Glucose downregulation of PKG-I protein mediates increased thrombospondin1-dependent TGF-β activity in vascular smooth muscle cells

American Journal of Physiology - Cell Physiology

Volumn 298, Issue 5, 2010, Pages

  Wang, Shuxia ^a,b   Lincoln, Thomas M ^c   Murphy Ullrich, Joanne E ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF SOUTH ALABAMA   (United States)

Author keywords

Fibronectin; Transforming growth factor

Indexed keywords

CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; FIBRONECTIN; GLUCOSE; MESSENGER RNA; NITRIC OXIDE DONOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; AORTA MEDIA; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DENSITOMETRY; DOWN REGULATION; IMMUNOBLOTTING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELLS, CULTURED; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DIABETES MELLITUS; DOWN-REGULATION; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE; RNA, MESSENGER; THROMBOSPONDIN 1; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

MURINAE;

EID: 77951488226     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00330.2009     Document Type: Article

References (53)

1. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, Rifkin DB. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem 216: 276-284, 1994. (Pubitemid 24076008)
2. Belmadani S, Bernal J, Wei CC, Pallero MA, Dell'italia L, Murphy-Ullrich JE, Berecek KH. A thrombospondin-1 antagonist of transforming growth factor-beta activation blocks cardiomyopathy in rats with diabetes and elevated angiotensin II. Am J Pathol 171: 777-789, 2007. (Pubitemid 47440977)
3. Bhattacharyya S, Marinic TE, Krukovets I, Hoppe G, Stenina OI. Cell type-specific post-transcriptional regulation of production of the potent antiangiogenic and proatherogenic protein thrombospondin-1 by high glucose. J Biol Chem 283: 5699-5707, 2008.
4. Boerth NJ, Dey NB, Cornwell TL, Lincoln TM. Cyclic GMP-dependent protein kinase regulates vascular smooth muscle cell phenotype. J Vasc Res 34: 245-259, 1997.
5. Bornstein P. Thrombospondins as matricellular modulators of cell function. J Clin Invest 107: 929-934, 2001. (Pubitemid 32323400)
6. Bornstein P, Agah A, Kyriakides TR. The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury. Int J Biochem Cell Biol 36: 1115-1125, 2004. (Pubitemid 38501563)
7. Carter AJ, Bailey L, Devries J, Hubbard B. The effects of uncontrolled hyperglycemia on thrombosis and formation of neointima after coronary stent placement in a novel diabetic porcine model of restenosis. Coron Artery Dis 11: 473-479, 2000. (Pubitemid 30663859)
8. Chamberlain J. Transforming growth factor-beta: a promising target for anti-stenosis therapy. Cardiovasc Drug Rev 19: 329-344, 2001. (Pubitemid 34260703)
9. Chamberlain J, Gunn J, Francis SE, Holt CM, Arnold ND, Cumberland DC, Ferguson MW, Crossman DC. TGFbeta is active, and correlates with activators of TGFbeta, following porcine coronary angioplasty. Cardiovasc Res 50: 125-136, 2001. (Pubitemid 32244392)
10. Crawford SE, Stellmach V, Murphy-Ullrich JE, Ribeiro SM, Lawler J, Hynes RO, Boivin GP, Bouck N. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 93: 1159-1170, 1998. (Pubitemid 28307421)
11. Dabir P, Marinic TE, Krukovets I, Stenina OI. Aryl hydrocarbon receptor is activated by glucose and regulates the thrombospondin-1 gene promoter in endothelial cells. Circ Res 102: 1558-1565, 2008.
12. Daniel C, Amann K, Hohenstein B, Bornstein P, Hugo C. Thrombospondin 2 functions as an endogenous regulator of angiogenesis and inflammation in experimental glomerulonephritis in mice. J Am Soc Nephrol 18: 788-798, 2007. (Pubitemid 46434496)
13. Daniel C, Schaub K, Amann K, Lawler J, Hugo C. Thrombospondin-1 is an endogenous activator of TGF-beta in experimental diabetic nephropathy in vivo. Diabetes 56: 2982-2989, 2007. (Pubitemid 350223633)
14. Daniel C, Takabatake Y, Mizui M, Isaka Y, Kawashi H, Rupprecht H, Imai E, Hugo C. Antisense oligonucleotides against thrombospondin-1 inhibit activation of TGF-beta in fibrotic renal disease in the rat in vivo. Am J Pathol 163: 1185-1192, 2003. (Pubitemid 37040154)
15. Daniel C, Wiede J, Krutzsch HC, Ribeiro SM, Roberts DD, Murphy-Ullrich JE, Hugo C. Thrombospondin-1 is a major activator of TGF-beta in fibrotic renal disease in the rat in vivo. Kidney Int 65: 459-468, 2004. (Pubitemid 38130640)
16. Dey NB, Boerth NJ, Murphy-Ullrich JE, Chang PL, Prince CW, Lincoln TM. Cyclic GMP-dependent protein kinase inhibits osteopontin and thrombospondin production in rat aortic smooth muscle cells. Circ Res 82: 139-146, 1998. (Pubitemid 28080096)
17. Donoviel DB, Amacher SL, Judge KW, Bornstein P. Thrombospondin gene expression is associated with mitogenesis in 3T3 cells: induction by basic fibroblast growth factor. J Cell Physiol 145: 16-23, 1990. (Pubitemid 20324592)
18. Hoffmann J, Simon P, Zimmermann AK, Lemancyk M, Walter T, Beyer M, Hoffmeister HM, Ziemer G, Wendel HP. Thrombospondin 1 as possible key factor in the hemocompatibility of endocoronary prostheses. Biomaterials 26: 5240-5250, 2005. (Pubitemid 40387846)
19. Hugo C, Pichler R, Meek R, Gordon K, Kyriakides T, Floege J, Bornstein P, Couser WG, Johnson RJ. Thrombospondin 1 is expressed by proliferating mesangial cells and is up-regulated by PDGF and bFGF in vivo. Kidney Int 48: 1846-1856, 1995.
20. Isenberg JS, Romeo MJ, Yu C, Yu CK, Nghiem K, Monsale J, Rick ME, Wink DA, Frazier WA, Roberts DD. Thrombospondin-1 stimulates platelet aggregation by blocking the antithrombotic activity of nitric oxide/cGMP signaling. Blood 111: 613-623, 2008.
21. Isenberg JS, Wink DA, Roberts DD. Thrombospondin-1 antagonizes nitric oxide-stimulated vascular smooth muscle cell responses. Cardiovasc Res 71: 785-793, 2006. (Pubitemid 44848003)
22. Kang JH, Chang SY, Yeom DH, Kim SA, Um SJ, Hong KJ. Weakening of the repressive YY-1 site on the thrombospondin-1 promoter via c-Jun/YY-1 interaction. Exp Mol Med 36: 300-310, 2004.
23. Kanzaki T, Shiina R, Saito Y, Zardi L, Morisaki N. Transforming growth factor-beta receptor and fibronectin expressions in aortic smooth muscle cells in diabetic rats. Diabetologia 40: 383-391, 1997. (Pubitemid 27132608)
24. Khan R, Agrotis A, Bobik A. Understanding the role of transforming growth factor-beta1 in intimal thickening after vascular injury. Cardiovasc Res 74: 223-234, 2007. (Pubitemid 46517511)
25. Liu S, Ma X, Gong M, Shi L, Lincoln T, Wang S. Glucose downregulation of cGMP-dependent protein kinase I expression in vascular smooth muscle cells involves NAD(P)H oxidase-derived reactive oxygen species. Free Radic Biol Med 42: 852-863, 2007. (Pubitemid 46274174)
26. Muniyappa R, Srinivas PR, Ram JL, Walsh MF, Sowers JR. Calcium and protein kinase C mediate high-glucose-induced inhibition of inducible nitric oxide synthase in vascular smooth muscle cells. Hypertension 31: 289-295, 1998. (Pubitemid 28124731)
27. Nabel EG, Shum L, Pompili VJ, Yang ZY, San H, Shu HB, Liptay S, Gold L, Gordon D, Derynck R, Nabel GJ. Direct transfer of transforming growth factor beta 1 gene into arteries stimulates fibrocellular hyperplasia. Proc Natl Acad Sci USA 90: 10759-10763, 1993. (Pubitemid 23347122)
28. Pallero MA, Talbert Roden M, Chen YF, Anderson PG, Lemons J, Brott BC, Murphy-Ullrich JE. Stainless steel ions stimulate increased thrombospondin-1- dependent TGF-Beta activation by vascular smooth muscle cells: implications for in-stent restenosis. J Vasc Res 47: 309-322, 2009.
29. Pandolfi A, Grilli A, Cilli C, Patruno A, Giaccari A, Di Silvestre S, De Lutiis MA, Pellegrini G, Capani F, Consoli A, Felaco M. Phenotype modulation in cultures of vascular smooth muscle cells from diabetic rats: association with increased nitric oxide synthase expression and superoxide anion generation. J Cell Physiol 196: 378-385, 2003. (Pubitemid 36775886)
30. Phelan MW, Forman LW, Perrine SP, Faller DV. Hypoxia increases thrombospondin-1 transcript and protein in cultured endothelial cells. J Lab Clin Med 132: 519-529, 1998. (Pubitemid 28564710)
31. Poczatek MH, Hugo C, Darley-Usmar V, Murphy-Ullrich JE. Glucose stimulation of transforming growth factor-beta bioactivity in mesangial cells is mediated by thrombospondin-1. Am J Pathol 157: 1353-1363, 2000.
32. Raman P, Krukovets I, Marinic TE, Bornstein P, Stenina OI. Glycosylation mediates up-regulation of a potent antiangiogenic and proatherogenic protein, thrombospondin-1, by glucose in vascular smooth muscle cells. J Biol Chem 282: 5704-5714, 2007. (Pubitemid 47093782)
33. Rasmussen LM, Heickendorff L. Accumulation of fibronectin in aortas from diabetic patients. A quantitative immunohistochemical and biochemical study. Lab Invest 61: 440-446, 1989. (Pubitemid 19269346)
34. Ray JL, Leach R, Herbert JM, Benson M. Isolation of vascular smooth muscle cells from a single murine aorta. Methods Cell Sci 23: 185-188, 2001. (Pubitemid 34863290)
35. Ribeiro SM, Poczatek M, Schultz-Cherry S, Villain M, Murphy- Ullrich JE. The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J Biol Chem 274: 13586-13593, 1999. (Pubitemid 129518577)
36. Schultz-Cherry S, Lawler J, Murphy-Ullrich JE. The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J Biol Chem 269: 26783-26788, 1994. (Pubitemid 24332872)
37. Schultz-Cherry S, Murphy-Ullrich JE. Thrombospondin causes activation of latent transforming growth factor-beta secreted by endothelial cells by a novel mechanism. J Cell Biol 122: 923-932, 1993. (Pubitemid 23241101)
38. Sharma K, Ziyadeh FN. Hyperglycemia and diabetic kidney disease. The case for transforming growth factor-beta as a key mediator. Diabetes 44: 1139-1146, 1995.
39. Smolenski A, Bachmann C, Reinhard K, Honig-Liedl P, Jarchau T, Hoschuetzky H, Walter U. Analysis and regulation of vasodilatorstimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J Biol Chem 273: 20029-20035, 1998. (Pubitemid 28377554)
40. Stenina OI, Krukovets I, Wang K, Zhou Z, Forudi F, Penn MS, Topol EJ, Plow EF. Increased expression of thrombospondin-1 in vessel wall of diabetic Zucker rat. Circulation 107: 3209-3215, 2003. (Pubitemid 36793093)
41. Tardif JC, Gregoire J, L'Allier PL. Prevention of restenosis with antioxidants: mechanisms and implications. Am J Cardiovasc Drugs 2: 323-334, 2002. (Pubitemid 35214935)
42. Tolsma SS, Volpert OV, Good DJ, Frazier WA, Polverini PJ, Bouck N. Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. J Cell Biol 122: 497-511, 1993. (Pubitemid 23210475)
43. Varma V, Yao-Borengasser A, Bodles AM, Rasouli N, Phanavanh B, Nolen GT, Kern EM, Nagarajan R, Spencer HJ 3rd, Lee MJ, Fried SK, McGehee RE Jr, Peterson CA, Kern PA. Thrombospondin-1 is an adipokine associated with obesity, adipose inflammation, and insulin resistance. Diabetes 57: 432-439, 2008.
44. Wahab NA, Schaefer L, Weston BS, Yiannikouris O, Wright A, Babelova A, Schaefer R, Mason RM. Glomerular expression of thrombospondin-1, transforming growth factor beta and connective tissue growth factor at different stages of diabetic nephropathy and their interdependent roles in mesangial response to diabetic stimuli. Diabetologia 4: 1-11, 2005. (Pubitemid 41738234)
45. Wang S, Shiva S, Poczatek MH, Darley-Usmar V, Murphy-Ullrich JE. Nitric oxide and cGMP-dependent protein kinase regulation of glucosemediated thrombospondin 1-dependent transforming growth factor-beta activation in mesangial cells. J Biol Chem 277: 9880-9888, 2002. (Pubitemid 34968093)
46. Wang S, Skorczewski J, Feng X, Mei L, Murphy-Ullrich JE. Glucose up-regulates thrombospondin 1 gene transcription and transforming growth factor-beta activity through antagonism of cGMP-dependent protein kinase repression via upstream stimulatory factor 2. J Biol Chem 279: 34311-34322, 2004. (Pubitemid 39318055)
47. Wang S, Wu X, Lincoln TM, Murphy-Ullrich JE. Expression of constitutively active cGMP-dependent protein kinase prevents glucose stimulation of thrombospondin 1 expression and TGF-beta activity. Diabetes 52: 2144-2150, 2003. (Pubitemid 36919810)
48. Wernet W, Flockerzi V, Hofmann F. The cDNA of the two isoforms of bovine cGMP-dependent protein kinase. FEBS Lett 251: 191-196, 1989. (Pubitemid 19181868)
49. Xia L, Wang H, Goldberg HJ, Munk S, Fantus IG, Whiteside CI. Mesangial cell NADPH oxidase upregulation in high glucose is protein kinase C dependent and required for collagen IV expression. Am J Physiol Renal Physiol 290: F345-F356, 2006. (Pubitemid 43724989)
50. Yokoyama H, Deckert T. Central role of TGF-beta in the pathogenesis of diabetic nephropathy and macrovascular complications: a hypothesis. Diabet Med 13: 313-320, 1996. (Pubitemid 26142882)
51. Young GD, Murphy-Ullrich JE. Molecular interactions that confer latency to transforming growth factor-beta. J Biol Chem 279: 38032-38039, 2004.
52. Young ME, Leighton B. Fuel oxidation in skeletal muscle is increased by nitric oxide/cGMP-evidence for involvement of cGMP-dependent protein kinase. FEBS Lett 424: 79-83, 1998. (Pubitemid 28130356)
53. Zhou J, Feng X, Ban B, Liu J, Wang Z, Xiao W. Elongation factor ELL (Eleven-Nineteen Lysine-rich Leukemia) acts as a transcription factor for direct thrombospondin-1 regulation. J Biol Chem 284: 19142-19152, 2009.