Glutathione restores the mechanism of synaptic plasticity in aged mice to that of the adult

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Robillard, Julie M ^a   Gordon, Grant R ^a   Choi, Hyun B ^a   Christie, Brian R ^b   MacVicar, Brian A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; CALCIUM CHANNEL L TYPE; GLUTATHIONE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AGE; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; SUPPLEMENTATION; ANIMAL; C57BL MOUSE; ELECTROPHYSIOLOGY; METABOLISM;

ANIMALIA; MUS;

ACETYLCYSTEINE; ANIMALS; CALCIUM CHANNELS, L-TYPE; ELECTROPHYSIOLOGY; GLUTATHIONE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 79957795797     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020676     Document Type: Article

References (42)

1. Tang LH, Aizenman E, (1993) The modulation of N-methyl-D-aspartate receptors by redox and alkylating reagents in rat cortical neurones in vitro. J Physiol(Lond.) 465: 303-323.
2. Bliss TV, Collingridge GL, (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39 doi:10.1038/361031a0.
3. Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel MF, et al. (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297: 211-218 doi:10.1126/science.1071795.
4. Maher P, (2005) The effects of stress and aging on glutathione metabolism. Ageing Res Rev 4: 288-314 doi:10.1016/j.arr.2005.02.005.
5. Serrano F, Klann E, (2004) Reactive oxygen species and synaptic plasticity in the aging hippocampus. Ageing Res Rev 3: 431-443 doi:10.1016/j.arr.2004.05.002.
6. Thibault O, Landfield PW, (1996) Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272: 1017-1020.
7. Burke SN, Barnes CA, (2010) Senescent synapses and hippocampal circuit dynamics. Trends Neurosci 33: 153-161 doi:10.1016/j.tins.2009.12.003.
8. Foster TC, (2007) Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 6: 319-325 doi:10.1111/j.1474-9726.2007.00283.x.
9. Shankar S, Teyler TJ, Robbins N, (1998) Aging differentially alters forms of long-term potentiation in rat hippocampal area CA1. J Neurophysiol 79: 334-341.
10. Fu A-L, Dong Z-H, Sun M-J, (2006) Protective effect of N-acetyl-L-cysteine on amyloid beta-peptide-induced learning and memory deficits in mice. Brain Res 1109: 201-206 doi:10.1016/j.brainres.2006.06.042.
11. Scragg JL, Dallas ML, Wilkinson JA, Varadi G, Peers C, (2008) Carbon monoxide inhibits L-type Ca2+ channels via redox modulation of key cysteine residues by mitochondrial reactive oxygen species. J Biol Chem 283: 24412-24419 doi:10.1074/jbc.M803037200.
12. Lipton SA, Choi Y-B, Takahashi H, Zhang D, Li W, et al. (2002) Cysteine regulation of protein function--as exemplified by NMDA-receptor modulation. Trends Neurosci 25: 474-480.
13. Choi YB, Lipton SA, (2000) Redox modulation of the NMDA receptor. Cell Mol Life Sci 57: 1535-1541.
14. Bodhinathan K, Kumar A, Foster TC, (2010) Intracellular redox state alters NMDA receptor response during aging through Ca2+/calmodulin-dependent protein kinase II. J Neurosci 30: 1914-1924 doi:10.1523/JNEUROSCI.5485-09.2010.
15. Steullet P, Neijt HC, Cuénod M, Do KQ, (2006) Synaptic plasticity impairment and hypofunction of NMDA receptors induced by glutathione deficit: relevance to schizophrenia. Neuroscience 137: 807-819 doi:10.1016/j.neuroscience.2005.10.014.
16. Almaguer-Melian W, Cruz-Aguado R, Bergado JA, (2000) Synaptic plasticity is impaired in rats with a low glutathione content. Synapse 38: 369-374 doi:10.1002/1098-2396(20001215)38:4<369::AID-SYN1>3.0.CO;2-Q.
17. Bindokas VP, Jordán J, Lee CC, Miller RJ, (1996) Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J Neurosci 16: 1324-1336.
18. Klann E, (1998) Cell-permeable scavengers of superoxide prevent long-term potentiation in hippocampal area CA1. J Neurophysiol 80: 452-457.
19. Knapp LT, Klann E, (2002) Potentiation of hippocampal synaptic transmission by superoxide requires the oxidative activation of protein kinase C. J Neurosci 22: 674-683.
20. Thiels E, Urban NN, Gonzalez-Burgos GR, Kanterewicz BI, Barrionuevo G, et al. (2000) Impairment of Long-term Potentiation and Associative Memory in Mice That Overexpress Extracellular Superoxide Dismutase. The Journal of Neuroscience 20: 7631-7639.
21. Auerbach JM, Segal M, (1997) Peroxide modulation of slow onset potentiation in rat hippocampus. J Neurosci 17: 8695-8701.
22. Kamsler A, Segal M, (2003) Hydrogen peroxide modulation of synaptic plasticity. J Neurosci 23: 269-276.
23. Foster TC, (2002) Regulation of synaptic plasticity in memory and memory decline with aging. Prog Brain Res 138: 283-303 doi:10.1016/S0079-6123(02)38083-X.
24. Ercal N, Treeratphan P, Hammond TC, Matthews RH, Grannemann NH, et al. (1996) In vivo indices of oxidative stress in lead-exposed C57BL/6 mice are reduced by treatment with meso-2,3-dimercaptosuccinic acid or N-acetylcysteine. Free Radic Biol Med 21: 157-161.
25. Lavoie S, Murray MM, Deppen P, Knyazeva MG, Berk M, et al. (2008) Glutathione precursor, N-acetyl-cysteine, improves mismatch negativity in schizophrenia patients. Neuropsychopharmacology 33: 2187-2199 doi:10.1038/sj.npp.1301624.
26. Shaw CA, (1998) Glutathione In The Nervous System. CRC Press 1st ed.
27. Koller KJ, Coyle JT, (1985) The characterization of the specific binding of [3H]-N-acetylaspartylglutamate to rat brain membranes. J Neurosci 5: 2882-2888.
28. Janáky R, Ogita K, Pasqualotto BA, Bains JS, Oja SS, et al. (1999) Glutathione and signal transduction in the mammalian CNS. J Neurochem 73: 889-902.
29. Aoyama K, Watabe M, Nakaki T, (2008) Regulation of neuronal glutathione synthesis. J Pharmacol Sci 108: 227-238.
30. Köhr G, Eckardt S, Lüddens H, Monyer H, Seeburg PH, (1994) NMDA receptor channels: subunit-specific potentiation by reducing agents. Neuron 12: 1031-1040.
31. Sommer D, Coleman S, Swanson SA, Stemmer PM, (2002) Differential susceptibilities of serine/threonine phosphatases to oxidative and nitrosative stress. Arch Biochem Biophys 404: 271-278.
32. Moussawi K, Pacchioni A, Moran M, Olive MF, Gass JT, et al. (2009) N-Acetylcysteine reverses cocaine-induced metaplasticity. Nat Neurosci 12: 182-189 doi:10.1038/nn.2250.
33. Pessah IN, Kim KH, Feng W, (2002) Redox sensing properties of the ryanodine receptor complex. Front Biosci 7: a72-79.
34. Hidalgo C, Bull R, Behrens MI, Donoso P, (2004) Redox regulation of RyR-mediated Ca2+ release in muscle and neurons. Biol Res 37: 539-552.
35. Bodhinathan K, Kumar A, Foster TC, (2010) Redox sensitive calcium stores underlie enhanced after hyperpolarization of aged neurons: role for ryanodine receptor mediated calcium signaling. J Neurophysiol 104: 2586-2593 doi:10.1152/jn.00577.2010.
36. Gant JC, Sama MM, Landfield PW, Thibault O, (2006) Early and simultaneous emergence of multiple hippocampal biomarkers of aging is mediated by Ca2+-induced Ca2+ release. J Neurosci 26: 3482-3490 doi:10.1523/JNEUROSCI.4171-05.2006.
37. Kumar A, Foster TC, (2004) Enhanced long-term potentiation during aging is masked by processes involving intracellular calcium stores. J Neurophysiol 91: 2437-2444 doi:10.1152/jn.01148.2003.
38. Hjelmstad GO, Nicoll RA, Malenka RC, (1997) Synaptic refractory period provides a measure of probability of release in the hippocampus. Neuron 19: 1309-1318.
39. Kato K, Clifford DB, Zorumski CF, (1993) Long-term potentiation during whole-cell recording in rat hippocampal slices. Neuroscience 53: 39-47.
40. Manabe T, Wyllie DJ, Perkel DJ, Nicoll RA, (1993) Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol 70: 1451-1459.
41. Perkel DJ, Nicoll RA, (1993) Evidence for all-or-none regulation of neurotransmitter release: implications for long-term potentiation. J Physiol (Lond.) 471: 481-500.
42. Ikegaya Y, Le Bon-Jego M, Yuste R, (2005) Large-scale imaging of cortical network activity with calcium indicators. Neurosci Res 52: 132-138 doi:10.1016/j.neures.2005.02.004.