Histidine-specific Bioconjugation Visible-light-promoted Thioacetal Activation

Overview

Journal Chem Sci

Publisher Royal Society of Chemistry

Specialty Chemistry

Date 2022 Aug 3

PMID 35919717

Authors

Chuan Wan

Yuena Wang

Chenshan Lian

Qi Chang

Yuhao An

Jiean Chen

Jinming Sun

Zhanfeng Hou

Dongyan Yang

Xiaochun Guo

Feng Yin

Rui Wang

Zigang Li

Affiliations

Soon will be listed here.

Abstract

Histidine (His, H) undergoes various post-translational modifications (PTMs) and plays multiple roles in protein interactions and enzyme catalyzed reactions. However, compared with other amino acids such as Lys or Cys, His modification is much less explored. Herein we describe a novel visible-light-driven thioacetal activation reaction which enables facile modification on histidine residues. An efficient addition to histidine imidazole N3 under biocompatible conditions was achieved with an electrophilic thionium intermediate. This method allows chemo-selective modification on peptides and proteins with good conversions and efficient histidine-proteome profiling with cell lysates. 78 histidine containing proteins were for the first time found with significant enrichment, most functioning in metal accumulation in brain related diseases. This facile His modification method greatly expands the chemo-selective toolbox for histidine-targeted protein conjugation and helps to reveal histidine's role in protein functions.

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References

Vinogradova E, Zhang X, Remillard D, Lazar D, Suciu R, Wang Y . An Activity-Guided Map of Electrophile-Cysteine Interactions in Primary Human T Cells. Cell. 2020; 182(4):1009-1026.e29. PMC: 7775622. DOI: 10.1016/j.cell.2020.07.001. View

Kapanidis A, Ebright Y, Ebright R . Site-specific incorporation of fluorescent probes into protein: hexahistidine-tag-mediated fluorescent labeling with (Ni(2+):nitrilotriacetic Acid (n)-fluorochrome conjugates. J Am Chem Soc. 2001; 123(48):12123-5. DOI: 10.1021/ja017074a. View

Speers A, Cravatt B . A tandem orthogonal proteolysis strategy for high-content chemical proteomics. J Am Chem Soc. 2005; 127(28):10018-9. PMC: 1538546. DOI: 10.1021/ja0532842. View

Lin S, Yang X, Jia S, Weeks A, Hornsby M, Lee P . Redox-based reagents for chemoselective methionine bioconjugation. Science. 2017; 355(6325):597-602. PMC: 5827972. DOI: 10.1126/science.aal3316. View

Ashburner M, Ball C, Blake J, Botstein D, Butler H, Cherry J . Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25(1):25-9. PMC: 3037419. DOI: 10.1038/75556. View

Gutteridge A, Thornton J . Understanding nature's catalytic toolkit. Trends Biochem Sci. 2005; 30(11):622-9. DOI: 10.1016/j.tibs.2005.09.006. View

Chen D, Feng Q, Yang Y, Cai X, Wang F, Huang S . Metal-free O-H/C-H difunctionalization of phenols by -hydroxyarylsulfonium salts in water. Chem Sci. 2017; 8(2):1601-1606. PMC: 5361865. DOI: 10.1039/c6sc04504a. View

Ma N, Hu J, Zhang Z, Liu W, Huang M, Fan Y . 2-Azirine-Based Reagents for Chemoselective Bioconjugation at Carboxyl Residues Inside Live Cells. J Am Chem Soc. 2020; 142(13):6051-6059. DOI: 10.1021/jacs.9b12116. View

Vantourout J, Adusumalli S, Knouse K, Flood D, Ramirez A, Padial N . Serine-Selective Bioconjugation. J Am Chem Soc. 2020; 142(41):17236-17242. PMC: 8350984. DOI: 10.1021/jacs.0c05595. View

10.

Lorenzi M, Puppo C, Lebrun R, Lignon S, Roubaud V, Martinho M . Tyrosine-targeted spin labeling and EPR spectroscopy: an alternative strategy for studying structural transitions in proteins. Angew Chem Int Ed Engl. 2011; 50(39):9108-11. DOI: 10.1002/anie.201102539. View

11.

Jia S, He D, Chang C . Bioinspired Thiophosphorodichloridate Reagents for Chemoselective Histidine Bioconjugation. J Am Chem Soc. 2019; 141(18):7294-7301. PMC: 6996876. DOI: 10.1021/jacs.8b11912. View

12.

Ban H, Gavrilyuk J, Barbas 3rd C . Tyrosine bioconjugation through aqueous ene-type reactions: a click-like reaction for tyrosine. J Am Chem Soc. 2010; 132(5):1523-5. DOI: 10.1021/ja909062q. View

13.

Xie Y, Du S, Liu Z, Liu M, Xu Z, Wang X . Chemical Biology Tools for Protein Lysine Acylation. Angew Chem Int Ed Engl. 2022; 61(21):e202200303. DOI: 10.1002/anie.202200303. View

14.

Agostini F, Voller J, Koksch B, Acevedo-Rocha C, Kubyshkin V, Budisa N . Biocatalysis with Unnatural Amino Acids: Enzymology Meets Xenobiology. Angew Chem Int Ed Engl. 2017; 56(33):9680-9703. DOI: 10.1002/anie.201610129. View

15.

Li J, Chen J, Sang R, Ham W, Plutschack M, Berger F . Photoredox catalysis with aryl sulfonium salts enables site-selective late-stage fluorination. Nat Chem. 2019; 12(1):56-62. DOI: 10.1038/s41557-019-0353-3. View

16.

Koniev O, Wagner A . Developments and recent advancements in the field of endogenous amino acid selective bond forming reactions for bioconjugation. Chem Soc Rev. 2015; 44(15):5495-551. DOI: 10.1039/c5cs00048c. View

17.

Jarrige L, Levitre G, Masson G . Visible-Light Photoredox-Catalyzed Coupling Reaction of Azoles with α-Carbamoyl Sulfides. J Org Chem. 2016; 81(16):7230-6. DOI: 10.1021/acs.joc.6b01108. View

18.

Yanagi T, Otsuka S, Kasuga Y, Fujimoto K, Murakami K, Nogi K . Metal-Free Approach to Biaryls from Phenols and Aryl Sulfoxides by Temporarily Sulfur-Tethered Regioselective C-H/C-H Coupling. J Am Chem Soc. 2016; 138(44):14582-14585. DOI: 10.1021/jacs.6b10278. View

19.

Antos J, Francis M . Selective tryptophan modification with rhodium carbenoids in aqueous solution. J Am Chem Soc. 2004; 126(33):10256-7. DOI: 10.1021/ja047272c. View

20.

Lanzi M, Merad J, Boyarskaya D, Maestri G, Allain C, Masson G . Visible-Light-Triggered C-C and C-N Bond Formation by C-S Bond Cleavage of Benzylic Thioethers. Org Lett. 2018; 20(17):5247-5250. DOI: 10.1021/acs.orglett.8b02196. View