Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus

Journal of Neuroscience

Volumn 34, Issue 32, 2014, Pages 10528-10540

  Eyo, Ukpong B ^a   Peng, Jiyun ^a   Swiatkowski, Przemyslaw ^a   Mukherjee, Aparna ^a   Bispo, Ashley ^a   Wu, Long Jun ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Epilepsy; Glutamate; Microglia; NMDA receptor; P2Y12 receptor; Process extension

Indexed keywords

EPILEPSY; GLUTAMATE; MICROGLIA; NMDA RECEPTOR; P2Y12 RECEPTOR; PROCESS EXTENSION;

ANIMALS; CELL SURFACE EXTENSIONS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID AGENTS; FEMALE; HIPPOCAMPUS; LUMINESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; NEURONS; POTASSIUM CHLORIDE; RECEPTORS, CHEMOKINE; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, PURINERGIC P2Y12; SODIUM CHANNEL BLOCKERS; STATUS EPILEPTICUS;

EID: 84905686370     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0416-14.2014     Document Type: Article

References (58)

1. Avignone E., Ulmann L, Levavasseur F, Rassendren F, Audinat E (2008) Status epilepticus induces a particular microglial activation state characterized by enhanced purinergic signaling. J Neurosci 28:9133-9144. CrossRef Medline
2. Beach T. G, Woodhurst WB, MacDonald DB, Jones MW (1995) Reactive microglia in hippocampal sclerosis associated with human temporal lobe epilepsy. Neurosci Lett 191:27-30. CrossRef Medline
3. Boucsein C., Kettenmann H, Nolte C (2000) Electrophysiological properties of microglial cells in normal and pathologic rat brain slices. Eur J Neurosci 12:2049-2058. CrossRef Medline
4. Butovsky O., Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T., Dake B, Wu PM, Doykan CE, Fanek Z, Liu L, Chen Z, Rothstein J. D, Ransohoff RM, Gygi SP, Antel JP, Weiner HL (2014) Identification of a unique TGF-beta-dependent molecular and functional signature in microglia. Nat Neurosci 17:131-143. CrossRef Medline
5. Cavus I., Kasoff WS, Cassaday MP, Jacob R, Gueorguieva R, Sherwin RS, Krystal J. H, Spencer DD, Abi-Saab WM (2005) Extracellular metabolites in the cortex and hippocampus of epileptic patients. Ann Neurol 57:226-235. CrossRef Medline
6. Davalos D., Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-758. CrossRef Medline
7. Davalos D., Ryu JK, Merlini M, Baeten KM, Le Moan N, Petersen MA, Deerinck TJ, Smirnoff DS, Bedard C, Hakozaki H, Gonias Murray S, Ling JB, Lassmann H., Degen JL, Ellisman MH, Akassoglou K (2012) Fibrinogeninduced perivascular microglial clustering is required for the development of axonal damage in neuroinflammation. Nat Commun 3:1227. CrossRef Medline
8. Dibaj P., Nadrigny F, Steffens H, Scheller A, Hirrlinger J, Schomburg ED, Neusch C., Kirchhoff F (2010) NO mediates microglial response to acute spinal cord injury under ATP control in vivo. Glia 58:1133-1144. CrossRef Medline
9. Drage M. G, Holmes GL, Seyfried TN (2002) Hippocampal neurons and glia in epileptic EL mice. J Neurocytol 31:681-692. CrossRef Medline
10. During M. J, Spencer DD (1993) Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341:1607-1610. CrossRef Medline
11. Eyo U., Dailey ME (2012) Effects of oxygen-glucose deprivation on microglial mobility and viability in developing mouse hippocampal tissues. Glia 60:1747-1760. CrossRef Medline
12. Eyo U. B, Dailey ME (2013) Microglia: key elements in neural development, plasticity, and pathology. J Neuroimmune Pharmacol 8:494-509. CrossRef Medline
13. Eyo U. B, Wu LJ (2013) Bi-directional microglia-neuron communication in the healthy brain. Neural Plast 2013:456857. CrossRef Medline
14. Färber K., Markworth S, Pannasch U, Nolte C, Prinz V, Kronenberg G, Gertz K, Endres M, Bechmann I, Enjyoji K, Robson SC, Kettenmann H (2008) The ectonucleotidase cd39/ENTPDase1 modulates purinergic-mediated microglial migration. Glia 56:331-341. CrossRef Medline
15. Feng G., Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne J. M, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51. CrossRef Medline
16. Fisher R. S, van Emde Boas W, Blume W, Elger C, Genton P, Lee P, Engel J Jr (2005) Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 46:470-472. CrossRef Medline
17. Fontainhas A. M, Wang M, Liang KJ, Chen S, Mettu P, Damani M, Fariss RN, Li W., Wong WT (2011) Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission. PLoS One 6:e15973. CrossRef Medline
18. Haynes S. E, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D (2006) The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9:1512-1519. CrossRef Medline
19. Hines D. J, Hines RM, Mulligan SJ, Macvicar BA (2009) Microglia processes block the spread of damage in the brain and require functional chloride channels. Glia 57:1610-1618. CrossRef Medline
20. Huang Y. J, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD (2007) The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci U S A 104:6436-6441. CrossRef Medline
21. Jung S., Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20:4106-4114. CrossRef Medline
22. Kaindl A. M, Degos V, Peineau S, Gouadon E, Chhor V, Loron G, Le Charpentier T, Josserand J, Ali C, Vivien D, Collingridge GL, Lombet A, Issa L, Rene F., Loeffler JP, Kavelaars A, Verney C, Mantz J, Gressens P (2012) Activation of microglial N-methyl-D-aspartate receptors triggers inflammation and neuronal cell death in the developing and mature brain. Ann Neurol 72:536-549. CrossRef Medline
23. Kang J., Kang N, Lovatt D, Torres A, Zhao Z, Lin J, Nedergaard M (2008) Connexin 43 hemichannels are permeable to ATP. J Neurosci 28:4702-4711. CrossRef Medline
24. Kobayashi K., Yamanaka H, Fukuoka T, Dai Y, Obata K, Noguchi K (2008) P2Y12 receptor upregulation in activated microglia is a gateway of p38 signaling and neuropathic pain. J Neurosci 28:2892-2902. CrossRef Medline
25. Kuhn B., Denk W, Bruno RM (2008) In vivo two-photon voltage-sensitive dye imaging reveals top-down control of cortical layers 1 and 2 during wakefulness. Proc Natl Acad Sci U S A 105:7588-7593. CrossRef Medline
26. Kurtenbach S., Prochnow N, Kurtenbach S, Klooster J, Zoidl C, Dermietzel R, Kamermans M., Zoidl G (2013) Pannexin1 channel proteins in the zebrafish retina have shared and unique properties. PLoS One 8:e77722. CrossRef Medline
27. Liang K. J, Lee JE, Wang YD, Ma W, Fontainhas AM, Fariss RN, Wong WT (2009) Regulation of dynamic behavior of retinal microglia by CX3CR1 signaling. Invest Ophthalmol Vis Sci 50:4444-4451. CrossRef Medline
28. Li Y., Du XF, Liu CS, Wen ZL, Du JL (2012) Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev Cell 23: 1189-1202. CrossRef Medline
29. Liu G. J, Nagarajah R, Banati RB, Bennett MR (2009) Glutamate induces directed chemotaxis of microglia. Eur J Neurosci 29:1108-1118. CrossRef Medline
30. Locovei S., Wang J, Dahl G (2006) Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 580:239-244. CrossRef Medline
31. MacVicar B. A, Thompson RJ (2010) Non-junction functions of pannexin-1 channels. Trends Neurosci 33:93-102. CrossRef Medline
32. Marín-Teva J. L, Dusart I, Colin C, Gervais A, van Rooijen N, Mallat M (2004) Microglia promote the death of developing Purkinje cells. Neuron 41: 535-547. CrossRef Medline
33. Meurs A., Clinckers R, Ebinger G, Michotte Y, Smolders I (2008) Seizure activity and changes in hippocampal extracellular glutamate, GABA, dopamine and serotonin. Epilepsy Res 78:50-59. CrossRef Medline
34. Murugan M., Sivakumar V, Lu J, Ling EA, Kaur C (2011) Expression of N-methyl D-aspartate receptor subunits in amoeboid microglia mediates production of nitric oxide via NF-kappaB signaling pathway and oligodendrocyte cell death in hypoxic postnatal rats. Glia 59:521-539. CrossRef Medline
35. Nimmerjahn A., Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314-1318. CrossRef Medline
36. Ohsawa K., Sanagi T, Nakamura Y, Suzuki E, Inoue K, Kohsaka S (2012) Adenosine A3 receptor is involved in ADP-induced microglial process extension and migration. J Neurochem 121:217-227. CrossRef Medline
37. Orellana J. A, Montero TD, von Bernhardi R (2013) Astrocytes inhibit nitric oxide-dependent Ca(2+) dynamics in activated microglia: involvement of ATP released via pannexin 1 channels. Glia 61:2023-2037. CrossRef Medline
38. Paolicelli R. C, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, Giustetto M, Ferreira TA, Guiducci E, Dumas L, Ragozzino D, Gross CT (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333:1456-1458. CrossRef Medline
39. Pascual O., Ben Achour S, Rostaing P, Triller A, Bessis A (2012) Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission. Proc Natl Acad Sci U S A 109:E197-205. CrossRef Medline
40. Racine R. J (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294. CrossRef Medline
41. Ransohoff R. M, Perry VH (2009) Microglial physiology: unique stimuli, specialized responses. Annu Rev Immunol 27:119-145. CrossRef Medline
42. Sasaki Y., Hoshi M, Akazawa C, Nakamura Y, Tsuzuki H, Inoue K, Kohsaka S (2003) Selective expression of Gi/o-coupled ATP receptor P2Y12 in microglia in rat brain. Glia 44:242-250. CrossRef Medline
43. Schafer D. P, Lehrman EK, Stevens B (2013) The "quad-partite" synapse: microglia-synapse interactions in the developing and mature CNS. Glia 61:24-36. CrossRef Medline
44. Schafer D. P, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complementdependent manner. Neuron 74:691-6705. CrossRef Medline
45. Shapiro L. A, Wang L, Ribak CE (2008) Rapid astrocyte and microglial activation following pilocarpine-induced seizures in rats. Epilepsia 49 [Suppl 2]:33-41. CrossRef Medline
46. Sieger D., Moritz C, Ziegenhals T, Prykhozhij S, Peri F (2012) Long-range Ca2+ waves transmit brain-damage signals to microglia. Dev Cell 22: 1138-1148. CrossRef Medline
47. Thompson R. J, Jackson MF, Olah ME, Rungta RL, Hines DJ, Beazely MA, MacDonald J. F, MacVicar BA (2008) Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322: 1555-1559. CrossRef Medline
48. Tozaki-Saitoh H., Tsuda M, Miyata H, Ueda K, Kohsaka S, Inoue K (2008) P2Y12 receptors in spinal microglia are required for neuropathic pain after peripheral nerve injury. J Neurosci 28:4949-4956. CrossRef Medline
49. Tremblay M. É, Lowery RL, Majewska AK (2010) Microglial interactions with synapses are modulated by visual experience. PLoS Biol 8:e1000527. CrossRef Medline
50. Tzingounis A. V, Wadiche JI (2007) Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 8:935-947. CrossRef Medline
51. Ueda Y., Doi T, Tokumaru J, Yokoyama H, Nakajima A, Mitsuyama Y, Ohya-Nishiguchi H, Kamada H, Willmore LJ (2001) Collapse of extracellular glutamate regulation during epileptogenesis: down-regulation and functional failure of glutamate transporter function in rats with chronic seizures induced by kainic acid. J Neurochem 76:892-900. Medline
52. Ueno M., Fujita Y, Tanaka T, Nakamura Y, Kikuta J, Ishii M, Yamashita T (2013) Layer V cortical neurons require microglial support for survival during postnatal development. Nat Neurosci 16:543-551. CrossRef Medline
53. Vezzani A., French J, Bartfai T, Baram TZ (2011) The role of inflammation in epilepsy. Nat Rev Neurol 7:31-40. CrossRef Medline
54. Vinet J., Weering HR, Heinrich A, Kälin RE, Wegner A, Brouwer N, Heppner FL, Rooijen Nv, Boddeke HW, Biber K (2012) Neuroprotective function for ramified microglia in hippocampal excitotoxicity. J Neuroinflammation 9:27. CrossRef Medline
55. Wake H., Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J (2009) Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci 29:3974-3980. CrossRef Medline
56. Wu L. J, Zhuo M (2008) Resting microglial motility is independent of synaptic plasticity in mammalian brain. J Neurophysiol 99:2026-2032. CrossRef Medline
57. Wu L. J, Vadakkan KI, Zhuo M (2007) ATP-induced chemotaxis of microglial processes requires P2Y receptor-activated initiation of outward potassium currents. Glia 55:810-821. CrossRef Medline
58. Wu L. J, Wu G, Akhavan Sharif MR, Baker A, Jia Y, Fahey FH, Luo HR, Feener EP, Clapham DE (2012) The voltage-gated proton channel Hv1 enhances brain damage from ischemic stroke. Nat Neurosci 15:565-573. CrossRef Medline