The Transcription Factor Sp3 Cooperates with HDAC2 to Regulate Synaptic Function and Plasticity in Neurons

Cell Reports

Volumn 20, Issue 6, 2017, Pages 1319-1334

  Yamakawa, Hidekuni ^a,c   Cheng, Jemmie ^a   Penney, Jay ^a   Gao, Fan ^a   Rueda, Richard ^a   Wang, Jun ^a   Yamakawa, Satoko ^a   Kritskiy, Oleg ^a   Gjoneska, Elizabeta ^a   Tsai, Li Huei ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c SHIONOGI AND CO LTD   (Japan)

Author keywords

Alzheimer's disease; epigenetic; histone acetylation; memory; synaptic plasticity

Indexed keywords

HISTONE DEACETYLASE 2; TRANSCRIPTION FACTOR SP3; HDAC2 PROTEIN, MOUSE; HISTONE; SP3 PROTEIN, MOUSE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE SILENCING; GENOMICS; MALE; MEMORY; MOUSE; NERVE CELL PLASTICITY; NERVE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SYNAPSE; ANIMAL; GENETIC EPIGENESIS; GENETICS; HISTONE CODE; METABOLISM; NERVE CELL; PHYSIOLOGY;

ALZHEIMER DISEASE; ANIMALS; EPIGENESIS, GENETIC; FEMALE; HISTONE CODE; HISTONE DEACETYLASE 2; HISTONES; MALE; MEMORY; MICE; NEURONAL PLASTICITY; NEURONS; SP3 TRANSCRIPTION FACTOR;

EID: 85026865683     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.07.044     Document Type: Article

References (54)

1. +/− mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42 (2004), 947–959.
2. Ali, A., Bluteau, O., Messaoudi, K., Palazzo, A., Boukour, S., Lordier, L., Lecluse, Y., Rameau, P., Kraus-Berthier, L., Jacquet-Bescond, A., et al. Thrombocytopenia induced by the histone deacetylase inhibitor abexinostat involves p53-dependent and -independent mechanisms. Cell Death Dis., 4, 2013, e738.
3. Bantscheff, M., Hopf, C., Savitski, M.M., Dittmann, A., Grandi, P., Michon, A.M., Schlegl, J., Abraham, Y., Becher, I., Bergamini, G., et al. Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nat. Biotechnol. 29 (2011), 255–265.
4. Boutillier, S., Lannes, B., Buée, L., Delacourte, A., Rouaux, C., Mohr, M., Bellocq, J.P., Sellal, F., Larmet, Y., Boutillier, A.L., Loeffler, J.P., Sp3 and sp4 transcription factor levels are increased in brains of patients with Alzheimer's disease. Neurodegener. Dis. 4 (2007), 413–423.
5. Cominski, T.P., Jiao, X., Catuzzi, J.E., Stewart, A.L., Pang, K.C., The role of the hippocampus in avoidance learning and anxiety vulnerability. Front. Behav. Neurosci., 8, 2014, 273.
6. Covington, H.E. 3rd, Maze, I., LaPlant, Q.C., Vialou, V.F., Ohnishi, Y.N., Berton, O., Fass, D.M., Renthal, W., Rush, A.J. 3rd, Wu, E.Y., et al. Antidepressant actions of histone deacetylase inhibitors. J. Neurosci. 29 (2009), 11451–11460.
7. Cruz, J.C., Tseng, H.C., Goldman, J.A., Shih, H., Tsai, L.H., Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 40 (2003), 471–483.
8. Cruz, J.C., Kim, D., Moy, L.Y., Dobbin, M.M., Sun, X., Bronson, R.T., Tsai, L.H., p25/cyclin-dependent kinase 5 induces production and intraneuronal accumulation of amyloid beta in vivo. J. Neurosci. 26 (2006), 10536–10541.
9. Dannenberg, J.H., David, G., Zhong, S., van der Torre, J., Wong, W.H., Depinho, R.A., mSin3A corepressor regulates diverse transcriptional networks governing normal and neoplastic growth and survival. Genes Dev. 19 (2005), 1581–1595.
10. Dobbin, M.M., Madabhushi, R., Pan, L., Chen, Y., Kim, D., Gao, J., Ahanonu, B., Pao, P.C., Qiu, Y., Zhao, Y., Tsai, L.H., SIRT1 collaborates with ATM and HDAC1 to maintain genomic stability in neurons. Nat. Neurosci. 16 (2013), 1008–1015.
11. Eberharter, A., Becker, P.B., Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep. 3 (2002), 224–229.
12. Eom, G.H., Nam, Y.S., Oh, J.G., Choe, N., Min, H.K., Yoo, E.K., Kang, G., Nguyen, V.H., Min, J.J., Kim, J.K., et al. Regulation of acetylation of histone deacetylase 2 by p300/CBP-associated factor/histone deacetylase 5 in the development of cardiac hypertrophy. Circ. Res. 114 (2014), 1133–1143.
13. Falkenberg, K.J., Johnstone, R.W., Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nat. Rev. Drug Discov. 13 (2014), 673–691.
14. Fischer, A., Sananbenesi, F., Pang, P.T., Lu, B., Tsai, L.H., Opposing roles of transient and prolonged expression of p25 in synaptic plasticity and hippocampus-dependent memory. Neuron 48 (2005), 825–838.
15. Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M., Tsai, L.H., Recovery of learning and memory is associated with chromatin remodelling. Nature 447 (2007), 178–182.
16. Flavell, S.W., Greenberg, M.E., Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu. Rev. Neurosci. 31 (2008), 563–590.
17. Frantseva, M.V., Fitzgerald, P.B., Chen, R., Möller, B., Daigle, M., Daskalakis, Z.J., Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill learning. Cereb. Cortex 18 (2008), 990–996.
18. Gjoneska, E., Pfenning, A.R., Mathys, H., Quon, G., Kundaje, A., Tsai, L.H., Kellis, M., Conserved epigenomic signals in mice and humans reveal immune basis of Alzheimer's disease. Nature 518 (2015), 365–369.
19. Gonzalez-Zuñiga, M., Contreras, P.S., Estrada, L.D., Chamorro, D., Villagra, A., Zanlungo, S., Seto, E., Alvarez, A.R., c-Abl stabilizes HDAC2 levels by tyrosine phosphorylation repressing neuronal gene expression in Alzheimer's disease. Mol. Cell 56 (2014), 163–173.
20. Gräff, J., Rei, D., Guan, J.S., Wang, W.Y., Seo, J., Hennig, K.M., Nieland, T.J., Fass, D.M., Kao, P.F., Kahn, M., et al. An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature 483 (2012), 222–226.
21. Gräff, J., Joseph, N.F., Horn, M.E., Samiei, A., Meng, J., Seo, J., Rei, D., Bero, A.W., Phan, T.X., Wagner, F., et al. Epigenetic priming of memory updating during reconsolidation to attenuate remote fear memories. Cell 156 (2014), 261–276.
22. Guan, J.S., Haggarty, S.J., Giacometti, E., Dannenberg, J.H., Joseph, N., Gao, J., Nieland, T.J., Zhou, Y., Wang, X., Mazitschek, R., et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459 (2009), 55–60.
23. Hanson, J.E., Deng, L., Hackos, D.H., Lo, S.C., Lauffer, B.E., Steiner, P., Zhou, Q., Histone deacetylase 2 cell autonomously suppresses excitatory and enhances inhibitory synaptic function in CA1 pyramidal neurons. J. Neurosci. 33 (2013), 5924–5929.
24. Hawrylycz, M.J., Lein, E.S., Guillozet-Bongaarts, A.L., Shen, E.H., Ng, L., Miller, J.A., van de Lagemaat, L.N., Smith, K.A., Ebbert, A., Riley, Z.L., et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489 (2012), 391–399.
25. Heideman, M.R., Lancini, C., Proost, N., Yanover, E., Jacobs, H., Dannenberg, J.H., Sin3a-associated Hdac1 and Hdac2 are essential for hematopoietic stem cell homeostasis and contribute differentially to hematopoiesis. Haematologica 99 (2014), 1292–1303.
26. Horvath, S., Zhang, B., Carlson, M., Lu, K.V., Zhu, S., Felciano, R.M., Laurance, M.F., Zhao, W., Qi, S., Chen, Z., et al. Analysis of oncogenic signaling networks in glioblastoma identifies ASPM as a molecular target. Proc. Natl. Acad. Sci. USA 103 (2006), 17402–17407.
27. Howland, J.G., Wang, Y.T., Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog. Brain Res. 169 (2008), 145–158.
28. Huang, D.W., Sherman, B.T., Lempicki, R.A., Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37 (2009), 1–13.
29. Huang, D.W., Sherman, B.T., Lempicki, R.A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4 (2009), 44–57.
30. Jaenisch, R., Bird, A., Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33:Suppl (2003), 245–254.
31. Kim, D., Frank, C.L., Dobbin, M.M., Tsunemoto, R.K., Tu, W., Peng, P.L., Guan, J.S., Lee, B.H., Moy, L.Y., Giusti, P., et al. Deregulation of HDAC1 by p25/Cdk5 in neurotoxicity. Neuron 60 (2008), 803–817.
32. Korzus, E., Rosenfeld, M.G., Mayford, M., CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42 (2004), 961–972.
33. Kurita, M., Holloway, T., García-Bea, A., Kozlenkov, A., Friedman, A.K., Moreno, J.L., Heshmati, M., Golden, S.A., Kennedy, P.J., Takahashi, N., et al. HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity. Nat. Neurosci. 15 (2012), 1245–1254.
34. Liang, W.S., Reiman, E.M., Valla, J., Dunckley, T., Beach, T.G., Grover, A., Niedzielko, T.L., Schneider, L.E., Mastroeni, D., Caselli, R., et al. Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc. Natl. Acad. Sci. USA 105 (2008), 4441–4446.
35. Lu, T., Aron, L., Zullo, J., Pan, Y., Kim, H., Chen, Y., Yang, T.H., Kim, H.M., Drake, D., Liu, X.S., et al. REST and stress resistance in ageing and Alzheimer's disease. Nature 507 (2014), 448–454.
36. Madabhushi, R., Gao, F., Pfenning, A.R., Pan, L., Yamakawa, S., Seo, J., Rueda, R., Phan, T.X., Yamakawa, H., Pao, P.C., et al. Activity-induced DNA breaks govern the expression of neuronal early-response genes. Cell 161 (2015), 1592–1605.
37. Morris, M.J., Mahgoub, M., Na, E.S., Pranav, H., Monteggia, L.M., Loss of histone deacetylase 2 improves working memory and accelerates extinction learning. J. Neurosci. 33 (2013), 6401–6411.
38. Penney, J., Tsai, L.H., Histone deacetylases in memory and cognition. Sci. Signal., 7, 2014, re12.
39. Ross, S., Tienhaara, A., Lee, M.S., Tsai, L.H., Gill, G., GC box-binding transcription factors control the neuronal specific transcription of the cyclin-dependent kinase 5 regulator p35. J. Biol. Chem. 277 (2002), 4455–4464.
40. Ryu, H., Lee, J., Zaman, K., Kubilis, J., Ferrante, R.J., Ross, B.D., Neve, R., Ratan, R.R., Sp1 and Sp3 are oxidative stress-inducible, antideath transcription factors in cortical neurons. J. Neurosci. 23 (2003), 3597–3606.
41. Seo, J., Giusti-Rodríguez, P., Zhou, Y., Rudenko, A., Cho, S., Ota, K.T., Park, C., Patzke, H., Madabhushi, R., Pan, L., et al. Activity-dependent p25 generation regulates synaptic plasticity and Aβ-induced cognitive impairment. Cell 157 (2014), 486–498.
42. Siegel, D., Hussein, M., Belani, C., Robert, F., Galanis, E., Richon, V.M., Garcia-Vargas, J., Sanz-Rodriguez, C., Rizvi, S., Vorinostat in solid and hematologic malignancies. J. Hematol. Oncol., 2, 2009, 31.
43. Sun, J.M., Chen, H.Y., Moniwa, M., Litchfield, D.W., Seto, E., Davie, J.R., The transcriptional repressor Sp3 is associated with CK2-phosphorylated histone deacetylase 2. J. Biol. Chem. 277 (2002), 35783–35786.
44. Sundaram, J.R., Poore, C.P., Sulaimee, N.H., Pareek, T., Asad, A.B., Rajkumar, R., Cheong, W.F., Wenk, M.R., Dawe, G.S., Chuang, K.H., et al. Specific inhibition of p25/Cdk5 activity by the Cdk5 inhibitory peptide reduces neurodegeneration in vivo. J. Neurosci. 33 (2013), 334–343.
45. Tong, J.K., Hassig, C.A., Schnitzler, G.R., Kingston, R.E., Schreiber, S.L., Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 395 (1998), 917–921.
46. Wang, Z., Zang, C., Cui, K., Schones, D.E., Barski, A., Peng, W., Zhao, K., Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138 (2009), 1019–1031.
47. Wang, W.Y., Pan, L., Su, S.C., Quinn, E.J., Sasaki, M., Jimenez, J.C., Mackenzie, I.R., Huang, E.J., Tsai, L.H., Interaction of FUS and HDAC1 regulates DNA damage response and repair in neurons. Nat. Neurosci. 16 (2013), 1383–1391.
48. Wen, Y., Yu, W.H., Maloney, B., Bailey, J., Ma, J., Marié, I., Maurin, T., Wang, L., Figueroa, H., Herman, M., et al. Transcriptional regulation of beta-secretase by p25/cdk5 leads to enhanced amyloidogenic processing. Neuron 57 (2008), 680–690.
49. West, A.C., Johnstone, R.W., New and emerging HDAC inhibitors for cancer treatment. J. Clin. Invest. 124 (2014), 30–39.
50. Wilting, R.H., Yanover, E., Heideman, M.R., Jacobs, H., Horner, J., van der Torre, J., DePinho, R.A., Dannenberg, J.H., Overlapping functions of Hdac1 and Hdac2 in cell cycle regulation and haematopoiesis. EMBO J. 29 (2010), 2586–2597.
51. Won, J., Yim, J., Kim, T.K., Sp1 and Sp3 recruit histone deacetylase to repress transcription of human telomerase reverse transcriptase (hTERT) promoter in normal human somatic cells. J. Biol. Chem. 277 (2002), 38230–38238.
52. Wu, W.S., Vallian, S., Seto, E., Yang, W.M., Edmondson, D., Roth, S., Chang, K.S., The growth suppressor PML represses transcription by functionally and physically interacting with histone deacetylases. Mol. Cell. Biol. 21 (2001), 2259–2268.
53. Yu, B., Datta, P.K., Bagchi, S., Stability of the Sp3-DNA complex is promoter-specific: Sp3 efficiently competes with Sp1 for binding to promoters containing multiple Sp-sites. Nucleic Acids Res. 31 (2003), 5368–5376.
54. Zhang, Y., Sun, Z.W., Iratni, R., Erdjument-Bromage, H., Tempst, P., Hampsey, M., Reinberg, D., SAP30, a novel protein conserved between human and yeast, is a component of a histone deacetylase complex. Mol. Cell 1 (1998), 1021–1031.