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OroshiMass SpectrometryShotgun proteomicsNot availablePost-translational modificationEmbryonicDynamicPhosphorylationPhosphoproteomicsStem cellMescSignal transductionEpilcEasyphosProteomicsDifferentiationMass spectrometryPluripotencyhttp://www.ebi.ac.uk/pride/archive/projects/PXD010621EmbryoStem CellCell lysates were processed using the EasyPhos platform. Detailed protocols are provided in the associated manuscript.PrideNot availablephosphorylated residueMass spectrometry RAW data were processed using MaxQuant and analysed using Perseus. Detailed settings are provided in the associated manuscript.ProteomicsMultiomicsMatthias MannQ ExactivePARTIALDepartment of Proteomics and Signal Transduction Max Planck Institute of BiochemistryMus Musculus (mouse)31078527 Yang P, Humphrey SJ, Cinghu S, Pathania R, Oldfield AJ, Kumar D, Perera D, Yang JYH, James DE, Mann M, Jothi R. Multi-omic Profiling Reveals Dynamics of the Phased Progression of Pluripotency. Cell Syst. 2019 8(5):427-445.e10 10.1016/j.cels.2019.03.012oroshi@biochem.mpg.deBiologicalProteomicsGermanyPluripotency is highly dynamic and progresses through a continuum of pluripotent stem cell states. The two states that bookend the pluripotency continuum, naive and primed, are well characterized, but our understanding of the intermediate states and transitions between them remains incomplete. Here, we dissect the dynamics of pluripotent state transitions underlying pre- to post-implantation epiblast differentiation. Through comprehensive mapping of the proteome, phosphoproteome, transcriptome, and epigenome of embryonic stem cells transitioning from naive to primed pluripotency, we find that rapid, acute, and widespread changes to the phosphoproteome precede ordered changes to the epigenome, transcriptome, and proteome. Reconstruction of the kinase-substrate networks reveals signaling cascades, dynamics, and crosstalk. Distinct waves of global proteomic changes mark discrete phases of pluripotency, with cell-state-specific surface markers tracking pluripotent state transitions. Our data provide new insights into multi-layered control of the phased progression of pluripotency and a foundation for modeling mechanisms regulating pluripotent state transitions (www.stemcellatlas.org).Multi-omic Profiling Reveals Dynamics of the Phased Progression of Pluripotency.Yang Pengyi P, Humphrey Sean J SJ, Cinghu Senthilkumar S, Pathania Rajneesh R, Oldfield Andrew J AJ, Kumar Dhirendra D, Perera Dinuka D, Yang Jean Y H JYH, James David E DE, Mann Matthias M, Jothi Raja RTaf[[II]]250, Manuscripts., Taf200, dTAF[[II]]230, TAF[[II]]250, d230, dTAF[[II]]250, TAF[[II]]230, TFIID TAF250, cel, cell, TAF200, l(3)84Ab, dTAFII250, Taf1p, TAF[II]250, BG:DS00004.13, TAFII-250, CG17603, TAF250/230, TAF[[II]], EfW1, Cell, dTAF230, dTAF250, dmTAF[[II]]230, TAFII250, DmelCG17603, Taf250, dmTAF1, SR3-5, Taf230, p230, TAF[[II]]250/230, TFIID, associated, TAF, TAF230, TAF250, TAF1phase, Progression, Phased, Multiple, Phase, Cancer Progression, progression, Multi, Disease Progression., Cancer Disease Progression, disease progression, Tumor Progression, MULTIPLE, StageMass Spectrum Analysis, Spectroscopy, Svc, Manuscripts., Mass Spectrum, Bru, data, Col4a-1, Raw, Analyses, Mass, Spectrometry, Del(8)44H, Analysis, associated, Spectrum Analyses, Mass Spectrum Analyses, Spectrum Analysis, Mass SpectroscopyCPD photolyase activity, d230, biological signaling, Par1c, PhrB photolyase activity, Transcriptome Profile, Stem Cells, Par-1c, Gene Expression Profile, Gene, stalk, dTAFII250, Profiles, photoreactivating enzyme activity, pigmented epithelium, EfW1, DmelCG8201, deoxyribodipyrimidine photolyase activity, stratum pigmentosum retinae, dmTAF[[II]]230, Readability, surface, dmTAF1, Taf230, dPAR-1, 3, stratum pigmentosa retinae, NUP96, Kinase, outer pigmented layer of retina, dPar-1, primary stem, epithelium, Phosphotransferase, integumentum commune, TAF250, Taf200, 27C1, MOS3, dTAF[[II]]250, deoxyribocyclobutadipyrimidine pyrimidine-lyase activity, TFIID TAF250, reference sample, PRECOCIOUS, cel, cell, Embryonic Stem Cell, l(2)k06323, Profile, pigmented retina, F23A5.3, primitive ectoderm, Taf1p, Transphosphorylase, DNA Methylomes, Signatures, culm, DNA cyclobutane dipyrimidine photolyase activity, SUPPRESSOR OF AUXIN RESISTANCE 3, dTAF250, PAR-1, pigment epithelium of retina, Expression Signature, signaling process, pigmented retina epithelium, Transcriptomes, Par-1, TAF, ATP Phosphotransferases, CG16701, F23A5_3, ATP, single organism signaling, Controlled, PRE, par1, data, Controlling, dTAF[[II]]230, TAF[[II]]250, Transcriptome, CG8201, external covering of organism, axis, Methylomes, deoxyribonucleic cyclobutane dipyrimidine photolyase activity, Expression Profiles, TAF200, incomplete, dPAR1, total expressed protein, dPar1, l(3)84Ab, dMARK, organism surface, BG:DS00004.13, ectoblast, TAFII-250, pigmented retinal epithelium, TAF250/230, CG11960, Cell, Phosphotransferases, dTAF230, Acute onset, CG30131, CG30132, abolished, Gene Expression, EMK, stratum pigmentosum (retina), TAFII250, MODIFIER OF SNC1, retinal pigment, Stem Cell, p230, Expression Signatures, Gene Expression Signatures, anon-WO0210402.19, DPAR-1, deoxyribonucleic photolyase activity, TAF[[II]]250/230, dipyrimidine photolyase (photosensitive), TFIID, Gene Expression Signature, blastocyst, Expression Profile, Methylome, retinal pigment layer, Transcriptome Profiles, Embryonic, Taf[[II]]250, Transphosphorylases, RPE, TAF[[II]]230, distinct, Foundation., Epigenomes, photolyase activity, Kinases, body surface, retinal pigmented epithelium, epiblast, TAF[II]250, Understanding, CG17603, TAF[[II]], retinal pigment epithelium, signalling, p. pigmentosa retinae, phr A photolyase activity, l(2)27C1, DmelCG17603, DNA-photoreactivating enzyme, signalling process, primary axis, Taf250, BcDNA:RH48823, integumentary system, SR3-5, Gene Expression Profiles, Cells, MARK, DPar1, deoxyribonucleate pyrimidine dimer lyase (photosensitive), PAR1, Par1, DNA, Signature, epiblastus, Embryonic Stem, dermal system, Proteomes, TAF230, TAF1, DNA MethylomeCPD photolyase activity, Par1c, PhrB photolyase activity, Stem Cells, Gene Expression Profile, Profiles, NK/GPI., pigmented epithelium, Foundation, DmelCG8201, dmTAF[[II]]230, Readability, 3, NUP96, Kinase, outer pigmented layer of retina, Gpi-1, epithelium, integumentum commune, TFIID TAF250, reference sample, cel, Nlk, pigmented retina, DNA Methylomes, Signatures, DNA cyclobutane dipyrimidine photolyase activity, SUPPRESSOR OF AUXIN RESISTANCE 3, pigment epithelium of retina, Expression Signature, signaling process, pigmented retina epithelium, Transcriptomes, ATP Phosphotransferases, CG16701, ATP, single organism signaling, Gpi, PRE, dTAF[[II]]230, CG8201, external covering of organism, Methylomes, deoxyribonucleic cyclobutane dipyrimidine photolyase activity, Expression Profiles, incomplete, TAF200, dMARK, organism surface, pigmented retinal epithelium, TAFII-250, TAF250/230, CG11960, Acute onset, CG30131, CG30132, abolished, Gene Expression, EMK, TAFII250, mOC-X, retinal pigment, Stem Cell, Expression Signatures, DPAR-1, dipyrimidine photolyase (photosensitive), NK|GPI, Expression Profile, Methylome, retinal pigment layer, Transcriptome Profiles, Transphosphorylases, ORG, Org, retinal pigmented epithelium, epiblast, Gpi1-r, Gpi1-s, CG17603, Gpi1-t, TAF[[II]], phr A photolyase activity, l(2)27C1, DNA-photoreactivating enzyme, Taf250, BcDNA:RH48823, integumentary system, SR3-5, Cells, MARK, DNA, Embryonic Stem, dermal system, Proteomes, Bglap-rs1, TAF230, Gpi1s, DNA Methylome, biological signaling, d230, Transcriptome Profile, AI461847, Par-1c, Gene, dTAFII250, photoreactivating enzyme activity, EfW1, deoxyribodipyrimidine photolyase activity, stratum pigmentosum retinae, surface, dmTAF1, dPAR-1, Taf230, Pgi, stratum pigmentosa retinae, dPar-1, Phosphotransferase, TAF250, 27C1, Taf200, MOS3, deoxyribocyclobutadipyrimidine pyrimidine-lyase activity, dTAF[[II]]250, PRECOCIOUS, cell, Gpi-1r, Embryonic Stem Cell, l(2)k06323, Gpi-1s, Profile, Phi, Gpi-1t, F23A5.3, primitive ectoderm, Taf1p, Transphosphorylase, dTAF250, PAR-1, Par-1, TAF, F23A5_3, Controlled, par1, data, Controlling, TAF[[II]]250, Transcriptome, dPAR1, total expressed protein, dPar1, l(3)84Ab, ectoblast, BG:DS00004.13, MF, Amf, Cell, Phosphotransferases, dTAF230, stratum pigmentosum (retina), MODIFIER OF SNC1, PSC cell, p230, Gene Expression Signatures, anon-WO0210402.19, deoxyribonucleic photolyase activity, TAF[[II]]250/230, TFIID, Gene Expression Signature, blastocyst, NK, Embryonic, Taf[[II]]250, RPE, TAF[[II]]230, distinct, Epigenomes, photolyase activity, Kinases, body surface, TAF[II]250, Understanding, retinal pigment epithelium, signalling, p. pigmentosa retinae, DmelCG17603, signalling process, Gene Expression Profiles, DPar1, deoxyribonucleate pyrimidine dimer lyase (photosensitive), PAR1, Par1, Signature, epiblastus, TAF1phase, Progression, Phased, Multiple, Phase, Cancer Progression, progression, Multi, Disease Progression., Cancer Disease Progression, disease progression, Tumor Progression, MULTIPLE, StagefalseMulti-Omic Profiling Reveals Dynamics of the Phased Progression of PluripotencyPluripotency is highly dynamic and progresses through a continuum of pluripotent stem-cell states. The two states that bookend the pluripotency continuum, naïve and primed, are well characterized, but our understanding of the intermediate states and transitions between them remain incomplete. Here, we dissect the dynamics of pluripotent state transitions underlying pre- to post-implantation epiblast differentiation. Through comprehensive mapping of the proteome, phosphoproteome, transcriptome, and epigenome of embryonic stem cells transitioning from naïve to primed pluripotency, we find that rapid, acute, and widespread changes to the phosphoproteome precede ordered changes to the epigenome, transcriptome, and proteome. Reconstruction of kinase-substrate networks reveals signaling cascades, dynamics, and crosstalk. Distinct waves of global proteomic changes mark discrete phases of pluripotency, with cell state-specific surface markers tracking pluripotent state transitions. Our data provide new insights into the multi-layered control of the phased progression of pluripotency and a foundation for modeling mechanisms regulating pluripotent state transitions (www.stemcellatlasorg).2019-05-072018-07-30PXD0106212806551646099180498511145422492156843544071284218327042363336351198343006636362758385696363121766668888111430155571145263145262364934613126957366649239161936413645106656889511363647627236611123294422295558326813042323122586365434607925193659106321432059712938655819125023254537111957748186619682158672256807617554373592536685862740816918045427877512010892250583674147956410039236942049433445974142001258641935293NCBITaxon:77643671567593643867716054048313152826930456271639162429204277944762376369612181003296292211376394863948840479NCBITaxon:215713152731051067125027820596875497792016516368407173630969893610478214836432042929410106132049138169374327732046640707453511110310780621745921612928867128867641006945694101676341021076127735113165821358430141729817463367541287356756840301350621813019411192943936711041136445913949843202530127032022149875110475941204788613474951537211097165299827905135551398031758543980126086639808137575551832019644719821114155421932555211383439119318198139818102697026635311069955529NCBITaxon:47518502983354764146547798251021691572739823897648407413735186287054824153NCBITaxon:505579844675251000364334147548021035974137081154665478983532215998381067710348198523487804225314884142228632266347946157187125939915991915729529292117527198601488406334249518691234235238152335985898598865597464998703920211107263990363527215987419082874394232418235024145113969293190259390719017463601237474636172262536001319722119158531058859698951105198997237989772000263419610264266722758858156899628737562690724420237172019998570724074767927459615333554319311671833554184005136861505968666211961748666134751536329NCBITaxon:17632862871103411033348837670580271848186536859598607575527472036105135294296110098402321000734882412336363071047005187878945556449447NCBITaxon:13356262664955419591399878168119011478281055524NCBITaxon:96063181781358584690081366848197915351930728593008526411409005118499526225412133759139014381113944235084370416744312044143708351581990119519532590841370137023943222774862615835583715371633376057267998086371137121906503714759172073127262981274575727090309031637910372814243371421044792491108239412NCBITaxon:9615658858147802692661006581373527504541356638164752037506442236695021293497905463224555253651997649908143899237453747264732376026473128870559553614169152527403271602938511497864794363755293824794372251177529912044741673872175091938441376593934347393271591002263767423444234546700128768959119846704146479293652803428038280351080348330779179392112621229502711311803738681911265269971028622527391076015973611432425071140981087135547743658142450722953379698204232124223321803369822130080347081645733185889716546759928777020382931412529550811481744888643745264999728303571830855071762997076789268370415156288765138856392456115293202086595551655181135491432137159749535026143213858781707683194963401614280053164686275110466038151845474485009747697477118051240174841855601555479204274381513201488711053253297261005941289093164351211604990013894382835423242331082934122058560416299131122731701879915429131267818187104931640729946714423683033373304852646383011306413992530642369923121162065261610337286129940207340115357652611114716133865431201725323712552329935316317NCBITaxon:11084993841063267872862321933486208621160791392227681196125522814953932132232334774121827532917573129948861814084341033519963139248913924881153381153393304393755699286265599339112094886241571839975864442374864353324442606653324134390976821271786371979856863999839986865535291486541042986357358257632884019864982380111911028688999586652203411508599632138119380625631886571303443112130886581144889198466645463NCBITaxon:11072NCBITaxon:11071142800628835374375116597145943116598854331116781077854314408043933434NCBITaxon:11082693977381382189931824431935128387145953116885311213278695berry8694100333586972443664701501114286921504751499105484204714722354025120847014649744497431170089306218644193061107632330805660396016217974825853946055396513212790568813377512981766378876017112147861050236694657349632051124501897441739412450128853183889198679488531911137910371647351660152943631631198573896939343237956026087121346334323223544314275241433611334565560291699636436802790105603140818838185733703401881274414936530437552196969716203871398558408172405598609183827275921274423408170275981274420127442623545513656531762793821176275943286303902474801199150956481882291690255120455148167238473848190695148498101510693731263753405203860186497405224052141856451804NCBITaxon:8134780091522754847938703338493871917226175610946161435120325812055052352594473205493864112572265121651253880376686120678112202230743220118670511867057387334869121938791868023980071868012154514683514081861508471206777691838851608611388869152167786721279010087043512317196928123929486771331548454226126219813188268241122926571632957693812471246148545132838834839294911390363120416266589077151488003694269416943694518790101508081705394206542105568731744712701532924281411194669116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