802
Views
21
CrossRef citations to date
0
Altmetric
Review

Progress and pitfalls of using isobaric mass tags for proteome profiling

ORCID Icon & ORCID Icon
Pages 149-161 | Received 17 Dec 2019, Accepted 14 Feb 2020, Published online: 20 Feb 2020

References

  • Ong SE, Mann M. Mass spectrometry–based proteomics turns quantitative. Nat Chem Biol. 2005;1(5):252–262.
  • Thompson A, Schäfer J, Kuhn K, et al. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem. 2003;75(8):1895–1904.
  • Ross PL, Huang YN, Marchese JN, et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics. 2004;3(12):1154–1169.
  • Dayon L, Hainard A, Licker V, et al. Relative quantification of proteins in human cerebrospinal fluids by MS/MS using 6-plex isobaric tags. Anal Chem. 2008;80(8):2921–2931.
  • Christoforou AL, Lilley KS. Isobaric tagging approaches in quantitative proteomics: the ups and downs. Anal Bioanal Chem. 2012;404(4):1029–1037.
  • Pappireddi N, Martin L, Wühr M. A review on quantitative multiplexed proteomics. ChemBioChem. 2019;20(10):1210–1224.
  • Rauniyar N, Yates JR. Isobaric labeling-based relative quantification in shotgun proteomics. J Proteome Res. 2014;13(12):5293–5309.
  • Arul AB, Robinson RAS. Sample multiplexing strategies in quantitative proteomics. Anal Chem. 2019;91(1):178–189.
  • Choe L, D’Ascenzo M, Relkin NR, et al. 8-Plex quantitation of changes in cerebrospinal fluid protein expression in subjects undergoing intravenous immunoglobulin treatment for Alzheimer’s disease. Proteomics. 2007;7(20):3651–3660.
  • Sleno L. The use of mass defect in modern mass spectrometry. J Mass Spectrom. 2012;47(2):226–236.
  • Eliuk S, Makarov A. Evolution of orbitrap mass spectrometry instrumentation. In: Cooks RG, Pemberton JE, editors. Annual review of analytical chemistry. Palo Alto (CA): Annual Reviews Inc; 2015. p. 61–80.
  • McAlister GC, Huttlin EL, Haas W, et al. Increasing the multiplexing capacity of TMTs using reporter ion isotopologues with isobaric masses. Anal Chem. 2012;84(17):7469–7478.
  • Werner T, Becher I, Sweetman G, et al. High-resolution enabled TMT 8-plexing. Anal Chem. 2012;84(16):7188–7194.
  • Thompson A, Wölmer N, Koncarevic S, et al. TMTpro: design, synthesis, and initial evaluation of a proline-based isobaric 16-plex tandem mass tag reagent set. Anal Chem. 2019;91(24):15941–15950.
  • Pichler P, Köcher T, Holzmann J, et al. Peptide labeling with isobaric tags yields higher identification rates using iTRAQ 4-plex compared to TMT 6-plex and iTRAQ 8-plex on LTQ orbitrap. Anal Chem. 2010;82(15):6549–6558.
  • Thingholm TE, Palmisano G, Kjeldsen F, et al. Undesirable charge-enhancement of isobaric tagged phosphopeptides leads to reduced identification efficiency. J Proteome Res. 2010;9(8):4045–4052.
  • Pottiez G, Wiederin J, Fox HS, et al. Comparison of 4-plex to 8-plex iTRAQ quantitative measurements of proteins in human plasma samples. J Proteome Res. 2012;11(7):3774–3781.
  • Frost DC, Greer T, Li L. High-resolution enabled 12-plex DiLeu isobaric tags for quantitative proteomics. Anal Chem. 2015;87(3):1646–1654.
  • Xiang F, Ye H, Chen R, et al. N,N-dimethyl leucines as novel isobaric tandem mass tags for quantitative proteomics and peptidomics. Anal Chem. 2010;82(7):2817–2825.
  • Chen Z, Wang Q, Lin L, et al. Comparative evaluation of two isobaric labeling tags, DiART and iTRAQ. Anal Chem. 2012;84(6):2908–2915.
  • Zhang J, Wang Y, Li S. Deuterium isobaric amine-reactive tags for quantitative proteomics. Anal Chem. 2010;82(18):7588–7595.
  • Zhang R, Sioma CS, Thompson RA, et al. Controlling deuterium isotope effects in comparative proteomics. Anal Chem. 2002;74(15):3662–3669.
  • Ren Y, He Y, Lin Z, et al. Reagents for isobaric labeling peptides in quantitative proteomics. Anal Chem. 2018;90(21):12366–12371.
  • Bachor R, Waliczek M, Stefanowicz P, et al. Trends in the design of new isobaric labeling reagents for quantitative proteomics. Molecules. 2019;24:4.
  • Dephoure N, Gygi SP. Hyperplexing: a method for higher-order multiplexed quantitative proteomics provides a map of the dynamic response to rapamycin in yeast. Sci Signal. 2012;5:217.
  • Frost DC, Rust CJ, Robinson RAS, et al. Increased N,N-dimethyl leucine isobaric tag multiplexing by a combined precursor isotopic labeling and isobaric tagging approach. Anal Chem. 2018;90(18):10664–10669.
  • Robinson RAS, Evans AR. Enhanced sample multiplexing for nitrotyrosine-modified proteins using combined precursor isotopic labeling and isobaric tagging. Anal Chem. 2012;84(11):4677–4686.
  • Muntel J, Kirkpatrick J, Bruderer R, et al. Comparison of protein quantification in a complex background by DIA and TMT workflows with fixed instrument time. J Proteome Res. 2019;18(3):1340–1351.
  • Bourassa S, Fournier F, Nehmé B, et al. Evaluation of iTRAQ and SWATH-MS for the quantification of proteins associated with insulin resistance in human duodenal biopsy samples. PLoS ONE. 2015;10(5):e0125934.
  • O’Connell JD, Paulo JA, O’Brien JJ, et al. Proteome-wide evaluation of two common protein quantification methods. J Proteome Res. 2018;17(5):1934–1942.
  • Hogrebe A, Von Stechow L, Bekker-Jensen DB, et al. Benchmarking common quantification strategies for large-scale phosphoproteomics. Nat Commun. 2018;9(1):1045.
  • Li Z, Adams RM, Chourey K, et al. Systematic comparison of label-free, metabolic labeling, and isobaric chemical labeling for quantitative proteomics on LTQ orbitrap velos. J Proteome Res. 2012;11(3):1582–1590.
  • 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;1(5):376–386.
  • Ong SE, Mann M. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat Protoc. 2007;1(6):2650–2660.
  • Hebert AS, Merrill AE, Bailey DJ, et al. Neutron-encoded mass signatures for multiplexed proteome quantification. Nat Methods. 2013;10(4):332–334.
  • Zhong X, Frost DC, Li L. High-resolution enabled 5-plex mass defect-based N,N-Dimethyl leucine tags for quantitative proteomics. Anal Chem. 2019;91(13):7991–7995.
  • Dayon L, Núñez Galindo A, Corthésy J, et al. Comprehensive and scalable highly automated MS-based proteomic workflow for clinical biomarker discovery in human plasma. J Proteome Res. 2014;13(8):3837–3845.
  • Kang UB, Yeom J, Kim H, et al. Quantitative analysis of mTRAQ-labeled proteome using full MS scans. J Proteome Res. 2010;9(7):3750–3758.
  • Paulo JA, Gygi SP. MTMT: an alternative, nonisobaric, tandem mass tag allowing for precursor-based quantification. Anal Chem. 2019;91(19):12167–12172.
  • Bakalarski CE, Kirkpatrick DS. A biologist’s field guide to multiplexed quantitative proteomics. Mol Cell Proteomics. 2016;15(5):1489–1497.
  • Palmese A, De CR, Chiappetta G, et al. Novel method to investigate protein carbonylation by iTRAQ strategy. Anal Bioanal Chem. 2012;404(6–7):1631–1635.
  • Hahne H, Neubert P, Kuhn K, et al. Carbonyl-reactive tandem mass tags for the proteome-wide quantification of N-linked glycans. Anal Chem. 2012;84(8):3716–3724.
  • Pan KT, Chen YY, Pu TH, et al. Mass spectrometry-based quantitative proteomics for dissecting multiplexed redox cysteine modifications in nitric oxide-protected cardiomyocyte under hypoxia. Antioxid Redox Signal. 2014;20(9):1365–1381.
  • Qu Z, Meng F, Bomgarden RD, et al. Proteomic quantification and site-mapping of S -nitrosylated proteins using isobaric iodoTMT reagents. J Proteome Res. 2014;13(7):3200–3211.
  • Panizza E, Branca RMM, Oliviusson P, et al. Isoelectric point-based fractionation by HiRIEF coupled to LC-MS allows for in-depth quantitative analysis of the phosphoproteome. Sci Rep. 2017;7:1.
  • Zhang Y, Wolf-Yadlin A, Ross PL, et al. Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol Cell Proteomics. 2005;4(9):1240–1250.
  • De Marchi U, Galindo AN, Thevenet J, et al. Mitochondrial lysine deacetylation promotes energy metabolism and calcium signaling in insulin-secreting cells. Faseb J. 2019;33(4):4660–4674.
  • Svinkina T, Gu H, Silva JC, et al. Deep, quantitative coverage of the lysine acetylome using novel anti-acetyl-lysine antibodies and an optimized proteomic workflow. Mol Cell Proteomics. 2015;14(9):2429–2440.
  • Kleifeld O, Doucet A, Auf Dem Keller U, et al. Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat Biotechnol. 2010;28(3):281–288.
  • Madzharova E, Sabino F, Auf Dem Keller U. Exploring extracellular matrix degradomes by TMT-TAILS N-terminomics. In: Sagi I, Afratis NA, editors. Methods in molecular biology. New York (NY): Humana Press Inc; 2019. p. 115–126.
  • Prudova A, Auf Dem Keller U, Butler GS, et al. Multiplex N-terminome analysis of MMP-2 and MMP-9 substrate degradomes by iTRAQ-TAILS quantitative proteomics. Mol Cell Proteomics. 2010;9(5):894–911.
  • Azurmendi L, Degos V, Tiberti N, et al. Measuring serum amyloid a for infection prediction in aneurysmal subarachnoid hemorrhage. J Proteome Res. 2015;14(9):3948–3956.
  • Dayon L, Turck N, Kienle S, et al. Isobaric tagging-based selection and quantitation of cerebrospinal fluid tryptic peptides with reporter calibration curves. Anal Chem. 2010;82(3):848–858.
  • Russell CL, Heslegrave A, Mitra V, et al. Combined tissue and fluid proteomics with tandem mass tags to identify low-abundance protein biomarkers of disease in peripheral body fluid: an Alzheimer’s disease case study. Rapid Commun Mass Spectrom. 2017;31(2):153–159.
  • 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;91(9):5794–5801.
  • 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;19:1.
  • Schoof EM, Rapin N, Savickas S, et al. A quantitative single-cell proteomics approach to characterize an acute myeloid leukemia hierarchy. bioRxiv. 2019;745679.DOI: 10.1101/745679
  • Dayon L, Turck N, Scherl A, et al. From relative to absolute quantification of tryptic peptides with tandem mass tags: application to cerebrospinal fluid. Chimia (Aarau). 2010;64(3):132–135.
  • Byers HL, Campbell J, van Ulsen P, et al. Candidate verification of iron-regulated Neisseria meningitidis proteins using isotopic versions of tandem mass tags (TMT) and single reaction monitoring. J Proteomics. 2009;73(2):231–239.
  • Desouza LV, Taylor AM, Li W, et al. Multiple reaction monitoring of mTRAQ-labeled peptides enables absolute quantification of endogenous levels of a potential cancer marker in cancerous and normal endometrial tissues. J Proteome Res. 2008;7(8):3525–3534.
  • Erickson BK, Rose CM, Braun CR, et al. A strategy to combine sample multiplexing with targeted proteomics assays for high-throughput protein signature characterization. Mol Cell. 2017;65(2):361–370.
  • Zhong X, Yu Q, Ma F, et al. HOTMAQ: a multiplexed absolute quantification method for targeted proteomics. Anal Chem. 2019;91(3):2112–2119.
  • Everley RA, Kunz RC, McAllister FE, et al. Increasing throughput in targeted proteomics assays: 54-plex quantitation in a single mass spectrometry run. Anal Chem. 2013;85(11):5340–5346.
  • Karp NA, Huber W, Sadowski PG, et al. Addressing accuracy and precision issues in iTRAQ quantitation. Mol Cell Proteomics. 2010;9(9):1885–1897.
  • Saw YO, Salim M, Noirel J, et al. iTRAQ underestimation in simple and complex mixtures: “The good, the bad and the ugly”. J Proteome Res. 2009;8(11):5347–5355.
  • Savitski MM, Sweetman G, Askenazi M, et al. Delayed fragmentation and optimized isolation width settings for improvement of protein identification and accuracy of isobaric mass tag quantification on orbitrap-type mass spectrometers. Anal Chem. 2011;83(23):8959–8967.
  • Ow SY, Salim M, Noirel J, et al. Minimising iTRAQ ratio compression through understanding LC-MS elution dependence and high-resolution HILIC fractionation. Proteomics. 2011;11(11):2341–2346.
  • Sandberg A, Branca RMM, Lehtiö J, et al. Quantitative accuracy in mass spectrometry based proteomics of complex samples: the impact of labeling and precursor interference. J Proteomics. 2014;96:133–144.
  • Ahrné E, Glatter T, Viganò C, et al. Evaluation and improvement of quantification accuracy in isobaric mass tag-based protein quantification experiments. J Proteome Res. 2016;15(8):2537–2547.
  • Bai B, Tan H, Pagala VR, et al. Deep profiling of proteome and phosphoproteome by isobaric labeling, extensive liquid chromatography, and mass spectrometryIn: Shukla AK, editor. Methods in enzymology. Cambridge (MA): Academic Press Inc; 2017. p. 377–395.
  • Burkhart JM, Vaudel M, Zahedi RP, et al. iTRAQ protein quantification: a quality-controlled workflow. Proteomics. 2011;11(6):1125–1134.
  • O’Brien JJ, O’Connell JD, Paulo JA, et al. Compositional proteomics: effects of spatial constraints on protein quantification utilizing isobaric tags. J Proteome Res. 2018;17(1):590–599.
  • Onsongo G, Stone MD, Van Riper SK, et al. LTQ-iQuant: a freely available software pipeline for automated and accurate protein quantification of isobaric tagged peptide data from LTQ instruments. Proteomics. 2010;10(19):3533–3538.
  • Savitski MM, Mathieson T, Zinn N, et al. Measuring and managing ratio compression for accurate iTRAQ/TMT quantification. J Proteome Res. 2013;12(8):3586–3598.
  • Wenger CD, Lee MV, Hebert AS, et al. Gas-phase purification enables accurate, multiplexed proteome quantification with isobaric tagging. Nat Methods. 2011;8(11):933–935.
  • Ting L, Rad R, Gygi SP, et al. MS3 eliminates ratio distortion in isobaric multiplexed quantitative proteomics. Nat Methods. 2011;8(11):937–940.
  • McAlister GC, Nusinow DP, Jedrychowski MP, et al. MultiNotch MS3 enables accurate, sensitive, and multiplexed detection of differential expression across cancer cell line proteomes. Anal Chem. 2014;86(14):7150–7158.
  • Dayon L, Sonderegger B, Kussmann M. Combination of gas-phase fractionation and MS3 acquisition modes for relative protein quantification with isobaric tagging. J Proteome Res. 2012;11(10):5081–5089.
  • Erickson BK, Mintseris J, Schweppe DK, et al. Active instrument engagement combined with a real-time database search for improved performance of sample multiplexing workflows. J Proteome Res. 2019;18(3):1299–1306.
  • Schweppe DK, Eng JK, Bailey D, et al. Full-featured, real-time database searching platform enables fast and accurate multiplexed quantitative proteomics. bioRxiv. 2019;668533.DOI: 10.1101/668533
  • Shliaha PV, Jukes-Jones R, Christoforou A, et al. Additional precursor purification in isobaric mass tagging experiments by traveling wave ion mobility separation (TWIMS). J Proteome Res. 2014;13(7):3360–3369.
  • Pfammatter S, Bonneil E, Thibault P. Improvement of quantitative measurements in multiplex proteomics using high-field asymmetric waveform spectrometry. J Proteome Res. 2016;15(12):4653–4665.
  • Pfammatter S, Bonneil E, McManus FP, et al. A novel differential ion mobility device expands the depth of proteome coverage and the sensitivity of multiplex proteomic measurements. Mol Cell Proteomics. 2018;17(10):2051–2067.
  • 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;91(6):4010–4016.
  • Paulo JA, O’Connell JD, Gygi SP. A triple knockout (TKO) proteomics standard for diagnosing ion interference in isobaric labeling experiments. J Am Soc Mass Spectrom. 2016;27(10):1620–1625.
  • Wühr M, Haas W, McAlister GC, et al. Accurate multiplexed proteomics at the MS2 level using the complement reporter ion cluster. Anal Chem. 2012;84(21):9214–9221.
  • Sonnett M, Yeung E, Wühr M. Accurate, sensitive, and precise multiplexed proteomics using the complement reporter ion cluster. Anal Chem. 2018;90(8):5032–5039.
  • Winter SV, Meier F, Wichmann C, et al. EASI-tag enables accurate multiplexed and interference-free MS2-based proteome quantification. Nat Methods. 2018;15(7):527–530.
  • Stadlmeier M, Bogena J, Wallner M, et al. A sulfoxide-based isobaric labelling reagent for accurate quantitative mass spectrometry. Angew Chem Int Ed. 2018;57(11):2958–2962.
  • Dayon L, Pasquarello C, Hoogland C, et al. Combining low- and high-energy tandem mass spectra for optimized peptide quantification with isobaric tags. J Proteomics. 2010;73(4):769–777.
  • Köcher T, Pichler P, Schutzbier M, et al. High precision quantitative proteomics using iTRAQ on an LTQ orbitrap: a new mass spectrometric method combining the benefits of all. J Proteome Res. 2009;8(10):4743–4752.
  • Park SKR, Aslanian A, McClatchy DB, et al. Census 2: isobaric labeling data analysis. Bioinformatics. 2014;30(15):2208–2209.
  • Tyanova S, Temu T, Cox J. The maxquant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc. 2016;11(12):2301–2319.
  • Ames RM, Lovell SC. DupliPHY-web: a web server for DupliPHY and DupliPHY-ML. Bioinformatics. 2015;31(3):416–417.
  • Deutsch EW, Mendoza L, Shteynberg D, et al. A guided tour of the trans-proteomic pipeline. Proteomics. 2010;10(6):1150–1159.
  • Arntzen MØ, Koehler CJ, Barsnes H, et al. IsobariQ: software for isobaric quantitative proteomics using IPTL, iTRAQ, and TMT. J Proteome Res. 2011;10(2):913–920.
  • Breitwieser FP, Müller A, Dayon L, et al. General statistical modeling of data from protein relative expression isobaric tags. J Proteome Res. 2011;10(6):2758–2766.
  • Maes E, Hadiwikarta WW, Mertens I, et al. CONSTANd: a normalization method for isobaric labeled spectra by constrained optimization. Mol Cell Proteomics. 2016;15(8):2779–2790.
  • D’Angelo G, Chaerkady R, Yu W, et al. Statistical models for the analysis of isobaric tags multiplexed quantitative proteomics. J Proteome Res. 2017;16(9):3124–3136.
  • Murie C, Sandri B, Sandberg AS, et al. Normalization of mass spectrometry data (NOMAD). In: Cocco L, editor. Advances in biological regulation. Amsterdam (Netherlands): Elsevier Ltd; 2018. p. 128–133.
  • Brenes A, Hukelmann J, Bensaddek D, et al. Multibatch TMT reveals false positives, batch effects and missing values. Mol Cell Proteomics. 2019;18(10):1967–1980.
  • Corthésy J, Theofilatos K, Mavroudi S, et al. An adaptive pipeline to maximize isobaric tagging data in large-scale MS-based proteomics. J Proteome Res. 2018;17(6):2165–2173.
  • Palstrøm NB, Matthiesen R, Beck HC. Data imputation in merged isobaric labeling-based relative quantification datasets. In: Matthiesen R, editor. Methods in molecular biology. New york (NY): Humana Press Inc; 2020. p. 297–308.
  • Shadforth IP, Dunkley TPJ, Lilley KS, et al. i-tracker: for quantitative proteomics using iTRAQ™. BMC Genomics. 2005;6:145.
  • Wen B, Zhou R, Feng Q, et al. IQuant: an automated pipeline for quantitative proteomics based upon isobaric tags. Proteomics. 2014;14(20):2280–2285.
  • Griss J, Vinterhalter G, Schwämmle V. IsoProt: a complete and reproducible workflow to analyze iTRAQ/TMT experiments. J Proteome Res. 2019;18(4):1751–1759.
  • Skillbäck T, Mattsson N, Hansson K, et al. A novel quantification-driven proteomic strategy identifies an endogenous peptide of pleiotrophin as a new biomarker of Alzheimer’s disease. Sci Rep. 2017;7:1.
  • Hung MC, Link W. Protein localization in disease and therapy. J Cell Sci. 2011;124(20):3381–3392.
  • Dunkley TPJ, Watson R, Griffin JL, et al. Localization of organelle proteins by isotope tagging (LOPIT). Mol Cell Proteomics. 2004;3(11):1128–1134.
  • Sadowski PG, Dunkley TPJ, Shadforth IP, et al. Quantitative proteomic approach to study subcellular localization of membrane proteins. Nat Protoc. 2006;1(4):1778–1789.
  • Christoforou A, Mulvey CM, Breckels LM, et al. A draft map of the mouse pluripotent stem cell spatial proteome. Nat Commun. 2016; 7:9992.
  • Mulvey CM, Breckels LM, Geladaki A, et al. Using hyperLOPIT to perform high-resolution mapping of the spatial proteome. Nat Protoc. 2017;12(6):1110–1135.
  • Geladaki A, Kočevar Britovšek N, Breckels LM, et al. Combining LOPIT with differential ultracentrifugation for high-resolution spatial proteomics. Nat Commun. 2019;10:1.
  • 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;17(6):2226–2236.
  • Santo-Domingo J, Galindo AN, Cominetti O, et al. Glucose-dependent phosphorylation signaling pathways and crosstalk to mitochondrial respiration in insulin secreting cells. Cell Commun Signal. 2019;17:1.
  • Becher I, Savitski MF, Bantscheff M. Quantifying small molecule-induced changes in cellular protein expression and posttranslational modifications using isobaric mass tags. In: Martins-de-Souza D, editor. Methods in molecular biology. New York (NY): Humana Press Inc; 2014. p. 431–443.
  • Santo-Domingo J, Dayon L, Wiederkehr A. Protein lysine acetylation: grease or sand in the gears of β-cell mitochondria? J Mol Biol. 2019. DOI: 10.1016/j.jmb.2019.09.011.
  • Savitski MM, Reinhard FBM, Franken H, et al. Tracking cancer drugs in living cells by thermal profiling of the proteome. Science. 2014;346(6205):1255784.
  • Becher I, Werner T, Doce C, et al. Thermal profiling reveals phenylalanine hydroxylase as an off-target of panobinostat. Nat Chem Biol. 2016;12(11):908–910.
  • Mateus A, Bobonis J, Kurzawa N, et al. Thermal proteome profiling in bacteria: probing protein state in vivo. Mol Syst Biol. 2018;14:7.
  • Savitski MM, Zinn N, Faelth-Savitski M, et al. Multiplexed proteome dynamics profiling reveals mechanisms controlling protein homeostasis. Cell. 2018;173(1):260–274.e225.
  • Sridharan S, Kurzawa N, Werner T, et al. Proteome-wide solubility and thermal stability profiling reveals distinct regulatory roles for ATP. Nat Commun. 2019;10:1.
  • Franken H, Mathieson T, Childs D, et al. Thermal proteome profiling for unbiased identification of direct and indirect drug targets using multiplexed quantitative mass spectrometry. Nat Protoc. 2015;10(10):1567–1593.
  • Mateus A, Määttä TA, Savitski MM. Thermal proteome profiling: unbiased assessment of protein state through heat-induced stability changes. Proteome Sci. 2017;15:1.
  • Leuenberger P, Ganscha S, Kahraman A, et al. Cell-wide analysis of protein thermal unfolding reveals determinants of thermostability. Science. 2017;355(6327):eaai7825.
  • Aebersold R, Mann M. Mass-spectrometric exploration of proteome structure and function. Nature. 2016;537(7620):347–355.
  • Dayon L, Núñez GA, Cominetti O, et al. A highly automated shotgun proteomic workflow: clinical scale and robustness for biomarker discovery in blood. In: Greening DW, Simpson RJ, editors. Methods in molecular biology. New York (NY): Humana Press Inc; 2017. p. 433–449.
  • Cominetti O, Núñez GA, Corthésy J, et al. Proteomic biomarker discovery in 1000 human plasma samples with mass spectrometry. J Proteome Res. 2016;15(2):389–399.
  • Geyer PE, Holdt LM, Teupser D, et al. Revisiting biomarker discovery by plasma proteomics. Mol Syst Biol. 2017;13:9.
  • Geyer PE, Kulak NA, Pichler G, et al. Plasma proteome profiling to assess human health and disease. Cell Syst. 2016;2(3):185–195.
  • Liu Y, Buil A, Collins BC, et al. Quantitative variability of 342 plasma proteins in a human twin population. Mol Syst Biol. 2015;11:2.
  • Cominetti O, Núñez Galindo A, Corthésy J, et al. Obesity shows preserved plasma proteome in large independent clinical cohorts. Sci Rep. 2018;8:1.
  • Dayon L, Cominetti O, Wojcik J, et al. Proteomes of paired human cerebrospinal fluid and plasma: relation to blood-brain barrier permeability in older adults. J Proteome Res. 2019;18(3):1162–1174.
  • Dayon L, Núñez Galindo A, Wojcik J, et al. Alzheimer disease pathology and the cerebrospinal fluid proteome. Alzheimers Res Ther. 2018;10:1.
  • Oller Moreno S, Cominetti O, Núñez Galindo A, et al. The differential plasma proteome of obese and overweight individuals undergoing a nutritional weight loss and maintenance intervention. Proteomics Clin Appl. 2018;12:1.
  • Moulder R, Bhosale SD, Goodlett DR, et al. Analysis of the plasma proteome using iTRAQ and TMT-based isobaric labelling. Mass Spectrom Rev. 2018;37(5):583–606.
  • Zecha J, Satpathy S, Kanashova T, et al. TMT labeling for the masses: a robust and cost-efficient, in-solution labeling approach. Mol Cell Proteomics. 2019;18(7):1468–1478.
  • Bruderer R, Muntel J, Müller S, et al. Analysis of 1508 plasma samples by capillary-flow data-independent acquisition profiles proteomics of weight loss and maintenance. Mol Cell Proteomics. 2019;18(6):1242–1254.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.