Sp3/REST/HDAC1/HDAC2 complex represses and Sp1/HIF-1/p300 complex activates ncx1 gene transcription, in brain ischemia and in ischemic brain preconditioning, by Epigenetic mechanism

Journal of Neuroscience

Volumn 35, Issue 19, 2015, Pages 7332-7348

  Formisano, Luigi ^a,b   Guida, Natascia ^c   Valsecchi, Valeria ^a,d   Cantile, Maria ^a   Cuomo, Ornella ^a   Vinciguerra, Antonio ^a   Laudati, Giusy ^a   Pignataro, Giuseppe ^a   Sirabella, Rossana ^c   Di Renzo, Gianfranco ^a   Annunziato, Lucio ^a,c  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF SANNIO   (Italy)

^c IRCCS SDN   (Italy)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

Acetylation; Brain ischemia; Epigenetic; Ischemic brain preconditioning; REST NRSF; Sodium calcium exchanger

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HYPOXIA INDUCIBLE FACTOR 1; RE1 SILENCING TRANSCRIPTION FACTOR; SMALL INTERFERING RNA; SODIUM CALCIUM EXCHANGE PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3; UNCLASSIFIED DRUG; BENZOIC ACID DERIVATIVE; C646 COMPOUND; ENZYME INHIBITOR; HDAC1 PROTEIN, HUMAN; HISTONE ACETYLTRANSFERASE PCAF; PYRAZOLE DERIVATIVE; RE1-SILENCING TRANSCRIPTION FACTOR; REPRESSOR PROTEIN; SODIUM-CALCIUM EXCHANGER 1;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ISCHEMIA; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; EPIGENETICS; GEL MOBILITY SHIFT ASSAY; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; ISCHEMIC PRECONDITIONING; LUCIFERASE ASSAY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BRAIN CORTEX; CYTOLOGY; DISEASE MODEL; GENETIC EPIGENESIS; GENETICS; METABOLISM; NERVE CELL; PATHOLOGY; SPRAGUE DAWLEY RAT; TRANSCRIPTION INITIATION;

ANIMALS; BENZOATES; BRAIN ISCHEMIA; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; EPIGENESIS, GENETIC; HISTONE DEACETYLASE 1; HUMANS; ISCHEMIC PRECONDITIONING; MALE; NEURONS; P300-CBP TRANSCRIPTION FACTORS; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; SODIUM-CALCIUM EXCHANGER; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

EID: 84929359474     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2174-14.2015     Document Type: Article

References (72)

1. Abel T, Zukin RS (2008) Epigenetic targets of HDAC inhibition in neuro-degenerative and psychiatric disorders. Curr Opin Pharmacol 8:57-64. CrossRef Medline
2. Ammanamanchi S, Brattain MG (2001) Sp3 is a transcriptional repressor of transforming growth factor-beta receptors. J Biol Chem 276:3348-3352. CrossRef Medline
3. Ammanamanchi S, Freeman JW, Brattain MG (2003) Acetylated sp3 is a transcriptional activator. J Biol Chem 278:35775-35780. CrossRef Medline
4. Annunziato L, Pignataro G, Di Renzo GF (2004) Pharmacology of brain Na+/Ca2+ exchanger: from molecular biology to therapeutic perspectives. Pharmacol Rev 56:633-654. CrossRef Medline
5. Azahri NS, Di Bartolo BA, Khachigian LM, Kavurma MM (2012) Spl, acetylated histone-3 and p300 regulate TRAIL transcription: mechanisms of PDGF-BB-mediated VSMC proliferation and migration. J Cell Biochem 113:2597-2606. CrossRef Medline
6. Barone FC, White RF, Spera PA, Ellison J, Currie RW, Wang X, Feuerstein GZ (1998) Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke 29: 1937-1950; discussion 1950-1951. CrossRef Medline
7. Bigger CB, Melnikova IN, Gardner PD (1997) Sp 1 and Sp3 regulate expression of the neuronal nicotinic acetylcholine receptor beta4 subunit gene. J Biol Chem 272:25976-25982. CrossRef Medline
8. Billon N, Carlisi D, Datto MB, van Grunsven LA, Watt A, Wang XF, Rudkin BB (1999) Cooperation of Spl and p300 in the induction of the CDK inhibitor p21WAFl/CIPl during NGF-mediated neuronal differentiation. Oncogene 18:2872-2882. CrossRef Medline
9. Boscia F, Gala R, Pignataro G, de Bartolomeis A, Cicale M, Ambesi-Impiombato A, Di Renzo G, Annunziato L (2006) Permanent focal brain ischemia induces isoform-dependent changes in the pattern of Na+/Ca2+ exchanger gene expression in the ischemic core, periinfarct area, and intact brain regions. J Cereb Blood Flow Metab 26:502-517. CrossRef Medline
10. Boscia F, D'Avanzo C, Pannaccione A, Secondo A, Casamassa A, Formisano L, Guida N, Sokolow S, Herchuelz A, Annunziato L (2012) Silencing or knocking out the Na(+)/Ca(2+) exchanger-3 (NCX3) impairs oligodendrocyte differentiation. Cell Death Differ 19:562-572. CrossRef Medline
11. Calderone A, Jover T, Noh KM, Tanaka H, Yokota H, Lin Y, Grooms SY, Regis R, Bennett MV, Zukin RS (2003) Ischemic insults derepress the gene silencer REST in neurons destined to die. J Neurosci 23:2112-2121. Medline
12. Carrasco-Serrano C, Campos-Caro A, Viniegra S, Ballesta JJ, Criado M (1998) GC-and E-box motifs as regulatory elements in the proximal promoter region of the neuronal nicotinic receptor alpha7 subunit gene. J Biol Chem 273:20021-20028. CrossRef Medline
13. Cassimere EK, Pyndiah S, Sakamuro D (2009) The c-MYC-interacting pro-apoptotic tumor suppressor BIN 1 is a transcriptional target for E2F1 in response to DNA damage. Cell Death Differ 16:1641-1653. CrossRef Medline
14. Chuang DM, Leng Y, Marinova Z, Kim HJ, Chiu CT (2009) Multiple roles of HDAC inhibition in neurodegenerative conditions. Trends Neurosci 32:591-601. CrossRef Medline
15. Federman N, de la Fuente V, Zalcman G, Corbi N, Onori A, Passananti C, Romano A (2013) Nuclear factor κB-dependent histone acetylation is specifically involved in persistent forms of memory. J Neurosci 33:7603-7614. CrossRef Medline
16. Formisano L, Noh KM, Miyawaki T, Mashiko T, Bennett MV, Zukin RS (2007) Ischemic insults promote epigenetic reprogramming of mu opioid receptor expression in hippocampal neurons. Proc Natl Acad Sci USA 104:4170-4175. CrossRef Medline
17. Formisano L, Saggese M, Secondo A, Sirabella R, Vito P, Valsecchi V, Molin-aro P, Di Renzo G, Annunziato L (2008) The two isoforms of the Na+/ Ca2+ exchanger, NCX1 and NCX3, constitute novel additional targets for the prosurvival action of Akt/protein kinase B pathway. Mol Pharmacol 73:727-737. CrossRef Medline
18. Formisano L, Guida N, Valsecchi V, Pignataro G, Vinciguerra A, Pannaccione A, Secondo A, Boscia F, Molinaro P, Sisalli MJ, Sirabella R, Casamassa A, Canzoniero LM, Di Renzo G, Annunziato L (2013) NCX1 is a new rest target gene: role in cerebral ischemia. Neurobiol Dis 50:76-85. CrossRef Medline
19. Formisano L, Guida N, Laudati G, Boscia F, Esposito A, Secondo A, Di Renzo G, Canzoniero LM (2015a) Extracellular signal-related kinase 2/specificity protein 1/specificity protein 3/repressor element-1 silencing transcription factor pathway is involved in Aroclor 1254-induced toxicity in SH-SY5Y neuronal cells. J Neurosci Res 93:167-177. CrossRef Medline
20. Formisano L, Guida N, Laudati G, Mascolo L, Di Renzo G, Canzoniero LM (2015b) MS-275 inhibits aroclor 1254-induced SH-SY5Y neuronal cell toxicity by preventing the formation of the HDAC3/REST complex on the synapsin-1 promoter. J Pharmacol Exp Ther 352:236-243. CrossRef Medline
21. Galmozzi A, Mitro N, Ferrari A, Gers E, Gilardi F, Godio C, Cermenati G, Gualerzi A, Donetti E, Rotili D, Valente S, Guerrini U, Caruso D, Mai A, Saez E, De Fabiani E, Crestani M (2013) Inhibition of class I histone deacetylases unveils a mitochondrial signature and enhances oxidative metabolism in skeletal muscle and adipose tissue. Diabetes 62:732-742. CrossRef Medline
22. Guida N, Laudati G, Galgani M, Santopaolo M, Montuori P, Triassi M, Di Renzo G, Canzoniero LM, Formisano L (2014) Histone deacetylase 4 promotes ubiquitin-dependent proteasomal degradation of Sp3 in SH-SY5Y cells treated with di(2-ethylhexyl)phthalate (DEHP), determining neuronal death. Toxicol Appl Pharmacol 280:190-198. CrossRef Medline
23. Hagen G, Müller S, Beato M, Suske G (1992) Cloning by recognition site screening of two novel GT box binding proteins: a family of Sp 1 related genes. Nucleic Acids Res 20:5519-5525. CrossRef Medline
24. Hwang CK, D'Souza UM, Eisch AJ, Yajima S, Lammers CH, Yang Y, Lee SH, Kim YM, Nestler EJ, Mouradian MM (2001) Dopamine receptor regulating factor, DRRF: a zinc finger transcription factor. Proc Natl Acad Sci USA 98:7558-7563. CrossRef Medline
25. Iannotti FA, Barrese V, Formisano L, Miceli F, Taglialatela M (2013) Specification of skeletal muscle differentiation by repressor element-1 silencing transcription factor (REST)-regulated Kv7.4 potassium channels. Mol Biol Cell 24:274-284. CrossRef Medline
26. Ishimaru N, Tabuchi A, Hara D, Hayashi H, Sugimoto T, Yasuhara M, Shiota J, Tsuda M (2007) Regulation of neurotrophin-3 gene transcription by Sp3 and Sp4 in neurons. J Neurochem 100:520-531. CrossRef Medline
27. Isomura H, Stinski MF, Kudoh A, Daikoku T, Shirata N, Tsurumi T (2005) Two Spl/Sp3 binding sites in the major immediate-early proximal enhancer of human cytomegalovirus have a significant role in viral replication. J Virol 79:9597-9607. CrossRef Medline
28. Iwamoto T, Inoue Y, Ito K, Sakaue T, Kita S, Katsuragi T (2004) The exchanger inhibitory peptide region-dependent inhibition of Na+/Ca 2+ exchange by SN-6 [2-[4-(4-nitrobenzyloxy)benzyl]thiazolidine-4-carboxylic add ethyl ester], a novel benzyloxyphenyl derivative. Mol Pharmacol 66:45-55. CrossRef Medline
29. Jiang BH, Jiang G, Zheng JZ, Lu Z, Hunter T, Vogt PK (2001) Phosphati-dylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1. Cell Growth Differ 12:363-369. Medline
30. Jin HO, An S, Lee HC, Woo SH, Seo SK, Choe TB, Yoo DH, Lee SB, Um HD, Lee SJ, Park MJ, Kim JI, Hong SI, Rhee CH, Park IC (2007) Hypoxic condition-and high cell density-induced expression of Redd 1 is regulated by activation of hypoxia-inducible factor-1 alpha and Spl through the phosphatidylinositol 3-kinase/Akt signaling pathway. Cell Signal 19: 1393-1403. CrossRef Medline
31. Kaneko N, Hwang JY, Gertner M, Pontarelli F, Zukin RS (2014) Casein kinase 1 suppresses activation of REST in insulted hippocampal neurons and halts ischemia-induced neuronal death. J Neurosci 34:6030-6039. CrossRef Medline
32. Ke Q, Costa M (2006) Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70:1469-1480. CrossRef Medline
33. Khalil MI, Hay J, Ruyechan WT (2008) Cellular transcription factors Spl and Sp3 suppress varicella-zoster virus origin-dependent DNA replication. J Virol 82:11723-11733. CrossRef Medline
34. Kim CS, Choi HS, Hwang CK, Song KY, Lee BK, Law PY, Wei LN, Loh HH (2006) Evidence of the neuron-restrictive silencer factor (NRSF) interaction with Sp3 and its synergic repression to the mu opioid receptor (MOR) gene. Nucleic Acids Res 34:6392-6403. CrossRef Medline
35. Ko JL, Liu HC, Minnerath SR, Loh HH (1998) Transcriptional regulation of mouse mu-opioid receptor gene. J Biol Chem 273:27678-27685. CrossRef Medline
36. Koh JY, Choi DW (1987) Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Methods 20:83-90. CrossRef Medline
37. Lanzillotta A, Pignataro G, Branca C, Cuomo O, Sarnico I, Benarese M, Annunziato L, Spano P, Pizzi M (2013) Targeted acetylation ofNF-kap-paB/RelA and histones by epigenetic drugs reduces post-ischemic brain injury in mice with an extended therapeutic window. Neurobiol Dis 49: 177-189. CrossRef Medline
38. Law AY, Yeung BH, Ching LY, Wong CK (2011) Spl is a transcription repressor to stanniocalcin-1 expression in TSA-treated human colon cancer cells, HT29. J Cell Biochem 112:2089-2096. CrossRef Medline
39. Lee J, Kosaras B, Aleyasin H, Han JA, Park DS, Ratan RR, Kowall NW, Fer-rante RJ, Lee SW, Ryu H (2006) Role of cyclooxygenase-2 induction by transcription factor Spl and Sp3 in neuronal oxidative and DNA damage response. FASEB J 20:2375-2377. CrossRef Medline
40. Lerner LE, Gribanova YE, Whitaker L, Knox BE, Farber DB (2002) The rod cGMP-phosphodiesterase beta-subunit promoter is a specific target for Sp4 and is not activated by other Sp proteins or CRX. J Biol Chem 277: 25877-25883. CrossRef Medline
41. Lerner LE, Peng GH, Gribanova YE, Chen S, Farber DB (2005) Sp4 is expressed in retinal neurons, activates transcription of photoreceptor-specific genes, and synergizes with Crx. J Biol Chem 280:20642-20650. CrossRef Medline
42. Matrone C, Pignataro G, Molinaro P, Irace C, Scorziello A, Di Renzo GF, Annunziato L (2004) HIF-lalpha reveals a binding activity to the promoter of iNOS gene after permanent middle cerebral artery occlusion. J Neurochem 90:368-378. CrossRef Medline
43. Min SW, Cho SH, Zhou Y, Schroeder S, Haroutunian V, Seeley WW, Huang EJ, Shen Y, Masliah E, Mukherjee C, Meyers D, Cole PA, Ott M, Gan L (2010) Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron 67:953-966. CrossRef Medline
44. Mora-López F, Pedreño-Horrillo N, Delgado-Pérez L, Brieva JA, Campos-Caro A (2008) Transcription of PRDM1, the master regulator for plasma cell differentiation, depends on an SP1/SP3/EGR-1 GC-box. Eur J Immunol 38:2316-2324. CrossRef Medline
45. Nguyen-Huynh AT, Schaffer PA (1998) Cellular transcription factors enhance herpes simplex virus type 1 oriS-dependent DNA replication. J Virol 72:3635-3645. Medline
46. Noh KM, Hwang JY, Follenzi A, Athanasiadou R, Miyawaki T, Greally JM, Bennett MV, Zukin RS (2012) Repressor element ! silencing transcrip-tion factor (REST)-dependent epigenetic remodeling is critical to ischemia-induced neuronal death. Proc Natl Acad Sci U S A 109:E962-E971. CrossRef Medline
47. Ooi L, Wood IC (2007) Chromatin crosstalk in development and disease: lessons from REST. Nat Rev Genet 8:544-554. CrossRef Medline
48. Pawlus MR, Hu CJ (2013) Enhanceosomes as integrators of hypoxia inducible factor (HIF) and other transcription factors in the hypoxic transcriptional response. Cell Signal 25:1895-1903. CrossRef Medline
49. Philipsen S, Suske G (1999) A tale of three fingers: the family of mammalian Sp/XKLF transcription factors. Nucleic Acids Res 27:2991-3000. CrossRef Medline
50. Pignataro G, GalaR, Cuomo O, Tortiglione A, Giaccio L, Castaldo P, Sirabella R, Matrone C, Canitano A, Amoroso S, Di Renzo G, Annunziato L (2004) Two sodium/calcium exchanger gene products, NCX1 and NCX3, play a major role in the development of permanent focal cerebral ischemia. Stroke 35:2566-2570. CrossRef Medline
51. Pignataro G, Esposito E, Cuomo O, Sirabella R, Boscia F, Guida N, Di Renzo G, Annunziato L (2011) The NCX3 isoform of the Na+/Ca2+ exchanger contributes to neuroprotection elicited by ischemic postconditioning. J Cereb Blood Flow Metab 31:362-370. CrossRef Medline
52. Pignataro G, Boscia F, Esposito E, Sirabella R, Cuomo O, Vinciguerra A, Di Renzo G, Annunziato L (2012) NCX1 and NCX3: two new effectors of delayed preconditioning in brain ischemia. Neurobiol Dis 45:616-623. CrossRef Medline
53. Pinacho R, Villalmanzo N, Lalonde J, Haro JM, Meana JJ, Gill G, Ramos B (2011) The transcription factor SP4 is reduced in postmortem cerebellum of bipolar disorder subjects: control by depolarization and lithium. Bipolar Disord 13:474-485. CrossRef Medline
54. Plaisance V, Niederhauser G, Azzouz F, Lenain V, Haefliger JA, Waeber G, Abderrahmani A (2005) The repressor element silencing transcription factor (REST)-mediated transcriptional repression requires the inhibition of Spl. J Biol Chem 280:401-407. CrossRef Medline
55. Ramos B, Gaudillière B, Bonni A, Gill G (2007) Transcription factor Sp4 regulates dendritic patterning during cerebellar maturation. Proc Natl Acad Sci U S A 104:9882-9887. CrossRef Medline
56. Ramos B, Valin A, Sun X, Gill G (2009) Sp4-dependent repression of neurotrophin-3 limits dendritic branching. Mol Cell Neurosci 42:152-159. CrossRef Medline
57. Ravache M, Weber C, Mérienne K, Trottier Y (2010) Transcriptional activation of REST by Spl in Huntington's disease models. PLoS One 5:el4311. CrossRef Medline
58. Renthal W, Maze I, Krishnan V, Covington HE 3rd, Xiao G, Kumar A, Russo SJ, Graham A, TsankovaN, Kippin TE, Kerstetter KA, Neve RL, Haggarty SJ, McKinsey TA, Bassel-Duby R, Olson EN, Nestler EJ (2007) Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56:517-529. CrossRef Medline
59. Rodenas-Ruano A, Chávez AE, Cossio MJ, Castillo PE, Zukin RS (2012) REST-dependent epigenetic remodeling promotes the developmental switch in synaptic NMDA receptors. Nat Neurosci 15:1382-1390. CrossRef Medline
60. Ryu H, Lee J, Zaman K, Kubilis J, Ferrante RJ, Ross BD, Neve R, Ratan RR (2003) Spl and Sp3 are oxidative stress-inducible, antideath transcription factors in cortical neurons. J Neurosci 23:3597-3606. Medline
61. Schweizer S, Meisel A, Märschenz S (2013) Epigenetic mechanisms in cerebral ischemia. J Cereb Blood Flow Metab 33:1335-1346. CrossRef Medline
62. Simonini MV, Camargo LM, Dong E, Maloku E, Veldic M, Costa E, Guidotti A (2006) The benzamide MS-275 is a potent, long-lasting brain region-selective inhibitor of histone deacetylases. Proc Natl Acad Sci U S A 103: 1587-1592. CrossRef Medline
63. Sirabella R, Secondo A, Pannaccione A, Scorziello A, Valsecchi V, Adornetto A, Bilo L, Di Renzo G, Annunziato L (2009) Anoxia-induced NF-kappaB-dependent upregulation of NCX1 contributes to Ca2+ refilling into endoplasmic reticulum in cortical neurons. Stroke 40:922-929. CrossRef Medline
64. Sirabella R, Secondo A, Pannaccione A, Molinaro P, Formisano L, Guida N, Di Renzo G, Annunziato L, Cataldi M (2012) ERK1/2, p38, and JNK regulate the expression and the activity of the three isoforms of the Na(+) /Ca(2+) exchanger, NCX1, NCX2, and NCX3, in neuronal PC12 cells. J Neurochem 122:911-922. CrossRef Medline
65. Sisalli MJ, Secondo A, Esposito A, Valsecchi V, Savoia C, Di Renzo GF, An-nunziato L, Scorziello A (2014) Endoplasmic reticulum refilling and mitochondrial calcium extrusion promoted in neurons by NCX1 and NCX3 in ischemic preconditioning are determinant for neuroprotection. Cell Death Differ 21:1142-1149. CrossRef Medline
66. Stains JP, Lecanda F, Screen J, Towler DA, Civitelli R (2003) Gap junctional communication modulates gene transcription by altering the recruitment of Spl and Sp3 to connexin-response elements in osteoblast promoters. J Biol Chem 278:24377-24387. CrossRef Medline
67. Sun JM, Chen HY, Moniwa M, Litchfield DW, Seto E, Davie JR (2002) The transcriptional repressor Sp3 is associated with CK2-phosphorylated histone deacetylase 2. J Biol Chem 277:35783-35786. CrossRef Medline
68. Suske G (1999) The Sp-family of transcription factors. Gene 238:291-300. CrossRef Medline
69. Tan NY, Khachigian LM (2009) Spl phosphorylation and its regulation of gene transcription. Mol Cell Biol 29:2483-2488. CrossRef Medline
70. Valsecchi V, Pignataro G, Del Prete A, Sirabella R, Matrone C, Boscia F, Scorziello A, Sisalli MJ, Esposito E, Zambrano N, Di Renzo G, Annunziato L (2011) NCX1 is a novel target gene for hypoxia-inducible factor-1 in ischemic brain preconditioning. Stroke 42:754-763. CrossRef Medline
71. Won J, Yim J, Kim TK (2002) Spl and Sp3 recruit histone deacetylase to repress transcription of human telomerase reverse transcriptase (hTERT) promoter in normal human somatic cells. J Biol Chem 277:38230-38238. CrossRef Medline
72. Yeo M, Berglund K, Augustine G, Liedtke W (2009) Novel repression of Kcc2 transcription by REST-RE-1 controls developmental switch in neuronal chloride. J Neurosci 29:14652-14662. CrossRef Medline