Study of metalation of thioredoxin by gold(I) therapeutic compounds using combined liquid chromatography/capillary electrophoresis with inductively coupled plasma/electrospray MS/MS detection.
Au(I) complexes
ESI–MS
ICP-MS
Metal-binding site
Metal-protein adducts
Trx
Journal
Analytical and bioanalytical chemistry
ISSN: 1618-2650
Titre abrégé: Anal Bioanal Chem
Pays: Germany
ID NLM: 101134327
Informations de publication
Date de publication:
20 Jan 2024
20 Jan 2024
Historique:
received:
16
11
2023
accepted:
09
01
2024
revised:
22
12
2023
medline:
20
1
2024
pubmed:
20
1
2024
entrez:
20
1
2024
Statut:
aheadofprint
Résumé
The reactivity of thioredoxin (Trx1) with the Au(I) drug auranofin (AF) and two therapeutic N-heterocyclic carbene (NHC)
Identifiants
pubmed: 38244050
doi: 10.1007/s00216-024-05140-z
pii: 10.1007/s00216-024-05140-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature.
Références
Zhang J, Li X, Han X, Liu R, Fang J. Targeting the thioredoxin system for cancer therapy. Trends Pharmacol Sci. 2017;38(9):794–808. https://doi.org/10.1016/j.tips.2017.06.001 .
doi: 10.1016/j.tips.2017.06.001
pubmed: 28648527
Ghareeb H, Metanis N. The thioredoxin system: a promising target for cancer drug development. Chemistry. 2020;26(45):10175–84. https://doi.org/10.1002/chem.201905792 .
doi: 10.1002/chem.201905792
pubmed: 32097513
Arnér ES, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem. 2000;267(20):6102–9. https://doi.org/10.1046/j.1432-1327.2000.01701.x .
doi: 10.1046/j.1432-1327.2000.01701.x
pubmed: 11012661
Pearson RG. Hard and soft acids and bases—the evolution of a chemical concept. Coord Chem Rev. 1990;100:403–25. https://doi.org/10.1016/0010-8545(90)85016-L .
doi: 10.1016/0010-8545(90)85016-L
Bhabak KP, Bhuyan BJ, Mugesh G. Bioinorganic and medicinal chemistry: aspects of gold(i)-protein complexes. Dalton Trans. 2011;40(10):2099. https://doi.org/10.1039/c0dt01057j .
doi: 10.1039/c0dt01057j
pubmed: 21321730
Zhang X, Selvaraju K, Saei AA, et al. Repurposing of auranofin: thioredoxin reductase remains a primary target of the drug. Biochimie. 2019;162:46–54. https://doi.org/10.1016/j.biochi.2019.03.015 .
doi: 10.1016/j.biochi.2019.03.015
pubmed: 30946948
Pratesi A, Gabbiani C, Ginanneschi M, Messori L. Reactions of medicinally relevant gold compounds with the C-terminal motif of thioredoxin reductase elucidated by MS analysis. Chem Commun. 2010;46(37):7001–3. https://doi.org/10.1039/C0CC01465F .
doi: 10.1039/C0CC01465F
Pratesi A, Gabbiani C, Michelucci E, et al. Insights on the mechanism of thioredoxin reductase inhibition by gold N-heterocyclic carbene compounds using the synthetic linear selenocysteine containing C-terminal peptide hTrxR(488–499): an ESI-MS investigation. J Inorg Biochem. 2014;136:161–9. https://doi.org/10.1016/j.jinorgbio.2014.01.009 .
doi: 10.1016/j.jinorgbio.2014.01.009
pubmed: 24524917
Lamarche J, Alcoceba Álvarez E, Cordeau E, et al. Comparative reactivity of medicinal gold(i) compounds with the cyclic peptide vasopressin and its diselenide analogue. Dalton Trans. 2021;50(47):17487–90. https://doi.org/10.1039/D1DT03470G .
doi: 10.1039/D1DT03470G
pubmed: 34796892
Ronga L, Tolbatov I, Giorgi E, et al. Mechanistic evaluations of the effects of auranofin triethylphosphine replacement with a trimethylphosphite moiety. Inorg Chem. 2023;62(26):10389–96. https://doi.org/10.1021/acs.inorgchem.3c01280 .
doi: 10.1021/acs.inorgchem.3c01280
pubmed: 37342994
pmcid: 10324304
Mora M, Gimeno MC, Visbal R. Recent advances in gold–NHC complexes with biological properties. Chem Soc Rev. 2019;48(2):447–62. https://doi.org/10.1039/C8CS00570B .
doi: 10.1039/C8CS00570B
pubmed: 30474097
Geri A, Massai L, Messori L. Protein metalation by medicinal gold compounds: identification of the main features of the metalation process through ESI MS experiments. Molecules. 2023;28(13). https://doi.org/10.3390/molecules28135196 .
Zoppi C, Massai L, Cirri D, Gabbiani C, Pratesi A, Messori L. Protein metalation by two structurally related gold(I) carbene complexes: an ESI MS study. Inorg Chim Acta. 2021;520: 120297. https://doi.org/10.1016/j.ica.2021.120297 .
doi: 10.1016/j.ica.2021.120297
Augello G, Azzolina A, Rossi F, et al. New insights into the behavior of NHC-gold complexes in cancer cells. Pharmaceutics. 2023;15(2):466. https://doi.org/10.3390/pharmaceutics15020466 .
doi: 10.3390/pharmaceutics15020466
pubmed: 36839788
pmcid: 9963827
Bernabeu de Maria M, Lamarche J, Ronga L, Messori L, Szpunar J, Lobinski R. Selenol (-SeH) as a target for mercury and gold in biological systems: contributions of mass spectrometry and atomic spectroscopy. Coord Chem Rev. 2023;474:214836. https://doi.org/10.1016/j.ccr.2022.214836 .
doi: 10.1016/j.ccr.2022.214836
Holmgren A. Thioredoxin structure and mechanism: conformational changes on oxidation of the active-site sulfhydryls to a disulfide. Structure. 1995;3(3):239–43. https://doi.org/10.1016/S0969-2126(01)00153-8 .
doi: 10.1016/S0969-2126(01)00153-8
pubmed: 7788289
Gimeno MC, Laguna A, Visbal R. N-heterocyclic carbene coinage metal complexes as intense blue-green emitters. Organometallics. 2012;31(20):7146–57. https://doi.org/10.1021/om300571m .
doi: 10.1021/om300571m
Liu W, Bensdorf K, Proetto M, Hagenbach A, Abram U, Gust R. Synthesis, characterization, and in vitro studies of bis[1,3-diethyl-4,5-diarylimidazol-2-ylidene]gold(I/III) complexes. J Med Chem. 2012;55(8):3713–24. https://doi.org/10.1021/jm3000196 .
doi: 10.1021/jm3000196
pubmed: 22424185
Wróblewska AM, Samsonowicz-Górski J, Kamińska E, Drozd M, Matczuk M. Optimization of a CE-ICP-MS/MS method for the investigation of liposome–cisplatin nanosystems and their interactions with transferrin. J Anal At Spectrom. 2022;37(7):1442–9. https://doi.org/10.1039/D1JA00459J .
doi: 10.1039/D1JA00459J
Massai L, Zoppi C, Cirri D, Pratesi A, Messori L. Reactions of medicinal gold(III) compounds with proteins and peptides explored by electrospray ionization mass spectrometry and complementary biophysical methods. Front Chem. 2020;8: 581648. https://doi.org/10.3389/fchem.2020.581648 .
doi: 10.3389/fchem.2020.581648
pubmed: 33195070
pmcid: 7609534
Zoppi C, Messori L, Pratesi A. ESI MS studies highlight the selective interaction of auranofin with protein free thiols. Dalton Trans. 2020;49(18):5906–13. https://doi.org/10.1039/D0DT00283F .
doi: 10.1039/D0DT00283F
pubmed: 32314767
Colotti G, Baiocco P, Fiorillo A, et al. Structural insights into the enzymes of the trypanothione pathway: targets for antileishmaniasis drugs. Future Med Chem. 2013;5(15):1861–75. https://doi.org/10.4155/fmc.13.146 .
doi: 10.4155/fmc.13.146
pubmed: 24144416
Ilari A, Baiocco P, Messori L, et al. A gold-containing drug against parasitic polyamine metabolism: the X-ray structure of trypanothione reductase from Leishmania infantum in complex with auranofin reveals a dual mechanism of enzyme inhibition. Amino Acids. 2012;42(2):803–11. https://doi.org/10.1007/s00726-011-0997-9 .
doi: 10.1007/s00726-011-0997-9
pubmed: 21833767
Lamarche J, Bierla K, Ouerdane L, Szpunar J, Ronga L, Lobinski R. Mass spectrometry insights into interactions of selenoprotein P with auranofin and cisplatin. J Anal At Spectrom. 2022;37(5):1010–22. https://doi.org/10.1039/D2JA00090C .
doi: 10.1039/D2JA00090C
Szpunar J. Advances in analytical methodology for bioinorganic speciation analysis: metallomics, metalloproteomics and heteroatom-tagged proteomics and metabolomics. Analyst. 2005;130(4):442–65. https://doi.org/10.1039/B418265K .
doi: 10.1039/B418265K
pubmed: 15776152
Nguyen TTTN, Østergaard J, Gammelgaard B. A method for studies on interactions between a gold-based drug and plasma proteins based on capillary electrophoresis with inductively coupled plasma mass spectrometry detection. Anal Bioanal Chem. 2015;407(28):8497–503. https://doi.org/10.1007/s00216-015-8997-3 .
doi: 10.1007/s00216-015-8997-3
pubmed: 26329282
Kupiec M, Tomaszewska A, Jakubczak W, Haczyk-Więcek M, Pawlak K. Speciation analysis highlights the interactions of auranofin with the cytoskeleton proteins of lung cancer cells. Pharmaceuticals (Basel). 2022;15(10):1285. https://doi.org/10.3390/ph15101285 .
doi: 10.3390/ph15101285
pubmed: 36297397
Kallis GB, Holmgren A. Differential reactivity of the functional sulfhydryl groups of cysteine-32 and cysteine-35 present in the reduced form of thioredoxin from Escherichia coli. J Biol Chem. 1980;255(21):10261–5. https://doi.org/10.1016/S0021-9258(19)70458-X .
doi: 10.1016/S0021-9258(19)70458-X
pubmed: 7000775
Giglione C, Boularot A, Meinnel T. Protein N-terminal methionine excision. Cell Mol Life Sci. 2004;61(12):1455–74. https://doi.org/10.1007/s00018-004-3466-8 .
doi: 10.1007/s00018-004-3466-8
pubmed: 15197470
Pratesi A, Cirri D, Ciofi L, Messori L. Reactions of auranofin and its pseudohalide derivatives with serum albumin investigated through ESI-Q-TOF MS. Inorg Chem. 2018;57(17):10507–10. https://doi.org/10.1021/acs.inorgchem.8b02177 .
doi: 10.1021/acs.inorgchem.8b02177
pubmed: 30109928
Dupree EJ, Jayathirtha M, Yorkey H, Mihasan M, Petre BA, Darie CC. A critical review of bottom-up proteomics: the good, the bad, and the future of this field. Proteomes. 2020;8(3). https://doi.org/10.3390/proteomes8030014 .
Tolbatov I, Coletti C, Marrone A, Re N. Reactivity of gold(I) monocarbene complexes with protein targets: a theoretical study. Int J Mol Sci. 2019;20(4):820. https://doi.org/10.3390/ijms20040820 .
doi: 10.3390/ijms20040820
pubmed: 30769823
pmcid: 6412330