Integrative genomic analysis of DLBCL identifies immune environments associated with bispecific antibody response

S Sravya Tumuluru (1Weill Cornell Medicine, Hematology and Oncology, New York, United States) J James K. Godfrey (2Department of Hematology & Hematopoietic Cell Transplantation, City of Hope, Duarte, CA) A Alan Cooper (3Yale University School of Medicine, New Haven, United States) J Jovian Yu (15AbbVie Inc., North Chicago, United States) X Xiufen Chen (3Section of Hematology/Oncology, Department of Medicine, The University of Chicago, Chicago, IL) B Brendan W. MacNabb (4Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA) G Girish Venkataraman (2University of Chicago, Department of Pathology, Illinois, United States) Y Yuanyuan Zha B Benedikt Pelzer (1Weill Cornell Medicine, Hematology and Oncology, New York, United States) J Joo Song (1City of Hope National Medical Center, Department of Hematology and Hematopoietic Cell Transplantation, Duarte, United States) G Gerben Duns (1Centre for Lymphoid Cancer, British Columbia Cancer, Vancouver, BC, Canada) B Brian J. Sworder S Sandeep Raj (1Adult Bone Marrow Transplantation Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY) C Christopher Bolen (11Genentech Inc, South San Francisco, CA) E Elicia Penuel (12Genentech, Inc, South San Francisco, CA) E Ekaterina Postovalova N Nikita Kotlov (2BostonGene Corporation, Waltham, United States) A Aleksander Bagaev (12BostonGene Corporation, Waltham, MA) N Nathan Fowler (39Department of Hematology and Oncology, MD Anderson Cancer Center, Houston, TX) R Roni Shouval (1Adult Bone Marrow Transplantation Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY) S Sonali M. Smith (3Section of Hematology/Oncology, Department of Medicine, The University of Chicago, Chicago, IL) A Ash A. Alizadeh C Christian Steidl (5Centre for Lymphoid Cancer, British Columbia Cancer, Vancouver, Canada) J Justin Kline (16University of Chicago Comprehensive Cancer Center, Chicago, United States)

Abstract

Abstract Most patients with diffuse large B-cell lymphoma (DLBCL) treated with immunotherapies such as bispecific antibodies (BsAbs) or chimeric antigen receptor (CAR) T cells fail to achieve durable treatment responses, underscoring the need for a deeper understanding of mechanisms that regulate the immune environment and response to treatment. Here, an integrative multiomics approach was applied to multiple large independent data sets to characterize DLBCL immune environments and to define their association with tumor cell–intrinsic genomic alterations and outcomes to CD19-directed CAR T-cell and CD20 × CD3 BsAb therapies. This approach effectively segregated DLBCLs into 4 immune quadrants (IQs) defined by cell-of-origin and immune-related gene set expression scores. These quadrants consisted of activated B cell–like (ABC) hot, ABC cold, germinal center B cell–like (GCB) hot, and GCB cold DLBCLs. Recurrent genomic alterations were enriched in each IQ, suggesting that lymphoma cell-intrinsic alterations contribute significantly to orchestrating unique DLBCL immune environments. For instance, SOCS1 loss-of-function mutations were significantly enriched among GCB hot DLBCLs, identifying a putative subset of inflamed DLBCLs that may be inherently susceptible to immunotherapy. In patients with relapsed/refractory DLBCL, DLBCL-IQ assignment correlated significantly with clinical benefit with a CD20 × CD3 BsAb (N = 74), but not with CD19-directed CAR T cells (Stanford, N = 51; Memorial Sloan Kettering Cancer Center, N = 69). Thus, DLBCL-IQ provides a new framework to conceptualize the DLBCL immune landscape and suggests the endogenous immune environment has a more significant impact on outcomes to BsAb than CAR T-cell treatment.

Article Details

Journal Blood
Volume / Issue Vol. 145, Issue 21
Published May 22, 2025
Pages 2460-2472
ISSN 0006-4971
Publisher Elsevier BV

Journal Info

Blood

Elsevier BV

ISSN: 0006-4971 Health Sciences

Authors (24)

S

Sravya Tumuluru

1Weill Cornell Medicine, Hematology and Oncology, New York, United States

J

James K. Godfrey

2Department of Hematology & Hematopoietic Cell Transplantation, City of Hope, Duarte, CA

A

Alan Cooper

3Yale University School of Medicine, New Haven, United States

J

Jovian Yu

15AbbVie Inc., North Chicago, United States

X

Xiufen Chen

3Section of Hematology/Oncology, Department of Medicine, The University of Chicago, Chicago, IL

B

Brendan W. MacNabb

4Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA

G

Girish Venkataraman

2University of Chicago, Department of Pathology, Illinois, United States

Y

Yuanyuan Zha

B

Benedikt Pelzer

1Weill Cornell Medicine, Hematology and Oncology, New York, United States

J

Joo Song

1City of Hope National Medical Center, Department of Hematology and Hematopoietic Cell Transplantation, Duarte, United States

G

Gerben Duns

1Centre for Lymphoid Cancer, British Columbia Cancer, Vancouver, BC, Canada

B

Brian J. Sworder

S

Sandeep Raj

1Adult Bone Marrow Transplantation Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY

C

Christopher Bolen

11Genentech Inc, South San Francisco, CA

E

Elicia Penuel

12Genentech, Inc, South San Francisco, CA

E

Ekaterina Postovalova

N

Nikita Kotlov

2BostonGene Corporation, Waltham, United States

A

Aleksander Bagaev

12BostonGene Corporation, Waltham, MA

N

Nathan Fowler

39Department of Hematology and Oncology, MD Anderson Cancer Center, Houston, TX

R

Roni Shouval

1Adult Bone Marrow Transplantation Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY

S

Sonali M. Smith

3Section of Hematology/Oncology, Department of Medicine, The University of Chicago, Chicago, IL

A

Ash A. Alizadeh

C

Christian Steidl

5Centre for Lymphoid Cancer, British Columbia Cancer, Vancouver, Canada

J

Justin Kline

16University of Chicago Comprehensive Cancer Center, Chicago, United States