Signatures of copy number alterations in human cancer
Gains and losses of DNA are prevalent in cancer and emerge as a consequence of inter-related processes of replication stress, mitotic errors, spindle multipolarity and breakage–fusion–bridge cycles, among others, which may lead to chromosomal instability and aneuploidy 1 , 2 . These copy number alte...
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| Published in: | Nature (London) Vol. 606; no. 7916; pp. 984 - 991 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
London
Nature Publishing Group UK
30.06.2022
Nature Publishing Group |
| Subjects: | |
| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
| Online Access: | Get full text |
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| Abstract | Gains and losses of DNA are prevalent in cancer and emerge as a consequence of inter-related processes of replication stress, mitotic errors, spindle multipolarity and breakage–fusion–bridge cycles, among others, which may lead to chromosomal instability and aneuploidy
1
,
2
. These copy number alterations contribute to cancer initiation, progression and therapeutic resistance
3
–
5
. Here we present a conceptual framework to examine the patterns of copy number alterations in human cancer that is widely applicable to diverse data types, including whole-genome sequencing, whole-exome sequencing, reduced representation bisulfite sequencing, single-cell DNA sequencing and SNP6 microarray data. Deploying this framework to 9,873 cancers representing 33 human cancer types from The Cancer Genome Atlas
6
revealed a set of 21 copy number signatures that explain the copy number patterns of 97% of samples. Seventeen copy number signatures were attributed to biological phenomena of whole-genome doubling, aneuploidy, loss of heterozygosity, homologous recombination deficiency, chromothripsis and haploidization. The aetiologies of four copy number signatures remain unexplained. Some cancer types harbour amplicon signatures associated with extrachromosomal DNA, disease-specific survival and proto-oncogene gains such as
MDM2
. In contrast to base-scale mutational signatures, no copy number signature was associated with many known exogenous cancer risk factors. Our results synthesize the global landscape of copy number alterations in human cancer by revealing a diversity of mutational processes that give rise to these alterations.
A new framework enables a pan-cancer reference set of copy number signatures derived from allele-specific profiles from different experimental assays. |
|---|---|
| AbstractList | Gains and losses of DNA are prevalent in cancer and emerge as a consequence of inter-related processes of replication stress, mitotic errors, spindle multipolarity and breakage–fusion–bridge cycles, among others, which may lead to chromosomal instability and aneuploidy1,2. These copy number alterations contribute to cancer initiation, progression and therapeutic resistance3–5. Here we present a conceptual framework to examine the patterns of copy number alterations in human cancer that is widely applicable to diverse data types, including whole-genome sequencing, whole-exome sequencing, reduced representation bisulfite sequencing, single-cell DNA sequencing and SNP6 microarray data. Deploying this framework to 9,873 cancers representing 33 human cancer types from The Cancer Genome Atlas6 revealed a set of 21 copy number signatures that explain the copy number patterns of 97% of samples. Seventeen copy number signatures were attributed to biological phenomena of whole-genome doubling, aneuploidy, loss of heterozygosity, homologous recombination deficiency, chromothripsis and haploidization. The aetiologies of four copy number signatures remain unexplained. Some cancer types harbour amplicon signatures associated with extrachromosomal DNA, disease-specific survival and proto-oncogene gains such as MDM2. In contrast to base-scale mutational signatures, no copy number signature was associated with many known exogenous cancer risk factors. Our results synthesize the global landscape of copy number alterations in human cancer by revealing a diversity of mutational processes that give rise to these alterations. A new framework enables a pan-cancer reference set of copy number signatures derived from allele-specific profiles from different experimental assays. Gains and losses of DNA are prevalent in cancer and emerge as a consequence of inter-related processes of replication stress, mitotic errors, spindle multipolarity and breakage–fusion–bridge cycles, among others, which may lead to chromosomal instability and aneuploidy 1 , 2 . These copy number alterations contribute to cancer initiation, progression and therapeutic resistance 3 – 5 . Here we present a conceptual framework to examine the patterns of copy number alterations in human cancer that is widely applicable to diverse data types, including whole-genome sequencing, whole-exome sequencing, reduced representation bisulfite sequencing, single-cell DNA sequencing and SNP6 microarray data. Deploying this framework to 9,873 cancers representing 33 human cancer types from The Cancer Genome Atlas 6 revealed a set of 21 copy number signatures that explain the copy number patterns of 97% of samples. Seventeen copy number signatures were attributed to biological phenomena of whole-genome doubling, aneuploidy, loss of heterozygosity, homologous recombination deficiency, chromothripsis and haploidization. The aetiologies of four copy number signatures remain unexplained. Some cancer types harbour amplicon signatures associated with extrachromosomal DNA, disease-specific survival and proto-oncogene gains such as MDM2 . In contrast to base-scale mutational signatures, no copy number signature was associated with many known exogenous cancer risk factors. Our results synthesize the global landscape of copy number alterations in human cancer by revealing a diversity of mutational processes that give rise to these alterations. A new framework enables a pan-cancer reference set of copy number signatures derived from allele-specific profiles from different experimental assays. Gains and losses of DNA are prevalent in cancer and emerge as a consequence of inter-related processes of replication stress, mitotic errors, spindle multipolarity and breakage-fusion-bridge cycles, among others, which may lead to chromosomal instability and aneuploidy1,2. These copy number alterations contribute to cancer initiation, progression and therapeutic resistance3-5. Here we present a conceptual framework to examine the patterns of copy number alterations in human cancer that is widely applicable to diverse data types, including whole-genome sequencing, whole-exome sequencing, reduced representation bisulfite sequencing, single-cell DNA sequencing and SNP6 microarray data. Deploying this framework to 9,873 cancers representing 33 human cancer types from The Cancer Genome Atlas6 revealed a set of 21 copy number signatures that explain the copy number patterns of 97% of samples. Seventeen copy number signatures were attributed to biological phenomena of whole-genome doubling, aneuploidy, loss of heterozygosity, homologous recombination deficiency, chromothripsis and haploidization. The aetiologies of four copy number signatures remain unexplained. Some cancer types harbour amplicon signatures associated with extrachromosomal DNA, disease-specific survival and proto-oncogene gains such as MDM2. In contrast to base-scale mutational signatures, no copy number signature was associated with many known exogenous cancer risk factors. Our results synthesize the global landscape of copy number alterations in human cancer by revealing a diversity of mutational processes that give rise to these alterations. Gains and losses of DNA are prevalent in cancer and emerge as a consequence of inter-related processes of replication stress, mitotic errors, spindle multipolarity and breakage–fusion–bridge cycles, among others, which may lead to chromosomal instability and aneuploidy 1,2 . These copy number alterations contribute to cancer initiation, progression and therapeutic resistance 3–5 . Here we present a conceptual framework to examine the patterns of copy number alterations in human cancer that is widely applicable to diverse data types, including whole-genome sequencing, whole-exome sequencing, reduced representation bisulfite sequencing, single-cell DNA sequencing and SNP6 microarray data. Deploying this framework to 9,873 cancers representing 33 human cancer types from The Cancer Genome Atlas 6 revealed a set of 21 copy number signatures that explain the copy number patterns of 97% of samples. Seventeen copy number signatures were attributed to biological phenomena of whole-genome doubling, aneuploidy, loss of heterozygosity, homologous recombination deficiency, chromothripsis and haploidization. The aetiologies of four copy number signatures remain unexplained. Some cancer types harbour amplicon signatures associated with extrachromosomal DNA, disease-specific survival and proto-oncogene gains such as MDM2 . In contrast to base-scale mutational signatures, no copy number signature was associated with many known exogenous cancer risk factors. Our results synthesize the global landscape of copy number alterations in human cancer by revealing a diversity of mutational processes that give rise to these alterations. Gains and losses of DNA are prevalent in cancer and emerge as a consequence of inter-related processes of replication stress, mitotic errors, spindle multipolarity and breakage-fusion-bridge cycles, among others, which may lead to chromosomal instability and aneuploidy1,2. These copy number alterations contribute to cancer initiation, progression and therapeutic resistance3-5. Here we present a conceptual framework to examine the patterns of copy number alterations in human cancer that is widely applicable to diverse data types, including whole-genome sequencing, whole-exome sequencing, reduced representation bisulfite sequencing, single-cell DNA sequencing and SNP6 microarray data. Deploying this framework to 9,873 cancers representing 33 human cancer types from The Cancer Genome Atlas6 revealed a set of 21 copy number signatures that explain the copy number patterns of 97% of samples. Seventeen copy number signatures were attributed to biological phenomena of whole-genome doubling, aneuploidy, loss of heterozygosity, homologous recombination deficiency, chromothripsis and haploidization. The aetiologies of four copy number signatures remain unexplained. Some cancer types harbour amplicon signatures associated with extrachromosomal DNA, disease-specific survival and proto-oncogene gains such as MDM2. In contrast to base-scale mutational signatures, no copy number signature was associated with many known exogenous cancer risk factors. Our results synthesize the global landscape of copy number alterations in human cancer by revealing a diversity of mutational processes that give rise to these alterations.Gains and losses of DNA are prevalent in cancer and emerge as a consequence of inter-related processes of replication stress, mitotic errors, spindle multipolarity and breakage-fusion-bridge cycles, among others, which may lead to chromosomal instability and aneuploidy1,2. These copy number alterations contribute to cancer initiation, progression and therapeutic resistance3-5. Here we present a conceptual framework to examine the patterns of copy number alterations in human cancer that is widely applicable to diverse data types, including whole-genome sequencing, whole-exome sequencing, reduced representation bisulfite sequencing, single-cell DNA sequencing and SNP6 microarray data. Deploying this framework to 9,873 cancers representing 33 human cancer types from The Cancer Genome Atlas6 revealed a set of 21 copy number signatures that explain the copy number patterns of 97% of samples. Seventeen copy number signatures were attributed to biological phenomena of whole-genome doubling, aneuploidy, loss of heterozygosity, homologous recombination deficiency, chromothripsis and haploidization. The aetiologies of four copy number signatures remain unexplained. Some cancer types harbour amplicon signatures associated with extrachromosomal DNA, disease-specific survival and proto-oncogene gains such as MDM2. In contrast to base-scale mutational signatures, no copy number signature was associated with many known exogenous cancer risk factors. Our results synthesize the global landscape of copy number alterations in human cancer by revealing a diversity of mutational processes that give rise to these alterations. Gains and losses of DNA are prevalent in cancer and emerge as a consequence of inter-related processes of replication stress, mitotic errors, spindle multipolarity and breakage-fusion-bridge cycles, among others, which may lead to chromosomal instability and aneuploidy . These copy number alterations contribute to cancer initiation, progression and therapeutic resistance . Here we present a conceptual framework to examine the patterns of copy number alterations in human cancer that is widely applicable to diverse data types, including whole-genome sequencing, whole-exome sequencing, reduced representation bisulfite sequencing, single-cell DNA sequencing and SNP6 microarray data. Deploying this framework to 9,873 cancers representing 33 human cancer types from The Cancer Genome Atlas revealed a set of 21 copy number signatures that explain the copy number patterns of 97% of samples. Seventeen copy number signatures were attributed to biological phenomena of whole-genome doubling, aneuploidy, loss of heterozygosity, homologous recombination deficiency, chromothripsis and haploidization. The aetiologies of four copy number signatures remain unexplained. Some cancer types harbour amplicon signatures associated with extrachromosomal DNA, disease-specific survival and proto-oncogene gains such as MDM2. In contrast to base-scale mutational signatures, no copy number signature was associated with many known exogenous cancer risk factors. Our results synthesize the global landscape of copy number alterations in human cancer by revealing a diversity of mutational processes that give rise to these alterations. |
| Author | Lechner, Matt Proszek, Paula Flanagan, Adrienne M. Verfaillie, Annelien McLatchie, Alex Light, Nicholas Dhami, Pawan Haase, Kerstin Ajayi, Dolapo Lesluyes, Tom Pillay, Nischalan Khandekar, Azhar Alexandrov, Ludmil B. Abbasi, Ammal Steele, Christopher D. Bowes, Amy L. Mertens, Fredrik Shlien, Adam Malkin, David Van Loo, Peter Hames-Fathi, Shadi Feber, Andrew Islam, S. M. Ashiqul Tarabichi, Maxime |
| Author_xml | – sequence: 1 givenname: Christopher D. surname: Steele fullname: Steele, Christopher D. organization: Research Department of Pathology, Cancer Institute, University College London – sequence: 2 givenname: Ammal surname: Abbasi fullname: Abbasi, Ammal organization: Department of Cellular and Molecular Medicine, UC San Diego, Department of Bioengineering, UC San Diego, Moores Cancer Center, UC San Diego – sequence: 3 givenname: S. M. Ashiqul surname: Islam fullname: Islam, S. M. Ashiqul organization: Department of Cellular and Molecular Medicine, UC San Diego, Department of Bioengineering, UC San Diego, Moores Cancer Center, UC San Diego – sequence: 4 givenname: Amy L. surname: Bowes fullname: Bowes, Amy L. organization: Research Department of Pathology, Cancer Institute, University College London, Cancer Genomics Laboratory, The Francis Crick Institute – sequence: 5 givenname: Azhar surname: Khandekar fullname: Khandekar, Azhar organization: Department of Cellular and Molecular Medicine, UC San Diego, Department of Bioengineering, UC San Diego, Moores Cancer Center, UC San Diego – sequence: 6 givenname: Kerstin orcidid: 0000-0002-0944-5618 surname: Haase fullname: Haase, Kerstin organization: Cancer Genomics Laboratory, The Francis Crick Institute – sequence: 7 givenname: Shadi surname: Hames-Fathi fullname: Hames-Fathi, Shadi organization: Research Department of Pathology, Cancer Institute, University College London – sequence: 8 givenname: Dolapo surname: Ajayi fullname: Ajayi, Dolapo organization: Research Department of Pathology, Cancer Institute, University College London – sequence: 9 givenname: Annelien surname: Verfaillie fullname: Verfaillie, Annelien organization: Cancer Genomics Laboratory, The Francis Crick Institute – sequence: 10 givenname: Pawan surname: Dhami fullname: Dhami, Pawan organization: CRUK–UCL Cancer Institute Translational Technology Platform (Genomics) – sequence: 11 givenname: Alex surname: McLatchie fullname: McLatchie, Alex organization: CRUK–UCL Cancer Institute Translational Technology Platform (Genomics) – sequence: 12 givenname: Matt orcidid: 0000-0002-7123-0773 surname: Lechner fullname: Lechner, Matt organization: Research Department of Oncology, UCL Cancer Institute – sequence: 13 givenname: Nicholas surname: Light fullname: Light, Nicholas organization: Genetics and Genome Biology, The Hospital for Sick Children, Institute of Medical Science, University of Toronto – sequence: 14 givenname: Adam orcidid: 0000-0002-0368-5370 surname: Shlien fullname: Shlien, Adam organization: Institute of Medical Science, University of Toronto, Department of Laboratory Medicine and Pathobiology, University of Toronto, Department of Paediatric Laboratory Medicine, The Hospital for Sick Children – sequence: 15 givenname: David orcidid: 0000-0001-5752-9763 surname: Malkin fullname: Malkin, David organization: Genetics and Genome Biology, The Hospital for Sick Children, Division of Hematology/Oncology, The Hospital for Sick Children, Department of Paediatrics, University of Toronto – sequence: 16 givenname: Andrew surname: Feber fullname: Feber, Andrew organization: Translational Epigenetics, Division of Molecular Pathology, Institute of Cancer Research, Clinical Genomics, Translational Research Laboratory, Royal Marsden NHS Trust – sequence: 17 givenname: Paula orcidid: 0000-0002-0780-6790 surname: Proszek fullname: Proszek, Paula organization: Translational Epigenetics, Division of Molecular Pathology, Institute of Cancer Research, Clinical Genomics, Translational Research Laboratory, Royal Marsden NHS Trust – sequence: 18 givenname: Tom orcidid: 0000-0003-2251-5884 surname: Lesluyes fullname: Lesluyes, Tom organization: Cancer Genomics Laboratory, The Francis Crick Institute – sequence: 19 givenname: Fredrik orcidid: 0000-0002-6278-5232 surname: Mertens fullname: Mertens, Fredrik organization: Division of Clinical Genetics, Department of Laboratory Medicine, Lund University, Department of Clinical Genetics and Pathology, Division of Laboratory Medicine – sequence: 20 givenname: Adrienne M. orcidid: 0000-0002-2832-1303 surname: Flanagan fullname: Flanagan, Adrienne M. organization: Research Department of Pathology, Cancer Institute, University College London, Department of Cellular and Molecular Pathology, Royal National Orthopaedic Hospital NHS Trust – sequence: 21 givenname: Maxime orcidid: 0000-0002-1635-2348 surname: Tarabichi fullname: Tarabichi, Maxime organization: Cancer Genomics Laboratory, The Francis Crick Institute, Institute for Interdisciplinary Research, Université Libre de Bruxelles – sequence: 22 givenname: Peter orcidid: 0000-0003-0292-1949 surname: Van Loo fullname: Van Loo, Peter organization: Cancer Genomics Laboratory, The Francis Crick Institute – sequence: 23 givenname: Ludmil B. surname: Alexandrov fullname: Alexandrov, Ludmil B. email: L2alexandrov@health.ucsd.edu organization: Department of Cellular and Molecular Medicine, UC San Diego, Department of Bioengineering, UC San Diego, Moores Cancer Center, UC San Diego – sequence: 24 givenname: Nischalan orcidid: 0000-0003-0579-4105 surname: Pillay fullname: Pillay, Nischalan email: N.pillay@ucl.ac.uk organization: Research Department of Pathology, Cancer Institute, University College London, Department of Cellular and Molecular Pathology, Royal National Orthopaedic Hospital NHS Trust |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35705804$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | 13 13/31 45/22 45/23 45/61 631/114/2785 631/67/69 Aneuploidy Basic Medicine Bisulfite Cancer Cancer and Oncology Cancer och onkologi Chromosomes Chromothripsis Clinical Medicine Copy number Deoxyribonucleic acid DNA DNA Copy Number Variations - genetics DNA microarrays DNA Mutational Analysis DNA sequencing Exome Sequencing Genomes Genomic instability Haploidy Health risks Heterozygosity Homologous recombination Homologous Recombination - genetics Homology Humanities and Social Sciences Humans Klinisk medicin Loss of heterozygosity Loss of Heterozygosity - genetics MDM2 protein Medical and Health Sciences Medical Genetics and Genomics (including Gene Therapy) Medicin och hälsovetenskap Medicinsk genetik och genomik (Här ingår: Genterapi) Medicinska och farmaceutiska grundvetenskaper multidisciplinary Mutation Neoplasms - genetics Neoplasms - pathology Ovaries Risk analysis Risk factors Science Science (multidisciplinary) Signatures Whole genome sequencing |
| Title | Signatures of copy number alterations in human cancer |
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