BTLA dysregulation correlates with poor outcome and diminished T cell-mediated antitumor responses in chronic lymphocytic leukemia
Patients with chronic lymphocytic leukemia (CLL) progressively develop marked immunosuppression, dampening innate and adaptive-driven antitumor responses. However, the underlying mechanisms promoting immune exhaustion are largely unknown. Herein, we provide new insights into the role of BTLA/HVEM ax...
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Published in | Cancer Immunology, Immunotherapy Vol. 72; no. 7; pp. 2529 - 2539 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Berlin/Heidelberg
Springer Berlin Heidelberg
01.07.2023
Springer Nature B.V |
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Abstract | Patients with chronic lymphocytic leukemia (CLL) progressively develop marked immunosuppression, dampening innate and adaptive-driven antitumor responses. However, the underlying mechanisms promoting immune exhaustion are largely unknown. Herein, we provide new insights into the role of BTLA/HVEM axis promoting defects in T cell-mediated responses against leukemic cells. Increased expression of BTLA, an inhibitory immune checkpoint, was detected on the surface of CD4 + and CD8 + T lymphocytes in patients with CLL. Moreover, high levels of BTLA on CD4 + T cells correlated with diminished time to treatment. Signaling through BTLA activation led to decreased IL-2 and IFN-γ production ex vivo, whereas BTLA/HVEM binding disruption enhanced IFN-γ + CD8 + T lymphocytes. Accordingly, BTLA blockade in combination with bispecific anti-CD3/anti-CD19 antibody promoted CD8 + T cell-mediated anti-leukemic responses. Finally, treatment with an anti-BLTA blocking monoclonal antibody alone or in combination with ibrutinib-induced leukemic cell depletion in vitro. Altogether, our data reveal that BTLA dysregulation has a prognostic role and is limiting T cell-driven antitumor responses, thus providing new insights about immune exhaustion in patients with CLL. |
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AbstractList | Patients with chronic lymphocytic leukemia (CLL) progressively develop marked immunosuppression, dampening innate and adaptive-driven antitumor responses. However, the underlying mechanisms promoting immune exhaustion are largely unknown. Herein, we provide new insights into the role of BTLA/HVEM axis promoting defects in T cell-mediated responses against leukemic cells. Increased expression of BTLA, an inhibitory immune checkpoint, was detected on the surface of CD4 + and CD8 + T lymphocytes in patients with CLL. Moreover, high levels of BTLA on CD4 + T cells correlated with diminished time to treatment. Signaling through BTLA activation led to decreased IL-2 and IFN-γ production ex vivo, whereas BTLA/HVEM binding disruption enhanced IFN-γ + CD8 + T lymphocytes. Accordingly, BTLA blockade in combination with bispecific anti-CD3/anti-CD19 antibody promoted CD8 + T cell-mediated anti-leukemic responses. Finally, treatment with an anti-BLTA blocking monoclonal antibody alone or in combination with ibrutinib-induced leukemic cell depletion in vitro. Altogether, our data reveal that BTLA dysregulation has a prognostic role and is limiting T cell-driven antitumor responses, thus providing new insights about immune exhaustion in patients with CLL. Abstract Patients with chronic lymphocytic leukemia (CLL) progressively develop marked immunosuppression, dampening innate and adaptive-driven antitumor responses. However, the underlying mechanisms promoting immune exhaustion are largely unknown. Herein, we provide new insights into the role of BTLA/HVEM axis promoting defects in T cell-mediated responses against leukemic cells. Increased expression of BTLA, an inhibitory immune checkpoint, was detected on the surface of CD4 + and CD8 + T lymphocytes in patients with CLL. Moreover, high levels of BTLA on CD4 + T cells correlated with diminished time to treatment. Signaling through BTLA activation led to decreased IL-2 and IFN-γ production ex vivo, whereas BTLA/HVEM binding disruption enhanced IFN-γ + CD8 + T lymphocytes. Accordingly, BTLA blockade in combination with bispecific anti-CD3/anti-CD19 antibody promoted CD8 + T cell-mediated anti-leukemic responses. Finally, treatment with an anti-BLTA blocking monoclonal antibody alone or in combination with ibrutinib-induced leukemic cell depletion in vitro. Altogether, our data reveal that BTLA dysregulation has a prognostic role and is limiting T cell-driven antitumor responses, thus providing new insights about immune exhaustion in patients with CLL. |
Author | Gonzalez, Segundo Sordo-Bahamonde, Christian López-Soto, Alejandro Martínez-Pérez, Alejandra Aguilar-García, Candelaria Gonzalez-Rodriguez, Ana P. García-Torre, Alejandra González-García, Esther González-Rodríguez, Sara Payer, Ángel R. Lorenzo-Herrero, Seila |
Author_xml | – sequence: 1 givenname: Christian surname: Sordo-Bahamonde fullname: Sordo-Bahamonde, Christian email: christiansbl87@gmail.com organization: Department of Functional Biology, Immunology, Universidad de Oviedo, Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA) – sequence: 2 givenname: Seila surname: Lorenzo-Herrero fullname: Lorenzo-Herrero, Seila organization: Department of Functional Biology, Immunology, Universidad de Oviedo, Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA) – sequence: 3 givenname: Alejandra surname: Martínez-Pérez fullname: Martínez-Pérez, Alejandra organization: Department of Functional Biology, Immunology, Universidad de Oviedo, Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA) – sequence: 4 givenname: Ana P. surname: Gonzalez-Rodriguez fullname: Gonzalez-Rodriguez, Ana P. organization: Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Department of Hematology, Hospital Universitario Central de Asturias (HUCA) – sequence: 5 givenname: Ángel R. surname: Payer fullname: Payer, Ángel R. organization: Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Department of Hematology, Hospital Universitario Central de Asturias (HUCA) – sequence: 6 givenname: Esther surname: González-García fullname: González-García, Esther organization: Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Department of Hematology, Hospital de Cabueñes – sequence: 7 givenname: Candelaria surname: Aguilar-García fullname: Aguilar-García, Candelaria organization: Department of Functional Biology, Immunology, Universidad de Oviedo, Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA) – sequence: 8 givenname: Sara surname: González-Rodríguez fullname: González-Rodríguez, Sara organization: Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Department of Medicine, Universidad de Oviedo – sequence: 9 givenname: Alejandro surname: López-Soto fullname: López-Soto, Alejandro organization: Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Department of Biochemistry and Molecular Biology, Universidad of Oviedo – sequence: 10 givenname: Alejandra surname: García-Torre fullname: García-Torre, Alejandra organization: Department of Immunology, Hospital Universitario Central de Asturias (HUCA) – sequence: 11 givenname: Segundo surname: Gonzalez fullname: Gonzalez, Segundo email: segundog@uniovi.es organization: Department of Functional Biology, Immunology, Universidad de Oviedo, Instituto Universitario de Oncología del Principado de Asturias (IUOPA), Instituto de Investigación Sanitaria del Principado de Asturias (ISPA) |
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CitedBy_id | crossref_primary_10_1177_25151355231192043 crossref_primary_10_1016_j_isci_2024_110253 crossref_primary_10_1186_s40364_024_00556_2 crossref_primary_10_1186_s12943_023_01845_4 |
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Keywords | BTLA CLL Checkpoint HVEM Leukemia T cell |
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Snippet | Patients with chronic lymphocytic leukemia (CLL) progressively develop marked immunosuppression, dampening innate and adaptive-driven antitumor responses.... Abstract Patients with chronic lymphocytic leukemia (CLL) progressively develop marked immunosuppression, dampening innate and adaptive-driven antitumor... |
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SubjectTerms | Antigens, CD19 - metabolism Antitumor activity Brief Report BTLA protein Cancer Research CD19 antigen CD3 antigen CD4 antigen CD4-Positive T-Lymphocytes CD8 antigen CD8-Positive T-Lymphocytes Chronic lymphocytic leukemia Humans Immune checkpoint Immunology Immunosuppression Interleukin 2 Leukemia Leukemia, Lymphocytic, Chronic, B-Cell - metabolism Lymphocytes Lymphocytes T Medicine Medicine & Public Health Monoclonal antibodies Oncology Receptors, Immunologic - metabolism γ-Interferon |
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Title | BTLA dysregulation correlates with poor outcome and diminished T cell-mediated antitumor responses in chronic lymphocytic leukemia |
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