Extracellular matrix gene expression in the developing mouse aorta (original) (raw)

Abstract

sparkles

AI

This research examines the extracellular matrix (ECM) gene expression associated with the development of the mouse aorta. The study emphasizes the significance of ECM in vascular smooth muscle cell (SMC) differentiation and the mechanical properties of the vessel wall, while also exploring the roles of various ECM molecules in mediating cellular functions and signaling during embryogenesis. By focusing on the changes in ECM composition throughout vessel wall maturation, the work contributes to a deeper understanding of vascular biology and its implications for developmental and pathophysiological processes.

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (174)

  1. Abe, M., Hasegawa, K., Wada, H., Morimoto, T., Yanazume, T., Kawamura, T., Hirai, M., Furukawa, Y., Kita, T. 2003. GATA-6 is involved in PPAR-mediated activation of diVerentiated phenotype in human vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 23, 404-410.
  2. Adams, L.D., Geary, R.L., McManus, B., Schwartz, S.M. 2000. A comparison of aorta and vena cava medial message expression by cDNA array analysis identifies a set of 68 consis- tently diVerentially expressed genes, all in aortic media. Circ. Res. 87, 623-631.
  3. Adams, R.H., Wilkinson, G.A., Weiss, C., Diella, F., Gale, N.W., Deutsch, U., Risau, W., Klein, R. 1999. Roles of ephrinB ligands and EphB receptors in cardiovascular develop- ment: Demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev. 13, 295-306.
  4. Agrotis, A., Samuel, M., Prapas, G., Bobik, A. 1996. Vascular smooth muscle cells express multiple type I receptors for TGF-ß, activin, and bone morphogenetic proteins. Biochem. Biophys. Res. Commun. 219, 613-618.
  5. Akimoto, T., Hammerman, M.R. 2003. Fibroblast growth factor 2 promotes microvessel formation from mouse embryonic aorta. Am. J. Physiol. Cell. Physiol. 284, C371-C377.
  6. Albert, E.N. 1972. Developing elastic tissue. An electron microscopic study. Am. J. Pathol. 69, 89-102.
  7. Arman, E., HaVner-Krausz, R., Chen, Y., Heath, J.K., Lonai, P. 1998. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrula- tion mammalian development. Proc. Natl. Acad. Sci. USA 95, 5082-5087.
  8. BergwerV, M., Gittenberger-de Groot, A.C., De Ruiter, M.C., van Iperen, L., Meijlink, F., Poelmann, R.E. 1998. Patterns of paired-related homeobox genes Prx1 and Prx2 suggest involvement in matrix modulation in the developing chick vascular system. Dev. Dyn. 213, 59-70.
  9. BergwerV, M., Gittenberger-de Groot, A.C., Wisse, L.J., De Ruiter, M.C., Wessels, A., Martin, J.F., Olson, E.N., Kern, M.J. 2000. Loss of function of the Prx1 and Prx2 homeobox genes alters architecture of the great elastic arteries and ductus arteriosus. Virchows Archiv. 436, 12-19.
  10. Berry, C.L., Looker, T., Germain, J. 1972. The growth and development of the rat aorta. I. Morphological aspects. J. Anat. 113, 1-16.
  11. Bondjers, C., Kalen, M., Hellstrom, M., Scheidl, S.J., Abramsson, A., Renner, O., Lindahl, P., Cho, H., Kehrl, J., Betsholtz, C. 2003. Transcription profiling of platelet-derived growth factor-B-deficient mouse embryos identifies RGS5 as a novel marker for pericytes and vascular smooth muscle cells. Am. J. Pathol. 162, 721-729.
  12. Bostrom, H., Willetts, K., Pekny, M., Leveen, P., Lindahl, P., Hedstrand, H., Pekna, M., Hellstrom, M., Gebre-Medhin, S., Schalling, M., Nilsson, M., Kurland, S., Tornell, J., Heath, J.K., Betsholtz, C. 1996. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 85, 863-873.
  13. Bouloumie, A., Drexler, H.C., Lafontan, M., Busse, R. 1998. Leptin, the product of Ob gene, promotes angiogenesis. Circ. Res. 83, 1059-1066.
  14. Bradham, D., Igarashi, A., Potter, R., Grotendorst, G. 1991. Connective tissue growth factor: A cysteine-rich mitogen secreted by human vascular endothelial cells is related to the SRC-induced immediate early gene product CEF-10. J. Cell. Biol. 114, 1285-1294.
  15. Brekken, R.A., Sage, E.H. 2001. SPARC, a matricellular protein: At the crossroads of cell- matrix communication. Matrix Biol. 19, 816-827.
  16. Carlin, B., JaVe, R., Bender, B., Chung, A.E. 1981. Entactin, a novel basal lamina-associated sulfated glycoprotein. J. Biol. Chem. 256, 5209-5214.
  17. Carmeliet, P., Moons, L., Ploplis, V., Plow, E., Collen, D. 1997. Impaired arterial neointima formation in mice with disruption of the plasminogen gene. J. Clin. Invest. 99, 200-208.
  18. Chen, B., Bronson, R.T., Klaman, L.D., Hampton, T.G., Wang, J.F., Green, P.J., Magnuson, T., Douglas, P.S., Morgan, J.P., Neel, B.G. 2000. Mice mutant for Egfr and Shp2 have defective cardiac semilunar valvulogenesis. Nat. Genet. 24, 296-299.
  19. Chen, S.L., Wang, S.C., Hosking, B., Muscat, G.E. 2001. Subcellular localization of the steroid receptor coactivators (SRCs) and MEF2 in muscle and rhabdomyosarcoma cells. Mol. Endocrinol. 15, 296-299.
  20. Cheng, L., Mantile, G., Pauly, R., Nater, C., Felici, A., Monticone, R., Bilato, C., Gluzband, Y.A., Crow, M.T., Stetler-Stevenson, W., Capogrossi, M.C. 1998. Adenovirus-mediated gene transfer of the human tissue inhibitor of metalloproteinase-2 blocks vascular smooth muscle cell invasiveness in vitro and modulates neointimal development in vivo. Circulation 98, 2195-2201.
  21. Cheng, N., Brantley, D.M., Chen, J. 2002. The ephrins and Eph receptors in angiogenesis. Cytokine Growth Factor Rev. 13, 75-85.
  22. Cho, H., Harrison, K., Schwartz, O., Kehrl, J.H. 2003. The aorta and heart diVerentially express RGS (regulators of G-protein signaling) proteins that selectively regulate sphingo- sine 1-phosphate, angiotensin II and endothelin-1 signaling. Biochem. J. 371, 973-980.
  23. Chung, A.E., Freeman, I.L., Braginski, J.E. 1977. A novel extracellular membrane elaborated by a mouse embryonal carcinoma-derived cell line. Biochem. Biophys. Res. Commun. 79, 859-868.
  24. Ciruna, B., Schwartz, L., Harpal, K., Yamaguchi, T., Rossant, J. 1997. Chimeric analysis of fibroblast growth factor receptor-1 (Fgfr1) function: A role for FGFR1 in morphogenetic movement through the primitive streak. Development 124, 2829-2841.
  25. Cornelius, L.A., Nehring, L.C., Harding, E., Bolanowski, M., Welgus, H.G., Kobayashi, D.K., Pierce, R.A., Shapiro, S.D. 1998. Matrix metalloproteinases generate angiostatin: EVects on neovascularization. J. Immunol. 161, 6845-6852.
  26. Corson, G.M., Charbonneau, N.L., Keene, D.R., Sakai, L.Y. 2004. DiVerential expression of fibrillin-3 adds to microfibril variety in human and avian, but not rodent, connective tissues. Genomics 83, 461-472.
  27. Dawson, D.W., Pearce, S.F., Zhong, R., Silverstein, R.L., Frazier, W.A., Bouck, N.P. 1997. CD36 mediates the In vitro inhibitory eVects of thrombospondin-1 on endothelial cells. J. Cell. Biol. 138, 707-717.
  28. Dimmeler, S., Fleming, I., Fisslthaler, B., Hermann, C., Busse, R., Zeiher, A.M. 1999. Activa- tion of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399, 601-605.
  29. Dollery, C.M., McEwan, J.R., Henney, A.M. 1995. Matrix metalloproteinases and cardiovas- cular disease. Circ. Res. 77, 863-868.
  30. Downes, M., Koopman, P. 2001. SOX18 and the transcriptional regulation of blood vessel development. Trends Cardiovasc. Med. 11, 318-324.
  31. Dufourcq, P., CouYnhal, T., Alzieu, P., Daret, D., Moreau, C., Duplaa, C., Bonnet, J. 2002. Vitronectin is up-regulated after vascular injury and vitronectin blockade prevents neointi- ma formation. Circ. Res. 53, 952-962.
  32. Eguchi, S., Numaguchi, K., Iwasaki, H., Matsumoto, T., Yamakawa, T., Utsunomiya, H., Motley, E.D., Kawakatsu, H., Owada, K.M., Hirata, Y., Marumo, F., Inagami, T. 1998. Calcium-dependent epidermal growth factor receptor transactivation mediates the angio- tensin II-induced mitogen-activated protein kinase activation in vascular smooth muscle cells. J. Biol. Chem. 273, 8890-8896.
  33. Ekblom, P., Timpl, R. 1996. The Laminins, New York: Harwold Academic Publishers.
  34. Esteve, P., Bovolenta, P. 1999. cSix4, a member of the six gene family of transcription factors, is expressed during placode and somite development. Mech. Dev. 85, 161-165.
  35. Ewart, A.K., Morris, C.A., Atkinson, D., Jin, W., Sternes, K., Spallone, P., Stock, A.D., Leppert, M., Keating, M.T. 1993a. Hemizygosity at the elastin locus in a developmental disorder, Williams syndrome. Nat. Genet. 5, 11-16.
  36. Ewart, A.K., Morris, C.A., Ensing, G.J., Loker, J., Moore, C., Leppert, M., Keating, M. 1993b. A human vascular disorder, supravalvular aortic stenosis, maps to chromosome 7. Proc Natl. Acad. Sci. USA 90, 3226-3230.
  37. Febbraio, M., Hajjar, D.P., Silverstein, R.L. 2001. CD36: A class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J. Clin. Invest. 108, 785-791.
  38. Felbor, U., Dreier, L., Bryant, R.A., Ploegh, H.L., Olsen, B.R., Mothes, W. 2000. Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J. 19, 1187-1194.
  39. Forsythe, J.A., Jiang, B.H., Iyer, N.V., Agani, F., Leung, S.W., Koos, R.D., Semenza, G.L. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia- inducible factor 1. Mol. Cell Biol. 16, 4604-4613.
  40. Francis, S.E., Goh, K.L., Hodivala-Dilke, K., Bader, B.L., Stark, M., Davidson, D., Hynes, R.O. 2002. Central roles of alpha5beta1 integrin and fibronectin in vascular develop- ment in mouse embryos and embryoid bodies. Arterioscler. Thromb. Vasc. Biol. 22, 927-933.
  41. Frazier, K., Williams, S., Kothapalli, D., Klapper, H., Grotendorst, G.R. 1996. Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor. J. Invest. Derm. 107, 404-411.
  42. Frid, M.G., Moiseeva, E.P., Stenmark, K.R. 1994. Multiple phenotypically distinct smooth muscle cell populations exist in the adult and developing bovine pulmonary arterial media in vivo. Circ. Res. 75, 669-681.
  43. Friedrichsen, S., Heuer, H., Christ, S., Winckler, M., Brauer, D., Bauer, K., Raivich, G. 2003. CTGF expression during mouse embryonic development. Cell Tiss. Res. 312, 175-188.
  44. Gacko, M., Chyczewski, L. 1997. Activity and localization of cathepsin B, D and G in aortic aneurysm. Int. Surg. 82, 398-402.
  45. Gacko, M., Glowinski, S. 1998. Cathepsin D and cathepsin L activities in aortic aneurysm wall and parietal thrombus. Clin. Chem. Lab. Med. 36, 449-452.
  46. Galvin, K.M., Donovan, M.J., Lynch, C.A., Meyer, R.I., Paul, R.J., Lorenz, J.N., Fairchild- Huntress, V., Dixon, K.L., Dunmore, J.H., Gimbrone, M.A., Jr., Falb, D., Huszar, D. 2000. A role for smad6 in development and homeostasis of the cardiovascular system. Nat. Genet. 24, 171-174.
  47. Garbers, D.L., Dubois, S.K. 1999. The molecular basis of hypertension. Ann. Rev. Biochem. 68, 127-155.
  48. Gerety, S.S., Wang, H.U., Chen, Z.F., Anderson, D.J. 1999. Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Molec. Cell 4, 403-414.
  49. Gerrity, R.G., CliV, W.J. 1975. The aortic tunica media of the developing rat. I. Quantitative stereologic and biochemical analysis. Lab. Invest. 32, 585-600.
  50. Gittenberger-de Groot, A.C., De Ruiter, M.C., BergwerV, M., Poelmann, R.E. 1999. Smooth muscle cell origin and its relation to heterogeneity in development and disease. Arterioscler Thromb. Vasc. Biol. 19, 1589-1594.
  51. Glukhova, M.A., Koteliansky, V.E. 1995. Integrins, Cytoskeletal and Extracellular Matrix Proteins in Developing Smooth Muscle Cells of Human Aorta. In: The Vascular Smooth Muscle Cell: Molecular and Biological Responses to the Extracellular Matrix (Schwartz, Mecham, Eds.), San Diego: Academic Press, pp. 37-79.
  52. Goetze, S., Kintscher, U., Kim, S., Meehan, W.P., Kaneshiro, K., Collins, A.R., Fleck, E., Hsueh, W.A., Law, R.E. 2001. Peroxisome proliferator-activated receptor-gamma ligands inhibit nuclear but not cytosolic extracellular signal-regulated kinase/mitogen-activated protein kinase-regulated steps in vascular smooth muscle cell migration. J. Cardiovasc. Pharmacol. 38, 909-921.
  53. Goetze, S., Xi, X.P., Kawano, H., Gotlibowski, T., Fleck, E., Hsueh, W.A., Law, R.E. 1999. PPAR gamma-ligands inhibit migration mediated by multiple chemoattractants in vascular smooth muscle cells. J. Cardiovasc. Pharmacol. 33, 798-806.
  54. Gorski, D.H., Walsh, K. 2000. The role of homeobox genes in vascular remodeling and angiogenesis. Circ. Res. 87, 865-872.
  55. Goumans, M.J., Mummery, C. 2000. Functional analysis of the TGF-ß receptor/Smad pathway through gene ablation in mice. Int. J. Dev. Biol. 44, 253-265.
  56. Groth, C., Lardelli, M. 2002. The structure and function of vertebrate fibroblast growth factor receptor 1. Int. J. Develop. Biol. 46, 393-400.
  57. Gu, Z., Reynolds, E., Song, J., Lei, H., Feijen, A., Yu, L., He, W., MacLaughlin, D., van den Eijnden-van Raaij, J., Donahoe, P., Li, E. 1999. The type I serine/threonine kinase receptor ActRIA (ALK2) is required for gastrulation of the mouse embryo. Development 126, 2551-2561.
  58. Hamblet, N.S., Lijam, N., Ruiz-Lozano, P., Wang, J., Yang, Y., Luo, Z., Mei, L., Chien, K.R., Sussman, D.J., Wynshaw-Boris, A. 2002. Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129, 5827-5838.
  59. Han, R.N., Post, M., Tanswell, A.K., Lye, S.J. 2003. Insulin-like growth factor-I receptor- mediated vasculogenesis/angiogenesis in human lung development. Am. J. Resp. Cell. Molec. Biol. 28, 159-169.
  60. Handford, P.A., Downing, A.K., Reinhardt, D.P., Sakai, L.Y. 2000. Fibrillin: From domain structure to supramolecular assembly. Matrix Biol. 19, 457-470.
  61. Harrelson, Z., Kelly, R.G., Goldin, S.N., Gibson-Brown, J.J., Bollag, R.J., Silver, L.M., Papaioannou, V.E. 2004. Tbx2 is essential for patterning the atrioventricular canal and for morphogenesis of the outflow tract during heart development. Development 131, 5041-5052.
  62. Haust, M.D., More, R.H., Benscome, S.A., Balis, J.U. 1965. Elastogenesis in human aorta: An electron microscopic study. Exp. Mol. Pathol. 4, 508-524.
  63. Hautmann, M.B., Thompson, M.M., Swartz, E.A., Olson, E.N., Owens, G.K. 1997. Angioten- sin II-induced stimulation of smooth muscle alpha-actin expression by serum response factor and the homeodomain transcription factor MHox. Circ. Res. 81, 600-610.
  64. Hellstrom, M., Kal n, M., Lindahl, P., Abramsson, A., Betsholtz, C. 1999. Role of PDGF-B and PDGFR-ß in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126, 3047-3055.
  65. Heximer, S.P., Knutsen, R.H., Sun, X., Kaltenbronn, K.M., Rhee, M.H., Peng, N., Oliveira- dos-Santos, A., Penninger, J.M., Muslin, A.J., Steinberg, T.H., Wyss, J.M., Mecham, R.P., Blumer, K.J. 2003. Hypertension and prolonged vasoconstrictor signaling in RGS2-deficient mice. J. Clin. Invest. 111, 445-452.
  66. Hilgers, K.F., Reddi, V., Krege, J.H., Smithies, O., Gomez, R.A. 1997. Aberrant renal vascular morphology and renin expression in mutant mice lacking angiotensin-converting enzyme. Hypertension 29, 216-221.
  67. Hishikawa, K., Nakaki, T., Fujii, T. 1999. Transforming growth factor-beta(1) induces apo- ptosis via connective tissue growth factor in human aortic smooth muscle cells. Eur. J. Pharmacol. 385, 287-290.
  68. Hishikawa, K., Nakaki, T., Fujii, T. 2000. Connective tissue growth factor induces apoptosis via caspase 3 in cultured human aortic smooth muscle cells. Eur. J. Pharmacol. 392, 19-22.
  69. Hixon, M.L., Muro-Cacho, C., Wagner, M.W., Obejero-Paz, C., Millie, E., Fujio, Y., Kureishi, Y., Hassold, T., Walsh, K., Gualberto, A. 2000. Akt1/PKB upregulation leads to vascular smooth muscle cell hypertrophy and polyploidization. J. Clin. Invest. 106, 1011-1020.
  70. Horiuchi, K., Weskamp, G., Lum, L., Hammes, H.P., Cai, H., Brodie, T.A., Ludwig, T., Chiusaroli, R., Baron, R., Preissner, K.T., Manova, K., Blobel, C.P. 2003. Potential role for ADAM15 in pathological neovascularization in mice. Molec. Cell. Biol. 23, 5614-5624.
  71. Hornstra, I.K., Birge, S., Starcher, B., Bailey, A.J., Mecham, R.P., Shapiro, S.D. 2003. Lysyl oxidase is required for vascular and diaphragmatic development in mice. J. Biol. Chem. 278, 14387-14393.
  72. Hungerford, J.E., Owens, G.K., Argraves, W.S., Little, C.D. 1996. Development of the aortic vessel wall as defined by vascular smooth muscle and extracellular matrix markers. Devel- op. Biol. 178, 375-392.
  73. Hynes, R.O. 2002. A reevaluation of integrins as regulators of angiogenesis. Nat. Med. 8, 918-921.
  74. Iaccarino, G., Ciccarelli, M., Sorriento, D., Cipolletta, E., Cerullo, V., Iovino, G.L., Paudice, A., Elia, A., Santulli, G., Campanile, A., Arcucci, O., Pastore, L., Salvatore, F., Condorelli, G., Trimarco, B. 2004. AKT Participates in Endothelial Dysfunction in Hypertension. Circulation 109, 2587-2593.
  75. Iozzo, R.V., Murdoch, A.D. 1996. Proteoglycans of the extracellular environment: Clues from the gene and protein side oVer novel perspectives in molecular diversity and function. FASEB J. 10, 598-614.
  76. Ishii, M., Kurachi, Y. 2003. Physiological actions of regulators of G-protein signaling (RGS) proteins. Life Sci. 74, 163-171.
  77. Jimenez, B., Volpert, O.V., Crawford, S.E., Febbraio, M., Silverstein, R.L., Bouck, N. 2000. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospon- din-1. Nat. Med. 6, 41-48.
  78. Johnsen, S.A., Subramaniam, M., Monroe, D.G., Janknecht, R., Spelsberg, T.C. 2002. Modu- lation of transforming growth factor beta (TGF-ß)/Smad transcriptional responses through targeted degradation of TGF-ß-inducible early gene-1 by human seven in absentia homologue. J. Biol. Chem. 277, 30754-30759.
  79. Jones, P.L., Rabinovitch, M. 1996. Tenascin-C is induced with progressive pulmonary vascu- lar disease in rats and is functionally related to increased smooth muscle cell proliferation. Circ. Res. 79, 1131-1142.
  80. Kaartinen, V., Dudas, M., Nagy, A., Sridurongrit, S., Lu, M.M., Epstein, J.A. 2004. Cardiac outflow tract defects in mice lacking ALK2 in neural crest cells. Development 131, 3481-3490.
  81. Kagiyama, S., Eguchi, S., Frank, G.D., Inagami, T., Zhang, Y.C., Phillips, M.I. 2002. Angio- tensin II-induced cardiac hypertrophy and hypertension are attenuated by epidermal growth factor receptor antisense. Circulation 106, 909-912.
  82. Kalinichenko, V.V., Gusarova, G.A., Tan, Y., Wang, I.C., Major, M.L., Wang, X., Yoder, H. M., Costal, R.H. 2003. Ubiquitous expression of the forkhead box M1B transgene accel- erates proliferation of distinct pulmonary cell types following lung injury. J. Biol. Chem. 278, 37888-37894.
  83. Karnik, S.K., Brooke, B.S., Bayes-Genis, A., Sorensen, L., Wythe, J.D., Schwartz, R.S., Keating, M.T., Li, D.Y. 2003. A critical role for elastin signaling in vascular morphogenesis and disease. Development 130, 411-423.
  84. Karrer, H.E. 1961. An electron microscope study of the aorta in young and aging mice. J. Ultrastruct. Res. 5, 1-17.
  85. Kelleher, C.M., McLean, S.E., Mecham, R.P. 2004. Vascular extracellular matrix and aortic development. Curr. Top. Dev. Biol. 62, 153-188.
  86. Kielty, C.M., Sherratt, M.J., Shuttleworth, C.A. 2002. Elastic fibres. J. Cell. Sci. 115, 2817-2828.
  87. Kim, R.Y., Robertson, E.J., Solloway, M.J. 2001. Bmp6 and Bmp7 are required for cushion formation and septation in the developing mouse heart. Develop. Biol. 235, 449-466.
  88. King, K.E., Iyemere, V.P., Weissberg, P.L., Shanahan, C.M. 2003. Kruppel-like factor 4 (KLF4/ GKLF) is a target of bone morphogenetic proteins and transforming growth factor beta 1 in the regulation of vascular smooth muscle cell phenotype. J. Biol. Chem. 278, 11661-11669.
  89. Kirby, R.J., Hamilton, G.M., Finnegan, D.J., Johnson, K.J., Jarman, A.P. 2001. Drosophila homolog of the myotonic dystrophy-associated gene, SIX5, is required for muscle and gonad development. Curr. Biol. 11, 1044-1049.
  90. Krege, J.H., John, S.W., Langenbach, L.L., Hodgin, J.B., Hagaman, J.R., Bachman, E.S., Jennette, J.C., O'Brien, D.A., Smithies, O. 1995. Male-female diVerences in fertility and blood pressure in ACE-deficient mice. Nature 375, 146-148.
  91. Kuo, C.T., Veselits, M.L., Barton, K.P., Lu, M.M., Clendenin, C., Leiden, J.M. 1997. The LKLF transcription factor is required for normal tunica media formation and blood vessel stabilization during murine embryogenesis. Genes Dev. 11, 2996-3006.
  92. Langille, B.L. 1996. Arterial remodeling: Relation to hemodynamics. Can. J. Physiol. Pharma- col. 74, 834-841.
  93. Larsson, J., Goumans, M.J., Sjostrand, L.J., van Rooijen, M.A., Ward, D., Leveen, P., Xu, X., ten Dijke, P., Mummery, C.L., Karlsson, S. 2001. Abnormal angiogenesis but intact hema- topoietic potential in TGF-beta type I receptor-deficient mice. EMBO J. 20, 1663-1673.
  94. Lechleider, R.J., Ryan, J.L., Garrett, L., Eng, C., Deng, C., Wynshaw-Boris, A., Roberts, A.B. 2001. Targeted mutagenesis of Smad1 reveals an essential role in chorioallantoic fusion. Dev. Biol. 240, 157-167.
  95. Li, C., Wong, W.H. 2001. Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proc. Natl. Acad. Sci. USA 98, 31-36.
  96. Li, D.Y., Brooke, B., Davis, E.C., Mecham, R.P., Sorensen, L.K., Boak, B.B., Eichwald, E., Keating, M.T. 1998a. Elastin is an essential determinant of arterial morphogenesis. Nature 393, 276-280.
  97. Li, D.Y., Faury, G., Taylor, D.G., Davis, E.C., Boyle, W.A., Mecham, R.P., Stenzel, P., Boak, B., Keating, M.T. 1998b. Novel arterial pathology in mice and humans hemizygous for elastin. J. Clin. Invest. 102, 1783-1777.
  98. Li, D.Y., Sorensen, L.K., Brooke, B.S., Urness, L.D., Davis, E.C., Taylor, D.G., Boak, B.B., Wendel, D.P. 1999. Defective angiogenesis in mice lacking endoglin. Science 284, 1534-1537.
  99. Li, S., Edgar, D., Fassler, R., Wadsworth, W., Yurchenco, P.D. 2003. The role of laminin in embryonic cell polarization and tissue organization. Dev. Cell 4, 613-624.
  100. Lijnen, H.R., Ugwu, F., Bini, A., Collen, D. 1998. Generation of an angiostatin-like fragment from plasminogen by stromelysin-1 (MMP-3). Biochemistry 37, 4699-4702.
  101. Lin, Q., Lu, J., Yanagisawa, H., Webb, R., Lyons, G.E., Richardson, J.A., Olson, E.N. 1998. Requirement of the MADS-box transcription factor MEF2C for vascular development. Development 125, 4565-4574.
  102. Ma, J.X., Yang, Z., Chao, J., Chao, L. 1995. Intramuscular delivery of rat kallikrein-binding protein gene reverses hypotension in transgenic mice expressing human tissue kallikrein. J. Biol. Chem. 270, 451-455.
  103. Macias-Silva, M., Hoodless, P.A., Tang, S.J., Buchwald, M., Wrana, J.L. 1998. Specific Activation of Smad1 Signaling Pathways by the BMP7 Type I Receptor, ALK2. J. Biol. Chem. 273, 25628-25636.
  104. Maltepe, E., Schmidt, J.V., Baunoch, D., Bradfield, C.A., Simon, M.C. 1997. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386, 403-407.
  105. Martin, K.M., Ellis, P.D., Metcalfe, J.C., Kemp, P.R. 2003. Selective modulation of the SM22alpha promoter by the binding of BTEB3 (basal transcription element-binding protein 3) to TGGG repeats. Biochem. J. 375, 457-463.
  106. McCawley, L.J., Matrisian, L.M. 2001. Matrix metalloproteinases: They're not just for matrix anymore!. Curr. Opin. Cell Biol. 13, 534-540.
  107. Mecham, R.P. 1998. Overview of extracellular matrix. Current Protocols in Cell Biology, New York: John Wiley & Sons Inc., pp. 10.1.1-10.1.13.
  108. Mecham, R.P., Davis, E.C. 1994. Elastic fiber structure and assembly. In: Extracellular Matrix Assembly and Structure (Yurchenko, Birk, Mecham, Eds.), San Diego: Academic Press, pp. 281-314.
  109. Miano, J.M., Topouzis, S., Majesky, M.W., Olson, E.N. 1996. Retinoid receptor expression and all-trans retinoic acid-mediated growth inhibition in vascular smooth muscle cells. Circula- tion 93, 1886-1895.
  110. Miettinen, P.J., Berger, J.E., Meneses, J., Phung, Y., Pedersen, R.A., Werb, Z., Derynck, R. 1995. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376, 337-341.
  111. Morikawa, W., Yamamoto, K., Ishikawa, S., Takemoto, S., Ono, M., Fukushi, J., Naito, S., Nozaki, C., Iwanaga, S., Kuwano, M. 2000. Angiostatin generation by cathepsin D secreted by human prostate carcinoma cells. J. Biol. Chem. 275, 38912-38920.
  112. Mudgett, J.S., Hutchinson, N.I., Chartrain, N.A., Forsyth, A.J., McDonnell, J., Singer, II, Bayne, E.K., Flanagan, J., Kawka, D., Shen, C.F., Stevens, K., Chen, H., Trumbauer, M., Visco, D.M. 1998. Susceptibility of stromelysin 1-deficient mice to collagen-induced arthritis and cartilage destruction. Arthritis. Rheum. 41, 110-121.
  113. Muragaki, Y., Timmons, S., GriYth, C.M., Oh, S.P., Fadel, B., Quertermous, T., Olsen, B.R. 1995. Mouse Col18a1 is expressed in a tissue-specific manner as three alternative variants and is localized in basement membrane zones. Proc. Natl. Acad. Sci. USA 92, 8763-8767.
  114. Nabel, E.G., Yang, Z.Y., Plautz, G., Forough, R., Zhan, X., Haudenschild, C.C., Maciag, T., Nabel, G.J. 1993. Recombinant fibroblast growth factor-1 promotes intimal hyperplasia and angiogenesis in arteries in vivo. Nature 362, 844-846.
  115. Nakamura, H. 1988. Electron microscopic study of the prenatal development of the thoracic aorta in the rat. Am. J. Anat. 181, 406-418.
  116. Nguyen, L.L., D'Amore, P.A. 2001. Cellular interactions in vascular growth and diVerentiation. Int. Rev. Cytol. 204, 1-48.
  117. O'Reilly, M.S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W.S., Flynn, E., Birkhead, J.R., Olsen, B.R., Folkman, J. 1997. Endostatin: An endogenous inhibitor of angiogenesis and tumor growth. Cell 88, 277-285.
  118. Oh, S.P., Seki, T., Goss, K.A., Imamura, T., Yi, Y., Donahoe, P.K., Li, L., Miyazono, K., ten Dijke, P., Kim, S., Li, E. 2000. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc. Natl. Acad. Sci. USA 97, 2626-2631.
  119. Olson, T.M., Michels, V.V., Urban, Z., Csiszar, K., Christiano, A.M., Driscoll, D.J., Feldt, R.H., Boyd, C.D., Thibodeau, S.N. 1995. A 30 kb deletion within the elastin gene results in familial supravalvular aortic stenosis. Hum. Molec. Gen. 4, 1677-1679.
  120. Onda, M., Ishiwata, T., Kawahara, K., Wang, R., Naito, Z., Sugisaki, Y. 2002. Expression of lumican in thickened intima and smooth muscle cells in human coronary atherosclerosis. Exp. Molec. Pathol. 72, 142-149.
  121. Ornitz, D.M., Xu, J., Colvin, J.S., McEwen, D.G., MacArthur, C.A., Coulier, F., Gao, G., Goldfarb, M. 1996. Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271, 15292-15297.
  122. Owens, G.K. 1995. Regulation of diVerentiation of vascular smooth muscle cells. Physiol. Rev. 75, 487-517.
  123. Owens, G.K., Kumar, M.S., WamhoV, B.R. 2004. Molecular regulation of vascular smooth muscle cell diVerentiation in development and disease. Physiol. Rev. 84, 767-801.
  124. Ozaki, H., Watanabe, Y., Takahashi, K., Kitamura, K., Tanaka, A., Urase, K., Momoi, T., Sudo, K., Sakagami, J., Asano, M., Iwakura, Y., Kawakami, K. 2001. Six4, a putative myogenin gene regulator, is not essential for mouse embryonal development. Molec. Cell. Biol. 21, 3343-3350.
  125. Paule, W.J. 1963. Electron microscopy of the newborn rat aorta. J. Ultrastruct. Res. 8, 219-235.
  126. Pease, D.C., Paule, W.J. 1960. Electron microscopy of elastic arteries; the thoracic aorta of the rat. J. Ultrastruct. Res. 3, 469-483.
  127. Peng, J., Zhang, L., Drysdale, L., Fong, G.H. 2000. The transcription factor EPAS-1/hypoxia- inducible factor 2alpha plays an important role in vascular remodeling. Proc. Natl. Acad. Sci. USA 97, 8386-8391.
  128. Pepper, M.S. 2001. Extracellular proteolysis and angiogenesis. Thromb. Haemost. 86, 346-355.
  129. Petajaniemi, N., Korhonen, M., Kortesmaa, J., Tryggvason, K., Sekiguchi, K., Fujiwara, H., Sorokin, L., Thornell, L.E., Wondimu, Z., Assefa, D., Patarroyo, M., Virtanen, I. 2002. Localization of laminin alpha4-chain in developing and adult human tissues. J. Histochem. Cytochem. 50, 1113-1130.
  130. Ploplis, V.A., Carmeliet, P., Vazirzadeh, S., Van Vlaenderen, I., Moons, L., Plow, E.F., Collen, D. 1995. EVects of disruption of the plasminogen gene on thrombosis, growth, and health in mice. Circulation 92, 2585-2593.
  131. Riquelme, C., Larrain, J., Schonherr, E., Henriquez, J.P., Kresse, H., Brandan, E. 2001. Antisense inhibition of decorin expression in myoblasts decreases cell responsiveness to transforming growth factor beta and accelerates skeletal muscle diVerentiation. J. Biol. Chem. 276, 3589-3596.
  132. Risau, W., Flamme, I. 1995. Vasculogenesis. Annu. Rev. Cell. Dev. Biol. 11, 73-91.
  133. Roose, J., Korver, W., Oving, E., Wilson, A., Wagenaar, G., Markman, M., Lamers, W., Clevers, H. 1998. High expression of the HMG box factor sox-13 in arterial walls during embryonic development. Nucleic Acids Res. 26, 469-476.
  134. Rossant, J.a.H., Lorraine 2002. Signaling Pathways in Vascular Development. Annu. Rev. Cell. Dev. Biol. 18, 541-573.
  135. Ruegg, C., Mariotti, A. 2003. Vascular integrins: Pleiotropic adhesion and signaling molecules in vascular homeostasis and angiogenesis. Cell Molec. Life Sci. 60, 1135-1157.
  136. Sambhi, M.P., Swaminathan, N., Wang, H., Rong, H. 1992. Increased EGF binding and EGFR mRNA expression in rat aorta with chronic administration of pressor angiotensin II. Biochem. Med. Metab. Biol. 48, 8-18.
  137. Santiago, F.S., Atkins, D.G., Khachigian, L.M. 1999. Vascular smooth muscle cell proliferation and regrowth after mechanical injury in vitro are Egr-1/NGFI-A-dependent. Am. J. Pathol. 155, 897-905.
  138. Schwartz, S.M., Mecham, R.P. 1995. In: The Vascular Smooth Muscle Cell: Molecular and Biological Responses to the Extracellular Matrix San Diego: Academic Press, p. 410.
  139. Shapiro, S.D., GriYn, G.L., Gilbert, D.J., Jenkins, N.A., Copeland, N.G., Welgus, H.G., Senior, R.M., Ley, T.J. 1992. Molecular cloning, chromsomal localization, and bacterial expression of a muring macrophage metalloelastase. J. Biol. Chem. 267, 4664-4671.
  140. Shi, Y., Patel, S., Niculescu, R., Chung, W., Desrochers, P., Zalewski, A. 1999. Role of matrix metalloproteinases and their tissue inhibitors in the regulation of coronary cell migration. Arterioscler. Thromb. Vasc. Biol. 19, 1150-1155.
  141. Shiojima, I., Walsh, K. 2002. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ. Res. 90, 1243-1250.
  142. Sibilia, M., Steinbach, J.P., Stingl, L., Aguzzi, A., Wagner, E.F. 1998. A strain-independent postnatal neurodegeneration in mice lacking the EGF receptor. EMBO J. 17, 719-731.
  143. Sibilia, M., Wagner, E.F. 1995. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269, 234-238.
  144. Silverman, E.S., Khachigian, L.M., Santiago, F.S., Williams, A.J., Lindner, V., Collins, T. 1999. Vascular smooth muscle cells express the transcriptional corepressor NAB2 in response to injury. Am. J. Pathol. 155, 1311-1317.
  145. Smyth, N., Vatansever, H.S., Murray, P., Meyer, M., Frie, C., Paulsson, M., Edgar, D. 1999. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm diVerentiation. J. Cell. Biol. 144, 151-160.
  146. Soriano, P. 1994. Abnormal kidney development and hematological disorders in PDGF beta- receptor mutant mice. Genes Dev. 8, 1888-1896.
  147. Sorokin, L.M., Pausch, F., Frieser, M., Kroger, S., Ohage, E., Deutzmann, R. 1997. Develop- mental regulation of the laminin alpha5 chain suggests a role in epithelial and endothelial cell maturation. Dev. Biol. 189, 285-300.
  148. Spurbeck, W.W., Ng, C.Y., Strom, T.S., Vanin, E.F., DavidoV, A.M. 2002. Enforced expres- sion of tissue inhibitor of matrix metalloproteinase-3 aVects functional capillary morpho- genesis and inhibits tumor growth in a murine tumor model. Blood 100, 3361-3368.
  149. Strydom, D.J. 1998. The angiogenins. Cell. Molec. Life Sci. 54, 811-824.
  150. Swaminathan, N., Vincent, M., Sassard, J., Sambhi, M.P. 1996. Elevated epidermal growth factor receptor levels in hypertensive Lyon rat kidney and aorta. Clin. Exp. Pharmacol. Physiol. 23, 793-796.
  151. Tanaka, K., Hiraiwa, N., Hashimoto, H., Yamazaki, Y., Kusakabe, M. 2004. Tenascin-C regulates angiogenesis in tumor through the regulation of vascular endothelial growth factor expression. Int. J. Cancer 108, 31-40.
  152. Tang, M., Wang, G., Lu, P., Karas, R.H., Aronovitz, M., Heximer, S.P., Kaltenbronn, K.M., Blumer, K.J., Siderovski, D.P., Zhu, Y., Mendelsohn, M.E. 2003. Regulator of G-protein signaling-2 mediates vascular smooth muscle relaxation and blood pressure. Nat. Med. 9, 1506-1512.
  153. Theocharis, A.D., Karamanos, N.K. 2002. Decreased biglycan expression and diVerential decorin localization in human abdominal aortic aneurysms. Atherosclerosis 165, 221-230.
  154. Threadgill, D.W., Dlugosz, A.A., Hansen, L.A., Tennenbaum, T., Lichti, U., Yee, D., LaMantia, C., Mourton, T., Herrup, K., Harris, R.C., et al. 1995. Targeted disruption of mouse EGF receptor: EVect of genetic background on mutant phenotype. Science 269, 230-234.
  155. Thyberg, J., Hinek, A., Nilsson, J., Friberg, U. 1979. Electron microscopic and cytochemical studies of rat aorta. Intracellular vesicles containing elastin-and collagen-like material. Histochem. J. 11, 1-17.
  156. Thyboll, J., Kortesmaa, J., Cao, R., Soininen, R., Wang, L., Iivanainen, A., Sorokin, L., Risling, M., Cao, Y., Tryggvason, K. 2002. Deletion of the laminin alpha4 chain leads to impaired microvessel maturation. Molec. Cell. Biol. 22, 1194-1202.
  157. Timpl, R., Dziadek, M., Fujiwara, S., Nowack, H., Wick, G. 1983. Nidogen: A new, self- aggregating basement membrane protein. Eur. J. Biochem. 137, 455-465.
  158. Trask, B.C., Trask, T.M., Broekelmann, T., Mecham, R.P. 2000. The microfibrillar proteins MAGP-1 and fibrillin-1 form a ternary complex with the chondroitin sulfate proteoglycan decorin. Molec. Biol. Cell. 11, 1499-1507.
  159. Tremblay, K.D., Dunn, N.R., Robertson, E.J. 2001. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 128, 3609-3621.
  160. Urness, L.D., Sorensen, L.K., Li, D.Y. 2000. Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat. Genet. 26, 328-331.
  161. van Gijn, M.E., Blankesteijn, W.M., Smits, J.F., Hierck, B., Gittenberger-de Groot, A.C. 2001. Frizzled 2 is transiently expressed in neural crest-containing areas during development of the heart and great arteries in the mouse. Anat. Embryol. 203, 185-192.
  162. Vandromme, M., Rochat, A., Meier, R., Carnac, G., Besser, D., Hemmings, B.A., Fernandez, A., Lamb, N.J.C. 2001. Protein kinase B beta /Akt2 plays a specific role in muscle diVer- entiation. J. Biol. Chem. 276, 8173-8179.
  163. Wang, H.U., Chen, Z.F., Anderson, D.J. 1998. Molecular distinction and angiogenic interac- tion between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93, 741-753.
  164. Wang, J., Xiong, W., Yang, Z., Davis, T., Dewey, M.J., Chao, J., Chao, L. 1994. Human tissue kallikrein induces hypotension in transgenic mice. Hypertension 23, 236-243.
  165. Wang, L.C., Kuo, F., Fujiwara, Y., Gilliland, D.G., Golub, T.R., Orkin, S.H. 1997. Yolk sac angiogenic defect and intra-embryonic apoptosis in mice lacking the Ets-related factor TEL. EMBO J. 16, 4374-4383.
  166. Wight, T.N. 2002. Versican: A versatile extracellular matrix proteoglycan in cell biology. Curr. Opin. Cell. Biol. 14, 617-623.
  167. Wolinsky, H., Glagov, S. 1967. A lamellar unit of aortic medial structure and function in mammals. Circ. Res. 20, 99-111.
  168. Wu, L., Tanimoto, A., Murata, Y., Sasaguri, T., Fan, J., Sasaguri, Y., Watanabe, T. 2003. Matrix metalloproteinase-12 gene expression in human vascular smooth muscle cells. Genes Cells 8, 225-234.
  169. Xin, X., Yang, S., Kowalski, J., Gerritsen, M.E. 1999. Peroxisome proliferator-activated receptor gamma ligands are potent inhibitors of angiogenesis in vitro and in vivo. J. Biol. Chem. 274, 9116-9121.
  170. Xu, H., el-Gewely, M.R. 2001. P53-responsive genes and the potential for cancer diagnostics and therapeutics development. Biotechnology Annu. Rev. 7, 131-164.
  171. Xu, W., Baribault, H., Adamson, E.D. 1998. Vinculin knockout results in heart and brain defects during embryonic development. Development 125, 327-337.
  172. Yamaguchi, T.P., Harpal, K., Henkemeyer, M., Rossant, J. 1994. Fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 8, 3032-3044.
  173. Yang, X., Castilla, L.H., Xu, X., Li, C., Gotay, J., Weinstein, M., Liu, P.P., Deng, C.X. 1999. Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development 126, 1571-1580.
  174. Yao, L.Y., Moody, C., Schonherr, E., Wight, T.N., Sandell, L.J. 1994. Identification of the proteoglycan versican in aorta and smooth muscle cells by DNA sequence analysis, in situ hybridization and immunohistochemistry. Matrix Biol. 14, 213-225.