Polyamines mediate cellular energetics and lipid metabolism through mitochondrial respiration to facilitate virus replication.

Polyamines are critical cellular components that regulate a variety of processes, including translation, cell cycling, and nucleic acid metabolism. The polyamines, putrescine, spermidine, and spermine, are found abundantly within cells and are positively-charged at physiological pH. Polyamine metabo...

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Main Authors: Yazmin E Cruz-Pulido, Natalie J LoMascolo, Delaina May, Jomana Hatahet, Caroline E Thomas, Andrea K W Chu, Samantha P Stacey, Maria Del Mar Villanueva Guzman, Gregory Aubert, Bryan C Mounce
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-11-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1012711
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author Yazmin E Cruz-Pulido
Natalie J LoMascolo
Delaina May
Jomana Hatahet
Caroline E Thomas
Andrea K W Chu
Samantha P Stacey
Maria Del Mar Villanueva Guzman
Gregory Aubert
Bryan C Mounce
author_facet Yazmin E Cruz-Pulido
Natalie J LoMascolo
Delaina May
Jomana Hatahet
Caroline E Thomas
Andrea K W Chu
Samantha P Stacey
Maria Del Mar Villanueva Guzman
Gregory Aubert
Bryan C Mounce
author_sort Yazmin E Cruz-Pulido
collection DOAJ
description Polyamines are critical cellular components that regulate a variety of processes, including translation, cell cycling, and nucleic acid metabolism. The polyamines, putrescine, spermidine, and spermine, are found abundantly within cells and are positively-charged at physiological pH. Polyamine metabolism is connected to distinct other metabolic pathways, including nucleotide and amino acid metabolism. However, the breadth of the effect of polyamines on cellular metabolism remains to be fully understood. We recently demonstrated a role for polyamines in cholesterol metabolism, and following these studies, we measured the impact of polyamines on global lipid metabolism. We find that lipid droplets increase in number and size with polyamine depletion. We further demonstrate that lipid anabolism is markedly decreased, and lipid accumulation is due to reduced mitochondrial fatty acid oxidation. In fact, mitochondrial structure and function are largely ablated with polyamine depletion. To compensate, cells depleted of polyamines switch from aerobic respiration to glycolysis in a polyamine depletion-mediated Warburg-like effect. Finally, we show that inhibitors of lipid metabolism are broadly antiviral, suggesting that polyamines and lipids are promising antiviral targets. Together, these data demonstrate a novel role for polyamines in mitochondrial function, lipid metabolism, and cellular energetics.
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issn 1553-7366
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language English
publishDate 2024-11-01
publisher Public Library of Science (PLoS)
record_format Article
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spelling doaj-art-d983bd7d75674f19918999e146f2fd682025-08-20T02:21:46ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742024-11-012011e101271110.1371/journal.ppat.1012711Polyamines mediate cellular energetics and lipid metabolism through mitochondrial respiration to facilitate virus replication.Yazmin E Cruz-PulidoNatalie J LoMascoloDelaina MayJomana HatahetCaroline E ThomasAndrea K W ChuSamantha P StaceyMaria Del Mar Villanueva GuzmanGregory AubertBryan C MouncePolyamines are critical cellular components that regulate a variety of processes, including translation, cell cycling, and nucleic acid metabolism. The polyamines, putrescine, spermidine, and spermine, are found abundantly within cells and are positively-charged at physiological pH. Polyamine metabolism is connected to distinct other metabolic pathways, including nucleotide and amino acid metabolism. However, the breadth of the effect of polyamines on cellular metabolism remains to be fully understood. We recently demonstrated a role for polyamines in cholesterol metabolism, and following these studies, we measured the impact of polyamines on global lipid metabolism. We find that lipid droplets increase in number and size with polyamine depletion. We further demonstrate that lipid anabolism is markedly decreased, and lipid accumulation is due to reduced mitochondrial fatty acid oxidation. In fact, mitochondrial structure and function are largely ablated with polyamine depletion. To compensate, cells depleted of polyamines switch from aerobic respiration to glycolysis in a polyamine depletion-mediated Warburg-like effect. Finally, we show that inhibitors of lipid metabolism are broadly antiviral, suggesting that polyamines and lipids are promising antiviral targets. Together, these data demonstrate a novel role for polyamines in mitochondrial function, lipid metabolism, and cellular energetics.https://doi.org/10.1371/journal.ppat.1012711
spellingShingle Yazmin E Cruz-Pulido
Natalie J LoMascolo
Delaina May
Jomana Hatahet
Caroline E Thomas
Andrea K W Chu
Samantha P Stacey
Maria Del Mar Villanueva Guzman
Gregory Aubert
Bryan C Mounce
Polyamines mediate cellular energetics and lipid metabolism through mitochondrial respiration to facilitate virus replication.
PLoS Pathogens
title Polyamines mediate cellular energetics and lipid metabolism through mitochondrial respiration to facilitate virus replication.
title_full Polyamines mediate cellular energetics and lipid metabolism through mitochondrial respiration to facilitate virus replication.
title_fullStr Polyamines mediate cellular energetics and lipid metabolism through mitochondrial respiration to facilitate virus replication.
title_full_unstemmed Polyamines mediate cellular energetics and lipid metabolism through mitochondrial respiration to facilitate virus replication.
title_short Polyamines mediate cellular energetics and lipid metabolism through mitochondrial respiration to facilitate virus replication.
title_sort polyamines mediate cellular energetics and lipid metabolism through mitochondrial respiration to facilitate virus replication
url https://doi.org/10.1371/journal.ppat.1012711
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