Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1993 Apr 2;121(2):423–438. doi: 10.1083/jcb.121.2.423

Thyroid hormone receptor/c-erbA: control of commitment and differentiation in the neuronal/chromaffin progenitor line PC12

PMCID: PMC2200090  PMID: 8385673

Abstract

The c-erbA proto-oncogenes encode nuclear receptors for thyroid hormone (T3), a hormone intimately involved in mammalian brain maturation. To study thyroid hormone receptor (TR) action on neuronal cells in vitro, we expressed the chicken c-erbA/TR alpha-1 as well as its oncogenic variant v-erbA in the adrenal medulla progenitor cell line PC12. In the absence of T3, exogenous TR alpha-1 inhibits NGF-induced neuronal differentiation and represses neuron-specific gene expression. In contrast, TR alpha-1 allows normal differentiation and neuronal gene expression to occur in the presence of T3. Finally, TR alpha-1- expressing cells become NGF-responsive for proliferation when T3 is absent, but NGF-dependent for survival in presence of T3. A similar differentiation induction by NGF plus T3 was observed in a central nervous system-derived neuronal cell line (E 18) expressing exogenous TR alpha-1. Together with the finding that TR alpha-1 constitutively blocked dexamethasone-induced differentiation of PC12 cells into the chromaffin pathway, these results suggest that TR alpha-1 plays an important role in regulating commitment and maturation of neuronal progenitors. In contrast, the v-erbA oncogene, a mutated, oncogenic version of TR alpha-1, partially but constitutively inhibited NGF- induced neuronal differentiation of PC12 cells and potentiated dexamethasone-induced chromaffin differentiation, giving rise to an aberrant "interlineage" cell phenotype.

Full Text

The Full Text of this article is available as a PDF (4.1 MB).

Selected References

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

  1. Anderson D. J., Axel R. A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. Cell. 1986 Dec 26;47(6):1079–1090. doi: 10.1016/0092-8674(86)90823-8. [DOI] [PubMed] [Google Scholar]
  2. Barde Y. A., Edgar D., Thoenen H. Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1982;1(5):549–553. doi: 10.1002/j.1460-2075.1982.tb01207.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barr P. J. Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell. 1991 Jul 12;66(1):1–3. doi: 10.1016/0092-8674(91)90129-m. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Berkemeier L. R., Winslow J. W., Kaplan D. R., Nikolics K., Goeddel D. V., Rosenthal A. Neurotrophin-5: a novel neurotrophic factor that activates trk and trkB. Neuron. 1991 Nov;7(5):857–866. doi: 10.1016/0896-6273(91)90287-a. [DOI] [PubMed] [Google Scholar]
  6. Bernal J., Pekonen F. Ontogenesis of the nuclear 3,5,3'-triiodothyronine receptor in the human fetal brain. Endocrinology. 1984 Feb;114(2):677–679. doi: 10.1210/endo-114-2-677. [DOI] [PubMed] [Google Scholar]
  7. Beug H., Blundell P. A., Graf T. Reversibility of differentiation and proliferative capacity in avian myelomonocytic cells transformed by tsE26 leukemia virus. Genes Dev. 1987 May;1(3):277–286. doi: 10.1101/gad.1.3.277. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Bradley D. J., Young W. S., 3rd, Weinberger C. Differential expression of alpha and beta thyroid hormone receptor genes in rat brain and pituitary. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7250–7254. doi: 10.1073/pnas.86.18.7250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  11. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clos J., Legrand C. An interaction between thyroid hormone and nerve growth factor promotes the development of hippocampus, olfactory bulbs and cerebellum: a comparative biochemical study of normal and hypothyroid rats. Growth Factors. 1990;3(3):205–220. doi: 10.3109/08977199009043905. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Damm K., Thompson C. C., Evans R. M. Protein encoded by v-erbA functions as a thyroid-hormone receptor antagonist. Nature. 1989 Jun 22;339(6226):593–597. doi: 10.1038/339593a0. [DOI] [PubMed] [Google Scholar]
  15. Desbois C., Pain B., Guilhot C., Benchaibi M., Ffrench M., Ghysdael J., Madjar J. J., Samarut J. v-erbA oncogene abrogates growth inhibition of chicken embryo fibroblasts induced by retinoic acid. Oncogene. 1991 Nov;6(11):2129–2135. [PubMed] [Google Scholar]
  16. Disela C., Glineur C., Bugge T., Sap J., Stengl G., Dodgson J., Stunnenberg H., Beug H., Zenke M. v-erbA overexpression is required to extinguish c-erbA function in erythroid cell differentiation and regulation of the erbA target gene CAII. Genes Dev. 1991 Nov;5(11):2033–2047. doi: 10.1101/gad.5.11.2033. [DOI] [PubMed] [Google Scholar]
  17. Doherty P., Rowett L. H., Moore S. E., Mann D. A., Walsh F. S. Neurite outgrowth in response to transfected N-CAM and N-cadherin reveals fundamental differences in neuronal responsiveness to CAMs. Neuron. 1991 Feb;6(2):247–258. doi: 10.1016/0896-6273(91)90360-c. [DOI] [PubMed] [Google Scholar]
  18. Doupe A. J., Landis S. C., Patterson P. H. Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors, and chromaffin cell plasticity. J Neurosci. 1985 Aug;5(8):2119–2142. doi: 10.1523/JNEUROSCI.05-08-02119.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Doupe A. J., Patterson P. H., Landis S. C. Small intensely fluorescent cells in culture: role of glucocorticoids and growth factors in their development and interconversions with other neural crest derivatives. J Neurosci. 1985 Aug;5(8):2143–2160. doi: 10.1523/JNEUROSCI.05-08-02143.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Dussault J. H., Ruel J. Thyroid hormones and brain development. Annu Rev Physiol. 1987;49:321–334. doi: 10.1146/annurev.ph.49.030187.001541. [DOI] [PubMed] [Google Scholar]
  21. Falcone G., Boettiger D., Alemà S., Tatò F. Role of cell division in differentiation of myoblasts infected with a temperature-sensitive mutant of Rous sarcoma virus. EMBO J. 1984 Jun;3(6):1327–1331. doi: 10.1002/j.1460-2075.1984.tb01971.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  24. Forrest D., Hallbök F., Persson H., Vennström B. Distinct functions for thyroid hormone receptors alpha and beta in brain development indicated by differential expression of receptor genes. EMBO J. 1991 Feb;10(2):269–275. doi: 10.1002/j.1460-2075.1991.tb07947.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Forrest D., Sjöberg M., Vennström B. Contrasting developmental and tissue-specific expression of alpha and beta thyroid hormone receptor genes. EMBO J. 1990 May;9(5):1519–1528. doi: 10.1002/j.1460-2075.1990.tb08270.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gage F. H. Repopulating the mortal brain with immortal cells. Curr Biol. 1992 May;2(5):232–234. doi: 10.1016/0960-9822(92)90351-a. [DOI] [PubMed] [Google Scholar]
  27. Glineur C., Zenke M., Beug H., Ghysdael J. Phosphorylation of the v-erbA protein is required for its function as an oncogene. Genes Dev. 1990 Oct;4(10):1663–1676. doi: 10.1101/gad.4.10.1663. [DOI] [PubMed] [Google Scholar]
  28. Goldberg Y., Glineur C., Gesquière J. C., Ricouart A., Sap J., Vennström B., Ghysdael J. Activation of protein kinase C or cAMP-dependent protein kinase increases phosphorylation of the c-erbA-encoded thyroid hormone receptor and of the v-erbA-encoded protein. EMBO J. 1988 Aug;7(8):2425–2433. doi: 10.1002/j.1460-2075.1988.tb03088.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gould E., Butcher L. L. Developing cholinergic basal forebrain neurons are sensitive to thyroid hormone. J Neurosci. 1989 Sep;9(9):3347–3358. doi: 10.1523/JNEUROSCI.09-09-03347.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Gunning P. W., Landreth G. E., Bothwell M. A., Shooter E. M. Differential and synergistic actions of nerve growth factor and cyclic AMP in PC12 cells. J Cell Biol. 1981 May;89(2):240–245. doi: 10.1083/jcb.89.2.240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Halegoua S., Armstrong R. C., Kremer N. E. Dissecting the mode of action of a neuronal growth factor. Curr Top Microbiol Immunol. 1991;165:119–170. doi: 10.1007/978-3-642-75747-1_7. [DOI] [PubMed] [Google Scholar]
  34. Hallbök F., Ibáez C. F., Persson H. Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron. 1991 May;6(5):845–858. doi: 10.1016/0896-6273(91)90180-8. [DOI] [PubMed] [Google Scholar]
  35. Hohn A., Leibrock J., Bailey K., Barde Y. A. Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature. 1990 Mar 22;344(6264):339–341. doi: 10.1038/344339a0. [DOI] [PubMed] [Google Scholar]
  36. Holtzman D. M., Li Y., Parada L. F., Kinsman S., Chen C. K., Valletta J. S., Zhou J., Long J. B., Mobley W. C. p140trk mRNA marks NGF-responsive forebrain neurons: evidence that trk gene expression is induced by NGF. Neuron. 1992 Sep;9(3):465–478. doi: 10.1016/0896-6273(92)90184-f. [DOI] [PubMed] [Google Scholar]
  37. Hudson L. G., Santon J. B., Glass C. K., Gill G. N. Ligand-activated thyroid hormone and retinoic acid receptors inhibit growth factor receptor promoter expression. Cell. 1990 Sep 21;62(6):1165–1175. doi: 10.1016/0092-8674(90)90393-s. [DOI] [PubMed] [Google Scholar]
  38. Ito E., Sweterlitsch L. A., Tran P. B., Rauscher F. J., 3rd, Narayanan R. Inhibition of PC-12 cell differentiation by the immediate early gene fra-1. Oncogene. 1990 Dec;5(12):1755–1760. [PubMed] [Google Scholar]
  39. Johnson J. E., Birren S. J., Anderson D. J. Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature. 1990 Aug 30;346(6287):858–861. doi: 10.1038/346858a0. [DOI] [PubMed] [Google Scholar]
  40. Jones K. R., Reichardt L. F. Molecular cloning of a human gene that is a member of the nerve growth factor family. Proc Natl Acad Sci U S A. 1990 Oct;87(20):8060–8064. doi: 10.1073/pnas.87.20.8060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Koenig R. J., Lazar M. A., Hodin R. A., Brent G. A., Larsen P. R., Chin W. W., Moore D. D. Inhibition of thyroid hormone action by a non-hormone binding c-erbA protein generated by alternative mRNA splicing. Nature. 1989 Feb 16;337(6208):659–661. doi: 10.1038/337659a0. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Lazar M. A., Hodin R. A., Chin W. W. Human carboxyl-terminal variant of alpha-type c-erbA inhibits trans-activation by thyroid hormone receptors without binding thyroid hormone. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7771–7774. doi: 10.1073/pnas.86.20.7771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Leibrock J., Lottspeich F., Hohn A., Hofer M., Hengerer B., Masiakowski P., Thoenen H., Barde Y. A. Molecular cloning and expression of brain-derived neurotrophic factor. Nature. 1989 Sep 14;341(6238):149–152. doi: 10.1038/341149a0. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. 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]
  47. Lewis P. D., Patel A. J., Johnson A. L., Balázs R. Effect of thyroid deficiency on cell acquistion in the postnatal rat brain: a quantitative histological study. Brain Res. 1976 Mar 5;104(1):49–62. doi: 10.1016/0006-8993(76)90646-6. [DOI] [PubMed] [Google Scholar]
  48. Lin L. F., Mismer D., Lile J. D., Armes L. G., Butler E. T., 3rd, Vannice J. L., Collins F. Purification, cloning, and expression of ciliary neurotrophic factor (CNTF). Science. 1989 Nov 24;246(4933):1023–1025. doi: 10.1126/science.2587985. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Lo L. C., Johnson J. E., Wuenschell C. W., Saito T., Anderson D. J. Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev. 1991 Sep;5(9):1524–1537. doi: 10.1101/gad.5.9.1524. [DOI] [PubMed] [Google Scholar]
  51. 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]
  52. Maisonpierre P. C., Belluscio L., Squinto S., Ip N. Y., Furth M. E., Lindsay R. M., Yancopoulos G. D. Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science. 1990 Mar 23;247(4949 Pt 1):1446–1451. doi: 10.1126/science.247.4949.1446. [DOI] [PubMed] [Google Scholar]
  53. 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]
  54. Mellström B., Naranjo J. R., Santos A., Gonzalez A. M., Bernal J. Independent expression of the alpha and beta c-erbA genes in developing rat brain. Mol Endocrinol. 1991 Sep;5(9):1339–1350. doi: 10.1210/mend-5-9-1339. [DOI] [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. Milbrandt J. Nerve growth factor induces a gene homologous to the glucocorticoid receptor gene. Neuron. 1988 May;1(3):183–188. doi: 10.1016/0896-6273(88)90138-9. [DOI] [PubMed] [Google Scholar]
  57. Morgan J. I., Curran T. Role of ion flux in the control of c-fos expression. Nature. 1986 Aug 7;322(6079):552–555. doi: 10.1038/322552a0. [DOI] [PubMed] [Google Scholar]
  58. Muñoz A., Höppner W., Sap J., Brady G., Nordström K., Seitz H. J., Vennström B. The chicken c-erbA alpha-product induces expression of thyroid hormone-responsive genes in 3,5,3'-triiodothyronine receptor-deficient rat hepatoma cells. Mol Endocrinol. 1990 Feb;4(2):312–320. doi: 10.1210/mend-4-2-312. [DOI] [PubMed] [Google Scholar]
  59. Muñoz A., Rodriguez-Peña A., Perez-Castillo A., Ferreiro B., Sutcliffe J. G., Bernal J. Effects of neonatal hypothyroidism on rat brain gene expression. Mol Endocrinol. 1991 Feb;5(2):273–280. doi: 10.1210/mend-5-2-273. [DOI] [PubMed] [Google Scholar]
  60. Muñoz A., Zenke M., Gehring U., Sap J., Beug H., Vennström B. Characterization of the hormone-binding domain of the chicken c-erbA/thyroid hormone receptor protein. EMBO J. 1988 Jan;7(1):155–159. doi: 10.1002/j.1460-2075.1988.tb02795.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Oppenheim R. W. Cell death during development of the nervous system. Annu Rev Neurosci. 1991;14:453–501. doi: 10.1146/annurev.ne.14.030191.002321. [DOI] [PubMed] [Google Scholar]
  62. Patel A. J., Hayashi M., Hunt A. Role of thyroid hormone and nerve growth factor in the development of choline acetyltransferase and other cell-specific marker enzymes in the basal forebrain of the rat. J Neurochem. 1988 Mar;50(3):803–811. doi: 10.1111/j.1471-4159.1988.tb02984.x. [DOI] [PubMed] [Google Scholar]
  63. Prentice H. M., Moore S. E., Dickson J. G., Doherty P., Walsh F. S. Nerve growth factor-induced changes in neural cell adhesion molecule (N-CAM) in PC12 cells. EMBO J. 1987 Jul;6(7):1859–1863. doi: 10.1002/j.1460-2075.1987.tb02444.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Rentoumis A., Chatterjee V. K., Madison L. D., Datta S., Gallagher G. D., Degroot L. J., Jameson J. L. Negative and positive transcriptional regulation by thyroid hormone receptor isoforms. Mol Endocrinol. 1990 Oct;4(10):1522–1531. doi: 10.1210/mend-4-10-1522. [DOI] [PubMed] [Google Scholar]
  65. Samuels H. H., Stanley F., Shapiro L. E. Dose-dependent depletion of nuclear receptors by L-triiodothyronine: evidence for a role in induction of growth hormone synthesis in cultured GH1 cells. Proc Natl Acad Sci U S A. 1976 Nov;73(11):3877–3881. doi: 10.1073/pnas.73.11.3877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Samuels H. H., Stanley F., Shapiro L. E. Modulation of thyroid hormone nuclear receptor levels by 3,5,3'-triiodo-L-thyronine in GH1 cells. Evidence for two functional components of nuclear-bound receptor and relationship to the induction of growth hormone synthesis. J Biol Chem. 1977 Sep 10;252(17):6052–6060. [PubMed] [Google Scholar]
  67. Sap J., Muñoz A., Damm K., Goldberg Y., Ghysdael J., Leutz A., Beug H., Vennström B. The c-erb-A protein is a high-affinity receptor for thyroid hormone. Nature. 1986 Dec 18;324(6098):635–640. doi: 10.1038/324635a0. [DOI] [PubMed] [Google Scholar]
  68. Sap J., Muñoz A., Schmitt J., Stunnenberg H., Vennström B. Repression of transcription mediated at a thyroid hormone response element by the v-erb-A oncogene product. Nature. 1989 Jul 20;340(6230):242–244. doi: 10.1038/340242a0. [DOI] [PubMed] [Google Scholar]
  69. Scheibe R. J., Ginty D. D., Wagner J. A. Retinoic acid stimulates the differentiation of PC12 cells that are deficient in cAMP-dependent protein kinase. J Cell Biol. 1991 Jun;113(5):1173–1182. doi: 10.1083/jcb.113.5.1173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Schroeder C., Gibson L., Beug H. The v-erbA oncogene requires cooperation with tyrosine kinases to arrest erythroid differentiation induced by ligand-activated endogenous c-erbA and retinoic acid receptor. Oncogene. 1992 Feb;7(2):203–216. [PubMed] [Google Scholar]
  71. Schroeder C., Gibson L., Zenke M., Beug H. Modulation of normal erythroid differentiation by the endogenous thyroid hormone and retinoic acid receptors: a possible target for v-erbA oncogene action. Oncogene. 1992 Feb;7(2):217–227. [PubMed] [Google Scholar]
  72. Stein R., Mori N., Matthews K., Lo L. C., Anderson D. J. The NGF-inducible SCG10 mRNA encodes a novel membrane-bound protein present in growth cones and abundant in developing neurons. Neuron. 1988 Aug;1(6):463–476. doi: 10.1016/0896-6273(88)90177-8. [DOI] [PubMed] [Google Scholar]
  73. 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]
  74. Strait K. A., Schwartz H. L., Seybold V. S., Ling N. C., Oppenheimer J. H. Immunofluorescence localization of thyroid hormone receptor protein beta 1 and variant alpha 2 in selected tissues: cerebellar Purkinje cells as a model for beta 1 receptor-mediated developmental effects of thyroid hormone in brain. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3887–3891. doi: 10.1073/pnas.88.9.3887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Szeberényi J., Cai H., Cooper G. M. Effect of a dominant inhibitory Ha-ras mutation on neuronal differentiation of PC12 cells. Mol Cell Biol. 1990 Oct;10(10):5324–5332. doi: 10.1128/mcb.10.10.5324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Tata J. R., Kawahara A., Baker B. S. Prolactin inhibits both thyroid hormone-induced morphogenesis and cell death in cultured amphibian larval tissues. Dev Biol. 1991 Jul;146(1):72–80. doi: 10.1016/0012-1606(91)90447-b. [DOI] [PubMed] [Google Scholar]
  77. Van Hooff C. O., Holthuis J. C., Oestreicher A. B., Boonstra J., De Graan P. N., Gispen W. H. Nerve growth factor-induced changes in the intracellular localization of the protein kinase C substrate B-50 in pheochromocytoma PC12 cells. J Cell Biol. 1989 Mar;108(3):1115–1125. doi: 10.1083/jcb.108.3.1115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Vennström B., Bishop J. M. Isolation and characterization of chicken DNA homologous to the two putative oncogenes of avian erythroblastosis virus. Cell. 1982 Jan;28(1):135–143. doi: 10.1016/0092-8674(82)90383-x. [DOI] [PubMed] [Google Scholar]
  79. Weinberger C., Thompson C. C., Ong E. S., Lebo R., Gruol D. J., Evans R. M. The c-erb-A gene encodes a thyroid hormone receptor. Nature. 1986 Dec 18;324(6098):641–646. doi: 10.1038/324641a0. [DOI] [PubMed] [Google Scholar]
  80. Zenke M., Kahn P., Disela C., Vennström B., Leutz A., Keegan K., Hayman M. J., Choi H. R., Yew N., Engel J. D. v-erbA specifically suppresses transcription of the avian erythrocyte anion transporter (band 3) gene. Cell. 1988 Jan 15;52(1):107–119. doi: 10.1016/0092-8674(88)90535-1. [DOI] [PubMed] [Google Scholar]
  81. Zenke M., Muñoz A., Sap J., Vennström B., Beug H. v-erbA oncogene activation entails the loss of hormone-dependent regulator activity of c-erbA. Cell. 1990 Jun 15;61(6):1035–1049. doi: 10.1016/0092-8674(90)90068-p. [DOI] [PubMed] [Google Scholar]
  82. Zhang X. K., Wills K. N., Husmann M., Hermann T., Pfahl M. Novel pathway for thyroid hormone receptor action through interaction with jun and fos oncogene activities. Mol Cell Biol. 1991 Dec;11(12):6016–6025. doi: 10.1128/mcb.11.12.6016. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES