Skip to main content
SpringerLink
Log in

DNA Damage Responses, the Trump Card of Stem Cells in the Survival Game

  • Chapter
  • First Online:
Advances in Experimental Medicine and Biology

Abstract

Stem cells, as a group of undifferentiated cells, are enriched with self-renewal and high proliferative capacity, which have attracted the attention of many researchers as a promising approach in the treatment of many diseases over the past years. However, from the cellular and molecular point of view, the DNA repair system is one of the biggest challenges in achieving therapeutic goals through stem cell technology. DNA repair mechanisms are an advantage for stem cells that are constantly multiplying to deal with various types of DNA damage. However, this mechanism can be considered a trump card in the game of cell survival and treatment resistance in cancer stem cells, which can hinder the curability of various types of cancer. Therefore, getting a deep insight into the DNA repair system can bring researchers one step closer to achieving major therapeutic goals. The remarkable thing about the DNA repair system is that this system is not only under the control of genetic factors, but also under the control of epigenetic factors. Therefore, it is necessary to investigate the role of the DNA repair system in maintaining the survival of cancer stem cells from both aspects.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

Abbreviations

3′UTRs:

3′ untranslated regions

53BP1:

P53-binding protein 1

6-4PPs:

6-4 photoproducts

AGO:

Argonaute

AGT:

O6-alkylguanine DNA alkyltransferase

ALDH:

Aldehyde dehydrogenase

A-NHEJ:

Alternative NHEJ

ANRIL:

Antisense noncoding RNA in the INK4 locus

APE1:

AP endonuclease

ATM:

Ataxia telangiectasia mutated

ATR:

Ataxia telangiectasia and Rad3-related protein

BARD1 9′L:

BRCA1-associated RING domain protein 1 9′L

BCSLCs:

Bladder CSCs

BER:

Base excision repair

BM:

Bone marrow

CD10:

Cluster of differentiation 10

CGIs:

CpG islands

Chk1:

Checkpoint protein kinases 1

Chk2:

Checkpoint protein kinases 2

circRNAs:

Circular RNAs

C-NHEJ:

Canonical or classical NHEJ

CRC:

Colorectal cancer

CSCs:

Cancer stem cells

CtIP:

C-terminal binding protein-interacting protein

DDR:

DNA damage response

DDRNAs:

Drosha- and Dicer-dependent small RNAs

DDSR1:

DNA damage- sensitive RNA1

dilncRNAs:

Damage-induced long ncRNAs

diRNAs:

DSB-induced small RNAs

DNA-PKcs:

DNA-dependent protein kinase catalytic subunit

dRP:

Deoxyribose phosphate

DSBR:

Double-strand break repair

DSBs:

Double-strand breaks

ESCs:

Embryonic stem cells

EXO1:

Exonuclease 1

FA:

Fanconi Anemia

GADD45A:

DNA damage-inducible 45 alpha

GG-NER:

Global genomic NER

HDACs:

Histone deacetylases

HDR:

Homology-directed repair

HK2:

Hexokinase 2

HR:

Homologous recombination

HSCs:

Hematopoietic stem cells

HSPC:

Hematopoietic stem and progenitor cells

ICL:

DNA interstrand crosslink

ICM:

Inner cell mass

iPSCs:

Induced pluripotent stem cells

IR:

Ionizing radiation

Linc-ROR:

Long intergenic non-protein coding RNA, regulator of reprogramming

LINP1:

LncRNA in non-homologous end joining pathway 1

lncRNAs:

Long ncRNAs

LOXs:

Lysyl oxidases

MALAT1:

Metastasis-associated lung adenocarcinoma transcript 1

MCM:

Minichromosome maintenance

miRNAs:

MicroRNAs

MMR:

Mismatch repair

MPG:

N-methylpurine DNA Glycosylase

MSCs:

Mesenchymal stem cells

MUTYH:

MutY Homolog

NADPH:

Nicotinamide adenine dinucleotide phosphate

ncRNAs:

Non-coding RNAs

NCTD:

Norcantharidin

NEIL1:

Nei-like DNA glycosylase 1

NEIL1:

Nei-like DNA glycosylase 2

NER:

Nucleotide excision repair

NHEJ:

Non-homologous end joining

NOXs:

Nicotinamide adenine dinucleotide phosphate oxidases

NSCLC:

Non-small-cell lung cancer

NTHL1:

Nth Like DNA Glycosylase 1

OXPHOS:

Oxidative phosphorylation

PANDA:

P21-associated ncRNA DNA damage activated

PB:

Peripheral blood

PCNA:

Proliferating cell nuclear antigen

PDAC:

Pancreatic ductal adenocarcinoma

piRNAs:

PIWI-interacting RNAs

PLs:

Photolyases

PPP1R13B:

Protein phosphatase 1 regulatory subunit 13B

RISC:

RNA-induced silencing complex

ROS:

Reactive oxygen species

RPA:

Replication protein A

SDSA:

Synthesis-dependent strand annealing

sncRNAs:

Small ncRNAs

SSBR:

Single-strand break repair

SSBs:

Single-strand breaks

SUMO:

Small ubiquitin-like modifier

TC-NER:

Transcription-coupled NER

TERRA:

Telomeric repeat-containing RNA

TLS:

Translesion synthesis

Trp53cor1:

Tumor protein p53 pathway corepressor 1

UCB:

Umbilical cord blood

UCP2:

Uncoupling protein-2

UV:

Ultraviolet

UVR:

Ultraviolet radiation

WRA-P53:

WD repeat containing antisense to TP53

WRN:

Werner DNA helicase

XP:

Xeroderma pigmentosum

References

  • Abad E, Graifer D, Lyakhovich A (2020) DNA damage response and resistance of cancer stem cells. Cancer Lett 474:106–117

    Google Scholar 

  • Abbotts R, Thompson N, Madhusudan S (2014) DNA repair in cancer: emerging targets for personalized therapy. Cancer Manag Res 6:77

    Google Scholar 

  • Abdelalim EM, Tooyama I (2014) Knockdown of p53 suppresses Nanog expression in embryonic stem cells. Biochem Biophys Res Commun 443(2):652–657

    Google Scholar 

  • Aghayan HR, Hosseini MS, Gholami M, Mohamadi-Jahani F, Tayanloo-Beik A, Alavi-Moghadam S et al (2022) Mesenchymal stem cells’ seeded amniotic membrane as a tissue-engineered dressing for wound healing. Drug Deliv Transl Res 12(3):538–549

    Google Scholar 

  • Ahmad A, Li Y, Bao B, Sarkar FH (2013) Resistance and DNA repair mechanisms of cancer stem cells: potential molecular targets for therapy. In: DNA repair of cancer stem cells. Springer, pp 33–52

    Google Scholar 

  • Ahmad A, Nay SL, O’Connor TR (2015) Direct reversal repair in mammalian cells. Adv DNA Repair:95–128

    Google Scholar 

  • Al-Ejeh F, Pajic M, Shi W, Kalimutho M, Miranda M, Nagrial AM et al (2014) Gemcitabine and CHK1 inhibition potentiate EGFR-directed radioimmunotherapy against pancreatic ductal adenocarcinoma anti-EGFR radioimmunotherapy in pancreatic cancer. Clin Cancer Res 20(12):3187–3197

    Google Scholar 

  • Argunhan B, Murayama Y, Iwasaki H (2017) The differentiated and conserved roles of Swi5-Sfr1 in homologous recombination. FEBS Lett 591(14):2035–2047

    Google Scholar 

  • Arjmand B, Ranjbaran N, Khatami F, Hashemi M (2019a) Different gene expression profile of mesenchymal stem cells from various sources. In: Genomics, proteomics, and metabolomics. Springer, pp 83–96

    Google Scholar 

  • Arjmand B, Goodarzi P, Aghayan HR, Payab M, Rahim F, Alavi-Moghadam S et al (2019b) Co-transplantation of human fetal mesenchymal and hematopoietic stem cells in type 1 diabetic mice model. Front Endocrinol 10:761

    Google Scholar 

  • Arjmand B, Hamidpour SK, Alavi-Moghadam S, Yavari H, Shahbazbadr A, Tavirani MR et al (2022a) Molecular docking as a therapeutic approach for targeting cancer stem cell metabolic processes. Front Pharmacol 13

    Google Scholar 

  • Arjmand B, Hamidpour SK, Tayanloo-Beik A, Goodarzi P, Aghayan HR, Adibi H et al (2022b) Machine learning: a new prospect in multi-omics data analysis of cancer. Front Genet 13

    Google Scholar 

  • Azhagiri MKK, Babu P, Venkatesan V, Thangavel S (2021) Homology-directed gene-editing approaches for hematopoietic stem and progenitor cell gene therapy. Stem Cell Res Ther 12(1):1–12

    Google Scholar 

  • Azzoni V, Wicinski J, Macario M, Castagné M, Finetti P, Ambrosova K et al (2022) BMI1 nuclear location is critical for RAD51-dependent response to replication stress and drives chemoresistance in breast cancer stem cells. Cell Death Dis 13(2):1–15

    Google Scholar 

  • Baddock HT, Yosaatmadja Y, Newman JA, Schofield CJ, Gileadi O, McHugh PJ (2020) The SNM1A DNA repair nuclease. DNA Repair 95:102941

    Google Scholar 

  • Baldeck N, Janel-Bintz R, Wagner J, Tissier A, Fuchs RP, Burkovics P et al (2015) FF483–484 motif of human Polη mediates its interaction with the POLD2 subunit of Polδ and contributes to DNA damage tolerance. Nucleic Acids Res 43(4):2116–2125

    Google Scholar 

  • Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB et al (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444(7120):756–760

    Google Scholar 

  • Barnieh FM, Loadman PM, Falconer RA (2021) Progress towards a clinically-successful ATR inhibitor for cancer therapy. Curr Res Pharmacol Drug Discov 2:100017

    Google Scholar 

  • Bartocci C, Denchi EL (2013) Put a RING on it: regulation and inhibition of RNF8 and RNF168 RING finger E3 ligases at DNA damage sites. Front Genet 4:128

    Google Scholar 

  • Bartucci M, Svensson S, Romania P, Dattilo R, Patrizii M, Signore M et al (2012) Therapeutic targeting of Chk1 in NSCLC stem cells during chemotherapy. Cell Death Different 19(5):768–778

    Google Scholar 

  • Behrens A, Van Deursen JM, Rudolph KL, Schumacher B (2014) Impact of genomic damage and ageing on stem cell function. Nat Cell Biol 16(3):201–207

    Google Scholar 

  • Benitez EK, Lomova Kaufman A, Cervantes L, Clark DN, Ayoub PG, Senadheera S et al (2020) Global and local manipulation of DNA repair mechanisms to alter site-specific gene editing outcomes in hematopoietic stem cells. Front Genome Edit 2:601541

    Google Scholar 

  • Bernstein C, Bernstein H (2018) The role of DNA repair and the epigenetic markers left after repair in neurologic functions, including memory and learning. In: DNA repair-an update. IntechOpen

    Google Scholar 

  • Bernstein C, Prasad AR, Nfonsam V, Bernstein H (2013) DNA damage, DNA repair and cancer. InTech Rijeka, Croatia

    Google Scholar 

  • Bian Y, Teper Y, Mathews Griner LA, Aiken TJ, Shukla V, Guha R et al (2019) Target deconvolution of a multikinase inhibitor with antimetastatic properties identifies TAOK3 as a key contributor to a cancer stem cell–like phenotype TAOK3 is a novel target in pancreatic cancer stem cells. Mol Cancer Ther 18(11):2097–2110

    Google Scholar 

  • Biechonski S, Yassin M, Milyavsky M (2017) DNA-damage response in hematopoietic stem cells: an evolutionary trade-off between blood regeneration and leukemia suppression. Carcinogenesis 38(4):367–377

    Google Scholar 

  • Blakemore D, Vilaplana-Lopera N, Almaghrabi R, Gonzalez E, Moya M, Ward C et al (2021) MYBL2 and ATM suppress replication stress in pluripotent stem cells. EMBO Rep 22(5):e51120

    Google Scholar 

  • Bolderson E, Petermann E, Croft L, Suraweera A, Pandita RK, Pandita TK et al (2014) Human single-stranded DNA binding protein 1 (hSSB1/NABP2) is required for the stability and repair of stalled replication forks. Nucleic Acids Res 42(10):6326–6336

    Google Scholar 

  • Bose M, Sachsenweger J, Laurila N, Parplys AC, Willmann J, Jungwirth J et al (2019) BRCA1 mislocalization leads to aberrant DNA damage response in heterozygous ABRAXAS1 mutation carrier cells. Hum Mol Genet 28(24):4148–4160

    Google Scholar 

  • Caffrey PJ, Kher R, Bian K, Li D, Delaney S (2020) Comparison of the base excision and direct reversal repair pathways for correcting 1, N 6-ethenoadenine in strongly positioned nucleosome core particles. Chem Res Toxicol 33(7):1888–1896

    Google Scholar 

  • Caldecott KW (2003) DNA single-strand break repair and spinocerebellar ataxia. Cell 112(1):7–10

    Google Scholar 

  • Callen E, Faryabi RB, Luckey M, Hao B, Daniel JA, Yang W et al (2012) The DNA damage-and transcription-associated protein paxip1 controls thymocyte development and emigration. Immunity 37(6):971–985

    Google Scholar 

  • Carroll D (2013) Genetic recombination. In: Maloy S, Hughes K (eds) Brenner’s encyclopedia of genetics, 2nd edn. Academic, San Diego, pp 277–280

    Google Scholar 

  • Carroll D, St Clair DK (2018) Hematopoietic stem cells: normal versus malignant. Antioxid Redox Signal 29(16):1612–1632

    Google Scholar 

  • Carter M, Jemth A-S, Hagenkort A, Page BD, Gustafsson R, Griese JJ et al (2015) Crystal structure, biochemical and cellular activities demonstrate separate functions of MTH1 and MTH2. Nat Commun 6(1):1–10

    Google Scholar 

  • Ceccaldi R, Parmar K, Mouly E, Delord M, Kim JM, Regairaz M et al (2012) Bone marrow failure in Fanconi anemia is triggered by an exacerbated p53/p21 DNA damage response that impairs hematopoietic stem and progenitor cells. Cell Stem Cell 11(1):36–49

    Google Scholar 

  • Chan YW, West S (2015) GEN1 promotes Holliday junction resolution by a coordinated nick and counter-nick mechanism. Nucleic Acids Res 43(22):10882–10892

    Google Scholar 

  • Chatterjee N, Walker GC (2017) Mechanisms of DNA damage, repair, and mutagenesis. Environ Mol Mutagen 58(5):235–263

    Google Scholar 

  • Chen Y, Yang R, Guo P, Ju Z (2014) Gadd45a deletion aggravates hematopoietic stem cell dysfunction in ATM-deficient mice. Protein Cell 5(1):80–89

    Google Scholar 

  • Chen Y, Sun Z, Zhong T (2019) RDM1 promotes critical processes in breast cancer tumorigenesis. J Cell Mol Med 23(8):5432–5439

    Google Scholar 

  • Chen Y, Sun J, Ju Z, Wang ZQ, Li T (2021) Nbs1-mediated DNA damage repair pathway regulates haematopoietic stem cell development and embryonic haematopoiesis. Cell Prolif 54(3):e12972

    Google Scholar 

  • Choi EH, Yoon S, Koh YE, Seo YJ, Kim KP (2020) Maintenance of genome integrity and active homologous recombination in embryonic stem cells. Exp Mol Med 52(8):1220–1229

    Google Scholar 

  • Ciccia A, Constantinou A, West SC (2003) Identification and characterization of the human mus81-eme1 endonuclease. J Biol Chem 278(27):25172–25178

    Google Scholar 

  • Cinat D, Coppes RP, Barazzuol L (2021) DNA damage-induced inflammatory microenvironment and adult stem cell response. Front Cell Dev Biol:2497

    Google Scholar 

  • Coster G, Goldberg M (2010) The cellular response to DNA damage: a focus on MDC1 and its interacting proteins. Nucleus 1(2):166–178

    Google Scholar 

  • Couturier AM, Fleury H, Patenaude A-M, Bentley VL, Rodrigue A, Coulombe Y et al (2016) Roles for APRIN (PDS5B) in homologous recombination and in ovarian cancer prediction. Nucleic Acids Res:gkw921

    Google Scholar 

  • Cruet-Hennequart S, Prendergast AM, Barry FP, Carty MP (2010) Human mesenchymal stem cells (hMSCs) as targets of DNA damaging agents in cancer therapy. Curr Cancer Drug Targets 10(4):411–421

    Google Scholar 

  • Cubillos-Rojas M, Amair-Pinedo F, Peiró-Jordán R, Bartrons R, Ventura F, Rosa JL (2014) The E3 ubiquitin protein ligase HERC2 modulates the activity of tumor protein p53 by regulating its oligomerization. J Biol Chem 289(21):14782–14795

    Google Scholar 

  • De La Fuente R, Baumann C, Viveiros MM (2011) Role of ATRX in chromatin structure and function: implications for chromosome instability and human disease. Reproduction (Cambridge, England) 142(2):221

    Google Scholar 

  • Deans AJ, West SC (2011) DNA interstrand crosslink repair and cancer. Nat Rev Cancer 11(7):467–480

    Google Scholar 

  • Deriano L, Roth DB (2013) Modernizing the nonhomologous end-joining repertoire: alternative and classical NHEJ share the stage. Annu Rev Genet 47(1):433–455

    Google Scholar 

  • Desai A, Qing Y, Gerson SL (2014a) Exonuclease 1 is a critical mediator of survival during DNA double strand break repair in nonquiescent hematopoietic stem and progenitor cells. Stem Cells 32(2):582–593

    Google Scholar 

  • Desai A, Webb B, Gerson SL (2014b) CD133+ cells contribute to radioresistance via altered regulation of DNA repair genes in human lung cancer cells. Radiother Oncol 110(3):538–545

    Google Scholar 

  • Deshmukh AL, Porro A, Mohiuddin M, Lanni S, Panigrahi GB, Caron M-C et al (2021) FAN1, a DNA repair nuclease, as a modifier of repeat expansion disorders. J Huntington’s Dis 10(1):95–122

    Google Scholar 

  • Dinant C, Houtsmuller AB, Vermeulen W (2008) Chromatin structure and DNA damage repair. Epigenetics Chromatin 1(1):1–13

    Google Scholar 

  • Ding DC, Shyu WC, Lin SZ (2011) Mesenchymal stem cells. Cell Transplant 20(1):5–14

    Google Scholar 

  • Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315–317

    Google Scholar 

  • Dong H, Nebert DW, Bruford EA, Thompson DC, Joenje H, Vasiliou V (2015) Update of the human and mouse Fanconi anemia genes. Hum Genomics 9(1):1–10

    Google Scholar 

  • Dueva R, Iliakis G (2013) Alternative pathways of non-homologous end joining (NHEJ) in genomic instability and cancer. Transl Cancer Res 2(3):163–177

    Google Scholar 

  • Durut N, Mittelsten Scheid O (2019) The role of noncoding RNAs in double-strand break repair. Front Plant Sci 10:1155

    Google Scholar 

  • El-Hattab AW, Craigen WJ, Scaglia F (2017) Mitochondrial DNA maintenance defects. Biochim Biophys Acta (BBA)-Mol Basis Dis 1863(6):1539–1555

    Google Scholar 

  • Espada L, Ermolaeva MA (2016) DNA damage as a critical factor of stem cell aging and organ homeostasis. Curr Stem Cell Rep 2(3):290–298

    Google Scholar 

  • Falahzadeh K, Jalalvand M, Alavi-Moghadam S, Bana N, Negahdari B (2019) Trying to reveal the mysteries of stem cells using “omics” strategies. In: Genomics, proteomics, and metabolomics. Springer, pp 1–50

    Google Scholar 

  • Ffrench B, Gasch C, Hokamp K, Spillane C, Blackshields G, Mahgoub TM et al (2017) CD10−/ALDH− cells are the sole cisplatin-resistant component of a novel ovarian cancer stem cell hierarchy. Cell Death Dis 8(10):e3128-e

    Google Scholar 

  • Fisher R, Pusztai L, Swanton C (2013) Cancer heterogeneity: implications for targeted therapeutics. Br J Cancer 108(3):479–485

    Google Scholar 

  • Flach J, Bakker ST, Mohrin M, Conroy PC, Pietras EM, Reynaud D et al (2014) Replication stress is a potent driver of functional decline in ageing haematopoietic stem cells. Nature 512(7513):198–202

    Google Scholar 

  • Franklin R, Guo Y, He S, Chen M, Ji F, Zhou X et al (2022) Regulation of chromatin accessibility by the histone chaperone CAF-1 sustains lineage fidelity. Nat Commun 13(1):1–17

    Google Scholar 

  • Frosina G (2009) DNA repair in normal and cancer stem cells, with special reference to the central nervous system. Curr Med Chem 16(7):854–866

    Google Scholar 

  • Frosina G (2010) The bright and the dark sides of DNA repair in stem cells. J Biomed Biotechnol 2010:845396

    Google Scholar 

  • Fu X, Cui K, Yi Q, Yu L, Xu Y (2017) DNA repair mechanisms in embryonic stem cells. Cell Mol Life Sci 74(3):487–493

    Google Scholar 

  • Fu X, Wu S, Li B, Xu Y, Liu J (2020) Functions of p53 in pluripotent stem cells. Protein Cell 11(1):71–78

    Google Scholar 

  • Fugger K, Bajrami I, Silva Dos Santos M, Young SJ, Kunzelmann S, Kelly G et al (2021) Targeting the nucleotide salvage factor DNPH1 sensitizes BRCA-deficient cells to PARP inhibitors. Science 372(6538):156–165

    Google Scholar 

  • Fuss JO, Cooper PK (2006) DNA repair: dynamic defenders against cancer and aging. PLoS Biol 4(6):e203

    Google Scholar 

  • Gamsby JJ, Loros JJ, Dunlap JC (2009) A phylogenetically conserved DNA damage response resets the circadian clock. J Biol Rhythm 24(3):193–202

    Google Scholar 

  • Gangula NR, Maddika S (2013) WD repeat protein WDR48 in complex with deubiquitinase USP12 suppresses Akt-dependent cell survival signaling by stabilizing PH domain leucine-rich repeat protein phosphatase 1 (PHLPP1). J Biol Chem 288(48):34545–34554

    Google Scholar 

  • Garcia-Martinez J, Bakker B, Schukken KM, Simon JE, Foijer F (2016) Aneuploidy in stem cells. World J Stem Cells 8(6):216–222

    Google Scholar 

  • Gayarre J, Kamieniak MM, Cazorla-Jiménez A, Muñoz-Repeto I, Borrego S, García-Donas J et al (2016) The NER-related gene GTF2H5 predicts survival in high-grade serous ovarian cancer patients. Journal of. Gynecol Oncol 27(1)

    Google Scholar 

  • German SD, Campbell KH, Thornton E, McLachlan G, Sweetman D, Alberio R (2015) Ovine induced pluripotent stem cells are resistant to reprogramming after nuclear transfer. Cell Reprogram 17(1):19–27

    Google Scholar 

  • Ghatak D, Das Ghosh D, Roychoudhury S (2021) Cancer stemness: p53 at the wheel. Front Oncol 10

    Google Scholar 

  • Ghezelayagh Z, Zabihi M, Zarkesh I, Gonçalves CA, Larsen M, Hagh-Parast N et al (2021) Improved differentiation of hESC-derived pancreatic progenitors by using human fetal pancreatic mesenchymal cells in a micro-scalable three-dimensional co-culture system. Stem Cell Rev Rep:1–18

    Google Scholar 

  • Giglia-Mari G, Zotter A, Vermeulen W (2011) DNA damage response. Cold Spring Harb Perspect Biol 3(1):a000745

    Google Scholar 

  • Gong F, Miller KM (2019) Histone methylation and the DNA damage response. Mutat Res/Rev Mutat Res 780:37–47

    Google Scholar 

  • Goodarzi P, Aghayan HR, Soleimani M, Norouzi-Javidan A, Mohamadi-Jahani F, Jahangiri S et al (2014) Stem cell therapy for treatment of epilepsy. Acta Med Iran:651–655

    Google Scholar 

  • Goodarzi P, Alavi-Moghadam S, Payab M, Larijani B, Rahim F, Gilany K et al (2019) Metabolomics analysis of mesenchymal stem cells. Int J Mol Cell Med 8(Suppl1):30

    Google Scholar 

  • Guirouilh-Barbat J, Lambert S, Bertrand P, Lopez BS (2014) Is homologous recombination really an error-free process? Front Genet 5:175

    Google Scholar 

  • Guo Y, Tocchini C, Ciosk R (2021) CLK-2/TEL2 is a conserved component of the nonsense-mediated mRNA decay pathway. PLoS One 16(1):e0244505

    Google Scholar 

  • Hakem R (2008) DNA-damage repair; the good, the bad, and the ugly. EMBO J 27(4):589–605

    Google Scholar 

  • Hamadeh Z, Lansdorp P (2020) RECQL5 at the intersection of replication and transcription. Front Cell Dev Biol 324

    Google Scholar 

  • Hambarde S, Tsai C-L, Pandita RK, Bacolla A, Maitra A, Charaka V et al (2021) EXO5-DNA structure and BLM interactions direct DNA resection critical for ATR-dependent replication restart. Mol Cell 81(14):2989–3006.e9

    Google Scholar 

  • Hare I, Gencheva M, Evans R, Fortney J, Piktel D, Vos JA et al (2016) In vitro expansion of bone marrow derived mesenchymal stem cells alters DNA double strand break repair of etoposide induced DNA damage. Stem Cells Int 2016:8270464

    Google Scholar 

  • Harfouche G, Martin MT (2010) Response of normal stem cells to ionizing radiation: a balance between homeostasis and genomic stability. Mutat Res/Rev Mutat Res 704(1–3):167–174

    Google Scholar 

  • Harrision D, Gravells P, Thompson R, Bryant HE (2020) Poly (ADP-ribose) glycohydrolase (PARG) vs. poly (ADP-ribose) polymerase (PARP)–function in genome maintenance and relevance of inhibitors for anti-cancer therapy. Front Mol Biosci 191

    Google Scholar 

  • Hegde ML, Hazra TK, Mitra S (2008) Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res 18(1):27–47

    Google Scholar 

  • Herreros-Villanueva M, Bujanda L, Billadeau DD, Zhang JS (2014) Embryonic stem cell factors and pancreatic cancer. World J Gastroenterol 20(9):2247–2254

    Google Scholar 

  • Hu Q, Botuyan MV, Zhao D, Cui G, Mer E, Mer G (2021) Mechanisms of BRCA1–BARD1 nucleosome recognition and ubiquitylation. Nature 596(7872):438–443

    Google Scholar 

  • Hunt CR, Ramnarain D, Horikoshi N, Iyengar P, Pandita RK, Shay JW et al (2013) Histone modifications and DNA double-strand break repair after exposure to ionizing radiations. Radiat Res 179(4):383–392

    Google Scholar 

  • Iles N, Rulten S, El-Khamisy SF, Caldecott KW (2007) APLF (C2orf13) is a novel human protein involved in the cellular response to chromosomal DNA strand breaks. Mol Cell Biol 27(10):3793–3803

    Google Scholar 

  • Jabbarpour Z, Aghayan S, Arjmand B, Fallahzadeh K, Alavi-Moghadam S, Larijani B et al (2022) Xeno-free protocol for GMP-compliant manufacturing of human fetal pancreas-derived mesenchymal stem cells. Stem Cell Res Ther 13(1):1–12

    Google Scholar 

  • Johann T, Berens P, Molinier J (2020) Formation and recognition of UV-induced DNA damage within genome complexity. Int J Mol Sci 21(18):6689

    Google Scholar 

  • Kamp J, Lemmens B, Romeijn R, Changoer S, van Schendel R, Tijsterman M (2021) Helicase Q promotes homology-driven DNA double-strand break repair and prevents tandem duplications. Nat Commun 12(1):1–12

    Google Scholar 

  • Kee Y, D’Andrea AD (2010) Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev 24(16):1680–1694

    Google Scholar 

  • Keyvani-Ghamsari S, Khorsandi K, Rasul A, Zaman MK (2021) Current understanding of epigenetics mechanism as a novel target in reducing cancer stem cells resistance. Clin Epigenetics 13(1):1–31

    Google Scholar 

  • Kiss L, Clift D, Renner N, Neuhaus D, James LC (2021) RING domains act as both substrate and enzyme in a catalytic arrangement to drive self-anchored ubiquitination. Nat Commun 12(1):1–12

    Google Scholar 

  • Kreuzer KN (2020) Replicating and repairing the genome: from basic mechanisms to modern genetic technologies. World Scientific

    Google Scholar 

  • Krogan NJ, Lam MH, Fillingham J, Keogh M-C, Gebbia M, Li J et al (2004) Proteasome involvement in the repair of DNA double-strand breaks. Mol Cell 16(6):1027–1034

    Google Scholar 

  • Krokan HE, Bjørås M (2013) Base excision repair. Cold Spring Harb Perspect Biol 5(4):a012583

    Google Scholar 

  • Kumar R, Cheok CF (2014) RIF1: a novel regulatory factor for DNA replication and DNA damage response signaling. DNA Repair 15:54–59

    Google Scholar 

  • Kuschal C, Botta E, Orioli D, Digiovanna JJ, Seneca S, Keymolen K et al (2016) GTF2E2 mutations destabilize the general transcription factor complex TFIIE in individuals with DNA repair-proficient trichothiodystrophy. Am J Hum Genet 98(4):627–642

    Google Scholar 

  • Langelier M-F, Eisemann T, Riccio AA, Pascal JM (2018) PARP family enzymes: regulation and catalysis of the poly (ADP-ribose) posttranslational modification. Curr Opin Struct Biol 53:187–198

    Google Scholar 

  • Lee S-H, Oshige M, Durant ST, Rasila KK, Williamson EA, Ramsey H et al (2005) The SET domain protein Metnase mediates foreign DNA integration and links integration to nonhomologous end-joining repair. Proc Natl Acad Sci 102(50):18075–18080

    Google Scholar 

  • Leulmi R, Polge C, Claustre A, Jarzaguet M, Bechet D, Combaret L et al (2014) UBE2B is implicated in myofibrillar protein loss in catabolic C2C12 myotubes. In: Molecular biology of muscle development and regeneration

    Google Scholar 

  • Levitus M, Joenje H, de Winter JP (2006) The Fanconi anemia pathway of genomic maintenance. Anal Cell Pathol 28(1–2):3–29

    Google Scholar 

  • Li Y, Wu Q, Wang Y, Li L, Bu H, Bao J (2017) Senescence of mesenchymal stem cells (review). Int J Mol Med 39(4):775–782

    Google Scholar 

  • Liang L, Feng J, Zuo P, Yang J, Lu Y, Yin Y (2020) Molecular basis for assembly of the shieldin complex and its implications for NHEJ. Nat Commun 11(1):1–15

    Google Scholar 

  • Lim JR, Mouawad J, Gorton OK, Bubb WA, Kwan AH (2021) Cancer stem cell characteristics and their potential as therapeutic targets. Med Oncol 38(7):1–12

    Google Scholar 

  • Lin J-R, Zeman MK, Chen J-Y, Yee M-C, Cimprich KA (2011) SHPRH and HLTF act in a damage-specific manner to coordinate different forms of postreplication repair and prevent mutagenesis. Mol Cell 42(2):237–249

    Google Scholar 

  • Lin Z, Hollinger MK, Wu Z, Sun W, Batey K, Kim J et al (2021) Sirolimus augments hematopoietic stem and progenitor cell regeneration following hematopoietic insults. Stem Cells 39(2):240–252

    Google Scholar 

  • Machida YJ, Machida Y, Chen Y, Gurtan AM, Kupfer GM, D’Andrea AD et al (2006) UBE2T is the E2 in the Fanconi anemia pathway and undergoes negative autoregulation. Mol Cell 23(4):589–596

    Google Scholar 

  • Majumdar D, Pietras EM, Pawar SA (2021) Analysis of radiation-induced changes in cell cycle and DNA damage of murine hematopoietic stem cells by multi-color flow cytometry. Curr Protoc 1(8):e216

    Google Scholar 

  • Mani C, Reddy PH, Palle K (2020) DNA repair fidelity in stem cell maintenance, health, and disease. Biochim Biophys Acta Mol basis Dis 1866(4):165444

    Google Scholar 

  • Martin LJ (2008) DNA damage and repair: relevance to mechanisms of neurodegeneration. J Neuropathol Exp Neurol 67(5):377–387

    Google Scholar 

  • Martin SA (2016) Chapter 6 – the DNA mismatch repair pathway. In: Kelley MR, Fishel ML (eds) DNA repair in cancer therapy, 2nd edn. Academic, Boston, pp 151–177

    Google Scholar 

  • Masutani C, Kusumoto R, Iwai S, Hanaoka F (2000) Mechanisms of accurate translesion synthesis by human DNA polymerase η. EMBO J 19(12):3100–3109

    Google Scholar 

  • Mazouzi A, Velimezi G, Loizou JI (2014) DNA replication stress: causes, resolution and disease. Exp Cell Res 329(1):85–93

    Google Scholar 

  • Mehta KP, Lovejoy CA, Zhao R, Heintzman DR, Cortez D (2020) HMCES maintains replication fork progression and prevents double-strand breaks in response to APOBEC deamination and abasic site formation. Cell Rep 31(9):107705

    Google Scholar 

  • Menck CF, Munford V (2014) DNA repair diseases: what do they tell us about cancer and aging? Genet Mol Biol 37:220–233

    Google Scholar 

  • Mijnes J, Veeck J, Gaisa NT, Burghardt E, de Ruijter TC, Gostek S et al (2018) Promoter methylation of DNA damage repair (DDR) genes in human tumor entities: RBBP8/CtIP is almost exclusively methylated in bladder cancer. Clin Epigenetics 10(1):1–20

    Google Scholar 

  • Mishina Y, Duguid EM, He C (2006) Direct reversal of DNA alkylation damage. Chem Rev 106(2):215–232

    Google Scholar 

  • Moehrle BM, Geiger H (2016) Aging of hematopoietic stem cells: DNA damage and mutations? Exp Hematol 44(10):895–901

    Google Scholar 

  • Momčilović O, Schatten G (2013) DNA repair in normal stem cells. In: DNA repair of cancer stem cells. Springer, pp 53–87

    Google Scholar 

  • Morita Y, Shibutani T, Nakanishi N, Nishikura K, Iwai S, Kuraoka I (2013) Human endonuclease V is a ribonuclease specific for inosine-containing RNA. Nat Commun 4(1):1–10

    Google Scholar 

  • Nayak S, Calvo JA, Cantor SB (2021) Targeting translesion synthesis (TLS) to expose replication gaps, a unique cancer vulnerability. Expert Opin Ther Targets 25(1):27–36

    Google Scholar 

  • Ohnuki M, Takahashi K (2015) Present and future challenges of induced pluripotent stem cells. Philos Trans R Soc Lond Ser B Biol Sci 370(1680):20140367

    Google Scholar 

  • Pan G, Thomson JA (2007) Nanog and transcriptional networks in embryonic stem cell pluripotency. Cell Res 17(1):42–49

    Google Scholar 

  • Panich U, Sittithumcharee G, Rathviboon N, Jirawatnotai S (2016) Ultraviolet radiation-induced skin aging: the role of DNA damage and oxidative stress in epidermal stem cell damage mediated skin aging. Stem Cells Int 2016

    Google Scholar 

  • Pardo B, Moriel-Carretero M, Vicat T, Aguilera A, Pasero P (2020) Homologous recombination and Mus81 promote replication completion in response to replication fork blockage. EMBO Rep 21(7):e49367

    Google Scholar 

  • Park H, Cho B, Kim J (2020) Rad50 mediates DNA demethylation to establish pluripotent reprogramming. Exp Mol Med 52(7):1116–1127

    Google Scholar 

  • Parvathaneni S, Lu X, Chaudhary R, Lal A, Madhusudan S, Sharma S (2017) RECQ1 expression is upregulated in response to DNA damage and in a p53-dependent manner. Oncotarget 8(44):75924

    Google Scholar 

  • Picerno A, Stasi A, Franzin R, Curci C, di Bari I, Gesualdo L et al (2021) Why stem/progenitor cells lose their regenerative potential. World J Stem Cells 13(11):1714

    Google Scholar 

  • Poljsak B, Šuput D, Milisav I (2013) Achieving the balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxidative Med Cell Longev 2013

    Google Scholar 

  • Polo SE, Jackson SP (2011) Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 25(5):409–433

    Google Scholar 

  • Potts PR, Porteus MH, Yu H (2006) Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J 25(14):3377–3388

    Google Scholar 

  • Prakash R, Sandoval T, Morati F, Zagelbaum JA, Lim P-X, White T et al (2021) Distinct pathways of homologous recombination controlled by the SWS1–SWSAP1–SPIDR complex. Nat Commun 12(1):1–15

    Google Scholar 

  • Rafalski VA, Mancini E, Brunet A (2012) Energy metabolism and energy-sensing pathways in mammalian embryonic and adult stem cell fate. J Cell Sci 125(23):5597–5608

    Google Scholar 

  • Rappold I, Iwabuchi K, Date T, Chen J (2001) Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage–signaling pathways. J Cell Biol 153(3):613–620

    Google Scholar 

  • Reh WA, Nairn RS, Lowery MP, Vasquez KM (2017) The homologous recombination protein RAD51D protects the genome from large deletions. Nucleic Acids Res 45(4):1835–1847

    Google Scholar 

  • Ren R, Ocampo A, Liu GH, Izpisua Belmonte JC (2017) Regulation of stem cell aging by metabolism and epigenetics. Cell Metab 26(3):460–474

    Google Scholar 

  • Richarme G, Mihoub M, Dairou J, Bui LC, Leger T, Lamouri A (2015) Parkinsonism-associated protein DJ-1/Park7 is a major protein deglycase that repairs methylglyoxal-and glyoxal-glycated cysteine, arginine, and lysine residues. J Biol Chem 290(3):1885–1897

    Google Scholar 

  • Rossi DJ, Seita J, Czechowicz A, Bhattacharya D, Bryder D, Weissman IL (2007) Hematopoietic stem cell quiescence attenuates DNA damage response and permits DNA damage accumulation during aging. Cell Cycle 6(19):2371–2376

    Google Scholar 

  • Sahu S, Sridhar D, Abnave P, Kosaka N, Dattani A, Thompson JM et al (2021) Ongoing repair of migration-coupled DNA damage allows planarian adult stem cells to reach wound sites. elife 10:e63779

    Google Scholar 

  • Schär P, Fritsch O (2011) DNA repair and the control of DNA methylation. Epigenet Dis:51–68

    Google Scholar 

  • Schiroli G, Conti A, Ferrari S, Della Volpe L, Jacob A, Albano L et al (2019) Precise gene editing preserves hematopoietic stem cell function following transient p53-mediated DNA damage response. Cell Stem Cell 24(4):551–65.e8

    Google Scholar 

  • Schulz A, Meyer F, Dubrovska A, Borgmann K (2019) Cancer stem cells and radioresistance: DNA repair and beyond. Cancers 11(6):862

    Google Scholar 

  • Schwertman P, Vermeulen W, Marteijn JA (2013) UVSSA and USP7, a new couple in transcription-coupled DNA repair. Chromosoma 122(4):275–284

    Google Scholar 

  • Sharma V, Misteli T (2013) Non-coding RNAs in DNA damage and repair. FEBS Lett 587(13):1832–1839

    Google Scholar 

  • Shi X, Chen S, Zhang Y, Xie W, Hu Z, Li H et al (2019) Norcantharidin inhibits the DDR of bladder cancer stem-like cells through cdc6 degradation. Onco Targets Ther 12:4403

    Google Scholar 

  • Shimada M, Dumitrache LC, Russell HR, McKinnon PJ (2015) Polynucleotide kinase–phosphatase enables neurogenesis via multiple DNA repair pathways to maintain genome stability. EMBO J 34(19):2465–2480

    Google Scholar 

  • Shimura T, Noma N, Oikawa T, Ochiai Y, Kakuda S, Kuwahara Y et al (2012) Activation of the AKT/cyclin D1/Cdk4 survival signaling pathway in radioresistant cancer stem cells. Oncogenesis 1(6):e12-e

    Google Scholar 

  • Shinmura K, Kato H, Kawanishi Y, Igarashi H, Goto M, Tao H et al (2016) Abnormal expressions of DNA glycosylase genes NEIL1, NEIL2, and NEIL3 are associated with somatic mutation loads in human cancer. Oxidative Med Cell Longev 2016

    Google Scholar 

  • Signore M, Buccarelli M, Pilozzi E, De Luca G, Cappellari M, Fanciulli M et al (2016) UCN-01 enhances cytotoxicity of irinotecan in colorectal cancer stem-like cells by impairing DNA damage response. Oncotarget 7(28):44113

    Google Scholar 

  • Sishc BJ, Davis AJ (2017) The role of the core non-homologous end joining factors in carcinogenesis and cancer. Cancers 9(7):81

    Google Scholar 

  • Srivastava AK, Han C, Zhao R, Cui T, Dai Y, Mao C et al (2015) Enhanced expression of DNA polymerase eta contributes to cisplatin resistance of ovarian cancer stem cells. Proc Natl Acad Sci 112(14):4411–4416

    Google Scholar 

  • Stingele J, Bellelli R, Alte F, Hewitt G, Sarek G, Maslen SL et al (2016) Mechanism and regulation of DNA-protein crosslink repair by the DNA-dependent metalloprotease SPRTN. Mol Cell 64(4):688–703

    Google Scholar 

  • Strässler ET, Aalto-Setälä K, Kiamehr M, Landmesser U, Kränkel N (2018) Age is relative-impact of donor age on induced pluripotent stem cell-derived cell functionality. Front Cardiovasc Med 5:4

    Google Scholar 

  • Strzalka W, Ziemienowicz A (2011) Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation. Ann Bot 107(7):1127–1140

    Google Scholar 

  • Szpirer J, Pedeutour F, Kesti T, Riviere M, Syväoja JE, Turc-Carel C et al (1994) Localization of the gene for DNA polymerase ϵ (POLE) to human chromosome 12q24. 3 and rat chromosome 12 by somatic cell hybrid panels and fluorescence in situ hybridization. Genomics 20(2):223–226

    Google Scholar 

  • Tachon G, Cortes U, Guichet P-O, Rivet P, Balbous A, Masliantsev K et al (2018) Cell cycle changes after glioblastoma stem cell irradiation: the major role of RAD51. Int J Mol Sci 19(10):3018

    Google Scholar 

  • Takata M, Sasaki MS, Sonoda E, Fukushima T, Morrison C, Albala JS et al (2000) The Rad51 paralog Rad51B promotes homologous recombinational repair. Mol Cell Biol 20(17):6476–6482

    Google Scholar 

  • Tayanloo-Beik A, Sarvari M, Payab M, Gilany K, Alavi-Moghadam S, Gholami M et al (2020) OMICS insights into cancer histology; metabolomics and proteomics approach. Clin Biochem 84:13–20

    Google Scholar 

  • Tayanloo-Beik A, Rabbani Z, Soveyzi F, Alavi-Moghadam S, Rezaei-Tavirani M, Goodarzi P et al (2021) Cellular therapy for treatment of spinal cord injury in zebrafish model. Mol Biol Rep 48(2):1787–1800

    Google Scholar 

  • Técher H, Pasero P (2021) The replication stress response on a narrow path between genomic instability and inflammation. Front Cell Dev Biol 9

    Google Scholar 

  • Toh TB, Lim JJ, Chow EK-H (2017) Epigenetics in cancer stem cells. Mol Cancer 16(1):1–20

    Google Scholar 

  • Tsai RY (2016) Balancing self-renewal against genome preservation in stem cells: how do they manage to have the cake and eat it too? Cell Mol Life Sci 73(9):1803–1823

    Google Scholar 

  • Tsuda M, Kitamasu K, Kumagai C, Sugiyama K, Nakano T, Ide H (2020) Tyrosyl-DNA phosphodiesterase 2 (TDP2) repairs topoisomerase 1 DNA-protein crosslinks and 3′-blocking lesions in the absence of tyrosyl-DNA phosphodiesterase 1 (TDP1). DNA Repair 91:102849

    Google Scholar 

  • Tubbs A, Nussenzweig A (2017) Endogenous DNA damage as a source of genomic instability in cancer. Cell 168(4):644–656

    Google Scholar 

  • Turinetto V, Orlando L, Giachino C (2017) Induced pluripotent stem cells: advances in the quest for genetic stability during reprogramming process. Int J Mol Sci 18(9):1952

    Google Scholar 

  • Unk I, Hajdú I, Fátyol K, Hurwitz J, Yoon J-H, Prakash L et al (2008) Human HLTF functions as a ubiquitin ligase for proliferating cell nuclear antigen polyubiquitination. Proc Natl Acad Sci 105(10):3768–3773

    Google Scholar 

  • Van Esch H, Colnaghi R, Freson K, Starokadomskyy P, Zankl A, Backx L et al (2019) Defective DNA polymerase α-primase leads to X-linked intellectual disability associated with severe growth retardation, microcephaly, and hypogonadism. Am J Hum Genet 104(5):957–967

    Google Scholar 

  • Vitale I, Manic G, De Maria R, Kroemer G, Galluzzi L (2017) DNA damage in stem cells. Mol Cell 66(3):306–319

    Google Scholar 

  • Volk T, Pannicke U, Reisli I, Bulashevska A, Ritter J, Björkman A et al (2015) DCLRE1C (ARTEMIS) mutations causing phenotypes ranging from atypical severe combined immunodeficiency to mere antibody deficiency. Hum Mol Genet 24(25):7361–7372

    Google Scholar 

  • Wan L, Han J, Liu T, Dong S, Xie F, Chen H et al (2013) Scaffolding protein SPIDR/KIAA0146 connects the Bloom syndrome helicase with homologous recombination repair. Proc Natl Acad Sci 110(26):10646–10651

    Google Scholar 

  • Wang Q-E (2015) DNA damage responses in cancer stem cells: implications for cancer therapeutic strategies. World J Biol Chem 6(3):57

    Google Scholar 

  • Wang LC, Gautier J (2010) The Fanconi anemia pathway and ICL repair: implications for cancer therapy. Crit Rev Biochem Mol Biol 45(5):424–439

    Google Scholar 

  • Wang X, Andreassen PR, D’Andrea AD (2004) Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol Cell Biol 24(13):5850–5862

    Google Scholar 

  • Waters LS, Minesinger BK, Wiltrout ME, D’Souza S, Woodruff RV, Walker GC (2009) Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol Mol Biol Rev 73(1):134–154

    Google Scholar 

  • Weber GF (2015) DNA damaging drugs. In: Molecular therapies of cancer. Springer, pp 9–112

    Google Scholar 

  • Weiss RS, Leder P, Vaziri C (2003) Critical role for mouse Hus1 in an S-phase DNA damage cell cycle checkpoint. Mol Cell Biol 23(3):791–803

    Google Scholar 

  • Williams AB, Schumacher B (2016) p53 in the DNA-damage-repair process. Cold Spring Harb Perspect Med 6(5):a026070

    Google Scholar 

  • Williamson EA, Wray JW, Bansal P, Hromas R (2012) Overview for the histone codes for DNA repair. Prog Mol Biol Transl Sci 110:207–227

    Google Scholar 

  • Williamson AK, Zhu Z, Yuan Z-M (2018) Epigenetic mechanisms behind cellular sensitivity to DNA damage. Cell Stress 2(7):176

    Google Scholar 

  • Wood RD, Mitchell M, Sgouros J, Lindahl T (2001) Human DNA repair genes. Science 291(5507):1284–1289

    Google Scholar 

  • Yadav S, Kowolik CM, Lin M, Zuro D, Hui SK, Riggs AD et al (2019) SMC1A is associated with radioresistance in prostate cancer and acts by regulating epithelial-mesenchymal transition and cancer stem-like properties. Mol Carcinog 58(1):113–125

    Google Scholar 

  • Yamane K, Wu X, Chen J (2002) A DNA damage-regulated BRCT-containing protein, TopBP1, is required for cell survival. Mol Cell Biol 22(2):555–566

    Google Scholar 

  • Yamashita M, Nitta E, Suda T (2016) Regulation of hematopoietic stem cell integrity through p53 and its related factors. Ann N Y Acad Sci 1370(1):45–54

    Google Scholar 

  • Yamashita M, Dellorusso PV, Olson OC, Passegué E (2020) Dysregulated haematopoietic stem cell behaviour in myeloid leukaemogenesis. Nat Rev Cancer 20(7):365–382

    Google Scholar 

  • Yan Z, Guo R, Paramasivam M, Shen W, Ling C, Fox D III et al (2012) A ubiquitin-binding protein, FAAP20, links RNF8-mediated ubiquitination to the Fanconi anemia DNA repair network. Mol Cell 47(1):61–75

    Google Scholar 

  • Yang M, Qiu Y, Yang Y, Wang W (2022) An integrated analysis of the identified PRPF19 as an onco-immunological biomarker encompassing the tumor microenvironment, disease progression, and prognoses in hepatocellular carcinoma. Front Cell Dev Biol 10

    Google Scholar 

  • Ye L, Swingen C, Zhang J (2013) Induced pluripotent stem cells and their potential for basic and clinical sciences. Curr Cardiol Rev 9(1):63–72

    Google Scholar 

  • Yi C, He C (2013) DNA repair by reversal of DNA damage. Cold Spring Harb Perspect Biol 5(1):a012575

    Google Scholar 

  • Young RA (2011) Control of the embryonic stem cell state. Cell 144(6):940–954

    Google Scholar 

  • Yu Z, Pestell TG, Lisanti MP, Pestell RG (2012) Cancer stem cells. Int J Biochem Cell Biol 44(12):2144–2151

    Google Scholar 

  • Zeman MK, Cimprich KA (2014) Causes and consequences of replication stress. Nat Cell Biol 16(1):2–9

    Google Scholar 

  • Zhang M, Yang C, Liu H, Sun Y (2013) Induced pluripotent stem cells are sensitive to DNA damage. Genomics Proteomics Bioinformatics 11(5):320–326

    Google Scholar 

  • Zhang M, Wang L, An K, Cai J, Li G, Yang C et al (2018) Lower genomic stability of induced pluripotent stem cells reflects increased non-homologous end joining. Cancer Commun (Lond) 38(1):49

    Google Scholar 

  • Zheng L, Meng Y, Campbell JL, Shen B (2020) Multiple roles of DNA2 nuclease/helicase in DNA metabolism, genome stability and human diseases. Nucleic Acids Res 48(1):16–35

    Google Scholar 

  • Zhou D, Shao L, Spitz DR (2014) Reactive oxygen species in normal and tumor stem cells. Adv Cancer Res Elsevier 122:1–67

    Google Scholar 

Download references

Conflict of Interest

None.

Funding

None.

Author information

Authors and Affiliations

  1. Cell Therapy and Regenerative Medicine Research Center, Endocrinology and Metabolism Molecular-Cellular Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran

    Akram Tayanloo-Beik, Rasta Arjmand & Babak Arjmand

  2. Iranian Cancer Control Center (MACSA), Tehran, Iran

    Shayesteh Kokabi Hamidpour

  3. School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

    Amirabbas Nikkhah

  4. Department of Radiation Oncology, Imam Hossein Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Ahmad Rezazadeh Mafi

  5. Proteomics Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Mostafa Rezaei-Tavirani

  6. Endocrinology and Metabolism Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical sciences, Tehran, Iran

    Bagher Larijani

  7. Integrative Oncology Department, Breast Cancer Research Center, Motamed Cancer Institute, ACECR, Tehran, Iran

    Kambiz Gilany

  8. Reproductive Immunology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran

    Kambiz Gilany

Authors
  1. Akram Tayanloo-Beik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shayesteh Kokabi Hamidpour
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amirabbas Nikkhah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rasta Arjmand
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ahmad Rezazadeh Mafi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mostafa Rezaei-Tavirani
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bagher Larijani
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kambiz Gilany
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Babak Arjmand
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Babak Arjmand .

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Tayanloo-Beik, A. et al. (2023). DNA Damage Responses, the Trump Card of Stem Cells in the Survival Game. In: Advances in Experimental Medicine and Biology(). Springer, Cham. https://doi.org/10.1007/5584_2023_791

Download citation

  • DOI: https://doi.org/10.1007/5584_2023_791

  • Published:

  • Publisher Name: Springer, Cham

Publish with us

Policies and ethics

Search

Navigation