The co-evolution of the genome and epigenome in colorectal cancer

Colorectal malignancies are a leading cause of cancer-related death 1 and have undergone extensive genomic study 2 , 3 . However, DNA mutations alone do not fully explain malignant transformation 4 – 7 . Here we investigate the co-evolution of the genome and epigenome of colorectal tumours at single...

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Published in:	Nature (London) Vol. 611; no. 7937; pp. 733 - 743
Main Authors:	Heide, Timon, Househam, Jacob, Cresswell, George D., Spiteri, Inmaculada, Lynn, Claire, Mossner, Maximilian, Kimberley, Chris, Fernandez-Mateos, Javier, Chen, Bingjie, Zapata, Luis, James, Chela, Barozzi, Iros, Chkhaidze, Ketevan, Nichol, Daniel, Gunasri, Vinaya, Berner, Alison, Schmidt, Melissa, Lakatos, Eszter, Baker, Ann-Marie, Costa, Helena, Mitchinson, Miriam, Piazza, Rocco, Jansen, Marnix, Caravagna, Giulio, Ramazzotti, Daniele, Shibata, Darryl, Bridgewater, John, Rodriguez-Justo, Manuel, Magnani, Luca, Graham, Trevor A., Sottoriva, Andrea
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 24.11.2022 Nature Publishing Group
Subjects:	45 45/23 631/114 631/208/177 631/67/2329 631/67/69 692/699/67/1504/1885 Accessibility Adenoma - genetics Adenoma - pathology Biological evolution Cancer Cell growth Cell Transformation, Neoplastic - genetics Cell Transformation, Neoplastic - metabolism Cell Transformation, Neoplastic - pathology Chromatin Chromatin - genetics Chromatin - metabolism Cloning Coevolution Colorectal cancer Colorectal carcinoma Colorectal Neoplasms - genetics Colorectal Neoplasms - pathology Datasets Deoxyribonucleic acid DNA DNA methylation Epigenetics Epigenome - genetics Evolution Evolution & development Genes Genome, Human - genetics Genomes Heterogeneity Humanities and Social Sciences Humans Interferon Interferons Malignancy multidisciplinary Mutation Oncogenes - genetics Patients Positive selection Regulatory sequences Science Science (multidisciplinary) Signature analysis Transcription factors Transcription Factors - metabolism Transcriptomes Tumorigenesis Tumors
ISSN:	0028-0836, 1476-4687, 1476-4687
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Abstract	Colorectal malignancies are a leading cause of cancer-related death 1 and have undergone extensive genomic study 2 , 3 . However, DNA mutations alone do not fully explain malignant transformation 4 – 7 . Here we investigate the co-evolution of the genome and epigenome of colorectal tumours at single-clone resolution using spatial multi-omic profiling of individual glands. We collected 1,370 samples from 30 primary cancers and 8 concomitant adenomas and generated 1,207 chromatin accessibility profiles, 527 whole genomes and 297 whole transcriptomes. We found positive selection for DNA mutations in chromatin modifier genes and recurrent somatic chromatin accessibility alterations, including in regulatory regions of cancer driver genes that were otherwise devoid of genetic mutations. Genome-wide alterations in accessibility for transcription factor binding involved CTCF, downregulation of interferon and increased accessibility for SOX and HOX transcription factor families, suggesting the involvement of developmental genes during tumourigenesis. Somatic chromatin accessibility alterations were heritable and distinguished adenomas from cancers. Mutational signature analysis showed that the epigenome in turn influences the accumulation of DNA mutations. This study provides a map of genetic and epigenetic tumour heterogeneity, with fundamental implications for understanding colorectal cancer biology. A study maps genetic and epigenetic heterogeneity of primary colorectal adenomas and cancers at single-clone resolution through spatial multi-omic profiling of individual glands and adjacent normal tissue.
AbstractList	Colorectal malignancies are a leading cause of cancer-related death1 and have undergone extensive genomic study2,3. However, DNA mutations alone do not fully explain malignant transformation4-7. Here we investigate the co-evolution of the genome and epigenome of colorectal tumours at single-clone resolution using spatial multi-omic profiling of individual glands. We collected 1,370 samples from 30 primary cancers and 8 concomitant adenomas and generated 1,207 chromatin accessibility profiles, 527 whole genomes and 297 whole transcriptomes. We found positive selection for DNA mutations in chromatin modifier genes and recurrent somatic chromatin accessibility alterations, including in regulatory regions of cancer driver genes that were otherwise devoid of genetic mutations. Genome-wide alterations in accessibility for transcription factor binding involved CTCF, downregulation of interferon and increased accessibility for SOX and HOX transcription factor families, suggesting the involvement of developmental genes during tumourigenesis. Somatic chromatin accessibility alterations were heritable and distinguished adenomas from cancers. Mutational signature analysis showed that the epigenome in turn influences the accumulation of DNA mutations. This study provides a map of genetic and epigenetic tumour heterogeneity, with fundamental implications for understanding colorectal cancer biology. Colorectal malignancies are a leading cause of cancer-related death 1 and have undergone extensive genomic study 2 , 3 . However, DNA mutations alone do not fully explain malignant transformation 4 – 7 . Here we investigate the co-evolution of the genome and epigenome of colorectal tumours at single-clone resolution using spatial multi-omic profiling of individual glands. We collected 1,370 samples from 30 primary cancers and 8 concomitant adenomas and generated 1,207 chromatin accessibility profiles, 527 whole genomes and 297 whole transcriptomes. We found positive selection for DNA mutations in chromatin modifier genes and recurrent somatic chromatin accessibility alterations, including in regulatory regions of cancer driver genes that were otherwise devoid of genetic mutations. Genome-wide alterations in accessibility for transcription factor binding involved CTCF, downregulation of interferon and increased accessibility for SOX and HOX transcription factor families, suggesting the involvement of developmental genes during tumourigenesis. Somatic chromatin accessibility alterations were heritable and distinguished adenomas from cancers. Mutational signature analysis showed that the epigenome in turn influences the accumulation of DNA mutations. This study provides a map of genetic and epigenetic tumour heterogeneity, with fundamental implications for understanding colorectal cancer biology. A study maps genetic and epigenetic heterogeneity of primary colorectal adenomas and cancers at single-clone resolution through spatial multi-omic profiling of individual glands and adjacent normal tissue. Colorectal malignancies are a leading cause of cancer-related death1 and have undergone extensive genomic study2,3. However, DNA mutations alone do not fully explain malignant transformation4-7. Here we investigate the co-evolution of the genome and epigenome of colorectal tumours at single-clone resolution using spatial multi-omic profiling of individual glands. We collected 1,370 samples from 30 primary cancers and 8 concomitant adenomas and generated 1,207 chromatin accessibility profiles, 527 whole genomes and 297 whole transcriptomes. We found positive selection for DNA mutations in chromatin modifier genes and recurrent somatic chromatin accessibility alterations, including in regulatory regions of cancer driver genes that were otherwise devoid of genetic mutations. Genome-wide alterations in accessibility for transcription factor binding involved CTCF, downregulation of interferon and increased accessibility for SOX and HOX transcription factor families, suggesting the involvement of developmental genes during tumourigenesis. Somatic chromatin accessibility alterations were heritable and distinguished adenomas from cancers. Mutational signature analysis showed that the epigenome in turn influences the accumulation of DNA mutations. This study provides a map of genetic and epigenetic tumour heterogeneity, with fundamental implications for understanding colorectal cancer biology.Colorectal malignancies are a leading cause of cancer-related death1 and have undergone extensive genomic study2,3. However, DNA mutations alone do not fully explain malignant transformation4-7. Here we investigate the co-evolution of the genome and epigenome of colorectal tumours at single-clone resolution using spatial multi-omic profiling of individual glands. We collected 1,370 samples from 30 primary cancers and 8 concomitant adenomas and generated 1,207 chromatin accessibility profiles, 527 whole genomes and 297 whole transcriptomes. We found positive selection for DNA mutations in chromatin modifier genes and recurrent somatic chromatin accessibility alterations, including in regulatory regions of cancer driver genes that were otherwise devoid of genetic mutations. Genome-wide alterations in accessibility for transcription factor binding involved CTCF, downregulation of interferon and increased accessibility for SOX and HOX transcription factor families, suggesting the involvement of developmental genes during tumourigenesis. Somatic chromatin accessibility alterations were heritable and distinguished adenomas from cancers. Mutational signature analysis showed that the epigenome in turn influences the accumulation of DNA mutations. This study provides a map of genetic and epigenetic tumour heterogeneity, with fundamental implications for understanding colorectal cancer biology. Colorectal malignancies are a leading cause of cancer-related death1 and have undergone extensive genomic study2,3. However, DNA mutations alone do not fully explain malignant transformation4–7. Here we investigate the co-evolution of the genome and epigenome of colorectal tumours at single-clone resolution using spatial multi-omic profiling of individual glands. We collected 1,370 samples from 30 primary cancers and 8 concomitant adenomas and generated 1,207 chromatin accessibility profiles, 527 whole genomes and 297 whole transcriptomes. We found positive selection for DNA mutations in chromatin modifier genes and recurrent somatic chromatin accessibility alterations, including in regulatory regions of cancer driver genes that were otherwise devoid of genetic mutations. Genome-wide alterations in accessibility for transcription factor binding involved CTCF, downregulation of interferon and increased accessibility for SOX and HOX transcription factor families, suggesting the involvement of developmental genes during tumourigenesis. Somatic chromatin accessibility alterations were heritable and distinguished adenomas from cancers. Mutational signature analysis showed that the epigenome in turn influences the accumulation of DNA mutations. This study provides a map of genetic and epigenetic tumour heterogeneity, with fundamental implications for understanding colorectal cancer biology. A study maps genetic and epigenetic heterogeneity of primary colorectal adenomas and cancers at single-clone resolution through spatial multi-omic profiling of individual glands and adjacent normal tissue. Colorectal malignancies are a leading cause of cancer-related death 1 and have undergone extensive genomic study 2,3 . However, DNA mutations alone do not fully explain malignant transformation 4–7 . Here we investigate the co-evolution of the genome and epigenome of colorectal tumours at single-clone resolution using spatial multi-omic profiling of individual glands. We collected 1,370 samples from 30 primary cancers and 8 concomitant adenomas and generated 1,207 chromatin accessibility profiles, 527 whole genomes and 297 whole transcriptomes. We found positive selection for DNA mutations in chromatin modifier genes and recurrent somatic chromatin accessibility alterations, including in regulatory regions of cancer driver genes that were otherwise devoid of genetic mutations. Genome-wide alterations in accessibility for transcription factor binding involved CTCF, downregulation of interferon and increased accessibility for SOX and HOX transcription factor families, suggesting the involvement of developmental genes during tumourigenesis. Somatic chromatin accessibility alterations were heritable and distinguished adenomas from cancers. Mutational signature analysis showed that the epigenome in turn influences the accumulation of DNA mutations. This study provides a map of genetic and epigenetic tumour heterogeneity, with fundamental implications for understanding colorectal cancer biology. Colorectal malignancies are a leading cause of cancer-related death and have undergone extensive genomic study . However, DNA mutations alone do not fully explain malignant transformation . Here we investigate the co-evolution of the genome and epigenome of colorectal tumours at single-clone resolution using spatial multi-omic profiling of individual glands. We collected 1,370 samples from 30 primary cancers and 8 concomitant adenomas and generated 1,207 chromatin accessibility profiles, 527 whole genomes and 297 whole transcriptomes. We found positive selection for DNA mutations in chromatin modifier genes and recurrent somatic chromatin accessibility alterations, including in regulatory regions of cancer driver genes that were otherwise devoid of genetic mutations. Genome-wide alterations in accessibility for transcription factor binding involved CTCF, downregulation of interferon and increased accessibility for SOX and HOX transcription factor families, suggesting the involvement of developmental genes during tumourigenesis. Somatic chromatin accessibility alterations were heritable and distinguished adenomas from cancers. Mutational signature analysis showed that the epigenome in turn influences the accumulation of DNA mutations. This study provides a map of genetic and epigenetic tumour heterogeneity, with fundamental implications for understanding colorectal cancer biology.
Author	Zapata, Luis Bridgewater, John Gunasri, Vinaya Rodriguez-Justo, Manuel Mossner, Maximilian Lakatos, Eszter Cresswell, George D. Chkhaidze, Ketevan Costa, Helena Shibata, Darryl Piazza, Rocco Kimberley, Chris Baker, Ann-Marie Nichol, Daniel Sottoriva, Andrea James, Chela Mitchinson, Miriam Berner, Alison Chen, Bingjie Spiteri, Inmaculada Househam, Jacob Fernandez-Mateos, Javier Ramazzotti, Daniele Barozzi, Iros Schmidt, Melissa Heide, Timon Jansen, Marnix Magnani, Luca Graham, Trevor A. Caravagna, Giulio Lynn, Claire
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Department of Surgery and Cancer, Imperial College London – sequence: 30 givenname: Trevor A. orcidid: 0000-0001-9582-1597 surname: Graham fullname: Graham, Trevor A. email: trevor.graham@icr.ac.uk organization: Centre for Evolution and Cancer, The Institute of Cancer Research, Evolution and Cancer Lab, Centre for Genomics and Computational Biology, Barts Cancer Institute, Queen Mary University of London – sequence: 31 givenname: Andrea orcidid: 0000-0001-6709-9533 surname: Sottoriva fullname: Sottoriva, Andrea email: andrea.sottoriva@fht.org organization: Centre for Evolution and Cancer, The Institute of Cancer Research, Computational Biology Research Centre, Human Technopole
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/36289335$$D View this record in MEDLINE/PubMed
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Copyright	The Author(s) 2022. corrected publication 2022 2022. The Author(s). Copyright Nature Publishing Group Nov 24, 2022 The Author(s) 2022, corrected publication 2022
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Snippet	Colorectal malignancies are a leading cause of cancer-related death 1 and have undergone extensive genomic study 2 , 3 . However, DNA mutations alone do not... Colorectal malignancies are a leading cause of cancer-related death 1 and have undergone extensive genomic study 2,3 . However, DNA mutations alone do not... Colorectal malignancies are a leading cause of cancer-related death and have undergone extensive genomic study . However, DNA mutations alone do not fully... Colorectal malignancies are a leading cause of cancer-related death1 and have undergone extensive genomic study2,3. However, DNA mutations alone do not fully... Colorectal malignancies are a leading cause of cancer-related death1 and have undergone extensive genomic study2,3. However, DNA mutations alone do not fully...
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SubjectTerms	45 45/23 631/114 631/208/177 631/67/2329 631/67/69 692/699/67/1504/1885 Accessibility Adenoma - genetics Adenoma - pathology Biological evolution Cancer Cell growth Cell Transformation, Neoplastic - genetics Cell Transformation, Neoplastic - metabolism Cell Transformation, Neoplastic - pathology Chromatin Chromatin - genetics Chromatin - metabolism Cloning Coevolution Colorectal cancer Colorectal carcinoma Colorectal Neoplasms - genetics Colorectal Neoplasms - pathology Datasets Deoxyribonucleic acid DNA DNA methylation Epigenetics Epigenome - genetics Evolution Evolution & development Genes Genome, Human - genetics Genomes Heterogeneity Humanities and Social Sciences Humans Interferon Interferons Malignancy multidisciplinary Mutation Oncogenes - genetics Patients Positive selection Regulatory sequences Science Science (multidisciplinary) Signature analysis Transcription factors Transcription Factors - metabolism Transcriptomes Tumorigenesis Tumors
Title	The co-evolution of the genome and epigenome in colorectal cancer
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