Purinergic receptors on microglial cells: functional expression in acute brain slices and modulation of microglial activation in vitro
Abstract
Microglial cells are the pathologic sensors in the brain. ATP released from damaged cells is a candidate for signalling neural injury to microglia. Moreover, ATP is an extracellular messenger for propagating astrocyte activity in the form of Ca2+ waves. To test for the functional expression of purinoreceptors in microglial cells we employed the patch-clamp technique in acute slices of adult mouse brain. ATP triggered a nonselective cationic and a K+ current. Pharmacological screening with purinergic ligands indicated the presence of P2Y1 and P2Y2/4 receptors linked to the activation of a K+ current and P2X receptors, including P2X7, linked to the activation of a nonselective cationic current. These findings suggest that microglial cells in situ express different purinergic receptors with distinct sensitivity and functional coupling. To test for the involvement of purinoreceptors in microglial activation, we stimulated cultured microglial cells with lipopolysaccharide and measured the release of tumour necrosis factor alpha, interleukin-6, interleukin-12 and macrophage inflammatory protein 1alpha, induction of K+ outward currents and nitric oxide release. All these parameters were reduced in the presence of purinergic ligands, indicating that purinergic receptor activation attenuated indicators of microglial activation.
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Microglia filled with biocytin during recording exhibited ramified morphology comparable to that reported previously.
“microglia filled with biocytin during recording exhibited ramified morphology comparable to that reported previously (Boucsein et al., 2000; Boucsein et al., 2003)”
From Local cues establish and maintain region-specific phenotypes of basal ganglia microglia (2017) · cites this paper as Boucsein et al., 2003
VTA and SNc microglia have resting potentials similar to those reported for cortical microglia.
“VTA and SNc microglia exhibited resting potentials similar to those reported for cortical microglia (Boucsein et al., 2000; Boucsein et al., 2003)”
From Local cues establish and maintain region-specific phenotypes of basal ganglia microglia (2017) · cites this paper as Boucsein et al., 2003
Cites
Hamill, O. P., Marty, A., Neher, E., Sakmann, B., & Sigworth, F. J. (1981) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00656997 · Cited by 18,436 · see citing works
Microglia: a sensor for pathological events in the CNS
Kreutzberg, G. W. (1996) · Trends in Neurosciences · doi:10.1016/0166-2236(96)10049-7 · Cited by 4,396 · see citing works
Receptors for Purines and Pyrimidines
Burnstock, G., & Verkhratsky, A. (2012) · Springer eBooks · doi:10.1007/978-3-642-28863-0_5 · Cited by 3,973 · see citing works
Activated microglia mediate neuronal cell injury via a nitric oxide mechanism
Chao, C. C., Hu, S., Molitor, T. W., Shaskan, E. G., & Peterson, P. K. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.149.8.2736 · Cited by 1,137 · see citing works
Functional plasticity of microglia: A review
Streit, W. J., Graeber, M. B., & Kreutzberg, G. W. (1988) · Glia · doi:10.1002/glia.440010502 · Cited by 937 · see citing works
ATP Released from Astrocytes Mediates Glial Calcium Waves
Guthrie, P. B., Knappenberger, J., Segal, M., Bennett, M. V. L., Charles, A. C., & Kater, S. B. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-02-00520.1999 · Cited by 806 · see citing works
Charles, A. C., Merrill, J. E., Dirksen, E. R., & Sandersont, M. J. (1991) · Neuron · doi:10.1016/0896-6273(91)90238-u · Cited by 736 · see citing works
Ferrari, D., Chiozzi, P., Falzoni, S., Hanau, S., & Virgilio, F. D. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.185.3.579 · Cited by 474 · see citing works
Calcium Waves in Retinal Glial Cells
Newman, E. A., & Zahs, K. R. (1997) · Science · doi:10.1126/science.275.5301.844 · Cited by 457 · see citing works
Extracellular ATP Triggers Tumor Necrosis Factor‐α Release from Rat Microglia
Hide, I., Tanaka, M., Inoue, A., Nakajima, K., Kohsaka, S., Inoue, K., & Nakata, Y. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0750965.x · Cited by 447 · see citing works
Signalling via ATP in the nervous system
Zimmermann, H. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90016-7 · Cited by 439 · see citing works
BIOCHEMISTRY, LOCALIZATION AND FUNCTIONAL ROLES OF ECTO-NUCLEOTIDASES IN THE NERVOUS SYSTEM
Zimmermann, H. (1996) · Progress in Neurobiology · doi:10.1016/0301-0082(96)00026-3 · Cited by 426 · see citing works
Trophic effects of purines in neurons and glial cells
Rathbone, M. P., Middlemiss, P. J., Gysbers, J. W., Andrew, C. M., Herman, M. A. R., Reed, J. K., Ciccarelli, R., Iorio, P. D., & Caciagli, F. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(99)00017-9 · Cited by 398 · see citing works
Kinetics and Mechanism of ATP-Dependent IL-1β Release from Microglial Cells
Sanz, J. M., & Virgilio, F. D. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.9.4893 · Cited by 274 · see citing works
ATP-mediated cytotoxicity in microglial cells
Ferrari, D., Chiozzi, P., Falzoni, S., Susino, M. D., Collo, G., Buell, G. N., & Virgilio, F. D. (1997) · Neuropharmacology · doi:10.1016/s0028-3908(97)00137-8 · Cited by 274 · see citing works
Astrocyte Ca 2+ waves trigger responses in microglial cells in brain slices
Schipke, C. G., Boucsein, C., Ohlemeyer, C., Kirchhoff, F., & Kettenmann, H. (2001) · The FASEB Journal · doi:10.1096/fj.01-0514fje · Cited by 252 · see citing works
Self-citationATP Mediates Calcium Signaling Between Astrocytes and Microglial Cells: Modulation by IFN-γ
Verderio, C., & Matteoli, M. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.10.6383 · Cited by 242 · see citing works
Direct Observation of Calcium-Independent Intercellular ATP Signaling in Astrocytes
Wang, Z., Haydon, P. G., & Yeung, E. S. (2000) · Analytical Chemistry · doi:10.1021/ac9912146 · Cited by 219 · see citing works
Cunha, R. A., Sebastião, A. M., & Ribeiro, J. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-06-01987.1998 · Cited by 217 · see citing works
Production of nitrite by neonatal rat microglial cells/ brain macrophages
Zielasek, J., Tausch, M., Toyka, K. V., & Hartung, H. (1992) · Cellular Immunology · doi:10.1016/0008-8749(92)90131-8 · Cited by 195 · see citing works
Walz, W., Ilschner, S., Ohlemeyer, C., Banati, R. B., & Kettenmann, H. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-10-04403.1993 · Cited by 175 · see citing works
Self-citationShigemoto‐Mogami, Y., Koizumi, S., Tsuda, M., Ohsawa, K., Kohsaka, S., & Inoue, K. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00514.x · Cited by 173 · see citing works
Electrophysiological properties of microglial cells in normal and pathologic rat brain slices
Boucsein, C., Kettenmann, H., & Nolte, C. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00100.x · Cited by 166 · see citing works
Self-citationA Kv1.5 to Kv1.3 Switch in Endogenous Hippocampal Microglia and a Role in Proliferation
Kotecha, S. A., & Schlichter, L. C. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-10680.1999 · Cited by 155 · see citing works
Molecular cloning and functional expression of a novel rat heart P2X purinoceptor
García‐Guzmán, M., Soto, F., Laube, B., & Stühmer, W. (1996) · FEBS Letters · doi:10.1016/0014-5793(96)00499-1 · Cited by 125 · see citing works
Microglia, an in vivo source of reactive oxygen species in the brain.
Colton, C. A., & Gilbert, D. L. (1993) · PubMed · Cited by 113 · see citing works
ATP stimulation of Ca2+‐dependent plasminogen release from cultured microglia
Inoue, K., Nakajima, K., Morimoto, T., Kikuchi, Y., Koizumi, S., Illés, P., & Kohsaka, S. (1998) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0701732 · Cited by 112 · see citing works
Prinz, M., Kann, O., Draheim, H. J., Schumann, R. R., Kettenmann, H., Weber, J. R., & Hanisch, U. (1999) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199910000-00006 · Cited by 111 · see citing works
Self-citationHanisch, U., Lyons, S. A., Prinz, M., Nolte, C., Weber, J. R., Kettenmann, H., & Kirchhoff, F. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.46.28853 · Cited by 109 · see citing works
Self-citationInflammatory stimuli induce a new K+ outward current in cultured rat microglia
Nörenberg, W., Gebicke-Haerter, P. J., & Illéš, P. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90587-w · Cited by 106 · see citing works
ATP-induced membrane currents in ameboid microglia acutely isolated from mouse brain slices
Haas, S. A., Brockhaus, J., Verkhratsky, A., & Kettenmann, H. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00270-9 · Cited by 101 · see citing works
Self-citationTwo different ionotropic receptors are activated by ATP in rat microglia
Visentin, S., Renzi, M., Frank, C., Greco, A., & Levi, G. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0723n.x · Cited by 94 · see citing works
Cunha, R. A., Sebastião, A. M., & Ribeiro, J. A. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb09420.x · Cited by 78 · see citing works
Chapter 29 The P2Z/P2X7 receptor of microglial cells: A novel immunomodulatory receptor
Virgilio, F. D., Sanz, J. M., Chiozzi, P., & Falzoni, S. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)63569-4 · Cited by 77 · see citing works
Illés, P., Nörenberg, W., & Gebicke-Haerter, P. J. (1996) · Neurochemistry International · doi:10.1016/0197-0186(95)00133-6 · Cited by 77 · see citing works
Tumor Necrosis Factor Mediates Myelin Damage in Organotypic Cultures of Nervous Tissuea
Selmaj, K. W., & Raine, C. S. (1988) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1988.tb27175.x · Cited by 66 · see citing works
Coexistence of purino‐ and pyrimidinoceptors on activated rat microglial cells
Nörenberg, W., Cordes, A., Blöhbaum, G., Fröhlich, R., & Illés, P. (1997) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0701241 · Cited by 64 · see citing works
Draheim, H. J., Prinz, M., Weber, J. R., Weiser, T. W., Kettenmann, H., & Hanisch, U. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00407-2 · Cited by 62 · see citing works
Self-citationCharacterization and transduction mechanisms of purinoceptors in activated rat microglia
Langosch, J. M., Gebicke‐Haerter, P. J., Nörenberg, W., & Illés, P. (1994) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1994.tb16169.x · Cited by 58 · see citing works
Ohtani, Y., Minami, M., & Satoh, M. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01478-6 · Cited by 36 · see citing works
Increased intercellular communication in mouse astrocytes exposed to hyposmotic shocks
Scemes, E., & Spray, D. C. (1998) · Glia · doi:10.1002/(sici)1098-1136(199809)24:1 · Cited by 33 · see citing works
Banerjee, R. K. (1981) · Molecular and Cellular Biochemistry · doi:10.1007/bf02354932 · Cited by 20 · see citing works
Pipitone, N., Sinha, M., Theodoridis, E., Goulding, N. J., Hall, M. D., Lanchbury, J. S. S., Corrigall, V., Panayi, G. S., & Pitzalis, C. (2001) · European Journal of Immunology · doi:10.1002/1521-4141(200107)31:7 · Cited by 19 · see citing works
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Microglia: Active sensor and versatile effector cells in the normal and pathologic brain
Hanisch, U.-K., & Kettenmann, H. (2007) · Nature Neuroscience · doi:10.1038/nn1997 · Cited by 3,676 · see citing works
Self-citationKettenmann, H., Hanisch, U.-K., Noda, M., & Verkhratsky, A. (2011) · Physiological Reviews · doi:10.1152/physrev.00011.2010 · Cited by 3,547 · see citing works
Self-citationMicroglial physiology: unique stimuli, specialized responses
Ransohoff, R. M., & Perry, V. H. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132528 · Cited by 1,858 · see citing works
Physiology and Pathophysiology of Purinergic Neurotransmission
Burnstock, G. (2007) · Physiological Reviews · doi:10.1152/physrev.00043.2006 · Cited by 1,579 · see citing works
Bours, M. J. L., Swennen, E. L. R., Di Virgilio, F., Cronstein, B. N., & Dagnelie, P. C. (2006) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2005.04.013 · Cited by 1,030 · see citing works
Purinergic signalling in neuron–glia interactions
Fields, R. D., & Burnstock, G. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1928 · Cited by 852 · see citing works
Cellular Distribution and Functions of P2 Receptor Subtypes in Different Systems
Burnstock, G., & Knight, G. E. (2004) · International review of cytology · doi:10.1016/s0074-7696(04)40002-3 · Cited by 796 · see citing works
Integrating neuroimmune systems in the neurobiology of depression
Wohleb, E. S., Franklin, T., Iwata, M., & Duman, R. S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.69 · Cited by 668 · see citing works
Neurotransmitter receptors on microglia
Pocock, J. M., & Kettenmann, H. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.07.007 · Cited by 650 · see citing works
Self-citationMicroglia during development and aging
Harry, G. J. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.04.013 · Cited by 524 · see citing works
Transcriptional and Translational Differences of Microglia from Male and Female Brains
Guneykaya, D., Ivanov, A., Hernandez, D. P., Haage, V., Wojtas, B., Meyer, N., Maricos, M., Jordan, P., Buonfiglioli, A., Gielniewski, B., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.001 · Cited by 477 · see citing works
Self-citationMadry, C., Kyrargyri, V., Arancibia-Cárcamo, I. L., Jolivet, R., Kohsaka, S., Bryan, R. M., & Attwell, D. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.002 · Cited by 464 · see citing works
Local cues establish and maintain region-specific phenotypes of basal ganglia microglia
De Biase, L. M., Schuebel, K. E., Fusfeld, Z. H., Jair, K., Hawes, I. A., Cimbro, R., Zhang, H.-Y., Liu, Q.-R., Shen, H., Xi, Z.-X., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.020 · Cited by 432 · see citing works
Purinergic signalling: From normal behaviour to pathological brain function
Burnstock, G., Krügel, U., Abbracchio, M. P., & Illés, P. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.08.006 · Cited by 394 · see citing works
P2X7 receptors in the nervous system
Sperlágh, B., Vizi, E. S., Wirkner, K., & Illés, P. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2006.03.007 · Cited by 374 · see citing works
Avignone, E., Ulmann, L., Levavasseur, F., Rassendren, F., & Audinat, É. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1820-08.2008 · Cited by 286 · see citing works
Liu, W., Tang, Y., & Feng, J. (2011) · Life Sciences · doi:10.1016/j.lfs.2011.05.011 · Cited by 303 · see citing works
ATP as a multi-target danger signal in the brain
Rodrigues, R. J., Tomé, Â. R., & Cunha, R. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00148 · Cited by 262 · see citing works
Dopamine and noradrenaline control distinct functions in rodent microglial cells
Färber, K., Pannasch, U., & Kettenmann, H. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.01.003 · Cited by 238 · see citing works
Self-citationRegulation of Microglial Functions by Purinergic Mechanisms in the Healthy and Diseased CNS
Illés, P., Rubini, P., Ulrich, H., Zhao, Y., & Tang, Y. (2020) · Cells · doi:10.3390/cells9051108 · Cited by 235 · see citing works
van Rossum, D., & Hanisch, U. (2004) · Metabolic Brain Disease · doi:10.1023/b:mebr.0000043984.73063.d8 · Cited by 234 · see citing works
Self-citationKaindl, A. M., Degos, V., Peineau, S., Gouadon, E., Chhor, V., Loron, G., Charpentier, T. L., Josserand, J., Ali, C., Vivien, D., et al. (2012) · Annals of Neurology · doi:10.1002/ana.23626 · Cited by 230 · see citing works
Microglia express GABA(B) receptors to modulate interleukin release
Kuhn, S. A., van Landeghem, F. K. H., Zacharias, R., Färber, K., Rappert, A., Pavlovic, S., Hoffmann, A., Nolte, C., & Kettenmann, H. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2003.10.023 · Cited by 218 · see citing works
Self-citationCapotondo, A., Milazzo, R., Politi, L. S., Quattrini, A., Palini, A. G., Plati, T., Merella, S., Nonis, A., Serio, C. D., Montini, E., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205858109 · Cited by 207 · see citing works
Functional role of calcium signals for microglial function
Färber, K., & Kettenmann, H. (2006) · Glia · doi:10.1002/glia.20412 · Cited by 198 · see citing works
Self-citationBrain-derived neurotrophic factor from microglia: a molecular substrate for neuropathic pain
Trang, T., Beggs, S., & Salter, M. W. (2011) · Neuron Glia Biology · doi:10.1017/s1740925x12000087 · Cited by 197 · see citing works
Physiology of microglial cells
Färber, K., & Kettenmann, H. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.12.003 · Cited by 195 · see citing works
Self-citationAdenosine and ATP Receptors in the Brain
Burnstock, G., Fredholm, B. B., & Verkhratsky, A. (2011) · Current Topics in Medicinal Chemistry · doi:10.2174/156802611795347627 · Cited by 188 · see citing works
Koizumi, S., Ohsawa, K., Inoue, K., & Kohsaka, S. (2013) · Glia · doi:10.1002/glia.22358 · Cited by 184 · see citing works
P2 receptors and neuronal injury
Franke, H., Krügel, U., & Illés, P. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0071-8 · Cited by 184 · see citing works
Zhou, M., Schools, G. P., & Kimelberg, H. K. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00570.2005 · Cited by 176 · see citing works
Krabbe, G., Matyash, V., Pannasch, U., Mamer, L., Boddeke, H. W. G. M., & Kettenmann, H. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.12.002 · Cited by 170 · see citing works
Self-citationNeurotransmitter signaling in the pathophysiology of microglia
Domercq, M., Vázquez‐Villoldo, N., & Matute, C. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00049 · Cited by 170 · see citing works
Gundersen, V., Storm‐Mathisen, J., & Bergersen, L. H. (2015) · Physiological Reviews · doi:10.1152/physrev.00024.2014 · Cited by 172 · see citing works
Purinergic signaling and microglia
Färber, K., & Kettenmann, H. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0064-7 · Cited by 163 · see citing works
Self-citationATP receptors gate microglia signaling in neuropathic pain
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Wu, L., Vadakkan, K. I., & Zhuo, M. (2007) · Glia · doi:10.1002/glia.20500 · Cited by 156 · see citing works
Sodium channel activity modulates multiple functions in microglia
Black, J. A., Liu, S., & Waxman, S. G. (2008) · Glia · doi:10.1002/glia.20830 · Cited by 156 · see citing works
Bianco, F., Fumagalli, M., Pravettoni, E., D’Ambrosi, N., Volonté, C., Matteoli, M., Abbracchio, M. P., & Verderio, C. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.12.004 · Cited by 151 · see citing works
Melani, A., Amadio, S., Gianfriddo, M., Vannucchi, M. G., Volonté, C., Bernardi, G., Pedata, F., & Sancesario, G. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600250 · Cited by 142 · see citing works
Targeting ischemic penumbra Part I: from pathophysiology to therapeutic strategy
Liu, S., Levine, S. R., & Winn, H. R. (2010) · Journal of Experimental Stroke and Translational Medicine · doi:10.6030/1939-067x-3.1.47 · Cited by 137 · see citing works
Modulation of glial cell functions by adenosine receptors
Daré, E., Schulte, G., Karovic, O., Hammarberg, C., & Fredholm, B. B. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.05.031 · Cited by 135 · see citing works
Planas, A. M. (2024) · Glia · doi:10.1002/glia.24501 · Cited by 133 · see citing works
Fiebich, B. L., Akter, S., & Akundi, R. S. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00260 · Cited by 126 · see citing works
Garaschuk, O., & Verkhratsky, A. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9658-2_3 · Cited by 124 · see citing works
Takenouchi, T., OGIHARA, K., Sato, M., & Kitani, H. (2005) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2005.08.001 · Cited by 127 · see citing works
Takenouchi, T., Nakai, M., Iwamaru, Y., Sugama, S., Tsukimoto, M., Fujita, M., Wei, J., Sekigawa, A., Sato, M., Kojima, S., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802577 · Cited by 126 · see citing works
Expression of P2 nucleotide receptors varies with age and sex in murine brain microglia
Crain, J. M., Nikodémová, M., & Watters, J. J. (2009) · Journal of Neuroinflammation · doi:10.1186/1742-2094-6-24 · Cited by 122 · see citing works
Roles of P2 receptors in glial cells: focus on astrocytes
Abbracchio, M. P., & Ceruti, S. (2006) · Purinergic Signalling · doi:10.1007/s11302-006-9016-0 · Cited by 116 · see citing works
Glia: A Neglected Player in Non-invasive Direct Current Brain Stimulation
Gellner, A., Reis, J., & Fritsch, B. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00188 · Cited by 114 · see citing works
Receptors, Ion Channels, and Signaling Mechanisms Underlying Microglial Dynamics
Madry, C., & Attwell, D. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.637157 · Cited by 109 · see citing works
“Indeed, in microglia in situ, only extracellular nucleotides such as ATP, ADP, and UDP evoke inward membrane currents through ionotropic P2X (presumably P2X4 and P2X7) receptors and outward K currents via G protein-coupled (P2Y) purinergic receptors (23, 31–33, 35, 50), whereas other neurotransmitters (glutamate, GABA…”
BackgroundLabrousse, V. F., Costes, L., Aubert, A., Darnaudéry, M., Ferreira, G., Amédée, T., & Layé, S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006006 · Cited by 106 · see citing works
Ion Channels and Receptors as Determinants of Microglial Function
Izquierdo, P., Attwell, D., & Madry, C. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2018.12.007 · Cited by 102 · see citing works
The ectonucleotidase cd39/ENTPDase1 modulates purinergic‐mediated microglial migration
Färber, K., Markworth, S., Pannasch, U., Nolte, C., Prinz, V., Kronenberg, G., Gertz, K. R., Endres, M., Bechmann, I., Enjyoji, K., et al. (2007) · Glia · doi:10.1002/glia.20606 · Cited by 102 · see citing works
Self-citationDe Simone, R., Niturad, C. E., De Nuccio, C., Ajmone‐Cat, M. A., Visentin, S., & Minghetti, L. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06937.x · Cited by 104 · see citing works
Scheffel, J., Regen, T., van Rossum, D., Seifert, S., Ribes, S., Nau, R., Parsa, R., Harris, R. A., Boddeke, H. W. G. M., Chuang, H., et al. (2012) · Glia · doi:10.1002/glia.22409 · Cited by 102 · see citing works
Self-citationNeuronal and glial purinergic receptors functions in neuron development and brain disease
del Puerto, A., Wandosell, F. G., & Garrido, J. J. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00197 · Cited by 101 · see citing works
Purinergic modulation of microglial cell activation
Sperlágh, B., & Illés, P. (2006) · Purinergic Signalling · doi:10.1007/s11302-006-9043-x · Cited by 99 · see citing works
Plescher, M., Seifert, G., Hansen, J. N., Bedner, P., Steinhäuser, C., & Halle, A. (2018) · Glia · doi:10.1002/glia.23318 · Cited by 101 · see citing works
Purinergic signaling orchestrating neuron-glia communication
Agostinho, P. M., Madeira, D., Dias, L., Simões, A. P., Cunha, R. A., & Canas, P. M. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.105253 · Cited by 91 · see citing works
Therapeutic potential of mGluR5 targeting in Alzheimer's disease
Kumar, A., Dhull, D. K., & Mishra, P. S. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00215 · Cited by 92 · see citing works
Heterogeneity and potentiation of AMPA type of glutamate receptors in rat cultured microglia
Hagino, Y., Kariura, Y., Manago, Y., Amano, T., Wang, B., Sekiguchi, M., Nishikawa, K., Aoki, S., Wada, K., & Noda, M. (2004) · Glia · doi:10.1002/glia.20034 · Cited by 91 · see citing works
Rappold, P. M., Lynd‐Balta, E., & Joseph, S. (2006) · Brain Research · doi:10.1016/j.brainres.2006.03.040 · Cited by 90 · see citing works
Weisman, G. A., Camden, J. M., Peterson, T. S., Ajit, D., Woods, L. T., & Erb, L. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8263-z · Cited by 85 · see citing works
P2Y2 Nucleotide Receptor-Mediated Responses in Brain Cells
Peterson, T. S., Camden, J. M., Wang, Y., Seye, C. I., Wood, W. G., Sun, G. Y., Erb, L., Petris, M. J., & Weisman, G. A. (2010) · Molecular Neurobiology · doi:10.1007/s12035-010-8115-7 · Cited by 84 · see citing works
Kurpius, D., Nolley, E. P., & Dailey, M. E. (2007) · Glia · doi:10.1002/glia.20509 · Cited by 83 · see citing works
Jabs, R., Matthias, K., Grote, A., Grauer, M., Seifert, G., & Steinhäuser, C. (2007) · Glia · doi:10.1002/glia.20580 · Cited by 81 · see citing works
Purinoceptors in microglia and neuropathic pain
Trang, T., Beggs, S., & Salter, M. W. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0074-5 · Cited by 80 · see citing works
Garg, S., Syed, M., & Kielian, T. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03384.x · Cited by 80 · see citing works
Swiatkowski, P., Murugan, M., Eyo, U. B., Wāng, Y., Rangaraju, S., Oh, S. B., & Wu, L. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.01.008 · Cited by 75 · see citing works
Microglial K+ channel expression in young adult and aged mice
Schilling, T., & Eder, C. (2014) · Glia · doi:10.1002/glia.22776 · Cited by 77 · see citing works
Potential of Glial Cell Modulators in the Management of Substance Use Disorders
Jones, J. D. (2020) · CNS Drugs · doi:10.1007/s40263-020-00721-9 · Cited by 78 · see citing works
Newell, E. W., & Schlichter, L. C. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.092056 · Cited by 75 · see citing works
P2X7 receptor activation regulates microglial cell death during oxygen-glucose deprivation
Eyo, U. B., Miner, S. A., Ahlers‐Dannen, K. E., Wu, L., & Dailey, M. E. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.05.032 · Cited by 75 · see citing works
Microglia sense neuronal activity via GABA in the early postnatal hippocampus
Logiacco, F., Xia, P., Georgiev, S. V., Franconi, C., Chang, Y.-J., Ugursu, B., Sporbert, A., Kühn, R., Kettenmann, H., & Semtner, M. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.110128 · Cited by 72 · see citing works
Self-citationBernardino, L., Balosso, S., Ravizza, T., Marchi, N., Ku, G., Randle, J. C. R., Malva, J., & Vezzani, A. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05387.x · Cited by 87 · see citing works
Duong, P., Tenkorang, M. A. A., Trieu, J., McCuiston, C., Rybalchenko, N., & Cunningham, R. L. (2020) · Biology of Sex Differences · doi:10.1186/s13293-020-0283-1 · Cited by 72 · see citing works
Microglia Ontology and Signaling
ElAli, A., & Rivest, S. (2016) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2016.00072 · Cited by 73 · see citing works
P2 Receptor Signaling in Neurons and Glial Cells of the Central Nervous System
Köles, L., Leichsenring, A., Rubini, P., & Illés, P. (2011) · Advances in pharmacology · doi:10.1016/b978-0-12-385526-8.00014-x · Cited by 71 · see citing works
van der Putten, C., Zuiderwijk-Sick, E. A., van Straalen, L., de Geus, E. D., Boven, L. A., Kondova, I. I., IJzerman, A. P., & Bajramovic, J. J. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803383 · Cited by 71 · see citing works
The Role of Glial Adenosine Receptors in Neural Resilience and the Neurobiology of Mood Disorders
van Calker, D., & Biber, K. P. H. (2005) · Neurochemical Research · doi:10.1007/s11064-005-8792-1 · Cited by 70 · see citing works
Lam, D., Lively, S. S., & Schlichter, L. C. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0941-3 · Cited by 71 · see citing works
Pannell, M., Meier, M. A., Szulzewsky, F., Matyash, V., Endres, M., Kronenberg, G., Prinz, V., Waiczies, S., Wolf, S. A., & Kettenmann, H. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0962-y · Cited by 69 · see citing works
Self-citationWendt, S., Maricos, M., Vana, N., Meyer, N., Guneykaya, D., Semtner, M., & Kettenmann, H. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.05.027 · Cited by 69 · see citing works
Self-citationDifferential Regulation of Adhesion and Phagocytosis of Resting and Activated Microglia by Dopamine
Yang, F., Chen, Z., Pathak, J. L., Carneiro, A. M. D., & Chung, C. Y. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00309 · Cited by 66 · see citing works
Prowse, N. A., & Hayley, S. P. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.018 · Cited by 67 · see citing works
Opioid use affects antioxidant activity and purine metabolism: preliminary results
Mannelli, P., Patkar, A. A., Rozen, S., Matson, W. R., Krishnan, R. R., & Kaddurah-Daouk, R. F. (2009) · Human Psychopharmacology Clinical and Experimental · doi:10.1002/hup.1068 · Cited by 66 · see citing works
Ion channel expression in resting and activated microglia of hippocampal slices from juvenile mice
Schilling, T., & Eder, C. (2007) · Brain Research · doi:10.1016/j.brainres.2007.10.027 · Cited by 66 · see citing works
P2X4 purinoceptor signaling in chronic pain
Trang, T., & Salter, M. W. (2012) · Purinergic Signalling · doi:10.1007/s11302-012-9306-7 · Cited by 66 · see citing works
Cavaliere, F., Dinkel, K., & Reymann, K. G. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.04.038 · Cited by 64 · see citing works
Robertson, J., Lang, S., Lambert, P. A., & Martin, P. E. (2010) · Biochemical Journal · doi:10.1042/bj20091753 · Cited by 63 · see citing works
Potucek, Y., Crain, J. M., & Watters, J. J. (2006) · Neurochemistry International · doi:10.1016/j.neuint.2006.04.005 · Cited by 61 · see citing works
Regulation of cell-to-cell communication mediated by astrocytic ATP in the CNS
Koizumi, S., Fujishita, K., & Inoue, K. (2005) · Purinergic Signalling · doi:10.1007/s11302-005-6321-y · Cited by 59 · see citing works
Ballerini, P., Iorio, P. D., Ciccarelli, R., Caciagli, F., Polp, A., Beraudi, A., Buccella, S., D’Alimonte, I., D’Auro, M., Nargi, E., et al. (2005) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463200501800208 · Cited by 59 · see citing works
Dutot, M., Pouzaud, F., Larosche, I., Brignole‐Baudouin, F., Warnet, J., & Rat, P. (2006) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.06-0224 · Cited by 58 · see citing works
Seo, D. R., Kim, K. Y., & Lee, Y. B. (2004) · Neuroreport · doi:10.1097/00001756-200405190-00015 · Cited by 58 · see citing works
Li, F., Wang, L., Li, J., Gong, M., He, L., Feng, R., Dai, Z., & Li, S. (2011) · BMC Neuroscience · doi:10.1186/1471-2202-12-111 · Cited by 57 · see citing works
Murphy, N., Cowley, T. R., Richardson, J. C., Virley, D. J., Upton, N., Walter, D. S., & Lynch, M. A. (2011) · Brain Pathology · doi:10.1111/j.1750-3639.2011.00531.x · Cited by 56 · see citing works
Nguyen, H. M., Lucente, J. D., Chen, Y., Cui, Y., Ibrahim, R. H., Pennington, M. W., Jin, L., Maezawa, I., & Wulff, H. (2020) · Glia · doi:10.1002/glia.23847 · Cited by 54 · see citing works
Interaction of P2 purinergic receptors with cellular macromolecules
Köles, L., Gerevich, Z., Oliveira, J. F., Zádori, Z., Wirkner, K., & Illés, P. (2007) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-007-0222-2 · Cited by 53 · see citing works
- Authors
- Boucsein, C., Zacharias, R., Färber, K., Pavlovic, S., Hanisch, U., & Kettenmann, H.
- Affiliations
- Max Delbrück Center (DE)
- Corresponding author
- Kettenmann, Helmut
- ORCID
- Kettenmann, Helmut
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2003-06
- Volume
- 17
- Issue
- 11
- Pages
- 2267-2276
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2074389121
- Cited by
- 203
- References
- 44
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 4 · 2023: 8 · 2022: 3 · 2021: 4 · 2020: 10 · 2019: 9 · 2018: 7 · 2017: 8 · 2016: 10 · 2015: 7 · 2014: 11 · 2013: 7 · 2012: 18
- FWCI
- 6.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Keywords
- microglial cells, purinergic receptors, ATP signalling, P2Y receptors, P2X7 receptor, microglial activation, potassium currents, lipopolysaccharide, neuroinflammation, nitric oxide, TNF-α, interleukin-6, IL-12, macrophage inflammatory protein-1alpha, acute brain slices
- MeSH terms
- Adenosine Triphosphate, Animals, Animals, Newborn, Brain, Calcium, Cell Survival, Cells, Cultured, Dose-Response Relationship, Drug, Drug Interactions, Lipopolysaccharides, Magnesium, Membrane Potentials, Mice, Inbred C57BL, Neural Conduction, Nitric Oxide, Receptors, Purinergic, Time Factors, Uridine Diphosphate, Uridine Triphosphate, Vasodilator Agents, Potassium Channels, Microglia, Chloride Channels, Patch-Clamp Techniques, Adenosine-5'-(N-ethylcarboxamide), Mice, In Vitro Techniques
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