Pervasive Genomic Damage in Experimental Intracerebral Hemorrhage: Therapeutic Potential of a Mechanistic-Based Carbon NanoparticleClick to copy article linkArticle link copied!
- Prakash DharmalingamPrakash DharmalingamDepartment of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United StatesMore by Prakash Dharmalingam
- Girish TalakattaGirish TalakattaDepartment of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United StatesMore by Girish Talakatta
- Joy MitraJoy MitraDepartment of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United StatesMore by Joy Mitra
- Haibo WangHaibo WangDepartment of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United StatesMore by Haibo Wang
- Paul J. DerryPaul J. DerryInstitute of Biosciences and Technology, Texas A&M Health Science Center, Houston, Texas 77030, United StatesMore by Paul J. Derry
- Lizanne Greer NilewskiLizanne Greer NilewskiDepartment of Chemistry, Rice University, Houston, Texas 77005, United StatesMore by Lizanne Greer Nilewski
- Emily A. McHughEmily A. McHughDepartment of Chemistry, Rice University, Houston, Texas 77005, United StatesMore by Emily A. McHugh
- Roderic H. FabianRoderic H. FabianDepartment of Neurology, Baylor College of Medicine, and Michael E. DeBakey VA Medical Center, Houston, Texas 77030, United StatesMore by Roderic H. Fabian
- Kimberly MendozaKimberly MendozaDepartment of Chemistry, Rice University, Houston, Texas 77005, United StatesMore by Kimberly Mendoza
- Velmarini VasquezVelmarini VasquezDepartment of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United StatesMore by Velmarini Vasquez
- Pavana M. HegdePavana M. HegdeDepartment of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United StatesMore by Pavana M. Hegde
- Eugenia KakadiarisEugenia KakadiarisDepartment of Chemistry, Rice University, Houston, Texas 77005, United StatesMore by Eugenia Kakadiaris
- Trenton RoyTrenton RoyDepartment of Chemistry, Rice University, Houston, Texas 77005, United StatesMore by Trenton Roy
- Istvan BoldoghIstvan BoldoghDepartment of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas 77555, United StatesMore by Istvan Boldogh
- Venkatesh L. HegdeVenkatesh L. HegdeDepartment of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United StatesMore by Venkatesh L. Hegde
- Sankar MitraSankar MitraDepartment of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United StatesWeill Medical College of Cornell University, New York, New York 10065, United StatesMore by Sankar Mitra
- James M. Tour*James M. Tour*Email: [email protected]Departments of Chemistry, Computer Science, Materials Science and NanoEngineering, Smalley-Curl Institute and the NanoCarbon Center, Rice University, Houston, Texas 77005, United StatesMore by James M. Tour
- Thomas A. Kent*Thomas A. Kent*Email: [email protected]Institute of Biosciences and Technology, Texas A&M Health Science Center, Houston, Texas 77030, United StatesDepartment of Chemistry, Rice University, Houston, Texas 77005, United StatesStanley H. Appel Department of Neurology, Houston Methodist Hospital and Research Institute, Houston, Texas 77030, United StatesMore by Thomas A. Kent
- Muralidhar L. Hegde*Muralidhar L. Hegde*Email: [email protected]Department of Radiation Oncology, Houston Methodist Research Institute, Houston, Texas 77030, United StatesWeill Medical College of Cornell University, New York, New York 10065, United StatesCenter for Neuroregeneration, Department of Neurosurgery, Houston Methodist Neurological Institute, Houston Methodist, Houston, Texas 77030, United StatesMore by Muralidhar L. Hegde
Abstract
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.
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