DNA damage in cells exhibiting radiation-induced genomic instability

Keszenman, Deborah J.; Kolodiuk, Lucia; Baulch, Janet E.

doi:10.1093/mutage/gev006

Title: DNA damage in cells exhibiting radiation-induced genomic instability

Abstract

Cells exhibiting radiation induced genomic instability exhibit varied spectra of genetic and chromosomal aberrations. Even so, oxidative stress remains a common theme in the initiation and/or perpetuation of this phenomenon. Isolated oxidatively modified bases, abasic sites, DNA single strand breaks and clustered DNA damage are induced in normal mammalian cultured cells and tissues due to endogenous reactive oxygen species generated during normal cellular metabolism in an aerobic environment. While sparse DNA damage may be easily repaired, clustered DNA damage may lead to persistent cytotoxic or mutagenic events that can lead to genomic instability. In this study, we tested the hypothesis that DNA damage signatures characterised by altered levels of endogenous, potentially mutagenic, types of DNA damage and chromosomal breakage are related to radiation-induced genomic instability and persistent oxidative stress phenotypes observed in the chromosomally unstable progeny of irradiated cells. The measurement of oxypurine, oxypyrimidine and abasic site endogenous DNA damage showed differences in non-double-strand breaks (DSB) clusters among the three of the four unstable clones evaluated as compared to genomically stable clones and the parental cell line. These three unstable clones also had increased levels of DSB clusters. The results of this study demonstrate that each unstable cell line hasmore »« less

Authors:

Keszenman, Deborah J. ^[1]; Kolodiuk, Lucia ^[2]; Baulch, Janet E. ^[3]

Brookhaven National Lab. (BNL), Upton, NY (United States). Biosciences Dept.; CENUR del Noroeste, Salto (Uruguay). Lab. of Medical and Environmental Radiobiology
Stony Brook Univ., Stony Brook, NY (United States)
Univ. of California, Irvine, CA (United States). Dept. of Radiation Oncology

Publication Date:: Sun Feb 22 00:00:00 EST 2015

Research Org.:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Org.:: USDOE Laboratory Directed Research and Development (LDRD) Program

OSTI Identifier:: 1214533

Report Number(s):: BNL-108343-2015-JA
Journal ID: ISSN 0267-8357; R&D Project: 12-012; YN0100000

Grant/Contract Number:: SC00112704

Resource Type:: Accepted Manuscript

Journal Name:: Mutagenesis

Additional Journal Information:: Journal Volume: 30; Journal Issue: 3; Journal ID: ISSN 0267-8357

Publisher:: Oxford University Press

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; oxidative stress; DNA damage; genomic instability; radiation

Citation Formats


                    Keszenman, Deborah J., Kolodiuk, Lucia, and Baulch, Janet E. DNA damage in cells exhibiting radiation-induced genomic instability.  United States: N. p., 2015. 
Web.  doi:10.1093/mutage/gev006.

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                    Keszenman, Deborah J., Kolodiuk, Lucia, & Baulch, Janet E. DNA damage in cells exhibiting radiation-induced genomic instability.  United States.  https://doi.org/10.1093/mutage/gev006

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                    Keszenman, Deborah J., Kolodiuk, Lucia, and Baulch, Janet E. Sun .  
"DNA damage in cells exhibiting radiation-induced genomic instability".  United States.  https://doi.org/10.1093/mutage/gev006.  https://www.osti.gov/servlets/purl/1214533.

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@article{osti_1214533,

  title        = {DNA damage in cells exhibiting radiation-induced genomic instability},

  author       = {Keszenman, Deborah J. and Kolodiuk, Lucia and Baulch, Janet E.},

  abstractNote = {Cells exhibiting radiation induced genomic instability exhibit varied spectra of genetic and chromosomal aberrations. Even so, oxidative stress remains a common theme in the initiation and/or perpetuation of this phenomenon. Isolated oxidatively modified bases, abasic sites, DNA single strand breaks and clustered DNA damage are induced in normal mammalian cultured cells and tissues due to endogenous reactive oxygen species generated during normal cellular metabolism in an aerobic environment. While sparse DNA damage may be easily repaired, clustered DNA damage may lead to persistent cytotoxic or mutagenic events that can lead to genomic instability. In this study, we tested the hypothesis that DNA damage signatures characterised by altered levels of endogenous, potentially mutagenic, types of DNA damage and chromosomal breakage are related to radiation-induced genomic instability and persistent oxidative stress phenotypes observed in the chromosomally unstable progeny of irradiated cells. The measurement of oxypurine, oxypyrimidine and abasic site endogenous DNA damage showed differences in non-double-strand breaks (DSB) clusters among the three of the four unstable clones evaluated as compared to genomically stable clones and the parental cell line. These three unstable clones also had increased levels of DSB clusters. The results of this study demonstrate that each unstable cell line has a unique spectrum of persistent damage and lead us to speculate that alterations in DNA damage signaling and repair may be related to the perpetuation of genomic instability.},

  doi          = {10.1093/mutage/gev006},

  journal      = {Mutagenesis},

  number       = 3,

  volume       = 30,

  place        = {United States},

  year         = {Sun Feb 22 00:00:00 EST 2015},

  month        = {Sun Feb 22 00:00:00 EST 2015}

}

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Ionizing Radiation and Complex DNA Damage: From Prediction to Detection Challenges and Biological Significance
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Radiation interactions with biological systems
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Title: DNA damage in cells exhibiting radiation-induced genomic instability

Abstract

Citation Formats

Expression of theE. coli fpg protein in CHO cells lowers endogenous oxypurine clustered damage levels and decreases accumulation of endogenousHprt mutations journal, June 2006

The role of mitochondria in the oncogenic signal transduction journal, March 2014

Chromosomal instability induced by heavy ion irradiation journal, January 2000

Clustered DNA damages induced in isolated DNA and in human cells by low doses of ionizing radiation journal, January 2000

Clustered Damages and Total Lesions Induced in DNA by Ionizing Radiation: Oxidized Bases and Strand Breaks † journal, July 2000

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Endogenously induced DNA double strand breaks arise in heterochromatic DNA regions and require ataxia telangiectasia mutated and Artemis for their repair journal, May 2011

A Role for Mitochondrial Dysfunction in Perpetuating Radiation-Induced Genomic Instability journal, November 2006

Unrepaired clustered DNA lesions induce chromosome breakage in human cells journal, April 2011

Clustered DNA lesion repair in eukaryotes: Relevance to mutagenesis and cell survival journal, June 2011

Analysis of bleomycin-induced chromosomal aberrations in Chinese hamster primary embryonic cells by FISH using arm-specific painting probes journal, July 1999

Biological consequences of formation and repair of complex DNA damage journal, December 2012

Cause and Consequences of Genetic and Epigenetic Alterations in Human Cancer journal, September 2008

Hallmarks of Cancer: The Next Generation journal, March 2011

Induction and Repair of Clustered DNA Lesions: What Do We Know So Far? journal, July 2013

Expression of delayed toxicity and lethal mutations in the progeny of human cells surviving exposure to radiation and other environmental mutagens journal, January 1998

Mitochondrial Dysfunction in Cancer journal, January 2013

Mitochondrial Complex II Dysfunction Can Contribute Significantly to Genomic Instability after Exposure to Ionizing Radiation journal, December 2009

Delayed chromosomal instability induced by DNA damage. journal, November 1993

Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures journal, January 1996

Melatonin protects human cells from clustered DNA damages, killing and acquisition of soft agar growth induced by X-rays or 970 MeV/n Fe ions journal, March 2011

Yields of Clustered DNA Damage Induced by Charged-Particle Radiations of Similar Kinetic Energy per Nucleon: LET Dependence in Different DNA Microenvironments journal, August 2010

Use of multicolour chromosome painting to identify chromosomal rearrangements in human lymphocytes exposed to bleomycin: A comparison with conventional cytogenetic analysis of giemsa-stained chromosomes journal, January 1995

Endogenous DNA damage clusters in human hematopoietic stem and progenitor cells journal, November 2008

Low levels of endogenous oxidative damage cluster levels in unirradiated viral and human DNAs journal, September 2003

Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes journal, September 2010

Biological Consequences of Radiation-induced DNA Damage: Relevance to Radiotherapy journal, October 2013

Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks journal, October 2004

Overexpression of enzymes that repair endogenous damage to DNA: Overexpression of DNA repair enzymes journal, April 2000

Responses to ionizing radiation mediated by inflammatory mechanisms: Tissue responses in radiation pathology journal, January 2014

Abasic sites preferentially form at regions undergoing DNA replication journal, May 2010

Oxidatively induced DNA damage: Mechanisms, repair and disease journal, December 2012

Evaluation of Number Average Length Analysis in Quantifying Double Strand Breaks in Genomic DNAs † journal, March 2003

Dynamics and diversions in base excision DNA repair of oxidized abasic lesions journal, December 2002

Are endogenous clustered dna damages induced in human cells? journal, August 2004

Biomarkers of oxidative damage in cigarette smokers: Which biomarkers might reflect acute versus chronic oxidative stress? journal, June 2011

Endogenous DNA damage clusters in human skin, 3-D model, and cultured skin cells journal, September 2005

Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer journal, October 2003

Base Excision Repair Processing of Radiation-induced Clustered DNA Lesions journal, September 2001

Tumors induce complex DNA damage in distant proliferative tissues in vivo journal, September 2010

Regulation of DNA repair throughout the cell cycle journal, February 2008

Mitochondria and cancer journal, September 2012

Accumulation of oxidatively induced clustered DNA lesions in human tumor tissues journal, March 2009

Transfection of the Escherichia coli nth Gene into Radiosensitive Chinese Hamster Cells: Effects on Sensitivity to Radiation, Hydrogen Peroxide, and Bleomycin Sulfate journal, October 1992

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Physiological Roles of Mitochondrial Reactive Oxygen Species journal, October 2012

Metabolic Reprogramming: A Cancer Hallmark Even Warburg Did Not Anticipate journal, March 2012

Instability and decay of the primary structure of DNA journal, April 1993

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Clustered DNA Damages Induced by X Rays in Human Cells journal, June 2002

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Hallmarks of Cancer: The Next Generation
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Yields of Clustered DNA Damage Induced by Charged-Particle Radiations of Similar Kinetic Energy per Nucleon: LET Dependence in Different DNA Microenvironments
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Low levels of endogenous oxidative damage cluster levels in unirradiated viral and human DNAs
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Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes
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Attempted base excision repair of ionizing radiation damage in human lymphoblastoid cells produces lethal and mutagenic double strand breaks
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Overexpression of enzymes that repair endogenous damage to DNA: Overexpression of DNA repair enzymes
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Abasic sites preferentially form at regions undergoing DNA replication
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Oxidatively induced DNA damage: Mechanisms, repair and disease
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Evaluation of Number Average Length Analysis in Quantifying Double Strand Breaks in Genomic DNAs ^†
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Dynamics and diversions in base excision DNA repair of oxidized abasic lesions
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Are endogenous clustered dna damages induced in human cells?
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Biomarkers of oxidative damage in cigarette smokers: Which biomarkers might reflect acute versus chronic oxidative stress?
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Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer
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Base Excision Repair Processing of Radiation-induced Clustered DNA Lesions
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Tumors induce complex DNA damage in distant proliferative tissues in vivo
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Regulation of DNA repair throughout the cell cycle
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Mitochondria and cancer
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Transfection of the Escherichia coli nth Gene into Radiosensitive Chinese Hamster Cells: Effects on Sensitivity to Radiation, Hydrogen Peroxide, and Bleomycin Sulfate
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Instability and decay of the primary structure of DNA
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Hydrogen peroxide mediates the radiation-induced mutator phenotype in mammalian cells
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Quantitative proteomic analysis of mitochondrial proteins reveals prosurvival mechanisms in the perpetuation of radiation-induced genomic instability
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Clustered DNA Damages Induced by X Rays in Human Cells
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Ionizing Radiation and Complex DNA Damage: From Prediction to Detection Challenges and Biological Significance
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Radiation interactions with biological systems
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