Glutamatergic synaptic input to glioma cells drives brain tumour progression
A network of communicating tumour cells that is connected by tumour microtubes mediates the progression of incurable gliomas. Moreover, neuronal activity can foster malignant behaviour of glioma cells by non-synaptic paracrine and autocrine mechanisms. Here we report a direct communication channel b...
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| Published in | Nature (London) Vol. 573; no. 7775; pp. 532 - 538 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.09.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | A network of communicating tumour cells that is connected by tumour microtubes mediates the progression of incurable gliomas. Moreover, neuronal activity can foster malignant behaviour of glioma cells by non-synaptic paracrine and autocrine mechanisms. Here we report a direct communication channel between neurons and glioma cells in different disease models and human tumours: functional bona fide chemical synapses between presynaptic neurons and postsynaptic glioma cells. These neurogliomal synapses show a typical synaptic ultrastructure, are located on tumour microtubes, and produce postsynaptic currents that are mediated by glutamate receptors of the AMPA subtype. Neuronal activity including epileptic conditions generates synchronised calcium transients in tumour-microtube-connected glioma networks. Glioma-cell-specific genetic perturbation of AMPA receptors reduces calcium-related invasiveness of tumour-microtube-positive tumour cells and glioma growth. Invasion and growth are also reduced by anaesthesia and the AMPA receptor antagonist perampanel, respectively. These findings reveal a biologically relevant direct synaptic communication between neurons and glioma cells with potential clinical implications.
Neurons form glutamatergic synapses with glioma cells in mice and humans, and inhibition of AMPA receptors reduces glioma cell invasion and growth. |
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| AbstractList | A network of communicating tumour cells that is connected by tumour microtubes mediates the progression of incurable gliomas. Moreover, neuronal activity can foster malignant behaviour of glioma cells by non-synaptic paracrine and autocrine mechanisms. Here we report a direct communication channel between neurons and glioma cells in different disease models and human tumours: functional bona fide chemical synapses between presynaptic neurons and postsynaptic glioma cells. These neurogliomal synapses show a typical synaptic ultrastructure, are located on tumour microtubes, and produce postsynaptic currents that are mediated by glutamate receptors of the AMPA subtype. Neuronal activity including epileptic conditions generates synchronised calcium transients in tumour-microtube-connected glioma networks. Glioma-cell-specific genetic perturbation of AMPA receptors reduces calcium-related invasiveness of tumour-microtube-positive tumour cells and glioma growth. Invasion and growth are also reduced by anaesthesia and the AMPA receptor antagonist perampanel, respectively. These findings reveal a biologically relevant direct synaptic communication between neurons and glioma cells with potential clinical implications. A network of communicating tumour cells that is connected by tumour microtubes mediates the progression of incurable gliomas. Moreover, neuronal activity can foster malignant behaviour of glioma cells by non-synaptic paracrine and autocrine mechanisms. Here we report a direct communication channel between neurons and glioma cells in different disease models and human tumours: functional bona fide chemical synapses between presynaptic neurons and postsynaptic glioma cells. These neurogliomal synapses show a typical synaptic ultrastructure, are located on tumour microtubes, and produce postsynaptic currents that are mediated by glutamate receptors of the AMPA subtype. Neuronal activity including epileptic conditions generates synchronised calcium transients in tumour-microtube-connected glioma networks. Glioma-cell-specific genetic perturbation of AMPA receptors reduces calcium-related invasiveness of tumour-microtube-positive tumour cells and glioma growth. Invasion and growth are also reduced by anaesthesia and the AMPA receptor antagonist perampanel, respectively. These findings reveal a biologically relevant direct synaptic communication between neurons and glioma cells with potential clinical implications. Neurons form glutamatergic synapses with glioma cells in mice and humans, and inhibition of AMPA receptors reduces glioma cell invasion and growth. A network of communicating tumour cells that is connected by tumour microtubes mediates the progression of incurable gliomas. Moreover, neuronal activity can foster malignant behaviour of glioma cells by non-synaptic paracrine and autocrine mechanisms. Here we report a direct communication channel between neurons and glioma cells in different disease models and human tumours: functional bona fide chemical synapses between presynaptic neurons and postsynaptic glioma cells. These neurogliomal synapses show a typical synaptic ultrastructure, are located on tumour microtubes, and produce postsynaptic currents that are mediated by glutamate receptors of the AMPA subtype. Neuronal activity including epileptic conditions generates synchronised calcium transients in tumour-microtube-connected glioma networks. Glioma-cell-specific genetic perturbation of AMPA receptors reduces calcium-related invasiveness of tumour-microtube-positive tumour cells and glioma growth. Invasion and growth are also reduced by anaesthesia and the AMPA receptor antagonist perampanel, respectively. These findings reveal a biologically relevant direct synaptic communication between neurons and glioma cells with potential clinical implications. Neurons form glutamatergic synapses with glioma cells in mice and humans, and inhibition of AMPA receptors reduces glioma cell invasion and growth. |
| Audience | Academic |
| Author | Ratliff, Miriam Tanev, Dimitar Ivanov Studier-Fischer, Alexander Sahm, Felix Fankhauser, Laura Strahle, Christopher Xie, Ruifan Wick, Wolfgang Acikgöz, Azer Aylin Bergles, Dwight E. Venkataramani, Varun Messer, Mirko Horstmann, Heinz Turcan, Sevin Agarwal, Amit Kuner, Thomas Kardorff, Markus Miletic, Hrvoje Knabbe, Johannes Herrmannsdörfer, Frank Hänggi, Daniel Winkler, Frank Kurz, Felix T. Körber, Christoph Kessler, Tobias Chalmers, Anthony Liu, Hai-Kun Mawrin, Christian Paik, Sang Peter |
| Author_xml | – sequence: 1 givenname: Varun surname: Venkataramani fullname: Venkataramani, Varun email: varun.venkataramani@med.uni-heidelberg.de organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University, Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg, Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 2 givenname: Dimitar Ivanov surname: Tanev fullname: Tanev, Dimitar Ivanov organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University, Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg, Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 3 givenname: Christopher surname: Strahle fullname: Strahle, Christopher organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University – sequence: 4 givenname: Alexander surname: Studier-Fischer fullname: Studier-Fischer, Alexander organization: Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg, Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 5 givenname: Laura surname: Fankhauser fullname: Fankhauser, Laura organization: Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg, Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 6 givenname: Tobias surname: Kessler fullname: Kessler, Tobias organization: Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg, Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 7 givenname: Christoph surname: Körber fullname: Körber, Christoph organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University – sequence: 8 givenname: Markus surname: Kardorff fullname: Kardorff, Markus organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University – sequence: 9 givenname: Miriam surname: Ratliff fullname: Ratliff, Miriam organization: Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ), Neurosurgery Clinic, University Hospital Mannheim – sequence: 10 givenname: Ruifan surname: Xie fullname: Xie, Ruifan organization: Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg, Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 11 givenname: Heinz surname: Horstmann fullname: Horstmann, Heinz organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University – sequence: 12 givenname: Mirko surname: Messer fullname: Messer, Mirko organization: Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg, Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 13 givenname: Sang Peter surname: Paik fullname: Paik, Sang Peter organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University – sequence: 14 givenname: Johannes surname: Knabbe fullname: Knabbe, Johannes organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University – sequence: 15 givenname: Felix surname: Sahm fullname: Sahm, Felix organization: Department of Neuropathology, Institute of Pathology, Ruprecht-Karls University Heidelberg, Clinical Cooperation Unit Neuropathology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 16 givenname: Felix T. surname: Kurz fullname: Kurz, Felix T. organization: Department of Neuroradiology, University Hospital Heidelberg – sequence: 17 givenname: Azer Aylin surname: Acikgöz fullname: Acikgöz, Azer Aylin organization: Division of Molecular Neurogenetics, DKFZ-ZMBH Alliance, German Cancer Research Center (DKFZ) – sequence: 18 givenname: Frank surname: Herrmannsdörfer fullname: Herrmannsdörfer, Frank organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University – sequence: 19 givenname: Amit surname: Agarwal fullname: Agarwal, Amit organization: The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, CHS Research Group, Institute for Anatomy and Cell Biology, Heidelberg University – sequence: 20 givenname: Dwight E. surname: Bergles fullname: Bergles, Dwight E. organization: CHS Research Group, Institute for Anatomy and Cell Biology, Heidelberg University – sequence: 21 givenname: Anthony surname: Chalmers fullname: Chalmers, Anthony organization: Institute of Cancer Sciences, University of Glasgow – sequence: 22 givenname: Hrvoje surname: Miletic fullname: Miletic, Hrvoje organization: Department of Biomedicine, University of Bergen, Department of Pathology, Haukeland University Hospital – sequence: 23 givenname: Sevin surname: Turcan fullname: Turcan, Sevin organization: Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg – sequence: 24 givenname: Christian surname: Mawrin fullname: Mawrin, Christian organization: Institute for Neuropathology, Otto-von-Guericke University – sequence: 25 givenname: Daniel surname: Hänggi fullname: Hänggi, Daniel organization: Neurosurgery Clinic, University Hospital Mannheim – sequence: 26 givenname: Hai-Kun surname: Liu fullname: Liu, Hai-Kun organization: Division of Molecular Neurogenetics, DKFZ-ZMBH Alliance, German Cancer Research Center (DKFZ) – sequence: 27 givenname: Wolfgang surname: Wick fullname: Wick, Wolfgang organization: Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg, Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 28 givenname: Frank surname: Winkler fullname: Winkler, Frank email: frank.winkler@med.uni-heidelberg.de organization: Neurology Clinic and National Center for Tumor Diseases, University Hospital Heidelberg, Clinical Cooperation Unit Neurooncology, German Cancer Consortium (DKTK), German Cancer Research Center (DKFZ) – sequence: 29 givenname: Thomas surname: Kuner fullname: Kuner, Thomas email: thomas.kuner@uni-heidelberg.de organization: Department of Functional Neuroanatomy, Institute for Anatomy and Cell Biology, Heidelberg University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31534219$$D View this record in MEDLINE/PubMed |
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| Copyright | The Author(s), under exclusive licence to Springer Nature Limited 2019 COPYRIGHT 2019 Nature Publishing Group Copyright Nature Publishing Group Sep 26, 2019 |
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| Title | Glutamatergic synaptic input to glioma cells drives brain tumour progression |
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