Modulation of ischemia-induced NMDAR1 activation by environmental enrichment decreases oxidative damage

Journal of Neurotrauma

Volumn 28, Issue 12, 2011, Pages 2485-2492

  Briones, Teresita L ^a,b   Rogozinska, Magdalena ^b   Woods, Julie ^b  

^a WAYNE STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

complex environment; NMDAR1; oxidative DNA damage; oxidative stress; protein oxidation

Indexed keywords

GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL HOUSING; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CONDITIONING; CONTROLLED STUDY; DNA DAMAGE; EXCITOTOXICITY; HIPPOCAMPUS; MALE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; SHAM PROCEDURE; TASK PERFORMANCE;

ANIMALS; BRAIN ISCHEMIA; DNA DAMAGE; ENVIRONMENT; HIPPOCAMPUS; MALE; OXIDATIVE STRESS; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SOCIAL ENVIRONMENT;

EID: 83455163272     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1842     Document Type: Article

References (49)

1. Abe, K., Aoki, M., Kawagoe, J., Yoshida, T., Hattori, A., Kogure, K., and Itoyama, Y. (1994). Ischemic delayed neuronal death. Stroke 26, 1478-1489.
2. Andin, J., Hallbeck, M., Mohammed, A.H., and Marcusson, J. (2007). Influence of environmental enrichment on steady-state mRNA levels for EAAC1, AMPA1 and NMDA2A receptors subunits in rat hippocampus. Brain Res. 1174, 18-27. (Pubitemid 47451354)
3. Ankarcrona, M., Dypbukt, J.H., Bonfoco, E., Zhivotovsky, B., Porrenius, S., Lipton, S.A., and Nicotera, P. (1995). Gluta-mate-induced neuronal death: a succession of necrosis or apoptosis depending on mitchondrial function. Neuron 15, 961-973.
4. Artola, A., von Frijtag, J.C., Fermont, P.C.J., Gispen, W.H., Schrama, L.H., Kamal, A., and Spruijt, B.M. (2006). Long-lasting modulation of the inducion of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur. J. Neurosci. 23, 261-272.
5. Beckman, J. S., and W. H. Koppenol (1996). Nitric oxide, su-peroxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol. 271, C1424-C1437.
6. Belayev, A., Saul, I., Liu, Y., Zhao, W., Ginsberg, M.D., Valdes, M.A., Busto, R., and Belayev, L. (2003). Enriched environment delays the onset of hippocampal damage after global cerebral ischemia in rats. Brain Res. 964, 121-127. (Pubitemid 36165077)
7. Briones, T. L., Suh, E., Hattar, H., and Wadowska, M. (2005). Dentate gyrus neurogenesis after cerebral ischemia and behavioral training. Biol. Res. Nurs. 6, 167-179. (Pubitemid 43920962)
8. Briones, T. L., Suh, E., Jozsa, L., Hattar, H., Chai, J., and Wa-dowska, M. (2004). Behaviorally-induced ultrastructural plasticity in the hippocampal region after cerebral ischemia. Brain Res. 997, 137-146. (Pubitemid 38058518)
9. Briones, T. L., Suh, E., Jozsa, L., and Woods, J. (2006a). Beha-viorally induced synaptogenesis and dendritic growth in the hippocampal region following transient global cerebral ischemia are accompanied by improvement in spatial learning. Exp. Neurol. 198, 530-538.
10. Briones, T. L., Therrien, B., and Metzger, B. (2000). Effects of environment on enhancing functional plasticity following cerebral ischemia. Biol. Res. Nurs. 1, 299-309.
11. Briones, T. L., Woods, J., Wadowska, M., and Rogozinska, M. (2006b). Amelioration of cognitive impairment and changes in microtubule-associated protein 2 after transient global cerebral ischemia are influenced by complex environment experience. Behav. Brain Res. 168, 261-271. (Pubitemid 43201943)
12. Briones, T. L., Woods, J., Wadowska, M., Rogozinska, M., and Nguyen, M. (2006c). Astrocytic changes in the hippocampus and functional recovery after cerebral ischemia are facilitated by rehabilitation training. Behav. Brain Res. 171, 17-25. (Pubitemid 43728396)
13. Candelario-Jalil, E., Mhadu, N.H., Al-Dalain, S.M., Martinez, G., and León, O.S. (2001). Time course of oxidative damage in different brain regions following transient cerebral ischemia in gerbils. Neurosci. Res. 41, 233-241. (Pubitemid 32988398)
14. Cardozo-Pelaez, F., Brook, P.J., Stedeford, T., Song, S., and Sanchez-Ramos, J. (2000). DNA damage, repair, and antioxi-dant systems in brain regions: a correlatove study. Free Radic. Biol. Med. 28, 779-785. (Pubitemid 30171292)
15. Chan, P. H. (2001). Reactive oxygen radicals in signaling and damage in the ischemic brain. J. Cereb. Blood Flow Metab. 21, 2-14. (Pubitemid 32036708)
16. Choi, D. W., and S. M. Rothman (1990). The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Ann. Rev. Neurosci. 13, 171-182. (Pubitemid 20100647)
17. Crozier, R. A., Bi, C., Han, Y.R., and Plummer, M.R. (2008). BDNF modulation of NMDA receptors is activity dependent. J. Neurophysiol. 100, 3264-3274.
18. Cui, Z., Lindl, K.A., Mei, B., Zhang, S., and Tsien, J.Z. (2005). Requirement of NMDA receptor reactivation for consolidation and storage of nondeclarative taste memory revealed by in-ducible NR1 knockout. Eur. J. Neurosci. 22, 755-763. (Pubitemid 41192285)
19. Cui, Z., Wang, H., Tan, Y., Zaia, K.A., Zhang, S., and Tsien, J.Z. (2004). Inducible and reversible NR1 knockout reveals crucial role of the NMDA receptor in preserving remote memories in the brain. Neuron 41, 781-793. (Pubitemid 38326840)
20. Culcasi, M., Lafon-Cazal, M., Pietri, S., and Bockaert, J. (1994). Glutamate receptors induce a burst of superoxide via activation of nitric oxide synthase in arginine-depleted neurons. J. Biol. Chem. 269, 12589-12593. (Pubitemid 24202045)
21. Eliasson, M. J., Sampei, K., Mandir, A.S., Hurn, P.D., Traystman, R.J., Bao, J., Pieper, A., Wang, Z.Q., Dawson, T.M., Synder, S.H., and Dawson, V.L. (1997). Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat. Med. 1997, 1089-1095. (Pubitemid 27444449)
22. Endres, M., Wang, Z.Q., Namura, S., Waeber, C., and Mosko-witz, M.A. (1997). Ischemic brain injury is mediated by the activation of poly(ADP-ribose) polymerase. J. Cereb. Blood Flow Metab. 17, 1143-1151. (Pubitemid 27514738)
23. 2+ entry resulting in apoptosis. J. Neurochem. 104, 1177-1189.
24. Gruart, A., and J. M. Delgado-Garcia (2007). Activity-dependent chnages of the hippocamal CA3-CA1 synapse during the acquisition of associative learning in conscious mice. Genes Brain Behav. 6, Suppl. 1, 24-31. (Pubitemid 46744108)
25. Hou, S. T., and J. P. MacManus (2002). Molecular mechanisms of cerebral ischemia-induced neuronal death. Int Rev Cytol 221, 93-148. (Pubitemid 35429861)
26. Hu, B. R., Martone, M.E., Jones, Y.Z., and Liu, C.L. (2000). Protein aggregation after transient cerebral ischemia. J. Neu-rosci. 20, 3191-3199. (Pubitemid 30263136)
27. Iadecola, C., Zhang, F., Casey, R., Clark, H.B., and Ross, M.E. (1996). Inducible nitric oxide synthase gene expression in vascular cells after transient focal cerebral ischemia. Stroke 27, 1373-1380. (Pubitemid 26286171)
28. Kannan, K., and S. K. Jain (2000). Oxidative stress and apoptosis. Pathophysiology 7, 153-163.
29. Kauppinen, T. M., and R. A. Swanson (2007). The role of Poly(ADP-ribose) polymerase-1 in CNS disease. Neuroscience 145, 1267-1272. (Pubitemid 46602734)
30. Kirino, T. (2000). Delayed neuronal death. Neuropathology 20, S95-S97.
31. Lafon-Cazal, M., Pietri, S., Culcasi, M., and Bockaert, J. (1993). NMDA-dependent superoxide production and neurotoxicity. Nature 364, 535-537. (Pubitemid 23273099)
32. Li, C., Niu, W., Jiang, C.H., and Hu, Y. (2007). Effects of enriched environment on gene expression and signal pathways in cortex of hippocampal CA1 specific NMDAR1 knockout mice. Brain Res Bull 71, 568-577. (Pubitemid 46217833)
33. Madara, J. C., and E. S. Levine (2008). Presynaptic and post-synaptic NMDA receptors mediate distinct effects of brain-derived neurotrophic factor on synaptic transmission. J. Neurophysiol. 100, 3175-3184.
34. Martin, L. J. (2008). DNA damage and repair: relevance to mechanisms of neurodegeneration. J. Neuropathol. Exp. Neurol. 67, 377-387. (Pubitemid 351653537)
35. Matsuo, Y., Kihara, T., Ikeda, M., Ninomiya, M., Onodera, H., and Kogure, K. (1995). Role of neutrophils in radical production during ischemia and reperfusion of the rat brain: effect of neutrophil depletion on extracellular ascorbyl radical formation. J. Cereb Blood Flow Metab. 15, 941-947.
36. Moroni, F., and A. Chiarugi (2008). Post-ischemic brain damage: targeting PARP-1 within the ischemic neurovascular units as a realistic avenue to stroke treatment. FEBS J. 276, 36-45.
37. Papadia, S., Soriano, F.X., Léveille, F., Martel, M-A., Dakin, K.A., Hansen, H.H., Kaindl, A., Sifringer, M., Fowler, J., Stefovska, V., McKenzie, G., Craigon, M., Corriveau, R., Ghazal, P., Horsburgh, K., Yankner, B.A., Wyllie, D.J.A., Ikonomidou, C., and Hardingham, G.E. (2008). Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat. Neurosci. 11, 476-487. (Pubitemid 351441886)
38. Pereira, L. O., Nabinger, P.M., Strapasson, A.C., Nardin, P., Gonçalves, C.A., Siqueira, I.R., and Netto, C.A. (2009). Long-term effects of environmental stimulation following hypoxia-ischemia on the oxidative state and BDNF levels in rat hippocampus and frontal cortex. Brain Res. 1247, 188-195.
39. Saucier, D. M., Yager, J.Y., and Armstrong, E.A. (2010). Housing environment and sex affect behavioral recovery from ischemic brain damage. Behav. Brain Res. 214, 48-54.
40. Sharma, R. A., McLelland, H.R., and Hill, K.A. (2001). Pharma-codynamic and pharmacokinetic study of oral Curcuma extract in patients with colorectal cancer. Clin. Cancer Res. 7, 1894-1900. (Pubitemid 32994823)
41. Taylor, J. M., and P. J. Crack (2004). Impact of oxidative stress on neuronal survival. Clin. Exp. Pharmacol. Physiol. 31, 397-406. (Pubitemid 39044117)
42. Tsien, J. Z., Huerta, P.T., and Tonegawa, S. (1996). The essential role of hippocampal CA1 NMDA receptor-dependent synap-tic plasticity in spatial memory. Cell 87, 1327-1338. (Pubitemid 27010115)
43. Wang, Q., Simonyi, A., Li, W., Sisk, B.A, Miller, R.L., MacDonald, R.S., Lubahn, D.E., Sun, G.Y., and Sun, A.Y. (2005). Dietary grape supplement ameliorates cerebral ischemia-induced neu-ronal death in gerbils. Mol. Nutr. Food Res. 49, 443-451. (Pubitemid 40780391)
44. Wang, Q., Sun, A.Y., Simonyi, A., Miller, D.K., Smith, R.E., Luchtefeld, R.G., Korthuis, R.J., and Sun, G.Y. (2009). Oral administration of grape polyphenol extract ameliorates cerebral ischemia/reperfusion-induced neuronal damage and behavioral deficits in gerbils: comparison of pre-and post-ischemic administration. J Nutr Biochem 20, 369-377.
45. Wang, Q., Xu, J., and Rottinghaus, G.E. (2002). Resveratrol protects against global cerebral ischemia in gerbils. Brain Res. 958, 439-447. (Pubitemid 35441199)
46. Wang, X., and E. K. Michaelis (2010). Selective neuronal vulnerability to oxidative stress in the brain. Front. Aging Neu-rosci. 2, 1-13.
47. Will, B., Galani, R., Kelche, C., and Rosenzweig, M.R. (2004). Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog. Brain Res. 72, 167-182. (Pubitemid 38591294)
48. Wood, D. A., Buse, J.E., Wellman, C.L., and Rebec, G.V. (2005). Differential environmental exposure alters NMDA but not AMPA receptor subunit expression in nucleus accumbens core and shell. Brain Res. 1042, 176-183. (Pubitemid 40591727)
49. Xu, X., Ye, L., and Ruan, Q. (2009). Environmental enrichment induces synaptic structural modification after transient focal cerebral ischemia in rats. Exp. Biol. Med. 234, 296-305.