An NMR-Based Biosensor to Measure Stereospecific Methionine Sulfoxide Reductase Activities in Vitro and in Vivo*.
diastereoisomers
in-cell NMR
methionine oxidation
methionine sulfoxide reductase
zebrafish
Journal
Chemistry (Weinheim an der Bergstrasse, Germany)
ISSN: 1521-3765
Titre abrégé: Chemistry
Pays: Germany
ID NLM: 9513783
Informations de publication
Date de publication:
20 Nov 2020
20 Nov 2020
Historique:
received:
01
06
2020
pubmed:
6
6
2020
medline:
17
2
2021
entrez:
6
6
2020
Statut:
ppublish
Résumé
Oxidation of protein methionines to methionine-sulfoxides (MetOx) is associated with several age-related diseases. In healthy cells, MetOx is reduced to methionine by two families of conserved methionine sulfoxide reductase enzymes, MSRA and MSRB that specifically target the S- or R-diastereoisomers of methionine-sulfoxides, respectively. To directly interrogate MSRA and MSRB functions in cellular settings, we developed an NMR-based biosensor that we call CarMetOx to simultaneously measure both enzyme activities in single reaction setups. We demonstrate the suitability of our strategy to delineate MSR functions in complex biological environments, including cell lysates and live zebrafish embryos. Thereby, we establish differences in substrate specificities between prokaryotic and eukaryotic MSRs and introduce CarMetOx as a highly sensitive tool for studying therapeutic targets of oxidative stress-related human diseases and redox regulated signaling pathways.
Identifiants
pubmed: 32501570
doi: 10.1002/chem.202002645
doi:
Substances chimiques
Methionine
AE28F7PNPL
Methionine Sulfoxide Reductases
EC 1.8.4.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
14838-14843Informations de copyright
© 2020 Wiley-VCH GmbH.
Références
D. B. Oien, J. Moskovitz, Biochim. Biophys. Acta, Mol. Basis Dis. 2019, 1865, 1756-1762.
B. C. Lee, V. N. Gladyshev, Free Radical Biol. Med. 2011, 50, 221-227.
X. H. Zhang, H. Weissbach, Biol. Rev. Camb. Philos. Soc. 2008, 83, 249-257.
F. Etienne, D. Spector, N. Brot, H. Weissbach, Biochem. Biophys. Res. Commun. 2003, 300, 378-382;
D. T. Le, B. C. Lee, S. M. Marino, Y. Zhang, D. E. Fomenko, A. Kaya, E. Hacioglu, G. H. Kwak, A. Koc, H. Y. Kim, V. N. Gladyshev, J. Biol. Chem. 2009, 284, 4354-4364.
A. Gennaris, B. Ezraty, C. Henry, R. Agrebi, A. Vergnes, E. Oheix, J. Bos, P. Leverrier, L. Espinosa, J. Szewczyk, D. Vertommen, O. Iranzo, J. F. Collet, F. Barras, Nature 2015, 528, 409-412;
N. Makukhin, V. Havelka, E. Polachova, P. Rampirova, V. Tarallo, K. Strisovsky, J. Misek, FEBS J. 2019, 286, 4024-4035.
J. M. Lim, G. Kim, R. L. Levine, Neurochem. Res. 2019, 44, 247-257.
B. J. He, M. L. Joiner, M. V. Singh, E. D. Luczak, P. D. Swaminathan, O. M. Koval, W. Kutschke, C. Allamargot, J. Yang, X. Guan, K. Zimmerman, I. M. Grumbach, R. M. Weiss, D. R. Spitz, C. D. Sigmund, W. M. Blankesteijn, S. Heymans, P. J. Mohler, M. E. Anderson, Nat. Med. 2011, 17, 1610-1618.
F. J. Veredas, F. R. Canton, J. C. Aledo, Sci. Rep. 2017, 7, 40403.
A. Drazic, H. Miura, J. Peschek, Y. Le, N. C. Bach, T. Kriehuber, J. Winter, Proc. Natl. Acad. Sci. USA 2013, 110, 9493-9498.
M. Kato, Y. S. Yang, B. M. Sutter, Y. Wang, S. L. McKnight, B. P. Tu, Cell 2019, 177, 711-721 e718.
B. C. Lee, Z. Peterfi, F. W. Hoffmann, R. E. Moore, A. Kaya, A. Avanesov, L. Tarrago, Y. Zhou, E. Weerapana, D. E. Fomenko, P. R. Hoffmann, V. N. Gladyshev, Mol. Cell 2013, 51, 397-404;
B. Manta, V. N. Gladyshev, Free Radic. Biol. Med. 2017, 109, 141-155.
J. R. Erickson, M. L. Joiner, X. Guan, W. Kutschke, J. Yang, C. V. Oddis, R. K. Bartlett, J. S. Lowe, S. E. O'Donnell, N. Ayki nBurns, M. C. Zimmerman, K. Zimmerman, A. J. Ham, R. M. Weiss, D. R. Spitz, M. A. Shea, R. J. Colbran, P. J. Mohler, M. E. Anderson, Cell 2008, 133, 462-474.
C. Achilli, A. Ciana, G. Minetti, Biofactors 2015, 41, 135-152.
N. Makukhin, V. Tretyachenko, J. Moskovitz, J. Misek, Angew. Chem. Int. Ed. 2016, 55, 12727-12730;
Angew. Chem. 2016, 128, 12919-12922;
L. Zhang, S. Peng, J. Sun, J. Yao, J. Kang, Y. Hu, J. Fang, Chem. Sci. 2017, 8, 2966-2972.
L. Tarrago, Z. Peterfi, B. C. Lee, T. Michel, V. N. Gladyshev, Nat. Chem. Biol. 2015, 11, 332-338.
A. Binolfi, A. Limatola, S. Verzini, J. Kosten, F. X. Theillet, H. M. Rose, B. Bekei, M. Stuiver, M. van Rossum, P. Selenko, Nat. Commun. 2016, 7, 10251.
R. Hänsel, L. M. Luh, I. Corbeski, L. Trantirek, V. Dotsch, Angew. Chem. Int. Ed. 2014, 53, 10300-10314;
Angew. Chem. 2014, 126, 10466-10480;
N. Nishida, Y. Ito, I. Shimada, Biochim. Biophys. Acta Gen. Subj. 2020, 1864, 129364;
G. Siegal, P. Selenko, J. Magn. Reson. 2019, 306, 202-212.
M. J. Davies, Biochem. J. 2016, 473, 805-825.
M. J. Smith, C. B. Marshall, F. X. Theillet, A. Binolfi, P. Selenko, M. Ikura, Curr. Opin. Struct. Biol. 2015, 32, 39-47.
G. H. Kwak, K. Y. Hwang, H. Y. Kim, Arch. Biochem. Biophys. 2012, 527, 1-5.
A. Limatola, C. Eichmann, R. S. Jacob, G. Ben-Nissan, M. Sharon, A. Binolfi, P. Selenko, Proteomics 2018, 18, 1800056;
F. X. Theillet, A. Binolfi, B. Bekei, A. Martorana, H. M. Rose, M. Stuiver, S. Verzini, D. Lorenz, M. van Rossum, D. Goldfarb, P. Selenko, Nature 2016, 530, 45-50.
A. Binolfi, G. R. Lamberto, R. Duran, L. Quintanar, C. W. Bertoncini, J. M. Souza, C. Cervenansky, M. Zweckstetter, C. Griesinger, C. O. Fernandez, J. Am. Chem. Soc. 2008, 130, 11801-11812.
P. Schanda, E. Kupce, B. Brutscher, J. Biomol. NMR 2005, 33, 199-211.
L. Tarrago, A. Kaya, E. Weerapana, S. M. Marino, V. N. Gladyshev, J. Biol. Chem. 2012, 287, 24448-24459.
A. Kaya, B. C. Lee, V. N. Gladyshev, Antioxid. Redox Signaling 2015, 23, 814-822.
B. C. Lee, D. T. Le, V. N. Gladyshev, J. Biol. Chem. 2008, 283, 28361-28369.
P. Selenko, D. P. Frueh, S. J. Elsaesser, W. Haas, S. P. Gygi, G. Wagner, Nat. Struct. Mol. Biol. 2008, 15, 321-329;
T. Müntener, D. Haussinger, P. Selenko, F. X. Theillet, J. Phys. Chem. Lett. 2016, 7, 2821-2825.
M. Bastawrous, A. Jenne, M. Tabatabaei Anaraki, A. J. Simpson, Metabolites 2018, 8, 35;
D. Lane, T. E. Skinner, N. I. Gershenzon, W. Bermel, R. Soong, R. Dutta Majumdar, Y. Liaghati Mobarhan, S. Schmidt, H. Heumann, M. Monette, M. J. Simpson, A. J. Simpson, J. Biomol. NMR 2019, 73, 31-42.
R. Fuentes, J. Fernandez, Dev. Dyn. 2010, 239, 2172-2189.
V. K. Singh, K. Singh, K. Baum, Antioxidants (Basel) 2018, 7, 128.