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01-06-2012 | Original Article

The roles of P2X7 receptor in regional-specific microglial responses in the rat brain following status epilepticus

Authors: Hea Kyung Choi, Hea Jin Ryu, Ji-Eun Kim, Seung-Mook Jo, Hui-Chul Choi, Hong-Ki Song, Tae-Cheon Kang

Published in: Neurological Sciences | Issue 3/2012

Abstract

Recently, we have reported that astroglial activations in response to status epilepticus (SE) show regional-specific manners in the rat hippocampus. However, it is unknown that microglial responses to SE would show regional-specific patterns. Therefore, the present study was designed to elucidate the regional-specific microglial activation and relationship between P2X7 receptor functions and SE-induced microglial responses in the rat brain. Following SE, microglia appeared amoeboid or phagocytic in the dentate gyrus and the piriform cortex. In contrast, elongated microglia were observed in the CA1 hippocampal regions and the frontoparietal cortex. In the dentate gyrus, the CA1 hippocampal regions, and the frontoparietal cortex, these microglial activation accelerated by BzATP (a P2X7 receptor agonist)-infusion, but inhibited by OxATP (a P2X7 receptor antagonist). However, SE-induced microglial activation in the piriform cortex was not affected by BzATP or OxATP-infusion. Therefore, our findings indicate that SE-induced microglial activation may show regional-specific manners, and suggest that P2X7 receptor function differently modulates SE-induced microglial responses in distinct brain regions.

Margerison JH, Corsellis JA (1966) Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89:499–530PubMedCrossRef

Wittner L, Maglóczky Z, Borhegyi Z, Halász P, Tóth S, Eross L, Szabó Z, Freund TF (2001) Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus. Neuroscience 108:587–600PubMedCrossRef

Mathern GW, Babb TL, Vickrey BG, Melendez M, Pretorius JK (1995) The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 118:105–118PubMedCrossRef

Briellmann RS, Kalnins RM, Berkovic SF, Jackson GD (2002) Hippocampal pathology in refractory temporal lobe epilepsy: T2-weighted signal change reflects dentate gliosis. Neurology 58:265–271PubMedCrossRef

Vessal M, Dugani CB, Solomon DA, McIntyre Burnham W, Ivy GO (2005) Might astrocytes play a role in maintaining the seizure-prone state? Brain Res 1044:190–196PubMedCrossRef

Kang TC, Kim DS, Kwak SE, Kim JE, Won MH, Kim DW, Choi SY, Kwon OS (2006) Epileptogenic roles of astroglial death and regeneration in the dentate gyrus of experimental temporal lobe epilepsy. Glia 54:258–271PubMedCrossRef

Revuelta R, Arriada-Mendicoa N, Ramirez-Alba J, Soto-Hernandez JL (2002) Simultaneous treatment of a pituitary adenoma and an internal carotid artery aneurysm through a supraorbital keyhole approach. Minim Invasive Neurosurg 45:109–111PubMedCrossRef

Kim JE, Kwak SE, Choi SY, Kang TC (2008) Region-specific alterations in astroglial TWIK-related acid-sensitive K + −1 channel immunoreactivity in the rat hippocampal complex following pilocarpine-induced status epilepticus. J Comp Neurol 510:463–474PubMedCrossRef

Kim JE, Yeo SI, Ryu HJ, Kim MJ, Kim DS, Jo SM, Kang TC (2010) Astroglial loss and edema formation in the rat piriform cortex and hippocampus following pilocarpine-induced status epilepticus. J Comp Neurol 518:4612–4628PubMedCrossRef

10.

Kim JE, Ryu HJ, Yeo SI, Seo CH, Lee BC, Choi IG, Kim DS, Kang TC (2009) Differential expressions of aquaporin subtypes in astroglia in the hippocampus of chronic epileptic rats. Neuroscience 163:781–789PubMedCrossRef

11.

Sheen SH, Kim JE, Ryu HJ, Yang Y, Choi KC, Kang TC (2011) Decrease in dystrophin expression prior to disruption of brain–blood barrier within the rat piriform cortex following status epilepticus. Brain Res 1369:173–183PubMedCrossRef

12.

Shapiro LA, Wang L, Ribak CE (2008) Rapid astrocyte and microglial activation following pilocarpine-induced seizures in rats. Epilepsia 2:33–41CrossRef

13.

Melani A, Amadio S, Gianfriddo M, Vannucchi MG, Volontè C, Bernardi G, Pedata F, Sancesario G (2006) P2X7 receptor modulation on microglial cells and reduction of brain infarct caused by middle cerebral artery occlusion in rat. J Cereb Blood Flow Metab 26:974–982PubMedCrossRef

14.

Parvathenani LK, Tertyshnikova S, Greco CR, Roberts SB, Robertson B, Posmantur R (2003) P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer’s disease. J Biol Chem 278:1331–13309CrossRef

15.

McLarnon JG, Ryu JK, Walker DG, Choi HB (2006) Upregulated expression of purinergic P2X(7) receptor in Alzheimer disease and amyloid-beta peptide-treated microglia and in peptide-injected rat hippocampus. J Neuropathol Exp Neurol 65:1090–1097PubMedCrossRef

16.

Ferrari D, Chiozzi P, Falzoni S, Hanau S, Di Virgilio F (1997) Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin. J Exp Med 185:579–582PubMedCrossRef

17.

Brough D, Le Feuvre RA, Iwakura Y, Rothwell NJ (2002) Purinergic (P2X7) receptor activation of microglia induces cell death via an interleukin-1-independent mechanism. Mol Cell Neurosci 19:272–280PubMedCrossRef

18.

Chakfe Y, Seguin R, Antel JP, Morissette C, Malo D, Henderson D, Séguéla P (2002) ADP and AMP induce interleukin-1beta release from microglial cells through activation of ATP-primed P2X7 receptor channels. J Neurosci 22:3061–3069PubMed

19.

Le Feuvre RA, Brough D, Touzani O, Rothwell NJ (2003) Role of P2X7 receptors in ischemic and excitotoxic brain injury in vivo. J Cereb Blood Flow Metab 23:381–384PubMedCrossRef

20.

Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. Academic Press, San Diego

21.

Siuciak JA, Boylan C, Fritsche M, Altar CA, Lindsay RM (1996) BDNF increases monoaminergic activity in rat brain following intracerebroventricular or intraparenchymal administration. Brain Res 710:11–20PubMedCrossRef

22.

Pencea V, Bingaman KD, Wiegand SJ, Luskin MB (2001) Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J Neurosci 21:6706–6717PubMed

23.

Kroon JP, Riley AL (1986) A microcomputer-based system for stereotaxic coordinates in the rat brain. Physiol Behav 38:593–596PubMedCrossRef

24.

Kim JE, Kim DW, Kwak SE, Ryu HJ, Yeo SI, Kwon OS, Choi SY, Kang TC (2009) Pyridoxal-5′-phosphate phosphatase/chronophin inhibits long-term potentiation induction in the rat dentate gyrus. Hippocampus 19:1078–1089PubMedCrossRef

25.

Streit WJ, Walter SA, Pennell NA (1999) Reactive microgliosis. Prog Neurobiol 57:563–581PubMedCrossRef

26.

Blinzinger K, Kreutzberg G (1968) Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Zeitschrift für Zellforschung und Mikroskopische Anatomie 85:145–157PubMedCrossRef

27.

Trapp BD, Wujek JR, Criste GA, Jalabi W, Yin X, Kidd GJ, Stohlman S, Ransohoff R (2007) Evidence for synaptic stripping by cortical microglia. Glia 55:360–368PubMedCrossRef

28.

Graeber MB, Streit WJ, Kreutzberg GW (1988) Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J Neurosci Res 21:18–24PubMedCrossRef

29.

Streit WJ, Kreutzberg GW (1988) Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J Comp Neurol 268:248–263PubMedCrossRef

30.

Svensson M, Aldskogius H (1993) Synaptic density of axotomized hypoglossal motorneurons following pharmacological blockade of the microglial cell proliferation. Exp Neurol 120:123–131PubMedCrossRef

31.

Graeber MB, Bise K, Mehraein P (1993) Synaptic stripping in the human facial nucleus. Acta Neuropathol 86:179–181PubMedCrossRef

32.

Brännström T, Kellerth JO (1998) Changes in synaptology of adult cat spinal alpha-motoneurons after axotomy. Exp Brain Res 118:1–13PubMedCrossRef

33.

Oliveira AL, Thams S, Lidman O, Piehl F, Hökfelt T, Kärre K, Lindå H, Cullheim S (2004) A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc Natl Acad Sci USA 101:17843–17848PubMedCrossRef

34.

Lindå H, Shupliakov O, Ornung G, Ottersen OP, Storm-Mathisen J, Risling M, Cullheim S (2000) Ultrastructural evidence for a preferential elimination of glutamate-immunoreactive synaptic terminals from spinal motoneurons after intramedullary axotomy. J Comp Neurol 425:10–23PubMedCrossRef

35.

Swann JW, Al-Noori S, Jiang M, Lee CL (2000) Spine loss and other dendritic abnormalities in epilepsy. Hippocampus 10:617–625PubMedCrossRef

36.

Sperk G (1994) Kainic acid seizures in the rat. Prog Neurobiol 42:1–32PubMedCrossRef

37.

Covolan L, Mello LE (2000) Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus. Epilepsy Res 39:133–152PubMedCrossRef

38.

Nairismägi J, Gröhn OH, Kettunen MI, Nissinen J, Kauppinen RA, Pitkänen A (2004) Progression of brain damage after status epilepticus and its association with epileptogenesis: a quantitative MRI study in a rat model of temporal lobe epilepsy. Epilepsia 45:1024–2034PubMedCrossRef

39.

Löscher W, Ebert U (1996) The role of the piriform cortex in kindling. Prog Neurobiol 50:427–481PubMedCrossRef

40.

McIntyre DC, Kelly ME (2000) The parahippocampal cortices and kindling. NYork Acad Sci 911:343–354CrossRef

41.

Emerson MR, Nelson SR, Samson FE, Pazdernik TL (1999) Hypoxia preconditioning attenuates brain edema associated with kainic acid-induced status epilepticus in rats. Brain Res 825:189–193PubMedCrossRef

42.

Guerra AN, Fisette PL, Pfeiffer ZA, Quinchia-Rios BH, Prabhu U, Aga M, Denlinger LC, Guadarrama AG, Abozeid S, Sommer JA, Proctor RA, Bertics PJ (2003) Purinergic receptor regulation of LPS-induced signaling and pathophysiology. J Endotoxin Res 9:256–263PubMed

43.

North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013–1067PubMed

44.

Rothwell N (2003) Interleukin-1 and neuronal injury: Mechanisms, modification, and therapeutic potential. Brain Behav Immun 17:152–157PubMedCrossRef

45.

Sim JA, Young MT, Sung HY, North RA, Surprenant A (2004) Reanalysis of P2X7 receptor expression in rodent brain. J Neurosci 24:6307–6314PubMedCrossRef

46.

Pfeiffer ZA, Aga M, Prabhu U, Watters JJ, Hall DJ, Bertics PJ (2004) The nucleotide receptor P2X7 mediates actin reorganization and membrane blebbing in RAW 264.7 macrophages via p38 MAP kinase and Rho. J Leukoc Biol 75:1173–1182PubMedCrossRef

47.

Verhoef PA, Estacion M, Schilling W, Dubyak GR (2003) P2X7 receptor-dependent blebbing and activation of rho-effector kinases, caspases and IL-1 release. J Immunol 170:5728–5738PubMed

48.

Kataoka A, Tozaki-Saitoh H, Koga Y, Tsuda M, Inoue K (2009) Activation of P2X7 receptors induces CCL3 production in microglial cells through transcription factor NFAT. J Neurochem 108:115–125PubMedCrossRef

49.

Sharp AJ, Polak PE, Simonini V, Lin SX, Richardson JC, Bongarzone ER, Feinstein DL (2008) P2X7 deficiency suppresses development of experimental autoimmune encephalomyelitis. J Neuroinflamm 8:5–33

50.

Bernardino L, Balosso S, Ravizza T, Marchi N, Ku G, Randle JC, Malva JO, Vezzani A (2008) Inflammatory events in hippocampal slice cultures prime neuronal susceptibility to excitotoxic injury: a crucial role of P2X7 receptor-mediated IL-1beta release. J Neurochem 106:271–280PubMedCrossRef

51.

Monif M, Reid CA, Powell KL, Smart ML, Williams DA (2009) The P2X7 receptor drives microglial activation and proliferation: a trophic role for P2X7R pore. J Neurosci 29:3781–3791PubMedCrossRef

52.

Rappold PM, Lynd-Balta E, Joseph SA (2006) P2X7 receptor immunoreactive profile confined to resting and activated microglia in the epileptic brain. Brain Res 1089:171–178PubMedCrossRef

Title: The roles of P2X7 receptor in regional-specific microglial responses in the rat brain following status epilepticus
Authors: Hea Kyung Choi
Hea Jin Ryu
Ji-Eun Kim
Seung-Mook Jo
Hui-Chul Choi
Hong-Ki Song
Tae-Cheon Kang
Publication date: 01-06-2012
Publisher: Springer Milan
Published in: Neurological Sciences / Issue 3/2012
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-011-0740-z

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The roles of P2X7 receptor in regional-specific microglial responses in the rat brain following status epilepticus

Abstract

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Abstract

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