A Specific LSD1/KDM1A Isoform Regulates Neuronal Differentiation through H3K9 Demethylation

Molecular Cell

Volumn 57, Issue 6, 2015, Pages 957-970

  Laurent, Benoit ^a,b   Ruitu, Lv ^c   Murn, Jernej ^a,b   Hempel, Kristina ^a,b   Ferrao, Ryan ^a,b,d   Xiang, Yang ^a,b   Liu, Shichong ^e   Garcia, Benjamin A ^e   Wu, Hao ^a,b,d   Wu, Feizhen ^c   Steen, Hanno ^a   Shi, Yang ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c FUDAN UNIVERSITY   (China)

^d Weill Graduate School of Medical Sciences of Cornell University   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; HISTONE H3; HISTONE H3K9; ISOPROTEIN; LYSINE SPECIFIC DEMETHYLASE 1; PROTEIN; SUPERVILLIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; HISTONE; HISTONE DEMETHYLASE; KDM1A PROTEIN, HUMAN; LYSINE; MEMBRANE PROTEIN; SVIL PROTEIN, HUMAN;

ALTERNATIVE RNA SPLICING; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; GENE EXPRESSION; HISTONE DEMETHYLATION; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; PROMOTER REGION; PROTEIN LOCALIZATION; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HELA CELL LINE; METABOLISM; METHYLATION; NERVE CELL;

ALTERNATIVE SPLICING; CELL DIFFERENTIATION; CELL MOVEMENT; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HISTONE DEMETHYLASES; HISTONES; HUMANS; LYSINE; MEMBRANE PROTEINS; METHYLATION; MICROFILAMENT PROTEINS; NEURONS; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS;

EID: 84925199744     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.01.010     Document Type: Article

References (42)

1. Andrés M.E., Burger C., Peral-Rubio M.J., Battaglioli E., Anderson M.E., Grimes J., Dallman J., Ballas N., Mandel G. CoREST: a functional corepressor required for regulation of neural-specific gene expression. Proc. Natl. Acad. Sci. USA 1999, 96:9873-9878.
2. Archer S.K., Claudianos C., Campbell H.D. Evolution of the gelsolin family of actin-binding proteins as novel transcriptional coactivators. Bioessays 2005, 27:388-396.
3. Ballas N., Battaglioli E., Atouf F., Andres M.E., Chenoweth J., Anderson M.E., Burger C., Moniwa M., Davie J.R., Bowers W.J., et al. Regulation of neuronal traits by a novel transcriptional complex. Neuron 2001, 31:353-365.
4. Baron R., Vellore N.A. LSD1/CoREST is an allosteric nanoscale clamp regulated by H3-histone-tail molecular recognition. Proc. Natl. Acad. Sci. USA 2012, 109:12509-12514.
5. Baron R., Vellore N.A. LSD1/CoREST reversible opening-closing dynamics: discovery of a nanoscale clamp for chromatin and protein binding. Biochemistry 2012, 51:3151-3153.
6. Bhuwania R., Cornfine S., Fang Z., Krüger M., Luna E.J., Linder S. Supervillin couples myosin-dependent contractility to podosomes and enables their turnover. J.Cell Sci. 2012, 125:2300-2314.
7. Busskamp V., Lewis N.E., Guye P., Ng A.H., Shipman S.L., Byrne S.M., Sanjana N.E., Murn J., Li Y., Li S., et al. Rapid neurogenesis through transcriptional activation in human stem cells. Mol. Syst. Biol. 2014, 10:760.
8. Chandra T., Kirschner K., Thuret J.Y., Pope B.D., Ryba T., Newman S., Ahmed K., Samarajiwa S.A., Salama R., Carroll T., et al. Independence of repressive histone marks and chromatin compaction during senescent heterochromatic layer formation. Mol. Cell 2012, 47:203-214.
9. Encinas M., Iglesias M., Liu Y., Wang H., Muhaisen A., Ceña V., Gallego C., Comella J.X. Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J.Neurochem. 2000, 75:991-1003.
10. Fang Z., Luna E.J. Supervillin-mediated suppression of p53 protein enhances cell survival. J.Biol. Chem. 2013, 288:7918-7929.
11. Fang Z., Takizawa N., Wilson K.A., Smith T.C., Delprato A., Davidson M.W., Lambright D.G., Luna E.J. The membrane-associated protein, supervillin, accelerates F-actin-dependent rapid integrin recycling and cell motility. Traffic 2010, 11:782-799.
12. Forneris F., Binda C., Vanoni M.A., Mattevi A., Battaglioli E. Histone demethylation catalysed by LSD1 is a flavin-dependent oxidative process. FEBS Lett. 2005, 579:2203-2207.
13. Forneris F., Binda C., Dall'Aglio A., Fraaije M.W., Battaglioli E., Mattevi A. A highly specific mechanism of histone H3-K4 recognition by histone demethylase LSD1. J.Biol. Chem. 2006, 281:35289-35295.
14. Forneris F., Binda C., Adamo A., Battaglioli E., Mattevi A. Structural basis of LSD1-CoREST selectivity in histone H3 recognition. J.Biol. Chem. 2007, 282:20070-20074.
15. Fuentes P., Cánovas J., Berndt F.A., Noctor S.C., Kukuljan M. CoREST/LSD1 control the development of pyramidal cortical neurons. Cereb. Cortex 2012, 22:1431-1441.
16. Garcia-Bassets I., Kwon Y.S., Telese F., Prefontaine G.G., Hutt K.R., Cheng C.S., Ju B.G., Ohgi K.A., Wang J., Escoubet-Lozach L., et al. Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell 2007, 128:505-518.
17. Hakimi M.A., Bochar D.A., Chenoweth J., Lane W.S., Mandel G., Shiekhattar R. A core-BRAF35 complex containing histone deacetylase mediates repression of neuronal-specific genes. Proc. Natl. Acad. Sci. USA 2002, 99:7420-7425.
18. Hou H., Yu H. Structural insights into histone lysine demethylation. Curr. Opin. Struct. Biol. 2010, 20:739-748.
19. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
20. Jie Z., Li T., Jia-Yun H., Qiu J., Ping-Yao Z., Houyan S. Trans-2-phenylcyclopropylamine induces nerve cells apoptosis in zebrafish mediated by depression of LSD1 activity. Brain Res. Bull. 2009, 80:79-84.
21. Le M.T., Xie H., Zhou B., Chia P.H., Rizk P., Um M., Udolph G., Yang H., Lim B., Lodish H.F. MicroRNA-125b promotes neuronal differentiation in human cells by repressing multiple targets. Mol. Cell. Biol. 2009, 29:5290-5305.
22. Metzger E., Wissmann M., Yin N., Müller J.M., Schneider R., Peters A.H., Günther T., Buettner R., Schüle R. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005, 437:436-439.
23. Nair S.S., Guo Z., Mueller J.M., Koochekpour S., Qiu Y., Tekmal R.R., Schüle R., Kung H.J., Kumar R., Vadlamudi R.K. Proline-, glutamic acid-, and leucine-rich protein-1/modulator of nongenomic activity of estrogen receptor enhances androgen receptor functions through LIM-only coactivator, four-and-a-half LIM-only protein 2. Mol. Endocrinol. 2007, 21:613-624.
24. Nair S.S., Nair B.C., Cortez V., Chakravarty D., Metzger E., Schüle R., Brann D.W., Tekmal R.R., Vadlamudi R.K. PELP1 is a reader of histone H3 methylation that facilitates oestrogen receptor-alpha target gene activation by regulating lysine demethylase 1 specificity. EMBO Rep. 2010, 11:438-444.
25. Nishida Y., Adati N., Ozawa R., Maeda A., Sakaki Y., Takeda T. Identification and classification of genes regulated by phosphatidylinositol 3-kinase- and TRKB-mediated signalling pathways during neuronal differentiation in two subtypes of the human neuroblastoma cell line SH-SY5Y. BMC Res. Notes 2008, 1:95.
26. Perillo B., Ombra M.N., Bertoni A., Cuozzo C., Sacchetti S., Sasso A., Chiariotti L., Malorni A., Abbondanza C., Avvedimento E.V. DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science 2008, 319:202-206.
27. Rudolph T., Yonezawa M., Lein S., Heidrich K., Kubicek S., Schäfer C., Phalke S., Walther M., Schmidt A., Jenuwein T., Reuter G. Heterochromatin formation in Drosophila is initiated through active removal of H3K4 methylation by the LSD1 homolog SU(VAR)3-3. Mol. Cell 2007, 26:103-115.
28. Rusconi F., Paganini L., Braida D., Ponzoni L., Toffolo E., Maroli A., Landsberger N., Bedogni F., Turco E., Pattini L., et al. LSD1 Neurospecific Alternative Splicing Controls Neuronal Excitability in Mouse Models of Epilepsy. Cereb Cortex. 2014, Published online April 15, 2014. 10.1093/cercor/bhu070.
29. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., Casero R.A., Shi Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
30. Shi Y.J., Matson C., Lan F., Iwase S., Baba T., Shi Y. Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell 2005, 19:857-864.
31. Smith T.C., Fang Z., Luna E.J. Novel interactors and a role for supervillin in early cytokinesis. Cytoskeleton (Hoboken) 2010, 67:346-364.
32. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
33. Sun G., Alzayady K., Stewart R., Ye P., Yang S., Li W., Shi Y. Histone demethylase LSD1 regulates neural stem cell proliferation. Mol. Cell. Biol. 2010, 30:1997-2005.
34. Sun G., Ye P., Murai K., Lang M.F., Li S., Zhang H., Li W., Fu C., Yin J., Wang A., et al. miR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cells. Nat. Commun. 2011, 2:529.
35. Ting H.J., Yeh S., Nishimura K., Chang C. Supervillin associates with androgen receptor and modulates its transcriptional activity. Proc. Natl. Acad. Sci. USA 2002, 99:661-666.
36. Toffolo E., Rusconi F., Paganini L., Tortorici M., Pilotto S., Heise C., Verpelli C., Tedeschi G., Maffioli E., Sala C., et al. Phosphorylation of neuronal Lysine-Specific Demethylase 1LSD1/KDM1A impairs transcriptional repression by regulating interaction with CoREST and histone deacetylases HDAC1/2. J.Neurochem. 2014, 128:603-616.
37. Vadlamudi R.K., Wang R.A., Mazumdar A., Kim Y., Shin J., Sahin A., Kumar R. Molecular cloning and characterization of PELP1, a novel human coregulator of estrogen receptor alpha. J.Biol. Chem. 2001, 276:38272-38279.
38. Wang J., Scully K., Zhu X., Cai L., Zhang J., Prefontaine G.G., Krones A., Ohgi K.A., Zhu P., Garcia-Bassets I., et al. Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 2007, 446:882-887.
39. Whyte W.A., Bilodeau S., Orlando D.A., Hoke H.A., Frampton G.M., Foster C.T., Cowley S.M., Young R.A. Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 2012, 482:221-225.
40. Wulfkuhle J.D., Donina I.E., Stark N.H., Pope R.K., Pestonjamasp K.N., Niswonger M.L., Luna E.J. Domain analysis of supervillin, an F-actin bundling plasma membrane protein with functional nuclear localization signals. J.Cell Sci. 1999, 112:2125-2136.
41. Yang M., Gocke C.B., Luo X., Borek D., Tomchick D.R., Machius M., Otwinowski Z., Yu H. Structural basis for CoREST-dependent demethylation of nucleosomes by the human LSD1 histone demethylase. Mol. Cell 2006, 23:377-387.
42. Zibetti C., Adamo A., Binda C., Forneris F., Toffolo E., Verpelli C., Ginelli E., Mattevi A., Sala C., Battaglioli E. Alternative splicing of the histone demethylase LSD1/KDM1 contributes to the modulation of neurite morphogenesis in the mammalian nervous system. J.Neurosci. 2010, 30:2521-2532.