A TIM-3-Fc decoy secreted by engineered T cells improves CD19 CAR T-cell therapy in B-cell acute lymphoblastic leukemia.


Por: Falgàs A, Lázaro-Gorines R, Zanetti SR, Rubio-Pérez L, Martinez-Moreno A, Vinyoles M, Guerrero-Murillo M, Fernandez-Fuentes N, Roca-Ho H, Tirado N, Panisello C, Velasco-Hernandez T, Mayado A, Pérez-Pons A, Genesca E, Ribera JM, Ribera J, Camós-Guijosa M, Ramírez-Orellana M, Anguita E, Ballerini P, Fuster JL, Juan M, González-Navarro EAA, Locatelli F, Stam RWW, Querol S, Velasco P, Ortiz-Maldonado V, Martínez-Cibrian N, Delgado J, Orfao A, Alvarez-Vallina L, Bueno C and Menendez P

Publicada: 29 may 2025 Ahead of Print: 1 may 2025
Resumen:
Relapsed or refractory (R/R) B-cell acute lymphoblastic leukemia (B-ALL) remains a challenging disease with dismal prognosis. Despite the revolutionary impact of CD19-directed chimeric antigen receptor (CAR19) T-cell therapy, >50% of patients relapse within a year. Both leukemia cell-intrinsic factors favoring immune escape and poor CAR T-cell persistence contribute to clinical failure. Moreover, the expression of immune checkpoint receptors (ICRs) and their ligands within the bone marrow (BM) microenvironment may contribute to leukemia progression and therapy resistance. Here, we characterized the expression of ICRs and their ligands in leukemic blasts, T cells, and mesenchymal stromal cells (MSCs) from B-ALL BM samples at diagnosis and relapse, comparing them with age-matched healthy BM controls. Our findings reveal a significantly upregulated expression of TIM-3 in T cells and its ligand, galectin-9, in both blasts and MSCs throughout disease progression. The expression of galectin-9 in B-ALL blasts and TIM-3 in CAR19 T cells negatively correlates with clinical outcome. Furthermore, we demonstrate that galectin-9 impairs CAR19 T-cell homeostasis and cytotoxicity. Notably, an engineered TIM-3-Fc decoy receptor, delivered either by primary T cells coadministered with CAR19 T cells or via a bicistronic all-in-one CAR19-TIM-3-Fc construct, improved the antileukemia efficacy and persistence of CAR19 T cells in B-ALL xenograft models. Mechanistically, CAR19-TIM-3-Fc T-cell treatment promotes the in vivo expansion of transduced and bystander effector and memory T cells, as determined by spectral flow cytometry. Collectively, these TIM-3-Fc decoy-armored CAR19 T cells offer a promising therapeutic strategy for patients with R/R B-ALL.

Filiaciones:
Falgàs A:
 Josep Carreras Leukemia Research Institute, Barcelona, Spain

Lázaro-Gorines R:
 Centro Nacional de Investigaciones Oncológicas (CNIO), Madrid, Spain

Zanetti SR:
 Josep Carreras Leukemia Research Institute, Barcelona, Spain

Rubio-Pérez L:
 Hospital Universitario 12 de Octubre, Madrid, Spain

Martinez-Moreno A:
 Josep Carreras Leukaemia Research Institute, Department of Biomedicine, School of Medicine,, Barcelona, Spain

Vinyoles M:
 Josep Carreras Leukemia Research Institute, Barcelona, Spain

Guerrero-Murillo M:
 Josep Carreras Leukaemia Research Institute, Barcelona, Spain

Fernandez-Fuentes N:
 Josep Carreras Leukemia Research Institute., Barcelona, Spain

Roca-Ho H:
 IJC, Barcelona, Spain

Tirado N:
 Josep Carreras Leukaemia Research Institute, Barcelona, Spain

Panisello C:
 Josep Carreras Leukemia Research Institute, Barcelona, Spain

Velasco-Hernandez T:
 University of Barcelona, Barcelona, Spain

Mayado A:
 Centro de Investigación del Cáncer (IBMCC-CSIC/USAL and IBSAL),Biomedical Research Networking Centre Consortium of Oncology (CIBERONC) (CB16/12/00400), Instituto de Salud Carlos III, Salamanca, Spain

Pérez-Pons A:
 University of Salamanca. Cancer Research Center (IBMCC, USAL-CSIC) and IBSAL, Salamanca, Spain

Genesca E:
 Josep Carreras Leukaemia Research Institute, Badalona, Spain

Ribera JM:
 Institut Català d'Oncologia-Hospital Germans Trias i Pujol. Josep Carreras Research Institute. Badalona. Universitat Autònoma de Barcelona, Badalona, Spain

Ribera J:
 ICO-Hospital Germans Trias i Pujol. Institut de Recerca contra la Leucèmia Josep Carreras, Badalona, Spain

Camós-Guijosa M:
 Hospital Sant Joan de Déu, Barcelona, Spain

Ramírez-Orellana M:
 Department of Pediatric Hematology and Oncology, Hospital Infantil Universitario Niño Jesús, Madrid, Spain

Anguita E:
 University Complutense, Madrid, Spain

Ballerini P:
 Hopital A. TROUSSEAU, Sorbonne Université, AP-HP, Paris, France

Fuster JL:
 Hospital Clínico Universitario Virgen de la Arrixaca. Instituto Murciano de Investigación Biosanitaria (IMIB), Pilar de la Horadada. Alicante, Spain

Juan M:
 Hospital Clínic de Barcelona, Barcelona, Spain

González-Navarro EAA:
 Hospital Clinic, Barcelona, Spain

Locatelli F:
 Bambino Gesù Children's Hospital, Roma, Italy

Stam RWW:
 Princess Maxima Center for Pediatric Oncology, Utrecht, Netherlands

Querol S:
 Fundació Internacional Josep Carreras, Barcelona, Spain

Velasco P:
 University Hospital Vall d´Hebron, BARCELONA, Spain

Ortiz-Maldonado V:
 Hospital Clinic, Barcelona, Spain

Martínez-Cibrian N:
 Hospital Clinic, Barcelona, Spain

Delgado J:
 Hospital Clinic, Barcelona, Spain

Orfao A:
 University of Salamanca, Salamanca, Spain

Alvarez-Vallina L:
 Spanish National Cancer Reserach Centre (CNIO), Madrid, Spain

Bueno C:
 Josep Carreras Leukemia Research Institute, Barcelona, Spain

:
 Josep Carreras Leukaemia Research Institute, Barcelona, Spain
ISSN: 00064971





BLOOD
Editorial
ELSEVIER, RADARWEG 29, 1043 NX AMSTERDAM, NETHERLANDS, Estados Unidos America
Tipo de documento: Article
Volumen: 145 Número: 22
Páginas: 2599-2613
WOS Id: 001505196400013
ID de PubMed: 40090006
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