- -

Comprehensive identification of SWI/SNF complex subunits underpins deep eukaryotic ancestry and reveals new plant components.

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

Comprehensive identification of SWI/SNF complex subunits underpins deep eukaryotic ancestry and reveals new plant components.

Mostrar el registro sencillo del ítem

Ficheros en el ítem

Thumbnail
Nombre: Hernandez-GarciaD ...
Tamaño: 2.014Mb
Formato: PDF
Descripción: Versión editorial
Abrir
dc.contributor.author Hernández-García, Jorge es_ES
dc.contributor.author Diego-Martín, Borja es_ES
dc.contributor.author Kuo, Peggy Hsuanyu es_ES
dc.contributor.author Jami-Alahmadi, Yasaman es_ES
dc.contributor.author Vashisht, Ajay A. es_ES
dc.contributor.author Wohlschlegel, James es_ES
dc.contributor.author Jacobsen, Steven E. es_ES
dc.contributor.author BLAZQUEZ RODRIGUEZ, MIGUEL ANGEL es_ES
dc.contributor.author Gallego-Bartolomé, Javier es_ES
dc.date.accessioned 2023-07-26T18:01:57Z
dc.date.available 2023-07-26T18:01:57Z
dc.date.issued 2022-06-06 es_ES
dc.identifier.uri http://hdl.handle.net/10251/195595
dc.description.abstract [EN] Over millions of years, eukaryotes evolved from unicellular to multicellular organisms with increasingly complex genomes and sophisticated gene expression networks. Consequently, chromatin regulators evolved to support this increased complexity. The ATP-dependent chromatin remodelers of the SWI/SNF family are multiprotein complexes that modulate nucleosome positioning and appear under different configurations, which perform distinct functions. While the composition, architecture, and activity of these subclasses are well understood in a limited number of fungal and animal model organisms, the lack of comprehensive information in other eukaryotic organisms precludes the identification of a reliable evolutionary model of SWI/SNF complexes. Here, we performed a systematic analysis using 36 species from animal, fungal, and plant lineages to assess the conservation of known SWI/SNF subunits across eukaryotes. We identified evolutionary relationships that allowed us to propose the composition of a hypothetical ancestral SWI/SNF complex in the last eukaryotic common ancestor. This last common ancestor appears to have undergone several rounds of lineage-specific subunit gains and losses, shaping the current conformation of the known subclasses in animals and fungi. In addition, our results unravel a plant SWI/SNF complex, reminiscent of the animal BAF subclass, which incorporates a set of plant-specific subunits of still unknown function. es_ES
dc.description.sponsorship We thank Ceejay Lee and Nathan Cai for their technical support. We thank Drs Jake Harris and Bruno Catarino for their critical reading of the manuscript. This work was supported by grants NIH Grant R35 GM130272 [to S.E.J.], RYC2018-024108-I [to J.G.-B.] funded by MCIN/AEI/10.13039/501100011033 and by "ESF Investing in your future", and PID2019-108577GA-I00 [to J.G.-B.] and PID2019-110717GB [to M.A.B.] funded by MCIN/AEI/10.13039/501100011033. S.E.J. is a Howard Hughes Medical Institute investigator. es_ES
dc.language Inglés es_ES
dc.publisher Springer Nature es_ES
dc.relation.ispartof Communications Biology es_ES
dc.rights Reconocimiento (by) es_ES
dc.title Comprehensive identification of SWI/SNF complex subunits underpins deep eukaryotic ancestry and reveals new plant components. es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1038/s42003-022-03490-x es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-108577GA-I00/ES/FUNCION DE LAS PROTEINS PHD EN COMPLEJOS DE REMODELACION DE CROMATINA SWI%2FSNF EN PLANTAS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/NIH//R35 GM130272/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110717GB-I00/ES/EVOLUCION DEL MECANISMO DE INTEGRACION DE LA SEÑALIZACION POR LUZ Y TEMPERATURA EN PLANTAS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MICINN//RYC2018-024108-I/ es_ES
dc.rights.accessRights Abierto es_ES
dc.description.bibliographicCitation Hernández-García, J.; Diego-Martín, B.; Kuo, PH.; Jami-Alahmadi, Y.; Vashisht, AA.; Wohlschlegel, J.; Jacobsen, SE.... (2022). Comprehensive identification of SWI/SNF complex subunits underpins deep eukaryotic ancestry and reveals new plant components. Communications Biology. 5(1):1-11. https://doi.org/10.1038/s42003-022-03490-x es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1038/s42003-022-03490-x es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 11 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 5 es_ES
dc.description.issue 1 es_ES
dc.identifier.eissn 2399-3642 es_ES
dc.identifier.pmid 35668117 es_ES
dc.identifier.pmcid PMC9170682 es_ES
dc.relation.pasarela S\487322 es_ES
dc.contributor.funder European Social Fund es_ES
dc.contributor.funder Howard Hughes Medical Institute es_ES
dc.contributor.funder Agencia Estatal de Investigación es_ES
dc.contributor.funder Ministerio de Ciencia e Innovación es_ES
dc.contributor.funder National Institutes of Health, EEUU es_ES
dc.description.references Clapier, C. R. Sophisticated conversations between chromatin and chromatin remodelers, and dissonances in cancer. Int. J. Mol. Sci. https://doi.org/10.3390/ijms22115578 (2021). es_ES
dc.description.references Kadoch, C. & Crabtree, G. R. Mammalian SWI/SNF chromatin remodeling complexes and cancer: Mechanistic insights gained from human genomics. Sci. Adv. 1, e1500447 (2015). es_ES
dc.description.references Jerzmanowski, A. SWI/SNF chromatin remodeling and linker histones in plants. Biochim. Biophys. Acta 1769, 330–345 (2007). es_ES
dc.description.references Dingwall, A. K. et al. The Drosophila snr1 and brm proteins are related to yeast SWI/SNF proteins and are components of a large protein complex. Mol. Biol. Cell 6, 777–791 (1995). es_ES
dc.description.references Stern, M., Jensen, R. & Herskowitz, I. Five SWI genes are required for expression of the HO gene in yeast. J. Mol. Biol. 178, 853–868 (1984). es_ES
dc.description.references Sarnowska, E. et al. The role of SWI/SNF chromatin remodeling complexes in hormone crosstalk. Trends Plant Sci. 21, 594–608 (2016). es_ES
dc.description.references Ho, L. & Crabtree, G. R. Chromatin remodelling during development. Nature 463, 474–484 (2010). es_ES
dc.description.references Hodges, C., Kirkland, J. G. & Crabtree, G. R. The many roles of BAF (mSWI/SNF) and PBAF complexes in cancer. Cold Spring Harbor Perspect. Med. https://doi.org/10.1101/cshperspect.a026930 (2016). es_ES
dc.description.references Wang, W. et al. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 15, 5370–5382 (1996). es_ES
dc.description.references Kadoch, C. et al. Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet. 45, 592–601 (2013). es_ES
dc.description.references Alpsoy, A. & Dykhuizen, E. C. Glioma tumor suppressor candidate region gene 1 (GLTSCR1) and its paralog GLTSCR1-like form SWI/SNF chromatin remodeling subcomplexes. J. Biol. Chem. 293, 3892–3903 (2018). es_ES
dc.description.references Wang, X. et al. BRD9 defines a SWI/SNF sub-complex and constitutes a specific vulnerability in malignant rhabdoid tumors. Nat. Commun. 10, 1881 (2019). es_ES
dc.description.references Michel, B. C. et al. A non-canonical SWI/SNF complex is a synthetic lethal target in cancers driven by BAF complex perturbation. Nat. Cell Biol. 20, 1410–1420 (2018). es_ES
dc.description.references Pan, J. et al. Interrogation of mammalian protein complex structure, function, and membership using genome-scale fitness screens. Cell Syst. 6, 555–568 (2018). e557. es_ES
dc.description.references Lessard, J. et al. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55, 201–215 (2007). es_ES
dc.description.references Ho, L. et al. An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc. Natl Acad. Sci. USA 106, 5181–5186 (2009). es_ES
dc.description.references Staahl, B. T. et al. Kinetic analysis of npBAF to nBAF switching reveals exchange of SS18 with CREST and integration with neural developmental pathways. J. Neurosci. 33, 10348–10361 (2013). es_ES
dc.description.references Wilsker, D. et al. Nomenclature of the ARID family of DNA-binding proteins. Genomics 86, 242–251 (2005). es_ES
dc.description.references Nie, Z. et al. A specificity and targeting subunit of a human SWI/SNF family-related chromatin-remodeling complex. Mol. Cell. Biol. 20, 8879–8888 (2000). es_ES
dc.description.references Mohrmann, L. et al. Differential targeting of two distinct SWI/SNF-related Drosophila chromatin-remodeling complexes. Mol. Cell. Biol. 24, 3077–3088 (2004). es_ES
dc.description.references Satterwhite, E. et al. The BCL11 gene family: involvement of BCL11A in lymphoid malignancies. Blood 98, 3413–3420 (2001). es_ES
dc.description.references Xue, Y. et al. The human SWI/SNF-B chromatin-remodeling complex is related to yeast rsc and localizes at kinetochores of mitotic chromosomes. Proc. Natl Acad. Sci. USA 97, 13015–13020 (2000). es_ES
dc.description.references Cairns, B. R. et al. Two functionally distinct forms of the RSC nucleosome-remodeling complex, containing essential AT hook, BAH, and bromodomains. Mol. Cell 4, 715–723 (1999). es_ES
dc.description.references Wang, W. et al. Architectural DNA binding by a high-mobility-group/kinesin-like subunit in mammalian SWI/SNF-related complexes. Proc. Natl Acad. Sci. USA 95, 492–498 (1998). es_ES
dc.description.references Monahan, B. J. et al. Fission yeast SWI/SNF and RSC complexes show compositional and functional differences from budding yeast. Nat. Struct. Mol. Biol. 15, 873–880 (2008). es_ES
dc.description.references Papoulas, O. et al. The HMG-domain protein BAP111 is important for the function of the BRM chromatin-remodeling complex in vivo. Proc. Natl Acad. Sci. USA 98, 5728–5733 (2001). es_ES
dc.description.references Vercruyssen, L. et al. ANGUSTIFOLIA3 binds to SWI/SNF chromatin remodeling complexes to regulate transcription during Arabidopsis leaf development. Plant Cell 26, 210–229 (2014). es_ES
dc.description.references Jarończyk, K. et al. Bromodomain-containing subunits BRD1, BRD2, and BRD13 are required for proper functioning of SWI/SNF complexes in Arabidopsis. Plant Commun. 2, 100174 (2021). es_ES
dc.description.references Yu, Y. et al. Bromodomain-containing proteins BRD1, BRD2, and BRD13 are core subunits of SWI/SNF complexes and vital for their genomic targeting in Arabidopsis. Mol. Plant 14, 888–904 (2021). es_ES
dc.description.references Nelissen, H. et al. Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf. Plant Cell 27, 1605–1619 (2015). es_ES
dc.description.references Yu, Y. et al. BRAHMA-interacting proteins BRIP1 and BRIP2 are core subunits of Arabidopsis SWI/SNF complexes. Nat. Plants 6, 996–1007 (2020). es_ES
dc.description.references Kim, J. H. & Tsukaya, H. Regulation of plant growth and development by the GROWTH-REGULATING FACTOR and GRF-INTERACTING FACTOR duo. J. Exp. Bot. 66, 6093–6107 (2015). es_ES
dc.description.references Wilson, B., Erdjument-Bromage, H., Tempst, P. & Cairns, B. R. The RSC chromatin remodeling complex bears an essential fungal-specific protein module with broad functional roles. Genetics 172, 795–809 (2006). es_ES
dc.description.references Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845–858 (2015). es_ES
dc.description.references Lu, R. & Wang, G. G. Tudor: a versatile family of histone methylation ‘readers’. Trends Biochem. Sci. 38, 546–555 (2013). es_ES
dc.description.references Buszewicz, D. et al. HD2C histone deacetylase and a SWI/SNF chromatin remodelling complex interact and both are involved in mediating the heat stress response in Arabidopsis. Plant Cell Environ. 39, 2108–2122 (2016). es_ES
dc.description.references Zhang, H. et al. DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. Proc. Natl Acad. Sci. USA 110, 8290–8295 (2013). es_ES
dc.description.references Pandey, R. et al. Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res. 30, 5036–5055 (2002). es_ES
dc.description.references Marcum, R. D., Reyes, A. A. & He, Y. Structural insights into the evolutionarily conserved BAF chromatin remodeling complex. Biology https://doi.org/10.3390/biology9070146 (2020). es_ES
dc.description.references Mani, U., Goutham, R. N. A. & Mohan, S. S. SWI/SNF infobase-an exclusive information portal for SWI/SNF remodeling complex subunits. PLoS ONE 12, e0184445 (2017). es_ES
dc.description.references He, S. et al. Structure of nucleosome-bound human BAF complex. Science 367, 875–881 (2020). es_ES
dc.description.references Mashtalir, N. et al. A structural model of the endogenous human BAF complex informs disease mechanisms. Cell 183, 802–817 (2020). e824. es_ES
dc.description.references Wang, C. et al. Structure of the yeast Swi/Snf complex in a nucleosome free state. Nat. Commun. 11, 3398 (2020). es_ES
dc.description.references Han, Y., Reyes, A. A., Malik, S. & He, Y. Cryo-EM structure of SWI/SNF complex bound to a nucleosome. Nature 579, 452–455 (2020). es_ES
dc.description.references Ye, Y. et al. Structure of the RSC complex bound to the nucleosome. Science 366, 838–843 (2019). es_ES
dc.description.references Sang, Y. et al. Mutations in two non-canonical Arabidopsis SWI2/SNF2 chromatin remodeling ATPases cause embryogenesis and stem cell maintenance defects. Plant J. 72, 1000–1014 (2012). es_ES
dc.description.references Law, J. A. et al. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498, 385–389 (2013). es_ES
dc.description.references Clayton, C. Regulation of gene expression in trypanosomatids: living with polycistronic transcription. Open Biol. 9, 190072 (2019). es_ES
dc.description.references Wallace, I. M., O’Sullivan, O., Higgins, D. G. & Notredame, C. M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res. 34, 1692–1699 (2006). es_ES
dc.description.references Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010). es_ES
dc.description.references Wongpalee, S. P. et al. CryoEM structures of Arabidopsis DDR complexes involved in RNA-directed DNA methylation. Nat. Commun. 10, 3916 (2019). es_ES
dc.description.references Jami-Alahmadi, Y., Pandey, V., Mayank, A. K. & Wohlschlegel, J. A. A robust method for packing high resolution C18 RP-nano-HPLC columns. J. Vis. Exp. https://doi.org/10.3791/62380 (2021). es_ES
dc.description.references Izquierdo-González, J. J. et al. Proteomic analysis of goat milk kefir: profiling the fermentation-time dependent protein digestion and identification of potential peptides with biological activity. Food Chem. 295, 456–465 (2019). es_ES
dc.description.references Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008). es_ES
dc.description.references Curtis, M. D. & Grossniklaus, U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462–469 (2003). es_ES
dc.description.references Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021). es_ES
dc.description.references Pettersen, E. F. et al. UCSF chimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021). es_ES


Este ítem aparece en la(s) siguiente(s) colección(ones)

Mostrar el registro sencillo del ítem