Lanthanum chloride reduces lactate production in primary culture rat cortical astrocytes and suppresses primary co-culture rat cortical astrocyte-neuron lactate transport

Fühner-Wieland's Sammlung von Vergiftungsfällen - Tập 92 - Trang 1407-1419 - 2017
Yaling Sun1, Jinghua Yang1, Xiaoyu Hu1, Xiang Gao1, Yingqi Li1, Miao Yu1, Shiyu Liu1, Xiaobo Lu1, Cuihong Jin1, Shengwen Wu1, Yuan Cai1
1Department of Toxicology, School of Public Health, China Medical University, Shenyang, People’s Republic of China

Tóm tắt

Lanthanum (La) can impair learning memory and induce behavioral abnormalities in animals. However, the mechanism underlying these adverse effects of La is still elusive. It has been demonstrated that lactate derived from astrocytes is the major energy source for neurons during long-term memory (LTM) formation and the deficiency of lactate supply can result in LTM damage. However, little work has been done with respect to the impact of La on the lactate production in astrocytes and astrocyte-neuron lactate transport (ANLT). Herein, experiments were undertaken to explore if there was such an adverse effect of La. Primary culture rat cortical astrocytes and primary co-culture rat cortical astrocyte-neuron were treated with (0.125, 0.25 and 0.5 mM) lanthanum chloride (LaCl3) for 24 h. The results showed that LaCl3 treatment significantly downregulated the mRNA and protein expression of glucose transporter 1 (GLUT1), glycogen synthase (GS), glycogen phosphorylase (GP), lactate dehydrogenase A (LDHA), and monocarboxylate transporter 1, 2 and 4 (MCT 1 2 and 4); upregulated the mRNA and protein expression of lactate dehydrogenase B (LDHB); and decreased the glycogen level, total LDH and GP activity, GS/p-GS ratio and lactate contents. Moreover, rolipram (20, 40 μM) or forskolin (20, 40 μM) could increase the lactate content by upregulating GP expression and the GS/p-GS ratio, as well as antagonize the effects of La. These results suggested that La-induced learning-memory damage was probably related to its suppression of lactate production in astrocytes and ANLT. This study provides some novel clues for clarifying the mechanism underlying the neurotoxicity of La.

Tài liệu tham khảo

Andreev VA et al (2007) Measurement of the muon capture rate in hydrogen gas and determination of the proton’s pseudoscalar coupling gP. Phys Rev Lett 99:032002. https://doi.org/10.1103/PhysRevLett.99.032002 Belanger M, Allaman I, Magistretti PJ (2011) Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14:724–738. https://doi.org/10.1016/j.cmet.2011.08.016 Benarroch EE (2014) Brain glucose transporters: implications for. Neurol Dis Neurol 82:1374–1379. https://doi.org/10.1212/WNL.0000000000000328 Blokland A, Schreiber R, Prickaerts J (2006) Improving memory: a role for phosphodiesterases. Curr Pharm Des 12:2511–2523 Bouskila M et al (2010) Allosteric regulation of glycogen synthase controls glycogen synthesis in muscle. Cell Metab 12:456–466. https://doi.org/10.1016/j.cmet.2010.10.006 Chen Z (2004) The hormesis effect of rare earths and potential impact of application in agriculture on the agriculture environment. Rural Ecol Environ 20:1–5 (in Chinese) Chen Z (2005) Brain accumulation, toxicity and potential hazards to human health in rare earths. Rural Ecol Environ 72:73–80 (in Chinese) Choeiri C, Staines W, Miki T, Seino S, Messier C (2005) Glucose transporter plasticity during memory processing. Neuroscience 130:591–600. https://doi.org/10.1016/j.neuroscience.2004.09.011 Chuquet J, Quilichini P, Nimchinsky EA, Buzsaki G (2010) Predominant enhancement of glucose uptake in astrocytes versus neurons during activation of the somatosensory cortex. J Neurosci 30:15298–15303. https://doi.org/10.1523/JNEUROSCI.0762-10.2010 Clarke LE, Barres BA (2013) Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 14:311–321. https://doi.org/10.1038/nrn3484 Cm C, George MA (2016) The popliteal vein thrombosis in a pediatric patient: a case report. J Orthop Case Rep 6:72–74. https://doi.org/10.13107/jocr.2250-0685.442 Daneman R, Prat A (2015) The blood–brain barrier. Cold Spring Harb Perspect Biol. 7:a020412. https://doi.org/10.1101/cshperspect.a020412 Dawson DM, Goodfriend TL, Kaplan NO (1964) Lactic dehydrogenases: functions of the two types rates of synthesis of the two major forms can be correlated with metabolic differentiation. Science 143:929–933 Dawson VL, Dawson TM, London ED, Bredt DS, Snyder SH (1991) Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 88:6368–6371 Fan G, Yuan Z, Zheng H, Liu Z (2004) Study on the effects of exposure to rare earth elements and health-responses in children aged 7–10 years. Wei sheng yan jiu = J Hyg Res 33:23–28 Fellin T, Pascual O, Haydon PG (2006) Astrocytes coordinate synaptic networks: balanced excitation and inhibition. Physiology 21:208–215. https://doi.org/10.1152/physiol.00161.2005 Ghosh A, Highton D, Kolyva C, Tachtsidis I, Elwell CE, Smith M (2017) Hyperoxia results in increased aerobic metabolism following acute brain injury. J Cereb Blood Flow Metab 37:2910–2920. https://doi.org/10.1177/0271678X16679171 Gibbs ME (2015) Role of glycogenolysis in memory and learning: regulation by noradrenaline, serotonin and ATP. Front Integr Neurosci. 9:70 https://doi.org/10.3389/fnint.2015.00070 Gibbs ME, Hertz L (2008) Inhibition of astrocytic energy metabolism by d-lactate exposure impairs memory. Neurochem Int 52:1012–1018. https://doi.org/10.1016/j.neuint.2007.10.014 Gibbs ME, O’Dowd BS, Hertz E, Hertz L (2006) Astrocytic energy metabolism consolidates memory in young chicks. Neuroscience 141:9–13. https://doi.org/10.1016/j.neuroscience.2006.04.038 Gramowski A, Jugelt K, Schroder OH, Weiss DG, Mitzner S (2011) Acute functional neurotoxicity of lanthanum(III) in primary cortical networks. Toxicol Sci 120:173–183. https://doi.org/10.1093/toxsci/kfq385 Greenberg CC, Jurczak MJ, Danos AM, Brady MJ (2006) Glycogen branches out: new perspectives on the role of glycogen metabolism in the integration of metabolic pathways. Am J Physiol Endocrinol Metab 291:E1–E8. https://doi.org/10.1152/ajpendo.00652.2005 Hartline DK (2011) The evolutionary origins of glia. Glia 59:1215–1236. https://doi.org/10.1002/glia.21149 Heitland P, Koster HD (2006) Biomonitoring of 30 trace elements in urine of children and adults by ICP-MS. Clin Chim Acta 365:310–318. https://doi.org/10.1016/j.cca.2005.09.013 Jakoby P, Schmidt E, Ruminot I, Gutierrez R, Barros LF, Deitmer JW (2014) Higher transport and metabolism of glucose in astrocytes compared with neurons: a multiphoton study of hippocampal and cerebellar tissue slices. Cereb Cortex 24:222–231. https://doi.org/10.1093/cercor/bhs309 Jancic D, Lopez de Armentia M, Valor LM, Olivares R, Barco A (2009) Inhibition of cAMP response element-binding protein reduces neuronal excitability and plasticity, and triggers neurodegeneration. Cereb Cortex 19:2535–2547. https://doi.org/10.1093/cercor/bhp004 Jiang C et al (2014) Low glucose utilization and neurodegenerative changes caused by sodium fluoride exposure in rat’s developmental brain. Neuromol Med 16:94–105. https://doi.org/10.1007/s12017-013-8260-z Jin M, Huang Y, Hu Y, Qiao M, Wang X (2014) Rare earth elements content and health risk assessment of soil and crops in typical rare earth mine area in Jiangxi Province. Acta Sci Circumst 34:3084–3093 Kettenmann H, Verkhratsky A (2008) Neuroglia: the 150 years after. Trends Neurosci 31:653–659. https://doi.org/10.1016/j.tins.2008.09.003 Li N, Duan Y, Zhou M, Liu C, Hong F (2009) The effects of lanthanoid on the structure–function of lactate dehydrogenase from mice heart Biol. Trace Elem Res 132:164–175. https://doi.org/10.1007/s12011-009-8374-1 Libao R, Xiaoyan W, Qing X, Jingxiu L, Zhuo H, Ying D, Jingyu W (2007) Study on the correlation of light rare earth elements content in rat brain tissue. Chin J Anal Lab. https://doi.org/10.13595/j.cnki.issn1000-0720.2007.0214 Liu H et al (2014) Lanthanum chloride impairs spatial memory through ERK/MSK1 signaling pathway of hippocampus in rats. Neurochem Res 39:2479–2491. https://doi.org/10.1007/s11064-014-1452-6 Lu W et al (2015) Changes in lactate content and monocarboxylate transporter 2 expression in Abeta(2)(5)(-)(3)(5)-treated rat model of Alzheimer’s disease. Neurol Sci 36:871–876. https://doi.org/10.1007/s10072-015-2087-3 Lundgaard I et al (2015) Direct neuronal glucose uptake heralds activity-dependent increases in cerebral metabolism. Nat Commun 6:6807. https://doi.org/10.1038/ncomms7807 Machler P et al (2016) In vivo evidence for a lactate gradient from astrocytes to neurons. Cell Metab 23:94–102. https://doi.org/10.1016/j.cmet.2015.10.010 Magistretti PJ, Allaman I (2015) A cellular perspective on brain energy metabolism and functional imaging. Neuron 86:883–901. https://doi.org/10.1016/j.neuron.2015.03.035 Maragakis NJ, Rothstein JD (2006) Mechanisms of disease: astrocytes in neurodegenerative disease. Nat Clin Pract Neurol 2:679–689. https://doi.org/10.1038/ncpneuro0355 Matsui T, Omuro H, Liu YF, Soya M, Shima T, McEwen BS, Soya H (2017) Astrocytic glycogen-derived lactate fuels the brain during exhaustive exercise to maintain endurance capacity. Proc Natl Acad Sci USA 114:6358–6363. https://doi.org/10.1073/pnas.1702739114 Newman LA, Korol DL, Gold PE (2011) Lactate produced by glycogenolysis in astrocytes regulates memory processing. PloS One. https://doi.org/10.1371/journal.pone.0028427 Obel LF, Muller MS, Walls AB, Sickmann HM, Bak LK, Waagepetersen HS, Schousboe A (2012) Brain glycogen-new perspectives on its metabolic function and regulation at the subcellular level. Front Neuroenerg 4:3. https://doi.org/10.3389/fnene.2012.00003 Oz G et al (2007) Human brain glycogen content and metabolism: implications on its role in brain energy metabolism. Am J Physiol Endocrinol Metab 292:E946–E951. https://doi.org/10.1152/ajpendo.00424.2006 Pellerin L, Magistretti PJ (1994) Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA 91:10625–10629 Pellerin L, Bouzier-Sore AK, Aubert A, Serres S, Merle M, Costalat R, Magistretti PJ (2007) Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55:1251–1262. https://doi.org/10.1002/glia.20528 Pfeiffer B, Elmer K, Roggendorf W, Reinhart PH, Hamprecht B (1990) Immunohistochemical demonstration of glycogen phosphorylase in rat brain slices. Histochemistry 94:73–80 Pierre K, Pellerin L (2005) Monocarboxylate transporters in the central nervous system: distribution, regulation and function. J Neurochem 94:1–14. https://doi.org/10.1111/j.1471-4159.2005.03168.x Roach PJ et al (1998) Novel aspects of the regulation of glycogen storage. J Basic Clin Physiol Pharmacol 9:139–151 Rutten K, Lieben C, Smits L, Blokland A (2007a) The PDE4 inhibitor rolipram reverses object memory impairment induced by acute tryptophan depletion in the rat. Psychopharmacology (Berl) 192:275–282. https://doi.org/10.1007/s00213-006-0697-4 Rutten K, Prickaerts J, Hendrix M, van der Staay FJ, Sik A, Blokland A (2007b) Time-dependent involvement of cAMP and cGMP in consolidation of object memory: studies using selective phosphodiesterase type 2, 4 and 5 inhibitors. Eur J Pharmacol 558:107–112. https://doi.org/10.1016/j.ejphar.2006.11.041 Shammas FV, Engeset A (1986) Glycogen content and PAS staining pattern of human megakaryocytes. Scand J Haematol 37:237–242 Steinman MQ, Gao V, Alberini CM (2016) The role of lactate-mediated metabolic coupling between astrocytes and neurons in long-term memory formation. Front Integr Neurosci 10:10 https://doi.org/10.3389/fnint.2016.00010 Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ, Alberini CM (2011) Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144:810–823. https://doi.org/10.1016/j.cell.2011.02.018 Swanson RA, Choi DW (1993) Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J Cereb Blood Flow Metab 13:162–169. https://doi.org/10.1038/jcbfm.1993.19 Tabatabaei Shafiei M, Carvajal Gonczi CM, Rahman MS, East A, Francois J, Darlington PJ (2014) Detecting glycogen in peripheral blood mononuclear cells with periodic acid schiff staining. J Vis Exp. https://doi.org/10.3791/52199 Tadi M, Allaman I, Lengacher S, Grenningloh G, Magistretti PJ (2015) Learning-induced gene expression in the hippocampus reveals a role of neuron -astrocyte metabolic coupling in long term memory. PloS One 10:e0141568. https://doi.org/10.1371/journal.pone.0141568 Temple S (2001) The development of neural stem cells. Nature 414:112–117. https://doi.org/10.1038/35102174 Wang DD, Bordey A (2008) The astrocyte odyssey. Progress Neurobiol 86:342–367. https://doi.org/10.1016/j.pneurobio.2008.09.015 Wang J et al (2007) Acute toxicity and biodistribution of different sized titanium dioxide particles in mice after oral administration. Toxicol Lett 168:176–185. https://doi.org/10.1016/j.toxlet.2006.12.001 Wyss MT, Jolivet R, Buck A, Magistretti PJ, Weber B (2011) In vivo evidence for lactate as a neuronal energy source. J Neurosci 31:7477–7485. https://doi.org/10.1523/JNEUROSCI.0415-11.2011 Xiaofei L, Zhibiao C, yonghe Z, Zhiqiang C (2013) Evaluation of rare earth elements content and health risk of soil and vegetables in rare earth mining area. J Environ Sci:835–843 Yang J et al (2009) Lanthanum chloride impairs memory, decreases pCaMK IV, pMAPK and pCREB expression of hippocampus in rats. Toxicol Lett 190:208–214. https://doi.org/10.1016/j.toxlet.2009.07.016 Yang J, Liu Q, Qi M, Lu S, Wu S, Xi Q, Cai Y (2013) Lanthanum chloride promotes mitochondrial apoptotic pathway in primary cultured rat astrocytes. Environ Toxicol 28:489–497. https://doi.org/10.1002/tox.20738 Zhang XJ, Li TY, Liu YX, Chen J, Qu P, Wei XP, He J (2010) Primary culture of rat hippocampal neurons and detection of the neuronal excitability. Nan fang yi ke da xue xue bao = J South Med Univ 30:2080–2083 Zhang L et al (2017a) The effect of nuclear factor erythroid 2-related factor/antioxidant response element signalling pathway in the lanthanum chloride-induced impairment of learning and memory in rats. J Neurochem 140:463–475. https://doi.org/10.1111/jnc.13895 Zhang L et al (2017b) Activation of Nrf2/ARE signaling pathway attenuates lanthanum chloride induced injuries in primary rat astrocytes. Metallomics 9:1120–1131. https://doi.org/10.1039/c7mt00182g Zhao Y, Yang J, QufangLiu, Jin C, Wu S, Wang C, Cai Y (2013) Effects of lanthanum on the spatial learning, memory,c AMP content and PKA expression in the hippocampus of rats. J Toxicol:321–324 Zheng L et al (2013) Lanthanum chloride impairs spatial learning and memory and downregulates NF-kappaB signalling pathway in rats. Arch Toxicol 87:2105–2117. https://doi.org/10.1007/s00204-013-1076-7