Evolution of lysine-specific demethylase 1 and REST corepressor gene families and their molecular interaction.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
14 Dec 2023
14 Dec 2023
Historique:
received:
26
11
2021
accepted:
30
11
2023
medline:
15
12
2023
pubmed:
15
12
2023
entrez:
14
12
2023
Statut:
epublish
Résumé
Lysine-specific demethylase 1A (LSD1) binds to the REST corepressor (RCOR) protein family of corepressors to erase transcriptionally active marks on histones. Functional diversity in these complexes depends on the type of RCOR included, which modulates the catalytic activity of the complex. Here, we studied the duplicative history of the RCOR and LSD gene families and analyzed the evolution of their interaction. We found that RCOR genes are the product of the two rounds of whole-genome duplications that occurred early in vertebrate evolution. In contrast, the origin of the LSD genes traces back before to the divergence of animals and plants. Using bioinformatics tools, we show that the RCOR and LSD1 interaction precedes the RCOR repertoire expansion that occurred in the last common ancestor of jawed vertebrates. Overall, we trace LSD1-RCOR complex evolution and propose that animal non-model species offer advantages in addressing questions about the molecular biology of this epigenetic complex.
Identifiants
pubmed: 38097664
doi: 10.1038/s42003-023-05652-x
pii: 10.1038/s42003-023-05652-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1267Subventions
Organisme : Fondo Nacional de Desarrollo Científico y Tecnológico (National Fund for Scientific and Technological Development)
ID : 1210471
Informations de copyright
© 2023. The Author(s).
Références
Shi, Y. et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941–953 (2004).
pubmed: 15620353
doi: 10.1016/j.cell.2004.12.012
Forneris, F., Binda, C., Vanoni, M. A., Battaglioli, E. & Mattevi, A. Human histone demethylase LSD1 reads the histone code. J. Biol. Chem. 280, 41360–41365 (2005).
pubmed: 16223729
doi: 10.1074/jbc.M509549200
Forneris, F., Binda, C., Adamo, A., Battaglioli, E. & Mattevi, A. Structural basis of LSD1-CoREST selectivity in histone H3 recognition. J. Biol. Chem. 282, 20070–20074 (2007).
pubmed: 17537733
doi: 10.1074/jbc.C700100200
Shi, Y.-J. et al. Regulation of LSD1 histone demethylase activity by its associated factors. Mol. Cell 19, 857–864 (2005).
pubmed: 16140033
doi: 10.1016/j.molcel.2005.08.027
Lee, M. G., Wynder, C., Cooch, N. & Shiekhattar, R. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 437, 432–435 (2005).
pubmed: 16079794
doi: 10.1038/nature04021
Barrios, Á. P. et al. Differential properties of transcriptional complexes formed by the CoREST family. Mol. Cell. Biol. 34, 2760–2770 (2014).
pubmed: 24820421
pmcid: 4097654
doi: 10.1128/MCB.00083-14
Yang, M. et al. Structural basis for CoREST-dependent demethylation of nucleosomes by the human LSD1 histone demethylase. Mol. Cell 23, 377–387 (2006).
pubmed: 16885027
doi: 10.1016/j.molcel.2006.07.012
Pilotto, S. et al. Interplay among nucleosomal DNA, histone tails, and corepressor CoREST underlies LSD1-mediated H3 demethylation. Proc. Natl Acad. Sci. USA. 112, 2752–2757 (2015).
pubmed: 25730864
pmcid: 4352788
doi: 10.1073/pnas.1419468112
Barrios, A. P. et al. Differential properties of transcriptional complexes formed by the CoREST family. Mol. Cell. Biol. 34, 2760–2770 (2014).
Ballas, N., Grunseich, C., Lu, D. D., Speh, J. C. & Mandel, G. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121, 645–657 (2005).
pubmed: 15907476
doi: 10.1016/j.cell.2005.03.013
Yao, H. et al. Corepressor Rcor1 is essential for murine erythropoiesis. Blood 123, 3175–3184 (2014).
pubmed: 24652990
pmcid: 4023423
doi: 10.1182/blood-2013-11-538678
Xiong, Y. et al. Inhibiting the coregulator CoREST impairs Foxp3 Treg function and promotes antitumor immunity. J. Clin. Invest. 130, 1830–1842 (2020).
Zhou, G., Du, T. & Roizman, B. HSV carrying WT REST establishes latency but reactivates only if the synthesis of REST is suppressed. Proc. Natl Acad. Sci. USA. 110, E498–E506 (2013).
pubmed: 23341636
pmcid: 3568314
doi: 10.1073/pnas.1222497110
Yang, P. et al. RCOR2 is a subunit of the LSD1 complex that regulates ESC property and substitutes for SOX2 in reprogramming somatic cells to pluripotency. Stem Cells 29, 791–801 (2011).
pubmed: 21433225
doi: 10.1002/stem.634
Wang, Y. et al. LSD1 co-repressor Rcor2 orchestrates neurogenesis in the developing mouse brain. Nat. Commun. 7, 10481 (2016).
pubmed: 26795843
pmcid: 4736047
doi: 10.1038/ncomms10481
Monaghan, C. E. et al. REST corepressors RCOR1 and RCOR2 and the repressor INSM1 regulate the proliferation-differentiation balance in the developing brain. Proc. Natl Acad. Sci. USA. 114, E406–E415 (2017).
pubmed: 28049845
pmcid: 5255626
doi: 10.1073/pnas.1620230114
Upadhyay, G., Chowdhury, A. H., Vaidyanathan, B., Kim, D. & Saleque, S. Antagonistic actions of Rcor proteins regulate LSD1 activity and cellular differentiation. Proc. Natl Acad. Sci. USA. 111, 8071–8076 (2014).
pubmed: 24843136
pmcid: 4050576
doi: 10.1073/pnas.1404292111
Zhou, X. & Ma, H. Evolutionary history of histone demethylase families: distinct evolutionary patterns suggest functional divergence. BMC Evol. Biol. 8, 294 (2008).
pubmed: 18950507
pmcid: 2579438
doi: 10.1186/1471-2148-8-294
Qiu, H., Hildebrand, F., Kuraku, S. & Meyer, A. Unresolved orthology and peculiar coding sequence properties of lamprey genes: the KCNA gene family as test case. BMC Genomics 12, 325 (2011).
pubmed: 21699680
pmcid: 3141671
doi: 10.1186/1471-2164-12-325
Smith, J. J. et al. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat. Genet. 45(415–421), 421e1–422e1 (2013).
Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017).
pubmed: 28387841
doi: 10.1093/molbev/msx116
Meyer, A. & Schartl, M. Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr. Opin. Cell Biol. 11, 699–704 (1999).
pubmed: 10600714
doi: 10.1016/S0955-0674(99)00039-3
McLysaght, A., Hokamp, K. & Wolfe, K. H. Extensive genomic duplication during early chordate evolution. Nat. Genet. 31, 200–204 (2002).
pubmed: 12032567
doi: 10.1038/ng884
Dehal, P. & Boore, J. L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314 (2005).
pubmed: 16128622
pmcid: 1197285
doi: 10.1371/journal.pbio.0030314
Hoegg, S. & Meyer, A. Hox clusters as models for vertebrate genome evolution. Trends Genet. 21, 421–424 (2005).
pubmed: 15967537
doi: 10.1016/j.tig.2005.06.004
Putnam, N. H. et al. The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064–1071 (2008).
pubmed: 18563158
doi: 10.1038/nature06967
Simakov, O. et al. Deeply conserved synteny resolves early events in vertebrate evolution. Nat. Ecol. Evol. 4, 820–830 (2020).
pubmed: 32313176
pmcid: 7269912
doi: 10.1038/s41559-020-1156-z
Nakatani, Y. et al. Reconstruction of proto-vertebrate, proto-cyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution. Nat. Commun. 12, 4489 (2021).
pubmed: 34301952
pmcid: 8302630
doi: 10.1038/s41467-021-24573-z
Ohno, S. Evolution by Gene Duplication (Springer Berlin Heidelberg, 1970).
Singh, P. P. & Isambert, H. OHNOLOGS v2: a comprehensive resource for the genes retained from whole genome duplication in vertebrates. Nucleic Acids Res. 48, D724–D730 (2020).
pubmed: 31612943
Roizman, B., Zhou, G. & Du, T. Checkpoints in productive and latent infections with herpes simplex virus 1: conceptualization of the issues. J. Neurovirol. 17, 512–517 (2011).
pubmed: 22052379
doi: 10.1007/s13365-011-0058-x
Xiong, Y. et al. Inhibiting the coregulator CoREST impairs Foxp3+ Treg function and promotes antitumor immunity. J. Clin. Invest. 130, 1830–1842 (2020).
pubmed: 31917688
pmcid: 7108912
doi: 10.1172/JCI131375
Fuentes, P., Cánovas, J., Berndt, F. A., Noctor, S. C. & Kukuljan, M. CoREST/LSD1 control the development of pyramidal cortical neurons. Cereb. Cortex 22, 1431–1441 (2012).
pubmed: 21878487
doi: 10.1093/cercor/bhr218
Zibetti, C. et al. Alternative splicing of the histone demethylase LSD1/KDM1 contributes to the modulation of neurite morphogenesis in the mammalian nervous system. J. Neurosci. 30, 2521–2532 (2010).
pubmed: 20164337
pmcid: 6634524
doi: 10.1523/JNEUROSCI.5500-09.2010
Rusconi, F. et al. LSD1 modulates stress-evoked transcription of immediate early genes and emotional behavior. Proc. Natl Acad. Sci. USA. 113, 3651–3656 (2016).
pubmed: 26976584
pmcid: 4822633
doi: 10.1073/pnas.1511974113
Wang, J. et al. LSD1n is an H4K20 demethylase regulating memory formation via transcriptional elongation control. Nat. Neurosci. 18, 1256–1264 (2015).
pubmed: 26214369
pmcid: 4625987
doi: 10.1038/nn.4069
Longaretti, A. et al. LSD1 is an environmental stress-sensitive negative modulator of the glutamatergic synapse. Neurobiol. Stress 13, 100280 (2020).
pubmed: 33457471
pmcid: 7794663
doi: 10.1016/j.ynstr.2020.100280
Tamaoki, J. et al. Splicing- and demethylase-independent functions of LSD1 in zebrafish primitive hematopoiesis. Sci. Rep. 10, 8521 (2020).
pubmed: 32444613
pmcid: 7244555
doi: 10.1038/s41598-020-65428-9
Hwang, I. et al. Far upstream element-binding protein 1 regulates LSD1 alternative splicing to promote terminal differentiation of neural progenitors. Stem Cell Rep. 10, 1208–1221 (2018).
doi: 10.1016/j.stemcr.2018.02.013
Rusconi, F. et al. LSD1 neurospecific alternative splicing controls neuronal excitability in mouse models of epilepsy. Cereb. Cortex 25, 2729–2740 (2015).
pubmed: 24735673
doi: 10.1093/cercor/bhu070
Ashkenazy, H. et al. ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res. 44, W344–W350 (2016).
pubmed: 27166375
pmcid: 4987940
doi: 10.1093/nar/gkw408
Ashkenazy, H., Erez, E., Martz, E., Pupko, T. & Ben-Tal, N. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38, W529–W533 (2010).
pubmed: 20478830
pmcid: 2896094
doi: 10.1093/nar/gkq399
Landau, M. et al. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33, W299–W302 (2005).
Paysan-Lafosse, T. et al. InterPro in 2022. Nucleic Acids Res. 51, D418–D427 (2023).
pubmed: 36350672
doi: 10.1093/nar/gkac993
Erdős, G., Pajkos, M. & Dosztányi, Z. IUPred3: prediction of protein disorder enhanced with unambiguous experimental annotation and visualization of evolutionary conservation. Nucleic Acids Res. 49, W297–W303 (2021).
pubmed: 34048569
pmcid: 8262696
doi: 10.1093/nar/gkab408
Hu, G. et al. flDPnn: accurate intrinsic disorder prediction with putative propensities of disorder functions. Nat. Commun. 12, 4438 (2021).
pubmed: 34290238
pmcid: 8295265
doi: 10.1038/s41467-021-24773-7
Høie, M. H. et al. NetSurfP-3.0: accurate and fast prediction of protein structural features by protein language models and deep learning. Nucleic Acids Res. 50, W510–W515 (2022).
pubmed: 35648435
pmcid: 9252760
doi: 10.1093/nar/gkac439
Musselman, C. A. & Kutateladze, T. G. Characterization of functional disordered regions within chromatin-associated proteins. iScience 24, 102070 (2021).
pubmed: 33604523
pmcid: 7873657
doi: 10.1016/j.isci.2021.102070
Hwang, S., Schmitt, A. A., Luteran, A. E., Toone, E. J. & McCafferty, D. G. Thermodynamic characterization of the binding interaction between the histone demethylase LSD1/KDM1 and CoREST. Biochemistry 50, 546–557 (2011).
pubmed: 21142040
doi: 10.1021/bi101776t
Kim, S.-A., Zhu, J., Yennawar, N., Eek, P. & Tan, S. Crystal structure of the LSD1/CoREST histone demethylase bound to its nucleosome substrate. Mol. Cell 78, 903–914.e4 (2020).
pubmed: 32396821
pmcid: 7275924
doi: 10.1016/j.molcel.2020.04.019
Song, Y. et al. Mechanism of crosstalk between the LSD1 demethylase and HDAC1 deacetylase in the CoREST complex. Cell Rep. 30, 2699–2711.e8 (2020).
pubmed: 32101746
pmcid: 7043024
doi: 10.1016/j.celrep.2020.01.091
Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022).
pubmed: 35637307
pmcid: 9184281
doi: 10.1038/s41592-022-01488-1
Evans, R. et al. Protein complex prediction with AlphaFold-Multimer. Preprint at bioRxiv 2021.10.04.463034 https://doi.org/10.1101/2021.10.04.463034 (2022).
Yates, A. D. et al. Ensembl 2020. Nucleic Acids Res. 48, D682–D688 (2020).
pubmed: 31691826
Herrero, J. et al. Ensembl comparative genomics resources. Database (Oxford) 2016, bav096 (2016).
Sharma, S. et al. The NCBI BioCollections Database. Database (Oxford) 2018, bay006 (2018).
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712
doi: 10.1016/S0022-2836(05)80360-2
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
pubmed: 25371430
doi: 10.1093/molbev/msu300
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Guindon, S. Bayesian estimation of divergence times from large sequence alignments. Mol. Biol. Evol. 27, 1768–1781 (2010).
pubmed: 20194424
doi: 10.1093/molbev/msq060
Anisimova, M. & Gascuel, O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 55, 539–552 (2006).
pubmed: 16785212
doi: 10.1080/10635150600755453
Minh, B. Q., Nguyen, M. A. T. & von Haeseler, A. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 30, 1188–1195 (2013).
pubmed: 23418397
pmcid: 3670741
doi: 10.1093/molbev/mst024
Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B. Q. & Vinh, L. S. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522 (2018).
pubmed: 29077904
doi: 10.1093/molbev/msx281
Tatusova, T. A. & Madden, T. L. BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174, 247–250 (1999).
pubmed: 10339815
doi: 10.1111/j.1574-6968.1999.tb13575.x
Schwartz, S. et al. PipMaker-a web server for aligning two genomic DNA sequences. Genome Res. 10, 577–586 (2000).
pubmed: 10779500
pmcid: 310868
doi: 10.1101/gr.10.4.577
Pupko, T., Bell, R. E., Mayrose, I., Glaser, F. & Ben-Tal, N. Rate4Site: an algorithmic tool for the identification of functional regions in proteins by surface mapping of evolutionary determinants within their homologues. Bioinformatics 18(Suppl 1), S71–S77 (2002).
pubmed: 12169533
doi: 10.1093/bioinformatics/18.suppl_1.S71
Mayrose, I., Graur, D., Ben-Tal, N. & Pupko, T. Comparison of site-specific rate-inference methods for protein sequences: empirical Bayesian methods are superior. Mol. Biol. Evol. 21, 1781–1791 (2004).
pubmed: 15201400
doi: 10.1093/molbev/msh194
Suyama, M., Torrents, D. & Bork, P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609–W612 (2006).
pubmed: 16845082
pmcid: 1538804
doi: 10.1093/nar/gkl315
Delsuc, F., Tsagkogeorga, G., Lartillot, N. & Philippe, H. Additional molecular support for the new chordate phylogeny. Genesis 46, 592–604 (2008).
pubmed: 19003928
doi: 10.1002/dvg.20450
Upham, N. S., Esselstyn, J. A. & Jetz, W. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol. 17, e3000494 (2019).
pubmed: 31800571
pmcid: 6892540
doi: 10.1371/journal.pbio.3000494
Prum, R. O. et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).
pubmed: 26444237
doi: 10.1038/nature15697
Hara, Y. et al. Shark genomes provide insights into elasmobranch evolution and the origin of vertebrates. Nat. Ecol. Evol. 2, 1761–1771 (2018).
pubmed: 30297745
doi: 10.1038/s41559-018-0673-5