A review on mass spectrometry-based quantitative proteomics: Targeted and data independent acquisition.

Mass spectrometry (MS) based proteomics have achieved a near-complete proteome coverage in humans and in several other organisms, producing a wealth of information stored in databases and bioinformatics resources. Recent implementation of selected/multiple reaction monitoring (SRM/MRM) technology in targeted proteomics introduced the possibility of quantitatively follow-up specific protein targets in a hypothesis-driven experiment. In contrast to immunoaffinity-based workflows typically used in biological and clinical research for protein quantification, SRM/MRM is characterized by high selectivity, large capacity for multiplexing (approx. 200 proteins per analysis) and rapid, cost-effective transition from assay development to deployment. The concept of SRM/MRM utilizes triple quadrupole (QqQ) mass analyzer to provide inherent reproducibility, unparalleled sensitivity and selectivity to efficiently differentiate isoforms, post-translational modifications and mutated forms of proteins. SRM-like targeted acquisitions such as parallel reaction monitoring (PRM) are pioneered on high resolution/accurate mass (HR/AM) platforms based on the quadrupole-orbitrap (Q-orbitrap) mass spectrometer. The expansion of HR/AM also caused development in data independent acquisition (DIA). This review presents a step-by-step tutorial on development of SRM/MRM protein assay intended for researchers without prior experience in proteomics. We discus practical aspects of SRM-based quantitative proteomics workflow, summarize milestones in basic biological and medical research as well as recent trends and emerging techniques.

[1]  John D. Venable,et al.  Automated approach for quantitative analysis of complex peptide mixtures from tandem mass spectra , 2004, Nature Methods.

[2]  R. Aebersold,et al.  Systematic measurement of transcription factor-DNA interactions by targeted mass spectrometry identifies candidate gene regulatory proteins , 2013, Proceedings of the National Academy of Sciences.

[3]  Emanuel Schwarz,et al.  Label-free LC-MS/MS quantitative proteomics for large-scale biomarker discovery in complex samples. , 2007, Journal of separation science.

[4]  B. Domon,et al.  Targeted Proteomic Quantification on Quadrupole-Orbitrap Mass Spectrometer* , 2012, Molecular & Cellular Proteomics.

[5]  O. Jensen,et al.  Depletion of abundant plasma proteins by poly(N-isopropylacrylamide-acrylic acid) hydrogel particles. , 2014, Analytical chemistry.

[6]  D. Chan,et al.  Translation of proteomic biomarkers into FDA approved cancer diagnostics: issues and challenges , 2013, Clinical Proteomics.

[7]  M. Mann,et al.  Mass Spectrometry-based Proteomics Using Q Exactive, a High-performance Benchtop Quadrupole Orbitrap Mass Spectrometer* , 2011, Molecular & Cellular Proteomics.

[8]  Reinout Raijmakers,et al.  Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics , 2009, Nature Protocols.

[9]  Henry H. N. Lam,et al.  PeptideAtlas: a resource for target selection for emerging targeted proteomics workflows , 2008, EMBO reports.

[10]  Lars Malmström,et al.  Proteome-wide selected reaction monitoring assays for the human pathogen Streptococcus pyogenes , 2012, Nature Communications.

[11]  H. Towbin,et al.  Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Brendan MacLean,et al.  Label-Free Quantitation of Protein Modifications by Pseudo Selected Reaction Monitoring with Internal Reference Peptides , 2012, Journal of proteome research.

[13]  A. Zarrine-Afsar,et al.  Protein species as diagnostic markers. , 2016, Journal of proteomics.

[14]  Amos Bairoch,et al.  Detailed peptide characterization using PEPTIDEMASS – a World‐Wide‐Web‐accessible tool , 1997, Electrophoresis.

[15]  Valsamo Anagnostou,et al.  Antibody validation. , 2010, BioTechniques.

[16]  Leigh Anderson,et al.  Quantitative Mass Spectrometric Multiple Reaction Monitoring Assays for Major Plasma Proteins* , 2006, Molecular & Cellular Proteomics.

[17]  M. Mann,et al.  Stable Isotope Labeling by Amino Acids in Cell Culture, SILAC, as a Simple and Accurate Approach to Expression Proteomics* , 2002, Molecular & Cellular Proteomics.

[18]  Robertson Craig,et al.  Open source system for analyzing, validating, and storing protein identification data. , 2004, Journal of proteome research.

[19]  E. Engvall,et al.  Enzyme-linked immunosorbent assay (ELISA). Quantitative assay of immunoglobulin G. , 1971, Immunochemistry.

[20]  J. Yates,et al.  A model for random sampling and estimation of relative protein abundance in shotgun proteomics. , 2004, Analytical chemistry.

[21]  Cathy H. Wu,et al.  UniProt: the Universal Protein knowledgebase , 2004, Nucleic Acids Res..

[22]  David Fenyö,et al.  Evaluation of the variation in sample preparation for comparative proteomics using stable isotope labeling by amino acids in cell culture. , 2009, Journal of proteome research.

[23]  Darryl B. Hardie,et al.  Mass spectrometric quantitation of peptides and proteins using Stable Isotope Standards and Capture by Anti-Peptide Antibodies (SISCAPA). , 2004, Journal of proteome research.

[24]  Tao Ji,et al.  Effects of Calibration Approaches on the Accuracy for LC–MS Targeted Quantification of Therapeutic Protein , 2014, Analytical chemistry.

[25]  T. Annesley Ion suppression in mass spectrometry. , 2003, Clinical chemistry.

[26]  L L Needham,et al.  Isotope dilution--mass spectrometric quantification of specific proteins: model application with apolipoprotein A-I. , 1996, Clinical chemistry.

[27]  Bernd Thiede,et al.  Isobaric protein and peptide quantification: perspectives and issues , 2010, Expert review of proteomics.

[28]  Lukas N. Mueller,et al.  Full Dynamic Range Proteome Analysis of S. cerevisiae by Targeted Proteomics , 2009, Cell.

[29]  Ronald J. Moore,et al.  Targeted quantification of low ng/mL level proteins in human serum without immunoaffinity depletion. , 2013, Journal of proteome research.

[30]  Jack D. Henion,et al.  Ion spray interface for combined liquid chromatography/atmospheric pressure ionization mass spectrometry , 1987 .

[31]  Pei Wang,et al.  A targeted proteomics–based pipeline for verification of biomarkers in plasma , 2011, Nature Biotechnology.

[32]  Ruedi Aebersold,et al.  The Mtb proteome library: a resource of assays to quantify the complete proteome of Mycobacterium tuberculosis. , 2013, Cell host & microbe.

[33]  D. Lauffenburger,et al.  Multiple reaction monitoring for robust quantitative proteomic analysis of cellular signaling networks , 2007, Proceedings of the National Academy of Sciences.

[34]  Andrew N Hoofnagle,et al.  Multiple-reaction monitoring-mass spectrometric assays can accurately measure the relative protein abundance in complex mixtures. , 2012, Clinical chemistry.

[35]  Elizabeth M. Smigielski,et al.  dbSNP: the NCBI database of genetic variation , 2001, Nucleic Acids Res..

[36]  Michael S. Bereman,et al.  Development and Characterization of a Novel Plug and Play Liquid Chromatography-Mass Spectrometry (LC-MS) Source That Automates Connections between the Capillary Trap, Column, and Emitter* , 2013, Molecular & Cellular Proteomics.

[37]  D R Mani,et al.  Interlaboratory Evaluation of Automated, Multiplexed Peptide Immunoaffinity Enrichment Coupled to Multiple Reaction Monitoring Mass Spectrometry for Quantifying Proteins in Plasma* , 2011, Molecular & Cellular Proteomics.

[38]  Phillip C. Wright,et al.  An insight into iTRAQ: where do we stand now? , 2012, Analytical and Bioanalytical Chemistry.

[39]  Christoph H Borchers,et al.  Multiple Reaction Monitoring-based, Multiplexed, Absolute Quantitation of 45 Proteins in Human Plasma* , 2009, Molecular & Cellular Proteomics.

[40]  Mark P. Molloy,et al.  How specific is my SRM?: The issue of precursor and product ion redundancy , 2009, Proteomics.

[41]  J. Yates,et al.  An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database , 1994, Journal of the American Society for Mass Spectrometry.

[42]  Knut Reinert,et al.  Tools for Label-free Peptide Quantification , 2012, Molecular & Cellular Proteomics.

[43]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[44]  P. Atadja,et al.  Absolute quantification of histone PTM marks by MRM-based LC-MS/MS. , 2014, Analytical chemistry.

[45]  Bruno Domon,et al.  Large-Scale Targeted Proteomics Using Internal Standard Triggered-Parallel Reaction Monitoring (IS-PRM)* , 2015, Molecular & Cellular Proteomics.

[46]  J. Banoub,et al.  Absolute quantification of Atlantic salmon and rainbow trout vitellogenin by the 'signature peptide' approach using electrospray ionization QqToF tandem mass spectrometry. , 2006, Journal of mass spectrometry : JMS.

[47]  Andrew H. Thompson,et al.  Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. , 2003, Analytical chemistry.

[48]  Eric W. Deutsch,et al.  The PeptideAtlas project , 2005, Nucleic Acids Res..

[49]  Kai Pong Law,et al.  Recent advances in mass spectrometry: data independent analysis and hyper reaction monitoring , 2013, Expert review of proteomics.

[50]  Lennart Martens,et al.  PRIDE: The proteomics identifications database , 2005, Proteomics.

[51]  C. Sander,et al.  Applications of targeted proteomics in systems biology and translational medicine , 2015, Proteomics.

[52]  Howard Rosenbaum,et al.  Effects of reading proficiency on embedded stem priming in primary school children , 2021 .

[53]  Vic Spicer,et al.  Predicting Peptide Retention Times for Proteomics , 2010, Current protocols in bioinformatics.

[54]  Ruedi Aebersold,et al.  Reproducible Quantification of Cancer-Associated Proteins in Body Fluids Using Targeted Proteomics , 2012, Science Translational Medicine.

[55]  T. Pearson,et al.  Multiplexed longitudinal measurement of protein biomarkers in DBS using an automated SISCAPA workflow. , 2016, Bioanalysis.

[56]  Mu Wang,et al.  A multiple reaction monitoring method for absolute quantification of the human liver alcohol dehydrogenase ADH1C1 isoenzyme. , 2007, Analytical biochemistry.

[57]  Ludovic C. Gillet,et al.  Targeted Data Extraction of the MS/MS Spectra Generated by Data-independent Acquisition: A New Concept for Consistent and Accurate Proteome Analysis* , 2012, Molecular & Cellular Proteomics.

[58]  John R Yates,et al.  Mass spectrometry in high-throughput proteomics: ready for the big time , 2010, Nature Methods.

[59]  E. Diamandis,et al.  Toward an integrated pipeline for protein biomarker development. , 2015, Biochimica et biophysica acta.

[60]  Christie G. Enke,et al.  Selected Ion Fragmentation with a Tandem Quadrupole Mass Spectrometer. , 1978 .

[61]  이화영 X , 1960, Chinese Plants Names Index 2000-2009.

[62]  P. Taylor Matrix effects: the Achilles heel of quantitative high-performance liquid chromatography-electrospray-tandem mass spectrometry. , 2005, Clinical biochemistry.

[63]  R. Aebersold,et al.  Selected reaction monitoring for quantitative proteomics: a tutorial , 2008, Molecular systems biology.

[64]  M. Mann,et al.  More than 100,000 detectable peptide species elute in single shotgun proteomics runs but the majority is inaccessible to data-dependent LC-MS/MS. , 2011, Journal of proteome research.

[65]  R. Aebersold,et al.  Scoring proteomes with proteotypic peptide probes , 2005, Nature Reviews Molecular Cell Biology.

[66]  Luis Mendoza,et al.  PASSEL: The PeptideAtlas SRMexperiment library , 2012, Proteomics.

[67]  Ruedi Aebersold,et al.  A stress test for mass spectrometry–based proteomics , 2009, Nature Methods.

[68]  B. Domon,et al.  Selected reaction monitoring applied to proteomics. , 2011, Journal of mass spectrometry : JMS.

[69]  Martin Kircher,et al.  Deep proteome and transcriptome mapping of a human cancer cell line , 2011, Molecular systems biology.

[70]  J. Ellenberg,et al.  The quantitative proteome of a human cell line , 2011, Molecular systems biology.

[71]  J. Griffiths,et al.  A sensitive mass spectrometric method for hypothesis-driven detection of peptide post-translational modifications: multiple reaction monitoring-initiated detection and sequencing (MIDAS) , 2009, Nature Protocols.

[72]  Pei Wang,et al.  Demonstrating the feasibility of large-scale development of standardized assays to quantify human proteins , 2013, Nature Methods.

[73]  V. Marx Targeted proteomics , 2013, Nature Methods.

[74]  Amos Bairoch,et al.  neXtProt: a knowledge platform for human proteins , 2011, Nucleic Acids Res..

[75]  Susan E Abbatiello,et al.  Effect of collision energy optimization on the measurement of peptides by selected reaction monitoring (SRM) mass spectrometry. , 2010, Analytical chemistry.

[76]  Eric W. Deutsch,et al.  A complete mass-spectrometric map of the yeast proteome applied to quantitative trait analysis , 2013, Nature.

[77]  H. Lilja,et al.  Identification of a Novel Proteoform of Prostate Specific Antigen (SNP-L132I) in Clinical Samples by Multiple Reaction Monitoring* , 2013, Molecular & Cellular Proteomics.

[78]  Lars Malmström,et al.  A Computational Tool to Detect and Avoid Redundancy in Selected Reaction Monitoring , 2012, Molecular & Cellular Proteomics.

[79]  Ruedi Aebersold,et al.  Options and considerations when selecting a quantitative proteomics strategy , 2010, Nature Biotechnology.

[80]  S. Gygi,et al.  Quantitative analysis of complex protein mixtures using isotope-coded affinity tags , 1999, Nature Biotechnology.

[81]  R. Aebersold,et al.  Mass spectrometry-based proteomics , 2003, Nature.

[82]  H. Yin,et al.  Microfluidic chip for peptide analysis with an integrated HPLC column, sample enrichment column, and nanoelectrospray tip. , 2005, Analytical chemistry.

[83]  Tony Pawson,et al.  Temporal regulation of EGF signaling networks by the scaffold protein Shc1 , 2013, Nature.

[84]  T. Pawson,et al.  Selected reaction monitoring mass spectrometry reveals the dynamics of signaling through the GRB2 adaptor , 2011, Nature Biotechnology.

[85]  Daniel B. Martin,et al.  Computational prediction of proteotypic peptides for quantitative proteomics , 2007, Nature Biotechnology.

[86]  Brendan MacLean,et al.  Panorama: A Targeted Proteomics Knowledge Base , 2014, Journal of proteome research.

[87]  Daniel J. Crichton,et al.  A framework for organizing cancer-related variations from existing databases, publications and NGS data using a High-performance Integrated Virtual Environment (HIVE) , 2014, Database J. Biol. Databases Curation.

[88]  Brendan MacLean,et al.  MSstats: an R package for statistical analysis of quantitative mass spectrometry-based proteomic experiments , 2014, Bioinform..

[89]  Yassene Mohammed,et al.  PeptidePicker: a scientific workflow with web interface for selecting appropriate peptides for targeted proteomics experiments. , 2014, Journal of proteomics.

[90]  M. Holčapek,et al.  Recent developments in liquid chromatography-mass spectrometry and related techniques. , 2012, Journal of chromatography. A.

[91]  Lisa M. Chung,et al.  Review of software tools for design and analysis of large scale MRM proteomic datasets. , 2013, Methods.

[92]  Brendan MacLean,et al.  Bioinformatics Applications Note Gene Expression Skyline: an Open Source Document Editor for Creating and Analyzing Targeted Proteomics Experiments , 2022 .

[93]  R. Aebersold,et al.  Systematic quantification of peptides/proteins in urine using selected reaction monitoring , 2011, Proteomics.

[94]  Mark Brönstrup,et al.  Absolute quantification strategies in proteomics based on mass spectrometry , 2004, Expert review of proteomics.

[95]  Ludovic C. Gillet,et al.  Quantitative measurements of N‐linked glycoproteins in human plasma by SWATH‐MS , 2013, Proteomics.

[96]  Chris Sander,et al.  Human SRMAtlas: A Resource of Targeted Assays to Quantify the Complete Human Proteome , 2016, Cell.

[97]  James P. Reilly,et al.  A computational approach toward label-free protein quantification using predicted peptide detectability , 2006, ISMB.

[98]  Lloyd M. Smith,et al.  Proteoform: a single term describing protein complexity , 2013, Nature Methods.

[99]  R. Aebersold,et al.  Increased Selectivity, Analytical Precision, and Throughput in Targeted Proteomics , 2010, Molecular & Cellular Proteomics.

[100]  Ruedi Aebersold,et al.  Mass spectrometric protein maps for biomarker discovery and clinical research , 2013, Expert review of molecular diagnostics.

[101]  A. Heck,et al.  The quantitative proteomes of human-induced pluripotent stem cells and embryonic stem cells , 2011, Molecular systems biology.

[102]  Claus Jørgensen,et al.  Systematic evaluation of quantotypic peptides for targeted analysis of the human kinome , 2014, Nature Methods.

[103]  S. Markey Quantitative mass spectrometry. , 1981, Biomedical mass spectrometry.

[104]  P. Bork,et al.  Cell type-specific nuclear pores: a case in point for context-dependent stoichiometry of molecular machines , 2013, Molecular systems biology.

[105]  M. Duncan Good mass spectrometry and its place in good science. , 2012, Journal of mass spectrometry : JMS.

[106]  J. Mesirov,et al.  Prediction of high-responding peptides for targeted protein assays by mass spectrometry , 2009, Nature Biotechnology.

[107]  K. Parker,et al.  Multiplexed Protein Quantitation in Saccharomyces cerevisiae Using Amine-reactive Isobaric Tagging Reagents*S , 2004, Molecular & Cellular Proteomics.

[108]  Christopher M Rose,et al.  Neutron encoded labeling for peptide identification. , 2013, Analytical chemistry.

[109]  Chad R. Weisbrod,et al.  Accurate peptide fragment mass analysis: multiplexed peptide identification and quantification. , 2012, Journal of proteome research.

[110]  Ruedi Aebersold,et al.  Proteomics meets the scientific method , 2013, Nature Methods.

[111]  Samuel I. Miller,et al.  Precursor acquisition independent from ion count: how to dive deeper into the proteomics ocean. , 2009, Analytical chemistry.

[112]  Ying-yong Zhao,et al.  UPLC-MS(E) application in disease biomarker discovery: the discoveries in proteomics to metabolomics. , 2014, Chemico-biological interactions.

[113]  J. M. Jameson,et al.  Quantitative Chemical Analysis , 1944, Nature.

[114]  Olivier Heudi,et al.  Towards absolute quantification of therapeutic monoclonal antibody in serum by LC-MS/MS using isotope-labeled antibody standard and protein cleavage isotope dilution mass spectrometry. , 2008, Analytical chemistry.

[115]  N. Anderson,et al.  The clinical plasma proteome: a survey of clinical assays for proteins in plasma and serum. , 2010, Clinical chemistry.

[116]  E. Dratz,et al.  Absolute quantification of the G protein-coupled receptor rhodopsin by LC/MS/MS using proteolysis product peptides and synthetic peptide standards. , 2003, Analytical chemistry.

[117]  Miss A.O. Penney (b) , 1974, The New Yale Book of Quotations.

[118]  Ruedi Aebersold,et al.  On the development of plasma protein biomarkers. , 2011, Journal of proteome research.

[119]  Susan E. Abbatiello,et al.  Targeted Peptide Measurements in Biology and Medicine: Best Practices for Mass Spectrometry-based Assay Development Using a Fit-for-Purpose Approach* , 2014, Molecular & Cellular Proteomics.

[120]  Maria P. Pavlou,et al.  The long journey of cancer biomarkers from the bench to the clinic. , 2013, Clinical chemistry.

[121]  John B. Shoven,et al.  I , Edinburgh Medical and Surgical Journal.

[122]  H. Berman The Protein Data Bank: a historical perspective. , 2008, Acta crystallographica. Section A, Foundations of crystallography.

[123]  R. Yost,et al.  Triple quadrupole mass spectrometry for direct mixture analysis and structure elucidation. , 1979, Analytical chemistry.

[124]  S. Gygi,et al.  Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[125]  F. Lottspeich,et al.  Evaluation of protein loading techniques and improved separation in OFFGEL isoelectric focusing , 2011, Electrophoresis.

[126]  Christoph H Borchers,et al.  Multi-site assessment of the precision and reproducibility of multiple reaction monitoring–based measurements of proteins in plasma , 2009, Nature Biotechnology.

[127]  R. Aebersold,et al.  mProphet: automated data processing and statistical validation for large-scale SRM experiments , 2011, Nature Methods.

[128]  Bruno Domon,et al.  Selectivity of LC-MS/MS analysis: implication for proteomics experiments. , 2013, Journal of proteomics.

[129]  G. Jarvik,et al.  Parallel reaction monitoring (PRM) and selected reaction monitoring (SRM) exhibit comparable linearity, dynamic range and precision for targeted quantitative HDL proteomics. , 2015, Journal of proteomics.

[130]  Chih-Chiang Tsou,et al.  DIA-Umpire: comprehensive computational framework for data-independent acquisition proteomics , 2015, Nature Methods.

[131]  Derek J. Bailey,et al.  Parallel Reaction Monitoring for High Resolution and High Mass Accuracy Quantitative, Targeted Proteomics* , 2012, Molecular & Cellular Proteomics.

[132]  Jarrett D. Egertson,et al.  Multiplexed MS/MS for Improved Data Independent Acquisition , 2013, Nature Methods.

[133]  Lennart Martens,et al.  Ariadne's Thread: A Robust Software Solution Leading to Automated Absolute and Relative Quantification of SRM Data. , 2015, Journal of proteome research.

[134]  Birgit Schilling,et al.  Repeatability and reproducibility in proteomic identifications by liquid chromatography-tandem mass spectrometry. , 2010, Journal of proteome research.