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 Translational Epigenetics
Epigenetics and DNA
Damage
Volume 33
Edited by
Miriam Galvonas Jasiulionis
Department of Pharmacology, Universidade Federal de São Paulo,
São Paulo, Brazil

Laboratory of Ontogeny and Epigenetics, Escola Paulista de Medicina,

Universidade Federal de São Paulo, São Paulo, Brazil
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Contents

Contributors ........................................................................................................................................ xiii

Preface ............................................................................................................................................... xvii

SECTION 1 Understanding the relationship between DNA damage

and epigenetic mechanisms
CHAPTER 1 DNA damage and DNA methylation ................................................ 3
Salimata Ousmane Sall, Philippe Johann To Berens, and Jean Molinier
Introduction..................................................................................................................3
Base modifications ......................................................................................................4
DNA methylation.................................................................................................... 4
Deamination............................................................................................................ 4
Alkylation ............................................................................................................... 4
Oxidation................................................................................................................. 6
Cross-links .............................................................................................................. 6
DNA methylation and DNA damageability................................................................7
Dynamics of DNA methylation ..................................................................................8
Establishment of DNA methylation ....................................................................... 8
Maintenance of DNA methylation patterns ........................................................... 9
Active DNA demethylation.................................................................................... 9
DNA repair factors and DNA methylation .................................................................9
DNA methylation upon DNA repair.........................................................................10
References..................................................................................................................11

CHAPTER 2 DNA damage and histone modifications ....................................... 17

Hieu T. Van and Margarida A. Santos
Introduction................................................................................................................17
Histone modifications in DNA double-stranded break repair ..................................18
Phosphorylation .................................................................................................... 19
Ubiquitination ....................................................................................................... 22
Methylation ........................................................................................................... 23
Acetylation............................................................................................................ 24
Histone modifications in DNA excision repair ........................................................25
Histone modifications in DNA mismatch repair ......................................................26
Concluding remarks...................................................................................................26
References..................................................................................................................26

v
vi Contents

CHAPTER 3 DNA damage and histone variants ............................................... 33

Sebastiano Giallongo, Oriana Lo Re, and Manlio Vinciguerra
Introduction................................................................................................................33
DDR mechanisms ......................................................................................................34
Histone variants .........................................................................................................39
Role of histone variants in DDR...............................................................................42
Conclusions................................................................................................................46
References..................................................................................................................46

CHAPTER 4 DNA damage and miRNAs ........................................................... 55

Khalil Azizian, Moein Shirzad, Negar Gorjizadeh, and Ansar Karimian
MicroRNA biogenesis and maturation......................................................................55
Effects of DDR on miRNA biogenesis.....................................................................56
miRNAs and double-strand break (DSB) repair.......................................................57
miRNAs and homologous recombination (HR) repair .............................................57
miRNAs and nonhomologous end-joining (NHEJ) repair .......................................58
miRNAs and base excision repair (BER) .................................................................58
miRNAs and nucleotide excision repair (NER) .......................................................58
miRNAs DNA mismatch repair (MMR) ..................................................................58
Role of miRNAs in cell cycle arrest and apoptosis..................................................60
DDR, miRNAs, and cancer development and treatment..........................................62
References..................................................................................................................63

CHAPTER 5 DNA damage and lncRNAs .......................................................... 69

Negar Gorjizadeh, Nassim Gorjizadeh, Khalil Azizian, Ansar Karimian,
and Moein Shirzad
Introduction................................................................................................................69
lncRNAs and their biogenesis ...................................................................................72
lncRNAs and DNA damage ................................................................................. 73
lncRNAs in other signaling pathways.......................................................................78
lncRNAs and DNA repair .........................................................................................79
The role of lncRNAs in the DDR regulation............................................................80
Conclusion .................................................................................................................81
References..................................................................................................................81

CHAPTER 6 DNA damage, sirtuins, and epigenetic marks ............................... 87

Debora Kristina Alves-Fernandes and Miriam Galvonas Jasiulionis
Sirtuins .......................................................................................................................87
Sirtuins and chromatin remodeling ...........................................................................88
 Contents vii

Sirtuins and epigenetic modifications .......................................................................92

Histone acetylation and deacetylation.................................................................. 92
Histone methylation.............................................................................................. 94
Sirtuins and telomere maintenance ...........................................................................95
Sirtuins and genomic stability...................................................................................96
Sirtuins and diseases..................................................................................................98
Concluding remarks...................................................................................................99
References................................................................................................................100

SECTION 2 DNA damage and epigenetics—Their impact in the

onset of diseases
CHAPTER 7 DNA damage, metabolism, and epigenetic regulation ................ 111
Shinjini Ganguly, Anthony Ghanem, and Omar Y. Mian
Introduction........................................................................................................... 111
The interplay between epigenetics and metabolism........................................ 111
Metabolic dysfunction and DNA repair .......................................................... 112
Crosstalk between epigenetics and metabolism in cancer................................... 114
DNA damage.................................................................................................... 114
Role of epigenetic alterations in cellular metabolism..................................... 114
Role of metabolic dysfunction in the context of epigenetics.......................... 117
Metabolic dysfunction, epigenetic modification, and genomic instability ......... 120
Epigenetics and steroid hormone metabolism in endocrine-driven cancer......... 123
Epigenetic alterations in prostate cancer progression ..................................... 124
Epigenetic alterations in breast cancer progression ........................................ 126
Conclusions and perspectives............................................................................... 127
Acknowledgments ................................................................................................ 128
References............................................................................................................. 128

CHAPTER 8 DNA damage, epigenetics, and aging ....................................... 139

Apiwat Mutirangura
Introduction........................................................................................................... 139
Epigenetic modifications versus DNA damage ................................................... 139
DNA damage causes cellular senescence and aging ........................................... 140
Epigenetic marks that prevent DNA damage and aging: Youth-associated
genome-stabilizing epigenetic marks ............................................................... 141
How epigenetic modifications prevent DNA damage and the aging
process: DNA Protection vs. DNA repair........................................................ 141
IRS hypomethylation drives the molecular pathogenesis of age-related
noncommunicable diseases............................................................................... 143
viii Contents

What are an IRS, the structure of each IRS element, and the
distribution of methylation marks in the genome? ...................................... 143
IRS methylation levels and pattern changes in human diseases..................... 145
Mechanisms of IRS hypomethylation and hypermethylation ......................... 146
Youth-DNA-GAPs................................................................................................ 149
The fountain of youth........................................................................................... 150
References............................................................................................................. 150

CHAPTER 9 DNA damage signaling, cell reprogramming,

and differentiation................................................................... 157
Mikio Shimada and Tomoko Miyake
Introduction........................................................................................................... 157
DNA damage signaling in cell reprogramming and differentiation.................... 159
iPS cells derived from DNA repair-deficient disease.......................................... 160
Ataxia telangiectasia (A-T).............................................................................. 160
ATR-Seckel syndrome (ATR-SS).................................................................... 161
Fanconi anemia ................................................................................................ 161
Nijmegen breakage syndrome (NBS) .............................................................. 162
NHEJ factors (DNA-PKcs, LIG IV, and Artemis) .............................................. 162
Conclusion ............................................................................................................ 163
References............................................................................................................. 163

CHAPTER 10 The interplay between DNA damage and epigenetics

in cancer................................................................................ 167
Dayna Challis and Kate H. Brettingham-Moore
Introduction........................................................................................................... 167
Genetic factors ...................................................................................................... 168
Environmental exposures ..................................................................................... 170
The cancer epigenome and DNA damage ........................................................... 172
DNA methylation ............................................................................................. 172
Histone modifications ...................................................................................... 173
Noncoding RNAs ............................................................................................. 175
Chromatin remodelers ...................................................................................... 176
Higher order chromatin structure..................................................................... 177
Susceptibility of the cancer epigenome to DNA damage ................................... 178
Targeting DNA damage and epigenetic changes in cancer diagnosis
and treatment .................................................................................................... 179
Conclusion ............................................................................................................ 180
References............................................................................................................. 181
 Contents ix

CHAPTER 11 Oncometabolites, epigenetic marks, and DNA repair.................. 191

Jonathan Dow and Peter M. Glazer
Oncometabolite biology ....................................................................................... 191
Bridging two hallmarks: Altered metabolism and
genomic instability ....................................................................................... 191
Oncometabolites’ identification in cancer ....................................................... 192
Oncometabolites induce global histone and DNA hypermethylation
via αKG-dependent dioxygenase inhibition................................................. 192
Oncometabolites and DNA repair ........................................................................ 194
Early implications of oncometabolites in DNA damage
repair ............................................................................................................. 194
Identification of the oncometabolite-induced HDR deficiency ...................... 194
Oncometabolites disrupt HDR signaling via H3K9
hypermethylation .......................................................................................... 196
Therapeutic strategies targeting the oncometabolite-induced
HDR defect ................................................................................................... 198
References............................................................................................................. 199

SECTION 3 Therapeutic strategies inducing DNA damage

and epigenetic alterations
CHAPTER 12 Cancer therapies inducing DNA damage ................................... 205
Jessica Buck, Nikola Bowden, and Raelene Endersby
Introduction........................................................................................................... 205
Mechanisms of DNA damage by radiotherapy.................................................... 206
Use of radiotherapy to treat cancer.................................................................. 206
Conventional radiotherapy ............................................................................... 207
Proton radiotherapy .......................................................................................... 208
FLASH radiotherapy ........................................................................................ 209
High LET particles in cancer therapy.............................................................. 210
DNA damage-inducing chemotherapies .............................................................. 210
Alkylating agents.............................................................................................. 211
Platinum-based compounds.............................................................................. 213
Cisplatin analogs .............................................................................................. 215
Antimetabolites................................................................................................. 216
Topoisomerase poisons .................................................................................... 217
Conclusions........................................................................................................... 217
Acknowledgments ................................................................................................ 218
References............................................................................................................. 218
x Contents

CHAPTER 13 Epigenetic therapy and DNA damage response .......................... 227

Marina Baretti and Nilofer S. Azad
Introduction........................................................................................................... 227
Commonly altered epigenetic regulatory proteins implicated
in cancer and their implication for therapy ..................................................... 228
Therapies for aberrant DNA methylation........................................................ 230
Inhibitors of histone modifications .................................................................. 231
Targeting epigenetic readers ............................................................................ 234
Targeting the epigenetics of the DNA damage response in cancer:
The concept of synthetic lethality .................................................................... 235
Epigenetic inhibitors in combination with chemotherapy
and radiotherapy: Synthetic lethal interactions and clinical
applications ................................................................................................... 237
Epigenetic changes of DNA damage repair genes as predictive
markers of response to chemotherapy.......................................................... 238
Epigenetic inhibitors in combination with drugs that target DNA
repair components for synthetic lethal therapy............................................ 240
Conclusion: Implications of epigenetic regulation for improved
cancer treatment................................................................................................ 244
References............................................................................................................. 244

SECTION 4 Experimental approaches to study DNA damage

and epigenetic modifications
CHAPTER 14 Useful protocols to study DNA damage ..................................... 255
Giovana da Silva Leandro, Marcela Teatin Latancia,
Nathalia Quintero-Ruiz, and Carlos Frederico Martins Menck
Introduction........................................................................................................... 255
Alkaline comet assay............................................................................................ 255
Before you begin .............................................................................................. 256
Materials and equipment.................................................................................. 258
Step-by-step method details ............................................................................. 259
DNA lesions immunodetection ............................................................................ 263
Immunofluorescence (IF) to detect phosphorylated histone
H2AX (Ser139)............................................................................................. 263
Immuno-slot-blot assay for pyrimidine dimers ............................................... 271
Final remarks ........................................................................................................ 280
Acknowledgments ................................................................................................ 280
References............................................................................................................. 281
 Contents xi

CHAPTER 15 Useful methods to study epigenetic marks: DNA methylation,

histone modifications, chromatin structure,
and noncoding RNAs ............................................................... 283
Ana Luisa Pedroso Ayub, Bruna de Oliveira Perestrelo,
Guilherme Cavalcante Pessoa, and Miriam Galvonas Jasiulionis
Introduction........................................................................................................... 283
Methods used to study DNA methylation............................................................ 284
Based on bisulfite treatment ............................................................................ 285
Based on CpG capture ..................................................................................... 288
5mC content ..................................................................................................... 289
Methods used to study histone modifications...................................................... 290
Chromatin immunoprecipitation (ChIP) .......................................................... 290
Immunodetection with specific antibodies ...................................................... 291
Proteomics ........................................................................................................ 292
Methods used to study chromatin accessibility ................................................... 292
Deoxyribonuclease treatment followed by DNA sequencing
(DNase-seq) .................................................................................................. 293
Formaldehyde-assisted isolation of regulatory elements followed
by sequencing (FAIRE-seq) ......................................................................... 294
Micrococcal nuclease treatment followed by DNA sequencing
(MNase-seq).................................................................................................. 294
Assay for transposase-accessible chromatin with high-throughput
sequencing (ATAC-seq) ............................................................................... 294
Methods used to identify chromatin-associated proteins..................................... 295
Chromatin enrichment for proteomics (ChEP)................................................ 295
Methods used to study noncoding RNAs (ncRNA) ............................................ 295
ncRNA gene expression analysis..................................................................... 295
miRNA-mediated posttranscriptional regulation analysis............................... 297
Noncoding RNA-protein interactions .............................................................. 298
LncRNA and chromatin interaction................................................................. 299
ncRNA localization .......................................................................................... 300
ncRNA gene expression modulation methods................................................. 300
Conclusions........................................................................................................... 303
References............................................................................................................. 303

Index .................................................................................................................................................. 311

This page intentionally left blank
Contributors
D
ebora Kristina Alves-Fernandes
Department of Pharmacology, Escola Paulista de Medicina, Universidade Federal de São Paulo,
São Paulo, SP, Brazil
Ana Luisa Pedroso Ayub
Department of Pharmacology, Escola Paulista de Medicina, Universidade Federal de São Paulo,
São Paulo, SP, Brazil
Nilofer S. Azad
Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins Hospital, Baltimore, MD,
United States
Khalil Azizian
Department of Microbiology, Faculty of Medicine, Kurdistan University of Medical Sciences,
Sanandaj, Iran
Marina Baretti
Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins Hospital, Baltimore, MD,
United States
Nikola Bowden
Hunter Medical Research Institute and University of Newcastle, Callaghan, NSW, Australia
Kate H. Brettingham-Moore
Tasmanian School of Medicine, University of Tasmania, Hobart, TAS, Australia
Jessica Buck
Telethon Kids Institute, Brain Tumour Research, Perth; University of WA, Centre for Child Health
Research, Crawley, WA, Australia
Dayna Challis
Tasmanian School of Medicine, University of Tasmania, Hobart, TAS, Australia
Jonathan Dow
Yale University School of Medicine, New Haven, CT, United States
Raelene Endersby
Telethon Kids Institute, Brain Tumour Research, Perth; University of WA, Centre for Child Health
Research, Crawley, WA, Australia
Shinjini Ganguly
Cleveland Clinic, Cleveland, OH, United States
Anthony Ghanem
Cleveland Clinic, Cleveland, OH, United States
Sebastiano Giallongo
International Clinical Research Center, St’ Anne University Hospital; Department of Biology, Faculty
of Medicine, Masaryk University, Brno, Czech Republic

xiii
xiv Contributors

Peter M. Glazer
Yale University School of Medicine, New Haven, CT, United States
Nassim Gorjizadeh
Cellular and Molecular Biology Research Center, Health Research Institute, Babol University of
Medical Sciences, Babol, Iran
Negar Gorjizadeh
Department of Cell and Molecular Biology, Faculty of Biological Sciences, Kharazmi University,
Tehran; Cellular and Molecular Biology Research Center, Health Research Institute, Babol
University of Medical Sciences, Babol, Iran
Miriam Galvonas Jasiulionis
Department of Pharmacology, Escola Paulista de Medicina, Universidade Federal de São Paulo,
São Paulo, SP, Brazil
Philippe Johann To Berens
Institut de biologie mol
eculaire des plantes, Strasbourg, France
Ansar Karimian
Cellular and Molecular Biology Research Center, Health Research Institute, Babol University of
Medical Sciences, Babol, Iran
Marcela Teatin Latancia
Department of Microbiology, Institute of Biomedical Sciences—University of São Paulo (USP),
São Paulo, Brazil
Giovana da Silva Leandro
Department of Microbiology, Institute of Biomedical Sciences—University of São Paulo (USP),
São Paulo, Brazil
Oriana Lo Re
International Clinical Research Center, St’ Anne University Hospital, Brno, Czech Republic;
Department of Stem Cell Biology and Transplantology, Research Institute of the Medical University-
Varna, Varna, Bulgaria
Carlos Frederico Martins Menck
Department of Microbiology, Institute of Biomedical Sciences—University of São Paulo (USP),
São Paulo, Brazil
Omar Y. Mian
Cleveland Clinic, Cleveland, OH, United States
Tomoko Miyake
Laboratory for Zero-Carbon Energy, Institute of Innovative Research, Tokyo Institute of Technology,
Tokyo, Japan
Jean Molinier
Institut de biologie mol
eculaire des plantes, Strasbourg, France
Apiwat Mutirangura
Department of Anatomy, Faculty of Medicine, Center of Excellence in Molecular Genetics of Cancer
and Human Disease, Chulalongkorn University, Bangkok, Thailand
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- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Definition: Study tips and learning strategies
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Critical analysis and evaluation
• Key terms and definitions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Current trends and future directions
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Definition: Historical development and evolution
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Definition: Statistical analysis and interpretation
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Practice 5: Comparative analysis and synthesis
Note: Current trends and future directions
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Practice Problem 41: Research findings and conclusions
• Ethical considerations and implications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 42: Diagram/Chart/Graph]
Definition: Historical development and evolution
• Problem-solving strategies and techniques
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Important: Case studies and real-world applications
• Statistical analysis and interpretation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Definition: Case studies and real-world applications
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Key Concept: Best practices and recommendations
• Statistical analysis and interpretation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Definition: Comparative analysis and synthesis
• Case studies and real-world applications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
Important: Case studies and real-world applications
• Literature review and discussion
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Note: Research findings and conclusions
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Remember: Comparative analysis and synthesis
• Historical development and evolution
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Conclusion 6: Current trends and future directions
Example 50: Fundamental concepts and principles
• Case studies and real-world applications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Practice Problem 51: Learning outcomes and objectives
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Note: Experimental procedures and results
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Current trends and future directions
• Statistical analysis and interpretation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Study tips and learning strategies
• Current trends and future directions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Example 55: Historical development and evolution
• Interdisciplinary approaches
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 56: Diagram/Chart/Graph]
Definition: Comparative analysis and synthesis
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Key Concept: Ethical considerations and implications
• Practical applications and examples
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Practical applications and examples
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Critical analysis and evaluation
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
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