Recurrent Somatic Structural Variations Contribute to Tumorigenesis in Pediatric Osteosarcoma

Pediatric osteosarcoma is characterized by multiple somatic chromosomal lesions, including structural variations (SVs) and copy number alterations (CNAs). To define the landscape of somatic mutations in pediatric osteosarcoma, we performed whole-genome sequencing of DNA from 20 osteosarcoma tumor sa...

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Vydáno v:Cell reports (Cambridge) Ročník 7; číslo 1; s. 104 - 112
Hlavní autoři: Chen, Xiang, Bahrami, Armita, Pappo, Alberto, Easton, John, Dalton, James, Hedlund, Erin, Ellison, David, Shurtleff, Sheila, Wu, Gang, Wei, Lei, Parker, Matthew, Rusch, Michael, Nagahawatte, Panduka, Wu, Jianrong, Mao, Shenghua, Boggs, Kristy, Mulder, Heather, Yergeau, Donald, Lu, Charles, Ding, Li, Edmonson, Michael, Qu, Chunxu, Wang, Jianmin, Li, Yongjin, Navid, Fariba, Daw, Najat C., Mardis, Elaine R., Wilson, Richard K., Downing, James R., Zhang, Jinghui, Dyer, Michael A.
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States Elsevier 01.04.2014
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ISSN:2211-1247, 2211-1247
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Abstract Pediatric osteosarcoma is characterized by multiple somatic chromosomal lesions, including structural variations (SVs) and copy number alterations (CNAs). To define the landscape of somatic mutations in pediatric osteosarcoma, we performed whole-genome sequencing of DNA from 20 osteosarcoma tumor samples and matched normal tissue in a discovery cohort, as well as 14 samples in a validation cohort. Single-nucleotide variations (SNVs) exhibited a pattern of localized hypermutation called kataegis in 50% of the tumors. We identified p53 pathway lesions in all tumors in the discovery cohort, nine of which were translocations in the first intron of the TP53 gene. Beyond TP53, the RB1, ATRX, and DLG2 genes showed recurrent somatic alterations in 29%-53% of the tumors. These data highlight the power of whole-genome sequencing for identifying recurrent somatic alterations in cancer genomes that may be missed using other methods.
AbstractList Pediatric osteosarcoma is characterized by multiple somatic chromosomal lesions, including structural variations (SVs) and copy number alterations (CNAs). To define the landscape of somatic mutations in pediatric osteosarcoma, we performed whole-genome sequencing of DNA from 20 osteosarcoma tumor samples and matched normal tissue in a discovery cohort, as well as 14 samples in a validation cohort. Single-nucleotide variations (SNVs) exhibited a pattern of localized hypermutation called kataegis in 50% of the tumors. We identified p53 pathway lesions in all tumors in the discovery cohort, nine of which were translocations in the first intron of the TP53 gene. Beyond TP53, the RB1, ATRX, and DLG2 genes showed recurrent somatic alterations in 29%-53% of the tumors. These data highlight the power of whole-genome sequencing for identifying recurrent somatic alterations in cancer genomes that may be missed using other methods.
Osteosarcoma is a neoplasm of mesenchymal origin with features of osteogenic differentiation. Patients with recurrent or metastatic disease have a very poor prognosis. To define the landscape of somatic mutations in pediatric osteosarcoma, we performed whole-genome sequencing of DNA from 20 osteosarcoma tumor samples and matched normal tissue (obtained from 19 patients) in the discovery cohort as well as 14 samples from 13 patients in the validation cohort. Our results demonstrate that pediatric osteosarcoma is characterized by multiple somatic chromosomal lesions, including structural variations (SVs) and copy number alterations (CNAs). Moreover, single nucleotide variations (SNVs) exhibit a pattern of localized hypermutation called “kataegis” in 50% of the tumors. Despite these regions of kataegis across the osteosarcoma genomes, we detected relatively few recurrent SNVs, and only when SVs were included did we identify the major pathways that are mutated in osteosarcoma. We identified p53 pathway lesions in all 19 patient’s tumors in the discovery cohort, 9 of which were translocations in the first intron of the TP53 gene, leading to gene inactivation. This mechanism of p53 gene inactivation is unique to osteosarcoma among pediatric cancers. In an additional cohort of 32 patients, TP53 gene alterations were identified in 29 of those tumors. Beyond TP53, the RB1, ATRX and DLG2 genes showed recurrent somatic alterations (SNVs and/or SVs) in 29–53% of the tumors. These data highlight the power of whole-genome sequencing in identifying recurrent somatic alterations in cancer genomes that may be missed using other methods.
Pediatric osteosarcoma is characterized by multiple somatic chromosomal lesions, including structural variations (SVs) and copy number alterations (CNAs). To define the landscape of somatic mutations in pediatric osteosarcoma, we performed whole-genome sequencing of DNA from 20 osteosarcoma tumor samples and matched normal tissue in a discovery cohort, as well as 14 samples in a validation cohort. Single-nucleotide variations (SNVs) exhibited a pattern of localized hypermutation called kataegis in 50% of the tumors. We identified p53 pathway lesions in all tumors in the discovery cohort, nine of which were translocations in the first intron of the TP53 gene. Beyond TP53, the RB1, ATRX, and DLG2 genes showed recurrent somatic alterations in 29%-53% of the tumors. These data highlight the power of whole-genome sequencing for identifying recurrent somatic alterations in cancer genomes that may be missed using other methods.Pediatric osteosarcoma is characterized by multiple somatic chromosomal lesions, including structural variations (SVs) and copy number alterations (CNAs). To define the landscape of somatic mutations in pediatric osteosarcoma, we performed whole-genome sequencing of DNA from 20 osteosarcoma tumor samples and matched normal tissue in a discovery cohort, as well as 14 samples in a validation cohort. Single-nucleotide variations (SNVs) exhibited a pattern of localized hypermutation called kataegis in 50% of the tumors. We identified p53 pathway lesions in all tumors in the discovery cohort, nine of which were translocations in the first intron of the TP53 gene. Beyond TP53, the RB1, ATRX, and DLG2 genes showed recurrent somatic alterations in 29%-53% of the tumors. These data highlight the power of whole-genome sequencing for identifying recurrent somatic alterations in cancer genomes that may be missed using other methods.
Author Mulder, Heather
Ellison, David
Lu, Charles
Mardis, Elaine R.
Mao, Shenghua
Edmonson, Michael
Bahrami, Armita
Easton, John
Qu, Chunxu
Zhang, Jinghui
Nagahawatte, Panduka
Wu, Jianrong
Dalton, James
Navid, Fariba
Wilson, Richard K.
Wang, Jianmin
Wu, Gang
Ding, Li
Shurtleff, Sheila
Rusch, Michael
Wei, Lei
Yergeau, Donald
Dyer, Michael A.
Downing, James R.
Chen, Xiang
Li, Yongjin
Daw, Najat C.
Parker, Matthew
Boggs, Kristy
Pappo, Alberto
Hedlund, Erin
AuthorAffiliation 4 Department of Biostatistics, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, USA
10 Department of Developmental Neurobiology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, USA
7 Department of Genetics, Washington University School of Medicine in St. Louis, St. Louis, Missouri 63108, USA
6 The Genome Institute, Washington University School of Medicine in St. Louis, St. Louis, Missouri 63108, USA
8 Department of Medicine, Washington University School of Medicine in St. Louis, St. Louis, Missouri 63108, USA
11 Howard Hughes Medical Institute, Chevy Chase, Maryland 20815, USA
3 Department of Oncology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, USA
2 Department of Pathology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, USA
1 Department of Computational Biology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, USA
9 Siteman Cancer Center, Washington University School of Medicine in St. Louis, St. Louis, Mi
AuthorAffiliation_xml – name: 2 Department of Pathology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, USA
– name: 3 Department of Oncology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, USA
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– name: 1 Department of Computational Biology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, USA
– name: 6 The Genome Institute, Washington University School of Medicine in St. Louis, St. Louis, Missouri 63108, USA
– name: 9 Siteman Cancer Center, Washington University School of Medicine in St. Louis, St. Louis, Missouri 63108, USA
– name: 7 Department of Genetics, Washington University School of Medicine in St. Louis, St. Louis, Missouri 63108, USA
– name: 10 Department of Developmental Neurobiology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, USA
– name: 11 Howard Hughes Medical Institute, Chevy Chase, Maryland 20815, USA
– name: 8 Department of Medicine, Washington University School of Medicine in St. Louis, St. Louis, Missouri 63108, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/24703847$$D View this record in MEDLINE/PubMed
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Snippet Pediatric osteosarcoma is characterized by multiple somatic chromosomal lesions, including structural variations (SVs) and copy number alterations (CNAs). To...
Osteosarcoma is a neoplasm of mesenchymal origin with features of osteogenic differentiation. Patients with recurrent or metastatic disease have a very poor...
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StartPage 104
SubjectTerms Adolescent
Bone Neoplasms - genetics
Bone Neoplasms - pathology
Carcinogenesis - genetics
Carcinogenesis - pathology
Child
Child, Preschool
Disease Progression
DNA Copy Number Variations
DNA, Neoplasm - genetics
Genome, Human
Humans
Mutation
Neoplasm Metastasis
Osteosarcoma - genetics
Osteosarcoma - pathology
Polymorphism, Single Nucleotide
Title Recurrent Somatic Structural Variations Contribute to Tumorigenesis in Pediatric Osteosarcoma
URI https://www.ncbi.nlm.nih.gov/pubmed/24703847
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https://www.proquest.com/docview/1544013095
https://pubmed.ncbi.nlm.nih.gov/PMC4096827
https://doaj.org/article/40f55a27461a4869b9e264b8b60dc172
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