520)
21. MatthewsDR, Hosker JP, Rudenski AS, Naylor BA, TreacherDF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412-419 (Pubitemid 15018832)
22. Gonzalez-Navarro H, Vinue A, Vila-Caballer M, Fortuno A, Beloqui O, Zalba G, BurksD,Diez J,Andres V.Molecularmechanisms of atherosclerosis inmetabolic syndrome: role of reduced IRS2-dependent signaling. Arterioscler Thromb Vasc Biol 2008; 28:2187-2194
23. Withers DJ, Burks DJ, Towery HH, Altamuro SL, Flint CL, White MF. IRS-2 coordinates IGF-1 receptor-mediated beta-cell development and peripheral insulin signalling. Nat Genet 1999;23:32-40 (Pubitemid 29418784)
24. Cho H, Mu J, Kim JK, Thorvaldsen JL, Chu Q, Crenshaw EB III, Kaestner KH, Bartolomei MS, Shulman GI, Birnbaum MJ. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 2001;292: 1728-1731 (Pubitemid 32506248)
25. Gorenne I, Kavurma M, Scott S, Bennett M. Vascular smooth muscle cell senescence in atherosclerosis. Cardiovasc Res 2006;72:9-17 (Pubitemid 44310633)
26. Combadiere C, Potteaux S, Gao JL, Esposito B, Casanova S, Lee EJ, Debre P, Tedgui A, Murphy PM, Mallat Z. Decreased atherosclerotic lesion formation in CX3CR1/apolipoprotein E double knockout mice. Circulation 2003;107:1009-1016 (Pubitemid 36258725)
27. Kozakova M, Natali A, Dekker J, Beck-Nielsen H, Laakso M, Nilsson P, Balkau B, Ferrannini E. Insulin sensitivity and carotid intima-media thickness: relationship between insulin sensitivity and cardiovascular risk study. Arterioscler Thromb Vasc Biol 2013;33:1409-1417
28. Polak JF, Person SD, Wei GS, Godreau A, Jacobs DR Jr, Harrington A, Sidney S, O'Leary DH. Segment-specific associations of carotid intima-media thickness with cardiovascular risk factors: the Coronary Artery Risk Development in Young Adults (CARDIA) study. Stroke 2010;41:9-15
29. American Heart Association. Heart and stroke Facts: 2001 Statistical Supplement. Dallas: American Heart Association, 2001
30. RiusC,Company C, Piqueras L, Cerda-Nicolas JM, Gonzalez C, Servera E, LudwigA, Morcillo EJ, Sanz MJ. Critical role of fractalkine (CX3CL1) in cigarette smokeinduced mononuclear cell adhesion to the arterial endothelium. Thorax 2013;68: 177-186
31. Teupser D, Pavlides S, Tan M, Gutierrez-Ramos JC, Kolbeck R, Breslow JL. Major reduction of atherosclerosis in fractalkine (CX3CL1)-deficient mice is at the brachiocephalic artery, not the aortic root. Proc Natl Acad Sci USA 2004;101:17795-17800 (Pubitemid 40051966)
32. White GE, Greaves DR. Fractalkine: A survivor's guide: chemokines as antiapoptotic mediators. Arterioscler Thromb Vasc Biol 2012;32:589-594
33. Cardellini M, Menghini R, Luzi A, Davato F, Cardolini I, D'Alfonso R, Gentileschi P, Rizza S, Marini MA, Porzio O, Lauro D, Sbraccia P, Lauro R, Federici M. Decreased IRS2 and TIMP3 expression in monocytes from offspring of type 2 diabetic patients is correlated with insulin resistance and increased intima-media thickness. Diabetes 2011;60: 3265-3270
34. Baumgartl J, Baudler S, Scherner M, Babaev V, Makowski L, Suttles J, McDuffie M, Tobe K, Kadowaki T, Fazio S, Kahn CR, Hotamisligil GS, KroneW, Linton M, Bruning JC. Myeloid lineage cell-restricted insulin resistance protects apolipoprotein E-deficient mice against atherosclerosis. Cell Metab 2006;3:247-256
35. Liang CP, Han S, Okamoto H, Carnemolla R, Tabas I, Accili D, Tall AR. Increased CD36 protein as a response to defective insulin signaling in macrophages. J Clin Invest 2004;113: 764-773 (Pubitemid 38544170)
36. Han S, LiangCP, DeVries-SeimonT, Ranalletta M,Welch CL, Collins-Fletcher K, Accili D, Tabas I, Tall AR. Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions. Cell Metab 2006;3:257-266
37. Howard G, O'Leary DH, Zaccaro D, Haffner S, Rewers M, Hamman R, Selby JV, Saad MF, Savage P, Bergman R. Insulin sensitivity and atherosclerosis. The Insulin Resistance Atherosclerosis Study (IRAS) Investigators. Circulation 1996;93:1809-1817 (Pubitemid 26154032)
38. Shai SY, Sukhanov S, Higashi Y, Vaughn C, Kelly J, Delafontaine P. Smooth muscle cellspecific insulin-like growth factor-1 overexpression in Apoe-/- mice does not alter atherosclerotic plaque burden but increases features of plaque stability. Arterioscler Thromb Vasc Biol 2010;30:1916-1924
39. Allard D, Figg N, Bennett MR, Littlewood TD. Akt regulates the survival of vascular smooth muscle cells via inhibition of FoxO3a and GSK3. J Biol Chem 2008;283: 19739-19747
40. Fernandez-Hernando C, Jozsef L, Jenkins D, Di Lorenzo A, Sessa WC. Absence of Akt1 reduces vascular smooth muscle cell migration and survival and induces features of plaque vulnerability and cardiac dysfunction during atherosclerosis. Arterioscler Thromb Vasc Biol 2009;29:2033-2040
41. Castro C, Diez-Juan A, Cortes MJ, Andres V. Distinct regulation of mitogen-activated protein kinases and p27Kip1 in smooth muscle cells fromdifferent vascular beds. A potential role in establishing regional phenotypic variance. J Biol Chem 2003;278:4482-4490 (Pubitemid 36800943)
42. Hennige AM, Burks DJ, Ozcan U, Kulkarni RN, Ye J, Park S, Schubert M, Fisher TL, DowMA, Leshan R, Zakaria M, Mossa-Basha M, WhiteMF. Upregulation of insulin receptor substrate-2 in pancreatic beta cells prevents diabetes. J Clin Invest 2003;112: 1521-1532 (Pubitemid 38056278)
43. Apostolakis S, Baritaki S, KochiadakisGE, IgoumenidisNE, Panutsopulos D, SpandidosDA. Effects of polymorphismsin chemokine ligands and receptors on susceptibility to coronary artery disease. Thromb Res 2007;119:63-71 (Pubitemid 44724920)
44. Lucas AD, Bursill C, Guzik TJ, Sadowski J, Channon KM, Greaves DR. Smooth muscle cells in human atherosclerotic plaques express the fractalkine receptor CX3CR1 and undergo chemotaxis to the CX3C chemokine fractalkine (CX3CL1). Circulation 2003; 108:2498-2504 (Pubitemid 37444412)