Specificity protein 1 (Sp1)-dependent activation of the synapsin I gene (SYN1) is modulated by RE1-silencing transcription factor (REST) and 5'-cytosine-phosphoguanine (CPG) methylation

Journal of Biological Chemistry

Volumn 288, Issue 5, 2013, Pages 3227-3239

  Paonessa, Francesco ^a   Latifi, Shahrzad ^a   Scarongella, Helena ^a   Cesca, Fabrizia ^a   Benfenati, Fabio ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING MOTIF; DOWN-REGULATION; FUNCTIONAL ASSAYS; GENE TRANSCRIPTIONS; MASTER REGULATORS; MEDIATED TRANSCRIPTION; MOLECULAR MECHANISM; NEUROBLASTOMAS; NEUROPSYCHIATRIC DISORDER; PHYSICAL INTERACTIONS; PROMOTER REGION; SPECIFICITY PROTEIN 1; SYNAPSIN I; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; TRANSCRIPTIONAL ACTIVATORS; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL REGULATION;

ALKYLATION; BINDING SITES; CHEMICAL ACTIVATION; GENES; METHYLATION; NEURONS; TISSUE; TRANSCRIPTION FACTORS;

TRANSCRIPTION;

5' CYTOSINE PHOSPHOGUANINE; GUANINE DERIVATIVE; RE1 SILENCING TRANSCRIPTION FACTOR; SYNAPSIN I; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; GENE ACTIVATION; GENE EXPRESSION; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INHIBITION KINETICS; MOUSE; NERVE CELL DIFFERENTIATION; NEUROBLASTOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN METHYLATION; PROTEIN MOTIF; PROTEIN STABILITY; SYN1 GENE; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; CONSERVED SEQUENCE; CPG ISLANDS; DNA METHYLATION; HUMANS; MICE; MICE, INBRED C57BL; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NEURONS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STABILITY; REPRESSOR PROTEINS; SP1 TRANSCRIPTION FACTOR; SYNAPSINS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84873323128     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.399782     Document Type: Article

References (56)

1. Clinton, M., Manson, J., McBride, D., and Miele, G. (2000) Gene expression changes during murine postnatal brain development. Genome Biol. 1, RESEARCH0005
2. Mody, M., Cao, Y., Cui, Z., Tay, K. Y., Shyong, A., Shimizu, E., Pham, K., Schultz, P., Welsh, D., and Tsien, J. Z. (2001) Genome-wide gene expression profiles of the developing mouse hippocampus. Proc. Natl. Acad. Sci. U. S. A. 98, 8862-8867
3. Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., Chen, L., Chen, L., Chen, T. M., Chin, M. C., Chong, J., Crook, B. E., Czaplinska, A., Dang, C. N., Datta, S., Dee, N. R., Desaki, A. L., Desta, T., Diep, E., Dolbeare, T. A., Donelan, M. J., Dong, H. W., Dougherty, J. G., Duncan, B. J., Ebbert, A. J., Eichele, G., Estin, L. K., Faber, C., Facer, B. A., Fields, R., Fischer, S. R., Fliss, T. P., Frensley, C., Gates, S. N., Glattfelder, K. J., Halverson, K. R., Hart, M. R., Hohmann, J. G., Howell, M. P., Jeung, D. P., Johnson, R. A., Karr, P. T., Kawal, R., Kidney, J. M., Knapik, R. H., Kuan, C. L., Lake, J. H., Laramee, A. R., Larsen, K. D., Lau, C., Lemon, T. A., Liang, A. J., Liu, Y., Luong, L. T., Michaels, J., Morgan, J. J., Morgan, R. J., Mortrud, M. T., Mosqueda, N. F., Ng, L. L., Ng, R., Orta, G. J., Overly, C. C., Pak, T. H., Parry, S. E., Pathak, S. D., Pearson, O. C., Puchalski, R. B., Riley, Z. L., Rockett, H. R., Rowland, S. A., Royall, J. J., Ruiz, M. J., Sarno, N. R., Schaffnit, K., Shapovalova, N. V., Sivisay, T., Slaughterbeck, C. R., Smith, S. C., Smith, K. A., Smith, B. I., Sodt, A. J., Stewart, N. N., Stumpf, K. R., Sunkin, S. M., Sutram, M., Tam, A., Teemer, C. D., Thaller, C., Thompson, C. L., Varnam, L. R., Visel, A., Whitlock, R. M., Wohnoutka, P. E., Wolkey, C. K., Wong, V. Y., Wood, M., Yaylaoglu, M. B., Young, R. C., Youngstrom, B. L., Yuan, X. F., Zhang, B., Zwingman, T. A., and Jones, A. R. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176
4. Sunkin, S. M., and Hohmann, J. G. (2007) Insights from spatially mapped gene expression in the mouse brain. Hum. Mol. Genet. 16, Spec. No. 2, R209-R219
5. Strathdee, G., Davies, B. R., Vass, J. K., Siddiqui, N., and Brown, R. (2004) Cell type-specific methylation of an intronic CpG island controls expression of the MCJ gene. Carcinogenesis 25, 693-701
6. Ladd-Acosta, C., Pevsner, J., Sabunciyan, S., Yolken, R. H., Webster, M. J., Dinkins, T., Callinan, P. A., Fan, J. B., Potash, J. B., and Feinberg, A. P. (2007) DNA methylation signatures within the human brain. Am. J. Hum. Genet. 81, 1304-1315
7. Zuccato, C., Tartari, M., Crotti, A., Goffredo, D., Valenza, M., Conti, L., Cataudella, T., Leavitt, B. R., Hayden, M. R., Timmusk, T., Rigamonti, D., and Cattaneo, E. (2003) Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat. Genet. 35, 76-83
8. Bassuk, A. G., Wallace, R. H., Buhr, A., Buller, A. R., Afawi, Z., Shimojo, M., Miyata, S., Chen, S., Gonzalez-Alegre, P., Griesbach, H. L., Wu, S., Nashelsky, M., Vladar, E. K., Antic, D., Ferguson, P. J., Cirak, S., Voit, T., Scott, M. P., Axelrod, J. D., Gurnett, C., Daoud, A. S., Kivity, S., Neufeld, M. Y., Mazarib, A., Straussberg, R., Walid, S., Korczyn, A. D., Slusarski, D. C., Berkovic, S. F., and El-Shanti, H. I. (2008) A homozygous mutation in human PRICKLE1 causes an autosomal-recessive progressive myoclonus epilepsy-ataxia syndrome. Am. J. Hum. Genet. 83, 572-581
9. Cesca, F., Baldelli, P., Valtorta, F., and Benfenati, F. (2010) The synapsins: key actors of synapse function and plasticity. Prog. Neurobiol. 91, 313-348
10. Bogen, I. L., Jensen, V., Hvalby, O., and Walaas, S. I. (2009) Synapsin-dependent development of glutamatergic synaptic vesicles and presynaptic plasticity in postnatal mouse brain. Neuroscience 158, 231-241
11. Rosahl, T. W., Spillane, D., Missler, M., Herz, J., Selig, D. K., Wolff, J. R., Hammer, R. E., Malenka, R. C., and Südhof, T. C. (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375, 488-493
12. Corradi, A., Zanardi, A., Giacomini, C., Onofri, F., Valtorta, F., Zoli, M., and Benfenati, F. (2008) Synapsin-I-and synapsin-II-null mice display an increased age-dependent cognitive impairment. J. Cell Sci. 121, 3042-3051
13. Baldelli, P., Fassio, A., Valtorta, F., and Benfenati, F. (2007) Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses. J. Neurosci. 27, 13520-13531
14. Chiappalone, M., Casagrande, S., Tedesco, M., Valtorta, F., Baldelli, P., Martinoia, S., and Benfenati, F. (2009) Opposite changes in glutamatergic and GABAergic transmission underlie the diffuse hyperexcitability of synapsin I-deficient cortical networks. Cereb. Cortex 19, 1422-1439
15. Fassio, A., Patry, L., Congia, S., Onofri, F., Piton, A., Gauthier, J., Pozzi, D., Messa, M., Defranchi, E., Fadda, M., Corradi, A., Baldelli, P., Lapointe, L., St-Onge, J., Meloche, C., Mottron, L., Valtorta, F., Khoa Nguyen, D., Rouleau, G. A., Benfenati, F., and Cossette, P. (2011) SYN1 loss-of-function mutations in autism and partial epilepsy cause impaired synaptic function. Hum. Mol. Genet 20, 2297-2307
16. Sauerwald, A., Hoesche, C, Oschwald, R., and Kilimann, M. W. (1990) The 5'-flanking region of the synapsin I gene: a G + C-rich, TATA-and CAAT-less, phylogenetically conserved sequence with cell type-specific promoter function. J. Biol. Chem. 265, 14932-14937
17. Thiel, G., Greengard, P., and Südhof, T. C. (1991) Characterization of tissue-specific transcription by the human synapsin I gene promoter. Proc. Natl. Acad. Sci. U. S. A. 88, 3431-3435
18. Schoenherr, C. J., and Anderson, D. J. (1995) The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267, 1360-1363
19. Grimes, J. A., Nielsen, S. J., Battaglioli, E., Miska, E. A., Speh, J. C., Berry, D. L., Atouf, F., Holdener, B. C., Mandel, G., and Kouzarides, T. (2000) The co-repressor mSin3A is a functional component of the REST-CoREST repressor complex. J. Biol. Chem. 275, 9461-9467
20. Andrés, M. E., Burger, C., Peral-Rubio, M. J., Battaglioli, E., Anderson, M. E., Grimes, J., Dallman, J., Ballas, N, and Mandel, G. (1999) CoREST: a functional corepressor required for regulation of neural-specific gene expression. Proc. Natl. Acad. Sci. U. S. A. 96, 9873-9878
21. Ooi, L., and Wood, I. C. (2007) Chromatin crosstalk in development and disease: lessons from REST. Nat. Rev. Genet 8, 544-554
22. Palm, K., Belluardo, N, Metsis, M., and Timmusk, T. (1998) Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene. J. Neurosci. 18, 1280-1296
23. Wood, I. C, Belyaev, N. D., Bruce, A. W., Jones, C, Mistry, M., Roopra, A., and Buckley, N. J. (2003) Interaction of the repressor element 1-silencing transcription factor (REST) with target genes. J. Mol. Biol. 334, 863-874
24. Philipsen, S., and Suske, G. (1999) A tale of three fingers: the family of mammalian Sp/XKLF transcription factors. Nucleic Acids Res. 27, 2991-3000
25. Wierstra, I. (2008) Sp1: emerging roles-beyond constitutive activation of TATA-less housekeeping genes. Biochem. Biophys. Res. Commun. 372, 1-13
26. Babu, H., Cheung, G., Kettenmann, H., Palmer, T. D., and Kempermann, G. (2007) Enriched monolayer precursor cell cultures from micro-dissected adult mouse dentate gyrus yield functional granule cell-like neurons. PLoS One 2, e388
27. Babu, H., Claasen, J. H., Kannan, S., Rünker, A. E., Palmer, T., and Kempermann, G. (2011) A protocol for isolation and enriched monolayer cultivation of neural precursor cells from mouse dentate gyrus. Front Neurosci. 5, 89
28. Hoesche, C, Sauerwald, A., Veh, R. W., Krippl, B., and Kilimann, M. W. (1993) The 5'-flanking region of the rat synapsin I gene directs neuronspecific and developmentally regulated reporter gene expression in transgenic mice. J. Biol. Chem. 268, 26494-26502
29. Cartharius, K., Frech, K., Grote, K., Klocke, B., Haltmeier, M., Klingenhoff A., Frisch, M., Bayerlein, M., and Werner, T. (2005) MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21, 2933-2942
30. Huber, R., Schlessinger, D., and Pilia, G. (1998) Multiple Sp1 sites efficiently drive transcription of the TATA-less promoter of the human glypican 3 (GPC3) gene. Gene 214, 35-44
31. Rivero, S., Ruiz-García, A., Díaz-Guerra, M. J., Laborda, J., and García-Ramírez, J. J. (2011) Characterization of a proximal Sp1 response element in the mouse Dlk2 gene promoter. BMC Mol. Biol. 12, 52
32. Plaisance, V., Niederhauser, G., Azzouz, F., Lenain, V., Haefliger, J. A., Waeber, G., and Abderrahmani, A. (2005) The repressor element silencing transcription factor (REST)-mediated transcriptional repression requires the inhibition of Sp1. J. Biol. Chem. 280, 401-407
33. Schoch, S., Cibelli, G., and Thiel, G. (1996) Neuron-specific gene expression of synapsin I: major role of a negative regulatory mechanism. J. Biol. Chem. 271, 3317-3323
34. Lietz, M., Cicchetti, P., and Thiel, G. (1998) Inverse expression pattern of REST and synapsin I in human neuroblastoma cells. Biol. Chem. 379, 1301-1304
35. Palm, K., Metsis, M., and Timmusk, T. (1999) Neuron-specific splicing of zinc finger transcription factor REST/NRSF/XBR is frequent in neuroblastomas and conserved in human, mouse, and rat. Brain Res. Mol. Brain Res. 72, 30-39
36. Strathdee, G., Sim, A., and Brown, R. (2004) Control of gene expression by CpG island methylation in normal cells. Biochem. Soc. Trans. 32, 913-915
37. Li, L. C., and Dahiya, R. (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18, 1427-1431
38. Clark, S. J., Harrison, J., and Molloy, P. L. (1997) Sp1 binding is inhibited by mCpmCpG methylation. Gene 195, 67-71
39. Butta, N., Larrucea, S., Alonso, S., Rodriguez, R. B., Arias-Salgado, E. G., Ayuso, M. S., González-Manchón, C., and Parrilla, R. (2006) Role of transcription factor Sp1 and CpG methylation on the regulation of the human podocalyxin gene promoter. BMC Mol. Biol. 7, 17
40. Ekici, M., Schmitz, F., Hohl, M., Seigel, G. M., and Thiel, G. (2008) Chromatin structure and expression of synapsin I and synaptophysin in retinal precursor cells. Neurochem. Int. 53, 165-172
41. Jüngling, S., Cibelli, G., Czardybon, M., Gerdes, H. H., and Thiel, G. (1994) Differential regulation of chromogranin B and synapsin I gene promoter activity by cAMP and cAMP-dependent protein kinase. Eur. J. Biochem. 226, 925-935
42. Thiel, G., Schoch, S., and Petersohn, D. (1994) Regulation of synapsin I gene expression by the zinc finger transcription factor zif268/egr-1. J. Biol. Chem. 269, 15294-15301
43. James, A. B., Conway, A. M., Thiel, G., and Morris, B. J. (2004) Egr-1 modulation of synapsin I expression: permissive effect of forskolin via cAMP. Cell Signal 16, 1355-1362
44. Chang, L., Schwarzenbach, H., Meyer-Staeckling, S., Brandt, B., Mayr, G. W., Weitzel, J. M., and Windhorst, S. (2011) Expression regulation of the metastasis-promoting protein InsP3-kinase-A in tumor cells. Mol. Cancer Res. 9, 1-10
45. Park, S. Y., Kim, J. B., and Han, Y. M. (2007) REST is a key regulator in brain-specific homeobox gene expression during neuronal differentiation. J. Neurochem. 103, 2565-2574
46. Lietz, M., Hohl, M., and Thiel, G. (2003) RE-1 silencing transcription factor (REST) regulates human synaptophysin gene transcription through an intronic sequence-specific DNA-binding site. Eur. J. Biochem. 270, 2-9
47. Hagen, G., Müller, S., Beato, M., and Suske, G. (1994) Sp1-mediated transcriptional activation is repressed by Sp3. EMBO J. 13, 3843-3851
48. Futscher, B. W., Oshiro, M. M., Wozniak, R. J., Holtan, N., Hanigan, C. L., Duan, H., and Domann, F. E. (2002) Role for DNA methylation in the control of cell type specific maspin expression. Nat. Genet. 31, 175-179
49. Kudo, S., and Fukuda, M. (1995) Tissue-specific transcriptional regulation of human leukosialin (CD43) geneisachieved by DNA methylation. J. Biol. Chem. 270, 13298-13302
50. Kudo, S. (1998) Methyl-CpG-binding protein MeCP2 represses Sp1-activated transcription of the human leukosialin gene when the promoter is methylated. Mol. Cell Biol. 18, 5492-5499
51. Kitazawa, S., Kitazawa, R., and Maeda, S. (1999) Transcriptional regulation of rat cyclin D1 gene by CpG methylation status in promoter region. J. Biol. Chem. 274, 28787-28793
52. Cao, Y. X., Jean, J. C., and Williams, M. C. (2000) Cytosine methylation of an Sp1 site contributes to organ-specific and cell-specific regulation of expression of the lung epithelial gene t1a. Biochem. J. 350, 883-890
53. Lunyak, V. V., Burgess, R., Prefontaine, G. G., Nelson, C., Sze, S. H., Chenoweth, J., Schwartz, P., Pevzner, P. A., Glass, C., Mandel, G., and Rosenfeld, M. G. (2002) Corepressor-dependent silencing of chromosomal regions encoding neuronal genes. Science 298, 1747-1752
54. Feng, J., Zhou, Y., Campbell, S. L., Le, T., Li, E., Sweatt, J. D., Silva, A. J., and Fan, G. (2010) Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat. Neurosci. 13, 423-430
55. Chestnut, B. A., Chang, Q., Price, A., Lesuisse, C., Wong, M., and Martin, L. J. (2011) Epigenetic regulationof motor neuron cell death through DNA methylation. J. Neurosci. 31, 16619-16636
56. Zhu, Q., Wang, L., Zhang, Y., Zhao, F. H., Luo, J., Xiao, Z., Chen, G. J., and Wang, X. F. (2012) Increased expression of DNA methyltransferase 1 and 3a in human temporal lobe epilepsy. J. Mol. Neurosci. 46, 420-426