Single-cell panleukemia signatures of HSPC-like blasts predict drug response and clinical outcome

C Changya Chen (2Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, China) J Jason Xu J Jonathan H. Sussman T Tiffaney Vincent (3Division of Oncology and Center for Childhood Cancer Research, Children's Hospital of Philadelphia, Philadelphia, PA) J Joseph S. Tumulty (3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA) S Satoshi Yoshimura (Department of Pharmacy and Pharmaceutical Sciences) F Fatemeh Alikarami (1Center for Childhood Cancer Research, The Children's Hospital of Philadelphia, Oncology, Philadelphia, United States) W Wenbao Yu (2Children's Hospital of Philadelphia, Philadelphia, United States) Y Yang-yang Ding (8Departments of Oncology and Pediatrics, Johns Hopkins University School of Medicine and Sidney Kimmel Comprehensive Cancer Center, Baltimore, MD) C Chia-Hui Chen (5Children's Hospital of Philadelphia, Center for Childhood Cancer Research, Philadelphia, United States) E Elizabeth Y. Li (3Division of Oncology and Center for Childhood Cancer Research, Children's Hospital of Philadelphia, Philadelphia, PA) A Austin Yang (7Division of Oncology, Children’s Hospital of Philadelphia, Philadelphia, PA) X Xiaohuan Qin S Shovik Bandyopadhyay (2Medical Scientist Training Program, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA) J Jacqueline Peng (4Graduate Group in Genomics and Computational Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA) P Petri Pölönen H Haley Newman (1Children's Hospital of Philadelphia, Division of Oncology, Philadelphia, United States) B Brent L. Wood (Department of Pathology and Laboratory Medicine, Children’s Hospital of Los Angeles, Los Angeles) J Jianzhong Hu R Rawan Shraim A Andrew D. Hughes (3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA) C Caroline Diorio L Lahari Uppuluri (4Children's Hospital of Philadelphia, Division of Oncology and Center for Childhood Cancer Research, Philadelphia, United States) G Gongping Shi (3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA) T Theresa Ryan (3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA) T Tori Fuller (3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA) M Mignon L. Loh (Seattle Children’s Hospital, Seattle) E Elizabeth A. Raetz (Department of Pediatrics and Perlmutter Cancer Center, NYU Langone Health, New York) S Stephen P. Hunger (Department of Pediatrics and the Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia) S Stanley B. Pounds (3Department of Biostatistics, St. Jude Children’s Research Hospital, Memphis, TN) C Charles G. Mullighan D David Frank J Jun J. Yang (Department of Pharmacy and Pharmaceutical Sciences) K Kathrin M. Bernt D David T. Teachey K Kai Tan

Abstract

Abstract The critical role of leukemia-initiating cells as a therapy-resistant population in myeloid leukemia is well established. However, the molecular signatures of such cells in acute lymphoblastic leukemia remain underexplored. Moreover, their role in therapy response and patient prognosis is yet to be systematically investigated across various types of acute leukemia. We used single-cell multiomics to analyze diagnostic specimens from 96 pediatric patients with acute lymphoblastic, myeloid, and lineage-ambiguous leukemias. Through the integration of single-cell multiomics with extensive bulk RNA sequencing and clinical data sets, we uncovered a prevalent, chemotherapy-resistant subpopulation that resembles hematopoietic stem and progenitor cells (HSPC-like) and is associated with poor clinical outcomes across all subtypes investigated. We identified a core transcriptional regulatory network (TRN) in HSPC-like blasts that is combinatorially controlled by HOXA/AP1/CEBPA. This TRN signature can predict chemotherapy response and long-term clinical outcomes. We identified shared potential therapeutic targets against HSPC-like blasts, including FLT3, BCL2, and the PI3K pathway. Our study provides a framework for linking intratumoral heterogeneity with therapy response, patient outcomes, and the discovery of new therapeutic targets for pediatric acute leukemias.

Article Details

Journal Blood
Volume / Issue Vol. 145, Issue 23
Published June 05, 2025
Pages 2685-2700
ISSN 0006-4971
Publisher Elsevier BV

Journal Info

Blood

Elsevier BV

ISSN: 0006-4971 Health Sciences

Authors (36)

C

Changya Chen

2Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, China

J

Jason Xu

J

Jonathan H. Sussman

T

Tiffaney Vincent

3Division of Oncology and Center for Childhood Cancer Research, Children's Hospital of Philadelphia, Philadelphia, PA

J

Joseph S. Tumulty

3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA

S

Satoshi Yoshimura

Department of Pharmacy and Pharmaceutical Sciences

F

Fatemeh Alikarami

1Center for Childhood Cancer Research, The Children's Hospital of Philadelphia, Oncology, Philadelphia, United States

W

Wenbao Yu

2Children's Hospital of Philadelphia, Philadelphia, United States

Y

Yang-yang Ding

8Departments of Oncology and Pediatrics, Johns Hopkins University School of Medicine and Sidney Kimmel Comprehensive Cancer Center, Baltimore, MD

C

Chia-Hui Chen

5Children's Hospital of Philadelphia, Center for Childhood Cancer Research, Philadelphia, United States

E

Elizabeth Y. Li

3Division of Oncology and Center for Childhood Cancer Research, Children's Hospital of Philadelphia, Philadelphia, PA

A

Austin Yang

7Division of Oncology, Children’s Hospital of Philadelphia, Philadelphia, PA

X

Xiaohuan Qin

S

Shovik Bandyopadhyay

2Medical Scientist Training Program, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA

J

Jacqueline Peng

4Graduate Group in Genomics and Computational Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA

P

Petri Pölönen

H

Haley Newman

1Children's Hospital of Philadelphia, Division of Oncology, Philadelphia, United States

B

Brent L. Wood

Department of Pathology and Laboratory Medicine, Children’s Hospital of Los Angeles, Los Angeles

J

Jianzhong Hu

R

Rawan Shraim

A

Andrew D. Hughes

3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA

C

Caroline Diorio

L

Lahari Uppuluri

4Children's Hospital of Philadelphia, Division of Oncology and Center for Childhood Cancer Research, Philadelphia, United States

G

Gongping Shi

3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA

T

Theresa Ryan

3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA

T

Tori Fuller

3Division of Oncology and Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia, PA

M

Mignon L. Loh

Seattle Children’s Hospital, Seattle

E

Elizabeth A. Raetz

Department of Pediatrics and Perlmutter Cancer Center, NYU Langone Health, New York

S

Stephen P. Hunger

Department of Pediatrics and the Center for Childhood Cancer Research, Children’s Hospital of Philadelphia, Philadelphia

S

Stanley B. Pounds

3Department of Biostatistics, St. Jude Children’s Research Hospital, Memphis, TN

C

Charles G. Mullighan

D

David Frank

J

Jun J. Yang

Department of Pharmacy and Pharmaceutical Sciences

K

Kathrin M. Bernt

D

David T. Teachey

K

Kai Tan