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Quantification of Thyroglobulin, a Low-Abundance Serum Protein, by Immunoaffinity Peptide Enrichment and Tandem Mass Spectrometry
Open accessAbstract
Background: Quantification of serum tumor markers plays an important role in determining whether patients treated for cancer require further therapy. Whereas large-scale proteomic efforts aim to identify novel tumor markers to facilitate early detection, optimization of methods for quantifying known tumor markers offers another approach to improving management of malignancies. For example, immunoassays used in clinical practice to measure established tumor markers suffer from potential interference from endogenous immunoglobulins and imperfect concordance across platforms—problems that also plague many other immunoassays. To address these important limitations, this study used peptide immunoaffinity enrichment in concert with liquid chromatography–tandem mass spectrometry (LC-MS/MS) to quantify thyroglobulin, a well-characterized tumor marker. Methods: We identified 3 peptides in tryptic digests of thyroglobulin that were detected at low concentrations by tandem mass spectrometry, raised polyclonal antibodies to those peptides, and used the antibodies to extract the 3 corresponding peptides from tryptic digests of human serum. We quantified each endogenous peptide using LC-MS/MS and multiple reaction monitoring with external calibrators. Results: The detection limit for endogenous thyroglobulin in serum was 2.6 μg/L (4 pmol/L). Direct comparison with immunoassay revealed good correlation (r2 = 0.81). Conclusions: Immunoaffinity peptide enrichment–tandem mass spectrometry can detect tryptic peptides of thyroglobulin at picomolar concentrations while also digesting the endogenous immunoglobulins that can potentially interfere with traditional immunoassays. Our observations suggest a general analytical strategy for using immunoaffinity isolation together with tandem mass spectrometry to quantify tumor antigens and other low-abundance proteins in human serum.
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“Most known neosubstrate proteins have been identified through proteomic analyses of different cell lineages11,15,165,166.”
From Cancer therapies based on targeted protein degradation — lessons learned with lenalidomide (2021) · cites this paper as [166]
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“This strategy has been reported for thyroglobulin, a protein with known autoantibody interferences [9,10].”
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Clinical applications of mass spectrometry‐based proteomics in cancer: Where are we?
Boys, E. L., Liu, J., Robinson, P. J., & Reddel, R. R. (2022) · PROTEOMICS · doi:10.1002/pmic.202200238 · Cited by 67
Thyroglobulin measurement in the management of patients with differentiated thyroid cancer
Algeciras-Schimnich, A. (2018) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/10408363.2018.1450830 · Cited by 63
“[47] and other methods have been published subsequently [37,48,49].”
MethodFu, Q., Murray, C. I., Karpov, O. A., & Eyk, J. E. V. (2021) · Mass Spectrometry Reviews · doi:10.1002/mas.21750 · Cited by 67
Xu, Y., Mehl, J. T., Bakhtiar, R., & Woolf, E. (2010) · Analytical Chemistry · doi:10.1021/ac1009832 · Cited by 64
Application of Proteomics in Biomarker Discovery: a Primer for the Clinician
Tambor, V., Fučíková, A., Lenčo, J., Kacerovský, M., Řeháček, V., Stulík, J., & Pudil, R. (2010) · Physiological Research · doi:10.33549/physiolres.931758 · Cited by 62
Quantification of growth hormone in serum by isotope dilution mass spectrometry
Arsene, C. G., Henrion, A., Diekmann, N., Manolopoulou, J., & Bidlingmaier, M. (2009) · Analytical Biochemistry · doi:10.1016/j.ab.2010.03.005 · Cited by 62
Haqqani, A. S., Caram‐Salas, N. L., Ding, W., Brunette, E., Delaney, C. E., Baumann, E., Boileau, E., & Stanimirovic, D. B. (2012) · Molecular Pharmaceutics · doi:10.1021/mp3004995 · Cited by 63
Lee, A. Y. H., Chappell, D. L., Bak, M. J., Judo, M., Liang, L. A., Churakova, T., Ayanoglu, G., Castro‐Perez, J. M., Zhou, H., Previs, S. F., et al. (2015) · Clinical Chemistry · doi:10.1373/clinchem.2015.244251 · Cited by 59
Advances in Proteomic Technologies and Its Contribution to the Field of Cancer
Mesri, M. (2014) · Advances in Medicine · doi:10.1155/2014/238045 · Cited by 61
“, who implemented SISCAPA assays for quantification of low-abundance serum thyroglobulin, and simultaneous measurement of apolipoprotein A–I and apolipoprotein B [133, 173].”
BackgroundMethodFirst Steps toward Harmonization of LC-MS/MS Thyroglobulin Assays
Netzel, B. C., Grant, R. P., Hoofnagle, A. N., Rockwood, A. L., Shuford, C. M., & Grebe, S. K. G. (2015) · Clinical Chemistry · doi:10.1373/clinchem.2015.245266 · Cited by 58
Self-citationSchoenherr, R. M., Zhao, L., Whiteaker, J. R., Feng, L.-C., Li, L., Liu, L., Liu, X., & Paulovich, A. G. (2009) · Journal of Immunological Methods · doi:10.1016/j.jim.2009.11.017 · Cited by 57
“) These performance characteristics are consistent with those reported in polyclonal antibody-based SISCAPA assays,(Berna et al., 2006; Whiteaker et al., 2007a; Hoofnagle et al., 2008; Kuhn et al., 2009) demonstrate the feasibility of using a monoclonal antibody for SISCAPA, and raise the possibility of identifying ve…”
MethodResultAzmat, U., Porter, K. M., Senter, L. A., Ringel, M. D., & Nabhan, F. A. (2016) · Thyroid · doi:10.1089/thy.2016.0210 · Cited by 57
Jung, S., Whiteaker, J. R., Zhao, L., Yoo, H., Paulovich, A. G., & Hahn, S. H. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00828 · Cited by 56
Rockwood, A. L., Kushnir, M. M., & Clarke, N. J. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-816063-3.00002-5 · Cited by 55
Emerging role of clinical mass spectrometry in pathology
Fung, A. W. S., Sugumar, V., Ren, A. H., & Kulasingam, V. (2019) · Journal of Clinical Pathology · doi:10.1136/jclinpath-2019-206269 · Cited by 53
Biochemical Testing in Thyroid Disorders
Esfandiari, N. H., & Papaleontiou, M. (2017) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2017.04.002 · Cited by 50
Multiple Reaction Monitoring (MRM)
Freue, G. V. C., & Borchers, C. H. (2012) · Circulation Cardiovascular Genetics · doi:10.1161/circgenetics.111.959528 · Cited by 52
Rappold, B. A. (2021) · Annals of Laboratory Medicine · doi:10.3343/alm.2022.42.2.121 · Cited by 56
Tsikas, D. (2009) · Journal of Chromatography B · doi:10.1016/j.jchromb.2009.11.008 · Cited by 51
Mass spectrometry‐based targeted proteomics for analysis of protein mutations
Lin, T., Zhang, T., Kitata, R. B., Liu, T., Smith, R. D., Qian, W., & Shi, T. (2021) · Mass Spectrometry Reviews · doi:10.1002/mas.21741 · Cited by 51
Schoenherr, R. M., Whiteaker, J. R., Zhao, L., Ivey, R. G., Trute, M., Kennedy, J. J., Voytovich, U. J., Yan, P., Lin, C., & Paulovich, A. G. (2012) · PROTEOMICS · doi:10.1002/pmic.201100587 · Cited by 50
“[27] propose that the peptides hydrolyze slowly from the resin.”
BackgroundKaiser, P., Akerboom, T. P. M., Ohlendorf, R., & Reinauer, H. (2010) · Clinical Chemistry · doi:10.1373/clinchem.2009.139477 · Cited by 50
The current status of clinical proteomics and the use of MRM and MRM3for biomarker validation
Lemoine, J., Fortin, T., Salvador, A., Jaffuel, A., Charrier, J., & Choquet‐Kastylevsky, G. (2012) · Expert Review of Molecular Diagnostics · doi:10.1586/erm.12.32 · Cited by 49
Boja, E. S., & Rodriguez, H. (2011) · Annals of Laboratory Medicine · doi:10.3343/kjlm.2011.31.2.61 · Cited by 56
“LDTs have historically been a general subject of FDA enforcement discretion.”
MethodInfluentialKennedy, J. J., Whiteaker, J. R., Schoenherr, R. M., Yan, P., Allison, K. H., Shipley, M., Lerch, M. L., Hoofnagle, A. N., Baird, G. S., & Paulovich, A. G. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00245 · Cited by 48
Self-citation
Metadata
- Authors
- Hoofnagle, A. N., Becker, J. O., Wener, M. H., & Heinecke, J. W.
- Affiliations
- Departments of Laboratory Medicine and
- University of Washington (US)
- Corresponding author
- Hoofnagle, Andrew N
- Venue
- Clinical Chemistry
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-11-01
- Volume
- 54
- Issue
- 11
- Pages
- 1796-1804
- ISSN
- 0009-9147 (ISSN-L)
- 1530-8561
- PMC
- PMC2739673
- OpenAlex
- W2167033601
- Cited by
- 314
- References
- 34
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 12 · 2023: 13 · 2022: 9 · 2021: 10 · 2020: 16 · 2019: 9 · 2018: 16 · 2017: 21 · 2016: 25 · 2015: 15 · 2014: 28 · 2013: 26 · 2012: 31
- FWCI
- 10.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Clinical Chemistry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of Washington
- 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 › Advanced Biosensing Techniques and Applications
- Keywords
- thyroglobulin, tumor markers, immunoassay interference, polyclonal antibodies, tryptic peptides, multiple reaction monitoring, detection limit
- MeSH terms
- Amino Acid Sequence, Chromatography, Affinity, Chromatography, High Pressure Liquid, Humans, Immunoassay, Peptide Fragments, Peptide Mapping, Reference Standards, Sensitivity and Specificity, Thyroglobulin, Reproducibility of Results, Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization, Tandem Mass Spectrometry
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