基于质谱的磷酸化蛋白质组学:富集、检测、鉴定和定量
|
摘要
磷酸化是一种调控生命活动的重要翻译后修饰,调控生物的生长发育、信号转导、以及疾病的发生发展.从上世纪80年代开始,质谱应用于蛋白质磷酸化的检测中,极大地推动了磷酸化蛋白质组学的发展.质谱检测拥有高灵敏度、高通量的特点,更重要的是具有位点分辨率,因此基于质谱的磷酸化蛋白质组检测方法得到不断的发展和推广.常见的磷酸化蛋白质组研究,首先对磷酸化肽段进行富集,然后进行串联质谱分析,最后通过搜索引擎对修饰位点进行鉴定和定量.本文从这个三个基本方面,对磷酸化蛋白质组研究进行综述,并对未来研究发展方向进行讨论.
Protein phosphorylation is one of post-translational modifications(PTM), which plays a role in regulation of development, signal transduction, and processes of diseases. Because of high sensitivity, considerable throughput, and residue resolution, mass spectrometry(MS) has been the most popular tool for phosphorylation modification analysis. Common MS-centric phosphoproteomics workflow includes phosphorylation modified peptides sampling, LC-MS/MS detection, phosphorylation sites assignment and quantification. We summarized and discussed these workflow parts in this review.
Protein phosphorylation is one of post-translational modifications(PTM), which plays a role in regulation of development, signal transduction, and processes of diseases. Because of high sensitivity, considerable throughput, and residue resolution, mass spectrometry(MS) has been the most popular tool for phosphorylation modification analysis. Common MS-centric phosphoproteomics workflow includes phosphorylation modified peptides sampling, LC-MS/MS detection, phosphorylation sites assignment and quantification. We summarized and discussed these workflow parts in this review.
引文
[1]Kosako H,Nagano K.Quantitative phosphoproteomics strategies for understanding protein kinase-mediated signal transduction pathways.Expert Review of Proteomics,2011,8(1):81-94
[2]Zhu W G.Regulation of p53 acetylation.Science China Life Science,2017,60(3):321-323
[3]Lu H,Zhang Y,Yang P.Advancements in mass spectrometry-based glycoproteomics and glycomics.National Science Review,2016,3(3):345-364
[4]Olsen J V,Blagoev B,Gnad F,et al.Global,in vivo,and site-specific phosphorylation dynamics in signaling networks.Cell,2006,127(3):635-648
[5]Cohen P.The role of protein phosphorylation in human health and disease.European Journal of Biochemistry,2001,268(19):5001-5010
[6]Johnson L N.The regulation of protein phosphorylation.Biochemical Society Transactions,2009,37(4):627-641
[7]Moorhead G B,De Wever V,Templeton G,et al.Evolution of protein phosphatases in plants and animals.Biochemical Journal,2009,417(2):401-409
[8]Daub H,Olsen J V,Bairlein M,et al.Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle.Molecular Cell,2008,31(3):438-448
[9]Huttlin E L,Jedrychowski M P,Elias J E,et al.A tissue-specific atlas of mouse protein phosphorylation and expression.Cell,2010,143(7):1174-1189
[10]Sacco F,Humphrey S J,Cox J,et al.Glucose-regulated and drug-perturbed phosphoproteome reveals molecular mechanisms controlling insulin secretion.Nature Communications,2016,7:13250(DOI:10.1038/comms13250)
[11]Pierobon M,Wulfkuhle J,Liotta L,et al.Application of molecular technologies for phosphoproteomic analysis of clinical samples.Oncogene,2015,34(7):805-814
[12]Maes E,Tirez K,Baggerman G,et al.The use of elemental mass spectrometry in phosphoproteomic applications.Mass Spectrom Review,2016,35(3):350-360
[13]Chen I H,Xue L,Hsu C C,et al.Phosphoproteins in extracellular vesicles as candidate markers for breast cancer.Proc Natl Acad Sci,2017,114(12):3175-3180
[14]Liu J J,Sharma K,Zangrandi L,et al.In vivo brain GPCR signaling elucidated by phosphoproteomics.Science,2018,360(6395),pii:eaao4927.doi:10.1126/science.aao4927
[15]Macek B,Mann M,Olsen J V.Global and site-specific quantitative phosphoproteomics:principles and applications.Annu Review of Pharmacology and Toxicology,2009,49(1):199-221
[16]Doll S,Burlingame A L.Mass spectrometry-based detection and assignment of protein posttranslational modifications.ACSChemical Biology,2015,10(1):63-71
[17]Nilsson C L.Advances in quantitative phosphoproteomics.Analytical Chemistry,2012,84(2):735-746
[18]Mertins P,Tang L C,Krug K,et al.Reproducible workflow for multiplexed deep-scale proteome and phosphoproteome analysis of tumor tissues by liquid chromatography-mass spectrometry.Nature Protocols,2018,13(7):1632-1661
[19]Kanshin E,Tyers M,Thibault P.Sample collection method bias effects in quantitative phosphoproteomics.Journal of Proteome Research,2015,14(7):2998-3004
[20]Mertins P,Yang F,Liu T,et al.Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels.Molecular&Cellular Proteomics,2014:mcp.M113.036392
[21]Riley N M,Coon J J.Phosphoproteomics in the age of rapid and deep proteome profiling.Analytical Chemistry,2016,88(1):74-94
[22]Possemato A P,Paulo J A,Mulhern D,et al.Multiplexed phosphoproteomic profiling using titanium dioxide and immunoaffinity enrichments reveals complementary phosphorylation events.Journal of Proteome Research,2017,16(4):1506-1514
[23]Tsai C F,Hsu C C,Hung J N,et al.Sequential phosphoproteomic enrichment through complementary metal-directed immobilized metal ion affinity chromatography.Analytical Chemistry,2014,86(1):685-693
[24]Lai A C Y,Tsai C F,Hsu C C,et al.Complementary Fe3+-and Ti4+-immobilized metal ion affinity chromatography for purification of acidic and basic phosphopeptides.Rapid Communications in Mass Spectrometry,2012,26(18):2186-2194
[25]Abelin J G,Trantham P D,Penny S A,et al.Complementary IMACenrichment methods for HLA-associated phosphopeptide identification by mass spectrometry.Nature Protocols,2015,10(9):1308-1318
[26]Zhou H,Ye M,Dong J,et al.Robust phosphoproteome enrichment using monodisperse microsphere-based immobilized titanium(IV)ion affinity chromatography.Nature Protocols,2013,8(3):461-480
[27]Kanshin E,Michnick S W,Thibault P.Displacement of N/Q-rich peptides on TiO2beads enhances the depth and coverage of yeast phosphoproteome analyses.Journal of Proteome Research,2013,12(6):2905-2913
[28]Vilasi A,Fiume I,Pace P,et al.Enrichment specificity of micro and nano-sized titanium and zirconium dioxides particles in phosphopeptide mapping.Journal of Mass Spectrometry,2013,48(11):1188-1198
[29]Berard A,Kroeker A,Mcqueen P,et al.Methods and approaches to disease mechanisms using systems kinomics.Synthetic and Systems Biotechnology,2017,3(1):34-43
[30]Matheron L,Van Den Toorn H,Heck A J R,et al.Characterization of biases in phosphopeptide enrichment by Ti4+-immobilized metal affinity chromatography and TiO2using a massive synthetic library and human cell digests.Analytical Chemistry,2014,86(16):8312-8320
[31]Kettenbach A N,Gerber S A.Rapid and reproducible single-stage phosphopeptide enrichment of complex peptide mixtures:application to general and phosphotyrosine-specific phosphoproteomics experiments.Analytical Chemistry,2011,83(20):7635-7644
[32]Di Palma S,Zoumaro-Djayoon A,Peng M,et al.Finding the same needles in the haystack?A comparison of phosphotyrosine peptides enriched by immuno-affinity precipitation and metal-based affinity chromatography.Journal of Proteomics,2013,91:331-337(DOI:10.1016/prot.2013.07.024)
[33]Van Der Mijn J C,Labots M,Piersma S R,et al.Evaluation of different phospho-tyrosine antibodies for label-free phosphoproteomics.Journal of Proteomics,2015,127(B):259-263
[34]Du J,Bernasconi P,Clauser K R,et al.Bead-based profiling of tyrosine kinase phosphorylation identifies SRC as a potential target for glioblastoma therapy.Nature Biotechnology,2008,27(1):77-83
[35]Dickhut C,Feldmann I,Lambert J,et al.Impact of digestion conditions on phosphoproteomics.Journal of Proteome Research,2014,13(6):2761-2770
[36]Giansanti P,Aye T T,Van Den Toorn H,et al.An augmented multiple-protease-based human phosphopeptide atlas.Cell Reports,2015,11(11):1834-1843
[37]Bian Y,Ye M,Song C,et al.Improve the coverage for the analysis of phosphoproteome of He La cells by a tandem digestion approach.Journal of Proteome Research,2012,11(5):2828-2837
[38]Glatter T,Ludwig C,AhrnéE,et al.Large-scale quantitative assessment of different in-solution protein digestion protocols reveals superior cleavage efficiency of tandem Lys-C/trypsin proteolysis over trypsin digestion.Journal of Proteome Research,2012,11(11):5145-5156
[39]Ruprecht B,Koch H,Medard G,et al.Comprehensive and reproducible phosphopeptide enrichment using iron immobilized metal ion affinity chromatography(Fe-IMAC)columns.Molecular&Cellular Proteomics,2015,14(1):205-215
[40]Lombardi B,Rendell N,Edwards M,et al.Evaluation of phosphopeptide enrichment strategies for quantitative TMTanalysis of complex network dynamics in cancer-associated cell signalling.EuPA Open Proteomics,2015,6(C):10-15
[41]Batth T S,Francavilla C,Olsen J V.Off-line high-pH reversedphase fractionation for in-depth phosphoproteomics.Journal of Proteome Research,2014,13(12):6176-6186
[42]Hoehenwarter W,Thomas M,Nukarinen E,et al.Identification of novel in vivo MAP kinase substrates in Arabidopsis thaliana through use of tandem metal oxide affinity chromatography.Molecular&Cellular Proteomics,2013,12(2):369-380
[43]Zhang Y,Fonslow B R,Shan B,et al.Protein analysis by shotgun/bottom-up proteomics.Chemical Reviews,2013,113(4):2343-2394
[44]Syka J E P,Marto J A,Bai D L,et al.Novel linear quadrupole ion trap/FT mass spectrometer:?performance characterization and use in the comparative analysis of histone H3 post-translational modifications.Journal of Proteome Research,2004,3(3):621-626
[45]Michalski A,Damoc E,Hauschild J-P,et al.Mass spectrometrybased proteomics using Q Exactive,a high-performance benchtop quadrupole orbitrap mass spectrometer.Molecular&Cellular Proteomics,2011:mcp.M111.011015
[46]Michalski A,Damoc E,Lange O,et al.Ultra high resolution linear ion trap orbitrap mass spectrometer(Orbitrap Elite)facilitates top down LC MS/MS and versatile peptide fragmentation modes.Molecular&Cellular Proteomics,2012,11(3):O111.013698
[47]Senko M W,Remes P M,Canterbury J D,et al.Novel parallelized quadrupole/linear ion trap/orbitrap tribrid mass spectrometer improving proteome coverage and peptide identification rates.Analytical Chemistry,2013,85(24):11710-11714
[48]Erickson B K,Jedrychowski M P,Mcalister G C,et al.Evaluating multiplexed quantitative phosphopeptide analysis on a hybrid quadrupole mass filter/linear ion trap/orbitrap mass spectrometer.Analytical Chemistry,2015,87(2):1241-1249
[49]Kelstrup C D,Jersie-Christensen R R,Batth T S,et al.Rapid and deep proteomes by faster sequencing on a benchtop quadrupole ultra-high-field orbitrap mass spectrometer.Journal of Proteome Research,2014,13(12):6187-6195
[50]Law K P,Lim Y P.Recent advances in mass spectrometry:data independent analysis and hyper reaction monitoring.Expert Review of Proteomics,2013,10(6):551-566
[51]Graumann J,Scheltema R A,Zhang Y,et al.A framework for intelligent data acquisition and real-time database searching for shotgun proteomics.Molecular&Cellular Proteomics,2012,11(3):M111.013185
[52]Bailey D J,Mcdevitt M T,Westphall M S,et al.Intelligent data acquisition blends targeted and discovery methods.Journal of Proteome Research,2014,13(4):2152-2161
[53]Narumi R,Murakami T,Kuga T,et al.A strategy for large-scale phosphoproteomics and SRM-based validation of human breast cancer tissue samples.Journal of Proteome Research,2012,11(11):5311-5322
[54]Cui L,Reid G E.Examining factors that influence erroneous phosphorylation site localization via competing fragmentation and rearrangement reactions during ion trap CID-MS/MS and MS3.Proteomics,2013,13(6):964-973
[55]Syka J E,Coon J J,Schroeder M J,et al.Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry.Proc Natl Acad Sci,2004,101(26):9528-9533
[56]Sarbu M,Ghiulai R M,Zamfir A D.Recent developments and applications of electron transfer dissociation mass spectrometry in proteomics.Amino Acids,2014,46(7):1625-1634
[57]Frese C K,Altelaar A M,Van Den Toorn H,et al.Toward full peptide sequence coverage by dual fragmentation combining electron-transfer and higher-energy collision dissociation tandem mass spectrometry.Analytical Chemistry,2012,84(22):9668-9673
[58]Frese C K,Zhou H,Taus T,et al.Unambiguous phosphosite localization using electron-transfer/higher-energy collision dissociation(EThcD).Journal of Proteome Research,2013,12(3):1520-1525
[59]Gunawardena H P,Emory J F,Mcluckey S A.Phosphopeptide anion characterization via sequential charge inversion and electron-transfer dissociation.Analytical Chemistry,2006,78(11):3788-3793
[60]Robinson M R,Moore K L,Brodbelt J S.Direct identification of tyrosine sulfation by using ultraviolet photodissociation mass spectrometry.Journal of the American Society for Mass Spectrometry,2014,25(8):1461-1471
[61]Zanivan S,Meves A,Behrendt K,et al.In vivo SILAC-based proteomics reveals phosphoproteome changes during mouse skin carcinogenesis.Cell Reports,2013,3(2):552-566
[62]Oppermann F S,Klammer M,Bobe C,et al.Comparison of SILACand mTRAQ quantification for phosphoproteomics on a quadrupole orbitrap mass spectrometer.Journal of Proteome Research,2013,12(9):4089-4100
[63]Wilson-Grady J T,Haas W,Gygi S P.Quantitative comparison of the fasted and re-fed mouse liver phosphoproteomes using lower pH reductive dimethylation.Methods,2013,61(3):277-286
[64]Mcalister G C,Huttlin E L,Haas W,et al.Increasing the multiplexing capacity of TMTs using reporter ion isotopologues with isobaric masses.Analytical Chemistry,2012,84(17):7469-7478
[65]Mertins P,Udeshi N D,Clauser K R,et al.iTRAQ labeling is superior to mTRAQ for quantitative global proteomics and phosphoproteomics.Molecular&Cellular Proteomics,2012,11(6):M111.014423
[66]Xue L,Wang P,Cao P,et al.Identification of ERK1 direct substrates using stable isotope labeled kinase assay-linked phosphoproteomics.Molecular&Cellular Proteomics,2014,mcp.O114.038588
[67]Neilson K A,Ali N A,Muralidharan S,et al.Less label,more free:approaches in label‐free quantitative mass spectrometry.Proteomics,2011,11(4):535-553
[68]Schilling B,Rardin M J,Maclean B X,et al.Platform-independent and label-free quantitation of proteomic data using MS1 extracted ion chromatograms in skyline:application to protein acetylation and phosphorylation.Molecular&Cellular Proteomics,2012,11(5):202-214
[69]Tyanova S,Temu T,Cox J.The MaxQuant computational platform for mass spectrometry-based shotgun proteomics.Nature Protocols,2016,11(12):2301
[70]Eng J K,Searle B C,Clauser K R,et al.A face in the crowd:recognizing peptides through database search.Molecular&Cellular Proteomics,2011,10(11):R111.009522
[71]Chalkley R J,Clauser K R.Modification site localization scoring:strategies and performance.Molecular&Cellular Proteomics,2012,11(5):3-14
[72]Elias J E,Gygi S P.Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry.Nature Methods,2007,4(3):207-214
[73]Fermin D,Walmsley S J,Gingras A-C,et al.LuciPHOr:algorithm for phosphorylation site localization with false localization rate estimation using target-decoy approach.Molecular&Cellular Proteomics,2013,mcp.M113.028928
[74]Savitski M M,Lemeer S,Boesche M,et al.Confident phosphorylation site localization using the Mascot Delta Score.Molecular&Cellular Proteomics,2011,10(2):M110.003830
[75]Baker P R,Trinidad J C,Chalkley R J.Modification site localization scoring integrated into a search engine.Molecular&Cellular Proteomics,2011,mcp.M111.008078
[76]Beausoleil S A,Villén J,Gerber S A,et al.A probability-based approach for high-throughput protein phosphorylation analysis and site localization.Nature Biotechnology,2006,24(10):1285-1292
[77]Tanner S,Shu H,Frank A,et al.InsPecT:identification of posttranslationally modified peptides from tandem mass spectra.Analytical Chemistry,2005,77(14):4626-4639
[78]Bailey C M,Sweet S M,Cunningham D L,et al.SLo Mo:automated site localization of modifications from ETD/ECD mass spectra.Journal of Proteome Research,2009,8(4):1965-1971
[79]Phanstiel D H,Brumbaugh J,Wenger C D,et al.Proteomic and phosphoproteomic comparison of human ES and iPS cells.Nature Methods,2011,8(10):821-827
[80]Taus T,Kocher T,Pichler P,et al.Universal and confident phosphorylation site localization using phosphoRS.Journal of Proteome Research,2011,10(12):5354-5362
[81]Shi Q,Chen Y G.Interplay between TGF-beta signaling and receptor tyrosine kinases in tumor development.Science China Life Science,2017,60(10):1133-1141
[82]Li X,Wang W,Chen J.Recent progress in mass spectrometry proteomics for biomedical research.Science China Life Science,2017,60(10):1093-1113
[83]Strahl B,Allis C.The language of covalent histone.Nature,2000,403(6765):41-45
[84]Potel C M,Lin M H,Heck A J R,et al.Widespread bacterial protein histidine phosphorylation revealed by mass spectrometry-based proteomics.Nature Methods,2018,15(3):187-190
[85]Zhu Y,Guo T.Towards a one-stop solution for large-scale proteomics data analysis.Science China Life Science,2018,61(3):351-354
[86]Feng J,Ding C,Qiu N,et al.Firmiana:towards a one-stop proteomic cloud platform for data processing and analysis.Nature Biotechnology,2017,35(5):409-412
[87]Robles M S,Humphrey S J,Mann M.Phosphorylation is a central mechanism for circadian control of metabolism and physiology.Cell Metabolism,2017,25(1):118-127
[88]Hunter T.The age of crosstalk:phosphorylation,ubiquitination,and beyond.Molecular Cell,2007,28(5):730-738
[89]Zhou J M,Yang W C.Receptor-like kinases take center stage in plant biology.Science China Life Science,2016,59(9):863-866
[2]Zhu W G.Regulation of p53 acetylation.Science China Life Science,2017,60(3):321-323
[3]Lu H,Zhang Y,Yang P.Advancements in mass spectrometry-based glycoproteomics and glycomics.National Science Review,2016,3(3):345-364
[4]Olsen J V,Blagoev B,Gnad F,et al.Global,in vivo,and site-specific phosphorylation dynamics in signaling networks.Cell,2006,127(3):635-648
[5]Cohen P.The role of protein phosphorylation in human health and disease.European Journal of Biochemistry,2001,268(19):5001-5010
[6]Johnson L N.The regulation of protein phosphorylation.Biochemical Society Transactions,2009,37(4):627-641
[7]Moorhead G B,De Wever V,Templeton G,et al.Evolution of protein phosphatases in plants and animals.Biochemical Journal,2009,417(2):401-409
[8]Daub H,Olsen J V,Bairlein M,et al.Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle.Molecular Cell,2008,31(3):438-448
[9]Huttlin E L,Jedrychowski M P,Elias J E,et al.A tissue-specific atlas of mouse protein phosphorylation and expression.Cell,2010,143(7):1174-1189
[10]Sacco F,Humphrey S J,Cox J,et al.Glucose-regulated and drug-perturbed phosphoproteome reveals molecular mechanisms controlling insulin secretion.Nature Communications,2016,7:13250(DOI:10.1038/comms13250)
[11]Pierobon M,Wulfkuhle J,Liotta L,et al.Application of molecular technologies for phosphoproteomic analysis of clinical samples.Oncogene,2015,34(7):805-814
[12]Maes E,Tirez K,Baggerman G,et al.The use of elemental mass spectrometry in phosphoproteomic applications.Mass Spectrom Review,2016,35(3):350-360
[13]Chen I H,Xue L,Hsu C C,et al.Phosphoproteins in extracellular vesicles as candidate markers for breast cancer.Proc Natl Acad Sci,2017,114(12):3175-3180
[14]Liu J J,Sharma K,Zangrandi L,et al.In vivo brain GPCR signaling elucidated by phosphoproteomics.Science,2018,360(6395),pii:eaao4927.doi:10.1126/science.aao4927
[15]Macek B,Mann M,Olsen J V.Global and site-specific quantitative phosphoproteomics:principles and applications.Annu Review of Pharmacology and Toxicology,2009,49(1):199-221
[16]Doll S,Burlingame A L.Mass spectrometry-based detection and assignment of protein posttranslational modifications.ACSChemical Biology,2015,10(1):63-71
[17]Nilsson C L.Advances in quantitative phosphoproteomics.Analytical Chemistry,2012,84(2):735-746
[18]Mertins P,Tang L C,Krug K,et al.Reproducible workflow for multiplexed deep-scale proteome and phosphoproteome analysis of tumor tissues by liquid chromatography-mass spectrometry.Nature Protocols,2018,13(7):1632-1661
[19]Kanshin E,Tyers M,Thibault P.Sample collection method bias effects in quantitative phosphoproteomics.Journal of Proteome Research,2015,14(7):2998-3004
[20]Mertins P,Yang F,Liu T,et al.Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels.Molecular&Cellular Proteomics,2014:mcp.M113.036392
[21]Riley N M,Coon J J.Phosphoproteomics in the age of rapid and deep proteome profiling.Analytical Chemistry,2016,88(1):74-94
[22]Possemato A P,Paulo J A,Mulhern D,et al.Multiplexed phosphoproteomic profiling using titanium dioxide and immunoaffinity enrichments reveals complementary phosphorylation events.Journal of Proteome Research,2017,16(4):1506-1514
[23]Tsai C F,Hsu C C,Hung J N,et al.Sequential phosphoproteomic enrichment through complementary metal-directed immobilized metal ion affinity chromatography.Analytical Chemistry,2014,86(1):685-693
[24]Lai A C Y,Tsai C F,Hsu C C,et al.Complementary Fe3+-and Ti4+-immobilized metal ion affinity chromatography for purification of acidic and basic phosphopeptides.Rapid Communications in Mass Spectrometry,2012,26(18):2186-2194
[25]Abelin J G,Trantham P D,Penny S A,et al.Complementary IMACenrichment methods for HLA-associated phosphopeptide identification by mass spectrometry.Nature Protocols,2015,10(9):1308-1318
[26]Zhou H,Ye M,Dong J,et al.Robust phosphoproteome enrichment using monodisperse microsphere-based immobilized titanium(IV)ion affinity chromatography.Nature Protocols,2013,8(3):461-480
[27]Kanshin E,Michnick S W,Thibault P.Displacement of N/Q-rich peptides on TiO2beads enhances the depth and coverage of yeast phosphoproteome analyses.Journal of Proteome Research,2013,12(6):2905-2913
[28]Vilasi A,Fiume I,Pace P,et al.Enrichment specificity of micro and nano-sized titanium and zirconium dioxides particles in phosphopeptide mapping.Journal of Mass Spectrometry,2013,48(11):1188-1198
[29]Berard A,Kroeker A,Mcqueen P,et al.Methods and approaches to disease mechanisms using systems kinomics.Synthetic and Systems Biotechnology,2017,3(1):34-43
[30]Matheron L,Van Den Toorn H,Heck A J R,et al.Characterization of biases in phosphopeptide enrichment by Ti4+-immobilized metal affinity chromatography and TiO2using a massive synthetic library and human cell digests.Analytical Chemistry,2014,86(16):8312-8320
[31]Kettenbach A N,Gerber S A.Rapid and reproducible single-stage phosphopeptide enrichment of complex peptide mixtures:application to general and phosphotyrosine-specific phosphoproteomics experiments.Analytical Chemistry,2011,83(20):7635-7644
[32]Di Palma S,Zoumaro-Djayoon A,Peng M,et al.Finding the same needles in the haystack?A comparison of phosphotyrosine peptides enriched by immuno-affinity precipitation and metal-based affinity chromatography.Journal of Proteomics,2013,91:331-337(DOI:10.1016/prot.2013.07.024)
[33]Van Der Mijn J C,Labots M,Piersma S R,et al.Evaluation of different phospho-tyrosine antibodies for label-free phosphoproteomics.Journal of Proteomics,2015,127(B):259-263
[34]Du J,Bernasconi P,Clauser K R,et al.Bead-based profiling of tyrosine kinase phosphorylation identifies SRC as a potential target for glioblastoma therapy.Nature Biotechnology,2008,27(1):77-83
[35]Dickhut C,Feldmann I,Lambert J,et al.Impact of digestion conditions on phosphoproteomics.Journal of Proteome Research,2014,13(6):2761-2770
[36]Giansanti P,Aye T T,Van Den Toorn H,et al.An augmented multiple-protease-based human phosphopeptide atlas.Cell Reports,2015,11(11):1834-1843
[37]Bian Y,Ye M,Song C,et al.Improve the coverage for the analysis of phosphoproteome of He La cells by a tandem digestion approach.Journal of Proteome Research,2012,11(5):2828-2837
[38]Glatter T,Ludwig C,AhrnéE,et al.Large-scale quantitative assessment of different in-solution protein digestion protocols reveals superior cleavage efficiency of tandem Lys-C/trypsin proteolysis over trypsin digestion.Journal of Proteome Research,2012,11(11):5145-5156
[39]Ruprecht B,Koch H,Medard G,et al.Comprehensive and reproducible phosphopeptide enrichment using iron immobilized metal ion affinity chromatography(Fe-IMAC)columns.Molecular&Cellular Proteomics,2015,14(1):205-215
[40]Lombardi B,Rendell N,Edwards M,et al.Evaluation of phosphopeptide enrichment strategies for quantitative TMTanalysis of complex network dynamics in cancer-associated cell signalling.EuPA Open Proteomics,2015,6(C):10-15
[41]Batth T S,Francavilla C,Olsen J V.Off-line high-pH reversedphase fractionation for in-depth phosphoproteomics.Journal of Proteome Research,2014,13(12):6176-6186
[42]Hoehenwarter W,Thomas M,Nukarinen E,et al.Identification of novel in vivo MAP kinase substrates in Arabidopsis thaliana through use of tandem metal oxide affinity chromatography.Molecular&Cellular Proteomics,2013,12(2):369-380
[43]Zhang Y,Fonslow B R,Shan B,et al.Protein analysis by shotgun/bottom-up proteomics.Chemical Reviews,2013,113(4):2343-2394
[44]Syka J E P,Marto J A,Bai D L,et al.Novel linear quadrupole ion trap/FT mass spectrometer:?performance characterization and use in the comparative analysis of histone H3 post-translational modifications.Journal of Proteome Research,2004,3(3):621-626
[45]Michalski A,Damoc E,Hauschild J-P,et al.Mass spectrometrybased proteomics using Q Exactive,a high-performance benchtop quadrupole orbitrap mass spectrometer.Molecular&Cellular Proteomics,2011:mcp.M111.011015
[46]Michalski A,Damoc E,Lange O,et al.Ultra high resolution linear ion trap orbitrap mass spectrometer(Orbitrap Elite)facilitates top down LC MS/MS and versatile peptide fragmentation modes.Molecular&Cellular Proteomics,2012,11(3):O111.013698
[47]Senko M W,Remes P M,Canterbury J D,et al.Novel parallelized quadrupole/linear ion trap/orbitrap tribrid mass spectrometer improving proteome coverage and peptide identification rates.Analytical Chemistry,2013,85(24):11710-11714
[48]Erickson B K,Jedrychowski M P,Mcalister G C,et al.Evaluating multiplexed quantitative phosphopeptide analysis on a hybrid quadrupole mass filter/linear ion trap/orbitrap mass spectrometer.Analytical Chemistry,2015,87(2):1241-1249
[49]Kelstrup C D,Jersie-Christensen R R,Batth T S,et al.Rapid and deep proteomes by faster sequencing on a benchtop quadrupole ultra-high-field orbitrap mass spectrometer.Journal of Proteome Research,2014,13(12):6187-6195
[50]Law K P,Lim Y P.Recent advances in mass spectrometry:data independent analysis and hyper reaction monitoring.Expert Review of Proteomics,2013,10(6):551-566
[51]Graumann J,Scheltema R A,Zhang Y,et al.A framework for intelligent data acquisition and real-time database searching for shotgun proteomics.Molecular&Cellular Proteomics,2012,11(3):M111.013185
[52]Bailey D J,Mcdevitt M T,Westphall M S,et al.Intelligent data acquisition blends targeted and discovery methods.Journal of Proteome Research,2014,13(4):2152-2161
[53]Narumi R,Murakami T,Kuga T,et al.A strategy for large-scale phosphoproteomics and SRM-based validation of human breast cancer tissue samples.Journal of Proteome Research,2012,11(11):5311-5322
[54]Cui L,Reid G E.Examining factors that influence erroneous phosphorylation site localization via competing fragmentation and rearrangement reactions during ion trap CID-MS/MS and MS3.Proteomics,2013,13(6):964-973
[55]Syka J E,Coon J J,Schroeder M J,et al.Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry.Proc Natl Acad Sci,2004,101(26):9528-9533
[56]Sarbu M,Ghiulai R M,Zamfir A D.Recent developments and applications of electron transfer dissociation mass spectrometry in proteomics.Amino Acids,2014,46(7):1625-1634
[57]Frese C K,Altelaar A M,Van Den Toorn H,et al.Toward full peptide sequence coverage by dual fragmentation combining electron-transfer and higher-energy collision dissociation tandem mass spectrometry.Analytical Chemistry,2012,84(22):9668-9673
[58]Frese C K,Zhou H,Taus T,et al.Unambiguous phosphosite localization using electron-transfer/higher-energy collision dissociation(EThcD).Journal of Proteome Research,2013,12(3):1520-1525
[59]Gunawardena H P,Emory J F,Mcluckey S A.Phosphopeptide anion characterization via sequential charge inversion and electron-transfer dissociation.Analytical Chemistry,2006,78(11):3788-3793
[60]Robinson M R,Moore K L,Brodbelt J S.Direct identification of tyrosine sulfation by using ultraviolet photodissociation mass spectrometry.Journal of the American Society for Mass Spectrometry,2014,25(8):1461-1471
[61]Zanivan S,Meves A,Behrendt K,et al.In vivo SILAC-based proteomics reveals phosphoproteome changes during mouse skin carcinogenesis.Cell Reports,2013,3(2):552-566
[62]Oppermann F S,Klammer M,Bobe C,et al.Comparison of SILACand mTRAQ quantification for phosphoproteomics on a quadrupole orbitrap mass spectrometer.Journal of Proteome Research,2013,12(9):4089-4100
[63]Wilson-Grady J T,Haas W,Gygi S P.Quantitative comparison of the fasted and re-fed mouse liver phosphoproteomes using lower pH reductive dimethylation.Methods,2013,61(3):277-286
[64]Mcalister G C,Huttlin E L,Haas W,et al.Increasing the multiplexing capacity of TMTs using reporter ion isotopologues with isobaric masses.Analytical Chemistry,2012,84(17):7469-7478
[65]Mertins P,Udeshi N D,Clauser K R,et al.iTRAQ labeling is superior to mTRAQ for quantitative global proteomics and phosphoproteomics.Molecular&Cellular Proteomics,2012,11(6):M111.014423
[66]Xue L,Wang P,Cao P,et al.Identification of ERK1 direct substrates using stable isotope labeled kinase assay-linked phosphoproteomics.Molecular&Cellular Proteomics,2014,mcp.O114.038588
[67]Neilson K A,Ali N A,Muralidharan S,et al.Less label,more free:approaches in label‐free quantitative mass spectrometry.Proteomics,2011,11(4):535-553
[68]Schilling B,Rardin M J,Maclean B X,et al.Platform-independent and label-free quantitation of proteomic data using MS1 extracted ion chromatograms in skyline:application to protein acetylation and phosphorylation.Molecular&Cellular Proteomics,2012,11(5):202-214
[69]Tyanova S,Temu T,Cox J.The MaxQuant computational platform for mass spectrometry-based shotgun proteomics.Nature Protocols,2016,11(12):2301
[70]Eng J K,Searle B C,Clauser K R,et al.A face in the crowd:recognizing peptides through database search.Molecular&Cellular Proteomics,2011,10(11):R111.009522
[71]Chalkley R J,Clauser K R.Modification site localization scoring:strategies and performance.Molecular&Cellular Proteomics,2012,11(5):3-14
[72]Elias J E,Gygi S P.Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry.Nature Methods,2007,4(3):207-214
[73]Fermin D,Walmsley S J,Gingras A-C,et al.LuciPHOr:algorithm for phosphorylation site localization with false localization rate estimation using target-decoy approach.Molecular&Cellular Proteomics,2013,mcp.M113.028928
[74]Savitski M M,Lemeer S,Boesche M,et al.Confident phosphorylation site localization using the Mascot Delta Score.Molecular&Cellular Proteomics,2011,10(2):M110.003830
[75]Baker P R,Trinidad J C,Chalkley R J.Modification site localization scoring integrated into a search engine.Molecular&Cellular Proteomics,2011,mcp.M111.008078
[76]Beausoleil S A,Villén J,Gerber S A,et al.A probability-based approach for high-throughput protein phosphorylation analysis and site localization.Nature Biotechnology,2006,24(10):1285-1292
[77]Tanner S,Shu H,Frank A,et al.InsPecT:identification of posttranslationally modified peptides from tandem mass spectra.Analytical Chemistry,2005,77(14):4626-4639
[78]Bailey C M,Sweet S M,Cunningham D L,et al.SLo Mo:automated site localization of modifications from ETD/ECD mass spectra.Journal of Proteome Research,2009,8(4):1965-1971
[79]Phanstiel D H,Brumbaugh J,Wenger C D,et al.Proteomic and phosphoproteomic comparison of human ES and iPS cells.Nature Methods,2011,8(10):821-827
[80]Taus T,Kocher T,Pichler P,et al.Universal and confident phosphorylation site localization using phosphoRS.Journal of Proteome Research,2011,10(12):5354-5362
[81]Shi Q,Chen Y G.Interplay between TGF-beta signaling and receptor tyrosine kinases in tumor development.Science China Life Science,2017,60(10):1133-1141
[82]Li X,Wang W,Chen J.Recent progress in mass spectrometry proteomics for biomedical research.Science China Life Science,2017,60(10):1093-1113
[83]Strahl B,Allis C.The language of covalent histone.Nature,2000,403(6765):41-45
[84]Potel C M,Lin M H,Heck A J R,et al.Widespread bacterial protein histidine phosphorylation revealed by mass spectrometry-based proteomics.Nature Methods,2018,15(3):187-190
[85]Zhu Y,Guo T.Towards a one-stop solution for large-scale proteomics data analysis.Science China Life Science,2018,61(3):351-354
[86]Feng J,Ding C,Qiu N,et al.Firmiana:towards a one-stop proteomic cloud platform for data processing and analysis.Nature Biotechnology,2017,35(5):409-412
[87]Robles M S,Humphrey S J,Mann M.Phosphorylation is a central mechanism for circadian control of metabolism and physiology.Cell Metabolism,2017,25(1):118-127
[88]Hunter T.The age of crosstalk:phosphorylation,ubiquitination,and beyond.Molecular Cell,2007,28(5):730-738
[89]Zhou J M,Yang W C.Receptor-like kinases take center stage in plant biology.Science China Life Science,2016,59(9):863-866