Novel ideas of gene therapy for atherosclerosis: Modulation of cellular signal transduction of TGF-Β family

Current Pharmaceutical Design

Volumn 12, Issue 7, 2006, Pages 877-886

  Ishisaki, Akira ^a   Matsuno, Hiroyuki ^b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b DOSHISHA WOMEN'S COLLEGE OF LIBERAL ARTS   (Japan)

Author keywords

Activin A; Atherosclerosis; BMP; Gene therapy; Smad; TGF

Indexed keywords

ACTIVIN A; BLEOMYCIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 9; CHORDIN; NOGGIN; SMAD4 PROTEIN; SMAD6 PROTEIN; SMAD7 PROTEIN; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL CALCIFICATION; CELL DIFFERENTIATION; DISEASE COURSE; GENE OVEREXPRESSION; GENE THERAPY; HUMAN; LUNG FIBROSIS; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SYSTEMATIC REVIEW; UPREGULATION; VASCULAR SMOOTH MUSCLE; ANIMAL; BIOLOGICAL MODEL; GENETICS; METHODOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ATHEROSCLEROSIS; GENE THERAPY; HUMANS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 33645321892     PISSN: 13816128     EISSN: None     Source Type: Journal    
DOI: 10.2174/138161206776056083     Document Type: Review

References (140)

1. Stary HC, Chandler AB, Glaskov S, Guyton JR, Insull Jr W, Rosenfeld ME, et al. A definition of intimal, fatty streak and intermediate lesions of atherosclerosis. A report from the Committee on Vasculer Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb 1994; 14: 840-856.
2. Lusis AJ. Atherosclerosis. Nature 2000; 407: 233-241.
3. Starry HC, Chandler AB, Dinsmore RE, Foster V, Glagov S, Insull Jr W, 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.
4. Dhore CR, Cleutjens JP, Ludgens E, Cleutjens KB, Geusens PP, Kitslaar PJ, et al. Differential expression of bone matrix regulatory proteins in human atherosclerotic plaques. Arterioscler Thromb Vas Biol 2001; 21: 1998-2003.
5. Griethe W, Schmitt R, Jurgensen JS, Bachmann S, Eckardt KU, Schindler R. Bone morphogenetic protein-4 expression in vascular lesions of calciphylaxis. J Nephrol 2003; 16: 728-732.
6. Davies MR, Lund RJ, Hruska KA. BMP-7 is an efficacious treatment of vascular calcification in a murine model of atherosclerosis and chronic renal failure. J Am Soc Nephrol 2003; 14: 1559-1567.
7. Schluesener HJ, Meyerman R. Immunolocalization of BMP-6, a novel TGF-β-related cytokine, in normal and atherosclerotic smooth muscle cells. Atherosclerosis 1995; 113: 153-156.
8. Inoue S, Orimo A, Hosoi T, Ikegami A, Kozaki K, Ouchi Y, et al. Demonstration of activin-A in arteriosclerotic lesions. Biochem Biophys Res Commun 1994; 205: 441-448.
9. Pawlowski JE, Taylor DS, Valentine M, Hail ME, Ferrer P, Kowara MC, et al. Stimulation of activin A expression in rat aortic SMCs by thrombin and angiotensin II correlates with neointimal formation in vivo. J Clin Invest 1997; 100: 639-648.
10. Nikol S, Isner JM, Pickering JG, Kearney M, Leclerc G, Weir L. Expression of transforming growth factor-beta 1 is increased in human vascular restenosis lesions. J Clin Invest 1992; 90: 1582-1592.
11. Demer LL, Watson KE, Boström K. Mechanism of calcification in atherosclerosis. Trends Cardiovasc Med 1994; 4: 45-49.
12. Wexler L, Brundage B, Crouse J, Detrano R, Fuster V, Maddani J, et al. Coronary artery calcification: pathophysiology, epidemiology, imaging methods and clinical implications. Circulation 1996; 94: 1175-1192.
13. Wilson PWF, Kauppila LI, O'Donnel CJ, Kiel DP, Hannan M, Polak JM, et al. Abdominal aortic calcific deposits are an important predictor of vascular morbidity and mortality. Circulation 2001; 103: 1529-1534.
14. Gronholdt ML, Wagner A, Wiebe BM, Hansen JU, Schroeder TV, Wilhjelm JE, et al. Spiral computed tomographic imaging related to computerized ultrasonographic images of carotid plaque morphology and histology. J Ultrasound Med 2001; 20: 451-458.
15. Boström K, Watson KE, Stanford WP, Demer LL. Atherosclerotic calcification: relation to developmental osteogenesis. Am J Cardiol 1995; 75: 88B-91B.
16. Schmid K, McSharry WO, Pameijer CH, Binette JP. Chemical and physicochemical studies on the mineral deposits of the human atherosclerotic aorta. Atherosclerosis 1980; 37: 199-210.
17. Deneke Y, Langner K, Grewe PH, Harrer E, Müller KM. Ossification in atherosclerotic arteries. Z Kardiol 2001; 90: III-106-III-115.
18. Shioi A, Mori K, Jono S, Wakikawa T, Hiura Y, Koyama H, et al. Mechanism of atherosclerotic calcification. Z Kardiol 2000; 89: II75-II79.
19. Tyson KL, Reynolds JL, McNair R, Zhang Q, Weissberg PL, Shanahan CM. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arteriosc Thromb Vasc Biol 2003; 23: 489-494.
20. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, et al. Targeted disruption of Cbfal results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997; 89: 755-764.
21. Wilkie AO, Tang Z, Elanko N, Walsh S, Twigg SR, Hurst JA, et al. Functional haploinsufficiency of the human homeobox gene MSX2 causes defects in skull ossification. Nat Genet 2000; 24: 387-390.
22. Schor AM, Allen TD, Canfield AE, Sloan P, Schor SL. Pericytes derived from the retinal microvasculature undergo calcification in vitro. J Cell Sci 1990; 97: 449-461.
23. Boström K, Watson KE, Hom S, Wortham C, Herman IM, Demer LL. Bone morphogenetic protein expression in human atherosclerotic lesion. J Clin Invest 1993; 91: 1800-1809.
24. Watson KE, Boström K, Ravindranath R, Lam T, Norton B, Demer LL. TGF-beta 1 and 1 and 25-hydroxychoresterol stimulate osteoblast-like vascular cells to calcify. J Clin Invest 1994; 93: 2106-2113.
25. Tintut Y, Parhami F, Boström K, Jackson SM, Demer LL. cAMP stimulates osteoblast-like differentiation of calcifying vascular cells: potential signaling pathway for vascular calcification. J Biol Chem 1998; 273: 7547-7553.
26. Steitz SA, Speer MY, Curinga G, Yang HY, Haynes P, Aebersold R, et al. Smooth muscle cell phenotypic transition associated with calcification. Upregulation of Cbfal and downregulation of smooth muscle lineage markers. Circ Res 2001; 89: 1147-1154.
27. Khouri RK, Koudsi B, Reddi H. Tissue transformation into bone in vivo. A potential practical application. JAMA 1991; 266: 1953-1955.
28. Yudell RM, Block MS. Bone gap healing in the dog using recombinant human bone morphogenetic protein-2. J Oral Maxillofac Surg 2000; 58: 761-766.
29. Katagiri T, Yamaguchi A, Ikeda T, Yoshiki S, Wozny JM, Rosen V, et al. Tanaka H, Omura S, Suda T. The non-osteogenic mouse pluripotent cell line, C3H10T1/2, is induced to differentiate into osteoblastic cells by recombinant human bone morphogenetic protein-2. Biochem Biophys Res Commn 1990; 172: 295-299.
30. Wnag EA, Israel DI, Kelly S, Luxenberg DP. Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells. Growth Factors 1993; 9: 57-71.
31. Asahina I, Sampath TK, Hauschka PV. Human osteogenic protein-1 induces chondroblastic, osteoblastic and/or adipocytic differentiation of clonal murine target cells. Exp Cell Res 1996; 222: 38-47.
32. Ahrens M, Ankenbauer T, Schroder D, Hollnagel A, Mayer H, Gross G. Expression of human bone morphogenetic protein-2 or -4 in murine mesenchymal progenitor C3H101/2 cells induces differentiation into distinct mesenchymal cell lineages. DNA Cell Biol 1993; 12: 871-880.
33. Yamaguchi A, Katagiri T, Ikeda T, Wozny JM, Rosen V, Wang EA, et al. Recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J Cell Biol 1991; 113: 681-687.
34. Takuwa Y, Ohse C, Wang EA, Wozny JM, Yamashita K. Bone morphogenetic protein-2 stimulates alkaline phosphatase activity and collagen synthesis in cultured osteoblastic cells, MC3T3-E1. Biochem Biophys Res Commun 1991; 174: 96-101.
35. Yamaguchi A, Ishizuka T, Kintou N, Wada Y, Katagiri T, Wozny JM, et al. Effects of BMP-2, BMP-4 and BMP-6 on osteoblast differentiation of bone marrow-derived stromal cell line, ST2 and MC3T3-G2/PA6. Biochem Biophys Res Commun 1996; 220: 366-371.
36. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signaling from cell membrane to nucleous through SMAD proteins. Nature 1997; 390: 465-471.
37. Whitman M. Smads and early developmental signaling by the TGFbeta superfamily. Genes Dev 1998; 12: 2445-2462.
38. Massaguè J, Chen YG. Controlling TGF-beta signaling. Genes Dev 2000; 14: 627-644.
39. Miyazono K, ten Dijke P, Heldin CH. TGF-beta signaling by Smad proteins. Adv Immunol 2000; 75: 115-157.
40. ten Dijke P, Goumans MJ, Itoh F, Itoh S. Regulation of cell proliferation by smad proteins. J Cell Physiol 2002; 191: 1-16.
41. Wrana JL, Attisano L, Wieser R, Ventura F, Massagué J. Mechanism of activation of the TGF-beta receptor. Nature 1994; 370: 341-347.
42. Attisano L, Wrana JL. Smads as transcriptional co-modulators. Curr Opin Cell Biol 2000; 12: 235-243.
43. Massagué J, Wotton D. Transcriptional control by the TGF-β/ Smad signaling system. EMBO J 2000; 19: 1745-1754.
44. Dennler S, Itoh S, Viven D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3 and Smad4 to critical TGFβ-inducible elements in the promoter of human plasminogen activator inhibitor-type I gene. EMBO J 1998; 17: 3091-3100.
45. Shi Y, Wang YF, Jayaraman L, Yang H, Massagué J, Pavletich NP. Crystal structure of a Smad MH1 domain bound to DNA: insights on DNA binding in TGF-β signaling. Cell 1998; 94: 585-594.
46. Dennler S, Huet S, Gauthier JM. A short amino acid sequence in MH1 domain is responsible for functional differences between Smad2 and Smad3. Oncogene 1999; 18: 1643-1648.
47. Feng XH, Zhang Y, Wu RY, Derynck R. The tumor suppressor Smad4/DPC4 and transcriptional adaptor CBP/p300 are coactivators for Smad3 in TGF-β-induced transcriptional activation. Genes Dev 1998; 12: 2153-2163.
48. Janknecht R, Wells NJ, Hunter T. TGF-β-stimulated cooperation of Smad proteins with the coactivators CBP/p300. Genes Dev 12, 1998: 2114-2119.
49. Topper JN, DiChiara MR, Brown JD, Williams AJ, Falb D, Collins T, et al. CREB binding protein is a required coactivator for Smad-dependent, transforming growth factor β Transcriptional responses in endothelial cells. Pros Natl Acad Sci USA 1998; 95: 9506-9511.
50. Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, et al. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 1999; 284: 479-482.
51. Pearson KL, Hunter T, Janknecht R. Activation of Smad1-mediated transcription by p300/CBP. Biochim Biophys Acta 1999; 1489: 354-364.
52. Nishihara A, Hanai J, Imamura T, Miyazono K, Kawabata M. E1 A inhibits transforming growth factor-beta signaling through binding to Smad proteins. J Biol Chem 1999; 274: 28716-28723.
53. Kim RH, Wang D, Tsang M, Martin J, Huff C, de Caestecker MP, et al. A novel smad nuclear interacting protein, SNIP 1, suppresses p300-dependent TGF-beta signal transduction. Genes Dev 2000; 14: 1605-1616.
54. Hata A, Seoane J, Lagna G, Montalvo E, Hemmati-Brivanlou A, Massagué J. OAZ uses distinct DNA- and protein-binding zinc fingers in separate BMP-Smad and Olf signaling pathways. Cell 2000; 100: 229-240.
55. Shibuya H, Iwata H, Masuyama N, Gotoh, Y, Yamaguchi K, Irie K, et al. Role of TAK1 and TAB1 in BMP signaling in early Xenopus development. EMBO J 1998; 17: 1019-1028.
56. Yamaguchi K, Nagai S, Ninomiya-Tsuji J, Nishita M, Tamai K, Irie K, et al. XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB1-TAK1 in the BMP signaling pathway. EMBO J 1999; 18: 179-187.
57. Banerjee C, McCabe LR, Choi JY, Hiebert SW, Stein JL, Stein GS, et al. Runt homology domain proteins in osteoblast differentiation: AML3/CBFA1 is a major component of a bone-specific complex. J Cell Biochem 1997; 66: 1-8.
58. Tsuji K, Ito Y, Noda M. Expression of the PEBP2alphaA/AML3/CBFA1 gene is regulated by BMP4/7 heterodimer and its overex-pression suppresses type I collagen and osteocalcin gene expression in osteoblastic and nonosteoblastic mesenchymal cells. Bone 1998; 22: 87-92.
59. Harada H, Tagashira S, Fujiwara M, Ogawa S, Katsumata T, Yamaguchi A, et al. Cbfal isoforms exert functional differences in osteoblast differentiation. J Biol Chem 1999; 274: 6972-6978.
60. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. Cbfal/Osf2: a transcriptional activator of osteoblast differentiation. Cell 1997; 89: 747-754.
61. Lee MH, Javed A, Kim HJ, Shin HI, Gutierrez S, Choi YJ, et al. Transient upregulation of CBFA1 in response to bone morphogenetic protein-2 and transforming growth factor β1 in C2C12 myogenic cells coincides with suppression of the myogenic phenotype but is not sufficient for osteoblast differentiation. J Cell Biochem 1999; 73: 114-125.
62. Nishimura R, Hata K, Harris SE, Ikeda F, Yoneda T. Core-binding factor alpha 1 (Cbfa1) induces osteoblastic differentiation of C2C12 cells without interactions with Smad1 and Smad5. Bone 2002; 31: 303-312.
63. Engelse MA, Neele JM, Bronckers ALJJ, Pannekoek H, de Vries CJM. Vascular calcification: expression patterns of the osteoblast-specific gene core binding factor α-1 and the protective factor matrix gla protein in human atherogenesis. Cardiovas Res 2001; 52: 281-289.
64. Proudfoot D, Skepper JN, Hegyi L, Bennett MR, Shanahan CM, Weissberg PL. Apoptosis regulates human vascular calcification in vitro: evidence for initiation of vascular calcification by apoptotic bodies. Circ Res 2000; 87: 1055-1062.
65. Onichtchouk D, Chen YG, Dosch R, Gawantka V, Delius H, Massagué J, et al. Silencing of TGF-beta signaling by the pseudore-ceptor BAMB1. Nature, 401: 480-485.
66. Grotewold L, Plum M, Dildrop R, Peters T, Ruther U. Bambi is coexpressed with BMP-4 during mouse embryogenesis. Mech Dev 2001; 100: 327-330.
67. Zhu H, Kavsak P, Abdollah S, Wrana JL, Thomsen GH. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 1999; 400: 687-693.
68. Arora K, Warrior R. A new Smurf in the Village. Dev Cell 2001; 1: 441-442.
69. Yoshida Y, Tanaka S, Umemori H, Minowa O, Usui M, Ikematsu N, et al. Negative regulation of BMP/Smad signaling by Tob in osteoblasts. Cell 2000; 103: 1085-1097.
70. Li Y, Turck CM, Teumer JK, Stavnezer E. Unique sequence, ski, in Sloan-Ketterring avian retrovirus with properties of a new cell-derived oncogene. J Vilol 1986; 57: 1065-1072.
71. Wang W, Mariani FV, Harland RM, Luo K. Ski represses bone morphogenetic protein signaling in Xenopus and mammalian cells. Proc Natl Acad Sci USA 2000; 97, 14394-14399.
72. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, et at. Smad6 inhibits signaling by the TGF-beta superfamily. Nature 1997; 389, 622-626.
73. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, Grinnell BW, et al. The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 1997; 89: 1165-1173.
74. Nakao A, Afrakhte M, Morén A, Nakayama T, Christian JL, Heuchel R, et al. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signaling. Nature 1997; 389: 631-635.
75. Souchelnytskyi S, Nakayama T, Nakao A, Morén A, Heldin CH, Christian JL, et al. Physical and functional interaction of murine and Xenopus Smad7 with bone morphogenetic protein receptors and transforming growth factor-beta receptors. J Biol Chem 1998; 273: 25364-25370.
76. Hata A, Lagna G, Massaguè J, Hemmati-Brivanlou A. Smad6 inhibits BMP/ Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 1998; 12: 186-197.
77. Nakayama T, Gardner H, Berg LK, Christian JL. Smad6 functions as an intracellular antagonist of some TGF-beta family members during Xenopus enbryogenesis. Genes Cells 1998; 3: 387-394.
78. Ishisaki A, Yamato K, Nakao A, Nonaka K, Ohguchi M, ten Dijke P, et al. Smad7 is an activin-inducible inhibitor of activin-induced growth arrest and apoptosis in mouse B cells. J Biol Chem 1998; 273:24293-24296.
79. Ishisaki A, Yamato K, Hashimoto S, Nakao A, Tamaki K, Nonaka K, et al. Differential inhibition of Smad6 and Smad7 on bone morphogenetic protein- and activin-mediated growth arrest and apoptosis in B cells. J Biol Chem 1999; 274: 13637-13642.
80. Zhao J, Shi W, Chen H, Warburton D. Smad7 and Smad6 differentially modulate transforming growth factor beta-induced inhibition of embryonic lung morphogenesis. J Biol Chem 2000; 275: 23992-23997.
81. Smith WC, Harland RM. Expression cloning of noggin, a new dorsalizing factor localized to the Speman organizer in Xenopus embryos. Cell 1992; 70: 829-840.
82. Zimmerman LB, De Jesus-Escobar JM, Harland RM. The Speman organizer signal Noggin binds and inactivates bone morphogenetic protein-4. Cell 1996; 86: 599-606.
83. Gazzerro E, Gangji V, Canalis E. Bone morphogenetic proteins induce the expression of Noggin, which limits their activity in cultured rat fibroblast. J Clin Invest 1998; 102: 2106-2114.
84. Abe E, Yamamoto M, Taguchi Y, Lecka-Czernik B, O'Brien CA, Economides AN, et al. Essential requirement of BMPs-2/4 for both osteoblast and osteoclast formation in murine bone marrow cultures from adult mice: antagonism by Noggin. J Bone Miner Res 2000; 15: 663-673.
85. Piccolo S, Sasai Y, Lu B, De Robertis EM. Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 1996; 86: 589-598.
86. Larrain J, Bachiller D, Lu B, Agius E, Piccolo S, De Robertis EM. BMP-binding modules in chordin: a model for signaling regulation in the extracellular space. Development 2000; 127: 821-830.
87. Boström K. Insights into the mechanism of vascular calcification. Am J Cardiol 2001; 88: 20E-22E.
88. Zebboudj AF, Imura M, Boström K. Matrix GLA protein, a regulatory protein for bone morphogenetic protein-2. J Biol Chem 2002; 277: 4388-4394.
89. Boström K, Tsao D, Shen S, Wang Y, Demer LL. Matrix GLA protein modulates differentiation induced by bone morphogenetic protein-2 in C3HI0T1/2 cells. J Biol Chem 2001; 276: 14044-14052.
90. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med 1999; 340: 115-126.
91. Bobik A, Agrotis A, Kanellakis P, Dilley R, Krushinsky A, Smirnov V, et al. Distinct patterns of transforming growth factor-β isoform and receptor expression in human atherosclerotic lesions: colocalization implicates TGF-β in fibrofatty lesion development. Circulation 1999; 99: 2883-2891.
92. Lutgens E, Cleutjens KB, Heeneman S, Koteliansky VE, Burkly LC, Daemen MJ. Both early and delayed anti-CD40L antibody treatment induces a stable plaque phenotype. Proc Natl Acad Sci USA 2000; 97: 7464-7469.
93. Vodovotz Y, Bogdan C, Paik J, Xie QW, Nathan C. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor-β. J Exp Med 1993; 178: 605-613.
94. Mallat Z, Gojova A, Marchiol-Fournigault C, Esposito B, Kamaté C, Merval R, et al. Inhibition of transforming growth factor-β signaling accelerates atherosclerosis and induces an unstable plaque phonotype in mice. Circ Res 2001; 89: 930-934.
95. Robertson AK, Rudling M, Zhou X, Gorelik L, Flavell RA, Hansson GK. Disruption of TGF-β signaling in T cells accelerates atherosclerosis. J Clin Invest 2003; 112: 1342-1350.
96. McCaffrey TA, Du B, Consigli S, Szabo P, Bray PJ, Hartner L, et al. Genomic instability in the type II TGF-β1 receptor gene in atherosclerotic and restenotic vascular cells. J Clin Invest 1997; 100: 2182-2188.
97. McCaffrey TA, Consigh S, Du B, Falcone DJ, Sanborn TA, Spokojny AM, et al. Decreased type II/type I TGF-beta receptor ratio in cells derived from human atherosclerotic lesions. Conversion from an antiproliferative to profibrotic response to TGF-betal. J Clin Invest 1995; 96: 2667-2675.
98. Ma X, Labinaz M, Goldstein J, Miller H, Koen WJ, Letarte M, et al. Endoglin is overexpressed after arterial injury and is required for transforming growth factor-β-induced inhibition of smooth muscle cell migration. Arterioscler Thromb Vasc Biol 2000; 20: 2546-2552.
99. Yamashita H, Ichijo H, Grimsby S, Morén A, ten Dijke P, Miyazono K. Endoglin forms a heteromeric complex with the signaling receptors for transforming growth factor-β. J Biol Chem 1994; 269: 1995-2001.
100. Caniggia I, Taylor CV, Ritchie JWK, Lye SJ, Letarte M. Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous explants. Endocrinology 1997; 138: 4977-4988.
101. Vale W, Hsueh A, Rivier C, Yu J. The inbibin/activin family of hormones and growth factors. In Peptide Growth Factors and Their Receptors II, pp 211-248. Eds MB Sporn, AB Roberts. New York: Springer-Verlag.
102. Thomsen G, Woolf T, Whitman M, Sokol S, Vaughan J, Vale W, et al. Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 1990; 63: 485-493.
103. Murata M, Eto Y, Sakai M, Muramatsu M. Erythroid differentiation factor is encoded by the same mRNA as that of the inhibin βA chain. Proc Natl Acad Sci USA 1988; 85: 2434-2438.
104. Kojima I, Mogami H, Kawamura N, Yasuda H, Shibata H. Modulation of growth of vascular SMC by activin A. Exp Cell Res 1993; 206: 152-156.
105. Engelse MA, Neele JM, van Achterberg TA, van Aken BE, van Schaik RH, Pannekoek H, et al. Human activin A is expressed in the atherosclerotic lesion and promotes the contractile phenotype of smooth muscle cells. Circ Res 1999; 85: 931-939.
106. Nakaoka T, Gonda K, Ogita T, Otawara-Hamamoto Y, Okabe F, Kira Y, et al. Inhibition of rat vascular SMC proliferation in vitro and in vivo by BMP-2. J Clin Invest 1997; 100: 2824-2832.
107. Engelse MA, Lardenoye JH, Neele JM, Grimbergen JM, de Vries MR, Lamfers ML, et al. Adenoviral activin A expression prevents intimal hyperplasia in human and murine blood vessels by maintaining the contractile smooth muscle cell phenotype. Circ Res 2002; 90: 1128-1134.
108. Arciniegas E, Sutton AB, Allen TD, Schor AM. Transforming growth factor beta 1 promotes the differentiation of endothelial cells into smooth muscle-like cells in vitro. J Cell Sci 1992; 103: 521-529.
109. Nakajima Y, Mironov V, Yamagishi T, Nakamura H, Markwald RR. Expression of smooth muscle alpha-actin in mesenchymal cells during formation of avian endocardial cushion tissue: a role for transforming growth factor beta3. Dev Dyn 1997; 209: 296-309.
110. Ishisaki A, Hayashi H, Li AJ, Imamura T. Human umbilical vein endothelium-derived cells retain potential to differentiate into smooth muscle-like cells. J Biol Chem 2003; 278: 1303-1309.
111. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med 2000; 6: 389-395.
112. Hellström M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999; 126: 3047-3055.
113. Hirschi KK, Rohovsky SA, D'Amore PA. PDGF, TGF-beta and heterotypic cell-cell interactions mediate endothelial cell-induced recruitrnent of 10T1/2 cells and their differentiation to a smooth muscle fate. J Cell Biol 1998; 141:805-814.
114. Poole TJ, Finkelstein EB, Cox CM. The role of FGF and VEGF in angioblast induction and migration during vascular development. Dev Dyn 2001; 220:1-17.
115. Cox CM, Poole TJ. Angioblast differentiation is influenced by the local environment: FGF-2 induces angioblasts and patterns vessel formation in the quail embryo. Dev Dyn 2000; 218: 371-382.
116. Rafii S. Circulating endothelial precursors: mystery, reality and promise. J Clin Invest 2000; 105: 17-19.
117. Isner JM, Asahara T. Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest 1999; 103: 1231-1236.
118. DeRuiter MC, Poelmann RE, VanMunsteren JC, Mironov V, Markwald RR, Gittenberger-de Groot AC. Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro. Circ Res 1997; 80: 444-451.
119. Frid MG, Kale VA, Stenmark KR. Mature vascular endothelium can give rise to smooth muscle cells via endothelial-mesencymal transdifferentiation: in vitro analysis. Circ Res 2002; 90: 1189-1196.
120. Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T, et al. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 2000; 408: 92-96.
121. Araki S, Shimada Y, Kaji K, Hayashi H. Apoptosis of vascular endothelial cells by fibroblast growth factor deprivation. Biochem Biophys Res Commun 1990; 168: 1194-1200.
122. Garfinkel S, Hu X, Prudovsky IA, McMahon GA, Kapnik EM, McDowell SD, et al. FGF-1-dependent proliferative and migratory responses are impaired in senescent human umbilical vein endothelial cells and correlate with the inability to signal tyrosine phosphorylation of fibroblast growth factor receptor-1 substrates. J Cell Biol 1996; 134: 783-791.
123. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, et al. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 2002; 8: 403-409.
124. Chen S, Kulik M, Lechleider RJ. Smad proteins regulate transcriptional induction of SM22α gene by TGF-β. Nucleic Acid Res 2003; 31: 1302-1310.
125. Mack CA, Patel SR, Schwartz EA, Zanzonico P, Hahn RT, Ilercil A, et al. Biologic bypass with the use of adenovirus-mediated gene transfer of the complementary deoxyribonucleic acid for VEGF 121 improves myocardial perfusion and function in the ischaemic porcine heart. J Thorac Cardiovasc Surg 1998; 115: 168-177.
126. Takeshita S, Zheng LP, Brogi E, Kearney M, Pu LQ, Bunting S, et al. Therapeutic angiogenesis: a single intraarterial bolus of VEGF augments revascularization in a rabbit ishemic hind limb model. J Clin Invest 1994; 93: 662-670.
127. Safi J, DiPaula AF, Riccioni T, Kajstura J, Ambrosio G, Becker LC, et al. Adenovirus-mediated acidic FGF gene transfer induces angiogenesis in the nonishemic rabbit heart. Microvasc Res 1999; 58: 238-249.
128. Celetti FL, Waugh JM, Amabile PG, Brendolan A, Hilfiker PR, Dake MD. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nature Med 2001; 7:425-429.
129. Cuevas P, Garcia-Calvo M, Carceller F, Reimers D, Zazo M, Cuevas B, et al. Correction of hypertension by normalization of endothelial levels of fibroblast growth factor and nitric oxide synthase in spontaneously hypertensive rats. Proc Natl Acad Sci USA 1996; 93: 11996-12001.
130. Isner JM. Still more debate over VEGF. Nat Med 2001; 6: 639-641.
131. Morishita R, Yamada S, Yamamoto K, Tomita N, Kida I, Sakurabayashi I, et al. Novel therapeutic strategy for atherosclerosis: ribozyme oligonucleotides against apolipoprotein(a) selectively inhibit apolipoprotein(a) but not plasminogen gene expression. Circulation 1998; 98: 1898-1904.
132. Nakao A, Fujii M, Matsumura R, Kumano K, Saito Y, Miyazono K, et al. Transient gene transfer and expression of Smad7 prevents bleomycin-induced lung fibrosis in mice. J Clin Invest 1999; 104:5-11.
133. Lan HY, Mu W, Tomita N, Huang XR, Li JH, Morishita R, et al. Inhibition of renal fibrosis by gene transfer of inducible Smad7 using ultrasound-microbubble system in rat UUO model. J Am Soc Nephrol 2003; 14: 1535-1548.
134. Duda DG, Sunamura M, Lefter LP, Furukawa T, Yokoyama T, Yatsuoka T, et al. Restoration of SMAD4 by gene therapy reverses the invasive phenotype in pancreatic adenocarcinoma cells. Oncogene 2003; 22: 6857-6864.
135. Alden TD, Beres EJ, Laurent JS, Engh JA, Das S, London SD, et al. The use of bone morphogenetic protein gene therapy in craniofacial bone repair. J Craniofac Surg 2000; 11: 24-30.
136. Tan J, Hu Y, Zheng H, Li S. Construction of recombinant adenoviral vector Ad-CMV-hTGFbeta1 for reversion of intervertebral disc degeneration by gene transfer. Chin J Traumatol 2002; 5: 97-102.
137. Haviv YS, Takayama Y, Nagi PA, Tousson A, Cook W, Wang M, et al. Modulation of renal glomerular disease using remote delivery of adenoviral-encoded soluble type II TGF-beta receptor fusion molecule. J Gene Med 2003; 5: 839-851.
138. Desideri G, Ferri C. Endothelial activation. Sliding door to atherosclerosis. Curr Pharm Des 2005; 11(17): 2163-75.
139. Flyvbjerg A, Khatir DS, Jensen LJ, Dagnaes-Hansen F, Gronbaek H, Rasch R. The involvement of growth hormone (GH), insulin-like growth factors (IGFs) and vascular endothelial growth factor (VEGF) in diabetic kidney disease. Curr Pharm Des 2004; 10(27): 3385-94.
140. Stefanidakis M, Koivunen E. Peptide-mediated delivery of therapeutic and imaging agents into mammalian cells. Curr Pharm Des 2004; 10(24): 3033-44.