Extrachromosomal DNA in the cancerous transformation of Barrett's oesophagus. Luebeck, J., Ng, A. W. T., Galipeau, P. C., Li, X., Sanchez, C. A., Katz-Summercorn, A. C., Kim, H., Jammula, S., He, Y., Lippman, S. M., Verhaak, R. G. W., Maley, C. C., Alexandrov, L. B., Reid, B. J., Fitzgerald, R. C., Paulson, T. G., Chang, H. Y., Wu, S., Bafna, V., & Mischel, P. S. Nature, 616(7958):798-805, 2023. 1476-4687 Luebeck, Jens Orcid: 0000-0003-4391-979x Ng, Alvin Wei Tian Galipeau, Patricia C Orcid: 0000-0001-7961-7430 Li, Xiaohong Orcid: 0000-0003-4438-2664 Sanchez, Carissa A Katz-Summercorn, Annalise C Kim, Hoon Jammula, Sriganesh He, Yudou Lippman, Scott M Verhaak, Roel G W Orcid: 0000-0003-2773-0436 Maley, Carlo C Orcid: 0000-0002-0745-7076 Alexandrov, Ludmil B Reid, Brian J Fitzgerald, Rebecca C Paulson, Thomas G Chang, Howard Y Orcid: 0000-0002-9459-4393 Wu, Sihan Orcid: 0000-0001-8329-7492 Bafna, Vineet Orcid: 0000-0002-5810-6241 Mischel, Paul S Orcid: 0000-0002-4560-2211 R01 CA238249/CA/NCI NIH HHS/United States U24 CA264379/CA/NCI NIH HHS/United States R01 ES032547/ES/NIEHS NIH HHS/United States OT2 CA278635/CA/NCI NIH HHS/United States R01 GM114362/GM/NIGMS NIH HHS/United States Journal Article England 2023/04/13 Nature. 2023 Apr;616(7958):798-805. doi: 10.1038/s41586-023-05937-5. Epub 2023 Apr 12.
doi  abstract   bibtex   
Oncogene amplification on extrachromosomal DNA (ecDNA) drives the evolution of tumours and their resistance to treatment, and is associated with poor outcomes for patients with cancer(1-6). At present, it is unclear whether ecDNA is a later manifestation of genomic instability, or whether it can be an early event in the transition from dysplasia to cancer. Here, to better understand the development of ecDNA, we analysed whole-genome sequencing (WGS) data from patients with oesophageal adenocarcinoma (EAC) or Barrett's oesophagus. These data included 206 biopsies in Barrett's oesophagus surveillance and EAC cohorts from Cambridge University. We also analysed WGS and histology data from biopsies that were collected across multiple regions at 2 time points from 80 patients in a case-control study at the Fred Hutchinson Cancer Center. In the Cambridge cohorts, the frequency of ecDNA increased between Barrett's-oesophagus-associated early-stage (24%) and late-stage (43%) EAC, suggesting that ecDNA is formed during cancer progression. In the cohort from the Fred Hutchinson Cancer Center, 33% of patients who developed EAC had at least one oesophageal biopsy with ecDNA before or at the diagnosis of EAC. In biopsies that were collected before cancer diagnosis, higher levels of ecDNA were present in samples from patients who later developed EAC than in samples from those who did not. We found that ecDNAs contained diverse collections of oncogenes and immunomodulatory genes. Furthermore, ecDNAs showed increases in copy number and structural complexity at more advanced stages of disease. Our findings show that ecDNA can develop early in the transition from high-grade dysplasia to cancer, and that ecDNAs progressively form and evolve under positive selection.
@article{RN6046,
   author = {Luebeck, J. and Ng, A. W. T. and Galipeau, P. C. and Li, X. and Sanchez, C. A. and Katz-Summercorn, A. C. and Kim, H. and Jammula, S. and He, Y. and Lippman, S. M. and Verhaak, R. G. W. and Maley, C. C. and Alexandrov, L. B. and Reid, B. J. and Fitzgerald, R. C. and Paulson, T. G. and Chang, H. Y. and Wu, S. and Bafna, V. and Mischel, P. S.},
   title = {Extrachromosomal DNA in the cancerous transformation of Barrett's oesophagus},
   journal = {Nature},
   volume = {616},
   number = {7958},
   pages = {798-805},
   note = {1476-4687
Luebeck, Jens
Orcid: 0000-0003-4391-979x
Ng, Alvin Wei Tian
Galipeau, Patricia C
Orcid: 0000-0001-7961-7430
Li, Xiaohong
Orcid: 0000-0003-4438-2664
Sanchez, Carissa A
Katz-Summercorn, Annalise C
Kim, Hoon
Jammula, Sriganesh
He, Yudou
Lippman, Scott M
Verhaak, Roel G W
Orcid: 0000-0003-2773-0436
Maley, Carlo C
Orcid: 0000-0002-0745-7076
Alexandrov, Ludmil B
Reid, Brian J
Fitzgerald, Rebecca C
Paulson, Thomas G
Chang, Howard Y
Orcid: 0000-0002-9459-4393
Wu, Sihan
Orcid: 0000-0001-8329-7492
Bafna, Vineet
Orcid: 0000-0002-5810-6241
Mischel, Paul S
Orcid: 0000-0002-4560-2211
R01 CA238249/CA/NCI NIH HHS/United States
U24 CA264379/CA/NCI NIH HHS/United States
R01 ES032547/ES/NIEHS NIH HHS/United States
OT2 CA278635/CA/NCI NIH HHS/United States
R01 GM114362/GM/NIGMS NIH HHS/United States
Journal Article
England
2023/04/13
Nature. 2023 Apr;616(7958):798-805. doi: 10.1038/s41586-023-05937-5. Epub 2023 Apr 12.},
   abstract = {Oncogene amplification on extrachromosomal DNA (ecDNA) drives the evolution of tumours and their resistance to treatment, and is associated with poor outcomes for patients with cancer(1-6). At present, it is unclear whether ecDNA is a later manifestation of genomic instability, or whether it can be an early event in the transition from dysplasia to cancer. Here, to better understand the development of ecDNA, we analysed whole-genome sequencing (WGS) data from patients with oesophageal adenocarcinoma (EAC) or Barrett's oesophagus. These data included 206 biopsies in Barrett's oesophagus surveillance and EAC cohorts from Cambridge University. We also analysed WGS and histology data from biopsies that were collected across multiple regions at 2 time points from 80 patients in a case-control study at the Fred Hutchinson Cancer Center. In the Cambridge cohorts, the frequency of ecDNA increased between Barrett's-oesophagus-associated early-stage (24%) and late-stage (43%) EAC, suggesting that ecDNA is formed during cancer progression. In the cohort from the Fred Hutchinson Cancer Center, 33% of patients who developed EAC had at least one oesophageal biopsy with ecDNA before or at the diagnosis of EAC. In biopsies that were collected before cancer diagnosis, higher levels of ecDNA were present in samples from patients who later developed EAC than in samples from those who did not. We found that ecDNAs contained diverse collections of oncogenes and immunomodulatory genes. Furthermore, ecDNAs showed increases in copy number and structural complexity at more advanced stages of disease. Our findings show that ecDNA can develop early in the transition from high-grade dysplasia to cancer, and that ecDNAs progressively form and evolve under positive selection.},
   keywords = {Humans
*Adenocarcinoma/genetics/pathology
*Barrett Esophagus/genetics/pathology
Case-Control Studies
*DNA/genetics
*Esophageal Neoplasms/genetics/pathology
*Carcinogenesis/genetics
Whole Genome Sequencing
Cohort Studies
Biopsy
*Disease Progression
Oncogenes
Immunomodulation
DNA Copy Number Variations
Gene Amplification
*Early Detection of Cancer/methods},
   ISSN = {0028-0836 (Print)
0028-0836},
   DOI = {10.1038/s41586-023-05937-5},
   year = {2023},
   type = {Journal Article}
}

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