Automating data analysis for hydrogen/deuterium exchange mass spectrometry using data-independent acquisition methodology.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
11 Mar 2024
11 Mar 2024
Historique:
received:
16
08
2023
accepted:
22
02
2024
medline:
12
3
2024
pubmed:
12
3
2024
entrez:
12
3
2024
Statut:
epublish
Résumé
We present a hydrogen/deuterium exchange workflow coupled to tandem mass spectrometry (HX-MS
Identifiants
pubmed: 38467655
doi: 10.1038/s41467-024-46610-3
pii: 10.1038/s41467-024-46610-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2200Subventions
Organisme : Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (Conseil de Recherches en Sciences Naturelles et en Génie du Canada)
ID : RGPIN 2017-04879
Organisme : Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (Conseil de Recherches en Sciences Naturelles et en Génie du Canada)
ID : RGPIN 2019-04829
Informations de copyright
© 2024. The Author(s).
Références
Englander, S. W. & Mayne, L. The nature of protein folding pathways. Proc. Natl Acad. Sci. USA 111, 15873–15880 (2014).
pubmed: 25326421
pmcid: 4234557
doi: 10.1073/pnas.1411798111
Marciano, D. P., Dharmarajan, V. & Griffin, P. R. HDX-MS guided drug discovery: small molecules and biopharmaceuticals. Curr. Opin. Struct. Biol. 28, 105–111 (2014).
pubmed: 25179005
doi: 10.1016/j.sbi.2014.08.007
Zhu, S. et al. Epitope screening using Hydrogen/Deuterium Exchange Mass Spectrometry (HDX-MS): an accelerated workflow for evaluation of lead monoclonal antibodies. Biotechnol. J. 17, e2100358 (2022).
pubmed: 34747565
doi: 10.1002/biot.202100358
James, E. I., Murphree, T. A., Vorauer, C., Engen, J. R. & Guttman, M. Advances in hydrogen/deuterium exchange mass spectrometry and the pursuit of challenging biological systems. Chem. Rev. 122, 7562–7623 (2022).
pubmed: 34493042
doi: 10.1021/acs.chemrev.1c00279
Sun, H. et al. Research advances in hydrogen–deuterium exchange mass spectrometry for protein epitope mapping. Anal. Bioanal. Chem. 413, 2345–2359 (2021).
pubmed: 33404742
doi: 10.1007/s00216-020-03091-9
Engen, J. R., Botzanowski, T., Peterle, D., Georgescauld, F. & Wales, T. E. Developments in hydrogen/deuterium exchange mass spectrometry. Anal. Chem. 93, 567–582 (2021).
pubmed: 33112590
doi: 10.1021/acs.analchem.0c04281
Kaltashov, I. A., Bobst, C. E., Pawlowski, J. & Wang, G. Mass spectrometry-based methods in characterization of the higher order structure of protein therapeutics. J. Pharm. Biomed. Anal. 184, 113169 (2020).
pubmed: 32092629
pmcid: 7162711
doi: 10.1016/j.jpba.2020.113169
Trabjerg, E., Nazari, Z. E. & Rand, K. D. Conformational analysis of complex protein states by hydrogen/deuterium exchange mass spectrometry (HDX-MS): Challenges and emerging solutions. TrAC Trends Anal. Chem. 106, 125–138 (2018).
doi: 10.1016/j.trac.2018.06.008
Deng, B., Lento, C. & Wilson, D. J. Hydrogen deuterium exchange mass spectrometry in biopharmaceutical discovery and development – a review. Anal. Chim. Acta https://doi.org/10.1016/j.aca.2016.08.006 . (2016)
Balasubramaniam, D. & Komives, E. A. Hydrogen-exchange mass spectrometry for the study of intrinsic disorder in proteins. Biochim. Biophys. Acta - Proteins Proteom. 1834, 1202–1209 (2013).
doi: 10.1016/j.bbapap.2012.10.009
Percy, A. J., Rey, M., Burns, K. M. & Schriemer, D. C. Probing protein interactions with hydrogen/deuterium exchange and mass spectrometry-a review. Anal. Chim. Acta 721, 7–21 (2012).
pubmed: 22405295
doi: 10.1016/j.aca.2012.01.037
Konermann, L., Pan, J. & Liu, Y. H. Hydrogen exchange mass spectrometry for studying protein structure and dynamics. Chem. Soc. Rev. 40, 1224–1234 (2011).
pubmed: 21173980
doi: 10.1039/C0CS00113A
Masson, G. R. et al. Recommendations for performing, interpreting and reporting hydrogen deuterium exchange mass spectrometry (HDX-MS) experiments. Nat. Methods https://doi.org/10.1038/s41592-019-0459-y . (2019)
Khakinejad, M. et al. Combining ion mobility spectrometry with hydrogen-deuterium exchange and top-down MS for peptide ion structure analysis. J. Am. Soc. Mass Spectrom. 25, 2103–2115 (2014).
pubmed: 25267084
doi: 10.1007/s13361-014-0990-0
Cryar, A., Groves, K. & Quaglia, M. Online Hydrogen-Deuterium Exchange Traveling Wave Ion Mobility Mass Spectrometry (HDX-IM-MS): a systematic evaluation. J. Am. Soc. Mass Spectrom. 28, 1192–1202 (2017).
pubmed: 28374315
pmcid: 5438439
doi: 10.1007/s13361-017-1633-z
Sheff, J. G., Hepburn, M., Yu, Y., Lees-Miller, S. P. & Schriemer, D. C. Nanospray HX-MS configuration for structural interrogation of large protein systems. Analyst 142, 904–910 (2017).
pubmed: 28154854
doi: 10.1039/C6AN02707E
Espada, A. et al. A decoupled automation platform for hydrogen/deuterium exchange mass spectrometry experiments. J. Am. Soc. Mass Spectrom. 30, 2580–2583 (2019).
pubmed: 31724102
doi: 10.1007/s13361-019-02331-2
Cummins, D. J. et al. Two-site evaluation of the repeatability and precision of an automated dual-column hydrogen/deuterium exchange mass spectrometry platform. Anal. Chem. 88, 6607–6614 (2016).
pubmed: 27224086
doi: 10.1021/acs.analchem.6b01650
Watson, M. J. et al. Simple platform for automating decoupled LC-MS analysis of hydrogen/deuterium exchange samples. J. Am. Soc. Mass Spectrom. 32, 597–600 (2021).
pubmed: 33284630
doi: 10.1021/jasms.0c00341
Wales, T. E., Fadgen, K. E., Eggertson, M. J. & Engen, J. R. Subzero Celsius separations in three-zone temperature controlled hydrogen deuterium exchange mass spectrometry. J. Chromatogr. A 1523, 275–282 (2017).
pubmed: 28596009
pmcid: 5675777
doi: 10.1016/j.chroma.2017.05.067
Lau, A. M., Claesen, J., Hansen, K. & Politis, A. Deuteros 2.0: peptide-level significance testing of data from hydrogen deuterium exchange mass spectrometry. Bioinformatics 37, 270–272 (2021).
pubmed: 32722756
pmcid: 8055227
doi: 10.1093/bioinformatics/btaa677
Lumpkin, R. J. & Komives, E. A. DECA, a comprehensive, automatic post-processing program for HDX-MS data. Mol. Cell. Proteom. 18, 2516–2523 (2019).
doi: 10.1074/mcp.TIR119.001731
Kan, Z.-Y., Ye, X., Skinner, J. J., Mayne, L. & Englander, S. W. ExMS2: an integrated solution for hydrogen-deuterium exchange mass spectrometry data analysis. Anal. Chem. 91, 7474–7481 (2019).
pubmed: 31082210
doi: 10.1021/acs.analchem.9b01682
Bouyssié, D. et al. HDX-Viewer: interactive 3D visualization of hydrogen–deuterium exchange data. Bioinformatics 35, 5331–5333 (2019).
pubmed: 31287496
pmcid: 6954641
doi: 10.1093/bioinformatics/btz550
Na, S., Lee, J.-J., Joo, J. W. J., Lee, K.-J. & Paek, E. deMix: decoding deuterated distributions from heterogeneous protein states via HDX-MS. Sci. Rep. 9, 3176 (2019).
pubmed: 30816214
pmcid: 6395696
doi: 10.1038/s41598-019-39512-8
Seetaloo, N., Kish, M. & Phillips, J. J. HDfleX: software for flexible high structural resolution of hydrogen/deuterium-exchange mass spectrometry data. Anal. Chem. https://doi.org/10.1021/acs.analchem.1c05339 . (2022)
Cupp-Sutton, K. A. et al. The deuterium calculator: an open-source tool for hydrogen–deuterium exchange mass spectrometry analysis. J. Proteome Res. https://doi.org/10.1021/acs.jproteome.2c00558 . (2023)
Rand, K. D., Zehl, M. & Jørgensen, T. J. D. Measuring the hydrogen/deuterium exchange of proteins at high spatial resolution by mass spectrometry: overcoming gas-phase hydrogen/deuterium scrambling. Acc. Chem. Res. 47, 3018–3027 (2014).
pubmed: 25171396
doi: 10.1021/ar500194w
Percy, A. J., Slysz, G. W. & Schriemer, D. C. Surrogate H/D detection strategy for protein conformational analysis using MS/MS data. Anal. Chem. 81, 7900–7907 (2009).
pubmed: 19681596
doi: 10.1021/ac901148u
Rand, K. D. & Jørgensen, T. J. D. Development of a peptide probe for the occurrence of hydrogen (1H/2H) scrambling upon gas-phase fragmentation. Anal. Chem. 79, 8686–8693 (2007).
pubmed: 17935303
doi: 10.1021/ac0710782
Johnson, R. S., Krylov, D. & Walsh, K. A. Proton mobility within electrosprayed peptide ions. J. Mass Spectrom. 30, 386–387 (1995).
doi: 10.1002/jms.1190300224
Wollenberg, D. T. W. et al. Avoiding H/D scrambling with minimal ion transmission loss for HDX-MS/MS-ETD analysis on a high-resolution Q-TOF mass spectrometer. Anal. Chem. 92, 7453–7461 (2020).
pubmed: 32427467
doi: 10.1021/acs.analchem.9b05208
Rand, K. D., Adams, C. M., Zubarev, R. A. & Jørgensen, T. J. D. Electron capture dissociation proceeds with a low degree of intramolecular migration of peptide amide hydrogens. J. Am. Chem. Soc. 130, 1341–1349 (2008).
pubmed: 18171065
doi: 10.1021/ja076448i
Zehl, M., Rand, K. D., Jensen, O. N. & Jorgensen, T. J. D. Electron transfer dissociation facilitates the measurement of deuterium incorporation into selectively labeled peptides with single residue resolution. J. Am. Chem. Soc. 130, 17453–17459 (2008).
pubmed: 19035774
doi: 10.1021/ja805573h
Burns, K. M., Sarpe, V., Wagenbach, M., Wordeman, L. & Schriemer, D. C. HX-MS2 for high performance conformational analysis of complex protein states. Protein Sci. https://doi.org/10.1002/pro.2707 . (2015)
Slysz, G. W., Percy, A. J. & Schriemer, D. C. Restraining expansion of the peak envelope in H/D exchange-MS and its application in detecting perturbations of protein structure/dynamics. Anal. Chem. 80, 7004–7011 (2008).
pubmed: 18707134
doi: 10.1021/ac800897q
Raval, S. et al. Improving spectral validation rates in hydrogen-deuterium exchange data analysis. Anal. Chem. 93, 4246–4254 (2021).
pubmed: 33592142
doi: 10.1021/acs.analchem.0c05045
Delatour, T., Mottier, P. & Gremaud, E. Limits of suspicion, recognition and confirmation as concepts that account for the confirmation transitions at the detection limit for quantification by liquid chromatography-tandem mass spectrometry. J. Chromatogr. A 1169, 103–110 (2007).
pubmed: 17880986
doi: 10.1016/j.chroma.2007.08.065
Syed, A. et al. Novobiocin blocks nucleic acid binding to Polθ and inhibits stimulation of its ATPase activity. Nucleic Acids Res. 51, 9920–9937 (2023).
pubmed: 37665033
pmcid: 10570058
doi: 10.1093/nar/gkad727
Chen, X. S. & Pomerantz, R. T. DNA polymerase θ: a cancer drug target with reverse transcriptase activity. Genes (Basel) 12, 1146 (2021).
pubmed: 34440316
doi: 10.3390/genes12081146
Zhou, J. et al. A first-in-class polymerase theta inhibitor selectively targets homologous-recombination-deficient tumors. Nat. Cancer 2, 598–610 (2021).
pubmed: 34179826
pmcid: 8224818
doi: 10.1038/s43018-021-00203-x
Liang, S. et al. Structural insights into inhibitor regulation of the DNA repair protein DNA-PKcs. Nature 601, 643–648 (2022).
pubmed: 34987222
pmcid: 8791830
doi: 10.1038/s41586-021-04274-9
Chen, S., Lees-Miller, J. P., He, Y. & Lees-Miller, S. P. Structural insights into the role of DNA-PK as a master regulator in NHEJ. Genome Instab. Dis. 2, 195 (2021).
pubmed: 34723130
pmcid: 8549938
doi: 10.1007/s42764-021-00047-w
Fok, J. H. L. et al. AZD7648 is a potent and selective DNA-PK inhibitor that enhances radiation, chemotherapy and olaparib activity. Nat. Commun. 10, 5065 (2019).
pubmed: 31699977
pmcid: 6838110
doi: 10.1038/s41467-019-12836-9
Hepburn, M. et al. The active DNA-PK holoenzyme occupies a tensed state in a staggered synaptic complex. Structure 29, 467–478.e6 (2021).
pubmed: 33412091
pmcid: 8675206
doi: 10.1016/j.str.2020.12.006
Kelstrup, C. D., Young, C., Lavallee, R., Nielsen, M. L. & Olsen, J. V. Optimized fast and sensitive acquisition methods for shotgun proteomics on a quadrupole orbitrap mass spectrometer. J. Proteome Res. 11, 3487–3497 (2012).
pubmed: 22537090
doi: 10.1021/pr3000249
Newman, J. A., Cooper, C. D. O., Aitkenhead, H. & Gileadi, O. Structure of the helicase domain of DNA polymerase theta reveals a possible role in the microhomology-mediated end-joining pathway. Structure 23, 2319–2330 (2015).
pubmed: 26636256
pmcid: 4671958
doi: 10.1016/j.str.2015.10.014
Ding, Q. et al. Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. Mol. Cell. Biol. 23, 5836–5848 (2003).
pubmed: 12897153
pmcid: 166339
doi: 10.1128/MCB.23.16.5836-5848.2003
Rey, M. et al. Mass spec studio for integrative structural biology. Structure 22, 1538–1548 (2014).
pubmed: 25242457
pmcid: 4391204
doi: 10.1016/j.str.2014.08.013
Kavan, D. & Man, P. MSTools—Web based application for visualization and presentation of HXMS data. Int. J. Mass Spectrom. 302, 53–58 (2011).
doi: 10.1016/j.ijms.2010.07.030
Deutsch, E. W. et al. The ProteomeXchange consortium at 10 years: 2023 update. Nucleic Acids Res. 51, D1539–D1548 (2023).
pubmed: 36370099
doi: 10.1093/nar/gkac1040