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RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia

In hypoxic stress conditions, glycolysis enzymes assemble into singular cytoplasmic granules called glycolytic (G) bodies. G body formation in yeast correlates with increased glucose consumption and cell survival. However, the physical properties and organizing principles that define G body formatio...

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Autores principales: Fuller, Gregory G, Han, Ting, Freeberg, Mallory A, Moresco, James J, Ghanbari Niaki, Amirhossein, Roach, Nathan P, Yates, John R, Myong, Sua, Kim, John K
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7162659/
https://www.ncbi.nlm.nih.gov/pubmed/32298230
http://dx.doi.org/10.7554/eLife.48480
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author Fuller, Gregory G
Han, Ting
Freeberg, Mallory A
Moresco, James J
Ghanbari Niaki, Amirhossein
Roach, Nathan P
Yates, John R
Myong, Sua
Kim, John K
author_facet Fuller, Gregory G
Han, Ting
Freeberg, Mallory A
Moresco, James J
Ghanbari Niaki, Amirhossein
Roach, Nathan P
Yates, John R
Myong, Sua
Kim, John K
author_sort Fuller, Gregory G
collection PubMed
description In hypoxic stress conditions, glycolysis enzymes assemble into singular cytoplasmic granules called glycolytic (G) bodies. G body formation in yeast correlates with increased glucose consumption and cell survival. However, the physical properties and organizing principles that define G body formation are unclear. We demonstrate that glycolysis enzymes are non-canonical RNA binding proteins, sharing many common mRNA substrates that are also integral constituents of G bodies. Targeting nonspecific endoribonucleases to G bodies reveals that RNA nucleates G body formation and maintains its structural integrity. Consistent with a phase separation mechanism of biogenesis, recruitment of glycolysis enzymes to G bodies relies on multivalent homotypic and heterotypic interactions. Furthermore, G bodies fuse in vivo and are largely insensitive to 1,6-hexanediol, consistent with a hydrogel-like composition. Taken together, our results elucidate the biophysical nature of G bodies and demonstrate that RNA nucleates phase separation of the glycolysis machinery in response to hypoxic stress.
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spelling pubmed-71626592020-04-20 RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia Fuller, Gregory G Han, Ting Freeberg, Mallory A Moresco, James J Ghanbari Niaki, Amirhossein Roach, Nathan P Yates, John R Myong, Sua Kim, John K eLife Cell Biology In hypoxic stress conditions, glycolysis enzymes assemble into singular cytoplasmic granules called glycolytic (G) bodies. G body formation in yeast correlates with increased glucose consumption and cell survival. However, the physical properties and organizing principles that define G body formation are unclear. We demonstrate that glycolysis enzymes are non-canonical RNA binding proteins, sharing many common mRNA substrates that are also integral constituents of G bodies. Targeting nonspecific endoribonucleases to G bodies reveals that RNA nucleates G body formation and maintains its structural integrity. Consistent with a phase separation mechanism of biogenesis, recruitment of glycolysis enzymes to G bodies relies on multivalent homotypic and heterotypic interactions. Furthermore, G bodies fuse in vivo and are largely insensitive to 1,6-hexanediol, consistent with a hydrogel-like composition. Taken together, our results elucidate the biophysical nature of G bodies and demonstrate that RNA nucleates phase separation of the glycolysis machinery in response to hypoxic stress. eLife Sciences Publications, Ltd 2020-04-16 /pmc/articles/PMC7162659/ /pubmed/32298230 http://dx.doi.org/10.7554/eLife.48480 Text en © 2020, Fuller et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Fuller, Gregory G
Han, Ting
Freeberg, Mallory A
Moresco, James J
Ghanbari Niaki, Amirhossein
Roach, Nathan P
Yates, John R
Myong, Sua
Kim, John K
RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia
title RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia
title_full RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia
title_fullStr RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia
title_full_unstemmed RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia
title_short RNA promotes phase separation of glycolysis enzymes into yeast G bodies in hypoxia
title_sort rna promotes phase separation of glycolysis enzymes into yeast g bodies in hypoxia
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7162659/
https://www.ncbi.nlm.nih.gov/pubmed/32298230
http://dx.doi.org/10.7554/eLife.48480
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