Skip to main content
NCBI home page
The American Journal of Pathology logoLink to The American Journal of Pathology
. 1996 Dec;149(6):2119–2131.

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

J A Winkles 1, G F Alberts 1, K A Peifley 1, K Nomoto 1, G Liau 1, M W Majesky 1
PMCID: PMC1865367  PMID: 8952544

Abstract

Fibroblast growth factor (FGF)-1 and FGF-2 are potent angiogenic factors and vascular smooth muscle cell (SMC) mitogens in vivo. They function via binding to a family of structurally related cell surface receptors that possess intrinsic tyrosine kinase activity. Several studies have indicated that increased FGF and/or FGF receptor (FGFR) expression may correlate with adult SMC proliferation in vivo. In this study, we used Northern blot hybridization and reverse transcription-polymerase chain reaction assays to compare the FGF and FGFR mRNA levels in newborn rat aorta, where SMCs have a high replication index, to those in adult rat aorta, where SMCs are relatively quiescent. We found that FGF-2 and FGFR-2 mRNA expression was elevated 8.2- and 5.6-fold, respectively, in adult aorta. Increased FGF-2 protein expression in the adult aorta was confirmed by Western blot analysis. We also examined FGF and FGFR mRNA expression levels in SMC cultures derived from newborn or adult rat aorta. FGF-1 transcripts were more abundant in newborn SMCs whereas FGF-2 and FGFR-1 mRNA expression was higher in adult SMCs. Furthermore, FGF-1 and FGF-2 mRNA expression levels were altered by cell culture density and by serum treatment. We conclude that elevated FGF ligand and receptor expression does not always correlate with a high SMC proliferative index, that FGF-1 or FGF-2 may not be the primary mitogens responsible for newborn SMC growth in vivo, and that FGF-1 and FGF-2 may serve nonmitogenic functions within the mature, adult vessel wall.

Full text

PDF
2119

Images in this article

2122Figure 1
on p.2122
2123Figure 2
on p.2123
2123Figure 3
on p.2123
2124Figure 5
on p.2124
2125Figure 6
on p.2125
2125Figure 7
on p.2125
2126Figure 8
on p.2126

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alberts G. F., Hsu D. K., Peifley K. A., Winkles J. A. Differential regulation of acidic and basic fibroblast growth factor gene expression in fibroblast growth factor-treated rat aortic smooth muscle cells. Circ Res. 1994 Aug;75(2):261–267. doi: 10.1161/01.res.75.2.261. [DOI] [PubMed] [Google Scholar]
  2. Alberts G. F., Peifley K. A., Johns A., Kleha J. F., Winkles J. A. Constitutive endothelin-1 overexpression promotes smooth muscle cell proliferation via an external autocrine loop. J Biol Chem. 1994 Apr 1;269(13):10112–10118. [PubMed] [Google Scholar]
  3. Avivi A., Zimmer Y., Yayon A., Yarden Y., Givol D. Flg-2, a new member of the family of fibroblast growth factor receptors. Oncogene. 1991 Jun;6(6):1089–1092. [PubMed] [Google Scholar]
  4. Berry C. L., Looker T., Germain J. The growth and development of the rat aorta. I. Morphological aspects. J Anat. 1972 Oct;113(Pt 1):1–16. [PMC free article] [PubMed] [Google Scholar]
  5. Bjornsson T. D., Dryjski M., Tluczek J., Mennie R., Ronan J., Mellin T. N., Thomas K. A. Acidic fibroblast growth factor promotes vascular repair. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8651–8655. doi: 10.1073/pnas.88.19.8651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bochaton-Piallat M. L., 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 Jan;26(1):1–8. [PubMed] [Google Scholar]
  7. Bost L. M., Aotaki-Keen A. E., Hjelmeland L. M. Cellular adhesion regulates bFGF gene expression in human retinal pigment epithelial cells. Exp Eye Res. 1994 May;58(5):545–552. doi: 10.1006/exer.1994.1048. [DOI] [PubMed] [Google Scholar]
  8. Boussairi E. H., Sassard J. Cardiovascular effects of basic fibroblast growth factor in rats. J Cardiovasc Pharmacol. 1994 Jan;23(1):99–102. doi: 10.1097/00005344-199401000-00013. [DOI] [PubMed] [Google Scholar]
  9. Brogi E., Winkles J. A., Underwood R., Clinton S. K., Alberts G. F., Libby P. Distinct patterns of expression of fibroblast growth factors and their receptors in human atheroma and nonatherosclerotic arteries. Association of acidic FGF with plaque microvessels and macrophages. J Clin Invest. 1993 Nov;92(5):2408–2418. doi: 10.1172/JCI116847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bucher B., Travo P., Laurent P., Stoclet J. C. Use of vascular smooth-muscle single cell suspensions for rapid cell number determination in rat thoracic aorta media layer. Cell Biol Int Rep. 1982 Feb;6(2):113–123. doi: 10.1016/0309-1651(82)90087-x. [DOI] [PubMed] [Google Scholar]
  11. Casscells W., Lappi D. A., Olwin B. B., Wai C., Siegman M., Speir E. H., Sasse J., Baird A. Elimination of smooth muscle cells in experimental restenosis: targeting of fibroblast growth factor receptors. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7159–7163. doi: 10.1073/pnas.89.15.7159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chellaiah A. T., McEwen D. G., Werner S., Xu J., Ornitz D. M. 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 Apr 15;269(15):11620–11627. [PubMed] [Google Scholar]
  13. Chotani M. A., Payson R. A., Winkles J. A., Chiu I. M. 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 Feb 11;23(3):434–441. doi: 10.1093/nar/23.3.434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cook C. L., Weiser M. C., Schwartz P. E., Jones C. L., Majack R. A. Developmentally timed expression of an embryonic growth phenotype in vascular smooth muscle cells. Circ Res. 1994 Feb;74(2):189–196. doi: 10.1161/01.res.74.2.189. [DOI] [PubMed] [Google Scholar]
  15. Cook P. W., Coffey R. J., Jr, Magun B. E., Pittelkow M. R., Shipley G. D. Expression and regulation of mRNA coding for acidic and basic fibroblast growth factor and transforming growth factor alpha in cells derived from human skin. Mol Endocrinol. 1990 Sep;4(9):1377–1385. doi: 10.1210/mend-4-9-1377. [DOI] [PubMed] [Google Scholar]
  16. Cuevas P., Carceller F., Ortega S., Zazo M., Nieto I., Giménez-Gallego G. Hypotensive activity of fibroblast growth factor. Science. 1991 Nov 22;254(5035):1208–1210. doi: 10.1126/science.1957172. [DOI] [PubMed] [Google Scholar]
  17. Cuevas P., Gonzalez A. M., 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 Aug;69(2):360–369. doi: 10.1161/01.res.69.2.360. [DOI] [PubMed] [Google Scholar]
  18. Daley S. J., Gotlieb A. I. Fibroblast growth factor receptor-1 expression is associated with neointimal formation in vitro. Am J Pathol. 1996 Apr;148(4):1193–1202. [PMC free article] [PubMed] [Google Scholar]
  19. Dionne C. A., Crumley G., Bellot F., Kaplow J. M., Searfoss G., Ruta M., Burgess W. H., 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 Sep;9(9):2685–2692. doi: 10.1002/j.1460-2075.1990.tb07454.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Edelman E. R., Nugent M. A., Smith L. T., Karnovsky M. J. Basic fibroblast growth factor enhances the coupling of intimal hyperplasia and proliferation of vasa vasorum in injured rat arteries. J Clin Invest. 1992 Feb;89(2):465–473. doi: 10.1172/JCI115607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fishel R. S., Thourani V., Eisenberg S. J., Shai S. Y., Corson M. A., Nabel E. G., Bernstein K. E., Berk B. C. Fibroblast growth factor stimulates angiotensin converting enzyme expression in vascular smooth muscle cells. Possible mediator of the response to vascular injury. J Clin Invest. 1995 Jan;95(1):377–387. doi: 10.1172/JCI117666. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Flugelman M. Y., Virmani R., Correa R., Yu Z. X., Farb A., Leon M. B., Elami A., Fu Y. M., Casscells W., Epstein S. E. Smooth muscle cell abundance and fibroblast growth factors in coronary lesions of patients with nonfatal unstable angina. A clue to the mechanism of transformation from the stable to the unstable clinical state. Circulation. 1993 Dec;88(6):2493–2500. doi: 10.1161/01.cir.88.6.2493. [DOI] [PubMed] [Google Scholar]
  23. Fox J. C., Shanley J. R. Antisense inhibition of basic fibroblast growth factor induces apoptosis in vascular smooth muscle cells. J Biol Chem. 1996 May 24;271(21):12578–12584. doi: 10.1074/jbc.271.21.12578. [DOI] [PubMed] [Google Scholar]
  24. Gerrity R. G., Cliff W. J. The aortic tunica media of the developing rat. I. Quantitative stereologic and biochemical analysis. Lab Invest. 1975 May;32(5):585–600. [PubMed] [Google Scholar]
  25. 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 Jun 14;177(2):867–873. doi: 10.1016/0006-291x(91)91870-i. [DOI] [PubMed] [Google Scholar]
  26. Goldsmith K. T., Gammon R. B., Garver R. I., Jr Modulation of bFGF in lung fibroblasts by TGF-beta and PDGF. Am J Physiol. 1991 Dec;261(6 Pt 1):L378–L385. doi: 10.1152/ajplung.1991.261.6.L378. [DOI] [PubMed] [Google Scholar]
  27. Han D. K., Liau G. Identification and characterization of developmentally regulated genes in vascular smooth muscle cells. Circ Res. 1992 Sep;71(3):711–719. doi: 10.1161/01.res.71.3.711. [DOI] [PubMed] [Google Scholar]
  28. Hughes S. E., Crossman D., Hall P. A. Expression of basic and acidic fibroblast growth factors and their receptor in normal and atherosclerotic human arteries. Cardiovasc Res. 1993 Jul;27(7):1214–1219. doi: 10.1093/cvr/27.7.1214. [DOI] [PubMed] [Google Scholar]
  29. Hultgãrdh-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 Sep;214(1):297–302. doi: 10.1006/excr.1994.1261. [DOI] [PubMed] [Google Scholar]
  30. Hultgårdh-Nilsson A., Krondahl U., Jiang W. Q., Nilsson J., Ringertz N. R. Endogenous activation of c-myc expression and DNA synthesis in serum-starved neonatal rat smooth muscle cells. Differentiation. 1993 Jan;52(2):161–168. doi: 10.1111/j.1432-0436.1993.tb00626.x. [DOI] [PubMed] [Google Scholar]
  31. Hultgårdh-Nilsson A., Krondahl U., Querol-Ferrer V., Ringertz N. R. Differences in growth factor response in smooth muscle cells isolated from adult and neonatal rat arteries. Differentiation. 1991 Jul;47(2):99–105. doi: 10.1111/j.1432-0436.1991.tb00227.x. [DOI] [PubMed] [Google Scholar]
  32. Johnson D. E., Williams L. T. Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res. 1993;60:1–41. doi: 10.1016/s0065-230x(08)60821-0. [DOI] [PubMed] [Google Scholar]
  33. Kennedy S. H., Qin H., Lin L., Tan E. M. Basic fibroblast growth factor regulates type I collagen and collagenase gene expression in human smooth muscle cells. Am J Pathol. 1995 Mar;146(3):764–771. [PMC free article] [PubMed] [Google Scholar]
  34. Kitaoka T., Bost L. M., Ishigooka H., Aotaki-Keen A. E., Hjelmeland L. M. Increasing cell density down-regulates the expression of acidic FGF by human RPE cells in vitro. Curr Eye Res. 1993 Nov;12(11):993–999. doi: 10.3109/02713689309029225. [DOI] [PubMed] [Google Scholar]
  35. Lemire J. M., Covin C. W., White S., Giachelli C. M., Schwartz S. M. Characterization of cloned aortic smooth muscle cells from young rats. Am J Pathol. 1994 May;144(5):1068–1081. [PMC free article] [PubMed] [Google Scholar]
  36. Liau G., Winkles J. A., Cannon M. S., Kuo L., Chilian W. M. Dietary-induced atherosclerotic lesions have increased levels of acidic FGF mRNA and altered cytoskeletal and extracellular matrix mRNA expression. J Vasc Res. 1993 Nov-Dec;30(6):327–332. doi: 10.1159/000159014. [DOI] [PubMed] [Google Scholar]
  37. Liaw L., Schwartz S. M. Comparison of gene expression in bovine aortic endothelium in vivo versus in vitro. Differences in growth regulatory molecules. Arterioscler Thromb. 1993 Jul;13(7):985–993. doi: 10.1161/01.atv.13.7.985. [DOI] [PubMed] [Google Scholar]
  38. Lindner V., Lappi D. A., Baird A., Majack R. A., Reidy M. A. Role of basic fibroblast growth factor in vascular lesion formation. Circ Res. 1991 Jan;68(1):106–113. doi: 10.1161/01.res.68.1.106. [DOI] [PubMed] [Google Scholar]
  39. Lindner V., Majack R. A., Reidy M. A. Basic fibroblast growth factor stimulates endothelial regrowth and proliferation in denuded arteries. J Clin Invest. 1990 Jun;85(6):2004–2008. doi: 10.1172/JCI114665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lindner V., Reidy M. A. Expression of basic fibroblast growth factor and its receptor by smooth muscle cells and endothelium in injured rat arteries. An en face study. Circ Res. 1993 Sep;73(3):589–595. doi: 10.1161/01.res.73.3.589. [DOI] [PubMed] [Google Scholar]
  41. Lindner V., Reidy M. A. Proliferation of smooth muscle cells after vascular injury is inhibited by an antibody against basic fibroblast growth factor. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3739–3743. doi: 10.1073/pnas.88.9.3739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lombardi D. M., Reidy M. A., Schwartz S. M. Methodologic considerations important in the accurate quantitation of aortic smooth muscle cell replication in the normal rat. Am J Pathol. 1991 Feb;138(2):441–446. [PMC free article] [PubMed] [Google Scholar]
  43. Looker T., Berry C. L. The growth and development of the rat aorta. II. Changes in nucleic acid and scleroprotein content. J Anat. 1972 Oct;113(Pt 1):17–34. [PMC free article] [PubMed] [Google Scholar]
  44. Majesky M. W., Benditt E. P., Schwartz S. M. 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 U S A. 1988 Mar;85(5):1524–1528. doi: 10.1073/pnas.85.5.1524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Majesky M. W., Daemen M. J., Schwartz S. M. Alpha 1-adrenergic stimulation of platelet-derived growth factor A-chain gene expression in rat aorta. J Biol Chem. 1990 Jan 15;265(2):1082–1088. [PubMed] [Google Scholar]
  46. Majesky M. W., Giachelli C. M., Reidy M. A., Schwartz S. M. Rat carotid neointimal smooth muscle cells reexpress a developmentally regulated mRNA phenotype during repair of arterial injury. Circ Res. 1992 Oct;71(4):759–768. doi: 10.1161/01.res.71.4.759. [DOI] [PubMed] [Google Scholar]
  47. Majors A., Ehrhart L. A. 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 May;13(5):680–686. doi: 10.1161/01.atv.13.5.680. [DOI] [PubMed] [Google Scholar]
  48. Miano J. M., Vlasic N., Tota R. R., Stemerman M. B. Smooth muscle cell immediate-early gene and growth factor activation follows vascular injury. A putative in vivo mechanism for autocrine growth. Arterioscler Thromb. 1993 Feb;13(2):211–219. doi: 10.1161/01.atv.13.2.211. [DOI] [PubMed] [Google Scholar]
  49. Miki T., Bottaro D. P., Fleming T. P., Smith C. L., Burgess W. H., Chan A. M., Aaronson S. A. Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):246–250. doi: 10.1073/pnas.89.1.246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Moffett J., Kratz E., Florkiewicz R., Stachowiak M. K. Promoter regions involved in density-dependent regulation of basic fibroblast growth factor gene expression in human astrocytic cells. Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2470–2475. doi: 10.1073/pnas.93.6.2470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. More R. S., Brack M. J., Underwood M. J., Gershlick A. H. Growth factor persistence after vessel wall injury in a rabbit angioplasty model. Am J Cardiol. 1994 May 15;73(13):1031–1032. doi: 10.1016/0002-9149(94)90168-6. [DOI] [PubMed] [Google Scholar]
  52. More R. S., Underwood M. J., Brack M. J., de Bono D. P., Gershlick A. H. Changes in vessel wall plasminogen activator activity and smooth muscle cell proliferation and activation after arterial injury. Cardiovasc Res. 1995 Jan;29(1):22–26. [PubMed] [Google Scholar]
  53. Murphy P. R., Sato R., Sato Y., Friesen H. G. Fibroblast growth factor messenger ribonucleic acid expression in a human astrocytoma cell line: regulation by serum and cell density. Mol Endocrinol. 1988 Jul;2(7):591–598. doi: 10.1210/mend-2-7-591. [DOI] [PubMed] [Google Scholar]
  54. Nabel E. G., Yang Z. Y., Plautz G., Forough R., Zhan X., Haudenschild C. C., Maciag T., Nabel G. J. Recombinant fibroblast growth factor-1 promotes intimal hyperplasia and angiogenesis in arteries in vivo. Nature. 1993 Apr 29;362(6423):844–846. doi: 10.1038/362844a0. [DOI] [PubMed] [Google Scholar]
  55. Nguyen H. C., Steinberg B. M., LeBoutillier M., 3rd, Baumann F. G., Rifkin D. B., Grossi E. A., Galloway A. C. Suppression of neointimal lesions after vascular injury: a role for polyclonal anti-basic fibroblast growth factor antibody. Surgery. 1994 Aug;116(2):456–462. [PubMed] [Google Scholar]
  56. Olivetti G., Anversa P., Melissari M., Loud A. V. Morphometric study of early postnatal development of the thoracic aorta in the rat. Circ Res. 1980 Sep;47(3):417–424. doi: 10.1161/01.res.47.3.417. [DOI] [PubMed] [Google Scholar]
  57. Olson N. E., Chao S., Lindner V., Reidy M. A. Intimal smooth muscle cell proliferation after balloon catheter injury. The role of basic fibroblast growth factor. Am J Pathol. 1992 May;140(5):1017–1023. [PMC free article] [PubMed] [Google Scholar]
  58. Ornitz D. M., Leder P. Ligand specificity and heparin dependence of fibroblast growth factor receptors 1 and 3. J Biol Chem. 1992 Aug 15;267(23):16305–16311. [PubMed] [Google Scholar]
  59. Owens G. K., Thompson M. M. Developmental changes in isoactin expression in rat aortic smooth muscle cells in vivo. Relationship between growth and cytodifferentiation. J Biol Chem. 1986 Oct 5;261(28):13373–13380. [PubMed] [Google Scholar]
  60. Peoples G. E., Blotnick S., Takahashi K., Freeman M. R., Klagsbrun M., Eberlein T. J. 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 U S A. 1995 Jul 3;92(14):6547–6551. doi: 10.1073/pnas.92.14.6547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Powell P. P., Klagsbrun M. Regulation of basic fibroblast growth factor mRNA expression in rat C6 glioma cells. Exp Cell Res. 1993 Dec;209(2):224–230. doi: 10.1006/excr.1993.1305. [DOI] [PubMed] [Google Scholar]
  62. Powell P. P., 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 Aug;148(2):202–210. doi: 10.1002/jcp.1041480204. [DOI] [PubMed] [Google Scholar]
  63. Pu L. Q., Sniderman A. D., Brassard R., Lachapelle K. J., Graham A. M., Lisbona R., Symes J. F. Enhanced revascularization of the ischemic limb by angiogenic therapy. Circulation. 1993 Jul;88(1):208–215. doi: 10.1161/01.cir.88.1.208. [DOI] [PubMed] [Google Scholar]
  64. 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 Mar;158(3):435–443. doi: 10.1002/jcp.1041580307. [DOI] [PubMed] [Google Scholar]
  65. Ron D., Reich R., Chedid M., Lengel C., Cohen O. E., Chan A. M., Neufeld G., Miki T., Tronick S. R. 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 Mar 15;268(8):5388–5394. [PubMed] [Google Scholar]
  66. Root L. L., Shipley G. D. Human dermal fibroblasts express multiple bFGF and aFGF proteins. In Vitro Cell Dev Biol. 1991 Oct;27A(10):815–822. doi: 10.1007/BF02631248. [DOI] [PubMed] [Google Scholar]
  67. Rosenblatt S., Irikura K., Caday C. G., Finklestein S. P., Moskowitz M. A. Basic fibroblast growth factor dilates rat pial arterioles. J Cereb Blood Flow Metab. 1994 Jan;14(1):70–74. doi: 10.1038/jcbfm.1994.11. [DOI] [PubMed] [Google Scholar]
  68. Sarzani R., Brecher P., Chobanian A. V. Growth factor expression in aorta of normotensive and hypertensive rats. J Clin Invest. 1989 Apr;83(4):1404–1408. doi: 10.1172/JCI114029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Schmidt M. F., Kater S. B. Fibroblast growth factors, depolarization, and substratum interact in a combinatorial way to promote neuronal survival. Dev Biol. 1993 Jul;158(1):228–237. doi: 10.1006/dbio.1993.1181. [DOI] [PubMed] [Google Scholar]
  70. Stark K. L., McMahon J. A., McMahon A. P. 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 Oct;113(2):641–651. doi: 10.1242/dev.113.2.641. [DOI] [PubMed] [Google Scholar]
  71. Sternfeld M. D., Hendrickson J. E., Keeble W. W., Rosenbaum J. T., Robertson J. E., Pittelkow M. R., Shipley G. D. Differential expression of mRNA coding for heparin-binding growth factor type 2 in human cells. J Cell Physiol. 1988 Aug;136(2):297–304. doi: 10.1002/jcp.1041360212. [DOI] [PubMed] [Google Scholar]
  72. 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 U S A. 1991 Apr 15;88(8):3372–3376. doi: 10.1073/pnas.88.8.3372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Tanaka H., Sukhova G., Schwartz D., Libby P. Proliferating arterial smooth muscle cells after balloon injury express TNF-alpha but not interleukin-1 or basic fibroblast growth factor. Arterioscler Thromb Vasc Biol. 1996 Jan;16(1):12–18. doi: 10.1161/01.atv.16.1.12. [DOI] [PubMed] [Google Scholar]
  74. Terracio L., Rönnstrand L., Tingström 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 Nov;107(5):1947–1957. doi: 10.1083/jcb.107.5.1947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Villaschi S., Nicosia R. F. Angiogenic role of endogenous basic fibroblast growth factor released by rat aorta after injury. Am J Pathol. 1993 Jul;143(1):181–190. [PMC free article] [PubMed] [Google Scholar]
  76. Williams E. J., Furness J., Walsh F. S., Doherty P. Characterisation of the second messenger pathway underlying neurite outgrowth stimulated by FGF. Development. 1994 Jun;120(6):1685–1693. doi: 10.1242/dev.120.6.1685. [DOI] [PubMed] [Google Scholar]
  77. Winkles J. A., Gay C. G. 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 Nov;2(11):531–540. [PubMed] [Google Scholar]
  78. Wu Y. Y., Bradshaw R. A. Effect of nerve growth factor and fibroblast growth factor on PC12 cells: inhibition by orthovanadate. J Cell Biol. 1993 Apr;121(2):409–422. doi: 10.1083/jcb.121.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Xin X., Johnson A. D., 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 Oct 28;204(2):557–564. doi: 10.1006/bbrc.1994.2495. [DOI] [PubMed] [Google Scholar]
  80. Yan G., Fukabori Y., McBride G., Nikolaropolous S., McKeehan W. L. 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 Aug;13(8):4513–4522. doi: 10.1128/mcb.13.8.4513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Zeymer U., Fishbein M. C., Forrester J. S., Cercek B. Proliferating cell nuclear antigen immunohistochemistry in rat aorta after balloon denudation. Comparison with thymidine and bromodeoxyuridine labeling. Am J Pathol. 1992 Sep;141(3):685–690. [PMC free article] [PubMed] [Google Scholar]
  82. Zhao X. M., Yeoh T. K., Hiebert M., Frist W. H., Miller G. G. The expression of acidic fibroblast growth factor (heparin-binding growth factor-1) and cytokine genes in human cardiac allografts and T cells. Transplantation. 1993 Nov;56(5):1177–1182. doi: 10.1097/00007890-199311000-00025. [DOI] [PubMed] [Google Scholar]
  83. van Neck J. W., Medina J. J., Onnekink C., Schwartz S. M., Bloemers H. P. Expression of basic fibroblast growth factor and fibroblast growth factor receptor genes in cultured rat aortic smooth muscle cells. Biochim Biophys Acta. 1995 Apr 4;1261(2):210–214. doi: 10.1016/0167-4781(94)00247-z. [DOI] [PubMed] [Google Scholar]
  84. van Neck J. W., van Berkel P. H., Telleman P., Steijns L. S., Onnekink C., Bloemers H. P. Effect of ploidy on transcription levels in cultured rat aortic smooth muscle cells. FEBS Lett. 1992 Feb 3;297(1-2):189–195. doi: 10.1016/0014-5793(92)80358-n. [DOI] [PubMed] [Google Scholar]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology

RESOURCES