Cargando…

Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies

Spatial reorganization of metabolic enzymes to form the “metabolic enzymes transiently assembling (META) body” is increasingly recognized as a mechanism contributing to regulation of cellular metabolism in response to environmental changes. A number of META body-forming enzymes, including enolase (E...

Descripción completa

Detalles Bibliográficos
Autores principales: Utsumi, Ryotaro, Murata, Yuki, Ito-Harashima, Sayoko, Akai, Misaki, Miura, Natsuko, Kuroda, Kouichi, Ueda, Mitsuyoshi, Kataoka, Michihiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10101385/
https://www.ncbi.nlm.nih.gov/pubmed/37053166
http://dx.doi.org/10.1371/journal.pone.0283002
_version_ 1785025501975281664
author Utsumi, Ryotaro
Murata, Yuki
Ito-Harashima, Sayoko
Akai, Misaki
Miura, Natsuko
Kuroda, Kouichi
Ueda, Mitsuyoshi
Kataoka, Michihiko
author_facet Utsumi, Ryotaro
Murata, Yuki
Ito-Harashima, Sayoko
Akai, Misaki
Miura, Natsuko
Kuroda, Kouichi
Ueda, Mitsuyoshi
Kataoka, Michihiko
author_sort Utsumi, Ryotaro
collection PubMed
description Spatial reorganization of metabolic enzymes to form the “metabolic enzymes transiently assembling (META) body” is increasingly recognized as a mechanism contributing to regulation of cellular metabolism in response to environmental changes. A number of META body-forming enzymes, including enolase (Eno2p) and phosphofructokinase, have been shown to contain condensate-forming regions. However, whether all META body-forming enzymes have condensate-forming regions or whether enzymes have multiple condensate-forming regions remains unknown. The condensate-forming regions of META body-forming enzymes have potential utility in the creation of artificial intracellular enzyme assemblies. In the present study, the whole sequence of yeast pyruvate kinase (Cdc19p) was searched for condensate-forming regions. Four peptide fragments comprising 27–42 amino acids were found to form condensates. Together with the fragment previously identified from Eno2p, these peptide regions were collectively termed “META body-forming sequences (METAfos).” METAfos-tagged yeast alcohol dehydrogenase (Adh1p) was found to co-localize with META bodies formed by endogenous Cdc19p under hypoxic conditions. The effect of Adh1p co-localization with META bodies on cell metabolism was further evaluated. Expression of Adh1p fused with a METAfos-tag increased production of ethanol compared to acetic acid, indicating that spatial reorganization of metabolic enzymes affects cell metabolism. These results contribute to understanding of the mechanisms and biological roles of META body formation.
format Online
Article
Text
id pubmed-10101385
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-101013852023-04-14 Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies Utsumi, Ryotaro Murata, Yuki Ito-Harashima, Sayoko Akai, Misaki Miura, Natsuko Kuroda, Kouichi Ueda, Mitsuyoshi Kataoka, Michihiko PLoS One Research Article Spatial reorganization of metabolic enzymes to form the “metabolic enzymes transiently assembling (META) body” is increasingly recognized as a mechanism contributing to regulation of cellular metabolism in response to environmental changes. A number of META body-forming enzymes, including enolase (Eno2p) and phosphofructokinase, have been shown to contain condensate-forming regions. However, whether all META body-forming enzymes have condensate-forming regions or whether enzymes have multiple condensate-forming regions remains unknown. The condensate-forming regions of META body-forming enzymes have potential utility in the creation of artificial intracellular enzyme assemblies. In the present study, the whole sequence of yeast pyruvate kinase (Cdc19p) was searched for condensate-forming regions. Four peptide fragments comprising 27–42 amino acids were found to form condensates. Together with the fragment previously identified from Eno2p, these peptide regions were collectively termed “META body-forming sequences (METAfos).” METAfos-tagged yeast alcohol dehydrogenase (Adh1p) was found to co-localize with META bodies formed by endogenous Cdc19p under hypoxic conditions. The effect of Adh1p co-localization with META bodies on cell metabolism was further evaluated. Expression of Adh1p fused with a METAfos-tag increased production of ethanol compared to acetic acid, indicating that spatial reorganization of metabolic enzymes affects cell metabolism. These results contribute to understanding of the mechanisms and biological roles of META body formation. Public Library of Science 2023-04-13 /pmc/articles/PMC10101385/ /pubmed/37053166 http://dx.doi.org/10.1371/journal.pone.0283002 Text en © 2023 Utsumi et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Utsumi, Ryotaro
Murata, Yuki
Ito-Harashima, Sayoko
Akai, Misaki
Miura, Natsuko
Kuroda, Kouichi
Ueda, Mitsuyoshi
Kataoka, Michihiko
Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies
title Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies
title_full Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies
title_fullStr Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies
title_full_unstemmed Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies
title_short Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies
title_sort foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (meta) bodies
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10101385/
https://www.ncbi.nlm.nih.gov/pubmed/37053166
http://dx.doi.org/10.1371/journal.pone.0283002
work_keys_str_mv AT utsumiryotaro fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT muratayuki fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT itoharashimasayoko fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT akaimisaki fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT miuranatsuko fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT kurodakouichi fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT uedamitsuyoshi fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT kataokamichihiko fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies