TY - JOUR
T1 - Molecular characterization of Barrett's esophagus at single-cell resolution
AU - Busslinger, Georg A
AU - de Barbanson, Buys
AU - Oka, Rurika
AU - Weusten, Bas L A
AU - de Maat, Michiel
AU - van Hillegersberg, Richard
AU - Brosens, Lodewijk A A
AU - van Boxtel, Ruben
AU - van Oudenaarden, Alexander
AU - Clevers, Hans
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank Sabine Middendorp for arranging ethical approval to obtain biopsies and are grateful to her, Nikki Kroon, and Eke van Lunteren for help with the selection of patients. We also thank the FACS facilities at the Hubrecht Institute (Reinier van der Linden and Stefan van der Elst) and Jochem Bernink for cell sorting. We thank Josi Peterson for advice on the scDNAseq protocol and the Single Cell Discoveries company (https://www.scdiscoveries.com) for providing help with scRNAseq. This research was supported by the European Research Council (Advanced Grant ERC-AdG 67013-Organoid to H.C. and G.A.B.) and funded by MKMD Grant 114021012 from Netherlands Organization for Scientific Research (NWO-ZonMw).
Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.
PY - 2021/11/23
Y1 - 2021/11/23
N2 - Barrett's esophagus (BE) is categorized, based on morphological appearance, into different stages, which correlate with the risk of developing esophageal adenocarcinoma. More advanced stages are more likely to acquire chromosomal instabilities, but stage-specific markers remain elusive. Here, we performed single-cell DNA-sequencing experiments (scDNAseq) with fresh BE biopsies. Dysplastic BE cells frequently contained chromosomal instability (CIN) regions, and these CIN cells carried mutations corresponding to the COSMIC mutational signature SBS17, which were not present in biopsy-matched chromosomally stable (CS) cells or patient-matched nondiseased control cells. CS cells were predominantly found in nondysplastic BE biopsies. The single-base substitution (SBS) signatures of all CS BE cells analyzed were indistinguishable from those of nondiseased esophageal or gastric cells. Single-cell RNA-sequencing (scRNAseq) experiments with BE biopsies identified two sets of marker genes which facilitate the distinction between columnar BE epithelium and nondysplastic/dysplastic stages. Moreover, histological validation confirmed a correlation between increased CLDN2 expression and the presence of dysplastic BE stages. Our scDNAseq and scRNAseq datasets, which are a useful resource for the community, provide insight into the mutational landscape and gene expression pattern at different stages of BE development.
AB - Barrett's esophagus (BE) is categorized, based on morphological appearance, into different stages, which correlate with the risk of developing esophageal adenocarcinoma. More advanced stages are more likely to acquire chromosomal instabilities, but stage-specific markers remain elusive. Here, we performed single-cell DNA-sequencing experiments (scDNAseq) with fresh BE biopsies. Dysplastic BE cells frequently contained chromosomal instability (CIN) regions, and these CIN cells carried mutations corresponding to the COSMIC mutational signature SBS17, which were not present in biopsy-matched chromosomally stable (CS) cells or patient-matched nondiseased control cells. CS cells were predominantly found in nondysplastic BE biopsies. The single-base substitution (SBS) signatures of all CS BE cells analyzed were indistinguishable from those of nondiseased esophageal or gastric cells. Single-cell RNA-sequencing (scRNAseq) experiments with BE biopsies identified two sets of marker genes which facilitate the distinction between columnar BE epithelium and nondysplastic/dysplastic stages. Moreover, histological validation confirmed a correlation between increased CLDN2 expression and the presence of dysplastic BE stages. Our scDNAseq and scRNAseq datasets, which are a useful resource for the community, provide insight into the mutational landscape and gene expression pattern at different stages of BE development.
KW - Barrett's esophagus
KW - Single-base substitution 17 (SBS17a and SBS17b)
KW - Single-cell RNA and DNA analyses
UR - https://www.scopus.com/pages/publications/85120359183
U2 - 10.1073/pnas.2113061118
DO - 10.1073/pnas.2113061118
M3 - Article
C2 - 34795059
SN - 0027-8424
VL - 118
SP - 1
EP - 12
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 47
M1 - e2113061118
ER -