Ezh1 and Ezh2 differentially regulate PSD-95 gene transcription in developing hippocampal neurons

Molecular and Cellular Neuroscience

Volumn 57, Issue , 2013, Pages 130-143

  Henriquez, Berta ^a   Bustos, Fernando J ^a,b,d   Aguilar, Rodrigo ^a,d   Becerra, Alvaro ^a,c   Simon, Felipe ^a,c   Montecino, Martin ^a,d   van Zundert, Brigitte ^a  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

^b UNIVERSITY OF CONCEPCIÓN   (Chile)

^c Pontificia Universidad Católica de Chile   (Chile)

^d Fondap Center of Genome Regulation   (Chile)

Author keywords

Ezh1; Ezh2; Neuron; PcG; PSD 95

Indexed keywords

HISTONE DEMETHYLASE; HISTONE H3; POLYCOMB REPRESSIVE COMPLEX 2; POSTSYNAPTIC DENSITY PROTEIN 95; RNA POLYMERASE II; TRANSCRIPTION FACTOR EZH2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE REPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HIPPOCAMPUS; HUMAN; NERVE CELL DIFFERENTIATION; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; RAT; TRANSCRIPTION REGULATION;

MAMMALIA;

4′,6-DIAMIDINO-2-PHENYLINDOLE; ALDEHYDE DEHYDROGENASE 1 FAMILY, MEMBER L1; ALDH1L1; ANALYSIS OF VARIANCE; ANOVA; ARAC; CHIP; CHROMATIN IMMUNOPRECIPITATION; CYTOSINE ARABINOSIDE; DAPI; DAYS IN VITRO; DIV; EED; EGS; EMBRYONIC ECTODERM DEVELOPMENT; ENHANCER OF ZESTE HOMOLOG 1/2; ETHYLENE GLYCOL-BIS(SUCCINIC ACID N-HYDROXYSUCCINIMIDE ESTER); EZH1; EZH1/2; EZH2; GAPDH; GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE; HDAC2; HISTONE DEACETYLASE 2; JMJD3; JUMONJI DOMAIN-CONTAINING PROTEIN 3; NEURON; PCG; POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 1/2; POLYVINYLIDENE DIFLUORIDE; PRC1/2; PSD-95; PVDF; RNA POL II; RNA POLYMERASE II; S.E.M; STANDARD ERROR OF THE MEAN; SUPPRESSOR OF ZESTE 12; SUZ12; UBIQUITOUSLY TRANSCRIBED TETRATRICOPEPTIDE REPEAT, X CHROMOSOME; UTX;

ANIMALS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; HISTONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NEURONS; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION, GENETIC;

EID: 84888133782     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2013.07.012     Document Type: Article

References (58)

1. Agger K., Cloos P.A., Christensen J., Pasini D., Rose S., Rappsilber J., Issaeva I., Canaani E., Salcini A.E., Helin K. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007, 449:731-734.
2. Bao J., Lin H., Ouyang Y., Lei D., Osman A., Kim T.W., Mei L., Dai P., Ohlemiller K.K., Ambron R.T. Activity-dependent transcription regulation of PSD-95 by neuregulin-1 and Eos. Nat. Neurosci. 2004, 7:1250-1258.
3. Benoit Y.D., Laursen K.B., Witherspoon M.S., Lipkin S.M., Gudas L.J. Inhibition of 814 PRC2 histone methyltransferase activity increases TRAIL-mediated apoptosis sensitivity in human colon cancer cells. J. Cell. Physiol. 2012, 228:764-772.
4. Borrelli E., Nestler E.J., Allis C.D., Sassone-Corsi P. Decoding the epigenetic language of neuronal plasticity. Neuron 2008, 60:961-974.
5. Buerli T., Pellegrino C., Baer K., Lardi-Studler B., Chudotvorova I., Fritschy J., Medina I., Fuhrer C. Efficient transfection of DNA or shRNA vectors into neurons using magnetofection. Nat. Protoc. 2007, 2:3090-3101.
6. Cao Q., Yu J., Dhanasekaran S.M., Kim J.H., Mani R.S., Tomlins S.A., Mehra R., Laxman B., Cao X., Kleer C.G., Varambally S., Chinnaiyan A.M. Repression of E-cadherin by the polycomb group protein EZH2 in cancer. Oncogene 2008, 27:7274-7284.
7. Charych E.I., Akum B.F., Goldberg J.S., Jornsten R.J., Rongo C., Zheng J.Q., Firestein B.L. Activity-independent regulation of dendrite patterning by postsynaptic density protein PSD-95. J. Neurosci. 2006, 26:10164-10176.
8. Chen S., Shi Y. A new horizon for epigenetic medicine?. Cell Res. 2013, 23:326-328.
9. Cruzat F., Henriquez B., Villagra A., Hepp M., Lian J.B., van Wijnen A.J., Stein J.L., Imbalzano A.N., Stein G.S., Montecino M. SWI/SNF-independent nuclease hypersensitivity and an increased level of histone acetylation at the P1 promoter accompany active transcription of the bone master gene Runx2. Biochemistry 2009, 48:7287-7295.
10. Day J.J., Sweatt J.D. Epigenetic mechanisms in cognition. Neuron 2011, 70:813-829.
11. Elias G.M., Nicoll R.A. Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell Biol. 2007, 17:343-352.
12. Ezhkova E., Pasolli H.A., Parker J.S., Stokes N., Su I.H., Hannon G., Tarakhovsky A., Fuchs E. Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 2009, 136:1122-1135.
13. Ezhkova E., Lien W.H., Stokes N., Pasolli H.A., Silva J.M., Fuchs E. EZH1 and EZH2 cogovern histone H3K27 trimethylation and are essential for hair follicle homeostasis and wound repair. Genes Dev. 2011, 25:485-498.
14. Fallini C., Bassell G.J., Rossoll W. High-efficiency transfection of cultured primary motor neurons to study protein localization, trafficking, and function. Mol. Neurodegener. 2010, 5:17-26.
15. Fleet J.C., Hock J.M. Identification of osteocalcin mRNA in nonosteoid tissue of rats and humans by reverse transcription-polymerase chain reaction. J. Bone Miner. Res. 1994, 9:1565-1573.
16. Funke L., Dakoji S., Bredt D.S. Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu. Rev. Biochem. 2005, 74:219-245.
17. Gao Z., Zhang J., Bonasio R., Strino F., Sawai A., Parisi F., Kluger Y., Reinberg D. PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol. Cell 2012, 45:344-356.
18. Gardner K.E., Allis C.D., Strahl B.D. Operating on chromatin, a colorful language where context matters. J. Mol. Biol. 2011, 409:36-46.
19. Gehani S.S., Agrawal-Singh S., Dietrich N., Christophersen N.S., Helin K., Hansen K. Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol. Cell 2010, 39:886-900.
20. Graff J., Kim D., Dobbin M.M., Tsai L.H. Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiol. Rev. 2011, 91:603-649.
21. Guan J.S., Haggarty S.J., Giacometti E., Dannenberg J.H., Joseph N., Gao J., Nieland T.J., Zhou Y., Wang X., Mazitschek R., Bradner J.E., DePinho R.A., Jaenisch R., Tsai L.H. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009, 459:55-60.
22. He A., Ma Q., Cao J., von Gise A., Zhou P., Xie H., Zhang B., Hsing M., Christodoulou D.C., Cahan P., Daley G.Q., Kong S.W., Orkin S.H., Seidman C.E., Seidman J.G., Pu W.T. Polycomb repressive complex 2 regulates normal development of the mouse heart. Circ. Res. 2012, 110:406-415.
23. Henriquez B., Hepp M., Merino P., Sepulveda H., van Wijnen A.J., Lian J.B., Stein G.S., Stein J.L., Montecino M. C/EBPbeta binds the P1 promoter of the Runx2 gene and up-regulates Runx2 transcription in osteoblastic cells. J. Cell. Physiol. 2011, 226:3043-3052.
24. 2+-phosphate transfection efficiency in low-density neuronal cultures. Nat. Protoc. 2006, 1:695-700.
25. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
26. Laible G., Wolf A., Dorn R., Reuter G., Nislow C., Lebersorger A., Popkin D., Pillus L., Jenuwein T. Mammalian homologues of the polycomb-group gene enhancer of zeste mediate gene silencing in Drosophila heterochromatin and at S. cerevisiae telomeres. EMBO J. 1997, 16:3219-3232.
27. Lan F., Bayliss P.E., Rinn J.L., Whetstine J.R., Wang J.K., Chen S., Iwase S., Alpatov R., Issaeva I., Canaani E., Roberts T.M., Chang H.Y., Shi Y. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 2007, 449:689-694.
28. Lau P.N., Cheung P. Histone code pathway involving H3 S28 phosphorylation and K27 acetylation activates transcription and antagonizes polycomb silencing. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2801-2806.
29. Lund A.H., van Lohuizen M. Polycomb complexes and silencing mechanisms. Curr. Opin. Cell Biol. 2004, 16:239-246.
30. Margueron R., Reinberg D. The polycomb complex PRC2 and its mark in life. Nature 2011, 469:343-349.
31. Margueron R., Li G., Sarma K., Blais A., Zavadil J., Woodcock C.L., Dynlacht B.D., Reinberg D. Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol. Cell 2008, 32:503-518.
32. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., Lee W., Mendenhall E., O'Donovan A., Presser A., Russ C., Xie X., Meissner A., Wernig M., Jaenisch R., Nusbaum C., Lander E.S., Bernstein B.E. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
33. Mousavi K., Zare H., Wang A.H., Sartorelli V. Polycomb protein Ezh1 promotes RNA polymerase II elongation. Mol. Cell 2012, 45:255-262.
34. Nekrasov M., Klymenko T., Fraterman S., Papp B., Oktaba K., Kocher T., Cohen A., Stunnenberg H.G., Wilm M., Muller J. Pcl-PRC2 is needed to generate high levels of H3-K27 trimethylation at Polycomb target genes. EMBO J. 2007, 26:4078-4088.
35. Nunez-Villena F., Becerra A., Echeverria C., Briceno N., Porras O., Armisen R., Varela D., Montorfano I., Sarmiento D., Simon F. Increased expression of the transient receptor potential melastatin 7 channel is critically involved in lipopolysaccharide-induced reactive oxygen species-mediated neuronal death. Antioxid. Redox Signal. 2011, 15:2425-2438.
36. O'Meara M.M., Simon J.A. Inner workings and regulatory inputs that control polycomb repressive complex 2. Chromosoma 2012, 121:221-234.
37. Parrish J.Z., Emoto K., Jan L.Y., Jan Y.N. Polycomb genes interact with the tumor suppressor genes hippo and warts in the maintenance of Drosophila sensory neuron dendrites. Genes Dev. 2007, 21:956-972.
38. Pasini D., Malatesta M., Jung H.R., Walfridsson J., Willer A., Olsson L., Skotte J., Wutz A., Porse B., Jensen O.N., Helin K. Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of polycomb group target genes. Nucleic Acids Res. 2010, 38:4958-4969.
39. Pereira J.D., Sansom S.N., Smith J., Dobenecker M.W., Tarakhovsky A., Livesey F.J. Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15957-15962.
40. Sarma K., Margueron R., Ivanov A., Pirrotta V., Reinberg D. Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol. Cell. Biol. 2008, 28:2718-2731.
41. Schmitges F.W., Prusty A.B., Faty M., Stutzer A., Lingaraju G.M., Aiwazian J., Sack R., Hess D., Li L., Zhou S., Bunker R.D., Wirth U., Bouwmeester T., Bauer A., Ly-Hartig N., Zhao K., Chan H., Gu J., Gut H., Fischle W., Muller J., Thoma N.H. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 2011, 42:330-341.
42. Schwartz Y.B., Kahn T.G., Stenberg P., Ohno K., Bourgon R., Pirrotta V. Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet. 2010, 6:e1000805.
43. Seenundun S., Rampalli S., Liu Q.C., Aziz A., Palii C., Hong S., Blais A., Brand M., Ge K., Dilworth F.J. UTX mediates demethylation of H3K27me3 at muscle-specific genes during myogenesis. EMBO J. 2010, 29:1401-1411.
44. Sepulveda F.J., Bustos F.J., Inostroza E., Zuniga F.A., Neve R.L., Montecino M., van Zundert B. Differential roles of NMDA receptor subtypes NR2A and NR2B in dendritic branch development and requirement of RasGRF1. J. Neurophysiol. 2010, 103:1758-1770.
45. Shen X., Liu Y., Hsu Y.J., Fujiwara Y., Kim J., Mao X., Yuan G.C., Orkin S.H. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell 2008, 32:491-502.
46. Sher F., Boddeke E., Copray S. Ezh2 expression in astrocytes induces their dedifferentiation toward neural stem cells. Cell. Reprogram. 2011, 13:1-6.
47. Soutoglou E., Talianidis I. Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 2002, 295:1901-1904.
48. Sparmann A., van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer 2006, 6:846-856.
49. Stojic L., Jasencakova Z., Prezioso C., Stutzer A., Bodega B., Pasini D., Klingberg R., Mozzetta C., Margueron R., Puri P.L., Schwarzer D., Helin K., Fischle W., Orlando V. Chromatin regulated interchange between polycomb repressive complex 2 (PRC2)-Ezh2 and PRC2-Ezh1 complexes controls myogenin activation in skeletal muscle cells. Epigenetics Chromatin 2011, 4:16.
50. Tea J.S., Luo L. The chromatin remodeling factor Bap55 functions through the TIP60 complex to regulate olfactory projection neuron dendrite targeting. Neural Dev. 2011, 6:5.
51. Tie F., Banerjee R., Stratton C.A., Prasad-Sinha J., Stepanik V., Zlobin A., Diaz M.O., Scacheri P.C., Harte P.J. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila polycomb silencing. Development 2009, 136:3131-3141.
52. van Zundert B., Yoshii A., Constantine-Paton M. Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci. 2004, 27:428-437.
53. Varela-Nallar L., Grabowski C.P., Alfaro I.E., Alvarez A.R., Inestrosa N.C. Role of the Wnt receptor Frizzled-1 in presynaptic differentiation and function. Neural Dev. 2009, 4:41.
54. Weng M.K., Zimmer B., Pöltl D., Broeg M.P., Ivanova V., Gaspar J.A., Sachinidis A., Wüllner U., Waldmann T., Leist M. Extensive transcriptional regulation of chromatin modifiers during human neurodevelopment. PLoS One 2012, 7:e36708.
55. Wilke S.A., Hall B.J., Antonios J.K., Denardo L.A., Otto S., Yuan B., Chen F., Robbins E.M., Tiglio K., Williams M.E., Qiu Z., Biederer T., Ghosh A. NeuroD2 regulates the development of hippocampal mossy fiber synapses. Neural Dev. 2012, 7:9.
56. Xiao T., Hall H., Kizer K.O., Shibata Y., Hall M.C., Borchers C.H., Strahl B.D. Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 2003, 17:654-663.
57. Zaidi S.K., Young D.W., Montecino M.A., Lian J.B., Van Wijnen A.J., Stein J.L., Stein G.S. Mitotic bookmarking of genes: a novel dimension to epigenetic control. Nat. Rev. Genet. 2010, 11:583-589.
58. Zeng P.Y., Vakoc C.R., Chen Z.C., Blobel G.A., Berger S.L. In vivo dual cross-linking for identification of indirect DNA-associated proteins by chromatin immunoprecipitation. Biotechniques 2006, 41. (694, 696, 698).