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Identification of Formaldehyde-Induced DNA–RNA Cross-Links in the A/J Mouse Lung Tumorigenesis Model
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    Identification of Formaldehyde-Induced DNA–RNA Cross-Links in the A/J Mouse Lung Tumorigenesis Model
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    • Romel P. Dator
      Romel P. Dator
      Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota 55455, United States
    • Kevin J. Murray
      Kevin J. Murray
      Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, St. Paul, Minnesota 55108, United States
      Center for Mass Spectrometry and Proteomics, University of Minnesota, St. Paul, Minnesota 55108, United States
    • Matthew W. Luedtke
      Matthew W. Luedtke
      Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota 55455, United States
    • Foster C. Jacobs
      Foster C. Jacobs
      Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota 55455, United States
      Division of Environmental Health Sciences, School of Public Health, University of Minnesota, Minneapolis, Minnesota 55455, United States
    • Fekadu Kassie
      Fekadu Kassie
      Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota 55455, United States
      Department of Veterinary Clinical Sciences, College of Veterinary Medicine, University of Minnesota, St. Paul, Minnesota 55108, United States
    • Hai Dang Nguyen
      Hai Dang Nguyen
      Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota 55455, United States
      Department of Pharmacology, College of Medicine, University of Minnesota, Minneapolis, Minnesota 55455, United States
    • Peter W. Villalta
      Peter W. Villalta
      Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota 55455, United States
      Department of Medicinal Chemistry, College of Pharmacy, University of Minnesota, Minneapolis, Minnesota 55455, United States
    • Silvia Balbo*
      Silvia Balbo
      Masonic Cancer Center, University of Minnesota, Minneapolis, Minnesota 55455, United States
      Division of Environmental Health Sciences, School of Public Health, University of Minnesota, Minneapolis, Minnesota 55455, United States
      *Email: [email protected]. Phone: (612) 624-4240. Fax: (612) 624-3869.
      More by Silvia Balbo
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    Chemical Research in Toxicology

    Cite this: Chem. Res. Toxicol. 2022, 35, 11, 2025–2036
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    https://doi.org/10.1021/acs.chemrestox.2c00206
    Published November 10, 2022
    Copyright © 2022 American Chemical Society

    Abstract

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    4-(Methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) is a potent lung carcinogen present in tobacco products, and exposure to it is likely one of the factors contributing to the development of lung cancer in cigarette smokers. To exert its carcinogenic effects, NNK must be metabolically activated into highly reactive species generating a wide spectrum of DNA damage. We have identified a new class of DNA adducts, DNA–RNA cross-links found for the first time in NNK-treated mice lung DNA using our improved high-resolution accurate mass segmented full scan data-dependent neutral loss MS3 screening strategy. The levels of these DNA–RNA cross-links were found to be significantly higher in NNK-treated mice compared to the corresponding controls, which is consistent with higher levels of formaldehyde due to NNK metabolism as compared to endogenous levels. We hypothesize that this DNA–RNA cross-linking occurs through reaction with NNK-generated formaldehyde and speculate that this phenomenon has broad implications for NNK-induced carcinogenesis. The structures of these cross-links were characterized using high-resolution LC–MS2 and LC–MS3 accurate mass spectral analysis and comparison to a newly synthesized standard. Taken together, our data demonstrate a previously unknown link between DNA–RNA cross-link adducts and NNK and provide a unique opportunity to further investigate how these novel NNK-derived DNA–RNA cross-links contribute to carcinogenesis in the future.

    Copyright © 2022 American Chemical Society

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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/acs.chemrestox.2c00206.

    • Scheme of animal experiment, in vitro incubation of DNA and RNA with formaldehyde and HPLC-UV chromatograms, targeted LC–MS2 data for the DNA–RNA cross-links, NMR spectra for synthesized standard, list of target DNA adducts and cross-links for LC–MS2 assay (PDF)

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    Cited By

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    This article is cited by 5 publications.

    1. Scott J. Walmsley, Jingshu Guo, Anamary Tarifa, Anthony P. DeCaprio, Marcus S. Cooke, Robert J. Turesky, Peter W. Villalta. Mass Spectral Library for DNA Adductomics. Chemical Research in Toxicology 2024, 37 (2) , 302-310. https://doi.org/10.1021/acs.chemrestox.3c00302
    2. Nagarjunachary Ragi, Scott J. Walmsley, Foster C. Jacobs, Thomas A. Rosenquist, Viktoriya S. Sidorenko, Lihua Yao, Laura A. Maertens, Christopher J. Weight, Silvia Balbo, Peter W. Villalta, Robert J. Turesky. Screening DNA Damage in the Rat Kidney and Liver by Untargeted DNA Adductomics. Chemical Research in Toxicology 2024, 37 (2) , 340-360. https://doi.org/10.1021/acs.chemrestox.3c00333
    3. Chiung-Wen Hu, Yuan-Jhe Chang, Wei-Hung Chang, Marcus S. Cooke, Yet-Ran Chen, Mu-Rong Chao. A Novel Adductomics Workflow Incorporating FeatureHunter Software: Rapid Detection of Nucleic Acid Modifications for Studying the Exposome. Environmental Science & Technology 2024, 58 (1) , 75-89. https://doi.org/10.1021/acs.est.3c04674
    4. Kevin J. Murray, Peter W. Villalta, Timothy J. Griffin, Silvia Balbo. Discovery of Modified Metabolites, Secondary Metabolites, and Xenobiotics by Structure-Oriented LC–MS/MS. Chemical Research in Toxicology 2023, 36 (11) , 1666-1682. https://doi.org/10.1021/acs.chemrestox.3c00209
    5. Rajendra Bose Muthukumaran, Pritha Bhattacharjee, Priya Bhowmick, Lalrinawma Zote, Malsawmtluangi, Nachimuthu Senthil Kumar, Lalrintluanga Jahau, Marcus S. Cooke, Chiung-Wen Hu, Mu-Rong Chao. Genetic and epigenetic instability induced by betel quid associated chemicals. Toxicology Reports 2023, 10 , 223-234. https://doi.org/10.1016/j.toxrep.2023.02.001

    Chemical Research in Toxicology

    Cite this: Chem. Res. Toxicol. 2022, 35, 11, 2025–2036
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.chemrestox.2c00206
    Published November 10, 2022
    Copyright © 2022 American Chemical Society

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