Skip to main content
Erschienen in: Journal of Neural Transmission 12/2016

04.06.2016 | Translational Neurosciences - Review Article

Astrocytic and microglial nicotinic acetylcholine receptors: an overlooked issue in Alzheimer’s disease

verfasst von: Saeed Sadigh-Eteghad, Alireza Majdi, Javad Mahmoudi, Samad E. J. Golzari, Mahnaz Talebi

Erschienen in: Journal of Neural Transmission | Ausgabe 12/2016

Einloggen, um Zugang zu erhalten

Abstract

It is increasingly recognized that astrocytes and microglia-associated dysfunction contribute to AD pathology. In addition, glial nicotinic acetylcholine receptors (nAChRs) play a role in AD-related phenomena, such as neuron survival, synaptic plasticity, and memory. From mechanistic point of view, the glial regulation of pro-inflammatory cytokines, as common contributors in AD, is modulated by nAChRs. Astrocytic and microglial nAChRs contribute to Aβ metabolism, including Aβ phagocytosis and degradation as well as Aβ-related oxidative stress and neurotoxicity. These receptors are also involved in neurotransmission and gliotransmission through indirect interaction with N-Methyl-d-aspartate (NMDA) and a-amino-3-hydroxy-5-methyl-4 isoxazolepropionic acid (AMPA) receptors as well as gamma-aminobutyric acid (GABA) and intracellular calcium regulation. In addition, glial nAChRs participate in trophic factors-induced neuroprotection. This review gathers the most recent advances along with the previous data on astrocytic and microglial nAChRs role in AD pathogenesis.
Literatur
Zurück zum Zitat Agostinho P, Cunha RA, Oliveira C (2010) Neuroinflammation, oxidative stress and the pathogenesis of Alzheimer’s disease. Curr Pharm Des 16:2766–2778CrossRefPubMed Agostinho P, Cunha RA, Oliveira C (2010) Neuroinflammation, oxidative stress and the pathogenesis of Alzheimer’s disease. Curr Pharm Des 16:2766–2778CrossRefPubMed
Zurück zum Zitat Allen NJ, Barres BA (2009) Neuroscience: glia—more than just brain glue. Nature 457:675–677CrossRefPubMed Allen NJ, Barres BA (2009) Neuroscience: glia—more than just brain glue. Nature 457:675–677CrossRefPubMed
Zurück zum Zitat Banerjee J, Alkondon M, Pereira EF, Albuquerque EX (2012) Regulation of GABAergic inputs to CA1 pyramidal neurons by nicotinic receptors and kynurenic acid. J Pharmacol Exp Ther 341:500–509CrossRefPubMedPubMedCentral Banerjee J, Alkondon M, Pereira EF, Albuquerque EX (2012) Regulation of GABAergic inputs to CA1 pyramidal neurons by nicotinic receptors and kynurenic acid. J Pharmacol Exp Ther 341:500–509CrossRefPubMedPubMedCentral
Zurück zum Zitat Beggiato S, Antonelli T, Tomasini MC, Tanganelli S, Fuxe K, Schwarcz R, Ferraro L (2013) Kynurenic acid, by targeting alpha7 nicotinic acetylcholine receptors, modulates extracellular GABA levels in the rat striatum in vivo. Eur J Neurosci 37:1470–1477. doi:10.1111/ejn.12160 CrossRefPubMed Beggiato S, Antonelli T, Tomasini MC, Tanganelli S, Fuxe K, Schwarcz R, Ferraro L (2013) Kynurenic acid, by targeting alpha7 nicotinic acetylcholine receptors, modulates extracellular GABA levels in the rat striatum in vivo. Eur J Neurosci 37:1470–1477. doi:10.​1111/​ejn.​12160 CrossRefPubMed
Zurück zum Zitat Brawek B, Garaschuk O (2013) Microglial calcium signaling in the adult, aged and diseased brain. Cell Calcium 53:159–169CrossRefPubMed Brawek B, Garaschuk O (2013) Microglial calcium signaling in the adult, aged and diseased brain. Cell Calcium 53:159–169CrossRefPubMed
Zurück zum Zitat Dani JW, Chernjavsky A, Smith SJ (1992) Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8:429–440CrossRefPubMed Dani JW, Chernjavsky A, Smith SJ (1992) Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8:429–440CrossRefPubMed
Zurück zum Zitat De Simone R, Ajmone-Cat MA, Carnevale D, Minghetti L (2005) Activation of α7 nicotinic acetylcholine receptor by nicotine selectively up-regulates cyclooxygenase-2 and prostaglandin E2 in rat microglial cultures. J Neuroinflammation 2:4CrossRefPubMedPubMedCentral De Simone R, Ajmone-Cat MA, Carnevale D, Minghetti L (2005) Activation of α7 nicotinic acetylcholine receptor by nicotine selectively up-regulates cyclooxygenase-2 and prostaglandin E2 in rat microglial cultures. J Neuroinflammation 2:4CrossRefPubMedPubMedCentral
Zurück zum Zitat Della Bianca V, Dusi S, Bianchini E, Dal Prà I, Rossi F (1999) β-Amyloid Activates the O-2 Forming NADPH Oxidase in Microglia, Monocytes, and neutrophils A possible inflammatory mechanism of neuronal damage in Alzheimer’s disease. J Biol Chem 274:15493–15499CrossRef Della Bianca V, Dusi S, Bianchini E, Dal Prà I, Rossi F (1999) β-Amyloid Activates the O-2 Forming NADPH Oxidase in Microglia, Monocytes, and neutrophils A possible inflammatory mechanism of neuronal damage in Alzheimer’s disease. J Biol Chem 274:15493–15499CrossRef
Zurück zum Zitat Depino AM et al (2003) Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson’s disease. Eur J Neurosci 18:2731–2742CrossRefPubMed Depino AM et al (2003) Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson’s disease. Eur J Neurosci 18:2731–2742CrossRefPubMed
Zurück zum Zitat Dorey E, Chang N, Liu QY, Yang Z, Zhang W (2014) Apolipoprotein E, amyloid-beta, and neuroinflammation in Alzheimer’s disease. Neurosci Bull 30:317–330CrossRefPubMed Dorey E, Chang N, Liu QY, Yang Z, Zhang W (2014) Apolipoprotein E, amyloid-beta, and neuroinflammation in Alzheimer’s disease. Neurosci Bull 30:317–330CrossRefPubMed
Zurück zum Zitat Eikelenboom P, Veerhuis R, Scheper W, Rozemuller A, Van Gool W, Hoozemans J (2006) The significance of neuroinflammation in understanding Alzheimer’s disease. J Neural Transm 113:1685–1695CrossRefPubMed Eikelenboom P, Veerhuis R, Scheper W, Rozemuller A, Van Gool W, Hoozemans J (2006) The significance of neuroinflammation in understanding Alzheimer’s disease. J Neural Transm 113:1685–1695CrossRefPubMed
Zurück zum Zitat Filipcik P, Cente M, Ferencik M, Hulin I, Novak M (2006) The role of oxidative stress in the pathogenesis of Alzheimer’s disease. Bratislavske lekarske listy 107:384–394PubMed Filipcik P, Cente M, Ferencik M, Hulin I, Novak M (2006) The role of oxidative stress in the pathogenesis of Alzheimer’s disease. Bratislavske lekarske listy 107:384–394PubMed
Zurück zum Zitat Gordon GR, Iremonger KJ, Kantevari S, Ellis-Davies GC, MacVicar BA, Bains JS (2009) Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 64:391–403CrossRefPubMedPubMedCentral Gordon GR, Iremonger KJ, Kantevari S, Ellis-Davies GC, MacVicar BA, Bains JS (2009) Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 64:391–403CrossRefPubMedPubMedCentral
Zurück zum Zitat Gozzelino R, Jeney V, Soares MP (2010) Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 50:323–354CrossRefPubMed Gozzelino R, Jeney V, Soares MP (2010) Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 50:323–354CrossRefPubMed
Zurück zum Zitat Gu Z, Lamb PW, Yakel JL (2012) Cholinergic coordination of presynaptic and postsynaptic activity induces timing-dependent hippocampal synaptic plasticity. J Neurosci 32:12337–12348CrossRefPubMedPubMedCentral Gu Z, Lamb PW, Yakel JL (2012) Cholinergic coordination of presynaptic and postsynaptic activity induces timing-dependent hippocampal synaptic plasticity. J Neurosci 32:12337–12348CrossRefPubMedPubMedCentral
Zurück zum Zitat Guan Y-Z et al (2015) Nicotine inhibits microglial proliferation and is neuroprotective in global ischemia rats. Mol Neurobiol 51:1480–1488CrossRefPubMed Guan Y-Z et al (2015) Nicotine inhibits microglial proliferation and is neuroprotective in global ischemia rats. Mol Neurobiol 51:1480–1488CrossRefPubMed
Zurück zum Zitat Hensley K (2010) Neuroinflammation in Alzheimer’s disease: mechanisms, pathologic consequences, and potential for therapeutic manipulation. J Alzheimer’s Dis JAD 21:1–14. doi:10.3233/JAD-2010-1414 PubMed Hensley K (2010) Neuroinflammation in Alzheimer’s disease: mechanisms, pathologic consequences, and potential for therapeutic manipulation. J Alzheimer’s Dis JAD 21:1–14. doi:10.​3233/​JAD-2010-1414 PubMed
Zurück zum Zitat Hilmas C, Pereira E, Alkondon M, Rassoulpour A, Schwarcz R, Albuquerque E (2001) The brain metabolite kynurenic acid inhibits α7 nicotinic receptor expression: physiopathological implications. J Neurosci 21:7463–7473PubMed Hilmas C, Pereira E, Alkondon M, Rassoulpour A, Schwarcz R, Albuquerque E (2001) The brain metabolite kynurenic acid inhibits α7 nicotinic receptor expression: physiopathological implications. J Neurosci 21:7463–7473PubMed
Zurück zum Zitat Hua S, Ek CJ, Mallard C, Johansson ME (2014) Perinatal hypoxia-ischemia reduces α7 nicotinic receptor expression and selective α7 nicotinic receptor stimulation suppresses inflammation and promotes microglial mox phenotype. Biomed Res Int Hua S, Ek CJ, Mallard C, Johansson ME (2014) Perinatal hypoxia-ischemia reduces α7 nicotinic receptor expression and selective α7 nicotinic receptor stimulation suppresses inflammation and promotes microglial mox phenotype. Biomed Res Int
Zurück zum Zitat Hung J, Chansard M, Ousman SS, Nguyen MD, Colicos MA (2010) Activation of microglia by neuronal activity: results from a new in vitro paradigm based on neuronal-silicon interfacing technology. Brain Behav Immun 24:31–40CrossRefPubMed Hung J, Chansard M, Ousman SS, Nguyen MD, Colicos MA (2010) Activation of microglia by neuronal activity: results from a new in vitro paradigm based on neuronal-silicon interfacing technology. Brain Behav Immun 24:31–40CrossRefPubMed
Zurück zum Zitat Jo S et al (2014) GABA from reactive astrocytes impairs memory in mouse models of Alzheimer’s disease. Nat Med 20:886–896CrossRefPubMed Jo S et al (2014) GABA from reactive astrocytes impairs memory in mouse models of Alzheimer’s disease. Nat Med 20:886–896CrossRefPubMed
Zurück zum Zitat Kalashnyk O, Lykhmus O, Oliinyk O, Komisarenko S, Skok M (2014) α7 Nicotinic acetylcholine receptor-specific antibody stimulates interleukin-6 production in human astrocytes through p38-dependent pathway. Int Immunopharmacol 23:475–479CrossRefPubMed Kalashnyk O, Lykhmus O, Oliinyk O, Komisarenko S, Skok M (2014) α7 Nicotinic acetylcholine receptor-specific antibody stimulates interleukin-6 production in human astrocytes through p38-dependent pathway. Int Immunopharmacol 23:475–479CrossRefPubMed
Zurück zum Zitat Kamynina AV, Holmström KM, Koroev DO, Volpina OM, Abramov AY (2013) Acetylcholine and antibodies against the acetylcholine receptor protect neurons and astrocytes against beta-amyloid toxicity. Int J Biochem Cell Biol 45:899–907CrossRefPubMedPubMedCentral Kamynina AV, Holmström KM, Koroev DO, Volpina OM, Abramov AY (2013) Acetylcholine and antibodies against the acetylcholine receptor protect neurons and astrocytes against beta-amyloid toxicity. Int J Biochem Cell Biol 45:899–907CrossRefPubMedPubMedCentral
Zurück zum Zitat Kettenmann H, Hanisch U-K, Noda M, Verkhratsky A (2011) Physiol Microglia Physiol Rev 91:461–553CrossRefPubMed Kettenmann H, Hanisch U-K, Noda M, Verkhratsky A (2011) Physiol Microglia Physiol Rev 91:461–553CrossRefPubMed
Zurück zum Zitat Kim EJ, Kwon KJ, Park JY, Lee SH, Moon CH, Baik EJ (2002) Neuroprotective effects of prostaglandin E2 or cAMP against microglial and neuronal free radical mediated toxicity associated with inflammation. J Neurosci Res 70:97–107CrossRefPubMed Kim EJ, Kwon KJ, Park JY, Lee SH, Moon CH, Baik EJ (2002) Neuroprotective effects of prostaglandin E2 or cAMP against microglial and neuronal free radical mediated toxicity associated with inflammation. J Neurosci Res 70:97–107CrossRefPubMed
Zurück zum Zitat Kim SY, Moon JH, Lee HG, Kim SU, Lee YB (2007) ATP released from β-amyloid-stimulated microglia induces reactive oxygen species production in an autocrine fashion. Exp Mol Med 39:820–827CrossRefPubMed Kim SY, Moon JH, Lee HG, Kim SU, Lee YB (2007) ATP released from β-amyloid-stimulated microglia induces reactive oxygen species production in an autocrine fashion. Exp Mol Med 39:820–827CrossRefPubMed
Zurück zum Zitat Konishi Y, Yang L-B, He P, Lindholm K, Lu B, Li R, Shen Y (2014) Deficiency of GDNF receptor GFRα1 in Alzheimer’s neurons results in neuronal death. J Neurosci Res 34:13127–13138 Konishi Y, Yang L-B, He P, Lindholm K, Lu B, Li R, Shen Y (2014) Deficiency of GDNF receptor GFRα1 in Alzheimer’s neurons results in neuronal death. J Neurosci Res 34:13127–13138
Zurück zum Zitat Lalo U, Pankratov Y, Parpura V, Verkhratsky A (2011) Ionotropic receptors in neuronal–astroglial signalling: what is the role of “excitable” molecules in non-excitable cells (BBA). Mol Cell Res 1813:992–1002 Lalo U, Pankratov Y, Parpura V, Verkhratsky A (2011) Ionotropic receptors in neuronal–astroglial signalling: what is the role of “excitable” molecules in non-excitable cells (BBA). Mol Cell Res 1813:992–1002
Zurück zum Zitat Laudenbach V, Medja F, Zoli M, Rossi FM, Evrard P, Changeux J-P, Gressens P (2002) Selective activation of central subtypes of the nicotinic acetylcholine receptor has opposite effects on neonatal excitotoxic brain injuries. FASEB J 16:423–425PubMed Laudenbach V, Medja F, Zoli M, Rossi FM, Evrard P, Changeux J-P, Gressens P (2002) Selective activation of central subtypes of the nicotinic acetylcholine receptor has opposite effects on neonatal excitotoxic brain injuries. FASEB J 16:423–425PubMed
Zurück zum Zitat Lee M (2013) Neurotransmitters and microglial-mediated neuroinflammation. Curr Protein Pept Sci 14:21–32CrossRefPubMed Lee M (2013) Neurotransmitters and microglial-mediated neuroinflammation. Curr Protein Pept Sci 14:21–32CrossRefPubMed
Zurück zum Zitat Lee L, Kosuri P, Arancio O (2014) Picomolar amyloid-beta peptides enhance spontaneous astrocyte calcium transients. J Alzheimer’s Dis JAD 38:49–62. doi:10.3233/JAD-130740 PubMed Lee L, Kosuri P, Arancio O (2014) Picomolar amyloid-beta peptides enhance spontaneous astrocyte calcium transients. J Alzheimer’s Dis JAD 38:49–62. doi:10.​3233/​JAD-130740 PubMed
Zurück zum Zitat Levi G, Minghetti L, Aloisi F (1998) Regulation of prostanoid synthesis in microglial cells and effects of prostaglandin E2 on microglial functions. Biochimie 80:899–904CrossRefPubMed Levi G, Minghetti L, Aloisi F (1998) Regulation of prostanoid synthesis in microglial cells and effects of prostaglandin E2 on microglial functions. Biochimie 80:899–904CrossRefPubMed
Zurück zum Zitat Li S, Jin M, Koeglsperger T, Shepardson NE, Shankar GM, Selkoe DJ (2011) Soluble Abeta oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J Neurosci Off J Soc Neurosci 31:6627–6638. doi:10.1523/JNEUROSCI.0203-11.2011 CrossRef Li S, Jin M, Koeglsperger T, Shepardson NE, Shankar GM, Selkoe DJ (2011) Soluble Abeta oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J Neurosci Off J Soc Neurosci 31:6627–6638. doi:10.​1523/​JNEUROSCI.​0203-11.​2011 CrossRef
Zurück zum Zitat Li Z, Cao J, Ren X, Zhao Q, Zhou M, Zang W (2013) Nicotine protects dopaminergic neurons against lipopolysaccharide-induced damage through a7 nAChRs in microglia. Life Sci J 10 Li Z, Cao J, Ren X, Zhao Q, Zhou M, Zang W (2013) Nicotine protects dopaminergic neurons against lipopolysaccharide-induced damage through a7 nAChRs in microglia. Life Sci J 10
Zurück zum Zitat Liu Y et al (2012) α7 nicotinic acetylcholine receptor-mediated neuroprotection against dopaminergic neuron loss in an MPTP mouse model via inhibition of astrocyte activation. J Neuroinflammation 9:2094–2099 Liu Y et al (2012) α7 nicotinic acetylcholine receptor-mediated neuroprotection against dopaminergic neuron loss in an MPTP mouse model via inhibition of astrocyte activation. J Neuroinflammation 9:2094–2099
Zurück zum Zitat Liu Y et al (2015) Activation of α7 nicotinic acetylcholine receptors protects astrocytes against oxidative stress-induced apoptosis: implications for Parkinson’s disease. Neuropharmacology 91:87–96CrossRefPubMed Liu Y et al (2015) Activation of α7 nicotinic acetylcholine receptors protects astrocytes against oxidative stress-induced apoptosis: implications for Parkinson’s disease. Neuropharmacology 91:87–96CrossRefPubMed
Zurück zum Zitat Lopes C, Pereira EF, Wu H-Q, Purushottamachar P, Njar V, Schwarcz R, Albuquerque EX (2007) Competitive antagonism between the nicotinic allosteric potentiating ligand galantamine and kynurenic acid at α7 nicotinic receptors. J Pharmacol Exp Ther 322:48–58CrossRefPubMed Lopes C, Pereira EF, Wu H-Q, Purushottamachar P, Njar V, Schwarcz R, Albuquerque EX (2007) Competitive antagonism between the nicotinic allosteric potentiating ligand galantamine and kynurenic acid at α7 nicotinic receptors. J Pharmacol Exp Ther 322:48–58CrossRefPubMed
Zurück zum Zitat Lozada AF, Wang X, Gounko NV, Massey KA, Duan J, Liu Z, Berg DK (2012) Glutamatergic synapse formation is promoted by α7-containing nicotinic acetylcholine receptors. J Neurosci 32:7651–7661CrossRefPubMedPubMedCentral Lozada AF, Wang X, Gounko NV, Massey KA, Duan J, Liu Z, Berg DK (2012) Glutamatergic synapse formation is promoted by α7-containing nicotinic acetylcholine receptors. J Neurosci 32:7651–7661CrossRefPubMedPubMedCentral
Zurück zum Zitat Lutz JA, Kulshrestha M, Rogers DT, Littleton JM (2014) A nicotinic receptor-mediated anti-inflammatory effect of the flavonoid rhamnetin in BV2 microglia. Fitoterapia 98:11–21CrossRefPubMedPubMedCentral Lutz JA, Kulshrestha M, Rogers DT, Littleton JM (2014) A nicotinic receptor-mediated anti-inflammatory effect of the flavonoid rhamnetin in BV2 microglia. Fitoterapia 98:11–21CrossRefPubMedPubMedCentral
Zurück zum Zitat Mashimo M, Okubo Y, Yamazawa T, Yamasaki M, Watanabe M, Murayama T, Iino M (2010) Inositol 1, 4, 5-trisphosphate signaling maintains the activity of glutamate uptake in Bergmann glia. Eur J Neurosci 32:1668–1677CrossRefPubMed Mashimo M, Okubo Y, Yamazawa T, Yamasaki M, Watanabe M, Murayama T, Iino M (2010) Inositol 1, 4, 5-trisphosphate signaling maintains the activity of glutamate uptake in Bergmann glia. Eur J Neurosci 32:1668–1677CrossRefPubMed
Zurück zum Zitat Mencel M, Nash M, Jacobson C (2013) Neuregulin upregulates microglial α7 nicotinic acetylcholine receptor expression in immortalized cell lines: implications for regulating neuroinflammation. PLoS One 8:e70338CrossRefPubMedPubMedCentral Mencel M, Nash M, Jacobson C (2013) Neuregulin upregulates microglial α7 nicotinic acetylcholine receptor expression in immortalized cell lines: implications for regulating neuroinflammation. PLoS One 8:e70338CrossRefPubMedPubMedCentral
Zurück zum Zitat Moon JH, Kim SY, Lee HG, Kim SU, Lee YB (2008) Activation of nicotinic acetylcholine receptor prevents the production of reactive oxygen species in fibrillar β amyloid peptide (1-42)-stimulated microglia. Exp Mol Med 40:11–18CrossRefPubMedPubMedCentral Moon JH, Kim SY, Lee HG, Kim SU, Lee YB (2008) Activation of nicotinic acetylcholine receptor prevents the production of reactive oxygen species in fibrillar β amyloid peptide (1-42)-stimulated microglia. Exp Mol Med 40:11–18CrossRefPubMedPubMedCentral
Zurück zum Zitat Morioka N et al (2014) Primary cultures of rat cortical microglia treated with nicotine increases in the expression of excitatory amino acid transporter 1 (GLAST) via the activation of the α7 nicotinic acetylcholine receptor. Neuroscience 258:374–384CrossRefPubMed Morioka N et al (2014) Primary cultures of rat cortical microglia treated with nicotine increases in the expression of excitatory amino acid transporter 1 (GLAST) via the activation of the α7 nicotinic acetylcholine receptor. Neuroscience 258:374–384CrossRefPubMed
Zurück zum Zitat Nagele RG, D’Andrea MR, Lee H, Venkataraman V, Wang HY (2003) Astrocytes accumulate A beta 42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains. Brain Res 971:197–209CrossRefPubMed Nagele RG, D’Andrea MR, Lee H, Venkataraman V, Wang HY (2003) Astrocytes accumulate A beta 42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains. Brain Res 971:197–209CrossRefPubMed
Zurück zum Zitat Navarrete M, Perea G, de Sevilla DF, Gómez-Gonzalo M, Núñez A, Martín ED, Araque A (2012) Astrocytes mediate in vivo cholinergic-induced synaptic plasticity. PLoS Biol 10:e1001259CrossRefPubMedPubMedCentral Navarrete M, Perea G, de Sevilla DF, Gómez-Gonzalo M, Núñez A, Martín ED, Araque A (2012) Astrocytes mediate in vivo cholinergic-induced synaptic plasticity. PLoS Biol 10:e1001259CrossRefPubMedPubMedCentral
Zurück zum Zitat Niranjan R, Nath C, Shukla R (2012) Melatonin attenuated mediators of neuroinflammation and alpha-7 nicotinic acetylcholine receptor mRNA expression in lipopolysaccharide (LPS) stimulated rat astrocytoma cells, C6. Free Radic Res 46:1167–1177CrossRefPubMed Niranjan R, Nath C, Shukla R (2012) Melatonin attenuated mediators of neuroinflammation and alpha-7 nicotinic acetylcholine receptor mRNA expression in lipopolysaccharide (LPS) stimulated rat astrocytoma cells, C6. Free Radic Res 46:1167–1177CrossRefPubMed
Zurück zum Zitat Oikawa H, Nakamichi N, Kambe Y, Ogura M, Yoneda Y (2005) An increase in intracellular free calcium ions by nicotinic acetylcholine receptors in a single cultured rat cortical astrocyte. J Neurosci Res 79:535–544CrossRefPubMed Oikawa H, Nakamichi N, Kambe Y, Ogura M, Yoneda Y (2005) An increase in intracellular free calcium ions by nicotinic acetylcholine receptors in a single cultured rat cortical astrocyte. J Neurosci Res 79:535–544CrossRefPubMed
Zurück zum Zitat Oz M, E Lorke D, S Yang KH, Petroianu G (2013) On the interaction of β-amyloid peptides and α7-nicotinic acetylcholine receptors in Alzheimer’s disease. Curr Alzheimer Res 10:618–630CrossRefPubMed Oz M, E Lorke D, S Yang KH, Petroianu G (2013) On the interaction of β-amyloid peptides and α7-nicotinic acetylcholine receptors in Alzheimer’s disease. Curr Alzheimer Res 10:618–630CrossRefPubMed
Zurück zum Zitat Palop JJ, Mucke L (2010) Amyloid-[beta]-induced neuronal dysfunction in Alzheimer’s disease: from synapses toward neural networks. Nat Neurosci 13:812–818CrossRefPubMedPubMedCentral Palop JJ, Mucke L (2010) Amyloid-[beta]-induced neuronal dysfunction in Alzheimer’s disease: from synapses toward neural networks. Nat Neurosci 13:812–818CrossRefPubMedPubMedCentral
Zurück zum Zitat Parada E et al (2013) The microglial α7-acetylcholine nicotinic receptor is a key element in promoting neuroprotection by inducing heme oxygenase-1 via nuclear factor erythroid-2-related factor 2. Antioxid Redox Signal 19:1135–1148CrossRefPubMedPubMedCentral Parada E et al (2013) The microglial α7-acetylcholine nicotinic receptor is a key element in promoting neuroprotection by inducing heme oxygenase-1 via nuclear factor erythroid-2-related factor 2. Antioxid Redox Signal 19:1135–1148CrossRefPubMedPubMedCentral
Zurück zum Zitat Parpura V, Verkhratsky A (2012) Neuroglia at the crossroads of homoeostasis, metabolism and signalling: evolution of the concept ASN neuro 4:AN20120019 Parpura V, Verkhratsky A (2012) Neuroglia at the crossroads of homoeostasis, metabolism and signalling: evolution of the concept ASN neuro 4:AN20120019
Zurück zum Zitat Parri HR, Hernandez CM, Dineley KT (2011) Research update: Alpha7 nicotinic acetylcholine receptor mechanisms in Alzheimer’s disease. Biochem Pharmacol 82:931–942CrossRefPubMed Parri HR, Hernandez CM, Dineley KT (2011) Research update: Alpha7 nicotinic acetylcholine receptor mechanisms in Alzheimer’s disease. Biochem Pharmacol 82:931–942CrossRefPubMed
Zurück zum Zitat Perea G, Araque A (2005) Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 25:2192–2203CrossRefPubMed Perea G, Araque A (2005) Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J Neurosci 25:2192–2203CrossRefPubMed
Zurück zum Zitat Perea G, Sur M, Araque A (2014a) Neuron-glia networks: integral gear of brain function Perea G, Sur M, Araque A (2014a) Neuron-glia networks: integral gear of brain function
Zurück zum Zitat Perea G, Yang A, Boyden ES, Sur M (2014b) Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo. Nat Commun 5 Perea G, Yang A, Boyden ES, Sur M (2014b) Optogenetic astrocyte activation modulates response selectivity of visual cortex neurons in vivo. Nat Commun 5
Zurück zum Zitat Perez-Alvarez A, Araque A (2013) Astrocyte-neuron interaction at tripartite synapses. Curr Drug Targets 14:1220–1224CrossRefPubMed Perez-Alvarez A, Araque A (2013) Astrocyte-neuron interaction at tripartite synapses. Curr Drug Targets 14:1220–1224CrossRefPubMed
Zurück zum Zitat Pihlaja R, Koistinaho J, Malm T, Sikkila H, Vainio S, Koistinaho M (2008) Transplanted astrocytes internalize deposited beta-amyloid peptides in a transgenic mouse model of Alzheimer’s disease. Glia 56:154–163. doi:10.1002/glia.20599 CrossRefPubMed Pihlaja R, Koistinaho J, Malm T, Sikkila H, Vainio S, Koistinaho M (2008) Transplanted astrocytes internalize deposited beta-amyloid peptides in a transgenic mouse model of Alzheimer’s disease. Glia 56:154–163. doi:10.​1002/​glia.​20599 CrossRefPubMed
Zurück zum Zitat Pirttimaki TM et al (2013) α7 nicotinic receptor-mediated astrocytic gliotransmitter release: Aβ effects in a preclinical Alzheimer’s mouse model. PLoS One 8:e81828CrossRefPubMedPubMedCentral Pirttimaki TM et al (2013) α7 nicotinic receptor-mediated astrocytic gliotransmitter release: Aβ effects in a preclinical Alzheimer’s mouse model. PLoS One 8:e81828CrossRefPubMedPubMedCentral
Zurück zum Zitat Pocock JM, Kettenmann H (2007) Neurotransmitter receptors on microglia. Trends Neurosci 30:527–535CrossRefPubMed Pocock JM, Kettenmann H (2007) Neurotransmitter receptors on microglia. Trends Neurosci 30:527–535CrossRefPubMed
Zurück zum Zitat Pym L, Kemp M, Raymond-Delpech V, Buckingham S, Boyd C, Sattelle D (2005) Subtype-specific actions of β-amyloid peptides on recombinant human neuronal nicotinic acetylcholine receptors (α7, α4β2, α3β4) expressed in Xenopus laevis oocytes. Br J Pharmacol 146:964–971CrossRefPubMedPubMedCentral Pym L, Kemp M, Raymond-Delpech V, Buckingham S, Boyd C, Sattelle D (2005) Subtype-specific actions of β-amyloid peptides on recombinant human neuronal nicotinic acetylcholine receptors (α7, α4β2, α3β4) expressed in Xenopus laevis oocytes. Br J Pharmacol 146:964–971CrossRefPubMedPubMedCentral
Zurück zum Zitat Rocha SM, Cristovão AC, Campos FL, Fonseca CP, Baltazar G (2012) Astrocyte-derived GDNF is a potent inhibitor of microglial activation. Neurobiol Dis 47:407–415CrossRefPubMed Rocha SM, Cristovão AC, Campos FL, Fonseca CP, Baltazar G (2012) Astrocyte-derived GDNF is a potent inhibitor of microglial activation. Neurobiol Dis 47:407–415CrossRefPubMed
Zurück zum Zitat Sadigh-Eteghad S, Talebi M, Farhoudi M, Golzari SE, Sabermarouf B, Mahmoudi J (2014) Beta-amyloid exhibits antagonistic effects on alpha 7 nicotinic acetylcholine receptors in orchestrated manner. J Med Hypotheses Ideas 8:49–52 Sadigh-Eteghad S, Talebi M, Farhoudi M, Golzari SE, Sabermarouf B, Mahmoudi J (2014) Beta-amyloid exhibits antagonistic effects on alpha 7 nicotinic acetylcholine receptors in orchestrated manner. J Med Hypotheses Ideas 8:49–52
Zurück zum Zitat Sadigh-Eteghad S, Sabermarouf B, Majdi A, Talebi M, Farhoudi M, Mahmoudi J (2015b) Amyloid-beta: a crucial factor in Alzheimer’s disease. Med Princ Pract Int J Kuwait Univ Health Sci Centre 24:1–10. doi:10.1159/000369101 Sadigh-Eteghad S, Sabermarouf B, Majdi A, Talebi M, Farhoudi M, Mahmoudi J (2015b) Amyloid-beta: a crucial factor in Alzheimer’s disease. Med Princ Pract Int J Kuwait Univ Health Sci Centre 24:1–10. doi:10.​1159/​000369101
Zurück zum Zitat Sadigh-Eteghad S, Talebi M, Mahmoudi J, Babri S, Shanehbandi D (2015c) Selective activation of α 7 nicotinic acetylcholine receptor by PHA-543613 improves Aβ 25–35-mediated cognitive deficits in mice. Neuroscience 298:81–93CrossRefPubMed Sadigh-Eteghad S, Talebi M, Mahmoudi J, Babri S, Shanehbandi D (2015c) Selective activation of α 7 nicotinic acetylcholine receptor by PHA-543613 improves Aβ 25–35-mediated cognitive deficits in mice. Neuroscience 298:81–93CrossRefPubMed
Zurück zum Zitat Sanz-Blasco S, Piña-Crespo J, Talantova M, Lipton S (2010) Abeta-mediated glutamate release from astrocytes. Alzheimers Dement 6:S398CrossRef Sanz-Blasco S, Piña-Crespo J, Talantova M, Lipton S (2010) Abeta-mediated glutamate release from astrocytes. Alzheimers Dement 6:S398CrossRef
Zurück zum Zitat Seifert S, Pannell M, Uckert W, Färber K, Kettenmann H (2011) Transmitter-and hormone-activated Ca 2+ responses in adult microglia/brain macrophages in situ recorded after viral transduction of a recombinant Ca 2+ sensor. Cell Calcium 49:365–375CrossRefPubMed Seifert S, Pannell M, Uckert W, Färber K, Kettenmann H (2011) Transmitter-and hormone-activated Ca 2+ responses in adult microglia/brain macrophages in situ recorded after viral transduction of a recombinant Ca 2+ sensor. Cell Calcium 49:365–375CrossRefPubMed
Zurück zum Zitat Sharma G, Vijayaraghavan S (2001) Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc Natl Acad Sci 98:4148–4153CrossRefPubMedPubMedCentral Sharma G, Vijayaraghavan S (2001) Nicotinic cholinergic signaling in hippocampal astrocytes involves calcium-induced calcium release from intracellular stores. Proc Natl Acad Sci 98:4148–4153CrossRefPubMedPubMedCentral
Zurück zum Zitat Shteingauz A, Cohen E, Biala Y, Treinin M (2009) The BTB-MATH protein BATH-42 interacts with RIC-3 to regulate maturation of nicotinic acetylcholine receptors. J Cell Sci 122:807–812CrossRefPubMed Shteingauz A, Cohen E, Biala Y, Treinin M (2009) The BTB-MATH protein BATH-42 interacts with RIC-3 to regulate maturation of nicotinic acetylcholine receptors. J Cell Sci 122:807–812CrossRefPubMed
Zurück zum Zitat Shytle RD et al (2004) Cholinergic modulation of microglial activation by α7 nicotinic receptors. J Neurochem 89:337–343CrossRefPubMed Shytle RD et al (2004) Cholinergic modulation of microglial activation by α7 nicotinic receptors. J Neurochem 89:337–343CrossRefPubMed
Zurück zum Zitat Shytle D, Tah J, Sanberg P (2006) Cholinergic modulation of microglial activation via alpha-7 nicotinic receptors. Google Patents Shytle D, Tah J, Sanberg P (2006) Cholinergic modulation of microglial activation via alpha-7 nicotinic receptors. Google Patents
Zurück zum Zitat Silver J, Schwab ME, Popovich PG (2014) Central nervous system regenerative failure: role of oligodendrocytes, astrocytes, and microglia. Cold Spring Harbor Perspect Biol. doi:10.1101/cshperspect.a020602 Silver J, Schwab ME, Popovich PG (2014) Central nervous system regenerative failure: role of oligodendrocytes, astrocytes, and microglia. Cold Spring Harbor Perspect Biol. doi:10.​1101/​cshperspect.​a020602
Zurück zum Zitat Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119:7–35CrossRefPubMed Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119:7–35CrossRefPubMed
Zurück zum Zitat Sotelo C (2003) Viewing the brain through the master hand of Ramon y Cajal. Nat Rev Neurosci 4:71–77CrossRefPubMed Sotelo C (2003) Viewing the brain through the master hand of Ramon y Cajal. Nat Rev Neurosci 4:71–77CrossRefPubMed
Zurück zum Zitat Stahnisch FW, Bulloch AG (2011) Mihály (Michael von) Lenhossék (1863–1937). J Neurol 258:1901–1903CrossRefPubMed Stahnisch FW, Bulloch AG (2011) Mihály (Michael von) Lenhossék (1863–1937). J Neurol 258:1901–1903CrossRefPubMed
Zurück zum Zitat Straten G, Eschweiler GW, Maetzler W, Laske C, Leyhe T (2009) Glial cell-line derived neurotrophic factor (GDNF) concentrations in cerebrospinal fluid and serum of patients with early Alzheimer’s disease and normal controls. J Alzheimer’s Dis JAD 18:331–337PubMed Straten G, Eschweiler GW, Maetzler W, Laske C, Leyhe T (2009) Glial cell-line derived neurotrophic factor (GDNF) concentrations in cerebrospinal fluid and serum of patients with early Alzheimer’s disease and normal controls. J Alzheimer’s Dis JAD 18:331–337PubMed
Zurück zum Zitat Suzuki T et al (2006) Microglial α7 nicotinic acetylcholine receptors drive a phospholipase C/IP3 pathway and modulate the cell activation toward a neuroprotective role. J Neurosci Res 83:1461–1470CrossRefPubMed Suzuki T et al (2006) Microglial α7 nicotinic acetylcholine receptors drive a phospholipase C/IP3 pathway and modulate the cell activation toward a neuroprotective role. J Neurosci Res 83:1461–1470CrossRefPubMed
Zurück zum Zitat Takarada T et al (2012) Possible neuroprotective property of nicotinic acetylcholine receptors in association with predominant upregulation of glial cell line-derived neurotrophic factor in astrocytes. J Neurosci Res 90:2074–2085CrossRefPubMed Takarada T et al (2012) Possible neuroprotective property of nicotinic acetylcholine receptors in association with predominant upregulation of glial cell line-derived neurotrophic factor in astrocytes. J Neurosci Res 90:2074–2085CrossRefPubMed
Zurück zum Zitat Takata K et al (2010) Galantamine-induced amyloid-β clearance mediated via stimulation of microglial nicotinic acetylcholine receptors. J Biol Chem 285:40180–40191CrossRefPubMedPubMedCentral Takata K et al (2010) Galantamine-induced amyloid-β clearance mediated via stimulation of microglial nicotinic acetylcholine receptors. J Biol Chem 285:40180–40191CrossRefPubMedPubMedCentral
Zurück zum Zitat Teaktong T et al (2003) Alzheimer’s disease is associated with a selective increase in α7 nicotinic acetylcholine receptor immunoreactivity in astrocytes. Glia 41:207–211CrossRefPubMed Teaktong T et al (2003) Alzheimer’s disease is associated with a selective increase in α7 nicotinic acetylcholine receptor immunoreactivity in astrocytes. Glia 41:207–211CrossRefPubMed
Zurück zum Zitat Temburni MK, Jacob MH (2001) New functions for glia in the brain PANS 98:3631–3632 Temburni MK, Jacob MH (2001) New functions for glia in the brain PANS 98:3631–3632
Zurück zum Zitat Texidó L, Martín-Satué M, Alberdi E, Solsona C, Matute C (2011) Amyloid β peptide oligomers directly activate NMDA receptors. Cell Calcium 49:184–190CrossRefPubMed Texidó L, Martín-Satué M, Alberdi E, Solsona C, Matute C (2011) Amyloid β peptide oligomers directly activate NMDA receptors. Cell Calcium 49:184–190CrossRefPubMed
Zurück zum Zitat Tsvetkova D, Obreshkova D, Zheleva-Dimitrova D, Saso L (2013) Antioxidant activity of galantamine and some of its derivatives. Curr Med Chem 20:4595–4608CrossRefPubMed Tsvetkova D, Obreshkova D, Zheleva-Dimitrova D, Saso L (2013) Antioxidant activity of galantamine and some of its derivatives. Curr Med Chem 20:4595–4608CrossRefPubMed
Zurück zum Zitat Tuppo EE, Arias HR (2005) The role of inflammation in Alzheimer’s disease. Int J Biochem Cell Biol 37:289–305CrossRefPubMed Tuppo EE, Arias HR (2005) The role of inflammation in Alzheimer’s disease. Int J Biochem Cell Biol 37:289–305CrossRefPubMed
Zurück zum Zitat Vallés AS, Barrantes FJ (2012) Chaperoning α7 neuronal nicotinic acetylcholine receptors (BBA). Biomembranes 1818:718–729 Vallés AS, Barrantes FJ (2012) Chaperoning α7 neuronal nicotinic acetylcholine receptors (BBA). Biomembranes 1818:718–729
Zurück zum Zitat Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626–640CrossRefPubMed Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6:626–640CrossRefPubMed
Zurück zum Zitat Wang H et al (2003) Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation. Nature 421:384–388CrossRefPubMed Wang H et al (2003) Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation. Nature 421:384–388CrossRefPubMed
Zurück zum Zitat Wang X, Lippi G, Carlson DM, Berg DK (2013) Activation of α7-containing nicotinic receptors on astrocytes triggers AMPA receptor recruitment to glutamatergic synapses. J Neurochem 127:632–643CrossRefPubMedPubMedCentral Wang X, Lippi G, Carlson DM, Berg DK (2013) Activation of α7-containing nicotinic receptors on astrocytes triggers AMPA receptor recruitment to glutamatergic synapses. J Neurochem 127:632–643CrossRefPubMedPubMedCentral
Zurück zum Zitat Watters JJ, Pocock JM (2014) Microglial physiology. In: Microglia in health and disease. Springer, pp 47–79 Watters JJ, Pocock JM (2014) Microglial physiology. In: Microglia in health and disease. Springer, pp 47–79
Zurück zum Zitat Wessler I, Reinheimer T, Klapproth H, Schneider F-J, Racké K, Hammer R (1997) Mammalian glial cells in culture synthesize acetylcholine. Naunyn Schmiedebergs Arch Pharmacol 356:694–697CrossRefPubMed Wessler I, Reinheimer T, Klapproth H, Schneider F-J, Racké K, Hammer R (1997) Mammalian glial cells in culture synthesize acetylcholine. Naunyn Schmiedebergs Arch Pharmacol 356:694–697CrossRefPubMed
Zurück zum Zitat Wisniewski HM, Wegiel J (1991) Spatial relationships between astrocytes and classical plaque components. Neurobiol Aging 12:593–600CrossRefPubMed Wisniewski HM, Wegiel J (1991) Spatial relationships between astrocytes and classical plaque components. Neurobiol Aging 12:593–600CrossRefPubMed
Zurück zum Zitat Yu W-F, Guan Z-Z, Bogdanovic N, Nordberg A (2005a) High selective expression of α7 nicotinic receptors on astrocytes in the brains of patients with sporadic Alzheimer’s disease and patients carrying Swedish APP 670/671 mutation: a possible association with neuritic plaques. Exp Neurol 192:215–225CrossRefPubMed Yu W-F, Guan Z-Z, Bogdanovic N, Nordberg A (2005a) High selective expression of α7 nicotinic receptors on astrocytes in the brains of patients with sporadic Alzheimer’s disease and patients carrying Swedish APP 670/671 mutation: a possible association with neuritic plaques. Exp Neurol 192:215–225CrossRefPubMed
Zurück zum Zitat Yu WF, Guan ZZ, Bogdanovic N, Nordberg A (2005b) High selective expression of alpha7 nicotinic receptors on astrocytes in the brains of patients with sporadic Alzheimer’s disease and patients carrying Swedish APP 670/671 mutation: a possible association with neuritic plaques. Exp Neurol 192:215–225. doi:10.1016/j.expneurol.2004.12.015 CrossRefPubMed Yu WF, Guan ZZ, Bogdanovic N, Nordberg A (2005b) High selective expression of alpha7 nicotinic receptors on astrocytes in the brains of patients with sporadic Alzheimer’s disease and patients carrying Swedish APP 670/671 mutation: a possible association with neuritic plaques. Exp Neurol 192:215–225. doi:10.​1016/​j.​expneurol.​2004.​12.​015 CrossRefPubMed
Zurück zum Zitat Yu W, Mechawar N, Krantic S, Chabot J-G, Quirion R (2012) Upregulation of astrocytic α7 nicotinic receptors in Alzheimer’s disease brain-possible relevant to amyloid pathology. Mol Neurodegener. doi:10.1186/1750-1326-7-S1-O7 PubMed Yu W, Mechawar N, Krantic S, Chabot J-G, Quirion R (2012) Upregulation of astrocytic α7 nicotinic receptors in Alzheimer’s disease brain-possible relevant to amyloid pathology. Mol Neurodegener. doi:10.​1186/​1750-1326-7-S1-O7 PubMed
Zurück zum Zitat Zhang J, Rivest S (2001) Anti-inflammatory effects of prostaglandin E2 in the central nervous system in response to brain injury and circulating lipopolysaccharide. J Neurochem 76:855–864CrossRefPubMed Zhang J, Rivest S (2001) Anti-inflammatory effects of prostaglandin E2 in the central nervous system in response to brain injury and circulating lipopolysaccharide. J Neurochem 76:855–864CrossRefPubMed
Metadaten
Titel
Astrocytic and microglial nicotinic acetylcholine receptors: an overlooked issue in Alzheimer’s disease
verfasst von
Saeed Sadigh-Eteghad
Alireza Majdi
Javad Mahmoudi
Samad E. J. Golzari
Mahnaz Talebi
Publikationsdatum
04.06.2016
Verlag
Springer Vienna
Erschienen in
Journal of Neural Transmission / Ausgabe 12/2016
Print ISSN: 0300-9564
Elektronische ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-016-1580-z

Weitere Artikel der Ausgabe 12/2016

Journal of Neural Transmission 12/2016 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.