CREM, a master-switch in the nuclear response to cAMP signaling

  • Janet S. Lee
  • Enzo Lalli
  • Denis Masquilier
  • Florence Schlotter
  • Carlos A. Molina
  • Nicholas S. Foulkes
  • Paolo Sassone-Corsi
Part of the Progress in Gene Expression book series (PRGE)


The regulation of gene expression by specific signal transduction pathways is tightly connected to the cell phenotype. The response elicited by a given transduction pathway will vary according to the cell type. The finding that most of the known nuclear oncogenes encode proteins involved in the regulation of gene expression inspired the concept that the aberrant expression of some key genes could cause cellular transformation or altered proliferation (Lewin, 1991). The study, and ultimately the understanding, of these processes will help us, it is hoped, to unravel the profound changes that cause cancer and by the same token the physiology of normal growth.


Pineal Gland Leucine Zipper cAMP Signaling Nuclear Response Luteinizing Hormone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andrisani OM, Hayes TE, Roos B, Dixon JE (1987): Identification of the promoter sequences involved in the cell-specific expression of the rat somatostatin gene. Nucleic Acids Res 15: 5715–5728PubMedGoogle Scholar
  2. Auwerx J, Sassone-Corsi P (1991): IP-1: A dominant inhibitor of fos/jun whose activity is modulated by phosphorylation. Cell 64: 983–993PubMedGoogle Scholar
  3. Axelrod, J (1988): The pineal gland: a neurochemical transducer Science 184: 1 091Google Scholar
  4. Benbrook DM, Jones NC (1990): Heterodimer formation between CREB and Jun proteins. Oncogene 5: 295–302PubMedGoogle Scholar
  5. Berkowitz LA, Riabowol KT, Gilman MZ (1989): Multiple sequence elements of a single functional class are required for cyclic AMP responsiveness of the mouse c-fos promoter. Mol Cell Biol 9: 4272–4281PubMedGoogle Scholar
  6. Berridge M J (1987): Inositol trisphosphate and diacy lglycerol: two interacting second messengers. Ann Rev Biochem 56: 159–193PubMedGoogle Scholar
  7. Biownstein M, Axelrod J (1974): Pineal gland: 24-hour rhythm in norepinephrine turnover. Science 184: 165Google Scholar
  8. Borrelli E, Heyman R, Arias C, Sawchenko P, Evans RM (1989): Transgenic mice with inducible dwarfism. Nature 339: 538–541PubMedGoogle Scholar
  9. Borrelli E, Montmayeur JP, Foulkes NS, Sassone-Corsi P (1992): Signal transduction and gene control: the cAMP pathway. Critical Rev Oncogenesis 3: 321–338Google Scholar
  10. Bravo R, Zerial M, Toschi L, Schurmann M, Muller R, Hirai SI, Yaniv M, Almendral JM, Ryseck RP (1988): Identification of growth factor-inducible genes in mouse fibroblasts. Cold Spring Harbor Symp Quant Biol 53: 901–905PubMedGoogle Scholar
  11. Bullitt E (1989): Induction of c-fos-like protein within the lumbar spinal cord and thalamus of the rat following peripheral stimulation. Brain Res 391–397Google Scholar
  12. Busch SJ, Sassone-Corsi P (1990): Dimers, leucine zippers and DNA binding domains. Trends Genet 6: 36–40PubMedGoogle Scholar
  13. Cambier JC, Newell NK, Justement LB, McGuire JC, Leach KL, Chen ZZ (1987): Ia binding ligand and cAMP stimulates nuclear translocation of PKC in β lymphocytes. Nature 327: 629–632PubMedGoogle Scholar
  14. Carter DA, Murphy D (1990): Regulation of c-fos and c-jun expression in the rat supraoptic nucleus. Mol Cell Neurobiol 10: 435–446Google Scholar
  15. Cattanach BM, Iddon CA, Charlton HM, Chiappa SA, Fink G (1977): Gonadotropin releasing hormone deficiency in a mutant mouse with hypogonadism. Nature 269: 338–340PubMedGoogle Scholar
  16. Cole TJ, Copeland NC, Gilbert DJ, Jenkins NA, Schütz G, Ruppert S (1992): The mouse CREB (cAMP responsive element binding protein) gene: structure, promoter analysis and chromosomal localization. Genomics 13: 974.PubMedGoogle Scholar
  17. Comb M, Birnberg NC, Seasholtz A, Herbert E, Goodman HM (1986): A cyclic-AMP and Phorbol Ester-inducible DNA Element. Nature 323: 353–356PubMedGoogle Scholar
  18. Courey AJ, Tjian R (1989): Analysis of Spl in vivo reveals multiple transcriptional domains, including a novel glutaminę activation motif. Cell 55: 887–898Google Scholar
  19. Craft, CM, Morgan, WW, Reiter RJ (1984): 24 hour changes in catecholamine synthesis in rat and hamster pineal glands. Neuroendocrinology 38: 193Google Scholar
  20. Dash PK, Karl KA, Colicos MA, Prywes R, Kandel ER (1991): cAMP response element-binding protein is activated by Ca2+/calmodulin-as well as cAMP-dependent protein kinase. Proc Natl Acad Sci USA 88: 5061–5065Google Scholar
  21. deGroot RP, Sassone-Corsi P (1993): Hormonal control of gene expression: multiplicity and versatility of cyclic adenosine 3′, 5′-monophosphate-responsive nuclear regulators. Mol Endocrinol 7: 145–153Google Scholar
  22. de Groot RP, den Hertog J, Vandenheede JR, Goris J, Sassone-Corsi P (1993a): Multiple and cooperative phosphorylation events regulate the CREM activator function. EMBO J 12: 3903–3911PubMedGoogle Scholar
  23. de Groot RP, Derua R, Goris J, Sassone-Corsi P (1993b): Phosphorylation and negative regulation of the transcriptional activator CREM by p34cdc2. Mol Endocrinol 7: 1495–1501PubMedGoogle Scholar
  24. Delegeane A, Ferland L, Mellon PL (1987): Tissue specific enhancer of the human glycoprotein hormone a-subunit gene: dependence on cyclic AMP-inducible elements. Mol Cell Biol 7: 3994–4002PubMedGoogle Scholar
  25. Delmas V, Laoide BM, Masquilier D, de Groot RP, Foulkes NS, Sassone-Corsi P (1992): Alternative usage of initiation codons in mRNA encoding the cAMP-responsive-element modulator (CREM) generates regulators with opposite functions. Proc Natl Acad Sci USA 89: 4226–4230PubMedGoogle Scholar
  26. Delmas V, van der Hoorn F, Mellström B, Jégou B, Sassone-Corsi P (1993): Induction of CREM activator proteins in spermatids: down-stream targets and implications for haploid germ cell differentiation. Mol Endocrinol 7: 1502–1514PubMedGoogle Scholar
  27. Deutsch PJ, Hoeffler JP, Jameson JL, Habener JF (1988): Cyclic AMP and phorbol ester-stimulated transcription mediated by similar DNA elements that bind distinct proteins. Proc Natl Acad Sci USA 85: 7922–7926PubMedGoogle Scholar
  28. Flint KJ, Jones NC (1991): Differential regulation of three members of the ATF/CREB family of DNA-binding proteins. Oncogene 6: 2019–2026PubMedGoogle Scholar
  29. Foulkes NS, Sassone-Corsi P (1992): More is better: activators and repressors from the same gene. Cell 68: 411–414PubMedGoogle Scholar
  30. Foulkes NS, Borrelli E, Sassone-Corsi P (1991a): CREM gene: use of alternative DNA binding domains generates multiple antagonists of cAMP-induced transcription. Cell 64: 739–749PubMedGoogle Scholar
  31. Foulkes NS, Laoide BM, Schlotter F, Sassone-Corsi P (1991b): Transcriptional antagonist CREM down-regulates c-fos cAMP-induced expression. Proc Natl Acad Sci USA 88: 5448–5452PubMedGoogle Scholar
  32. Foulkes NS, Mellström B, Benusiglio E, Sassone-Corsi P (1992): Developmental switch of CREM function during spermatogenesis: from antagonist to transcriptional activator. Nature 355: 80–84PubMedGoogle Scholar
  33. Foulkes NS, Schlotter F, Pévet P, Sassone-Corsi P (1993): Pituitary hormone FSH directs the CREM functional switch during spermatogenesis. Nature 362: 264–267PubMedGoogle Scholar
  34. Gilman AG (1987): G Proteins: transducers of receptor-generated signals. Ann Rev Blochem 86: 615–649Google Scholar
  35. Ginty DD, Głowacka D, Bader DS, Hidaka H, Wagner JA (1991): Induction of immediate early genes by Ca2 + influx requires cAMP-dependent protein kinase in PC12 cells. J Biol Chem 266: 17454–17458PubMedGoogle Scholar
  36. Gonzalez GA, Montminy MR (1989): Cyclic AMP stimulates somatostain gene transcription by phosphorylation of CREB at ser 133. Cell 59: 675–680PubMedGoogle Scholar
  37. Gonzalez GA, Menzel P, Leonard J, Fischer WH, Montminy MR (1991): Characterization of motifs which are critical for activity of the cyclic AMP-responsive transcription factor CREB. Mol Cell Biol 11: 1306–1312PubMedGoogle Scholar
  38. Gonzalez GA, Yamamoto KK, Fischer WH, Karr K, Menzel P, Briggs III W, Vale WW, Montminy MR (1989): A cluster of phosphorylation sites on the cAMP-regulated nuclear factor CREB predicted by its sequence. Nature 337: 749–752PubMedGoogle Scholar
  39. Grootegoed JA, Oonk RB, Toebosch AMW, Jansen R (1986): Extracellular factors that contribute to the development of spermatogenic cells. In: Molecular and Cellular Endocrinology of the Testis, Stefanini M, Conti M, Geremia R, Ziparo E, eds. Amsterdam: Excerpta MedicaGoogle Scholar
  40. Habener J (1990): Cyclic AMP response element binding proteins: a cornucopia of transcription factors. Mol Endocrinol 4: 1087–1094PubMedGoogle Scholar
  41. Hagiwara M, Alberts A, Brindle P, Meinkoth J, Feramisco J, Deng T, Karin M, Shenolikar S, Montminy M (1992): Transcriptional attenuation following cAMP induction requires PP-1-mediated dephosphorylation of CREB. Cell 70: 105–113PubMedGoogle Scholar
  42. Hai T-Y, Liu F, Coukos WJ, Green MR (1989): Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA binding heterodimers. Genes Dev 3: 2083–2090PubMedGoogle Scholar
  43. Heidaran MA, Kozak CA, Kistler WS (1989): Nucleotide sequence of the Stp-1 gene coding for rat spermatid nuclear transition protein 1 (TP1): homology with protamine PI and assignment of the mouse Stp-1 gene to chromosome 1. Gene 75: 39–46PubMedGoogle Scholar
  44. Hoeffler JP, Meyer TE, Yun Y, Jameson JL, Habener JF (1988): Cyclic AMP-responsive DNA-binding protein: structure based on a cloned placental cDNA. Science 242: 1430–1433PubMedGoogle Scholar
  45. Hummler E, Cole TJ, Blendy JA, Ganss R, Aguzzi A, Schmid W, Beerman F, Schütz G (1994): Targeted mutation of the CREB gene: Compensation within the CREB/ATF Family of transcription factors. Proc Natl Acad Sci 91: 5647–5651PubMedGoogle Scholar
  46. Illnervoa H, Vanecek J, Wetterberg L, Sääf JJ (1979): Effect of one minute exposure to light at night on rat pineal serotonin N-acetyltransferase and melatonin. Neurochem 32: 673Google Scholar
  47. Jégou B, Syed V, Sourdaine P, Byers S, Gérard N, Velez de la Calle J, Pineau C, Garnier DH, Bauché F (1992): The dialogue between late spermatids and Sertoli cells in vertebrates: a century of research. In: Spermatogenesis. Fertilization. Contraception. Molecular, Cellular and Endocrine Events in Male Reproduction, Nieschlag E, Habenicht U-F, eds. New York: Springer Verlag.Google Scholar
  48. Johnson P, Peschon JJ, Yelick PC, Palmiter RD, Hecht NB (1988): Sequence homologies in the mouse protamine 1 and 2 genes. Biochim Biophys Acta 950: 45–53PubMedGoogle Scholar
  49. Klein DC (1985): Photoneural regulation of the mammalial pineal gland. In: Photoperiodism, Melatonin and the Pineal Gland, London: PitmanGoogle Scholar
  50. Kramer IJM, Koornneef I, de Laat SW, van den Eijnden-van Raaij AJM (1991): TFG-β1 induces phosphorylation of the cyclic AMP responsive element binding protein in ML-CCL64 cells. EM BO J 10: 1083–1089Google Scholar
  51. Krebs EG, Beavo JA (1979): Phosphorylation-dephosphorylation of enzymes. Ann Rev Biochem 48: 923–959PubMedGoogle Scholar
  52. Landschulz WH, Johnson PF, McKnight SL (1988): The leucine-zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240: 1759–1764PubMedGoogle Scholar
  53. Laoide BM, Foulkes NF, Schlotter F, Sassone-Corsi P (1993): The functional versatility of CREM is determined by its modular structure. EM BO J 12: 1179–1191Google Scholar
  54. Lee CQ, Yun Y, Hoeffler JP, Habener JF (1990): Cyclic-AMP-responsive transcriptional activation involves interdependent phosphorylated subdomains. EMBO J 9: 4455–4465PubMedGoogle Scholar
  55. Leff S E, Rosenfeld M G, Evans R M (1986): Complex transcriptional units: diversity in gene expression by alternative RNA processing. Ann Rev Biochem 55: 1091–1117PubMedGoogle Scholar
  56. Leonard J, Serup P, Gonzalez G, Edlund T, Montminy M (1992): The LIM family transcription factor Isl-1 requires cAMP response element binding protein to promote somatostatin expression in pancreatic islet cells. Proc Natl Acad Sci USA 89: 6247–6251PubMedGoogle Scholar
  57. Lewin B (1991): Oncogenic conversion by regulatory changes in transcription factors. Cell 64: 303–312PubMedGoogle Scholar
  58. Lin SC, Morrison-Bogorad M (1991): Cloning and characterization of a testis-specific thymosin β 10 cDNA. J Biol Chem 266: 23347–23353PubMedGoogle Scholar
  59. Lonnerberg P, Parvinen M, Jahnsen T, Hansson V, Persson H (1992): Stage- and cell-specific expression of cyclic adenosine 3′, 5′-monophosphate-dependent protein kinases in rat seminiferous epithelium. Biol Reprod 46: 1057–1068PubMedGoogle Scholar
  60. Lostroh AJ (1976): Hormonal control of spermatogenesis. In: Regulation Mechanisms of Male Reproductive Physiology, Spilman CH, Lobl TJ, Kirton KT, eds. Amsterdam: Excerpta MedicaGoogle Scholar
  61. Maekawa T, Sakura H, Kanei-Ishii C, Sudo T, Yoshimura T, Fujisawa J, Yoshida M, Ishii S (1989): Leucine zipper structure of the protein CRE-BP1 binding to the cyclic AMP response element in brain. EMBO J 8: 2023–2028PubMedGoogle Scholar
  62. Masquilier D, Sassone-Corsi P (1992): Transcriptional cross-talk: nuclear factors CREM and CREB bind to AP-1 sites and inhibit activation by Jun. J Biol Chem 267: 22460–22466PubMedGoogle Scholar
  63. Masquilier D, Foulkes NS, Mattei MG, Sassone-Corsi P (1993): Human CREM gene: Evolutionary conservation, chromosomal localization, and inducibility of the transcript. Cell Growth & Differentiation 4: 931–937Google Scholar
  64. McCormick A, Brady H, Theill L, Karin M (1990): Regulation of the pituitary-specific homeobox gene GHF1 by cell-autonomous and environmental cues. Nature 345: 829–832PubMedGoogle Scholar
  65. McKnight SG, Clegg CH, Uhler MD, Chrivia JC, Cadd GG, Correll LA, Otten AD (1988): Analysis of the cAMP-dependent protein kinase system using molecular genetic approaches. Rec Progr Horm Res 44: 307–335PubMedGoogle Scholar
  66. Meijer GH (1991): In: Suprachiasmatic Nucleus/The Mind’s Clock, Klein DC, Moore RY, Reppert SM, eds. Oxford: Oxford University PressGoogle Scholar
  67. Mellon PL, Clegg CH, Correll LA, McKnight SG (1989): Regulation of transcription by cyclic AMP-dependent protein kinase. Proc Natl Acad Sci USA 86:4887–4891PubMedGoogle Scholar
  68. Mellström B, Naranjo JR, Foulkes NS, Lafarga M, Sassone-Corsi P (1993): Transcriptional response to cAMP in brain: specific distribution and induction of CREM antagonists. Neuron 10: 655–665PubMedGoogle Scholar
  69. Meyer TE, Weaber G, Lin J, Beckman W, Habener JF (1993): The promoter of the gene encoding 3′, 5′-cyclic adenosine monophosphate (cAMP) response element binding protein contains cAMP response elements: evidence for positive auto-regulation of gene transcription. Endocrinology 132: 770PubMedGoogle Scholar
  70. Mizuki N, Sarapata DE, Garcia-Sanz JA, Kasahara M (1992): The mouse male germ cell-specific gene Tpx-1: molecular structure, mode of expression in spermatogenesis, and sequence similarity to two non-mammalian genes. Mammalian Genome 3: 274–280PubMedGoogle Scholar
  71. Molina CA, Foulkes NS, Lalli E, Sassone-Corsi, P (1993): Inducibility and negative autoregulation of CREM: an alternative promoter directs the expression of ICER, and early response repressor. Cell 75: 875–886PubMedGoogle Scholar
  72. Montmayeur JP, Borrelli E (1991): Transcription mediated by a cAMP-responsive promoter element is reduced upon activation of dopamine D2 receptors. Proc Natl Acad Sci USA 88: 3135–3139PubMedGoogle Scholar
  73. Moore RY (1978): Neuroendocrine regulation of reproduction. In: Reproductive Endocrinology, Yen SSC, Jaffe RB, eds. Philadelphia: SandersGoogle Scholar
  74. Morgan JI, Cohen DR, Hempstead JL, Curran T (1987): Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237: 192–197PubMedGoogle Scholar
  75. Nathans D, Lau LF, Christy B, Hartzell S, Nakabeppu Y, Ryder K (1988): Genomic response to growth factors. Cold Spring Harbor Symp Quant Biol 53: 893PubMedGoogle Scholar
  76. Nichols M, Weih F, Schmid W, DeVack C, Kowenz-Leutz E, Luckow B, Boshart M, Schütz G (1992): Phosphorylation of CREB affects its binding to high and low affinity sites: implications for cAMP induced gene transcription. EM BO J 11: 3337–3346Google Scholar
  77. Nishizuka Y (1986): Studies and perspectives of protein kinase C. Science 233: 305–312PubMedGoogle Scholar
  78. Oakberg J (1956): Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 99: 504–516Google Scholar
  79. Oyen O, Scott JD, Cadd GG, McKnight GS, Krebs EB, Hansson V, Jahnsen T (1988): A unique mRNA species for a regulatory subunit of cAMP-dependent protein kinase is specifically induced in haploid germ cells. FEBS Lett 229: 391–394PubMedGoogle Scholar
  80. Oyen O, Myklebust F, Scott JD, Cadd GG, McKnight SG, Hansson V, Jahnsen T (1990): Subunits of cyclic adenosine 3′, 5′-monophosphate-dependent protein kinase show differential and distinct expression patterns during germ cell differentiation: alternative polyadenylation in germ cells gives rise to unique smaller-sized mRNA species. Biol Reprod 43: 46–54PubMedGoogle Scholar
  81. Pariset C, Feinberg J, Dacheux JL, Oyen O, Jahnsen T, Weinman S (1989): Differential expression and subcellular localization for subunits of cAMP-dependent protein kinase during ram spermatogenesis. J Cell Biol 109: 1195–1205PubMedGoogle Scholar
  82. Perlow MJ, Reppert SM, Tamarkin L, Wyatt RJ, Klein DC (1980): Photic regulation of the melatonin rhythm: monkey and man are not the same. Brain Res 182: 211 Rehfuss RP, Walton KM, Loriaux MM, Goodman RH (1991): The cAMP-regulated enhancer-binding protein ATF-1 activates transcription in response to cAMP-dependent protein kinase A. J Biol Chem 266: 18431–18434Google Scholar
  83. Reiter RJ (1991): Pineal gland. Interface between the photoperiodic environment and the endocrine system. Trends Endocr Met 1:13Google Scholar
  84. Roesler WJ, Vanderbark GR, Hanson RW (1988): Cyclic AMP and the induction of eukaryotic gene expression. J Biol Chem 263: 9063–9066PubMedGoogle Scholar
  85. Ruppert S, Cole TJ, Boshart M, Schmid E, Schu\dtz G (1992): Multiple mRNA isoforms of the transcription activator protein CREB: generation by alternative splicing and specific expression in primary spermatocytes. EMBO J 11: 1503–1512PubMedGoogle Scholar
  86. Russell LD (1980): Sertoli-germ cell interrelations: a review. Gamete Res 3: 179–202Google Scholar
  87. Sagar SM, Sharp FR, Curran T (1988): Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240: 1328–1331PubMedGoogle Scholar
  88. Santen RJ (1987): The testis. In: Endocrinology and Metabolism, Felig P, Baxter JD, Broadus AE, Frohman LA, eds. New York: McGraw-HillGoogle Scholar
  89. Sassone-Corsi P (1988): Cyclic AMP induction of early adenovirus promoters involves sequences required for ElA-transactivation. Proc Natl Acad Sci USA 85: 7192–7196PubMedGoogle Scholar
  90. Sassone-Corsi P, Ransone LJ, Verma IM (1990): Cross-talk in signal transduction: TPA-inducible factor Jun/AP-1 activates cAMP responsive enhancer elements. Oncogene 5: 427–431PubMedGoogle Scholar
  91. Sassone-Corsi P, Visvader J, Ferland L, Mellon PL, Verma IM (1988): Induction of proto-oncogene fos transcription through the adenylate cyclase pathway: characterization of a cAMP-responsive element. Genes Dev 2: 1529–1538PubMedGoogle Scholar
  92. Sharp FR, Sagar SM, Hicks K, Lowenstein D, Hisanaga K (1991): c-fos mRNA, Fos and Fos-related antigen induction by hypertonic saline and stress. J Neurosci 11: 2321–2331PubMedGoogle Scholar
  93. Shaw G, Kamen R (1986): A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46: 659–667PubMedGoogle Scholar
  94. Sheng M, McFadden G, Greenberg ME (1990): Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 4: 571–582PubMedGoogle Scholar
  95. Sheng M, Thompson MA, Greenberg ME (1991): CREB: a Ca2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252: 1427–1430PubMedGoogle Scholar
  96. Sherman TG, McKelvy JF, Watson S J (1986): Vasopressin mRNA regulation in individual hypothalamic nuclei: a northern and in situ hybridization analysis. J Neurosci 6: 1685–1694PubMedGoogle Scholar
  97. Stehle JH, Foules NS, Molina CA, Simonneaux V, Pévet P, Sassone-Corsi P (1993): Adrenergic signals direct rhythmic expression of transcriptional repressor CREM in the pineal gland. Nature 365: 314–320PubMedGoogle Scholar
  98. Steinberger E (1971): Hormonal control of mammalian spermatogenesis. Physiol Rev 51: 1–22Google Scholar
  99. Struthers RS, Vale WW, Arias C, Sawchenko PE, Montminy MR (1991): Somatotroph hypoplasia and dwarfism in transgenic mice expressing a non-phosphorylatable CREB mutant. Nature 350: 622–624PubMedGoogle Scholar
  100. Sudgen D, Vanecek J, Klein DC, Thomas TD (1985): Activation of protein kinase C potentiates isoprenaline-induced cyclic AMP accumulation in rat pinealocytes. Nature 314: 359Google Scholar
  101. Takahashi JS (1993): Circadian clocks à la CREM Nature 365: 299PubMedGoogle Scholar
  102. Tamarkin L, Reppert SM, Klein DC (1979): Regulation of pineal melatonin in the Syrian hamster. Endocrinology 104: 385PubMedGoogle Scholar
  103. Tamarkin L, Baird CJ, Almeida OFX (1985): Melatonin: a coordinating signal for mammalian reproduction? Science 227: 774Google Scholar
  104. van der Hoorn FA, Tarnasky HA (1992): Factors involved in regulation of the RT7 promoter in a male germ cell-derived in vitro transcription system. Proc Natl Acad Sci USA 89: 703–707PubMedGoogle Scholar
  105. Vanecek J, Sudgen D, Weiler J, Klein DC (1985): Atypical synergistic al and β-adrenergic regulation of adenosine 3′,5′-Endocrinology 116: 2167Google Scholar
  106. Veldhuis JD (1991): The hypothalamic-pituitary-testicular axis. In: Reproductive Endocrinology Yen SSC, Jaffe RB, eds. Philadelphia: W.B. SaundersGoogle Scholar
  107. Verma IM, Sassone-Corsi P (1987): Proto-oncogene fos: complex but versatile regulation. Cell 51: 513–514PubMedGoogle Scholar
  108. Vinson CR, Sigler P, McKnight SL (1989): Scissor-grip model for DNA recognition by a family of leucine zipper proteins. Science 246: 911–922PubMedGoogle Scholar
  109. Waeber G, Meyer TE, LeSieur M, Hermann HL, Gérard N, Habener JF (1991): Developmental stage-specific expression of cyclic adenosine 3′,5′-monophosphate response element-binding protein CREB during spermatogenesis involves alternative exon splicing. Mol Endocrinol 5: 1418–1430PubMedGoogle Scholar
  110. Williams T, Admon A, Luscher B, Tjian R (1988): Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements. Genes Devi: 1557–1569Google Scholar
  111. Yamamoto KK, Gonzales GA, Briggs III WH, Montminy MR (1988): Phosphorylation-induced binding and transcriptional efficiency of nuclear factor CREB. Nature 334: 494–498PubMedGoogle Scholar
  112. Yoshimasa T, Sibley DR, Bouvier M, Lefkowitz RJ, Caron MG (1987): Cross-talk between cellular signalling pathways suggested by phorbol ester adenylate cyclase phosphorylation. Nature 327: 67–70PubMedGoogle Scholar
  113. Ziff EB (1990): Transcription factors: a new family gathers at the cAMP response site. Trends Genet 6: 69–72PubMedGoogle Scholar

Copyright information

© Birkhäuser Boston 1995

Authors and Affiliations

  • Janet S. Lee
  • Enzo Lalli
  • Denis Masquilier
  • Florence Schlotter
  • Carlos A. Molina
  • Nicholas S. Foulkes
  • Paolo Sassone-Corsi

There are no affiliations available

Personalised recommendations