Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1991 Sep 1;114(5):1037–1048. doi: 10.1083/jcb.114.5.1037

NGF-induction of the metalloproteinase-transin/stromelysin in PC12 cells: involvement of multiple protein kinases

PMCID: PMC2289118  PMID: 1908468

Abstract

In previous work, we found that nerve growth factor (NGF) induced expression of the mRNA transcript encoding the metalloproteinase transin/stromelysin in PC12 cells. Transin was found, moreover, to be a "late" gene product whose expression correlated with neurites extension. In this study, various aspects of the NGF intracellular signaling pathway in PC12 cells are investigated. We show that the protein kinase inhibitor staurosporine, but not various other kinase inhibitors, specifically blocked the NGF induction of transin. Preliminary characterization of this staurosporine-sensitive kinase suggest that it does not correspond to a tyrosine kinase, nor various serine kinases, and that it is involved both at the transcriptional and posttranscriptional levels of transin gene regulation. In contrast to these effects of staurosporine, various activators of protein kinases C and A augmented the NGF induction of transin. Similar effects of these kinase inhibitors and activators were also observed with the expression of various immediate-early genes that have been proposed to mediate the transcriptional effects of NGF, including c-fos and c-jun. These data suggest, therefore, that the NGF induction of transin mRNA expression involves multiple protein kinases acting at a number of postreceptor regulatory steps in the NGF signaling pathway.

Full Text

The Full Text of this article is available as a PDF (2.2 MB).

Selected References

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

  1. Bartel D. P., Sheng M., Lau L. F., Greenberg M. E. Growth factors and membrane depolarization activate distinct programs of early response gene expression: dissociation of fos and jun induction. Genes Dev. 1989 Mar;3(3):304–313. doi: 10.1101/gad.3.3.304. [DOI] [PubMed] [Google Scholar]
  2. Bixby J. L. Protein kinase C is involved in laminin stimulation of neurite outgrowth. Neuron. 1989 Sep;3(3):287–297. doi: 10.1016/0896-6273(89)90253-5. [DOI] [PubMed] [Google Scholar]
  3. Blenis J., Erikson R. L. Regulation of protein kinase activities in PC12 pheochromocytoma cells. EMBO J. 1986 Dec 20;5(13):3441–3447. doi: 10.1002/j.1460-2075.1986.tb04667.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boonstra J., Mummery C. L., Feyen A., de Hoog W. J., van der Saag P. T., de Laat S. W. Epidermal growth factor receptor expression during morphological differentiation of pheochromocytoma cells, induced by nerve growth factor or dibutyryl cyclic AMP. J Cell Physiol. 1987 Jun;131(3):409–417. doi: 10.1002/jcp.1041310313. [DOI] [PubMed] [Google Scholar]
  5. Bottenstein J. E., Sato G. H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci U S A. 1979 Jan;76(1):514–517. doi: 10.1073/pnas.76.1.514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brady M. J., Nairn A. C., Wagner J. A., Palfrey H. C. Nerve growth factor-induced down-regulation of calmodulin-dependent protein kinase III in PC12 cells involves cyclic AMP-dependent protein kinase. J Neurochem. 1990 Mar;54(3):1034–1039. doi: 10.1111/j.1471-4159.1990.tb02354.x. [DOI] [PubMed] [Google Scholar]
  7. Chao M. V., Bothwell M. A., Ross A. H., Koprowski H., Lanahan A. A., Buck C. R., Sehgal A. Gene transfer and molecular cloning of the human NGF receptor. Science. 1986 Apr 25;232(4749):518–521. doi: 10.1126/science.3008331. [DOI] [PubMed] [Google Scholar]
  8. Christy B., Nathans D. DNA binding site of the growth factor-inducible protein Zif268. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8737–8741. doi: 10.1073/pnas.86.22.8737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cooper D. R., Watson J. E., Acevedo-Duncan M., Pollet R. J., Standaert M. L., Farese R. V. Retention of specific protein kinase C isozymes following chronic phorbol ester treatment in BC3H-1 myocytes. Biochem Biophys Res Commun. 1989 May 30;161(1):327–334. doi: 10.1016/0006-291x(89)91600-8. [DOI] [PubMed] [Google Scholar]
  10. Costello B., Meymandi A., Freeman J. A. Factors influencing GAP-43 gene expression in PC12 pheochromocytoma cells. J Neurosci. 1990 Apr;10(4):1398–1406. doi: 10.1523/JNEUROSCI.10-04-01398.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cremins J., Wagner J. A., Halegoua S. Nerve growth factor action is mediated by cyclic AMP- and Ca+2/phospholipid-dependent protein kinases. J Cell Biol. 1986 Sep;103(3):887–893. doi: 10.1083/jcb.103.3.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Curran T., Morgan J. I. Superinduction of c-fos by nerve growth factor in the presence of peripherally active benzodiazepines. Science. 1985 Sep 20;229(4719):1265–1268. doi: 10.1126/science.4035354. [DOI] [PubMed] [Google Scholar]
  13. Damon D. H., D'Amore P. A., Wagner J. A. Nerve growth factor and fibroblast growth factor regulate neurite outgrowth and gene expression in PC12 cells via both protein kinase C- and cAMP-independent mechanisms. J Cell Biol. 1990 Apr;110(4):1333–1339. doi: 10.1083/jcb.110.4.1333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Doherty P., Mann D. A., Walsh F. S. Comparison of the effects of NGF, activators of protein kinase C, and a calcium ionophore on the expression of Thy-1 and N-CAM in PC12 cell cultures. J Cell Biol. 1988 Jul;107(1):333–340. doi: 10.1083/jcb.107.1.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. End D., Tolson N., Yu M. Y., Guroff G. Effects of 12-0-Tetradecanoylphorbol-13-acetate (TPA) on rat pheochromocytoma (PC12) cells: interactions with epidermal growth factor and nerve growth factor. J Cell Physiol. 1982 May;111(2):140–148. doi: 10.1002/jcp.1041110204. [DOI] [PubMed] [Google Scholar]
  17. Federoff H. J., Grabczyk E., Fishman M. C. Dual regulation of GAP-43 gene expression by nerve growth factor and glucocorticoids. J Biol Chem. 1988 Dec 25;263(36):19290–19295. [PubMed] [Google Scholar]
  18. Fournier A., Murray A. W. Application of phorbol ester to mouse skin causes a rapid and sustained loss of protein kinase C. Nature. 1987 Dec 24;330(6150):767–769. doi: 10.1038/330767a0. [DOI] [PubMed] [Google Scholar]
  19. Gizang-Ginsberg E., Ziff E. B. Nerve growth factor regulates tyrosine hydroxylase gene transcription through a nucleoprotein complex that contains c-Fos. Genes Dev. 1990 Apr;4(4):477–491. doi: 10.1101/gad.4.4.477. [DOI] [PubMed] [Google Scholar]
  20. Glowacka D., Wagner J. A. Role of the cAMP-dependent protein kinase and protein kinase C in regulating the morphological differentiation of PC12 cells. J Neurosci Res. 1990 Apr;25(4):453–462. doi: 10.1002/jnr.490250403. [DOI] [PubMed] [Google Scholar]
  21. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Greenberg M. E., Greene L. A., Ziff E. B. Nerve growth factor and epidermal growth factor induce rapid transient changes in proto-oncogene transcription in PC12 cells. J Biol Chem. 1985 Nov 15;260(26):14101–14110. [PubMed] [Google Scholar]
  23. Greene L. A., Tischler A. S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2424–2428. doi: 10.1073/pnas.73.7.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Guroff G., Dickens G., End D. The induction of ornithine decarboxylase by nerve growth factor and epidermal growth factor in PC12 cells. J Neurochem. 1981 Aug;37(2):342–349. doi: 10.1111/j.1471-4159.1981.tb00461.x. [DOI] [PubMed] [Google Scholar]
  25. Halazonetis T. D., Georgopoulos K., Greenberg M. E., Leder P. c-Jun dimerizes with itself and with c-Fos, forming complexes of different DNA binding affinities. Cell. 1988 Dec 2;55(5):917–924. doi: 10.1016/0092-8674(88)90147-x. [DOI] [PubMed] [Google Scholar]
  26. Hall F. L., Fernyhough P., Ishii D. N., Vulliet P. R. Suppression of nerve growth factor-directed neurite outgrowth in PC12 cells by sphingosine, an inhibitor of protein kinase C. J Biol Chem. 1988 Mar 25;263(9):4460–4466. [PubMed] [Google Scholar]
  27. Hama T., Huang K. P., Guroff G. Protein kinase C as a component of a nerve growth factor-sensitive phosphorylation system in PC12 cells. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2353–2357. doi: 10.1073/pnas.83.8.2353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hashimoto S., Hagino A. Blockage of nerve growth factor action in PC12h cells by staurosporine, a potent protein kinase inhibitor. J Neurochem. 1989 Dec;53(6):1675–1685. doi: 10.1111/j.1471-4159.1989.tb09230.x. [DOI] [PubMed] [Google Scholar]
  29. Heasley L. E., Johnson G. L. Regulation of protein kinase C by nerve growth factor, epidermal growth factor, and phorbol esters in PC12 pheochromocytoma cells. J Biol Chem. 1989 May 25;264(15):8646–8652. [PubMed] [Google Scholar]
  30. Hempstead B. L., Martin-Zanca D., Kaplan D. R., Parada L. F., Chao M. V. High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature. 1991 Apr 25;350(6320):678–683. doi: 10.1038/350678a0. [DOI] [PubMed] [Google Scholar]
  31. Inagaki M., Hagiwara M., Saitoh M., Hidaka H. Protein kinase C negatively modulated by phorbol ester. FEBS Lett. 1986 Jul 7;202(2):277–281. doi: 10.1016/0014-5793(86)80701-3. [DOI] [PubMed] [Google Scholar]
  32. Kalman D., Wong B., Horvai A. E., Cline M. J., O'Lague P. H. Nerve growth factor acts through cAMP-dependent protein kinase to increase the number of sodium channels in PC12 cells. Neuron. 1990 Mar;4(3):355–366. doi: 10.1016/0896-6273(90)90048-k. [DOI] [PubMed] [Google Scholar]
  33. Kaplan D. R., Hempstead B. L., Martin-Zanca D., Chao M. V., Parada L. F. The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. Science. 1991 Apr 26;252(5005):554–558. doi: 10.1126/science.1850549. [DOI] [PubMed] [Google Scholar]
  34. Kerr L. D., Holt J. T., Matrisian L. M. Growth factors regulate transin gene expression by c-fos-dependent and c-fos-independent pathways. Science. 1988 Dec 9;242(4884):1424–1427. doi: 10.1126/science.2462278. [DOI] [PubMed] [Google Scholar]
  35. Kerr L. D., Miller D. B., Matrisian L. M. TGF-beta 1 inhibition of transin/stromelysin gene expression is mediated through a Fos binding sequence. Cell. 1990 Apr 20;61(2):267–278. doi: 10.1016/0092-8674(90)90807-q. [DOI] [PubMed] [Google Scholar]
  36. Klein R., Jing S. Q., Nanduri V., O'Rourke E., Barbacid M. The trk proto-oncogene encodes a receptor for nerve growth factor. Cell. 1991 Apr 5;65(1):189–197. doi: 10.1016/0092-8674(91)90419-y. [DOI] [PubMed] [Google Scholar]
  37. Koizumi S., Contreras M. L., Matsuda Y., Hama T., Lazarovici P., Guroff G. K-252a: a specific inhibitor of the action of nerve growth factor on PC 12 cells. J Neurosci. 1988 Feb;8(2):715–721. doi: 10.1523/JNEUROSCI.08-02-00715.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kouzarides T., Ziff E. The role of the leucine zipper in the fos-jun interaction. Nature. 1988 Dec 15;336(6200):646–651. doi: 10.1038/336646a0. [DOI] [PubMed] [Google Scholar]
  39. Kruijer W., Schubert D., Verma I. M. Induction of the proto-oncogene fos by nerve growth factor. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7330–7334. doi: 10.1073/pnas.82.21.7330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kujubu D. A., Lim R. W., Varnum B. C., Herschman H. R. Induction of transiently expressed genes in PC-12 pheochromocytoma cells. Oncogene. 1987;1(3):257–262. [PubMed] [Google Scholar]
  41. Landreth G. E., Smith D. S., McCabe C., Gittinger C. Characterization of a nerve growth factor-stimulated protein kinase in PC12 cells which phosphorylates microtubule-associated protein 2 and pp250. J Neurochem. 1990 Aug;55(2):514–523. doi: 10.1111/j.1471-4159.1990.tb04165.x. [DOI] [PubMed] [Google Scholar]
  42. Lazarovici P., Levi B. Z., Lelkes P. I., Koizumi S., Fujita K., Matsuda Y., Ozato K., Guroff G. K-252a inhibits the increase in c-fos transcription and the increase in intracellular calcium produced by nerve growth factor in PC12 cells. J Neurosci Res. 1989 May;23(1):1–8. doi: 10.1002/jnr.490230102. [DOI] [PubMed] [Google Scholar]
  43. Leonard D. G., Ziff E. B., Greene L. A. Identification and characterization of mRNAs regulated by nerve growth factor in PC12 cells. Mol Cell Biol. 1987 Sep;7(9):3156–3167. doi: 10.1128/mcb.7.9.3156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Levi-Montalcini R. The nerve growth factor 35 years later. Science. 1987 Sep 4;237(4819):1154–1162. doi: 10.1126/science.3306916. [DOI] [PubMed] [Google Scholar]
  45. Levi A., Biocca S., Cattaneo A., Calissano P. The mode of action of nerve growth factor in PC12 cells. Mol Neurobiol. 1988 Fall;2(3):201–226. doi: 10.1007/BF02935346. [DOI] [PubMed] [Google Scholar]
  46. Lindenbaum M. H., Carbonetto S., Grosveld F., Flavell D., Mushynski W. E. Transcriptional and post-transcriptional effects of nerve growth factor on expression of the three neurofilament subunits in PC-12 cells. J Biol Chem. 1988 Apr 25;263(12):5662–5667. [PubMed] [Google Scholar]
  47. Machida C. M., Muldoon L. L., Rodland K. D., Magun B. E. Transcriptional modulation of transin gene expression by epidermal growth factor and transforming growth factor beta. Mol Cell Biol. 1988 Jun;8(6):2479–2483. doi: 10.1128/mcb.8.6.2479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Machida C. M., Rodland K. D., Matrisian L., Magun B. E., Ciment G. NGF induction of the gene encoding the protease transin accompanies neuronal differentiation in PC12 cells. Neuron. 1989 Jun;2(6):1587–1596. doi: 10.1016/0896-6273(89)90047-0. [DOI] [PubMed] [Google Scholar]
  49. Mains R. E., Patterson P. H. Primary cultures of dissociated sympathetic neurons. I. Establishment of long-term growth in culture and studies of differentiated properties. J Cell Biol. 1973 Nov;59(2 Pt 1):329–345. doi: 10.1083/jcb.59.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Mann D. A., Doherty P., Walsh F. S. Increased intracellular cyclic AMP differentially modulates nerve growth factor induction of three neuronal recognition molecules involved in neurite outgrowth. J Neurochem. 1989 Nov;53(5):1581–1588. doi: 10.1111/j.1471-4159.1989.tb08555.x. [DOI] [PubMed] [Google Scholar]
  51. Matrisian L. M., Glaichenhaus N., Gesnel M. C., Breathnach R. Epidermal growth factor and oncogenes induce transcription of the same cellular mRNA in rat fibroblasts. EMBO J. 1985 Jun;4(6):1435–1440. doi: 10.1002/j.1460-2075.1985.tb03799.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Matrisian L. M., Leroy P., Ruhlmann C., Gesnel M. C., Breathnach R. Isolation of the oncogene and epidermal growth factor-induced transin gene: complex control in rat fibroblasts. Mol Cell Biol. 1986 May;6(5):1679–1686. doi: 10.1128/mcb.6.5.1679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Matrisian L. M. Metalloproteinases and their inhibitors in matrix remodeling. Trends Genet. 1990 Apr;6(4):121–125. doi: 10.1016/0168-9525(90)90126-q. [DOI] [PubMed] [Google Scholar]
  54. Matsuda Y., Nakanishi N., Dickens G., Guroff G. A nerve growth factor-sensitive S6 kinase in cell-free extracts from PC12 cells. J Neurochem. 1986 Dec;47(6):1728–1734. doi: 10.1111/j.1471-4159.1986.tb13081.x. [DOI] [PubMed] [Google Scholar]
  55. Matthies H. J., Palfrey H. C., Hirning L. D., Miller R. J. Down regulation of protein kinase C in neuronal cells: effects on neurotransmitter release. J Neurosci. 1987 Apr;7(4):1198–1206. doi: 10.1523/JNEUROSCI.07-04-01198.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. McDonnell S. E., Kerr L. D., Matrisian L. M. Epidermal growth factor stimulation of stromelysin mRNA in rat fibroblasts requires induction of proto-oncogenes c-fos and c-jun and activation of protein kinase C. Mol Cell Biol. 1990 Aug;10(8):4284–4293. doi: 10.1128/mcb.10.8.4284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Milbrandt J. A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science. 1987 Nov 6;238(4828):797–799. doi: 10.1126/science.3672127. [DOI] [PubMed] [Google Scholar]
  58. Milbrandt J. Nerve growth factor rapidly induces c-fos mRNA in PC12 rat pheochromocytoma cells. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4789–4793. doi: 10.1073/pnas.83.13.4789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Mitchell P. J., Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989 Jul 28;245(4916):371–378. doi: 10.1126/science.2667136. [DOI] [PubMed] [Google Scholar]
  60. Miyasaka T., Chao M. V., Sherline P., Saltiel A. R. Nerve growth factor stimulates a protein kinase in PC-12 cells that phosphorylates microtubule-associated protein-2. J Biol Chem. 1990 Mar 15;265(8):4730–4735. [PubMed] [Google Scholar]
  61. Pittman R. N. Release of plasminogen activator and a calcium-dependent metalloprotease from cultured sympathetic and sensory neurons. Dev Biol. 1985 Jul;110(1):91–101. doi: 10.1016/0012-1606(85)90067-3. [DOI] [PubMed] [Google Scholar]
  62. Rauscher F. J., 3rd, Voulalas P. J., Franza B. R., Jr, Curran T. Fos and Jun bind cooperatively to the AP-1 site: reconstitution in vitro. Genes Dev. 1988 Dec;2(12B):1687–1699. doi: 10.1101/gad.2.12b.1687. [DOI] [PubMed] [Google Scholar]
  63. Reinhold D. S., Neet K. E. The lack of a role for protein kinase C in neurite extension and in the induction of ornithine decarboxylase by nerve growth factor in PC12 cells. J Biol Chem. 1989 Feb 25;264(6):3538–3544. [PubMed] [Google Scholar]
  64. Rowland E. A., Müller T. H., Goldstein M., Greene L. A. Cell-free detection and characterization of a novel nerve growth factor-activated protein kinase in PC12 cells. J Biol Chem. 1987 Jun 5;262(16):7504–7513. [PubMed] [Google Scholar]
  65. Seasholtz A. F., Thompson R. C., Douglass J. O. Identification of a cyclic adenosine monophosphate-responsive element in the rat corticotropin-releasing hormone gene. Mol Endocrinol. 1988 Dec;2(12):1311–1319. doi: 10.1210/mend-2-12-1311. [DOI] [PubMed] [Google Scholar]
  66. Secrist J. P., Sehgal I., Powis G., Abraham R. T. Preferential inhibition of the platelet-derived growth factor receptor tyrosine kinase by staurosporine. J Biol Chem. 1990 Nov 25;265(33):20394–20400. [PubMed] [Google Scholar]
  67. Sheng M., Greenberg M. E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron. 1990 Apr;4(4):477–485. doi: 10.1016/0896-6273(90)90106-p. [DOI] [PubMed] [Google Scholar]
  68. Sigmund O., Naor Z., Anderson D. J., Stein R. Effect of nerve growth factor and fibroblast growth factor on SCG10 and c-fos expression and neurite outgrowth in protein kinase C-depleted PC12 cells. J Biol Chem. 1990 Feb 5;265(4):2257–2261. [PubMed] [Google Scholar]
  69. Stein R., Orit S., Anderson D. J. The induction of a neural-specific gene, SCG10, by nerve growth factor in PC12 cells is transcriptional, protein synthesis dependent, and glucocorticoid inhibitable. Dev Biol. 1988 Jun;127(2):316–325. doi: 10.1016/0012-1606(88)90318-1. [DOI] [PubMed] [Google Scholar]
  70. Swarup G., Cohen S., Garbers D. L. Inhibition of membrane phosphotyrosyl-protein phosphatase activity by vanadate. Biochem Biophys Res Commun. 1982 Aug;107(3):1104–1109. doi: 10.1016/0006-291x(82)90635-0. [DOI] [PubMed] [Google Scholar]
  71. Tamaoki T., Nomoto H., Takahashi I., Kato Y., Morimoto M., Tomita F. Staurosporine, a potent inhibitor of phospholipid/Ca++dependent protein kinase. Biochem Biophys Res Commun. 1986 Mar 13;135(2):397–402. doi: 10.1016/0006-291x(86)90008-2. [DOI] [PubMed] [Google Scholar]
  72. Tischler A. S., Ruzicka L. A., Dobner P. R. A protein kinase inhibitor, staurosporine, mimics nerve growth factor induction of neurotensin/neuromedin N gene expression. J Biol Chem. 1991 Jan 15;266(2):1141–1146. [PubMed] [Google Scholar]
  73. Tischler A. S., Ruzicka L. A., Perlman R. L. Mimicry and inhibition of nerve growth factor effects: interactions of staurosporine, forskolin, and K252a in PC12 cells and normal rat chromaffin cells in vitro. J Neurochem. 1990 Oct;55(4):1159–1165. doi: 10.1111/j.1471-4159.1990.tb03120.x. [DOI] [PubMed] [Google Scholar]
  74. Van Buskirk R., Corcoran T., Wagner J. A. Clonal variants of PC12 pheochromocytoma cells with defects in cAMP-dependent protein kinases induce ornithine decarboxylase in response to nerve growth factor but not to adenosine agonists. Mol Cell Biol. 1985 Aug;5(8):1984–1992. doi: 10.1128/mcb.5.8.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Volonté C., Rukenstein A., Loeb D. M., Greene L. A. Differential inhibition of nerve growth factor responses by purine analogues: correlation with inhibition of a nerve growth factor-activated protein kinase. J Cell Biol. 1989 Nov;109(5):2395–2403. doi: 10.1083/jcb.109.5.2395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Vyas S., Faucon Biguet N., Mallet J. Transcriptional and post-transcriptional regulation of tyrosine hydroxylase gene by protein kinase C. EMBO J. 1990 Nov;9(11):3707–3712. doi: 10.1002/j.1460-2075.1990.tb07583.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Wu B. Y., Fodor E. J., Edwards R. H., Rutter W. J. Nerve growth factor induces the proto-oncogene c-jun in PC12 cells. J Biol Chem. 1989 May 25;264(15):9000–9003. [PubMed] [Google Scholar]
  78. Yonemoto W., Filson A. J., Queral-Lustig A. E., Wang J. Y., Brugge J. S. Detection of phosphotyrosine-containing proteins in polyomavirus middle tumor antigen-transformed cells after treatment with a phosphotyrosine phosphatase inhibitor. Mol Cell Biol. 1987 Feb;7(2):905–913. doi: 10.1128/mcb.7.2.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. 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]

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

RESOURCES