A proteomics strategy for the identification of multiple sites in sulfur mustard-modified HSA and screening potential biomarkers for retrospective analysis of exposed human plasma.


Journal

Analytical and bioanalytical chemistry
ISSN: 1618-2650
Titre abrégé: Anal Bioanal Chem
Pays: Germany
ID NLM: 101134327

Informations de publication

Date de publication:
Jun 2022
Historique:
received: 02 03 2022
accepted: 06 04 2022
revised: 27 03 2022
pubmed: 29 4 2022
medline: 25 5 2022
entrez: 28 4 2022
Statut: ppublish

Résumé

A major challenge for the unequivocal verification of alleged exposure to sulfur mustard (HD) lies in identifying its multiple modifications on endogenous proteins and utilizing these modified proteins to achieve accurate, sensitive, and rapid detection for retrospective analysis of HD exposure. As the most abundant protein in human plasma, human serum albumin (HSA) can react with many xenobiotics, such as HD, to protect the body from damage. The HSA adducts induced by HD have been used as biomarkers for the verification of HD exposure. In this study, the modification sites on HSA by HD were identified through application of the bottom-up strategy used in proteomics, and 41 modified sites were discovered with seven types of amino acids, of which 3 types were not previously reported. Then, different enzymes, including pepsin, endoproteinase Glu-C, and pronase, were applied to digest HD-HSA to produce adducts with hydroxyethylthioethyl (HETE) groups, which may be used as potential biomarkers for HD exposure. As candidates for retrospective analysis, sixteen adducts were obtained and characterized with ultra-high-pressure liquid chromatography coupled with quadrupole-Orbitrap mass spectrometry (UHPLC-QE Focus MS). These potential biomarkers were evaluated in human plasma that was exposed in vitro to HD and five of its analogues. This study integrated the identification of modification sites through application of the bottom-up strategy of proteomics and screening biomarkers, providing a novel strategy for retrospective detection of the exposure of xenobiotic chemicals.

Identifiants

pubmed: 35478034
doi: 10.1007/s00216-022-04070-y
pii: 10.1007/s00216-022-04070-y
doi:

Substances chimiques

Biomarkers 0
Chemical Warfare Agents 0
Mustard Gas T8KEC9FH9P
Serum Albumin, Human ZIF514RVZR

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

4179-4188

Informations de copyright

© 2022. Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Borak J, Sidell FR. Agents of chemical warfare: sulfur mustard. Ann Emerg Med. 1992;21(3):303–8.
pubmed: 1536492 doi: 10.1016/S0196-0644(05)80892-3
Jan Y-H, Heck DE, Laskin DL, Laskin JD. DNA damage signaling in the cellular responses to mustard vesicants. Toxicol Lett. 2020;326:78–82.
pubmed: 32173488 pmcid: 7224631 doi: 10.1016/j.toxlet.2020.03.008
Khan F, Niaz K, Hassan FI, Abdollahi M. An evidence-based review of the genotoxic and reproductive effects of sulfur mustard (vol 91, pg 1143, 2017). Arch Toxicol. 2018;92(7):2407–8.
pubmed: 29936630 doi: 10.1007/s00204-018-2221-0
Mishra N, Raina K, Agarwal R. Deciphering the role of microRNAs in mustard gas-induced toxicity. Ann NY Acad Sci. 2020.
Ruszkiewicz JA, Buerkle A, Mangerich A. NAD(+) in sulfur mustard toxicity. Toxicol Lett. 2020;324:95–103.
pubmed: 32017979 doi: 10.1016/j.toxlet.2020.01.024
Borna H, Noe SHHQ, Harchegani AB, Talatappe NR, Ghatrehsamani M, Ghanei M, et al. A review on proteomics analysis to reveal biological pathways and predictive proteins in sulfur mustard exposed patients: roles of inflammation and oxidative stress. Inhal Toxicol. 2019;31(1):3–11.
pubmed: 31010353 doi: 10.1080/08958378.2018.1558316
Lixin S, Lipeng PEI, Liming Z, Ju LI, Jian S. Effect of mustard gas at LD_(50) dose on reproductive system of rats. Acad J Second Mil Univ. 2007;28(6):637–9.
Azizi F, Keshavarz A, Roshanzamir F, Nafarabadi M. Reproductive function in men following exposure to chemical warfare with sulphur mustard. Med War. 1995;11(1):34–44.
pubmed: 7731411 doi: 10.1080/07488009508409195
Balali-Mood M, Hefazi M. The pharmacology, toxicology, and medical treatment of sulphur mustard poisoning. Fund Clin Pharmacol. 2005;19(3):297–315.
doi: 10.1111/j.1472-8206.2005.00325.x
Abbas F. Report of the specialists appointed by the Secretary-General of the United Nations to investigate allegations by the Islamic Republic of Iran concerning the use of chemical weapons. Mol Ecol. 1984;15(14):4577–88.
Prescott T. Accidental sulfur mustard exposure from explosive ordnance in a UK military service person. BMJ Mil Health. 2020.
John H, Koller M, Worek F, Thiermann H, Siegert M. Forensic evidence of sulfur mustard exposure in real cases of human poisoning by detection of diverse albumin-derived protein adducts. Arch Toxicol. 2019;93(7):1881–91.
pubmed: 31069408 doi: 10.1007/s00204-019-02461-2
Xia Z. Chemical weapons: defense and destruction. Xia Z, editor. Beijing: Chemical Industry Publishing House; 2014.
Orlova OI, Savel’eva EI, Khlebnikova NS. Methods for the detection of sulfur mustard metabolites in biological materials: an analytical review. J Anal Chem+. 2012;68(1):1–11.
Popiel S, Nawala J, Dziedzic D, Soderstrom M, Vanninen P. Determination of mustard gas hydrolysis products thiodiglycol and thiodiglycol sulfoxide by gas chromatography-tandem mass spectrometry after trifluoroacetylation. Anal Chem. 2014;86(12):5865–72.
pubmed: 24831983 doi: 10.1021/ac500656g
Halme M, Karjalainen M, Kiljunen H, Vanninen P. Development and validation of efficient stable isotope dilution LC-HESI-MS/MS method for the verification of beta-lyase metabolites in human urine after sulfur mustard exposure. J Chromatogr B. 2011;879(13–14):908–14.
doi: 10.1016/j.jchromb.2011.02.043
Bevan MJ, Wogen MT, Lunda MD, Saravia SA. High throughput quantitative analysis of the beta-lyase sulfur mustard metabolite, 1,1 ’-sulfonylbis 2-(methylsulfinyl)ethane in urine via high performance liquid chromatography tandem mass spectrometry. J Chromatogr B. 2017;1051:1–8.
doi: 10.1016/j.jchromb.2017.02.030
Liu CC, Liu SL, Xi HL, Yu HL, Zhou SK, Huang GL, et al. Simultaneous quantification of four metabolites of sulfur mustard in urine samples by ultra-high performance liquid chromatography-tandem mass spectrometry after solid phase extraction. J Chromatogr A. 2017;1492:41–8.
pubmed: 28284764 doi: 10.1016/j.chroma.2017.02.056
Yue LJ, Wei YX, Chen J, Shi HQ, Liu Q, Zhang YJ, et al. Abundance of four sulfur mustard-DNA adducts ex vivo and in vivo revealed by simultaneous quantification in stable isotope dilution-ultrahigh performance liquid chromatography-tandem mass spectrometry. Chem Res Toxicol. 2014;27(4):490–500.
pubmed: 24467472 doi: 10.1021/tx4003403
Zhang YJ, Yue LJ, Nie ZY, Chen J, Guo L, Wu BD, et al. Simultaneous determination of four sulfur mustard-DNA adducts in rabbit urine after dermal exposure by isotope-dilution liquid chromatography-tandem mass spectrometry. J Chromatogr B. 2014;961:29–35.
doi: 10.1016/j.jchromb.2014.04.050
Black RM, Clarke RJ, Harrison JM, Read RW. Biological fate of sulphur mustard: identification of valine and histidine adducts in haemoglobin from casualties of sulphur mustard poisoning. Xenobiotica. 1997;27(5):499–512.
pubmed: 9179990 doi: 10.1080/004982597240460
Noort D, Fidder A, Hulst AG, Woolfitt AR, Ash D, Barr JR. Retrospective detection of exposure to sulfur mustard: improvements on an assay for liquid chromatography-tandem mass spectrometry analysis of albumin/sulfur mustard adducts. J Anal Toxicol. 2004;28(5):333–8.
pubmed: 15239852 doi: 10.1093/jat/28.5.333
Steinritz D, Striepling E, Rudolf K-D, Schroeder-Kraft C, Pueschel K, Hullard-Pulstinger A, et al. Medical documentation, bioanalytical evidence of an accidental human exposure to sulfur mustard and general therapy recommendations. Toxicol Lett. 2016;244:112–20.
pubmed: 26321678 doi: 10.1016/j.toxlet.2015.08.1105
Steinritz D, Lueling R, Siegert M, Herbert J, Mueckter H, Taeger CD, et al. Alkylated epidermal creatine kinase as a biomarker for sulfur mustard exposure: comparison to adducts of albumin and DNA in an in vivo rat study. Arch Toxicol. 2021.
Schmeisser W, Lueling R, Steinritz D, Thiermann H, Rein T, John H. Transthyretin as a target of alkylation and a potential biomarker for sulfur mustard poisoning: electrophoretic and mass spectrometric identification and characterization. Drug Test Anal. 2021.
Lueling R, Singer H, Popp T, John H, Boekhoff I, Thiermann H, et al. Sulfur mustard alkylates steroid hormones and impacts hormone function in vitro. Arch Toxicol. 2019;93(11):3141–52.
doi: 10.1007/s00204-019-02571-x
Grigoryan H, Edmands W, Lu SS, Yano Y, Regazzoni L, Iavarone AT, et al. Adductomics pipeline for untargeted analysis of modifications to Cys34 of human serum albumin. Anal Chem. 2016;88(21):10504–12.
pubmed: 27684351 pmcid: 5555296 doi: 10.1021/acs.analchem.6b02553
Andacht TM, Pantazides BG, Crow BS, Fidder A, Noort D, Thomas JD, et al. Enhanced throughput method for quantification of sulfur mustard adducts to human serum albumin via isotope dilution tandem mass spectrometry. J Anal Toxicol. 2014;38(1):8–15.
pubmed: 24201816 doi: 10.1093/jat/bkt088
Liu C, Liang L, Xiang Y, Yu H, Zhou S, Xi H, et al. An improved method for retrospective quantification of sulfur mustard exposure by detection of its albumin adduct using ultra-high pressure liquid chromatography-tandem mass spectrometry. Anal Bioanal Chem. 2015;407(23):7037–46.
pubmed: 26164303 doi: 10.1007/s00216-015-8842-8
Pantazides BG, Quinones-Gonzalez J, Nazario DMR, Crow BS, Perez JW, Blake TA, et al. A quantitative method to detect human exposure to sulfur and nitrogen mustards via protein adducts. J Chromatogr B. 2019;1121:9–17.
doi: 10.1016/j.jchromb.2019.05.005
Gandor F, Gawlik M, Thiermann H, John H. Evidence of sulfur mustard exposure in human plasma by LC-ESI-MS-MS detection of the albumin-derived alkylated HETE-CP dipeptide and chromatographic investigation of its Cis/Trans isomerism. J Anal Toxicol. 2015;39(4):270–9.
pubmed: 25712440 doi: 10.1093/jat/bkv010
John H, Willoh S, Hoermann P, Siegert M, Vondran A, Thiermann H. Procedures for analysis of dried plasma using microsampling devices to detect sulfur mustard-albumin adducts for verification of poisoning. Anal Chem. 2016;88(17):8787–94.
pubmed: 27482832 doi: 10.1021/acs.analchem.6b02199
Chen B, Yu H-L, Liu S-L, Liu C-C, Liang L-H, Li X-H, et al. A sensitive quantification approach for detection of HETE-CP adduct after benzyl chloroformate derivatization using ultra-high-pressure liquid chromatography tandem mass spectrometry. Anal Bioanal Chem. 2019;411(15):3405–15.
pubmed: 31011788 doi: 10.1007/s00216-019-01820-3
Richter A, Siegert M, Thiermann H, John H. Alkylated albumin-derived dipeptide C(-HETE)P derivatized by propionic anhydride as a biomarker for the verification of poisoning with sulfur mustard. Anal Bioanal Chem. 2021;413(19):4907–16.
pubmed: 34215915 pmcid: 8318952 doi: 10.1007/s00216-021-03454-w
John H, Richter A, Thiermann H. Evidence of sulfur mustard poisoning by detection of the albumin-derived dipeptide biomarker C(-HETE)P after nicotinylation. Drug Test Anal. 2021.
John H, Siegert M, Gandor F, Gawlik M, Kranawetvogl A, Karaghiosoff K, et al. Optimized verification method for detection of an albumin-sulfur mustard adduct at Cys(34) using a hybrid quadrupole time-of-flight tandem mass spectrometer after direct plasma proteolysis. Toxicol Lett. 2016;244:103–11.
pubmed: 26449527 doi: 10.1016/j.toxlet.2015.09.027
Siegert M, Gandor F, Kranawetvogl A, Boerner H, Thiermann H, John H. Methionine(329) in human serum albumin: a novel target for alkylation by sulfur mustard. Drug Test Anal. 2019;11(5):659–68.
pubmed: 30468304 doi: 10.1002/dta.2548
Work Instruction for the Reporting of the Results of the OPCW Biomedical Proficiency Tests. Technical Secretariat of OPCW. 2021.
Final Report of Sixth Official OPCW Biomedical Proficiency Test. Technical Secretariat of OPCW. 2021.
Yang Y, Shu Y-Z, Humphreys WG. Label-free bottom-up proteomic workflow for simultaneously assessing the target specificity of covalent drug candidates and their off-target reactivity to selected proteins. Chem Res Toxicol. 2016;29(1):109–16.
pubmed: 26675335 doi: 10.1021/acs.chemrestox.5b00460
Fu F, Gao R, Zhang R, Zhao P, Lu X, Li L, et al. Verification of soman-related nerve agents via detection of phosphonylated adducts from rabbit albumin in vitro and in vivo. Arch Toxicol. 2019;93(7):1853–63.
pubmed: 31161358 doi: 10.1007/s00204-019-02485-8
Bollineni RC, Hoffmann R, Fedorova M. Identification of protein carbonylation sites by two-dimensional liquid chromatography in combination with MALDI- and ESI-MS. J Proteomics. 2011;74(11):2338–50.
pubmed: 21777707 doi: 10.1016/j.jprot.2011.07.002
Zhao MZ, Wu FL, Xu P. Development of a rapid high-efficiency scalable process for acetylated Sus scrofa cationic trypsin production from Escherichia coli inclusion bodies. Protein Expres Purif. 2015;116:120–6.
doi: 10.1016/j.pep.2015.08.025
Bent HE. THE LABORATORY PREPARATION OF MUSTARD GAS. Science. 1947;106(2755):374–5.
pubmed: 17752824 doi: 10.1126/science.106.2755.374
Williams AH, Woodward FN. New organic sulphur vesicants; analogues of 2:2'-dichlorodiethyl sulphide and 2:2'-di(chloroethylthio)diethyl ether. ether. J Chem Soc. 1948;16:38–42.
Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26(12):1367–1372.
Wisniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods. 2009;6(5):359–62.
pubmed: 19377485 doi: 10.1038/nmeth.1322
Smith JR, Capacio BR, Korte WD, Woolfitt AR, Barr JR. Analysis for plasma protein biomarkers following an accidental human exposure to sulfur mustard. J Anal Toxicol. 2008;32(1):17–24.
pubmed: 18269788 doi: 10.1093/jat/32.1.17
Black RM, Harrison JM, Read RW. Biological fate of sulphur mustard: in vitro alkylation of human haemoglobin by sulphur mustard. Xenobiotica. 1997;27(1):11–32.
pubmed: 9041676 doi: 10.1080/004982597240730
Lawrence RJ, Smith JR, Boyd BL, Capacio BR. Improvements in the methodology of monitoring sulfur mustard exposure by gas chromatography-mass spectrometry analysis of cleaved and derivatized blood protein adducts. J Anal Toxicol. 2008;32(1):31–6.
pubmed: 18269790 doi: 10.1093/jat/32.1.31
Young SA, Capacio BR. Gas chromatography-tandem mass spectrometry verification of sulfur mustard exposure in humans through the conversion of protein adducts to free sulfur mustard. Chem Res Toxicol. 2020;33(7):1941–9.
pubmed: 32567850 doi: 10.1021/acs.chemrestox.0c00134
Chen B, Yu H, Liu S, Liu C, Liang L, Yang Y, et al. Analysis of the sulfur mustard adduct to human hemoglobin in blood samples exposed to trace sulfur mustard by UHPLC-MS/MS. J Chin Mass Spec Soc. 2019;40(4):305–13.
Timperley CM, Black RM, Bird M, Holden I, Mundy JL, Read RW. Hydrolysis and oxidation products of the chemical warfare agents 1,2-bis (2-chloroethyl)thio ethane Q and 2,2 ’-bis(2-chloroethylthio)diethyl ether T. Phosphorus Sulfur Silicon. 2003;178(9):2027–46.
doi: 10.1080/10426500390228710
Interim design assessment for the blue grass chemical agent destruction pilot plan. In: Council NR, editor. Washington, DC: The National Academies Press; 2005.

Auteurs

Bo Chen (B)

State Key Laboratory of NBC Protection for Civilian, Laboratory of Analytical Chemistry, Research Institute of Chemical Defence, Beijing, 102205, People's Republic of China.

Qiaoli Zhang (Q)

State Key Laboratory of NBC Protection for Civilian, Laboratory of Analytical Chemistry, Research Institute of Chemical Defence, Beijing, 102205, People's Republic of China.

Zhe Ren (Z)

School of Chemistry and Chemical Engineering, Nanjing University of Sciences & Technology, Nanjing, 210094, People's Republic of China.

Tao Zhang (T)

State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences (Beijing), Research Unit of Proteomics & Research, Development of New Drug of Chinese Academy of Medical Sciences, Institute of Lifeomics, Beijing, 102206, People's Republic of China.

Huilan Yu (H)

State Key Laboratory of NBC Protection for Civilian, Laboratory of Analytical Chemistry, Research Institute of Chemical Defence, Beijing, 102205, People's Republic of China.

Changcai Liu (C)

State Key Laboratory of NBC Protection for Civilian, Laboratory of Analytical Chemistry, Research Institute of Chemical Defence, Beijing, 102205, People's Republic of China.

Yang Yang (Y)

State Key Laboratory of NBC Protection for Civilian, Laboratory of Analytical Chemistry, Research Institute of Chemical Defence, Beijing, 102205, People's Republic of China.

Ping Xu (P)

State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences (Beijing), Research Unit of Proteomics & Research, Development of New Drug of Chinese Academy of Medical Sciences, Institute of Lifeomics, Beijing, 102206, People's Republic of China. xuping_bprc@126.com.

Shilei Liu (S)

State Key Laboratory of NBC Protection for Civilian, Laboratory of Analytical Chemistry, Research Institute of Chemical Defence, Beijing, 102205, People's Republic of China. liu_shilei@lacricd.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH