Age-dependent neurodegeneration accompanying memory loss in transgenic mice defective in mitochondrial aldehyde dehydrogenase 2 activity

Journal of Neuroscience

Volumn 28, Issue 24, 2008, Pages 6239-6249

  Ohsawa, Ikuroh ^a   Nishimaki, Kiyomi ^a   Murakami, Yayoi ^a   Suzuki, Yuko ^a   Ishikawa, Masahiro ^a   Ohta, Shigeo ^a,b  

^a Graduate School of Medicine   (Japan)

^b Graduate School of Medicine   (Japan)

Author keywords

ALDH2; HNE; Memory loss; Mitochondria; Oxidative stress; Transgenic mice

Indexed keywords

4 HYDROXYNONENAL; ALDEHYDE; ALDEHYDE DEHYDROGENASE ISOENZYME 2; APOLIPOPROTEIN E; TAU PROTEIN; WATER; 4-HYDROXY-2-NONENAL; ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE 2, MOUSE; ELONGATION FACTOR 1; NERVE PROTEIN;

AMNESIA; ANIMAL MODEL; ARTICLE; BRAIN CELL; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DETOXIFICATION; DISEASE COURSE; ENZYME ACTIVITY; FEMALE; LIFESPAN; MALE; MAZE TEST; MOUSE; NERVE DEGENERATION; NONHUMAN; OXIDATION; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RECOGNITION; TRANSGENIC MOUSE; AGING; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; BRAIN CORTEX; C57BL MOUSE; CELL CULTURE; DEGENERATIVE DISEASE; EMBRYO (ANATOMY); EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MEMORY DISORDER; METABOLISM; METHODOLOGY; NERVE CELL; NICK END LABELING; PATHOLOGY; PATTERN RECOGNITION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE;

AGING; ALDEHYDE DEHYDROGENASE; ALDEHYDES; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IN SITU NICK-END LABELING; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; NEURONS; PATTERN RECOGNITION, VISUAL; PEPTIDE ELONGATION FACTOR 1; PSYCHOMOTOR PERFORMANCE;

EID: 46749095534     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4956-07.2008     Document Type: Article

References (66)

1. Amamoto K, Okamura T, Tamaki S, Kita Y, Tsujita Y, Kadowaki T, Nakamura Y, Ueshima H (2002) Epidemiologic study of the association of low-Km mitochondrial acetaldehyde dehydrogenase genotypes with blood pressure level and the prevalence of hypertension in a general population. Hypertens Res 25:857-864.
2. Biernat J, Mandelkow EM, Schröter C, Lichtenberg-Kraag B, Steiner B, Berling B, Meyer H, Mercken M, Vandermeeren A, Goedert M, Mandelkow E (1992) The switch of tau protein to an Alzheimer-like state includes the phosphorylation of two serine-proline motifs upstream of the microtubule binding region. EMBO J 11:1593-1597.
3. Bosron WF, Li TK (1986) Genetic polymorphism of human liver alcohol and aldehyde dehydrogenases, and their relationship to alcohol metabolism and alcoholism. Hepatology 6:502-510.
4. Chen Z, Stamler JS (2006) Bioactivation of nitroglycerin by the mitochondrial aldehyde dehydrogenase. Trends Cardiovasc Med 16:259-265.
5. Chen Z, Zhang J, Stamler JS (2002) Identification of the enzymatic mechanism of nitroglycerin bioactivation. Proc Natl Acad Sci USA 99:8306-8311.
6. Cruz JC, Tsai LH (2004) A Jekyll and Hyde kinase: roles for Cdk5 in brain development and disease. Curr Opin Neurobiol 14:390-394.
7. D'Hooge R, De Deyn PP (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 36:60-90.
8. Esposito LA, Kokoszka JE, Waymire KG, Cottrell B, MacGregor GR, Wallace DC (2000) Mitochondrial oxidative stress in mice lacking the glutathione peroxidase-1 gene. Free Radic Biol Med 28:754-766.
9. Gadoni E, Olivero A, Miglietta A, Bocca C, Gabriel L (1993) Cytoskeletal modifications induced by 4-hydroxynonenal. Cytotechnology 11 [Suppl 1]:S62-S64.
10. Hamann M, Meisler MH, Richter A (2003) Motor disturbances in mice with deficiency of the sodium channel gene Scn8a show features of human dystonia. Exp Neurol 184:830-838.
11. Higuchi S, Matsushita S, Masaki T, Yokoyama A, Kimura M, Suzuki G, Mochizuki H (2004) Influence of genetic variations of ethanol-metabolizing enzymes on phenotypes of alcohol-related disorders. Ann NY Acad Sci 1025:472-480.
12. Ho YS, Xiong Y, Ma W, Spector A, Ho DS (2004) Mice lacking catalase develop normally but show differential sensitivity to oxidant tissue injury. J Biol Chem 279:32804-32812.
13. Imai H, Hirao F, Sakamoto T, Sekine K, Mizukura Y, Saito M, Kitamoto T, Hayasaka M, Hanaoka K, Nakagawa Y (2003) Early embryonic lethality caused by targeted disruption of the mouse PHGPx gene. Biochem Biophys Res Commun 305:278-286.
14. Isacson O, Fischer W, Wictorin K, Dawbarn D, Björklund A (1987) Astroglial response in the excitotoxically lesioned neostriatum and its projection areas in the rat. Neuroscience 20:1043-1056.
15. Jo SA, Kim E, Han C, Park MH, Jo I (2007) P-166A Glu487Lys polymorphism in the gene for mitochondrial aldehyde dehydrogenase 2 is associated with mild cognitive impairment in elderly Korean men. Alzheimers Dement 3:S151.
16. Kamino K, Nagasaka K, Imagawa M, Yamamoto H, Yoneda H, Ueki A, Kitamura S, Namekata K, Miki T, Ohta S (2000) Deficiency in mitochondrial aldehyde dehydrogenase increases the risk for late-onset Alzheimer's disease in the Japanese population. Biochem Biophys Res Commun 273:192-196.
17. Kim KS, Lee KW, Lee KW, Im JY, Yoo JY, Kim SW, Lee JK, Nestler EJ, Han PL (2006) Adenylyl cyclase type 5 (AC5) is an essential mediator of morphine action. Proc Natl Acad Sci USA 103:3908-3913.
18. Kitagawa K, Kawamoto T, Kunugita N, Tsukiyama T, Okamoto K, Yoshida A, Nakayama K, Nakayama K (2000) Aldehyde dehydrogenase (ALDH) 2 associates with oxidation of methoxyacetaldehyde; in vitro analysis with liver subcellular fraction derived from human and Aldh2 gene targeting mouse. FEBS Lett 476:306-311.
19. Liou YC, Sun A, Ryo A, Zhou XZ, Yu ZX, Huang HK, Uchida T, Bronson R, Bing G, Li X, Hunter T, Lu KP (2003) Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature 424:556-561.
20. Liu Q, Smith MA, Aváil J, DeBernardis J, Kansal M, Takeda A, Zhu X, Nunomura A, Honda K, Moreira PI, Oliveira CR, Santos MS, Shimohama S, Aliev G, de la Torre J, Ghanbari HA, Siedlak SL, Harris PL, Sayre LM, Perry G (2005) Alzheimer-specific epitopes of tau represent lipid peroxidation-induced conformations. Free Radic Biol Med 38:746-754.
21. Lovell MA, Ehmann WD, Mattson MP, Markesbery WR (1997) Elevated 4-hydroxynonenal in ventricular fluid in Alzheimer's disease. Neurobiol Aging 18:457-461.
22. Mark RJ, Pang Z, Geddes JW, Uchida K, Mattson MP (1997) Amyloid β-peptide impairs glucose transport in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J Neurosci 17:1046-1054.
23. Mattson MP (2004) Pathways towards and away from Alzheimer's disease. Nature 430:631-639.
24. Melov S, Schneider JA, Day BJ, Hinerfeld D, Coskun P, Mirra SS, Crapo JD, Wallace DC (1998) A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat Genet 18:159-163.
25. Miyakawa T, Yared E, Pak JH, Huang FL, Huang KP, Crawley JN (2001) Neurogranin null mutant mice display performance deficits on spatial learning tasks with anxiety related components. Hippocampus 11:763-775.
26. Miyamoto Y, Chen L, Sato M, Sokabe M, Nabeshima T, Pawson T, Sakai R, Mori N (2005) Hippocampal synaptic modulation by the phosphotyrosine adapter protein ShcC/N-Shc via interaction with the NMDA receptor. J Neurosci 25:1826-1835.
27. Mizushima S, Nagata S (1990) pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res 18:5322.
28. Montine KS, Olson SJ, Amarnath V, Whetsell Jr WO, Graham DG, Montine TJ (1997) Immunohistochemical detection of 4-hydroxy-2-nonenal adducts in Alzheimer's disease is associated with inheritance of APOE4. Am J Pathol 150:437-443.
29. Murakami Y, Ohsawa I, Kasahara T, Ohta S (2008) Cytoprotective role of mitochondrial amyloid beta peptide-binding alcohol dehydrogenase against a cytotoxic aldehyde. Neurobiol Aging, in press.
30. Murphy TC, Amarnath V, Gibson KM, Picklo Sr MJ (2003) Oxidation of 4-hydroxy-2-nonenal by succinic semialdehyde dehydrogenase (ALDH5A). J Neurochem 86:298-305.
31. Murray IV, Liu L, Komatsu H, Uryu K, Xiao G, Lawson JA, Axelsen PH (2007) Membrane-mediated amyloidogenesis and the promotion of oxidative lipid damage by amyloid beta proteins. J Biol Chem 282:9335-9345.
32. Neely MD, Sidell KR, Graham DG, Montine TJ (1999) The lipid peroxidation product 4-hydroxynonenal inhibits neurite outgrowth, disrupts neuronal microtubules, and modifies cellular tubulin. J Neurochem 72:2323-2333.
33. Ohsawa I, Nishimaki K, Yasuda C, Kamino K, Ohta S (2003a) Deficiency in a mitochondrial aldehyde dehydrogenase increases vulnerability to oxidative stress in PC12 cells. J Neurochem 84:1110-1117.
34. Ohsawa I, Kamino K, Nagasaka K, Ando F, Niino N, Shimokata H, Ohta S (2003b) Genetic deficiency of a mitochondrial aldehyde dehydrogenase increases serum lipid peroxides in community-dwelling females. J Hum Genet 48:404-409.
35. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, Katsura K, Katayama Y, Asoh S, Ohta S (2007) Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med 13:688-694.
36. Ohta S, Ohsawa I, Kamino K, Ando F, Shimokata H (2004) Mitochondrial ALDH2 deficiency as an oxidative stress. Ann NY Acad Sci 1011:36-44.
37. Pedersen WA, Cashman NR, Mattson MP (1999) The lipid peroxidation product 4-hydroxynonenal impairs glutamate and glucose transport and choline acetyltransferase activity in NSC-19 motor neuron cells. Exp Neurol 155:1-10.
38. Pedersen WA, Chan SL, Mattson MP (2000) A mechanism for the neuroprotective effect of apolipoprotein E: isoform-specific modification by the lipid peroxidation product 4-hydroxynonenal. J Neurochem 74:1426-1433.
39. Picklo MJ, Olson SJ, Markesbery WR, Montine TJ (2001) Expression and activities of aldo-keto oxidoreductases in Alzheimer disease. J Neuropathol Exp Neurol 60:686-695.
40. Praticò D, Clark CM, Liun F, Rokach J, Lee VY, Trojanowski JQ (2002) Increase of brain oxidative stress in mild cognitive impairment: a possible predictor of Alzheimer disease. Arch Neurol 59:972-976.
41. Reagan LP, Magariños AM, Yee DK, Swzeda LI, Van Bueren A, McCall AL, McEwen BS (2000) Oxidative stress and HNE conjugation of GLUT3 are increased in the hippocampus of diabetic rats subjected to stress. Brain Res 862:292-300.
42. Reaume AG, Elliott JL, Hoffman EK, Kowall NW, Ferrante RJ, Siwek DF, Wilcox HM, Flood DG, Beal MF, Brown Jr RH, Scott RW, Snider WD (1996) Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat Genet 13:43-47.
43. Sayre LM, Zelasko DA, Harris PL, Perry G, Salomon RG, Smith MA (1997) 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J Neurochem 68:2092-2097.
44. Schneider C, Tallman KA, Porter NA, Brash AR (2001) Two distinct pathways of formation of 4-hydroxynonenal. Mechanisms of nonenzymatic transformation of the 9- and 13-hydroperoxides of linoleic acid to 4-hydroxyalkenals. J Biol Chem 276:20831-20838.
45. Siems W, Grune T (2003) Intracellular metabolism of 4-hydroxynonenal. Mol Aspects Med 24:167-175.
46. Srivastava S, Chandra A, Ansari NH, Srivastava SK, Bhatnagar A (1998) Identification of cardiac oxidoreductase(s) involved in the metabolism of the lipid peroxidation-derived aldehyde-4-hydroxynonenal. Biochem J 329:469-475.
47. Suzuki Y, Muramatsu T, Taniyama M, Atsumi Y, Suematsu M, Kawaguchi R, Higuchi S, Asahina T, Murata C, Handa M, Matsuoka K (1996) Mitochondrial aldehyde dehydrogenase in diabetes associated with mitochondrial tRNA(Leu(UUR)) mutation at position 3243. Diabetes Care 19:1423-1425.
48. Takagi S, Iwai N, Yamauchi R, Kojima S, Yasuno S, Baba T, Terashima M, Tsutsumi Y, Suzuki S, Morii I, Hanai S, Ono K, Baba S, Tomoike H, Kawamura A, Miyazaki S, Nonogi H, Goto Y (2002) Aldehyde dehydrogenase 2 gene is a risk factor for myocardial infarction in Japanese men. Hypertens Res 25:677-681.
49. Takashima A (2006) GSK-3 is essential in the pathogenesis of Alzheimer's disease. J Alzheimers Dis 9:309-317.
50. Takeda A, Smith MA, Avilá J, Nunomura A, Siedlak SL, Zhu X, Perry G, Sayre LM (2000) In Alzheimer's disease, heme oxygenase is coincident with Alz50, an epitope of tau induced by 4-hydroxy-2-nonenal modification. J Neurochem 75:1234-1241.
51. Tang FR, Chia SC, Zhang S, Chen PM, Gao H, Liu CP, Khanna S, Lee WL (2005) Glutamate receptor 1-immunopositive neurons in the gliotic CA1 area of the mouse hippocampus after pilocarpine-induced status epilepticus. Eur J Neurosci 21:2361-2374.
52. Tjalkens RB, Cook LW, Petersen DR (1999) Formation and export of the glutathione conjugate of 4-hydroxy-2,3-E-nonenal (4-HNE) in hepatoma cells. Arch Biochem Biophys 361:113-119.
53. Uchida K (2003) 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 42:318-343.
54. Vasiliou V, Nebert DW (2005) Analysis and update of the human aldehyde dehydrogenase (ALDH) gene family. Hum Genomics 2:138-143.
55. Vasiliou V, Pappa A, Estey T (2004) Role of human aldehyde dehydrogenases in endobiotic and xenobiotic metabolism. Drug Metab Rev 36:279-299.
56. Wakabayashi-Ito N, Nagata S (1994) Characterization of the regulatory elements in the promoter of the human elongation factor-1 alpha gene. J Biol Chem 269:29831-29837.
57. Wang B, Wang J, Zhou S, Tan S, He X, Yang Z, Xie YC, Li S, Zheng C, Ma X (2008) The association of mitochondrial aldehyde dehydrogenase gene (ALDH2) polymorphism with susceptibility to late-onset Alzheimer's disease in Chinese. J Neurol Sci 268:172-175.
58. Wang H, Ferguson GD, Pineda VV, Cundiff PE, Storm DR (2004) Overexpression of type-1 adenylyl cyclase in mouse forebrain enhances recognition memory and LTP. Nat Neurosci 7:635-642.
59. Wenzel P, Hink U, Oelze M, Schuppan S, Schaeuble K, Schildknecht S, Ho KK, Weiner H, Bachschmid M, Munzel T, Daiber A (2007) Role of reduced lipoic acid in the redox regulation of mitochondrial aldehyde dehydrogenase (ALDH-2) activity. Implications for mitochondrial oxidative stress and nitrate tolerance. J Biol Chem 282:792-799.
60. Williams TI, Lynn BC, Markesbery WR, Lovell MA (2006) Increased levels of 4-hydroxynonenal and acrolein, neurotoxic markers of lipid peroxidation, in the brain in Mild Cognitive Impairment and early Alzheimer's disease. Neurobiol Aging 27:1094-1099.
61. Xie C, Lovell MA, Markesbery WR (1998) Glutathione transferase protects neuronal cultures against four hydroxynonenal toxicity. Free Radic Biol Med 25:979-988.
62. Yamaguchi J, Hasegawa Y, Kawasaki M, Masui T, Kanoh T, Ishiguro N, Hamajima N (2006) ALDH2 polymorphisms and bone mineral density in an elderly Japanese population. Osteoporos Int 17:908-913.
63. Yokoyama A, Omori T (2003) Genetic polymorphisms of alcohol and aldehyde dehydrogenases and risk for esophageal and head and neck cancers. Jpn J Clin Oncol 33:111-121.
64. Yoon M, Madden MC, Barton HA (2006) Developmental expression of aldehyde dehydrogenase in rat: a comparison of liver and lung development. Toxicol Sci 89:386-398.
65. Yoritaka A, Hattori N, Uchida K, Tanaka M, Stadtman ER, Mizuno Y (1996) Immunohistochemical detection of 4-hydroxynonenal protein adducts in Parkinson disease. Proc Natl Acad Sci USA 93:2696-2701.
66. Zarkovic K (2003) 4-Hydroxynonenal and neurodegenerative diseases. Mol Aspects Med 24:293-303.