Model for MLL translocations in therapy-related leukemia involving topoisomerase IIβ-mediated DNA strand breaks and gene proximity.

PubWeight™: 1.29‹?› | Rank: Top 10%

🔗 View Article (PMC 3384169)

Published in Proc Natl Acad Sci U S A on May 21, 2012

Authors

Ian G Cowell1, Zbyslaw Sondka, Kayleigh Smith, Ka Cheong Lee, Catriona M Manville, Malgorzata Sidorczuk-Lesthuruge, Holly Ashlene Rance, Kay Padget, Graham Hunter Jackson, Noritaka Adachi, Caroline A Austin

Author Affiliations

1: Institute for Cellular and Molecular Biosciences, Newcastle University, Newcastle upon Tyne, NE2 4HH, United Kingdom.

Articles citing this

Drugging topoisomerases: lessons and challenges. ACS Chem Biol (2013) 2.46

The structure of DNA-bound human topoisomerase II alpha: conformational mechanisms for coordinating inter-subunit interactions with DNA cleavage. J Mol Biol (2012) 1.87

Phosphorylated Ribosomal Protein S6 Is Required for Akt-Driven Hyperplasia and Malignant Transformation, but Not for Hypertrophy, Aneuploidy and Hyperfunction of Pancreatic β-Cells. PLoS One (2016) 1.38

Topoisomerase-mediated chromosomal break repair: an emerging player in many games. Nat Rev Cancer (2015) 1.15

Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nat Rev Mol Cell Biol (2016) 1.05

Topoisomerase II and leukemia. Ann N Y Acad Sci (2014) 1.04

Dynamics of double strand breaks and chromosomal translocations. Mol Cancer (2014) 0.97

Mechanism of generation of therapy related leukemia in response to anti-topoisomerase II agents. Int J Environ Res Public Health (2012) 0.97

Secondary leukemia associated with the anti-cancer agent, etoposide, a topoisomerase II inhibitor. Int J Environ Res Public Health (2012) 0.96

Transcription factories. Front Genet (2012) 0.95

On the structural basis and design guidelines for type II topoisomerase-targeting anticancer drugs. Nucleic Acids Res (2013) 0.92

Complex correlations: replication timing and mutational landscapes during cancer and genome evolution. Curr Opin Genet Dev (2014) 0.92

Proteolytic degradation of topoisomerase II (Top2) enables the processing of Top2·DNA and Top2·RNA covalent complexes by tyrosyl-DNA-phosphodiesterase 2 (TDP2). J Biol Chem (2014) 0.91

Leukemogenic rearrangements at the mixed lineage leukemia gene (MLL)-multiple rather than a single mechanism. Front Cell Dev Biol (2015) 0.90

Tyrosyl DNA phosphodiesterase 2, an enzyme fit for purpose. Nat Struct Mol Biol (2012) 0.84

Replication-dependent and transcription-dependent mechanisms of DNA double-strand break induction by the topoisomerase 2-targeting drug etoposide. PLoS One (2013) 0.83

Classifying leukemia types with chromatin conformation data. Genome Biol (2014) 0.83

Catalytic core of human topoisomerase IIα: insights into enzyme-DNA interactions and drug mechanism. Biochemistry (2014) 0.81

DNA damage accumulation and repair defects in acute myeloid leukemia: implications for pathogenesis, disease progression, and chemotherapy resistance. Chromosoma (2014) 0.81

Etoposide quinone is a covalent poison of human topoisomerase IIβ. Biochemistry (2014) 0.80

Topoisomerase II beta interacts with cohesin and CTCF at topological domain borders. Genome Biol (2016) 0.80

The broken MLL gene is frequently located outside the inherent chromosome territory in human lymphoid cells treated with DNA topoisomerase II poison etoposide. PLoS One (2013) 0.79

Use of Genome Engineering to Create Patient Specific MLL Translocations in Primary Human Hematopoietic Stem and Progenitor Cells. PLoS One (2015) 0.79

Creating cancer translocations in human cells using Cas9 DSBs and nCas9 paired nicks. Methods Enzymol (2014) 0.78

Structure-based design, synthesis and biological testing of etoposide analog epipodophyllotoxin-N-mustard hybrid compounds designed to covalently bind to topoisomerase II and DNA. Bioorg Med Chem (2014) 0.78

Genome-wide ChIP-seq analysis of human TOP2B occupancy in MCF7 breast cancer epithelial cells. Biol Open (2015) 0.77

Nitric oxide inhibits topoisomerase II activity and induces resistance to topoisomerase II-poisons in human tumor cells. Biochim Biophys Acta (2016) 0.77

The molecular mechanics of mixed lineage leukemia. Oncogene (2016) 0.76

A role for epigenetics in the formation of chromosome translocations in acute leukemia. Cancer Genet (2015) 0.75

Collision of Trapped Topoisomerase 2 with Transcription and Replication: Generation and Repair of DNA Double-Strand Breaks with 5' Adducts. Genes (Basel) (2016) 0.75

Inhibition of Zn(II) binding type IA topoisomerases by organomercury compounds and Hg(II). PLoS One (2015) 0.75

Environmental and chemotherapeutic agents induce breakage at genes involved in leukemia-causing gene rearrangements in human hematopoietic stem/progenitor cells. Mutat Res (2015) 0.75

Myeloperoxidase Enhances Etoposide and Mitoxantrone-Mediated DNA Damage: A Target for Myeloprotection in Cancer Chemotherapy. Mol Pharmacol (2016) 0.75

Phenanthriplatin Acts As a Covalent Poison of Topoisomerase II Cleavage Complexes. ACS Chem Biol (2016) 0.75

Do transcription factories and TOP2B provide a recipe for chromosome translocations in therapy-related leukemia? Cell Cycle (2012) 0.75

Mechanisms of Action and Reduced Cardiotoxicity of Pixantrone; a Topoisomerase II Targeting Agent with Cellular Selectivity for the Topoisomerase IIα Isoform. J Pharmacol Exp Ther (2015) 0.75

The ascidian natural product eusynstyelamide B is a novel topoisomerase II poison that induces DNA damage and growth arrest in prostate and breast cancer cells. Oncotarget (2015) 0.75

Natural variation in a single amino acid substitution underlies physiological responses to topoisomerase II poisons. PLoS Genet (2017) 0.75

TDP2 suppresses chromosomal translocations induced by DNA topoisomerase II during gene transcription. Nat Commun (2017) 0.75

Genome-wide TOP2A DNA cleavage is biased towards translocated and highly transcribed loci. Genome Res (2017) 0.75

Articles cited by this

Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A (1987) 14.25

Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet (2004) 9.57

A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science (2006) 6.71

CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species. Mol Cell (2004) 5.51

The in vitro micronucleus technique. Mutat Res (2000) 5.22

Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol (1997) 5.00

Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol (2007) 4.35

Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell (2012) 4.02

Chromatin motion is constrained by association with nuclear compartments in human cells. Curr Biol (2002) 3.99

Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nat Genet (2010) 3.83

Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol (2007) 3.82

The connection between transcription and genomic instability. EMBO J (2002) 3.44

Human chromosomal translocations at CpG sites and a theoretical basis for their lineage and stage specificity. Cell (2008) 3.31

DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science (2008) 3.09

Origin of chromosomal translocations in lymphoid cancer. Cell (2010) 2.94

Spatial genome organization in the formation of chromosomal translocations. Semin Cancer Biol (2006) 2.12

gammaH2AX foci form preferentially in euchromatin after ionising-radiation. PLoS One (2007) 2.07

A model for all genomes: the role of transcription factories. J Mol Biol (2009) 2.02

Rearrangements of the MLL gene in therapy-related acute myeloid leukemia in patients previously treated with agents targeting DNA-topoisomerase II. Blood (1993) 1.94

Triggers for genomic rearrangements: insights into genomic, cellular and environmental influences. Nat Rev Genet (2010) 1.82

A novel DNA-dependent protein kinase inhibitor, NU7026, potentiates the cytotoxicity of topoisomerase II poisons used in the treatment of leukemia. Blood (2004) 1.65

DNA cleavage within the MLL breakpoint cluster region is a specific event which occurs as part of higher-order chromatin fragmentation during the initial stages of apoptosis. Mol Cell Biol (1997) 1.51

International workshop on the relationship of prior therapy to balanced chromosome aberrations in therapy-related myelodysplastic syndromes and acute leukemia: overview report. Genes Chromosomes Cancer (2002) 1.48

Estrogen treatment induces MLL aberrations in human lymphoblastoid cells. Leuk Res (2009) 1.48

Hypersensitivity of nonhomologous DNA end-joining mutants to VP-16 and ICRF-193: implications for the repair of topoisomerase II-mediated DNA damage. J Biol Chem (2003) 1.47

DNA topoisomerase IIalpha is required for RNA polymerase II transcription on chromatin templates. Nature (2001) 1.32

An in vivo topoisomerase II cleavage site and a DNase I hypersensitive site colocalize near exon 9 in the MLL breakpoint cluster region. Blood (1998) 1.27

Etoposide targets topoisomerase IIalpha and IIbeta in leukemic cells: isoform-specific cleavable complexes visualized and quantified in situ by a novel immunofluorescence technique. Mol Pharmacol (1998) 1.26

Apoptotic triggers initiate translocations within the MLL gene involving the nonhomologous end joining repair system. Cancer Res (2001) 1.20

DNA sequence selectivity of topoisomerases and topoisomerase poisons. Biochim Biophys Acta (1998) 1.20

Genome organization influences partner selection for chromosomal rearrangements. Trends Genet (2010) 1.15

Transcription linked to recombination: a gene-internal promoter coincides with the recombination hot spot II of the human MLL gene. Oncogene (2006) 1.14

DNA structural properties of AF9 are similar to MLL and could act as recombination hot spots resulting in MLL/AF9 translocations and leukemogenesis. Hum Mol Genet (2000) 1.12

Mixed lineage leukemia: roles in human malignancies and potential therapy. FEBS J (2010) 1.12

NK314, a topoisomerase II inhibitor that specifically targets the alpha isoform. J Biol Chem (2008) 1.04

Reciprocal DNA topoisomerase II cleavage events at 5'-TATTA-3' sequences in MLL and AF-9 create homologous single-stranded overhangs that anneal to form der(11) and der(9) genomic breakpoint junctions in treatment-related AML without further processing. Oncogene (2003) 1.03

Nucleotide-resolution mapping of topoisomerase-mediated and apoptotic DNA strand scissions at or near an MLL translocation hotspot. Am J Hum Genet (2006) 1.00

The transcriptome of human CD34+ hematopoietic stem-progenitor cells. Proc Natl Acad Sci U S A (2009) 0.98

Topoisomerase IIbeta negatively modulates retinoic acid receptor alpha function: a novel mechanism of retinoic acid resistance. Mol Cell Biol (2008) 0.98

Molecular cytogenetic characterization of the KG-1 and KG-1a acute myeloid leukemia cell lines by use of spectral karyotyping and fluorescence in situ hybridization. Genes Chromosomes Cancer (2003) 0.91

Role of Topoisomerase IIβ in DNA Damage Response following IR and Etoposide. J Nucleic Acids (2010) 0.84

An overview of the visualisation and quantitation of low and high MW DNA adducts using the trapped in agarose DNA immunostaining (TARDIS) assay. Mutagenesis (2010) 0.83

Evidence for the involvement of DNA topoisomerase II in neutrophil-granulocyte differentiation. Leukemia (1987) 0.79

Articles by these authors

Bidirectional gene organization: a common architectural feature of the human genome. Cell (2002) 3.47

gammaH2AX foci form preferentially in euchromatin after ionising-radiation. PLoS One (2007) 2.07

Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. EMBO J (2006) 1.97

The structure of DNA-bound human topoisomerase II alpha: conformational mechanisms for coordinating inter-subunit interactions with DNA cleavage. J Mol Biol (2012) 1.87

A novel DNA-dependent protein kinase inhibitor, NU7026, potentiates the cytotoxicity of topoisomerase II poisons used in the treatment of leukemia. Blood (2004) 1.65

Digitoxin inhibits the growth of cancer cell lines at concentrations commonly found in cardiac patients. J Nat Prod (2005) 1.42

The embryonic lethality in DNA ligase IV-deficient mice is rescued by deletion of Ku: implications for unifying the heterogeneous phenotypes of NHEJ mutants. DNA Repair (Amst) (2002) 1.41

Simple one-week method to construct gene-targeting vectors: application to production of human knockout cell lines. Biotechniques (2006) 1.36

The novel poly(ADP-Ribose) polymerase inhibitor, AG14361, sensitizes cells to topoisomerase I poisons by increasing the persistence of DNA strand breaks. Clin Cancer Res (2005) 1.35

Genetic evidence that the non-homologous end-joining repair pathway is involved in LINE retrotransposition. PLoS Genet (2009) 1.28

Generation and characterization of endonuclease G null mice. Mol Cell Biol (2005) 1.25

LEDGF/p75-independent HIV-1 replication demonstrates a role for HRP-2 and remains sensitive to inhibition by LEDGINs. PLoS Pathog (2012) 1.25

Genetic interactions between BLM and DNA ligase IV in human cells. J Biol Chem (2004) 1.25

The iron chelator Dp44mT causes DNA damage and selective inhibition of topoisomerase IIalpha in breast cancer cells. Cancer Res (2009) 1.17

Enforced cytokinesis without complete nuclear division in embryonic cells depleting the activity of DNA topoisomerase IIalpha. Genes Cells (2003) 1.14

DNA-dependent protein kinase is a therapeutic target and an indicator of poor prognosis in B-cell chronic lymphocytic leukemia. Clin Cancer Res (2008) 1.13

Loss of Bloom syndrome protein destabilizes human gene cluster architecture. Hum Mol Genet (2009) 1.12

Fen-1 facilitates homologous recombination by removing divergent sequences at DNA break ends. Mol Cell Biol (2005) 1.09

Vertebrate cells lacking FEN-1 endonuclease are viable but hypersensitive to methylating agents and H2O2. Nucleic Acids Res (2002) 1.05

OGFOD1, a member of the 2-oxoglutarate and iron dependent dioxygenase family, functions in ischemic signaling. FEBS Lett (2010) 1.04

The requirement of Artemis in double-strand break repair depends on the type of DNA damage. DNA Cell Biol (2008) 1.04

Impact of non-homologous end-joining deficiency on random and targeted DNA integration: implications for gene targeting. Nucleic Acids Res (2008) 1.04

NK314, a topoisomerase II inhibitor that specifically targets the alpha isoform. J Biol Chem (2008) 1.04

Molecular mechanism of protein assembly on DNA double-strand breaks in the non-homologous end-joining pathway. J Radiat Res (2009) 1.04

The helicase domain and C-terminus of human RecQL4 facilitate replication elongation on DNA templates damaged by ionizing radiation. Carcinogenesis (2012) 0.98

Differences in the longevity of topo IIalpha and topo IIbeta drug-stabilized cleavable complexes and the relationship to drug sensitivity. Cancer Chemother Pharmacol (2003) 0.98

Mechanism of generation of therapy related leukemia in response to anti-topoisomerase II agents. Int J Environ Res Public Health (2012) 0.97

Overview of the transcriptome profiles identified in hagfish, shark, and bichir: current issues arising from some nonmodel vertebrate taxa. J Exp Zool B Mol Dev Evol (2011) 0.97

Curcumin induces high levels of topoisomerase I- and II-DNA complexes in K562 leukemia cells. J Nat Prod (2007) 0.96

Guanidine-reactive agent phenylglyoxal induces DNA damage and cancer cell death. Pharmacol Rep (2012) 0.96

Artemis C-terminal region facilitates V(D)J recombination through its interactions with DNA Ligase IV and DNA-PKcs. J Exp Med (2012) 0.95

Both CpG methylation and activation-induced deaminase are required for the fragility of the human bcl-2 major breakpoint region: implications for the timing of the breaks in the t(14;18) translocation. Mol Cell Biol (2012) 0.94

Enhanced gene targeting efficiency by siRNA that silences the expression of the Bloom syndrome gene in human cells. Genes Cells (2006) 0.94

Human Mus81 and FANCB independently contribute to repair of DNA damage during replication. Genes Cells (2007) 0.94

The role of topoisomerase II in the excision of DNA loop domains during apoptosis. J Biol Chem (2002) 0.93

Alchemix: a novel alkylating anthraquinone with potent activity against anthracycline- and cisplatin-resistant ovarian cancer. Mol Cancer Ther (2003) 0.93

Poly(ADP-ribose) polymerases PARP1 and PARP2 modulate topoisomerase II beta (TOP2B) function during chromatin condensation in mouse spermiogenesis. Biol Reprod (2011) 0.93

53BP1 contributes to survival of cells irradiated with X-ray during G1 without Ku70 or Artemis. Genes Cells (2006) 0.92

KU70/80, DNA-PKcs, and Artemis are essential for the rapid induction of apoptosis after massive DSB formation. Cell Signal (2008) 0.91

Heterozygous inactivation of human Ku70/Ku86 heterodimer does not affect cell growth, double-strand break repair, or genome integrity. DNA Repair (Amst) (2005) 0.90

FEN1 functions in long patch base excision repair under conditions of oxidative stress in vertebrate cells. Mol Cancer Res (2010) 0.90

Green tea constituents (-)-epigallocatechin-3-gallate (EGCG) and gallic acid induce topoisomerase I- and topoisomerase II-DNA complexes in cells mediated by pyrogallol-induced hydrogen peroxide. Mutagenesis (2011) 0.89

Functions and regulation of Artemis: a goddess in the maintenance of genome integrity. J Radiat Res (2010) 0.88

MRE11 facilitates the removal of human topoisomerase II complexes from genomic DNA. Biol Open (2012) 0.88

Cells lacking DNA topoisomerase II beta are resistant to genistein. J Nat Prod (2007) 0.86

Mutation P732L in human DNA topoisomerase IIbeta abolishes DNA cleavage in the presence of calcium and confers drug resistance. Mol Pharmacol (2005) 0.86

The dietary flavonoids myricetin and fisetin act as dual inhibitors of DNA topoisomerases I and II in cells. Mutat Res (2009) 0.85

In vitro oocyte culture and somatic cell nuclear transfer used to produce a live-born cloned goat. Cloning Stem Cells (2003) 0.85

Position-specific trapping of topoisomerase II by benzo[a]pyrene diol epoxide adducts: implications for interactions with intercalating anticancer agents. Proc Natl Acad Sci U S A (2003) 0.85

Role of Topoisomerase IIβ in DNA Damage Response following IR and Etoposide. J Nucleic Acids (2010) 0.84

Poly(ADP-ribose) metabolism is essential for proper nucleoprotein exchange during mouse spermiogenesis. Biol Reprod (2010) 0.84

An overview of the visualisation and quantitation of low and high MW DNA adducts using the trapped in agarose DNA immunostaining (TARDIS) assay. Mutagenesis (2010) 0.83

C-Terminal region of DNA ligase IV drives XRCC4/DNA ligase IV complex to chromatin. Biochem Biophys Res Commun (2013) 0.83

The Dlx genes as clues to vertebrate genomics and craniofacial evolution. Semin Cell Dev Biol (2013) 0.83

Leptin up-regulates TLR2 in human monocytes. J Leukoc Biol (2013) 0.82

[FeFe]-hydrogenase-like gene is involved in the regulation of sensitivity to oxygen in yeast and nematode. Genes Cells (2009) 0.82

Developmental and evolutionary significance of the mandibular arch and prechordal/premandibular cranium in vertebrates: revising the heterotopy scenario of gnathostome jaw evolution. J Anat (2012) 0.82

Histone deacetylase inhibition redistributes topoisomerase IIβ from heterochromatin to euchromatin. Nucleus (2011) 0.82

Improved applications of the tetracycline-regulated gene depletion system. Biosci Trends (2009) 0.82

Overexpression of HAM1 gene detoxifies 5-bromodeoxyuridine in the yeast Saccharomyces cerevisiae. Curr Genet (2007) 0.81

Mutation E522K in human DNA topoisomerase IIbeta confers resistance to methyl N-(4'-(9-acridinylamino)-phenyl)carbamate hydrochloride and methyl N-(4'-(9-acridinylamino)-3-methoxy-phenyl) methane sulfonamide but hypersensitivity to etoposide. Mol Pharmacol (2004) 0.81

Kinetic analysis of human topoisomerase IIalpha and beta DNA binding by surface plasmon resonance. FEBS Lett (2003) 0.81

Broken colinearity of the amphioxus Hox cluster. Evodevo (2012) 0.81

Formation and longevity of idarubicin-induced DNA topoisomerase II cleavable complexes in K562 human leukaemia cells. Biochem Pharmacol (2002) 0.81

Loss of DNA ligase IV prevents recognition of DNA by double-strand break repair proteins XRCC4 and XLF. Nucleic Acids Res (2008) 0.80

In vitro and in vivo developmental potential of nuclear transfer embryos using bovine cumulus cells prepared in four different conditions. Cloning Stem Cells (2003) 0.80

The impact of the human DNA topoisomerase II C-terminal domain on activity. PLoS One (2008) 0.80

Characterisation of the DNA-dependent ATPase activity of human DNA topoisomerase IIbeta: mutation of Ser165 in the ATPase domain reduces the ATPase activity and abolishes the in vivo complementation ability. Nucleic Acids Res (2002) 0.80

5-Bromo-2'-deoxyuridine efficiently suppresses division potential of the yeast Saccharomyces cerevisiae. Biosci Biotechnol Biochem (2002) 0.80

Alpha, beta-unsaturated lactones 2-furanone and 2-pyrone induce cellular DNA damage, formation of topoisomerase I- and II-DNA complexes and cancer cell death. Toxicol Lett (2013) 0.79

Absence of p53 enhances growth defects and etoposide sensitivity of human cells lacking the Bloom syndrome helicase BLM. DNA Cell Biol (2007) 0.79

Salicylate, a catalytic inhibitor of topoisomerase II, inhibits DNA cleavage and is selective for the α isoform. Mol Pharmacol (2013) 0.79

Bovine nuclear transfer using fresh cumulus cell nuclei and in vivo- or in vitro-matured cytoplasts. Cloning Stem Cells (2008) 0.79

Heterozygous disruption of the DNA topoisomerase I gene confers cellular resistance to camptothecin in human cells. Biol Pharm Bull (2009) 0.78

The role of topoisomerase II beta on breakage and proximity of RUNX1 to partner alleles RUNX1T1 and EVI1. Genes Chromosomes Cancer (2013) 0.78

Topoisomerase IIalpha inhibition following DNA transfection greatly enhances random integration in a human pre-B lymphocyte cell line. Biochem Biophys Res Commun (2009) 0.78

Chromosomal manipulation by site-specific recombinases and fluorescent protein-based vectors. PLoS One (2010) 0.78

mAMSA resistant human topoisomerase IIbeta mutation G465D has reduced ATP hydrolysis activity. Nucleic Acids Res (2006) 0.78

Generation of tetracycline-inducible conditional gene knockout cells in a human Nalm-6 cell line. J Biotechnol (2008) 0.78

Chromosomal instability in the cattle clones derived by somatic cell nuclear-transfer. Mol Reprod Dev (2005) 0.78

Impaired cell adhesion, apoptosis, and signaling in WASP gene-disrupted Nalm-6 pre-B cells and recovery of cell adhesion using a transducible form of WASp. Int J Hematol (2012) 0.77

Evolution of the regionalization and patterning of the vertebrate telencephalon: what can we learn from cyclostomes? Curr Opin Genet Dev (2013) 0.77

Digitoxin, at concentrations commonly found in the plasma of cardiac patients, antagonizes etoposide and idarubicin activity in K562 leukemia cells. Leuk Res (2006) 0.77

Isolation and characterization of Vasa in the frog Rana rugosa. J Exp Zool A Ecol Genet Physiol (2010) 0.77

DNA ligase IV and artemis act cooperatively to suppress homologous recombination in human cells: implications for DNA double-strand break repair. PLoS One (2013) 0.77

Developmental ability of somatic cell nuclear transferred embryos aggregated at the 8-cell stage or 16- to 32-cell stage in cattle. J Reprod Dev (2011) 0.77

The impact of the C-terminal domain on the interaction of human DNA topoisomerase II α and β with DNA. PLoS One (2011) 0.77

Nucleofection-based gene targeting in human pre-B cells. Gene (2011) 0.77

Brief reports: Controlling the survival of human pluripotent stem cells by small molecule-based targeting of topoisomerase II alpha. Stem Cells (2015) 0.76

Restoration of mismatch repair functions in human cell line Nalm-6, which has high efficiency for gene targeting. PLoS One (2013) 0.76

Effect of phenazine compounds XR11576 and XR5944 on DNA topoisomerases. Cancer Chemother Pharmacol (2008) 0.76

Developmental potential of bovine nuclear transfer embryos and postnatal survival rate of cloned calves produced by two different timings of fusion and activation. Mol Reprod Dev (2003) 0.76

Interference in DNA replication can cause mitotic chromosomal breakage unassociated with double-strand breaks. PLoS One (2013) 0.76