Atherosclerosis
Volume 195, Issue 1 , Pages 23-30 , November 2007

Sirolimus blocks the accumulation of hyaluronan (HA) by arterial smooth muscle cells and reduces monocyte adhesion to the ECM

Received 20 June 2006 ,Revised 6 October 2006 ,Accepted 17 November 2006.

References 

  1. Sigwart U, Puel J, Mirkovitch V, Joffre F, Kappenberger L. Intravascular stents to prevent occlusion and restenosis after transluminal angioplasty. N Engl J Med. 1987;316:701–706
  2. Serruys PW, de Jaegere P, Kiemeneij F, et al. A comparison of balloon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease. Benestent Study Group. N Engl J Med. 1994;331:489–495
  3. Fischman DL, Leon MB, Baim DS, et al. A randomized comparison of coronary-stent placement and balloon angioplasty in the treatment of coronary artery disease. Stent Restenosis Study Investigators. N Engl J Med. 1994;331:496–501
  4. Hoffmann R, Mintz GS, Dussaillant GR, et al. Patterns and mechanisms of in-stent restenosis. A serial intravascular ultrasound study. Circulation. 1996;94:1247–1254
  5. Chung IM, Gold HK, Schwartz SM, Ikari Y, Reidy MA, Wight TN. Enhanced extracellular matrix accumulation in restenosis of coronary arteries after stent deployment. J Am Coll Cardiol. 2002;40:2072–2081
  6. Farb A, Kolodgie FD, Hwang JY, et al. Extracellular matrix changes in stented human coronary arteries. Circulation. 2004;110:940–947
  7. Riessen R, Wight TN, Pastore C, Henley C, Isner JM. Distribution of hyaluronan during extracellular matrix remodeling in human restenotic arteries and balloon-injured rat carotid arteries. Circulation. 1996;93:1141–1147
  8. Karnik SK, Brooke BS, Bayes-Genis A, et al. A critical role for elastin signaling in vascular morphogenesis and disease. Development. 2003;130:411–423
  9. Evanko SP, Angello JC, Wight TN. Formation of hyaluronan- and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 1999;19:1004–1013
  10. Fischer JW, Kinsella MG, Clowes MM, Lara S, Clowes AW, Wight TN. Local expression of bovine decorin by cell-mediated gene transfer reduces neointimal formation after balloon injury in rats. Circ Res. 2000;86:676–683
  11. Wight TN, Lara S, Riessen R, Le Baron R, Isner J. Selective deposits of versican in the extracellular matrix of restenotic lesions from human peripheral arteries. Am J Pathol. 1997;151:963–973
  12. Matsuura R, Isaka N, Imanaka-Yoshida K, Yoshida T, Sakakura T, Nakano T. Deposition of PG-M/versican is a major cause of human coronary restenosis after percutaneous transluminal coronary angioplasty. J Pathol. 1996;180:311–316
  13. LeBaron RG, Zimmermann DR, Ruoslahti E. Hyaluronate binding properties of versican. J Biol Chem. 1992;267:10003–10010
  14. Chang Y, Yanagishita M, Hascall VC, Wight TN. Proteoglycans synthesized by smooth muscle cells derived from monkey (Macaca nemestrina) aorta. J Biol Chem. 1983;258:5679–5688
  15. Wight TN, Merrilees MJ. Proteoglycans in atherosclerosis and restenosis: key roles for versican. Circ Res. 2004;94:1158–1167
  16. Majors AK, Austin RC, de la Motte CA, et al. Endoplasmic reticulum stress induces hyaluronan deposition and leukocyte adhesion. J Biol Chem. 2003;278:47223–47231
  17. Bauters C, Van Belle E, McFadden E, Lablanche JM, Bertrand ME. Restenosis after angioplasty. Arch Mal Coeur Vaiss. 1999;92:1579–1582
  18. Suzuki T, Kopia G, Hayashi S, et al. Stent-based delivery of sirolimus reduces neointimal formation in a porcine coronary model. Circulation. 2001;104:1188–1193
  19. Klugherz BD, Llanos G, Lieuallen W, et al. Twenty-eight-day efficacy and phamacokinetics of the sirolimus-eluting stent. Coron Artery Dis. 2002;13:183–188
  20. Sousa JE, Costa MA, Abizaid A, et al. Lack of neointimal proliferation after implantation of sirolimus-coated stents in human coronary arteries: a quantitative coronary angiography and three-dimensional intravascular ultrasound study. Circulation. 2001;103:192–195
  21. Sousa JE, Costa MA, Abizaid AC, et al. Sustained suppression of neointimal proliferation by sirolimus-eluting stents: one-year angiographic and intravascular ultrasound follow-up. Circulation. 2001;104:2007–2011
  22. Morice MC, Serruys PW, Sousa JE, et al. A randomized comparison of a sirolimus-eluting stent with a standard stent for coronary revascularization. N Engl J Med. 2002;346:1773–1780
  23. Gummert JF, Ikonen T, Morris RE. Newer immunosuppressive drugs: a review. J Am Soc Nephrol. 1999;10:1366–1380
  24. Sehgal SN. Rapamune (Sirolimus, rapamycin): an overview and mechanism of action. Ther Drug Monit. 1995;17:660–665
  25. Marx SO, Jayaraman T, Go LO, Marks AR. Rapamycin-FKBP inhibits cell cycle regulators of proliferation in vascular smooth muscle cells. Circ Res. 1995;76:412–417
  26. Poon M, Marx SO, Gallo R, Badimon JJ, Taubman MB, Marks AR. Rapamycin inhibits vascular smooth muscle cell migration. J Clin Invest. 1996;98:2277–2283
  27. Sehgal SN. Sirolimus: its discovery, biological properties, and mechanism of action. Transplant Proc. 2003;35:S7–S14
  28. Roque M, Reis ED, Cordon-Cardo C, et al. Effect of p27 deficiency and rapamycin on intimal hyperplasia: in vivo and in vitro studies using a p27 knockout mouse model. Lab Invest. 2001;81:895–903
  29. Terada N, Lucas JJ, Szepesi A, Franklin RA, Domenico J, Gelfand EW. Rapamycin blocks cell cycle progression of activated T cells prior to events characteristic of the middle to late G1 phase of the cycle. J Cell Physiol. 1993;154:7–15
  30. Chung IM, Gold HK, Schwartz SM, Ikari Y, Reidy MA, Wight TN. Enhanced extracellular matrix accumulation in restenosis of coronary arteries after stent deployment. J Am Coll Cardiol. 2002;40:2072–2081
  31. Evanko SP, Johnson PY, Braun KR, Underhill CB, Dudhia J, Wight TN. Platelet-derived growth factor stimulates the formation of versican-hyaluronan aggregates and pericellular matrix expansion in arterial smooth muscle cells. Arch Biochem Biophys. 2001;394:29–38
  32. Wilkinson TS, Potter-Perigo S, Tsoi C, Altman LC, Wight TN. Pro- and anti-inflammatory factors cooperate to control hyaluronan synthesis in lung fibroblasts. Am J Respir Cell Mol Biol. 2004;31:92–99
  33. Underhill CB. Hyaluronan is inversely correlated with the expression of CD44 in the dermal condensation of the embryonic hair follicle. J Invest Dermatol. 1993;101:820–826
  34. Wilkinson TS, Bressler SL, Evanko SP, Braun KR, Wight TN. Overexpression of hyaluronan synthases alters vascular smooth muscle cell phenotype and promotes monocyte adhesion. J Cell Physiol. 2006;206:378–385
  35. de La Motte CA, Hascall VC, Calabro A, Yen-Lieberman B, Strong SA. Mononuclear leukocytes preferentially bind via CD44 to hyaluronan on human intestinal mucosal smooth muscle cells after virus infection or treatment with poly(I:C). J Biol Chem. 1999;274:30747–30755
  36. de Belder AN, Wik KO. Preparation and properties of fluorescein-labelled hyaluronate. Carbohydrate Res. 1975;44:251–257
  37. Jain M, He Q, Lee WS, et al. Role of CD44 in the reaction of vascular smooth muscle cells to arterial wall injury. J Clin Invest. 1996;98:877
  38. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004;4:528–539
  39. Buerke M, Guckenbiehl M, Schwertz H, et al. Intramural delivery of Sirolimus prevents vascular remodeling following balloon injury. Biochim Biophys Acta, 2006, in press.
  40. Park J, Ha H, Ahn HJ, et al. Sirolimus inhibits platelet-derived growth factor-induced collagen synthesis in rat vascular smooth muscle cells. Transplant Proc. 2005;37:3459–3462
  41. Svegliati-Baroni G, Ridolfi F, Di Sario A, et al. Intracellular signaling pathways involved in acetaldehyde-induced collagen and fibronectin gene expression in human hepatic stellate cells. Hepatology. 2001;33:1130–1140
  42. Poulalhon N, Farge D, Roos N, et al. Modulation of collagen and MMP-1 gene expression in fibroblasts by the immunosuppressive drug rapamycin: a direct role as an anti-fibrotic agent?. J Biol Chem. 2006;281:33045–33052
  43. Starkman BG, Cravero JD, Delcarlo M, Loeser RF. IGF-I stimulation of proteoglycan synthesis by chondrocytes requires activation of the PI 3-kinase pathway but not ERK MAPK. Biochem J. 2005;389:723–729
  44. Sun J, Marx SO, Chen HJ, Poon M, Marks AR, Rabbani LE. Role for p27(Kip1) in vascular smooth muscle cell migration. Circulation. 2001;103:2967–2972
  45. Marks AR. Rapamycin: signaling in vascular smooth muscle. Transplant Proc. 2003;35:S231–S233
  46. Gingras AC, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 2001;15:807–826
  47. van den Boom M, Sarbia M, von Wnuck Lipinski K, et al. Differential regulation of hyaluronic acid synthase isoforms in human saphenous vein smooth muscle cells: possible implications for vein graft stenosis. Circ Res. 2006;98:36–44
  48. de La Motte C, Hascall V, Drazbe J, Strong S. Poly I:C induces mononuclear leukocyte adhesive hyaluronan structures on colon smooth muscle cells: I alpha I and versican facilitate adhesion. In:  Kennedy JF,  Phillips GO,  Williams PA,  Hascall VC editor. Hyaluronan, volume 1, Chemical, Biochemical and Biological Aspects.. Cambridge: Woodhead Publishing Ltd.; 2002;pp. 381–388
  49. de la Motte CA, Hascall VC, Drazba J, Bandyopadhyay SK, Strong SA. Mononuclear leukocytes bind to specific hyaluronan structures on colon mucosal smooth muscle cells treated with polyinosinic acid:polycytidylic acid: inter-alpha-trypsin inhibitor is crucial to structure and function. Am J Pathol. 2003;163:121–133
  50. Hascall VC, Majors AK, De La Motte CA, et al. Intracellular hyaluronan: a new frontier for inflammation?. Biochim Biophys Acta. 2004;1673:3–12
  51. Day AJ, de la Motte CA. Hyaluronan cross-linking: a protective mechanism in inflammation?. Trends Immunol. 2005;26:637–643
  52. Corrado E, Rizzo M, Tantillo R, et al. Markers of inflammation and infection influence the outcome of patients with baseline asymptomatic carotid lesions: a 5-year follow-up study. Stroke. 2006;37:482–486
  53. Ismail A, Khosravi H, Olson H. The role of infection in atherosclerosis and coronary artery disease: a new therapeutic target. Heart Dis. 1999;1:233–240
  54. Vink A, de Kleijn DP, Pasterkamp G. Functional role for toll-like receptors in atherosclerosis and arterial remodeling. Curr Opin Lipidol. 2004;15:515–521
  55. Sen GC, Sarkar SN. Transcriptional signaling by double-stranded RNA: role of TLR3. Cytokine Growth Factor Rev. 2005;16:1–14
  56. Monslow J, Williams JD, Norton N, et al. The human hyaluronan synthase genes: genomic structures, proximal promoters and polymorphic microsatellite markers. Int J Biochem Cell Biol. 2003;35:1272–1283
  57. Giordano A, Avellino R, Ferraro P, Romano S, Corcione N, Romano MF. Rapamycin antagonizes NF-{kappa}B nuclear translocation activated by TNF-{alpha} in primary vascular smooth muscle cells and enhances apoptosis. Am J Physiol Heart Circ Physiol. 2006;
  58. Thompson JE, Thompson CB. Putting the rap on Akt. J Clin Oncol. 2004;22:4217–4226
  59. Misra S, Ghatak S, Toole BP. Regulation of MDR1 expression and drug resistance by a positive feedback loop involving hyaluronan, phosphoinositide 3-kinase, and ErbB2. J Biol Chem. 2005;280:20310–20315
  60. Martin KA, Rzucidlo EM, Merenick BL, et al. The mTOR/p70 S6K1 pathway regulates vascular smooth muscle cell differentiation. Am J Physiol Cell Physiol. 2004;286:C507–C517
  61. Guerin P, Sauzeau V, Rolli-Derkinderen M, et al. Stent implantation activates RhoA in human arteries: inhibitory effect of rapamycin. J Vasc Res. 2005;42:21–28
  62. Bi D, Nishimura J, Niiro N, Hirano K, Kanaide H. Contractile properties of the cultured vascular smooth muscle cells: the crucial role played by RhoA in the regulation of contractility. Circ Res. 2005;96:890–897
  63. Merrilees MJ, Campbell JH, Spanidis E, Campbell GR. Glycosaminoglycan synthesis by smooth muscle cells of differing phenotype and their response to endothelial cell conditioned medium. Atherosclerosis. 1990;81:245–254
  64. Anwar KN, Fazal F, Malik AB, Rahman A. RhoA/Rho-associated kinase pathway selectively regulates thrombin-induced intercellular adhesion molecule-1 expression in endothelial cells via activation of I kappa B kinase beta and phosphorylation of RelA/p65. J Immunol. 2004;173:6965–6972

PII: S0021-9150(06)00697-6

doi: 10.1016/j.atherosclerosis.2006.11.023

Atherosclerosis
Volume 195, Issue 1 , Pages 23-30 , November 2007