Crossref journal-article
Cold Spring Harbor Laboratory
Genes & Development (246)
Abstract

We have studied nerve growth factor (NGF) regulation of the expression of the tyrosine hydroxylase (TH) gene in PC12 cells. The TH gene encodes the initial and rate-limiting enzyme of the catecholamine biosynthetic pathway. We show that the TH gene is transiently transcriptionally induced by a mechanism reliant on new protein synthesis during 1-2 hr of NGF stimulation, a time following the induction of the c-fos gene at 15 min post-NGF treatment. A potential regulatory sequence located within the TH gene promoter, the TH-FSE, shares homology to a known regulatory element, the fat-specific element (FSE), which is found upstream from genes activated during adipocyte differentiation and binds the Fos-Jun transcription factor complex. We show that the TH-FSE DNA sequence elevates the basal level of transcription from the rat TH promoter and is required for NGF inducibility. This DNA element binds authentic Fos-Jun products produced abundance during NGF stimulation and by in vitro translation. We demonstrate further that the TH-FSE can bind proteins present in PC12 nuclear extracts in a sequence-specific manner. The DNA/nucleoprotein complex that forms increases in abundance during NGF stimulation and reaches a maximum level at 4 hr of treatment. Antibody inhibition studies utilizing an anti-Fos antibody indicate that Fos and/or Fos-related antigen(s) associate with the TH-FSE and suggest that the Fos protein family contributes to the regulation of TH in vivo. These results support a model in which NGF-induced immediate early genes, including c-Fos, contribute to the regulation of delayed early genes such as TH and thereby control neuronal differentiation.

Bibliography

Gizang-Ginsberg, E., & Ziff, E. B. (1990). Nerve growth factor regulates tyrosine hydroxylase gene transcription through a nucleoprotein complex that contains c-Fos. Genes & Development, 4(4), 477–491.

Authors 2
  1. E Gizang-Ginsberg (first)
  2. E B Ziff (additional)
References 117 Referenced 190
  1. 10.1523/JNEUROSCI.04-07-01771.1984 / J. Neurosci. / Nerve growth factor-mediated enzyme induction in primary cultures of bovine adrenal chromaffin cells: Specificity and level of regulation. (1984)
  2. {'key': '2021111320044364000_4.4.477.2', 'first-page': '2140', 'article-title': 'Complexity of the early genetic response to growth factors in mouse fibroblasts.', 'volume': '8', 'year': '1988', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Complexity of the early genetic response to growth factors in mouse fibroblasts. (1988)
  3. 10.1073/pnas.76.3.1246
  4. 10.1016/0092-8674(86)90823-8
  5. 10.1016/0092-8674(87)90611-8
  6. 10.1101/gad.3.3.304
  7. 10.1016/S0021-9258(17)42883-3 / J. Biol. Chem. / Androgen-regulated orinthine decarboxylase mRNAs of mouse kidney. (1984)
  8. {'key': '2021111320044364000_4.4.477.8', 'first-page': '4272', 'article-title': 'Multiple sequence elements of a single functional class are required for cyclic AMP responsiveness of the mouse c-fos promoter.', 'volume': '9', 'year': '1989', 'journal-title': 'Mol. Cell Biol.'} / Mol. Cell Biol. / Multiple sequence elements of a single functional class are required for cyclic AMP responsiveness of the mouse c-fos promoter. (1989)
  9. 10.1126/science.2825349
  10. 10.1016/S0021-9258(18)67410-1 / Biol. Chem. / Identification of four phosphorylation sites in the M-terminal region of tyrosine hydroxylase. (1986)
  11. 10.1016/0092-8674(85)90174-6
  12. 10.1016/0092-8674(88)90076-1
  13. {'key': '2021111320044364000_4.4.477.13', 'first-page': '135', 'article-title': 'Nerve growth factor regulates gene expression by several distinct mechanisms.', 'volume': '9', 'year': '1989', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Nerve growth factor regulates gene expression by several distinct mechanisms. (1989)
  14. 10.1073/pnas.85.21.7857
  15. 10.1016/0092-8674(80)90238-X
  16. 10.1016/0092-8674(83)90037-5
  17. {'key': '2021111320044364000_4.4.477.17', 'first-page': '2063', 'article-title': 'Fra-1: A serum-inducible, immediate early gene that encodes a fos-related antigen.', 'volume': '8', 'year': '1988', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Fra-1: A serum-inducible, immediate early gene that encodes a fos-related antigen. (1988)
  18. 10.1016/0092-8674(88)90024-4
  19. 10.1126/science.4035354
  20. 10.1073/pnas.83.22.8521
  21. 10.1128/jvi.42.1.114-122.1982 / J. Virol. / Candidate product of the FBJ murine osteosarcoma virus oncogene: Characterization of a 55,000-dalton phosphoprotein. (1982)
  22. 10.1016/0042-6822(84)90132-6
  23. {'key': '2021111320044364000_4.4.477.23', 'first-page': '80', 'article-title': 'Isolation and characterization of the c-fos (rat) cDNA and analysis of post-translational modification in vitro.', 'volume': '2', 'year': '1987', 'journal-title': 'Oncogene'} / Oncogene / Isolation and characterization of the c-fos (rat) cDNA and analysis of post-translational modification in vitro. (1987)
  24. 10.1128/jvi.44.2.674-682.1982 / J. Virol. / FBJ murine osteosarcoma virus: Identification and molecular cloning of biologically active proviral DNA. (1982)
  25. {'key': '2021111320044364000_4.4.477.25', 'first-page': '1475', 'article-title': 'Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.', 'volume': '14', 'year': '1983', 'journal-title': 'Nucleic Acids Res.'} / Nucleic Acids Res. / Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. (1983)
  26. 10.1016/0092-8674(87)90621-0
  27. 10.1523/JNEUROSCI.05-08-02119.1985 / J. Neurosci. / Environmental influences in the development of neural crest derivates: glucocorticoids, growth factors and chromaffin cell plasticity. (1985)
  28. 10.1016/0006-8993(78)91070-3
  29. {'key': '2021111320044364000_4.4.477.29', 'first-page': '3490', 'article-title': 'c-fos sequence necessary for basal expression and induction by epidermal growth factor, 12-O-tetradecanoyl phorbol-13-acetate and the calcium ionophore.', 'volume': '7', 'year': '1987', 'journal-title': 'Mol. Cell Biol.'} / Mol. Cell Biol. / c-fos sequence necessary for basal expression and induction by epidermal growth factor, 12-O-tetradecanoyl phorbol-13-acetate and the calcium ionophore. (1987)
  30. 10.1016/S0021-9258(18)45580-9 / J. Biol. Chem. / Cis-acting elements of the rat growth hormone gene which mediates basal and regulated expression by thyroid hormone. (1987)
  31. 10.1126/science.2964084
  32. {'key': '2021111320044364000_4.4.477.32', 'first-page': '213', 'article-title': 'Analysis of fos protein complexes and fos-related antigens by high-resolution two-dimensional gel electrophoresis.', 'volume': '1', 'year': '1987', 'journal-title': 'Oncogene'} / Oncogene / Analysis of fos protein complexes and fos-related antigens by high-resolution two-dimensional gel electrophoresis. (1987)
  33. {'key': '2021111320044364000_4.4.477.33', 'first-page': '4305', 'article-title': 'Multiple protein-binding sites in the 5′-flanking region regulate c-fos expression.', 'volume': '6', 'year': '1986', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Multiple protein-binding sites in the 5′-flanking region regulate c-fos expression. (1986)
  34. 10.1073/pnas.75.9.4587
  35. 10.1083/jcb.84.3.495
  36. 10.1038/311433a0
  37. 10.1016/S0021-9258(17)38689-1 / J. Biol. Chem. / Nerve growth factor and epidermal growth factor induce transient changes in proto-oncogene transcription in PC12 cells. (1985)
  38. {'key': '2021111320044364000_4.4.477.38', 'first-page': '1050', 'article-title': 'Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription.', 'volume': '6', 'year': '1986', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription. (1986)
  39. {'key': '2021111320044364000_4.4.477.39', 'first-page': '1217', 'article-title': 'Mutation of the c-fos gene dyad symmetry element inhibits serum inducibility of transcription in vivo and the nuclear regulatory factor binding in vitro.', 'volume': '7', 'year': '1987', 'journal-title': 'Mel. Cell. Biol.'} / Mel. Cell. Biol. / Mutation of the c-fos gene dyad symmetry element inhibits serum inducibility of transcription in vivo and the nuclear regulatory factor binding in vitro. (1987)
  40. {'key': '2021111320044364000_4.4.477.40', 'first-page': '2424', 'article-title': 'Establishment of a nonadrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor.', 'volume': '23', 'year': '1976', 'journal-title': 'Proc. Natl. Acad. Sci.'} / Proc. Natl. Acad. Sci. / Establishment of a nonadrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. (1976)
  41. 10.1016/B978-0-12-008303-9.50016-5
  42. {'key': '2021111320044364000_4.4.477.42', 'first-page': '787', 'article-title': 'Isolation and characterization of full-length cDNA clones for human α, β, and γ-actin mRNAs: Skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed.', 'volume': '3', 'year': '1983', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Isolation and characterization of full-length cDNA clones for human α, β, and γ-actin mRNAs: Skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed. (1983)
  43. 10.1016/0092-8674(88)90147-X
  44. 10.1016/0006-8993(75)90826-4
  45. 10.1093/nar/15.5.2363
  46. 10.1016/0006-8993(81)91029-5
  47. 10.1101/gad.3.3.293
  48. 10.1073/pnas.85.22.8444
  49. 10.1002/j.1460-2075.1989.tb03525.x / EMBO J. / Characterization of junD: A new member of the jun proto-oncogene family. (1989)
  50. {'key': '2021111320044364000_4.4.477.50', 'first-page': '4225', 'article-title': 'A common trans-acting factor is involved in transcriptional regulation of neurotransmittter genes by cyclic AMP.', 'volume': '8', 'year': '1988', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / A common trans-acting factor is involved in transcriptional regulation of neurotransmittter genes by cyclic AMP. (1988)
  51. 10.1126/science.2462278
  52. 10.1002/j.1460-2075.1989.tb08394.x / EMBO J. / Autoregulation of fos: The dyad symmetry element as the major target of repression. (1989)
  53. 10.1038/336646a0
  54. 10.1073/pnas.82.21.7330
  55. {'key': '2021111320044364000_4.4.477.55', 'first-page': '865', 'article-title': 'Primary culture of chromaffin cells: Molecular mechanism for the induction of tyrosine hydroxylase mediated by 8-Br-cyclic AMP.', 'volume': '16', 'year': '1979', 'journal-title': 'Mol. Pharmacol.'} / Mol. Pharmacol. / Primary culture of chromaffin cells: Molecular mechanism for the induction of tyrosine hydroxylase mediated by 8-Br-cyclic AMP. (1979)
  56. 10.1073/pnas.82.2.488
  57. 10.1038/227680a0
  58. 10.1016/0166-2236(81)90056-4
  59. 10.1002/j.1460-2075.1985.tb04057.x / EMBO J. / Identification of a set of genes expressed during the G0/G1 transition of cultured mouse cells. (1985)
  60. 10.1073/pnas.84.5.1182
  61. 10.1016/0092-8674(87)90612-X
  62. 10.1038/325368a0
  63. {'key': '2021111320044364000_4.4.477.63', 'first-page': '3156', 'article-title': 'The detection and characterization of messenger RNAs regulated by nerve growth factor in PC12 cells.', 'volume': '7', 'year': '1987', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / The detection and characterization of messenger RNAs regulated by nerve growth factor in PC12 cells. (1987)
  64. 10.1083/jcb.106.1.181
  65. {'key': '2021111320044364000_4.4.477.65', 'first-page': '217', 'article-title': 'The nerve growth factor: Its mode of action on sensory and sympathetic nerve cells.', 'volume': '60', 'year': '1966', 'journal-title': 'Harvey Lect.'} / Harvey Lect. / The nerve growth factor: Its mode of action on sensory and sympathetic nerve cells. (1966)
  66. {'key': '2021111320044364000_4.4.477.66', 'first-page': '534', 'article-title': 'Nerve growth factor.', 'volume': '49', 'year': '1968', 'journal-title': 'Physiol. Rev.'} / Physiol. Rev. / Nerve growth factor. (1968)
  67. {'key': '2021111320044364000_4.4.477.67', 'first-page': '3332', 'article-title': 'Regulated expression of the tyrosine hydroxylase gene by epidermal growth factor.', 'volume': '7', 'year': '1987', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Regulated expression of the tyrosine hydroxylase gene by epidermal growth factor. (1987)
  68. 10.1073/pnas.84.11.3550
  69. 10.1016/0092-8674(80)90138-5
  70. {'key': '2021111320044364000_4.4.477.70', 'first-page': '1529', 'article-title': 'Anomalous placement of introns in a number of the intermediate filament multigene family: An evolutionary conundrum.', 'volume': '6', 'year': '1986', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Anomalous placement of introns in a number of the intermediate filament multigene family: An evolutionary conundrum. (1986)
  71. 10.1038/317632a0
  72. {'key': '2021111320044364000_4.4.477.72', 'first-page': '263', 'article-title': 'Cloning of tetradecanoyl phorbol ester-induced primary response sequences and their expression in density-arrested Swiss 3T3 cells and a TPA non-proliferative variant.', 'volume': '1', 'year': '1987', 'journal-title': 'Oncogene'} / Oncogene / Cloning of tetradecanoyl phorbol ester-induced primary response sequences and their expression in density-arrested Swiss 3T3 cells and a TPA non-proliferative variant. (1987)
  73. 10.1016/0306-4522(77)90132-4
  74. 10.1073/pnas.84.9.2848
  75. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
  76. 10.1101/SQB.1988.053.01.083
  77. 10.1073/pnas.83.13.4789
  78. 10.1126/science.3672127
  79. 10.1016/0896-6273(88)90138-9
  80. {'key': '2021111320044364000_4.4.477.80', 'first-page': '74', 'article-title': 'Increase in tyrosine hydroxylase activity after reserpine administration.', 'volume': '169', 'year': '1969', 'journal-title': 'J. Pharmocol. Exp. Ther.'} / J. Pharmocol. Exp. Ther. / Increase in tyrosine hydroxylase activity after reserpine administration. (1969)
  81. 10.1038/312716a0
  82. 10.1016/0092-8674(88)90146-8
  83. 10.1016/0012-1606(82)90182-8
  84. 10.1016/0896-6273(88)90189-4
  85. 10.1101/gad.3.7.921
  86. {'key': '2021111320044364000_4.4.477.86', 'first-page': '215', 'article-title': 'Regulation of peripherin in mouse neuroblastoma and rat PC12 cell lines.', 'volume': '6', 'year': '1984', 'journal-title': 'Dev. Neurosci.'} / Dev. Neurosci. / Regulation of peripherin in mouse neuroblastoma and rat PC12 cell lines. (1984)
  87. 10.1073/pnas.81.22.7161
  88. 10.1016/0092-8674(83)90016-8
  89. 10.1073/pnas.80.14.4218
  90. 10.1101/gad.2.12b.1687
  91. 10.1126/science.3130660
  92. 10.1016/S0092-8674(88)80039-4
  93. 10.1016/0006-8993(78)90554-1
  94. 10.1073/pnas.85.5.1487
  95. 10.1073/pnas.86.5.1500
  96. 10.1016/0022-2836(80)90196-5
  97. 10.1016/0092-8674(88)90077-3
  98. 10.1038/334629a0
  99. 10.1038/336692a0
  100. 10.1016/0092-8674(88)90195-X
  101. 10.1016/0006-8993(80)91160-9
  102. 10.1073/pnas.83.10.3213
  103. 10.1016/0092-8674(84)90424-0
  104. {'key': '2021111320044364000_4.4.477.104', 'first-page': '343', 'article-title': 'A novel early growth response gene rapidly induced by fibroblast, epithelial cell and lymphocyte mitogens.', 'volume': '1', 'year': '1987', 'journal-title': 'Oncogene Res.'} / Oncogene Res. / A novel early growth response gene rapidly induced by fibroblast, epithelial cell and lymphocyte mitogens. (1987)
  105. 10.1016/0092-8674(88)90485-0
  106. {'key': '2021111320044364000_4.4.477.106', 'first-page': '497', 'article-title': 'Indiction of mRNA for tyrosine hydroxylase by cyclic AMP and glucocorticoids in a rat pheochromocytoma cell line: Evidence for the migration of tyrosine hydroxylase synthesis by multiple mechanisms in cells exposed to elevated levels of both inducing agents.', 'volume': '30', 'year': '1986', 'journal-title': 'Mol. Pharmacol.'} / Mol. Pharmacol. / Indiction of mRNA for tyrosine hydroxylase by cyclic AMP and glucocorticoids in a rat pheochromocytoma cell line: Evidence for the migration of tyrosine hydroxylase synthesis by multiple mechanisms in cells exposed to elevated levels of both inducing agents. (1986)
  107. 10.1038/228861a0
  108. 10.1016/0896-6273(89)90228-6
  109. 10.1073/pnas.86.6.2088
  110. 10.1073/pnas.76.9.4350
  111. 10.1016/0092-8674(85)90285-5
  112. 10.1126/science.2494701
  113. 10.1073/pnas.75.7.3498
  114. 10.1002/jcp.1041380308
  115. 10.1073/pnas.77.1.92
  116. {'key': '2021111320044364000_4.4.477.116', 'first-page': '4213', 'article-title': 'The NGF I-B gene, a transcriptionally inducible member of the steroid receptor gene superfamily: Genomic structure and expression in rat brain after seizure induction.', 'volume': '9', 'year': '1989', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / The NGF I-B gene, a transcriptionally inducible member of the steroid receptor gene superfamily: Genomic structure and expression in rat brain after seizure induction. (1989)
  117. 10.1002/j.1460-2075.1989.tb03441.x / EMBO J. / The product of a novel growth factor activated gene, fosB, interacts with jun proteins enhancing their DNA binding activity. (1989)
Dates
Type When
Created 18 years, 2 months ago (June 5, 2007, 5:15 p.m.)
Deposited 3 years, 9 months ago (Nov. 13, 2021, 11:08 p.m.)
Indexed 1 month, 1 week ago (July 20, 2025, 6:55 p.m.)
Issued 35 years, 4 months ago (April 1, 1990)
Published 35 years, 4 months ago (April 1, 1990)
Published Online 35 years, 4 months ago (April 1, 1990)
Published Print 35 years, 4 months ago (April 1, 1990)
Funders 0

None

@article{Gizang_Ginsberg_1990, title={Nerve growth factor regulates tyrosine hydroxylase gene transcription through a nucleoprotein complex that contains c-Fos.}, volume={4}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.4.4.477}, DOI={10.1101/gad.4.4.477}, number={4}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Gizang-Ginsberg, E and Ziff, E B}, year={1990}, month=apr, pages={477–491} }