Peroxiredoxin II preserves cognitive function against age-linked hippocampal oxidative damage

Neurobiology of Aging

Volumn 32, Issue 6, 2011, Pages 1054-1068

  Kim, Sun Uk ^a   Jin, Mei Hua ^a,d   Kim, Yoon Sik ^f   Lee, Sang Hee ^c   Cho, Yee Sook ^a   Cho, Kyoung Joo ^g   Lee, Kyu Sun ^a   Kim, Yang In ^f   Kim, Gyung Whan ^g   Kim, Jin Man ^d   Lee, Tae Hoon ^e   Lee, Young Ho ^d   Shong, Minho ^d   Kim, Hyung Chun ^b   Chang, Kyu Tae ^a   Yu, Dae Yeul ^a   Lee, Dong Seok ^h  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Kangwon National University   (South Korea)

^c Korea Basic Science Institute (KBSI)   (South Korea)

^d Chungnam National University   (South Korea)

^e Chonnam National University   (South Korea)

^f Korea University College of Medicine   (South Korea)

^g Yonsei University College of Medicine   (South Korea)

^h Kyungpook National University   (South Korea)

Author keywords

Aging; Hippocampus; Long term potentiation; Mitochondria; Peroxiredoxin; Reactive oxygen species

Indexed keywords

ALPHA TOCOPHEROL; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PEROXIREDOXIN 2; REACTIVE OXYGEN METABOLITE;

AGE; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN MITOCHONDRION; COGNITIVE DEFECT; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG EFFECT; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LEARNING DISORDER; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; WILD TYPE;

ADMINISTRATION, ORAL; AGING; ANIMALS; ANTIOXIDANTS; BEHAVIOR, ANIMAL; COGNITION; CREB-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HIPPOCAMPUS; LEARNING DISORDERS; LONG-TERM POTENTIATION; MALE; MALONDIALDEHYDE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NEURONS; PEROXIREDOXINS; PROTEIN CARBONYLATION; REACTIVE OXYGEN SPECIES; VITAMIN E;

EID: 79955958990     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2009.05.017     Document Type: Article

References (72)

1. Ahmed T., Frey J.U. Plasticity-specific phosphorylation of CaMKII, MAP-kinases and CREB during late-LTP in rat hippocampal slices in vitro. Neuropharmacology 2005, 49:477-492.
2. Ames B.N. Delaying the mitochondrial decay of aging. Ann. NY Acad. Sci. 2004, 1019:406-411.
3. Auerbach J.M., Segal M. Peroxide modulation of slow onset potentiation in rat hippocampus. J. Neurosci. 1997, 17:8695-8701.
4. Barnes C.A. Long-term potentiation and the ageing brain. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2003, 358:765-772.
5. Blitzer R.D., Connor J.H., Brown G.P., Wong T., Shenolikar S., Iyengar R., Landau E.M. Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. Science 1998, 280:1940-1942.
6. Blitzer R.D., Wong T., Nouranifar R., Iyengar R., Landau E.M. Postsynaptic cAMP pathway gates early LTP in hippocampal CA1 region. Neuron 1995, 15:1403-1414.
7. Botia B., Seyer D., Ravni A., Benard M., Falluel-Morel A., Cosette P., Jouenne T., Fournier A., Vaudry H., Gonzalez B.J., Vaudry D. Peroxiredoxin 2 is involved in the neuroprotective effects of PACAP in cultured cerebellar granule neurons. J. Mol. Neurosci. 2008, 36:61-72.
8. Boulos S., Meloni B.P., Arthur P.G., Bojarski C., Knuckey N.W. Peroxiredoxin 2 overexpression protects cortical neuronal cultures from ischemic and oxidative injury but not glutamate excitotoxicity, whereas Cu/Zn superoxide dismutase 1 overexpression protects only against oxidative injury. J. Neurosci. Res. 2007, 85:3089-3097.
9. Chang J.W., Jeon H.B., Lee J.H., Yoo J.S., Chun J.S., Kim J.H., Yoo Y.J. Augmented expression of peroxiredoxin I in lung cancer. Biochem. Biophys. Res. Commun. 2001, 289:507-512.
10. Cho Y.S., Cho-Chung Y.S. Antisense protein kinase A RIalpha acts synergistically with hydroxycamptothecin to inhibit growth and induce apoptosis in human cancer cells: molecular basis for combinatorial therapy. Clin. Cancer Res. 2003, 9:1171-1178.
11. Choi M.H., Lee I.K., Kim G.W., Kim B.U., Han Y.H., Yu D.Y., Park H.S., Kim K.Y., Lee J.S., Choi C., Bae Y.S., Lee B.I., Rhee S.G., Kang S.W. Regulation of PDGF signalling and vascular remodelling by peroxiredoxin II. Nature 2005, 435:347-353.
12. D'Hooge R., De Deyn P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev. 2001, 36:60-90.
13. Draper H., Hadley M. Malondialdehyde determination as index of lipid peroxidation. Meth. Enzymol. 1990, 186:421-431.
14. Fang J., Nakamura T., Cho D.H., Gu Z., Lipton S.A. S-Nitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:18742-18747.
15. Fukui K., Omoi N.O., Hayasaka T., Shinnkai T., Suzuki S., Abe K., Urano S. Cognitive impairment of rats caused by oxidative stress and aging, and its prevention by vitamin E. Ann. NY Acad. Sci. 2002, 959:275-284.
16. 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.
17. Giasson B.I., Duda J.E., Murray I.V., Chen Q., Souza J.M., Hurtig H.I., Ischiropoulos H., Trojanowski J.Q., Lee V.M. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 2000, 290:985-989.
18. Halliwell B., Gutteridge J.M. Role of free radicals and catalytic metal ions in human disease: an overview. Meth. Enzymol. 1990, 186:1-85.
19. Hattori F., Murayama N., Noshita T., Oikawa S. Mitochondrial peroxiredoxin-3 protects hippocampal neurons from excitotoxic injury in vivo. J. Neurochem. 2003, 86:860-868.
20. Hidalgo C., Nunez M.T. Calcium, iron and neuronal function. IUBMB Life 2007, 59:280-285.
21. Hongpaisan J., Winters C.A., Andrews S.B. Calcium-dependent mitochondrial superoxide modulates nuclear CREB phosphorylation in hippocampal neurons. Mol. Cell. Neurosci. 2003, 24:1103-1115.
22. Jacobsen J.S., Wu C.C., Redwine J.M., Comery T.A., Arias R., Bowlby M., Martone R., Morrison J.H., Pangalos M.N., Reinhart P.H., Bloom F.E. Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:5161-5166.
23. Jeffery K.J. LTP and spatial learning-where to next?. Hippocampus 1997, 7:95-110.
24. Jin M.H., Lee Y.H., Kim J.M., Sun H.N., Moon E.Y., Shong M.H., Kim S.U., Lee S.H., Lee T.H., Yu D.Y., Lee D.S. Characterization of neural cell types expressing peroxiredoxins in mouse brain. Neurosci. Lett. 2005, 381:252-257.
25. Kamsler A., Segal M. Hydrogen peroxide as a diffusible signal molecule in synaptic plasticity. Mol. Neurobiol. 2004, 29:167-178.
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. Kappus H., Diplock A.T. Tolerance and safety of vitamin E: a toxicological position report. Free Radic. Biol. Med. 1992, 13:55-74.
28. Kelleher R.J., Govindarajan A., Jung H.Y., Kang H., Tonegawa S. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 2004, 116:467-479.
29. Kim G.W., Chan P.H. Oxidative stress and neuronal DNA fragmentation mediate age-dependent vulnerability to the mitochondrial toxin, 3-nitropropionic acid, in the mouse striatum. Neurobiol. Dis. 2001, 8:114-126.
30. Kim G.W., Gasche Y., Grzeschik S., Copin J.C., Maier C.M., Chan P.H. Neurodegeneration in striatum induced by the mitochondrial toxin 3-nitropropionic acid: role of matrix metalloproteinase-9 in early blood-brain barrier disruption?. J. Neurosci. 2003, 23:8733-8742.
31. Kim S.H., Fountoulakis M., Cairns N., Lubec G. Protein levels of human peroxiredoxin subtypes in brains of patients with Alzheimer's disease and Down syndrome. J. Neural Transm. Suppl. 2001, 61:223-235.
32. Knapp L.T., Klann E. Role of reactive oxygen species in hippocampal long-term potentiation: contributory or inhibitory?. J. Neurosci. Res. 2002, 70:1-7.
33. Krapfenbauer K., Engidawork E., Cairns N., Fountoulakis M., Lubec G. Aberrant expression of peroxiredoxin subtypes in neurodegenerative disorders. Brain Res. 2003, 967:152-160.
34. Krapfenbauer K., Yoo B.C., Fountoulakis M., Mitrova E., Lubec G. Expression patterns of antioxidant proteins in brains of patients with sporadic Creutzfeldt-Jacob disease. Electrophoresis 2002, 23:2541-2547.
35. Kuo J.F., Krueger B.K., Sanes J.R., Greengard P. Cyclic nucleotide-dependent protein kinases. V. Preparation and properties of adenosine 3′,5′-monophosphate-dependent protein kinase from various bovine tissues. Biochim. Biophys. Acta 1970, 212:79-91.
36. Lass A., Forster M.J., Sohal R.S. Effects of coenzyme Q10 and alpha-tocopherol administration on their tissue levels in the mouse: elevation of mitochondrial alpha-tocopherol by coenzyme Q10. Free Radic. Biol. Med. 1999, 26:1375-1382.
37. Lee T.H., Kim S.U., Yu S.L., Kim S.H., Park D.S., Moon H.B., Dho S.H., Kwon K.S., Kwon H.J., Han Y.H., Jeong S., Kang S.W., Shin H.S., Lee K.K., Rhee S.G., Yu D.Y. Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood 2003, 101:5033-5038.
38. Levine R.L., Garland D., Oliver C.N., Amici A., Climent I., Lenz A.G., Ahn B.W., Shaltiel S., Stadtman E.R. Determination of carbonyl content in oxidatively modified proteins. Meth. Enzymol. 1990, 186:464-478.
39. Levkovitz Y., Avignone E., Groner Y., Segal M. Upregulation of GABA neurotransmission suppresses hippocampal excitability and prevents long-term potentiation in transgenic superoxide dismutase-overexpressing mice. J. Neurosci. 1999, 19:10977-10984.
40. Li Z., Okamoto K., Hayashi Y., Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 2004, 119:873-887.
41. Linnarsson S., Bjorklund A., Ernfors P. Learning deficit in BDNF mutant mice. Eur. J. Neurosci. 1997, 9:2581-2587.
42. Lynch M.A. Long-term potentiation and memory. Physiol. Rev. 2004, 84:87-136.
43. Matthies H., Reymann K.G. Protein kinase A inhibitors prevent the maintenance of hippocampal long-term potentiation. Neuroreport 1993, 4:712-714.
44. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
45. Navarro A. Mitochondrial enzyme activities as biochemical markers of aging. Mol. Aspects Med. 2004, 25:37-48.
46. Nicolle M.M., Gonzalez J., Sugaya K., Baskerville K.A., Bryan D., Lund K., Gallagher M., McKinney M. Signatures of hippocampal oxidative stress in aged spatial learning-impaired rodents. Neuroscience 2001, 107:415-431.
47. O'Donnell E., Vereker E., Lynch M.A. Age-related impairment in LTP is accompanied by enhanced activity of stress-activated protein kinases: analysis of underlying mechanisms. Eur. J. Neurosci. 2000, 12:345-352.
48. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 1996, 16:1137-1145.
49. Patterson S.L., Grover L.M., Schwartzkroin P.A., Bothwell M. Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 1992, 9:1081-1088.
50. Patterson S.L., Pittenger C., Morozov A., Martin K.C., Scanlin H., Drake C., Kandel E.R. Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 2001, 32:123-140.
51. Pereira C., Santos M.S., Oliveira C. Involvement of oxidative stress on the impairment of energy metabolism induced by A beta peptides on PC12 cells: protection by antioxidants. Neurobiol. Dis. 1999, 6:209-219.
52. Prosperi M.T., Apiou F., Dutrillaux B., Goubin G. Organization and chromosomal assignment of two human PAG gene loci: PAGA encoding a functional gene and PAGB a processed pseudogene. Genomics 1994, 19:236-241.
53. Purpura D.P. Pathobiology of cortical neurons in metabolic and unclassified amentias. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 1979, 57:43-68.
54. Reynolds E.S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 1963, 17:208-212.
55. Rosenzweig E.S., Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog. Neurobiol. 2003, 69:143-179.
56. Seaver L.C., Imlay J.A. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 2001, 183:7173-7181.
57. Serrano F., Klann E. Reactive oxygen species and synaptic plasticity in the aging hippocampus. Ageing Res. Rev. 2004, 3:431-443.
58. Silva A.J., Giese K.P., Fedorov N.B., Frankland P.W., Kogan J.H. Molecular, cellular, and neuroanatomical substrates of place learning. Neurobiol. Learn. Mem. 1998, 70:44-61.
59. Smith M.A., Perry G. Free radical damage, iron, and Alzheimer's disease. J. Neurol. Sci. Suppl. 1995, 134:92-94.
60. Spurr A.R. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 1969, 26:31-43.
61. Sweatt J.D. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 2001, 76:1-10.
62. Tuzcu M., Baydas G. Effect of melatonin and vitamin E on diabetes-induced learning and memory impairment in rats. Eur. J. Pharmacol. 2006, 537:106-110.
63. Vaynman S., Ying Z., Gomez-Pinilla F. Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience 2003, 122:647-657.
64. Waltereit R., Weller M. Signaling from cAMP/PKA to MAPK and synaptic plasticity. Mol. Neurobiol. 2003, 27:99-106.
65. Watabe A.M., O'Dell T.J. Age-related changes in theta frequency stimulation-induced long-term potentiation. Neurobiol. Aging 2003, 24:267-272.
66. Watabe A.M., Zaki P.A., O'Dell T.J. Coactivation of beta-adrenergic and cholinergic receptors enhances the induction of long-term potentiation and synergistically activates mitogen-activated protein kinase in the hippocampal CA1 region. J. Neurosci. 2000, 20:5924-5931.
67. Watson J.B., Khorasani H., Persson A., Huang K.P., Huang F.L., O'Dell T.J. Age-related deficits in long-term potentiation are insensitive to hydrogen peroxide: coincidence with enhanced autophosphorylation of Ca2+/calmodulin-dependent protein kinase II. J. Neurosci. Res. 2002, 70:298-308.
68. Wu A., Ying Z., Gomez-Pinilla F. Dietary omega-3 fatty acids normalize BDNF levels, reduce oxidative damage, and counteract learning disability after traumatic brain injury in rats. J. Neurotrauma 2004, 21:1457-1467.
69. Wu A., Ying Z., Gomez-Pinilla F. The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. Eur. J. Neurosci. 2004, 19:1699-1707.
70. Yamada K., Tanaka T., Han D., Senzaki K., Kameyama T., Nabeshima T. Protective effects of idebenone and alpha-tocopherol on beta-amyloid-(1-42)-induced learning and memory deficits in rats: implication of oxidative stress in beta-amyloid-induced neurotoxicity in vivo. Eur. J. Neurosci. 1999, 11:83-90.
71. Yamamoto T., Matsui Y., Natori S., Obinata M. Cloning of a housekeeping-type gene (MER5) preferentially expressed in murine erythroleukemia cells. Gene 1989, 80:337-343.
72. Zakharenko S.S., Patterson S.L., Dragatsis I., Zeitlin S.O., Siegelbaum S.A., Kandel E.R., Morozov A. Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 2003, 39:975-990.