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Evolutionary perspective on mammalian inorganic polyphosphate (polyP) biology

Inorganic polyphosphate (polyP), the polymeric form of phosphate, is attracting ever-growing attention due to the many functions it appears to perform within mammalian cells. This essay does not aim to systematically review the copious mammalian polyP literature. Instead, we examined polyP synthesis...

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Detalles Bibliográficos
Autores principales: Borghi, Filipy, Saiardi, Adolfo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Portland Press Ltd. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10657179/
https://www.ncbi.nlm.nih.gov/pubmed/37844192
http://dx.doi.org/10.1042/BST20230483
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author Borghi, Filipy
Saiardi, Adolfo
author_facet Borghi, Filipy
Saiardi, Adolfo
author_sort Borghi, Filipy
collection PubMed
description Inorganic polyphosphate (polyP), the polymeric form of phosphate, is attracting ever-growing attention due to the many functions it appears to perform within mammalian cells. This essay does not aim to systematically review the copious mammalian polyP literature. Instead, we examined polyP synthesis and functions in various microorganisms and used an evolutionary perspective to theorise key issues of this field and propose solutions. By highlighting the presence of VTC4 in distinct species of very divergent eucaryote clades (Opisthokonta, Viridiplantae, Discoba, and the SAR), we propose that whilst polyP synthesising machinery was present in the ancestral eukaryote, most lineages subsequently lost it during evolution. The analysis of the bacteria-acquired amoeba PPK1 and its unique polyP physiology suggests that eukaryote cells must have developed mechanisms to limit cytosolic polyP accumulation. We reviewed the literature on polyP in the mitochondria from the perspective of its endosymbiotic origin from bacteria, highlighting how mitochondria could possess a polyP physiology reminiscent of their ‘bacterial’ beginning that is not yet investigated. Finally, we emphasised the similarities that the anionic polyP shares with the better-understood negatively charged polymers DNA and RNA, postulating that the nucleus offers an ideal environment where polyP physiology might thrive.
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spelling pubmed-106571792023-10-16 Evolutionary perspective on mammalian inorganic polyphosphate (polyP) biology Borghi, Filipy Saiardi, Adolfo Biochem Soc Trans Review Articles Inorganic polyphosphate (polyP), the polymeric form of phosphate, is attracting ever-growing attention due to the many functions it appears to perform within mammalian cells. This essay does not aim to systematically review the copious mammalian polyP literature. Instead, we examined polyP synthesis and functions in various microorganisms and used an evolutionary perspective to theorise key issues of this field and propose solutions. By highlighting the presence of VTC4 in distinct species of very divergent eucaryote clades (Opisthokonta, Viridiplantae, Discoba, and the SAR), we propose that whilst polyP synthesising machinery was present in the ancestral eukaryote, most lineages subsequently lost it during evolution. The analysis of the bacteria-acquired amoeba PPK1 and its unique polyP physiology suggests that eukaryote cells must have developed mechanisms to limit cytosolic polyP accumulation. We reviewed the literature on polyP in the mitochondria from the perspective of its endosymbiotic origin from bacteria, highlighting how mitochondria could possess a polyP physiology reminiscent of their ‘bacterial’ beginning that is not yet investigated. Finally, we emphasised the similarities that the anionic polyP shares with the better-understood negatively charged polymers DNA and RNA, postulating that the nucleus offers an ideal environment where polyP physiology might thrive. Portland Press Ltd. 2023-10-31 2023-10-16 /pmc/articles/PMC10657179/ /pubmed/37844192 http://dx.doi.org/10.1042/BST20230483 Text en © 2023 The Author(s) https://creativecommons.org/licenses/by/4.0/This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) . Open access for this article was enabled by the participation of University College London in an all-inclusive Read & Publish agreement with Portland Press and the Biochemical Society under a transformative agreement with JISC.
spellingShingle Review Articles
Borghi, Filipy
Saiardi, Adolfo
Evolutionary perspective on mammalian inorganic polyphosphate (polyP) biology
title Evolutionary perspective on mammalian inorganic polyphosphate (polyP) biology
title_full Evolutionary perspective on mammalian inorganic polyphosphate (polyP) biology
title_fullStr Evolutionary perspective on mammalian inorganic polyphosphate (polyP) biology
title_full_unstemmed Evolutionary perspective on mammalian inorganic polyphosphate (polyP) biology
title_short Evolutionary perspective on mammalian inorganic polyphosphate (polyP) biology
title_sort evolutionary perspective on mammalian inorganic polyphosphate (polyp) biology
topic Review Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10657179/
https://www.ncbi.nlm.nih.gov/pubmed/37844192
http://dx.doi.org/10.1042/BST20230483
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