Evolution of a histone variant involved in compartmental regulation of NAD metabolism
NAD metabolism is essential for all forms of life. Compartmental regulation of NAD consumption, especially between the nucleus and the mitochondria, is required for energy homeostasis. However, how compartmental regulation evolved remains unclear. In the present study, we investigated the evolution of the macrodomain-containing histone variant macroH2A1.1, an integral chromatin component that limits nuclear NAD consumption by inhibiting poly(ADP-ribose) polymerase 1 in vertebrate cells. We found that macroH2A originated in premetazoan protists. The crystal structure of the macroH2A macrodomain from the protist Capsaspora owczarzaki allowed us to identify highly conserved principles of ligand binding and pinpoint key residue substitutions, selected for during the evolution of the vertebrate stem lineage. Metabolic characterization of the Capsaspora lifecycle suggested that the metabolic function of macroH2A was associated with nonproliferative stages. Taken together, we provide insight into the evolution of a chromatin element involved in compartmental NAD regulation, relevant for understanding its metabolism and potential therapeutic applications.
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Nature Publishing Group
2021-12-09
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Subjects: | Histone variants, Metabolism, X-ray crystallography, |
Online Access: | http://hdl.handle.net/10261/263537 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100005774 http://dx.doi.org/10.13039/501100004189 http://dx.doi.org/10.13039/501100002809 http://dx.doi.org/10.13039/100012818 |
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Histone variants Metabolism X-ray crystallography Histone variants Metabolism X-ray crystallography |
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Histone variants Metabolism X-ray crystallography Histone variants Metabolism X-ray crystallography Guberovic, Iva Hurtado-Bagès, Sarah Rivera-Casas, Ciro Knobloch, Gunnar Malinverni, Roberto Valero, Vanesa Leger, Michelle M. García, Jesús Basquin, Jerome Gómez de Cedrón, Marta Frigolé-Vivas, Marta Cheema, Manjinder S. Pérez, Ainhoa Ausió, Juan Ramírez de Molina, Ana Salvatella, Xavier Ruiz-Trillo, Iñaki Eirín-López, José María Ladurner, Andreas G. Buschbeck, Marcus Evolution of a histone variant involved in compartmental regulation of NAD metabolism |
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NAD metabolism is essential for all forms of life. Compartmental regulation of NAD consumption, especially between the nucleus and the mitochondria, is required for energy homeostasis. However, how compartmental regulation evolved remains unclear. In the present study, we investigated the evolution of the macrodomain-containing histone variant macroH2A1.1, an integral chromatin component that limits nuclear NAD consumption by inhibiting poly(ADP-ribose) polymerase 1 in vertebrate cells. We found that macroH2A originated in premetazoan protists. The crystal structure of the macroH2A macrodomain from the protist Capsaspora owczarzaki allowed us to identify highly conserved principles of ligand binding and pinpoint key residue substitutions, selected for during the evolution of the vertebrate stem lineage. Metabolic characterization of the Capsaspora lifecycle suggested that the metabolic function of macroH2A was associated with nonproliferative stages. Taken together, we provide insight into the evolution of a chromatin element involved in compartmental NAD regulation, relevant for understanding its metabolism and potential therapeutic applications. |
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Max Planck Society |
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Max Planck Society Guberovic, Iva Hurtado-Bagès, Sarah Rivera-Casas, Ciro Knobloch, Gunnar Malinverni, Roberto Valero, Vanesa Leger, Michelle M. García, Jesús Basquin, Jerome Gómez de Cedrón, Marta Frigolé-Vivas, Marta Cheema, Manjinder S. Pérez, Ainhoa Ausió, Juan Ramírez de Molina, Ana Salvatella, Xavier Ruiz-Trillo, Iñaki Eirín-López, José María Ladurner, Andreas G. Buschbeck, Marcus |
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Histone variants Metabolism X-ray crystallography |
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Guberovic, Iva Hurtado-Bagès, Sarah Rivera-Casas, Ciro Knobloch, Gunnar Malinverni, Roberto Valero, Vanesa Leger, Michelle M. García, Jesús Basquin, Jerome Gómez de Cedrón, Marta Frigolé-Vivas, Marta Cheema, Manjinder S. Pérez, Ainhoa Ausió, Juan Ramírez de Molina, Ana Salvatella, Xavier Ruiz-Trillo, Iñaki Eirín-López, José María Ladurner, Andreas G. Buschbeck, Marcus |
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Guberovic, Iva |
title |
Evolution of a histone variant involved in compartmental regulation of NAD metabolism |
title_short |
Evolution of a histone variant involved in compartmental regulation of NAD metabolism |
title_full |
Evolution of a histone variant involved in compartmental regulation of NAD metabolism |
title_fullStr |
Evolution of a histone variant involved in compartmental regulation of NAD metabolism |
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Evolution of a histone variant involved in compartmental regulation of NAD metabolism |
title_sort |
evolution of a histone variant involved in compartmental regulation of nad metabolism |
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Nature Publishing Group |
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2021-12-09 |
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http://hdl.handle.net/10261/263537 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100005774 http://dx.doi.org/10.13039/501100004189 http://dx.doi.org/10.13039/501100002809 http://dx.doi.org/10.13039/100012818 |
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dig-ibe-es-10261-2635372022-11-15T16:32:26Z Evolution of a histone variant involved in compartmental regulation of NAD metabolism Guberovic, Iva Hurtado-Bagès, Sarah Rivera-Casas, Ciro Knobloch, Gunnar Malinverni, Roberto Valero, Vanesa Leger, Michelle M. García, Jesús Basquin, Jerome Gómez de Cedrón, Marta Frigolé-Vivas, Marta Cheema, Manjinder S. Pérez, Ainhoa Ausió, Juan Ramírez de Molina, Ana Salvatella, Xavier Ruiz-Trillo, Iñaki Eirín-López, José María Ladurner, Andreas G. Buschbeck, Marcus Max Planck Society Universidad de Barcelona Ministerio de Economía y Competitividad (España) Comunidad de Madrid La Caixa Generalitat de Catalunya Histone variants Metabolism X-ray crystallography NAD metabolism is essential for all forms of life. Compartmental regulation of NAD consumption, especially between the nucleus and the mitochondria, is required for energy homeostasis. However, how compartmental regulation evolved remains unclear. In the present study, we investigated the evolution of the macrodomain-containing histone variant macroH2A1.1, an integral chromatin component that limits nuclear NAD consumption by inhibiting poly(ADP-ribose) polymerase 1 in vertebrate cells. We found that macroH2A originated in premetazoan protists. The crystal structure of the macroH2A macrodomain from the protist Capsaspora owczarzaki allowed us to identify highly conserved principles of ligand binding and pinpoint key residue substitutions, selected for during the evolution of the vertebrate stem lineage. Metabolic characterization of the Capsaspora lifecycle suggested that the metabolic function of macroH2A was associated with nonproliferative stages. Taken together, we provide insight into the evolution of a chromatin element involved in compartmental NAD regulation, relevant for understanding its metabolism and potential therapeutic applications. For technical support, we thank the research service facilities of IJC and IGTP, the Crystallization Facility of the Max Planck Institute of Biochemistry, the ICTS NMR facility from the Scientific and Technological Centres of the University of Barcelona and Biophysics Core Facility of BMC-LMU. I.G. was a fellow of the Marie Skłodowska Curie Training network ‘ChroMe’ (H2020-MSCA-ITN-2015-675610, awarded to M.B. and A.G.L.). The project was further supported by national grants (nos. RTI2018-094005-B-I00 and BFU2015-66559-P from FEDER/Ministerio de Ciencia e Innovación—Agencia Estatal de Investigación to M.B.). Research in the participating labs was further supported by the following grants: the Marie Skłodowska Curie Training network ‘INTERCEPT-MDS’ no. H2020-MSCA-ITN-2020-953407 (to M.B.), MINECO-ISCIII no. PIE16/00011 (to M.B.); the Deutsche José Carreras Leukämie Stiftung DJCLS (no. 14R/2018 to M.B.), AGAUR (no. 2017-SGR-305 to M.B.), Fundació La Marató de TV3 (no. 257/C/2019 to M.B.), German Research Foundation Project (ID 213249687—SFB 1064 and Project ID 325871075—SFB 1309 to A.G.L.), the Spanish Ministry of Science (PID2019-110183RB-C21 to A.R.M.), Community of Madrid (P2018/BAA-4343-ALIBIRD2020-CM to A.R.M), Ramón Areces Foundation (to A.R.M.), National Science Foundation (EF-1921402 to J.M.E.L.), 2015 International Doctoral Fellowship La Caixa-Severo Ochoa (to M.F.V.), Marie Skłodowska-Curie Individual Fellowship (no. 747789 to M.M.L.), Juan de la Cierva-Incorporación (IJC2018-036657-I to M.M.L., ERC-2012-CoG-616960 to I.R.T.), MINECO (BFU2017-90114-P to I.R.T.), AGAUR (2017-SGR-324 to X.S.) and MINECO (BIO2015-70092-R and ERC-2014-CoG-648201 to X.S.). Research at the IJC is supported by the ‘La Caixa’ Foundation, Fundació Internacional Josep Carreras, Celgene Spain and the CERCA Programme/Generalitat de Catalunya. 2022-03-09T13:40:02Z 2022-03-09T13:40:02Z 2021-12-09 2022-03-09T13:40:03Z artículo http://purl.org/coar/resource_type/c_6501 doi: 10.1038/s41594-021-00692-5 issn: 1545-9985 Nature Structural and Molecular Biology 28: 1009-1019 (2021) http://hdl.handle.net/10261/263537 10.1038/s41594-021-00692-5 http://dx.doi.org/10.13039/501100003329 http://dx.doi.org/10.13039/501100005774 http://dx.doi.org/10.13039/501100004189 http://dx.doi.org/10.13039/501100002809 http://dx.doi.org/10.13039/100012818 #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-110183RB-C21/ES/DESARROLLO DE FORMULAS ALIMENTARIAS DE PRECISION DIRIGIDAS AL TRATAMIENTO DEL CANCER DE COLON: DISEÑO Y VALIDACION/ info:eu-repo/grantAgreement/EC/H2020/675610 info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RTI2018-094005-B-I00/ES/REGULACION DE LA ARQUITECTURA TRIDIMENSIONAL DE LA CROMATINA POR PARTE DE LAS VARIANTES DE HISTONA MACROH2A Y SU CAPACIDAD DE UNIR METABOLITOS/ http://doi.org/10.1038/s41594-021-00692-5 Sí none Nature Publishing Group |