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Applying Multimodal Mass Spectrometry to Image Tumors Undergoing Ferroptosis Following In Vivo Treatment with a Ferroptosis Inducer

  • Brittney L. Gorman
    Brittney L. Gorman
    Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington 99352, United States
  • Michael J. Taylor
    Michael J. Taylor
    Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington 99352, United States
  • Lia Tesfay
    Lia Tesfay
    Department of Molecular Biology and Biophysics, University of Connecticut Health, Farmington, Connecticut 06030, United States
    More by Lia Tesfay
  • Jessica K. Lukowski
    Jessica K. Lukowski
    Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington 99352, United States
    School of Medicine, Washington University in St. Louis, St. Louis, Missouri 63110, United States
  • Poornima Hegde
    Poornima Hegde
    Department of Pathology and Laboratory Medicine, University of Connecticut Health, Farmington, 06030, Connecticut United States
  • Josie G. Eder
    Josie G. Eder
    Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington 99352, United States
  • Kent J. Bloodsworth
    Kent J. Bloodsworth
    Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington 99352, United States
  • Jennifer E. Kyle
    Jennifer E. Kyle
    Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington 99352, United States
  • Suzy Torti
    Suzy Torti
    Department of Molecular Biology and Biophysics, University of Connecticut Health, Farmington, Connecticut 06030, United States
    More by Suzy Torti
  • , and 
  • Christopher R. Anderton*
    Christopher R. Anderton
    Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington 99352, United States
    *[email protected]
Cite this: J. Am. Soc. Mass Spectrom. 2024, 35, 1, 5–12
Publication Date (Web):December 11, 2023
https://doi.org/10.1021/jasms.3c00193
Copyright © 2023 American Society for Mass Spectrometry. Published by American Chemical Society. All rights reserved.

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    Abstract

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    Epithelial ovarian cancer (EOC) is the most common form of ovarian cancer. The poor prognosis generally associated with this disease has led to the search for improved therapies such as ferroptosis-inducing agents. Ferroptosis is a form of regulated cell death that is dependent on iron and is characterized by lipid peroxidation. Precise mapping of lipids and iron within tumors exposed to ferroptosis-inducing agents may provide insight into processes of ferroptosis in vivo and ultimately assist in the optimal deployment of ferroptosis inducers in cancer therapy. In this work, we present a method for combining matrix-assisted laser desorption/ionization (MALDI) mass spectrometry imaging (MSI) with secondary ion mass spectrometry (SIMS) to analyze changes in spatial lipidomics and metal composition, respectively, in ovarian tumors following exposure to a ferroptosis inducer. Tumors were obtained by injecting human ovarian cancer tumor-initiating cells into mice, followed by treatment with the ferroptosis inducer erastin. SIMS imaging detected iron accumulation in the tumor tissue, and sequential MALDI-MS imaging of the same tissue section displayed two chemically distinct regions of lipids. One region was associated with the iron-rich area detected with SIMS, and the other region encompassed the remainder of the tissue section. Bulk lipidomics confirmed the lipid assignments putatively assigned from the MALDI-MS data. Overall, we demonstrate the ability of multimodal MSI to identify the spatial locations of iron and lipids in the same tissue section and associate these regions with clinical pathology.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/jasms.3c00193.

    • Additional methods; Figure S1, optimization of the DHB matrix spraying conditions, Figure S2, effects of the matrix removal on the detection of Fe; Figure S3, additional MALDI-MSI and SIMS image overlays; Tables S1 and S2, MALDI-MSI annotations colocalized to chemically distinct regions 1 and region 2; and additional information on the effects of matrix removal on SIMS ion detection (PDF)

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