Electrical and synaptic integration of glioma into neural circuits.

Tytuł:: Electrical and synaptic integration of glioma into neural circuits.
Autorzy:: Venkatesh HS; Department of Neurology, Stanford University, Stanford, CA, USA.
Morishita W; Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.; Nancy Pritzker Laboratory, Stanford University, Stanford, CA, USA.
Geraghty AC; Department of Neurology, Stanford University, Stanford, CA, USA.
Silverbush D; Department of Pathology and Center for Cancer Research, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.; Klarman Cell Observatory, Broad Institute of Harvard and MIT, Cambridge, MA, USA.; Broad Institute of Harvard and MIT, Cambridge, MA, USA.
Gillespie SM; Department of Neurology, Stanford University, Stanford, CA, USA.
Arzt M; Department of Neurology, Stanford University, Stanford, CA, USA.
Tam LT; Department of Neurology, Stanford University, Stanford, CA, USA.
Espenel C; Cell Sciences Imaging Facility, Stanford University School of Medicine, Stanford, CA, USA.
Ponnuswami A; Department of Neurology, Stanford University, Stanford, CA, USA.
Ni L; Department of Neurology, Stanford University, Stanford, CA, USA.
Woo PJ; Department of Neurology, Stanford University, Stanford, CA, USA.
Taylor KR; Department of Neurology, Stanford University, Stanford, CA, USA.
Agarwal A; Department of Neuroscience, Johns Hopkins University, Baltimore, MA, USA.; The Chica and Heinz Schaller Research Group, Institute for Anatomy and Cell Biology, Heidelberg University, Heidelberg, Germany.
Regev A; Klarman Cell Observatory, Broad Institute of Harvard and MIT, Cambridge, MA, USA.; Broad Institute of Harvard and MIT, Cambridge, MA, USA.; Howard Hughes Medical Institute, Koch Institute for Integrative Cancer Research, Department of Biology, MIT, Cambridge, MA, USA.
Brang D; Department of Psychology, University of Michigan, Ann Arbor, MI, USA.
Vogel H; Department of Neurology, Stanford University, Stanford, CA, USA.; Department of Pathology, Stanford University, Stanford, CA, USA.; Department of Pediatrics, Stanford University, Stanford, CA, USA.
Hervey-Jumper S; Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, USA.
Bergles DE; Department of Neuroscience, Johns Hopkins University, Baltimore, MA, USA.
Suvà ML; Department of Pathology and Center for Cancer Research, Massachusetts General Hospital and Harvard Medical School, Boston, MA, USA.; Klarman Cell Observatory, Broad Institute of Harvard and MIT, Cambridge, MA, USA.; Broad Institute of Harvard and MIT, Cambridge, MA, USA.
Malenka RC; Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA.; Nancy Pritzker Laboratory, Stanford University, Stanford, CA, USA.
Monje M; Department of Neurology, Stanford University, Stanford, CA, USA. .; Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA. .; Department of Pathology, Stanford University, Stanford, CA, USA. .; Department of Pediatrics, Stanford University, Stanford, CA, USA. .; Institute for Stem Cell Biology and Regenerative Medicine, Stanford University, Stanford, CA, USA. .
Źródło:: Nature [Nature] 2019 Sep; Vol. 573 (7775), pp. 539-545. Date of Electronic Publication: 2019 Sep 18.
Typ publikacji:: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't; Research Support, U.S. Gov't, Non-P.H.S.
Język:: English
Imprint Name(s):: Publication: Basingstoke : Nature Publishing Group
Original Publication: London, Macmillan Journals ltd.
MeSH Terms:: Electrophysiological Phenomena*
Brain/*physiopathology
Electrical Synapses/*pathology
Glioma/*physiopathology
Animals ; Brain/cytology ; Cell Membrane/pathology ; Cell Proliferation ; Gap Junctions/pathology ; Gene Expression Profiling ; Gene Expression Regulation, Neoplastic ; Heterografts ; Humans ; Mice ; Mice, Inbred NOD ; Neurons/pathology ; Optogenetics ; Potassium/metabolism ; Synaptic Transmission ; Tumor Cells, Cultured
References:: Venkatesh, H. S. et al. Neuronal activity promotes glioma growth through neuroligin-3 secretion. Cell 161, 803–816 (2015). (PMID: 25913192444712210.1016/j.cell.2015.04.012)
Venkatesh, H. S. et al. Targeting neuronal activity-regulated neuroligin-3 dependency in high-grade glioma. Nature 549, 533–537 (2017). (PMID: 28959975589183210.1038/nature24014)
Bergles, D. E., Roberts, J. D., Somogyi, P. & Jahr, C. E. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405, 187–191 (2000). (PMID: 10.1038/3501208310821275)
Káradóttir, R., Cavelier, P., Bergersen, L. H. & Attwell, D. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438, 1162–1166 (2005). (PMID: 16372011141628310.1038/nature04302)
LoTurco, J. J., Owens, D. F., Heath, M. J., Davis, M. B. & Kriegstein, A. R. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287–1298 (1995). (PMID: 10.1016/0896-6273(95)90008-X8845153)
Luk, K. C. & Sadikot, A. F. Glutamate and regulation of proliferation in the developing mammalian telencephalon. Dev. Neurosci. 26, 218–228 (2004). (PMID: 10.1159/00008213915711062)
Liu, X., Wang, Q., Haydar, T. F. & Bordey, A. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat. Neurosci. 8, 1179–1187 (2005). (PMID: 16116450138026310.1038/nn1522)
Deisseroth, K. et al. Excitation–neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42, 535–552 (2004). (PMID: 10.1016/S0896-6273(04)00266-115157417)
Kougioumtzidou, E. et al. Signalling through AMPA receptors on oligodendrocyte precursors promotes myelination by enhancing oligodendrocyte survival. eLife 6, e28080 (2017). (PMID: 28608780548461410.7554/eLife.28080)
Filbin, M. G. et al. Developmental and oncogenic programs in H3K27M gliomas dissected by single-cell RNA-seq. Science 360, 331–335 (2018). (PMID: 29674595594986910.1126/science.aao4750)
Venteicher, A. S. et al. Decoupling genetics, lineages, and microenvironment in IDH-mutant gliomas by single-cell RNA-seq. Science 355, eaai8478 (2017). (PMID: 28360267551909610.1126/science.aai8478)
Sommer, B., Köhler, M., Sprengel, R. & Seeburg, P. H. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11–19 (1991). (PMID: 10.1016/0092-8674(91)90568-J1717158)
Hollmann, M., Hartley, M. & Heinemann, S. Ca -permeable AMPA receptors regulate growth of human glioblastoma via Akt activation. J. Neurosci. 27, 7987–8001 (2007). (PMID: 17652589667271810.1523/JNEUROSCI.2180-07.2007)
Sontheimer, H. A role for glutamate in growth and invasion of primary brain tumors. J. Neurochem. 105, 287–295 (2008). (PMID: 18284616255706510.1111/j.1471-4159.2008.05301.x)
Lyons, S. A., Chung, W. J., Weaver, A. K., Ogunrinu, T. & Sontheimer, H. Autocrine glutamate signaling promotes glioma cell invasion. Cancer Res. 67, 9463–9471 (2007). (PMID: 17909056204507310.1158/0008-5472.CAN-07-2034)
Chen, Q. et al. Carcinoma-astrocyte gap junctions promote brain metastasis by cGAMP transfer. Nature 533, 493–498 (2016). (PMID: 27225120502119510.1038/nature18268)
Campbell, S. L., Buckingham, S. C. & Sontheimer, H. Human glioma cells induce hyperexcitability in cortical networks. Epilepsia 53, 1360–1370 (2012). (PMID: 22709330341846810.1111/j.1528-1167.2012.03557.x)
John Lin, C. C. et al. Identification of diverse astrocyte populations and their malignant analogs. Nat. Neurosci. 20, 396–405 (2017). (PMID: 10.1038/nn.449328166219)
Buckingham, S. C. et al. Glutamate release by primary brain tumors induces epileptic activity. Nat. Med. 17, 1269–1274 (2011). (PMID: 21909104319223110.1038/nm.2453)
Campbell, S. L. et al. GABAergic disinhibition and impaired KCC2 cotransporter activity underlie tumor-associated epilepsy. Glia 63, 23–36 (2015). (PMID: 10.1002/glia.2273025066727)
Ray, S., Crone, N. E., Niebur, E., Franaszczuk, P. J. & Hsiao, S. S. Neural correlates of high-gamma oscillations (60-200 Hz) in macaque local field potentials and their potential implications in electrocorticography. J. Neurosci. 28, 11526–11536 (2008). (PMID: 18987189271584010.1523/JNEUROSCI.2848-08.2008)
Yizhar, O. et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171–178 (2011). (PMID: 21796121415550110.1038/nature10360)
Hodgkin, A. L. & Katz, B. The effect of sodium ions on the electrical activity of giant axon of the squid. J. Physiol. 108, 37–77 (1949). (PMID: 10.1113/jphysiol.1949.sp004310)
Ransom, B. R. & Goldring, S. Ionic determinants of membrane potential of cells presumed to be glia in cerebral cortex of cat. J. Neurophysiol. 36, 855–868 (1973). (PMID: 10.1152/jn.1973.36.5.8554805015)
Bittman, K. S. & LoTurco, J. J. Differential regulation of connexin 26 and 43 in murine neocortical precursors. Cereb. Cortex 9, 188–195 (1999). (PMID: 10.1093/cercor/9.2.18810220231)
LoTurco, J. J., Blanton, M. G. & Kriegstein, A. R. Initial expression and endogenous activation of NMDA channels in early neocortical development. J. Neurosci. 11, 792–799 (1991). (PMID: 1825846657535110.1523/JNEUROSCI.11-03-00792.1991)
Marins, M. et al. Gap junctions are involved in cell migration in the early postnatal subventricular zone. Dev. Neurobiol. 69, 715–730 (2009). (PMID: 10.1002/dneu.2073719565626)
Ohtaka-Maruyama, C. et al. Synaptic transmission from subplate neurons controls radial migration of neocortical neurons. Science 360, 313–317 (2018). (PMID: 10.1126/science.aar286629674592)
Kuffler, S. W. Neuroglial cells: physiological properties and a potassium mediated effect of neuronal activity on the glial membrane potential. Proc. R. Soc. Lond. B 168, 1–21 (1967). (PMID: 10.1098/rspb.1967.00474382871)
Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M. & Deisseroth, K. Optogenetics in neural systems. Neuron 71, 9–34 (2011). (PMID: 10.1016/j.neuron.2011.06.00421745635)
Picelli, S. et al. Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9, 171–181 (2014). (PMID: 10.1038/nprot.2014.00624385147)
Tirosh, I. et al. Single-cell RNA-seq supports a developmental hierarchy in human oligodendroglioma. Nature 539, 309–313 (2016). (PMID: 27806376546581910.1038/nature20123)
Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018). (PMID: 29608179670074410.1038/nbt.4096)
Lin, G. L. et al. Non-inflammatory tumor microenvironment of diffuse intrinsic pontine glioma. Acta Neuropathol. Commun. 6, 51 (2018). (PMID: 29954445602271410.1186/s40478-018-0553-x)
Qin, E. Y. et al. Neural precursor-derived pleiotrophin mediates subventricular zone invasion by glioma. Cell 170, 845–859.e819 (2017). (PMID: 28823557558715910.1016/j.cell.2017.07.016)
Rueden, C. T. et al. ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics 18, 529 (2017). (PMID: 29187165570808010.1186/s12859-017-1934-z)
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012). (PMID: 2274377210.1038/nmeth.2019)
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012). (PMID: 22930834555454210.1038/nmeth.2089)
Pietzsch, T., Preibisch, S., Tomancák, P. & Saalfeld, S. ImgLib2—generic image processing in Java. Bioinformatics 28, 3009–3011 (2012). (PMID: 22962343349633910.1093/bioinformatics/bts543)
Wu, D. et al. Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP. Nature 544, 316–321 (2017). (PMID: 28355182573494210.1038/nature21720)
Guizar-Sicairos, M., Thurman, S. T. & Fienup, J. R. Efficient subpixel image registration algorithms. Opt. Lett. 33, 156–158 (2008). (PMID: 10.1364/OL.33.00015618197224)
Achanta, R. et al. SLIC superpixels compared to state-of-the-art superpixel methods. IEEE Trans. Pattern Anal. Mach. Intell. 34, 2274–2282 (2012). (PMID: 10.1109/TPAMI.2012.12022641706)
Pnevmatikakis, E. A. et al. Simultaneous denoising, deconvolution, and demixing of calcium imaging data. Neuron 89, 285–299 (2016). (PMID: 26774160488138710.1016/j.neuron.2015.11.037)
van der Walt, S. et al. scikit-image: image processing in Python. PeerJ 2, e453 (2014). (PMID: 25024921408127310.7717/peerj.453)
Kawahara, Y., Ito, K., Sun, H., Kanazawa, I. & Kwak, S. Low editing efficiency of GluR2 mRNA is associated with a low relative abundance of ADAR2 mRNA in white matter of normal human brain. Eur. J. Neurosci. 18, 23–33 (2003). (PMID: 10.1046/j.1460-9568.2003.02718.x12859334)
Sobolevsky, A. I., Rosconi, M. P. & Gouaux, E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462, 745–756 (2009). (PMID: 19946266286165510.1038/nature08624)
Vinci, M., Box, C. & Eccles, S. A. Three-dimensional (3D) tumor spheroid invasion assay. J. Vis. Exp. 99, 52686 (2015).
Vinci, M., Box, C., Zimmermann, M. & Eccles, S. A. Tumor spheroid-based migration assays for evaluation of therapeutic agents. Methods Mol. Biol. 986, 253–266 (2013). (PMID: 10.1007/978-1-62703-311-4_1623436417)
Grant Information:: T32 CA009302 United States CA NCI NIH HHS; P30 NS069375 United States NS NINDS NIH HHS; DP1 NS111132 United States NS NINDS NIH HHS; R01 NS092597 United States NS NINDS NIH HHS; United States HHMI Howard Hughes Medical Institute; P50 MH086403 United States MH NIMH NIH HHS; F31 CA200273 United States CA NCI NIH HHS; K08 NS110919 United States NS NINDS NIH HHS
Substance Nomenclature:: RWP5GA015D (Potassium)
Entry Date(s):: Date Created: 20190920 Date Completed: 20200327 Latest Revision: 20220418
Update Code:: 20240105
PubMed Central ID:: PMC7038898
DOI:: 10.1038/s41586-019-1563-y
PMID:: 31534222
: Czasopismo naukowe

Full Text Finder

High-grade gliomas are lethal brain cancers whose progression is robustly regulated by neuronal activity. Activity-regulated release of growth factors promotes glioma growth, but this alone is insufficient to explain the effect that neuronal activity exerts on glioma progression. Here we show that neuron and glioma interactions include electrochemical communication through bona fide AMPA receptor-dependent neuron-glioma synapses. Neuronal activity also evokes non-synaptic activity-dependent potassium currents that are amplified by gap junction-mediated tumour interconnections, forming an electrically coupled network. Depolarization of glioma membranes assessed by in vivo optogenetics promotes proliferation, whereas pharmacologically or genetically blocking electrochemical signalling inhibits the growth of glioma xenografts and extends mouse survival. Emphasizing the positive feedback mechanisms by which gliomas increase neuronal excitability and thus activity-regulated glioma growth, human intraoperative electrocorticography demonstrates increased cortical excitability in the glioma-infiltrated brain. Together, these findings indicate that synaptic and electrical integration into neural circuits promotes glioma progression.

Comment in: Nature. 2019 Sep;573(7775):499-501. (PMID: 31551543)
Comment in: Nat Rev Neurosci. 2019 Dec;20(12):716-717. (PMID: 31575987)
Comment in: Nat Rev Cancer. 2019 Dec;19(12):663. (PMID: 31595057)
Comment in: Trends Cancer. 2020 Jan;6(1):1-3. (PMID: 31952775)

Informacja