Intracellular redox state alters NMDA receptor response during aging through Ca2+/calmodulin-dependent protein kinase II

Journal of Neuroscience

Volumn 30, Issue 5, 2010, Pages 1914-1924

  Bodhinathan, Karthik ^a   Kumar, Ashok ^a   Foster, Thomas C ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AGE; AGED; AGING; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; HIPPOCAMPUS; MALE; NERVE CELL PLASTICITY; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; RAT;

AGING; ANIMALS; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; HIPPOCAMPUS; NEURONAL PLASTICITY; OXIDATION-REDUCTION; RATS; RATS, INBRED F344; REACTIVE OXYGEN SPECIES; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 76149095657     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5485-09.2010     Document Type: Article

References (56)

1. Abele R, Lampinen M, Keinänen K, Madden DR (1998) Disulfide bonding and cysteine accessibility in the alpha-amino-3-hydroxy-5-methylisoxazole-4- propionic acid receptor subunit GluRD. Implications for redox modulation of glutamate receptors. J Biol Chem 273:25132-25138.
2. Aizenman E, Lipton SA, Loring RH (1989) Selective modulation of NMDA responses by reduction and oxidation. Neuron 2:1257-1263.
3. Aizenman E, Hartnett KA, Reynolds IJ (1990) Oxygen free radicals regulate NMDA receptor function via a redox modulatory site. Neuron 5:841-846.
4. Barnes CA, Rao G, Shen J (1997) Age-related decrease in the N-methyl-D-aspartateR-mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol Aging 18:445-452.
5. Ben-Ari Y, Aniksztejn L, Bregestovski P (1992) Protein kinase C modulation of NMDA currents: an important link for LTP induction. Trends Neurosci 15:333-339.
6. Bernard CL, Hirsch JC, Khazipov R, Ben-Ari Y, Gozlan H (1997) Redox modulation of synaptic responses and plasticity in rat CA1 hippocampal neurons. Exp Brain Res 113:343-352.
7. Billard JM, Rouaud E (2007) Deficit of NMDA receptor activation in CA1 hippocampal area of aged rats is rescued by D-cycloserine. Eur J Neurosci 25:2260-2268.
8. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
9. Boric K, Muñoz P, Gallagher M, Kirkwood A (2008) Potential adaptive function for altered long-term potentiation mechanisms in aging hippocampus. J Neurosci 28:8034-8039.
10. Cady C, Evans MS, Brewer GJ (2001) Age-related differences in NMDA responses in cultured rat hippocampal neurons. Brain Res 921:1-11.
11. Cai SQ, Sesti F (2009) Oxidation of a potassium channel causes progressive sensory function loss during aging. Nat Neurosci 12:611-617.
12. Choi YB, Lipton SA (2000) Redox modulation of the NMDA receptor. Cell Mol Life Sci 57:1535-1541.
13. 2+ modulation of the nmda receptor. J Neurosci 21:392-400.
14. Ciorba MA, Heinemann SH, Weissbach H, Brot N, Hoshi T (1997) Modulation of potassium channel function by methionine oxidation and reduction. Proc Natl Acad Sci U S A 94:9932-9937.
15. Foster TC (1999) Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res Brain Res Rev 30:236-249.
16. Foster TC (2002) Regulation of synaptic plasticity in memory and memory decline with aging. Prog Brain Res 138:283-303.
17. Foster TC (2006) Biological markers of age-related memory deficits: treatment of senescent physiology. CNS Drugs 20:153-166.
18. Foster TC (2007) Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 6:319-325.
19. 2+ dysregulation with brain aging. J Neurosci 21:4066-4073.
20. Gardoni F, Mauceri D, Malinverno M, Polli F, Costa C, Tozzi A, Siliquini S, Picconi B, Cattabeni F, Calabresi P, Di Luca M (2009) Decreased NR2B subunit synaptic levels cause impaired long-term potentiation but not long-term depression. J Neurosci 29:669-677.
21. Gozlan H, Khazipov R, Diabira D, Ben-Ari Y (1995) In CA1 hippocampal neurons, the redox state of NMDA receptors determines LTP expressed by NMDA but not by AMPA receptors. J Neurophysiol 73:2612-2617.
22. Griendling KK, Sorescu D, Lassègue B, Ushio-Fukai M (2000) Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol 20:2175-2183.
23. Hsu KS, Huang CC, Liang YC, Wu HM, Chen YL, Lo SW, Ho WC (2002) Alterations in the balance of protein kinase and phosphatase activities and age-related impairments of synaptic transmission and long-term potentiation. Hippocampus 12:787-802.
24. Knapp LT, Klann E (2000) Superoxide-induced stimulation of protein kinase C via thiol modification and modulation of zinc content. J Biol Chem 275:24136-24145.
25. 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.
26. Li BS, Sun MK, Zhang L, Takahashi S, Ma W, Vinade L, Kulkarni AB, Brady RO, Pant HC (2001) Regulation of NMDA receptors by cyclin-dependent kinase-5. Proc Natl Acad Sci U S A 98:12742-12747.
27. Lieberman DN, Mody I (1994) Regulation of NMDA channel function by endogenous Ca(2+)-dependent phosphatase. Nature 369: 235-239.
28. Lipton SA, Choi YB, Takahashi H, Zhang D, Li W, Godzik A, Bankston LA (2002) Cysteine regulation of protein function - as exemplified by NMDA-receptor modulation. Trends Neurosci 25:474-480.
29. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175-190.
30. Long LH, Liu J, Liu RL, Wang F, Hu ZL, Xie N, Fu H, Chen JG (2009) Differential effects of methionine and cysteine oxidation on [Ca2+] i in cultured hippocampal neurons. Cell Mol Neurobiol 29:7-15.
31. Magnusson KR, Bai L, Zhao X (2005) The effects of aging on different C-terminal splice forms of the zeta1(NR1) subunit of the N-methyl-d-aspartate receptor in mice. Brain Res Mol Brain Res 135:141-149.
32. Magnusson KR, Kresge D, Supon J (2006) Differential effects of aging on NMDA receptors in the intermediate versus the dorsal hippocampus. Neurobiol Aging 27:324-333.
33. Mazor D, Golan E, Philip V, Katz M, Jafe A, Ben-Zvi Z, Meyerstein N (1996) Red blood cell permeability to thiol compounds following oxidative stress. Eur J Haematol 57:241-246.
34. Morishita W, Marie H, Malenka RC (2005) Distinct triggering and expression mechanisms underlie LTD of AMPA and NMDA synaptic responses. Nat Neurosci 8:1043-1050.
35. 2+ channels. J Neurosci 18:3171-3179.
36. Norris CM, Halpain S, Foster TC (1998b) Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging. J Neurophysiol 80:1567-1570.
37. Norris CM, Blalock EM, Chen KC, Porter NM, Thibault O, Kraner SD, Landfield PW (2010) Hippocampal 'zipper' slice studies reveal a necessary role for calcineurin in the increased activity of L-type Ca(2+) channels with aging. Neurobiol Aging 31:328-338.
38. Parihar MS, Kunz EA, Brewer GJ (2008) Age-related decreases in NAD(P)H and glutathione cause redox declines before ATP loss during glutamate treatment of hippocampal neurons. J Neurosci Res 86:2339-2352.
39. Poon HF, Calabrese V, Calvani M, Butterfield DA (2006) Proteomics analyses of specific protein oxidation and protein expression in aged rat brain and its modulation by L-acetylcarnitine: insights into the mechanisms of action of this proposed therapeutic agent for CNS disorders associated with oxidative stress. Antioxid Redox Signal 8:381-394.
40. Raynaud F, Evain-Brion D, Gerbaud P, Marciano D, Gorin I, Liapi C, Anderson WB (1997) Oxidative modulation of cyclic AMP-dependent protein kinase in human fibroblasts: possible role in psoriasis. Free Radic Biol Med 22:623-632.
41. Robison AJ, Bass MA, Jiao Y, MacMillan LB, Carmody LC, Bartlett RK, Colbran RJ (2005) Multivalent interactions of calcium/calmodulin-dependent protein kinase II with the postsynaptic density proteins NR2B, densin-180, and alpha-actinin-2. J Biol Chem 280:35329-35336.
42. Robison AJ, Winder DG, Colbran RJ, Bartlett RK (2007) Oxidation of cal-modulin alters activation and regulation of CaMKII. Biochem Biophys Res Commun 356:97-101.
43. Rosenzweig ES, Barnes CA (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69:143-179.
44. Schnabel R, Kilpatrick IC, Collingridge GL (2001) Protein phosphatase inhibitors facilitate DHPG-induced LTD in the CA1 region of the hippocampus. Br J Pharmacol 132:1095-1101.
45. 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.
46. Shetty PK, Huang FL, Huang KP (2008) Ischemia-elicited oxidative modulation of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 283:5389-5401.
47. Shih AY, Erb H, Sun X, Toda S, Kalivas PW, Murphy TH (2006) Cystine/ glutamate exchange modulates glutathione supply for neuroprotection from oxidative stress and cell proliferation. J Neurosci 26:10514-10523.
48. Shin EJ, Suh SK, Lim YK, Jhoo WK, Hjelle OP, Ottersen OP, Shin CY, Ko KH, Kim WK, Kim DS, Chun W, Ali S, Kim HC (2005) Ascorbate attenuates trimethyltin-induced oxidative burden and neuronal degeneration in the rat hippocampus by maintaining glutathione homeostasis. Neuroscience 133:715-727.
49. Susankova K, Tousova K, Vyklicky L, Teisinger J, Vlachova V (2006) Reducing and oxidizing agents sensitize heat-activated vanilloid receptor (TRPV1) current. Mol Pharmacol 70:383-394.
50. Tokumitsu H, Chijiwa T, Hagiwara M, Mizutani A, Terasawa M, Hidaka H (1990) KN-62, 1-[N,O-bis(5-isoquinolinesulfonyl)-N-methyl-L-tyrosyl]-4- phenylpiperazi ne, a specific inhibitor of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem 265:4315-4320.
51. Tsien JZ, Huerta PT, Tonegawa S (1996) The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87:1327-1338.
52. Wang LY, Orser BA, Brautigan DL, MacDonald JF (1994) Regulation of NMDA receptors in cultured hippocampal neurons by protein phosphatases 1 and 2A. Nature 369:230-232.
53. Westphal RS, Tavalin SJ, Lin JW, Alto NM, Fraser ID, Langeberg LK, Sheng M, Scott JD (1999) Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex. Science 285:93-96.
54. Yoneyama M, Nishiyama N, Shuto M, Sugiyama C, Kawada K, Seko K, Nagashima R, Ogita K (2008) In vivo depletion of endogenous glutathione facilitates trimethyltin-induced neuronal damage in the dentate gyrus of mice by enhancing oxidative stress. Neurochem Int 52:761-769.
55. Zhou Y, Takahashi E, Li W, Halt A, Wiltgen B, Ehninger D, Li GD, Hell JW, Kennedy MB, Silva AJ (2007) Interactions between the NR2B receptor and CaMKII modulate synaptic plasticity and spatial learning. J Neurosci 27:13843-13853.
56. Zou CG, Agar NS, Jone GL (2001) Oxidative insult in sheep red blood cells induced by T-butyl hydroperoxide: the roles of glutathione and glutathione peroxidase. Free Radic Res 34:45-56.