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Pervasive chromosomal instability and karyotype order in tumour evolution

by Wilson, Gareth A. , Petkovic, Marina , Rosenthal, Rachel , Cresswell, George D. , Turajlic, Samra , Dentro, Stefan C. , Horswell, Stuart , Tjan-Heijnen, Vivianne C. G. , McGranahan, Nicholas , Cho, Raymond J. , Swanton, Charles , Haase, Kerstin , Loi, Sherene , Dyrskjøt, Lars , Campbell, Peter J. , Andre, Fabrice , Elizalde, Sergi , Grönroos, Eva , Au, Lewis , Dietzen, Michelle , Vicier, Cécile , Brastianos, Priscilla K. , Jamal-Hanjani, Mariam , Litchfield, Kevin , Bastian, Boris C. , Rowan, Andrew , Demeulemeester, Jonas , Yates, Lucy R. , Escudero, Mickael , Tomlinson, Ian P. M. , Szallasi, Zoltan , Savas, Peter , Lim, Emilia L. , Biswas, Dhruva , Lamy, Philippe , Lu, Wei Ting , Castro-Giner, Francesc , Jönsson, Göran B. , Luscombe, Nicholas M. , Spain, Lavinia , Caramia, Franco , Steeghs, Neeltje , Dewhurst, Sally M. , Birkbak, Nicolai J. , Nordentoft, Iver , Bakir, Maise Al , Jaulin, Fanny , Schwarz, Roland F. , Moore, David A. , Harbst, Katja , Watkins, Thomas B. K. , Mourikis, Thanos P. , Xu, Hang , Van Loo, Peter , Bakhoum, Samuel F.

in 631/181/735 / 692/420/755 / 692/699/67/322 / 692/699/67/69 / Antigens / Breast cancer / Cell cycle / Cell division / Chromosomal Instability - genetics / Chromosome 11 / Chromosome 8 / Chromosomes / Chromosomes, Human, Pair 11 - genetics / Chromosomes, Human, Pair 8 - genetics / Clear cell-type renal cell carcinoma / Clone Cells - metabolism / Clone Cells - pathology / Copy number / Cyclin E - genetics / DNA Copy Number Variations - genetics / Dynamic stability / ErbB-2 protein / Evolution / Evolution, Molecular / Female / Gene expression / Genomes / Genomic instability / Heterogeneity / Heterozygosity / Histocompatibility antigen HLA / Humanities and Social Sciences / Humans / Instability / Karyotype / Karyotypes / Kidney cancer / Leukocytes / Loss of heterozygosity / Loss of Heterozygosity - genetics / Male / Mcl-1 protein / Metastases / Metastasis / multidisciplinary / Mutagenesis / Myc protein / Neoplasm Metastasis - genetics / Neoplasm Metastasis - pathology / Neoplasms - genetics / Neoplasms - pathology / Oncogene Proteins - genetics / Science / Science (multidisciplinary) / Tumors

2020

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2020

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2020

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Journal Article

Pervasive chromosomal instability and karyotype order in tumour evolution

Wilson, Gareth A.,

Petkovic, Marina,

Rosenthal, Rachel,

Cresswell, George D.,

Turajlic, Samra,

Dentro, Stefan C.,

Horswell, Stuart,

Tjan-Heijnen, Vivianne C. G.,

McGranahan, Nicholas,

Cho, Raymond J.,

Swanton, Charles,

Haase, Kerstin,

Loi, Sherene,

Dyrskjøt, Lars,

Campbell, Peter J.,

Andre, Fabrice,

Elizalde, Sergi,

Grönroos, Eva,

Au, Lewis,

Dietzen, Michelle,

Vicier, Cécile,

Brastianos, Priscilla K.,

Jamal-Hanjani, Mariam,

Litchfield, Kevin,

Bastian, Boris C.,

Rowan, Andrew,

Demeulemeester, Jonas,

Yates, Lucy R.,

Escudero, Mickael,

Tomlinson, Ian P. M.,

Szallasi, Zoltan,

Savas, Peter,

Lim, Emilia L.,

Biswas, Dhruva,

Lamy, Philippe,

Lu, Wei Ting,

Castro-Giner, Francesc,

Jönsson, Göran B.,

Luscombe, Nicholas M.,

Spain, Lavinia,

Caramia, Franco,

Steeghs, Neeltje,

Dewhurst, Sally M.,

Birkbak, Nicolai J.,

Nordentoft, Iver,

Bakir, Maise Al,

Jaulin, Fanny,

Schwarz, Roland F.,

Moore, David A.,

Harbst, Katja,

Watkins, Thomas B. K.,

Mourikis, Thanos P.,

Xu, Hang,

Van Loo, Peter,

Bakhoum, Samuel F.

2020

Overview

Chromosomal instability in cancer consists of dynamic changes to the number and structure of chromosomes 1 , 2 . The resulting diversity in somatic copy number alterations (SCNAs) may provide the variation necessary for tumour evolution 1 , 3 , 4 . Here we use multi-sample phasing and SCNA analysis of 1,421 samples from 394 tumours across 22 tumour types to show that continuous chromosomal instability results in pervasive SCNA heterogeneity. Parallel evolutionary events, which cause disruption in the same genes (such as BCL9 , MCL1 , ARNT (also known as HIF1B ), TERT and MYC ) within separate subclones, were present in 37% of tumours. Most recurrent losses probably occurred before whole-genome doubling, that was found as a clonal event in 49% of tumours. However, loss of heterozygosity at the human leukocyte antigen (HLA) locus and loss of chromosome 8p to a single haploid copy recurred at substantial subclonal frequencies, even in tumours with whole-genome doubling, indicating ongoing karyotype remodelling. Focal amplifications that affected chromosomes 1q21 (which encompasses BCL9, MCL1 and ARNT ), 5p15.33 ( TERT ), 11q13.3 ( CCND1 ), 19q12 ( CCNE1 ) and 8q24.1 ( MYC ) were frequently subclonal yet appeared to be clonal within single samples. Analysis of an independent series of 1,024 metastatic samples revealed that 13 focal SCNAs were enriched in metastatic samples, including gains in chromosome 8q24.1 (encompassing MYC ) in clear cell renal cell carcinoma and chromosome 11q13.3 (encompassing CCND1 ) in HER2 + breast cancer. Chromosomal instability may enable the continuous selection of SCNAs, which are established as ordered events that often occur in parallel, throughout tumour evolution. Chromosomal instability enables the continuous selection of somatic copy number alterations, which are established as ordered events that often occur in parallel, throughout tumour evolution and metastasis.

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