Glioblastoma-Associated Microglia Reprogramming Is Mediated by Functional Transfer of Extracellular miR-21
Gliomas are primary, diffusely infiltrating brain tumors. Microglia are innate immune cells in the CNS and make up a substantial portion of the tumor mass. Glioma cells shape their microenvironment, communicating with and reprogramming surrounding cells, resulting in enhanced angiogenesis, immune su...
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| Published in | Cell reports (Cambridge) Vol. 28; no. 12; pp. 3105 - 3119.e7 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
17.09.2019
Elsevier |
| Online Access | Get full text |
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| Abstract | Gliomas are primary, diffusely infiltrating brain tumors. Microglia are innate immune cells in the CNS and make up a substantial portion of the tumor mass. Glioma cells shape their microenvironment, communicating with and reprogramming surrounding cells, resulting in enhanced angiogenesis, immune suppression, and remodeling of the extracellular matrix. Glioma cells communicate with microglia, in part by releasing extracellular vesicles (EVs). Mouse glioma cells stably expressing a palmitoylated GFP to label EVs were implanted intracranially into syngeneic miR-21-null mice. Here, we demonstrate functional delivery of miR-21, regulating specific downstream mRNA targets in microglia after uptake of tumor-derived EVs. These findings attest to EV-dependent microRNA delivery as studied in an in vivo-based model and provide insight into the reprograming of microglial cells by tumor cells to create a favorable microenvironment for cancer progression.
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•Extracellular vesicles (EVs) shed by glioma cells are taken up by microglia in vivo•miR-21 is functionally transferred from glioma to microglia through EVs in vivo•miR-21 mRNA targets in microglia are downregulated upon EV uptake•Microglia proliferation is increased after miR-21 target Btg2 downregulation
Abels et al. show miR-21 transfer from glioma to microglia by palmitoylated GFP-labeled extracellular vesicles in vivo. This transfer results in miR-21 target-specific mRNA downregulation. Following downregulation of Btg2, proliferation in microglia is increased, suggesting reprogramming of microglia in the tumor microenvironment through extracellular vesicles shed by glioma cells. |
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| AbstractList | Gliomas are primary, diffusely infiltrating brain tumors. Microglia are innate immune cells in the CNS and make up a substantial portion of the tumor mass. Glioma cells shape their microenvironment, communicating with and reprogramming surrounding cells, resulting in enhanced angiogenesis, immune suppression, and remodeling of the extracellular matrix. Glioma cells communicate with microglia, in part by releasing extracellular vesicles (EVs). Mouse glioma cells stably expressing a palmitoylated GFP to label EVs were implanted intracranially into syngeneic miR-21-null mice. Here, we demonstrate functional delivery of miR-21, regulating specific downstream mRNA targets in microglia after uptake of tumor-derived EVs. These findings attest to EV-dependent microRNA delivery as studied in an in vivo-based model and provide insight into the reprograming of microglial cells by tumor cells to create a favorable microenvironment for cancer progression.
[Display omitted]
•Extracellular vesicles (EVs) shed by glioma cells are taken up by microglia in vivo•miR-21 is functionally transferred from glioma to microglia through EVs in vivo•miR-21 mRNA targets in microglia are downregulated upon EV uptake•Microglia proliferation is increased after miR-21 target Btg2 downregulation
Abels et al. show miR-21 transfer from glioma to microglia by palmitoylated GFP-labeled extracellular vesicles in vivo. This transfer results in miR-21 target-specific mRNA downregulation. Following downregulation of Btg2, proliferation in microglia is increased, suggesting reprogramming of microglia in the tumor microenvironment through extracellular vesicles shed by glioma cells. Gliomas are primary, diffusely infiltrating brain tumors. Microglia are innate immune cells in the CNS and make up a substantial portion of the tumor mass. Glioma cells shape their microenvironment, communicating with and reprogramming surrounding cells, resulting in enhanced angiogenesis, immune suppression, and remodeling of the extracellular matrix. Glioma cells communicate with microglia, in part by releasing extracellular vesicles (EVs). Mouse glioma cells stably expressing a palmitoylated GFP to label EVs were implanted intracranially into syngeneic miR-21-null mice. Here, we demonstrate functional delivery of miR-21, regulating specific downstream mRNA targets in microglia after uptake of tumor-derived EVs. These findings attest to EV-dependent microRNA delivery as studied in an in vivo -based model and provide insight into the reprograming of microglial cells by tumor cells to create a favorable microenvironment for cancer progression. Abels et al. show miR-21 transfer from glioma to microglia by palmitoylated GFP-labeled extracellular vesicles in vivo . This transfer results in miR-21 target-specific mRNA downregulation. Following downregulation of Btg2 , proliferation in microglia is increased, suggesting reprogramming of microglia in the tumor microenvironment through extracellular vesicles shed by glioma cells. Gliomas are primary, diffusely infiltrating brain tumors. Microglia are innate immune cells in the CNS and make up a substantial portion of the tumor mass. Glioma cells shape their microenvironment, communicating with and reprogramming surrounding cells, resulting in enhanced angiogenesis, immune suppression, and remodeling of the extracellular matrix. Glioma cells communicate with microglia, in part by releasing extracellular vesicles (EVs). Mouse glioma cells stably expressing a palmitoylated GFP to label EVs were implanted intracranially into syngeneic miR-21-null mice. Here, we demonstrate functional delivery of miR-21, regulating specific downstream mRNA targets in microglia after uptake of tumor-derived EVs. These findings attest to EV-dependent microRNA delivery as studied in an in vivo-based model and provide insight into the reprograming of microglial cells by tumor cells to create a favorable microenvironment for cancer progression. : Abels et al. show miR-21 transfer from glioma to microglia by palmitoylated GFP-labeled extracellular vesicles in vivo. This transfer results in miR-21 target-specific mRNA downregulation. Following downregulation of Btg2, proliferation in microglia is increased, suggesting reprogramming of microglia in the tumor microenvironment through extracellular vesicles shed by glioma cells. Gliomas are primary, diffusely infiltrating brain tumors. Microglia are innate immune cells in the CNS and make up a substantial portion of the tumor mass. Glioma cells shape their microenvironment, communicating with and reprogramming surrounding cells, resulting in enhanced angiogenesis, immune suppression, and remodeling of the extracellular matrix. Glioma cells communicate with microglia, in part by releasing extracellular vesicles (EVs). Mouse glioma cells stably expressing a palmitoylated GFP to label EVs were implanted intracranially into syngeneic miR-21-null mice. Here, we demonstrate functional delivery of miR-21, regulating specific downstream mRNA targets in microglia after uptake of tumor-derived EVs. These findings attest to EV-dependent microRNA delivery as studied in an in vivo-based model and provide insight into the reprograming of microglial cells by tumor cells to create a favorable microenvironment for cancer progression.Gliomas are primary, diffusely infiltrating brain tumors. Microglia are innate immune cells in the CNS and make up a substantial portion of the tumor mass. Glioma cells shape their microenvironment, communicating with and reprogramming surrounding cells, resulting in enhanced angiogenesis, immune suppression, and remodeling of the extracellular matrix. Glioma cells communicate with microglia, in part by releasing extracellular vesicles (EVs). Mouse glioma cells stably expressing a palmitoylated GFP to label EVs were implanted intracranially into syngeneic miR-21-null mice. Here, we demonstrate functional delivery of miR-21, regulating specific downstream mRNA targets in microglia after uptake of tumor-derived EVs. These findings attest to EV-dependent microRNA delivery as studied in an in vivo-based model and provide insight into the reprograming of microglial cells by tumor cells to create a favorable microenvironment for cancer progression. Gliomas are primary, diffusely infiltrating brain tumors. Microglia are innate immune cells in the CNS and make up a substantial portion of the tumor mass. Glioma cells shape their microenvironment, communicating with and reprogramming surrounding cells, resulting in enhanced angiogenesis, immune suppression, and remodeling of the extracellular matrix. Glioma cells communicate with microglia, in part by releasing extracellular vesicles (EVs). Mouse glioma cells stably expressing a palmitoylated GFP to label EVs were implanted intracranially into syngeneic miR-21-null mice. Here, we demonstrate functional delivery of miR-21, regulating specific downstream mRNA targets in microglia after uptake of tumor-derived EVs. These findings attest to EV-dependent microRNA delivery as studied in an in vivo-based model and provide insight into the reprograming of microglial cells by tumor cells to create a favorable microenvironment for cancer progression. |
| Author | Krichevsky, Anna M. Kolsteeg, Christy-Joy Dusoswa, Sophie A. El Khoury, Joseph Maas, Sybren L.N. Breakefield, Xandra O. Nieland, Lisa Abels, Erik R. Ting, David T. Hickman, Suzanne Wei, Zhiyun Tai, Eric Cheah, Pike See Broekman, Marike L.D. |
| AuthorAffiliation | 9 Department of Neurosurgery, Haaglanden Medical Center, 2512 VA The Hague, the Netherlands 11 Lead Contact 2 Department of Neurosurgery, UMC Utrecht Brain Center, University Medical Center, Utrecht University, 3584 CX Utrecht, the Netherlands 3 Department of Neurology, Ann Romney Center for Neurologic Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA 7 Center for Immunology & Inflammatory Diseases, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02129, USA 1 Departments of Neurology and Radiology, Massachusetts General Hospital, and NeuroDiscovery Center, Harvard Medical School, Boston, MA 02129, USA 6 Department of Molecular Cell Biology and Immunology, Amsterdam Infection & Immunology Institute and Cancer Center Amsterdam, Amsterdam UMC, 1081 HZ Amsterdam, the Netherlands 8 Department of Neurosurgery, Leiden University Medical Center, 2300 RC Leiden, the Netherlands 4 Department of Human Anatomy, Faculty of Medicine and Health Scienc |
| AuthorAffiliation_xml | – name: 1 Departments of Neurology and Radiology, Massachusetts General Hospital, and NeuroDiscovery Center, Harvard Medical School, Boston, MA 02129, USA – name: 7 Center for Immunology & Inflammatory Diseases, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02129, USA – name: 9 Department of Neurosurgery, Haaglanden Medical Center, 2512 VA The Hague, the Netherlands – name: 2 Department of Neurosurgery, UMC Utrecht Brain Center, University Medical Center, Utrecht University, 3584 CX Utrecht, the Netherlands – name: 10 Senior author – name: 6 Department of Molecular Cell Biology and Immunology, Amsterdam Infection & Immunology Institute and Cancer Center Amsterdam, Amsterdam UMC, 1081 HZ Amsterdam, the Netherlands – name: 8 Department of Neurosurgery, Leiden University Medical Center, 2300 RC Leiden, the Netherlands – name: 3 Department of Neurology, Ann Romney Center for Neurologic Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA – name: 4 Department of Human Anatomy, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, Serdang, Selangor 43400, Malaysia – name: 5 Cancer Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA – name: 11 Lead Contact |
| Author_xml | – sequence: 1 givenname: Erik R. surname: Abels fullname: Abels, Erik R. email: eabels@mgh.harvard.edu organization: Departments of Neurology and Radiology, Massachusetts General Hospital, and NeuroDiscovery Center, Harvard Medical School, Boston, MA 02129, USA – sequence: 2 givenname: Sybren L.N. surname: Maas fullname: Maas, Sybren L.N. organization: Department of Neurosurgery, UMC Utrecht Brain Center, University Medical Center, Utrecht University, 3584 CX Utrecht, the Netherlands – sequence: 3 givenname: Lisa surname: Nieland fullname: Nieland, Lisa organization: Departments of Neurology and Radiology, Massachusetts General Hospital, and NeuroDiscovery Center, Harvard Medical School, Boston, MA 02129, USA – sequence: 4 givenname: Zhiyun surname: Wei fullname: Wei, Zhiyun organization: Department of Neurology, Ann Romney Center for Neurologic Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA – sequence: 5 givenname: Pike See surname: Cheah fullname: Cheah, Pike See organization: Departments of Neurology and Radiology, Massachusetts General Hospital, and NeuroDiscovery Center, Harvard Medical School, Boston, MA 02129, USA – sequence: 6 givenname: Eric surname: Tai fullname: Tai, Eric organization: Cancer Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA – sequence: 7 givenname: Christy-Joy surname: Kolsteeg fullname: Kolsteeg, Christy-Joy organization: Departments of Neurology and Radiology, Massachusetts General Hospital, and NeuroDiscovery Center, Harvard Medical School, Boston, MA 02129, USA – sequence: 8 givenname: Sophie A. surname: Dusoswa fullname: Dusoswa, Sophie A. organization: Department of Molecular Cell Biology and Immunology, Amsterdam Infection & Immunology Institute and Cancer Center Amsterdam, Amsterdam UMC, 1081 HZ Amsterdam, the Netherlands – sequence: 9 givenname: David T. surname: Ting fullname: Ting, David T. organization: Cancer Center, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA – sequence: 10 givenname: Suzanne surname: Hickman fullname: Hickman, Suzanne organization: Center for Immunology & Inflammatory Diseases, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02129, USA – sequence: 11 givenname: Joseph surname: El Khoury fullname: El Khoury, Joseph organization: Center for Immunology & Inflammatory Diseases, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02129, USA – sequence: 12 givenname: Anna M. surname: Krichevsky fullname: Krichevsky, Anna M. organization: Department of Neurology, Ann Romney Center for Neurologic Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA – sequence: 13 givenname: Marike L.D. surname: Broekman fullname: Broekman, Marike L.D. organization: Department of Neurosurgery, Leiden University Medical Center, 2300 RC Leiden, the Netherlands – sequence: 14 givenname: Xandra O. surname: Breakefield fullname: Breakefield, Xandra O. email: breakefield@hms.harvard.edu organization: Departments of Neurology and Radiology, Massachusetts General Hospital, and NeuroDiscovery Center, Harvard Medical School, Boston, MA 02129, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31533034$$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 23 AUTHOR CONTRIBUTIONS E.R.A., S.L.N.M., X.O.B., M.L.D.B., and A.M.K. conceived the study. E.R.A., S.L.N.M., and X.O.B. designed the experiments. E.R.A., Z.W., L.N., P.S.C., and C.-J.K. performed and analyzed experiments. S.A.D. assisted during animal experiments. D.T.T. and E.T. assisted and performed RNA sequencing (RNA-seq) experiments. S.L.N.M. and E.T. performed the computational and statistical analysis of RNA-seq data. S.H. and J.E.K. provided advice on microglial isolation. X.O.B., M.L.D.B., and A.M.K. supervised the project. E.R.A. prepared figures. E.R.A. wrote the manuscript. All authors edited or commented on the manuscript. |
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| Title | Glioblastoma-Associated Microglia Reprogramming Is Mediated by Functional Transfer of Extracellular miR-21 |
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