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...

Full description

Bibliographic Details
Main Authors: Ryotaro Utsumi, Yuki Murata, Sayoko Ito-Harashima, Misaki Akai, Natsuko Miura, Kouichi Kuroda, Mitsuyoshi Ueda, Michihiko Kataoka
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0283002
_version_ 1797843262273224704
author Ryotaro Utsumi
Yuki Murata
Sayoko Ito-Harashima
Misaki Akai
Natsuko Miura
Kouichi Kuroda
Mitsuyoshi Ueda
Michihiko Kataoka
author_facet Ryotaro Utsumi
Yuki Murata
Sayoko Ito-Harashima
Misaki Akai
Natsuko Miura
Kouichi Kuroda
Mitsuyoshi Ueda
Michihiko Kataoka
author_sort Ryotaro Utsumi
collection DOAJ
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.
first_indexed 2024-04-09T17:02:18Z
format Article
id doaj.art-b0b937c83a3742d7aff019edfb424362
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-04-09T17:02:18Z
publishDate 2023-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-b0b937c83a3742d7aff019edfb4243622023-04-21T05:32:11ZengPublic Library of Science (PLoS)PLoS ONE1932-62032023-01-01184e028300210.1371/journal.pone.0283002Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies.Ryotaro UtsumiYuki MurataSayoko Ito-HarashimaMisaki AkaiNatsuko MiuraKouichi KurodaMitsuyoshi UedaMichihiko KataokaSpatial 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.https://doi.org/10.1371/journal.pone.0283002
spellingShingle Ryotaro Utsumi
Yuki Murata
Sayoko Ito-Harashima
Misaki Akai
Natsuko Miura
Kouichi Kuroda
Mitsuyoshi Ueda
Michihiko Kataoka
Foci-forming regions of pyruvate kinase and enolase at the molecular surface incorporate proteins into yeast cytoplasmic metabolic enzymes transiently assembling (META) bodies.
PLoS ONE
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
url https://doi.org/10.1371/journal.pone.0283002
work_keys_str_mv AT ryotaroutsumi fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT yukimurata fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT sayokoitoharashima fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT misakiakai fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT natsukomiura fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT kouichikuroda fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT mitsuyoshiueda fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies
AT michihikokataoka fociformingregionsofpyruvatekinaseandenolaseatthemolecularsurfaceincorporateproteinsintoyeastcytoplasmicmetabolicenzymestransientlyassemblingmetabodies