Activation of mGluR5 attenuates NMDA-induced neurotoxicity through disruption of the NMDAR-PSD-95 complex and preservation of mitochondrial function in differentiated PC12 cells

International Journal of Molecular Sciences

Volumn 15, Issue 6, 2014, Pages 10892-10907

  Dai, Shu Hui ^a   Qin, Na ^a   Chen, Tao ^a,b   Luo, Peng ^a   Zhang, Lei ^a   Rao, Wei ^a   Yang, Yue Fan ^a   Jiang, Xiao Fan ^a   Fei, Zhou ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b The 123th Hospital of PLA   (China)

Author keywords

Glutamate; MGlu receptor; Mitochondrial dysfunction; NMDAR (N methyl D aspartate receptor) receptor; Post synaptic density protein 95

Indexed keywords

2 CHLORO 5 HYDROXYPHENYLGLYCINE; CASPASE 3; CASPASE 9; CYTOCHROME C; IONOTROPIC RECEPTOR; LACTATE DEHYDROGENASE; METABOTROPIC RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; 2-CHLORO-5-HYDROXYPHENYLGLYCINE; CALCIUM; DLGH4 PROTEIN, RAT; GLYCINE; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYLASPARTIC ACID; PHENYLACETIC ACID DERIVATIVE; PROTEIN BINDING; SIGNAL PEPTIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EXCITOTOXICITY; FLOW CYTOMETRY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL MEMBRANE POTENTIAL; NEUROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; MITOCHONDRION; PC12 CELL LINE; STEREOISOMERISM; TOXICITY;

ANIMALS; APOPTOSIS; CALCIUM; CELL DIFFERENTIATION; CELL SURVIVAL; CYTOCHROMES C; GLYCINE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MEMBRANE PROTEINS; MITOCHONDRIA; N-METHYLASPARTATE; PC12 CELLS; PHENYLACETATES; PROTEIN BINDING; RATS; REACTIVE OXYGEN SPECIES; RECEPTOR, METABOTROPIC GLUTAMATE 5; RECEPTORS, N-METHYL-D-ASPARTATE; STEREOISOMERISM;

EID: 84902589983     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms150610892     Document Type: Article

References (51)

1. Durand, D.; Pampillo, M.; Caruso, C.; Lasaga, M. Role of metabotropic glutamate receptors in the control of neuroendocrine function. Neuropharmacology 2008, 55, 577-583.
2. Brittain, J.M.; Chen, L.; Wilson, S.M.; Brustovetsky, T.; Gao, X.; Ashpole, N.M.; Molosh, A.I.; You, H.; Hudmon, A.; Shekhar, A.; et al. Neuroprotection against traumatic brain injury by a peptide derived from the collapsin response mediator protein 2 (CRMP2). J. Biol. Chem. 2011, 286, 37778-37792.
3. Brennan-Minnella, A.M.; Shen, Y.; El-Benna, J.; Swanson, R.A. Phosphoinositide 3-kinase couples NMDA receptors to superoxide release in excitotoxic neuronal death. Cell Death Dis. 2013, 4, doi:10.1038/cddis.2013.111.
4. Degos, V.; Peineau, S.; Nijboer, C.; Kaindl, A.M.; Sigaut, S.; Favrais, G.; Plaisant, F.; Teissier, N.; Gouadon, E.; Lombet, A.; et al. G protein-coupled receptor kinase 2 and group I metabotropic glutamate receptors mediate inflammation-induced sensitization to excitotoxic neurodegeneration. Ann. Neurol. 2013, 73, 667-678.
5. Hsieh, M.H.; Ho, S.C.; Yeh, K.Y.; Pawlak, C.R.; Chang, H.M.; Ho, Y.J.; Lai, T.J.; Wu, F.Y. Blockade of metabotropic glutamate receptors inhibits cognition and neurodegeneration in an MPTP-induced Parkinson's disease rat model. Pharmacol. Biochem. Behav. 2012, 102, 64-71.
6. Sheng, M. The postsynaptic NMDA-receptor-PSD-95 signaling complex in excitatory synapses of the brain. J. Cell Sci. 2001, 114, 1251.
7. Martel, M.A.; Ryan, T.J.; Bell, K.F.; Fowler, J.H.; McMahon, A.; Al-Mubarak, B.; Komiyama, N.H.; Horsburgh, K.; Kind, P.C.; Grant, S.G.; et al. The subtype of GluN2 C-terminal domain determines the response to excitotoxic insults. Neuron 2012, 74, 543-556.
8. Li, B.; Otsu, Y.; Murphy, T.H.; Raymond, L.A. Developmental decrease in NMDA receptor desensitization associated with shift to synapse and interaction with postsynaptic density-95. J. Neurosci. 2003, 23, 11244-11254.
9. Hu, S.Q.; Zhu, J.; Pei, D.S.; Zong, Y.Y.; Yan, J.Z.; Hou, X.Y.; Zhang, G.Y. Overexpression of the PDZ1 domain of PSD-95 diminishes ischemic brain injury via inhibition of the GluR6. PSD-95. MLK3 pathway. J. Neurosci. Res. 2009, 87, 3626-3638.
10. Aarts, M.; Liu, Y.; Liu, L.; Besshoh, S.; Arundine, M.; Gurd, J.W.; Wang, Y.T.; Salter, M.W.; Tymianski, M. Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science 2002, 298, 846-850.
11. 2+ in neurons. J. Neurochem. 2013, 127, 620-631.
12. Alagarsamy, S.; Rouse, S.T.; Junge, C.; Hubert, G.W.; Gutman, D.; Smith, Y.; Conn, P.J. NMDA-induced phosphorylation and regulation of mGluR5. Pharmacol. Biochem. Behav. 2002, 73, 299-306.
13. Matta, J.A.; Ashby, M.C.; Sanz-Clemente, A.; Roche, K.W.; Isaac, J.T. mGluR5 and NMDA receptors drive the experience-and activity-dependent NMDA receptor NR2B to NR2A subunit switch. Neuron 2011, 70, 339-351.
14. Sureda, F.X.; Viu, E.; Zapata, A.; Capdevila, J.L.; Camins, A.; Escubedo, E.; Camarasa, J.; Trullas, R. Modulation of NMDA-induced cytosolic calcium levels by ACPC in cultured cerebellar granule cells. Neuroreport 1996, 7, 1824-1828.
15. Chen, T.; Fei, F.; Jiang, X.F.; Zhang, L.; Qu, Y.; Huo, K.; Fei, Z. Down-regulation of Homer1b/c attenuates glutamate-mediated excitotoxicity through endoplasmic reticulum and mitochondria pathways in rat cortical neurons. Free Radic. Biol. Med. 2012, 52, 208-217.
16. Byrnes, K.R.; Loane, D.J.; Stoica, B.A.; Zhang, J.; Faden, A.I. Delayed mGluR5 activation limits neuroinflammation and neurodegeneration after traumatic brain injury. J. Neuroinflamm. 2012, 9, doi:10.1186/1742-2094-9-43.
17. Izumi, Y.; Zorumski, C.F. NMDA receptors, mGluR5, and endocannabinoids are involved in a cascade leading to hippocampal long-term depression. Neuropsychopharmacology 2012, 37, 609-617.
18. Ben-Mabrouk, F.; Amos, L.B.; Tryba, A.K. Metabotropic glutamate receptors (mGluR5) activate transient receptor potential canonical channels to improve the regularity of the respiratory rhythm generated by the pre-Botzinger complex in mice. Eur. J. Neurosci. 2012, 35, 1725-1737.
19. Gerber, U.; Gee, C.E.; Benquet, P. Metabotropic glutamate receptors: intracellular signaling pathways. Curr. Opin. Pharmacol. 2007, 7, 56-61.
20. O'Leary, D.M.; Movsesyan, V.; Vicini, S.; Faden, A.I. Selective mGluR5 antagonists MPEP and SIB-1893 decrease NMDA or glutamate-mediated neuronal toxicity through actions that reflect NMDA receptor antagonism. Br. J. Pharmacol. 2000, 131, 1429-1437.
21. Movsesyan, V.A.; O'Leary, D.M.; Fan, L.; Bao, W.; Mullins, P.G.; Knoblach, S.M.; Faden, A.I. mGluR5 antagonists 2-methyl-6-(phenylethynyl)-pyridine and (E)-2-methyl-6-(2-phenylethenyl)-pyridine reduce traumatic neuronal injury in vitro and in vivo by antagonizing N-methyl-D-aspartate receptors. J. Pharmacol. Exp. Ther. 2001, 296, 41-47.
22. Allen, J.W.; Knoblach, S.M.; Faden, A.I. Activation of group I metabotropic glutamate receptors reduces neuronal apoptosis but increases necrotic cell death in vitro. Cell Death Differ. 2000, 7, 470-476.
23. Movsesyan, V.A.; Stoica, B.A.; Faden, A.I. MGLuR5 activation reduces beta-amyloid-induced cell death in primary neuronal cultures and attenuates translocation of cytochrome c and apoptosis-inducing factor. J. Neurochem. 2004, 89, 1528-1536.
24. Kemp, A.; Manahan-Vaughan, D. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc. Natl. Acad. Sci. USA 2004, 101, 8192-8197.
25. Chen, T.; Zhang, L.; Qu, Y.; Huo, K.; Jiang, X.; Fei, Z. The selective mGluR5 agonist CHPG protects against traumatic brain injury in vitro and in vivo via ERK and Akt pathway. Int. J. Mol. Med. 2012, 29, 630-636.
26. Chen, T.; Cao, L.; Dong, W.; Luo, P.; Liu, W.; Qu, Y.; Fei, Z. Protective effects of mGluR5 positive modulators against traumatic neuronal injury through PKC-dependent activation of MEK/ERK pathway. Neurochem. Res. 2012, 37, 983-990.
27. Brenman, J.E.; Chao, D.S.; Gee, S.H.; McGee, A.W.; Craven, S.E.; Santillano, D.R.; Wu, Z.; Huang, F.; Xia, H.; Peters, M.F.; et al. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 1996, 84, 757-767.
28. Luo, P.; Yang, Y.; Liu, W.; Rao, W.; Bian, H.; Li, X.; Chen, T.; Liu, M.; Zhao, Y.; Dai, S.; et al. Downregulation of postsynaptic density-95-interacting regulator of spine morphogenesis reduces glutamate-induced excitotoxicity by differentially regulating glutamate receptors in rat cortical neurons. FEBS J. 2013, 280, 6114-6127.
29. 2+-calmodulin dependent protein kinase II to N-methyl-D-aspartate receptor subunit 2B in rat brain. Acta Pharmacol. Sin. 2004, 25, 176-180.
30. Migaud, M.; Charlesworth, P.; Dempster, M.; Webster, L.C.; Watabe, A.M.; Makhinson, M.; He, Y.; Ramsay, M.F.; Morris, R.G.; Morrison, J.H.; et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 1998, 396, 433-439.
31. Sattler, R.; Xiong, Z.; Lu, W.Y.; Hafner, M.; MacDonald, J.F.; Tymianski, M. Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 1999, 284, 1845-1848.
32. Zhou, L.; Li, F.; Xu, H.B.; Luo, C.X.; Wu, H.Y.; Zhu, M.M.; Lu, W.; Ji, X.; Zhou, Q.G.; Zhu, D.Y. Treatment of cerebral ischemia by disrupting ischemia-induced interaction of nNOS with PSD-95. Nat. Med. 2010, 16, 1439-1443.
33. Zieminska, E.; Stafiej, A.; Lazarewicz, J.W. Role of group I metabotropic glutamate receptors and NMDA receptors in homocysteine-evoked acute neurodegeneration of cultured cerebellar granule neurones. Neurochem. Int. 2003, 43, 481-492.
34. Blaabjerg, M.; Kristensen, B.W.; Bonde, C.; Zimmer, J. The metabotropic glutamate receptor agonist 1S,3R-ACPD stimulates and modulates NMDA receptor mediated excitotoxicity in organotypic hippocampal slice cultures. Brain Res. 2001, 898, 91-104.
35. Bonsi, P.; Platania, P.; Martella, G.; Madeo, G.; Vita, D.; Tassone, A.; Bernardi, G.; Pisani, A. Distinct roles of group I mGlu receptors in striatal function. Neuropharmacology 2008, 55, 392-395.
36. Huang, H.; van den Pol, A.N. Rapid direct excitation and long-lasting enhancement of NMDA response by group I metabotropic glutamate receptor activation of hypothalamic melanin-concentrating hormone neurons. J. Neurosci. 2007, 27, 11560-11572.
37. Ciruela, F.; Soloviev, M.M.; Chan, W.Y.; McIlhinney, R.A. Homer-1c/Vesl-1L modulates the cell surface targeting of metabotropic glutamate receptor type 1α: Evidence for an anchoring function. Mol. Cell. Neurosci. 2000, 15, 36-50.
38. 2+ pump isoform 4b. Biochim. Biophys. Acta 2009, 1793, 1023-1032.
39. Hayashi, M.K.; Tang, C.; Verpelli, C.; Narayanan, R.; Stearns, M.H.; Xu, R.M.; Li, H.; Sala, C.; Hayashi, Y. The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 2009, 137, 159-171.
40. Khoboko, T.; Russell, V.A. Effects of development and dopamine depletion on striatal NMDA receptor-mediated calcium uptake. Metab. Brain Dis. 2008, 23, 9-30.
41. Clapham, D.E. Calcium signaling. Cell 2007, 131, 1047-1058.
42. Chen, T.; Yang, Y.F.; Luo, P.; Liu, W.; Dai, S.H.; Zheng, X.R.; Fei, Z.; Jiang, X.F. Homer1 knockdown protects dopamine neurons through regulating calcium homeostasis in an in vitro model of Parkinson's disease. Cell Signal. 2013, 25, 2863-2870.
43. +-induced cytotoxicity in PC12 cells: Potential role of Homer1. PLoS One 2013, 8, e55601.
44. Pivovarova, N.B.; Andrews, S.B. Calcium-dependent mitochondrial function and dysfunction in neurons. FEBS J. 2010, 277, 3622-3636.
45. Friberg, H.; Wieloch, T. Mitochondrial permeability transition in acute neurodegeneration. Biochimie 2002, 84, 241-250.
46. Norenberg, M.D.; Rao, K.V. The mitochondrial permeability transition in neurologic disease. Neurochem. Int. 2007, 50, 983-997.
47. Gibson, G.E.; Starkov, A.; Blass, J.P.; Ratan, R.R.; Beal, M.F. Cause and consequence: Mitochondrial dysfunction initiates and propagates neuronal dysfunction, neuronal death and behavioral abnormalities in age-associated neurodegenerative diseases. Biochim. Biophys. Acta 2010, 1802, 122-134.
48. Bezprozvanny, I. Calcium signaling and neurodegenerative diseases. Trends Mol. Med. 2009, 15, 89-100.
49. Lipton, S.A. Failures and successes of NMDA receptor antagonists: molecular basis for the use of open-channel blockers like memantine in the treatment of acute and chronic neurologic insults. NeuroRx 2004, 1, 101-110.
50. Wang, P.; Zhang, H.; Chu, F.; Xu, X.; Lin, J.; Chen, C.; Li, G.; Cheng, Y.; Wang, L.; Li, Q.; et al. Synthesis and protective effect of new ligustrazine-benzoic acid derivatives against CoCl2-induced neurotoxicity in differentiated PC12 cells. Molecules 2013, 18, 13027-13042.
51. Sung, D.K.; Chang, Y.S.; Kang, S.; Song, H.Y.; Park, W.S.; Lee, B.H. Comparative evaluation of hypoxic-ischemic brain injury by flow cytometric analysis of mitochondrial membrane potential with JC-1 in neonatal rats. J. Neurosci. Methods 2010, 193, 232-238.