Overexpression of polyphosphate polymerases and deletion of polyphosphate phosphatases shorten the replicative lifespan in yeast.
cellular senescence
phosphate starvation response
polyphosphate
replicative lifespan
stress sensitivity
yeast
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
revised:
29
07
2023
received:
12
06
2023
accepted:
03
08
2023
medline:
26
9
2023
pubmed:
14
8
2023
entrez:
13
8
2023
Statut:
ppublish
Résumé
We previously found that overexpression of phosphate starvation-responsive genes by disrupting PHO80 led to a shortened replicative lifespan in yeast. To identify lifespan-related genes, we screened upregulated genes in the pho80Δ mutant and focused on the VTC genes, which encode the vacuolar polyphosphate (polyP) polymerase complex. VTC1/VTC2/VTC4 deletion restored the lifespan and intracellular polyP levels in pho80Δ. In the wild type, overexpression of VTC5 or a combination of the other VTCs caused high polyP accumulation and shortened lifespan. Similar phenotypes were caused by the deletion of polyP phosphatase genes-vacuolar PPN1 and cytosolic PPX1. The polyP-accumulating strains exhibited stress sensitivities. Thus, we demonstrated that polyP metabolic enzymes participate in replicative lifespan, and extreme polyP accumulation shortens the lifespan.
Identifiants
pubmed: 37574219
doi: 10.1002/1873-3468.14715
doi:
Substances chimiques
Polyphosphates
0
Phosphoric Monoester Hydrolases
EC 3.1.3.2
Saccharomyces cerevisiae Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2316-2333Informations de copyright
© 2023 Federation of European Biochemical Societies.
Références
Docampo R and Huang G (2016) Acidocalcisomes of eukaryotes. Curr Opin Cell Biol 41, 66-72.
Kulaev IS, Vagabov VM and Kulakovskaya TV (2004) The Biochemistry of Inorganic Polyphosphates. 2nd edn. Wiley, Chichester, West Sussex; Hoboken, NJ.
Gerasimaite R and Mayer A (2016) Enzymes of yeast polyphosphate metabolism: structure, enzymology and biological roles. Biochem Soc Trans 44, 234-239.
Saito K, Ohtomo R, Kuga-Uetake Y, Aono T and Saito M (2005) Direct labeling of polyphosphate at the ultrastructural level in Saccharomyces cerevisiae by using the affinity of the polyphosphate binding domain of Escherichia coli exopolyphosphatase. Appl Environ Microbiol 71, 5692-5701.
Bru S, Martinez-Lainez JM, Hernandez-Ortega S, Quandt E, Torres-Torronteras J, Marti R, Canadell D, Arino J, Sharma S, Jimenez J et al. (2016) Polyphosphate is involved in cell cycle progression and genomic stability in Saccharomyces cerevisiae. Mol Microbiol 101, 367-380.
Kuroda A (2006) A polyphosphate-lon protease complex in the adaptation of Escherichia coli to amino acid starvation. Biosci Biotechnol Biochem 70, 325-331.
Abramov AY, Fraley C, Diao CT, Winkfein R, Colicos MA, Duchen MR, French RJ and Pavlov E (2007) Targeted polyphosphatase expression alters mitochondrial metabolism and inhibits calcium-dependent cell death. Proc Natl Acad Sci U S A 104, 18091-18096.
Zakharian E, Thyagarajan B, French RJ, Pavlov E and Rohacs T (2009) Inorganic polyphosphate modulates TRPM8 channels. PLoS One 4, e5404.
Hacchou Y, Uematsu T, Ueda O, Usui Y, Uematsu S, Takahashi M, Uchihashi T, Kawazoe Y, Shiba T, Kurihara S et al. (2007) Inorganic polyphosphate: a possible stimulant of bone formation. J Dent Res 86, 893-897.
Smith SA, Choi SH, Davis-Harrison R, Huyck J, Boettcher J, Rienstra CM and Morrissey JH (2010) Polyphosphate exerts differential effects on blood clotting, depending on polymer size. Blood 116, 4353-4359.
Azevedo C, Livermore T and Saiardi A (2015) Protein polyphosphorylation of lysine residues by inorganic polyphosphate. Mol Cell 58, 71-82.
Bentley-DeSousa A, Holinier C, Moteshareie H, Tseng YC, Kajjo S, Nwosu C, Amodeo GF, Bondy-Chorney E, Sai Y, Rudner A et al. (2018) A screen for candidate targets of lysine polyphosphorylation uncovers a conserved network implicated in ribosome biogenesis. Cell Rep 22, 3427-3439.
Guarente L and Kenyon C (2000) Genetic pathways that regulate ageing in model organisms. Nature 408, 255-262.
Kaeberlein M, Powers RW 3rd, Steffen KK, Westman EA, Hu D, Dang N, Kerr EO, Kirkland KT, Fields S and Kennedy BK (2005) Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310, 1193-1196.
Hughes AL and Gottschling DE (2012) An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492, 261-265.
Nakajima T, Maruhashi T, Morimatsu T and Mukai Y (2020) Cyclin-dependent kinase Pho85p and its cyclins are involved in replicative lifespan through multiple pathways in yeast. FEBS Lett 594, 1166-1175.
Ogawa N, DeRisi J and Brown PO (2000) New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Mol Biol Cell 11, 4309-4321.
Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P and Pringle JR (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961.
Wach A, Brachat A, Pohlmann R and Philippsen P (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.
Sakumoto N, Mukai Y, Uchida K, Kouchi T, Kuwajima J, Nakagawa Y, Sugioka S, Yamamoto E, Furuyama T, Mizubuchi H et al. (1999) A series of protein phosphatase gene disruptants in Saccharomyces cerevisiae. Yeast 15, 1669-1679.
Sherman BT, Hao M, Qiu J, Jiao X, Baseler MW, Lane HC, Imamichi T and Chang W (2022) DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Res 50, W216-W221.
Huang da W, Sherman BT and Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4, 44-57.
Kamei Y, Tamada Y, Nakayama Y, Fukusaki E and Mukai Y (2014) Changes in transcription and metabolism during the early stage of replicative cellular senescence in budding yeast. J Biol Chem 289, 32081-32093.
Auesukaree C, Tochio H, Shirakawa M, Kaneko Y and Harashima S (2005) Plc1p, Arg82p, and Kcs1p, enzymes involved in inositol pyrophosphate synthesis, are essential for phosphate regulation and polyphosphate accumulation in Saccharomyces cerevisiae. J Biol Chem 280, 25127-25133.
Bru S, Jimenez J, Canadell D, Arino J and Clotet J (2016) Improvement of biochemical methods of polyP quantification. Microb Cell 4, 6-15.
Lonetti A, Szijgyarto Z, Bosch D, Loss O, Azevedo C and Saiardi A (2011) Identification of an evolutionarily conserved family of inorganic polyphosphate endopolyphosphatases. J Biol Chem 286, 31966-31974.
Tanigawa M and Maeda T (2017) An in vitro TORC1 kinase assay that recapitulates the Gtr-independent glutamine-responsive TORC1 activation mechanism on yeast vacuoles. Mol Cell Biol 37, e00075-17.
Schweingruber ME, Fluri R, Maundrell K, Schweingruber AM and Dumermuth E (1986) Identification and characterization of thiamin repressible acid phosphatase in yeast. J Biol Chem 261, 15877-15882.
Desfougeres Y, Gerasimaite RU, Jessen HJ and Mayer A (2016) Vtc5, a novel subunit of the vacuolar transporter chaperone complex, regulates polyphosphate synthesis and phosphate homeostasis in yeast. J Biol Chem 291, 22262-22275.
Muller O, Bayer MJ, Peters C, Andersen JS, Mann M and Mayer A (2002) The Vtc proteins in vacuole fusion: coupling NSF activity to V(0) trans-complex formation. EMBO J 21, 259-269.
Uttenweiler A, Schwarz H, Neumann H and Mayer A (2007) The vacuolar transporter chaperone (VTC) complex is required for microautophagy. Mol Biol Cell 18, 166-175.
Andreeva N, Trilisenko L, Eldarov M and Kulakovskaya T (2015) Polyphosphatase PPN1 of Saccharomyces cerevisiae: switching of exopolyphosphatase and endopolyphosphatase activities. PLoS One 10, e0119594.
Lichko LP, Kulakovskaya TV and Kulaev IS (2006) Inorganic polyphosphate and exopolyphosphatase in the nuclei of Saccharomyces cerevisiae: dependence on the growth phase and inactivation of the PPX1 and PPN1 genes. Yeast 23, 735-740.
Gerasimaite R and Mayer A (2017) Ppn2, a novel Zn(2+)-dependent polyphosphatase in the acidocalcisome-like yeast vacuole. J Cell Sci 130, 1625-1636.
Lichko LP, Andreeva NA, Kulakovskaya TV and Kulaev IS (2003) Exopolyphosphatases of the yeast Saccharomyces cerevisiae. FEMS Yeast Res 3, 233-238.
Lee SS, Avalos Vizcarra I, Huberts DH, Lee LP and Heinemann M (2012) Whole lifespan microscopic observation of budding yeast aging through a microfluidic dissection platform. Proc Natl Acad Sci U S A 109, 4916-4920.
Wang L, Fraley CD, Faridi J, Kornberg A and Roth RA (2003) Inorganic polyphosphate stimulates mammalian TOR, a kinase involved in the proliferation of mammary cancer cells. Proc Natl Acad Sci U S A 100, 11249-11254.
Bonawitz ND, Rodeheffer MS and Shadel GS (2006) Defective mitochondrial gene expression results in reactive oxygen species-mediated inhibition of respiration and reduction of yeast life span. Mol Cell Biol 26, 4818-4829.
Grzelak A, Macierzynska E and Bartosz G (2006) Accumulation of oxidative damage during replicative aging of the yeast Saccharomyces cerevisiae. Exp Gerontol 41, 813-818.
Bian J, Wang L, Wu J, Simth N, Zhang L, Wang Y and Wu X (2021) MTM1 plays an important role in the regulation of zinc tolerance in Saccharomyces cerevisiae. J Trace Elem Med Biol 66, 126759.
Hothorn M, Neumann H, Lenherr ED, Wehner M, Rybin V, Hassa PO, Uttenweiler A, Reinhardt M, Schmidt A, Seiler J et al. (2009) Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science 324, 513-516.
Wurst H, Shiba T and Kornberg A (1995) The gene for a major exopolyphosphatase of Saccharomyces cerevisiae. J Bacteriol 177, 898-906.
Cartwright JL and McLennan AG (1999) The Saccharomyces cerevisiae YOR163w gene encodes a diadenosine 5′, 5″-P1,P6-hexaphosphate (Ap6A) hydrolase member of the MutT motif (Nudix hydrolase) family. J Biol Chem 274, 8604-8610.
Safrany ST, Ingram SW, Cartwright JL, Falck JR, McLennan AG, Barnes LD and Shears SB (1999) The diadenosine hexaphosphate hydrolases from Schizosaccharomyces pombe and Saccharomyces cerevisiae are homologues of the human diphosphoinositol polyphosphate phosphohydrolase. Overlapping substrate specificities in a MutT-type protein. J Biol Chem 274, 21735-21740.
Clark DW, Tkacz JS and Lampen JO (1982) Asparagine-linked carbohydrate does not determine the cellular location of yeast vacuolar nonspecific alkaline phosphatase. J Bacteriol 152, 865-873.
Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T, Ohyama Y, Kurabayashi M, Kaname T, Kume E et al. (1997) Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390, 45-51.
Ohnishi M and Razzaque MS (2010) Dietary and genetic evidence for phosphate toxicity accelerating mammalian aging. FASEB J 24, 3562-3571.
Tammenkoski M, Koivula K, Cusanelli E, Zollo M, Steegborn C, Baykov AA and Lahti R (2008) Human metastasis regulator protein H-prune is a short-chain exopolyphosphatase. Biochemistry 47, 9707-9713.