Adventitial growth factor signalling and vascular remodelling: Potential of perivascular gene transfer from the outside-in

Cardiovascular Research

Volumn 75, Issue 4, 2007, Pages 659-668

  Siow, Richard C M ^a   Churchman, Adrian T ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Adventitia; Antioxidant genes; Atherosclerosis; Coronary artery bypass graft; Gene therapy; Growth factor; Myofibroblasts; Progenitor cells; Reactive oxygen species; Restenosis; Smooth muscle cells; Vascular remodelling

Indexed keywords

ADENOVIRUS VECTOR; AUTACOID; CATALASE; CONNECTIVE TISSUE GROWTH FACTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GROWTH FACTOR; NEUTRALIZING ANTIBODY; PLATELET DERIVED GROWTH FACTOR BB; PROTEIN INHIBITOR; REACTIVE OXYGEN METABOLITE; RECOMBINANT RECEPTOR; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE INHIBITORY PEPTIDE; RETROVIRUS VECTOR; SUPEROXIDE DISMUTASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TRANSCRIPTION FACTOR NRF2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ADVENTITIA; ARTERY INTIMA PROLIFERATION; ATHEROGENESIS; ATHEROSCLEROSIS; BLOOD VESSEL INJURY; CAROTID ARTERY INJURY; CELL ACTIVATION; CELL MIGRATION; DISEASE COURSE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE TRANSFER; GRAFT FAILURE; HUMAN; INTIMA; LIPOSOMAL GENE DELIVERY SYSTEM; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PERCUTANEOUS TRANSLUMINAL ANGIOPLASTY; PRIORITY JOURNAL; RESTENOSIS; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; STEM CELL; TREATMENT OUTCOME; VASCULAR DISEASE; VEIN GRAFT DISEASE; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; ATHEROSCLEROSIS; CELL MOVEMENT; CONNECTIVE TISSUE; CORONARY VESSELS; GENE THERAPY; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; SIGNAL TRANSDUCTION; VASA VASORUM;

EID: 34547745932     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2007.06.007     Document Type: Review

References (111)

1. Sartore S., Chiavegato A., Faggin E., Franch R., Puato M., Ausoni S., et al. Contribution of adventitial fibroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ Res 89 (2001) 1111-1121
2. Shi Y., Pieniek M., Fard A., O'Brien J., Mannion J.D., and Zalewski A. Adventitial remodeling after coronary arterial injury. Circulation 93 (1996) 340-348
3. Schwartz S.M., deBlois D., and O'Brien E.R. The intima. Soil for atherosclerosis and restenosis. Circ Res 77 (1995) 445-465
4. Zalewski A., and Shi Y. Vascular myofibroblasts. Lessons from coronary repair and remodeling. Arterioscler Thromb Vasc Biol 17 (1997) 417-422
5. Li G., Chen S.J., Oparil S., Chen Y.F., and Thompson J.A. Direct in vivo evidence demonstrating neointimal migration of adventitial fibroblasts after balloon injury of rat carotid arteries. Circulation 101 (2000) 1362-1365
6. Shi Y., O'Brien J.E., Fard A., Mannion J.D., Wang D., and Zalewski A. Adventitial myofibroblasts contribute to neointimal formation in injured porcine coronary arteries. Circulation 94 (1996) 1655-1664
7. Shi Y., O'Brien Jr. J.E., Fard A., and Zalewski A. Transforming growth factor-beta 1 expression and myofibroblast formation during arterial repair. Arterioscler Thromb Vasc Biol 16 (1996) 1298-1305
8. Shi Y., O'Brien Jr. J.E., la-Kokko L., Chung W., Mannion J.D., and Zalewski A. Origin of extracellular matrix synthesis during coronary repair. Circulation 95 (1997) 997-1006
9. Rey F.E., and Pagano P.J. The reactive adventitia: fibroblast oxidase in vascular function. Arterioscler Thromb Vasc Biol 22 (2002) 1962-1971
10. Torsney E., Hu Y., and Xu Q. Adventitial progenitor cells contribute to arteriosclerosis. Trends Cardiovasc Med 15 (2005) 64-68
11. Faggin E., Puato M., Zardo L., Franch R., Millino C., Sarinella F., et al. Smooth muscle-specific SM22 protein is expressed in the adventitial cells of balloon-injured rabbit carotid artery. Arterioscler Thromb Vasc Biol 19 (1999) 1393-1404
12. Siow R.C., Mallawaarachchi C.M., and Weissberg P.L. Migration of adventitial myofibroblasts following vascular balloon injury: insights from in vivo gene transfer to rat carotid arteries. Cardiovasc Res 59 (2003) 212-221
13. Couffinhal T., Dufourcq P., Jaspard B., Daret D., Allieres C., Alzieu P., et al. Kinetics of adventitial repair in the rat carotid model. Coron Artery Dis 12 (2001) 635-648
14. Christen T., Verin V., Bochaton-Piallat M., Popowski Y., Ramaekers F., Debruyne P., et al. Mechanisms of neointima formation and remodeling in the porcine coronary artery. Circulation 103 (2001) 882-888
15. Xu Q. The impact of progenitor cells in atherosclerosis. Nat Clin Pract Cardiovasc Med 3 (2006) 94-101
16. Laitinen M., and Yla-Herttuala S. Adventitial gene transfer to arterial wall. Pharmacol Res 37 (1998) 251-254
17. Schwartz S.M. Smooth muscle migration in atherosclerosis and restenosis. J Clin Invest 100 (1997) S87-S89
18. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 340 (1999) 115-126
19. Khan R., Agrotis A., and Bobik A. Understanding the role of transforming growth factor-beta1 in intimal thickening after vascular injury. Cardiovasc Res 74 (2007) 223-234
20. Lindner V., Giachelli C.M., Schwartz S.M., and Reidy M.A. A subpopulation of smooth muscle cells in injured rat arteries expresses platelet-derived growth factor-B chain mRNA. Circ Res 76 (1995) 951-957
21. Levitzki A. PDGF receptor kinase inhibitors for the treatment of restenosis. Cardiovasc Res 65 (2005) 581-586
22. Ferns G.A., Raines E.W., Sprugel K.H., Motani A.S., Reidy M.A., and Ross R. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science 253 (1991) 1129-1132
23. Deguchi J., Namba T., Hamada H., Nakaoka T., Abe J., Sato O., et al. Targeting endogenous platelet-derived growth factor B-chain by adenovirus-mediated gene transfer potently inhibits in vivo smooth muscle proliferation after arterial injury. Gene Ther 6 (1999) 956-965
24. Kingston P.A., Sinha S., David A., Castro M.G., Lowenstein P.R., and Heagerty A.M. Adenovirus-mediated gene transfer of a secreted transforming growth factor-beta type II receptor inhibits luminal loss and constrictive remodeling after coronary angioplasty and enhances adventitial collagen deposition. Circulation 104 (2001) 2595-2601
25. Wolf Y.G., Rasmussen L.M., and Ruoslahti E. Antibodies against transforming growth factor-beta 1 suppress intimal hyperplasia in a rat model. J Clin Invest 93 (1994) 1172-1178
26. Smith J.D., Bryant S.R., Couper L.L., Vary C.P., Gotwals P.J., Koteliansky V.E., et al. Soluble transforming growth factor-beta type II receptor inhibits negative remodeling, fibroblast transdifferentiation, and intimal lesion formation but not endothelial growth. Circ Res 84 (1999) 1212-1222
27. Jiang Z., Yu P., Tao M., Fernandez C., Ifantides C., Moloye O., et al. TGF-beta/CTGF mediated fibroblast recruitment influences early outward vein graft remodeling. Am J Physiol Heart Circ Physiol (2007) 10.1152/ajpheart.01372.2006
28. Leask A., and Abraham D.J. The role of connective tissue growth factor, a multifunctional matricellular protein in fibroblast biology. Biochem Cell Biol 81 (2003) 355-363
29. Nykanen A.I., Krebs R., Tikkanen J.M., Raisky O., Sihvola R., Wood J., et al. Combined vascular endothelial growth factor and platelet-derived growth factor inhibition in rat cardiac allografts: beneficial effects on inflammation and smooth muscle cell proliferation. Transplantation 79 (2005) 182-189
30. Oparil S., Chen S.J., Chen Y.F., Durand J.N., Allen L., and Thompson J.A. Estrogen attenuates the adventitial contribution to neointima formation in injured rat carotid arteries. Cardiovasc Res 44 (1999) 608-614
31. Masur S.K., Dewal H.S., Dinh T.T., Erenburg I., and Petridou S. Myofibroblasts differentiate from fibroblasts when plated at low density. Proc Natl Acad Sci U S A 93 (1996) 4219-4223
32. Hu Y., Zhang Z., Torsney E., Afzal A.R., Davison F., Metzler B., et al. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest 113 (2004) 1258-1265
33. Simper D., Stalboerger P.G., Panetta C.J., Wang S., and Caplice N.M. Smooth muscle progenitor cells in human blood. Circulation 106 (2002) 1199-1204
34. Lu X., Dunn J., Dickinson A.M., Gillespie J.I., and Baudouin S.V. Smooth muscle alpha-actin expression in endothelial cells derived from CD34+ human cord blood cells. Stem Cells Dev 13 (2004) 521-527
35. Sata M., Fukuda D., Tanaka K., Kaneda Y., Yashiro H., and Shirakawa I. The role of circulating precursors in vascular repair and lesion formation. J Cell Mol Med 9 (2005) 557-568
36. Pearson J.D. Using endothelial progenitor cells for gene therapy. Arterioscler Thromb Vasc Biol 23 (2003) 2117-2118
37. Mallawaarachchi C.M., Weissberg P.L., and Siow R.C. Smad7 gene transfer attenuates adventitial cell migration and vascular remodeling after balloon injury. Arterioscler Thromb Vasc Biol 25 (2005) 1383-1387
38. Mallawaarachchi C.M., Weissberg P.L., and Siow R.C. Antagonism of platelet-derived growth factor by perivascular gene transfer attenuates adventitial cell migration after vascular injury: new tricks for old dogs?. FASEB J 20 (2006) 1686-1688
39. Nakao A., Afrakhte M., Moren A., Nakayama T., Christian J.L., Heuchel R., et al. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 389 (1997) 631-635
40. Attisano L., and Wrana J.L. Signal transduction by the TGF-beta superfamily. Science 296 (2002) 1646-1647
41. Ikedo H., Tamaki K., Ueda S., Kato S., Fujii M., Ten D.P., et al. Smad protein and TGF-beta signaling in vascular smooth muscle cells. Int J Mol Med 11 (2003) 645-650
42. Duan D.S., Pazin M.J., Fretto L.J., and Williams L.T. A functional soluble extracellular region of the platelet-derived growth factor (PDGF) beta-receptor antagonizes PDGF-stimulated responses. J Biol Chem 266 (1991) 413-418
43. Ross J.J., Hong Z., Willenbring B., Zeng L., Isenberg B., Lee E.H., et al. Cytokine-induced differentiation of multipotent adult progenitor cells into functional smooth muscle cells. J Clin Invest 116 (2006) 3139-3149
44. Liu C., Nath K.A., Katusic Z.S., and Caplice N.M. Smooth muscle progenitor cells in vascular disease. Trends Cardiovasc Med 14 (2004) 288-293
45. Wilcox J.N., Okamoto E.I., Nakahara K.I., and Vinten-Johansen J. Perivascular responses after angioplasty which may contribute to postangioplasty restenosis: a role for circulating myofibroblast precursors?. Ann N Y Acad Sci 947 (2001) 68-90
46. Lindskog H., Athley E., Larsson E., Lundin S., Hellstrom M., and Lindahl P. New insights to vascular smooth muscle cell and pericyte differentiation of mouse embryonic stem cells in vitro. Arterioscler Thromb Vasc Biol 26 (2006) 1457-1464
47. Luttun A., Carmeliet G., and Carmeliet P. Vascular progenitors: from biology to treatment. Trends Cardiovasc Med 12 (2002) 88-96
48. Carmeliet P. Angiogenesis in health and disease. Nat Med 9 (2003) 653-660
49. Hristov M., Erl W., and Weber P.C. Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler Thromb Vasc Biol 23 (2003) 1185-1189
50. Virmani R., Kolodgie F.D., Burke A.P., Finn A.V., Gold H.K., Tulenko T.N., et al. Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol 25 (2005) 2054-2061
51. Khurana R., Zhuang Z., Bhardwaj S., Murakami M., De M.E., Yla-Herttuala S., et al. Angiogenesis-dependent and independent phases of intimal hyperplasia. Circulation 110 (2004) 2436-2443
52. Khurana R., Shafi S., Martin J., and Zachary I. Vascular endothelial growth factor gene transfer inhibits neointimal macrophage accumulation in hypercholesterolemic rabbits. Arterioscler Thromb Vasc Biol 24 (2004) 1074-1080
53. Deiner C., Schwimmbeck P.L., Koehler I.S., Loddenkemper C., Noutsias M., Nikol S., et al. Adventitial VEGF165 gene transfer prevents lumen loss through induction of positive arterial remodeling after PTCA in porcine coronary arteries. Atherosclerosis 189 (2006) 123-132
54. Moreno P.R., Purushothaman K.R., Sirol M., Levy A.P., and Fuster V. Neovascularization in human atherosclerosis. Circulation 113 (2006) 2245-2252
55. Rotmans J.I., Heyligers J.M., Verhagen H.J., Velema E., Nagtegaal M.M., de Kleijn D.P., et al. In vivo cell seeding with anti-CD34 antibodies successfully accelerates endothelialization but stimulates intimal hyperplasia in porcine arteriovenous expanded polytetrafluoroethylene grafts. Circulation 112 (2005) 12-18
56. Moulton K.S. Angiogenesis in atherosclerosis: gathering evidence beyond speculation. Curr Opin Lipidol 17 (2006) 548-555
57. Galis Z.S., and Khatri J.J. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res 90 (2002) 251-262
58. Newby A.C. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev 85 (2005) 1-31
59. Hu Y., Baker A.H., Zou Y., Newby A.C., and Xu Q. Local gene transfer of tissue inhibitor of metalloproteinase-2 influences vein graft remodeling in a mouse model. Arterioscler Thromb Vasc Biol 21 (2001) 1275-1280
60. Meng Q.H., Jamal W., Hart S.L., and McEwan J.R. Application to vascular adventitia of a nonviral vector for TIMP-1 gene therapy to prevent intimal hyperplasia. Hum Gene Ther 17 (2006) 717-727
61. Lau H.K. Regulation of proteolytic enzymes and inhibitors in two smooth muscle cell phenotypes. Cardiovasc Res 43 (1999) 1049-1059
62. Hall M.C., Young D.A., Waters J.G., Rowan A.D., Chantry A., Edwards D.R., et al. The comparative role of activator protein 1 and Smad factors in the regulation of TIMP-1 and MMP-1 gene expression by transforming growth factor-beta 1. J Biol Chem 278 (2003) 10304-10313
63. Shi Y., Niculescu R., Wang D., Patel S., Davenpeck K.L., and Zalewski A. Increased NAD(P)H oxidase and reactive oxygen species in coronary arteries after balloon injury. Arterioscler Thromb Vasc Biol 21 (2001) 739-745
64. Bedard K., and Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87 (2007) 245-313
65. Cai H., Griendling K.K., and Harrison D.G. The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases. Trends Pharmacol Sci 24 (2003) 471-478
66. Ushio-Fukai M., and Alexander R.W. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol Cell Biochem 264 (2004) 85-97
67. Griendling K.K., and FitzGerald G.A. Oxidative stress and cardiovascular injury: part II: animal and human studies. Circulation 108 (2003) 2034-2040
68. Pollman M.J., Hall J.L., and Gibbons G.H. Determinants of vascular smooth muscle cell apoptosis after balloon angioplasty injury. Influence of redox state and cell phenotype. Circ Res 84 (1999) 113-121
69. Kappert K., Sparwel J., Sandin A., Seiler A., Siebolts U., Leppanen O., et al. Antioxidants relieve phosphatase inhibition and reduce PDGF signaling in cultured VSMCs and in restenosis. Arterioscler Thromb Vasc Biol 26 (2006) 2644-2651
70. Rey F.E., Li X.C., Carretero O.A., Garvin J.L., and Pagano P.J. Perivascular superoxide anion contributes to impairment of endothelium-dependent relaxation: role of gp91(phox). Circulation 106 (2002) 2497-2502
71. Tsutsui M., Chen A.F., O'Brien T., Crotty T.B., and Katusic Z.S. Adventitial expression of recombinant eNOS gene restores NO production in arteries without endothelium. Arterioscler Thromb Vasc Biol 18 (1998) 1231-1241
72. Gutterman D.D. Adventitia-dependent influences on vascular function. Am J Physiol 277 (1999) H1265-H1272
73. Dourron H.M., Jacobson G.M., Park J.L., Liu J., Reddy D.J., Scheel M.L., et al. Perivascular gene transfer of NADPH oxidase inhibitor suppresses angioplasty-induced neointimal proliferation of rat carotid artery. Am J Physiol Heart Circ Physiol 288 (2005) H946-H953
74. Liu J., Ormsby A., Oja-Tebbe N., and Pagano P.J. Gene transfer of NAD(P)H oxidase inhibitor to the vascular adventitia attenuates medial smooth muscle hypertrophy. Circ Res 95 (2004) 587-594
75. Kreuzer J., Viedt C., Brandes R.P., Seeger F., Rosenkranz A.S., Sauer H., et al. Platelet-derived growth factor activates production of reactive oxygen species by NAD(P)H oxidase in smooth muscle cells through Gi1,2. FASEB J 17 (2003) 38-40
76. Rhee S.G., Chae H.Z., and Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med 38 (2005) 1543-1552
77. Choi M.H., Lee I.K., Kim G.W., Kim B.U., Han Y.H., Yu D.Y., et al. Regulation of PDGF signalling and vascular remodelling by peroxiredoxin II. Nature 435 (2005) 347-353
78. Sturrock A., Cahill B., Norman K., Huecksteadt T.P., Hill K., Sanders K., et al. Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen species-dependent proliferation in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 290 (2006) L661-L673
79. Jobling M.F., Mott J.D., Finnegan M.T., Jurukovski V., Erickson A.C., Walian P.J., et al. Isoform-specific activation of latent transforming growth factor beta (LTGF-beta) by reactive oxygen species. Radiat Res 166 (2006) 839-848
80. Wang M., Zhao D., Spinetti G., Zhang J., Jiang L.Q., Pintus G., et al. Matrix metalloproteinase 2 activation of transforming growth factor-beta1 (TGF-beta1) and TGF-beta1-type II receptor signaling within the aged arterial wall. Arterioscler Thromb Vasc Biol 26 (2006) 1503-1509
81. Lindner V. Vascular repair processes mediated by transforming growth factor-beta. Z Kardiol 90 Suppl 3 (2001) 17-22
82. Jeremy J.Y., Shukla N., Muzaffar S., Handley A., and Angelini G.D. Reactive oxygen species vascular disease and cardiovascular surgery. Curr Vasc Pharmacol 2 (2004) 229-236
83. Tardif J.C., Gregoire J., Lavoie M.A., and L'allier P.L. Pharmacologic prevention of both restenosis and atherosclerosis progression: AGI-1067, probucol, statins, folic acid and other therapies. Curr Opin Lipidol 14 (2003) 615-620
84. Konneh M.K., Rutherford C., Li S.R., Anggard E.E., and Ferns G.A. Vitamin E inhibits the intimal response to balloon catheter injury in the carotid artery of the cholesterol-fed rat. Atherosclerosis 113 (1995) 29-39
85. Stocker R., and Keaney Jr. J.F. Role of oxidative modifications in atherosclerosis. Physiol Rev 84 (2004) 1381-1478
86. Durand E., Al Haj Z.A., Addad F., Brasselet C., Caligiuri G., Vinchon F., et al. Adenovirus-mediated gene transfer of superoxide dismutase and catalase decreases restenosis after balloon angioplasty. J Vasc Res 42 (2005) 255-265
87. Leite P.F., Danilovic A., Moriel P., Dantas K., Marklund S., Dantas A.P., et al. Sustained decrease in superoxide dismutase activity underlies constrictive remodeling after balloon injury in rabbits. Arterioscler Thromb Vasc Biol 23 (2003) 2197-2202
88. Levonen A.L., Inkala M., Heikura T., Jauhiainen S., Jyrkkanen H.K., Kansanen E., et al. Nrf2 gene transfer induces antioxidant enzymes and suppresses smooth muscle cell growth in vitro and reduces oxidative stress in rabbit aorta in vivo. Arterioscler Thromb Vasc Biol 27 (2007) 741-747
89. Motohashi H., and Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10 (2004) 549-557
90. Lee J.M., Li J., Johnson D.A., Stein T.D., Kraft A.D., Calkins M.J., et al. Nrf2, a multi-organ protector?. FASEB J 19 (2005) 1061-1066
91. Siow R.C., Sato H., and Mann G.E. Heme oxygenase-carbon monoxide signalling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxide?. Cardiovasc Res 41 (1999) 385-394
92. Ryter S.W., Alam J., and Choi A.M. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86 (2006) 583-650
93. Tulis D.A., Durante W., Liu X., Evans A.J., Peyton K.J., and Schafer A.I. Adenovirus-mediated heme oxygenase-1 gene delivery inhibits injury-induced vascular neointima formation. Circulation 104 (2001) 2710-2715
94. Tulis D.A., Keswani A.N., Peyton K.J., Wang H., Schafer A.I., and Durante W. Local administration of carbon monoxide inhibits neointima formation in balloon injured rat carotid arteries. Cell Mol Biol (Noisy -le-grand) 51 (2005) 441-446
95. Nakao A., Murase N., Ho C., Toyokawa H., Billiar T.R., and Kanno S. Biliverdin administration prevents the formation of intimal hyperplasia induced by vascular injury. Circulation 112 (2005) 587-591
96. Deng Y.M., Wu B.J., Witting P.K., and Stocker R. Probucol protects against smooth muscle cell proliferation by upregulating heme oxygenase-1. Circulation 110 (2004) 1855-1860
97. Sauer H., and Wartenberg M. Reactive oxygen species as signaling molecules in cardiovascular differentiation of embryonic stem cells and tumor-induced angiogenesis. Antioxid Redox Signal 7 (2005) 1423-1434
98. Yla-Herttuala S., and Martin J.F. Cardiovascular gene therapy. Lancet 355 (2000) 213-222
99. Khurana R., Martin J.F., and Zachary I. Gene therapy for cardiovascular disease: a case for cautious optimism. Hypertension (2001) 1210-1216
100. Schneider D.B., Sassani A.B., Vassalli G., Driscoll R.M., and Dichek D.A. Adventitial delivery minimizes the proinflammatory effects of adenoviral vectors. J Vasc Surg 29 (1999) 543-550
101. Laitinen M., Pakkanen T., Donetti E., Baetta R., Luoma J., Lehtolainen P., et al. Gene transfer into the carotid artery using an adventitial collar: comparison of the effectiveness of the plasmid-liposome complexes, retroviruses, pseudotyped retroviruses, S and adenoviruses. Hum Gene Ther 8 (1997) 1645-1650
102. Welt F.G., and Rogers C. Inflammation and restenosis in the stent era. Arterioscler Thromb Vasc Biol 22 (2002) 1769-1776
103. Inoue T., Sata M., Hikichi Y., Sohma R., Fukuda D., Uchida T., et al. Mobilization of CD34-positive bone marrow-derived cells after coronary stent implantation: impact on restenosis. Circulation 115 (2007) 553-561
104. Ohtani K., Egashira K., Ihara Y., Nakano K., Funakoshi K., Zhao G., et al. Angiotensin II type 1 receptor blockade attenuates in-stent restenosis by inhibiting inflammation and progenitor cells. Hypertension 48 (2006) 664-670
105. Isner J.M., Vale P.R., Symes J.F., and Losordo D.W. Assessment of risks associated with cardiovascular gene therapy in human subjects. Circ Res 89 (2001) 389-400
106. Dzau V.J., Beatt K., Pompilio G., and Smith K. Current perceptions of cardiovascular gene therapy. Am J Cardiol 92 (2003) 18N-23N
107. Forstermann U., and Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113 (2006) 1708-1714
108. Mallat Z., and Tedgui A. The role of transforming growth factor beta in atherosclerosis: novel insights and future perspectives. Curr Opin Lipidol 13 (2002) 523-529
109. Moulton K.S. Angiogenesis in atherosclerosis: gathering evidence beyond speculation. Curr Opin Lipidol 17 (2006) 548-555
110. Pires N.M., van der Hoeven B.L., de Vries M.R., Havekes L.M., van Vlijmen B.J., Hennink W.E., et al. Local perivascular delivery of anti-restenotic agents from a drug-eluting poly(epsilon-caprolactone) stent cuff. Biomaterials 26 (2005) 5386-5394
111. Jeremy J.Y., Gadsdon P., Shukla N., Vijayan V., Wyatt M., Newby A.C., et al. On the biology of saphenous vein grafts fitted with external synthetic sheaths and stents. Biomaterials 28 (2007) 895-908