A role for the transcriptional repressor REST in maintaining the phenotype of neurosecretory-deficient PC12 cells

Journal of Neurochemistry

Volumn 99, Issue 5, 2006, Pages 1435-1444

  Pance, Alena ^a   Livesey, Frederick J ^a,b   Jackson, Antony P ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Dense core granules; Microarray profiling; Pheochromocytoma 12; RE1 silencing transcription factor; Regulated secretion; Synaptic vesicles; Transcriptional repression

Indexed keywords

CELL PROTEIN; CHROMOGRANIN A; MESSENGER RNA; RE1 SILENCING TRANSCRIPTION FACTOR; SYNAPTOPHYSIN; SYNAPTOTAGMIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL GRANULE; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION PROFILING; GENE REPRESSION; MICROARRAY ANALYSIS; NEUROSECRETION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPSE VESICLE; TRANSCRIPTION REGULATION;

ANIMALS; BINDING SITES; CHROMOGRANIN A; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; NEURONS; NEUROSECRETION; NEUROSECRETORY SYSTEMS; PC12 CELLS; PHENOTYPE; PRESYNAPTIC TERMINALS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; REPRESSOR PROTEINS; RNA, MESSENGER; SECRETORY VESICLES; SODIUM CHANNELS; SYNAPTOPHYSIN; SYNAPTOTAGMINS; TRANSCRIPTION FACTORS;

EID: 33750914865     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04190.x     Document Type: Article

References (54)

1. Abderrahmani A., Niederhauser G., Plaisance V., Haefliger J. A., Regazzi R. and Waeber G. (2004) Neuronal traits are required for glucose-induced insulin secretion. FEBS Lett. 565, 133-138.
2. Acton S. L., Wong D. H., Parham P., Brodsky F. M. and Jackson A. P. (1993) Alteration of clathrin light chain expression by transfection and gene disruption. Mol. Biol. Cell 4, 647-660.
3. Al-Shahrour F., Diaz-Uriarte R. and Dopazo J. (2004) FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 20, 578-580.
4. Balbi D. and Allen J. M. (1994) Role of protein kinase C in mediating NGF effect on neuropeptide Y expression in PC12 cells. Brain Res. Mol. Brain Res. 23, 310-316.
5. Bartel D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
6. Bevilacqua A., Ceriani M. C., Capaccioli S. and Nicolin A. (2003) Post-transcriptional regulation of gene expression by degradation of messenger RNAs. J. Cell Physiol. 195, 356-372.
7. Boockvar J. A., Kapitonov D., Kapoor G., Schouten J., Counelis G. J., Bogler O., Snyder E. Y., McIntosh T. K. and O'Rourke D. M. (2003) Constitutive EGFR signaling confers a motile phenotype to neural stem cells. Mol. Cell Neurosci. 24, 1116-1130.
8. Borgonovo B., Racchetti G., Malosio M., Benfante R., Podini P., Rosa P. and Meldolesi J. (1998) Neurosecretion competence, an independently regulated trait of the neurosecretory cell phenotype. J. Biol. Chem. 273, 34 683-34 686.
9. Bruce A. W., Donaldson I. J., Wood I. C., Yerbury S. A., Sadowski M. I., Chapman M., Gottgens B. and Buckley N. J. (2004) Genome-wide analysis of repressor element 1 silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) target genes. Proc. Natl Acad. Sci. USA 101, 10 458-10 463.
10. Brunet J. F. and Pattyn A. (2002) Phox2 genes - from patterning to connectivity. Curr. Opin. Genet. Dev. 12, 435-440.
11. Burgoyne R. D. and Morgan A. (2003) Secretory granule exocytosis. Physiol. Rev. 83, 581-632.
12. Calderone A., Jover T., Noh K. M., Tanaka H., Yokota H., Lin Y., Grooms S. Y., Regis R., Bennett M. V. and Zukin R. S. (2003) Ischemic insults derepress the gene silencer REST in neurons destined to die. J. Neurosci. 23, 2112-2121.
13. Chong J. A., Tapia-Ramirez J., Kim S., Toledo-Aral J. J., Zheng Y., Boutros M. C., Altshuller Y. M., Frohman M. A., Kraner S. D. and Mandel G. (1995) REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 80, 949-957.
14. Cohen R. and Atlas D. (2004) R.-type voltage-gated Ca(2+) channel interacts with synaptic proteins and recruits synaptotagmin to the plasma membrane of Xenopus oocytes. Neuroscience 128, 831-841.
15. Collins R. T. and Cohen S. M. (2003) The secret life of Smoothened. Dev. Cell 5, 823-824.
16. Conaco C., Otto S., Han J. J. and Mandel G. (2006) Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl Acad. Sci. USA 103, 2422-2427.
17. Cowley D. J., Moore Y. R., Darling D. S., Joyce P. B. and Gorr S. U. (2000) N- and C-terminal domains direct cell type-specific sorting of chromogranin A to secretory granules. J. Biol. Chem. 275, 7743-7748.
18. Daly C. and Ziff E. B. (1997) Post-transcriptional regulation of synaptic vesicle protein expression and the developmental control of synaptic vesicle formation. J. Neurosci. 17, 2365-2375.
19. Fahmi A. I., Patel M., Stevens E. B., Fowden A. L., John J. E., 3rd, Lee K., Pinnock R., Morgan K., Jackson A. P. and Vandenberg J. I. (2001) The sodium channel beta-subunit SCN3b modulates the kinetics of SCN5a and is expressed heterogeneously in sheep heart. J. Physiol. 537, 693-700.
20. Gorr S. U. (1996) Differential storage of prolactin, granins (chromogranin B and secretogranin II), and constitutive secretory markers in rat pituitary GH4C1 cells. J. Biol. Chem. 271, 3575-3580.
21. 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.
22. Grundschober C., Malosio M. L., Astol. L., Giordano T., Nef P. and Meldolesi J. (2002) Neurosecretion competence. A comprehensive gene expression program identified in PC12 cells. J. Biol. Chem. 277, 36 715-36 724.
23. Harrison T. M., Chidgey M. A. and Uff S. (1996) Novel markers for constitutive secretion used to show that tissue plasminogen activator is sorted to the regulated pathway in transfected PC12 cells. Cell Biol. Int. 20, 293-299.
24. Jalava A. and Mai S. (1994) Fos and Jun form cell specific protein complexes at the neuropeptide tyrosine promoter. Oncogene 9, 2369-2375.
25. Jurata L. W., Kenny D. A. and Gill G. N. (1996) Nuclear LIM interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development. Proc. Natl Acad. Sci. USA 93, 11 693-11 698.
26. Karin M. and Mintz B. (1981) Receptor-mediated endocytosis of transferrin in developmentally totipotent mouse teratocarcinoma stem cells. J. Biol. Chem. 256, 3245-3252.
27. Kim T., Tao-Cheng J. H., Eiden L. E. and Loh Y. P. (2001) Chromogranin A, an 'on/off' switch controlling dense-core secretory granule biogenesis. Cell 106, 499-509.
28. Krichevsky A. M., King K. S., Donahue C. P., Khrapko K. and Kosik K. S. (2003) A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 9, 1274-1281.
29. Lee J. H., Shimojo M., Chai Y. G. and Hersh L. B. (2000) Studies on the interaction of REST4 with the cholinergic repressor element-1/neuron restrictive silencer element. Brain Res. Mol. Brain Res. 80, 88-98.
30. Leoni C., Menegon A., Benfenati F., Toniolo D., Pennuto M. and Valtorta F. (1999) Neurite extension occurs in the absence of regulated exocytosis in PC12 subclones. Mol. Biol. Cell 10, 2919-2931.
31. Li C., Takei K., Geppert M., Daniell L., Stenius K., Chapman E. R., Jahn R., De Camilli P. and Sudhof T. C. (1994) Synaptic targeting of rabphilin-3A, a synaptic vesicle Ca2+/phospholipid-binding protein, depends on rab3A/3C. Neuron 13, 885-898.
32. Lichtenstein Y., Desnos C., Faundez V., Kelly R. B. and Clift-O'Grady L. (1998) Vesiculation and sorting from PC12-derived endosomes in vitro. Proc. Natl Acad. Sci. USA 95, 11 223-11 228.
33. 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.
34. Livesey F. J., Furukawa T., Steffen M. A., Church G. M. and Cepko C. L. (2000) Microarray analysis of the transcriptional network controlled by the photoreceptor homeobox gene Crx. Curr. Biol. 10, 301-310.
35. Livesey F. J., Young T. L. and Cepko C. L. (2004) An analysis of the gene expression program of mammalian neural progenitor cells. Proc. Natl Acad. Sci. USA 101, 1374-1379.
36. Malosio M. L., Benfante R., Racchetti G., Borgonovo B., Rosa P. and Meldolesi J. (1999) Neurosecretory cells without neurosecretion: evidence of an independently regulated trait of the cell phenotype. J. Physiol. 520, 43-52.
37. Malosio M. L., Giordano T., Laslop A. and Meldolesi J. (2004) Dense-core granules: a specific hallmark of the neuronal/neurosecretory cell phenotype. J. Cell Sci. 117, 743-749.
38. Matsuuchi L. and Kelly R. B. (1991) Constitutive and basal secretion from the endocrine cell line, AtT-20. J. Cell Biol. 112, 843-852.
39. McDonald J. K. (1988) NPY and related substances. Crit. Rev. Neurobiol. 4, 97-135.
40. Morgan K., Stevens E. B., Shah B. et al. (2000) Beta 3: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics. Proc. Natl Acad. Sci. USA 97, 2308-2313.
41. Okano H., Imai T. and Okabe M. (2002) Musashi: a translational regulator of cell fate. J. Cell Sci. 115, 1355-1359.
42. Pance A., Morgan K., Guest P. C., Bowers K., Dean G. E., Cutler D. F. and Jackson A. P. (1999) A PC12 variant lacking regulated secretory organelles: aberrant protein targeting and evidence for a factor inhibiting neuroendocrine gene expression. J. Neurochem. 73, 21-30.
43. Roopra A., Sharling L., Wood I. C., Briggs T., Bachfischer U., Paquette A. J. and Buckley N. J. (2000) Transcriptional repression by neuron-restrictive silencer factor is mediated via the Sin3-histone deacetylase complex. Mol. Cell Biol. 20, 2147-2157.
44. Sampo B., Tricaud N., Leveque C., Seagar M., Couraud F. and Dargent B. (2000) Direct interaction between synaptotagmin and the intracellular loop I-II of neuronal voltage-sensitive sodium channels. Proc. Natl Acad. Sci. USA 97, 3666-3671.
45. 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.
46. Schoenherr C. J., Paquette A. J. and Anderson D. J. (1996) Identification of potential target genes for the neuron-restrictive silencer factor. Proc. Natl Acad. Sci. USA 93, 9881-9886.
47. Schrader M. (2004) Membrane targeting in secretion. Subcell Biochem. 37, 391-421.
48. Sudhof T. C. (2004) The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547.
49. Thiel G., Lietz M. and Cramer M. (1998) Biological activity and modular structure of RE-1-silencing transcription factor (REST), a repressor of neuronal genes. J. Biol. Chem. 273, 26 891-26 899.
50. Ungar D. and Hughson F. M. (2003) SNARE protein structure and function. Annu. Rev. Cell Dev. Biol. 19, 493-517.
51. 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.
52. Yeo M., Lee S. K., Lee B., Ruiz E. C., Pfaff S. L. and Gill G. N. (2005) Small CTD phosphatases function in silencing neuronal gene expression. Science 307, 596-600.
53. Zheng X. and Bobich J. A. (1998) MgATP-dependent and MgATP-independent [3H]noradrenaline release from perforated synaptosomes both use N-ethylmaleimide-sensitive fusion protein. Biochemistry 37, 12 569-12 575.
54. Zuccato C., Tartari M., Crotti A. et al. (2003) Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nat. Genet. 35, 76-83.