Ordered and deterministic cancer genome evolution after p53 loss

Although p53 inactivation promotes genomic instability 1 and presents a route to malignancy for more than half of all human cancers 2 , 3 , the patterns through which heterogenous TP53 (encoding human p53) mutant genomes emerge and influence tumorigenesis remain poorly understood. Here, in a mouse m...

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Vydáno v:	Nature (London) Ročník 608; číslo 7924; s. 795 - 802
Hlavní autoři:	Baslan, Timour, Morris, John P., Zhao, Zhen, Reyes, Jose, Ho, Yu-Jui, Tsanov, Kaloyan M., Bermeo, Jonathan, Tian, Sha, Zhang, Sean, Askan, Gokce, Yavas, Aslihan, Lecomte, Nicolas, Erakky, Amanda, Varghese, Anna M., Zhang, Amy, Kendall, Jude, Ghiban, Elena, Chorbadjiev, Lubomir, Wu, Jie, Dimitrova, Nevenka, Chadalavada, Kalyani, Nanjangud, Gouri J., Bandlamudi, Chaitanya, Gong, Yixiao, Donoghue, Mark T. A., Socci, Nicholas D., Krasnitz, Alex, Notta, Faiyaz, Leach, Steve D., Iacobuzio-Donahue, Christine A., Lowe, Scott W.
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	London Nature Publishing Group UK 25.08.2022 Nature Publishing Group
Témata:	13/1 13/106 13/31 13/51 14/19 14/32 14/63 45/23 45/29 45/77 59/57 631/67/68 631/67/69 64/60 Adenocarcinoma Adenocarcinoma - genetics Adenocarcinoma - pathology Animals Cancer Carcinogenesis - genetics Carcinogenesis - pathology Carcinoma, Pancreatic Ductal - genetics Carcinoma, Pancreatic Ductal - pathology Cell cycle Deactivation Disease Progression Evolution Evolution, Molecular Gene Deletion Gene sequencing Genes, p53 - genetics Genome - genetics Genomes Genomics Genotyping Heterogeneity Heterozygosity Humanities and Social Sciences Inactivation Loss of Heterozygosity Malignancy Mice Models, Genetic multidisciplinary Mutants Mutation p53 Protein Pancreatic cancer Pancreatic Neoplasms - genetics Pancreatic Neoplasms - pathology Science Science (multidisciplinary) Stem cells Tumor Suppressor Protein p53 - genetics Tumorigenesis Tumors
ISSN:	0028-0836, 1476-4687, 1476-4687
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Abstract	Although p53 inactivation promotes genomic instability 1 and presents a route to malignancy for more than half of all human cancers 2 , 3 , the patterns through which heterogenous TP53 (encoding human p53) mutant genomes emerge and influence tumorigenesis remain poorly understood. Here, in a mouse model of pancreatic ductal adenocarcinoma that reports sporadic p53 loss of heterozygosity before cancer onset, we find that malignant properties enabled by p53 inactivation are acquired through a predictable pattern of genome evolution. Single-cell sequencing and in situ genotyping of cells from the point of p53 inactivation through progression to frank cancer reveal that this deterministic behaviour involves four sequential phases— Trp53 (encoding mouse p53) loss of heterozygosity, accumulation of deletions, genome doubling, and the emergence of gains and amplifications—each associated with specific histological stages across the premalignant and malignant spectrum. Despite rampant heterogeneity, the deletion events that follow p53 inactivation target functionally relevant pathways that can shape genomic evolution and remain fixed as homogenous events in diverse malignant populations. Thus, loss of p53—the ‘guardian of the genome’—is not merely a gateway to genetic chaos but, rather, can enable deterministic patterns of genome evolution that may point to new strategies for the treatment of TP53- mutant tumours. Malignant evolution enabled by p53 inactivation in mice proceeds through an ordered and predictable pattern of Trp53 loss of heterozygosity, accumulation of deletions, genome doubling and the emergence of gains and amplifications.
AbstractList	Although p53 inactivation promotes genomic instability 1 and presents a route to malignancy for more than half of all human cancers 2,3 , the patterns through which heterogenous TP53 (encoding human p53) mutant genomes emerge and influence tumorigenesis remain poorly understood. Here, in a mouse model of pancreatic ductal adenocarcinoma that reports sporadic p53 loss of heterozygosity before cancer onset, we find that malignant properties enabled by p53 inactivation are acquired through a predictable pattern of genome evolution. Single-cell sequencing and in situ genotyping of cells from the point of p53 inactivation through progression to frank cancer reveal that this deterministic behaviour involves four sequential phases— Trp53 (encoding mouse p53) loss of heterozygosity, accumulation of deletions, genome doubling, and the emergence of gains and amplifications—each associated with specific histological stages across the premalignant and malignant spectrum. Despite rampant heterogeneity, the deletion events that follow p53 inactivation target functionally relevant pathways that can shape genomic evolution and remain fixed as homogenous events in diverse malignant populations. Thus, loss of p53—the ‘guardian of the genome’—is not merely a gateway to genetic chaos but, rather, can enable deterministic patterns of genome evolution that may point to new strategies for the treatment of TP53- mutant tumours. Although p53 inactivation promotes genomic instability 1 and presents a route to malignancy for more than half of all human cancers 2 , 3 , the patterns through which heterogenous TP53 (encoding human p53) mutant genomes emerge and influence tumorigenesis remain poorly understood. Here, in a mouse model of pancreatic ductal adenocarcinoma that reports sporadic p53 loss of heterozygosity before cancer onset, we find that malignant properties enabled by p53 inactivation are acquired through a predictable pattern of genome evolution. Single-cell sequencing and in situ genotyping of cells from the point of p53 inactivation through progression to frank cancer reveal that this deterministic behaviour involves four sequential phases— Trp53 (encoding mouse p53) loss of heterozygosity, accumulation of deletions, genome doubling, and the emergence of gains and amplifications—each associated with specific histological stages across the premalignant and malignant spectrum. Despite rampant heterogeneity, the deletion events that follow p53 inactivation target functionally relevant pathways that can shape genomic evolution and remain fixed as homogenous events in diverse malignant populations. Thus, loss of p53—the ‘guardian of the genome’—is not merely a gateway to genetic chaos but, rather, can enable deterministic patterns of genome evolution that may point to new strategies for the treatment of TP53- mutant tumours. Malignant evolution enabled by p53 inactivation in mice proceeds through an ordered and predictable pattern of Trp53 loss of heterozygosity, accumulation of deletions, genome doubling and the emergence of gains and amplifications. Although p53 inactivation promotes genomic instability1 and presents a route to malignancy for more than half of all human cancers2,3, the patterns through which heterogenous TP53 (encoding human p53) mutant genomes emerge and influence tumorigenesis remain poorly understood. Here, in a mouse model of pancreatic ductal adenocarcinoma that reports sporadic p53 loss of heterozygosity before cancer onset, we find that malignant properties enabled by p53 inactivation are acquired through a predictable pattern of genome evolution. Single-cell sequencing and in situ genotyping of cells from the point of p53 inactivation through progression to frank cancer reveal that this deterministic behaviour involves four sequential phases-Trp53 (encoding mouse p53) loss of heterozygosity, accumulation of deletions, genome doubling, and the emergence of gains and amplifications-each associated with specific histological stages across the premalignant and malignant spectrum. Despite rampant heterogeneity, the deletion events that follow p53 inactivation target functionally relevant pathways that can shape genomic evolution and remain fixed as homogenous events in diverse malignant populations. Thus, loss of p53-the 'guardian of the genome'-is not merely a gateway to genetic chaos but, rather, can enable deterministic patterns of genome evolution that may point to new strategies for the treatment of TP53-mutant tumours.Although p53 inactivation promotes genomic instability1 and presents a route to malignancy for more than half of all human cancers2,3, the patterns through which heterogenous TP53 (encoding human p53) mutant genomes emerge and influence tumorigenesis remain poorly understood. Here, in a mouse model of pancreatic ductal adenocarcinoma that reports sporadic p53 loss of heterozygosity before cancer onset, we find that malignant properties enabled by p53 inactivation are acquired through a predictable pattern of genome evolution. Single-cell sequencing and in situ genotyping of cells from the point of p53 inactivation through progression to frank cancer reveal that this deterministic behaviour involves four sequential phases-Trp53 (encoding mouse p53) loss of heterozygosity, accumulation of deletions, genome doubling, and the emergence of gains and amplifications-each associated with specific histological stages across the premalignant and malignant spectrum. Despite rampant heterogeneity, the deletion events that follow p53 inactivation target functionally relevant pathways that can shape genomic evolution and remain fixed as homogenous events in diverse malignant populations. Thus, loss of p53-the 'guardian of the genome'-is not merely a gateway to genetic chaos but, rather, can enable deterministic patterns of genome evolution that may point to new strategies for the treatment of TP53-mutant tumours. Although p53 inactivation promotes genomic instability and presents a route to malignancy for more than half of all human cancers , the patterns through which heterogenous TP53 (encoding human p53) mutant genomes emerge and influence tumorigenesis remain poorly understood. Here, in a mouse model of pancreatic ductal adenocarcinoma that reports sporadic p53 loss of heterozygosity before cancer onset, we find that malignant properties enabled by p53 inactivation are acquired through a predictable pattern of genome evolution. Single-cell sequencing and in situ genotyping of cells from the point of p53 inactivation through progression to frank cancer reveal that this deterministic behaviour involves four sequential phases-Trp53 (encoding mouse p53) loss of heterozygosity, accumulation of deletions, genome doubling, and the emergence of gains and amplifications-each associated with specific histological stages across the premalignant and malignant spectrum. Despite rampant heterogeneity, the deletion events that follow p53 inactivation target functionally relevant pathways that can shape genomic evolution and remain fixed as homogenous events in diverse malignant populations. Thus, loss of p53-the 'guardian of the genome'-is not merely a gateway to genetic chaos but, rather, can enable deterministic patterns of genome evolution that may point to new strategies for the treatment of TP53-mutant tumours. Although p53 inactivation promotes genomic instability1 and presents a route to malignancy for more than half of all human cancers2,3, the patterns through which heterogenous TP53 (encoding human p53) mutant genomes emerge and influence tumorigenesis remain poorly understood. Here, in a mouse model of pancreatic ductal adenocarcinoma that reports sporadic p53 loss of heterozygosity before cancer onset, we find that malignant properties enabled by p53 inactivation are acquired through a predictable pattern of genome evolution. Single-cell sequencing and in situ genotyping of cells from the point of p53 inactivation through progression to frank cancer reveal that this deterministic behaviour involves four sequential phases-Trp53 (encoding mouse p53) loss of heterozygosity, accumulation of deletions, genome doubling, and the emergence of gains and amplifications-each associated with specific histological stages across the premalignant and malignant spectrum. Despite rampant heterogeneity, the deletion events that follow p53 inactivation target functionally relevant pathways that can shape genomic evolution and remain fixed as homogenous events in diverse malignant populations. Thus, loss of p53-the 'guardian ofthe genome'-is not merely a gateway to genetic chaos but, rather, can enable deterministic patterns of genome evolution that may point to new strategies for the treatment of TP53-mutant tumours. Although p53 inactivation promotes genomic instability1 and presents a route to malignancy for more than half of all human cancers2,3, the patterns through which heterogenous TP53 (encoding human p53) mutant genomes emerge and influence tumorigenesis remain poorly understood. Here, in a mouse model of pancreatic ductal adenocarcinoma that reports sporadic p53 loss of heterozygosity before cancer onset, we find that malignant properties enabled by p53 inactivation are acquired through a predictable pattern of genome evolution. Single-cell sequencing and in situ genotyping of cells from the point of p53 inactivation through progression to frank cancer reveal that this deterministic behaviour involves four sequential phases—Trp53 (encoding mouse p53) loss of heterozygosity, accumulation of deletions, genome doubling, and the emergence of gains and amplifications—each associated with specific histological stages across the premalignant and malignant spectrum. Despite rampant heterogeneity, the deletion events that follow p53 inactivation target functionally relevant pathways that can shape genomic evolution and remain fixed as homogenous events in diverse malignant populations. Thus, loss of p53—the ‘guardian of the genome’—is not merely a gateway to genetic chaos but, rather, can enable deterministic patterns of genome evolution that may point to new strategies for the treatment of TP53-mutant tumours. Malignant evolution enabled by p53 inactivation in mice proceeds through an ordered and predictable pattern of Trp53 loss of heterozygosity, accumulation of deletions, genome doubling and the emergence of gains and amplifications.
Author	Bandlamudi, Chaitanya Iacobuzio-Donahue, Christine A. Baslan, Timour Askan, Gokce Reyes, Jose Chadalavada, Kalyani Zhang, Sean Wu, Jie Dimitrova, Nevenka Leach, Steve D. Krasnitz, Alex Gong, Yixiao Ho, Yu-Jui Nanjangud, Gouri J. Ghiban, Elena Zhao, Zhen Varghese, Anna M. Bermeo, Jonathan Kendall, Jude Morris, John P. Notta, Faiyaz Erakky, Amanda Tsanov, Kaloyan M. Tian, Sha Socci, Nicholas D. Zhang, Amy Lowe, Scott W. Yavas, Aslihan Chorbadjiev, Lubomir Donoghue, Mark T. A. Lecomte, Nicolas
Author_xml	– sequence: 1 givenname: Timour surname: Baslan fullname: Baslan, Timour organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center – sequence: 2 givenname: John P. surname: Morris fullname: Morris, John P. organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, Department of Pharmacology, University of North Carolina at Chapel Hill School of Medicine, Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill – sequence: 3 givenname: Zhen surname: Zhao fullname: Zhao, Zhen organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, Department of Pathology, Molecular and Cell-based Medicine, Icahn School of Medicine at Mount Sinai – sequence: 4 givenname: Jose surname: Reyes fullname: Reyes, Jose organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, Computational and Systems Biology Program, Memorial Sloan Kettering Cancer Center, Howard Hughes Medical Institute – sequence: 5 givenname: Yu-Jui surname: Ho fullname: Ho, Yu-Jui organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center – sequence: 6 givenname: Kaloyan M. surname: Tsanov fullname: Tsanov, Kaloyan M. organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center – sequence: 7 givenname: Jonathan orcidid: 0000-0002-9553-9222 surname: Bermeo fullname: Bermeo, Jonathan organization: Rubinstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center – sequence: 8 givenname: Sha surname: Tian fullname: Tian, Sha organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center – sequence: 9 givenname: Sean surname: Zhang fullname: Zhang, Sean organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center – sequence: 10 givenname: Gokce surname: Askan fullname: Askan, Gokce organization: Rubinstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center – sequence: 11 givenname: Aslihan orcidid: 0000-0002-8408-3063 surname: Yavas fullname: Yavas, Aslihan organization: Rubinstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center – sequence: 12 givenname: Nicolas surname: Lecomte fullname: Lecomte, Nicolas organization: Rubinstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center – sequence: 13 givenname: Amanda surname: Erakky fullname: Erakky, Amanda organization: Rubinstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center – sequence: 14 givenname: Anna M. surname: Varghese fullname: Varghese, Anna M. organization: Rubinstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center – sequence: 15 givenname: Amy surname: Zhang fullname: Zhang, Amy organization: PanCuRx Translational Research Initiative, Ontario Institute for Cancer Research – sequence: 16 givenname: Jude surname: Kendall fullname: Kendall, Jude organization: Cold Spring Harbor Laboratory – sequence: 17 givenname: Elena surname: Ghiban fullname: Ghiban, Elena organization: Cold Spring Harbor Laboratory – sequence: 18 givenname: Lubomir surname: Chorbadjiev fullname: Chorbadjiev, Lubomir organization: Technical School of Electronic Systems, Technical University of Sofia – sequence: 19 givenname: Jie orcidid: 0000-0002-0989-8115 surname: Wu fullname: Wu, Jie organization: Phillips Research North America, Oncology Informatics and Genomics – sequence: 20 givenname: Nevenka surname: Dimitrova fullname: Dimitrova, Nevenka organization: Phillips Research North America, Oncology Informatics and Genomics – sequence: 21 givenname: Kalyani surname: Chadalavada fullname: Chadalavada, Kalyani organization: Molecular Cytogenetics Core Facility, Memorial Sloan Kettering Cancer Center – sequence: 22 givenname: Gouri J. orcidid: 0000-0002-8547-1957 surname: Nanjangud fullname: Nanjangud, Gouri J. organization: Molecular Cytogenetics Core Facility, Memorial Sloan Kettering Cancer Center – sequence: 23 givenname: Chaitanya surname: Bandlamudi fullname: Bandlamudi, Chaitanya organization: Marie-Josee and Henry R. Kravis Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center – sequence: 24 givenname: Yixiao surname: Gong fullname: Gong, Yixiao organization: Marie-Josee and Henry R. Kravis Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center – sequence: 25 givenname: Mark T. A. surname: Donoghue fullname: Donoghue, Mark T. A. organization: Marie-Josee and Henry R. Kravis Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center – sequence: 26 givenname: Nicholas D. surname: Socci fullname: Socci, Nicholas D. organization: Marie-Josee and Henry R. Kravis Center for Molecular Oncology, Memorial Sloan Kettering Cancer Center – sequence: 27 givenname: Alex surname: Krasnitz fullname: Krasnitz, Alex organization: Cold Spring Harbor Laboratory – sequence: 28 givenname: Faiyaz surname: Notta fullname: Notta, Faiyaz organization: PanCuRx Translational Research Initiative, Ontario Institute for Cancer Research – sequence: 29 givenname: Steve D. orcidid: 0000-0002-2689-1871 surname: Leach fullname: Leach, Steve D. organization: Rubinstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center, Dartmouth Cancer Center – sequence: 30 givenname: Christine A. orcidid: 0000-0002-4672-3023 surname: Iacobuzio-Donahue fullname: Iacobuzio-Donahue, Christine A. organization: Rubinstein Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center – sequence: 31 givenname: Scott W. orcidid: 0000-0002-5284-9650 surname: Lowe fullname: Lowe, Scott W. email: lowes@mskcc.org organization: Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, Howard Hughes Medical Institute
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/35978189$$D View this record in MEDLINE/PubMed
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Snippet	Although p53 inactivation promotes genomic instability 1 and presents a route to malignancy for more than half of all human cancers 2 , 3 , the patterns... Although p53 inactivation promotes genomic instability 1 and presents a route to malignancy for more than half of all human cancers 2,3 , the patterns through... Although p53 inactivation promotes genomic instability and presents a route to malignancy for more than half of all human cancers , the patterns through which... Although p53 inactivation promotes genomic instability1 and presents a route to malignancy for more than half of all human cancers2,3, the patterns through...
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SubjectTerms	13/1 13/106 13/31 13/51 14/19 14/32 14/63 45/23 45/29 45/77 59/57 631/67/68 631/67/69 64/60 Adenocarcinoma Adenocarcinoma - genetics Adenocarcinoma - pathology Animals Cancer Carcinogenesis - genetics Carcinogenesis - pathology Carcinoma, Pancreatic Ductal - genetics Carcinoma, Pancreatic Ductal - pathology Cell cycle Deactivation Disease Progression Evolution Evolution, Molecular Gene Deletion Gene sequencing Genes, p53 - genetics Genome - genetics Genomes Genomics Genotyping Heterogeneity Heterozygosity Humanities and Social Sciences Inactivation Loss of Heterozygosity Malignancy Mice Models, Genetic multidisciplinary Mutants Mutation p53 Protein Pancreatic cancer Pancreatic Neoplasms - genetics Pancreatic Neoplasms - pathology Science Science (multidisciplinary) Stem cells Tumor Suppressor Protein p53 - genetics Tumorigenesis Tumors
Title	Ordered and deterministic cancer genome evolution after p53 loss
URI	https://link.springer.com/article/10.1038/s41586-022-05082-5 https://www.ncbi.nlm.nih.gov/pubmed/35978189 https://www.proquest.com/docview/2707254685 https://www.proquest.com/docview/2703986576 https://pubmed.ncbi.nlm.nih.gov/PMC9402436
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