Enhancer heterogeneity in acute lymphoblastic leukemia drives differential gene expression in patients

A Alastair L. Smith N Nicholas Denny (1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom) C Catherine Chahrour (1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom) K Kim Sharp (1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom) M Marta Arachi (1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom) A Ana M. Dopico-Fernandez (1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom) N Natalina Elliott (University of Oxford, Headington, United Kingdom) J Joe R. Harman (1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom) T Thomas Jackson H Huimin Geng O Owen Smith J Jonathan Bond (7National Children's Cancer Service, Children's Health Ireland at Crumlin, Dublin, Ireland) I Irene Roberts R Ronald W. Stam N Nicholas T. Crump (6Hugh and Josseline Langmuir Centre for Myeloma Research, Centre for Haematology, Department of Immunology and Inflammation, Imperial College London, London, United Kingdom) J James O. J. Davies A Anindita Roy T Thomas A. Milne (MRC Molecular Haematology Unit, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine)

Abstract

Abstract Genetic alterations alone cannot account for the diverse phenotypes of cancer cells. Even cancers with the same driver mutation show significant transcriptional heterogeneity and varied responses to therapy. However, the mechanisms underpinning this heterogeneity remain underexplored. Here, we find that novel enhancer usage is a common feature in acute lymphoblastic leukemia (ALL). In particular, KMT2A::AFF1 ALL, an aggressive leukemia with a poor prognosis and a low mutational burden, exhibits substantial transcriptional heterogeneity between individuals. Using single-cell multiome analysis and extensive chromatin profiling, we reveal that much transcriptional heterogeneity in KMT2A::AFF1 ALL is driven by novel enhancer usage. By generating high-resolution Micro Capture-C data in primary patient samples, we identify patient-specific enhancer activity at key oncogenes such as MEIS1 and RUNX2, driving high levels of expression of both oncogenes in a patient-specific manner. Overall, our data show that enhancer heterogeneity is highly prevalent in KMT2A::AFF1 ALL and may be a mechanism that drives transcriptional heterogeneity in cancer more generally.

Article Details

Journal Blood
Volume / Issue Vol. 146, Issue 17
Published October 23, 2025
Pages 2073-2087
ISSN 0006-4971
Publisher Elsevier BV

Journal Info

Blood

Elsevier BV

ISSN: 0006-4971 Health Sciences

Authors (18)

A

Alastair L. Smith

N

Nicholas Denny

1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom

C

Catherine Chahrour

1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom

K

Kim Sharp

1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom

M

Marta Arachi

1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom

A

Ana M. Dopico-Fernandez

1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom

N

Natalina Elliott

University of Oxford, Headington, United Kingdom

J

Joe R. Harman

1Medical Research Council Molecular Haematology Unit, Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom

T

Thomas Jackson

H

Huimin Geng

O

Owen Smith

J

Jonathan Bond

7National Children's Cancer Service, Children's Health Ireland at Crumlin, Dublin, Ireland

I

Irene Roberts

R

Ronald W. Stam

N

Nicholas T. Crump

6Hugh and Josseline Langmuir Centre for Myeloma Research, Centre for Haematology, Department of Immunology and Inflammation, Imperial College London, London, United Kingdom

J

James O. J. Davies

A

Anindita Roy

T

Thomas A. Milne

MRC Molecular Haematology Unit, MRC Weatherall Institute of Molecular Medicine, Radcliffe Department of Medicine