Journal Article
. 2020 May; 9:e53127.
doi: 10.7554/eLife.53127.

Translational control of one-carbon metabolism underpins ribosomal protein phenotypes in cell division and longevity

Nairita Maitra 1 Chong He 2 Heidi M Blank 1 Mitsuhiro Tsuchiya 3 Birgit Schilling 2 Matt Kaeberlein 3 Rodolfo Aramayo 4 Brian K Kennedy 2 Michael Polymenis 1 
  • PMID: 32432546
  •     104 References
  •     3 citations


A long-standing problem is how cells that lack one of the highly similar ribosomal proteins (RPs) often display distinct phenotypes. Yeast and other organisms live longer when they lack specific ribosomal proteins, especially of the large 60S subunit of the ribosome. However, longevity is neither associated with the generation time of RP deletion mutants nor with bulk inhibition of protein synthesis. Here, we queried actively dividing RP mutants through the cell cycle. Our data link transcriptional, translational, and metabolic changes to phenotypes associated with the loss of paralogous RPs. We uncovered translational control of transcripts encoding enzymes of methionine and serine metabolism, which are part of one-carbon (1C) pathways. Cells lacking Rpl22Ap, which are long-lived, have lower levels of metabolites associated with 1C metabolism. Loss of 1C enzymes increased the longevity of wild type cells. 1C pathways exist in all organisms and targeting the relevant enzymes could represent longevity interventions.

Keywords: Rpl22; S. cerevisiae; cell cycle; chromosomes; gene expression; genetics; genomics; longevity; one-carbon; ribosomal; translation.

edgeR: a versatile tool for the analysis of shRNA-seq and CRISPR-Cas9 genetic screens.
Zhiyin Dai, Julie M Sheridan, +8 authors, Matthew E Ritchie.
F1000Res, 2014 May 27; 3. PMID: 24860646    Free PMC article.
A Comprehensive Analysis of Replicative Lifespan in 4,698 Single-Gene Deletion Strains Uncovers Conserved Mechanisms of Aging.
Mark A McCormick, Joe R Delaney, +78 authors, Brian K Kennedy.
Cell Metab, 2015 Oct 13; 22(5). PMID: 26456335    Free PMC article.
Highly Cited.
One-carbon metabolism: an aging-cancer crossroad for the gerosuppressant metformin.
Javier A Menendez, Jorge Joven.
Aging (Albany NY), 2013 Mar 26; 4(12). PMID: 23525940    Free PMC article.
Cytoplasmic serine hydroxymethyltransferase mediates competition between folate-dependent deoxyribonucleotide and S-adenosylmethionine biosyntheses.
Katherine Herbig, En-Pei Chiang, +3 authors, Patrick J Stover.
J Biol Chem, 2002 Aug 06; 277(41). PMID: 12161434
Functional profiling of the Saccharomyces cerevisiae genome.
Guri Giaever, Angela M Chu, +70 authors, Mark Johnston.
Nature, 2002 Jul 26; 418(6896). PMID: 12140549
Highly Cited.
Translate to divide: сontrol of the cell cycle by protein synthesis.
Michael Polymenis, Rodolfo Aramayo.
Microb Cell, 2015 Mar 20; 2(4). PMID: 28357283    Free PMC article.
Nature of the G1 phase of the yeast Saccharomyces cerevisiae.
R A Singer, G C Johnston.
Proc Natl Acad Sci U S A, 1981 May 01; 78(5). PMID: 7019917    Free PMC article.
Ribosomopathies: There's strength in numbers.
Eric W Mills, Rachel Green.
Science, 2017 Nov 04; 358(6363). PMID: 29097519
Highly Cited. Review.
Functional specificity among ribosomal proteins regulates gene expression.
Suzanne Komili, Natalie G Farny, Frederick P Roth, Pamela A Silver.
Cell, 2007 Nov 06; 131(3). PMID: 17981122    Free PMC article.
Highly Cited.
Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients.
Matt Kaeberlein, R Wilson Powers, +7 authors, Brian K Kennedy.
Science, 2005 Nov 19; 310(5751). PMID: 16293764
Highly Cited.
Subtractional Heterogeneity: A Crucial Step toward Defining Specialized Ribosomes.
Joseph W Briggs, Jonathan D Dinman.
Mol Cell, 2017 Jul 08; 67(1). PMID: 28686875    Free PMC article.
Yeast protein extracts.
David C Amberg, Daniel J Burke, Jeffrey N Strathern.
CSH Protoc, 2006 Jan 01; 2006(1). PMID: 22485553
High frequency of RPL22 mutations in microsatellite-unstable colorectal and endometrial tumors.
Ana M Ferreira, Iina Tuominen, +9 authors, Robert M W Hofstra.
Hum Mutat, 2014 Sep 10; 35(12). PMID: 25196364
Beyond the Warburg Effect: How Do Cancer Cells Regulate One-Carbon Metabolism?
Adam Rosenzweig, John Blenis, Ana P Gomes.
Front Cell Dev Biol, 2018 Aug 31; 6. PMID: 30159313    Free PMC article.
Cell cycle regulation of folate-mediated one-carbon metabolism.
Xu Lan, Martha S Field, Patrick J Stover.
Wiley Interdiscip Rev Syst Biol Med, 2018 Jun 12; 10(6). PMID: 29889360
Differential analysis of gene regulation at transcript resolution with RNA-seq.
Cole Trapnell, David G Hendrickson, +3 authors, Lior Pachter.
Nat Biotechnol, 2012 Dec 12; 31(1). PMID: 23222703    Free PMC article.
Highly Cited.
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Ben Langmead, Cole Trapnell, Mihai Pop, Steven L Salzberg.
Genome Biol, 2009 Mar 06; 10(3). PMID: 19261174    Free PMC article.
Highly Cited.
Genetic determinants of cell size at birth and their impact on cell cycle progression in Saccharomyces cerevisiae.
Sandra K Truong, Ryan F McCormick, Michael Polymenis.
G3 (Bethesda), 2013 Jul 04; 3(9). PMID: 23821617    Free PMC article.
Serine and Functional Metabolites in Cancer.
Alice C Newman, Oliver D K Maddocks.
Trends Cell Biol, 2017 Jun 12; 27(9). PMID: 28601431
Yeast Vital Stains: DAPI Stain of Nuclear and Mitochondrial DNA.
David C Amberg, Daniel J Burke, Jeffrey N Strathern.
CSH Protoc, 2006 Jan 01; 2006(1). PMID: 22485564
Folate-mediated one-carbon metabolism.
Jennifer T Fox, Patrick J Stover.
Vitam Horm, 2008 Sep 23; 79. PMID: 18804690
Highly Cited.
Assessing gene-level translational control from ribosome profiling.
Adam B Olshen, Andrew C Hsieh, +3 authors, Barry S Taylor.
Bioinformatics, 2013 Sep 21; 29(23). PMID: 24048356    Free PMC article.
Ablation of ribosomal protein L22 selectively impairs alphabeta T cell development by activation of a p53-dependent checkpoint.
Stephen J Anderson, Jens Peter Holst Lauritsen, +7 authors, David L Wiest.
Immunity, 2007 Jun 09; 26(6). PMID: 17555992
Ssd1 and Gcn2 suppress global translation efficiency in replicatively aged yeast while their activation extends lifespan.
Zheng Hu, Bo Xia, +7 authors, Jessica K Tyler.
Elife, 2018 Aug 18; 7. PMID: 30117416    Free PMC article.
The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments.
Nicholas T Ingolia, Gloria A Brar, +2 authors, Jonathan S Weissman.
Nat Protoc, 2012 Jul 28; 7(8). PMID: 22836135    Free PMC article.
Highly Cited.
Megaloblastosis: from morphos to molecules.
K C Das, Monisha Das, +4 authors, S K Easow.
Med Princ Pract, 2005 Aug 17; 14 Suppl 1. PMID: 16103708
Principles of cellular resource allocation revealed by condition-dependent proteome profiling.
Eyal Metzl-Raz, Moshe Kafri, +3 authors, Naama Barkai.
Elife, 2017 Sep 01; 6. PMID: 28857745    Free PMC article.
A systematic analysis of cell cycle regulators in yeast reveals that most factors act independently of cell size to control initiation of division.
Scott A Hoose, Jeremy A Rawlings, +14 authors, Michael Polymenis.
PLoS Genet, 2012 Mar 23; 8(3). PMID: 22438835    Free PMC article.
Regulation of the balance of one-carbon metabolism in Saccharomyces cerevisiae.
M D Piper, S P Hong, G E Ball, I W Dawes.
J Biol Chem, 2000 Jun 29; 275(40). PMID: 10871621
A hierarchy of trans-acting factors modulates translation of an activator of amino acid biosynthetic genes in Saccharomyces cerevisiae.
A G Hinnebusch.
Mol Cell Biol, 1985 Sep 01; 5(9). PMID: 3915540    Free PMC article.
Highly Cited.
Synthesis of ribosomal proteins during the yeast cell cycle.
R W Shulman, L H Hartwell, J R Warner.
J Mol Biol, 1973 Feb 05; 73(4). PMID: 4577041
Comprehensive analysis of genes involved in the oxidative stress tolerance using yeast heterozygous deletion collection.
Natsumi Okada, Jun Ogawa, Jun Shima.
FEMS Yeast Res, 2014 Jan 15; 14(3). PMID: 24410772
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.
Michael I Love, Wolfgang Huber, Simon Anders.
Genome Biol, 2014 Dec 18; 15(12). PMID: 25516281    Free PMC article.
Highly Cited.
MetaboAnalystR 2.0: From Raw Spectra to Biological Insights.
Jasmine Chong, Mai Yamamoto, Jianguo Xia.
Metabolites, 2019 Mar 27; 9(3). PMID: 30909447    Free PMC article.
Highly Cited.
Microchemostat array with small-volume fraction replenishment for steady-state microbial culture.
Jaewon Park, Jianzhang Wu, Michael Polymenis, Arum Han.
Lab Chip, 2013 Aug 30; 13(21). PMID: 23986263
Protein biogenesis machinery is a driver of replicative aging in yeast.
Georges E Janssens, Anne C Meinema, +7 authors, Matthias Heinemann.
Elife, 2015 Oct 01; 4. PMID: 26422514    Free PMC article.
Generation of High-Quality SWATH® Acquisition Data for Label-free Quantitative Proteomics Studies Using TripleTOF® Mass Spectrometers.
Birgit Schilling, Bradford W Gibson, Christie L Hunter.
Methods Mol Biol, 2017 Feb 12; 1550. PMID: 28188533    Free PMC article.
Expression of the methionine sulfoxide reductase lost during evolution extends Drosophila lifespan in a methionine-dependent manner.
Byung Cheon Lee, Hae Min Lee, +5 authors, Vadim N Gladyshev.
Sci Rep, 2018 Jan 19; 8(1). PMID: 29343716    Free PMC article.
Riborex: fast and flexible identification of differential translation from Ribo-seq data.
Wenzheng Li, Weili Wang, +2 authors, Andrew D Smith.
Bioinformatics, 2017 Feb 06; 33(11). PMID: 28158331    Free PMC article.
Competition between sumoylation and ubiquitination of serine hydroxymethyltransferase 1 determines its nuclear localization and its accumulation in the nucleus.
Donald D Anderson, Jae Y Eom, Patrick J Stover.
J Biol Chem, 2011 Dec 24; 287(7). PMID: 22194612    Free PMC article.
Lifespan extension by methionine restriction requires autophagy-dependent vacuolar acidification.
Christoph Ruckenstuhl, Christine Netzberger, +15 authors, Frank Madeo.
PLoS Genet, 2014 May 03; 10(5). PMID: 24785424    Free PMC article.
Highly Cited.
Multiple knockout analysis of genetic robustness in the yeast metabolic network.
David Deutscher, Isaac Meilijson, Martin Kupiec, Eytan Ruppin.
Nat Genet, 2006 Aug 31; 38(9). PMID: 16941010
Ribosome deficiency protects against ER stress in Saccharomyces cerevisiae.
Kristan K Steffen, Mark A McCormick, +5 authors, Brian K Kennedy.
Genetics, 2012 Mar 02; 191(1). PMID: 22377630    Free PMC article.
Highly Cited.
Nobiletin is main fungistat in tangerines resistant to mal secco.
A Ben-Aziz.
Science, 1967 Feb 24; 155(3765). PMID: 17830494
Developmental arrest of T cells in Rpl22-deficient mice is dependent upon multiple p53 effectors.
Jason E Stadanlick, Zhiqiang Zhang, +7 authors, David L Wiest.
J Immunol, 2011 Jun 22; 187(2). PMID: 21690328    Free PMC article.
Nutrient-specific effects in the coordination of cell growth with cell division in continuous cultures of Saccharomyces cerevisiae.
Jinbai Guo, Brad A Bryan, Michael Polymenis.
Arch Microbiol, 2004 Sep 07; 182(4). PMID: 15349714
Scaling of G1 Duration with Population Doubling Time by a Cyclin in Saccharomyces cerevisiae.
Heidi M Blank, Michelle Callahan, +2 authors, Michael Polymenis.
Genetics, 2018 Aug 29; 210(3). PMID: 30150288    Free PMC article.
The Cost of Protein Production.
Moshe Kafri, Eyal Metzl-Raz, Ghil Jona, Naama Barkai.
Cell Rep, 2016 Jan 05; 14(1). PMID: 26725116    Free PMC article.
Highly Cited.
Transcriptome-wide measurement of translation by ribosome profiling.
Nicholas J McGlincy, Nicholas T Ingolia.
Methods, 2017 Jun 06; 126. PMID: 28579404    Free PMC article.
Highly Cited.
Evolution of 5' untranslated region length and gene expression reprogramming in yeasts.
Zhenguo Lin, Wen-Hsiung Li.
Mol Biol Evol, 2011 Oct 04; 29(1). PMID: 21965341    Free PMC article.
Global analysis of gene function in yeast by quantitative phenotypic profiling.
James A Brown, Gavin Sherlock, +6 authors, J Martin Brown.
Mol Syst Biol, 2006 Jun 02; 2. PMID: 16738548    Free PMC article.
Identification and classification of genes required for tolerance to freeze-thaw stress revealed by genome-wide screening of Saccharomyces cerevisiae deletion strains.
Akira Ando, Toshihide Nakamura, +2 authors, Jun Shima.
FEMS Yeast Res, 2006 Sep 23; 7(2). PMID: 16989656
Ribosome profiling the cell cycle: lessons and challenges.
Rodolfo Aramayo, Michael Polymenis.
Curr Genet, 2017 Apr 30; 63(6). PMID: 28451847    Free PMC article.
Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling.
Nicholas T Ingolia, Sina Ghaemmaghami, John R S Newman, Jonathan S Weissman.
Science, 2009 Feb 14; 324(5924). PMID: 19213877    Free PMC article.
Highly Cited.
Metformin induces a fasting- and antifolate-mimicking modification of systemic host metabolism in breast cancer patients.
Elisabet Cuyàs, Salvador Fernández-Arroyo, +22 authors, Javier A Menendez.
Aging (Albany NY), 2019 May 12; 11(9). PMID: 31076561    Free PMC article.
Pathways to Specialized Ribosomes: The Brussels Lecture.
Jonathan D Dinman.
J Mol Biol, 2016 Jan 15; 428(10 Pt B). PMID: 26764228    Free PMC article.
Highly Cited. Review.
Abundances of transcripts, proteins, and metabolites in the cell cycle of budding yeast reveal coordinate control of lipid metabolism.
Heidi M Blank, Ophelia Papoulas, +5 authors, Michael Polymenis.
Mol Biol Cell, 2020 Mar 05; 31(10). PMID: 32129706    Free PMC article.
Yeast life span extension by depletion of 60s ribosomal subunits is mediated by Gcn4.
Kristan K Steffen, Vivian L MacKay, +11 authors, Matt Kaeberlein.
Cell, 2008 Apr 22; 133(2). PMID: 18423200    Free PMC article.
Highly Cited.
Unification of Protein Abundance Datasets Yields a Quantitative Saccharomyces cerevisiae Proteome.
Brandon Ho, Anastasia Baryshnikova, Grant W Brown.
Cell Syst, 2018 Jan 24; 6(2). PMID: 29361465
Highly Cited.
Gene duplication and the evolution of ribosomal protein gene regulation in yeast.
Ilan Wapinski, Jenna Pfiffner, +3 authors, Aviv Regev.
Proc Natl Acad Sci U S A, 2010 Mar 10; 107(12). PMID: 20212107    Free PMC article.
Inactivation of ribosomal protein L22 promotes transformation by induction of the stemness factor, Lin28B.
Shuyun Rao, Sang-Yun Lee, +15 authors, David L Wiest.
Blood, 2012 Sep 15; 120(18). PMID: 22976955    Free PMC article.
Multiple metabolic requirements for size homeostasis and initiation of division in Saccharomyces cerevisiae.
Shivatheja Soma, Kailu Yang, Maria I Morales, Michael Polymenis.
Microb Cell, 2014 Aug 01; 1(8). PMID: 28357252    Free PMC article.
Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins.
Clement T Y Chan, Yan Ling Joy Pang, +4 authors, Peter C Dedon.
Nat Commun, 2012 Jul 05; 3. PMID: 22760636    Free PMC article.
Highly Cited.
Ribosomal Proteins Rpl22 and Rpl22l1 Control Morphogenesis by Regulating Pre-mRNA Splicing.
Yong Zhang, Monique N O'Leary, +10 authors, David L Wiest.
Cell Rep, 2017 Jan 12; 18(2). PMID: 28076796    Free PMC article.
Ribosomopathies and the paradox of cellular hypo- to hyperproliferation.
Kim De Keersmaecker, Sergey O Sulima, Jonathan D Dinman.
Blood, 2015 Jan 13; 125(9). PMID: 25575543    Free PMC article.
Improved Ribosome-Footprint and mRNA Measurements Provide Insights into Dynamics and Regulation of Yeast Translation.
David E Weinberg, Premal Shah, +3 authors, David P Bartel.
Cell Rep, 2016 Feb 16; 14(7). PMID: 26876183    Free PMC article.
Highly Cited.
Rare ribosomopathies: insights into mechanisms of cancer.
Anna Aspesi, Steven R Ellis.
Nat Rev Cancer, 2019 Jan 24; 19(4). PMID: 30670820
Highly Cited. Review.
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome.
Bo Li, Colin N Dewey.
BMC Bioinformatics, 2011 Aug 06; 12. PMID: 21816040    Free PMC article.
Highly Cited.
Ribosomal proteins and human diseases: pathogenesis, molecular mechanisms, and therapeutic implications.
Wei Wang, Subhasree Nag, +4 authors, Ruiwen Zhang.
Med Res Rev, 2014 Aug 29; 35(2). PMID: 25164622    Free PMC article.
Coupling of cell division to cell growth by translational control of the G1 cyclin CLN3 in yeast.
M Polymenis, E V Schmidt.
Genes Dev, 1997 Oct 23; 11(19). PMID: 9334317    Free PMC article.
Highly Cited.
Serine, glycine and one-carbon units: cancer metabolism in full circle.
Jason W Locasale.
Nat Rev Cancer, 2013 Jul 05; 13(8). PMID: 23822983    Free PMC article.
Highly Cited. Review.
Methionine restriction activates the retrograde response and confers both stress tolerance and lifespan extension to yeast, mouse and human cells.
Jay E Johnson, F Brad Johnson.
PLoS One, 2014 May 17; 9(5). PMID: 24830393    Free PMC article.
How common are extraribosomal functions of ribosomal proteins?
Jonathan R Warner, Kerri B McIntosh.
Mol Cell, 2009 Apr 14; 34(1). PMID: 19362532    Free PMC article.
Highly Cited. Review.
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data.
Heng Li.
Bioinformatics, 2011 Sep 10; 27(21). PMID: 21903627    Free PMC article.
Highly Cited.
Repressed synthesis of ribosomal proteins generates protein-specific cell cycle and morphological phenotypes.
Mamata Thapa, Ananth Bommakanti, +4 authors, Lasse Lindahl.
Mol Biol Cell, 2013 Oct 11; 24(23). PMID: 24109599    Free PMC article.
Enhanced longevity by ibuprofen, conserved in multiple species, occurs in yeast through inhibition of tryptophan import.
Chong He, Scott K Tsuchiyama, +12 authors, Michael Polymenis.
PLoS Genet, 2014 Dec 19; 10(12). PMID: 25521617    Free PMC article.
Hot topics in aging research: protein translation and TOR signaling, 2010.
Matt Kaeberlein, Brian K Kennedy.
Aging Cell, 2010 Dec 24; 10(2). PMID: 21176090    Free PMC article.
Frequent mutations in the RPL22 gene and its clinical and functional implications.
Akiva P Novetsky, Israel Zighelboim, +3 authors, Paul J Goodfellow.
Gynecol Oncol, 2012 Nov 07; 128(3). PMID: 23127973    Free PMC article.
Role of ribosomal protein mutations in tumor development (Review).
Kaveh M Goudarzi, Mikael S Lindström.
Int J Oncol, 2016 Feb 20; 48(4). PMID: 26892688    Free PMC article.
Highly Cited. Review.
Integrative genomics viewer.
James T Robinson, Helga Thorvaldsdóttir, +4 authors, Jill P Mesirov.
Nat Biotechnol, 2011 Jan 12; 29(1). PMID: 21221095    Free PMC article.
Highly Cited.
The ribosomal protein Rpl22 controls ribosome composition by directly repressing expression of its own paralog, Rpl22l1.
Monique N O'Leary, Katherine H Schreiber, +14 authors, Brian K Kennedy.
PLoS Genet, 2013 Aug 31; 9(8). PMID: 23990801    Free PMC article.
Antioxidative and Antidiabetic Effects of Natural Polyphenols and Isoflavones.
Aya Umeno, Masanori Horie, +2 authors, Yasukazu Yoshida.
Molecules, 2016 Jun 02; 21(6). PMID: 27248987    Free PMC article.
Temporary remissions in acute leukemia in children produced by folic acid antagonist, 4-aminopteroyl-glutamic acid.
N Engl J Med, 1948 Jun 03; 238(23). PMID: 18860765
Highly Cited.
DAF1, a mutant gene affecting size control, pheromone arrest, and cell cycle kinetics of Saccharomyces cerevisiae.
F R Cross.
Mol Cell Biol, 1988 Nov 01; 8(11). PMID: 3062366    Free PMC article.
Highly Cited.
Perturbations of Transcription and Gene Expression-Associated Processes Alter Distribution of Cell Size Values in Saccharomyces cerevisiae.
Nairita Maitra, Jayamani Anandhakumar, +2 authors, Michael Polymenis.
G3 (Bethesda), 2018 Nov 23; 9(1). PMID: 30463882    Free PMC article.
Translational control of lipogenic enzymes in the cell cycle of synchronous, growing yeast cells.
Heidi M Blank, Ricardo Perez, +9 authors, Michael Polymenis.
EMBO J, 2017 Jan 07; 36(4). PMID: 28057705    Free PMC article.
PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools.
Huaiyu Mi, Anushya Muruganujan, +2 authors, Paul D Thomas.
Nucleic Acids Res, 2018 Nov 09; 47(D1). PMID: 30407594    Free PMC article.
Highly Cited.
The Gene Ontology Resource: 20 years and still GOing strong.
The Gene Ontology Consortium.
Nucleic Acids Res, 2018 Nov 06; 47(D1). PMID: 30395331    Free PMC article.
Highly Cited.
The Sequence Alignment/Map format and SAMtools.
Heng Li, Bob Handsaker, +7 authors, 1000 Genome Project Data Processing Subgroup.
Bioinformatics, 2009 Jun 10; 25(16). PMID: 19505943    Free PMC article.
Highly Cited.
One-Carbon Metabolism in Health and Disease.
Gregory S Ducker, Joshua D Rabinowitz.
Cell Metab, 2016 Sep 20; 25(1). PMID: 27641100    Free PMC article.
Highly Cited. Review.
Synthesis of ribosomal proteins during the cell cycle of the yeast Saccharomyces cerevisiae.
S G Elliott, J R Warner, C S McLaughlin.
J Bacteriol, 1979 Feb 01; 137(2). PMID: 370092    Free PMC article.
Specialized ribosomes: a new frontier in gene regulation and organismal biology.
Shifeng Xue, Maria Barna.
Nat Rev Mol Cell Biol, 2012 May 24; 13(6). PMID: 22617470    Free PMC article.
Highly Cited. Review.
Amino acid analysis by reverse-phase high-performance liquid chromatography: precolumn derivatization with phenylisothiocyanate.
R L Heinrikson, S C Meredith.
Anal Biochem, 1984 Jan 01; 136(1). PMID: 6711815
Highly Cited.
Model for the regulation of mRNA translation applied to haemoglobin synthesis.
H F Lodish.
Nature, 1974 Oct 04; 251(5474). PMID: 4421673
Highly Cited.
Heterogeneous Ribosomes Preferentially Translate Distinct Subpools of mRNAs Genome-wide.
Zhen Shi, Kotaro Fujii, +4 authors, Maria Barna.
Mol Cell, 2017 Jun 20; 67(1). PMID: 28625553    Free PMC article.
Highly Cited.
Ser3p (Yer081wp) and Ser33p (Yil074cp) are phosphoglycerate dehydrogenases in Saccharomyces cerevisiae.
Eva Albers, Vincent Laizé, +2 authors, Lena Gustafsson.
J Biol Chem, 2003 Jan 15; 278(12). PMID: 12525494
Improving SNP discovery by base alignment quality.
Heng Li.
Bioinformatics, 2011 Feb 16; 27(8). PMID: 21320865    Free PMC article.
Highly Cited.
Ribosome Levels Selectively Regulate Translation and Lineage Commitment in Human Hematopoiesis.
Rajiv K Khajuria, Mathias Munschauer, +24 authors, Vijay G Sankaran.
Cell, 2018 Mar 20; 173(1). PMID: 29551269    Free PMC article.
Highly Cited.
Characterization of two 5-aminoimidazole-4-carboxamide ribonucleotide transformylase/inosine monophosphate cyclohydrolase isozymes from Saccharomyces cerevisiae.
A S Tibbetts, D R Appling.
J Biol Chem, 2000 Jul 06; 275(27). PMID: 10877846
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration.
Helga Thorvaldsdóttir, James T Robinson, Jill P Mesirov.
Brief Bioinform, 2012 Apr 21; 14(2). PMID: 22517427    Free PMC article.
Highly Cited.
Genetic interaction between a chaperone of small nucleolar ribonucleoprotein particles and cytosolic serine hydroxymethyltransferase.
Yunfeng Yang, U Thomas Meier.
J Biol Chem, 2003 Apr 18; 278(26). PMID: 12700234
Small and Large Ribosomal Subunit Deficiencies Lead to Distinct Gene Expression Signatures that Reflect Cellular Growth Rate.
Ze Cheng, Christopher Frederick Mugler, +7 authors, Gloria Ann Brar.
Mol Cell, 2018 Dec 07; 73(1). PMID: 30503772    Free PMC article.
Methionine restriction extends lifespan of Drosophila melanogaster under conditions of low amino-acid status.
Byung Cheon Lee, Alaattin Kaya, +6 authors, Vadim N Gladyshev.
Nat Commun, 2014 Apr 09; 5. PMID: 24710037    Free PMC article.
Highly Cited.
Measuring replicative life span in the budding yeast.
Kristan K Steffen, Brian K Kennedy, Matt Kaeberlein.
J Vis Exp, 2009 Jun 27; (28). PMID: 19556967    Free PMC article.
Ribosomal Protein uL11 as a Regulator of Metabolic Circuits Related to Aging and Cell Cycle.
Mateusz Mołoń, Eliza Molestak, +2 authors, Marek Tchórzewski.
Cells, 2020 Jul 28; 9(7). PMID: 32708309    Free PMC article.
Ribosomal proteins: mutant phenotypes by the numbers and associated gene expression changes.
Michael Polymenis.
Open Biol, 2020 Aug 19; 10(8). PMID: 32810425    Free PMC article.
A cell non-autonomous mechanism of yeast chronological aging regulated by caloric restriction and one-carbon metabolism.
Elisa Enriquez-Hesles, Daniel L Smith, +11 authors, Jeffrey S Smith.
J Biol Chem, 2020 Nov 28;. PMID: 33243834    Free PMC article.