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PMID: 8394370 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Neuronal growth factor regulation of two different sodium channel types through distinct signal transduction pathways.

The Journal of cell biology ·Vol. 122 ·No. 4 ·1993-08-00 ·Pages 915-21

D'Arcangelo G, Paradiso K, Shepherd D, Brehm P, Halegoua S, Mandel G

Abstract

Neuronal growth factors regulate the expression of voltage-activated sodium current in differentiating sympathetic neurons and PC12 cells. We show that, in PC12 cells, the NGF- and FGF-induced sodium current results from increased expression of two distinct sodium channel types. Sodium current results from the rapid induction of a novel sodium channel transcript, also found in peripheral neurons, and from the long term induction of brain type II/IIA mRNA. Expression of the type II/IIA sodium channel requires activation of the cyclic AMP-dependent protein kinase (A-kinase), whereas induction of the peripheral neuron type sodium channel occurs through an A-kinase-independent signal transduction pathway. These findings suggest that the two sodium channel types act in concert to ensure the generation of action potentials during neuronal differentiation.

MeSH Terms
Animals Cyclic AMP/physiology Fibroblast Growth Factors/pharmacology Gene Expression In Vitro Techniques Membrane Potentials Nerve Growth Factors/physiology PC12 Cells Protein Kinases/metabolism RNA, Messenger/genetics Rats Signal Transduction Sodium/physiology Sodium Channels/physiology Time Factors Transcription, Genetic
Chemicals
Nerve Growth Factors RNA, Messenger Sodium Channels Fibroblast Growth Factors Sodium Cyclic AMP Protein Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
D'Arcangelo G
Department of Neurobiology and Behavior, State University of New York, Stony Brook 11794-5230.
Paradiso K
Shepherd D
Brehm P
Halegoua S
Mandel G
References (46)
46 references, click to expand
  1. Characterization and isolation of proteolytically modified nerve growth factor.
    Biochemistry. 1976 Dec 14;15(25):5543-52 PMID: 999827
  2. The cytoplasmic raf oncogene induces a neuronal phenotype in PC12 cells: a potential role for cellular raf kinases in neuronal growth factor signal transduction.
    Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5016-20 PMID: 8389463
  3. 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):2424-8 PMID: 1065897
  4. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.
    Biochemistry. 1979 Nov 27;18(24):5294-9 PMID: 518835
  5. Physiological and morphological studies of rat pheochromocytoma cells (PC12) chemically fused and grown in culture.
    Proc Natl Acad Sci U S A. 1980 Mar;77(3):1701-5 PMID: 6929516
  6. Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter.
    J Mol Appl Genet. 1982;1(4):327-41 PMID: 6286831
  7. A method for isolation of intact, translationally active ribonucleic acid.
    DNA. 1983;2(4):329-35 PMID: 6198133
  8. Patch-clamp study of the tetrodotoxin-resistant sodium current in group C sensory neurones.
    Neurosci Lett. 1984 Oct 12;51(2):241-6 PMID: 6096775
  9. Antigenic differences among the voltage-sensitive sodium channels in the peripheral and central nervous systems and skeletal muscle.
    Brain Res. 1985 Apr 1;331(1):145-9 PMID: 2580596
  10. Nerve growth factor and other agents mediate phosphorylation and activation of tyrosine hydroxylase. A convergence of multiple kinase activities.
    J Biol Chem. 1985 Jul 25;260(15):9047-56 PMID: 2862143
  11. A threshold sodium current in pyramidal cells in rat hippocampus.
    Neurosci Lett. 1985 May 23;56(3):289-93 PMID: 2410817
  12. Existence of distinct sodium channel messenger RNAs in rat brain.
    Nature. 1986 Mar 13-19;320(6058):188-92 PMID: 3754035
  13. Nerve growth factor action is mediated by cyclic AMP- and Ca+2/phospholipid-dependent protein kinases.
    J Cell Biol. 1986 Sep;103(3):887-93 PMID: 2875079
  14. 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):1984-92 PMID: 3018542
  15. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene.
    Proc Natl Acad Sci U S A. 1986 Sep;83(18):6682-6 PMID: 2875459
  16. Nerve growth factor increases the number of functional Na channels and induces TTX-resistant Na channels in PC12 pheochromocytoma cells.
    J Neurosci. 1987 Jun;7(6):1613-25 PMID: 2439661
  17. Sodium currents in dissociated bull-frog sympathetic neurones.
    J Physiol. 1987 Aug;389:605-27 PMID: 2445980
  18. Tissue-specific expression of the RI and RII sodium channel subtypes.
    Proc Natl Acad Sci U S A. 1987 Dec;84(23):8682-6 PMID: 2446328
  19. Modulation of sodium-channel mRNA levels in rat skeletal muscle.
    Proc Natl Acad Sci U S A. 1987 Dec;84(23):8721-5 PMID: 2446331
  20. Selective induction of brain type II Na+ channels by nerve growth factor.
    Proc Natl Acad Sci U S A. 1988 Feb;85(3):924-8 PMID: 2448784
  21. Dissociation of c-fos from ODC expression and neuronal differentiation in a PC12 subline stably transfected with an inducible N-ras oncogene.
    Biochem Biophys Res Commun. 1988 Feb 15;150(3):1185-92 PMID: 3277634
  22. Functional expression of cloned cDNA encoding sodium channel III.
    FEBS Lett. 1988 Feb 8;228(1):195-200 PMID: 2449364
  23. p1B15: a cDNA clone of the rat mRNA encoding cyclophilin.
    DNA. 1988 May;7(4):261-7 PMID: 3293952
  24. A protein kinase inhibitor gene reduces both basal and multihormone-stimulated prolactin gene transcription.
    J Biol Chem. 1989 Jan 5;264(1):431-6 PMID: 2535842
  25. Properties of appropriately and inappropriately expressed sodium channels in squid giant axon and its somata.
    J Neurosci. 1989 Apr;9(4):1362-74 PMID: 2539444
  26. Molecular cloning of a putative tetrodotoxin-resistant rat heart Na+ channel isoform.
    Proc Natl Acad Sci U S A. 1989 Oct;86(20):8170-4 PMID: 2554302
  27. Differential regulation of three sodium channel messenger RNAs in the rat central nervous system during development.
    EMBO J. 1989 Dec 1;8(12):3611-6 PMID: 2555170
  28. Regulation of sodium currents and acetylcholine responses in PC12 cells.
    Brain Res. 1990 Jan 8;506(2):243-8 PMID: 2302564
  29. Neuron-specific expression of the rat brain type II sodium channel gene is directed by upstream regulatory elements.
    Neuron. 1990 Feb;4(2):223-31 PMID: 2155009
  30. Primary structure and expression of a sodium channel characteristic of denervated and immature rat skeletal muscle.
    Neuron. 1990 Feb;4(2):233-42 PMID: 2155010
  31. Nerve growth factor acts through cAMP-dependent protein kinase to increase the number of sodium channels in PC12 cells.
    Neuron. 1990 Mar;4(3):355-66 PMID: 1690563
  32. Phosphorylation of tyrosine hydroxylase in situ at serine 8, 19, 31, and 40.
    J Biol Chem. 1990 Jul 15;265(20):11682-91 PMID: 1973163
  33. Differential effects of NGF, FGF, EGF, cAMP, and dexamethasone on neurite outgrowth and sodium channel expression in PC12 cells.
    J Neurosci. 1990 Aug;10(8):2626-37 PMID: 2167354
  34. Effect of a dominant inhibitory Ha-ras mutation on neuronal differentiation of PC12 cells.
    Mol Cell Biol. 1990 Oct;10(10):5324-32 PMID: 2118994
  35. Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons.
    Neuron. 1989 Dec;3(6):695-704 PMID: 2561976
  36. Regulation of muscle sodium channel transcripts during development and in response to denervation.
    Dev Biol. 1990 Dec;142(2):360-7 PMID: 2175278
  37. Induction of neurite outgrowth by v-src mimics critical aspects of nerve growth factor-induced differentiation.
    Mol Cell Biol. 1991 Sep;11(9):4739-50 PMID: 1875950
  38. Developmentally regulated alternative RNA splicing of rat brain sodium channel mRNAs.
    Nucleic Acids Res. 1991 Oct 25;19(20):5673-9 PMID: 1658739
  39. Brain and heart sodium channel subtype mRNA expression in rat cerebral cortex.
    Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9453-7 PMID: 1658783
  40. The activity of cAMP-dependent protein kinase is required at a posttranslational level for induction of voltage-dependent sodium channels by peptide growth factors in PC12 cells.
    J Cell Biol. 1992 Mar;116(6):1465-73 PMID: 1311713
  41. Alternatively spliced sodium channel transcripts in brain and muscle.
    J Neurosci. 1992 Apr;12(4):1370-81 PMID: 1313493
  42. Tissue-specific expression of the voltage-sensitive sodium channel.
    J Membr Biol. 1992 Feb;125(3):193-205 PMID: 1313507
  43. The glial voltage-gated sodium channel: cell- and tissue-specific mRNA expression.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7272-6 PMID: 1379737
  44. Large and small vertebrate sensory neurons express different Na and K channel subtypes.
    Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9569-73 PMID: 1329102
  45. A branched signaling pathway for nerve growth factor is revealed by Src-, Ras-, and Raf-mediated gene inductions.
    Mol Cell Biol. 1993 Jun;13(6):3146-55 PMID: 8497245
  46. Nerve growth factor-induced increase in electrical excitability and acetylcholine sensitivity of a rat pheochromocytoma cell line.
    Nature. 1977 Aug 11;268(5620):501-4 PMID: 329148
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1993-08-00
Pages
915-21
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2119579
Subset
IM
Grants
NINDS NIH HHS · NS 18218 · United States
NINDS NIH HHS · NS 22518 · United States
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