2025
Eukaryotic Microproteins
Jaunbocus N, Ebenki V, Su H, Slavoff S. Eukaryotic Microproteins. Annual Review Of Biochemistry 2025, 94: 1-28. PMID: 40245354, PMCID: PMC12207985, DOI: 10.1146/annurev-biochem-080124-012840.Peer-Reviewed Original Research
2024
Expression of Random Sequences and de novo Evolved Genes From the Mouse in Human Cells Reveals Functional Diversity and Specificity
Aldrovandi S, Castro J, Ullrich K, Karger A, Luria V, Tautz D. Expression of Random Sequences and de novo Evolved Genes From the Mouse in Human Cells Reveals Functional Diversity and Specificity. Genome Biology And Evolution 2024, 16: evae175. PMID: 39663928, PMCID: PMC11635099, DOI: 10.1093/gbe/evae175.Peer-Reviewed Original ResearchConceptsOpen reading frameGene open reading frameCellular regulatory pathwaysNoncoding DNAReading frameHuman cell linesHuman genomeAlpha-helicesGrowth experimentsCellular physiologyFunctional diversityPositive selectionBeta-sheetTranscriptomic responseRegulatory pathwaysAdaptive advantageHuman cellsGenesCell clonesCell linesSequenceClonesRandom sequencePathwayCellsUPF1 regulates mRNA stability by sensing poorly translated coding sequences
Musaev D, Abdelmessih M, Vejnar C, Yartseva V, Weiss L, Strayer E, Takacs C, Giraldez A. UPF1 regulates mRNA stability by sensing poorly translated coding sequences. Cell Reports 2024, 43: 114074. PMID: 38625794, PMCID: PMC11259039, DOI: 10.1016/j.celrep.2024.114074.Peer-Reviewed Original ResearchConceptsUpstream open reading framesOpen reading frameRegulate mRNA stabilityNonsense-mediated decayMRNA stabilityReading frameOpen reading frame lengthRegulate mRNA decayAU-rich elementsMicroRNA Binding SitesCis-elementsTranslation initiationStop codonMRNA decayCodon optimizationUPF1Gene expressionBinding sitesCodonMRNAConvergent rolesHigher decay ratesMachine-learning analysisUTRExitron splicing of odor receptor genes in Drosophila
Shang X, Talross G, Carlson J. Exitron splicing of odor receptor genes in Drosophila. Proceedings Of The National Academy Of Sciences Of The United States Of America 2024, 121: e2320277121. PMID: 38507450, PMCID: PMC10990081, DOI: 10.1073/pnas.2320277121.Peer-Reviewed Original ResearchConceptsExitron splicingOdorant receptor genesCases of alternative splicingCanonical open reading framesExpression of odorant receptor genesFunction of olfactory systemReceptor geneProtein-coding exonsOpen reading frameAlternative splicing eventsOlfactory receptor neuronsAlternative polyadenylationReading frameExon-intronEncode proteinsSplicing eventsAlternative splicingNon-coding RNAsStable proteinsPheromone receptorsReceptor neuronsOptogenetic activationPheromone stimulationSplicingNeuronal activityEvolution of the functionality of microbial communities in patients with metastatic renal cell carcinoma (mRCC) receiving cabozantinib (cabo)/nivolumab (nivo) with or without CBM588: A randomized clinical trial.
Ebrahimi H, Meza L, Lee K, Malhotra J, Alcantara M, Zengin Z, Dizman N, Hsu J, Llamas-Quitiquit M, Castro D, Mercier B, Barragan-Carrillo R, Chawla N, Li X, Liu S, Chehrazi-Raffle A, Dorff T, Frankel P, Tripathi A, Pal S. Evolution of the functionality of microbial communities in patients with metastatic renal cell carcinoma (mRCC) receiving cabozantinib (cabo)/nivolumab (nivo) with or without CBM588: A randomized clinical trial. Journal Of Clinical Oncology 2024, 42: 460-460. DOI: 10.1200/jco.2024.42.4_suppl.460.Peer-Reviewed Original ResearchMetastatic renal cell carcinomaMetabolic pathwaysClinical outcomesAnnotated open reading framesFunction of microbial communitiesMetatranscriptomic sequencing dataWhole metagenome sequencingOpen reading frameGut microbial functionsGut microbiome functionsResponse rate to sorafenibExperimental armElectron transfer chainCancer cell typesAssociated with clinical outcomesRenal cell carcinomaReading frameSequence dataTaxonomic profilesBiosynthesis pathwayMetagenomic sequencingMicrobiome functionMicrobial functionsMolecular functionsRandomized clinical trialsA compact regulatory RNA element in mouse Hsp70 mRNA
Wang W, Liu F, Ugalde M, Pyle A. A compact regulatory RNA element in mouse Hsp70 mRNA. NAR Molecular Medicine 2024, 1: ugae002. PMID: 38318492, PMCID: PMC10840451, DOI: 10.1093/narmme/ugae002.Peer-Reviewed Original ResearchOpen reading frameRNA elementsHeat shockOpen reading frame sequenceRegulatory RNA elementsSecondary structure modelMessenger RNACap-independent mannerCap-dependent translationMolecular chaperone functionSequences of HSP70Reading frameMisfolded proteinsRNA foldingRegulate protein expressionChaperone functionMRNA sequencesUntranslated regionShort stretchSecondary structureCell stressGene expressionHSP70 gene expressionStructural basisMolecular mechanisms
2023
A conserved uORF in the ilvBNC mRNA of Corynebacterium species regulates ilv operon expression
Narunsky A, Kavita K, Panchapakesan S, Fris M, Breaker R. A conserved uORF in the ilvBNC mRNA of Corynebacterium species regulates ilv operon expression. Microbial Genomics 2023, 9: mgen001019. PMID: 37233150, PMCID: PMC10272879, DOI: 10.1099/mgen.0.001019.Peer-Reviewed Original ResearchConceptsBranched-chain amino acidsRNA motifsUpstream open reading framesTranscription attenuation mechanismStructured noncoding RNAsOpen reading frameRiboswitch classesTranscription attenuationProtein translationNoncoding RNAsOperon expressionGenetic approachesReading frameStart codonUORF translationStop codonBacterial speciesHost cellsGenesUORFsAmino acidsMotifCodonCommon mechanismCorynebacterium specieslinc-mipep and linc-wrb encode micropeptides that regulate chromatin accessibility in vertebrate-specific neural cells
Tornini V, Miao L, Lee H, Gerson T, Dube S, Schmidt V, Kroll F, Tang Y, Du K, Kuchroo M, Vejnar C, Bazzini A, Krishnaswamy S, Rihel J, Giraldez A. linc-mipep and linc-wrb encode micropeptides that regulate chromatin accessibility in vertebrate-specific neural cells. ELife 2023, 12: e82249. PMID: 37191016, PMCID: PMC10188112, DOI: 10.7554/elife.82249.Peer-Reviewed Original ResearchConceptsCell typesIntergenic non-coding RNAsChromatin architectural proteinCryptic open reading frameGene regulatory networksOpen reading frameNon-coding RNAsNew cell typesNeural cell typesBrain cell typesPutative lincRNAsVertebrate genomesArchitectural proteinsChromatin disruptionChromatin accessibilityRegulatory networksGenetic basisCell developmentMicropeptidesBrain cell developmentReceptor-mediated pathwaySystematic identificationLincRNAsNeural cellsCerebellar cellsChemical labeling and proteomics for characterization of unannotated small and alternative open reading frame-encoded polypeptides
Chen Y, Cao X, Loh K, Slavoff S. Chemical labeling and proteomics for characterization of unannotated small and alternative open reading frame-encoded polypeptides. Biochemical Society Transactions 2023, 51: 1071-1082. PMID: 37171061, PMCID: PMC10317152, DOI: 10.1042/bst20221074.Peer-Reviewed Original ResearchConceptsChemical labelingAlternative open reading framesOpen reading frameLimited sequence homologyMammalian genomesGene classesProtein domainsQuantitative proteomicsReading frameSequence homologyBiological roleProteomic discoveryMolecular levelSmORFsCell proliferationProteomicsInteractomeGenomeSpecific propertiesExperimental techniquesLabelingHomologyPolypeptideProteinFunctionalization
2022
Two neuronal peptides encoded from a single transcript regulate mitochondrial complex III in Drosophila
Bosch J, Ugur B, Pichardo-Casas I, Rabasco J, Escobedo F, Zuo Z, Brown B, Celniker S, Sinclair D, Bellen H, Perrimon N. Two neuronal peptides encoded from a single transcript regulate mitochondrial complex III in Drosophila. ELife 2022, 11: e82709. PMID: 36346220, PMCID: PMC9681215, DOI: 10.7554/elife.82709.Peer-Reviewed Original ResearchConceptsSmall open reading framesClasses of genesShares sequence similarityOpen reading frameSequence similarityBicistronic transcriptBiological functionsPhenotypic analysisMitochondrial functionImportant regulatorThousands of peptidesNeuronal functionGenesWealth of informationTranscriptsAnimal lethalityPeptidesRecent studiesParalogsDrosophilaSmORFsMitochondriaRegulatorRegulatesNeuronal peptidesMapping subcellular localizations of unannotated microproteins and alternative proteins with MicroID
Na Z, Dai X, Zheng SJ, Bryant CJ, Loh KH, Su H, Luo Y, Buhagiar AF, Cao X, Baserga SJ, Chen S, Slavoff SA. Mapping subcellular localizations of unannotated microproteins and alternative proteins with MicroID. Molecular Cell 2022, 82: 2900-2911.e7. PMID: 35905735, PMCID: PMC9662605, DOI: 10.1016/j.molcel.2022.06.035.Peer-Reviewed Original ResearchConceptsSubcellular localizationProximity biotinylationSmall open reading framesAlternative proteinsOpen reading frameHigh-throughput technologiesSubnuclear organellesCanonical proteinsRRNA transcriptionSubcellular compartmentsReading frameProteogenomic identificationProtein compositionAmino acidsMicroproteinsProteinBiotinylationLocalizationTurboIDTranscriptionOrganellesMouse modelPolypeptideNucleoliExpressionTranscriptional and Translational Dynamics of Zika and Dengue Virus Infection
Singh K, Martinez M, Lin J, Gregory J, Nguyen T, Abdelaal R, Kang K, Brennand K, Grünweller A, Ouyang Z, Phatnani H, Kielian M, Wendel H. Transcriptional and Translational Dynamics of Zika and Dengue Virus Infection. Viruses 2022, 14: 1418. PMID: 35891396, PMCID: PMC9316442, DOI: 10.3390/v14071418.Peer-Reviewed Original ResearchConceptsAminoacyl-tRNA synthetasesHuman neuronal progenitor cellsUpstream ORFsStress responseCellular stress responseOpen reading frameCell stress responseSimultaneous RNA sequencingViral RNA genomeGene expression dataNeuronal progenitor cellsZika virusRibosome occupancyDengue virusGenome sequenceTRNA synthetasesReading frameRNA sequencingRNA translationRNA genomeTranslation capacityKey enzymeViral translationExpression dataRNA viruses
2021
Cellular Adaptations to Cytoplasmic Mg2+ Limitation
Groisman EA, Chan C. Cellular Adaptations to Cytoplasmic Mg2+ Limitation. Annual Review Of Microbiology 2021, 75: 649-672. PMID: 34623895, DOI: 10.1146/annurev-micro-020518-115606.Peer-Reviewed Original ResearchConceptsCytoplasmic MgLeader regionATP-dependent proteaseTranscriptional regulator PhoPAbundant divalent cationOpen reading frameActivity of ribosomesSimilar adaptation strategiesRegulated proteolysisExpression of proteinsRegulator PhoPMicrobial speciesReading frameCellular adaptationDifferent genesCoding regionsBacterial speciesProtein synthesisSpeciesProteinAbundanceDivalent cationsExpressionCytoplasmic Mg2Enzymatic reactionsPhosphorylation of a Human Microprotein Promotes Dissociation of Biomolecular Condensates
Na Z, Luo Y, Cui DS, Khitun A, Smelyansky S, Loria JP, Slavoff SA. Phosphorylation of a Human Microprotein Promotes Dissociation of Biomolecular Condensates. Journal Of The American Chemical Society 2021, 143: 12675-12687. PMID: 34346674, PMCID: PMC8564862, DOI: 10.1021/jacs.1c05386.Peer-Reviewed Original ResearchConceptsMembraneless organellesSmall open reading framesP-body dynamicsLiquid-liquid phase separationOpen reading frameGrowth factor signalingPresence of RNAEvolutionary conservationP-bodiesCellular processesCell divisionReading frameProteogenomic identificationFactor signalingMacromolecular complexesBiomolecular condensatesSecondary structureAmino acidsCell growthMicroproteinsPhosphorylationCell proliferationOrganellesBiophysical processesProliferationNoncanonical open reading frames encode functional proteins essential for cancer cell survival
Prensner J, Enache O, Luria V, Krug K, Clauser K, Dempster J, Karger A, Wang L, Stumbraite K, Wang V, Botta G, Lyons N, Goodale A, Kalani Z, Fritchman B, Brown A, Alan D, Green T, Yang X, Jaffe J, Roth J, Piccioni F, Kirschner M, Ji Z, Root D, Golub T. Noncanonical open reading frames encode functional proteins essential for cancer cell survival. Nature Biotechnology 2021, 39: 697-704. PMID: 33510483, PMCID: PMC8195866, DOI: 10.1038/s41587-020-00806-2.Peer-Reviewed Original ResearchConceptsCancer cell linesOpen reading framePotential therapeutic targetCell linesGrowth inhibitory effectsCancer cell survivalInduced gene expression changesBreast cancerTherapeutic targetHuman cancer cell linesReading frameProtein expressionActive proteinProtein 1Gene expression changesCell survivalBiological effectsExpression changesViability defectsHuman genomeGenomic analysisCodon mutagenesisEctopic expressionFunctional proteinsKnockoutAlt-RPL36 downregulates the PI3K-AKT-mTOR signaling pathway by interacting with TMEM24
Cao X, Khitun A, Luo Y, Na Z, Phoodokmai T, Sappakhaw K, Olatunji E, Uttamapinant C, Slavoff SA. Alt-RPL36 downregulates the PI3K-AKT-mTOR signaling pathway by interacting with TMEM24. Nature Communications 2021, 12: 508. PMID: 33479206, PMCID: PMC7820019, DOI: 10.1038/s41467-020-20841-6.Peer-Reviewed Original ResearchMeSH KeywordsAlternative SplicingAmino Acid SequenceBase SequenceBiological TransportCell MembraneDown-RegulationEndoplasmic ReticulumHEK293 CellsHumansMembrane ProteinsMutationPhosphatidylinositol 3-KinasesPhosphatidylinositol 4,5-DiphosphateProtein BindingProto-Oncogene Proteins c-aktRibosomal ProteinsSignal TransductionTOR Serine-Threonine KinasesConceptsPI3K-AktEndoplasmic reticulumMTOR signalingHuman gene functionAlternative open reading framesOpen reading framePI3K signalingDifferent molecular mechanismsCanonical proteinsGene functionCell sizeReading framePrecursor phosphatidylinositolPlasma membraneTMEM24Upstream regulatorMolecular mechanismsPhosphoserine residuesK signalingPoint mutationsSignalingPhosphatidylinositolProteinReticulumRPL36
2020
TBIO-26. NON-CANONICAL OPEN READING FRAMES ENCODE FUNCTIONAL PROTEINS ESSENTIAL FOR CANCER CELL SURVIVAL
Prensner J, Enache O, Luria V, Krug K, Clauser K, Dempster J, Karger A, Wang L, Stumbraite K, Wang V, Botta G, Lyons N, Goodale A, Kalani Z, Fritchman B, Brown A, Alan D, Green T, Yang X, Jaffe J, Roth J, Piccioni F, Kirschner M, Ji Z, Root D, Golub T. TBIO-26. NON-CANONICAL OPEN READING FRAMES ENCODE FUNCTIONAL PROTEINS ESSENTIAL FOR CANCER CELL SURVIVAL. Neuro-Oncology 2020, 22: iii471-iii471. PMCID: PMC7715501, DOI: 10.1093/neuonc/noaa222.849.Peer-Reviewed Original ResearchOpen reading frameNon-canonical open reading framesProtein translationReading frameMultiple cancer typesPutative non-coding RNAProtein-coding genesSingle-cell RNA sequencingNon-canonical proteinsFunctional genomic screensCancer-implicated genesCancer cell linesCell-autonomous mannerNon-coding RNANon-coding RNAsGene expression changesPotential cancer therapeutic targetCell linesHEK293T cellsCancer cell survivalCancer therapeutic targetNon-gonadal tissuesCell cycle arrestRibosome profilingCancer cell typesZero-Valent Iron Sand Filtration Can Reduce Human and Plant Pathogenic Bacteria While Increasing Plant Growth Promoting Bacteria in Reclaimed Water
Kulkarni P, Olson N, Bui A, Bradshaw R, Del Collo L, Hittle L, Handy E, Paulson J, Ghurye J, Nasko D, East C, Van Kessel J, Kniel K, Chiu P, Mongodin E, Pop M, Sharma M, Sapkota A. Zero-Valent Iron Sand Filtration Can Reduce Human and Plant Pathogenic Bacteria While Increasing Plant Growth Promoting Bacteria in Reclaimed Water. Frontiers In Environmental Science 2020, 8: 541921. DOI: 10.3389/fenvs.2020.541921.Peer-Reviewed Original ResearchProportion of open reading framesNitrogen-fixing bacterial generaZVI-sand filtrationPlant pathogenic genusPlant growth-promoting bacteriaPlant pathogenic bacteriaRRNA gene sequencesOpen reading frameMetagenomic shotgun sequencingExploratory functional analysisAntimicrobial susceptibility testingGrowth-promoting bacteriaBacterial community structureTetracycline-resistant E. coliReclaimed waterOxidative stress responseShotgun sequencingReading frameZVI-sandGene sequencesBacterial generaPathogenic generaBacterial communitiesIron-rich environmentsPromoting bacteriaThe NBDY Microprotein Regulates Cellular RNA Decapping
Na Z, Luo Y, Schofield JA, Smelyansky S, Khitun A, Muthukumar S, Valkov E, Simon MD, Slavoff SA. The NBDY Microprotein Regulates Cellular RNA Decapping. Biochemistry 2020, 59: 4131-4142. PMID: 33059440, PMCID: PMC7682656, DOI: 10.1021/acs.biochem.0c00672.Peer-Reviewed Original ResearchConceptsP-bodiesNonsense-mediated decay factorsKO cellsSmall open reading framesCytoplasmic ribonucleoprotein granulesOpen reading frameSubstrate transcriptsCellular transcriptomeRibonucleoprotein granulesTarget transcriptsRNA stabilityKnockout cellsUTR lengthReading frameGlobal profilingProteogenomic identificationMacromolecular complexesHuman RNACellular RNACytoplasmic RNAGene stabilityAmino acidsCell growthMicroproteinsTranscriptsComparative Proteomic Profiling of Unannotated Microproteins and Alternative Proteins in Human Cell Lines
Cao X, Khitun A, Na Z, Dumitrescu DG, Kubica M, Olatunji E, Slavoff SA. Comparative Proteomic Profiling of Unannotated Microproteins and Alternative Proteins in Human Cell Lines. Journal Of Proteome Research 2020, 19: 3418-3426. PMID: 32449352, PMCID: PMC7429271, DOI: 10.1021/acs.jproteome.0c00254.Peer-Reviewed Original ResearchConceptsRibosome profilingHuman cell linesQuantitative mass spectrometry-based proteomicsCell linesMass spectrometry-based proteomicsLabel-free quantitative proteomicsComplex human proteomeLabel-free comparative proteomicsAlternative open reading framesStress-dependent expressionSpectrometry-based proteomicsTissue-specific expressionOpen reading frameComparative proteomic profilingUnannotated ORFsComparative proteomicsUnannotated proteinsMammalian cellsHuman proteomeQuantitative proteomicsDifferential translationReading frameProteomic profilingHuman leukemia cell linesRegulated expression
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