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. 1987 Mar 11;15(5):2363–2384. doi: 10.1093/nar/15.5.2363

Identification and cell type specificity of the tyrosine hydroxylase gene promoter.

C A Harrington, E J Lewis, D Krzemien, D M Chikaraishi
PMCID: PMC340639  PMID: 2882469

Abstract

Genomic DNA encoding the rat tyrosine hydroxylase (TH) gene was isolated from a lambda phage library using a nick-translated fragment from a cDNA clone for rat TH. We have determined the initiation site for TH RNA synthesis and have sequenced 1100 bases of the primary transcript and 5' flanking region. The 5' end of the transcript is the same in several rat tissues in which TH is expressed as well as in rat pheochromocytoma cells (PC). RNA prepared from PC cells that had been stimulated with dexamethasone also mapped to the same transcription start site. Sequence upstream from the initiation site contains the canonical TATA box, but no apparent CAAT box. When a portion of the 5' flanking region of the TH gene (-773 to + 27) is fused to the chloramphenicol acetyltransferase (CAT) gene, it promotes expression of CAT in pheochromocytoma cells and GH4 cells, but not in two neural tumour lines, RT4-D and B103, nor in several non neural cell lines. This suggests that this region of the TH gene has features that confer tissue-restricted expression on the TH promoter.

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Selected References

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  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. Auffray C., Rougeon F. Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem. 1980 Jun;107(2):303–314. doi: 10.1111/j.1432-1033.1980.tb06030.x. [DOI] [PubMed] [Google Scholar]
  3. Barta A., Richards R. I., Baxter J. D., Shine J. Primary structure and evolution of rat growth hormone gene. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4867–4871. doi: 10.1073/pnas.78.8.4867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beale E. G., Chrapkiewicz N. B., Scoble H. A., Metz R. J., Quick D. P., Noble R. L., Donelson J. E., Biemann K., Granner D. K. Rat hepatic cytosolic phosphoenolpyruvate carboxykinase (GTP). Structures of the protein, messenger RNA, and gene. J Biol Chem. 1985 Sep 5;260(19):10748–10760. [PubMed] [Google Scholar]
  5. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  6. Benyajati C., Spoerel N., Haymerle H., Ashburner M. The messenger RNA for alcohol dehydrogenase in Drosophila melanogaster differs in its 5' end in different developmental stages. Cell. 1983 May;33(1):125–133. doi: 10.1016/0092-8674(83)90341-0. [DOI] [PubMed] [Google Scholar]
  7. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Black I. B., Chikaraishi D. M., Lewis E. J. Trans-synaptic increase in RNA coding for tyrosine hydroxylase in a rat sympathetic ganglion. Brain Res. 1985 Jul 22;339(1):151–153. doi: 10.1016/0006-8993(85)90635-3. [DOI] [PubMed] [Google Scholar]
  9. Black I. B., Hendry I. A., Iversen L. L. Trans-synaptic regulation of growth and development of adrenergic neurones in a mouse sympathetic ganglion. Brain Res. 1971 Nov;34(2):229–240. doi: 10.1016/0006-8993(71)90278-2. [DOI] [PubMed] [Google Scholar]
  10. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  11. Brilliant M. H., Sueoka N., Chikaraishi D. M. Cloning of DNA corresponding to rare transcripts of rat brain: evidence of transcriptional and post-transcriptional control and of the existence of nonpolyadenylated transcripts. Mol Cell Biol. 1984 Oct;4(10):2187–2197. doi: 10.1128/mcb.4.10.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Camper S. A., Yao Y. A., Rottman F. M. Hormonal regulation of the bovine prolactin promoter in rat pituitary tumor cells. J Biol Chem. 1985 Oct 5;260(22):12246–12251. [PubMed] [Google Scholar]
  13. Chikaraishi D. M., Brilliant M. H., Lewis E. J. Cloning and characterization of rat-brain-specific transcripts: rare, brain-specific transcripts and tyrosine hydroxylase. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 1):309–318. doi: 10.1101/sqb.1983.048.01.034. [DOI] [PubMed] [Google Scholar]
  14. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  15. Cooke N. E., Baxter J. D. Structural analysis of the prolactin gene suggests a separate origin for its 5' end. Nature. 1982 Jun 17;297(5867):603–606. doi: 10.1038/297603a0. [DOI] [PubMed] [Google Scholar]
  16. Dierks P., van Ooyen A., Cochran M. D., Dobkin C., Reiser J., Weissmann C. Three regions upstream from the cap site are required for efficient and accurate transcription of the rabbit beta-globin gene in mouse 3T6 cells. Cell. 1983 Mar;32(3):695–706. doi: 10.1016/0092-8674(83)90055-7. [DOI] [PubMed] [Google Scholar]
  17. Dynan W. S., Tjian R. The promoter-specific transcription factor Sp1 binds to upstream sequences in the SV40 early promoter. Cell. 1983 Nov;35(1):79–87. doi: 10.1016/0092-8674(83)90210-6. [DOI] [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. Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
  20. Everett R. D., Baty D., Chambon P. The repeated GC-rich motifs upstream from the TATA box are important elements of the SV40 early promoter. Nucleic Acids Res. 1983 Apr 25;11(8):2447–2464. doi: 10.1093/nar/11.8.2447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Glanville N., Durnam D. M., Palmiter R. D. Structure of mouse metallothionein-I gene and its mRNA. Nature. 1981 Jul 16;292(5820):267–269. doi: 10.1038/292267a0. [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. Goodman R., Slater E., Herschman H. R. Epidermal growth factor induces tyrosine hydroxylase in a clonal pheochromocytoma cell line, PC-G2. J Cell Biol. 1980 Mar;84(3):495–500. doi: 10.1083/jcb.84.3.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gorman C. M., Merlino G. T., Willingham M. C., Pastan I., Howard B. H. The Rous sarcoma virus long terminal repeat is a strong promoter when introduced into a variety of eukaryotic cells by DNA-mediated transfection. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6777–6781. doi: 10.1073/pnas.79.22.6777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Grima B., Lamouroux A., Blanot F., Biguet N. F., Mallet J. Complete coding sequence of rat tyrosine hydroxylase mRNA. Proc Natl Acad Sci U S A. 1985 Jan;82(2):617–621. doi: 10.1073/pnas.82.2.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hanbauer I., Guidotti A., Costa E. Dexamethasone induces tyrosine hydroxylase in sympathetic ganglia but not in adrenal medulla. Brain Res. 1975 Mar 7;85(3):527–531. doi: 10.1016/0006-8993(75)90826-4. [DOI] [PubMed] [Google Scholar]
  30. Harrington C. A., Chikaraishi D. M. Identification and sequence of the initiation site for rat 45S ribosomal RNA synthesis. Nucleic Acids Res. 1983 May 25;11(10):3317–3332. doi: 10.1093/nar/11.10.3317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Imada M., Sueoka N. Clonal sublines of rat neurotumor RT4 and cell differentiation. I. Isolation and characterization of cell lines and cell type conversion. Dev Biol. 1978 Sep;66(1):97–108. doi: 10.1016/0012-1606(78)90276-2. [DOI] [PubMed] [Google Scholar]
  33. Kao F. T., Hartz J. A., Law M. L., Davidson J. N. Isolation and chromosomal localization of unique DNA sequences from a human genomic library. Proc Natl Acad Sci U S A. 1982 Feb;79(3):865–869. doi: 10.1073/pnas.79.3.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kiino D. R., Dannies P. S. Insulin and 17 beta-estradiol increase the intracellular prolactin content of GH4C1 cells. Endocrinology. 1981 Oct;109(4):1264–1269. doi: 10.1210/endo-109-4-1264. [DOI] [PubMed] [Google Scholar]
  35. Koontz J. W., Iwahashi M. Insulin as a potent, specific growth factor in a rat hepatoma cell line. Science. 1981 Feb 27;211(4485):947–949. doi: 10.1126/science.7008195. [DOI] [PubMed] [Google Scholar]
  36. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kozak M. Point mutations close to the AUG initiator codon affect the efficiency of translation of rat preproinsulin in vivo. Nature. 1984 Mar 15;308(5956):241–246. doi: 10.1038/308241a0. [DOI] [PubMed] [Google Scholar]
  38. Kumakura K., Guidotti A., Costa E. Primary cultures of chromaffin cells: molecular mechanisms for the induction of tyrosine hydroxylase mediated by 8-Br-cyclic AMP. Mol Pharmacol. 1979 Nov;16(3):865–876. [PubMed] [Google Scholar]
  39. 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]
  40. Mallet J., Faucon Biguet N., Buda M., Lamouroux A., Samolyk D. Detection and regulation of the tyrosine hydroxylase mRNA levels in rat adrenal medulla and brain tissues. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 1):305–308. doi: 10.1101/sqb.1983.048.01.033. [DOI] [PubMed] [Google Scholar]
  41. Maxwell I. H., Maxwell F., Hahn W. E. Removal of RNase activity from DNase by affinity chromatography on agarose coupled aminophenylphosphoryl-uridine-2' (3')-phosphate. Nucleic Acids Res. 1977 Jan;4(1):241–246. doi: 10.1093/nar/4.1.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. McKnight G. S., Palmiter R. D. Transcriptional regulation of the ovalbumin and conalbumin genes by steroid hormones in chick oviduct. J Biol Chem. 1979 Sep 25;254(18):9050–9058. [PubMed] [Google Scholar]
  43. McKnight S. L., Kingsbury R. C., Spence A., Smith M. The distal transcription signals of the herpesvirus tk gene share a common hexanucleotide control sequence. Cell. 1984 May;37(1):253–262. doi: 10.1016/0092-8674(84)90321-0. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Melton D. W., Konecki D. S., Brennand J., Caskey C. T. Structure, expression, and mutation of the hypoxanthine phosphoribosyltransferase gene. Proc Natl Acad Sci U S A. 1984 Apr;81(7):2147–2151. doi: 10.1073/pnas.81.7.2147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Montminy M. R., Goodman R. H., Horovitch S. J., Habener J. F. Primary structure of the gene encoding rat preprosomatostatin. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3337–3340. doi: 10.1073/pnas.81.11.3337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Montminy M. R., Sevarino K. A., Wagner J. A., Mandel G., Goodman R. H. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6682–6686. doi: 10.1073/pnas.83.18.6682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Mueller R. A., Thoenen H., Axelrod J. Increase in tyrosine hydroxylase activity after reserpine administration. J Pharmacol Exp Ther. 1969 Sep;169(1):74–79. [PubMed] [Google Scholar]
  49. Myers R. M., Larin Z., Maniatis T. Detection of single base substitutions by ribonuclease cleavage at mismatches in RNA:DNA duplexes. Science. 1985 Dec 13;230(4731):1242–1246. doi: 10.1126/science.4071043. [DOI] [PubMed] [Google Scholar]
  50. Naujoks K. W., Korsching S., Rohrer H., Thoenen H. Nerve growth factor-mediated induction of tyrosine hydroxylase and of neurite outgrowth in cultures of bovine adrenal chromaffin cells: dependence on developmental stage. Dev Biol. 1982 Aug;92(2):365–379. doi: 10.1016/0012-1606(82)90182-8. [DOI] [PubMed] [Google Scholar]
  51. Otten U., Thoenen H. Circadian rhythm of tyrosine hydroxylase induction by short-term cold stress: modulatory action of glucocorticoids in newborn and adult rats. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1415–1419. doi: 10.1073/pnas.72.4.1415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Schibler U., Hagenbüchle O., Wellauer P. K., Pittet A. C. Two promoters of different strengths control the transcription of the mouse alpha-amylase gene Amy-1a in the parotid gland and the liver. Cell. 1983 Jun;33(2):501–508. doi: 10.1016/0092-8674(83)90431-2. [DOI] [PubMed] [Google Scholar]
  53. Schubert D., Heinemann S., Carlisle W., Tarikas H., Kimes B., Patrick J., Steinbach J. H., Culp W., Brandt B. L. Clonal cell lines from the rat central nervous system. Nature. 1974 May 17;249(454):224–227. doi: 10.1038/249224a0. [DOI] [PubMed] [Google Scholar]
  54. Seif R., Cuzin F. Temperature-sensitive growth regulation in one type of transformed rat cells induced by the tsa mutant of polyoma virus. J Virol. 1977 Dec;24(3):721–728. doi: 10.1128/jvi.24.3.721-728.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Singh L., Jones K. W. The use of heparin as a simple cost-effective means of controlling background in nucleic acid hybridization procedures. Nucleic Acids Res. 1984 Jul 25;12(14):5627–5638. doi: 10.1093/nar/12.14.5627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Stachowiak M., Sebbane R., Stricker E. M., Zigmond M. J., Kaplan B. B. Effect of chronic cold exposure on tyrosine hydroxylase mRNA in rat adrenal gland. Brain Res. 1985 Dec 16;359(1-2):356–359. doi: 10.1016/0006-8993(85)91450-7. [DOI] [PubMed] [Google Scholar]
  57. Tank A. W., Lewis E. J., Chikaraishi D. M., Weiner N. Elevation of RNA coding for tyrosine hydroxylase in rat adrenal gland by reserpine treatment and exposure to cold. J Neurochem. 1985 Oct;45(4):1030–1033. doi: 10.1111/j.1471-4159.1985.tb05519.x. [DOI] [PubMed] [Google Scholar]
  58. Thoenen H., Barde Y. A. Physiology of nerve growth factor. Physiol Rev. 1980 Oct;60(4):1284–1335. doi: 10.1152/physrev.1980.60.4.1284. [DOI] [PubMed] [Google Scholar]
  59. Thoenen H., Mueller R. A., Axelrod J. Increased tyrosine hydroxylase activity after drug-induced alteration of sympathetic transmission. Nature. 1969 Mar 29;221(5187):1264–1264. doi: 10.1038/2211264a0. [DOI] [PubMed] [Google Scholar]
  60. Tischler A. S., Perlman R. L., Nunnemacher G., Morse G. M., DeLellis R. A., Wolfe H. J., Sheard B. E. Long-term effects of dexamethasone and nerve growth factor on adrenal medullary cells cultured from young adult rats. Cell Tissue Res. 1982;225(3):525–542. doi: 10.1007/BF00214802. [DOI] [PubMed] [Google Scholar]
  61. VOLKIN E., COHN W. E. On the structure of ribonucleic acids. II. The products of ribonuclease action. J Biol Chem. 1953 Dec;205(2):767–782. [PubMed] [Google Scholar]
  62. Warren S., Chute R. N. Pheochromocytoma. Cancer. 1972 Feb;29(2):327–331. doi: 10.1002/1097-0142(197202)29:2<327::aid-cncr2820290210>3.0.co;2-3. [DOI] [PubMed] [Google Scholar]
  63. Young R. A., Hagenbüchle O., Schibler U. A single mouse alpha-amylase gene specifies two different tissue-specific mRNAs. Cell. 1981 Feb;23(2):451–458. doi: 10.1016/0092-8674(81)90140-9. [DOI] [PubMed] [Google Scholar]

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