Loss of vacuolar acidity results in iron-sulfur cluster defects and divergent homeostatic responses during aging in Saccharomyces cerevisiae

Alberti S, Gitler AD, Lindquist S (2007) A suite of Gateway® cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast Chichester Engl 24:913–919 Alvaro D, Lisby M, Rothstein R (2007) Genome-wide analysis of Rad52 foci reveals diverse mechanisms impacting recombination. PLoS Genet 3:e228 Bakker E, Swain PS, Crane MM (2018) Morphologically constrained and data informed cell segmentation of budding yeast. Bioinformatics 34:88–96 Baxi K, Ghavidel A, Waddell B, Harkness TA, de Carvalho CE (2017) Regulation of lysosomal function by the DAF-16 forkhead transcription factor couples reproduction to aging in Caenorhabditis elegans. Genetics 207:83–101 Birkeland SR, Jin N, Ozdemir AC, Lyons RH, Weisman LS, Wilson TE (2010) Discovery of mutations in Saccharomyces cerevisiae by pooled linkage analysis and whole-genome sequencing. Genetics 186:1127–1137 Carmona-Gutierrez D, Hughes AL, Madeo F, Ruckenstuhl C (2016) The crucial impact of lysosomes in aging and longevity. Ageing Res Rev 32:2–12 Chen OS, Crisp RJ, Valachovic M, Bard M, Winge DR, Kaplan J (2004) Transcription of the yeast iron regulon does not respond directly to iron but rather to iron-sulfur cluster biosynthesis. J Biol Chem 279:29513–29518 Chen KL, Crane MM, Kaeberlein M (2017) Microfluidic technologies for yeast replicative lifespan studies. Mech Ageing Dev 161:262–269 Chen KL, Ven TN, Crane MM, Chen DE, Feng YC, Suzuki N, Russell AE, de Moraes D, Kaeberlein M (2019) An inexpensive microscopy system for microfluidic studies in budding yeast. Translational Medicine of Aging 3:52-56 Crane MM, Kaeberlein M (2018) The paths of mortality: how understanding the biology of aging can help explain systems behavior of single cells. Curr Opin Syst Biol 8:25–31 Crane MM, Clark IBN, Bakker E, Smith S, Swain PS (2014) A microfluidic system for studying ageing and dynamic single-cell responses in budding yeast. PLoS One 9:e100042 Davis-Kaplan SR, Ward DM, Shiflett SL, Kaplan J (2004) Genome-wide analysis of iron-dependent growth reveals a novel yeast gene required for vacuolar acidification. J Biol Chem 279:4322–4329 Díaz de la Loza MDC, Gallardo M, García-Rubio ML, Izquierdo A, Herrero E, Aguilera A, Wellinger RE (2011) Zim17/Tim15 links mitochondrial iron–sulfur cluster biosynthesis to nuclear genome stability. Nucleic Acids Res 39:6002–6015 de Silva D, Davis-Kaplan S, Fergestad J, Kaplan J (1997) Purification and characterization of Fet3 protein, a yeast homologue of ceruloplasmin. J Biol Chem 272:14208–14213 Diab HI, Kane PM (2013) Loss of vacuolar H+-ATPase (V-ATPase) activity in yeast generates an iron deprivation signal that is moderated by induction of the peroxiredoxin TSA2. J Biol Chem 288:11366–11377 Eide DJ, Bridgham JT, Zhao Z, Mattoon JR (1993) The vacuolar H(+)-ATPase of Saccharomyces cerevisiae is required for efficient copper detoxification, mitochondrial function, and iron metabolism. Mol Gen Genet 241:447–456 Follmann M, Ochrombel I, Kramer R, Trotschel C, Poetsch A, Ruckert C, Huser A, Persicke M, Seiferling D, Kalinowski J et al (2009) Functional genomics of pH homeostasis in Corynebacterium glutamicum revealed novel links between pH response, oxidative stress, iron homeostasis and methionine synthesis. BMC Genomics 10:621 Gasior SL, Wong AK, Kora Y, Shinohara A, Bishop DK (1998) Rad52 associates with RPA and functions with Rad55 and Rad57 to assemble meiotic recombination complexes. Genes Dev 12:2208–2221 Ghavidel A, Baxi K, Prusinkiewicz M, Swan C, Belak ZR, Eskiw CH, Carvalho CE, Harkness TA (2018) Rapid nuclear exclusion of Hcm1 in aging Saccharomyces cerevisiae leads to vacuolar alkalization and replicative senescence. G3 Genes Genomes Genet 8:1579–1592 Gomez M, Perez-Gallardo RV, Sanchez LA, Diaz-Perez AL, Cortes-Rojo C, Meza Carmen V, Saavedra-Molina A, Lara-Romero J, Jimenez-Sandoval S, Rodriguez F et al (2014) Malfunctioning of the iron-sulfur cluster assembly machinery in Saccharomyces cerevisiae produces oxidative stress via an iron-dependent mechanism, causing dysfunction in respiratory complexes. PLoS One 9:e111585 Henderson KA, Hughes AL, Gottschling DE (2014) Mother-daughter asymmetry of pH underlies aging and rejuvenation in yeast. Elife 3:e03504 Hughes AL, Gottschling DE (2012) An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492:261–265 Huh W-K, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O’Shea EK (2003) Global analysis of protein localization in budding yeast. Nature 425:686–691 Inoue H, Noumi T, Nagata M, Murakami H, Kanazawa H (1999) Targeted disruption of the gene encoding the proteolipid subunit of mouse vacuolar H+-ATPase leads to early embryonic lethality. Biochim Biophys Acta 1413:130–138 Jang S, Imlay JA (2007) Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J Biol Chem 282:929–937 Jensen LT, Culotta VC (2002) Regulation of Saccharomyces cerevisiae FET4 by oxygen and iron. J Mol Biol 318:251–260 Jin M, Li Y, O’Laughlin R, Bittihn P, Pillus L, Tsimring LS, Hasty J, Hao N (2019) Divergent aging of isogenic yeast cells revealed through single-cell phenotypic dynamics. Cell Syst 8:242–253.e3 Kidane TZ, Sauble E, Linder MC (2006) Release of iron from ferritin requires lysosomal activity. Am J Physiol Cell Physiol 291:C445–C455 Kispal G, Sipos K, Lange H, Fekete Z, Bedekovics T, Janáky T, Bassler J, Aguilar Netz DJ, Balk J, Rotte C, Lill R (2005) Biogenesis of cytosolic ribosomes requires the essential iron–sulphur protein Rli1p and mitochondria. EMBO J 24:589–598 Knieß RA, Mayer MP (2016) The oxidation state of the cytoplasmic glutathione redox system does not correlate with replicative lifespan in yeast. Npj Aging Mech Dis 2:1–11 Lee MB, Dowsett IT, Carr DT, Wasko BM, Stanton SG, Chung MS, Ghodsian N, Bode A, Kiflezghi MG, Uppal PA et al (2019) Defining the impact of mutation accumulation on replicative lifespan in yeast using cancer-associated mutator phenotypes. Proc Natl Acad Sci U A 116:3062–3071 Li SC, Kane PM (2009) The yeast lysosome-like vacuole: endpoint and crossroads. Biochim Biophys Acta 1793:650–663 Li H, Mapolelo DT, Dingra NN, Keller G, Riggs-Gelasco PJ, Winge DR, Johnson MK, Outten CE (2011) Histidine 103 in Fra2 is an iron-sulfur cluster ligand in the [2Fe-2S] Fra2-Grx3 complex and is required for in vivo iron signaling in yeast. J Biol Chem 286:867–876 Liao C, Hu B, Arno MJ, Panaretou B (2007) Genomic screening in vivo reveals the role played by vacuolar H+ ATPase and cytosolic acidification in sensitivity to DNA-damaging agents such as cisplatin. Mol Pharmacol 71:416–425 Lill R, Hoffmann B, Molik S, Pierik AJ, Rietzschel N, Stehling O, Uzarska MA, Webert H, Wilbrecht C, Mühlenhoff U (2012) The role of mitochondria in cellular iron–sulfur protein biogenesis and iron metabolism. Biochim. Biophys. Acta BBA - Mol. Cell Res. 1823:1491–1508 Lim J-H, Park J-W, Kim SJ, Kim M-S, Park S-K, Johnson RS, Chun Y-S (2007) ATP6V0C competes with von Hippel-Lindau protein in hypoxia-inducible factor 1alpha (HIF-1alpha) binding and mediates HIF-1alpha expression by bafilomycin A1. Mol Pharmacol 71:942–948 Lisby M, Rothstein R, Mortensen UH (2001) Rad52 forms DNA repair and recombination centers during S phase. Proc Natl Acad Sci 98:8276–8282 López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G (2013) The hallmarks of aging. Cell 153:1194–1217 Mahon MJ (2011) pHluorin2: an enhanced, ratiometric, pH-sensitive green florescent protein. Adv Biosci Biotechnol 2:132–137 Martinez-Munoz GA, Kane P (2008) Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast. J Biol Chem 283:20309–20319 McCormick MA, Delaney JR, Tsuchiya M, Tsuchiyama S, Shemorry A, Sim S, Chou AC-Z, Ahmed U, Carr D, Murakami CJ et al (2015) A comprehensive analysis of replicative lifespan in 4,698 single-gene deletion strains uncovers conserved mechanisms of aging. Cell Metab 22:895–906 Miles AL, Burr SP, Grice GL, Nathan JA (2017) The vacuolar-ATPase complex and assembly factors, TMEM199 and CCDC115, control HIF1α prolyl hydroxylation by regulating cellular iron levels. eLife 6:e22693 Milgrom E, Diab H, Middleton F, Kane PM (2007) Loss of vacuolar proton-translocating ATPase activity in yeast results in chronic oxidative stress. J Biol Chem 282:7125–7136 Nasmyth KA, Reed SI (1980) Isolation of genes by complementation in yeast: molecular cloning of a cell-cycle gene. Proc Natl Acad Sci 77:2119–2123 Netz DJA, Mascarenhas J, Stehling O, Pierik AJ, Lill R (2014) Maturation of cytosolic and nuclear iron–sulfur proteins. Trends Cell Biol 24:303–312 Novarina D, Mavrova SN, Janssens GE, Rempel IL, Veenhoff LM, Chang M (2017) Increased genome instability is not accompanied by sensitivity to DNA damaging agents in aged yeast cells. DNA Repair 54:1–7 Ohya Y, Ohsumi Y, Anraku Y (1986) Isolation and characterization of Ca2+-sensitive mutants of Saccharomyces cerevisiae. J Gen Microbiol 132:979–988 Perera RM, Zoncu R (2016) The lysosome as a regulatory hub. Annu Rev Cell Dev Biol 32:223–253 Philpott CC, Smith PM (2013). Iron Starvation Response in Saccharomyces cerevisiae. In Encyclopedia of Inorganic and Bioinorganic Chemistry, R.A. Scott (Ed.) Pijuan J, Maria C, Herrero E, Belli G (2015) Impaired mitochondrial Fe-S cluster biogenesis activates the DNA damage response through different signaling mediators. J Cell Sci 128:4653–4665 Rutherford JC, Ojeda L, Balk J, Mühlenhoff U, Lill R, Winge DR (2005) Activation of the iron regulon by the yeast Aft1/Aft2 transcription factors depends on mitochondrial but not cytosolic iron-sulfur protein biogenesis. J Biol Chem 280:10135–10140 Sasikumar AN, Killilea DW, Kennedy BK, Brem RB (2019) Potassium restriction boosts vacuolar acidity and extends lifespan in yeast. Exp Gerontol 120:101–106 Schleit J, Johnson SC, Bennett CF, Simko M, Trongtham N, Castanza A, Hsieh EJ, Moller RM, Wasko BM, Delaney JR et al (2013) Molecular mechanisms underlying genotype-dependent responses to dietary restriction. Aging Cell 12:1050–1061 Schneider LS, von Schwarzenberg K, Lehr T, Ulrich M, Kubisch-Dohmen R, Liebl J, Trauner D, Menche D, Vollmar AM (2015) Vacuolar-ATPase inhibition blocks Iron metabolism to mediate therapeutic effects in breast cancer. Cancer Res 75:2863–2874 Seo AY, Xu J, Servais S, Hofer T, Marzetti E, Wohlgemuth SE, Knutson MD, Chung HY, Leeuwenburgh C (2008) Mitochondrial iron accumulation with age and functional consequences. Aging Cell 7:706–716 Serrano R, Bernal D, Simon E, Arino J (2004) Copper and iron are the limiting factors for growth of the yeast Saccharomyces cerevisiae in an alkaline environment. J Biol Chem 279:19698–19704 Straud S, Zubovych I, De Brabander JK, Roth MG (2010) Inhibition of iron uptake is responsible for differential sensitivity to V-ATPase inhibitors in several cancer cell lines. PLoS One 5:e11629 Szczypka MS, Zhu Z, Silar P, Thiele DJ (1997) Saccharomyces cerevisiae mutants altered in vacuole function are defective in copper detoxification and iron-responsive gene transcription. Yeast Chichester Engl. 13:1423–1435 Ter Linde JJ, Steensma HY (2002) A microarray-assisted screen for potential Hap1 and Rox1 target genes in Saccharomyces cerevisiae. Yeast 19:825–840 Tong W-H, Rouault TA (2006) Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron-sulfur cluster biogenesis and iron homeostasis. Cell Metab 3:199–210 Uchiyama A, Kim J-S, Kon K, Jaeschke H, Ikejima K, Watanabe S, Lemasters JJ (2008) Translocation of iron from lysosomes into mitochondria is a key event during oxidative stress-induced hepatocellular injury. Hepatol Baltim Md 48:1644–1654 Veatch JR, McMurray MA, Nelson ZW, Gottschling DE (2009) Mitochondrial dysfunction leads to nuclear genome instability via an iron-sulfur cluster defect. Cell 137:1247–1258 Wasko BM, Holland CL, Resnick MA, Lewis LK (2009) Inhibition of DNA double-strand break repair by the Ku heterodimer in mrx mutants of Saccharomyces cerevisiae. DNA Repair 8:162–169 Wasko BM, Carr DT, Tung H, Doan H, Schurman N, Neault JR, Feng J, Lee J, Zipkin B, Mouser J et al (2013) Buffering the pH of the culture medium does not extend yeast replicative lifespan. F1000Res 2:216 Waters BM, Eide DJ (2002) Combinatorial control of yeast FET4 gene expression by iron, zinc, and oxygen. J Biol Chem 277:33749–33757