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Single-cell multi-omics identifies chronic inflammation as a driver of TP53-mutant leukemic evolution

Abstract:
Understanding the genetic and nongenetic determinants of tumor protein 53 (TP53)-mutation-driven clonal evolution and subsequent transformation is a crucial step toward the design of rational therapeutic strategies. Here we carry out allelic resolution single-cell multi-omic analysis of hematopoietic stem/progenitor cells (HSPCs) from patients with a myeloproliferative neoplasm who transform to TP53-mutant secondary acute myeloid leukemia (sAML). All patients showed dominant TP53 ‘multihit’ HSPC clones at transformation, with a leukemia stem cell transcriptional signature strongly predictive of adverse outcomes in independent cohorts, across both TP53-mutant and wild-type (WT) AML. Through analysis of serial samples, antecedent TP53-heterozygous clones and in vivo perturbations, we demonstrate a hitherto unrecognized effect of chronic inflammation, which suppressed TP53 WT HSPCs while enhancing the fitness advantage of TP53-mutant cells and promoted genetic evolution. Our findings will facilitate the development of risk-stratification, early detection and treatment strategies for TP53-mutant leukemia, and are of broad relevance to other cancer types.
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1038/s41588-023-01480-1

Authors

More by this author
Institution:
University of Oxford
Division:
MSD
Department:
RDM
Sub department:
Weatherall Insti. of Molecular Medicine
Role:
Author
ORCID:
0000-0001-9630-6968
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
RDM
Sub department:
Weatherall Insti. of Molecular Medicine
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
RDM
Sub department:
Weatherall Insti. of Molecular Medicine
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
RDM
Sub department:
Weatherall Insti. of Molecular Medicine
Role:
Author


Publisher:
Springer Nature
Journal:
Nature Genetics More from this journal
Volume:
55
Issue:
9
Pages:
1531–1541
Place of publication:
United States
Publication date:
2023-09-04
Acceptance date:
2023-07-20
DOI:
EISSN:
1546-1718
ISSN:
1061-4036
Pmid:
37666991


Language:
English
Keywords:
Pubs id:
1522015
Local pid:
pubs:1522015
Deposit date:
2024-01-10
ARK identifier:

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