Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1995 Sep;15(9):5123–5130. doi: 10.1128/mcb.15.9.5123

A Drosophila CREB/CREM homolog encodes multiple isoforms, including a cyclic AMP-dependent protein kinase-responsive transcriptional activator and antagonist.

J C Yin 1, J S Wallach 1, E L Wilder 1, J Klingensmith 1, D Dang 1, N Perrimon 1, H Zhou 1, T Tully 1, W G Quinn 1
PMCID: PMC230759  PMID: 7651429

Abstract

We have characterized a Drosophila gene that is a highly conserved homolog of the mammalian cyclic AMP (cAMP)-responsive transcription factors CREB and CREM. Uniquely among Drosophila genes characterized to date, it codes for a cAMP-responsive transcriptional activator. An alternatively spliced product of the same gene is a specific antagonist of cAMP-inducible transcription. Analysis of the splicing pattern of the gene suggests that the gene may be the predecessor of the mammalian CREB and CREM genes.

Full Text

The Full Text of this article is available as a PDF (415.2 KB).

Selected References

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

  1. Abel T., Bhatt R., Maniatis T. A Drosophila CREB/ATF transcriptional activator binds to both fat body- and liver-specific regulatory elements. Genes Dev. 1992 Mar;6(3):466–480. doi: 10.1101/gad.6.3.466. [DOI] [PubMed] [Google Scholar]
  2. Alberini C. M., Ghirardi M., Metz R., Kandel E. R. C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell. 1994 Mar 25;76(6):1099–1114. doi: 10.1016/0092-8674(94)90386-7. [DOI] [PubMed] [Google Scholar]
  3. Alberts A. S., Arias J., Hagiwara M., Montminy M. R., Feramisco J. R. Recombinant cyclic AMP response element binding protein (CREB) phosphorylated on Ser-133 is transcriptionally active upon its introduction into fibroblast nuclei. J Biol Chem. 1994 Mar 11;269(10):7623–7630. [PubMed] [Google Scholar]
  4. Bacskai B. J., Hochner B., Mahaut-Smith M., Adams S. R., Kaang B. K., Kandel E. R., Tsien R. Y. Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science. 1993 Apr 9;260(5105):222–226. doi: 10.1126/science.7682336. [DOI] [PubMed] [Google Scholar]
  5. Basler K., Struhl G. Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature. 1994 Mar 17;368(6468):208–214. doi: 10.1038/368208a0. [DOI] [PubMed] [Google Scholar]
  6. Buratowski S., Sopta M., Greenblatt J., Sharp P. A. RNA polymerase II-associated proteins are required for a DNA conformation change in the transcription initiation complex. Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7509–7513. doi: 10.1073/pnas.88.17.7509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Busch S. J., Sassone-Corsi P. Dimers, leucine zippers and DNA-binding domains. Trends Genet. 1990 Feb;6(2):36–40. doi: 10.1016/0168-9525(90)90071-d. [DOI] [PubMed] [Google Scholar]
  8. Büchler W., Walter U., Jastorff B., Lohmann S. M. Catalytic subunit of cAMP-dependent protein kinase is essential for cAMP-mediated mammalian gene expression. FEBS Lett. 1988 Feb 8;228(1):27–32. doi: 10.1016/0014-5793(88)80577-5. [DOI] [PubMed] [Google Scholar]
  9. Chrivia J. C., Kwok R. P., Lamb N., Hagiwara M., Montminy M. R., Goodman R. H. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature. 1993 Oct 28;365(6449):855–859. doi: 10.1038/365855a0. [DOI] [PubMed] [Google Scholar]
  10. Darrow A. L., Rickles R. J., Strickland S. Maintenance and use of F9 teratocarcinoma cells. Methods Enzymol. 1990;190:110–117. doi: 10.1016/0076-6879(90)90015-s. [DOI] [PubMed] [Google Scholar]
  11. Dash P. K., Hochner B., Kandel E. R. Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation. Nature. 1990 Jun 21;345(6277):718–721. doi: 10.1038/345718a0. [DOI] [PubMed] [Google Scholar]
  12. Delmas V., Laoide B. M., Masquilier D., de Groot R. P., Foulkes N. S., Sassone-Corsi P. Alternative usage of initiation codons in mRNA encoding the cAMP-responsive-element modulator generates regulators with opposite functions. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4226–4230. doi: 10.1073/pnas.89.10.4226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Deutsch P. J., Hoeffler J. P., Jameson J. L., Lin J. C., Habener J. F. Structural determinants for transcriptional activation by cAMP-responsive DNA elements. J Biol Chem. 1988 Dec 5;263(34):18466–18472. [PubMed] [Google Scholar]
  14. Drain P., Folkers E., Quinn W. G. cAMP-dependent protein kinase and the disruption of learning in transgenic flies. Neuron. 1991 Jan;6(1):71–82. doi: 10.1016/0896-6273(91)90123-h. [DOI] [PubMed] [Google Scholar]
  15. Dwarki V. J., Montminy M., Verma I. M. Both the basic region and the 'leucine zipper' domain of the cyclic AMP response element binding (CREB) protein are essential for transcriptional activation. EMBO J. 1990 Jan;9(1):225–232. doi: 10.1002/j.1460-2075.1990.tb08099.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eberl D. F., Perkins L. A., Engelstein M., Hilliker A. J., Perrimon N. Genetic and developmental analysis of polytene section 17 of the X chromosome of Drosophila melanogaster. Genetics. 1992 Mar;130(3):569–583. doi: 10.1093/genetics/130.3.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Echelard Y., Epstein D. J., St-Jacques B., Shen L., Mohler J., McMahon J. A., McMahon A. P. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell. 1993 Dec 31;75(7):1417–1430. doi: 10.1016/0092-8674(93)90627-3. [DOI] [PubMed] [Google Scholar]
  18. Edery I., Rutila J. E., Rosbash M. Phase shifting of the circadian clock by induction of the Drosophila period protein. Science. 1994 Jan 14;263(5144):237–240. doi: 10.1126/science.8284676. [DOI] [PubMed] [Google Scholar]
  19. Edlund T., Walker M. D., Barr P. J., Rutter W. J. Cell-specific expression of the rat insulin gene: evidence for role of two distinct 5' flanking elements. Science. 1985 Nov 22;230(4728):912–916. doi: 10.1126/science.3904002. [DOI] [PubMed] [Google Scholar]
  20. Fantozzi D. A., Harootunian A. T., Wen W., Taylor S. S., Feramisco J. R., Tsien R. Y., Meinkoth J. L. Thermostable inhibitor of cAMP-dependent protein kinase enhances the rate of export of the kinase catalytic subunit from the nucleus. J Biol Chem. 1994 Jan 28;269(4):2676–2686. [PubMed] [Google Scholar]
  21. Foulkes N. S., Borrelli E., Sassone-Corsi P. CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell. 1991 Feb 22;64(4):739–749. doi: 10.1016/0092-8674(91)90503-q. [DOI] [PubMed] [Google Scholar]
  22. Foulkes N. S., Mellström B., Benusiglio E., Sassone-Corsi P. Developmental switch of CREM function during spermatogenesis: from antagonist to activator. Nature. 1992 Jan 2;355(6355):80–84. doi: 10.1038/355080a0. [DOI] [PubMed] [Google Scholar]
  23. Foulkes N. S., Sassone-Corsi P. More is better: activators and repressors from the same gene. Cell. 1992 Feb 7;68(3):411–414. doi: 10.1016/0092-8674(92)90178-f. [DOI] [PubMed] [Google Scholar]
  24. Ginty D. D., Kornhauser J. M., Thompson M. A., Bading H., Mayo K. E., Takahashi J. S., Greenberg M. E. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science. 1993 Apr 9;260(5105):238–241. doi: 10.1126/science.8097062. [DOI] [PubMed] [Google Scholar]
  25. Gonzalez G. A., Menzel P., Leonard J., Fischer W. H., Montminy M. R. Characterization of motifs which are critical for activity of the cyclic AMP-responsive transcription factor CREB. Mol Cell Biol. 1991 Mar;11(3):1306–1312. doi: 10.1128/mcb.11.3.1306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gonzalez G. A., Montminy M. R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell. 1989 Nov 17;59(4):675–680. doi: 10.1016/0092-8674(89)90013-5. [DOI] [PubMed] [Google Scholar]
  27. Gonzalez G. A., Yamamoto K. K., Fischer W. H., Karr D., Menzel P., Biggs W., 3rd, Vale W. W., Montminy M. R. A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature. 1989 Feb 23;337(6209):749–752. doi: 10.1038/337749a0. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Hagiwara M., Brindle P., Harootunian A., Armstrong R., Rivier J., Vale W., Tsien R., Montminy M. R. Coupling of hormonal stimulation and transcription via the cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol Cell Biol. 1993 Aug;13(8):4852–4859. doi: 10.1128/mcb.13.8.4852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hai T. W., Liu F., Coukos W. J., Green M. R. Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev. 1989 Dec;3(12B):2083–2090. doi: 10.1101/gad.3.12b.2083. [DOI] [PubMed] [Google Scholar]
  31. Harootunian A. T., Adams S. R., Wen W., Meinkoth J. L., Taylor S. S., Tsien R. Y. Movement of the free catalytic subunit of cAMP-dependent protein kinase into and out of the nucleus can be explained by diffusion. Mol Biol Cell. 1993 Oct;4(10):993–1002. doi: 10.1091/mbc.4.10.993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Heemskerk J., DiNardo S. Drosophila hedgehog acts as a morphogen in cellular patterning. Cell. 1994 Feb 11;76(3):449–460. doi: 10.1016/0092-8674(94)90110-4. [DOI] [PubMed] [Google Scholar]
  33. Hoeffler J. P., Meyer T. E., Yun Y., Jameson J. L., Habener J. F. Cyclic AMP-responsive DNA-binding protein: structure based on a cloned placental cDNA. Science. 1988 Dec 9;242(4884):1430–1433. doi: 10.1126/science.2974179. [DOI] [PubMed] [Google Scholar]
  34. Hummler E., Cole T. J., Blendy J. A., Ganss R., Aguzzi A., Schmid W., Beermann F., Schütz G. Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors. Proc Natl Acad Sci U S A. 1994 Jun 7;91(12):5647–5651. doi: 10.1073/pnas.91.12.5647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kim K. S., Lee M. K., Carroll J., Joh T. H. Both the basal and inducible transcription of the tyrosine hydroxylase gene are dependent upon a cAMP response element. J Biol Chem. 1993 Jul 25;268(21):15689–15695. [PubMed] [Google Scholar]
  36. Knepel W., Chafitz J., Habener J. F. Transcriptional activation of the rat glucagon gene by the cyclic AMP-responsive element in pancreatic islet cells. Mol Cell Biol. 1990 Dec;10(12):6799–6804. doi: 10.1128/mcb.10.12.6799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Landschulz W. H., Johnson P. F., McKnight S. L. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 1988 Jun 24;240(4860):1759–1764. doi: 10.1126/science.3289117. [DOI] [PubMed] [Google Scholar]
  38. Lane M. E., Kalderon D. Genetic investigation of cAMP-dependent protein kinase function in Drosophila development. Genes Dev. 1993 Jul;7(7A):1229–1243. doi: 10.1101/gad.7.7a.1229. [DOI] [PubMed] [Google Scholar]
  39. Laoide B. M., Foulkes N. S., Schlotter F., Sassone-Corsi P. The functional versatility of CREM is determined by its modular structure. EMBO J. 1993 Mar;12(3):1179–1191. doi: 10.1002/j.1460-2075.1993.tb05759.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lee C. Q., Yun Y. D., Hoeffler J. P., Habener J. F. Cyclic-AMP-responsive transcriptional activation of CREB-327 involves interdependent phosphorylated subdomains. EMBO J. 1990 Dec;9(13):4455–4465. doi: 10.1002/j.1460-2075.1990.tb07896.x. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted]
  41. Levine J. D., Casey C. I., Kalderon D. D., Jackson F. R. Altered circadian pacemaker functions and cyclic AMP rhythms in the Drosophila learning mutant dunce. Neuron. 1994 Oct;13(4):967–974. doi: 10.1016/0896-6273(94)90262-3. [DOI] [PubMed] [Google Scholar]
  42. Leza M. A., Hearing P. Independent cyclic AMP and E1A induction of adenovirus early region 4 expression. J Virol. 1989 Jul;63(7):3057–3064. doi: 10.1128/jvi.63.7.3057-3064.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Liu F., Thompson M. A., Wagner S., Greenberg M. E., Green M. R. Activating transcription factor-1 can mediate Ca(2+)- and cAMP-inducible transcriptional activation. J Biol Chem. 1993 Mar 25;268(9):6714–6720. [PubMed] [Google Scholar]
  44. Maekawa T., Matsuda S., Fujisawa J., Yoshida M., Ishii S. Cyclic AMP response element-binding protein, CRE-BP1, mediates the E1A-induced but not the Tax-induced trans-activation. Oncogene. 1991 Apr;6(4):627–632. [PubMed] [Google Scholar]
  45. Masquilier D., Foulkes N. S., Mattei M. G., Sassone-Corsi P. Human CREM gene: evolutionary conservation, chromosomal localization, and inducibility of the transcript. Cell Growth Differ. 1993 Nov;4(11):931–937. [PubMed] [Google Scholar]
  46. Masson N., Ellis M., Goodbourn S., Lee K. A. Cyclic AMP response element-binding protein and the catalytic subunit of protein kinase A are present in F9 embryonal carcinoma cells but are unable to activate the somatostatin promoter. Mol Cell Biol. 1992 Mar;12(3):1096–1106. doi: 10.1128/mcb.12.3.1096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Meinkoth J. L., Montminy M. R., Fink J. S., Feramisco J. R. Induction of a cyclic AMP-responsive gene in living cells requires the nuclear factor CREB. Mol Cell Biol. 1991 Mar;11(3):1759–1764. doi: 10.1128/mcb.11.3.1759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Mellon P. L., Clegg C. H., Correll L. A., McKnight G. S. Regulation of transcription by cyclic AMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4887–4891. doi: 10.1073/pnas.86.13.4887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Mohler J., Vani K. Molecular organization and embryonic expression of the hedgehog gene involved in cell-cell communication in segmental patterning of Drosophila. Development. 1992 Aug;115(4):957–971. doi: 10.1242/dev.115.4.957. [DOI] [PubMed] [Google Scholar]
  50. Montminy M. R., Low M. J., Tapia-Arancibia L., Reichlin S., Mandel G., Goodman R. H. Cyclic AMP regulates somatostatin mRNA accumulation in primary diencephalic cultures and in transfected fibroblast cells. J Neurosci. 1986 Apr;6(4):1171–1176. doi: 10.1523/JNEUROSCI.06-04-01171.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. 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]
  52. Nigg E. A., Hilz H., Eppenberger H. M., Dutly F. Rapid and reversible translocation of the catalytic subunit of cAMP-dependent protein kinase type II from the Golgi complex to the nucleus. EMBO J. 1985 Nov;4(11):2801–2806. doi: 10.1002/j.1460-2075.1985.tb04006.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Nighorn A., Healy M. J., Davis R. L. The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron. 1991 Mar;6(3):455–467. doi: 10.1016/0896-6273(91)90253-v. [DOI] [PubMed] [Google Scholar]
  54. Pearson R. B., Kemp B. E. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 1991;200:62–81. doi: 10.1016/0076-6879(91)00127-i. [DOI] [PubMed] [Google Scholar]
  55. Rehfuss R. P., Walton K. M., Loriaux M. M., Goodman R. H. The cAMP-regulated enhancer-binding protein ATF-1 activates transcription in response to cAMP-dependent protein kinase A. J Biol Chem. 1991 Oct 5;266(28):18431–18434. [PubMed] [Google Scholar]
  56. Riabowol K. T., Fink J. S., Gilman M. Z., Walsh D. A., Goodman R. H., Feramisco J. R. The catalytic subunit of cAMP-dependent protein kinase induces expression of genes containing cAMP-responsive enhancer elements. Nature. 1988 Nov 3;336(6194):83–86. doi: 10.1038/336083a0. [DOI] [PubMed] [Google Scholar]
  57. Riabowol K. T., Gilman M. Z., Feramisco J. R. Microinjection of the catalytic subunit of cAMP-dependent protein kinase induces expression of the c-fos gene. Cold Spring Harb Symp Quant Biol. 1988;53(Pt 1):85–90. doi: 10.1101/sqb.1988.053.01.013. [DOI] [PubMed] [Google Scholar]
  58. Riddle R. D., Johnson R. L., Laufer E., Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell. 1993 Dec 31;75(7):1401–1416. doi: 10.1016/0092-8674(93)90626-2. [DOI] [PubMed] [Google Scholar]
  59. Roesler W. J., Vandenbark G. R., Hanson R. W. Cyclic AMP and the induction of eukaryotic gene transcription. J Biol Chem. 1988 Jul 5;263(19):9063–9066. [PubMed] [Google Scholar]
  60. Ruppert S., Cole T. J., Boshart M., Schmid E., Schütz G. Multiple mRNA isoforms of the transcription activator protein CREB: generation by alternative splicing and specific expression in primary spermatocytes. EMBO J. 1992 Apr;11(4):1503–1512. doi: 10.1002/j.1460-2075.1992.tb05195.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Seed B., Sheen J. Y. A simple phase-extraction assay for chloramphenicol acyltransferase activity. Gene. 1988 Jul 30;67(2):271–277. doi: 10.1016/0378-1119(88)90403-9. [DOI] [PubMed] [Google Scholar]
  62. Singh H., LeBowitz J. H., Baldwin A. S., Jr, Sharp P. A. Molecular cloning of an enhancer binding protein: isolation by screening of an expression library with a recognition site DNA. Cell. 1988 Feb 12;52(3):415–423. doi: 10.1016/s0092-8674(88)80034-5. [DOI] [PubMed] [Google Scholar]
  63. Smolik S. M., Rose R. E., Goodman R. H. A cyclic AMP-responsive element-binding transcriptional activator in Drosophila melanogaster, dCREB-A, is a member of the leucine zipper family. Mol Cell Biol. 1992 Sep;12(9):4123–4131. doi: 10.1128/mcb.12.9.4123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Staden R. Computer methods to locate signals in nucleic acid sequences. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):505–519. doi: 10.1093/nar/12.1part2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Stehle J. H., Foulkes N. S., Molina C. A., Simonneaux V., Pévet P., Sassone-Corsi P. Adrenergic signals direct rhythmic expression of transcriptional repressor CREM in the pineal gland. Nature. 1993 Sep 23;365(6444):314–320. doi: 10.1038/365314a0. [DOI] [PubMed] [Google Scholar]
  66. Struthers R. S., Vale W. W., Arias C., Sawchenko P. E., Montminy M. R. Somatotroph hypoplasia and dwarfism in transgenic mice expressing a non-phosphorylatable CREB mutant. Nature. 1991 Apr 18;350(6319):622–624. doi: 10.1038/350622a0. [DOI] [PubMed] [Google Scholar]
  67. Takahashi J. S. Circadian rhythms. ICER is nicer at night (sir!). Curr Biol. 1994 Feb 1;4(2):165–168. doi: 10.1016/s0960-9822(94)00040-0. [DOI] [PubMed] [Google Scholar]
  68. Usui T., Smolik S. M., Goodman R. H. Isolation of Drosophila CREB-B: a novel CRE-binding protein. DNA Cell Biol. 1993 Sep;12(7):589–595. doi: 10.1089/dna.1993.12.589. [DOI] [PubMed] [Google Scholar]
  69. Vinson C. R., Sigler P. B., McKnight S. L. Scissors-grip model for DNA recognition by a family of leucine zipper proteins. Science. 1989 Nov 17;246(4932):911–916. doi: 10.1126/science.2683088. [DOI] [PubMed] [Google Scholar]
  70. Waeber G., Meyer T. E., LeSieur M., Hermann H. L., Gérard N., Habener J. F. Developmental stage-specific expression of cyclic adenosine 3',5'-monophosphate response element-binding protein CREB during spermatogenesis involves alternative exon splicing. Mol Endocrinol. 1991 Oct;5(10):1418–1430. doi: 10.1210/mend-5-10-1418. [DOI] [PubMed] [Google Scholar]
  71. Yin J. C., Del Vecchio M., Zhou H., Tully T. CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell. 1995 Apr 7;81(1):107–115. doi: 10.1016/0092-8674(95)90375-5. [DOI] [PubMed] [Google Scholar]
  72. Yin J. C., Wallach J. S., Del Vecchio M., Wilder E. L., Zhou H., Quinn W. G., Tully T. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell. 1994 Oct 7;79(1):49–58. doi: 10.1016/0092-8674(94)90399-9. [DOI] [PubMed] [Google Scholar]
  73. Young M. W., Jackson F. R., Shin H. S., Bargiello T. A. A biological clock in Drosophila. Cold Spring Harb Symp Quant Biol. 1985;50:865–875. doi: 10.1101/sqb.1985.050.01.104. [DOI] [PubMed] [Google Scholar]
  74. Yun Y. D., Dumoulin M., Habener J. F. DNA-binding and dimerization domains of adenosine 3',5'- cyclic monophosphate-responsive protein CREB reside in the carboxyl-terminal 66 amino acids. Mol Endocrinol. 1990 Jun;4(6):931–939. doi: 10.1210/mend-4-6-931. [DOI] [PubMed] [Google Scholar]
  75. Ziff E. B. Transcription factors: a new family gathers at the cAMP response site. Trends Genet. 1990 Mar;6(3):69–72. doi: 10.1016/0168-9525(90)90081-g. [DOI] [PubMed] [Google Scholar]
  76. de Groot R. P., Sassone-Corsi P. Hormonal control of gene expression: multiplicity and versatility of cyclic adenosine 3',5'-monophosphate-responsive nuclear regulators. Mol Endocrinol. 1993 Feb;7(2):145–153. doi: 10.1210/mend.7.2.8385737. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES