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PMID: 1348250 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Concentration-dependent regulation of neuronal gene expression by nerve growth factor.

The Journal of cell biology ·Vol. 117 ·No. 1 ·1992-04-00 ·Pages 135-41

Ma Y, Campenot RB, Miller FD

Abstract

NGF is a neurotrophic protein that promotes the survival, growth, and differentiation of developing sympathetic neurons. To directly determine the effects of different concentrations of NGF on neuronal gene expression, we examined mRNAs encoding the p75 low-affinity NGF (LNGF) receptor, T alpha 1 alpha-tubulin (T alpha 1), and tyrosine hydroxylase (TH) in pure cultures of rat sympathetic neurons from postnatal day 1 superior cervical ganglia. Studies of the timecourse of gene expression during 2 wk in culture indicated that a 5-d incubation period would be optimal for the concentration-effect studies. Analysis of RNA isolated from neurons cultured in 2-200 ng/ml 2.5S NGF for 5 d revealed that, as the NGF concentration increased, neurons expressed correspondingly increased levels of all three mRNAs. Both LNGF receptor and TH mRNAs increased seven-fold, and T alpha 1 mRNA increased four-fold in neurons cultured in 200 versus 10 ng/ml NGF. In contrast, T26 alpha-tubulin mRNA, which is constitutively expressed, did not alter as a function of NGF concentration. When neurons were initially cultured in 10 ng/ml NGF for 5 d, and then 200 ng/ml NGF was added, LNGF receptor, T alpha 1, and TH mRNAs all increased within 48 h. The timecourse of induction differed: T alpha 1 mRNA was maximal by 5 h, whereas LNGF receptor and TH mRNAs first began to increase at 12 h after the NGF increase. These experiments show that NGF regulates expression of a subset of mRNAs important to neuronal growth and differentiation over a broad concentration range, suggesting that the effects of NGF may be mediated by more than just a single receptor operating at one fixed affinity. These results also suggest a mechanism for coupling neuronal synthesis of axonal proteins to increases in size of the innervated target territory during growth of the organism.

MeSH Terms
Animals Animals, Newborn Cells, Cultured Dose-Response Relationship, Drug Ganglia, Sympathetic/physiology Gene Expression Regulation/drug effects Kinetics Nerve Growth Factors/pharmacology Neurons/cytology,drug effects,physiology RNA, Messenger/genetics,metabolism Rats Receptors, Cell Surface/genetics Receptors, Nerve Growth Factor Tubulin/genetics Tyrosine 3-Monooxygenase/genetics
Chemicals
Nerve Growth Factors RNA, Messenger Receptors, Cell Surface Receptors, Nerve Growth Factor Tubulin Tyrosine 3-Monooxygenase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Ma Y
Department of Anatomy and Cell Biology, University of Alberta, Edmonton, Canada.
Campenot R B
Miller F D
References (58)
58 references, click to expand
  1. Long-term culture of dissociated sympathetic neurons.
    Methods Enzymol. 1979;58:574-84 PMID: 423793
  2. Growth of sympathetic nerve fibers in culture does not require extracellular calcium.
    Neuron. 1989 Dec;3(6):733-43 PMID: 2642016
  3. Role of nerve growth factor in the development of rat sympathetic neurons in vitro. II. Developmental studies.
    J Cell Biol. 1977 Dec;75(3):705-11 PMID: 925076
  4. Characterization and isolation of proteolytically modified nerve growth factor.
    Biochemistry. 1976 Dec 14;15(25):5543-52 PMID: 999827
  5. Regulation of nerve growth factor receptor gene expression by nerve growth factor in the developing peripheral nervous system.
    J Cell Biol. 1991 Jan;112(2):303-12 PMID: 1671048
  6. The trk proto-oncogene encodes a receptor for nerve growth factor.
    Cell. 1991 Apr 5;65(1):189-97 PMID: 1849459
  7. Molecular cloning and expression of brain-derived neurotrophic factor.
    Nature. 1989 Sep 14;341(6238):149-52 PMID: 2779653
  8. Regulation of neurotransmitter metabolic enzymes and tyrosine hydroxylase mRNA level by nerve growth factor in cultured sympathetic neurones.
    Development. 1988 Feb;102(2):361-8 PMID: 2901336
  9. PC12 cell mutants that possess low- but not high-affinity nerve growth factor receptors neither respond to nor internalize nerve growth factor.
    J Cell Biol. 1986 Mar;102(3):830-43 PMID: 3005338
  10. Gene transfer and molecular cloning of the rat nerve growth factor receptor.
    Nature. 1987 Feb 12-18;325(6105):593-7 PMID: 3027580
  11. Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system.
    Nature. 1988 Nov 10;336(6195):123-8 PMID: 3054564
  12. A histochemical study of the adrenergic innervation of the rat pineal gland: evidence for overlap of the innervation from the two superior cervical ganglia and for sprouting following unilateral denervation.
    Neuroscience. 1987 Jun;21(3):893-902 PMID: 3627441
  13. Evidence for sprouting specificity following medial septal lesions in the rat.
    J Comp Neurol. 1985 Jul 1;237(1):116-26 PMID: 4044889
  14. Analysis of the effects of the antiserum to the nerve growth factor in adult mice.
    Brain Res. 1971 Apr 2;27(2):343-55 PMID: 5552175
  15. Effects of long-term nerve growth factor deprivation on the nervous system of the adult rat: an experimental autoimmune approach.
    Brain Res. 1980 Sep 29;198(1):27-42 PMID: 6105903
  16. Regulation of tyrosine hydroxylase mRNA by glucocorticoid and cyclic AMP in a rat pheochromocytoma cell line. Isolation of a cDNA clone for tyrosine hydroxylase mRNA.
    J Biol Chem. 1983 Dec 10;258(23):14632-7 PMID: 6139379
  17. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose.
    Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201-5 PMID: 6159641
  18. Development of sympathetic neurons in compartmentalized cultures. Il Local control of neurite growth by nerve growth factor.
    Dev Biol. 1982 Sep;93(1):1-12 PMID: 7128926
  19. Somatic and behavioral postnatal effects of fetal injections of nerve growth factor antibodies in the rat.
    Nature. 1981 Jun 4;291(5814):413-5 PMID: 7242663
  20. High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor.
    Nature. 1991 Apr 25;350(6320):678-83 PMID: 1850821
  21. Nerve growth factor regulates tyrosine hydroxylase gene transcription through a nucleoprotein complex that contains c-Fos.
    Genes Dev. 1990 Apr;4(4):477-91 PMID: 1972929
  22. Increased expression of T alpha 1 alpha-tubulin mRNA during collateral and NGF-induced sprouting of sympathetic neurons.
    Dev Biol. 1990 Sep;141(1):84-92 PMID: 1975243
  23. Identification of a conserved protein motif in a group of growth factor receptors.
    FEBS Lett. 1990 Oct 15;272(1-2):7-11 PMID: 2172020
  24. Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family.
    Nature. 1990 Mar 22;344(6264):339-41 PMID: 2314473
  25. Neurotrophin-3: a neurotrophic factor related to NGF and BDNF.
    Science. 1990 Mar 23;247(4949 Pt 1):1446-51 PMID: 2321006
  26. Sympathetic sprouting into neonatally denervated contralateral target: superior cervical ganglion neuronal numbers and sizes.
    Brain Res Dev Brain Res. 1990 May 1;53(2):208-14 PMID: 2357794
  27. Expression of functional nerve growth factor receptors after gene transfer.
    Science. 1989 Jan 20;243(4889):373-5 PMID: 2536190
  28. Directed expression of NGF to pancreatic beta cells in transgenic mice leads to selective hyperinnervation of the islets.
    Cell. 1989 Jul 14;58(1):161-70 PMID: 2665941
  29. Isolation and characterization of a glycosylated form of beta nerve growth factor in mouse submandibular glands.
    J Biol Chem. 1989 Jul 25;264(21):12502-9 PMID: 2745457
  30. Compensatory changes in contralateral sympathetic neurons of the superior cervical ganglion and in their terminals in the pineal gland following unilateral ganglionectomy.
    J Neurosci. 1985 Jun;5(6):1522-6 PMID: 2861259
  31. Molecular and biochemical characterization of the human trk proto-oncogene.
    Mol Cell Biol. 1989 Jan;9(1):24-33 PMID: 2927393
  32. Molecular characteristics of nerve growth factor receptors on PC12 cells.
    J Biol Chem. 1985 Jan 10;260(1):655-62 PMID: 2981225
  33. Expression and structure of the human NGF receptor.
    Cell. 1986 Nov 21;47(4):545-54 PMID: 3022937
  34. Developmentally regulated expression of the nerve growth factor receptor gene in the periphery and brain.
    Proc Natl Acad Sci U S A. 1987 May;84(9):3060-3 PMID: 3033677
  35. Nerve growth factor enhances dendritic arborization of sympathetic ganglion cells in developing mammals.
    J Neurosci. 1988 Jul;8(7):2628-34 PMID: 3249248
  36. Evidence that endogenous beta nerve growth factor is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult rats.
    Proc Natl Acad Sci U S A. 1987 Sep;84(18):6596-600 PMID: 3306683
  37. Isotypes of alpha-tubulin are differentially regulated during neuronal maturation.
    J Cell Biol. 1987 Dec;105(6 Pt 2):3065-73 PMID: 3693406
  38. The nerve growth factor: purification as a 30,000-molecular-weight protein.
    Proc Natl Acad Sci U S A. 1969 Oct;64(2):787-94 PMID: 4982360
  39. Selective induction by nerve growth factor of tyrosine hydroxylase and dopamine- -hydroxylase in the rat superior cervical ganglia.
    Proc Natl Acad Sci U S A. 1971 Jul;68(7):1598-602 PMID: 5283951
  40. Association of 125I-nerve growth factor with PC12 pheochromocytoma cells. Evidence for internalization via high-affinity receptors only and for long-term regulation by nerve growth factor of both high- and low-affinity receptors.
    J Biol Chem. 1984 Dec 25;259(24):15509-16 PMID: 6096376
  41. Induction of tyrosine hydroxylase by nerve growth factor and by elevated K+ concentrations in cultures of dissociated sympathetic neurons.
    J Neurosci. 1982 Nov;2(11):1554-66 PMID: 6128379
  42. Nerve growth factor stimulates the development of substance P in sensory ganglia.
    Proc Natl Acad Sci U S A. 1980 Jan;77(1):649-52 PMID: 6153799
  43. Requirement of nerve growth factor for development of substance P-containing sensory neurones.
    Nature. 1980 Sep 11;287(5778):158-9 PMID: 6159533
  44. Developmental neuron death in the rat superior cervical sympathetic ganglion: cell counts and ultrastructure.
    J Neurocytol. 1983 Oct;12(5):727-38 PMID: 6644353
  45. Purification of a new neurotrophic factor from mammalian brain.
    EMBO J. 1982;1(5):549-53 PMID: 7188352
  46. Dorsal root ganglion neurons are destroyed by exposure in utero to maternal antibody to nerve growth factor.
    Science. 1980 Nov 21;210(4472):916-8 PMID: 7192014
  47. EXCESSIVE GROWTH OF THE SYMPATHETIC GANGLIA EVOKED BY A PROTEIN ISOLATED FROM MOUSE SALIVARY GLANDS.
    Proc Natl Acad Sci U S A. 1960 Mar;46(3):373-84 PMID: 16578496
  48. On the role of RNA synthesis in the selective induction of tyrosine hydroxylase by nerve growth factor.
    Brain Res. 1978 Dec 29;159(2):436-9 PMID: 31965
  49. Role of nerve growth factor in the development of rat sympathetic neurons in vitro. I. Survival, growth, and differentiation of catecholamine production.
    J Cell Biol. 1977 Dec;75(3):694-704 PMID: 925075
  50. Morphometric analysis of rat superior cervical ganglion after axotomy and nerve growth factor treatment.
    J Neurocytol. 1976 Jun;5(3):351-60 PMID: 939968
  51. Molecular investigations on the high-affinity nerve growth factor receptor.
    Neuron. 1991 Jan;6(1):153-63 PMID: 1702649
  52. The trk proto-oncogene product: a signal transducing receptor for nerve growth factor.
    Science. 1991 Apr 26;252(5005):554-8 PMID: 1850549
  53. Detection of brain-derived neurotrophic factor-like activity in fibroblasts and Schwann cells: inhibition by antibodies to NGF.
    Neuron. 1991 Aug;7(2):265-75 PMID: 1873030
  54. Binding of brain-derived neurotrophic factor to the nerve growth factor receptor.
    Neuron. 1990 Apr;4(4):487-92 PMID: 2157470
  55. Introduction of nerve growth factor (NGF) receptors into a medulloblastoma cell line results in expression of high- and low-affinity NGF receptors but not NGF-mediated differentiation.
    Proc Natl Acad Sci U S A. 1990 Nov;87(21):8496-500 PMID: 2172988
  56. Primary structure and biological activity of a novel human neurotrophic factor.
    Neuron. 1990 May;4(5):767-73 PMID: 2344409
  57. Nerve growth factor regulates sympathetic ganglion cell morphology and survival in the adult mouse.
    J Neurosci. 1990 Jul;10(7):2412-9 PMID: 2376779
  58. Identification of procollagen mRNAs transferred to diazobenzyloxymethyl paper from formaldehyde agarose gels.
    Nucleic Acids Res. 1979 Aug 10;6(11):3559-67 PMID: 573889
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1992-04-00
Pages
135-41
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2289402
Subset
IM
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