The CXCL16-CXCR6 axis in glioblastoma modulates T-cell activity in a spatiotemporal context
IntroductionGlioblastoma multiforme (GBM) pathobiology is characterized by its significant induction of immunosuppression within the tumor microenvironment, predominantly mediated by immunosuppressive tumor-associated myeloid cells (TAMCs). Myeloid cells play a pivotal role in shaping the GBM microe...
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1331287/full |
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| author | Tzu-Yi Chia Tzu-Yi Chia Leah K. Billingham Leah K. Billingham Lauren Boland Lauren Boland Lauren Boland Joshua L. Katz Joshua L. Katz Victor A. Arrieta Victor A. Arrieta Jack Shireman Aurora-Lopez Rosas Aurora-Lopez Rosas Susan L. DeLay Susan L. DeLay Kaylee Zillinger Kaylee Zillinger Yuheng Geng Yuheng Geng Jeandre Kruger Jeandre Kruger Caylee Silvers Caylee Silvers Hanxiang Wang Hanxiang Wang Gustavo Ignacio Vazquez Cervantes Gustavo Ignacio Vazquez Cervantes David Hou David Hou Si Wang Si Wang Hanxiao Wan Hanxiao Wan Adam Sonabend Adam Sonabend Peng Zhang Peng Zhang Catalina Lee-Chang Catalina Lee-Chang Jason Miska Jason Miska |
| author_facet | Tzu-Yi Chia Tzu-Yi Chia Leah K. Billingham Leah K. Billingham Lauren Boland Lauren Boland Lauren Boland Joshua L. Katz Joshua L. Katz Victor A. Arrieta Victor A. Arrieta Jack Shireman Aurora-Lopez Rosas Aurora-Lopez Rosas Susan L. DeLay Susan L. DeLay Kaylee Zillinger Kaylee Zillinger Yuheng Geng Yuheng Geng Jeandre Kruger Jeandre Kruger Caylee Silvers Caylee Silvers Hanxiang Wang Hanxiang Wang Gustavo Ignacio Vazquez Cervantes Gustavo Ignacio Vazquez Cervantes David Hou David Hou Si Wang Si Wang Hanxiao Wan Hanxiao Wan Adam Sonabend Adam Sonabend Peng Zhang Peng Zhang Catalina Lee-Chang Catalina Lee-Chang Jason Miska Jason Miska |
| author_sort | Tzu-Yi Chia |
| collection | DOAJ |
| description | IntroductionGlioblastoma multiforme (GBM) pathobiology is characterized by its significant induction of immunosuppression within the tumor microenvironment, predominantly mediated by immunosuppressive tumor-associated myeloid cells (TAMCs). Myeloid cells play a pivotal role in shaping the GBM microenvironment and influencing immune responses, with direct interactions with effector immune cells critically impacting these processes.MethodsOur study investigates the role of the CXCR6/CXCL16 axis in T-cell myeloid interactions within GBM tissues. We examined the surface expression of CXCL16, revealing its limitation to TAMCs, while microglia release CXCL16 as a cytokine. The study explores how these distinct expression patterns affect T-cell engagement, focusing on the consequences for T-cell function within the tumor environment. Additionally, we assessed the significance of CXCR6 expression in T-cell activation and the initial migration to tumor tissues.ResultsOur data demonstrates that CXCL16 surface expression on TAMCs results in predominant T-cell engagement with these cells, leading to impaired T-cell function within the tumor environment. Conversely, our findings highlight the essential role of CXCR6 expression in facilitating T-cell activation and initial migration to tumor tissues. The CXCL16-CXCR6 axis exhibits dualistic characteristics, facilitating the early stages of the T-cell immune response and promoting T-cell infiltration into tumors. However, once inside the tumor, this axis contributes to immunosuppression.DiscussionThe dual nature of the CXCL16-CXCR6 axis underscores its potential as a therapeutic target in GBM. However, our results emphasize the importance of carefully considering the timing and context of intervention. While targeting this axis holds promise in combating GBM, the complex interplay between TAMCs, microglia, and T cells suggests that intervention strategies need to be tailored to optimize the balance between promoting antitumor immunity and preventing immunosuppression within the dynamic tumor microenvironment. |
| first_indexed | 2024-03-08T13:33:23Z |
| format | Article |
| id | doaj.art-6a594d57504c4cf7a725f6df7d76a523 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-03-08T13:33:23Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-6a594d57504c4cf7a725f6df7d76a5232024-01-17T04:18:20ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-01-011410.3389/fimmu.2023.13312871331287The CXCL16-CXCR6 axis in glioblastoma modulates T-cell activity in a spatiotemporal contextTzu-Yi Chia0Tzu-Yi Chia1Leah K. Billingham2Leah K. Billingham3Lauren Boland4Lauren Boland5Lauren Boland6Joshua L. Katz7Joshua L. Katz8Victor A. Arrieta9Victor A. Arrieta10Jack Shireman11Aurora-Lopez Rosas12Aurora-Lopez Rosas13Susan L. DeLay14Susan L. DeLay15Kaylee Zillinger16Kaylee Zillinger17Yuheng Geng18Yuheng Geng19Jeandre Kruger20Jeandre Kruger21Caylee Silvers22Caylee Silvers23Hanxiang Wang24Hanxiang Wang25Gustavo Ignacio Vazquez Cervantes26Gustavo Ignacio Vazquez Cervantes27David Hou28David Hou29Si Wang30Si Wang31Hanxiao Wan32Hanxiao Wan33Adam Sonabend34Adam Sonabend35Peng Zhang36Peng Zhang37Catalina Lee-Chang38Catalina Lee-Chang39Jason Miska40Jason Miska41Department of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesStanley Manne Children’s Research Institute, Ann & Robert H. Lurie Children’s Hospital, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurosurgery, University of Wisconsin School of Medicine & Public Health, UW Carbone Cancer Center, Madison, WI, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesDepartment of Neurological Surgery, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesMalnati Brain Tumor Institute of the Robert H. Lurie Comprehensive Cancer Center, Feinberg School of Medicine, Northwestern University, Chicago, IL, United StatesIntroductionGlioblastoma multiforme (GBM) pathobiology is characterized by its significant induction of immunosuppression within the tumor microenvironment, predominantly mediated by immunosuppressive tumor-associated myeloid cells (TAMCs). Myeloid cells play a pivotal role in shaping the GBM microenvironment and influencing immune responses, with direct interactions with effector immune cells critically impacting these processes.MethodsOur study investigates the role of the CXCR6/CXCL16 axis in T-cell myeloid interactions within GBM tissues. We examined the surface expression of CXCL16, revealing its limitation to TAMCs, while microglia release CXCL16 as a cytokine. The study explores how these distinct expression patterns affect T-cell engagement, focusing on the consequences for T-cell function within the tumor environment. Additionally, we assessed the significance of CXCR6 expression in T-cell activation and the initial migration to tumor tissues.ResultsOur data demonstrates that CXCL16 surface expression on TAMCs results in predominant T-cell engagement with these cells, leading to impaired T-cell function within the tumor environment. Conversely, our findings highlight the essential role of CXCR6 expression in facilitating T-cell activation and initial migration to tumor tissues. The CXCL16-CXCR6 axis exhibits dualistic characteristics, facilitating the early stages of the T-cell immune response and promoting T-cell infiltration into tumors. However, once inside the tumor, this axis contributes to immunosuppression.DiscussionThe dual nature of the CXCL16-CXCR6 axis underscores its potential as a therapeutic target in GBM. However, our results emphasize the importance of carefully considering the timing and context of intervention. While targeting this axis holds promise in combating GBM, the complex interplay between TAMCs, microglia, and T cells suggests that intervention strategies need to be tailored to optimize the balance between promoting antitumor immunity and preventing immunosuppression within the dynamic tumor microenvironment.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1331287/fullglioblastomaCXCL16CXCR6immunotherapymyeloid cells |
| spellingShingle | Tzu-Yi Chia Tzu-Yi Chia Leah K. Billingham Leah K. Billingham Lauren Boland Lauren Boland Lauren Boland Joshua L. Katz Joshua L. Katz Victor A. Arrieta Victor A. Arrieta Jack Shireman Aurora-Lopez Rosas Aurora-Lopez Rosas Susan L. DeLay Susan L. DeLay Kaylee Zillinger Kaylee Zillinger Yuheng Geng Yuheng Geng Jeandre Kruger Jeandre Kruger Caylee Silvers Caylee Silvers Hanxiang Wang Hanxiang Wang Gustavo Ignacio Vazquez Cervantes Gustavo Ignacio Vazquez Cervantes David Hou David Hou Si Wang Si Wang Hanxiao Wan Hanxiao Wan Adam Sonabend Adam Sonabend Peng Zhang Peng Zhang Catalina Lee-Chang Catalina Lee-Chang Jason Miska Jason Miska The CXCL16-CXCR6 axis in glioblastoma modulates T-cell activity in a spatiotemporal context Frontiers in Immunology glioblastoma CXCL16 CXCR6 immunotherapy myeloid cells |
| title | The CXCL16-CXCR6 axis in glioblastoma modulates T-cell activity in a spatiotemporal context |
| title_full | The CXCL16-CXCR6 axis in glioblastoma modulates T-cell activity in a spatiotemporal context |
| title_fullStr | The CXCL16-CXCR6 axis in glioblastoma modulates T-cell activity in a spatiotemporal context |
| title_full_unstemmed | The CXCL16-CXCR6 axis in glioblastoma modulates T-cell activity in a spatiotemporal context |
| title_short | The CXCL16-CXCR6 axis in glioblastoma modulates T-cell activity in a spatiotemporal context |
| title_sort | cxcl16 cxcr6 axis in glioblastoma modulates t cell activity in a spatiotemporal context |
| topic | glioblastoma CXCL16 CXCR6 immunotherapy myeloid cells |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1331287/full |
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