Transforming growth factor-β regulation of proteoglycan synthesis in vascular smooth muscle: Contribution to lipid binding and accelerated atherosclerosis in diabetes

Journal of Diabetes

Volumn 2, Issue 4, 2010, Pages 233-242

  Yang, Sundy N Y ^a   Burch, Micah L ^a,b   Tannock, Lisa R ^c   Evanko, Stephen ^d   Osman, Narin ^a,b   Little, Peter J ^a,b  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF KENTUCKY   (United States)

^d BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

macrovascular disease; response to retention; Smads

Indexed keywords

AGGRECAN; BIGLYCAN; DECORIN; LIPID; LOW DENSITY LIPOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PERLECAN; PROTEOGLYCAN; SMAD PROTEIN; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; VERSICAN;

ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; DIABETES MELLITUS; HUMAN; HYPERGLYCEMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PHOSPHORYLATION; PROTEOGLYCAN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE;

ANIMALS; ATHEROSCLEROSIS; DIABETES MELLITUS; EXTRACELLULAR MATRIX; HUMANS; LIPOPROTEINS, LDL; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE, SMOOTH, VASCULAR; PROTEOGLYCANS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 78649645445     PISSN: 17530393     EISSN: 17530407     Source Type: Journal    
DOI: 10.1111/j.1753-0407.2010.00089.x     Document Type: Review

References (97)

1. Hozawa A, Folsom AR, Sharrett AR, Chambless LE,. Absolute and attributable risks of cardiovascular disease incidence in relation to optimal and borderline risk factors: Comparison of African American with white subjects Atherosclerosis Risk in Communities Study. Arch Intern Med. 2007; 167: 573-9.
2. Zimmet PZ, Mccarty DJ, De Courten MP,. The global epidemiology of non-insulin-dependent diabetes mellitus and the metabolic syndrome. J Diabetes Complications. 1997; 11: 60-8.
3. Hunt KJ, Resendez RG, Williams K, Haffner SM, Stern MP,. National Cholesterol Education Program versus World Health Organization metabolic syndrome in relation to all-cause and cardiovascular mortality in the San Antonio Heart Study. Circulation. 2004; 110: 1251-7.
4. Pfeiffer A, Schatz H,. Diabetic microvascular complications and growth factors. Exp Clin Endocrinol Diabetes. 1995; 103: 7-14.
5. Adler AI, Stratton IM, Neil HA, et al. Association of systolic blood pressure with macrovascular and microvascular complications of type 2 diabetes (UKPDS 36): Prospective observational study. BMJ. 2000; 321: 412-19.
6. Soedamah-Muthu SS, Fuller JH, Mulnier HE, et al. All-cause mortality rates in patients with type 1 diabetes mellitus compared with a non-diabetic population from the UK general practice research database, 1992-1999. Diabetologia. 2006; 49: 660-6.
7. Nigro J, Osman N, Dart AM, Little PJ,. Insulin resistance and atherosclerosis. Endocr Rev. 2006; 27: 242-59.
8. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M,. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med. 1998; 339: 229-34.
9. Howard G, O'leary DH, Zaccaro D, et al. Insulin sensitivity and atherosclerosis The Insulin Resistance Atherosclerosis Study (IRAS) Investigators. Circulation. 1996; 93: 1809-17.
10. Ross R,. The pathogenesis of atherosclerosis. N Engl J Med. 1986; 314: 488-500.
11. Ross R,. Atherosclerosis: An inflammatory disease. N Engl J Med. 1999; 340: 115-26.
12. Libby P,. Vascular biology of atherosclerosis: Overview and state of the art. Am J Cardiol. 2003; 91 (Suppl. 1): 3A-6A.
13. Williams KJ, Tabas I,. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol. 1995; 15: 551-61.
14. Little PJ, Osman N, O'brien KD,. Hyperelongated biglycan: The surreptitious initiator of atherosclerosis. Curr Opin Lipidol. 2008; 19: 448-54.
15. Davies MJ,. Stability and instability: Two faces of coronary atherosclerosis The Paul Dudley White lecture 1995. Circulation. 1996; 94: 2013-20.
16. Falk E,. Morphologic features of unstable atherothrombotic plaques underlying acute coronary syndromes. Am J Cardiol. 1989; 63: 114E-20E.
17. Cooper R, Cutler J, Desvigne-Nickens P, et al. Trends and disparities in coronary heart disease, stroke, and other cardiovascular diseases in the United States: Findings of the national conference on cardiovascular disease prevention. Circulation. 2000; 102: 3137-47.
18. Gaede P, Vedel P, Larsen N, et al. Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. N Engl J Med. 2003; 348: 383-93.
19. Finn AV, Kramer MC, Vorpahl M, Kolodgie FD, Virmani R,. Pharmacotherapy of coronary atherosclerosis. Expert Opin Pharmacother. 2009; 10: 1587-603.
20. Beckman JA, Creager MA, Libby P,. Diabetes and atherosclerosis: Epidemiology, pathophysiology, and management. JAMA. 2002; 287: 2570-81.
21. Berry C, Noble S, Gregoire JC, et al. Glycaemic status influences the nature and severity of coronary artery disease. Diabetologia. 2010; 53: 652-8.
22. Nissen SE, Wolski K,. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N Engl J Med. 2007; 356: 2457-71.
23. Diamond GA, Bax L, Kaul S,. Uncertain effects of rosiglitazone on the risk for myocardial infarction and cardiovascular death. Ann Intern Med. 2007; 147: 578-81.
24. Chait A, Bornfeldt KE,. Diabetes and atherosclerosis: Is there a role for hyperglycemia? J Lipid Res. 2009; 50 (Suppl.): S335-9.
25. Ross R, Glomset JA,. The pathogenesis of atherosclerosis (second of two parts). N Engl J Med. 1976; 295: 420-5.
26. Tabas I, Williams KJ, Boren J,. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: Update and therapeutic implications. Circulation. 2007; 116: 1832-44.
27. Berliner JA, Navab M, Fogelman AM, et al. Atherosclerosis: Basic mechanisms oxidation, inflammation, and genetics. Circulation. 1995; 91: 2488-96.
28. Brownlee M,. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001; 414: 813-20.
29. Cooper ME, Bonnet F, Oldfield M, Jandeleit-Dahm K,. Mechanisms of diabetic vasculopathy: An overview. Am J Hypertens. 2001; 14: 475-86.
30. Nakashima Y, Fujii H, Sumiyoshi S, Wight TN, Sueishi K,. Early human atherosclerosis: Accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler Thromb Vasc Biol. 2007; 27: 1159-65.
31. Nakashima Y, Wight TN, Sueishi K,. Early atherosclerosis in humans: Role of diffuse intimal thickening and extracellular matrix proteoglycans. Cardiovasc Res. 2008; 79: 14-23.
32. Wight TN,. Proteoglycans in pathological conditions: Atherosclerosis. Fed Proc. 1985; 44: 381-5.
33. Camejo G, Hurt-Camejo E, Olsson U, Bondjers G,. Proteoglycans and lipoproteins in atherosclerosis. Curr Opin Lipidol. 1993; 4: 385-91.
34. Little PJ, Ballinger ML, Osman N,. Vascular wall proteoglycan synthesis and structure as a target for the prevention of atherosclerosis. Vasc Health Risk Manag. 2007; 3: 1-8.
35. Ballinger ML, Nigro J, Frontanilla KV, Dart AM, Little PJ,. Regulation of glycosaminoglycan structure and atherogenesis. Cell Mol Life Sci. 2004; 61: 1296-306.
36. Tannock L, Little PJ, Wight TN, Chait A,. Arterial smooth muscle cell proteoglycans synthesized in the presence of glucosamine demonstrate reduced binding to LDL. J Lipid Res. 2002; 43: 149-57.
37. Wilson P, Drennon K, Tannock LR,. Regulation of vascular proteoglycan synthesis by metabolic factors associated with diabetes. J Investig Med. 2007; 55: 18-25.
38. Little PJ, Drennon KD, Tannock LR,. Glucosamine inhibits the synthesis of glycosaminoglycan chains on vascular smooth muscle cell proteoglycans by depletion of ATP. Arch Physiol Biochem. 2008; 114: 120-6.
39. Little PJ, Tannock L, Olin KL, Chait A, Wight TN,. Proteoglycans synthesized by arterial smooth muscle cells in the presence of transforming growth factor-beta1 exhibit increased binding to LDLs. Arterioscler Thromb Vasc Biol. 2002; 22: 55-60.
40. Silbert JE, Sugumaran G,. Biosynthesis of chondroitin/dermatan sulfate. IUBMB Life. 2002; 54: 177-86.
41. Arner P,. Insulin resistance in type 2 diabetes: Role of fatty acids. Diabetes Metab Res Rev. 2002; 18 (Suppl. 2): S5-9.
42. Olsson U, Bondjers G, Camejo G,. Fatty acids modulate the composition of extracellular matrix in cultured human arterial smooth muscle cells by altering the expression of genes for proteoglycan core proteins. Diabetes. 1999; 48: 616-22.
43. Sharma K, Ziyadeh FN, Alzahabi B, et al. Increased renal production of transforming growth factor-beta1 in patients with type II diabetes. Diabetes. 1997; 46: 854-9.
44. Schonherr E, Jarvelainen HT, Sandell LJ, Wight TN,. Effects of platelet-derived growth factor and transforming growth factor-beta 1 on the synthesis of a large versican-like chondroitin sulfate proteoglycan by arterial smooth muscle cells. J Biol Chem. 1991; 266: 17640-7.
45. Schonherr E, Jarvelainen HT, Kinsella MG, Sandell LJ, Wight TN,. Platelet-derived growth factor and transforming growth factor-beta 1 differentially affect the synthesis of biglycan and decorin by monkey arterial smooth muscle cells. Arterioscler Thromb. 1993; 13: 1026-36.
46. Dadlani H, Ballinger ML, Osman N, Getachew R, Little PJ,. Smad and p38 MAP kinase-mediated signaling of proteoglycan synthesis in vascular smooth muscle. J Biol Chem. 2008; 283: 7844-52.
47. Burch ML, Yang SN, Ballinger ML, et al. TGF-b stimulates biglycan synthesis via p38 and ERK phosphorylation of the linker region of Smad 2. Cell Mol Life Sci. 2010; 67: 2077-90.
48. Massague J, Blain SW, Lo RS,. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell. 2000; 103: 295-309.
49. Agrotis A, Kalinina N, Bobik A,. Transforming growth factor-beta, cell signaling and cardiovascular disorders. Curr Vasc Pharmacol. 2005; 3: 55-61.
50. Derynck R, Zhang YE,. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature. 2003; 425: 577-84.
51. Wu L, Derynck R,. Essential role of TGF-beta signaling in glucose-induced cell hypertrophy. Dev Cell. 2009; 17: 35-48.
52. Bobik A, Agrotis A, Kanellakis P, et al. Distinct patterns of transforming growth factor-beta isoform and receptor expression in human atherosclerotic lesions colocalization implicates TGF-beta in fibrofatty lesion development. Circulation. 1999; 99: 2883-91.
53. Evanko SP, Raines EW, Ross R, Gold LI, Wight TN,. Proteoglycan distribution in lesions of atherosclerosis depends on lesion severity, structural characteristics, and the proximity of platelet-derived growth factor and transforming growth factor-beta. Am J Pathol. 1998; 152: 533-46.
54. Massague J,. TGF-beta signal transduction. Annu Rev Biochem. 1998; 67: 753-91.
55. Grady WM,. Transforming growth factor-beta, Smads, and cancer. Clin Cancer Res. 2005; 11: 3151-4.
56. Taya Y, O'kane S, Ferguson MW,. Pathogenesis of cleft palate in TGF-beta3 knockout mice. Development. 1999; 126: 3869-79.
57. Letterio JJ, Roberts AB,. Transforming growth factor-beta1-deficient mice: Identification of isoform-specific activities in vivo. J Leukoc Biol. 1996; 59: 769-74.
58. Molin DG, Deruiter MC, Wisse LJ, et al. Altered apoptosis pattern during pharyngeal arch artery remodelling is associated with aortic arch malformations in Tgfbeta2 knock-out mice. Cardiovasc Res. 2002; 56: 312-22.
59. Derynck R, Jarrett JA, Chen EY, et al. Human transforming growth factor-beta complementary DNA sequence and expression in normal and transformed cells. Nature. 1985; 316: 701-5.
60. Khalil N,. TGF-beta: From latent to active. Microbes Infect. 1999; 1: 1255-63.
61. Rifkin DB,. Latent transforming growth factor-beta (TGF-beta) binding proteins: Orchestrators of TGF-beta availability. J Biol Chem. 2005; 280: 7409-12.
62. Dubois CM, Laprise MH, Blanchette F, Gentry LE, Leduc R,. Processing of transforming growth factor beta 1 precursor by human furin convertase. J Biol Chem. 1995; 270: 10 618-24.
63. Annes JP, Munger JS, Rifkin DB,. Making sense of latent TGFbeta activation. J Cell Sci. 2003; 116: 217-24.
64. Lee MK, Pardoux C, Hall MC, et al. TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. EMBO J. 2007; 26: 3957-67.
65. Dore JJ Jr, Edens M, Garamszegi N, Leof EB,. Heteromeric and homomeric transforming growth factor-beta receptors show distinct signaling and endocytic responses in epithelial cells. J Biol Chem. 1998; 273: 31277-7.
66. Cheifetz S, Andres JL, Massague J,. The transforming growth factor-beta receptor type III is a membrane proteoglycan Domain structure of the receptor. J Biol Chem. 1988; 263: 16984-91.
67. Munir S, Xu G, Wu Y, et al. Nodal and ALK7 inhibit proliferation and induce apoptosis in human trophoblast cells. J Biol Chem. 2004; 279: 31277-86.
68. Javelaud D, Mauviel A,. Crosstalk mechanisms between the mitogen-activated protein kinase pathways and Smad signaling downstream of TGF-beta: Implications for carcinogenesis. Oncogene. 2005; 24: 5742-50.
69. Moustakas A, Souchelnytskyi S, Heldin CH,. Smad regulation in TGF-beta signal transduction. J Cell Sci. 2001; 114: 4359-69.
70. Wu JW, Hu M, Chai J, et al. Crystal structure of a phosphorylated Smad2 recognition of phosphoserine by the MH2 domain and insights on Smad function in TGF-beta signaling. Mol Cell. 2001; 8: 1277-89.
71. Shi Y, Hata A, Lo RS, Massague J, Pavletich NP,. A structural basis for mutational inactivation of the tumour suppressor Smad4. Nature. 1997; 388: 87-93.
72. Itoh F, Asao H, Sugamura K, et al. Promoting bone morphogenetic protein signaling through negative regulation of inhibitory Smads. EMBO J. 2001; 20: 4132-42.
73. Kretzschmar M, Doody J, Timokhina I, Massague J,. A mechanism of repression of TGFbeta/Smad signaling by oncogenic Ras. Genes Dev. 1999; 13: 804-16.
74. Richardson PD, Davies MJ, Born GV,. Influence of plaque configuration and stress distribution on fissuring of coronary atherosclerotic plaques. Lancet. 1989; 2: 941-4.
75. Camejo G, Hurt-Camejo E, Wiklund O, Bondjers G,. Association of apo B lipoproteins with arterial proteoglycans: Pathological significance and molecular basis. Atherosclerosis. 1998; 139: 205-22.
76. Wight TN, Merrilees MJ,. Proteoglycans in atherosclerosis and restenosis: Key roles for versican. Circ Res. 2004; 94: 1158-67.
77. Yamaguchi Y, Mann DM, Ruoslahti E,. Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature. 1990; 346: 281-4.
78. Yanagishita M,. Function of proteoglycans in the extracellular matrix. Acta Pathol Jpn. 1993; 43: 283-93.
79. Lendon CL, Davies MJ, Born GV, Richardson PD,. Atherosclerotic plaque caps are locally weakened when macrophages density is increased. Atherosclerosis. 1991; 87: 87-90.
80. Davies MJ, Richardson PD, Woolf N, Katz DR, Mann J,. Risk of thrombosis in human atherosclerotic plaques: Role of extracellular lipid, macrophage, and smooth muscle cell content. Br Heart J. 1993; 69: 377-81.
81. Nikkari ST, Jarvelainen HT, Wight TN, Ferguson M, Clowes AW,. Smooth muscle cell expression of extracellular matrix genes after arterial injury. Am J Pathol. 1994; 144: 1348-56.
82. Davies MJ, Woolf N, Robertson WB,. Pathology of acute myocardial infarction with particular reference to occlusive coronary thrombi. Br Heart J. 1976; 38: 659-64.
83. Williams KJ, Fless GM, Petrie KA, et al. Mechanisms by which lipoprotein lipase alters cellular metabolism of lipoprotein(a), low density lipoprotein, and nascent lipoproteins roles for low density lipoprotein receptors and heparan sulfate proteoglycans. J Biol Chem. 1992; 267: 13284-92.
84. Little PJ, Ballinger ML, Burch ML, Osman N,. Biosynthesis of natural and hyperelongated chondroitin sulfate glycosaminoglycans: New insights into an elusive process. Open Biochem J. 2008; 2: 135-42.
85. Boren J, Olin K, Lee I, et al. Identification of the principal proteoglycan-binding site in LDL A single-point mutation in apo-B100 severely affects proteoglycan interaction without affecting LDL receptor binding. J Clin Invest. 1998; 101: 2658-64.
86. Flood C, Gustafsson M, Richardson PE, et al. Identification of the proteoglycan binding site in apolipoprotein B48. J Biol Chem. 2002; 277: 32228-33.
87. Hoff HF, Wagner WD,. Plasma low density lipoprotein accumulation in aortas of hypercholesterolemic swine correlates with modifications in aortic glycosaminoglycan composition. Atherosclerosis. 1986; 61: 231-6.
88. Libby P,. Inflammation in atherosclerosis. Nature. 2002; 420: 868-74.
89. Dahl-Jorgensen K, Larsen JR, Hanssen KF,. Atherosclerosis in childhood and adolescent type 1 diabetes: Early disease, early treatment? Diabetologia. 2005; 48: 1445-53.
90. Wight TN,. Cell biology of arterial proteoglycans. Artheriosclerosis. 1989; 9: 1-20.
91. Cardoso LEM, Little PJ, Ballinger ML, et al. Platelet-derived growth factor differentially regulates the expression and post-translational modification of versican by arterial smooth muscle cells through distinct protein kinase C and exracellular signal-regulated kinase pathways. J Biol Chem. 2009; 285: 6987-95.
92. Ballinger ML, Osman N, Hashimura K, et al. Imatinib inhibits vascular smooth muscle proteoglycan synthesis and reduces LDL binding in vitro and aortic lipid deposition in vivo. J Cell Mol Med. 2010; 14: 1408-18.
93. Ivey ME, Little PJ,. Thrombin regulates vascular smooth muscle cell proteoglycan synthesis via PAR-1 and multiple downstream signalling pathways. Thromb Res. 2008; 123: 280-97.
94. A receptors on human vascular smooth muscle cells to yield proteoglycans with increased binding to LDL. Atherosclerosis. 2009; 205: 451-7.
95. Yang SN, Burch ML, Getachew R, et al. Growth factor-mediated hyper-elongation of glycosaminoglycan chains on biglycan requires transcription and translation. Arch Physiol Biochem. 2009; 115: 147-54.
96. Nigro J, Dilley RJ, Little PJ,. Differential effects of gemfibrozil on migration, proliferation and proteoglycan production in human vascular smooth muscle cells. Atherosclerosis. 2002; 162: 119-29.
97. De Dios ST, Frontanilla KV, Nigro J, et al. Regulation of the atherogenic properties of vascular smooth muscle proteoglycans by oral anti-hyperglycemic agents. J Diabetes Complications. 2007; 21: 108-17.