Genomic Analysis of ATP Efflux in Saccharomyces cerevisiae

Adenosine triphosphate (ATP) plays an important role as a primary molecule for the transfer of chemical energy to drive biological processes. ATP also functions as an extracellular signaling molecule in a diverse array of eukaryotic taxa in a conserved process known as purinergic signaling. Given th...

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Main Authors:	Peters, Theodore W., Miller, Aaron W., Tourette, Cendrine, Agren, Hannah, Hubbard, Alan, Hughes, Robert E.
Format:	Online
Language:	English
Published:	Genetics Society of America 2015
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4704715/

id	pubmed-4704715
recordtype	oai_dc
spelling	pubmed-47047152016-01-08 Genomic Analysis of ATP Efflux in Saccharomyces cerevisiae Peters, Theodore W. Miller, Aaron W. Tourette, Cendrine Agren, Hannah Hubbard, Alan Hughes, Robert E. Investigations Adenosine triphosphate (ATP) plays an important role as a primary molecule for the transfer of chemical energy to drive biological processes. ATP also functions as an extracellular signaling molecule in a diverse array of eukaryotic taxa in a conserved process known as purinergic signaling. Given the important roles of extracellular ATP in cell signaling, we sought to comprehensively elucidate the pathways and mechanisms governing ATP efflux from eukaryotic cells. Here, we present results of a genomic analysis of ATP efflux from Saccharomyces cerevisiae by measuring extracellular ATP levels in cultures of 4609 deletion mutants. This screen revealed key cellular processes that regulate extracellular ATP levels, including mitochondrial translation and vesicle sorting in the late endosome, indicating that ATP production and transport through vesicles are required for efflux. We also observed evidence for altered ATP efflux in strains deleted for genes involved in amino acid signaling, and mitochondrial retrograde signaling. Based on these results, we propose a model in which the retrograde signaling pathway potentiates amino acid signaling to promote mitochondrial respiration. This study advances our understanding of the mechanism of ATP secretion in eukaryotes and implicates TOR complex 1 (TORC1) and nutrient signaling pathways in the regulation of ATP efflux. These results will facilitate analysis of ATP efflux mechanisms in higher eukaryotes. Genetics Society of America 2015-11-18 /pmc/articles/PMC4704715/ /pubmed/26585826 http://dx.doi.org/10.1534/g3.115.023267 Text en Copyright © 2016 Peters et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Peters, Theodore W. Miller, Aaron W. Tourette, Cendrine Agren, Hannah Hubbard, Alan Hughes, Robert E.
spellingShingle	Peters, Theodore W. Miller, Aaron W. Tourette, Cendrine Agren, Hannah Hubbard, Alan Hughes, Robert E. Genomic Analysis of ATP Efflux in Saccharomyces cerevisiae
author_facet	Peters, Theodore W. Miller, Aaron W. Tourette, Cendrine Agren, Hannah Hubbard, Alan Hughes, Robert E.
author_sort	Peters, Theodore W.
title	Genomic Analysis of ATP Efflux in Saccharomyces cerevisiae
title_short	Genomic Analysis of ATP Efflux in Saccharomyces cerevisiae
title_full	Genomic Analysis of ATP Efflux in Saccharomyces cerevisiae
title_fullStr	Genomic Analysis of ATP Efflux in Saccharomyces cerevisiae
title_full_unstemmed	Genomic Analysis of ATP Efflux in Saccharomyces cerevisiae
title_sort	genomic analysis of atp efflux in saccharomyces cerevisiae
description	Adenosine triphosphate (ATP) plays an important role as a primary molecule for the transfer of chemical energy to drive biological processes. ATP also functions as an extracellular signaling molecule in a diverse array of eukaryotic taxa in a conserved process known as purinergic signaling. Given the important roles of extracellular ATP in cell signaling, we sought to comprehensively elucidate the pathways and mechanisms governing ATP efflux from eukaryotic cells. Here, we present results of a genomic analysis of ATP efflux from Saccharomyces cerevisiae by measuring extracellular ATP levels in cultures of 4609 deletion mutants. This screen revealed key cellular processes that regulate extracellular ATP levels, including mitochondrial translation and vesicle sorting in the late endosome, indicating that ATP production and transport through vesicles are required for efflux. We also observed evidence for altered ATP efflux in strains deleted for genes involved in amino acid signaling, and mitochondrial retrograde signaling. Based on these results, we propose a model in which the retrograde signaling pathway potentiates amino acid signaling to promote mitochondrial respiration. This study advances our understanding of the mechanism of ATP secretion in eukaryotes and implicates TOR complex 1 (TORC1) and nutrient signaling pathways in the regulation of ATP efflux. These results will facilitate analysis of ATP efflux mechanisms in higher eukaryotes.
publisher	Genetics Society of America
publishDate	2015
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4704715/
_version_	1613521054401036288

Genomic Analysis of ATP Efflux in Saccharomyces cerevisiae

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