Fatty acid-induced atherogenic changes in extracellular matrix proteoglycans

Current Opinion in Lipidology

Volumn 18, Issue 5, 2007, Pages 546-553

  Rodriguéz Lee, Mariam ^a   Bondjers, Göran ^a,b   Camejo, Germán ^a,c  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b NORDIC SCHOOL OF PUBLIC HEALTH   (Sweden)

^c ASTRAZENECA R AND D   (Sweden)

Author keywords

Fatty acid; Hepatic proteoglycans; Intimal proteoglycans; LDL retention; VLDL remnants

Indexed keywords

BIGLYCAN; FATTY ACID; LINOLEIC ACID; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; PALMITIC ACID; PROTEIN KINASE C; PROTEOGLYCAN; VERSICAN; VERY LOW DENSITY LIPOPROTEIN;

ARTERY DISEASE; ARTERY INTIMA; ARTERY MUSCLE; ATHEROGENESIS; DYSLIPIDEMIA; ENDOTHELIUM CELL; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HUMAN; INSULIN RESISTANCE; LIVER CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REVIEW; SMOOTH MUSCLE FIBER; ZUCKER RAT;

ANIMALS; ATHEROSCLEROSIS; EXTRACELLULAR MATRIX; FATTY ACIDS; HUMANS; LIPOPROTEINS, LDL; LIPOPROTEINS, VLDL; MODELS, BIOLOGICAL; PROTEOGLYCANS;

RATTUS;

EID: 34648851432     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/MOL.0b013e3282ef534f     Document Type: Review

References (68)

1. Reaven G, Abbasi F, McLaughlin T. Obesity, insulin resistance, and cardiovascular disease. Rec Progr Horm Res 2004; 59:207-223.
2. Tannock LR, Chait A. Lipoprotein-matrix interactions in macrovascular disease in diabetes. Front Bioscien 2004; 9:1728-1742.
3. Lehto S, Rönnema T, Haffner S, et al. Dyslipidemia and hyperglycemia predict coronary heart disease events in middleaged patients with NIDDM. Diabetes 1997; 46:1354-1359.
4. Taskinen M-R. Diabetic dyslipidemia: from basic research to clinical practice. Diabetologia 2003; 46:733-749.
5. Reaven GM, Hollenbeck C, Jeng C-Y, et al. Measurement of plasma glucose free fatty acid, lactate and insulin for 24 h in patients with NIDDM. Diabetes 1989; 37:1020-1024.
6. Miles JM, Wooldridge D, Grellner WJ, et al. Nocturnal and postprandial free fatty acid kinetics in normal and type 2 diabetic subjects: effects of insulin sensitization therapy. Diabetes 2003; 52:675-681.
7. MacArthur JM, Bishop JR, Stanford KI, et al. Liver heparan sulfate proteoglycans mediate clearance of triglyceride-rich lipoproteins independently of LDL receptor family members. J Clin Invest 2007; 117:153-164. This article shows how inactivation of the enzyme complex that sulfates heparan glycosaminoglycans reduces the liver capacity to bind and internalize VLDL remnants leading to accumulation of apoB-48 and apoB-100 remnants in plasma. This effect was magnified in mice with LDL receptor deficiency.
8. Gayton J, Klemp K. Development of the lipid-rich core in human atherosclerosis. Atheroscler Thromb Vasc Biol 1996; 16:4-11.
9. Tamminen M, Mottino G, Qiao J, et al. Ultrastructure of early lipid accumulation in apoE-defficient mice. Arterioscler Thromb Vasc Biol 1999; 19:847-853.
10. Nakashima Y, Fujii H, Sumiyoshi S, et al. Early human atherosclerosis: accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler Thromb Vasc Biol 2007; 27:1159-1165. These valuable data support the hypothesis that lipid/lipoprotein deposition precedes macrophage infiltration in human coronaries.
11. Frayn K, Arner P, Yki-Jarvinen H. Fatty acid metabolism in adipose tissue, muscle and liver in health and disease. Essays Biochem 2006; 42:89-103. This is an excellent discussion of the complexities of fatty acid fluxes and utilization in different tissues with emphasis on the differences during fasting and after a meal. It provides a valuable discussion of the alterations of fatty metabolism in insulin resistance and diabetes.
12. Spector AA. Plasma albumin as a lipoprotein. In: Scanu AM, Spector AA, editors. Biochemistry and Biology of Plasma Lipoproteins. New York: Marcel Dekker; 1986. pp. 247-279.
13. Oram J, Bornfeldt K. Direct effects of long-chain nonesterified fatty acids on vascular cells and their relevance to macrovascular complications of diabetes. Front Bioscien 2004; 9:1240-1253.
14. Boden G, She P, Mozzoli M, et al. Free fatty acids produce insulin resistance and activate the proinflammatory nuclear factor-kappa B Pathway in rat liver. Diabetes 2005; 54:3458-3465.
15. Schwartz EA, Reaven PD. Molecular and signaling mechanisms of atherosclerosis in insulin resistance. Endocrinol Metab Clin Nor Amer 2006; 35:525-549. This is a comprehensive review about the basic mechanism linking atherosclerosis and insulin resistance with emphasis in the cross-talk between defects of insulin signaling and control of inflammatory pathways and cytokines.
16. Morino K, Petersen KF, Shulman GI. Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 2006; 55:S9-S15. This is an updated short review about one of the better documented hypotheses about generation of insulin resistance in humans. The discussion emphasizes data collected in vivo using nuclear magnetic resonance supporting the concept that fatty acid impairment of glucose uptake and impairment of mitochondrial function are at the root of skeletal muscle and hepatic insulin resistance.
17. Samuel VT, Liu Z-X, Wang A, et al. Inhibition of protein kinase C-epsilon prevents hepatic insulin resistance in nonalcoholic fatty liver disease. J Clin Invest 2007; 117:739-745. This provides solid data about the involvement of fatty acids and PKC activation as causes of hepatic insulin resistance.
18. 2 in vascular disease. Circ Res 2001; 89:298-304.
19. Khalil MF, Wagner WD, Goldberg IJ. Molecular interactions leading to lipoprotein retention and the initiation of atherosclerosis. Arterioscler Thromb Vasc Biol 2004; 24:2211-2218.
20. Öörni K, Kovanen P. Enhanced extracellular lipid accumulation in acidic environments. Curr Opin Lipidol 2006; 17:534-540. This is a concise review about the importance of the acid environment in LDL retention by proteoglycans and enzymatic modifications taking place in the intima.
21. Mahley RW, Huang Y. Atherogenic remnant lipoproteins: role for proteoglycans in trapping, transferring, and internalizing. [comment]. J Clin Invest 2007; 117:94-98. This is a good short discussion about the importance of the interactions of hepatic proteoglycans in processing VLDL remnants in tandem with LDL receptors and via receptor independent pathways.
22. Oakes ND, Thalen PG, Jacinto SM, Ljung B. Thiazolidinediones increase plasma-adipose tissue FFA exchange capacity and enhance insulin-mediated control of systemic FFA availability. Diabetes 2001; 50:1158-1165.
23. Hennig B, Lipke D, Biosonneault G, Ramasamy S. Role of fatty acids and eicosanoids in modulating proteoglycan metabolism in endothelial cells. Prostaglandins Leukot Essent Fatty Acids 1995; 53:315-324.
24. Hennig B, Meerani P, Ramadass P, et al. Fatty acid mediated activation of vascular endothelial cells. Metabolism 2000; 49:1006-1013.
25. Olsson U, Egnell AC, Rodríguez M, et al. Changes in matrix proteoglycans induced by insulin and fatty acids in hepatic cells may contribute to dyslipidemia of insulin resistance. Diabetes 2001; 50:2126-2132.
26. Desvergne B, Michalik L, Wahli W. Transcriptional regulation of metabolism. Physiol Rev 2006; 86:465-514. This is an extensive review on the control of integrated metabolic pathways by nuclear receptors. It provides a good discussion about how changes in genes serve metabolic adaptations.
27. Hulthe J, Bokemark L, Wikstrand J, Fagerberg BS. The metabolic syndrome, LDL particle size, and atherosclerosis: The atherosclerosis and insulin resistance (AIR) study. Arterioscler Thromb Vasc Biol 2000; 20:2140-2147.
28. Wasty F, Alavi MZ, Moore S. Distribution of glycosaminoglycans in the intima of human aortas: changes in atherosclerosis and diabetes mellitus. Diabetologia 1993; 36:316-322.
29. Camejo G. The interaction of lipids and lipoproteins with the intercellular matrix of arterial tissue: Its possible role in atherogenesis. Adv Lip Res 1982; 19:1-54.
30. Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol 1995; 15:551-561.
31. 2 in atherosclerosis. Atherosclerosis 1997; 132:1-8.
32. Öörni K, Pentikäinen M, Ala-Korpela M, Kovanen P. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J Lipid Res 2000; 41:1703-1714.
33. Gustafsson M, Borén J. Mechanisms of lipoprotein retention by the extracellular matrix. Curr Opin Lipidol 2004; 15:505-514.
34. Öörni K, Posio P, Ala-Korpela M, et al. Sphingomyelinase induces aggregation and fusion of small very low-density lipoprotein and intermediate-density lipoprotein particles and increases their retention to human arterial proteoglycans. Arterioscler Thromb Vasc Biol 2005; 25:1678-1683.
35. Vijayagopal P, Ciolino HP, Berenson GS. Endothelial cell-conditioned media modulates the synthesis and structure of proteoglycans in vascular smooth muscle cells. Biochim Biophys A 1992; 1135:129-140.
36. Vijayagopal P, Srinivasan SR, Xu J-H, et al. Lipoprotein- proteoglycan complexes induce continued cholesteryl ester accumulation in foam cells from rabbit atherosclerotic lesions. J Clin Invest 1993; 91:1011-1018.
37. Stary HC, Chandler AB, Dinsmore RE, et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis: A Report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 1995; 92:1355-1374.
38. Björnheden T, Babyi A, Bondjers G, Wiklund O. Accumulation of lipoprotein fractions and subfractions in the arterial wall, determined in an in vitro perfusion system. Atherosclerosis 1996; 123:43-56.
39. Woods A. Syndecans: transmembrane modulators of adhesion and matrix assembly. J Clin Invest 2001; 107:935-941.
40. 2 modification of lipoproteins: potential effects on atherogenesis. Adv Exp Med Biol 2002; 507:3-7.
41. Iozzo RV. Basement membrane proteoglycans from cellar to ceiling. Nature Rev Mol Cell Biol 2005; 6:646-656.
42. Little P, Tannock L, Olin K, et al. Proteoglycans synthesized by arterial smooth muscle cells in the presence of transforming growth factor-b1 exhibit increased binding to LDLs. Arterioscler Thromb Vasc Biol 2002; 22:55-60.
43. O'Brien KD, Lewis K, Fischer JW, et al. Smooth muscle cell biglycan overexpression results in increased lipoprotein retention on extracellular matrix: implications for the retention of lipoproteins in atherosclerosis. Atherosclerosis 2004; 177:29-35.
44. Wight TN, Merrilees MJ. Proteoglycans in atherosclerosis and restenosis: key roles for versican. Circ Res 2004; 94:1158-1167.
45. Han SH, Quon MJ, Koh KK. Reciprocal relationships between abnormal metabolic parameters and endothelial dysfunction. Curr Opin Lipidol 2007; 18:58-65. This is a balanced discussion about how metabolic parameters can affect insulin resistance and endothelial function and how their abnormalities can contribute to the clustering of the metabolic syndrome components and cardiovascular disease.
46. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993; 362:801-809.
47. Hsueh WA, Quinones MJ. Role of endothelial dysfunction in insulin resistance. Am J Cardiol 2003; 92:10J-17J.
48. Hennig B, Ramasamy S, Alvarado A, et al. Selective disruption of endothelial barrier function in culture by pure fatty acids and fatty acids derived from animal and plant fats. J Nutr 1993; 123:1208-1216.
49. Chen G, Wang D, Vikramadithyan R, et al. Inflammatory cytokines and fatty acids regulate endothelial cell heparanase expression. Biochemistry 2004; 43:4971-4977.
50. Pike RN, Buckle AM, le Bonniec BF, Church FC. Control of the coagulation system by serpins. Getting by with a little help from glycosaminoglycans. FEBS Journal 2005; 272:4842-4851.
51. Olsson U, Bondjers G, Camejo G. Fatty acids modulate the composition of extracellular matrix in cultured smooth muscle cells by altering the expression of genes for proteoglycan core proteins. Diabetes 1999; 48:616-622.
52. Oakes ND, Ljung B, Camejo G. Correction of dysfunctional fatty acid metabolism using peroxisome proliferator activated receptor gamma agonists. J Roy Soc Med 2002; 95:33-38.
53. Rodriguéz-Lee M, Ostergren-Lunden G, Wallin B, et al. Fatty acids cause alterations of human arterial smooth muscle cell proteoglycans that increase the affinity for low-density lipoprotein. Arterioscler Thromb Vasc Biol 2006; 26:130-135. To our knowledge this is the first description of the opposing effects of insulin and fatty acids on the control of the expression of the major cell-associated and secreted proteoglycans in aortic smooth muscle cells.
54. Kinsella MG, Bressler SL, Wight TN. The regulated synthesis of versican, decorin, and biglycan: extracellular matrix proteoglycans that influence cellular phenotype. Crit Rev Euk Gene Expr 2004; 14:203-234.
55. Jackson RL, Busch SJ, Cardin AD. Glycosaminoglycans: molecular properties, protein interactions and role in physiological processes. Physiol Rev 1991; 71:481-539.
56. Iozzo R. Matrix proteoglycans: From molecular design to cellular function. Ann Rev Biochem 1998; 67:609-652.
57. Vijayagopal P, Menon PV. Varied low density lipoprotein binding property of proteoglycans synthesized by vascular smooth muscle cells cultured on extracellular matrix. Atherosclerosis 2005; 178:75-82
58. Rask-Madsen C, King GL. Proatherosclerotic mechanisms involving protein kinase C in diabetes and insulin resistance. Arterioscler Thromb Vasc Biol 2005; 25:487-496.
59. Griffin M, Marcucci M, Cline G, et al. Free fatty acid-induced insulin resistance is associated with activation of protein kinase C θ and alterations in the insulin signaling cascade. Diabetes 1999; 48:1270-1274.
60. Getty-Kaushik L, Richard A-MT, Corkey BE. Free fatty acid regulation of glucose-dependent intrinsic oscillatory lipolysis in perifused isolated rat adipocytes. Diabetes 2005; 54:629-637.
61. Lu X, Yang Y, Howard R, Walsh JP. Fatty acids modulate protein kinase C activation in porcine vascular smooth muscle cells independently of their effect on the novo diacylglycerol synthesis. Diabetologia 2000; 43:1136-1144.
62. Lu G, Morinelli T, Meier K, et al. Oleic acid-induced mitogenic signaling in vascular smooth muscle cells: A role for protein kinase C. Circ Res 1996; 79:611-618.
63. Wallin B, Rodriguez M, Östergren G, et al. The PPARα/γ agonist tesaglitazar inhibits fatty acid-induced changes of smooth muscle cells proteoglycans: a potential antiatherogenic effect. Diabetologia 2003; 46:A292.
64. Low Wang C, Gurevich I, Draznin B. Insulin affects vascular smooth muscle cell phenotype and migration via distinct signaling pathways. Diabetes 2003; 52:2562-2569.
65. Merriles MJ, Campbell JH, Spanidis E, Campbell GR. Glycosaminoglycan synthesis by smooth muscle cells of differing phenotype and their response to endothelial cell conditioned media. Atherosclerosis 1990; 81:245-254.
66. Camejo G, Olofsson S-O, López F, et al. Identification of apoB-100 segments mediating the interaction of low density lipoproteins with arterial proteoglycans. Arteriosclerosis 1988; 8:368-377.
67. Hurt-Camejo E, Olsson U, Wiklund O, et al. Cellular consequences of the association of apoB lipoproteins with proteoglycans: potential contribution to atherogenesis. Arterioscler Thromb Vasc Biol 1997; 17:1011-1017.
68. Goldberg IJ, Dansky HM. Diabetic vascular disease: An experimental objective. Arterioscler Thromb Vasc Biol 2006; 26:1693-1701. This is an up-to-date discussion of the difficulties to evaluate the links between diabetes and atherosclerosis in available rodent models.