Role of antioxidant enzymes in redox regulation of N-methyl-D-aspartate receptor function and memory in middle-aged rats

Neurobiology of Aging

Volumn 35, Issue 6, 2014, Pages 1459-1468

  Lee, Wei Hua ^a   Kumar, Ashok ^b   Rani, Asha ^b   Foster, Thomas C ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

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

Author keywords

Aging; Catalase; Glutathione peroxidase; Learning and memory; NMDAR; Superoxide dismutase; Synaptic plasticity

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; CATALASE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATALYSIS; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; EPISODIC MEMORY; HIPPOCAMPUS; LIPID PEROXIDATION; LONG TERM POTENTIATION; MALE; MEMORY; MORRIS WATER MAZE TEST; NERVE CELL PLASTICITY; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; AGING; ANIMAL; DISEASE COURSE; ENZYMOLOGY; FISCHER 344 RAT; METABOLISM; NERVE CELL; NEURODEGENERATIVE DISEASES; PHYSIOLOGY; SYNAPSE;

AGING; ANIMALS; CATALASE; DISEASE PROGRESSION; HIPPOCAMPUS; MALE; MEMORY; NEURODEGENERATIVE DISEASES; NEURONAL PLASTICITY; NEURONS; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, INBRED F344; RECEPTORS, N-METHYL-D-ASPARTATE; SUPEROXIDE DISMUTASE; SYNAPSES;

EID: 84903362211     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.12.002     Document Type: Article

References (47)

1. Bar-Peled O., Korkotian E., Segal M., Groner Y. Constitutive overexpression of Cu/Zn superoxide dismutase exacerbates kainic acid-induced apoptosis of transgenic-Cu/Zn superoxide dismutase neurons. Proc Natl Acad Sci U S A 1996, 93:8530-8535.
2. Bartov O., Sultana R., Butterfield D.A., Atlas D. Low molecular weight thiol amides attenuate MAPK activity and protect primary neurons from Abeta(1-42) toxicity. Brain Res. 2006, 1069:198-206.
3. Bellia F., Calabrese V., Guarino F., Cavallaro M., Cornelius C., De Pinto V., Rizzarelli E. Carnosinase levels in aging brain: redox state induction and cellular stress response. Antioxid. Redox Signal 2009, 11:2759-2775.
4. Belrose J.C., Xie Y.F., Gierszewski L.J., MacDonald J.F., Jackson M.F. Loss of glutathione homeostasis associated with neuronal senescence facilitates TRPM2 channel activation in cultured hippocampal pyramidal neurons. Mol. Brain 2012, 5:11.
5. Bodhinathan K., Kumar A., Foster T.C. Intracellular redox state alters NMDA receptor response during aging through Ca2+/calmodulin-dependent protein kinase II. J.Neurosci. 2010, 30:1914-1924.
6. Bodhinathan K., Kumar A., Foster T.C. Redox sensitive calcium stores underlie enhanced after hyperpolarization of aged neurons: role for ryanodine receptor mediated calcium signaling. J.Neurophysiol. 2010, 104:2586-2593.
7. Borg J., Chereul E. Differential MRI patterns of brain atrophy in double or single transgenic mice for APP and/or SOD. J.Neurosci. Res. 2008, 86:3275-3284.
8. Brewer G.J., Torricelli J.R., Lindsey A.L., Kunz E.Z., Neuman A., Fisher D.R., Joseph J.A. Age-related toxicity of amyloid-beta associated with increased pERK and pCREB in primary hippocampal neurons: reversal by blueberry extract. J.Nutr. Biochem. 2010, 21:991-998.
9. Burger C., Gorbatyuk O.S., Velardo M.J., Peden C.S., Williams P., Zolotukhin S., Reier P.J., Mandel R.J., Muzyczka N. Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol. Ther. 2004, 10:302-317.
10. Chen T.S., Richie J.P., Lang C.A. The effect of aging on glutathione and cysteine levels in different regions of the mouse brain. Proc. Soc. Exp. Biol. Med. 1989, 190:399-402.
11. 2 in red blood cells. Antioxid. Redox Signal 2010, 12:1235-1246.
12. Crivello N.A., Rosenberg I.H., Shukitt-Hale B., Bielinski D., Dallal G.E., Joseph J.A. Aging modifies brain region-specific vulnerability to experimental oxidative stress induced by low dose hydrogen peroxide. Age (Dordr) 2007, 29:191-203.
13. de Bernardo S., Canals S., Casarejos M.J., Solano R.M., Menendez J., Mena M.A. Role of extracellular signal-regulated protein kinase in neuronal cell death induced by glutathione depletion in neuron/glia mesencephalic cultures. J.Neurochem. 2004, 91:667-682.
14. Dringen R., Kussmaul L., Gutterer J.M., Hirrlinger J., Hamprecht B. The glutathione system of peroxide detoxification is less efficient in neurons than in astroglial cells. J.Neurochem. 1999, 72:2523-2530.
15. Favilli F., Iantomasi T., Marraccini P., Stio M., Lunghi B., Treves C., Vincenzini M.T. Relationship between age and GSH metabolism in synaptosomes of rat cerebral cortex. Neurobiol. Aging 1994, 15:429-433.
16. Foster T.C. Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 2007, 6:319-325.
17. Foster T.C. Dissecting the age-related decline on spatial learning and memory tasks in rodent models: N-methyl-D-aspartate receptors and voltage-dependent Ca2+ channels in senescent synaptic plasticity. Prog. Neurobiol. 2012, 96:283-303.
18. Fullerton H.J., Ditelberg J.S., Chen S.F., Sarco D.P., Chan P.H., Epstein C.J., Ferriero D.M. Copper/zinc superoxide dismutase transgenic brain accumulates hydrogen peroxide after perinatal hypoxia ischemia. Ann. Neurol. 1998, 44:357-364.
19. Gahtan E., Auerbach J.M., Groner Y., Segal M. Reversible impairment of long-term potentiation in transgenic Cu/Zn-SOD mice. Eur. J. Neurosci. 1998, 10:538-544.
20. Ghosh D., LeVault K.R., Barnett A.J., Brewer G.J. Areversible early oxidized redox state that precedes macromolecular ROS damage in aging nontransgenic and 3xTg-AD mouse neurons. J.Neurosci. 2012, 32:5821-5832.
21. Handy D.E., Loscalzo J. Redox regulation of mitochondrial function. Antioxid. Redox Signal 2012, 16:1323-1367.
22. Haxaire C., Turpin F.R., Potier B., Kervern M., Sinet P.M., Barbanel G., Mothet J.P., Dutar P., Billard J.M. Reversal of age-related oxidative stress prevents hippocampal synaptic plasticity deficits by protecting D-serine-dependent NMDA receptor activation. Aging Cell 2012, 11:336-344.
23. Head E., Liu J., Hagen T.M., Muggenburg B.A., Milgram N.W., Ames B.N., Cotman C.W. Oxidative damage increases with age in a canine model of human brain aging. J.Neurochem. 2002, 82:375-381.
24. Hu D., Klann E., Thiels E. Superoxide dismutase and hippocampal function: age and isozyme matter. Antioxid. Redox Signal 2007, 9:201-210.
25. Jaarsma D., Haasdijk E.D., Grashorn J.A., Hawkins R., van Duijn W., Verspaget H.W., London J., Holstege J.C. Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol. Dis. 2000, 7(6 Pt B):623-643.
26. Kamsler A., Segal M. Paradoxical actions of hydrogen peroxide on long-term potentiation in transgenic superoxide dismutase-1 mice. J.Neurosci. 2003, 23:10359-10367.
27. Keelan J., Allen N.J., Antcliffe D., Pal S., Duchen M.R. Quantitative imaging of glutathione in hippocampal neurons and glia in culture using monochlorobimane. J.Neurosci. Res. 2001, 66:873-884.
28. Kumar A., Foster T.C. Linking redox regulation of NMDAR synaptic function to cognitive decline during aging. J.Neurosci. 2013, 33:15710-15715.
29. Kumar A., Rani A., Tchigranova O., Lee W.H., Foster T.C. Influence of late-life exposure to environmental enrichment or exercise on hippocampal function and CA1 senescent physiology. Neurobiol. Aging 2012, 33:828.e1-828.e17.
30. Lee W.H., Kumar A., Rani A., Herrera J., Xu J., Someya S., Foster T.C. Influence of viral vector-mediated delivery of superoxide dismutase and catalase to the hippocampus on spatial learning and memory during aging. Antioxid. Redox Signal 2012, 16:339-350.
31. Lu C., Chan S.L., Fu W., Mattson M.P. The lipid peroxidation product 4-hydroxynonenal facilitates opening of voltage-dependent Ca2+ channels in neurons by increasing protein tyrosine phosphorylation. J.Biol. Chem. 2002, 277:24368-24375.
32. Lu S.C. Regulation of hepatic glutathione synthesis: current concepts and controversies. FASEB J. 1999, 13:1169-1183.
33. Lubos E., Loscalzo J., Handy D.E. Glutathione peroxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid. Redox Signal 2011, 15:1957-1997.
34. Parihar M.S., Kunz E.A., Brewer G.J. Age-related decreases in NAD(P)H and glutathione cause redox declines before ATP loss during glutamate treatment of hippocampal neurons. J.Neurosci. Res. 2008, 86:2339-2352.
35. Perez V.I., Bokov A., Van Remmen H., Mele J., Ran Q., Ikeno Y., Richardson A. Is the oxidative stress theory of aging dead?. Biochim. Biophys. Acta 2009, 1790:1005-1014.
36. Pigeolet E., Corbisier P., Houbion A., Lambert D., Michiels C., Raes M., Zachary M.D., Remacle J. Glutathione peroxidase, superoxide dismutase, and catalase inactivation by peroxides and oxygen derived free radicals. Mech. Ageing Dev. 1990, 51:283-297.
37. Rebrin I., Forster M.J., Sohal R.S. Effects of age and caloric intake on glutathione redox state in different brain regions of C57BL/6 and DBA/2 mice. Brain Res. 2007, 1127:10-18.
38. Robillard J.M., Gordon G.R., Choi H.B., Christie B.R., MacVicar B.A. Glutathione restores the mechanism of synaptic plasticity in aged mice to that of the adult. PLoS One 2011, 6:e20676.
39. Salmon A.B., Richardson A., Perez V.I. Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging?. Free Radic. Biol. Med. 2010, 48:642-655.
40. Sasaki T., Senda M., Kim S., Kojima S., Kubodera A. Age-related changes of glutathione content, glucose transport and metabolism, and mitochondrial electron transfer function in mouse brain. Nucl. Med. Biol. 2001, 28:25-31.
41. Savvides S.N., Scheiwein M., Bohme C.C., Arteel G.E., Karplus P.A., Becker K., Schirmer R.H. Crystal structure of the antioxidant enzyme glutathione reductase inactivated by peroxynitrite. J.Biol. Chem. 2002, 277:2779-2784.
42. Schafer F.Q., Buettner G.R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 2001, 30:1191-1212.
43. Slivka A., Mytilineou C., Cohen G. Histochemical evaluation of glutathione in brain. Brain Res. 1987, 409:275-284.
44. Suh J.H., Wang H., Liu R.M., Liu J., Hagen T.M. (R)-alpha-lipoic acid reverses the age-related loss in GSH redox status in post-mitotic tissues: evidence for increased cysteine requirement for GSH synthesis. Arch. Biochem. Biophys. 2004, 423:126-135.
45. Thiels E., Klann E. Hippocampal memory and plasticity in superoxide dismutase mutant mice. Physiol. Behav. 2002, 77:601-605.
46. Yang Y.J., Wu P.F., Long L.H., Yu D.F., Wu W.N., Hu Z.L., Fu H., Xie N., Jin Y., Ni L., Wang J.Z., Wang F., Chen J.G. Reversal of aging-associated hippocampal synaptic plasticity deficits by reductants via regulation of thiol redox and NMDA receptor function. Aging Cell 2010, 9:709-721.
47. Ying W., Anderson C.M., Chen Y., Stein B.A., Fahlman C.S., Copin J.C., Chan P.H., Swanson R.A. Differing effects of copper, zinc superoxide dismutase overexpression on neurotoxicity elicited by nitric oxide, reactive oxygen species, and excitotoxins. J.Cereb. Blood Flow Metab. 2000, 20:359-368.