DNA replication stress and cancer chemotherapy

DNA replication is one of the fundamental biological processes in which dysregulation can cause genome instability. This instability is one of the hallmarks of cancer and confers genetic diversity during tumorigenesis. Numerous experimental and clinical studies have indicated that most tumors have experienced and overcome the stresses caused by the perturbation of DNA replication, which is also referred to as DNA replication stress (DRS). When we consider therapeutic approaches for tumors, it is important to exploit the differences in DRS between tumor and normal cells. In this review, we introduce the current understanding of DRS in tumors and discuss the underlying mechanism of cancer therapy from the aspect of DRS.

[1]  M. Oren,et al.  Mdm2 promotes the rapid degradation of p53 , 1997, Nature.

[2]  N. Rhind,et al.  Cdc25 mitotic inducer targeted by chk1 DNA damage checkpoint kinase. , 1997, Science.

[3]  S. Lowe,et al.  Oncogenic ras Provokes Premature Cell Senescence Associated with Accumulation of p53 and p16INK4a , 1997, Cell.

[4]  S. Elledge,et al.  Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. , 1997, Science.

[5]  C. Peng,et al.  Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. , 1997, Science.

[6]  Y Taya,et al.  Enhanced phosphorylation of p53 by ATM in response to DNA damage. , 1998, Science.

[7]  Y Taya,et al.  Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. , 1998, Science.

[8]  Y Taya,et al.  A role for ATR in the DNA damage-induced phosphorylation of p53. , 1999, Genes & development.

[9]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[10]  C. Wilson,et al.  Leucovorin and fluorouracil with or without oxaliplatin as first-line treatment in advanced colorectal cancer. , 2000, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[11]  S. Elledge,et al.  Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. , 2000, Genes & development.

[12]  R. Abraham.  Cell cycle checkpoint signaling through the ATM and ATR kinases. , 2001, Genes & development.

[13]  J. Diffley,et al.  Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint , 2001, Nature.

[14]  C. Smythe,et al.  Activation of mammalian Chk1 during DNA replication arrest , 2001, The Journal of cell biology.

[15]  JAMES C. Wang,et al.  Cellular roles of DNA topoisomerases: a molecular perspective , 2002, Nature Reviews Molecular Cell Biology.

[16]  P. Johnston,et al.  5-Fluorouracil: mechanisms of action and clinical strategies , 2003, Nature Reviews Cancer.

[17]  K. Kohn,et al.  Repair of and checkpoint response to topoisomerase I-mediated DNA damage. , 2003, Mutation research.

[18]  T. Hickish,et al.  Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. , 2004, The New England journal of medicine.

[19]  N. Suzuki,et al.  A novel combination antimetabolite, TAS-102, exhibits antitumor activity in FU-resistant human cancer cells through a mechanism involving FTD incorporation in DNA. , 2004, International journal of oncology.

[20]  A. Fujioka,et al.  An optimal dosing schedule for a novel combination antimetabolite, TAS-102, based on its intracellular metabolism and its incorporation into DNA. , 2004, International journal of molecular medicine.

[21]  Sonnet J. H. Arlander,et al.  Dial 9-1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1) clamp complex. , 2004, DNA repair.

[22]  S. Chaney,et al.  Recognition and processing of cisplatin- and oxaliplatin-DNA adducts. , 2005, Critical reviews in oncology/hematology.

[23]  Dimitris Kletsas,et al.  Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions , 2005, Nature.

[24]  T. Ørntoft,et al.  DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis , 2005, Nature.

[25]  A. Kumagai,et al.  TopBP1 Activates the ATR-ATRIP Complex , 2006, Cell.

[26]  R. Greenberg,et al.  Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. , 2006, Genes & development.

[27]  Dimitris Kletsas,et al.  Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints , 2006, Nature.

[28]  S. Galiègue,et al.  Repression of cell cycle–related proteins by oxaliplatin but not cisplatin in human colon cancer cells , 2006, Molecular Cancer Therapeutics.

[29]  Aaron Bensimon,et al.  Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication , 2006, Nature.

[30]  B. A. Ballif,et al.  ATM and ATR Substrate Analysis Reveals Extensive Protein Networks Responsive to DNA Damage , 2007, Science.

[31]  A. Marusyk,et al.  p53 Mediates Senescence-Like Arrest Induced by Chronic Replicational Stress , 2007, Molecular and Cellular Biology.

[32]  D. Gillespie,et al.  Chk1 regulates the density of active replication origins during the vertebrate S phase , 2007, The EMBO journal.

[33]  Marcus B Smolka,et al.  Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases , 2007, Proceedings of the National Academy of Sciences.

[34]  S. Gygi,et al.  Profiling of UV-induced ATM/ATR signaling pathways , 2007, Proceedings of the National Academy of Sciences.

[35]  J. Qin,et al.  A Proteomic Analysis of Ataxia Telangiectasia-mutated (ATM)/ATM-Rad3-related (ATR) Substrates Identifies the Ubiquitin-Proteasome System as a Regulator for DNA Damage Checkpoints* , 2007, Journal of Biological Chemistry.

[36]  Eduardo Sontag,et al.  Transcriptional control of human p53-regulated genes , 2008, Nature Reviews Molecular Cell Biology.

[37]  K. Cimprich,et al.  ATR: an essential regulator of genome integrity , 2008, Nature Reviews Molecular Cell Biology.

[38]  H. Lenz,et al.  Regulation of human dUTPase gene expression and p53-mediated transcriptional repression in response to oxaliplatin-induced DNA damage , 2008, Nucleic acids research.

[39]  I. Hickson,et al.  Replication stress induces sister-chromatid bridging at fragile site loci in mitosis , 2009, Nature Cell Biology.

[40]  C. Anderson,et al.  Posttranslational modification of p53: cooperative integrators of function. , 2009, Cold Spring Harbor perspectives in biology.

[41]  J. Glover,et al.  BACH1/FANCJ acts with TopBP1 and participates early in DNA replication checkpoint control. , 2010, Molecular cell.

[42]  H. Krokan,et al.  UNG-initiated base excision repair is the major repair route for 5-fluorouracil in DNA, but 5-fluorouracil cytotoxicity depends mainly on RNA incorporation , 2011, Nucleic acids research.

[43]  D. Hanahan,et al.  Hallmarks of Cancer: The Next Generation , 2011, Cell.

[44]  B. Kerem,et al.  Nucleotide Deficiency Promotes Genomic Instability in Early Stages of Cancer Development , 2011, Cell.

[45]  M. Morita,et al.  ATR-Chk1 signaling pathway and homologous recombinational repair protect cells from 5-fluorouracil cytotoxicity. , 2012, DNA repair.

[46]  Y. Kakeji,et al.  CtIP‐ and ATR‐dependent FANCJ phosphorylation in response to DNA strand breaks mediated by DNA replication , 2012, Genes to cells : devoted to molecular & cellular mechanisms.

[47]  K. Cimprich,et al.  Causes and consequences of replication stress , 2013, Nature Cell Biology.

[48]  Jiri Bartek,et al.  Replication stress links structural and numerical cancer chromosomal instability , 2013, Nature.

[49]  Replication stress links structural and numerical cancer chromosomal instability (vol 494, pg 492, 2013) , 2013 .

[50]  I. Hickson,et al.  How unfinished business from S‐phase affects mitosis and beyond , 2013, The EMBO journal.

[51]  Y. Liu,et al.  MUS81 promotes common fragile site expression , 2013, Nature Cell Biology.

[52]  A. Ryan,et al.  Replication Stress and Chromatin Context Link ATM Activation to a Role in DNA Replication , 2013, Molecular cell.

[53]  A. Fujioka,et al.  Repeated oral dosing of TAS-102 confers high trifluridine incorporation into DNA and sustained antitumor activity in mouse models , 2014, Oncology reports.

[54]  Matthias Dobbelstein,et al.  Targeting tumour-supportive cellular machineries in anticancer drug development , 2014, Nature Reviews Drug Discovery.

[55]  M. Nakanishi,et al.  Necessary and sufficient role for a mitosis skip in senescence induction. , 2014, Molecular cell.

[56]  E. Tokunaga,et al.  The 1,2-Diaminocyclohexane Carrier Ligand in Oxaliplatin Induces p53-Dependent Transcriptional Repression of Factors Involved in Thymidylate Biosynthesis , 2015, Molecular Cancer Therapeutics.

[57]  E. Tokunaga,et al.  Trifluridine Induces p53-Dependent Sustained G2 Phase Arrest with Its Massive Misincorporation into DNA and Few DNA Strand Breaks , 2015, Molecular Cancer Therapeutics.

[58]  A. Aguilera,et al.  Replication stress and cancer , 2015, Nature Reviews Cancer.

[59]  M. Dobbelstein,et al.  Exploiting replicative stress to treat cancer , 2015, Nature Reviews Drug Discovery.

[60]  B. Vogelstein,et al.  PD-1 blockade in tumors with mismatch repair deficiency. , 2015, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[61]  S. Boulton,et al.  FANCJ suppresses microsatellite instability and lymphomagenesis independent of the Fanconi anemia pathway , 2015, Genes & development.

[62]  Xingming Deng,et al.  Targeting DNA Replication Stress for Cancer Therapy , 2016, Genes.

[63]  M. A. O. Ignacio,et al.  How to cite this article , 2016 .

[64]  Kuniyoshi Iwabuchi,et al.  The distinctive cellular responses to DNA strand breaks caused by a DNA topoisomerase I poison in conjunction with DNA replication and RNA transcription. , 2015, Genes & genetic systems.

[65]  S. Di Marco,et al.  RECQ5 Helicase Cooperates with MUS81 Endonuclease in Processing Stalled Replication Forks at Common Fragile Sites during Mitosis. , 2017, Molecular cell.

[66]  Yves Pommier,et al.  A subset of platinum-containing chemotherapeutic agents kills cells by inducing ribosome biogenesis stress , 2017, Nature Medicine.

[67]  I. Hickson,et al.  The "enemies within": regions of the genome that are inherently difficult to replicate , 2017, F1000Research.