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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1989 May;86(10):3891–3895. doi: 10.1073/pnas.86.10.3891

Regulation of nerve growth factor biosynthesis by beta-adrenergic receptor activation in astrocytoma cells: a potential role of c-Fos protein.

I Mocchetti 1, M A De Bernardi 1, A M Szekely 1, H Alho 1, G Brooker 1, E Costa 1
PMCID: PMC287247  PMID: 2542953

Abstract

The chain of events that results in increased production of nerve growth factor (NGF) following beta-adrenergic receptor (BAR) stimulation has been investigated in the C6-2B rat astrocytoma cell line. Exposure of these cells to the BAR agonist isoproterenol elicits the following cascade of events: (i) increase of cAMP content; (ii) increase of c-Fos mRNA content; (iii) accumulation of c-Fos protein immunoreactivity in the nucleus; (iv) increase of NGF mRNA content. The increase in c-Fos mRNA and its translation product are early events (15 and 40 min, respectively) and precede the accumulation of NGF mRNA, which peaks at 3 hr. The increase in the two mRNAs appears interrelated because cycloheximide inhibits the accumulation of c-Fos protein and NGF mRNA elicited by isoproterenol. Moreover, the accumulation of nuclear c-Fos protein and NGF mRNA induced by BAR stimulation is reduced by 2-aminopurine, an inhibitor of c-Fos mRNA induction. These data suggest that, in C6-2B astrocytoma cells, the nuclear accumulation of c-Fos protein is required for the induction of NGF mRNA expression by BAR stimulation.

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Selected References

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  1. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barka T., Gubits R. M., van der Noen H. M. Beta-adrenergic stimulation of c-fos gene expression in the mouse submandibular gland. Mol Cell Biol. 1986 Aug;6(8):2984–2989. doi: 10.1128/mcb.6.8.2984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bohmann D., Bos T. J., Admon A., Nishimura T., Vogt P. K., Tjian R. Human proto-oncogene c-jun encodes a DNA binding protein with structural and functional properties of transcription factor AP-1. Science. 1987 Dec 4;238(4832):1386–1392. doi: 10.1126/science.2825349. [DOI] [PubMed] [Google Scholar]
  4. Bravo R., Neuberg M., Burckhardt J., Almendral J., Wallich R., Müller R. Involvement of common and cell type-specific pathways in c-fos gene control: stable induction of cAMP in macrophages. Cell. 1987 Jan 30;48(2):251–260. doi: 10.1016/0092-8674(87)90428-4. [DOI] [PubMed] [Google Scholar]
  5. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  6. Curran T., Franza B. R., Jr Fos and Jun: the AP-1 connection. Cell. 1988 Nov 4;55(3):395–397. doi: 10.1016/0092-8674(88)90024-4. [DOI] [PubMed] [Google Scholar]
  7. Curran T., MacConnell W. P., van Straaten F., Verma I. M. Structure of the FBJ murine osteosarcoma virus genome: molecular cloning of its associated helper virus and the cellular homolog of the v-fos gene from mouse and human cells. Mol Cell Biol. 1983 May;3(5):914–921. doi: 10.1128/mcb.3.5.914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Curran T., Van Beveren C., Verma I. M. Viral and cellular fos proteins are complexed with a 39,000-dalton cellular protein. Mol Cell Biol. 1985 Jan;5(1):167–172. doi: 10.1128/mcb.5.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dal Toso R., De Bernardi M. A., Brooker G., Costa E., Mocchetti I. Beta adrenergic and prostaglandin receptor activation increases nerve growth factor mRNA content in C6-2B rat astrocytoma cells. J Pharmacol Exp Ther. 1988 Sep;246(3):1190–1193. [PubMed] [Google Scholar]
  10. Dal Toso R., De Bernardi M. A., Costa E., Mocchetti I. Beta-adrenergic receptor regulation of NGF-mRNA content in rat C6-2B glioma cells. Neuropharmacology. 1987 Dec;26(12):1783–1786. doi: 10.1016/0028-3908(87)90133-x. [DOI] [PubMed] [Google Scholar]
  11. Danielson P. E., Forss-Petter S., Brow M. A., Calavetta L., Douglass J., Milner R. J., Sutcliffe J. G. p1B15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA. 1988 May;7(4):261–267. doi: 10.1089/dna.1988.7.261. [DOI] [PubMed] [Google Scholar]
  12. De Benedetti A., Baglioni C. Phosphorylation of initiation factor eIF-2 alpha, binding of mRNA to 48 S complexes, and its reutilization in initiation of protein synthesis. J Biol Chem. 1983 Dec 10;258(23):14556–14562. [PubMed] [Google Scholar]
  13. Farrell P. J., Balkow K., Hunt T., Jackson R. J., Trachsel H. Phosphorylation of initiation factor elF-2 and the control of reticulocyte protein synthesis. Cell. 1977 May;11(1):187–200. doi: 10.1016/0092-8674(77)90330-0. [DOI] [PubMed] [Google Scholar]
  14. Gilman A. G., Nirenberg M. Effect of catecholamines on the adenosine 3':5'-cyclic monophosphate concentrations of clonal satellite cells of neurons. Proc Natl Acad Sci U S A. 1971 Sep;68(9):2165–2168. doi: 10.1073/pnas.68.9.2165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Harrington C. A., Lewis E. J., Krzemien D., Chikaraishi D. M. Identification and cell type specificity of the tyrosine hydroxylase gene promoter. Nucleic Acids Res. 1987 Mar 11;15(5):2363–2384. doi: 10.1093/nar/15.5.2363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kurosawa A., Guidotti A., Costa E. Nuclear translocation of cyclic AMP-dependent protein kinase subunits during the transsynaptic activation of gene expression in rat adrenal medulla. Mol Pharmacol. 1979 Jan;15(1):115–130. [PubMed] [Google Scholar]
  17. Milner R. J., Sutcliffe J. G. Gene expression in rat brain. Nucleic Acids Res. 1983 Aug 25;11(16):5497–5520. doi: 10.1093/nar/11.16.5497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mocchetti I., Naranjo J. R., Costa E. Regulation of striatal enkephalin turnover in rats receiving antagonists of specific dopamine receptor subtypes. J Pharmacol Exp Ther. 1987 Jun;241(3):1120–1124. [PubMed] [Google Scholar]
  19. Montminy M. R., Goodman R. H., Horovitch S. J., Habener J. F. Primary structure of the gene encoding rat preprosomatostatin. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3337–3340. doi: 10.1073/pnas.81.11.3337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nickols G. A., Brooker G. Temperature sensitivity of cyclic AMP production and catecholamine-induced refractoriness in a rat astrocytoma cell line. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5520–5524. doi: 10.1073/pnas.75.11.5520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nudel U., Zakut R., Shani M., Neuman S., Levy Z., Yaffe D. The nucleotide sequence of the rat cytoplasmic beta-actin gene. Nucleic Acids Res. 1983 Mar 25;11(6):1759–1771. doi: 10.1093/nar/11.6.1759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rauscher F. J., 3rd, Cohen D. R., Curran T., Bos T. J., Vogt P. K., Bohmann D., Tjian R., Franza B. R., Jr Fos-associated protein p39 is the product of the jun proto-oncogene. Science. 1988 May 20;240(4855):1010–1016. doi: 10.1126/science.3130660. [DOI] [PubMed] [Google Scholar]
  23. Schwartz J. P., Chuang D. M., Costa E. Increase in nerve growth factor content of C6 glioma cells by the activation of a beta-adrenergic receptor. Brain Res. 1977 Dec 2;137(2):369–375. doi: 10.1016/0006-8993(77)90349-3. [DOI] [PubMed] [Google Scholar]
  24. Schwartz J. P., Costa E. Regulation of nerve growth factor content in C6 glioma cells by beta-adrenergic receptor stimulation. Naunyn Schmiedebergs Arch Pharmacol. 1977 Nov;300(2):123–129. doi: 10.1007/BF00505042. [DOI] [PubMed] [Google Scholar]
  25. Szekely A. M., Barbaccia M. L., Costa E. Activation of specific glutamate receptor subtypes increases C-fos proto-oncogene expression in primary cultures of neonatal rat cerebellar granule cells. Neuropharmacology. 1987 Dec;26(12):1779–1782. doi: 10.1016/0028-3908(87)90132-8. [DOI] [PubMed] [Google Scholar]
  26. Treisman R. Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5' element and c-fos 3' sequences. Cell. 1985 Oct;42(3):889–902. doi: 10.1016/0092-8674(85)90285-5. [DOI] [PubMed] [Google Scholar]
  27. Tsukada T., Horovitch S. J., Montminy M. R., Mandel G., Goodman R. H. Structure of the human vasoactive intestinal polypeptide gene. DNA. 1985 Aug;4(4):293–300. doi: 10.1089/dna.1985.4.293. [DOI] [PubMed] [Google Scholar]
  28. Ullrich A., Gray A., Berman C., Dull T. J. Human beta-nerve growth factor gene sequence highly homologous to that of mouse. Nature. 1983 Jun 30;303(5920):821–825. doi: 10.1038/303821a0. [DOI] [PubMed] [Google Scholar]
  29. Walsh J. Economists and inflation: which way out of the wilderness? Science. 1974 Oct 11;186(4159):122–125. doi: 10.1126/science.186.4159.122. [DOI] [PubMed] [Google Scholar]
  30. Waterman M., Murdoch G. H., Evans R. M., Rosenfeld M. G. Cyclic AMP regulation of eukaryotic gene transcription by two discrete molecular mechanisms. Science. 1985 Jul 19;229(4710):267–269. doi: 10.1126/science.2990047. [DOI] [PubMed] [Google Scholar]
  31. Zinn K., Keller A., Whittemore L. A., Maniatis T. 2-Aminopurine selectively inhibits the induction of beta-interferon, c-fos, and c-myc gene expression. Science. 1988 Apr 8;240(4849):210–213. doi: 10.1126/science.3281258. [DOI] [PubMed] [Google Scholar]

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