B-cell-specific checkpoint molecules that regulate anti-tumour immunity
The role of B cells in anti-tumour immunity is still debated and, accordingly, immunotherapies have focused on targeting T and natural killer cells to inhibit tumour growth 1 , 2 . Here, using high-throughput flow cytometry as well as bulk and single-cell RNA-sequencing and B-cell-receptor-sequencin...
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| Published in: | Nature (London) Vol. 619; no. 7969; pp. 348 - 356 |
|---|---|
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
London
Nature Publishing Group UK
13.07.2023
Nature Publishing Group |
| Subjects: | |
| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
| Online Access: | Get full text |
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| Abstract | The role of B cells in anti-tumour immunity is still debated and, accordingly, immunotherapies have focused on targeting T and natural killer cells to inhibit tumour growth
1
,
2
. Here, using high-throughput flow cytometry as well as bulk and single-cell RNA-sequencing and B-cell-receptor-sequencing analysis of B cells temporally during B16F10 melanoma growth, we identified a subset of B cells that expands specifically in the draining lymph node over time in tumour-bearing mice. The expanding B cell subset expresses the cell surface molecule T cell immunoglobulin and mucin domain 1 (TIM-1, encoded by
Havcr1
) and a unique transcriptional signature, including multiple co-inhibitory molecules such as PD-1, TIM-3, TIGIT and LAG-3. Although conditional deletion of these co-inhibitory molecules on B cells had little or no effect on tumour burden, selective deletion of
Havcr1
in B cells both substantially inhibited tumour growth and enhanced effector T cell responses. Loss of TIM-1 enhanced the type 1 interferon response in B cells, which augmented B cell activation and increased antigen presentation and co-stimulation, resulting in increased expansion of tumour-specific effector T cells. Our results demonstrate that manipulation of TIM-1-expressing B cells enables engagement of the second arm of adaptive immunity to promote anti-tumour immunity and inhibit tumour growth.
Manipulation of TIM-1-expressing B cells enables engagement of the second arm of adaptive immunity to promote anti-tumour immunity and inhibit tumour growth. |
|---|---|
| AbstractList | The role ofB cells in anti-tumour immunity is still debated and, accordingly, immunotherapies have focused on targeting T and natural killer cells to inhibit tumour growth1,2. Here, using high-throughput flow cytometry as well as bulk and single-cell RNA-sequencing and B-cell-receptor-sequencing analysis ofB cells temporally during B16F10 melanoma growth, we identified a subset of B cells that expands specifically in the draining lymph node over time in tumour-bearing mice. The expanding B cell subset expresses the cell surface molecule T cell immunoglobulin and mucin domain 1 (TIM-1, encoded by Haveri) and a unique transcriptional signature, including multiple co-inhibitory molecules such as PD-1, TIM-3, TIGIT and LAG-3. Although conditional deletion ofthese co-inhibitory molecules on B cells had little or no effect on tumour burden, selective deletion of Haveri in B cells both substantially inhibited tumour growth and enhanced effector T cell responses. Loss of TIM-1 enhanced the type 1 interferon response in B cells, which augmented B cell activation and increased antigen presentation and co-stimulation, resulting in increased expansion of tumour-specific effector T cells. Our results demonstrate that manipulation of TIM-1-expressing B cells enables engagement of the second arm of adaptive immunity to promote anti-tumour immunity and inhibit tumour growth. The role of B cells in anti-tumor immunity is still debated and accordingly, immunotherapies have focused on targeting T and NK cells to inhibit tumor growth1,2. Here, using high-throughput flow cytometry, bulk and single-cell RNA- and BCR-sequencing of B cells temporally during B16F10 melanoma growth, we identified a subset of B cells that expands specifically in the draining lymph node over time in tumor bearing-mice. The expanding B cell subset expresses the cell surface molecule T cell immunoglobulin and mucin domain 1 (TIM-1) and a unique transcriptional signature, including multiple co-inhibitory molecules such as PD-1, TIM-3, TIGIT and LAG-3. While conditional deletion of these co-inhibitory molecules on B cells had little or no effect on tumor burden, selective deletion of Havcr1 (the gene encoding TIM-1) in B cells both dramatically inhibited tumor growth and enhanced effector T cell responses. Loss of TIM-1 enhanced the type 1 interferon response in B cells, which augmented B cell activation and increased antigen presentation and co-stimulation, resulting in increased expansion of tumor-specific effector T cells. Our results demonstrate that manipulation of TIM-1-expressing B cells enables engagement of the second arm of adaptive immunity to promote anti-tumor immunity and inhibit tumor growth. The role of B cells in anti-tumour immunity is still debated and, accordingly, immunotherapies have focused on targeting T and natural killer cells to inhibit tumour growth . Here, using high-throughput flow cytometry as well as bulk and single-cell RNA-sequencing and B-cell-receptor-sequencing analysis of B cells temporally during B16F10 melanoma growth, we identified a subset of B cells that expands specifically in the draining lymph node over time in tumour-bearing mice. The expanding B cell subset expresses the cell surface molecule T cell immunoglobulin and mucin domain 1 (TIM-1, encoded by Havcr1) and a unique transcriptional signature, including multiple co-inhibitory molecules such as PD-1, TIM-3, TIGIT and LAG-3. Although conditional deletion of these co-inhibitory molecules on B cells had little or no effect on tumour burden, selective deletion of Havcr1 in B cells both substantially inhibited tumour growth and enhanced effector T cell responses. Loss of TIM-1 enhanced the type 1 interferon response in B cells, which augmented B cell activation and increased antigen presentation and co-stimulation, resulting in increased expansion of tumour-specific effector T cells. Our results demonstrate that manipulation of TIM-1-expressing B cells enables engagement of the second arm of adaptive immunity to promote anti-tumour immunity and inhibit tumour growth. The role of B cells in anti-tumour immunity is still debated and, accordingly, immunotherapies have focused on targeting T and natural killer cells to inhibit tumour growth1,2. Here, using high-throughput flow cytometry as well as bulk and single-cell RNA-sequencing and B-cell-receptor-sequencing analysis of B cells temporally during B16F10 melanoma growth, we identified a subset of B cells that expands specifically in the draining lymph node over time in tumour-bearing mice. The expanding B cell subset expresses the cell surface molecule T cell immunoglobulin and mucin domain 1 (TIM-1, encoded by Havcr1) and a unique transcriptional signature, including multiple co-inhibitory molecules such as PD-1, TIM-3, TIGIT and LAG-3. Although conditional deletion of these co-inhibitory molecules on B cells had little or no effect on tumour burden, selective deletion of Havcr1 in B cells both substantially inhibited tumour growth and enhanced effector T cell responses. Loss of TIM-1 enhanced the type 1 interferon response in B cells, which augmented B cell activation and increased antigen presentation and co-stimulation, resulting in increased expansion of tumour-specific effector T cells. Our results demonstrate that manipulation of TIM-1-expressing B cells enables engagement of the second arm of adaptive immunity to promote anti-tumour immunity and inhibit tumour growth.The role of B cells in anti-tumour immunity is still debated and, accordingly, immunotherapies have focused on targeting T and natural killer cells to inhibit tumour growth1,2. Here, using high-throughput flow cytometry as well as bulk and single-cell RNA-sequencing and B-cell-receptor-sequencing analysis of B cells temporally during B16F10 melanoma growth, we identified a subset of B cells that expands specifically in the draining lymph node over time in tumour-bearing mice. The expanding B cell subset expresses the cell surface molecule T cell immunoglobulin and mucin domain 1 (TIM-1, encoded by Havcr1) and a unique transcriptional signature, including multiple co-inhibitory molecules such as PD-1, TIM-3, TIGIT and LAG-3. Although conditional deletion of these co-inhibitory molecules on B cells had little or no effect on tumour burden, selective deletion of Havcr1 in B cells both substantially inhibited tumour growth and enhanced effector T cell responses. Loss of TIM-1 enhanced the type 1 interferon response in B cells, which augmented B cell activation and increased antigen presentation and co-stimulation, resulting in increased expansion of tumour-specific effector T cells. Our results demonstrate that manipulation of TIM-1-expressing B cells enables engagement of the second arm of adaptive immunity to promote anti-tumour immunity and inhibit tumour growth. The role of B cells in anti-tumour immunity is still debated and, accordingly, immunotherapies have focused on targeting T and natural killer cells to inhibit tumour growth 1 , 2 . Here, using high-throughput flow cytometry as well as bulk and single-cell RNA-sequencing and B-cell-receptor-sequencing analysis of B cells temporally during B16F10 melanoma growth, we identified a subset of B cells that expands specifically in the draining lymph node over time in tumour-bearing mice. The expanding B cell subset expresses the cell surface molecule T cell immunoglobulin and mucin domain 1 (TIM-1, encoded by Havcr1 ) and a unique transcriptional signature, including multiple co-inhibitory molecules such as PD-1, TIM-3, TIGIT and LAG-3. Although conditional deletion of these co-inhibitory molecules on B cells had little or no effect on tumour burden, selective deletion of Havcr1 in B cells both substantially inhibited tumour growth and enhanced effector T cell responses. Loss of TIM-1 enhanced the type 1 interferon response in B cells, which augmented B cell activation and increased antigen presentation and co-stimulation, resulting in increased expansion of tumour-specific effector T cells. Our results demonstrate that manipulation of TIM-1-expressing B cells enables engagement of the second arm of adaptive immunity to promote anti-tumour immunity and inhibit tumour growth. Manipulation of TIM-1-expressing B cells enables engagement of the second arm of adaptive immunity to promote anti-tumour immunity and inhibit tumour growth. |
| Author | Shi, Jingwen Li, Zhaorong Schnell, Alexandra Barilla, Rocky M. Apetoh, Lionel Torlai Triglia, Elena Sharpe, Arlene H. Giuliano, Christopher J. Xiao, Sheng Kuchroo, Vijay K. Fisher, David E. Zaghouani, Sarah Kuchroo, Juhi R. Kye, Yoon-Chul Quintana, Francisco J. Rothstein, David M. Slingerland, Nadine Ashenberg, Orr Regev, Aviv Mohib, Kanishka Bod, Lloyd Delorey, Toni Marie Rozenblatt-Rosen, Orit Ostrowski, Stephen M. Fessler, Johannes Von-Franque, Max Y. Christian, Elena |
| AuthorAffiliation | 5 Current address: Division of Immunology and Pathophysiology, Medical University of Graz, 8036 Graz, Austria 13 Currrent address: Genentech, 1 DNA Way, South San Francisco, CA 94025, USA 2 Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA, USA 14 Ann Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA 1 Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA 10 INSERM, U1100, Tours, France 3 Current address: Massachusetts General Hospital Cancer Center, Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA 6 Department of Dermatology, Massachusetts General Hospital, Boston, Massachusetts 7 Thomas E. Starzl Transplantation Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261 12 Howard Hughes Medical Institute, Department of Biology and Koch Institute of Integrative Cancer Research, Massac |
| AuthorAffiliation_xml | – name: 7 Thomas E. Starzl Transplantation Institute, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261 – name: 13 Currrent address: Genentech, 1 DNA Way, South San Francisco, CA 94025, USA – name: 2 Klarman Cell Observatory, Broad Institute of MIT and Harvard, Cambridge, MA, USA – name: 10 INSERM, U1100, Tours, France – name: 14 Ann Romney Center for Neurologic Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, USA – name: 1 Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, USA – name: 9 Current address: HiFiBio Therapeutics, Cambridge, MA 02139, USA – name: 5 Current address: Division of Immunology and Pathophysiology, Medical University of Graz, 8036 Graz, Austria – name: 8 Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA, USA – name: 4 Current address: BeiGene Co., Ltd., Beijing, China – name: 11 Faculté de Médecine, Université de Tours, Tours, France – name: 3 Current address: Massachusetts General Hospital Cancer Center, Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA – name: 12 Howard Hughes Medical Institute, Department of Biology and Koch Institute of Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA, USA – name: 6 Department of Dermatology, Massachusetts General Hospital, Boston, Massachusetts |
| Author_xml | – sequence: 1 givenname: Lloyd surname: Bod fullname: Bod, Lloyd organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Klarman Cell Observatory, Broad Institute of MIT and Harvard, Gene Lay Institute of Immunology and Inflammation, Brigham and Women’s Hospital, Massachusetts General Hospital and Harvard Medical School, Massachusetts General Hospital Cancer Center, Department of Medicine, Massachusetts General Hospital, Harvard Medical School – sequence: 2 givenname: Yoon-Chul orcidid: 0000-0003-0261-5247 surname: Kye fullname: Kye, Yoon-Chul organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Klarman Cell Observatory, Broad Institute of MIT and Harvard, Gene Lay Institute of Immunology and Inflammation, Brigham and Women’s Hospital, Massachusetts General Hospital and Harvard Medical School – sequence: 3 givenname: Jingwen surname: Shi fullname: Shi, Jingwen organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Klarman Cell Observatory, Broad Institute of MIT and Harvard, BeiGene – sequence: 4 givenname: Elena orcidid: 0000-0002-6059-0116 surname: Torlai Triglia fullname: Torlai Triglia, Elena organization: Klarman Cell Observatory, Broad Institute of MIT and Harvard – sequence: 5 givenname: Alexandra orcidid: 0000-0003-3442-7750 surname: Schnell fullname: Schnell, Alexandra organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Klarman Cell Observatory, Broad Institute of MIT and Harvard, Gene Lay Institute of Immunology and Inflammation, Brigham and Women’s Hospital, Massachusetts General Hospital and Harvard Medical School – sequence: 6 givenname: Johannes surname: Fessler fullname: Fessler, Johannes organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Division of Immunology and Pathophysiology, Medical University of Graz – sequence: 7 givenname: Stephen M. surname: Ostrowski fullname: Ostrowski, Stephen M. organization: Department of Dermatology, Massachusetts General Hospital – sequence: 8 givenname: Max Y. orcidid: 0000-0002-5232-6454 surname: Von-Franque fullname: Von-Franque, Max Y. organization: Department of Dermatology, Massachusetts General Hospital – sequence: 9 givenname: Juhi R. surname: Kuchroo fullname: Kuchroo, Juhi R. organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Microbiology and Immunobiology, Harvard Medical School – sequence: 10 givenname: Rocky M. orcidid: 0000-0002-8062-7246 surname: Barilla fullname: Barilla, Rocky M. organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Gene Lay Institute of Immunology and Inflammation, Brigham and Women’s Hospital, Massachusetts General Hospital and Harvard Medical School – sequence: 11 givenname: Sarah orcidid: 0000-0002-4467-6542 surname: Zaghouani fullname: Zaghouani, Sarah organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital – sequence: 12 givenname: Elena surname: Christian fullname: Christian, Elena organization: Klarman Cell Observatory, Broad Institute of MIT and Harvard – sequence: 13 givenname: Toni Marie orcidid: 0000-0001-6614-3803 surname: Delorey fullname: Delorey, Toni Marie organization: Klarman Cell Observatory, Broad Institute of MIT and Harvard – sequence: 14 givenname: Kanishka orcidid: 0000-0002-7332-5530 surname: Mohib fullname: Mohib, Kanishka organization: Thomas E. Starzl Transplantation Institute, University of Pittsburgh School of Medicine – sequence: 15 givenname: Sheng surname: Xiao fullname: Xiao, Sheng organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital – sequence: 16 givenname: Nadine orcidid: 0000-0002-3134-6472 surname: Slingerland fullname: Slingerland, Nadine organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Klarman Cell Observatory, Broad Institute of MIT and Harvard – sequence: 17 givenname: Christopher J. orcidid: 0000-0002-0586-6095 surname: Giuliano fullname: Giuliano, Christopher J. organization: Klarman Cell Observatory, Broad Institute of MIT and Harvard – sequence: 18 givenname: Orr surname: Ashenberg fullname: Ashenberg, Orr organization: Klarman Cell Observatory, Broad Institute of MIT and Harvard – sequence: 19 givenname: Zhaorong orcidid: 0000-0002-5268-6986 surname: Li fullname: Li, Zhaorong organization: Ann Romney Center for Neurologic Diseases, Brigham and Women’s Hospital, Harvard Medical School – sequence: 20 givenname: David M. orcidid: 0000-0002-9455-7971 surname: Rothstein fullname: Rothstein, David M. organization: Thomas E. Starzl Transplantation Institute, University of Pittsburgh School of Medicine – sequence: 21 givenname: David E. surname: Fisher fullname: Fisher, David E. organization: Department of Dermatology, Massachusetts General Hospital – sequence: 22 givenname: Orit orcidid: 0000-0001-6313-3570 surname: Rozenblatt-Rosen fullname: Rozenblatt-Rosen, Orit organization: Klarman Cell Observatory, Broad Institute of MIT and Harvard, Howard Hughes Medical Institute, Department of Biology and Koch Institute of Integrative Cancer Research, Massachusetts Institute of Technology – sequence: 23 givenname: Arlene H. orcidid: 0000-0002-9736-2109 surname: Sharpe fullname: Sharpe, Arlene H. organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Department of Microbiology and Immunobiology, Harvard Medical School – sequence: 24 givenname: Francisco J. orcidid: 0000-0001-8156-0736 surname: Quintana fullname: Quintana, Francisco J. organization: Klarman Cell Observatory, Broad Institute of MIT and Harvard, Howard Hughes Medical Institute, Department of Biology and Koch Institute of Integrative Cancer Research, Massachusetts Institute of Technology – sequence: 25 givenname: Lionel orcidid: 0000-0002-2774-438X surname: Apetoh fullname: Apetoh, Lionel organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, INSERM, Faculté de Médecine, Université de Tours – sequence: 26 givenname: Aviv orcidid: 0000-0003-3293-3158 surname: Regev fullname: Regev, Aviv email: aviv.regev.sc@gmail.com organization: Klarman Cell Observatory, Broad Institute of MIT and Harvard, Howard Hughes Medical Institute, Department of Biology and Koch Institute of Integrative Cancer Research, Massachusetts Institute of Technology, Genentech – sequence: 27 givenname: Vijay K. orcidid: 0000-0001-7177-2110 surname: Kuchroo fullname: Kuchroo, Vijay K. email: vkuchroo@rics.bwh.harvard.edu organization: Evergrande Center for Immunologic Diseases, Harvard Medical School and Brigham and Women’s Hospital, Klarman Cell Observatory, Broad Institute of MIT and Harvard, Gene Lay Institute of Immunology and Inflammation, Brigham and Women’s Hospital, Massachusetts General Hospital and Harvard Medical School |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37344597$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author’s contribution LB and VKK conceived the study. LB with assistance from YCK, JS, AS, SMO, MYVF, DEF, JF, RMB, SZ, SX, designed, performed and analyzed the biological experiments. LB with assistance from YCK, JS, AS, EC, TMD, performed the sequencing experiments, with guidance from AR and ORR. LB, NS,CJG,ZL, FJQ, OA and ETT designed and performed the computational analysis, with guidance from AR. LB, JS, ETT, LA, VKK and AR interpreted the results. JRK and AH S generated and provided the PD-1fl/fl mice. KM and DMR generated and performed the experiments using the CD19Cre/+ x IL-10fl/fl mice. The manuscript was written by LB with assistance from ETT and was edited by LA, AR, and VKK with input from all authors. |
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| Snippet | The role of B cells in anti-tumour immunity is still debated and, accordingly, immunotherapies have focused on targeting T and natural killer cells to inhibit... The role ofB cells in anti-tumour immunity is still debated and, accordingly, immunotherapies have focused on targeting T and natural killer cells to inhibit... The role of B cells in anti-tumor immunity is still debated and accordingly, immunotherapies have focused on targeting T and NK cells to inhibit tumor... |
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| SubjectTerms | 13/1 13/31 45 45/91 631/114 631/250/580 631/67/1813/1634 64/60 Adaptive immunity Animals Antigen Presentation Antigens B-Lymphocytes - cytology B-Lymphocytes - immunology B-Lymphocytes - metabolism Cancer CD223 antigen Cell activation Cell surface Cells Deletion Effector cells Flow Cytometry Gene sequencing Humanities and Social Sciences Immunoglobulins Immunotherapy Interferon Type I Lymph nodes Lymph Nodes - cytology Lymph Nodes - immunology Lymphocyte Activation Lymphocytes Lymphocytes B Lymphocytes T Melanoma Melanoma - immunology Melanoma - pathology Melanoma - prevention & control Melanoma, Experimental - immunology Melanoma, Experimental - pathology Mice multidisciplinary Natural killer cells PD-1 protein Receptors, Antigen, B-Cell - genetics Science Science (multidisciplinary) Sequence analysis Single-Cell Gene Expression Analysis T-Lymphocytes - cytology T-Lymphocytes - immunology Tumor Burden Tumors |
| Title | B-cell-specific checkpoint molecules that regulate anti-tumour immunity |
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