Postnatal regulation of fibroblast growth factor ligand and receptor gene expression in rat thoracic aorta

American Journal of Pathology

Volumn 149, Issue 6, 1996, Pages 2119-2131

  Winkles, Jeffrey A ^a,b   Alberts, Gregory F ^a   Peifley, Kimberly A ^a   Nomoto, Kenichi ^c,d   Liau, Gene ^a,b   Majesky, Mark W ^c  

^a HOLLAND LABORATORY   (United States)

^b GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d EISAI CO LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; GENE EXPRESSION REGULATION; GROWTH REGULATION; MITOGENESIS; NONHUMAN; NORTHERN BLOTTING; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER; THORACIC AORTA; VASCULAR SMOOTH MUSCLE;

ANIMALS; ANIMALS, NEWBORN; AORTA, THORACIC; BASE SEQUENCE; CELLS, CULTURED; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIGANDS; MUSCLE, SMOOTH; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, FIBROBLAST GROWTH FACTOR; RNA, MESSENGER;

EID: 0029826615     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (91)

1. Burgess WH, Winkles JA: The fibroblast growth factor family: multifunctional regulators of cell proliferation. Cell Proliferation in Cancer: Regulatory Mechanisms of Neoplastic Cell Growth. Edited by L Pusztai, CE Lewis, E Yap. Oxford, Oxford University Press, 1996, pp 154-217
2. Miyamoto M, Naruo K-I, Seko C, Matsumoto S, Kondo T, Kurokawa T: Molecular cloning of a novel cytokine cDNA encoding the ninth member of the fibroblast growth factor family, which has a unique secretion property. Mol Cell Biol 1993, 13:4251-4259
3. Edelman ER, Nugent MA, Smith LT, Karnovsky MJ: Basic fibroblast growth factor enhances the coupling of intimai hyperplasia and proliferation of vasa vasorum in injured rat arteries. J Clin Invest 1992, 89:465-473
4. Nabel EG, Yang Z-Y, Plautz G, Forough R, Zhan X, Haudenschild CC, Maciag T, Nabel GJ: Recombinant fibroblast growth factor-1 promotes intimai hyperplasia and angiogenesis in arteries in vivo. Nature 1993, 362: 844-846
5. Lindner V, Majack RA, Reidy MA: Basic fibroblast growth factor stimulates endothelial regrowth and proliferation in denuded arteries. J Clin Invest 1990, 85: 2004-2008
6. Lindner V, Lappi DA, Baird A, Majack RA, Reidy MA: Role of basic fibroblast growth factor in vascular lesion formation. Circ Res 1991, 68:106-113
7. Bjornsson TD, Dryjski M, Tluczek J, Mennie R, Ronan J, Mellin TN, Thomas KA: Acidic fibroblast growth factor promotes vascular repair. Proc Natl Acad Sci USA 1991, 88:8651-8655
8. Pu L-Q, Sniderman AD, Brassard R, Lachapelle KJ, Graham AM, Lisbona R, Symes JF: Enhanced revascularizat on of the ischemic limb by angiogenic therapy. Circulation 1993, 88:208-215
9. Cuevas P, Gonzalez AM, Carceller F, Baird A: Vascular response to basic fibroblast growth factor when infused onto the normal adventitia or into the injured media of the rat carotid artery. Circ Res 1991, 69:360-369
10. Asahara T, Bauters C, Zheng LP, Takeshita S, Bunting S, Ferrara N, Symes JF, Isner JM: Synergistic effect of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in vivo. Circulation 1995, 92(II):365-371
11. Flugelman MY, Virmani R, Correa R, Yu Z, Farb A, Leon MB, Elami A, Fu Y, Casscells W, Epstein SE: Smooth muscle cell abundance and fibroblast growth factors in coronary lesions of patients with nonfatal unstable angina. Circulation 1993, 88:2493-2500
12. Hughes SE, Crossman D, Hall PA: Expression of basic and acidic fibroblast growth factors and their receptor in normal and atherosclerotic human arteries. Cardiovasc Res 1993, 27:1214-1219
13. Peoples GE, Blotnick S, Takahashi K, Freeman MR, Klagsbrun M, Eberlein TJ: T lymphocytes that infiltrate tumors and atherosclerotic plaques produce heparin-binding epidermal growth factor-like growth factor and basic fibroblast growth factor: a potential pathologic role. Proc Natl Acad Sci USA 1995, 92:6547-6551
14. Brogi E, Winkles JA, Underwood R, Clinton SK, Alberts GF, Libby P: Distinct patterns of expression of fibroblast growth factors and their receptors in human atheroma and non-atherosclerotic arteries: association of acidic FGF with plaque microvessels and macrophages. J Clin Invest 1993, 92:2408-2418
15. Zhao X, Yeoh T, Hiebert M, Frist WH, Miller GG: The expression of acidic fibroblast growth factor (heparin-binding growth factor-1) and cytokine genes in human cardiac allografts and T cells. Transplantation 1993, 56:1177-1182
16. Lindner V, Reidy MA: Proliferation of smooth muscle cells after vascular injury is inhibited by an antibody against basic fibroblast growth factor. Proc Natl Acad Sci USA 1991, 88:3739-3743
17. Nguyen HC, Steinberg BM, LeBoutillier M III, Baumann FG, Rifkin DB, Grossi EA, Galloway AC: Suppression of neointimal lesions after vascular injury: a role for polyclonal anti-basic fibroblast growth factor antibody. Surgery 1994, 116:456-462
18. Johnson DE, Williams LT: Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 1993, 60:1-40
19. Miki T, Bottaro DP, Fleming TP, Smith CL, Burgess WH, Chan AML, Aaronson SA: Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc Natl Acad Sci USA 1992, 89:246-250
20. Chellaiah AT, McEwen DG, Werner S, Xu J, Ornitz DM: Fibroblast growth factor receptor (FGFR) 3: alternative splicing in immunoglobulin-like domain III creates a receptor highly specific for acidic FGF/FGF-1. J Biol Chem 1994, 269:11620-11627
21. Dionne CA, Crumley G, Bellot F, Kaplow JM, Searfoss G, Ruta M, Burgess WH, Jaye M, Schlessinger J: Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J 1990, 9:2685-2692
22. Ornitz DM, Leder P: Ligand specificity and heparin dependence of fibroblast growth factor receptor-1 and receptor-3. J Biol Chem 1992, 267:16305-16311
23. Ron D, Reich R, Chedid M, Lengel C, Cohen OE, Chan AM-L, Neufeld G, Miki T, Tronick SR: Fibroblast growth factor receptor 4 is a high affinity receptor for both acidic and basic fibroblast growth factor but not for keratinocyte growth factor. J Biol Chem 1993, 268: 5388-5394
24. Liau G, Winkles JA, Cannon MS, Kuo L, Chilian WM: Dietary-induced atherosclerotic lesions have increased levels of acidic FGF mRNA and altered cytoskeletal and extracellular matrix mRNA expression. J Vasc Res 1993, 30:327-332
25. Sarzani R, Brecher P, Chobanian AV: Growth factor expression in aorta of normotensive and hypertensive rats. J Clin Invest 1989, 83:1404-1408
26. Lindner V, Reidy MA: Expression of basic fibroblast growth factor and its receptor by smooth muscle cells and endothelium in injured rat arteries. Circ Res 1993, 73:589-595
27. Miano JM, Vlasic N, Tota RR, Stemerman MB: Smooth muscle cell immediate-early gene and growth factor activation follows vascular injury: a putative in vivo mechanism for autocrine growth. Arterioscler Thromb Vase Biol 1993, 13:211-219
28. Casscells W, Lappi DA, Olwin BB, Wai C, Siegman M, Speir EH, Sasse J, Baird A: Elimination of smooth muscle cells in experimental restenosis: targeting of fibroblast growth factor receptors. Proc Natl Acad Sci USA 1992, 89:7159-7163
29. Fishel RS, Thourani V, Eisenberg SJ, Shai SY, Corson MA, Nabel EG, Bernstein KE, Berk BC: Fibroblast growth factor stimulates angiotensin converting enzyme expression in vascular smooth muscle cells. J Clin Invest 1995, 95:377-387
30. More RS, Brack MJ, Underwood MJ, Gershlick AH: Growth factor persistence after vessel wall injury in a rabbit angioplasty model. Am J Cardiol 1994, 73:1031-1032
31. More RS, Underwood MJ, Brack MJ, de Bono DP, Gershlick AH: Changes in vessel wall plasminogen activator activity and smooth muscle cell proliferation and activation after arterial injury. Cardiovasc Res 1995, 29:22-26
32. Tanaka H, Sukhova G, Schwartz D, Libby P: Proliferating arterial smooth muscle cells after balloon injury express TNF-α but not interleukin-1 or basic fibroblast growth factor. Arterioscler Thromb Vase Biol 1996, 16: 12-18
33. Daley SJ, Gotlieb Al: Fibroblast growth factor receptor-1 expression is associated with neointimal formation in vitro. Am J Pathol 1996, 148:1193-1202
34. Olson NE, Chao S, Lindner V, Reidy MA: Intimai smooth muscle cell proliferation after balloon catheter injury: the role of basic fibroblast growth factor. Am J Pathol 1992, 140:1017-1023
35. Gerrity RG, Cliff WJ: The aortic tunica media of the developing rat. Lab Invest 1975, 32:585-600
36. Olivetti G, Anversa P, Melissari M, Loud AV: Morphometric study of early postnatal development of the thoracic aorta in the rat. Circ Res 1980, 47:417-424
37. Berry CL, Looker T, Germain J: The growth and development of the rat aorta. J Anal 1972, 113:1-16
38. Bucher B, Travo P, Laurent P, Stoclet JC: Use of vascular smooth muscle single cell suspensions for rapid cell number determination in rat thoracic aorta media layer. Cell Biol Int Rep 1982, 6:113-123
39. Cook CL, Weiser MCM, Schwartz PE, Jones CL, Majack RA: Developmentally timed expression of an embryonic growth phenotype in vascular smooth muscle cells. Circ Res 1994, 74:189-196
40. Owens GK, Thompson MM: Developmental changes in isoactin expression in rat aortic smooth muscle cells in vivo. J Biol Chem 1986, 261:13373-13380
41. Bochaton-Piallat ML, Gabbiani F, Gabbiani G: Heterogeneity of rat aortic smooth muscle cell replication during development: correlation with replicative activity after experimental endothelial denudation in adults. J Submicrosc Cytol Pathol 1994, 26:1-8
42. Lombardi DM, Reidy MA, Schwartz SM: Methodological considerations important in the accurate quantitation of aortic smooth muscle cell replication in the normal rat. Am J Pathol 1991, 138:441-446
43. Majesky MW, Benditt EP, Schwartz SM: Expression and developmental control of platelet-derived growth factor A-chain and B-chain/Sis genes in rat aortic smooth muscle cells. Proc Natl Acad Sci USA 1988, 85:1524-1528
44. 1Adrenergic stimulation of platelet-derived growth factor A-chain gene expression in rat aorta. J Biol Chem 1990, 265:1082-1088
45. Majesky MW, Giachelli CM, Reidy MA, Schwartz SM: Rat carotid neointimal smooth muscle cells reexpress a developmentally regulated mRNA phenotype during repair of artery injury. Circ Res 1992, 71:759-768
46. Alberts GF, Peifley KA, Johns A, Kleha JF, Winkles JA: Constitutive endothelin-1 overexpression promotes smooth muscle cell proliferation via an external autocrine loop J Biol Chem 1994, 269:10112-10118
47. Avivi A, Zimmer Y, Yayon A, Yarden Y, Givol D: Flg2, a new member of the family of fibroblast growth factor receptors. Oncogene 1991, 6:1089-1092
48. Avivi A, Zimmer Y, Yayon A, Yarden Y, Givol D: Flg2, a new member of the family of fibroblast growth factor receptors. Oncogene 1992, 7:823
49. Stark KL, McMahon JA, McMahon AP: FGFR-4, a new member of the fibroblast growth factor receptor family, expressed in the definitive endoderm and skeletal muscle lineages of the mouse. Development 1991, 113:641-651
50. Zeymer U, Fishbein MC, Forrester JS, Cercek B: Proliferating cell nuclear antigen immunohistochemistry in rat aorta after balloon denudation. Am J Pathol 1992, 141:685-690
51. Looker T, Berry CL: The growth and development of the rat aorta. J Anat 1972, 113:17-34
52. Alberts GF, Hsu DKW, Peifley KA, Winkles JA: Differential regulation of acidic and basic fibroblast growth factor gene expression in fibroblast growth factortreated rat aortic smooth muscle cells. Circ Res 1994, 75:261-267
53. Powell PP, Klagsbrun M: Three forms of rat basic fibroblast growth factor are made from a single mRNA and localize to the nucleus. J Cell Physiol 1991, 148:202-210
54. van Neck JW, van Berkel PHC, Telleman P, Steijns LSW, Onnekink C, Bloemers HPJ: Effect of ploidy on transcription levels in cultured rat aortic smooth muscle cells. FEBS Lett 1992, 297:189-195
55. Hultgardh-Nilsson A, Krondahl U, Querol-Ferrer V, Ringertz NR: Differences in growth factor response in smooth muscle cells isolated from adult and neonatal rat arteries. Differentiation 1991, 47:99-105
56. Hultgardh-Nilsson A, Querol-Ferrer V, Jonzon B, Krondahl U, Nilsson J: Cyclic AMP, early response gene expression, and DNA synthesis in rat smooth muscle cells. Exp Cell Res 1994, 214:297-302
57. Kaner RJ, Medina J, Nicholson AC, Ursea R, Schwartz SM, Hajjar DP: Developmentally regulated herpesvirus plaque formation in arterial smooth muscle cells. Circ Res 1993, 73:10-14
58. van Neck JW, Medina JJ, Onnekink C, Schwartz SM, Bloemers HPJ: Expression of basic fibroblast growth factor and fibroblast growth factor receptor genes in cultured rat aortic smooth muscle cells. Biochim Biophys Acta 1995, 1261:210-214
59. Lemire JM, Covin CW, White S, Giachelli CM, Schwartz SM: Characterization of cloned aortic smooth muscle cells from young rats. Am J Pathol 1994, 144:1068-1081
60. Van G, Fukabori Y, McBride G, Nikolaropolous S, McKeehan WL: Exon switching and activation of stromal and embryonic fibroblast growth factor (FGF)-FGF receptor genes in prostate epithelial cells accompany stromal independence and malignancy. Mol Cell Biol 1993, 13:4513-4522
61. Villaschi S, Nicosia RF: Angiogenic role of endogenous basic fibroblast growth factor released by rat aorta after injury. Am J Pathol 1993, 143:181-190
62. Hultgardh-Nilsson A, Krondahl U, Jiang W, Nilsson J, Ringertz NR: Endogenous activation of c-myc expression and DNA synthesis in serum-starved neonatal rat smooth muscle cells. Differentiation 1993, 52:161-168
63. Giachelli C, Bae N, Lombardi D, Majesky M, Schwartz S: Molecular cloning and characterization of 2B7, a rat mRNA which distinguishes smooth muscle cell phenotypes in vitro and is identical to osteopontin (secreted phosphoprotein I, 2aR). Biochem Biophys Res Commun 1991, 177:867-873
64. Han DKM, Liau G: Identification and characterization of developmentally regulated genes in vascular smooth muscle cells. Circ Res 1992, 71:711-719
65. Liau G, Han DKM: Smooth muscle gene expression during developmental maturation. The Smooth Muscle Cell. Edited by SM Schwartz, R Mecham. New York, Academic Press, 1995, pp 141-161
66. Kitaoka T, Bost LM, Ishigooka H, Aotaki-Keen AE, Hjelmeland LM: Increasing cell density down-regulates the expression of acidic FGF by human RPE cells in vitro. Curr Eye Res 1993, 12:993-999
67. Bost LM, Aotaki-Keen AE, Hjelmeland LM: Cellular adhesion regulates bFGF gene expression in human retinal pigment epithelial cells. Exp Eye Res 1994, 58: 545-552
68. Moffett J, Kratz E, Florkiewicz R, Stachowiak MK: Promoter regions involved in density-dependent regulation of basic fibroblast growth factor gene expression in human astrocytic cells. Proc Natl Acad Sci USA 1996, 93:2470-2475
69. Murphy PR, Sato R, Sato Y, Friesen HG: Fibroblast growth factor messenger ribonucleic acid expression in a human astrocytoma cell line: regulation by serum and cell density. Mol Endocrinol 1988, 2:591-598
70. Powell PP, Klagsbrun M: Regulation of basic fibroblast growth factor mRNA expression in rat C6 glioma cells. Exp Cell Res 1993, 209:224-230
71. Winkles JA, Gay CG: Serum, phorbol ester, and polypeptide mitogens increase class 1 and 2 heparin-binding (acidic and basic fibroblast) growth factor gene expression in human vascular smooth muscle cells. Cell Growth Differ 1991, 2:531-540
72. Chotani MA, Payson RA, Winkles JA, Chiu I: Human fibroblast growth factor 1 gene expression in vascular smooth muscle cells is modulated via an alternate promoter in response to serum and phorbol ester. Nucleic Acids Res 1995, 23:434-441
73. Cook PW, Coffey RJ Jr, Magun BE, Pittelkow MR, Shipley GD: Expression and regulation of mRNA coding for acidic and basic fibroblast growth factor and transforming growth factor-α in cells derived from human skin. Mol Endocrinol 1990, 4:1377-1385
74. Goldsmith KT, Gammon RB, Garver RI Jr: Modulation of bFGF in lung fibroblasts by TGF-β and PDGF. Am J Physiol 1991, 261:L378-L385
75. Root LL, Shipley GD: Human dermal fibroblasts express multiple bFGF and aFGF proteins. In Vitro Cell Dev Biol 1991, 27A:815-822
76. Sternfeld MD, Hendrickson JE, Keeble WW, Rosenbaum JT, Robertson JE, Pittelkow MR, Shipley GD: Differential expression of mRNA coding for heparin-binding growth factor type 2 in human cells. J Cell Physiol 1988, 136:297-304
77. Xin X, Johnson AD, Scott-Burden T, Engler D, Casscells W: The predominant form of fibroblast growth factor receptor expressed by proliferating human arterial smooth muscle cells in culture is type I. Biochem Biophys Res Commun 1994, 204:557-564
78. Liaw L, Schwartz SM: Comparison of gene expression in bovine aortic endothelium in vivo versus in vitro. Arterioscler Thromb 1993, 13:985-993
79. Terracio L, Ronnstrand L, Tingstrom A, Rubin K, Claesson-Welsh L, Funa K, Heldin C-H: Induction of platelet-derived growth factor receptor expression in smooth muscle cells and fibroblasts upon tissue culturing. J Cell Biol 1988, 107:1947-1957
80. Majors A, Ehrhart LA: Basic fibroblast growth factor in the extracellular matrix suppresses collagen synthesis and type III procollagen mRNA levels in arterial smooth muscle cell cultures. Arterioscler Thromb 1993, 13: 680-686
81. Kennedy SH, Qin H, Lin L, Tan EML: Basic fibroblast growth factor regulates type I collagen and collagenase gene expression in human smooth muscle cells. Am J Pathol 1995, 146:764-771
82. Tamm I, Kikuchi T, Zychlinsky A: Acidic and basic fibroblast growth factors are survival factors with distinctive activity in quiescent BALB/C 3T3 murine fibroblasts. Proc Natl Acad Sci USA 1991, 88:3372-3376
83. Renaud F, Oliver L, Desset S, Tassin J, Romquin N, Courtois Y, Laurent M: Up-regulation of aFGF expression in quiescent cells is related to cell survival. J Cell Physiol 1994, 158:435-443
84. Sweetnam PM, Sanon HR, White LA, Brass BJ, Jaye M, Whittemore SR: Differential effects of acidic and basic fibroblast growth factors on spinal cord cholinergic, , and glutamatergic neurons J Neurochem 1991, 57:237-249
85. Schmidt MF, Kater SB: Fibroblast growth factors, depolarization, and substratum interact in a combinatorial way to promote neuronal survival. Dev Biol 1993, 158: 228-237
86. Wu YY, Bradshaw RA: Effect of nerve growth factor and fibroblast growth factor on PC12 cells: inhibition by orthovanadate. J Cell Biol 1993, 121:409-422
87. Williams EJ, Furness J, Walsh FS. Doherty P: Characterisation of the second messenger pathway underlying neunte outgrowth stimulated by FGF. Development 1994, 120:1685-1693
88. Fox JC, Shanley JR: Antisense inhibition of basic fibroblast growth factor induces apoptosis in vascular smooth muscle cells. J Biol Chem 1996, 271:12578-12584
89. Cuevas P, Carceller F, Ortega S, Zazo M, Nieto I, Gimenezgallego G: Hypotensive activity of fibroblast growth factor. Science 1991, 254:1208-1210
90. Rosenblatt S, Irikura K, Caday CG, Finklestein SP, Moskowitz MA: Basic fibroblast growth factor dilates rat pial arterioles. J Cereb Blood Flow Metab 1994, 14:70-74
91. Boussairi EH, Sassard J: Cardiovascular effects of basic fibroblast growth factor in rats. J Cardiovasc Pharmacol 1994, 23:99-102