Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1994 Oct 1;127(1):203–223. doi: 10.1083/jcb.127.1.203

Regulation of bFGF gene expression and subcellular distribution of bFGF protein in adrenal medullary cells

PMCID: PMC2120178  PMID: 7929563

Abstract

Basic fibroblast growth factor (bFGF), a potent mitogenic/neurotrophic factor, controls the development and plasticity of many types of neural cells. In adrenal chromaffin cells, the appearance of bFGF protein coincided with the establishment of functional innervation, suggesting induction by trans-synaptic signals. In cultured bovine adrenal medullary cells Western blot analysis revealed 18-, 23-, and 24-kD bFGF isoforms in the cytosolic and nuclear fractions. Stimulation of acetylcholine nicotinic receptors or hormonal angiotensin II receptors or the direct stimulation of adenylate cyclase with forskolin or protein kinase C (PKC) with PMA increased the content of all bFGF isoforms. Increases in the levels of intracellular bFGF did not result in detectable presence of bFGF proteins in culture medium. Instead, bFGF proteins accumulated in the cytoplasm or the nucleus depending on whether PKC or cAMP pathways were activated. The long-term nuclear forskolin-induced accumulation of bFGF was prevented by cycloheximide or by antisense bFGF oligonucleotide and was also accompanied by an increase in bFGF mRNA. We used luciferase reporter plasmids containing the human bFGF promoter to show that the induction of bFGF resulted from transcriptional activation of the bFGF gene and was mediated by regulatory sequences located upstream from its transcription start site. Stimulation of bFGF gene expression by forskolin and PMA was synergistic and was mediated through different promoter regions. The results suggest that stimulation by cAMP and PKC is mediated through novel cis elements. The regulation of bFGF protein content also involves posttranscriptional mechanisms since changes in the levels of individual bFGF isoforms were different depending on whether cells were treated with carbachol or angiotensin II, forskolin, or PMA. The present study indicates that bFGF is an intracrine cytoplasmic-nuclear factor, whose expression is regulated by trans-synaptic and hormonal stimuli and which may act as a direct mediator of genomic responses to afferent stimulation.

Full Text

The Full Text of this article is available as a PDF (9.1 MB).

Selected References

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

  1. Abraham J. A., Mergia A., Whang J. L., Tumolo A., Friedman J., Hjerrild K. A., Gospodarowicz D., Fiddes J. C. Nucleotide sequence of a bovine clone encoding the angiogenic protein, basic fibroblast growth factor. Science. 1986 Aug 1;233(4763):545–548. doi: 10.1126/science.2425435. [DOI] [PubMed] [Google Scholar]
  2. Abraham J. A., Mergia A., Whang J. L., Tumolo A., Friedman J., Hjerrild K. A., Gospodarowicz D., Fiddes J. C. Nucleotide sequence of a bovine clone encoding the angiogenic protein, basic fibroblast growth factor. Science. 1986 Aug 1;233(4763):545–548. doi: 10.1126/science.2425435. [DOI] [PubMed] [Google Scholar]
  3. Abraham J. A., Whang J. L., Tumolo A., Mergia A., Friedman J., Gospodarowicz D., Fiddes J. C. Human basic fibroblast growth factor: nucleotide sequence and genomic organization. EMBO J. 1986 Oct;5(10):2523–2528. doi: 10.1002/j.1460-2075.1986.tb04530.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Acheson A. L., Naujoks K., Thoenen H. Nerve growth factor-mediated enzyme induction in primary cultures of bovine adrenal chromaffin cells: specificity and level of regulation. J Neurosci. 1984 Jul;4(7):1771–1780. doi: 10.1523/JNEUROSCI.04-07-01771.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ackerman S. L., Minden A. G., Yeung C. Y. The minimal self-sufficient element in a murine G+C-rich promoter is a large element with imperfect dyad symmetry. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11865–11869. doi: 10.1073/pnas.90.24.11865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Angel P., Imagawa M., Chiu R., Stein B., Imbra R. J., Rahmsdorf H. J., Jonat C., Herrlich P., Karin M. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell. 1987 Jun 19;49(6):729–739. doi: 10.1016/0092-8674(87)90611-8. [DOI] [PubMed] [Google Scholar]
  7. Araujo D. M., Cotman C. W. Basic FGF in astroglial, microglial, and neuronal cultures: characterization of binding sites and modulation of release by lymphokines and trophic factors. J Neurosci. 1992 May;12(5):1668–1678. doi: 10.1523/JNEUROSCI.12-05-01668.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bailey C. H., Kandel E. R. Structural changes accompanying memory storage. Annu Rev Physiol. 1993;55:397–426. doi: 10.1146/annurev.ph.55.030193.002145. [DOI] [PubMed] [Google Scholar]
  9. Baird A., Walicke P. A. Fibroblast growth factors. Br Med Bull. 1989 Apr;45(2):438–452. doi: 10.1093/oxfordjournals.bmb.a072333. [DOI] [PubMed] [Google Scholar]
  10. Bashkin P., Neufeld G., Gitay-Goren H., Vlodavsky I. Release of cell surface-associated basic fibroblast growth factor by glycosylphosphatidylinositol-specific phospholipase C. J Cell Physiol. 1992 Apr;151(1):126–137. doi: 10.1002/jcp.1041510117. [DOI] [PubMed] [Google Scholar]
  11. Blottner Dieter, Westermann Reiner, Grothe Claudia, Böhlen Peter, Unsicker Klaus. Basic Fibroblast Growth Factor in the Adrenal Gland. Eur J Neurosci. 1989 Sep;1(5):471–478. doi: 10.1111/j.1460-9568.1989.tb00353.x. [DOI] [PubMed] [Google Scholar]
  12. Boarder M. R., Plevin R., Marriott D. B. Angiotensin II potentiates prostaglandin stimulation of cyclic AMP levels in intact bovine adrenal medulla cells but not adenylate cyclase in permeabilized cells. J Biol Chem. 1988 Oct 25;263(30):15319–15324. [PubMed] [Google Scholar]
  13. Bouche G., Gas N., Prats H., Baldin V., Tauber J. P., Teissié J., Amalric F. Basic fibroblast growth factor enters the nucleolus and stimulates the transcription of ribosomal genes in ABAE cells undergoing G0----G1 transition. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6770–6774. doi: 10.1073/pnas.84.19.6770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Boyle W. J., Lampert M. A., Li A. C., Baluda M. A. Nuclear compartmentalization of the v-myb oncogene product. Mol Cell Biol. 1985 Nov;5(11):3017–3023. doi: 10.1128/mcb.5.11.3017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Brigstock D. R., Sasse J., Klagsbrun M. Subcellular distribution of basic fibroblast growth factor in human hepatoma cells. Growth Factors. 1991;4(3):189–196. doi: 10.3109/08977199109104815. [DOI] [PubMed] [Google Scholar]
  16. Couderc B., Prats H., Bayard F., Amalric F. Potential oncogenic effects of basic fibroblast growth factor requires cooperation between CUG and AUG-initiated forms. Cell Regul. 1991 Sep;2(9):709–718. doi: 10.1091/mbc.2.9.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. D'Mello S. R., Weisberg E. P., Stachowiak M. K., Turzai L. M., Gioio A. E., Kaplan B. B. Isolation and nucleotide sequence of a cDNA clone encoding bovine adrenal tyrosine hydroxylase: comparative analysis of tyrosine hydroxylase gene products. J Neurosci Res. 1988 Apr;19(4):440–449. doi: 10.1002/jnr.490190408. [DOI] [PubMed] [Google Scholar]
  18. Dreyer D., Lagrange A., Grothe C., Unsicker K. Basic fibroblast growth factor prevents ontogenetic neuron death in vivo. Neurosci Lett. 1989 Apr 24;99(1-2):35–38. doi: 10.1016/0304-3940(89)90260-7. [DOI] [PubMed] [Google Scholar]
  19. Edlund T., Walker M. D., Barr P. J., Rutter W. J. Cell-specific expression of the rat insulin gene: evidence for role of two distinct 5' flanking elements. Science. 1985 Nov 22;230(4728):912–916. doi: 10.1126/science.3904002. [DOI] [PubMed] [Google Scholar]
  20. Engele J., Bohn M. C. Effects of acidic and basic fibroblast growth factors (aFGF, bFGF) on glial precursor cell proliferation: age dependency and brain region specificity. Dev Biol. 1992 Aug;152(2):363–372. doi: 10.1016/0012-1606(92)90143-5. [DOI] [PubMed] [Google Scholar]
  21. Ernfors P., Lönnerberg P., Ayer-LeLievre C., Persson H. Developmental and regional expression of basic fibroblast growth factor mRNA in the rat central nervous system. J Neurosci Res. 1990 Sep;27(1):10–15. doi: 10.1002/jnr.490270103. [DOI] [PubMed] [Google Scholar]
  22. Feige J. J., Baird A. Basic fibroblast growth factor is a substrate for protein phosphorylation and is phosphorylated by capillary endothelial cells in culture. Proc Natl Acad Sci U S A. 1989 May;86(9):3174–3178. doi: 10.1073/pnas.86.9.3174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Florkiewicz R. Z., Baird A., Gonzalez A. M. Multiple forms of bFGF: differential nuclear and cell surface localization. Growth Factors. 1991;4(4):265–275. doi: 10.3109/08977199109043912. [DOI] [PubMed] [Google Scholar]
  24. Florkiewicz R. Z., Sommer A. Human basic fibroblast growth factor gene encodes four polypeptides: three initiate translation from non-AUG codons. Proc Natl Acad Sci U S A. 1989 Jun;86(11):3978–3981. doi: 10.1073/pnas.86.11.3978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Frödin M., Gammeltoft S. Insulin-like growth factors act synergistically with basic fibroblast growth factor and nerve growth factor to promote chromaffin cell proliferation. Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1771–1775. doi: 10.1073/pnas.91.5.1771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Goc A., Stachowiak M. K. Bovine tyrosine hydroxylase gene-promoter regions involved in basal and angiotensin II-stimulated expression in nontransformed adrenal medullary cells. J Neurochem. 1994 Mar;62(3):834–843. doi: 10.1046/j.1471-4159.1994.62030834.x. [DOI] [PubMed] [Google Scholar]
  27. Goelet P., Castellucci V. F., Schacher S., Kandel E. R. The long and the short of long-term memory--a molecular framework. 1986 Jul 31-Aug 6Nature. 322(6078):419–422. doi: 10.1038/322419a0. [DOI] [PubMed] [Google Scholar]
  28. Grothe C., Unsicker K. Immunocytochemical mapping of basic fibroblast growth factor in the developing and adult rat adrenal gland. Histochemistry. 1990;94(2):141–147. doi: 10.1007/BF02440180. [DOI] [PubMed] [Google Scholar]
  29. Grothe C., Zachmann K., Unsicker K. Basic FGF-like immunoreactivity in the developing and adult rat brainstem. J Comp Neurol. 1991 Mar 8;305(2):328–336. doi: 10.1002/cne.903050213. [DOI] [PubMed] [Google Scholar]
  30. Gualandris A., Coltrini D., Bergonzoni L., Isacchi A., Tenca S., Ginelli B., Presta M. The NH2-terminal extension of high molecular weight forms of basic fibroblast growth factor (bFGF) is not essential for the binding of bFGF to nuclear chromatin in transfected NIH 3T3 cells. Growth Factors. 1993;8(1):49–60. doi: 10.3109/08977199309029134. [DOI] [PubMed] [Google Scholar]
  31. Guidotti A., Costa E. A role for nicotinic receptors in the regulation of the adenylate cyclase of adrenal medulla. J Pharmacol Exp Ther. 1974 Jun;189(3):665–675. [PubMed] [Google Scholar]
  32. Gurney M. E., Yamamoto H., Kwon Y. Induction of motor neuron sprouting in vivo by ciliary neurotrophic factor and basic fibroblast growth factor. J Neurosci. 1992 Aug;12(8):3241–3247. doi: 10.1523/JNEUROSCI.12-08-03241.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hatten M. E., Lynch M., Rydel R. E., Sanchez J., Joseph-Silverstein J., Moscatelli D., Rifkin D. B. In vitro neurite extension by granule neurons is dependent upon astroglial-derived fibroblast growth factor. Dev Biol. 1988 Feb;125(2):280–289. doi: 10.1016/0012-1606(88)90211-4. [DOI] [PubMed] [Google Scholar]
  34. Hayek A., Culler F. L., Beattie G. M., Lopez A. D., Cuevas P., Baird A. An in vivo model for study of the angiogenic effects of basic fibroblast growth factor. Biochem Biophys Res Commun. 1987 Sep 15;147(2):876–880. doi: 10.1016/0006-291x(87)91011-4. [DOI] [PubMed] [Google Scholar]
  35. Huang Z. M., Thewke D., Gong Q. Q., Schlichter D., Wicks W. D. Functional recognition of the neuronal tyrosine hydroxylase cAMP regulatory element in different cell types. Brain Res Mol Brain Res. 1991 Oct;11(3-4):309–319. doi: 10.1016/0169-328x(91)90040-5. [DOI] [PubMed] [Google Scholar]
  36. Itoh H., Mukoyama M., Pratt R. E., Gibbons G. H., Dzau V. J. Multiple autocrine growth factors modulate vascular smooth muscle cell growth response to angiotensin II. J Clin Invest. 1993 May;91(5):2268–2274. doi: 10.1172/JCI116454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Johnson P. F., McKnight S. L. Eukaryotic transcriptional regulatory proteins. Annu Rev Biochem. 1989;58:799–839. doi: 10.1146/annurev.bi.58.070189.004055. [DOI] [PubMed] [Google Scholar]
  38. Keller J. M., Alwine J. C. Activation of the SV40 late promoter: direct effects of T antigen in the absence of viral DNA replication. Cell. 1984 Feb;36(2):381–389. doi: 10.1016/0092-8674(84)90231-9. [DOI] [PubMed] [Google Scholar]
  39. Kelner K. L., Pollard H. B. Glucocorticoid receptors and regulation of phenylethanolamine-N-methyltransferase activity in cultured chromaffin cells. J Neurosci. 1985 Aug;5(8):2161–2168. doi: 10.1523/JNEUROSCI.05-08-02161.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kniss D. A., Burry R. W. Serum and fibroblast growth factor stimulate quiescent astrocytes to re-enter the cell cycle. Brain Res. 1988 Jan 26;439(1-2):281–288. doi: 10.1016/0006-8993(88)91485-0. [DOI] [PubMed] [Google Scholar]
  41. Kurokawa T., Sasada R., Iwane M., Igarashi K. Cloning and expression of cDNA encoding human basic fibroblast growth factor. FEBS Lett. 1987 Mar 9;213(1):189–194. doi: 10.1016/0014-5793(87)81489-8. [DOI] [PubMed] [Google Scholar]
  42. Leonard S., Luthman D., Logel J., Luthman J., Antle C., Freedman R., Hoffer B. Acidic and basic fibroblast growth factor mRNAs are increased in striatum following MPTP-induced dopamine neurofiber lesion: assay by quantitative PCR. Brain Res Mol Brain Res. 1993 Jun;18(4):275–284. doi: 10.1016/0169-328x(93)90090-c. [DOI] [PubMed] [Google Scholar]
  43. Livett B. G., Boksa P., Dean D. M., Mizobe F., Lindenbaum M. H. Use of isolated chromaffin cells to study basic release mechanisms. J Auton Nerv Syst. 1983 Jan;7(1):59–86. doi: 10.1016/0165-1838(83)90069-3. [DOI] [PubMed] [Google Scholar]
  44. Lukas R. J., Bencherif M. Heterogeneity and regulation of nicotinic acetylcholine receptors. Int Rev Neurobiol. 1992;34:25–131. doi: 10.1016/s0074-7742(08)60097-5. [DOI] [PubMed] [Google Scholar]
  45. Maisonpierre P. C., Le Beau M. M., Espinosa R., 3rd, Ip N. Y., Belluscio L., de la Monte S. M., Squinto S., Furth M. E., Yancopoulos G. D. Human and rat brain-derived neurotrophic factor and neurotrophin-3: gene structures, distributions, and chromosomal localizations. Genomics. 1991 Jul;10(3):558–568. doi: 10.1016/0888-7543(91)90436-i. [DOI] [PubMed] [Google Scholar]
  46. Malvaldi G., Viola-Magni M. P. DNA turnover in adrenal medullary cells of different strains of rats and its enhancement after intermittent exposure to cold. Cell Tissue Kinet. 1972 Mar;5(2):103–113. doi: 10.1111/j.1365-2184.1972.tb01007.x. [DOI] [PubMed] [Google Scholar]
  47. Matsuda S., Desaki J., Okumura N., Shiosaka S., Imaoka S., Sakanaka M. Basic fibroblast growth factor-like immunoreactivity in the trigeminal proprioceptive and motor systems. Brain Res. 1992 Apr 10;577(1):92–100. doi: 10.1016/0006-8993(92)90541-g. [DOI] [PubMed] [Google Scholar]
  48. Mayer E., Dunnett S. B., Fawcett J. W. Mitogenic effect of basic fibroblast growth factor on embryonic ventral mesencephalic dopaminergic neurone precursors. Brain Res Dev Brain Res. 1993 Apr 16;72(2):253–258. doi: 10.1016/0165-3806(93)90190-l. [DOI] [PubMed] [Google Scholar]
  49. Mignatti P., Morimoto T., Rifkin D. B. Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J Cell Physiol. 1992 Apr;151(1):81–93. doi: 10.1002/jcp.1041510113. [DOI] [PubMed] [Google Scholar]
  50. Mizuuchi K., Mizuuchi M., Gellert M. Cruciform structures in palindromic DNA are favored by DNA supercoiling. J Mol Biol. 1982 Apr 5;156(2):229–243. doi: 10.1016/0022-2836(82)90325-4. [DOI] [PubMed] [Google Scholar]
  51. Morrison R. S. Suppression of basic fibroblast growth factor expression by antisense oligodeoxynucleotides inhibits the growth of transformed human astrocytes. J Biol Chem. 1991 Jan 15;266(2):728–734. [PubMed] [Google Scholar]
  52. Moscatelli D. Metabolism of receptor-bound and matrix-bound basic fibroblast growth factor by bovine capillary endothelial cells. J Cell Biol. 1988 Aug;107(2):753–759. doi: 10.1083/jcb.107.2.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Nakanishi Y., Kihara K., Mizuno K., Masamune Y., Yoshitake Y., Nishikawa K. Direct effect of basic fibroblast growth factor on gene transcription in a cell-free system. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5216–5220. doi: 10.1073/pnas.89.12.5216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Nozaki K., Finklestein S. P., Beal M. F. Basic fibroblast growth factor protects against hypoxia-ischemia and NMDA neurotoxicity in neonatal rats. J Cereb Blood Flow Metab. 1993 Mar;13(2):221–228. doi: 10.1038/jcbfm.1993.27. [DOI] [PubMed] [Google Scholar]
  55. Otto D., Unsicker K. Basic FGF reverses chemical and morphological deficits in the nigrostriatal system of MPTP-treated mice. J Neurosci. 1990 Jun;10(6):1912–1921. doi: 10.1523/JNEUROSCI.10-06-01912.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Peng H. B., Baker L. P., Chen Q. Induction of synaptic development in cultured muscle cells by basic fibroblast growth factor. Neuron. 1991 Feb;6(2):237–246. doi: 10.1016/0896-6273(91)90359-8. [DOI] [PubMed] [Google Scholar]
  57. 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]
  58. Prats H., Kaghad M., Prats A. C., Klagsbrun M., Lélias J. M., Liauzun P., Chalon P., Tauber J. P., Amalric F., Smith J. A. High molecular mass forms of basic fibroblast growth factor are initiated by alternative CUG codons. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1836–1840. doi: 10.1073/pnas.86.6.1836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Presta M., Rifkin D. B. Immunoreactive basic fibroblast growth factor-like proteins in chromaffin granules. J Neurochem. 1991 Mar;56(3):1087–1088. doi: 10.1111/j.1471-4159.1991.tb02034.x. [DOI] [PubMed] [Google Scholar]
  60. Puchacz E., Stachowiak E. K., Florkiewicz R. Z., Lukas R. J., Stachowiak M. K. Basic fibroblast growth factor (bFGF) regulates tyrosine hydroxylase and proenkephalin mRNA levels in adrenal chromaffin cells. Brain Res. 1993 Apr 30;610(1):39–52. doi: 10.1016/0006-8993(93)91214-d. [DOI] [PubMed] [Google Scholar]
  61. Quarto N., Talarico D., Florkiewicz R., Rifkin D. B. Selective expression of high molecular weight basic fibroblast growth factor confers a unique phenotype to NIH 3T3 cells. Cell Regul. 1991 Sep;2(9):699–708. doi: 10.1091/mbc.2.9.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Riva M. A., Gale K., Mocchetti I. Basic fibroblast growth factor mRNA increases in specific brain regions following convulsive seizures. Brain Res Mol Brain Res. 1992 Oct;15(3-4):311–318. doi: 10.1016/0169-328x(92)90123-s. [DOI] [PubMed] [Google Scholar]
  63. Rydel R. E., Greene L. A. Acidic and basic fibroblast growth factors promote stable neurite outgrowth and neuronal differentiation in cultures of PC12 cells. J Neurosci. 1987 Nov;7(11):3639–3653. doi: 10.1523/JNEUROSCI.07-11-03639.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Sato Y., Rifkin D. B. Autocrine activities of basic fibroblast growth factor: regulation of endothelial cell movement, plasminogen activator synthesis, and DNA synthesis. J Cell Biol. 1988 Sep;107(3):1199–1205. doi: 10.1083/jcb.107.3.1199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Schechter J. E. Is cellular disruption the mechanism of release of basic fibroblast growth factor from anterior pituitary gonadotropes? Tissue Cell. 1992;24(6):791–802. doi: 10.1016/0040-8166(92)90015-y. [DOI] [PubMed] [Google Scholar]
  66. Schweigerer L., Neufeld G., Mergia A., Abraham J. A., Fiddes J. C., Gospodarowicz D. Basic fibroblast growth factor in human rhabdomyosarcoma cells: implications for the proliferation and neovascularization of myoblast-derived tumors. Proc Natl Acad Sci U S A. 1987 Feb;84(3):842–846. doi: 10.1073/pnas.84.3.842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Shibata F., Baird A., Florkiewicz R. Z. Functional characterization of the human basic fibroblast growth factor gene promoter. Growth Factors. 1991;4(4):277–287. doi: 10.3109/08977199109043913. [DOI] [PubMed] [Google Scholar]
  68. Sonnenberg J. L., Rauscher F. J., 3rd, Morgan J. I., Curran T. Regulation of proenkephalin by Fos and Jun. Science. 1989 Dec 22;246(4937):1622–1625. doi: 10.1126/science.2512642. [DOI] [PubMed] [Google Scholar]
  69. Stachowiak M. K., Goc A., Hong J. S., Poisner A., Jiang H. K., Stachowiak E. K. Regulation of tyrosine hydroxylase gene expression in depolarized non-transformed bovine adrenal medullary cells: second messenger systems and promoter mechanisms. Brain Res Mol Brain Res. 1994 Mar;22(1-4):309–319. doi: 10.1016/0169-328x(94)90059-0. [DOI] [PubMed] [Google Scholar]
  70. Stachowiak M. K., Hong J. S., Viveros O. H. Coordinate and differential regulation of phenylethanolamine N-methyltransferase, tyrosine hydroxylase and proenkephalin mRNAs by neural and hormonal mechanisms in cultured bovine adrenal medullary cells. Brain Res. 1990 Mar 5;510(2):277–288. doi: 10.1016/0006-8993(90)91378-t. [DOI] [PubMed] [Google Scholar]
  71. Stachowiak M. K., Jiang H. K., Poisner A. M., Tuominen R. K., Hong J. S. Short and long term regulation of catecholamine biosynthetic enzymes by angiotensin in cultured adrenal medullary cells. Molecular mechanisms and nature of second messenger systems. J Biol Chem. 1990 Mar 15;265(8):4694–4702. [PubMed] [Google Scholar]
  72. Stachowiak M. K., Sar M., Tuominen R. K., Jiang H. K., An S., Iadarola M. J., Poisner A. M., Hong J. S. Stimulation of adrenal medullary cells in vivo and in vitro induces expression of c-fos proto-oncogene. Oncogene. 1990 Jan;5(1):69–73. [PubMed] [Google Scholar]
  73. Stemple D. L., Mahanthappa N. K., Anderson D. J. Basic FGF induces neuronal differentiation, cell division, and NGF dependence in chromaffin cells: a sequence of events in sympathetic development. Neuron. 1988 Aug;1(6):517–525. doi: 10.1016/0896-6273(88)90182-1. [DOI] [PubMed] [Google Scholar]
  74. Sumners C., Myers L. M., Kalberg C. J., Raizada M. K. Physiological and pharmacological comparisons of angiotensin II receptors in neuronal and astrocyte glial cultures. Prog Neurobiol. 1990;34(5):355–385. doi: 10.1016/0301-0082(90)90032-c. [DOI] [PubMed] [Google Scholar]
  75. Tischler A. S., DeLellis R. A., Nunnemacher G., Wolfe H. J. Acute stimulation of chromaffin cell proliferation in the adult rat adrenal medulla. Lab Invest. 1988 Jun;58(6):733–735. [PubMed] [Google Scholar]
  76. Tischler A. S., Riseberg J. C., Hardenbrook M. A., Cherington V. Nerve growth factor is a potent inducer of proliferation and neuronal differentiation for adult rat chromaffin cells in vitro. J Neurosci. 1993 Apr;13(4):1533–1542. doi: 10.1523/JNEUROSCI.13-04-01533.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Tuominen R. K., McMillian M. K., Ye H., Stachowiak M. K., Hudson P. M., Hong J. S. Long-term activation of protein kinase C by nicotine in bovine adrenal chromaffin cells. J Neurochem. 1992 May;58(5):1652–1658. doi: 10.1111/j.1471-4159.1992.tb10037.x. [DOI] [PubMed] [Google Scholar]
  78. Vescovi A. L., Reynolds B. A., Fraser D. D., Weiss S. bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron. 1993 Nov;11(5):951–966. doi: 10.1016/0896-6273(93)90124-a. [DOI] [PubMed] [Google Scholar]
  79. Vlodavsky I., Bar-Shavit R., Ishai-Michaeli R., Bashkin P., Fuks Z. Extracellular sequestration and release of fibroblast growth factor: a regulatory mechanism? Trends Biochem Sci. 1991 Jul;16(7):268–271. doi: 10.1016/0968-0004(91)90102-2. [DOI] [PubMed] [Google Scholar]
  80. Wagner J. A. The fibroblast growth factors: an emerging family of neural growth factors. Curr Top Microbiol Immunol. 1991;165:95–118. doi: 10.1007/978-3-642-75747-1_6. [DOI] [PubMed] [Google Scholar]
  81. Walton K. M., Rehfuss R. P. Molecular mechanisms of cAMP-regulated gene expression. Mol Neurobiol. 1990 Fall-Winter;4(3-4):197–210. doi: 10.1007/BF02780341. [DOI] [PubMed] [Google Scholar]
  82. Weich H. A., Iberg N., Klagsbrun M., Folkman J. Transcriptional regulation of basic fibroblast growth factor gene expression in capillary endothelial cells. J Cell Biochem. 1991 Oct;47(2):158–164. doi: 10.1002/jcb.240470209. [DOI] [PubMed] [Google Scholar]
  83. Westermann R., Johannsen M., Unsicker K., Grothe C. Basic fibroblast growth factor (bFGF) immunoreactivity is present in chromaffin granules. J Neurochem. 1990 Jul;55(1):285–292. doi: 10.1111/j.1471-4159.1990.tb08850.x. [DOI] [PubMed] [Google Scholar]
  84. Whiteside S. T., Goodbourn S. Signal transduction and nuclear targeting: regulation of transcription factor activity by subcellular localisation. J Cell Sci. 1993 Apr;104(Pt 4):949–955. doi: 10.1242/jcs.104.4.949. [DOI] [PubMed] [Google Scholar]
  85. Woodward W. R., Nishi R., Meshul C. K., Williams T. E., Coulombe M., Eckenstein F. P. Nuclear and cytoplasmic localization of basic fibroblast growth factor in astrocytes and CA2 hippocampal neurons. J Neurosci. 1992 Jan;12(1):142–152. doi: 10.1523/JNEUROSCI.12-01-00142.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Yamamori T. Molecular mechanisms for generation of neural diversity and specificity: roles of polypeptide factors in development of postmitotic neurons. Neurosci Res. 1992 Jan;12(5):545–582. doi: 10.1016/0168-0102(92)90064-j. [DOI] [PubMed] [Google Scholar]
  87. Yu Z. X., Biro S., Fu Y. M., Sanchez J., Smale G., Sasse J., Ferrans V. J., Casscells W. Localization of basic fibroblast growth factor in bovine endothelial cells: immunohistochemical and biochemical studies. Exp Cell Res. 1993 Feb;204(2):247–259. doi: 10.1006/excr.1993.1031. [DOI] [PubMed] [Google Scholar]
  88. Zúiga Mejía Borja A., Meijers C., Zeller R. Expression of alternatively spliced bFGF first coding exons and antisense mRNAs during chicken embryogenesis. Dev Biol. 1993 May;157(1):110–118. doi: 10.1006/dbio.1993.1116. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES