In PC12 cells, expression of neurosecretion and neurite outgrowth are governed by the transcription repressor REST/NRSF

Cellular and Molecular Neurobiology

Volumn 30, Issue 8, 2010, Pages 1295-1302

  D'Alessandro, Rosalba ^a   Meldolesi, Jacopo ^a  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Chromogranins; Clear vesicles; Dense core vesicles; Enlargeosomes; Exocytosis; Histone deacetylases; Nerve cells non nerve cells; Rac1; SNAREs

Indexed keywords

CHROMOGRANIN; HISTONE DEACETYLASE; NERVE GROWTH FACTOR RECEPTOR; RAC1 PROTEIN; REPRESSOR PROTEIN; SNARE PROTEIN;

CELL DIFFERENTIATION; CELL MATURATION; CELL ORGANELLE; CELL STRAIN; CONFERENCE PAPER; CYTOLOGY; DOWN REGULATION; EXOCYTOSIS; GENE EXPRESSION; GENETIC TRANSFECTION; NERVE CELL; NERVE FIBER GROWTH; NEUROBLASTOMA CELL; NEUROSECRETION; NEUROSECRETORY CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SYNAPSE VESICLE; WILD TYPE;

ANIMALS; MODELS, BIOLOGICAL; NEURITES; NEUROSECRETION; ORGANELLES; PC12 CELLS; RATS; REPRESSOR PROTEINS;

EID: 79151482286     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-010-9602-0     Document Type: Conference Paper

References (50)

1. A Abderrahmani G Niederhauser V Plaisance JA Haefliger R Regazzi G Waeber 2004 Neuronal traits are required for glucose-induced insulin secretion FEBS Lett 565 133 138 1:CAS:528:DC%2BD2cXjvVGrs74%3D 10.1016/j.febslet.2004.04.002 15135066
2. 2+ signaling mechanisms in pheochromocytoma PC12 cells Cell Calcium 47 360 368 1:CAS:528:DC%2BC3cXksVamtbo%3D 10.1016/j.ceca.2010.01.007 20171735
3. N Ballas G Mandel 2005 The many faces of REST oversee epigenetic programming of neuronal genes Curr Opin Neurobiol 15 500 506 1:CAS:528:DC%2BD2MXhtVynurnP 10.1016/j.conb.2005.08.015 16150588
4. CM Bittler MB Zhang BD Howard 1986 PC12 variants deficient in catecholamine transport J Neurochem 47 1286 1293 10.1111/j.1471-4159.1986. tb00752.x
5. B Borgonovo E Cocucci G Racchetti P Podini A Bachi J Meldolesi 2002 Regulated exocytosis: a novel, widely expressed system Nat Cell Biol 4 955 962 1:CAS:528:DC%2BD38XptFKmtL8%3D 10.1038/ncb888 12447386
6. AW Bruce IJ Donaldson IC Wood SA Yerbury MI Sadowski M Chapman B Gottgens NJ Buckley 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 10458 10463 1:CAS:528:DC%2BD2cXmtVyrsLs%3D 10.1073/pnas.0401827101 15240883
7. AW Bruce A Krejci L Ooi J Deuchars IC Wood V Dolezal NJ Buckley 2006 The transcriptional repressor REST is a critical regulator of the neurosecretory phenotype J Neurochem 98 1828 1840 1:CAS:528:DC%2BD28XhtVCksb7N 10.1111/j.1471-4159.2006.04010.x 16945103
8. AW Bruce AJ Lopez-Contreras P Ficeck P Dhami SC Dillon CM Koch CF Langford I Dunham RM Andrews D Vetrie 2009 Functional diversity for REST defined by in vivo binding affinity hierarchies at the DNA sequence level Genome Res 19 994 1005 1:CAS:528:DC%2BD1MXntFGrsLw%3D 10.1101/gr.089086.108 19401398
9. A Calderone T Jover K Noh H Tanaka H Yokota Y Lin S Grooms R Regis MV Bennett RS Zukin 2003 Ischemic insults derepress the gene silencer REST in neurons destined to die J Neurosci 23 2112 2121 1:CAS:528:DC%2BD3sXlsV2qsbo%3D 12657670
10. C Conaco S Otto JJ Han G Mandel 2006 Reciprocal actions of REST and microRNA promote neuronal identity Proc Natl Acad Sci USA 103 2422 2427 1:CAS:528:DC%2BD28XhslGjtLo%3D 10.1073/pnas.0511041103 16461918
11. N Corradi B Borgonovo E Clementi M Bassetti G Racchetti GG Consalez WB Huttner J Meldolesi P Rosa 1996 Overall lack of regulated secretion in a PC12 variant cell clone J Biol Chem 271 27116 27124 1:CAS:528:DyaK28XmsFSjtbg%3D 10.1074/jbc.271.43.27116 8900203
12. JM Coulson 2005 Transcriptional regulation: cancer, neurons and the REST Curr Biol 17 R665 R668 10.1016/j.cub.2005.08.032
13. M Courel C Rodemer ST Nguyen A Pance AP Jackson DT O'Connor L Taupenot 2006 Secretory granule biogenesis in sympathoadrenal cells: identification of a granulogenic determinant in the secretory prohormone chromogranin A J Biol Chem 281 38038 38051 1:CAS:528:DC%2BD28Xht1Kit7zE 10.1074/jbc.M604037200 17032650
14. R D'Alessandro A Klaijn L Stucchi P Podini ML Malosio J Meldolesi 2008 Expression of the neurosecretory process in PC12 cells is governed by REST J Neurochem 105 1369 1383 10.1111/j.1471-4159.2008.05259.x 18298477
15. R Day S Benjannet L Matsuuchi RB Kelly M Marchinkiewicz M Chrétien NG Seidah 1995 Maintained PC1 and PC2 expression in the AtT-20 variant cell line 6T3 lacking regulated secretion and POMC: restored POMC expression and regulated secretion after cAMP treatment DNA Cell Biol 14 175 188 1:CAS:528:DyaK2MXjvVynt7Y%3D 10.1089/dna.1995.14.175 7865135
16. M Ekici M Hohl F Schuit A Martinez-Serrano G Thiel 2008 Transcription of genes encoding synaptic vesicle proteins in human neural stem cells: chromatin accessibility, histome methylation pattern and the essential role of REST J Biol Chem 283 9257 9268 1:CAS:528:DC%2BD1cXjslyqsr8%3D 10.1074/jbc.M709388200 18234667
17. L Formisano KM Noh T Miyawaki T Mashiko MV Bennett RS Zukin 2003 Ischemic insults promote epigenetic reprogramming of mu opioid receptor expression in hippocampal neurons Proc Natl Acad Sci USA 104 4170 4175 10.1073/pnas.0611704104
18. M Garriga-Canut B Schoenike R Qazi K Bergendahl TJ Daley RM Pfender JF Morrison J Ockuly C Stafstrom T Sutula A Roopra 2006 2-Deoxy-d-glucose reduces epilepsy progression by NRSF/REST-dependent metabolic regulation of chromatin structure Nat Neurosci 9 1382 1387 1:CAS:528:DC%2BD28XhtFaksrfM 10.1038/nn1791 17041593
19. JD Greenway M Street A Jeffries NJ Buckley 2007 RE1 silencing transcription factor maintains a repressive chromatin environment in embryonic hippocampal neural stem cells Stem Cells 25 354 363 1:CAS:528: DC%2BD2sXivVOltrs%3D 10.1634/stemcells.2006-0207 17082226
20. C Grundschober ML Malosio L Astolfi T Giordano P Nef J Meldolesi 2002 Neurosecretion competence. A comprehensive gene expression program identified in PC12 cells J Biol Chem 277 36715 36724 1:CAS:528:DC%2BD38XnsVCitr4%3D 10.1074/jbc.M203777200 12070162
21. M Hohl G Thiel 2005 Cell type-specific regulation of RE-1 silencing transcription factor (REST) target genes Eur J Neurosci 22 2216 2230 10.1111/j.1460-9568.2005.04404.x 16262660
22. DS Johnson A Mortazavi RM Myers B Wold 2007 Genome-wide mapping of in vivo protein-DNA interactions Science 316 1497 1502 1:CAS:528: DC%2BD2sXmtFSjtrg%3D 10.1126/science.1141319 17540862
23. H Kasai T Kishimoto T-T Liu Y Miyashita P Podini F Grohovaz J Meldolesi 1999 Multiplicity and diversity of regulated exocytosis in wild-type and defective PC12 cells Proc Natl Acad Sci USA 96 945 949 1:CAS:528: DyaK1MXpvFajtw%3D%3D 10.1073/pnas.96.3.945 9927673
24. A Klajn C Ferrai L Stucchi I Prada P Podini T Baba M Rocchi J Meldolesi R D'Alessandro 2009 The rest repression of the neurosecretory phenotype is negatively modulated by BHC80, a protein of the BRAF/HDAC complex J Neurosci 29 6296 6307 1:CAS:528:DC%2BD1MXmt1Cmu7s%3D 10.1523/JNEUROSCI.5943-08.2009 19439607
25. CS Kim CH Hwang KY Song HS Choi K Kim do PY Law LN Wei HH Loh 2008 Novel function of neuron-restrictive silencing factor (NRSF) for posttranscriptional regulation Biochim Biophys Acta 1783 1835 1846 1:CAS:528:DC%2BD1cXhtV2is7fJ 10.1016/j.bbamcr.2008.06.019 18657578
26. C Leoni A Menegon F Benfenati D Toniolo M Pennuto F Valtorta 1999 Neurite extension occurs in the absence of regulated exocytosis in PC12 subclones Mol Biol Cell 10 2919 2931 1:CAS:528:DyaK1MXmtFeksbo%3D 10473636
27. Z Liu M Liu G Niu Y Cheng J Fei 2009 Genome-wide identification of target genes repressed by the zinc finger transcription factor REST/NRSF in the HEK 293 cell line Acta Biochim Biophys Sin (Shanghai) 41 1008 1017 1:CAS:528:DC%2BD1MXhsFaksLjF 10.1093/abbs/gmp095
28. H Lv G Pan G Zheng X Wu H Ren Y Liu J Wen 2010 Expression and functions of the repressor element 1 (RE-1)-silencing transcription factor (REST) in breast cancer J Cell Biochem 110 968 974 1:CAS:528:DC%2BC3cXotVOltLw%3D 10.1002/jcb.22610 20564196
29. A Magin M Lietz G Cibelli G Thiel 2002 RE-1 silencing transcription factor-4 (REST4) is neither a transcriptional repressor nor a de-repressor Neurochem Int 40 195 202 1:CAS:528:DC%2BD3MXptVSgtbY%3D 10.1016/S0197-0186(01) 00091-2 11741002
30. S Majumder 2008 REST in good times and bad. Roles of the tumor suppressor and oncogenic activities Cell Cycle 5 1929 1935 10.4161/cc.5.17.2982
31. D Martin F Allagnat G Chaffard D Caille M Fukuda R Regazzi A Abderrahmani G Waeber P Meda P Maechler J-A Haeflinger 2008 Functional significance of repressor element 1 silencing transcription factor (REST) target genes in pancreatic beta cells Diabetologia 51 1429 1439 1:CAS:528:DC%2BD1cXovF2htL0%3D 10.1007/s00125-008-0984-1 18385973
32. A Mortazavi EC Leeper Thompson T Garcia RM Myers B Wod 2006 Comparative genomics modeling of the NRSF/REST repressor network: from single conserved sites to genome-wide repertoire Genome Res 16 1208 1221 1:CAS:528: DC%2BD28XhtVOmtrnL 10.1101/gr.4997306 16963704
33. S Nihihara L Tsuda T Ogura 2002 The canonical Wnt pathway directly regulates NRSF/REST expression in chick spinal cord Biochem Biophys Res Commun 311 55 63 10.1016/j.bbrc.2003.09.158
34. L Ooi IC Wood 2007 Chromatin crosstalk in development and disease: lessons from REST Nat Rev Genet 8 544 554 1:CAS:528:DC%2BD2sXms1Skt7w%3D 10.1038/nrg2100 17572692
35. SJ Otto SR McCockle J Hover C Conaco JJ Han S Impey GS Yochum JJ Dunn RH Goodman G Mandel 2007 A new binding motif for the transcriptional repressor REST uncovers large gene networks devoted to neuronal functions J Neurosci 27 6729 6739 1:CAS:528:DC%2BD2sXnsVWqs7s%3D 10.1523/JNEUROSCI.0091-07.2007 17581960
36. K Palm M Metsis T Timmusk 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 1:CAS:528: DyaK1MXmsVWgurg%3D 10.1016/S0169-328X(99)00196-5 10521596
37. A Pance K Morgan PC Guest K Bowers GE Dean DF Cutler AP Jackson 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 1:CAS:528:DyaK1MXktVelsLk%3D 10.1046/j.1471-4159.1999.0730021.x 10386951
38. A Pance FJ Livesey AP Jackson 2006 A role for the transcriptional repressor REST in maintaining the phenotype of neurosecretory-deficient PC12 cells J Neurochem 99 1435 1444 1:CAS:528:DC%2BD28XhtlCntrnO 10.1111/j.1471-4159. 2006.04190.x 17064356
39. IA Qureshi MF Mehler 2009 Regulation of non-coding RNA networks in the nervous system. What's the REST of the story? Neurosci Lett 466 73 80 1:CAS:528:DC%2BD1MXhtlWhu7rK 10.1016/j.neulet.2009.07.093 19679163
40. G Racchetti A Lorusso C Schulte D Garavello V Carabelli R D'Alessandro J Meldolesi 2010 Rapid neurite outgrowth in neurosecretory cells and neurons sustained by the exocytosis of a cytoplasmic organelle, the enlargeosome J Cell Sci 123 165 170 1:CAS:528:DC%2BC3cXisVKgt7g%3D 10.1242/jcs.059634 20026640
41. S Schoch G Cibelli G Thiel 1996 Neuron-specific expression of synapsin I. Major role of a negative regulatory mechanism J Biol Chem 271 3317 3323 1:CAS:528:DyaK28XhtVajsLo%3D 10.1074/jbc.271.6.3317 8621737
42. CJ Schoenherr AJ Paquette DJ Anderson 1996 Identification of potential target genes for the neuron-restrictive silencer factor Proc Natl Acad Sci USA 93 9881 9886 1:CAS:528:DyaK28XlsFehur8%3D 10.1073/pnas.93.18.9881 8790425
43. C Schulte G Racchetti R D'Alessandro J Meldolesi 2010 A new form of neurite outgrowth is sustained by the exocytosis of enlargeosomes expressed under the control of REST Traffic 11 1304 1314 1:CAS:528:DC%2BC3cXht1CmsLzE 10.1111/j.1600-0854.2010.01095.x 20604903
44. KA Seth JA Majzoub 2001 Repressor element silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) can act as an enhancer as well as a repressor of corticotropin-releasing hormone gene transcription J Biol Chem 276 13917 13923 1:CAS:528:DC%2BD3MXjt12rsr8%3D 11278361
45. M Shimojo 2006 Characterization of the nuclear targeting signal of REST/NRSF Neurosci Lett 398 161 166 1:CAS:528:DC%2BD28XjvFShsbc%3D 10.1016/j.neulet.2005.12.080 16442230
46. A Tabuchi T Yamada S Sasagawa Y Naruse N Mori M Tsuda 2002 REST4-mediated modulation of REST/NRSF-silencing function during BDNF gene promoter activation Biochem Biophys Res Commun 290 415 420 1:CAS:528:DC%2BD38XhsFCnsA%3D%3D 10.1006/bbrc.2001.6194 11779185
47. TF Westbrook G Hu XL Ang P Mulligan NN Pavlova A Liang Y Leng R Maehr Y Shi JW Harper SJ Elledge 2008 SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation Nature 452 370 374 1:CAS:528:DC%2BD1cXjsFCnsLY%3D 10.1038/nature06780 18354483
48. J Wu X Xie 2006 Comparative sequence analysis reveals an intricate network among REST, CREB and miRNA in mediating neuronal gene expression Genome Biol 7 R85 10.1186/gb-2006-7-9-r85 17002790
49. AS Yoo BT Staahl I Chen GR Crabtree 2009 MicroRNA-mediated switching of chromatin-remodelling complexes in neural development Nature 460 642 646 1:CAS:528:DC%2BD1MXnslOjsL8%3D 19561591
50. D Zheng K Zhao MF Mehler 2009 Profiling RE1-REST-mediated histone modifications in the human genome Genome Biol 10 R9 10.1186/gb-2009-10-1-r9 19173732