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Pervasive Genomic Damage in Experimental Intracerebral Hemorrhage: Therapeutic Potential of a Mechanistic-Based Carbon Nanoparticle
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    Pervasive Genomic Damage in Experimental Intracerebral Hemorrhage: Therapeutic Potential of a Mechanistic-Based Carbon Nanoparticle
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    • Prakash Dharmalingam
      Prakash Dharmalingam
      Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United States
    • Girish Talakatta
      Girish Talakatta
      Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United States
    • Joy Mitra
      Joy Mitra
      Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United States
      More by Joy Mitra
    • Haibo Wang
      Haibo Wang
      Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United States
      More by Haibo Wang
    • Paul J. Derry
      Paul J. Derry
      Institute of Biosciences and Technology, Texas A&M Health Science Center, Houston, Texas 77030, United States
    • Lizanne Greer Nilewski
      Lizanne Greer Nilewski
      Department of Chemistry, Rice University, Houston, Texas 77005, United States
    • Emily A. McHugh
      Emily A. McHugh
      Department of Chemistry, Rice University, Houston, Texas 77005, United States
    • Roderic H. Fabian
      Roderic H. Fabian
      Department of Neurology, Baylor College of Medicine, and Michael E. DeBakey VA Medical Center, Houston, Texas 77030, United States
    • Kimberly Mendoza
      Kimberly Mendoza
      Department of Chemistry, Rice University, Houston, Texas 77005, United States
    • Velmarini Vasquez
      Velmarini Vasquez
      Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United States
    • Pavana M. Hegde
      Pavana M. Hegde
      Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United States
    • Eugenia Kakadiaris
      Eugenia Kakadiaris
      Department of Chemistry, Rice University, Houston, Texas 77005, United States
    • Trenton Roy
      Trenton Roy
      Department of Chemistry, Rice University, Houston, Texas 77005, United States
      More by Trenton Roy
    • Istvan Boldogh
      Istvan Boldogh
      Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas 77555, United States
    • Venkatesh L. Hegde
      Venkatesh L. Hegde
      Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United States
    • Sankar Mitra
      Sankar Mitra
      Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United States
      Weill Medical College of Cornell University, New York, New York 10065, United States
      More by Sankar Mitra
    • James M. Tour*
      James M. Tour
      Departments of Chemistry, Computer Science, Materials Science and NanoEngineering, Smalley-Curl Institute and the NanoCarbon Center, Rice University, Houston, Texas 77005, United States
      *Email: [email protected]
    • Thomas A. Kent*
      Thomas A. Kent
      Institute of Biosciences and Technology, Texas A&M Health Science Center, Houston, Texas 77030, United States
      Department of Chemistry, Rice University, Houston, Texas 77005, United States
      Stanley H. Appel Department of Neurology, Houston Methodist Hospital and Research Institute, Houston, Texas 77030, United States
      *Email: [email protected]
    • Muralidhar L. Hegde*
      Muralidhar L. Hegde
      Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United States
      Weill Medical College of Cornell University, New York, New York 10065, United States
      Center for Neuroregeneration, Department of Neurosurgery, Houston Methodist Neurological Institute, Houston Methodist, Houston, Texas 77030, United States
      *Email: [email protected]
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    ACS Nano

    Cite this: ACS Nano 2020, 14, 3, 2827–2846
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    https://doi.org/10.1021/acsnano.9b05821
    Published February 12, 2020
    Copyright © 2020 American Chemical Society

    Abstract

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    Therapy for intracerebral hemorrhage (ICH) remains elusive, in part dependent on the severity of the hemorrhage itself as well as multiple deleterious effects of blood and its breakdown products such as hemin and free iron. While oxidative injury and genomic damage have been seen following ICH, the details of this injury and implications remain unclear. Here, we discovered that, while free iron produced mostly reactive oxygen species (ROS)-related single-strand DNA breaks, hemin unexpectedly induced rapid and persistent nuclear and mitochondrial double-strand breaks (DSBs) in neuronal and endothelial cell genomes and in mouse brains following experimental ICH comparable to that seen with γ radiation and DNA-complexing chemotherapies. Potentially as a result of persistent DSBs and the DNA damage response, hemin also resulted in senescence phenotype in cultured neurons and endothelial cells. Subsequent resistance to ferroptosis reported in other senescent cell types was also observed here in neurons. While antioxidant therapy prevented senescence, cells became sensitized to ferroptosis. To address both senescence and resistance to ferroptosis, we synthesized a modified, catalytic, and rapidly internalized carbon nanomaterial, poly(ethylene glycol)-conjugated hydrophilic carbon clusters (PEG-HCC) by covalently bonding the iron chelator, deferoxamine (DEF). This multifunctional nanoparticle, DEF-HCC-PEG, protected cells from both senescence and ferroptosis and restored nuclear and mitochondrial genome integrity in vitro and in vivo. We thus describe a potential molecular mechanism of hemin/iron-induced toxicity in ICH that involves a rapid induction of DSBs, senescence, and the consequent resistance to ferroptosis and provide a mechanistic-based combinatorial therapeutic strategy.

    Copyright © 2020 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/acsnano.9b05821.

    • List of gene targets and primer sequences used for LA-PCR experiment and additional experimental data for dose and time kinetics of iron (FeSO4 and Fe-NTA)-induced cell death analysis and hemin purity analysis chromatogram; PGC-1α levels and DNA integrity in hemin-treated neurons; PGC-1α levels in ICH mice; DNA strand breaks quantitation in hemin-treated b.End3 cells and its amelioration by PEG-HCC; inhibition of hemin-induced senescence by PEG-HCC in b.End3 cells; GPx4 levels in hemin-treated iPSC-derived neurons together with erastin/ferrostatin controls; in vitro DNA damage by hemin and iron and characterization of nanoparticles via thermogravimetric analysis (PDF)

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    Cited By

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    This article is cited by 59 publications.

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    ACS Nano

    Cite this: ACS Nano 2020, 14, 3, 2827–2846
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsnano.9b05821
    Published February 12, 2020
    Copyright © 2020 American Chemical Society

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