Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1991 Jan 2;112(2):303–312. doi: 10.1083/jcb.112.2.303

Regulation of nerve growth factor receptor gene expression by nerve growth factor in the developing peripheral nervous system

PMCID: PMC2288812  PMID: 1671048

Abstract

Nerve growth factor (NGF) is a target-derived neurotrophic protein that promotes the survival and growth of developing sympathetic and sensory neurons. We have examined NGF receptor gene expression in these neurons after NGF administration. Northern blot and in situ hybridization analyses demonstrated that NGF given systemically to neonatal rats increased levels of NGF receptor mRNA in sympathetic neurons within the superior cervical ganglion. This increase was accompanied by a differential regulation of genes associated with neurotransmitter phenotype; tyrosine hydroxylase mRNA was increased, but neuropeptide Y mRNA was not. NGF receptor mRNA levels were also increased in L4-L5 dorsal root ganglia, although this mRNA was not expressed uniformly in sensory neurons of control or NGF-treated animals. Levels of T alpha 1 alpha-tubulin mRNA, a marker of neuronal growth, also increased. In contrast to developing neurons, systemic NGF did not increase NGF receptor mRNA in nonneuronal cells of the sciatic nerve. To determine if NGF regulated NGF receptor gene expression at the transcriptional level, we examined PC12 cells. NGF treatment for 6 h increased NGF receptor mRNA fourfold; this increase was inhibited by cycloheximide. Nuclear run-off transcription assays demonstrated that the increase in steady-state NGF receptor mRNA levels was mediated at the transcriptional level. In contrast, although NGF treatment increased steady-state tyrosine hydroxylase mRNA levels, this effect was not blocked by cycloheximide, and was not due to increased transcription. These data raise the possibility that transcriptional regulation of NGF receptor gene expression by target-derived NGF could be a molecular mechanism for potentiating NGF's effects on neurons during developmental periods of neuronal competition and cell death.

Full Text

The Full Text of this article is available as a PDF (2.5 MB).

Selected References

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

  1. 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]
  2. Allen J., Novotný J., Martin J., Heinrich G. Molecular structure of mammalian neuropeptide Y: analysis by molecular cloning and computer-aided comparison with crystal structure of avian homologue. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2532–2536. doi: 10.1073/pnas.84.8.2532. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aloe L., Cozzari C., Calissano P., Levi-Montalcini R. Somatic and behavioral postnatal effects of fetal injections of nerve growth factor antibodies in the rat. Nature. 1981 Jun 4;291(5814):413–415. doi: 10.1038/291413a0. [DOI] [PubMed] [Google Scholar]
  4. Aloe L., Mugnaini E., Levi-Montalcini R. Light and electron microscopic studies on the excessive growth of sympathetic ganglia in rats injected daily from birth with 6-OHDA and NGF. Arch Ital Biol. 1975 Dec;113(4):326–353. [PubMed] [Google Scholar]
  5. Angeletti P. U., Levi-Montalcini R., Caramia F. Analysis of the effects of the antiserum to the nerve growth factor in adult mice. Brain Res. 1971 Apr 2;27(2):343–355. doi: 10.1016/0006-8993(71)90259-9. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Bernd P., Greene L. A. 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):15509–15516. [PubMed] [Google Scholar]
  8. Buck C. R., Martinez H. J., Black I. B., Chao M. V. 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):3060–3063. doi: 10.1073/pnas.84.9.3060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cavicchioli L., Flanigan T. P., Vantini G., Fusco M., Polato P., Toffano G., Walsh F. S., Leon A. NGF Amplifies Expression of NGF Receptor Messenger RNA in Forebrain Cholinergic Neurons of Rats. Eur J Neurosci. 1989 May;1(3):258–262. doi: 10.1111/j.1460-9568.1989.tb00793.x. [DOI] [PubMed] [Google Scholar]
  10. Chandler C. E., Parsons L. M., Hosang M., Shooter E. M. A monoclonal antibody modulates the interaction of nerve growth factor with PC12 cells. J Biol Chem. 1984 Jun 10;259(11):6882–6889. [PubMed] [Google Scholar]
  11. Christy B. A., Lau L. F., Nathans D. A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with "zinc finger" sequences. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7857–7861. doi: 10.1073/pnas.85.21.7857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Cole A. J., Saffen D. W., Baraban J. M., Worley P. F. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature. 1989 Aug 10;340(6233):474–476. doi: 10.1038/340474a0. [DOI] [PubMed] [Google Scholar]
  14. Davies A. M., Bandtlow C., Heumann R., Korsching S., Rohrer H., Thoenen H. Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor. 1987 Mar 26-Apr 1Nature. 326(6111):353–358. doi: 10.1038/326353a0. [DOI] [PubMed] [Google Scholar]
  15. DiStefano P. S., Johnson E. M., Jr Identification of a truncated form of the nerve growth factor receptor. Proc Natl Acad Sci U S A. 1988 Jan;85(1):270–274. doi: 10.1073/pnas.85.1.270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DiStefano P. S., Johnson E. M., Jr Nerve growth factor receptors on cultured rat Schwann cells. J Neurosci. 1988 Jan;8(1):231–241. doi: 10.1523/JNEUROSCI.08-01-00231.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Diamond J., Coughlin M., Macintyre L., Holmes M., Visheau B. 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):6596–6600. doi: 10.1073/pnas.84.18.6596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Edgar D. H., Thoenen H. Selective enzyme induction in a nerve growth factor-responsive pheochromocytoma cell line (PC 12). Brain Res. 1978 Oct 6;154(1):186–190. doi: 10.1016/0006-8993(78)91070-3. [DOI] [PubMed] [Google Scholar]
  19. Ekblad E., Edvinsson L., Wahlestedt C., Uddman R., Håkanson R., Sundler F. Neuropeptide Y co-exists and co-operates with noradrenaline in perivascular nerve fibers. Regul Pept. 1984 Apr;8(3):225–235. doi: 10.1016/0167-0115(84)90064-8. [DOI] [PubMed] [Google Scholar]
  20. Ernfors P., Hallbök F., Ebendal T., Shooter E. M., Radeke M. J., Misko T. P., Persson H. Developmental and regional expression of beta-nerve growth factor receptor mRNA in the chick and rat. Neuron. 1988 Dec;1(10):983–996. doi: 10.1016/0896-6273(88)90155-9. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Goodman R., Herschman H. R. Nerve growth factor-mediated induction of tyrosine hydroxylase in a clonal pheochromocytoma cell line. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4587–4590. doi: 10.1073/pnas.75.9.4587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gorin P. D., Johnson E. M., Jr 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. doi: 10.1016/0006-8993(80)90341-8. [DOI] [PubMed] [Google Scholar]
  24. Green S. H., Greene L. A. A single Mr approximately 103,000 125I-beta-nerve growth factor-affinity-labeled species represents both the low and high affinity forms of the nerve growth factor receptor. J Biol Chem. 1986 Nov 15;261(32):15316–15326. [PubMed] [Google Scholar]
  25. Green S. H., Rydel R. E., Connolly J. L., Greene L. A. 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):830–843. doi: 10.1083/jcb.102.3.830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Greenberg M. E., Ziff E. B. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. doi: 10.1038/311433a0. [DOI] [PubMed] [Google Scholar]
  27. Groudine M., Peretz M., Weintraub H. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol Cell Biol. 1981 Mar;1(3):281–288. doi: 10.1128/mcb.1.3.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hatanaka H. Nerve growth factor-mediated stimulation of tyrosine hydroxylase activity in a clonal rat pheochromocytoma cell line. Brain Res. 1981 Oct 19;222(2):225–233. doi: 10.1016/0006-8993(81)91029-5. [DOI] [PubMed] [Google Scholar]
  29. Hefti F., Gnahn H., Schwab M. E., Thoenen H. 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):1554–1566. doi: 10.1523/JNEUROSCI.02-11-01554.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hempstead B. L., Schleifer L. S., Chao M. V. Expression of functional nerve growth factor receptors after gene transfer. Science. 1989 Jan 20;243(4889):373–375. doi: 10.1126/science.2536190. [DOI] [PubMed] [Google Scholar]
  31. Hendry I. A., Campbell J. Morphometric analysis of rat superior cervical ganglion after axotomy and nerve growth factor treatment. J Neurocytol. 1976 Jun;5(3):351–360. doi: 10.1007/BF01175120. [DOI] [PubMed] [Google Scholar]
  32. Hendry I. A. Cell division in the developing sympathetic nervous system. J Neurocytol. 1977 Jun;6(3):299–309. doi: 10.1007/BF01175193. [DOI] [PubMed] [Google Scholar]
  33. Heumann R., Korsching S., Bandtlow C., Thoenen H. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J Cell Biol. 1987 Jun;104(6):1623–1631. doi: 10.1083/jcb.104.6.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Heumann R., Lindholm D., Bandtlow C., Meyer M., Radeke M. J., Misko T. P., Shooter E., Thoenen H. Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8735–8739. doi: 10.1073/pnas.84.23.8735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Higgins G. A., Koh S., Chen K. S., Gage F. H. NGF induction of NGF receptor gene expression and cholinergic neuronal hypertrophy within the basal forebrain of the adult rat. Neuron. 1989 Aug;3(2):247–256. doi: 10.1016/0896-6273(89)90038-x. [DOI] [PubMed] [Google Scholar]
  36. Hosang M., Shooter E. M. Molecular characteristics of nerve growth factor receptors on PC12 cells. J Biol Chem. 1985 Jan 10;260(1):655–662. [PubMed] [Google Scholar]
  37. Johnson D., Lanahan A., Buck C. R., Sehgal A., Morgan C., Mercer E., Bothwell M., Chao M. Expression and structure of the human NGF receptor. Cell. 1986 Nov 21;47(4):545–554. doi: 10.1016/0092-8674(86)90619-7. [DOI] [PubMed] [Google Scholar]
  38. Johnson E. M., Jr, Gorin P. D., Brandeis L. D., Pearson J. Dorsal root ganglion neurons are destroyed by exposure in utero to maternal antibody to nerve growth factor. Science. 1980 Nov 21;210(4472):916–918. doi: 10.1126/science.7192014. [DOI] [PubMed] [Google Scholar]
  39. Kessler J. A., Black I. B. Nerve growth factor stimulates the development of substance P in sensory ganglia. Proc Natl Acad Sci U S A. 1980 Jan;77(1):649–652. doi: 10.1073/pnas.77.1.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kornblum H. I., Johnson E. M., Jr Time and dose dependencies of effects of nerve growth factor on sympathetic and sensory neurons in neonatal rats. Brain Res. 1982 Feb 18;234(1):41–51. doi: 10.1016/0006-8993(82)90471-1. [DOI] [PubMed] [Google Scholar]
  41. Korsching S., Thoenen H. Developmental changes of nerve growth factor levels in sympathetic ganglia and their target organs. Dev Biol. 1988 Mar;126(1):40–46. doi: 10.1016/0012-1606(88)90236-9. [DOI] [PubMed] [Google Scholar]
  42. Large T. H., Weskamp G., Helder J. C., Radeke M. J., Misko T. P., Shooter E. M., Reichardt L. F. Structure and developmental expression of the nerve growth factor receptor in the chicken central nervous system. Neuron. 1989 Feb;2(2):1123–1134. doi: 10.1016/0896-6273(89)90179-7. [DOI] [PubMed] [Google Scholar]
  43. Lemaire P., Revelant O., Bravo R., Charnay P. Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4691–4695. doi: 10.1073/pnas.85.13.4691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Lemke G., Chao M. Axons regulate Schwann cell expression of the major myelin and NGF receptor genes. Development. 1988 Mar;102(3):499–504. doi: 10.1242/dev.102.3.499. [DOI] [PubMed] [Google Scholar]
  45. Lenoir D., Battenberg E., Kiel M., Bloom F. E., Milner R. J. The brain-specific gene 1B236 is expressed postnatally in the developing rat brain. J Neurosci. 1986 Feb;6(2):522–530. doi: 10.1523/JNEUROSCI.06-02-00522.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. 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]
  47. Levi-Montalcini R., Angeletti P. U. Nerve growth factor. Physiol Rev. 1968 Jul;48(3):534–569. doi: 10.1152/physrev.1968.48.3.534. [DOI] [PubMed] [Google Scholar]
  48. Levi-Montalcini R., Booker B. DESTRUCTION OF THE SYMPATHETIC GANGLIA IN MAMMALS BY AN ANTISERUM TO A NERVE-GROWTH PROTEIN. Proc Natl Acad Sci U S A. 1960 Mar;46(3):384–391. doi: 10.1073/pnas.46.3.384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Levi-Montalcini R., Booker B. 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):373–384. doi: 10.1073/pnas.46.3.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Lewis E. J., Tank A. W., Weiner N., Chikaraishi D. M. 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):14632–14637. [PubMed] [Google Scholar]
  51. Lindsay R. M., Shooter E. M., Radeke M. J., Misko T. P., Dechant G., Thoenen H., Lindholm D. Nerve Growth Factor Regulates Expression of the Nerve Growth Factor Receptor Gene in Adult Sensory Neurons. Eur J Neurosci. 1990;2(5):389–396. doi: 10.1111/j.1460-9568.1990.tb00431.x. [DOI] [PubMed] [Google Scholar]
  52. Mathew T. C., Miller F. D. 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. doi: 10.1016/0012-1606(90)90103-p. [DOI] [PubMed] [Google Scholar]
  53. Max S. R., Rohrer H., Otten U., Thoenen H. Nerve growth factor-mediated induction of tyrosine hydroxylase in rat superior cervical ganglia in vitro. J Biol Chem. 1978 Nov 25;253(22):8013–8015. [PubMed] [Google Scholar]
  54. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. 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]
  56. Miller F. D., Naus C. C., Durand M., Bloom F. E., Milner R. J. Isotypes of alpha-tubulin are differentially regulated during neuronal maturation. J Cell Biol. 1987 Dec;105(6 Pt 2):3065–3073. doi: 10.1083/jcb.105.6.3065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Miller F. D., Naus C. C., Higgins G. A., Bloom F. E., Milner R. J. Developmentally regulated rat brain mRNAs: molecular and anatomical characterization. J Neurosci. 1987 Aug;7(8):2433–2444. [PMC free article] [PubMed] [Google Scholar]
  58. Miller F. D., Ozimek G., Milner R. J., Bloom F. E. Regulation of neuronal oxytocin mRNA by ovarian steroids in the mature and developing hypothalamus. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2468–2472. doi: 10.1073/pnas.86.7.2468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Miller F. D., Tetzlaff W., Bisby M. A., Fawcett J. W., Milner R. J. Rapid induction of the major embryonic alpha-tubulin mRNA, T alpha 1, during nerve regeneration in adult rats. J Neurosci. 1989 Apr;9(4):1452–1463. doi: 10.1523/JNEUROSCI.09-04-01452.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Njå A., Purves D. The effects of nerve growth factor and its antiserum on synapses in the superior cervical ganglion of the guinea-pig. J Physiol. 1978 Apr;277:53–75. [PMC free article] [PubMed] [Google Scholar]
  61. Osborn M., Weber K. Immunofluorescence and immunocytochemical procedures with affinity purified antibodies: tubulin-containing structures. Methods Cell Biol. 1982;24:97–132. doi: 10.1016/s0091-679x(08)60650-0. [DOI] [PubMed] [Google Scholar]
  62. Otten U., Goedert M., Mayer N., Lembeck F. Requirement of nerve growth factor for development of substance P-containing sensory neurones. Nature. 1980 Sep 11;287(5778):158–159. doi: 10.1038/287158a0. [DOI] [PubMed] [Google Scholar]
  63. Otten U., Towbin M. Permissive action of glucocorticoids in induction of tyrosine hydroxylase by nerve growth factor in a pheochromocytoma cell line. Brain Res. 1980 Jul 7;193(1):304–308. doi: 10.1016/0006-8993(80)90972-5. [DOI] [PubMed] [Google Scholar]
  64. Radeke M. J., Misko T. P., Hsu C., Herzenberg L. A., Shooter E. M. Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature. 1987 Feb 12;325(6105):593–597. doi: 10.1038/325593a0. [DOI] [PubMed] [Google Scholar]
  65. Rave N., Crkvenjakov R., Boedtker H. Identification of procollagen mRNAs transferred to diazobenzyloxymethyl paper from formaldehyde agarose gels. Nucleic Acids Res. 1979 Aug 10;6(11):3559–3567. doi: 10.1093/nar/6.11.3559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Raynaud B., Faucon-Biguet N., Vidal S., Mallet J., Weber M. J. Regulation of neurotransmitter metabolic enzymes and tyrosine hydroxylase mRNA level by nerve growth factor in cultured sympathetic neurones. Development. 1988 Feb;102(2):361–368. doi: 10.1242/dev.102.2.361. [DOI] [PubMed] [Google Scholar]
  67. Richardson P. M., Issa V. M., Riopelle R. J. Distribution of neuronal receptors for nerve growth factor in the rat. J Neurosci. 1986 Aug;6(8):2312–2321. doi: 10.1523/JNEUROSCI.06-08-02312.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Rohrer H., Otten U., Thoenen H. On the role of RNA synthesis in the selective induction of tyrosine hydroxylase by nerve growth factor. Brain Res. 1978 Dec 29;159(2):436–439. doi: 10.1016/0006-8993(78)90554-1. [DOI] [PubMed] [Google Scholar]
  69. Schibler U., Tosi M., Pittet A. C., Fabiani L., Wellauer P. K. Tissue-specific expression of mouse alpha-amylase genes. J Mol Biol. 1980 Sep 5;142(1):93–116. doi: 10.1016/0022-2836(80)90208-9. [DOI] [PubMed] [Google Scholar]
  70. Sehgal A., Patil N., Chao M. A constitutive promoter directs expression of the nerve growth factor receptor gene. Mol Cell Biol. 1988 Aug;8(8):3160–3167. doi: 10.1128/mcb.8.8.3160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Snider W. D. Nerve growth factor enhances dendritic arborization of sympathetic ganglion cells in developing mammals. J Neurosci. 1988 Jul;8(7):2628–2634. doi: 10.1523/JNEUROSCI.08-07-02628.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Sukhatme V. P., Cao X. M., Chang L. C., Tsai-Morris C. H., Stamenkovich D., Ferreira P. C., Cohen D. R., Edwards S. A., Shows T. B., Curran T. A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization. Cell. 1988 Apr 8;53(1):37–43. doi: 10.1016/0092-8674(88)90485-0. [DOI] [PubMed] [Google Scholar]
  73. Sutter A., Riopelle R. J., Harris-Warrick R. M., Shooter E. M. Nerve growth factor receptors. Characterization of two distinct classes of binding sites on chick embryo sensory ganglia cells. J Biol Chem. 1979 Jul 10;254(13):5972–5982. [PubMed] [Google Scholar]
  74. Taniuchi M., Clark H. B., Johnson E. M., Jr Induction of nerve growth factor receptor in Schwann cells after axotomy. Proc Natl Acad Sci U S A. 1986 Jun;83(11):4094–4098. doi: 10.1073/pnas.83.11.4094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Thoenen H., Angeletti P. U., Levi-Montalcini R., Kettler R. 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):1598–1602. doi: 10.1073/pnas.68.7.1598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Tischler A. S., Greene L. A. Nerve growth factor-induced process formation by cultured rat pheochromocytoma cells. Nature. 1975 Nov 27;258(5533):341–342. doi: 10.1038/258341a0. [DOI] [PubMed] [Google Scholar]
  78. Verge V. M., Riopelle R. J., Richardson P. M. Nerve growth factor receptors on normal and injured sensory neurons. J Neurosci. 1989 Mar;9(3):914–922. doi: 10.1523/JNEUROSCI.09-03-00914.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Wyatt S., Shooter E. M., Davies A. M. Expression of the NGF receptor gene in sensory neurons and their cutaneous targets prior to and during innervation. Neuron. 1990 Mar;4(3):421–427. doi: 10.1016/0896-6273(90)90054-j. [DOI] [PubMed] [Google Scholar]
  80. Yan Q., Johnson E. M., Jr An immunohistochemical study of the nerve growth factor receptor in developing rats. J Neurosci. 1988 Sep;8(9):3481–3498. doi: 10.1523/JNEUROSCI.08-09-03481.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES