Home LiteratureArticle Details
PMID: 24298051 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Review

Chromothripsis and beyond: rapid genome evolution from complex chromosomal rearrangements.

Genes & development ·Vol. 27 ·No. 23 ·2013-12-01 ·Pages 2513-30

Zhang CZ, Leibowitz ML, Pellman D

Abstract

Recent genome sequencing studies have identified several classes of complex genomic rearrangements that appear to be derived from a single catastrophic event. These discoveries identify ways that genomes can be altered in single large jumps rather than by many incremental steps. Here we compare and contrast these phenomena and examine the evidence that they arise "all at once." We consider the impact of massive chromosomal change for the development of diseases such as cancer and for evolution more generally. Finally, we summarize current models for underlying mechanisms and discuss strategies for testing these models.

Keywords
cancer chromoanasynthesis chromoplexy chromosomal translocation chromothripsis copy number alteration genome evolution
MeSH Terms
Chromosome Aberrations Evolution, Molecular Gene Rearrangement/genetics Genome, Human/genetics Genomic Instability Humans
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zhang Cheng-Zhong
Broad Institute of Harvard and Massachusetts Institute of Technology, Cambridge, Massachusetts 02142, USA;
Leibowitz Mitchell L
Pellman David
References (150)
150 references, click to expand
  1. TERT promoter mutations in familial and sporadic melanoma.
    Science. 2013 Feb 22;339(6122):959-61 PMID: 23348503
  2. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements.
    Cell. 2011 Sep 16;146(6):889-903 PMID: 21925314
  3. Spatial genome organization in the formation of chromosomal translocations.
    Semin Cancer Biol. 2007 Feb;17(1):80-90 PMID: 17137790
  4. The patterns and dynamics of genomic instability in metastatic pancreatic cancer.
    Nature. 2010 Oct 28;467(7319):1109-13 PMID: 20981101
  5. DNA replication timing, genome stability and cancer: late and/or delayed DNA replication timing is associated with increased genomic instability.
    Semin Cancer Biol. 2013 Apr;23(2):80-9 PMID: 23327985
  6. Extrachromosomal amplification mechanisms in a glioma with amplified sequences from multiple chromosome loci.
    Hum Mol Genet. 2010 Apr 1;19(7):1276-85 PMID: 20056677
  7. Chromatin organization is a major influence on regional mutation rates in human cancer cells.
    Nature. 2012 Aug 23;488(7412):504-7 PMID: 22820252
  8. Highly recurrent TERT promoter mutations in human melanoma.
    Science. 2013 Feb 22;339(6122):957-9 PMID: 23348506
  9. Mutational heterogeneity in cancer and the search for new cancer-associated genes.
    Nature. 2013 Jul 11;499(7457):214-218 PMID: 23770567
  10. The p53 response to DNA damage.
    DNA Repair (Amst). 2004 Aug-Sep;3(8-9):1049-56 PMID: 15279792
  11. Chromothripsis and human disease: piecing together the shattering process.
    Cell. 2012 Jan 20;148(1-2):29-32 PMID: 22265399
  12. Estimation of rearrangement phylogeny for cancer genomes.
    Genome Res. 2012 Feb;22(2):346-61 PMID: 21994251
  13. Chromothripsis: chromosomes in crisis.
    Dev Cell. 2012 Nov 13;23(5):908-17 PMID: 23153487
  14. Linking abnormal mitosis to the acquisition of DNA damage.
    J Cell Biol. 2012 Dec 10;199(6):871-81 PMID: 23229895
  15. Patterns of somatic mutation in human cancer genomes.
    Nature. 2007 Mar 8;446(7132):153-8 PMID: 17344846
  16. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells.
    Nature. 2005 Oct 13;437(7061):1043-7 PMID: 16222300
  17. Comprehensive mapping of long-range interactions reveals folding principles of the human genome.
    Science. 2009 Oct 9;326(5950):289-93 PMID: 19815776
  18. Chromothripsis identifies a rare and aggressive entity among newly diagnosed multiple myeloma patients.
    Blood. 2011 Jul 21;118(3):675-8 PMID: 21628407
  19. DNA lesions sequestered in micronuclei induce a local defective-damage response.
    DNA Repair (Amst). 2009 Oct 2;8(10):1225-34 PMID: 19683478
  20. Chromosome instability is common in human cleavage-stage embryos.
    Nat Med. 2009 May;15(5):577-83 PMID: 19396175
  21. Complex landscapes of somatic rearrangement in human breast cancer genomes.
    Nature. 2009 Dec 24;462(7276):1005-10 PMID: 20033038
  22. Poly-gene fusion transcripts and chromothripsis in prostate cancer.
    Genes Chromosomes Cancer. 2012 Dec;51(12):1144-53 PMID: 22927308
  23. Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing.
    Nat Genet. 2008 Jun;40(6):722-9 PMID: 18438408
  24. Haplotype phasing: existing methods and new developments.
    Nat Rev Genet. 2011 Sep 16;12(10):703-14 PMID: 21921926
  25. Evolution of the cancer genome.
    Nat Rev Genet. 2012 Nov;13(11):795-806 PMID: 23044827
  26. Double minute chromosomes in glioblastoma multiforme are revealed by precise reconstruction of oncogenic amplicons.
    Cancer Res. 2013 Oct 1;73(19):6036-45 PMID: 23940299
  27. Commonality but diversity in cancer gene fusions.
    Cell. 2009 May 1;137(3):391-5 PMID: 19410533
  28. Hallmarks of cancer: the next generation.
    Cell. 2011 Mar 4;144(5):646-74 PMID: 21376230
  29. Fine-scale structural variation of the human genome.
    Nat Genet. 2005 Jul;37(7):727-32 PMID: 15895083
  30. The DNA replication FoSTeS/MMBIR mechanism can generate genomic, genic and exonic complex rearrangements in humans.
    Nat Genet. 2009 Jul;41(7):849-53 PMID: 19543269
  31. The large-scale distribution of somatic mutations in cancer genomes.
    Hum Mutat. 2012 Jan;33(1):136-43 PMID: 21953857
  32. Architectures of somatic genomic rearrangement in human cancer amplicons at sequence-level resolution.
    Genome Res. 2007 Sep;17(9):1296-303 PMID: 17675364
  33. Gene amplification as double minutes or homogeneously staining regions in solid tumors: origin and structure.
    Genome Res. 2010 Sep;20(9):1198-206 PMID: 20631050
  34. Absolute quantification of somatic DNA alterations in human cancer.
    Nat Biotechnol. 2012 May;30(5):413-21 PMID: 22544022
  35. Catastrophic nuclear envelope collapse in cancer cell micronuclei.
    Cell. 2013 Jul 3;154(1):47-60 PMID: 23827674
  36. Mechanisms for Structural Variation in the Human Genome.
    Curr Genet Med Rep. 2013 Jun 1;1(2):81-90 PMID: 23730541
  37. Recombination-restarted replication makes inverted chromosome fusions at inverted repeats.
    Nature. 2013 Jan 10;493(7431):246-9 PMID: 23178809
  38. Human aneuploidy: mechanisms and new insights into an age-old problem.
    Nat Rev Genet. 2012 Jun 18;13(7):493-504 PMID: 22705668
  39. Gene amplification: yeast takes a turn.
    Cell. 2006 Jun 30;125(7):1237-40 PMID: 16814711
  40. Mutational processes molding the genomes of 21 breast cancers.
    Cell. 2012 May 25;149(5):979-93 PMID: 22608084
  41. DNA replication timing and long-range DNA interactions predict mutational landscapes of cancer genomes.
    Nat Biotechnol. 2011 Nov 20;29(12):1103-8 PMID: 22101487
  42. Genomic instability--an evolving hallmark of cancer.
    Nat Rev Mol Cell Biol. 2010 Mar;11(3):220-8 PMID: 20177397
  43. Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects.
    Cell Res. 2008 Jan;18(1):73-84 PMID: 18166977
  44. Functional genomic analysis of chromosomal aberrations in a compendium of 8000 cancer genomes.
    Genome Res. 2013 Feb;23(2):217-27 PMID: 23132910
  45. Cell-cycle checkpoints and cancer.
    Nature. 2004 Nov 18;432(7015):316-23 PMID: 15549093
  46. The human cleavage stage embryo is a cradle of chromosomal rearrangements.
    Cytogenet Genome Res. 2011;133(2-4):160-8 PMID: 21311182
  47. Half or more of the somatic mutations in cancers of self-renewing tissues originate prior to tumor initiation.
    Proc Natl Acad Sci U S A. 2013 Feb 5;110(6):1999-2004 PMID: 23345422
  48. Constitutional chromothripsis rearrangements involve clustered double-stranded DNA breaks and nonhomologous repair mechanisms.
    Cell Rep. 2012 Jun 28;1(6):648-55 PMID: 22813740
  49. Chromoanagenesis and cancer: mechanisms and consequences of localized, complex chromosomal rearrangements.
    Nat Med. 2012 Nov;18(11):1630-8 PMID: 23135524
  50. Cancer genome landscapes.
    Science. 2013 Mar 29;339(6127):1546-58 PMID: 23539594
  51. Chromothripsis is a common mechanism driving genomic rearrangements in primary and metastatic colorectal cancer.
    Genome Biol. 2011 Oct 19;12(10):R103 PMID: 22014273
  52. Transient nuclear envelope rupturing during interphase in human cancer cells.
    Nucleus. 2012 Jan-Feb;3(1):88-100 PMID: 22567193
  53. The haplotype-resolved genome and epigenome of the aneuploid HeLa cancer cell line.
    Nature. 2013 Aug 8;500(7461):207-11 PMID: 23925245
  54. Human mutation rate associated with DNA replication timing.
    Nat Genet. 2009 Apr;41(4):393-5 PMID: 19287383
  55. Chromothripsis and cancer: causes and consequences of chromosome shattering.
    Nat Rev Cancer. 2012 Oct;12(10):663-70 PMID: 22972457
  56. Inverted genomic segments and complex triplication rearrangements are mediated by inverted repeats in the human genome.
    Nat Genet. 2011 Oct 02;43(11):1074-81 PMID: 21964572
  57. Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions.
    Mol Cell. 2012 May 25;46(4):424-35 PMID: 22607975
  58. Premature condensation induces breaks at the interface of early and late replicating chromosome bands bearing common fragile sites.
    Proc Natl Acad Sci U S A. 2005 Dec 13;102(50):18069-74 PMID: 16330769
  59. Mutational and structural analysis of diffuse large B-cell lymphoma using whole-genome sequencing.
    Blood. 2013 Aug 15;122(7):1256-65 PMID: 23699601
  60. Causes and consequences of aneuploidy in cancer.
    Nat Rev Genet. 2012 Jan 24;13(3):189-203 PMID: 22269907
  61. Melanoma genome sequencing reveals frequent PREX2 mutations.
    Nature. 2012 May 09;485(7399):502-6 PMID: 22622578
  62. Chromothripsis as a mechanism driving complex de novo structural rearrangements in the germline.
    Hum Mol Genet. 2011 May 15;20(10):1916-24 PMID: 21349919
  63. The emerging role of nuclear architecture in DNA repair and genome maintenance.
    Nat Rev Mol Cell Biol. 2009 Apr;10(4):243-54 PMID: 19277046
  64. Gene fusions by chromothripsis of chromosome 5q in the VCaP prostate cancer cell line.
    Hum Genet. 2013 Jun;132(6):709-13 PMID: 23615946
  65. Transcription as a source of genome instability.
    Nat Rev Genet. 2012 Feb 14;13(3):204-14 PMID: 22330764
  66. Chromothripsis in congenital disorders and cancer: similarities and differences.
    Curr Opin Cell Biol. 2013 Jun;25(3):341-8 PMID: 23478216
  67. High order chromatin architecture shapes the landscape of chromosomal alterations in cancer.
    Nat Biotechnol. 2011 Nov 20;29(12):1109-13 PMID: 22101486
  68. Impact of replication timing on non-CpG and CpG substitution rates in mammalian genomes.
    Genome Res. 2010 Apr;20(4):447-57 PMID: 20103589
  69. The strength of combined cytogenetic and mate-pair sequencing techniques illustrated by a germline chromothripsis rearrangement involving FOXP2.
    Eur J Hum Genet. 2014 Mar;22(3):338-43 PMID: 23860044
  70. On the mechanism of gene amplification induced under stress in Escherichia coli.
    PLoS Genet. 2006 Apr;2(4):e48 PMID: 16604155
  71. Replication stress induces genome-wide copy number changes in human cells that resemble polymorphic and pathogenic variants.
    Am J Hum Genet. 2009 Mar;84(3):339-50 PMID: 19232554
  72. Genomic sequencing of meningiomas identifies oncogenic SMO and AKT1 mutations.
    Nat Genet. 2013 Mar;45(3):285-9 PMID: 23334667
  73. The human leulocyte test system. VII. Further investigations concerning micronucleus-derived premature chromosome condensation.
    Humangenetik. 1975 Nov 6;30(2):143-54 PMID: 1193601
  74. Chromosome pulverization in human binucleate cells following colcemid treatment.
    J Cell Biol. 1967 Jul;34(1):35-45 PMID: 6033541
  75. Reconstructing tumor genome architectures.
    Bioinformatics. 2003 Oct;19 Suppl 2:ii162-71 PMID: 14534186
  76. Chromothripsis in Hodgkin lymphoma.
    Genes Chromosomes Cancer. 2013 Aug;52(8):741-7 PMID: 23630094
  77. Replication stress and genome rearrangements: lessons from yeast models.
    Curr Opin Genet Dev. 2013 Apr;23(2):132-9 PMID: 23267817
  78. Computational methods for discovering structural variation with next-generation sequencing.
    Nat Methods. 2009 Nov;6(11 Suppl):S13-20 PMID: 19844226
  79. The DNA-damage response in human biology and disease.
    Nature. 2009 Oct 22;461(7267):1071-8 PMID: 19847258
  80. Characterization at nucleotide resolution of the homogeneously staining region sites of insertion in two cancer cell lines.
    Nucleic Acids Res. 2013 Sep;41(17):8210-9 PMID: 23821669
  81. Genome-wide identification of genes with amplification and/or fusion in small cell lung cancer.
    Genes Chromosomes Cancer. 2013 Sep;52(9):802-16 PMID: 23716474
  82. The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks.
    Cell. 2006 Jun 30;125(7):1283-96 PMID: 16814715
  83. Melanoma-associated mutations in protein phosphatase 6 cause chromosome instability and DNA damage owing to dysregulated Aurora-A.
    J Cell Sci. 2013 Aug 1;126(Pt 15):3429-40 PMID: 23729733
  84. Mammalian cell fusion: induction of premature chromosome condensation in interphase nuclei.
    Nature. 1970 May 23;226(5247):717-22 PMID: 5443247
  85. The landscape of somatic copy-number alteration across human cancers.
    Nature. 2010 Feb 18;463(7283):899-905 PMID: 20164920
  86. Massive genomic rearrangement acquired in a single catastrophic event during cancer development.
    Cell. 2011 Jan 7;144(1):27-40 PMID: 21215367
  87. Genomic restructuring in the Tasmanian devil facial tumour: chromosome painting and gene mapping provide clues to evolution of a transmissible tumour.
    PLoS Genet. 2012;8(2):e1002483 PMID: 22359511
  88. Higher-order genome organization in human disease.
    Cold Spring Harb Perspect Biol. 2010 Aug;2(8):a000794 PMID: 20591991
  89. Boveri revisited: chromosomal instability, aneuploidy and tumorigenesis.
    Nat Rev Mol Cell Biol. 2009 Jul;10(7):478-87 PMID: 19546858
  90. Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes.
    Nature. 2012 Feb 22;483(7391):589-93 PMID: 22367537
  91. The cancer genome.
    Nature. 2009 Apr 9;458(7239):719-24 PMID: 19360079
  92. Signatures of mutation and selection in the cancer genome.
    Nature. 2010 Feb 18;463(7283):893-8 PMID: 20164919
  93. Diverse mechanisms of somatic structural variations in human cancer genomes.
    Cell. 2013 May 9;153(4):919-29 PMID: 23663786
  94. Variation in the mutation rate across mammalian genomes.
    Nat Rev Genet. 2011 Oct 04;12(11):756-66 PMID: 21969038
  95. The genomic complexity of primary human prostate cancer.
    Nature. 2011 Feb 10;470(7333):214-20 PMID: 21307934
  96. Punctuated evolution of prostate cancer genomes.
    Cell. 2013 Apr 25;153(3):666-77 PMID: 23622249
  97. Oncogene-dependent apoptosis in extracts from drug-resistant cells.
    Genes Dev. 1997 May 15;11(10):1266-76 PMID: 9171371
  98. The clonal evolution of tumor cell populations.
    Science. 1976 Oct 1;194(4260):23-8 PMID: 959840
  99. Chromosomal breakage-fusion-bridge events cause genetic intratumor heterogeneity.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5357-62 PMID: 10805796
  100. Single-cell sequencing-based technologies will revolutionize whole-organism science.
    Nat Rev Genet. 2013 Sep;14(9):618-30 PMID: 23897237
  101. Mutations arising during repair of chromosome breaks.
    Annu Rev Genet. 2012;46:455-73 PMID: 23146099
  102. Mechanisms of programmed DNA lesions and genomic instability in the immune system.
    Cell. 2013 Jan 31;152(3):417-29 PMID: 23374339
  103. TP53 mutations in human cancers: origins, consequences, and clinical use.
    Cold Spring Harb Perspect Biol. 2010 Jan;2(1):a001008 PMID: 20182602
  104. An oncogene-induced DNA damage model for cancer development.
    Science. 2008 Mar 7;319(5868):1352-5 PMID: 18323444
  105. Resolution of anaphase bridges in cancer cells.
    Chromosoma. 2004 Jun;112(8):389-97 PMID: 15156327
  106. Sporadic and reversible chromothripsis in chronic lymphocytic leukemia revealed by longitudinal genomic analysis.
    Leukemia. 2013 Dec;27(12):2376-9 PMID: 23612016
  107. The genomic and transcriptomic landscape of a HeLa cell line.
    G3 (Bethesda). 2013 Aug 07;3(8):1213-24 PMID: 23550136
  108. A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders.
    Cell. 2007 Dec 28;131(7):1235-47 PMID: 18160035
  109. Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations.
    Cell. 2002 Jun 28;109(7):811-21 PMID: 12110179
  110. Cancer: When catastrophe strikes a cell.
    Nature. 2011 Feb 24;470(7335):476-7 PMID: 21350479
  111. Pan-cancer patterns of somatic copy number alteration.
    Nat Genet. 2013 Oct;45(10):1134-40 PMID: 24071852
  112. Break-induced DNA replication.
    Cold Spring Harb Perspect Biol. 2013 Dec 01;5(12):a010397 PMID: 23881940
  113. Differential relationship of DNA replication timing to different forms of human mutation and variation.
    Am J Hum Genet. 2012 Dec 7;91(6):1033-40 PMID: 23176822
  114. De novo CNV formation in mouse embryonic stem cells occurs in the absence of Xrcc4-dependent nonhomologous end joining.
    PLoS Genet. 2012 Sep;8(9):e1002981 PMID: 23028374
  115. Chromothripsis and focal copy number alterations determine poor outcome in malignant melanoma.
    Cancer Res. 2013 Mar 1;73(5):1454-60 PMID: 23271725
  116. Delayed replication timing leads to delayed mitotic chromosome condensation and chromosomal instability of chromosome translocations.
    Proc Natl Acad Sci U S A. 2001 Nov 6;98(23):13300-5 PMID: 11698686
  117. Breakpoint profiling of 64 cancer genomes reveals numerous complex rearrangements spawned by homology-independent mechanisms.
    Genome Res. 2013 May;23(5):762-76 PMID: 23410887
  118. Paired-end mapping reveals extensive structural variation in the human genome.
    Science. 2007 Oct 19;318(5849):420-6 PMID: 17901297
  119. Signatures of mutational processes in human cancer.
    Nature. 2013 Aug 22;500(7463):415-21 PMID: 23945592
  120. Characterizing complex structural variation in germline and somatic genomes.
    Trends Genet. 2012 Jan;28(1):43-53 PMID: 22094265
  121. Proliferation of aneuploid human cells is limited by a p53-dependent mechanism.
    J Cell Biol. 2010 Feb 8;188(3):369-81 PMID: 20123995
  122. Common fragile sites: mechanisms of instability revisited.
    Trends Genet. 2012 Jan;28(1):22-32 PMID: 22094264
  123. Multiple meiotic errors caused by predivision of chromatids in women of advanced maternal age undergoing in vitro fertilisation.
    Eur J Hum Genet. 2012 Jul;20(7):742-7 PMID: 22317970
  124. DNA breaks and chromosome pulverization from errors in mitosis.
    Nature. 2012 Jan 18;482(7383):53-8 PMID: 22258507
  125. Accumulation of driver and passenger mutations during tumor progression.
    Proc Natl Acad Sci U S A. 2010 Oct 26;107(43):18545-50 PMID: 20876136
  126. Spatial proximity of translocation-prone gene loci in human lymphomas.
    Nat Genet. 2003 Jul;34(3):287-91 PMID: 12808455
  127. Complex rearrangements in patients with duplications of MECP2 can occur by fork stalling and template switching.
    Hum Mol Genet. 2009 Jun 15;18(12):2188-203 PMID: 19324899
  128. Complex reorganization and predominant non-homologous repair following chromosomal breakage in karyotypically balanced germline rearrangements and transgenic integration.
    Nat Genet. 2012 Mar 04;44(4):390-7, S1 PMID: 22388000
  129. Mechanisms of change in gene copy number.
    Nat Rev Genet. 2009 Aug;10(8):551-64 PMID: 19597530
  130. Characterization of uterine leiomyomas by whole-genome sequencing.
    N Engl J Med. 2013 Jul 4;369(1):43-53 PMID: 23738515
  131. The Stability of Broken Ends of Chromosomes in Zea Mays.
    Genetics. 1941 Mar;26(2):234-82 PMID: 17247004
  132. Increased mutagenesis and unique mutation signature associated with mitotic gene conversion.
    Science. 2010 Jul 2;329(5987):82-5 PMID: 20595613
  133. Criteria for inference of chromothripsis in cancer genomes.
    Cell. 2013 Mar 14;152(6):1226-36 PMID: 23498933
  134. The impact of translocations and gene fusions on cancer causation.
    Nat Rev Cancer. 2007 Apr;7(4):233-45 PMID: 17361217
  135. Abrogation of oncogene-associated apoptosis allows transformation of p53-deficient cells.
    Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2026-30 PMID: 8134344
  136. Genome sequencing of pediatric medulloblastoma links catastrophic DNA rearrangements with TP53 mutations.
    Cell. 2012 Jan 20;148(1-2):59-71 PMID: 22265402
  137. Cancer genomes evolve by pulverizing single chromosomes.
    Cell. 2011 Jan 7;144(1):9-10 PMID: 21215363
  138. Chromothripsis under the microscope: a cytogenetic perspective of two cases of AML with catastrophic chromosome rearrangement.
    Cancer Genet. 2013 Jun;206(6):238-51 PMID: 23911237
  139. Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma.
    Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):20007-12 PMID: 18077431
  140. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer.
    Cell. 2009 Dec 11;139(6):1069-83 PMID: 19962179
  141. Chromatin condensation dynamics and implications of induced premature chromosome condensation.
    Biochimie. 2013 Feb;95(2):124-33 PMID: 23079335
  142. Recent progress in understanding mechanisms of mammalian DNA amplification.
    Cell. 1989 Jun 16;57(6):901-8 PMID: 2661014
  143. TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal.
    Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):6021-6 PMID: 23530248
  144. Clonal evolution in cancer.
    Nature. 2012 Jan 18;481(7381):306-13 PMID: 22258609
  145. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions.
    Nature. 2005 Apr 14;434(7035):907-13 PMID: 15829965
  146. Subgroup-specific structural variation across 1,000 medulloblastoma genomes.
    Nature. 2012 Aug 2;488(7409):49-56 PMID: 22832581
  147. Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements.
    Nat Genet. 2010 Aug;42(8):668-75 PMID: 20601956
  148. Complex human chromosomal and genomic rearrangements.
    Trends Genet. 2009 Jul;25(7):298-307 PMID: 19560228
  149. Mechanisms for recurrent and complex human genomic rearrangements.
    Curr Opin Genet Dev. 2012 Jun;22(3):211-20 PMID: 22440479
  150. Novel patterns of genome rearrangement and their association with survival in breast cancer.
    Genome Res. 2006 Dec;16(12):1465-79 PMID: 17142309
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
1549-5477
Published
2013-12-01
Pages
2513-30
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC3861665
Subset
IM
Grants
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · GM083299 · United States
NCI NIH HHS · U24CA143867 · United States
NIGMS NIH HHS · R01 GM083299 · United States
NCI NIH HHS · U24 CA143867 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com