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Glutamate Differently Modulates Metabotropic Glutamate Receptors in Neuronal and Glial Cells

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Abstract

Glutamate is an excitatory neurotransmitter implicated in learning and memory processes, but at high concentrations it acts as an excitotoxin causing degeneration and neuronal death. The aim of this work was to determine the excitotoxic effect of glutamate and the regulation of metabotropic glutamate receptors (mGluR) during excitotoxicity in neurons and C6 glioma cells. Results show that glutamate causes excitotoxic damage only in cortical neurons. Loss of cell viability in neurons was glutamate concentration- and time-dependent. Total mGluR levels were significantly reduced in these cells when exposed to glutamate. However, in C6 cells, which have been used as a model of glial cells, these receptors were regulated in a biphasic manner, decreased after 6 h, and increased after 24/48 h of treatment. Results show a cell dependent mGluR regulation by glutamate exposure which could mediate the vulnerability or not to glutamate mediated excitotoxicity.

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References

  1. Riedel G, Platt B, Micheau J (2003) Glutamate receptor function in learning and memory. Behav Brain Res 140(1–2):1–47

    Article  CAS  PubMed  Google Scholar 

  2. Meldrum BS (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 130(4S Suppl):1007S–1015S

    Google Scholar 

  3. Dingledine R, Borges K, Bowie D et al (1999) The glutamate receptor ion channels. Pharmacol Rev 51(1):7–61

    CAS  PubMed  Google Scholar 

  4. Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34(1):1–26

    Article  CAS  PubMed  Google Scholar 

  5. Conn PJ, Pin JP (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37:205–237

    Article  CAS  PubMed  Google Scholar 

  6. Dong XX, Wang Y, Qin ZH (2009) Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sin 30:379–387

    Article  CAS  PubMed  Google Scholar 

  7. Choi DW (1987) Ionic dependence of glutamate neurotoxicity. J Neurosci 7:369–379

    CAS  PubMed  Google Scholar 

  8. Olney JW (1969) Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 164(880):719–721

    Article  CAS  PubMed  Google Scholar 

  9. Hynd MR, Scott HL, Dodd PR (2004) Glutamate-mediated excitotoxicity and neurodegeneration in Alzheimer’s disease. Neurochem Int 45:583–595

    Article  CAS  PubMed  Google Scholar 

  10. Arundine M, Tymianski M (2003) Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34(4–5):325–337

    Article  CAS  PubMed  Google Scholar 

  11. Szydlowska K, Tymianski M (2010) Calcium, ischemia and excitotoxicity. Cell Calcium 47(2):122–129

    Article  CAS  PubMed  Google Scholar 

  12. Koller WC, Cersosimo MG (2004) Neuroprotection in Parkinson’s disease: an elusive goal. Curr Neurol Neurosci Rep 4(4):277–283

    Article  PubMed  Google Scholar 

  13. Rego AC, de Almeida LP (2005) Molecular targets and therapeutic strategies in Huntington’s disease. Curr Drug Targets CNS Neurol Disord 4(4):361–381

    Article  CAS  PubMed  Google Scholar 

  14. Yi JH, Hazell AS (2006) Excitotoxic mechanisms and the role of astrocytic glutamate transporters in traumatic brain injury. Neurochem Int 48(5):394–403

    Article  CAS  PubMed  Google Scholar 

  15. Corona JC, Tovar-y-Romo LB, Tapia R (2007) Glutamate excitotoxicity and therapeutic targets for amyotrophic lateral sclerosis. Expert Opin Ther Targets 11(11):1415–1428

    Article  CAS  PubMed  Google Scholar 

  16. Hazell AS (2007) Excitotoxic mechanisms in stroke: an update of concepts and treatment strategies. Neurochem Int 50(7–8):941–953

    Article  CAS  PubMed  Google Scholar 

  17. Mamelak M (2007) Alzheimer’s disease, oxidative stress and gammahydroxybutyrate. Neurobiol Aging 28(9):1340–1360

    Article  CAS  PubMed  Google Scholar 

  18. Farooqui AA, Ong W, Horrocks L (2008) Glutamate receptors and neurological disorders. In: Farooqui AA, Ong W, Horrocks L (eds) Neurochemical aspects of excitotoxicity. Springer, New York, pp 161–204

    Chapter  Google Scholar 

  19. Baskys A, Fang L, Bayazitov I (2005) Activation of neuroprotective pathways by metabotropic group I glutamate receptors: a potential target for drug discovery? Ann NY Acad Sci 1053:55–73

    Article  CAS  PubMed  Google Scholar 

  20. Baskys A, Bayazitov I, Zhu E et al (2007) Rab-mediated endocytosis: linking neurodegeneration, neuroprotection, and synaptic plasticity? Ann NY Acad Sci 1122:313–329

    Article  CAS  PubMed  Google Scholar 

  21. Nicoletti F, Battaglia G, Storto M et al (2007) Metabotropic glutamate receptors: beyond the regulation of synaptic transmission. Psychoneuroendocrinology 32(Suppl 1):S40–S45

    Google Scholar 

  22. Knopfel T, Uusisaari M (2008) Modulation of excitation by metabotropic glutamate receptors. Results Probl Cell Differ 44:163–175

    Article  CAS  PubMed  Google Scholar 

  23. Schiefer J, Sprunken A, Puls C et al (2004) The metabotropic glutamate receptor 5 antagonist MPEP and the mGluR2 agonist LY379268 modify disease progression in a transgenic mouse model of Huntington’s disease. Brain Res 1019(1–2):246–254

    Article  CAS  PubMed  Google Scholar 

  24. Dalfó E, Albasanz JL, Martín M et al (2004) Abnormal metabotropic glutamate receptor expression and signaling in the cerebral cortex in diffuse Lewy body disease is associated with irregular alpha-synuclein/phospholipase C (PLCbeta1) interactions. Brain Pathol 14(4):388–398

    Article  PubMed  Google Scholar 

  25. Rodríguez A, Freixes M, Dalfó E et al (2005) Metabotropic glutamate receptor/phospholipase C pathway: a vulnerable target to Creutzfeldt-Jakob disease in the cerebral cortex. Neuroscience 131(4):825–832

    PubMed  Google Scholar 

  26. Albasanz JL, Dalfo E, Ferrer I et al (2005) Impaired metabotropic glutamate receptor/phospholipase C signaling pathway in the cerebral cortex in Alzheimer’s disease and dementia with Lewy bodies correlates with stage of Alzheimer’s-disease-related changes. Neurobiol Dis 20(3):685–693

    Article  CAS  PubMed  Google Scholar 

  27. Kelly E, Bailey CP, Henderson G (2008) Agonist-selective mechanisms of GPCR desensitization. Br J Pharmacol 153(Suppl 1):S379–S388

    Google Scholar 

  28. Hanyaloglu AC, von Zastrow M (2008) Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu Rev Pharmacol Toxicol 48:537–568

    Article  CAS  PubMed  Google Scholar 

  29. Hukovic N, Panetta R, Kumar U et al (1996) Agonist-dependent regulation of cloned human somatostatin receptor types 1–5 (hSSTR1–5): subtype selective internalization or upregulation. Endocrinology 137(9):4046–4049

    Article  CAS  PubMed  Google Scholar 

  30. Broadley KJ (1999) Review of mechanisms involved in the apparent differential desensitization of beta1- and beta2-adrenoceptor-mediated functional responses. J Auton Pharmacol 19(6):335–345

    Article  CAS  PubMed  Google Scholar 

  31. Ramírez JL, Watt HL, Rocheville M et al (2005) Agonist-induced up-regulation of human somatostatin receptor type 1 is regulated by beta-arrestin-1 and requires an essential serine residue in the receptor C-tail. Biochim Biophys Acta 1669(2):182–192

    Article  PubMed  CAS  Google Scholar 

  32. Nelson CP, Challiss RA (2007) “Phenotypic” pharmacology: the influence of cellular environment on G protein-coupled receptor antagonist and inverse agonist pharmacology. Biochem Pharmacol 73(6):737–751

    Article  CAS  PubMed  Google Scholar 

  33. Dhami GK, Ferguson SS (2006) Regulation of metabotropic glutamate receptor signaling, desensitization and endocytosis. Pharmacol Ther 111:260–271

    Article  CAS  PubMed  Google Scholar 

  34. Achour L, Labbe-Jullie C, Scott MG et al (2008) An escort for GPCRs: implications for regulation of receptor density at the cell surface. Trends Pharmacol Sci 29:528–535

    Article  CAS  PubMed  Google Scholar 

  35. Ceccarelli I, Rossi A, Maddalena M et al (2009) Effects of morphine on testosterone levels in rat C6 glioma cells: modulation by anastrozole. J Cell Physiol 221:1–4

    Article  CAS  PubMed  Google Scholar 

  36. Sikka P, Walker R, Cockayne R et al (2010) D-Serine metabolism in C6 glioma cells: involvement of alanine-serine-cysteine transporter (ASCT2) and serine racemase (SRR) but not D-amino acid oxidase (DAO). J Neurosci Res [Epub ahead of print]

  37. Lo Vasco VR, Fabrizi C, Fumagalli L et al (2010) Expression of phosphoinositide-specific phospholipase C isoenzymes in cultured astrocytes activated after stimulation with lipopolysaccharide. J Cell Biochem [Epub ahead of print]

  38. Pav M, Kovaru H, Kovaru F et al (2009) Acute and chronic effects of antidepressants on the G-protein alpha subunit profiles in vitro and in vivo. Neuro Endocrinol Lett 30:592–598

    CAS  PubMed  Google Scholar 

  39. Dugan LL, Kim JS, Zhang Y et al (1999) Differential effects of cAMP in neurons and astrocytes. Role of B-raf. J Biol Chem 274:25842–25848

    Article  CAS  PubMed  Google Scholar 

  40. Castillo CA, Albasanz JL, Fernández M et al (2007) Endogenous expression of adenosine A1, A2 and A3 receptors in rat C6 glioma cells. Neurochem Res 32(6):1056–1070

    Article  CAS  PubMed  Google Scholar 

  41. Janssens N, Lesage AS (2001) Glutamate receptor subunit expression in primary neuronal and secondary glial cultures. J Neurochem 77(6):1457–1474

    Article  CAS  PubMed  Google Scholar 

  42. Albasanz JL, Ros M, Martin M (1997) Characterization of metabotropic glutamate receptors in rat C6 glioma cells. Eur J Pharmacol 326(1):85–91

    Article  CAS  PubMed  Google Scholar 

  43. Albasanz JL, Fernandez M, Martin M (2002) Internalization of metabotropic glutamate receptor in C6 cells through clathrin-coated vesicles. Brain Res Mol Brain Res 99(1):54–66

    Article  Google Scholar 

  44. Murphy MG, Moak CM, Byczko Z et al (1991) Adenosine-dependent regulation of cyclic AMP accumulation in primary cultures of rat astrocytes and neurons. J Neurosci Res 30(4):631–640

    Article  CAS  PubMed  Google Scholar 

  45. Castillo CA, León D, Ruiz MA et al (2008) Modulation of adenosine A(1) and A(2A) receptors in C6 glioma cells during hypoxia: involvement of endogenous adenosine. J Neurochem 105(6):2315–2329

    Article  CAS  PubMed  Google Scholar 

  46. Palmer S, Hughes KT, Lee DY et al (1989) Development of a novel, Ins(1, 4, 5)P3-specific binding assay. Its use to determine the intracellular concentration of Ins(1, 4, 5)P3 in unstimulated and vasopressin-stimulated rat hepatocytes. Cell Signal 1(2):147–156

    Article  CAS  PubMed  Google Scholar 

  47. Gerwins P (1993) Modification of a competitive protein binding assay for determination of inositol 1, 4, 5-trisphosphate. Anal Biochem 210(1):45–49

    Article  CAS  PubMed  Google Scholar 

  48. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65(1–2):55–63

    Article  CAS  PubMed  Google Scholar 

  49. Higuchi R, Fockler C, Dollinger G et al (1993) Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Biotechnology (N Y) 11(9):1026–1030

    Article  CAS  Google Scholar 

  50. Lowry OH, Rosebrough NJ, Farr AL et al (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275

    CAS  PubMed  Google Scholar 

  51. Lee BK, Lee DH, Park S et al (2009) Effects of KR-33028, a novel Na +/H + exchanger-1 inhibitor, on glutamate-induced neuronal cell death and ischemia-induced cerebral infarct. Brain Res 1248:22–30

    Article  CAS  PubMed  Google Scholar 

  52. Goforth PB, Ellis EF, Satin LS (1999) Enhancement of AMPA-mediated current after traumatic injury in cortical neurons. J Neurosci 19(17):7367–7374

    CAS  PubMed  Google Scholar 

  53. Yao HH, Ding JH, Zhou F et al (2005) Enhancement of glutamate uptake mediates the neuroprotection exerted by activating group II or III metabotropic glutamate receptors on astrocytes. J Neurochem 92(4):948–961

    Article  CAS  PubMed  Google Scholar 

  54. Puttonen KA, Lehtonen S, Lampela P et al (2008) Different viabilities and toxicity types after 6-OHDA and Ara-C exposure evaluated by four assays in five cell lines. Toxicol In Vitro 22(1):182–189

    Article  CAS  PubMed  Google Scholar 

  55. Bonfoco E, Krainc D, Ankarcrona M et al (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 92:7162–7166

    Article  CAS  PubMed  Google Scholar 

  56. Sribnick EA, Ray SK, Banik NL (2006) Estrogen prevents glutamate-induced apoptosis in C6 glioma cells by a receptor-mediated mechanism. Neuroscience 137:197–209

    Article  CAS  PubMed  Google Scholar 

  57. Gatti R, Belletti S, Orlandini G et al (1998) Comparison of annexin V and calcein-AM as early vital markers of apoptosis in adherent cells by confocal laser microscopy. J Histochem Cytochem 46:895–900

    CAS  PubMed  Google Scholar 

  58. Pérez-Capote K, Serratosa J, Sola C (2004) Glial activation modulates glutamate neurotoxicity in cerebellar granule cell cultures. Glia 45(3):258–268

    Article  PubMed  Google Scholar 

  59. Maragakis NJ, Rao MS, Llado J et al (2005) Glial restricted precursors protect against chronic glutamate neurotoxicity of motor neurons in vitro. Glia 50(2):145–159

    Article  PubMed  Google Scholar 

  60. Du Y, Chen CP, Tseng CY et al (2007) Astroglia-mediated effects of uric acid to protect spinal cord neurons from glutamate toxicity. Glia 55(5):463–472

    Article  PubMed  Google Scholar 

  61. Pellerin L, Bouzier-Sore AK, Aubert A et al (2007) Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 55(12):1251–1262

    Article  PubMed  Google Scholar 

  62. Gadea A, Lopez-Colome AM (2001) Glial transporters for glutamate, glycine and GABA I. Glutamate transporters. J Neurosci Res 63(6):453–460

    Article  CAS  PubMed  Google Scholar 

  63. Persson M, Sandberg M, Hansson E et al (2006) Microglial glutamate uptake is coupled to glutathione synthesis and glutamate release. Eur J Neurosci 24(4):1063–1070

    Article  PubMed  Google Scholar 

  64. Penela P, Ribas C, Mayor F Jr (2003) Mechanisms of regulation of the expression and function of G protein-coupled receptor kinases. Cell Signal 15(11):973–981

    Article  CAS  PubMed  Google Scholar 

  65. Shenoy SK, Lefkowitz RJ (2005) Seven-transmembrane receptor signaling through beta-arrestin. Sci STKE 2005(308):cm10

    Article  PubMed  Google Scholar 

  66. Marchese A, Paing MM, Temple BR et al (2008) G Protein-coupled receptor sorting to endosomes and lysosomes. Annu Rev Pharmacol Toxicol 48:601–629

    Article  CAS  PubMed  Google Scholar 

  67. León D, Albasanz JL, Iglesias I et al (2005) Effect of chronic glutamate administration to pregnant rats during gestation on metabotropic glutamate receptors from mothers and full-term fetuses brain. Amino Acids 28(2):127–137

    Article  CAS  Google Scholar 

  68. Dhami GK, Ferguson SS (2006) Regulation of metabotropic glutamate receptor signaling, desensitization and endocytosis. Pharmacol Ther 111(1):260–271

    Article  CAS  PubMed  Google Scholar 

  69. Thomas RF, Holt BD, Schwinn DA et al (1992) Long-term agonist exposure induces upregulation of beta 3-adrenergic receptor expression via multiple cAMP response elements. Proc Natl Acad Sci USA 89(10):4490–4494

    Article  CAS  PubMed  Google Scholar 

  70. Loumaye E, Catt KJ (1983) Agonist-induced regulation of pituitary receptors for gonadotropin-releasing hormone. Dissociation of receptor recruitment from hormone release in cultured gonadotrophs. J Biol Chem 258(19):12002–12009

    CAS  PubMed  Google Scholar 

  71. Cook LB, Hinkle PM (2004) Agonist-dependent up-regulation of thyrotrophin-releasing hormone receptor protein. Biochem J 380(Pt 3):815–821

    Article  CAS  PubMed  Google Scholar 

  72. Gentry CL, Lukas RJ (2002) Regulation of nicotinic acetylcholine receptor numbers and function by chronic nicotine exposure. Curr Drug Targets CNS Neurol Disord 1(4):359–385

    Article  CAS  PubMed  Google Scholar 

  73. Hukovic N, Rocheville M, Kumar U et al (1999) Agonist-dependent up-regulation of human somatostatin receptor type 1 requires molecular signals in the cytoplasmic C-tail. J Biol Chem 274(35):24550–24558

    Article  CAS  PubMed  Google Scholar 

  74. Bruno V, Battaglia G, Copani A et al (2001) An activity-dependent switch from facilitation to inhibition in the control of excitotoxicity by group I metabotropic glutamate receptors. Eur J Neurosci 13(8):1469–1478

    Article  CAS  PubMed  Google Scholar 

  75. Baskys A, Bayazitov I, Fang L et al (2005) Group I metabotropic glutamate receptors reduce excitotoxic injury and may facilitate neurogenesis. Neuropharmacology 49(Suppl 1):146–156

    Google Scholar 

  76. Bruno V, Battaglia G, Copani A et al (1995) Activation of class II or III metabotropic glutamate receptors protects cultured cortical neurons against excitotoxic degeneration. Eur J Neurosci 7(9):1906–1913

    Article  CAS  PubMed  Google Scholar 

  77. Hanoune J, Defer N (2001) Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol 41:145–174

    Article  CAS  PubMed  Google Scholar 

  78. Willoughby D, Cooper DM (2007) Organization and Ca2 + regulation of adenylyl cyclases in cAMP microdomains. Physiol Rev 87:965–1010

    Article  CAS  PubMed  Google Scholar 

  79. Beazely MA, Watts VJ (2006) Regulatory properties of adenylate cyclases type 5 and 6: a progress report. Eur J Pharmacol 535:1–12

    Article  CAS  PubMed  Google Scholar 

  80. Llansola M, Felipo V (2010) Metabotropic glutamate receptor 5, but not 1, modulates NMDA receptor-mediated activation of neuronal nitric oxide synthase. Neurochem Int 56(4):535–545

    Article  CAS  PubMed  Google Scholar 

  81. Wang H, Gong B, Vadakkan KI et al (2007) Genetic evidence for adenylyl cyclase 1 as a target for preventing neuronal excitotoxicity mediated by N-methyl-D-aspartate receptors. J Biol Chem 282:1507–1517

    Article  CAS  PubMed  Google Scholar 

  82. Franco R (2009) Neurotransmitter receptor heteromers in neurodegenerative diseases and neural plasticity. J Neural Transm 116:983–987

    Article  CAS  PubMed  Google Scholar 

  83. Ferre S, Baler R, Bouvier M et al (2009) Building a new conceptual framework for receptor heteromers. Nat Chem Biol 5:131–134

    Article  CAS  PubMed  Google Scholar 

  84. Ferre S, Karcz-Kubicha M, Hope BT et al (2002) Synergistic interaction between adenosine A2A and glutamate mGlu5 receptors: implications for striatal neuronal function. Proc Natl Acad Sci USA 99:11940–11945

    Article  CAS  PubMed  Google Scholar 

  85. Ciruela F, Escriche M, Burgueno J et al (2001) Metabotropic glutamate 1alpha and adenosine A1 receptors assemble into functionally interacting complexes. J Biol Chem 276:18345–18351

    Article  CAS  PubMed  Google Scholar 

  86. Hirono M, Yoshioka T, Konishi S (2001) GABA(B) receptor activation enhances mGluR-mediated responses at cerebellar excitatory synapses. Nat Neurosci 4:1207–1216

    Article  CAS  PubMed  Google Scholar 

  87. Gama L, Wilt SG, Breitwieser GE (2001) Heterodimerization of calcium sensing receptors with metabotropic glutamate receptors in neurons. J Biol Chem 276:39053–39059

    Article  CAS  PubMed  Google Scholar 

  88. Snyder EM, Philpot BD, Huber KM et al (2001) Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat Neurosci 4:1079–1085

    Article  CAS  PubMed  Google Scholar 

  89. Tu JC, Xiao B, Yuan JP et al (1998) Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21:717–726

    Article  CAS  PubMed  Google Scholar 

  90. Tu JC, Xiao B, Naisbitt S et al (1999) Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23:583–592

    Article  CAS  PubMed  Google Scholar 

  91. Lan JY, Skeberdis VA, Jover T et al (2001) Activation of metabotropic glutamate receptor 1 accelerates NMDA receptor trafficking. J Neurosci 21:6058–6068

    CAS  PubMed  Google Scholar 

  92. Davidkova G, Carroll RC (2007) Characterization of the role of microtubule-associated protein 1B in metabotropic glutamate receptor-mediated endocytosis of AMPA receptors in hippocampus. J Neurosci 27:13273–13278

    Article  CAS  PubMed  Google Scholar 

  93. Dalfó E, Albasanz JL, Rodríguez A et al (2005) Abnormal group I metabotropic glutamate receptor expression and signaling in the frontal cortex in Pick disease. J Neuropathol Exp Neurol 64(7):638–647

    PubMed  Google Scholar 

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Acknowledgments

This work has been supported by Ministerio de Ciencia e Innovación (BFU2008-00138), Consejería de Sanidad-FISCAM of JCCM (PI-2007/50), Consejería de Educación y Ciencia of JCCM (PCI08-0125) and by the European Union through the Marie-Curie Research Training Network PRAIRIES (MRTN-CT-2006-035810). D.A.L. is an experienced researcher hired by FISCAM (MOV-2006_IE/09). I. B-Y. is a “Juan de la Cierva” researcher hired by MICINN.

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Castillo, C.A., León, D.A., Ballesteros-Yáñez, I. et al. Glutamate Differently Modulates Metabotropic Glutamate Receptors in Neuronal and Glial Cells. Neurochem Res 35, 1050–1063 (2010). https://doi.org/10.1007/s11064-010-0154-y

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