Crosstalk Among Disrupted Glutamatergic and Cholinergic Homeostasis and Inflammatory Response in Mechanisms Elicited by Proline in Astrocytes
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  • 作者:Samanta Oliveira Loureiro ; Daniele Susana Volkart Sidegum…
  • 关键词:Proline ; Astrocyte ; Glutamate ; Inflammation ; Cholinergic system ; Acetylcholine ; Acetylcholinesterase ; Cytokine mediators ; TNF ; α ; IL ; ; IL ; 6 ; Excitotoxicity ; Glutamine synthetase
  • 刊名:Molecular Neurobiology
  • 出版年:2016
  • 出版时间:March 2016
  • 年:2016
  • 卷:53
  • 期:2
  • 页码:1065-1079
  • 全文大小:757 KB
  • 参考文献:1.Angulo MC, Le Meur K, Kozlov AS, Charpak S, Audinat E (2008) GABA, a forgotten gliotransmitter. Prog Neurobiol 86(3):297–303. doi:10.​1016/​j.​pneurobio.​2008.​08.​002 PubMed CrossRef
    2.Bergersen LH, Gundersen V (2009) Morphological evidence for vesicular glutamate release from astrocytes. Neuroscience 158(1):260–265. doi:10.​1016/​j.​neuroscience.​2008.​03.​074 PubMed CrossRef
    3.Halassa MM, Haydon PG (2010) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu Rev Physiol 72:335–355. doi:10.​1146/​annurev-physiol-021909-135843 PubMedCentral PubMed CrossRef
    4.Perea G, Araque A (2010) GLIA modulates synaptic transmission. Brain Res Rev 63(1–2):93–102. doi:10.​1016/​j.​brainresrev.​2009.​10.​005 PubMed CrossRef
    5.Parpura V, Verkhratsky A (2011) Homeostatic function of astrocytes: Ca(2+) and Na(+) signalling. Transl Neurosci 3(4):334–344. doi:10.​2478/​s13380-012-0040-y
    6.Gucek A, Vardjan N, Zorec R (2012) Exocytosis in astrocytes: transmitter release and membrane signal regulation. Neurochem Res 37(11):2351–2363. doi:10.​1007/​s11064-012-0773-6 PubMed CrossRef
    7.Zorec R, Araque A, Carmignoto G, Haydon PG, Verkhratsky A, Parpura V (2012) Astroglial excitability and gliotransmission: an appraisal of Ca2+ as a signalling route. ASN Neuro 4(2). doi:10.1042/AN20110061
    8.Bouzier-Sore AK, Pellerin L (2013) Unraveling the complex metabolic nature of astrocytes. Front Cell Neurosci 7:179. doi:10.​3389/​fncel.​2013.​00179 PubMedCentral PubMed CrossRef
    9.Krnjevic K (2004) How does a little acronym become a big transmitter? Biochem Pharmacol 68(8):1549–1555. doi:10.​1016/​j.​bcp.​2004.​06.​038 PubMed CrossRef
    10.Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65(1):1–105PubMed CrossRef
    11.Grewer C, Rauen T (2005) Electrogenic glutamate transporters in the CNS: molecular mechanism, pre-steady-state kinetics, and their impact on synaptic signaling. J Membr Biol 203(1):1–20. doi:10.​1007/​s00232-004-0731-6 PubMedCentral PubMed CrossRef
    12.Tzingounis AV, Wadiche JI (2007) Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 8(12):935–947. doi:10.​1038/​nrn2274 PubMed CrossRef
    13.Leveille F, El Gaamouch F, Gouix E, Lecocq M, Lobner D, Nicole O, Buisson A (2008) Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J 22(12):4258–4271. doi:10.​1096/​fj.​08-107268 PubMed CrossRef
    14.Kaufman AM, Milnerwood AJ, Sepers MD, Coquinco A, She K, Wang L, Lee H, Craig AM, Cynader M, Raymond LA (2012) Opposing roles of synaptic and extrasynaptic NMDA receptor signaling in cocultured striatal and cortical neurons. J Neurosci 32(12):3992–4003. doi:10.​1523/​JNEUROSCI.​4129-11.​2012 PubMed CrossRef
    15.Zhou X, Hollern D, Liao J, Andrechek E, Wang H (2013) NMDA receptor-mediated excitotoxicity depends on the coactivation of synaptic and extrasynaptic receptors. Cell Death Dis 4:e560. doi:10.​1038/​cddis.​2013.​82 PubMedCentral PubMed CrossRef
    16.Logan WJ, Snyder SH (1971) Unique high affinity uptake systems for glycine, glutamic and aspartic acids in central nervous tissue of the rat. Nature 234(5327):297–299PubMed CrossRef
    17.Divito CB, Underhill SM (2014) Excitatory amino acid transporters: roles in glutamatergic neurotransmission. Neurochem Int 73C:172–180. doi:10.​1016/​j.​neuint.​2013.​12.​008 CrossRef
    18.Vandenberg RJ, Ryan RM (2013) Mechanisms of glutamate transport. Physiol Rev 93(4):1621–1657. doi:10.​1152/​physrev.​00007.​2013 PubMed CrossRef
    19.O'Shea RD (2002) Roles and regulation of glutamate transporters in the central nervous system. Clin Exp Pharmacol Physiol 29(11):1018–1023PubMed CrossRef
    20.Sheldon AL, Robinson MB (2007) The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem Int 51(6–7):333–355. doi:10.​1016/​j.​neuint.​2007.​03.​012 PubMedCentral PubMed CrossRef
    21.Maragakis NJ, Rothstein JD (2004) Glutamate transporters: animal models to neurologic disease. Neurobiol Dis 15(3):461–473. doi:10.​1016/​j.​nbd.​2003.​12.​007 PubMed CrossRef
    22.Zheng K, Scimemi A, Rusakov DA (2008) Receptor actions of synaptically released glutamate: the role of transporters on the scale from nanometers to microns. Biophys J 95(10):4584–4596. doi:10.​1529/​biophysj.​108.​129874 PubMedCentral PubMed CrossRef
    23.Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22(1):183–192PubMed
    24.Rose CF, Verkhratsky A, Parpura V (2013) Astrocyte glutamine synthetase: pivotal in health and disease. Biochem Soc Trans 41(6):1518–1524. doi:10.​1042/​BST20130237 PubMed CrossRef
    25.Albrecht J, Sidoryk-Wegrzynowicz M, Zielinska M, Aschner M (2010) Roles of glutamine in neurotransmission. Neuron Glia Biol 6(4):263–276. doi:10.​1017/​S1740925X1100009​3 PubMed CrossRef
    26.Bak LK, Schousboe A, Waagepetersen HS (2006) The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem 98(3):641–653. doi:10.​1111/​j.​1471-4159.​2006.​03913.​x PubMed CrossRef
    27.Tani H, Dulla CG, Farzampour Z, Taylor-Weiner A, Huguenard JR, Reimer RJ (2014) A local glutamate–glutamine cycle sustains synaptic excitatory transmitter release. Neuron 81(4):888–900. doi:10.​1016/​j.​neuron.​2013.​12.​026 PubMedCentral PubMed CrossRef
    28.Massucci FA, DiNuzzo M, Giove F, Maraviglia B, Castillo IP, Marinari E, De Martino A (2013) Energy metabolism and glutamate–glutamine cycle in the brain: a stoichiometric modeling perspective. BMC Syst Biol 7:103. doi:10.​1186/​1752-0509-7-103 PubMedCentral PubMed CrossRef
    29.Fulmer CG, VonDran MW, Stillman AA, Huang Y, Hempstead BL, Dreyfus CF (2014) Astrocyte-derived BDNF supports myelin protein synthesis after cuprizone-induced demyelination. J Neurosci 34(24):8186–8196. doi:10.​1523/​JNEUROSCI.​ 4267-13.​2014 PubMedCentral PubMed CrossRef
    30.Talaveron R, Matarredona ER, de la Cruz RR, Macias D, Galvez V, Pastor AM (2014) Implanted neural progenitor cells regulate glial reaction to brain injury and establish gap junctions with host glial cells. Glia 62(4):623–638. doi:10.​1002/​glia.​22630 PubMed CrossRef
    31.Martin JL, Magistretti PJ, Allaman I (2013) Regulation of neurotrophic factors and energy metabolism by antidepressants in astrocytes. Curr Drug Targets 14(11):1308–1321PubMed CrossRef
    32.Aronica E, Ravizza T, Zurolo E, Vezzani A (2012) Astrocyte immune responses in epilepsy. Glia 60(8):1258–1268. doi:10.​1002/​glia.​22312 PubMed CrossRef
    33.Hulshof S, Montagne L, De Groot CJ, Van Der Valk P (2002) Cellular localization and expression patterns of interleukin-10, interleukin-4, and their receptors in multiple sclerosis lesions. Glia 38(1):24–35. doi:10.​1002/​glia.​10050 PubMed CrossRef
    34.Friedman WJ (2001) Cytokines regulate expression of the type 1 interleukin-1 receptor in rat hippocampal neurons and glia. Exp Neurol 168(1):23–31. doi:10.​1006/​exnr.​2000.​7595 PubMed CrossRef
    35.Mason JL, Suzuki K, Chaplin DD, Matsushima GK (2001) Interleukin-1beta promotes repair of the CNS. J Neurosci 21(18):7046–7052PubMed
    36.Chen G, Park CK, Xie RG, Berta T, Nedergaard M, Ji RR (2014) Connexin-43 induces chemokine release from spinal cord astrocytes to maintain late-phase neuropathic pain in mice. Brain. doi:10.​1093/​brain/​awu140
    37.Almolda B, Villacampa N, Manders P, Hidalgo J, Campbell IL, Gonzalez B, Castellano B (2014) Effects of astrocyte-targeted production of interleukin-6 in the mouse on the host response to nerve injury. Glia 62(7):1142–1161. doi:10.​1002/​glia.​22668 PubMed CrossRef
    38.Ellrichmann G, Reick C, Saft C, Linker RA (2013) The role of the immune system in Huntington's disease. Clin Dev Immunol 2013:541259. doi:10.​1155/​2013/​541259 PubMedCentral PubMed CrossRef
    39.Rossi S, Furlan R, De Chiara V, Motta C, Studer V, Mori F, Musella A, Bergami A, Muzio L, Bernardi G, Battistini L, Martino G, Centonze D (2012) Interleukin-1beta causes synaptic hyperexcitability in multiple sclerosis. Ann Neurol 71(1):76–83. doi:10.​1002/​ana.​22512 PubMed CrossRef
    40.Zhang XM, Zhu J (2011) Kainic acid-induced neurotoxicity: targeting glial responses and glia-derived cytokines. Curr Neuropharmacol 9(2):388–398. doi:10.​2174/​1570159117955965​40 PubMedCentral PubMed CrossRef
    41.Pavlov VA, Parrish WR, Rosas-Ballina M, Ochani M, Puerta M, Ochani K, Chavan S, Al-Abed Y, Tracey KJ (2009) Brain acetylcholinesterase activity controls systemic cytokine levels through the cholinergic anti-inflammatory pathway. Brain Behav Immun 23(1):41–45. doi:10.​1016/​j.​bbi.​2008.​06.​011 PubMedCentral PubMed CrossRef
    42.Scherer EB, Loureiro SO, Vuaden FC, da Cunha AA, Schmitz F, Kolling J, Savio LE, Bogo MR, Bonan CD, Netto CA, Wyse AT (2014) Mild hyperhomocysteinemia increases brain acetylcholinesterase and proinflammatory cytokine levels in different tissues. Mol Neurobiol 50(2):589–596. doi:10.​1007/​s12035-014-8660-6 PubMed CrossRef
    43.Lindblom RP, Strom M, Heinig M, Al Nimer F, Aeinehband S, Berg A, Dominguez CA, Vijayaraghavan S, Zhang XM, Harnesk K, Zelano J, Hubner N, Cullheim S, Darreh-Shori T, Diez M, Piehl F (2014) Unbiased expression mapping identifies a link between the complement and cholinergic systems in the rat central nervous system. J Immunol 192(3):1138–1153. doi:10.​4049/​jimmunol.​1301233 PubMed CrossRef
    44.Darreh-Shori T, Vijayaraghavan S, Aeinehband S, Piehl F, Lindblom RP, Nilsson B, Ekdahl KN, Langstrom B, Almkvist O, Nordberg A (2013) Functional variability in butyrylcholinesterase activity regulates intrathecal cytokine and astroglial biomarker profiles in patients with Alzheimer's disease. Neurobiol Aging 34(11):2465–2481. doi:10.​1016/​j.​neurobiolaging.​2013.​04.​027 PubMed CrossRef
    45.Phang JM, Hu CA, Valle D (2001) Disorders of proline and hydroxyproline metabolism. In: Scriver CR, Sly WS, Valle D (eds) The metabolic and molecular bases of inherited disease. McGraw-Hill, New York, pp 1821–1838
    46.Mitsubuchi H, Nakamura K, Matsumoto S, Endo F (2008) Inborn errors of proline metabolism. J Nutr 138(10):2016S–2020SPubMed
    47.Wyse AT, Netto CA (2011) Behavioral and neurochemical effects of proline. Metab Brain Dis 26(3):159–172. doi:10.​1007/​s11011-011-9246-x PubMed CrossRef
    48.Di Rosa G, Nicotera AG, Lenzo P, Spano M, Tortorella G (2014) Long-term neuropsychiatric follow-up in hyperprolinemia type I. Psychiatr Genet. doi:10.​1097/​YPG.​0000000000000037​ PubMed
    49.Srivastava D, Singh RK, Moxley MA, Henzl MT, Becker DF, Tanner JJ (2012) The three-dimensional structural basis of type II hyperprolinemia. J Mol Biol 420(3):176–189. doi:10.​1016/​j.​jmb.​2012.​04.​010 PubMedCentral PubMed CrossRef
    50.Clelland JD, Read LL, Drouet V, Kaon A, Kelly A, Duff KE, Nadrich RH, Rajparia A, Clelland CL (2014) Vitamin D insufficiency and schizophrenia risk: evaluation of hyperprolinemia as a mediator of association. Schizophr Res 156(1):15–22. doi:10.​1016/​j.​schres.​2014.​03.​017 PubMedCentral PubMed CrossRef
    51.Clelland CL, Read LL, Baraldi AN, Bart CP, Pappas CA, Panek LJ, Nadrich RH, Clelland JD (2011) Evidence for association of hyperprolinemia with schizophrenia and a measure of clinical outcome. Schizophr Res 131(1–3):139–145. doi:10.​1016/​j.​schres.​2011.​05.​006 PubMedCentral PubMed CrossRef
    52.Jacquet H, Demily C, Houy E, Hecketsweiler B, Bou J, Raux G, Lerond J, Allio G, Haouzir S, Tillaux A, Bellegou C, Fouldrin G, Delamillieure P, Menard JF, Dollfus S, D'Amato T, Petit M, Thibaut F, Frebourg T, Campion D (2005) Hyperprolinemia is a risk factor for schizoaffective disorder. Mol Psychiatry 10(5):479–485. doi:10.​1038/​sj.​mp.​4001597 PubMed CrossRef
    53.Cohen SM, Nadler JV (1997) Proline-induced potentiation of glutamate transmission. Brain Res 761(2):271–282PubMed CrossRef
    54.Rhoads DE, Peterson NA, Raghupathy E (1983) Selective inhibition of synaptosomal proline uptake by leucine and methionine enkephalins. J Biol Chem 258(20):12233–12237PubMed
    55.Martin D, Ault B, Nadler JV (1992) NMDA receptor-mediated depolarizing action of proline on CA1 pyramidal cells. Eur J Pharmacol 219(1):59–66PubMed CrossRef
    56.Fremeau RT Jr, Caron MG, Blakely RD (1992) Molecular cloning and expression of a high affinity L-proline transporter expressed in putative glutamatergic pathways of rat brain. Neuron 8(5):915–926PubMed CrossRef
    57.Nadler JV, Bray SD, Evenson DA (1992) Autoradiographic localization of proline uptake in excitatory hippocampal pathways. Hippocampus 2(3):269–278. doi:10.​1002/​hipo.​450020306 PubMed CrossRef
    58.Nadler JV (1987) Sodium-dependent proline uptake in the rat hippocampal formation: association with ipsilateral–commissural projections of CA3 pyramidal cells. J Neurochem 49(4):1155–1160PubMed CrossRef
    59.Delwing D, Sanna RJ, Wofchuk S, Wyse AT (2007) Proline promotes decrease in glutamate uptake in slices of cerebral cortex and hippocampus of rats. Life Sci 81(25–26):1645–1650. doi:10.​1016/​j.​lfs.​2007.​09.​031 PubMed CrossRef
    60.Ferreira AG, da Cunha AA, Scherer EB, Machado FR, da Cunha MJ, Braga A, Mussulini BH, Moreira JD, Wofchuk S, Souza DO, Wyse AT (2012) Evidence that hyperprolinemia alters glutamatergic homeostasis in rat brain: neuroprotector effect of guanosine. Neurochem Res 37(1):205–213. doi:10.​1007/​s11064-011-0604-1 PubMed CrossRef
    61.Loureiro SO, Romao L, Alves T, Fonseca A, Heimfarth L, Moura Neto V, Wyse AT, Pessoa-Pureur R (2010) Homocysteine induces cytoskeletal remodeling and production of reactive oxygen species in cultured cortical astrocytes. Brain Res 1355:151–164. doi:10.​1016/​j.​brainres.​2010.​07.​071 PubMed CrossRef
    62.Henrotin YE, Labasse AH, Simonis PE, Zheng SX, Deby GP, Famaey JP, Crielaard JM, Reginster JY (1999) Effects of nimesulide and sodium diclofenac on interleukin-6, interleukin-8, proteoglycans and prostaglandin E2 production by human articular chondrocytes in vitro. Clin Exp Rheumatol 17(2):151–160PubMed
    63.Fahmi H, He Y, Zhang M, Martel-Pelletier J, Pelletier JP, Di Battista JA (2001) Nimesulide reduces interleukin-1beta-induced cyclooxygenase-2 gene expression in human synovial fibroblasts. Osteoarthr Cartil 9(4):332–340. doi:10.​1053/​joca.​2000.​0393 PubMed CrossRef
    64.Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95PubMed CrossRef
    65.Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMed CrossRef
    66.Frizzo ME, Lara DR, Dahm KC, Prokopiuk AS, Swanson RA, Souza DO (2001) Activation of glutamate uptake by guanosine in primary astrocyte cultures. Neuroreport 12(4):879–881PubMed CrossRef
    67.Petito CK, Chung MC, Verkhovsky LM, Cooper AJ (1992) Brain glutamine synthetase increases following cerebral ischemia in the rat. Brain Res 569(2):275–280PubMed CrossRef
    68.Schmidt AP, Tort AB, Silveira PP, Bohmer AE, Hansel G, Knorr L, Schallenberger C, Dalmaz C, Elisabetsky E, Crestana RH, Lara DR, Souza DO (2009) The NMDA antagonist MK-801 induces hyperalgesia and increases CSF excitatory amino acids in rats: reversal by guanosine. Pharmacol Biochem Behav 91(4):549–553. doi:10.​1016/​j.​pbb.​2008.​09.​009 PubMed CrossRef
    69.McKenna MC, Sonnewald U, Huang X, Stevenson J, Zielke HR (1996) Exogenous glutamate concentration regulates the metabolic fate of glutamate in astrocytes. J Neurochem 66(1):386–393PubMed CrossRef
    70.Ward RJ, Colivicchi MA, Allen R, Schol F, Lallemand F, de Witte P, Ballini C, Corte LD, Dexter D (2009) Neuro-inflammation induced in the hippocampus of 'binge drinking' rats may be mediated by elevated extracellular glutamate content. J Neurochem 111(5):1119–1128. doi:10.​1111/​j.​1471-4159.​2009.​06389.​x PubMed CrossRef
    71.Castillo J, Davalos A, Alvarez-Sabin J, Pumar JM, Leira R, Silva Y, Montaner J, Kase CS (2002) Molecular signatures of brain injury after intracerebral hemorrhage. Neurology 58(4):624–629PubMed CrossRef
    72.Ault B, Wang CM, Yawn BC (1987) L-Proline depolarizes rat spinal motoneurones by an excitatory amino acid antagonist-sensitive mechanism. Br J Pharmacol 92(2):319–326PubMedCentral PubMed CrossRef
    73.Nadler JV, Wang A, Hakim A (1988) Toxicity of L-proline toward rat hippocampal neurons. Brain Res 456(1):168–172PubMed CrossRef
    74.Henzi V, Reichling DB, Helm SW, MacDermott AB (1992) L-Proline activates glutamate and glycine receptors in cultured rat dorsal horn neurons. Mol Pharmacol 41(4):793–801PubMed
    75.Arrieta-Cruz I, Su Y, Knight CM, Lam TK, Gutierrez-Juarez R (2013) Evidence for a role of proline and hypothalamic astrocytes in the regulation of glucose metabolism in rats. Diabetes 62(4):1152–1158. doi:db12-0228[pii]10.​2337/​db12-0228
    76.Pellerin L (2003) Lactate as a pivotal element in neuron-glia metabolic cooperation. Neurochem Int 43(4–5):331–338PubMed CrossRef
    77.Liu W, Le A, Hancock C, Lane AN, Dang CV, Fan TW, Phang JM (2012) Reprogramming of proline and glutamine metabolism contributes to the proliferative and metabolic responses regulated by oncogenic transcription factor c-MYC. Proc Natl Acad Sci U S A 109(23):8983–8988. doi:10.​1073/​pnas.​1203244109 PubMedCentral PubMed CrossRef
    78.Van Harreveld A, Fifkova E (1973) Effects of amino acids on the isolated chicken retina, and on its response to glutamate stimulation. J Neurochem 20(4):947–962PubMed CrossRef
    79.During MJ, Spencer DD (1993) Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341(8861):1607–1610PubMed CrossRef
    80.Cavus I, Kasoff WS, Cassaday MP, Jacob R, Gueorguieva R, Sherwin RS, Krystal JH, Spencer DD, Abi-Saab WM (2005) Extracellular metabolites in the cortex and hippocampus of epileptic patients. Ann Neurol 57(2):226–235. doi:10.​1002/​ana.​20380 PubMed CrossRef
    81.Sibson NR, Mason GF, Shen J, Cline GW, Herskovits AZ, Wall JE, Behar KL, Rothman DL, Shulman RG (2001) In vivo (13)C NMR measurement of neurotransmitter glutamate cycling, anaplerosis and TCA cycle flux in rat brain during. J Neurochem 76(4):975–989PubMed CrossRef
    82.Mason GF, Gruetter R, Rothman DL, Behar KL, Shulman RG, Novotny EJ (1995) Simultaneous determination of the rates of the TCA cycle, glucose utilization, alpha-ketoglutarate/glutamate exchange, and glutamine synthesis in human brain by NMR. J Cereb Blood Flow Metab 15(1):12–25. doi:10.​1038/​jcbfm.​1995.​2 PubMed CrossRef
    83.Tiwari V, Ambadipudi S, Patel AB (2013) Glutamatergic and GABAergic TCA cycle and neurotransmitter cycling fluxes in different regions of mouse brain. J Cereb Blood Flow Metab 33(10):1523–1531. doi:10.​1038/​jcbfm.​2013.​114 PubMedCentral PubMed CrossRef
    84.Coulter DA, Eid T (2012) Astrocytic regulation of glutamate homeostasis in epilepsy. Glia 60(8):1215–1226. doi:10.​1002/​glia.​22341 PubMedCentral PubMed CrossRef
    85.Longuemare MC, Swanson RA (1997) Net glutamate release from astrocytes is not induced by extracellular potassium concentrations attainable in brain. J Neurochem 69(2):879–882PubMed CrossRef
    86.Woo DH, Han KS, Shim JW, Yoon BE, Kim E, Bae JY, Oh SJ, Hwang EM, Marmorstein AD, Bae YC, Park JY, Lee CJ (2012) TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation. Cell 151(1):25–40. doi:10.​1016/​j.​cell.​2012.​09.​005 PubMed CrossRef
    87.Parpura V, Zorec R (2010) Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 63(1–2):83–92. doi:10.​1016/​j.​brainresrev.​2009.​11.​008 PubMedCentral PubMed CrossRef
    88.Parpura V, Zorec R (2008) Gliotransmission: exocytotic release from astrocytes. Brain Res Rev 63(1–2):83–92. doi:10.​1016/​j.​brainresrev.​2009.​11.​008
    89.Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A (2004) Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci 7(6):613–620. doi:10.​1038/​nn1246 PubMed CrossRef
    90.Santello M, Bezzi P, Volterra A (2011) TNFalpha controls glutamatergic gliotransmission in the hippocampal dentate gyrus. Neuron 69(5):988–1001. doi:10.​1016/​j.​neuron.​2011.​02.​003 PubMed CrossRef
    91.Listrom CD, Morizono H, Rajagopal BS, McCann MT, Tuchman M, Allewell NM (1997) Expression, purification, and characterization of recombinant human glutamine synthetase. Biochem J 328(Pt 1):159–163PubMedCentral PubMed CrossRef
    92.Takamori S (2006) VGLUTs: 'exciting' times for glutamatergic research? Neurosci Res 55(4):343–351. doi:10.​1016/​j.​neures.​2006.​04.​016 PubMed CrossRef
    93.Nissim I, Brosnan ME, Yudkoff M, Brosnan JT (1999) Studies of hepatic glutamine metabolism in the perfused rat liver with (15)N-labeled glutamine. J Biol Chem 274(41):28958–28965PubMed CrossRef
    94.Rosas-Ballina M, Tracey KJ (2009) Cholinergic control of inflammation. J Intern Med 265(6):663–679. doi:10.​1111/​j.​1365-2796.​2009.​02098.​x PubMedCentral PubMed CrossRef
    95.Sama DM, Norris CM (2013) Calcium dysregulation and neuroinflammation: discrete and integrated mechanisms for age-related synaptic dysfunction. Ageing Res Rev 12(4):982–995. doi:10.​1016/​j.​arr.​2013.​05.​008 PubMed CrossRef
    96.Balosso S, Ravizza T, Pierucci M, Calcagno E, Invernizzi R, Di Giovanni G, Esposito E, Vezzani A (2009) Molecular and functional interactions between tumor necrosis factor-alpha receptors and the glutamatergic system in the mouse hippocampus: implications for seizure susceptibility. Neuroscience 161(1):293–300. doi:10.​1016/​j.​neuroscience.​2009.​03.​005 PubMed CrossRef
    97.Stellwagen D, Beattie EC, Seo JY, Malenka RC (2005) Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J Neurosci 25(12):3219–3228. doi:10.​1523/​JNEUROSCI.​ 4486-04.​2005 PubMed CrossRef
    98.Qiu Z, Gruol DL (2003) Interleukin-6, beta-amyloid peptide and NMDA interactions in rat cortical neurons. J Neuroimmunol 139(1–2):51–57PubMed CrossRef
    99.Qiu Z, Sweeney DD, Netzeband JG, Gruol DL (1998) Chronic interleukin-6 alters NMDA receptor-mediated membrane responses and enhances neurotoxicity in developing CNS neurons. J Neurosci 18(24):10445–10456PubMed
    100.Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, Marinovich M (2003) Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23(25):8692–8700PubMed
    101.Bliss RM, Finckbone VL, Trice J, Strahlendorf H, Strahlendorf J (2011) Tumor necrosis factor-alpha (TNF-alpha) augments AMPA-induced Purkinje neuron toxicity. Brain Res 1386:1–14. doi:10.​1016/​j.​brainres.​2011.​01.​059 PubMed CrossRef
    102.Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391(6664):281–285. doi:10.​1038/​34651 PubMed CrossRef
    103.Domercq M, Brambilla L, Pilati E, Marchaland J, Volterra A, Bezzi P (2006) P2Y1 receptor-evoked glutamate exocytosis from astrocytes: control by tumor necrosis factor-alpha and prostaglandins. J Biol Chem 281(41):30684–30696. doi:10.​1074/​jbc.​M606429200 PubMed CrossRef
    104.Liu F, Zhou R, Yan H, Yin H, Wu X, Tan Y, Li L (2014) Metabotropic glutamate receptor 5 modulates calcium oscillation and innate immune response induced by lipopolysaccharide in microglial cell. Neuroscience 281C:24–34. doi:10.​1016/​j.​neuroscience.​2014.​09.​034 PubMed CrossRef
    105.Yoshio T, Okamoto H, Hirohata S, Minota S (2013) IgG anti-NR2 glutamate receptor autoantibodies from patients with systemic lupus erythematosus activate endothelial cells. Arthritis Rheum 65(2):457–463. doi:10.​1002/​art.​37745 PubMed CrossRef
    106.Werry EL, Liu GJ, Lovelace MD, Nagarajah R, Hickie IB, Bennett MR (2011) Lipopolysaccharide-stimulated interleukin-10 release from neonatal spinal cord microglia is potentiated by glutamate. Neuroscience 175:93–103. doi:10.​1016/​j.​neuroscience.​2010.​10.​080 PubMed CrossRef
    107.Loureiro SO, Heimfarth L, Scherer EB, da Cunha MJ, de Lima BO, Biasibetti H, Pessoa-Pureur R, Wyse AT (2013) Cytoskeleton of cortical astrocytes as a target to proline through oxidative stress mechanisms. Exp Cell Res 319(3):89–104. doi:10.​1016/​j.​yexcr.​2012.​11.​002 PubMed CrossRef
    108.Alghasham A, Salem TA, Meki AR (2013) Effect of cadmium-polluted water on plasma levels of tumor necrosis factor-alpha, interleukin-6 and oxidative status biomarkers in rats: protective effect of curcumin. Food Chem Toxicol 59:160–164. doi:10.​1016/​j.​fct.​2013.​05.​059 PubMed CrossRef
    109.Shytle RD, Mori T, Townsend K, Vendrame M, Sun N, Zeng J, Ehrhart J, Silver AA, Sanberg PR, Tan J (2004) Cholinergic modulation of microglial activation by alpha 7 nicotinic receptors. J Neurochem 89(2):337–343. doi:10.​1046/​j.​1471-4159.​2004.​02347.​x PubMed CrossRef
    110.Pavlov VA, Tracey KJ (2012) The vagus nerve and the inflammatory reflex—linking immunity and metabolism. Nat Rev Endocrinol 8(12):743–754. doi:10.​1038/​nrendo.​2012.​189 PubMedCentral PubMed CrossRef
    111.Brenner T, Nizri E, Irony-Tur-Sinai M, Hamra-Amitay Y, Wirguin I (2008) Acetylcholinesterase inhibitors and cholinergic modulation in myasthenia gravis and neuroinflammation. J Neuroimmunol 201–202:121–127. doi:10.​1016/​j.​jneuroim.​2008.​05.​022 PubMed CrossRef
    112.Wang J, Zhang HY, Tang XC (2010) Huperzine a improves chronic inflammation and cognitive decline in rats with cerebral hypoperfusion. J Neurosci Res 88(4):807–815. doi:10.​1002/​jnr.​22237 PubMed
    113.Vijayaraghavan S, Karami A, Aeinehband S, Behbahani H, Grandien A, Nilsson B, Ekdahl KN, Lindblom RP, Piehl F, Darreh-Shori T (2013) Regulated extracellular choline acetyltransferase activity—the plausible missing link of the distant action of acetylcholine in the cholinergic anti-inflammatory pathway. PLoS One 8(6):e65936. doi:10.​1371/​journal.​pone.​0065936 PubMedCentral PubMed CrossRef
    114.Dong H, Xiang YY, Farchi N, Ju W, Wu Y, Chen L, Wang Y, Hochner B, Yang B, Soreq H, Lu WY (2004) Excessive expression of acetylcholinesterase impairs glutamatergic synaptogenesis in hippocampal neurons. J Neurosci 24(41):8950–8960. doi:10.​1523/​JNEUROSCI.​ 2106-04.​2004 PubMed CrossRef
    115.Calderon FH, von Bernhardi R, De Ferrari G, Luza S, Aldunate R, Inestrosa NC (1998) Toxic effects of acetylcholinesterase on neuronal and glial-like cells in vitro. Mol Psychiatry 3(3):247–255PubMed CrossRef
    116.Niranjan R, Rajasekar N, Nath C, Shukla R (2012) The effect of guggulipid and nimesulide on MPTP-induced mediators of neuroinflammation in rat astrocytoma cells, C6. Chem Biol Interact 200(2–3):73–83. doi:10.​1016/​j.​cbi.​2012.​08.​008 PubMed CrossRef
    117.Al-Amin MM, Uddin MM, Rahman MM, Reza HM, Rana MS (2013) Effect of diclofenac and antidepressants on the inflammatory response in astrocyte cell culture. Inflammopharmacology 21(6):421–425. doi:10.​1007/​s10787-013-0181-9 PubMed CrossRef
    118.Anneken JH, Gudelsky GA (2012) MDMA produces a delayed and sustained increase in the extracellular concentration of glutamate in the rat hippocampus. Neuropharmacology 63(6):1022–1027. doi:10.​1016/​j.​neuropharm.​2012.​07.​026 PubMedCentral PubMed CrossRef
    119.Cali C, Lopatar J, Petrelli F, Pucci L, Bezzi P (2014) G-protein coupled receptor-evoked glutamate exocytosis from astrocytes: role of prostaglandins. Neural Plast 2014:254574. doi:10.​1155/​2014/​254574 PubMedCentral PubMed
    120.Verkhratsky A, Parpura V (2014) Calcium signalling and calcium channels: evolution and general principles. Eur J Pharmacol 739:1–3. doi:10.​1016/​j.​ejphar.​2013.​11.​013 PubMed CrossRef
    121.Muscoli C, Visalli V, Colica C, Nistico R, Palma E, Costa N, Rotiroti D, Nistico G, Mollace V (2005) The effect of inflammatory stimuli on NMDA-related activation of glutamine synthase in human cultured astroglial cells. Neurosci Lett 373(3):184–188. doi:10.​1016/​j.​neulet.​2004.​09.​079 PubMed CrossRef
    122.Fleischer-Lambropoulos E, Kazazoglou T, Geladopoulos T, Kentroti S, Stefanis C, Vernadakis A (1996) Stimulation of glutamine synthetase activity by excitatory amino acids in astrocyte cultures derived from aged mouse cerebral hemispheres may be associated with non-N-methyl-d -aspartate receptor activation. Int J Dev Neurosci 14(4):523–530PubMed CrossRef
    123.Broer A, Deitmer JW, Broer S (2004) Astroglial glutamine transport by system N is upregulated by glutamate. Glia 48(4):298–310. doi:10.​1002/​glia.​20081 PubMed CrossRef
    124.Lafon-Cazal M, Fagni L, Guiraud MJ, Mary S, Lerner-Natoli M, Pin JP, Shigemoto R, Bockaert J (1999) mGluR7-like metabotropic glutamate receptors inhibit NMDA-mediated excitotoxicity in cultured mouse cerebellar granule neurons. Eur J Neurosci 11(2):663–672PubMed CrossRef
    125.Liu X, Albano R, Lobner D (2014) FGF-2 induces neuronal death through upregulation of system xc. Brain Res 1547:25–33. doi:10.​1016/​j.​brainres.​2013.​12.​018 PubMed CrossRef
    126.Simoes AP, Duarte JA, Agasse F, Canas PM, Tome AR, Agostinho P, Cunha RA (2012) Blockade of adenosine A2A receptors prevents interleukin-1beta-induced exacerbation of neuronal toxicity through a p38 mitogen-activated protein kinase pathway. J Neuroinflammation 9:204. doi:10.​1186/​1742-2094-9-204 PubMedCentral PubMed CrossRef
    127.Kostandy BB (2012) The role of glutamate in neuronal ischemic injury: the role of spark in fire. Neurol Sci 33(2):223–237. doi:10.​1007/​s10072-011-0828-5 PubMed CrossRef
  • 作者单位:Samanta Oliveira Loureiro (1)
    Daniele Susana Volkart Sidegum (1)
    Helena Biasibetti (1)
    Mery Stefani Leivas Pereira (1)
    Diogo Losch de Oliveira (1)
    Regina Pessoa-Pureur (1)
    Angela T. S. Wyse (1)

    1. Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Rua Ramiro Barcelos 2600 anexo, 90035-003, Porto Alegre, RS, Brazil
  • 刊物主题:Neurosciences; Neurobiology; Cell Biology; Neurology;
  • 出版者:Springer US
  • ISSN:1559-1182
文摘
Hyperprolinemias are inherited disorder of proline (Pro) metabolism. Patients affected may present neurological manifestations, but the mechanisms of neural excitotoxicity elicited by hyperprolinemia are far from being understood. Considering that the astrocytes are important players in neurological disorders, the aim of the present work was to study the effects 1 mM Pro on glutamatergic and inflammatory parameters in cultured astrocytes from cerebral cortex of rats, exploring some molecular mechanisms underlying the disrupted homeostasis of astrocytes exposed to this toxic Pro concentration. We showed that cortical astrocytes of rats exposed to 1 mM Pro presented significantly elevated extracellular glutamate and glutamine levels, suggesting glutamate excitotoxicity. The excess of glutamate elicited by Pro together with increased glutamate uptake and upregulated glutamine synthetase (GS) activity supported misregulated glutamate homeostasis in astrocytic cells. High Pro levels also induced production/release of pro-inflammatory cytokines TNF-α, IL-1β, and IL-6. We also evidenced misregulation of cholinergic anti-inflammatory system with increased acetylcholinesterase (AChE) activity and decreased acetylcholine (ACh) levels, contributing to the inflammatory status in Pro-treated astrocytes. Our findings highlighted a crosstalk among disrupted glutamate homeostasis, cholinergic mechanisms, and inflammatory cytokines, since ionotropic (DL-AP5 and CNQX) and metabotropic (MCPG and MPEP) glutamate antagonists were able to restore the extracellular glutamate and glutamine levels; downregulate TNFα and IL6 production/release, modulate GS and AChE activities; and restore ACh levels. Otherwise, the non-steroidal anti-inflammatory drugs nimesulide, acetylsalicylic acid, ibuprofen, and diclofenac sodium decreased the extracellular glutamate and glutamine levels, downregulated GS and AChE activities, and restored ACh levels in Pro-treated astrocytes. Altogether, our results evidence that the vulnerability of metabolic homeostasis in cortical astrocytes might have important implications in the neurotoxicity of Pro. Keywords Proline Astrocyte Glutamate Inflammation Cholinergic system Acetylcholine Acetylcholinesterase Cytokine mediators TNF-α IL-1β IL-6 Excitotoxicity Glutamine synthetase

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