Enhancement of long-term depression by soluble amyloid β protein in rat hippocampus is mediated by metabotropic glutamate receptor and involves activation of p38MAPK, STEP and caspase-3

Neuroscience

Volumn 253, Issue , 2013, Pages 435-443

  Chen, X ^a   Lin, R ^a   Chang, L ^a   Xu, S ^a   Wei, X ^a   Zhang, J ^a   Wang, C ^a   Anwyl, R ^b   Wang, Q ^a  

^a NINGBO UNIVERSITY   (China)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Alzheimer's disease; Amyloid beta protein; Hippocampus; Long term depression; Metabotropic glumate receptor; Synaptic plasticity

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 3,5 DIHYDROXYPHENYLGLYCINE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; AMYLOID BETA PROTEIN[1-42]; ARSENOSOBENZENE; BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; MAMMALIAN TARGET OF RAPAMYCIN; METABOTROPIC RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; RAPAMYCIN; STRIATAL ENRICHED PROTEIN TYROSINE PHOSPHATASE; TAPI 2; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME INHIBITOR; UNCLASSIFIED DRUG; VANADATE SODIUM;

ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN SLICE; CONTROLLED STUDY; DENTATE GYRUS; DISEASE COURSE; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; GRANULE CELL; HIPPOCAMPUS; INTRACELLULAR SIGNALING; LEARNING DISORDER; LONG TERM DEPRESSION; MALE; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

3,5-DIHYDROXYPHENYLGLYCINE; A-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID RECEPTOR; AD; ALZHEIMER'S DISEASE; AMPAR; AMYLOID BETA PROTEIN; AMYLOID-Β PROTEIN; AΒ; DHPG; EPSP; EXCITATORY POSTSYNAPTIC POTENTIAL; FEPSPS; FIELD EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LONG-TERM DEPRESSION; LONG-TERM POTENTIATION; LTD; LTP; MAMMALIAN TARGET OF RAPAMYCIN; METABOTROPIC GLUMATE RECEPTOR; METRABOTROPIC GLUMATE RECEPTORS; MGLURS; MTOR; N-METHYL-D-ASPARTATE RECEPTOR; NEURONAL PENTRAXIN RECEPTOR; NMDAR; NPR; P38 MITOGEN-ACTIVATED PROTEIN KINASE; P38MAPK; PAO; PHENYLARSINE OXIDE; POSTSYNAPTIC PROTEIN TYROSINE PHOSPHATASE; PTP; SLFS; SO; SODIUM ORTHOVANADATE; STEP; STRIATAL-ENRICHED PROTEIN TYROSINE PHOSPHATASE; STRONG LOW-FREQUENCY STIMULATION; SYNAPTIC PLASTICITY; TACE; TUMOR NECROSIS FACTOR-Α CONVERTING ENZYME; WEAK LOW-FREQUENCY STIMULATION; WLFS;

2-AMINO-5-PHOSPHONOVALERATE; AMINO ACIDS; AMYLOID BETA-PEPTIDES; ANIMALS; CASPASE 3; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; HIPPOCAMPUS; IMMUNOSUPPRESSIVE AGENTS; LONG-TERM SYNAPTIC DEPRESSION; MALE; METHOXYHYDROXYPHENYLGLYCOL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PATCH-CLAMP TECHNIQUES; PEPTIDE FRAGMENTS; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; SIROLIMUS; XANTHENES;

EID: 84885197799     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.08.054     Document Type: Article

References (46)

1. Ashabi G., Ramin M., Azizi P., Taslimi Z., Alamdary S.Z., Haghparast A., Ansari N., Motamedi F., Khodagholi F. ERK and p38 inhibitors attenuate memory deficits and increase CREB phosphorylation and PGC-1alpha levels in Abeta-injected rats. Behav Brain Res 2012, 232:165-173.
2. Ashabi G., Alamdary S.Z., Ramin M., Khodagholi F. Reduction of hippocampal apoptosis by intracerebroventricular administration of extracellular signal-regulated protein kinase and/or p38 inhibitors in amyloid beta rat model of Alzheimer's disease: involvement of nuclear-related factor-2 and nuclear factor-kappaB. Basic Clin Pharmacol Toxicol 2013, 112:145-155.
3. Baudry M., Greget R., Pernot F., Bouteiller J.-M., Xiaoning B. Roles of group I metabotropic glutamate receptors under physiological conditions and in neurodegeneration. Wiley Interdiscip Rev 2012, 1:523-532.
4. Black R.A. Tumor necrosis factor-alpha converting enzyme. Int J Biochem Cell Biol 2002, 34:1-5.
5. Braithwaite S.P., Adkisson M., Leung J., Nava A., Masterson B., Urfer R., Oksenberg D., Nikolich K. Regulation of NMDA receptor trafficking and function by striatal-enriched tyrosine phosphatase (STEP). Eur J Neurosci 2006, 23:2847-2856.
6. Cavalli V., Vilbois F., Corti M., Marcote M.J., Tamura K., Karin M., Arkinstall S., Gruenberg J. The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol Cell 2001, 7:421-432.
7. Cheng L., Yin W.J., Zhang J.F., Qi J.S. Amyloid beta-protein fragments 25-35 and 31-35 potentiate long-term depression in hippocampal CA1 region of rats in vivo. Synapse 2009, 63:206-214.
8. Chin J., Palop J.J., Puolivali J., Massaro C., Bien-Ly N., Gerstein H., Scearce-Levie K., Masliah E., Mucke L. Fyn kinase induces synaptic and cognitive impairments in a transgenic mouse model of Alzheimer's disease. J Neurosci 2005, 25:9694-9703.
9. Cho R.W., Park J.M., Wolff S.B.E., Xu D., Hopf C., Kim J.-A., Reddy R.C., Petralia R.S., Perin M.S., Linden D.J. MGluR1/5-dependent long-term depression requires the regulated ectodomain cleavage of neuronal pentraxin NPR by TACE. Neuron 2008, 57:858-871.
10. Collingridge G.L., Peineau S., Howland J.G., Wang Y.T. Long-term depression in the CNS. Nat Rev Neurosci 2010, 11:459-473.
11. D'Amelio M., Cavallucci V., Cecconi F. Neuronal caspase-3 signaling: not only cell death. Cell Death Differ 2009, 17:1104-1114.
12. D'Amelio M., Cavallucci V., Middei S., Marchetti C., Pacioni S., Ferri A., Diamantini A., De Zio D., Carrara P., Battistini L., Moreno S., Bacci A., Ammassari-Teule M., Marie H., Cecconi F. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat Neurosci 2011, 14:69-76.
13. Hou L., Klann E. Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci 2004, 24:6352-6361.
14. Hou L., Antion M.D., Hu D., Spencer C.M., Paylor R., Klann E. Dynamic translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 2006, 51:441-454.
15. Huber K.M., Kayser M.S., Bear M.F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 2000, 288:1254-1257.
16. Jo J., Whitcomb D.J., Olsen K.M., Kerrigan T.L., Lo S.C., Bru-Mercier G., Dickinson B., Scullion S., Sheng M., Collingridge G., Cho K. Abeta(1-42) inhibition of LTP is mediated by a signaling pathway involving caspase-3, Akt1 and GSK-3beta. Nat Neurosci 2011, 14:545-547.
17. Kim J.-H., Anwyl R., Suh Y.-H., Djamgoz M.B.A., Rowan M.J. Use-dependent effects of amyloidogenic fragments of β-amyloid precursor protein on synaptic plasticity in rat hippocampus in vivo. J Neurosci 2001, 21:1327-1333.
18. Koffie R.M., Meyer-Luehmann M., Hashimoto T., Adams K.W., Mielke M.L., Garcia-Alloza M., Micheva K.D., Smith S.J., Kim M.L., Lee V.M., Hyman B.T., Spires-Jones T.L. Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci USA 2009, 106:4012-4017.
19. Kotilinek L.A., Westerman M.A., Wang Q., Panizzon K., Lim G.P., Simonyi A., Lesne S., Falinska A., Younkin L.H., Younkin S.G., Rowan M., Cleary J., Wallis R.A., Sun G.Y., Cole G., Frautschy S., Anwyl R., Ashe K.H. Cyclooxygenase-2 inhibition improves amyloid-beta-mediated suppression of memory and synaptic plasticity. Brain 2008, 131:651-664.
20. Kurup P., Zhang Y., Xu J., Venkitaramani D.V., Haroutunian V., Greengard P., Nairn A.C., Lombroso P.J. Abeta-mediated NMDA receptor endocytosis in Alzheimer's disease involves ubiquitination of the tyrosine phosphatase STEP61. J Neurosci 2010, 30:5948-5957.
21. Li Z., Sheng M. Caspases in synaptic plasticity. Mol Brain 2012, 5:15.
22. Li S., Hong S., Shepardson N.E., Walsh D.M., Shankar G.M., Selkoe D. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009, 62:788-801.
23. Li Z., Jo J., Jia J.M., Lo S.C., Whitcomb D.J., Jiao S., Cho K., Sheng M. Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 2010, 141:859-871.
24. Li S., Jin M., Koeglsperger T., Shepardson N.E., Shankar G.M., Selkoe D.J. Soluble Abeta oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J Neurosci 2011, 31:6627-6638.
25. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002, 25:103-126.
26. Moult P.R. Tyrosine phosphatases regulate AMPA receptor trafficking during metabotropic glutamate receptor-mediated long-term depression. J Neurosci 2006, 26:2544-2554.
27. Moult P.R., Correa S.A., Collingridge G.L., Fitzjohn S.M., Bashir Z.I. Co-activation of p38 mitogen-activated protein kinase and protein tyrosine phosphatase underlies metabotropic glutamate receptor-dependent long-term depression. J Physiol 2008, 586:2499-2510.
28. Nicholls R.E., Alarcon J.M., Malleret G., Carroll R.C., Grody M., Vronskaya S., Kandel E.R. Transgenic mice lacking NMDAR-dependent LTD exhibit deficits in behavioral flexibility. Neuron 2008, 58:104-117.
29. Olsen K.M., Sheng M. NMDA receptors and BAX are essential for Abeta impairment of LTP. Sci Rep 2012, 2:225.
30. Paul S., Nairn A.C., Wang P., Lombroso P.J. NMDA-mediated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling. Nat Neurosci 2003, 6:34-42.
31. Peineau S. A systematic investigation of the protein kinases involved in NMDA receptor-dependent LTD: evidence for a role of GSK-3 but not other serine/threonine kinases. Mol Brain 2009, 2:22.
32. Rowan M.J., Klyubin I., Wang Q., Anwyl R. Synaptic plasticity disruption by amyloid beta protein: modulation by potential Alzheimer's disease modifying therapies. Biochem Soc Trans 2005, 33:563-567.
33. Rush A.M., Wu J., Rowan M.J., Anwyl R. Group I metabotropic glutamate receptor (mGluR)-dependent long-term depression mediated via p38 mitogen-activated protein kinase is inhibited by previous high-frequency stimulation and activation of mGluRs and protein kinase C in the rat dentate gyrus in vitro. J Neurosci 2002, 22:6121-6128.
34. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
35. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., Brett F.M., Farrell M.A., Rowan M.J., Lemere C.A., Regan C.M., Walsh D.M., Sabatini B.L., Selkoe D.J. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 2008, 14:837-842.
36. Tsokas P., Ma T., Iyengar R., Landau E.M., Blitzer R.D. Mitogen-activated protein kinase upregulates the dendritic translation machinery in long-term potentiation by controlling the mammalian target of rapamycin pathway. J Neurosci 2007, 27:5885-5894.
37. Volk L.J., Pfeiffer B.E., Gibson J.R., Huber K.M. Multiple Gq-coupled receptors converge on a common protein synthesis-dependent long-term depression that is affected in fragile X syndrome mental retardation. J Neurosci 2007, 27:11624-11634.
38. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
39. Walsh D.M., Klyubin I., Fadeeva J.V., Rowan M.J., Selkoe D.J. Amyloid-beta oligomers: their production, toxicity and therapeutic inhibition. Biochem Soc Trans 2002, 30:552-557.
40. Wang Q., Walsh D.M., Rowan M.J., Selkoe D.J., Anwyl R. Block of long-term potentiation by naturally secreted and synthetic amyloid beta-peptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase, cyclin-dependent kinase 5, and p38 mitogen-activated protein kinase as well as metabotropic glutamate receptor type 5. J Neurosci 2004, 24:3370-3378.
41. Wang Q., Wu J., Rowan M.J., Anwyl R. Beta-amyloid inhibition of long-term potentiation is mediated via tumor necrosis factor. Eur J Neurosci 2005, 22:2827-2832.
42. Wang Q.W., Rowan M.J., Anwyl R. Inhibition of LTP by beta-amyloid is prevented by activation of beta2 adrenoceptors and stimulation of the cAMP/PKA signalling pathway. Neurobiol Aging 2009, 30:1608-1613.
43. Wong T.P., Howland J.G., Robillard J.M., Ge Y., Yu W., Titterness A.K., Brebner K., Liu L., Weinberg J., Christie B.R., Phillips A.G., Wang Y.T. Hippocampal long-term depression mediates acute stress-induced spatial memory retrieval impairment. Proc Natl Acad Sci USA 2007, 104:11471-11476.
44. Xu J., Kurup P., Zhang Y., Goebel-Goody S.M., Wu P.H., Hawasli A.H., Baum M.L., Bibb J.A., Lombroso P.J. Extrasynaptic NMDA receptors couple preferentially to excitotoxicity via calpain-mediated cleavage of STEP. J Neurosci 2009, 29:9330-9343.
45. Zhang Y., Venkitaramani D.V., Gladding C.M., Kurup P., Molnar E., Collingridge G.L., Lombroso P.J. The tyrosine phosphatase STEP mediates AMPA receptor endocytosis after metabotropic glutamate receptor stimulation. J Neurosci 2008, 28:10561-10566.
46. Zhang Y., Kurup P., Xu J., Carty N., Fernandez S.M., Nygaard H.B., Pittenger C., Greengard P., Strittmatter S.M., Nairn A.C., Lombroso P.J. Genetic reduction of striatal-enriched tyrosine phosphatase (STEP) reverses cognitive and cellular deficits in an Alzheimer's disease mouse model. Proc Natl Acad Sci USA 2010, 107:19014-19019.