Melatonin Synthesis in Retina: CAMP-dependent Transcriptional Regulation of Chicken Arylalkylamine N-acetyltransferase by a CRE-like Sequence and a TTATT Repeat Motif in the Proximal Promoter

Overview

Journal J Neurochem

Specialties Chemistry
Neurology

Date 2011 Jul 28

PMID 21790603

Citations 12

Authors

Rashidul Haque

Nelson W Chong

Fatima Ali

Shyam S Chaurasia

Trisha Sengupta

Eugene Chun

Jennifer C Howell

David C Klein

P Michael Iuvone

Affiliations

Soon will be listed here.

Abstract

Arylalkylamine N-acetyltransferase (AANAT) is the key regulatory enzyme controlling the daily rhythm of melatonin biosynthesis. In chicken retinal photoreceptor cells, Aanat transcription and AANAT activity are regulated in part by cAMP-dependent mechanisms. The purpose of this study was to identify regulatory elements within the chicken Aanat promoter responsible for cAMP-dependent induction. Photoreceptor-enriched retinal cell cultures were transfected with a luciferase reporter construct containing up to 4 kb of 5'-flanking region and the first exon of Aanat. Forskolin treatment stimulated luciferase activity driven by the ∼4 kb promoter construct and by all 5'-deletion constructs except the smallest, Aanat (-217 to +120)luc. Maximal basal and forskolin-stimulated expression levels were generated by the Aanat (-484 to +120)luc construct. This construct lacks a canonical cyclic AMP-response element (CRE), but contains two other potentially important elements in its sequence: an eight times TTATT repeat (TTATT₈) and a CRE-like sequence. Electrophoretic mobility shift assays, luciferase reporter assays, chromatin immunoprecipitation, and siRNA experiments provide evidence that these elements bind c-Fos, JunD, and CREB to enhance basal and forskolin-stimulated Aanat transcription. We propose that the CRE-like sequence and TTATT₈ elements in the 484 bp proximal promoter interact to mediate cAMP-dependent transcriptional regulation of Aanat.

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References

Hoeffler J, Meyer T, Yun Y, Jameson J, Habener J . Cyclic AMP-responsive DNA-binding protein: structure based on a cloned placental cDNA. Science. 1988; 242(4884):1430-3. DOI: 10.1126/science.2974179. View

Yamamoto K, Gonzalez G, Menzel P, Rivier J, Montminy M . Characterization of a bipartite activator domain in transcription factor CREB. Cell. 1990; 60(4):611-7. DOI: 10.1016/0092-8674(90)90664-z. View

Roesler W . What is a cAMP response unit?. Mol Cell Endocrinol. 2000; 162(1-2):1-7. DOI: 10.1016/s0303-7207(00)00198-2. View

Zawilska J, Wawrocka M, Zurawska E, Nowak J . Calcium channel blockers in vivo inhibit serotonin N-acetyltransferase (NAT) activity in chicken retina stimulated by darkness and not by agents elevating intracellular cyclic AMP level. J Pineal Res. 1992; 13(3):101-6. DOI: 10.1111/j.1600-079x.1992.tb00062.x. View

Montminy M . Transcriptional regulation by cyclic AMP. Annu Rev Biochem. 1997; 66:807-22. DOI: 10.1146/annurev.biochem.66.1.807. View

Iuvone P, Avendano G, Butler B, Adler R . Cyclic AMP-dependent induction of serotonin N-acetyltransferase activity in photoreceptor-enriched chick retinal cell cultures: characterization and inhibition by dopamine. J Neurochem. 1990; 55(2):673-82. DOI: 10.1111/j.1471-4159.1990.tb04186.x. View

Chong N, Bernard M, Klein D . Characterization of the chicken serotonin N-acetyltransferase gene. Activation via clock gene heterodimer/E box interaction. J Biol Chem. 2000; 275(42):32991-8. DOI: 10.1074/jbc.M005671200. View

Klein D . Arylalkylamine N-acetyltransferase: "the Timezyme". J Biol Chem. 2006; 282(7):4233-7. DOI: 10.1074/jbc.R600036200. View

Adler R, Lindsey J, Elsner C . Expression of cone-like properties by chick embryo neural retina cells in glial-free monolayer cultures. J Cell Biol. 1984; 99(3):1173-8. PMC: 2113377. DOI: 10.1083/jcb.99.3.1173. View

10.

Humphries A, Carter D . Circadian dependency of nocturnal immediate-early protein induction in rat retina. Biochem Biophys Res Commun. 2004; 320(2):551-6. DOI: 10.1016/j.bbrc.2004.06.006. View

11.

Klein D, Coon S, Roseboom P, Weller J, Bernard M, Gastel J . The melatonin rhythm-generating enzyme: molecular regulation of serotonin N-acetyltransferase in the pineal gland. Recent Prog Horm Res. 1997; 52:307-57; discussion 357-8. View

12.

Avendano G, Butler B, Iuvone P . K(+)-evoked depolarization induces serotonin N-acetyltransferase activity in photoreceptor-enriched retinal cell cultures. Involvement of calcium influx through l-type channels. Neurochem Int. 2010; 17(1):117-26. DOI: 10.1016/0197-0186(90)90075-5. View

13.

Liu X, Green C . Circadian regulation of nocturnin transcription by phosphorylated CREB in Xenopus retinal photoreceptor cells. Mol Cell Biol. 2002; 22(21):7501-11. PMC: 135673. DOI: 10.1128/MCB.22.21.7501-7511.2002. View

14.

Burke Z, Wells T, Carter D, Klein D, Baler R . Genetic targeting: the serotonin N-acetyltransferase promoter imparts circadian expression selectively in the pineal gland and retina of transgenic rats. J Neurochem. 1999; 73(4):1343-9. DOI: 10.1046/j.1471-4159.1999.0731343.x. View

15.

Coulon V, Chebli K, Cavelier P, Blanchard J . A novel mouse c-fos intronic promoter that responds to CREB and AP-1 is developmentally regulated in vivo. PLoS One. 2010; 5(6):e11235. PMC: 2888593. DOI: 10.1371/journal.pone.0011235. View

16.

Pozdeyev N, Taylor C, Haque R, Chaurasia S, Visser A, Thazyeen A . Photic regulation of arylalkylamine N-acetyltransferase binding to 14-3-3 proteins in retinal photoreceptor cells. J Neurosci. 2006; 26(36):9153-61. PMC: 6674502. DOI: 10.1523/JNEUROSCI.1384-06.2006. View

17.

Montminy M, Bilezikjian L . Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature. 1987; 328(6126):175-8. DOI: 10.1038/328175a0. View

18.

Du K, Montminy M . CREB is a regulatory target for the protein kinase Akt/PKB. J Biol Chem. 1998; 273(49):32377-9. DOI: 10.1074/jbc.273.49.32377. View

19.

Baler R, Covington S, Klein D . Rat arylalkylamine N-acetyltransferase gene: upstream and intronic components of a bipartite promoter. Biol Cell. 2000; 91(9):699-705. View

20.

Yamamoto K, Gonzalez G, Biggs 3rd W, Montminy M . Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB. Nature. 1988; 334(6182):494-8. DOI: 10.1038/334494a0. View