An Improved ATP FRET Sensor For Yeast Shows Heterogeneity During Nutrient Transitions.


Journal

ACS sensors
ISSN: 2379-3694
Titre abrégé: ACS Sens
Pays: United States
ID NLM: 101669031

Informations de publication

Date de publication:
27 03 2020
Historique:
pubmed: 23 2 2020
medline: 22 12 2020
entrez: 21 2 2020
Statut: ppublish

Résumé

Adenosine 5-triphosphate (ATP) is the main free energy carrier in metabolism. In budding yeast, shifts to glucose-rich conditions cause dynamic changes in ATP levels, but it is unclear how heterogeneous these dynamics are at a single-cell level. Furthermore, pH also changes and affects readout of fluorescence-based biosensors for single-cell measurements. To measure ATP changes reliably in single yeast cells, we developed yAT1.03, an adapted version of the AT1.03 ATP biosensor, that is pH-insensitive. We show that pregrowth conditions largely affect ATP dynamics during transitions. Moreover, single-cell analyses showed a large variety in ATP responses, which implies large differences of glycolytic startup between individual cells. We found three clusters of dynamic responses, and we show that a small subpopulation of wild-type cells reached an imbalanced state during glycolytic startup, characterized by low ATP levels. These results confirm the need for new tools to study dynamic responses of individual cells in dynamic environments.

Identifiants

pubmed: 32077276
doi: 10.1021/acssensors.9b02475
pmc: PMC7106129
doi:

Substances chimiques

Adenosine Triphosphate 8L70Q75FXE

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

814-822

Références

Nat Protoc. 2007;2(1):35-7
pubmed: 17401335
Cancer Res. 2012 Oct 1;72(19):4875-82
pubmed: 23002210
Cell Metab. 2008 Jan;7(1):11-20
pubmed: 18177721
Nat Chem Biol. 2016 Jul;12(7):482-9
pubmed: 27159581
Metab Eng. 2008 Jan;10(1):39-54
pubmed: 18054509
J Biol Chem. 1957 Feb;224(2):963-9
pubmed: 13405925
FEMS Yeast Res. 2001 Apr;1(1):33-45
pubmed: 12702461
Appl Environ Microbiol. 2008 Sep;74(18):5710-23
pubmed: 18641162
Trends Biochem Sci. 1998 May;23(5):162-9
pubmed: 9612078
Nat Protoc. 2015 Aug;10(8):1181-97
pubmed: 26158443
Crit Rev Biochem Mol Biol. 2018 Feb;53(1):99-114
pubmed: 29250983
Eur J Biochem. 1983 Dec 15;137(3):479-83
pubmed: 6229402
Res Microbiol. 1996 Jul-Sep;147(6-7):448-55
pubmed: 9084754
Nat Chem Biol. 2016 May;12(5):339-44
pubmed: 26999780
Mol Microbiol. 1996 Jun;20(5):981-91
pubmed: 8809751
Mol Syst Biol. 2010;6:344
pubmed: 20087341
Biochem J. 2010 Dec 1;432(2):399-406
pubmed: 20854260
Proc Natl Acad Sci U S A. 2008 Jul 8;105(27):9227-32
pubmed: 18574155
Biophys J. 2011 Aug 17;101(4):961-9
pubmed: 21843488
Cell. 2010 May 14;141(4):559-63
pubmed: 20478246
Genome Biol. 2012 Sep 10;13(9):R80
pubmed: 23021432
J Biol Chem. 1977 Sep 25;252(18):6394-8
pubmed: 19473
Eur J Biochem. 1997 Apr 15;245(2):324-33
pubmed: 9151960
Bioessays. 2015 Jan;37(1):34-45
pubmed: 25350875
Nat Commun. 2017 Oct 13;8(1):922
pubmed: 29030545
J Gen Microbiol. 1987 Aug;133(8):2197-205
pubmed: 2832519
Nat Rev Clin Oncol. 2017 Jan;14(1):11-31
pubmed: 27141887
J Cell Physiol. 2018 Apr;233(4):2839-2849
pubmed: 28488732
J Theor Biol. 1990 Mar 22;143(2):163-95
pubmed: 2200929
J Cell Sci. 2019 Apr 17;132(8):
pubmed: 30858198
Microbiology. 2009 Jan;155(Pt 1):268-278
pubmed: 19118367
Yeast. 1995 Feb;11(2):137-44
pubmed: 7732723
Yeast. 2000 Jun 30;16(9):797-809
pubmed: 10861904
Proc Natl Acad Sci U S A. 2013 Jun 11;110(24):10039-44
pubmed: 23630264
Science. 2014 Feb 28;343(6174):1245114
pubmed: 24436182
Nature. 2015 Jan 15;517(7534):302-10
pubmed: 25592535
Clin Cancer Res. 2015 Jul 1;21(13):2916-23
pubmed: 25838394
FEMS Yeast Res. 2002 Dec;2(4):539-50
pubmed: 12702270
Trends Biotechnol. 2014 Dec;32(12):608-16
pubmed: 25457387
Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15651-6
pubmed: 19720993
Sci Rep. 2019 Feb 19;9(1):2234
pubmed: 30783202
J Biol Chem. 2010 May 7;285(19):14603-9
pubmed: 20236929
Curr Opin Microbiol. 2018 Oct;45:30-38
pubmed: 29477028

Auteurs

Dennis Botman (D)

Systems Biology Lab/AIMMS, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands.

Johan H van Heerden (JH)

Systems Biology Lab/AIMMS, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands.

Bas Teusink (B)

Systems Biology Lab/AIMMS, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Adenosine Triphosphate Adenosine Diphosphate Mitochondrial ADP, ATP Translocases Binding Sites Mitochondria
Fragaria Light Plant Leaves Osmosis Stress, Physiological
Saccharomyces cerevisiae Aldehydes Biotransformation Flavoring Agents Lipoxygenase

Classifications MeSH