Targeted Peptide Measurements in Biology and Medicine: Best Practices for Mass Spectrometry-based Assay Development Using a Fit-for-Purpose Approach
Open accessAbstract
Adoption of targeted mass spectrometry (MS) approaches such as multiple reaction monitoring (MRM) to study biological and biomedical questions is well underway in the proteomics community. Successful application depends on the ability to generate reliable assays that uniquely and confidently identify target peptides in a sample. Unfortunately, there is a wide range of criteria being applied to say that an assay has been successfully developed. There is no consensus on what criteria are acceptable and little understanding of the impact of variable criteria on the quality of the results generated. Publications describing targeted MS assays for peptides frequently do not contain sufficient information for readers to establish confidence that the tests work as intended or to be able to apply the tests described in their own labs. Guidance must be developed so that targeted MS assays with established performance can be made widely distributed and applied by many labs worldwide. To begin to address the problems and their solutions, a workshop was held at the National Institutes of Health with representatives from the multiple communities developing and employing targeted MS assays. Participants discussed the analytical goals of their experiments and the experimental evidence needed to establish that the assays they develop work as intended and are achieving the required levels of performance. Using this "fit-for-purpose" approach, the group defined three tiers of assays distinguished by their performance and extent of analytical characterization. Computational and statistical tools useful for the analysis of targeted MS results were described. Participants also detailed the information that authors need to provide in their manuscripts to enable reviewers and readers to clearly understand what procedures were performed and to evaluate the reliability of the peptide or protein quantification measurements reported. This paper presents a summary of the meeting and recommendations.
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Clinical application of LC-MS/MS for protein biomarkers requires stringent criteria for bias and precision, which are particularly challenging in workflows involving enzymatic digestion of the protein measurand before LC-MS/MS peptide measurement.
“Clinical application of LC-MS/MS for protein biomarkers, furthermore, requires stringent criteria for bias and precision (28, 29) , which are particularly challenging in work flows involving enzymatic digestion of the protein measurand before LC-MS/MS peptide measurement (30) .”
From Automated multiplex LC-MS/MS assay for quantifying serum apolipoproteins A-I, B, C-I, C-II, C-III, and E with qualitative apolipoprotein E phenotyping (2016) · cites this paper as [28]
NCI hosts open-access repositories of unified proteogenomics datasets, assays and reagents, including the Proteomic Data Commons, a fit-for-purpose targeted assay site and an antibody portal, largely due to CPTAC efforts.
“Largely due to these efforts, NCI hosts open-access repositories of unified proteogenomics datasets, assays and reagents, including the Proteomic Data Commons (pdc.cancer.gov), a fit-for-purpose targeted assay site (assays.cancer.gov)102,106 and an Ab portal (antibodies.cancer.gov)107.”
From A high-stringency blueprint of the human proteome (2020) · cites this paper as [102]
CPTAC SRM studies were focused on achieving essentially clinical-grade assays for relatively discrete sets of targets.
“Another significant design difference is that CPTAC SRM studies were focused on achieving essentially clinical-grade assays68 for relatively discrete sets of targets.”
From Multi-laboratory assessment of reproducibility, qualitative and quantitative performance of SWATH-mass spectrometry (2017) · cites this paper as [68]
Targeted MS technologies such as SRM/MRM and PRM offer a promising alternative to the challenges of immunoassay validation.
“As an antibody-free platform with robust sensitivity, high accuracy, and an exceptional multiplex capacity, targeted MS technologies such as SRM/MRM and PRM offer a promising alternative to the challenges of immunoassay validation [184–187].”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [184]
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Skyline: an open source document editor for creating and analyzing targeted proteomics experiments
MacLean, B., Tomazela, D. M., Shulman, N., Chambers, M., Finney, G. L., Frewen, B., Kern, R., Tabb, D. L., Liebler, D. C., & MacCoss, M. J. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq054 · Cited by 4,697 · see citing works
Self-citationLimits for qualitative detection and quantitative determination. Application to radiochemistry
Currie, L. A. (1968) · Analytical Chemistry · doi:10.1021/ac60259a007 · Cited by 4,582 · see citing works
Gillet, L. C., Navarro, P., Tate, S., Röst, H., Selevsek, N., Reiter, L., Bonner, R., & Aebersold, R. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.o111.016717 · Cited by 2,877 · see citing works
Self-citationThe Proteomics Identifications (PRIDE) database and associated tools: status in 2013
Vizcaíno, J. A., Côté, R. G., Csordas, A., Dianes, J. A., Fabregat, A., Foster, J. M., Griss, J., Alpi, E., Birim, M., Contell, J., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1262 · Cited by 1,918 · see citing works
Protein biomarker discovery and validation: the long and uncertain path to clinical utility
Rifai, N., Gillette, M. A., & Carr, S. A. (2006) · Nature Biotechnology · doi:10.1038/nbt1235 · Cited by 1,867 · see citing works
Self-citationAbsolute quantification of proteins and phosphoproteins from cell lysates by tandem MS
Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W., & Gygi, S. P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0832254100 · Cited by 1,733 · see citing works
Selected reaction monitoring–based proteomics: workflows, potential, pitfalls and future directions
Picotti, P., & Aebersold, R. (2012) · Nature Methods · doi:10.1038/nmeth.2015 · Cited by 1,302 · see citing works
Self-citationPeterson, A. C., Russell, J. D., Bailey, D. J., Westphall, M. S., & Coon, J. J. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.o112.020131 · Cited by 1,288 · see citing works
Mechanistic investigation of ionization suppression in electrospray ionization
King, R. C., Bonfiglio, R., Fernández‐Metzler, C., Miller‐Stein, C. M., & Olah, T. V. (2000) · Journal of the American Society for Mass Spectrometry · doi:10.1016/s1044-0305(00)00163-x · Cited by 1,089 · see citing works
Addona, T. A., Abbatiello, S. E., Schilling, B., Skates, S. J., Mani, D. R., Bunk, D. M., Spiegelman, C. H., Zimmerman, L. J., Ham, A.-J. L., Keshishian, H., et al. (2009) · Nature Biotechnology · doi:10.1038/nbt.1546 · Cited by 1,037 · see citing works
Self-citationDesiere, F. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj040 · Cited by 910 · see citing works
Matuszewski, B. K., Constanzer, M. L., & Chavez-Eng, C. M. (1998) · Analytical Chemistry · doi:10.1021/ac971078+ · Cited by 881 · see citing works
Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present
Bantscheff, M., Lemeer, S., Savitski, M. M., & Kuster, B. (2012) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-012-6203-4 · Cited by 801 · see citing works
Automated approach for quantitative analysis of complex peptide mixtures from tandem mass spectra
Venable, J. D., Dong, M., Wohlschlegel, J. A., Dillin, A. G., & Yates, J. R. (2004) · Nature Methods · doi:10.1038/nmeth705 · Cited by 798 · see citing works
Fit-for-Purpose Method Development and Validation for Successful Biomarker Measurement
Lee, J. W., Devanarayan, V., Barrett, Y. C., WEINER, R. S., Allinson, J. L., Fountain, S. T., Keller, S., Weinryb, I., Green, M., Duan, L., et al. (2006) · Pharmaceutical Research · doi:10.1007/s11095-005-9045-3 · Cited by 770 · see citing works
Self-citationFull dynamic range proteome analysis of S. cerevisiae by targeted proteomics
Picotti, P., Bodenmiller, B., Mueller, L. N., Domon, B., & Aebersold, R. (2009) · Cell · doi:10.1016/j.cell.2009.05.051 · Cited by 744 · see citing works
Self-citationBioanalytical Method Validation
Garofolo, F. (2004) · doi:10.1002/0471463728.ch8 · Cited by 688 · see citing works
Keshishian, H., Addona, T. A., Burgess, M. W., Kuhn, E. W., & Carr, S. A. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m700354-mcp200 · Cited by 684 · see citing works
Self-citationUsing i RT , a normalized retention time for more targeted measurement of peptides
Escher, C., Reiter, L., MacLean, B., Ossola, R., Herzog, F., Chilton, J. M., MacCoss, M. J., & Rinner, O. (2012) · PROTEOMICS · doi:10.1002/pmic.201100463 · Cited by 586 · see citing works
Self-citationmProphet: automated data processing and statistical validation for large-scale SRM experiments
Reiter, L., Rinner, O., Picotti, P., Hüttenhain, R., Beck, M., Brusniak, M.-Y., Hengartner, M. O., & Aebersold, R. (2011) · Nature Methods · doi:10.1038/nmeth.1584 · Cited by 532 · see citing works
Self-citationKuzyk, M. A., Smith, D., Yang, J., Cross, T. J., Jackson, A. M., Hardie, D. B., Anderson, N. L., & Borchers, C. H. (2009) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m800540-mcp200 · Cited by 515 · see citing works
Self-citationTargeted Proteomic Quantification on Quadrupole-Orbitrap Mass Spectrometer
Gallien, S., Duriez, E., Crone, C., Kellmann, M., Moehring, T., & Domon, B. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.o112.019802 · Cited by 510 · see citing works
Self-citationThe Need for Guidelines in Publication of Peptide and Protein Identification Data
Carr, S. A., Aebersold, R. H., Baldwin, M. A., Burlingame, A. L., Clauser, K. R., & Nesvizhskii, A. I. (2004) · Molecular & Cellular Proteomics · doi:10.1074/mcp.t400006-mcp200 · Cited by 500 · see citing works
Self-citationQuantitative analysis of peptides and proteins in biomedicine by targeted mass spectrometry
Gillette, M. A., & Carr, S. A. (2012) · Nature Methods · doi:10.1038/nmeth.2309 · Cited by 497 · see citing works
Self-citationBeynon, R. J., Doherty, M. K., Pratt, J. M., & Gaskell, S. J. (2005) · Nature Methods · doi:10.1038/nmeth774 · Cited by 472 · see citing works
High-throughput generation of selected reaction-monitoring assays for proteins and proteomes
Picotti, P., Rinner, O., Stallmach, R., Dautel, F., Farrah, T., Domon, B., Wenschuh, H., & Aebersold, R. H. (2009) · Nature Methods · doi:10.1038/nmeth.1408 · Cited by 452 · see citing works
Self-citationIsotope-labeled Protein Standards
Brun, V., Dupuis, A., Adrait, A., Marcellin, M., Thomas, D. Y., Court, M., Vandenesch, F., & Garin, J. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m700163-mcp200 · Cited by 443 · see citing works
A targeted proteomics–based pipeline for verification of biomarkers in plasma
Whiteaker, J. R., Lin, C., Kennedy, J. J., Hou, L., Trute, M., Sokal, I., Yan, P., Schoenherr, R. M., Zhao, L., Voytovich, U. J., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1900 · Cited by 365 · see citing works
Self-citationLC-MS/MS in the Clinical Laboratory - Where to From Here?
Grebe, S. K. G., & Singh, R. J. (2011) · Europe PMC (PubMed Central) · Cited by 356 · see citing works
Barr, J. R., Maggio, V. L., Patterson, D. G., Cooper, G. R., Henderson, L. O., Turner, W. E., Smith, S. J., Hannon, W. H., Needham, L. L., & Sampson, E. J. (1996) · Clinical Chemistry · doi:10.1093/clinchem/42.10.1676 · Cited by 347 · see citing works
Evaluation of regression procedures for methods comparison studies
Línnet, K. (1993) · Clinical Chemistry · doi:10.1093/clinchem/39.3.424 · Cited by 324 · see citing works
Isotope dilution strategies for absolute quantitative proteomics
Brun, V., Masselon, C., Garin, J., & Dupuis, A. (2009) · Journal of Proteomics · doi:10.1016/j.jprot.2009.03.007 · Cited by 314 · see citing works
Multiplexed MS/MS for improved data-independent acquisition
Egertson, J. D., Kuehn, A., Merrihew, G. E., Bateman, N. W., MacLean, B., Ting, Y. S., Canterbury, J. D., Marsh, D. M., Kellmann, M., Zabrouskov, V., et al. (2013) · Nature Methods · doi:10.1038/nmeth.2528 · Cited by 305 · see citing works
Self-citationKeshishian, H., Addona, T. A., Burgess, M. W., Mani, D. R., Shi, X. D., Kuhn, E. W., Sabatine, M. S., Gerszten, R. E., & Carr, S. A. (2009) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m900140-mcp200 · Cited by 286 · see citing works
Self-citationGlobal chromatin profiling reveals NSD2 mutations in pediatric acute lymphoblastic leukemia
Jaffe, J. D., Wang, Y., Chan, H. M., Zhang, J., Huether, R., Kryukov, G. V., Bhang, H.-E. C., Taylor, J. E., Hu, M., Englund, N. P., et al. (2013) · Nature Genetics · doi:10.1038/ng.2777 · Cited by 282 · see citing works
Self-citationDNAzyme Targeting c- jun Suppresses Skin Cancer Growth
Cai, H., Santiago, F. S., Prado-Lourenço, L., Wang, B., Patrikakis, M., Davenport, M. P., Maghzal, G. J., Stocker, R., Parish, C. R., Chong, B. H., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003960 · Cited by 282 · see citing works
Precursor Acquisition Independent From Ion Count: How to Dive Deeper into the Proteomics Ocean
Panchaud, A., Scherl, A., Shaffer, S. A., von Haller, P. D., Kulasekara, H. D., Miller, S. I., & Goodlett, D. R. (2009) · Analytical Chemistry · doi:10.1021/ac900888s · Cited by 264 · see citing works
Statistical Design of Quantitative Mass Spectrometry-Based Proteomic Experiments
Oberg, A. L., & Olga Vitek, A. (2009) · Journal of Proteome Research · doi:10.1021/pr8010099 · Cited by 258 · see citing works
Addona, T. A., Shi, X. D., Keshishian, H., Mani, D. R., Burgess, M. W., Gillette, M. A., Clauser, K. R., Shen, D., Lewis, G. D., Farrell, L. A., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1899 · Cited by 249 · see citing works
Self-citationReproducible Quantification of Cancer-Associated Proteins in Body Fluids Using Targeted Proteomics
Hüttenhain, R., Soste, M., Selevsek, N., Röst, H. L., Sethi, A., Carapito, C., Farrah, T., Deutsch, E. W., Kusebauch, U., Moritz, R. L., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003989 · Cited by 245 · see citing works
Self-citationPaulovich, A. G., Whiteaker, J. R., Hoofnagle, A. N., & Wang, P. (2008) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.200780174 · Cited by 229 · see citing works
Self-citationReporting Protein Identification Data
Bradshaw, R. A., Burlingame, A. L., Carr, S. A., et al. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.e600005-mcp200 · Cited by 222 · see citing works
Self-citationShi, T., Fillmore, T., Sun, X., Zhao, R., Schepmoes, A., Hossain, M., Xie, F., Wu, S., Kim, J., Jones, N., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1204366109 · Cited by 220 · see citing works
Self-citationA database of mass spectrometric assays for the yeast proteome
Picotti, P., Lam, H., Campbell, D. S., Deutsch, E. W., Mirzaei, H., Ranish, J. A., Domon, B., & Aebersold, R. H. (2008) · Nature Methods · doi:10.1038/nmeth1108-913 · Cited by 209 · see citing works
Self-citationPASSEL : The P eptide A tlas SRM experiment library
Farrah, T., Deutsch, E. W., Kreisberg, R., Sun, Z., Campbell, D. S., Mendoza, L., Kusebauch, U., Brusniak, M., Hüttenhain, R., Schiess, R., et al. (2012) · PROTEOMICS · doi:10.1002/pmic.201100515 · Cited by 206 · see citing works
Self-citationMRM ‐based multiplexed quantitation of 67 putative cardiovascular disease biomarkers in human plasma
Domański, D., Percy, A. J., Yang, J., Chambers, A. G., Hill, J. S., Freue, G. V. C., & Borchers, C. H. (2012) · PROTEOMICS · doi:10.1002/pmic.201100568 · Cited by 205 · see citing works
Self-citationAbbatiello, S. E., Mani, D. R., Keshishian, H., & Carr, S. A. (2009) · Clinical Chemistry · doi:10.1373/clinchem.2009.138420 · Cited by 198 · see citing works
Self-citationKushnir, M. M., Rockwood, A. L., Roberts, W. L., Abraham, D., Hoofnagle, A. N., & Meikle, A. W. (2013) · Clinical Chemistry · doi:10.1373/clinchem.2012.195594 · Cited by 193 · see citing works
Self-citationKuhn, E. W., Whiteaker, J. R., Mani, D. R., Jackson, A., Zhao, L., Pope, M. E., SMITH, D. S. H., Rivera, K. D., Anderson, N. L., Skates, S. J., et al. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m111.013854 · Cited by 183 · see citing works
Self-citationMutant proteins as cancer-specific biomarkers
Wang, Q., Chaerkady, R., Wu, J., Hwang, H. J., Papadopoulos, N., Kopelovich, L., Maitra, A., Matthaei, H., Eshleman, J. R., Hruban, R. H., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019203108 · Cited by 168 · see citing works
Deutsch, E. W. (2009) · Methods in molecular biology · doi:10.1007/978-1-60761-444-9_19 · Cited by 139 · see citing works
Self-citationWhiteaker, J. R., Zhao, L., Abbatiello, S. E., Burgess, M. W., Kuhn, E. W., Lin, C., Pope, M. E., Razavi, M., Anderson, N. L., Pearson, T. W., et al. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.005645 · Cited by 135 · see citing works
Self-citationNeubert, H., Muirhead, D., Kabir, M., Grace, C., Cleton, A., & Arends, R. (2012) · Analytical Chemistry · doi:10.1021/ac303031q · Cited by 134 · see citing works
Self-citationPitt, J. J., Eggington, M., & Kahler, S. G. (2002) · Clinical Chemistry · doi:10.1093/clinchem/48.11.1970 · Cited by 123 · see citing works
Mani, D. R., Abbatiello, S. E., & Carr, S. A. (2012) · BMC Bioinformatics · doi:10.1186/1471-2105-13-s16-s9 · Cited by 117 · see citing works
Self-citationQuantitation of Endogenous Analytes in Biofluid without a True Blank Matrix
Li, W., & Cohen, L. H. (2003) · Analytical Chemistry · doi:10.1021/ac034505u · Cited by 116 · see citing works
Abbatiello, S. E., Mani, D. R., Schilling, B., MacLean, B., Zimmerman, L. J., Feng, X., Cusack, M. P., Sedransk, N., Hall, S. C., Addona, T. A., et al. (2013) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m112.027078 · Cited by 113 · see citing works
Self-citationFit-for-purpose biomarker method validation for application in clinical trials of anticancer drugs
on behalf of the Bioanalysis and Quality Assurance (BAQA) Group of the ECMC, Cummings, J., Raynaud, F. I., Jones, J. L., Sugar, R., & Dive, C. (2010) · British Journal of Cancer · doi:10.1038/sj.bjc.6605910 · Cited by 112 · see citing works
Zhang, H., Liu, Q., Zimmerman, L. J., Ham, A. L., Slebos, R. J. C., Rahman, J. S. M., Kikuchi, T., Massion, P. P., Carbone, D. P., Billheimer, D. D., et al. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.006593 · Cited by 110 · see citing works
Self-citationPartly Nonparametric Approach for Determining the Limit of Detection
Línnet, K., & Kondratovich, M. (2004) · Clinical Chemistry · doi:10.1373/clinchem.2003.029983 · Cited by 103 · see citing works
Mass Spectrometry-Based Approaches Toward Absolute Quantitative Proteomics
Kito, K., & Ito, T. (2008) · Current Genomics · doi:10.2174/138920208784533647 · Cited by 102 · see citing works
2012 White Paper on Recent Issues in Bioanalysis And Alignment of Multiple Guidelines
Desilva, B. S., Garofolo, F., Rocci, M. L., et al. (2012) · Bioanalysis · doi:10.4155/bio.12.205 · Cited by 101 · see citing works
Review of software tools for design and analysis of large scale MRM proteomic datasets
Colangelo, C. M., Chung, L. M., Bruce, C., & Cheung, K. (2013) · Methods · doi:10.1016/j.ymeth.2013.05.004 · Cited by 97 · see citing works
Quality concepts and practices applied to sampling—an exploratory study
Thompson, M., & Ramsey, M. H. (1995) · The Analyst · doi:10.1039/an9952000261 · Cited by 97 · see citing works
Pan, S., Chen, R., Brand, R. E., Hawley, S. J., Tamura, Y., Gafken, P. R., Milless, B. P., Goodlett, D. R., Rush, A. J., & Brentnall, T. A. (2012) · Journal of Proteome Research · doi:10.1021/pr201117w · Cited by 96 · see citing works
Neubert, H., Gale, J. D., & Muirhead, D. (2010) · Clinical Chemistry · doi:10.1373/clinchem.2010.144576 · Cited by 95 · see citing works
Self-citationEstablishing the fitness for purpose of mass spectrometric methods
Bethem, R. A., Boison, J. O. K., Gale, J. P., et al. (2003) · Journal of the American Society for Mass Spectrometry · doi:10.1016/s1044-0305(03)00137-5 · Cited by 93 · see citing works
Self-citationTimmerman, P., Kall, M. A., Gordon, B. H., et al. (2010) · Bioanalysis · doi:10.4155/bio.10.90 · Cited by 83 · see citing works
Shuford, C. M., Sederoff, R. R., Chiang, V. L., et al. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.o112.017145 · Cited by 80 · see citing works
Picard, G., Lebert, D., Louwagie, M., Adrait, A., Huillet, C., Vandenesch, F., Bruley, C., Garin, J., Jaquinod, M., & Brun, V. (2012) · Journal of Mass Spectrometry · doi:10.1002/jms.3106 · Cited by 79 · see citing works
Lee, J. W., Figeys, D., & Vasilescu, J. (2006) · Advances in cancer research · doi:10.1016/s0065-230x(06)96010-2 · Cited by 76 · see citing works
Self-citationBerna, M. J., Ott, L. W., Engle, S., Watson, D., Solter, P. F., & Ackermann, B. L. (2008) · Analytical Chemistry · doi:10.1021/ac702311m · Cited by 69 · see citing works
Self-citationSherrod, S. D., Myers, M. V., Li, M., Myers, J. S., Carpenter, K. L., MacLean, B., MacCoss, M. J., Liebler, D. C., & Ham, A. L. (2012) · Journal of Proteome Research · doi:10.1021/pr201240a · Cited by 68 · see citing works
Self-citationWhiteaker, J. R., Zhao, L., Lin, C., Yan, P., Wang, P., & Paulovich, A. G. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m111.015347 · Cited by 68 · see citing works
Self-citationBrusniak, M., Kwok, S.-T., Christiansen, M. W., Campbell, D. S., Reiter, L., Picotti, P., Kusebauch, U., Ramos, H., Deutsch, E. W., Chen, J., et al. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-78 · Cited by 67 · see citing works
Self-citationIf a job is worth doing, it is worth doing twice
Russell, J. F. (2013) · Nature · doi:10.1038/496007a · Cited by 64 · see citing works
Šurinová, S., Hüttenhain, R., Chang, C.-Y., Pernas, L. E., Olga Vitek, A., & Aebersold, R. H. (2013) · Nature Protocols · doi:10.1038/nprot.2013.091 · Cited by 63 · see citing works
Self-citationTimmerman, P., Herling, C., Stoellner, D., et al. (2012) · Bioanalysis · doi:10.4155/bio.12.164 · Cited by 59 · see citing works
Guidelines for reporting quantitative mass spectrometry based experiments in proteomics
Martínez‐Bartolomé, S., Deutsch, E. W., Binz, P., et al. (2013) · Journal of Proteomics · doi:10.1016/j.jprot.2013.02.026 · Cited by 59 · see citing works
Self-citationMass Spectrometric Protein Identification Using the Global Proteome Machine
Fenyö, D., Eriksson, J. W., & Beavis, R. C. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-842-3_11 · Cited by 58 · see citing works
Noninvasive human metabolome analysis for differential diagnosis of inborn errors of metabolism
Kuhara, T. (2007) · Journal of Chromatography B · doi:10.1016/j.jchromb.2007.03.031 · Cited by 56 · see citing works
The Scope of Mass Spectrometry in Clinical Chemistry
Lawson, A. (1975) · Clinical Chemistry · doi:10.1093/clinchem/21.7.803 · Cited by 53 · see citing works
Singh, R., Crow, F. W., Babić, N., et al. (2007) · Clinical Chemistry · doi:10.1373/clinchem.2006.078832 · Cited by 50 · see citing works
Hüttenhain, R., Šurinová, S., Ossola, R., Sun, Z., Campbell, D. S., Cerciello, F., Schiess, R., Bausch‐Fluck, D., Rosenberger, G., Chen, J., et al. (2013) · Molecular & Cellular Proteomics · doi:10.1074/mcp.o112.026617 · Cited by 50 · see citing works
Self-citationLi, W., Nemirovskiy, O. V., Fountain, S. T., Mathews, W. R., & Szekely‐Klepser, G. (2007) · Analytical Biochemistry · doi:10.1016/j.ab.2007.05.002 · Cited by 49 · see citing works
Remily-Wood, E. R., Liu, R. Z., Xiang, Y., Chen, Y., Thomas, C. E., Rajyaguru, N., Kaufman, L. M., Ochoa, J. E., Hazlehurst, L., Pinilla-Ibarz, J. A., et al. (2011) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.201000115 · Cited by 48 · see citing works
Self-citationVargo, J. D. (1998) · Analytical Chemistry · doi:10.1021/ac971365d · Cited by 40 · see citing works
Use of Mass Spectrometry for Confirmation of Animal Drug Residues
Sphon, J. A. (1978) · Journal of AOAC INTERNATIONAL · doi:10.1093/jaoac/61.5.1247 · Cited by 39 · see citing works
Tang, H., Beer, L. A., Barnhart, K. T., & Speicher, D. W. (2011) · Journal of Proteome Research · doi:10.1021/pr2002098 · Cited by 35 · see citing works
Rochat, B., Peduzzi, D., McMullen, J., Favre, A., Kottelat, E., Favrat, B., Tissot, J., Angelillo‐Scherrer, A., Bromirski, M., & Waldvogel, S. (2013) · Bioanalysis · doi:10.4155/bio.13.225 · Cited by 32 · see citing works
Revised Draft Guidelines for Proteomic Data Publication
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Self-citationBrusniak, M., Chu, C. S., Kusebauch, U., et al. (2012) · PROTEOMICS · doi:10.1002/pmic.201100571 · Cited by 28 · see citing works
Mass spectrometry in trace analysis
Bethem, R. A., & Boyd, R. K. (1998) · Journal of the American Society for Mass Spectrometry · doi:10.1016/s1044-0305(98)00032-4 · Cited by 23 · see citing works
Self-citationBrunley, W. C., & Sphon, J. A. (1981) · Journal of Mass Spectrometry · doi:10.1002/bms.1200080908 · Cited by 15 · see citing works
Huang, X., Liu, M., Nold, M. J., Tian, C., Fu, K., Zheng, J., Geromanos, S. J., & Ding, S. (2011) · Analytical Chemistry · doi:10.1021/ac201555m · Cited by 14 · see citing works
Timmerman, P., Lausecker, B., Barosso, B., et al. (2012) · Bioanalysis · doi:10.4155/bio.12.37 · Cited by 13 · see citing works
Stable isotopes in the management and diagnosis of inborn errors of metabolism
Parsons, H. G. (1990) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y90-144 · Cited by 4 · see citing works
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- [68]Kuhn E. Ross J. Abbatiello S. E. Mani D. R. Carr S. A. (2012) Reversing the Curve: Determining LOD in the Presence of Endogenous Signal using SID-MRM-MS. Presented at the 60th Annual Conference on Mass Spectrometry, Monday poster MP01, poster number 004
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- Authors
- Carr, S. A., Abbatiello, S. E., Ackermann, B. L., Borchers, C., Domon, B., Deutsch, E. W., Grant, R. P., Hoofnagle, A. N., Hüttenhain, R., Koomen, J. M., Liebler, D. C., Liu, T., MacLean, B., Mani, D., Mansfield, E., Neubert, H., Paulovich, A. G., Reiter, L., Vitek, O., Aebersold, R., Anderson, L., Bethem, R., Blonder, J., Boja, E., Botelho, J., Boyne, M., Bradshaw, R. A., Burlingame, A. L., Chan, D., Keshishian, H., Kuhn, E., Kinsinger, C., Lee, J. S. H., Lee, S.-W., Moritz, R., Oses-Prieto, J., Rifai, N., Ritchie, J., Rodriguez, H., Srinivas, P. R., Townsend, R. R., Van Eyk, J., Whiteley, G., Wiita, A., & Weintraub, S.
- Affiliations
- Broad Institute (US)
- Eli Lilly (United States) (US)
- University of Victoria (CA)
- Institute for Systems Biology (US)
- LabCorp (United States) (US)
- University of Washington (US)
- University of California, San Francisco (US)
- Moffitt Cancer Center (US)
- Vanderbilt University (US)
- Pacific Northwest National Laboratory (US)
- United States Food and Drug Administration (US)
- Pfizer (United States) (US)
- Fred Hutch Cancer Center (US)
- Biognosys (Switzerland) (CH)
- ETH Zurich (CH)
- National Cancer Institute (US)
- Centers for Disease Control and Prevention (US)
- Johns Hopkins University (US)
- Korea University (KR)
- Boston Children's Hospital (US)
- Emory University (US)
- National Heart, Lung, and Blood Institute (US)
- Washington University in St. Louis (US)
- The University of Texas at San Antonio Health Science Center (US)
- Corresponding author
- Carr, Steven A.
- ORCID
- Carr, Steven A.
- Abbatiello, Susan E.
- Borchers, Christoph
- Deutsch, Eric W.
- Grant, Russell P.
- Hoofnagle, Andrew N.
- Hüttenhain, Ruth
- Koomen, John M.
- Liebler, Daniel C.
- Liu, Tao
- MacLean, Brendan
- Mani, DR
- Neubert, Hendrik
- Paulovich, Amanda G.
- Reiter, Lukas
- Aebersold, Ruedi
- Boja, Emily
- Botelho, Julianne
- Burlingame, Alma L.
- Chan, Daniel
- Keshishian, Hasmik
- Kuhn, Eric
- Kinsinger, Christopher
- Lee, Jerry S.H.
- Lee, Sang-Won
- Moritz, Robert
- Rifai, Nader
- Ritchie, James
- Rodriguez, Henry
- Srinivas, Pothur R.
- Townsend, R. Reid
- Whiteley, Gordon
- Wiita, Arun
- Weintraub, Susan
- Venue
- Molecular & Cellular Proteomics
- Publisher
- Elsevier BV
- Published
- 2014-03
- Volume
- 13
- Issue
- 3
- Pages
- 907-917
- ISSN
- 1535-9476 (ISSN-L)
- PMC
- PMC3945918
- OpenAlex
- W2109326791
- Cited by
- 561
- References
- 97
- Citations by year
- 2026: 31 · 2025: 19 · 2024: 34 · 2023: 37 · 2022: 33 · 2021: 40 · 2020: 50 · 2019: 58 · 2018: 40 · 2017: 64 · 2016: 64 · 2015: 53 · 2014: 37
- FWCI
- 31.14
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Molecular & Cellular Proteomics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- National Institutes of Health (U24CA160034)
- Topics
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Physical Sciences › Chemistry › Spectroscopy › Mass Spectrometry Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- targeted mass spectrometry, multiple reaction monitoring, assay development, peptide quantification, protein quantification, analytical characterization, reproducibility
- MeSH terms
- Animals, Biological Assay, Biology, Humans, Isotope Labeling, Medicine, Peptides, Reference Standards, Software, Mass Spectrometry, Guidelines as Topic, Proteomics
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