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An Azidoribose Probe to Track Ketoamine Adducts in Histone Ribose Glycation

  • Igor Maksimovic
    Igor Maksimovic
    Tri-Institutional PhD Program in Chemical Biology, New York, New York 10065, United States
    Chemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York 10065, United States
  • Qingfei Zheng
    Qingfei Zheng
    Chemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York 10065, United States
  • Marissa N. Trujillo
    Marissa N. Trujillo
    Department of Pharmaocology and Toxicology, College of Pharmacy, University of Arizona, Tucson, Arizona 85721, United States
  • James J. Galligan
    James J. Galligan
    Department of Pharmaocology and Toxicology, College of Pharmacy, University of Arizona, Tucson, Arizona 85721, United States
  • , and 
  • Yael David*
    Yael David
    Tri-Institutional PhD Program in Chemical Biology, New York, New York 10065, United States
    Chemical Biology Program, Memorial Sloan Kettering Cancer Center, New York, New York 10065, United States
    Department of Pharmacology, Weill Cornell Medicine, New York, New York 10065, United States
    Department of Physiology, Biophysics and Systems Biology, Weill Cornell Medicine, New York, New York 10065, United States
    *[email protected]
    More by Yael David
Cite this: J. Am. Chem. Soc. 2020, 142, 22, 9999–10007
Publication Date (Web):May 10, 2020
https://doi.org/10.1021/jacs.0c01325
Copyright © 2020 American Chemical Society

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    Abstract

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    Reactive cellular metabolites can modify macromolecules and form adducts known as nonenzymatic covalent modifications (NECMs). The dissection of the mechanisms, regulation, and consequences of NECMs, such as glycation, has been challenging due to the complex and often ambiguous nature of the adducts formed. Specific chemical tools are required to directly track the formation of these modifications on key targets in order to uncover their underlying physiological importance. Here, we present the novel chemoenzymatic synthesis of an active azido-modified ribose analog, 5-azidoribose (5-AR), as well as the synthesis of an inactive control derivative, 1-azidoribose (1-AR), and their application toward understanding protein ribose-glycation in vitro and in cellulo. With these new probes we found that, similar to methylglyoxal (MGO) glycation, ribose glycation specifically accumulates on histones. In addition to fluorescent labeling, we demonstrate the utility of the probe in enriching modified targets, which were identified by label-free quantitative proteomics and high-resolution MS/MS workflows. Finally, we establish that the known oncoprotein and hexose deglycase, fructosamine 3-kinase (FN3K), recognizes and facilitates the removal of 5-AR glycation adducts in live cells, supporting the dynamic regulation of ribose glycation as well as validating the probe as a new platform to monitor FN3K activity. Altogether, we demonstrate this probe’s utilities to uncover ribose-glycation and deglycation events as well as track FN3K activity toward establishing its potential as a new cancer vulnerability.

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/jacs.0c01325. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via the PRIDE repository with the dataset identifier PXD019204. (61)

    • Complete experimental procedures and characterization data for all new compounds (PDF)

    • Raw proteomics dataset S1 (XLSX)

    • Raw proteomics dataset S2 (XLSX)

    • Raw proteomics dataset S3 (XLSX)

    • Gene list S1 (XLSX)

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    Cited By

    This article is cited by 18 publications.

    1. Devin M. Ray, Erin Q. Jennings, Igor Maksimovic, Xander Chai, James J. Galligan, Yael David, Qingfei Zheng. Chemical Labeling and Enrichment of Histone Glyoxal Adducts. ACS Chemical Biology 2022, 17 (4) , 756-761. https://doi.org/10.1021/acschembio.1c00864
    2. Nichole J. Pedowitz, Emma G. Jackson, Justin M. Overhulse, Charles E. McKenna, Jennifer J. Kohler, Matthew R. Pratt. Anomeric Fatty Acid Functionalization Prevents Nonenzymatic S-Glycosylation by Monosaccharide Metabolic Chemical Reporters. ACS Chemical Biology 2021, 16 (10) , 1924-1929. https://doi.org/10.1021/acschembio.1c00470
    3. Nan Zhang, Jinghua Wu, Qingfei Zheng. Chemical proteomics approaches for protein post-translational modification studies. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2024, 14 , 141017. https://doi.org/10.1016/j.bbapap.2024.141017
    4. Domenica Scumaci, Qingfei Zheng. Epigenetic meets metabolism: novel vulnerabilities to fight cancer. Cell Communication and Signaling 2023, 21 (1) https://doi.org/10.1186/s12964-023-01253-7
    5. Naoya Kitamura, James J. Galligan. A global view of the human post-translational modification landscape. Biochemical Journal 2023, 480 (16) , 1241-1265. https://doi.org/10.1042/BCJ20220251
    6. Marissa N. Trujillo, James J. Galligan. Reconsidering the role of protein glycation in disease. Nature Chemical Biology 2023, 19 (8) , 922-927. https://doi.org/10.1038/s41589-023-01382-7
    7. Zhentao Shao, Yingdi Zhu, Juan Li. Bioorthogonal Probes for Analyzing Non‐Enzymatic Post‐Translational Modifications. ChemBioChem 2023, 24 (9) https://doi.org/10.1002/cbic.202200763
    8. Anna Knörlein, Yang Xiao, Yael David. Leveraging histone glycation for cancer diagnostics and therapeutics. Trends in Cancer 2023, 9 (5) , 410-420. https://doi.org/10.1016/j.trecan.2023.01.005
    9. Meng Wang, Benjamin D. Sunkel, William C. Ray, Benjamin Z. Stanton. Chromatin structure in cancer. BMC Molecular and Cell Biology 2022, 23 (1) https://doi.org/10.1186/s12860-022-00433-6
    10. Zhentao Shao, Hui Yuan, Zhilan Zhou, Ya Wang, Peidong Hou, Hexin Nan, Wei Wang, Weihong Tan, Juan Li. Visualization of Protein‐Specific Glycation in Living Cells via Bioorthogonal Chemical Reporter. Angewandte Chemie 2022, 134 (41) https://doi.org/10.1002/ange.202210069
    11. Zhentao Shao, Hui Yuan, Zhilan Zhou, Ya Wang, Peidong Hou, Hexin Nan, Wei Wang, Weihong Tan, Juan Li. Visualization of Protein‐Specific Glycation in Living Cells via Bioorthogonal Chemical Reporter. Angewandte Chemie International Edition 2022, 61 (41) https://doi.org/10.1002/anie.202210069
    12. Shahnawaz Rehman, Mohammad Aatif, Zeeshan Rafi, Mohd Yasir Khan, Uzma Shahab, Saheem Ahmad, Mohd Farhan. Effect of non-enzymatic glycosylation in the epigenetics of cancer. Seminars in Cancer Biology 2022, 83 , 543-555. https://doi.org/10.1016/j.semcancer.2020.11.019
    13. Frederik Müggenburg, Sabine Müller. Azide‐Modified Nucleosides as Versatile Tools for Bioorthogonal Labeling and Functionalization. The Chemical Record 2022, 22 (5) https://doi.org/10.1002/tcr.202100322
    14. Abdul Rouf Mir, Safia Habib, Moin Uddin. Recent advances in histone glycation: emerging role in diabetes and cancer. Glycobiology 2021, 31 (9) , 1072-1079. https://doi.org/10.1093/glycob/cwab011
    15. Igor Maksimovic, Yael David. Non-enzymatic Covalent Modifications as a New Chapter in the Histone Code. Trends in Biochemical Sciences 2021, 46 (9) , 718-730. https://doi.org/10.1016/j.tibs.2021.04.004
    16. Sarah Faulkner, Igor Maksimovic, Yael David. A chemical field guide to histone nonenzymatic modifications. Current Opinion in Chemical Biology 2021, 63 , 180-187. https://doi.org/10.1016/j.cbpa.2021.05.002
    17. Jenna N. Beyer, Nicole R. Raniszewski, George M. Burslem. Advances and Opportunities in Epigenetic Chemical Biology. ChemBioChem 2021, 22 (1) , 17-42. https://doi.org/10.1002/cbic.202000459
    18. Amr Alderawi, Gaetano Caramori, Emma H Baker, Andrew William Hitchings, Irfan Rahman, Christos Rossios, Ian Adcock, Paolo Cassolari, Alberto Papi, Victor E Ortega, Jeffrey L Curtis, Simon Dunmore, Paul Kirkham. FN3K expression in COPD: a potential comorbidity factor for cardiovascular disease. BMJ Open Respiratory Research 2020, 7 (1) , e000714. https://doi.org/10.1136/bmjresp-2020-000714

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