Advances in the Pathogenesis of Alzheimer's Disease: Focusing on Tau-Mediated Neurodegeneration

Translational Neurodegeneration

Volumn 1, Issue , 2012, Pages

  Duan, Yale ^a   Dong, Suzhen ^a,b   Gu, Feng ^a   Hu, Yinghe ^a,b   Zhao, Zheng ^a  

^a B326 Science Building   (China)

^b EAST CHINA NORMAL UNIVERSITY   (China)

Author keywords

A beta; Alzheimer's disease; Intraneuronal neurofibrillary tangles; Tau; Tau hyperphosphorylation; Tauopathy

Indexed keywords

AMYLOID A PROTEIN; AMYLOID BETA PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN P35; PROTEIN P39; RNA; TAU PROTEIN;

ALTERNATIVE RNA SPLICING; ALZHEIMER DISEASE; CHROMOSOMAL INSTABILITY; HUMAN; MICROTUBULE; MICROTUBULE ASSEMBLY; MITOCHONDRIAL RESPIRATION; NERVE DEGENERATION; NERVE FIBER; NERVE FIBER GROWTH; NEUROFIBRILLARY TANGLE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; TRANSGENIC MOUSE;

EID: 84881128469     PISSN: None     EISSN: 20479158     Source Type: Journal    
DOI: 10.1186/2047-9158-1-24     Document Type: Review

References (68)

1. Lee VM, Goedert M, Trojanowski JQ. Neurodegenerative tauopathies. Annu Rev Neurosci 2001, 24:1121-1159. 10.1146/annurev.neuro.24.1.1121, 11520930.
2. Lee VMY. Tauists and baptists United-Well Almost!. Science 2001, 293:1446-1447. 10.1126/science.1064684, 11520974.
3. Dong SZ, Duan YL, Gu F, Hu YH, Zhao Z. Advances in the pathogenesis of Alzheimer's disease: a re-evaluation of amyloid cascade hypothesis. Translational Neurodegeneration 2012, 1:18. 10.1186/2047-9158-1-18, 3526416, 23210692.
4. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989, 3:519-526. 10.1016/0896-6273(89)90210-9, 2484340.
5. Lee G, Cowan N, Kirschner M. The primary structure and heterogeneity of tau protein from mouse brain. Science 1988, 239:285-288. 10.1126/science.3122323, 3122323.
6. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, Miller BI, Geschwind DH, Bird TD, McKeel D, Goate A, et al. Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 1998, 282:1914-1917.
7. Mazanetz MP, Fischer PM. Untangling tau hyperphosphorylation in drug design for neurodegenerative diseases. Nat Rev Drug Discov 2007, 6:464-479. 10.1038/nrd2111, 17541419.
8. Brion JP, Octave JN, Couck AM. Distribution of the phosphorylated microtubule-associated protein tau in developing cortical neurons. Neuroscience 1994, 63:895-909. 10.1016/0306-4522(94)90533-9, 7898684.
9. Yu Y, Run X, Liang Z, Li Y, Liu F, Liu Y, Iqbal K, Grundke-Iqbal I, Gong CX. Developmental regulation of tau phosphorylation, tau kinases, and tau phosphatases. J Neurochem 2009, 108:1480-1494. 10.1111/j.1471-4159.2009.05882.x, 2676439, 19183272.
10. Wang JZ, Liu F. Microtubule-associated protein tau in development, degeneration and protection of neurons. Prog Neurobiol 2008, 85:148-175. 10.1016/j.pneurobio.2008.03.002, 18448228.
11. Lee G, Newman ST, Gard DL, Band H, Panchamoorthy G. Tau interacts with src-family non-receptor tyrosine kinases. J Cell Sci 1998, 111(Pt 21):3167-3177.
12. Reynolds CH, Garwood CJ, Wray S, Price C, Kellie S, Perera T, Zvelebil M, Yang A, Sheppard PW, Varndell IM, et al. Phosphorylation regulates tau interactions with SH3 domains of phosphatidylinositol-3-kinase, phospholipase cgamma 1, GRB2 and SRC-family kinases. J Biol Chem 2008, 283(26):18177-86. 10.1074/jbc.M709715200, 18467332.
13. Sjoberg MK, Shestakova E, Mansuroglu Z, Maccioni RB, Bonnefoy E. Tau protein binds to pericentromeric DNA: a putative role for nuclear tau in nucleolar organization. J Cell Sci 2006, 119:2025-2034. 10.1242/jcs.02907, 16638814.
14. Rossi G, Dalpra L, Crosti F, Lissoni S, Sciacca FL, Catania M, Di Fede G, Mangieri M, Giaccone G, Croci D, Tagliavini F. A new function of microtubule-associated protein tau: involvement in chromosome stability. Cell Cycle 2008, 7:1788-1794. 10.4161/cc.7.12.6012, 18583940.
15. Wang JZ, Grundke-Iqbal I, Iqbal K. Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur J Neurosci 2007, 25:59-68. 10.1111/j.1460-9568.2006.05226.x, 3191918, 17241267.
16. Congdon EE, Kim S, Bonchak J, Songrug T, Matzavinos A, Kuret J. Nucleation-dependent Tau Filament Formation: the importance of dimerization and an estimation of elementary rate constants. J Biol Chem 2008, 283:13806-13816. 10.1074/jbc.M800247200, 2376241, 18359772.
17. Andersen JK. Oxidative stress in neurodegeneration: cause or consequence?. Nat Med 2004, 10(Suppl):S18-25.
18. King ME, Kan HM, Baas PW, Erisir A, Glabe CG, Bloom GS. Tau-dependent microtubule disassembly initiated by prefibrillar beta-amyloid. J Cell Biol 2006, 175:541-546. 10.1083/jcb.200605187, 2064590, 17101697.
19. Moreira PI, Smith MA, Zhu X, Nunomura A, Castellani RJ, Perry G. Oxidative stress and neurodegeneration. Ann N Y Acad Sci 2005, 1043:545-552. 10.1196/annals.1333.062, 16037277.
20. Rapoport M, Dawson HN, Binder LI, Vitek MP, Ferreira A. Tau is essential to beta -amyloid-induced neurotoxicity. PNAS 2002, 99:6364-6369. 10.1073/pnas.092136199, 122954, 11959919.
21. David DC, Hauptmann S, Scherping I, Schuessel K, Keil U, Rizzu P, Ravid R, Drose S, Brandt U, Muller WE, et al. Proteomic and functional analyses reveal a mitochondrial dysfunction in P301L tau transgenic mice. J Biol Chem 2005, 280:23802-23814. 10.1074/jbc.M500356200, 15831501.
22. Revett TJ, Baker GB, Jhamandas J, Kar S. Glutamate system, amyloid ss peptides and tau protein: functional interrelationships and relevance to Alzheimer disease pathology. J Psychiatry Neurosci 2012, 37:110190.
23. DuBoff B, Götz J, Feany Mel B. Tau Promotes Neurodegeneration via DRP1 Mislocalization In Vivo. Neuron 2012, 75:618-632. 10.1016/j.neuron.2012.06.026, 22920254.
24. Sotiropoulos I, Catania C, Pinto LG, Silva R, Pollerberg GE, Takashima A, Sousa N, Almeida OF. Stress acts cumulatively to precipitate Alzheimer's disease-like tau pathology and cognitive deficits. J Neurosci 2011, 31:7840-7847. 10.1523/JNEUROSCI.0730-11.2011, 21613497.
25. Ho YS, Yang X, Lau JC, Hung CH, Wuwongse S, Zhang Q, Wang J, Baum L, So KF, Chang RC. Endoplasmic reticulum stress induces tau pathology and forms a vicious cycle: implication in Alzheimer's disease pathogenesis. J Alzheimers Dis 2012, 28:839-854.
26. Kim I, Park EJ, Seo J, Ko SJ, Lee J, Kim CH. Zinc stimulates tau S214 phosphorylation by the activation of Raf/mitogen-activated protein kinase-kinase/extracellular signal-regulated kinase pathway. Neuroreport 2011, 22:839-844.
27. Tsai LH, Delalle I, Caviness VS, Chae T, Harlow E. p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature 1994, 371:419-423. 10.1038/371419a0, 8090221.
28. Hashiguchi M, Saito T, Hisanaga S, Hashiguchi T. Truncation of CDK5 activator p35 induces intensive phosphorylation of Ser202/Thr205 of human tau. J Biol Chem 2002, 277:44525-44530. 10.1074/jbc.M207426200, 12226093.
29. Patzke H, Tsai LH. Calpain-mediated cleavage of the cyclin-dependent kinase-5 activator p39 to p29. J Biol Chem 2002, 277:8054-8060. 10.1074/jbc.M109645200, 11784720.
30. Lee KY, Clark AW, Rosales JL, Chapman K, Fung T, Johnston RN. Elevated neuronal Cdc2-like kinase activity in the Alzheimer disease brain. Neurosci Res 1999, 34:21-29. 10.1016/S0168-0102(99)00026-7, 10413323.
31. Tseng HC, Zhou Y, Shen Y, Tsai LH. A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains. FEBS Lett 2002, 523:58-62. 10.1016/S0014-5793(02)02934-4, 12123804.
32. Ahlijanian MK, Barrezueta NX, Williams RD, Jakowski A, Kowsz KP, McCarthy S, Coskran T, Carlo A, Seymour PA, Burkhardt JE, et al. Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. PNAS 2000, 97:2910-2915. 10.1073/pnas.040577797, 16029, 10706614.
33. Cruz JC, Tseng HC, Goldman JA, Shih H, Tsai LH. Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 2003, 40:471-483. 10.1016/S0896-6273(03)00627-5, 14642273.
34. Van den Haute C, Spittaels K, Van Dorpe J, Lasrado R, Vandezande K, Laenen I, Geerts H, Van Leuven F. Coexpression of human cdk5 and its activator p35 with human protein tau in neurons in brain of triple transgenic mice. Neurobiol Dis 2001, 8:32-44. 10.1006/nbdi.2000.0333, 11162238.
35. Plattner F, Angelo M, Giese KP. The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J Biol Chem 2006, 281:25457-25465. 10.1074/jbc.M603469200, 16803897.
36. Lovestone S, Reynolds CH, Latimer D, Davis DR, Anderton BH, Gallo JM, Hanger D, Mulot S, Marquardt B, Stabel S, et al. Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr Biol 1994, 4:1077-1086. 10.1016/S0960-9822(00)00246-3, 7704571.
37. Sperber BR, Leight S, Goedert M, Lee VM. Glycogen synthase kinase-3 beta phosphorylates tau protein at multiple sites in intact cells. Neurosci Lett 1995, 197:149-153. 10.1016/0304-3940(95)11902-9, 8552282.
38. Hernandez F, Borrell J, Guaza C, Avila J, Lucas JJ. Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J Neurochem 2002, 83:1529-1533. 10.1046/j.1471-4159.2002.01269.x, 12472906.
39. Hurtado DE, Molina-Porcel L, Carroll JC, Macdonald C, Aboagye AK, Trojanowski JQ, Lee VM. Selectively silencing GSK-3 isoforms reduces plaques and tangles in mouse models of Alzheimer's disease. J Neurosci 2012, 32:7392-7402. 10.1523/JNEUROSCI.0889-12.2012, 3368584, 22623685.
40. Drewes G, Ebneth A, Preuss U, Mandelkow EM, Mandelkow E. MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 1997, 89:297-308. 10.1016/S0092-8674(00)80208-1, 9108484.
41. Kosuga S, Tashiro E, Kajioka T, Ueki M, Shimizu Y, Imoto M. GSK-3beta directly phosphorylates and activates MARK2/PAR-1. J Biol Chem 2005, 280:42715-42722. 10.1074/jbc.M507941200, 16257959.
42. Phiel CJ, Wilson CA, Lee VM, Klein PS. GSK-3alpha regulates production of Alzheimer's disease amyloid-beta peptides. Nature 2003, 423:435-439. 10.1038/nature01640, 12761548.
43. Lee MS, Kao SC, Lemere CA, Xia W, Tseng HC, Zhou Y, Neve R, Ahlijanian MK, Tsai LH. APP processing is regulated by cytoplasmic phosphorylation. J Cell Biol 2003, 163:83-95. 10.1083/jcb.200301115, 2173445, 14557249.
44. Gong CX, Shaikh S, Wang JZ, Zaidi T, Grundke-Iqbal I, Iqbal K. Phosphatase activity toward abnormally phosphorylated tau: decrease in Alzheimer disease brain. J Neurochem 1995, 65:732-738.
45. Chen S, Li B, Grundke-Iqbal I, Iqbal K. I1PP2A affects tau phosphorylation via association with the catalytic subunit of protein phosphatase 2A. J Biol Chem 2008, 283:10513-10521. 10.1074/jbc.M709852200, 2447634, 18245083.
46. Liu R, Zhou XW, Tanila H, Bjorkdahl C, Wang JZ, Guan ZZ, Cao Y, Gustafsson JA, Winblad B, Pei JJ. Phosphorylated PP2A (tyrosine 307) is associated with Alzheimer neurofibrillary pathology. J Cell Mol Med 2008, 12:241-257.
47. Martin L, Latypova X, Terro F. Post-translational modifications of tau protein: Implications for Alzheimer's disease. Neurochem Int 2011, 58:458-471. 10.1016/j.neuint.2010.12.023, 21215781.
48. Wang JZ, Xia YY, Grundke-Iqbal I, Iqbal K. Abnormal Hyperphosphorylation of Tau: Sites, Regulation, and Molecular Mechanism of Neurofibrillary Degeneration. J Alzheimers Dis 2012,
49. Irwin DJ, Cohen TJ, Grossman M, Arnold SE, Xie SX, Lee VMY, Trojanowski JQ. Acetylated tau, a novel pathological signature in Alzheimer's disease and other tauopathies. Brain 2012, 135:807-818. 10.1093/brain/aws013, 3286338, 22366796.
50. Min SW, Cho SH, Zhou Y, Schroeder S, Haroutunian V, Seeley WW, Huang EJ, Shen Y, Masliah E, Mukherjee C, et al. Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron 2010, 67:953-966. 10.1016/j.neuron.2010.08.044, 3035103, 20869593.
51. Santacruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, Guimaraes A, DeTure M, Ramsden M, McGowan E, et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005, 309:476-481. 10.1126/science.1113694, 1574647, 16020737.
52. Le Corre S, Klafki HW, Plesnila N, Hubinger G, Obermeier A, Sahagun H, Monse B, Seneci P, Lewis J, Eriksen J, et al. An inhibitor of tau hyperphosphorylation prevents severe motor impairments in tau transgenic mice. PNAS 2006, 103:9673-9678. 10.1073/pnas.0602913103, 1480465, 16769887.
53. Trojanowski JQ, Lee VM. Pathological tau: a loss of normal function or a gain in toxicity?. Nat Neurosci 2005, 8:1136-1137. 10.1038/nn0905-1136, 16127446.
54. Winklhofer KF, Tatzelt J, Haass C. The two faces of protein misfolding: gain- and loss-of-function in neurodegenerative diseases. EMBO J 2008, 27:336-349. 10.1038/sj.emboj.7601930, 2234348, 18216876.
55. Hyman BT, Trojanowski JQ. Consensus recommendations for the postmortem diagnosis of Alzheimer disease from the National Institute on Aging and the Reagan Institute Working Group on diagnostic criteria for the neuropathological assessment of Alzheimer disease. J Neuropathol Exp Neurol 1997, 56:1095-1097. 10.1097/00005072-199710000-00002, 9329452.
56. Frost B, Jacks RL, Diamond MI. Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 2009, 284:12845-12852. 10.1074/jbc.M808759200, 2676015, 19282288.
57. Guo JL, Lee VM. Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J Biol Chem 2011, 286:15317-15331. 10.1074/jbc.M110.209296, 3083182, 21372138.
58. Nonaka T, Watanabe ST, Iwatsubo T, Hasegawa M. Seeded aggregation and toxicity of {alpha}-synuclein and tau: cellular models of neurodegenerative diseases. J Biol Chem 2010, 285:34885-34898. 10.1074/jbc.M110.148460, 2966103, 20805224.
59. de Calignon A, Polydoro M, Suarez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, Pitstick R, Sahara N, Ashe KH, Carlson GA, et al. Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 2012, 73:685-697. 10.1016/j.neuron.2011.11.033, 3292759, 22365544.
60. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, Wu T, Gerstein H, Yu GQ, Mucke L. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 2007, 316:750-754. 10.1126/science.1141736, 17478722.
61. Guo JP, Arai T, Miklossy J, McGeer PL. Abeta and tau form soluble complexes that may promote self aggregation of both into the insoluble forms observed in Alzheimer's disease. PNAS 2006, 103:1953-1958. 10.1073/pnas.0509386103, 1413647, 16446437.
62. Bolmont T, Clavaguera F, Meyer-Luehmann M, Herzig MC, Radde R, Staufenbiel M, Lewis J, Hutton M, Tolnay M, Jucker M. Induction of tau pathology by intracerebral infusion of amyloid-beta -containing brain extract and by amyloid-beta deposition in APP x Tau transgenic mice. Am J Pathol 2007, 171:2012-2020. 10.2353/ajpath.2007.070403, 2111123, 18055549.
63. Fein JA, Sokolow S, Miller CA, Vinters HV, Yang F, Cole GM, Gylys KH. Co-localization of amyloid beta and tau pathology in Alzheimer's disease synaptosomes. Am J Pathol 2008, 172:1683-1692. 10.2353/ajpath.2008.070829, 2408427, 18467692.
64. Kimura R, Kamino K, Yamamoto M, Nuripa A, Kida T, Kazui H, Hashimoto R, Tanaka T, Kudo T, Yamagata H, et al. The DYRK1A gene, encoded in chromosome 21 Down syndrome critical region, bridges between beta-amyloid production and tau phosphorylation in Alzheimer disease. Hum Mol Genet 2007, 16:15-23.
65. Nussbaum JM, Schilling S, Cynis H, Silva A, Swanson E, Wangsanut T, Tayler K, Wiltgen B, Hatami A, Ronicke R, et al. Prion-like behaviour and tau-dependent cytotoxicity of pyroglutamylated amyloid-beta. Nature 2012, 485:651-655. 10.1038/nature11060, 3367389, 22660329.
66. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, Wolfing H, Chieng BC, Christie MJ, Napier IA, et al. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010, 142:387-397. 10.1016/j.cell.2010.06.036, 20655099.
67. Rhein V, Song X, Wiesner A, Ittner LM, Baysang G, Meier F, Ozmen L, Bluethmann H, Drose S, Brandt U, et al. Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice. PNAS 2009, 106:20057-20062. 2774257, 19897719.
68. Ittner LM, Götz J. Amyloid-β and tau - a toxic pas de deux in Alzheimer's disease. Nat Rev Neurosci 2010, 12:65-72.