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Review

Recent progress in quantitative phosphoproteomics

, , , , ORCID Icon & ORCID Icon
Pages 469-482 | Received 11 Aug 2023, Accepted 12 Dec 2023, Published online: 27 Dec 2023

References

  • Nilsson CL. Advances in quantitative phosphoproteomics. Anal Chem. 2012;84:735–746. American Chemical Society. doi: 10.1021/ac202877y
  • Conrads TP, Issaq HJ, Veenstra TD. New tools for quantitative phosphoproteome analysis. Biochem Biophys Res Commun. 2002;290:885–890. Academic Press: doi: 10.1006/bbrc.2001.6275
  • Navarrete-Perea J, Yu Q, Gygi SP, et al. Streamlined tandem mass tag (SL-TMT) protocol: an efficient strategy for quantitative (phospho)proteome profiling using tandem mass tag-synchronous precursor selection-MS3. J Proteome Res. 2018 Jun 1;17(6):2226–2236. doi: 10.1021/acs.jproteome.8b00217
  • Amoresano A, Marino G, Cirulli C, et al. Mapping phosphorylation sites: a new strategy based on the use of isotopically-labelled dithiothreitol and mass spectrometry. Eur J Mass Spectrom. 2004;10(3):401–412. doi: 10.1255/ejms.599
  • Cao P, Stults JT. Phosphopeptide analysis by on-line immobilized metal-ion affinity chromatography–capillary electrophoresis–electrospray ionization mass spectrometry. J Chromatogr A. 1999;853:225–235. Elsevier. doi: 10.1016/S0021-9673(99)00481-1
  • Humphrey SJ, Azimifar SB, Mann M. High-throughput phosphoproteomics reveals in vivo insulin signaling dynamics. Nat Biotechnol. 2015 Sep 10;33(9):990–995. doi: 10.1038/nbt.3327
  • Blazek M, Santisteban TS, Zengerle R, et al. Analysis of fast protein phosphorylation kinetics in single cells on a microfluidic chip. Lab Chip. 2015 Feb 7;15(3):726–734. doi: 10.1039/C4LC00797B
  • Nishi H, Shaytan A, Panchenko AR, Physicochemical mechanisms of protein regulation by phosphorylation. Front Genet. 2014;5. Frontiers Research Foundation. doi: 10.3389/fgene.2014.00270
  • Humphrey SJ, James DE, Mann M. Protein phosphorylation: a Major switch mechanism for metabolic regulation. Trends Endocrinol Metab. 2015;26:676–687. Elsevier Inc. doi: 10.1016/j.tem.2015.09.013
  • Martinez-Val A, Bekker-Jensen DB, Steigerwald S, et al. Spatial-proteomics reveals phospho-signaling dynamics at subcellular resolution. Nat Commun. 2021 Dec 1;12(1). doi: 10.1038/s41467-021-27398-y
  • Olsen JV, Blagoev B, Gnad F, et al. Global, in Vivo, and site-specific phosphorylation dynamics in signaling networks. Cell. 2006 Nov 3;127(3):635–648. doi: 10.1016/j.cell.2006.09.026
  • Xiao D, Caldow M, Kim HJ, et al. Time-resolved phosphoproteome and proteome analysis reveals kinase signaling on master transcription factors during myogenesis. iScience. 2022 Jun 17;25(6):104489. doi: 10.1016/j.isci.2022.104489
  • Zhao P, Malik S. The phosphorylation to acetylation/methylation cascade in transcriptional regulation: how kinases regulate transcriptional activities of DNA/histone-modifying enzymes. Cell Biosci. 2022;12(1):1–23. BioMed Central Ltd. doi: 10.1186/s13578-022-00821-7
  • Singh V, Ram M, Kumar R, et al. Phosphorylation: implications in cancer. Protein J. 2017;36(1):1–6. Springer Science and Business Media, LLC. doi: 10.1007/s10930-017-9696-z
  • Wu D, Hu D, Chen H, et al. Glucose-regulated phosphorylation of TET2 by AMPK reveals a pathway linking diabetes to cancer. Nature. 2018 Jul 26;559(7715):637–641. doi: 10.1038/s41586-018-0350-5
  • Oliveira J, Costa M, De Almeida MSC, et al. Protein Phosphorylation is a Key Mechanism in Alzheimer’s Disease. JJ Alzheimer’s Dis. 2017;58:953–978. IOS Press. doi: 10.3233/JAD-170176
  • Bonne Køhler J, Jers C, Senissar M, et al. Importance of protein Ser/Thr/Tyr phosphorylation for bacterial pathogenesis. FEBS Lett. 2020;594:2339–2369. Wiley Blackwell. doi: 10.1002/1873-3468.13797
  • Korecka M, Shaw LM. Mass spectrometry-based methods for robust measurement of Alzheimer’s disease biomarkers in biological fluids. J Neurochem. 2021;159:211–233. John Wiley and Sons Inc. doi: 10.1111/jnc.15465
  • Bhullar KS, Lagarón NO, McGowan EM, et al. Kinase-targeted cancer therapies: progress, challenges and future directions. Mol Cancer. 2018;17(1). BioMed Central Ltd. doi: 10.1186/s12943-018-0804-2
  • Roskoski R, Properties of FDA-approved small molecule protein kinase inhibitors: a 2023 update. Pharmacol Res. 2023;187: Academic Press. doi: 10.1016/j.phrs.2022.106552
  • Nirujogi RS, Tonelli F, Taylor M, et al. Development of a multiplexed targeted mass spectrometry assay for LRRK2-phosphorylated rabs and Ser910/Ser935 biomarker sites. Biochem J. 2021 Jan 1;478(2):299–326. doi: 10.1042/BCJ20200930
  • Hadisurya M, Li L, Kuwaranancharoen K, et al. Quantitative proteomics and phosphoproteomics of urinary extracellular vesicles define putative diagnostic biosignatures for Parkinson’s disease. Commun Med. 2023 May 10 [cited 2023 Jun 7];3(1):64. doi: 10.1038/s43856-023-00294-w
  • Sampadi B, Pines A, Munk S, et al. Quantitative phosphoproteomics to unravel the cellular response to chemical stressors with different modes of action. Arch Toxicol. 2020 May 1;94(5):1655–1671. doi: 10.1007/s00204-020-02712-7
  • Zhang L, Winkler S, Schlottmann FP, et al. Multiple layers of phospho-regulation coordinate metabolism and the cell cycle in budding yeast. Front Cell Dev Biol. 2019 Dec 17 [cited 2023 Jun 3];7:338. Available from: https://www.frontiersin.org/article/10.3389/fcell.2019.00338/full
  • Fricke AL, Mühlhäuser WWD, Reimann L, et al. Phosphoproteomics profiling defines a target landscape of the Basophilic protein kinases AKT, S6K, and RSK in Skeletal Myotubes. J Proteome Res. 2023 Mar 3;22(3):768–789. doi: 10.1021/acs.jproteome.2c00505
  • Paulo JA, McAllister FE, Everley RA, et al. Effects of MEK inhibitors GSK1120212 and PD0325901 in vivo using 10-plex quantitative proteomics and phosphoproteomics. Proteomics. 2015 Jan 1 [cited 2023 Jun 6];15(2–3):462–473. doi: 10.1002/pmic.201400154
  • Wang Z, Ma J, Miyoshi C, et al. Quantitative phosphoproteomic analysis of the molecular substrates of sleep need. Nature. 2018 Jun 21;558(7710):435–439. doi: 10.1038/s41586-018-0218-8
  • Hogrebe A, Von Stechow L, Bekker-Jensen DB, et al. Benchmarking common quantification strategies for large-scale phosphoproteomics. Nat Commun. 2018 Dec 1;9(1):1–13. doi: 10.1038/s41467-018-03309-6
  • O’Connell JD, Paulo JA, O’Brien JJ, et al. Proteome-wide Evaluation of two common protein quantification methods. J Proteome Res. 2018 May 4;17(5):1934–1942. doi: 10.1021/acs.jproteome.8b00016
  • Urban J. A review on recent trends in the phosphoproteomics workflow. From sample preparation to data analysis. Anal Chim Acta. 2022;1199:338857. Elsevier B.V. doi: 10.1016/j.aca.2021.338857
  • Iliuk A. Identification of phosphorylated proteins on a global scale. Curr Protoc Chem Biol. 2018 Sep 1;10(3):e48. doi: 10.1002/cpch.48
  • Rogers LD, Fang Y, Foster LJ. An integrated global strategy for cell lysis, fractionation, enrichment and mass spectrometric analysis of phosphorylated peptides. Mol Biosyst. 2010 May 10;6(5):822–829. doi: 10.1039/b915986j
  • Qiu W, Evans CA, Landels A, et al. Phosphopeptide enrichment for phosphoproteomic analysis - a tutorial and review of novel materials. Anal Chim Acta. 2020;1129:158–180. Elsevier B.V. doi: 10.1016/j.aca.2020.04.053
  • Xiao D, Chen C, Yang P. Computational systems approach towards phosphoproteomics and their downstream regulation. Proteomics. 2023 Feb 1 [cited 2023 Nov 1];23(3–4):2200068. Available from: https://pubmed.ncbi.nlm.nih.gov/35580145/
  • Varshney N, Mishra AK. Deep learning in phosphoproteomics: methods and application in cancer Drug discovery. Proteomes. 2023;11(2):16. MDPI. doi: 10.3390/proteomes11020016
  • Paulo JA, Schweppe DK. Advances in quantitative high‐throughput phosphoproteomics with sample multiplexing. Proteomics. 2021 May 30 [cited 2023 Jun 6];21(9):2000140. doi: 10.1002/pmic.202000140
  • Liu X, Fields R, Schweppe DK, et al. Strategies for mass spectrometry-based phosphoproteomics using isobaric tagging. Expert Rev Proteomics. 2021;18(9):795–807. doi: 10.1080/14789450.2021.1994390
  • Ino Y, Kinoshita E, Kinoshita‐Kikuta E, et al. Evaluation of four phosphopeptide enrichment strategies for mass spectrometry‐based proteomic analysis. Proteomics. 2022 Apr 28 [cited 2023 Jun 6];22(7):2100216. doi: 10.1002/pmic.202100216
  • Li J, Wang J, Yan Y, et al. Comprehensive Evaluation of different TiO2-based phosphopeptide enrichment and fractionation methods for phosphoproteomics. Cells. 2022 Jul 1;11(13):2047. doi: 10.3390/cells11132047
  • Hsu CC, Xue L, Arrington JV, et al. Estimating the efficiency of phosphopeptide identification by tandem mass spectrometry. J Am Soc Mass Spectrom. 2017 Jun 1;28(6):1127–1135. doi: 10.1007/s13361-017-1603-5
  • Winter D, Seidler J, Ziv Y, et al. Citrate boosts the performance of phosphopeptide analysis by UPLC-ESI-MS/MS. J Proteome Res. 2009 Jan;8(1):418–424.
  • Bugyi F, Tóth G, Kovács KB, et al. Comparison of solid-phase extraction methods for efficient purification of phosphopeptides with low sample amounts. J Chromatogr A. 2022 Dec 6;1685:463597. doi: 10.1016/j.chroma.2022.463597
  • Vlastaridis P, Kyriakidou P, Chaliotis A, et al. Estimating the total number of phosphoproteins and phosphorylation sites in eukaryotic proteomes. Gigascience. 2017 Feb 1;6(2). doi: 10.1093/gigascience/giw015
  • Macek B, Forchhammer K, Hardouin J, et al. Protein post-translational modifications in bacteria. Nat Rev Microbiol. 2019;17(11):651–664. Nature Publishing Group. doi: 10.1038/s41579-019-0243-0
  • Birk MS, Charpentier E, Frese CK. Automated phosphopeptide enrichment for gram-positive bacteria. J Proteome Res. 2021;20(10):4886–4892. doi: 10.1021/acs.jproteome.1c00364
  • Marzec KA, Rogers S, McCloy R, et al. SILAC kinase screen identifies potential MASTL substrates. Sci Rep. 2022 Dec 1;12(1):1–13. doi: 10.1038/s41598-022-14933-0
  • Sharma K, D’Souza RCJ, Tyanova S, et al. Ultradeep human phosphoproteome reveals a Distinct regulatory Nature of Tyr and Ser/Thr-based signaling. Cell Rep. 2014 Sep 11;8(5):1583–1594. doi: 10.1016/j.celrep.2014.07.036
  • Liu X, Rossio V, Thakurta SG, et al. Fe3±NTA magnetic beads as an alternative to spin column-based phosphopeptide enrichment. J Proteomics. 2022 May 30;260:104561. doi: 10.1016/j.jprot.2022.104561
  • Olsen JV, Vermeulen M, Santamaria A, et al. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal. 2010 Jan 12 [cited 2023 Aug 3];3(104). Available from: https://pubmed.ncbi.nlm.nih.gov/20068231/
  • Koenig C, Martinez‐Val A, Franciosa G, et al. Optimal analytical strategies for sensitive and quantitative phosphoproteomics using TMT‐based multiplexing. Proteomics. 2022 Oct 1 [cited 2023 Jun 6];22(19–20):2100245. doi: 10.1002/pmic.202100245.
  • Tsai CF, Zhang P, Scholten D, et al. Surfactant-assisted one-pot sample preparation for label-free single-cell proteomics. Commun Biol. 2021 Dec 1;4(1):1–12. doi: 10.1038/s42003-021-01797-9
  • Tsai CF, Wang YT, Hsu CC, et al. A streamlined tandem tip-based workflow for sensitive nanoscale phosphoproteomics. Commun Biol. 2023 Dec 1;6(1). doi: 10.1038/s42003-022-04400-x
  • Yi L, Tsai CF, Dirice E, et al. Boosting to amplify signal with isobaric labeling (BASIL) strategy for Comprehensive quantitative phosphoproteomic characterization of small Populations of cells. Anal Chem. 2019 May 7;91(9):5794–801. doi: 10.1021/acs.analchem.9b00024
  • Tsai CF, Zhao R, Williams SM, et al. An improved boosting to amplify signal with isobaric labeling (iBASIL) strategy for precise quantitative single-cell proteomics. Mol Cell Proteomics. 2020 May 1;19(5):828–838. doi: 10.1074/mcp.RA119.001857
  • Budnik B, Levy E, Harmange G, et al. SCoPE-MS: mass spectrometry of single mammalian cells quantifies proteome heterogeneity during cell differentiation. Genome Biol. 2018 Oct 22 [cited 2023 Jun 7];19(1):161. 10.1186/s13059-018-1547-5
  • Stopfer LE, Conage-Pough JE, White FM, Quantitative Consequences of protein Carriers in Immunopeptidomics and tyrosine phosphorylation MS2 analyses. Mol Cell Proteomics. 2021 Jan 1 [cited 2023 Aug 3];20:100104. Available from: https://pubmed.ncbi.nlm.nih.gov/34052394/
  • Chua XY, Mensah T, Aballo T, et al. Tandem mass tag approach utilizing pervanadate BOOST channels delivers deeper quantitative characterization of the tyrosine phosphoproteome. Mol Cell Proteomics. 2020 [cited 2023 Aug 3];19:730–743. Available from: https://pubmed.ncbi.nlm.nih.gov/32071147/
  • Piehowski PD, Petyuk VA, Sontag RL, et al. Residual tissue repositories as a resource for population-based cancer proteomic studies. Clin Proteomics. 2018 Aug 3 [cited 2023 Jun 8];15(1): 26. doi: 10.1186/s12014-018-9202-4
  • Friedrich C, Schallenberg S, Kirchner M, et al. Comprehensive micro-scaled proteome and phosphoproteome characterization of archived retrospective cancer repositories. Nat Commun. 2021 Dec 1;12(1):1–15. doi: 10.1038/s41467-021-23855-w
  • Pujari GP, Mangalaparthi KK, Madden BJ, et al. A high-throughput workflow for FFPE tissue proteomics. J Am Soc Mass Spectrom. 2023 Jul 5;34(7):1225–1229. doi: 10.1021/jasms.3c00099
  • Wang F, Veth T, Kuipers M, et al. Optimized Suspension trapping method for phosphoproteomics sample preparation. Anal Chem. 2023 Jun 27;95(25):9471–9479. doi: 10.1021/acs.analchem.3c00324
  • Zougman A, Selby PJ, Banks RE. Suspension trapping (STrap) sample preparation method for bottom‐up proteomics analysis. Proteomics. 2014 May 26 [cited 2023 Nov 1];14(9):1006–1000. doi: 10.1002/pmic.201300553
  • Swaney DL, Wenger CD, Coon JJ. Value of using multiple proteases for large-scale mass spectrometry-based proteomics. J Proteome Res. 2010 Mar 5;9(3):1323–1329. doi: 10.1021/pr900863u
  • Dickhut C, Feldmann I, Lambert J, et al. Impact of digestion conditions on phosphoproteomics. J Proteome Res. 2014 Jun 6;13(6):2761–2770. doi: 10.1021/pr401181y
  • Bubis JA, Gorshkov V, Gorshkov MV, et al. PhosphoShield: improving trypsin digestion of phosphoproteins by shielding the negatively charged phosphate moiety. J Am Soc Mass Spectrom. 2020 Oct 7;31(10):2053–2060. doi: 10.1021/jasms.0c00171
  • Abe Y, Nagano M, Tada A, et al. Deep phosphotyrosine proteomics by optimization of phosphotyrosine enrichment and MS/MS parameters. J Proteome Res. 2017 Feb 3;16(2):1077–1086. doi: 10.1021/acs.jproteome.6b00576
  • Kinoshita E, Kinoshita-Kikuta E, Koike T. History of phos-tag technology for phosphoproteomics. J Proteomics. 2022;252:104432. Elsevier B.V. doi: 10.1016/j.jprot.2021.104432
  • Carregari VC. Phosphopeptide enrichment techniques: a pivotal step for phosphoproteomic studies. Adv Exp Med Biol. 2022;1382:17–27.
  • Zhu B, Zhou Q, Zhen D, et al. Preparation of TiO2/Bi/Fe/Zr nanocomposite for the highly selective enrichment of phosphopeptides. Talanta. 2019 Mar 1;194:870–875. doi: 10.1016/j.talanta.2018.10.073
  • McNulty DE, Annan RS. Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Mol Cell Proteomics. 2008 May;7(5):971–980. doi: 10.1074/mcp.M700543-MCP200
  • Villén J, Gygi SP. The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat Protoc. 2008 Oct 2;3(10):1638. doi: 10.1038/nprot.2008.150
  • Batth TS, Francavilla C, Olsen JV. Off-line high-pH reversed-phase fractionation for in-depth phosphoproteomics. J Proteome Res. 2014 Dec 5;13(12):6176–6186. doi: 10.1021/pr500893m
  • Kwon Y, Lee S, Park N, et al. Phosphoproteome profiling using an isobaric carrier without the need for phosphoenrichment. Anal Chem. 2022 Mar 15;94(10):4192–4200. doi: 10.1021/acs.analchem.1c04188
  • Callesen AK, Madsen JS, Vach W, et al. Serum protein profiling by solid phase extraction and mass spectrometry: a future diagnostics tool? Proteomics. 2009 Mar 1 [cited 2023 Jun 8];9(6):1428–1441. doi: 10.1002/pmic.200800382.
  • West C, Elfakir C, Lafosse M. Porous graphitic carbon: A versatile stationary phase for liquid chromatography. J Chromatogr A. 2010;1217(19):3201–3216. Elsevier. doi: 10.1016/j.chroma.2009.09.052
  • Ogata K, Ishihama Y. CoolTip: low-temperature solid-phase extraction microcolumn for capturing hydrophilic peptides and phosphopeptides. Mol Cell Proteomics. 2021 Nov 2;20:100170. doi: 10.1016/j.mcpro.2021.100170
  • Ong SE, Blagoev B, Kratchmarova I, et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics. 2002 May 1;1(5):376–386. doi: 10.1074/mcp.M200025-MCP200
  • Goshe MB, Conrads TP, Panisko EA, et al. Phosphoprotein isotope-coded affinity tag approach for isolating and quantitating phosphopeptides in proteome-wide analyses. Anal Chem. 2001 Jun 1;73(11):2578–2586. doi: 10.1021/ac010081x
  • Gygi SP, Rist B, Gerber SA, et al. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat Biotechnol. 1999 Oct;17(10):994–999.
  • Dan Y, Radic N, Gay M, et al. Characterization of p38α signaling networks in cancer CellsUsing quantitative proteomics and phosphoproteomics. Mol Cell Proteomics. 2023 Apr 1;22(4):100527. doi: 10.1016/j.mcpro.2023.100527
  • Gratani FL, Englert T, Nashier P, et al. E. coli toxin YjjJ (HipH) is a Ser/Thr protein kinase that Impacts cell Division, Carbon Metabolism, and ribosome assembly. mSystems. 2023 Feb 23;8(1). doi: 10.1128/msystems.01043-22
  • Geiger T, Cox J, Ostasiewicz P, et al. Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat Methods. 2010 May 4;7(5):383–385. doi: 10.1038/nmeth.1446
  • Güran A, Ji Y, Fang P, et al. Quantitative analysis of the cardiac phosphoproteome in response to acute β-adrenergic receptor stimulation in vivo. Int J Mol Sci. 2021 Nov 22 [cited 2023 Jun 12];22(22): 12584. doi: 10.3390/ijms222212584
  • Doherty MK, Hammond DE, Clague MJ, et al. Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. J Proteome Res. 2009 Jan;8(1):104–112.
  • Wu C, Ba Q, Lu D, et al. Global and site-specific effect of phosphorylation on protein turnover. Dev Cell. 2021 Jan 11;56(1):111–124.e6. doi: 10.1016/j.devcel.2020.10.025
  • Trentini DB, Suskiewicz MJ, Heuck A, et al. Arginine phosphorylation marks proteins for degradation by a Clp protease. Nature. 2016 Oct 6;539(7627):48–53. doi: 10.1038/nature20122
  • Swaney DL, Rodríguez‐Mias RA, Villén J. Phosphorylation of ubiquitin at Ser65 affects its polymerization, targets, and proteome‐wide turnover. EMBO Rep. 2015 Sep 3 [cited 2023 Jun 10];16(9):1131–1144. Available from https://www.embopress.org/doi/10.15252/embr.201540298
  • Hammarén HM, Geissen EM, Potel CM, et al. Protein-peptide turnover profiling reveals the order of PTM addition and removal during protein maturation. Nat Commun. 2022 Dec 1;13(1):1–15. doi: 10.1038/s41467-022-35054-2
  • Boersema PJ, Raijmakers R, Lemeer S, et al. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc. 2009 Mar 19;4(4):484–494. doi: 10.1038/nprot.2009.21
  • Hsu JL, Huang SY, Chow NH, et al. Stable-isotope dimethyl labeling for quantitative proteomics. Anal Chem. 2003 Dec 15;75(24):6843–6852. doi: 10.1021/ac0348625
  • Kalpongnukul N, Bootsri R, Wongkongkathep P, et al. Phosphoproteomic analysis defines BABAM1 as mTORC2 downstream effector promoting DNA damage response in Glioblastoma cells. J Proteome Res. 2022 Dec 2;21(12):2893–2904. doi: 10.1021/acs.jproteome.2c00240
  • Chang YW, Wang CC, Yin CF, et al. Quantitative phosphoproteomics reveals ectopic ATP synthase on mesenchymal stem cells to promote tumor progression via ERK/c-fos pathway activation. Mol Cell Proteomics. 2022 Jun 1;21(6):100237. doi: 10.1016/j.mcpro.2022.100237
  • Senturk A, Sahin AT, Armutlu A, et al. Quantitative phosphoproteomics analysis uncovers PAK2- and CDK1-mediated malignant signaling pathways in clear cell renal cell carcinoma. Mol Cell Proteomics. 2022 Nov 1;21(11):100417. doi: 10.1016/j.mcpro.2022.100417
  • Frost DC, Greer T, Li L. High-resolution enabled 12-plex DiLeu isobaric tags for quantitative proteomics. Anal Chem. 2015 Feb 3;87(3):1646–1654. doi: 10.1021/ac503276z
  • Zhong X, Lietz CB, Shi X, et al. Highly multiplexed quantitative proteomic and phosphoproteomic analyses in vascular smooth muscle cell dedifferentiation. Anal Chim Acta. 2020 Aug 29;1127:163–173. doi: 10.1016/j.aca.2020.06.054
  • Li J, Cai Z, Bomgarden RD, et al. Tmtpro-18plex: the expanded and complete set of TMTpro reagents for sample multiplexing. J Proteome Res. 2021 May 7;20(5):2964–2972. doi: 10.1021/acs.jproteome.1c00168
  • Schweppe DK, Rusin SF, Gygi SP, et al. Optimized workflow for multiplexed phosphorylation analysis of TMT-Labeled peptides using high-field asymmetric waveform ion mobility spectrometry. J Proteome Res. 2020 Jan 3;19(1):554–560. doi: 10.1021/acs.jproteome.9b00759
  • Ogata K, Tsai CF, Ishihama Y. Nanoscale Solid-Phase Isobaric Labeling for Multiplexed Quantitative Phosphoproteomics. J Proteome Res. 2021 Aug 6;20(8):4193–4202. doi: 10.1021/acs.jproteome.1c00444
  • Cox J, Hein MY, Luber CA, et al. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics. 2014 Sep 1;13(9):2513–2526. doi: 10.1074/mcp.M113.031591
  • Potel CM, Lemeer S, Heck AJR. Phosphopeptide fragmentation and site localization by mass spectrometry: an update. Anal Chem. 2019;91(1):126–141. American Chemical Society. doi: 10.1021/acs.analchem.8b04746
  • Villén J, Beausoleil SA, Gygi SP. Evaluation of the utility of neutral-loss-dependent MS3 strategies in large-scale phosphorylation analysis. Proteomics. 2008 Nov 1 [cited 2023 Jun 10];8(21):4444–4452. 10.1002/pmic.200800283
  • Escobar EE, Venkat Ramani MK, Zhang Y, et al. Evaluating spatiotemporal dynamics of phosphorylation of RNA polymerase II carboxy-terminal domain by ultraviolet photodissociation mass spectrometry. J Am Chem Soc. 2021 Jun 9 [cited 2023 Aug 3];143(22):8488–8498. doi: 10.1021/jacs.1c03321
  • Brunner AM, Lössl P, Liu F, et al. Benchmarking multiple fragmentation methods on an orbitrap fusion for top-down phospho-proteoform characterization. Anal Chem. 2015 Apr 21;87(8):4152–4158. doi: 10.1021/acs.analchem.5b00162
  • Schweppe DK, Prasad S, Belford MW, et al. Characterization and optimization of multiplexed quantitative analyses using high-field asymmetric-waveform ion mobility mass spectrometry. Anal Chem. 2019 Mar 19;91(6):4010–4016. doi: 10.1021/acs.analchem.8b05399
  • Muehlbauer LK, Hebert AS, Westphall MS, et al. Global phosphoproteome analysis using high-field asymmetric waveform ion mobility spectrometry on a hybrid Orbitrap mass spectrometer. Anal Chem. 2020 Dec 15;92(24):15959–15967. doi: 10.1021/acs.analchem.0c03415
  • Toby TK, Fornelli L, Kelleher NL. Progress in top-down proteomics and the analysis of proteoforms. Annual Rev Anal Chem. 2016;9(1):499–519. Annual Reviews Inc. doi: 10.1146/annurev-anchem-071015-041550
  • Chapman EA, Aballo TJ, Melby JA, et al. Defining the sarcomeric proteoform landscape in ischemic cardiomyopathy by top-down proteomics. J Proteome Res. 2023 Mar 3;22(3):931–941. doi: 10.1021/acs.jproteome.2c00729
  • Melby JA, Brown KA, Gregorich ZR, et al. High sensitivity top-down proteomics captures single muscle cell heterogeneity in large proteoforms. Proc Natl Acad Sci U S A. 2023 May 9;120(19). doi: 10.1073/pnas.2222081120
  • Vidova V, Spacil Z. A review on mass spectrometry-based quantitative proteomics: targeted and data independent acquisition. Anal Chim Acta. 2017;964:7–23. Elsevier B.V. doi: 10.1016/j.aca.2017.01.059
  • Wu X, Liu YK, Iliuk AB, et al. Mass spectrometry-based phosphoproteomics in clinical applications. TrAC - Trends Analyt Chemy. 2023;163:117066. Elsevier B.V. doi: 10.1016/j.trac.2023.117066
  • Stopfer LE, Flower CT, Gajadhar AS, et al. High-density, targeted monitoring of tyrosine phosphorylation reveals activated signaling networks in human tumors. Cancer Res. 2021 May 1;81(9):2495–2509. doi: 10.1158/0008-5472.CAN-20-3804
  • Martínez-Val A, Fort K, Koenig C, et al. Hybrid-DIA: intelligent data acquisition integrates targeted and discovery proteomics to analyze phospho-signaling in single spheroids. Nat Commun. 2023 Dec 1;14(1):1–18. doi: 10.1038/s41467-023-39347-y
  • Humphrey SJ, Karayel O, James DE, et al. High-throughput and high-sensitivity phosphoproteomics with the EasyPhos platform. Nat Protoc. 2018 Sep 1;13(9):1897–1916. doi: 10.1038/s41596-018-0014-9
  • Leutert M, Rodríguez‐Mias RA, Fukuda NK, et al. R2‐P2 rapid‐robotic phosphoproteomics enables multidimensional cell signaling studies. Mol Syst Biol. 2019 Dec;15(12). doi: 10.15252/msb.20199021
  • Leutert M, Barente AS, Fukuda NK, et al. The regulatory landscape of the yeast phosphoproteome. Nat Struct Mol Biol. 2023 Oct 16;1–3. Available from: https://www.nature.com/articles/s41594-023-01115-3
  • Müller T, Kalxdorf M, Longuespée R, et al. Automated sample preparation with SP 3 for low‐input clinical proteomics. Mol Syst Biol. 2020 Jan 16 [cited 2023 Jun 8];16(1): e9111. [internet]. doi: 10.15252/msb.20199111
  • Post H, Penning R, Fitzpatrick MA, et al. Robust, sensitive, and automated phosphopeptide enrichment optimized for low sample amounts applied to primary hippocampal neurons. J Proteome Res. 2017 Feb 3;16(2):728–737. doi: 10.1021/acs.jproteome.6b00753
  • Tavassoly I, Goldfarb J, Iyengar R. Systems biology primer: the basic methods and approaches. Essays Biochem. 2018;62:487–500. Portland Press Ltd. doi: 10.1042/EBC20180003
  • Liu Y, Chance MR. Integrating phosphoproteomics in systems biology. Comput Struct Biotechnol J. 2014;10(17):90–97. Elsevier B.V. doi: 10.1016/j.csbj.2014.07.003
  • Kreitmaier P, Katsoula G, Zeggini E. Insights from multi-omics integration in complex disease primary tissues. Trends Genet. 2023;39:46–58. Elsevier Ltd. doi: 10.1016/j.tig.2022.08.005
  • Aggarwal S, Tolani P, Gupta S, et al. Posttranslational modifications in systems biology. Adv Protein Chem Struct Biol. 2021;127:93–126. Academic Press Inc.
  • Vandereyken K, Sifrim A, Thienpont B, et al. Methods and applications for single-cell and spatial multi-omics. Nat Rev Genet. 2023;24:494–515. doi: 10.1038/s41576-023-00580-2
  • Gu Y, Zhou Y, Ju S, et al. Multi-omics profiling visualizes dynamics of cardiac development and functions. Cell Rep. 2022 Dec 27;41(13):111891. doi: 10.1016/j.celrep.2022.111891
  • Pang H, Jiang Y, Li J, et al. Aberrant NAD+ metabolism underlies Zika virus–induced microcephaly. Nat Metab. 2021 Aug 1;3(8):1109–1124. doi: 10.1038/s42255-021-00437-0
  • Zhao P, Feng Y, Wu J, et al. Efficient sample preparation System for multi-omics analysis via single cell mass spectrometry. Anal Chem. 2022 May 9;95(18):7212–7219
  • Li Y, Li H, Xie Y, et al. An integrated strategy for mass spectrometry-based Multiomics analysis of single cells. Anal Chem. 2021 Oct 26;93(42):14059–14067. doi: 10.1021/acs.analchem.0c05209
  • Leutert M, Entwisle SW, Villén J. Decoding post-translational modification crosstalk with proteomics. Mol Cell Proteomics. 2021;20:100129. American Society for Biochemistry and Molecular Biology Inc. doi: 10.1016/j.mcpro.2021.100129
  • Adoni KR, Cunningham DL, Heath JK, et al. FAIMS enhances the detection of PTM crosstalk sites. J Proteome Res. 2022 Apr 1;21(4):930–939. doi: 10.1021/acs.jproteome.1c00721
  • Fulzele A, Bennett EJ. Ubiquitin diGLY Proteomics as an Approach to Identify and Quantify the Ubiquitin-Modified Proteome. In: Mayor T, Kleiger G, editors. The Ubiquitin Proteasome System. Methods in Molecular Biology. Vol. 1844. New York, NY: Humana Press; 2018. doi: 10.1007/978-1-4939-8706-1_23
  • Schilling B, Meyer JG, Wei L, et al. High-Resolution Mass Spectrometry to Identify and Quantify Acetylation Protein Targets. In: Brosh R Jr, editor. Protein Acetylation. Methods in Molecular Biology. Vol. 1983. New York, NY: Humana; 2019. doi: 10.1007/978-1-4939-9434-2_1
  • Mertins P, Qiao JW, Patel J, et al. Integrated proteomic analysis of post-translational modifications by serial enrichment. Nat Methods. 2013 Jul 9;10(7):634–637. doi: 10.1038/nmeth.2518
  • Liu R, Gao W, Yang J, et al. A novel graphene oxide/chitosan foam incorporated with metal–organic framework stationary phase for simultaneous enrichment of glycopeptide and phosphopeptide with high efficiency. Anal Bioanal Chem. 2022 Mar 1;414(6):2251–2263. doi: 10.1007/s00216-021-03861-z
  • Fan Z, Li J, Liu T, et al. A new tandem enrichment strategy for the simultaneous profiling of: O-GlcNAcylation and phosphorylation in RNA-binding proteome. Analyst. 2021 Feb 21;146(4):1188–1197. doi: 10.1039/D0AN02305A
  • Abelin JG, Bergstrom EJ, Rivera KD, et al. Workflow enabling deepscale immunopeptidome, proteome, ubiquitylome, phosphoproteome, and acetylome analyses of sample-limited tissues. Nat Commun. 2023 Dec 1;14(1):1851. doi: 10.1038/s41467-023-37547-0.
  • Ashrafian S, Zarrineh M, Jensen P, et al. Quantitative phosphoproteomics and acetylomics of safranal anticancer effects in Triple-negative breast cancer cells. J Proteome Res. 2022 Nov 4;21(11):2566–2585. doi: 10.1021/acs.jproteome.2c00168
  • Pino LK, Just SC, MacCoss MJ, et al. Acquiring and analyzing data independent acquisition proteomics experiments without spectrum libraries. Mol & Cell Proteomics. 2020 Jul 1;19(7):1088–1103. doi: 10.1074/mcp.P119.001913
  • Röst HL, Rosenberger G, Navarro P, et al. OpenSWATH enables automated, targeted analysis of data-independent acquisition MS data. Nat Biotechnol. 2014;32(3):219–223. doi: 10.1038/nbt.2841. Nature Publishing Group
  • Krasny L, Huang PH. Data-independent acquisition mass spectrometry (DIA-MS) for proteomic applications in oncology. Mol Omics. 2021;17(1):29–42. Royal Society of Chemistry. doi: 10.1039/D0MO00072H
  • MacLean B, Tomazela DM, Shulman N, et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics. 2010 Feb 9;26(7):966–968. doi: 10.1093/bioinformatics/btq054
  • Desiere F, Deutsch EW, King NL, et al. The PeptideAtlas project. Nucleic Acids Res. 2006;34(Database issue):D655–D658. doi: 10.1093/nar/gkj040
  • Wang M, Wang J, Carver J, et al. Assembling the community-scale discoverable human proteome. Cell Syst. 2018 Oct 24;7(4):412–421.e5. doi: 10.1016/j.cels.2018.08.004
  • Searle BC, Swearingen KE, Barnes CA, et al. Generating high quality libraries for DIA MS with empirically corrected peptide predictions. Nat Commun. 2020 Dec 1;11(1). doi: 10.1038/s41467-020-15346-1
  • Sinitcyn P, Hamzeiy H, Salinas Soto F, et al. MaxDIA enables library-based and library-free data-independent acquisition proteomics. Nat Biotechnol. 2021 Dec 1;39(12):1563–1573. doi: 10.1038/s41587-021-00968-7
  • Gessulat S, Schmidt T, Zolg DP, et al. Prosit: proteome-wide prediction of peptide tandem mass spectra by deep learning. Nat Methods. 2019 Jun 1;16(6):509–518. doi: 10.1038/s41592-019-0426-7
  • Lou R, Liu W, Li R, et al. DeepPhospho accelerates DIA phosphoproteome profiling through in silico library generation. Nat Commun. 2021 Dec 1;12(1). doi: 10.1038/s41467-021-26979-1
  • Bekker-Jensen DB, Bernhardt OM, Hogrebe A, et al. Rapid and site-specific deep phosphoproteome profiling by data-independent acquisition without the need for spectral libraries. Nat Commun. 2020 Dec 1;11(1). doi: 10.1038/s41467-020-14609-1
  • Demichev V, Messner CB, Vernardis SI, et al. DIA-NN: neural networks and interference correction enable deep proteome coverage in high throughput. Nat Methods. 2020 Jan 1;17(1):41–44. doi: 10.1038/s41592-019-0638-x
  • Lou R, Cao Y, Li S, et al. Benchmarking commonly used software suites and analysis workflows for DIA proteomics and phosphoproteomics. Nat Commun. 2023 Dec 1;14(1). doi: 10.1038/s41467-022-35740-1
  • Skowronek P, Thielert M, Voytik E, et al. Rapid and in-depth coverage of the (phospho-) proteome with deep libraries and optimal Window Design for dia-PASEF. Mol Cell Proteomics. 2022 Sep 1;21(9):100279. doi: 10.1016/j.mcpro.2022.100279
  • Pasquier C, Robichon A. Evolutionary divergence of phosphorylation to regulate interactive protein networks in lower and higher species. Int J Mol Sci. 2022 Nov 1;23(22):14429. doi: 10.3390/ijms232214429
  • Ochoa D, Jarnuczak AF, Viéitez C, et al. The functional landscape of the human phosphoproteome. Nat Biotechnol. 2020 Mar 1;38(3):365–373. doi: 10.1038/s41587-019-0344-3
  • Huang JX, Lee G, Cavanaugh KE, et al. High throughput discovery of functional protein modifications by hotspot thermal profiling. Nat Methods. 2019 Sep 1;16(9):894–901. doi: 10.1038/s41592-019-0499-3
  • Potel CM, Kurzawa N, Becher I, et al. Impact of phosphorylation on thermal stability of proteins. Nat Methods. 2021;18:757–759. Nature Research. doi: 10.1038/s41592-021-01177-5
  • Krug K, Mertins P, Zhang B, et al. A curated resource for Phosphosite-specific signature analysis. Mol Cell Proteomics. 2019 Mar 1;18(3):576–593. doi: 10.1074/mcp.TIR118.000943
  • Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545–15550. doi: 10.1073/pnas.0506580102
  • Seymour RW, van der Post S, Mooradian AD, et al. ProteoSushi: a software tool to biologically annotate and quantify modification-specific, peptide-centric proteomics data Sets. J Proteome Res. 2021 Jul 2;20(7):3621–3628. doi: 10.1021/acs.jproteome.1c00203

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