Repression of tau hyperphosphorylation by chronic endurance exercise in aged transgenic mouse model of tauopathies

Journal of Neuroscience Research

Volumn 87, Issue 11, 2009, Pages 2561-2570

  Leem, Yea Hyun ^a   Lim, Hwa Ja ^b   Shim, Sun Bo ^b   Cho, Joon Yong ^c   Kim, Bum Soo ^d   Han, Pyung Lim ^a  

^a Ewha Womans University   (South Korea)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c Korea National Sport University   (South Korea)

^d Sungshin Women's University   (South Korea)

Author keywords

Alzheimer; Cu Zn SOD; Exercise; Tau; Wnt

Indexed keywords

BETA CATENIN; CYCLIN D1; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; SERINE; SUPEROXIDE DISMUTASE; T CELL FACTOR PROTEIN; T CELL FACTOR PROTEIN 4; TAU PROTEIN; THREONINE; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDURANCE; ENZYME ACTIVITY; EXERCISE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; TAUOPATHY; TRANSGENIC MOUSE; TREADMILL EXERCISE; UPREGULATION; AGING; ANIMAL; BRAIN; DISEASE MODEL; ENZYMOLOGY; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AGING; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; PHYSICAL CONDITIONING, ANIMAL; SIGNAL TRANSDUCTION; TAU PROTEINS; TAUOPATHIES;

EID: 70349256254     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22075     Document Type: Article

References (48)

1. Adlard PA, Perreau VM, Pop V, Cotman CW. 2005. Voluntary exercise decreased amyloid load in a transgenic model of Alzheimer's disease. J Neurosci 25:4217-4221. (Pubitemid 40628765)
2. Alkon DL, Sun MK, Nelson TJ. 2007. PKC signaling deficits: a mechanistic hypothesis for the origins of Alzheimer's disease. Trends Pharmacol Sci 28:51-60.
3. Andreadis A, Broderick JA, Kosik KS. 1995. Relative exon affinities and suboptimal splice site signals lead to non-equivalence of two cassette exons. Nucleic Acids Res 23:3585-3593.
4. Asuni AA, Hooper C, Reynolds CH, Lovestone S, Anderton BH, Killick R. 2006. GSK3alpha exhibits beta-catenin and tau directed kinase activities that are modulated by Wnt. Eur J Neurosci 24:3387-3392. (Pubitemid 44952605)
5. Bayer TA, Schafer S, Simons A, Kemmling A, Kamer T, Tepest R, Eckert A, Schussel K, Eikenberg O, Staufenbiel M, Multhaup G. 2003. Dietary Cu stabilizes brain superoxide dismutase 1 activity and reduces amyloid Abeta production in APP23 transgenic mic. Proc Natl Acad Sci U S A 100:14187-14192. (Pubitemid 37499212)
6. Bellucci A, Rosi MC, Grossi C, Fiorentini A, Luccarini I, Casamenti F. 2007. Abnormal processing of tau in the brain of aged TgCRND8 mice. Neurobiol Dis 27:328-338. (Pubitemid 47333192)
7. Blennow K, de Leon MJ, Zetterberg H. 2006. Alzheimer's disease. Lancet 368:387-403.
8. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR. 2000. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 33:95-130. (Pubitemid 30680029)
9. Casado A, Encarnación López-Fernández M, Concepción Casado M, de La Torre R. 2008. Lipid peroxidation and antioxidant enzyme activities in vascular and Alzheimer dementias. Neurochem Res 33:450-458. (Pubitemid 351230446)
10. Cho JH, Johnson GV. 2003. Primed phosphorylation of tau at Thr231 by glycogen synthase kinase 3beta (GSK3beta) plays a critical role in regulating tau's ability to bind and stabilize microtubules. J Neurochem 88:349-358.
11. Chow LS, Greenlund LJ, Asmann YW, Short KR, McCrady SK, Levine JA, Nair KS. 2007. Impact of endurance training on murine spontaneous activity, muscle mitochondrial DNA abundance, gene transcripts, and function. J Appl Physiol 102:1078-1089.
12. Cotman CW, Berchtold NC. 2002. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295-301.
13. Le Corre S, Klafki HW, Plesnila N, Hübinger G, Obermeier A, Sahagún H, Monse B, Seneci P, Lewis J, Eriksen J, Zehr C, Yue M, McGowan E, Dickson DW, Hutton M, Roder HM. 2006. An inhibitor of tau hyperphosphorylation prevents severe motor impairments in tau transgenic mice. Proc Natl Acad Sci U S A 103:9673-9678. (Pubitemid 43955883)
14. Devi SA, Kiran TR. 2004. Regional responses in antioxidant system to exercise training and dietary vitamin E in aging rat brain. Neurobiol Aging 25:501-508.
15. Ferrer I, Blanco R, Carmona M, Puig B. 2001. Phosphorylated mitogen-activated protein kinase (MAPK/ERK-P), protein kinase of 38 kDa (p38-P), stress-activated protein kinase (SAPK/JNK-P), and calcium/calmodulin-dependent kinase II (CaM kinase II) are differentially expressed in tau deposits in neurons and glial cells in tauopathies. J Neural Transm 108:1397-1415. (Pubitemid 34020445)
16. Friedland RP, Fritsch T, Smyth KA, Koss E, Lerner AJ, Chen CH, Petot GJ.Debanne SM. 2001. Patients with Alzheimer's disease have reduced activities in middlelife compared with healthy control group members. Proc Natl Acad Sci U S A 98:3440-3445. (Pubitemid 32220864)
17. Kirschenbaum F, Hsu SC, Cordell B, McCarthy JV. 2001. Glycogen synthase kinase-3beta regulates presenilin 1 C-terminal fragment levels. J Biol Chem 276:30701-30707. (Pubitemid 37384925)
18. Gibson GE, Huang HM. 2002. Oxidative processes in the brain and non-neuronal tissues as biomarkers of Alzheimer's disease. Front Biosci 7:d1007-d1015.
19. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA. 1989. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3:519-526.
20. Gong CX, Liu F, Grundke-Iqbal I, Iqbal K. 2005. Posttranslational modifications of tau protein in Alzheimer's disease. J Neural Transm 112:813-838. (Pubitemid 40655573)
21. Goto S, Naito H, Kaneko T, Chung HY, Radák Z. 2007. Hormetic effects of regular exercise in aging: correlation with oxidative stress. Appl Physiol Nutr Metab 32:948-953.
22. Hernández F, Avila J. 2007. Tauopathies. Cell Mol Life Sci 64:2219-2233.
23. Kaczor JJ, Hall JE, Payne E, Tarnopolsky MA. 2007. Low intensity training decreases markers of oxidative stress in skeletal muscle of mdx mice. Free Radic Biol Med 43:145-154. (Pubitemid 46874844)
24. Kaytor MD, Orr HT. 2002. The GSK3 beta signaling cascade and neurodegenerative disease. Curr Opin Neurobiol 12:275-278.
25. Kosik KS, Shimura H. 2005. Phosphorylated tau and the neurodegenerative foldopathies. Biochim Biophys Acta 1739:298-310.
26. Kramer AF, Hahn S, Cohen NJ, Banich MT, McAuley E, Harrison CR, Chason J, Vakil E, Bardell L, Boileau RA.Colcombe A. 1999. Aging, fitness and neurocognitive function. Nature 400:418-419.
27. Lee KW, Kim JB, Seo JS, Kim TK, Im JY, Baek IS, Kim KS, Lee JK, Han PL. 2009. Behavioral stress enhances Alzheimer's disease pathogenesis via metabolic oxidative stress. J Neurochem 108:165-175.
28. Lerman I, Harrison BC, Freeman K, Hewett TE, Allen DL.Robbins J, Leinwand LA. 2002. Genetic variability in forced and viloutary endurance exercise performance in seven inbred mouse strains. J Appl Physiol 92:2245-2255. (Pubitemid 34666344)
29. Liu J, Yeo HC, Overvik-Douki E, Hagen T, Doniger SJ, Chyu DW, Brooks GA, Ames BN. 2000. Chronically and acutely exercised rats: biomarkers of oxidative stress and endogenous antioxidants. J Appl Physiol 89:21-28. (Pubitemid 30482559)
30. Liu SJ, Zhang AH, Li HL, Wang Q, Deng HM, Netzer WJ, Xu H, Wang JZ. 2003. Overactivation of glycogen synthase kinase-3 by inhibition of phosphoinositol-3 kinase and protein kinase C leads to hyperphosphorylation of tau and impairment of spatial memory. J Neurochem 87:1333-1344. (Pubitemid 38020568)
31. Liu SJ, Zhang JY, Li HL, Fang ZY, Wang Q, Deng HM, Gong CX, Grundke-Iqbal I, Iqbal K, Wang JZ. 2004. Tau becomes a more favorable substrate for GSK-3 when it is prephosphorylated by PKA in rat brain. J Biol Chem 279:50078-50088. (Pubitemid 39577819)
32. Marcus DL, Strafaci JA, Freedman ML. 2006. Differential neuronal expression of manganese superoxide dismutase in Alzheimer's disease. Med Sci Monit 12:BR8-BR14.
33. Massett MP, Berk BC. 2005. Strain-dependent differences in response to exercise training in inbred and hybrid mice. Am J Physiol Regul Integr Comp Physiol 288:R1006-R1014.
34. Mattson PM. 2004. Pathways towards and away from Alzheimer's disease. Nature 430:631-639. (Pubitemid 39061671)
35. Moon RT, Kohn AD, De Ferrari GV, Kaykas A. 2004. Wnt and β-catenin signaling: disease and therapies. Nature 5:689-699. (Pubitemid 39150127)
36. Navarro A, Gomez C, López-Cepero JM, Boveris A. 2004. Beneficial effects of moderate exercise on mice aging: survival, behavior, oxidative stress, and mitochondrial electron transfer. Am J Physiol Regul Integr Comp Physiol 286:R505-R511. (Pubitemid 38252615)
37. Nelson WJ, Nusse R. 2004. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303:1483-1487. (Pubitemid 38314410)
38. Noble W, Planel E, Zehr C, Olm V, Meyerson J, Suleman F, Gaynor K, Wang L, LaFrancois J, Feinstein B, Burns M, Krishnamurthy P, Wen Y, Bhat R, Lewis J, Dickson D, Duff K. 2005. Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad Sci U S A 102:6990-6995. (Pubitemid 40675429)
39. Nusse R. 2005. Wnt signaling in disease and in development. Cell Res 15:28-32.
40. Romanick MA, Rakoczy SG, Brown-Borg HM. 2004. Long-lived Ames dwarf mouse exhibits increased antioxidant defense in skeletal muscle. Mech Ageing 125:269-281.
41. Rosa EF, Silva AC, Ihara SS, Mora OA, Aboulafia J, Nouailhetas VL. 2005. Habitual exercise program protects murine intestinal, skeletal, and cardiac muscles against aging. J Appl Physiol 99:1569-1575. (Pubitemid 43014368)
42. Schuessel K, Schafer S, Bayer TA, Czech C, Pradier L, Muller-Spahn F, Muller WE, Eckert A. 2005. Impared Cu/Zn-SOD activity contributes to increased oxidative damage in APP transgenic mice. Neurobiol Dis 18:89-99. (Pubitemid 40092899)
43. Shim SB, Lim HJ, Chae KR, Kim CK, Hwang DY, Jee SW, Lee SH, Sin JS, Leem YH, Lee SH, Cho JS, Lee HH, Choi SY, Kim YK. 2007. Tau overexpression in transgenic mice induces glycogen synthase kinase 3beta and beta-catenin phosphorylation. Neuroscience 146:730-740.
44. Somani SM, Husain K, Diaz-Phillips L, Lanzotti DJ, Kareti KR, Trammell GL. 1996. Interaction of exercise and ethanol on antioxidant enzymes in brain regions of the rat. Alcohol 13:603-610. (Pubitemid 26404181)
45. Stoothoff WH, Cho JH, McDonald RP, Johnson GV. 2005. FRAT-2 preferentially increases glycogen synthase kinase 3 beta-mediated phosphorylation of primed sites, which results in enhanced tau phosphorylation. J Biol Chem 280:270-276.
46. Takashima A, Murayama M, Murayama O. 1998. Presenilin 1 associates with glycogen synthase kinase and its substrate. Proc Natl Acad Sci U S A 95:9637-9641. (Pubitemid 28506284)
47. Thinakaran G, Borchelt DR, Lee MK, Slunt HH, Spitzer L, Kim G, Ratovitsky T, Davenport F, Nordstedt C, Seeger M, Hardy J, Levey AI, Gandy SE, Jenkins NA, Copeland NG, Price DL, Sisodia SS. 1996. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron 17:181-190. (Pubitemid 26251602)
48. Zhu X, Rottkamp CA, Hartzler A, Sun Z, Takeda A, Boux H, Shimohama S, Perry G, Smith MA. 2001. Activation of MKK6, an upstream activator of p38, in Alzheimer's disease. J Neurochem 79:311-318. (Pubitemid 32988947)