{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,8]],"date-time":"2026-02-08T10:39:55Z","timestamp":1770547195910,"version":"3.49.0"},"reference-count":54,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2024,1,25]],"date-time":"2024-01-25T00:00:00Z","timestamp":1706140800000},"content-version":"vor","delay-in-days":24,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100020595","name":"National Science and Technology Council","doi-asserted-by":"publisher","award":["109-2313-B-002-023-MY3"],"award-info":[{"award-number":["109-2313-B-002-023-MY3"]}],"id":[{"id":"10.13039\/100020595","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100020595","name":"National Science and Technology Council","doi-asserted-by":"publisher","award":["112-2313-B-002-049-MY3"],"award-info":[{"award-number":["112-2313-B-002-049-MY3"]}],"id":[{"id":"10.13039\/100020595","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,1,9]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Ribosome assembly defects result in ribosomopathies, primarily caused by inadequate protein synthesis and induced oxidative stress. This study aimed to investigate the link between deleting one ribosomal protein gene (RPG) paralog and oxidative stress response. Our results indicated that RPG mutants exhibited higher oxidant sensitivity than the wild type (WT). The concentrations of H2O2 were increased in the RPG mutants. Catalase and superoxide dismutase (SOD) activities were generally higher at the stationary phase, with catalase showing particularly elevated activity in the RPG mutants. While both catalase genes, CTT1 and CTA1, consistently exhibited higher transcription in RPG mutants, Ctt1 primarily contributed to the increased catalase activity. Stress-response transcription factors Msn2, Msn4, and Hog1 played a role in regulating these processes. Previous studies have demonstrated that H2O2 can cleave 25S rRNA via the Fenton reaction, enhancing ribosomes\u2019 ability to translate mRNAs associated with oxidative stress-related genes. The cleavage of 25S rRNA was consistently more pronounced, and the translation efficiency of CTT1 and CTA1 mRNAs was altered in RPG mutants. Our results provide evidence that the mutations in RPGs increase H2O2 levels in vivo and elevate catalase expression through both transcriptional and translational controls.<\/jats:p>","DOI":"10.1093\/femsyr\/foae005","type":"journal-article","created":{"date-parts":[[2024,1,25]],"date-time":"2024-01-25T19:54:35Z","timestamp":1706212475000},"source":"Crossref","is-referenced-by-count":5,"title":["Mutations of ribosomal protein genes induce overexpression of catalase in <i>Saccharomyces cerevisiae<\/i>"],"prefix":"10.1093","volume":"24","author":[{"given":"Ching-Hsiang","family":"Hsu","sequence":"first","affiliation":[{"name":"Department of Agricultural Chemistry National Taiwan University Agricultural Chemistry Building No. 2 , Rm. 233 No. 1, Sec. 4, Roosevelt Rd. Taipei 10617 ,","place":["Taiwan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ching-Yu","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Agricultural Chemistry National Taiwan University Agricultural Chemistry Building No. 2 , Rm. 233 No. 1, Sec. 4, Roosevelt Rd. Taipei 10617 ,","place":["Taiwan"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0440-6836","authenticated-orcid":false,"given":"Kai-Yin","family":"Lo","sequence":"additional","affiliation":[{"name":"Department of Agricultural Chemistry National Taiwan University Agricultural Chemistry Building No. 2 , Rm. 233 No. 1, Sec. 4, Roosevelt Rd. Taipei 10617 ,","place":["Taiwan"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2024,1,25]]},"reference":[{"key":"2024121916320192600_bib1","doi-asserted-by":"crossref","first-page":"31907","DOI":"10.1074\/jbc.R110.144196","article-title":"Power of yeast for analysis of eukaryotic translation initiation","volume":"285","author":"Altmann","year":"2010","journal-title":"J Biol Chem"},{"key":"2024121916320192600_bib2","doi-asserted-by":"crossref","first-page":"1138","DOI":"10.1002\/pbc.22700","article-title":"SBDS-deficiency results in deregulation of reactive oxygen species leading to increased cell death and decreased cell growth","volume":"55","author":"Ambekar","year":"2010","journal-title":"Pediatr Blood Cancer"},{"key":"2024121916320192600_bib3","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1146\/annurev-biochem-013118-110817","article-title":"Eukaryotic ribosome assembly","volume":"88","author":"Bassler","year":"2019","journal-title":"Annu Rev Biochem"},{"key":"2024121916320192600_bib4","doi-asserted-by":"crossref","first-page":"4789","DOI":"10.1073\/pnas.85.13.4789","article-title":"The copper, zinc-superoxide dismutase gene of Saccharomyces cerevisiae: cloning, sequencing, and biological activity","volume":"85","author":"Bermingham-McDonogh","year":"1988","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024121916320192600_bib5","doi-asserted-by":"crossref","first-page":"1760","DOI":"10.1126\/science.7681220","article-title":"An osmosensing signal transduction pathway in yeast","volume":"259","author":"Brewster","year":"1993","journal-title":"Science"},{"key":"2024121916320192600_bib6","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1007\/BF00383315","article-title":"Isolation of the catalase A gene of Saccharomyces cerevisiae by complementation of the cta1 mutation","volume":"200","author":"Cohen","year":"1985","journal-title":"Mol Gen Genet"},{"key":"2024121916320192600_bib7","first-page":"Unit13 12","article-title":"Preparation of yeast RNA","volume":"Chapter 13","author":"Collart","year":"2001","journal-title":"Curr Protoc Mol Biol"},{"key":"2024121916320192600_bib10","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1038\/nrm2256","article-title":"ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis","volume":"8","author":"D'Autreaux","year":"2007","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2024121916320192600_bib8","doi-asserted-by":"crossref","first-page":"1262","DOI":"10.1182\/blood.2019000947","article-title":"Diamond-Blackfan anemia","volume":"136","author":"Da\u00a0Costa","year":"2020","journal-title":"Blood"},{"key":"2024121916320192600_bib9","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1242\/dmm.020529","article-title":"Ribosomopathies: how a common root can cause a tree of pathologies","volume":"8","author":"Danilova","year":"2015","journal-title":"Dis Model Mech"},{"key":"2024121916320192600_bib11","doi-asserted-by":"crossref","first-page":"2344","DOI":"10.1158\/0008-5472.CAN-21-4087","article-title":"Ribosome biogenesis: a central player in cancer metastasis and therapeutic resistance","volume":"82","author":"Elhamamsy","year":"2022","journal-title":"Cancer Res"},{"key":"2024121916320192600_bib12","first-page":"3872","article-title":"Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant of Saccharomyces cerevisiae","volume":"13","author":"Estruch","year":"1993","journal-title":"Mol Cell Biol"},{"key":"2024121916320192600_bib13","doi-asserted-by":"crossref","first-page":"6982","DOI":"10.1128\/MCB.17.12.6982","article-title":"Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions","volume":"17","author":"Fernandes","year":"1997","journal-title":"Mol Cell Biol"},{"key":"2024121916320192600_bib14","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1101\/gad.12.4.586","article-title":"Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity","volume":"12","author":"Gorner","year":"1998","journal-title":"Gene Dev"},{"key":"2024121916320192600_bib15","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1089\/ars.2010.3699","article-title":"Regulation of translation by hydrogen peroxide","volume":"15","author":"Grant","year":"2011","journal-title":"Antioxid Redox Sign"},{"key":"2024121916320192600_bib16","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1128\/EC.01.1.22-32.2002","article-title":"Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress","volume":"1","author":"Hinnebusch","year":"2002","journal-title":"Eukar Cell"},{"key":"2024121916320192600_bib17","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1146\/annurev.micro.57.030502.090938","article-title":"Pathways of oxidative damage","volume":"57","author":"Imlay","year":"2003","journal-title":"Annu Rev Microbiol"},{"key":"2024121916320192600_bib18","doi-asserted-by":"crossref","first-page":"8572","DOI":"10.1039\/C5AY02278A","article-title":"A rapid method to assess reactive oxygen species in yeast using H2DCF-DA","volume":"7","author":"James","year":"2015","journal-title":"Anal Methods"},{"key":"2024121916320192600_bib19","doi-asserted-by":"crossref","first-page":"1511","DOI":"10.1002\/(SICI)1097-0061(199812)14:16<1511::AID-YEA356>3.0.CO;2-S","article-title":"Oxidative stress responses of the yeast Saccharomyces cerevisiae","volume":"14","author":"Jamieson","year":"1998","journal-title":"Yeast"},{"key":"2024121916320192600_bib20","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1038\/s41392-022-01285-4","article-title":"Ribosome biogenesis in disease: new players and therapeutic targets","volume":"8","author":"Jiao","year":"2023","journal-title":"Signal Transduct Target Ther"},{"key":"2024121916320192600_bib21","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1038\/s41375-018-0176-z","article-title":"The ribosomal RPL10 R98S mutation drives IRES-dependent BCL-2 translation in T-ALL","volume":"33","author":"Kampen","year":"2019","journal-title":"Leukemia"},{"key":"2024121916320192600_bib22","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1093\/nar\/gkz637","article-title":"Hallmarks of ribosomopathies","volume":"48","author":"Kampen","year":"2020","journal-title":"Nucleic Acids Res"},{"key":"2024121916320192600_bib23","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1038\/s41392-021-00728-8","article-title":"Ribosomal proteins and human diseases: molecular mechanisms and targeted therapy","volume":"6","author":"Kang","year":"2021","journal-title":"Signal Transduct Target Ther"},{"key":"2024121916320192600_bib24","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1007\/s12275-011-1154-6","article-title":"Adaptive stress response to menadione-induced oxidative stress in Saccharomyces cerevisiae KNU5377","volume":"49","author":"Kim","year":"2011","journal-title":"J Microbiol"},{"key":"2024121916320192600_bib25","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1038\/s41580-018-0078-y","article-title":"Ribosome assembly coming into focus","volume":"20","author":"Klinge","year":"2019","journal-title":"Nat Rev Mol Cell Bio"},{"key":"2024121916320192600_bib26","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1016\/j.cell.2007.08.037","article-title":"Functional specificity among ribosomal proteins regulates gene expression","volume":"131","author":"Komili","year":"2007","journal-title":"Cell"},{"key":"2024121916320192600_bib27","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1002\/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U","article-title":"Additional modules for versatile and economical PCR-based gene deletion and modification in","volume":"14","author":"Longtine","year":"1998","journal-title":"Yeast"},{"key":"2024121916320192600_bib28","doi-asserted-by":"crossref","first-page":"779","DOI":"10.3390\/cells8080779","article-title":"Nucleolar and ribosomal DNA structure under stress: yeast lessons for aging and cancer","volume":"8","author":"Matos-Perdomo","year":"2019","journal-title":"Cells-Basel"},{"key":"2024121916320192600_bib29","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1038\/ng1994","article-title":"The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast","volume":"39","author":"Menne","year":"2007","journal-title":"Nat Genet"},{"key":"2024121916320192600_bib30","first-page":"11919","article-title":"Msn2\/4 transcription factors positively regulate expression of Atg39 ER-phagy receptor","volume-title":"Sci Rep","author":"Mizuno","year":"2021"},{"key":"2024121916320192600_bib31","doi-asserted-by":"crossref","first-page":"27986","DOI":"10.1039\/C4RA13315C","article-title":"Free radicals, natural antioxidants, and their reaction mechanisms","volume":"5","author":"Nimse","year":"2015","journal-title":"RSC Adv"},{"key":"2024121916320192600_bib32","doi-asserted-by":"crossref","first-page":"e1644","DOI":"10.1002\/wrna.1644","article-title":"Ribosome heterogeneity and specialization in development","volume":"12","author":"Norris","year":"2021","journal-title":"Wires RNA"},{"key":"2024121916320192600_bib33","doi-asserted-by":"crossref","first-page":"5496","DOI":"10.3390\/ijms22115496","article-title":"Ribosome biogenesis and cancer: overview on ribosomal proteins","volume":"22","author":"Pecoraro","year":"2021","journal-title":"Int J Mol Sci"},{"key":"2024121916320192600_bib34","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1038\/nsmb.3454","article-title":"Eukaryotic ribosome assembly, transport and quality control","volume":"24","author":"Pena","year":"2017","journal-title":"Nat Struct Mol Biol"},{"key":"2024121916320192600_bib35","doi-asserted-by":"crossref","first-page":"1354","DOI":"10.1016\/j.bbamcr.2008.01.023","article-title":"Reactive oxygen species and yeast apoptosis","volume":"1783","author":"Perrone","year":"2008","journal-title":"Biochim Biophys Acta"},{"key":"2024121916320192600_bib36","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1042\/bj20040042","article-title":"Dual targeting of yeast catalase A to peroxisomes and mitochondria","volume":"380","author":"Petrova","year":"2004","journal-title":"Biochem J"},{"key":"2024121916320192600_bib37","doi-asserted-by":"crossref","first-page":"987","DOI":"10.1091\/mbc.10.4.987","article-title":"Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae","volume":"10","author":"Powers","year":"1999","journal-title":"Mol Biol Cell"},{"key":"2024121916320192600_bib38","doi-asserted-by":"crossref","first-page":"18628","DOI":"10.1074\/jbc.M117.801704","article-title":"The stress-regulatory transcription factors Msn2 and Msn4 regulate fatty acid oxidation in budding yeast","volume":"292","author":"Rajvanshi","year":"2017","journal-title":"J Biol Chem"},{"key":"2024121916320192600_bib39","doi-asserted-by":"crossref","first-page":"1147","DOI":"10.1091\/mbc.10.4.1147","article-title":"Kinase activity-dependent nuclear export opposes stress-induced nuclear accumulation and retention of Hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae","volume":"10","author":"Reiser","year":"1999","journal-title":"Mol Biol Cell"},{"key":"2024121916320192600_bib40","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1007\/s00425-005-0125-8","article-title":"Mode of translational activation of the catalase (cat1) mRNA of rye leaves (Secale cereale L.) and its control through blue light and reactive oxygen","volume":"223","author":"Schmidt","year":"2006","journal-title":"Planta"},{"key":"2024121916320192600_bib41","doi-asserted-by":"crossref","first-page":"5777","DOI":"10.1073\/pnas.93.12.5777","article-title":"Msn2p, a zinc finger DNA-binding protein, is the transcriptional activator of the multistress response in Saccharomyces cerevisiae","volume":"93","author":"Schmitt","year":"1996","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024121916320192600_bib42","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1007\/BF00351681","article-title":"The Par1 (Yap1\/Snq3) gene of Saccharomyces-cerevisiae, a C-Jun homolog, is involved in oxygen-metabolism","volume":"21","author":"Schnell","year":"1992","journal-title":"Curr Genet"},{"key":"2024121916320192600_bib43","doi-asserted-by":"crossref","first-page":"18469","DOI":"10.1074\/jbc.M117.800003","article-title":"Endonucleolytic cleavage in the expansion segment 7 of 25S rRNA is an early marker of low-level oxidative stress in yeast","volume":"292","author":"Shedlovskiy","year":"2017","journal-title":"J Biol Chem"},{"key":"2024121916320192600_bib44","doi-asserted-by":"crossref","first-page":"3671","DOI":"10.1073\/pnas.88.9.3671","article-title":"Intracellular heterogeneity in mitochondrial-membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1","volume":"88","author":"Smiley","year":"1991","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024121916320192600_bib45","doi-asserted-by":"crossref","first-page":"2336","DOI":"10.1016\/j.cub.2013.09.043","article-title":"Msn2 coordinates a stoichiometric gene expression program","volume":"23","author":"Stewart-Ornstein","year":"2013","journal-title":"Curr Biol"},{"key":"2024121916320192600_bib46","doi-asserted-by":"crossref","first-page":"2512","DOI":"10.18632\/aging.101922","article-title":"Impaired ribosome biogenesis: mechanisms and relevance to cancer and aging","volume":"11","author":"Turi","year":"2019","journal-title":"Aging"},{"key":"2024121916320192600_bib47","doi-asserted-by":"crossref","first-page":"3820","DOI":"10.1073\/pnas.83.11.3820","article-title":"A yeast mutant lacking mitochondrial manganese-superoxide dismutase is hypersensitive to oxygen","volume":"83","author":"van\u00a0Loon","year":"1986","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024121916320192600_bib48","doi-asserted-by":"crossref","first-page":"1511","DOI":"10.1126\/science.1104879","article-title":"When the stress of your environment makes you go HOG wild","volume":"306","author":"Westfall","year":"2004","journal-title":"Science"},{"key":"2024121916320192600_bib49","doi-asserted-by":"crossref","first-page":"4305","DOI":"10.1182\/blood-2011-06-353938","article-title":"Defective ribosome assembly in Shwachman-Diamond syndrome","volume":"118","author":"Wong","year":"2011","journal-title":"Blood"},{"key":"2024121916320192600_bib50","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1038\/nrm3359","article-title":"Specialized ribosomes: a new frontier in gene regulation and organismal biology","volume":"13","author":"Xue","year":"2012","journal-title":"Nat Rev Mol Cell Bio"},{"key":"2024121916320192600_bib51","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.redox.2018.08.016","article-title":"Ribosomal protein L10 in mitochondria serves as a regulator for ROS level in pancreatic cancer cells","volume":"19","author":"Yang","year":"2018","journal-title":"Redox Biol"},{"key":"2024121916320192600_bib52","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1093\/jmcb\/mjv014","article-title":"Ribosomal proteins: functions beyond the ribosome","volume":"7","author":"Zhou","year":"2015","journal-title":"J Mol Cell Biol"},{"key":"2024121916320192600_bib53","doi-asserted-by":"crossref","first-page":"14237","DOI":"10.1074\/jbc.RA118.004174","article-title":"Iron-dependent cleavage of ribosomal RNA during oxidative stress in the yeast Saccharomyces cerevisiae","volume":"293","author":"Zinskie","year":"2018","journal-title":"J Biol Chem"},{"key":"2024121916320192600_bib54","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1152\/physrev.00026.2013","article-title":"Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release","volume":"94","author":"Zorov","year":"2014","journal-title":"Physiol Rev"}],"container-title":["FEMS Yeast Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/femsyr\/advance-article-pdf\/doi\/10.1093\/femsyr\/foae005\/56421400\/foae005.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/femsyr\/article-pdf\/doi\/10.1093\/femsyr\/foae005\/61020209\/foae005.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/femsyr\/article-pdf\/doi\/10.1093\/femsyr\/foae005\/61020209\/foae005.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,19]],"date-time":"2024-12-19T16:40:13Z","timestamp":1734626413000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/femsyr\/article\/doi\/10.1093\/femsyr\/foae005\/7589740"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024]]},"references-count":54,"URL":"https:\/\/doi.org\/10.1093\/femsyr\/foae005","relation":{},"ISSN":["1567-1364"],"issn-type":[{"value":"1567-1364","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024]]},"published":{"date-parts":[[2024]]},"article-number":"foae005"}}