A versatile system to introduce clusters of genomic double-strand breaks in large cell populations.


Journal

Genes, chromosomes & cancer
ISSN: 1098-2264
Titre abrégé: Genes Chromosomes Cancer
Pays: United States
ID NLM: 9007329

Informations de publication

Date de publication:
05 2021
Historique:
revised: 19 07 2020
received: 10 05 2020
accepted: 21 07 2020
pubmed: 1 8 2020
medline: 16 2 2022
entrez: 1 8 2020
Statut: ppublish

Résumé

In vitro assays for clustered DNA lesions will facilitate the analysis of the mechanisms underlying complex genome rearrangements such as chromothripsis, including the recruitment of repair factors to sites of DNA double-strand breaks (DSBs). We present a novel method generating localized DNA DSBs using UV irradiation with photomasks. The size of the damage foci and the spacing between lesions are fully adjustable, making the assay suitable for different cell types and targeted areas. We validated this setup with genomically stable epithelial cells, normal fibroblasts, pluripotent stem cells, and patient-derived primary cultures. Our method does not require a specialized device such as a laser, making it accessible to a broad range of users. Sensitization by 5-bromo-2-deoxyuridine incorporation is not required, which enables analyzing the DNA damage response in post-mitotic cells. Irradiated cells can be cultivated further, followed by time-lapse imaging or used for downstream biochemical analyses, thanks to the high throughput of the system. Importantly, we showed genome rearrangements in the irradiated cells, providing a proof of principle for the induction of structural variants by localized DNA lesions.

Identifiants

pubmed: 32734664
doi: 10.1002/gcc.22890
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

303-313

Informations de copyright

© 2020 The Authors. Genes, Chromosomes and Cancer published by Wiley Periodicals LLC.

Références

Rausch T, Jones DT, Zapatka M, et al. Genome sequencing of pediatric medulloblastoma links catastrophic DNA rearrangements with TP53 mutations. Cell. 2012;148(1-2):59-71.
Stephens PJ, Greenman CD, Fu B, et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell. 2011;144(1):27-40.
Rode A, Maass KK, Willmund KV, Lichter P, Ernst A. Chromothripsis in cancer cells: an update. Int J Cancer. 2016;138(10):2322-2333.
Ratnaparkhe M, Wong JKL, Wei PC, et al. Defective DNA damage repair leads to frequent catastrophic genomic events in murine and human tumors. Nat Commun. 2018;9(1):4760.
Suzuki K, Yamauchi M, Oka Y, Suzuki M, Yamashita S. Creating localized DNA double-strand breaks with microirradiation. Nat Protoc. 2011;6(2):134-139.
Holton NW, Andrews JF, Gassman NR. Application of laser micro-irradiation for examination of single and double strand break repair in mammalian cells. J Visualized Exp: JoVE. 2017;127:1-12.
Nelms BE, Maser RS, MacKay JF, Lagally MG, Petrini JH. In situ visualization of DNA double-strand break repair in human fibroblasts. Science. 1998;280(5363):590-592.
Morishita M, Muramatsu T, Suto Y, et al. Chromothripsis-like chromosomal rearrangements induced by ionizing radiation using proton microbeam irradiation system. Oncotarget. 2016;7(9):10182-10192.
Klambauer G, Schwarzbauer K, Mayr A, et al. Cn.MOPS: mixture of poissons for discovering copy number variations in next-generation sequencing data with a low false discovery rate. Nucleic Acids Res. 2012;40(9):e69.
Cibulskis K, Lawrence MS, Carter SL, et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotechnol. 2013;31(3):213-219.
Alexandrov LB, Kim J, Haradhvala NJ, et al. The repertoire of mutational signatures in human cancer. Nature. 2020;578(7793):94-101.
Schmezer P, Rajaee-Behbahani N, Risch A, et al. Rapid screening assay for mutagen sensitivity and DNA repair capacity in human peripheral blood lymphocytes. Mutagenesis. 2001;16(1):25-30.
Greve B, Bolling T, Amler S, et al. Evaluation of different biomarkers to predict individual radiosensitivity in an inter-laboratory comparison-lessons for future studies. PLoS One. 2012;7(10):e47185.
Datta K, Neumann RD, Winters TA. Characterization of complex apurinic/apyrimidinic-site clustering associated with an authentic site-specific radiation-induced DNA double-strand break. Proc Natl Acad Sci U S A. 2005;102(30):10569-10574.
Jiang Y, Ke C, Mieczkowski PA, Marszalek PE. Detecting ultraviolet damage in single DNA molecules by atomic force microscopy. Biophys J. 2007;93(5):1758-1767.
Lehner B, Sandner B, Marschallinger J, et al. The dark side of BrdU in neural stem cell biology: detrimental effects on cell cycle, differentiation and survival. Cell Tissue Res. 2011;345(3):313-328.
Potapova TA, Unruh JR, Box AC, et al. Karyotyping human and mouse cells using probes from single-sorted chromosomes and open source software. BioTechniques. 2015;59(6):335-336. 338, 340-332 passim.
Zhang CZ, Spektor A, Cornils H, et al. Chromothripsis from DNA damage in micronuclei. Nature. 2015;522(7555):179-184.
Maitra A, Arking DE, Shivapurkar N, et al. Genomic alterations in cultured human embryonic stem cells. Nat Genet. 2005;37(10):1099-1103.
Maciejowski J, Li Y, Bosco N, Campbell PJ, de Lange T. Chromothripsis and Kataegis induced by telomere crisis. Cell. 2015;163(7):1641-1654.
Mardin BR, Drainas AP, Waszak SM, et al. A cell-based model system links chromothripsis with hyperploidy. Mol Syst Biol. 2015;11(9):828.

Auteurs

Thorsten Kolb (T)

Group Genome Instability in Tumors, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Umar Khalid (U)

Group Genome Instability in Tumors, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Milena Simović (M)

Group Genome Instability in Tumors, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Manasi Ratnaparkhe (M)

Group Genome Instability in Tumors, German Cancer Research Center (DKFZ), Heidelberg, Germany.

John Wong (J)

Division of Molecular Genetics, German Cancer Research Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Anna Jauch (A)

Institute of Human Genetics, University of Heidelberg, Heidelberg, Germany.

Peter Schmezer (P)

Division of Epigenomics and Cancer Risk Factors, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Agata Rode (A)

Division of Molecular Genetics, German Cancer Research Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Shulamit Sebban (S)

Department of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem, Israel.

Daniel Haag (D)

Hopp Children's Cancer Center at the NCT (KiTZ), Heidelberg, Germany.

Michaela Hergt (M)

Group Genome Instability in Tumors, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Frauke Devens (F)

Group Genome Instability in Tumors, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Yosef Buganim (Y)

Department of Developmental Biology and Cancer Research, Institute for Medical Research Israel-Canada, The Hebrew University-Hadassah Medical School, Jerusalem, Israel.

Marc Zapatka (M)

Division of Molecular Genetics, German Cancer Research Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Peter Lichter (P)

Division of Molecular Genetics, German Cancer Research Consortium (DKTK), German Cancer Research Center (DKFZ), Heidelberg, Germany.

Aurélie Ernst (A)

Group Genome Instability in Tumors, German Cancer Research Center (DKFZ), Heidelberg, Germany.

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