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 evoluti...

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Autores: Guberovic, Iva, Hurtado-Bagès, Sarah, 1990-, Rivera Casas, Ciro, Knobloch, Gunnar, Malinverni, Roberto, Valero, Vanesa, Leger, Michelle M., Garcia, Jesús, Basquin, Jerome, Gómez de Cedron, Marta, Frigolé Vivas, Marta, Cheema, Manjinder S., Pérez, Ainhoa, Ausió, Juan, Ramírez de Molina, Ana, Salvatella i Giralt, Xavier, Ruiz Trillo, Iñaki, Eirin Lopez, Jose M., Ladurner, Andreas G., Buschbeck, Marcus
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2021
País:España
Institución:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:2445/183063
Acceso en línea:https://hdl.handle.net/2445/183063
Access Level:acceso abierto
Palabra clave:Cromatina
Metabolisme
Histones
Chromatin
Metabolism
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spelling Evolution of a histone variant involved in compartmental regulation of NAD metabolismGuberovic, IvaHurtado-Bagès, Sarah, 1990-Rivera Casas, CiroKnobloch, GunnarMalinverni, RobertoValero, VanesaLeger, Michelle M.Garcia, JesúsBasquin, JeromeGómez de Cedron, MartaFrigolé Vivas, MartaCheema, Manjinder S.Pérez, AinhoaAusió, JuanRamírez de Molina, AnaSalvatella i Giralt, XavierRuiz Trillo, IñakiEirin Lopez, Jose M.Ladurner, Andreas G.Buschbeck, MarcusCromatinaMetabolismeHistonesChromatinMetabolismHistonesNAD 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. MacroH2A histone variants originated before the split of fungi and animals. ADP-ribose binding is an ancestral feature of their macrodomains and is linked to the compartmental regulation of NAD metabolism. This function was selected for during the evolution of metazoans.2022202220212022info:eu-repo/semantics/articleinfo:eu-repo/semantics/acceptedVersion38application/pdfhttps://hdl.handle.net/2445/183063Articles publicats en revistes (Institut de Recerca Biomèdica (IRB Barcelona))reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésVersió postprint del document publicat a: https://doi.org/10.1038/s41594-021-00692-5Nature Structural & Molecular Biology, 2021, vol. 28, num. 12, p. 1009-1019https://doi.org/10.1038/s41594-021-00692-5info:eu-repo/grantAgreement/EC/H2020/675610(c) Guberovic, Iva et al., 2021info:eu-repo/semantics/openAccessoai:recercat.cat:2445/1830632026-05-29T05:05:01Z
dc.title.none.fl_str_mv Evolution of a histone variant involved in compartmental regulation of NAD metabolism
title Evolution of a histone variant involved in compartmental regulation of NAD metabolism
spellingShingle Evolution of a histone variant involved in compartmental regulation of NAD metabolism
Guberovic, Iva
Cromatina
Metabolisme
Histones
Chromatin
Metabolism
Histones
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
title_full_unstemmed 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
dc.creator.none.fl_str_mv Guberovic, Iva
Hurtado-Bagès, Sarah, 1990-
Rivera Casas, Ciro
Knobloch, Gunnar
Malinverni, Roberto
Valero, Vanesa
Leger, Michelle M.
Garcia, Jesús
Basquin, Jerome
Gómez de Cedron, Marta
Frigolé Vivas, Marta
Cheema, Manjinder S.
Pérez, Ainhoa
Ausió, Juan
Ramírez de Molina, Ana
Salvatella i Giralt, Xavier
Ruiz Trillo, Iñaki
Eirin Lopez, Jose M.
Ladurner, Andreas G.
Buschbeck, Marcus
author Guberovic, Iva
author_facet Guberovic, Iva
Hurtado-Bagès, Sarah, 1990-
Rivera Casas, Ciro
Knobloch, Gunnar
Malinverni, Roberto
Valero, Vanesa
Leger, Michelle M.
Garcia, Jesús
Basquin, Jerome
Gómez de Cedron, Marta
Frigolé Vivas, Marta
Cheema, Manjinder S.
Pérez, Ainhoa
Ausió, Juan
Ramírez de Molina, Ana
Salvatella i Giralt, Xavier
Ruiz Trillo, Iñaki
Eirin Lopez, Jose M.
Ladurner, Andreas G.
Buschbeck, Marcus
author_role author
author2 Hurtado-Bagès, Sarah, 1990-
Rivera Casas, Ciro
Knobloch, Gunnar
Malinverni, Roberto
Valero, Vanesa
Leger, Michelle M.
Garcia, Jesús
Basquin, Jerome
Gómez de Cedron, Marta
Frigolé Vivas, Marta
Cheema, Manjinder S.
Pérez, Ainhoa
Ausió, Juan
Ramírez de Molina, Ana
Salvatella i Giralt, Xavier
Ruiz Trillo, Iñaki
Eirin Lopez, Jose M.
Ladurner, Andreas G.
Buschbeck, Marcus
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Cromatina
Metabolisme
Histones
Chromatin
Metabolism
Histones
topic Cromatina
Metabolisme
Histones
Chromatin
Metabolism
Histones
description 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. MacroH2A histone variants originated before the split of fungi and animals. ADP-ribose binding is an ancestral feature of their macrodomains and is linked to the compartmental regulation of NAD metabolism. This function was selected for during the evolution of metazoans.
publishDate 2021
dc.date.none.fl_str_mv 2021
2022
2022
2022
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/acceptedVersion
format article
status_str acceptedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/183063
url https://hdl.handle.net/2445/183063
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Versió postprint del document publicat a: https://doi.org/10.1038/s41594-021-00692-5
Nature Structural & Molecular Biology, 2021, vol. 28, num. 12, p. 1009-1019
https://doi.org/10.1038/s41594-021-00692-5
info:eu-repo/grantAgreement/EC/H2020/675610
dc.rights.none.fl_str_mv (c) Guberovic, Iva et al., 2021
info:eu-repo/semantics/openAccess
rights_invalid_str_mv (c) Guberovic, Iva et al., 2021
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 38
application/pdf
dc.source.none.fl_str_mv Articles publicats en revistes (Institut de Recerca Biomèdica (IRB Barcelona))
reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.812429

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