Dissociation of tau toxicity and phosphorylation: Role of GSK-3β, MARK and Cdk5 in a Drosophila model

Human Molecular Genetics

Volumn 18, Issue 1, 2009, Pages 164-177

  Chatterjee, Shreyasi ^a   Sang, Tzu Kang ^b   Lawless, George M ^a   Jackson, George R ^a,c,d,e,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e University of Texas Medical Branch School of Medicine   (United States)

^f UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEINASE ACTIVATED RECEPTOR 1; TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; IMMUNOREACTIVITY; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; TAUOPATHY; TISSUE LEVEL; TRANSGENE; WILD TYPE;

ALZHEIMER DISEASE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CYCLIN-DEPENDENT KINASE 5; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MICROTUBULES; MUTATION, MISSENSE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; TAU PROTEINS;

ANIMALIA;

EID: 57649203362     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn326     Document Type: Article

References (68)

1. Morishima-Kawashima, M., Hasegawa, M., Takio, K., Suzuki, M., Yoshida, H., Watanabe, A., Titani, K. and Ihara, Y. (1995) Hyperphosphorylation of tau in PHF. Neurobiol. Aging, 16, 365-371.
2. Johnson, G.V. and Bailey, C.D. (2002) Tau, where are we now? J. Alzheimers Dis., 4, 375-398.
3. Cho, J.H. and Johnson, G.V. (2003) Glycogen synthase kinase 3beta phosphorylates tau at both primed and unprimed sites. Differential impact on microtubule binding. J. Biol. Chem., 278, 187-193.
4. Augustinack, J.C., Schneider, A., Mandelkow, E.M. and Hyman, B.T. (2002) Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol. (Berl.), 103, 26-35.
5. Baum, L., Hansen, L., Masliah, E. and Saitoh, T. (1996) Glycogen synthase kinase 3 alteration in Alzheimer disease is related to neurofibrillary tangle formation. Mol. Chem. Neuropathol., 29 253-261.
6. Lovestone, S., Reynolds, C.H., Latimer, D., Davis, D.R., Anderton, B.H., Gallo, J.M., Hanger, D., Mulot, S., Marquardt, B., Stabel, S. et al. (1994) Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr. Biol., 4, 1077-1086.
7. Mandelkow, E.M., Drewes, G., Biernat, J., Gustke, N., Van Lint, J., Vandenheede, J.R. and Mandelkow, E. (1992) Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett., 314, 315-321.
8. Mulot, S.F., Hughes, K., Woodgett, J.R., Anderton, B.H. and Hanger, D.P. (1994) PHF-tau from Alzheimer's brain comprises four species on SDS-PAGE which can be mimicked by in vitro phosphorylation of human brain tau by glycogen synthase kinase-3 beta. FEBS Lett., 349, 359-364.
9. Kobayashi, S., Ishiguro, K., Omori, A., Takamatsu, M., Arioka, M., Imahori, K. and Uchida, T. (1993) A cdc2-related kinase PSSALRE/cdk5 is homologous with the 30 kDa subunit of tau protein kinase II, a proline-directed protein kinase associated with microtubule. FEBS Lett., 335, 171-175.
10. Singh, T.J., Zaidi, T., Grundke-Iqbal, I. and Iqbal, K. (1995) Modulation of GSK-3-catalyzed phosphorylation of microtubule-associated protein tau by non-proline-dependent protein kinases. FEBS Lett., 358, 4-8.
11. Sperber, B.R., Leight, S., Goedert, M. and Lee, V.M. (1995) Glycogen synthase kinase-3 beta phosphorylates tau protein at multiple sites in intact cells. Neurosci. Lett., 197, 149-153.
12. Zheng-Fischhofer, Q., Biernat, J., Mandelkow, E.M., Illenberger, S., Godemann, R. and Mandelkow, E. (1998) Sequential phosphorylation of Tau by glycogen synthase kinase-3beta and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical-filament-like conformation. Eur. J. Biochem., 252, 542-552.
13. Reynolds, C.H., Utton, M.A., Gibb, G.M., Yates, A. and Anderton, B.H. (1997) Stress-activated protein kinase/c-jun N-terminal kinase phosphorylates tau protein. J. Neurochem., 68, 1736-1744.
14. Roder, H.M., Eden, P.A. and Ingram, V.M. (1993) Brain protein kinase PK40erk converts TAU into a PHF-like form as found in Alzheimer's disease. Biochem. Biophys. Res. Commun., 193, 639-647.
15. Hyman, B.T., Elvhage, T.E. and Reiter, J. (1994) Extracellular signal regulated kinases. Localization of protein and mRNA in the human hippocampal formation in Alzheimer's disease. Am. J. Pathol., 144, 565-572.
16. Ledesma, M.D., Correas, I., Avila, J. and Diaz-Nido, J. (1992) Implication of brain cdc2 and MAP2 kinases in the phosphorylation of tau protein in Alzheimer's disease. FEBS Lett., 308, 218-224.
17. Robertson, J., Loviny, T.L., Goedert, M., Jakes, R., Murray, K.J., Anderton, B.H. and Hanger, D.P. (1993) Phosphorylation of tau by cyclic-AMP-dependent protein kinase. Dementia, 4, 256-263.
18. Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E.M. and Mandelkow, E. (1997) MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell, 89, 297-308.
19. Jenkins, S.M., Zinnerman, M., Garner, C. and Johnson, G.V. (2000) Modulation of tau phosphorylation and intracellular localization by cellular stress. Biochem. J., 345, 263-270.
20. Kannanayakal, T.J., Tao, H., Vandre, D.D. and Kuret, J. (2006) Casein kinase-1 isoforms differentially associate with neurofibrillary and granulovacuolar degeneration lesions. Acta Neuropathol., 111 413-421.
21. Jackson, G.R., Wiedau-Pazos, M., Sang, T.K., Wagle, N., Brown, C.A., Massachi, S. and Geschwind, D.H. (2002) Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron, 34, 509-519.
22. Wittmann, C.W., Wszolek, M.F., Shulman, J.M., Salvaterra, P.M., Lewis, J., Hutton, M. and Feany, M.B. (2001) Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science, 293 711-714.
23. Williams, D.W., Tyrer, M. and Shepherd, D. (2000) Tau and tau reporters disrupt central projections of sensory neurons in Drosophila. J. Comp. Neurol., 428, 630-640.
24. Shulman, J.M., Benton, R. and St Johnston, D. (2000) The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell, 101, 377-388.
25. Nishimura, I., Yang, Y. and Lu, B. (2004) PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila. Cell, 116, 671-682.
26. Steinhilb, M.L., Dias-Santagata, D., Fulga, T.A., Felch, D.L. and Feany, M.B. (2007) Tau phosphorylation sites work in concert to promote neurotoxicity in vivo. Mol. Biol. Cell., 18, 5060-5068.
27. Steinhilb, M.L., Dias-Santagata, D., Mulkearns, E.E., Shulman, J.M., Biernat, J., Mandelkow, E.M. and Feany, M.B. (2007) S/P and T/P phosphorylation is critical for tau neurotoxicity in Drosophila. J. Neurosci. Res., 85, 1271-1278.
28. Khurana, V., Lu, Y., Steinhilb, M.L., Oldham, S., Shulman, J.M. and Feany, M.B. (2006) TOR-mediated cell-cycle activation causes neurodegeneration in a Drosophila tauopathy model. Curr. Biol. 16, 230-241.
29. Plattner, F., Angelo, M. and Giese, K.P. (2006) The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J. Biol. Chem., 281, 25457-25465.
30. Maccioni, R.B., Otth, C., Concha, I.I. and Munoz, J.P. (2001) The protein kinase Cdk5. Structural aspects, roles in neurogenesis and involvement in Alzheimer's pathology. Eur. J. Biochem., 268, 1518-1527.
31. Smith, D.S., Greer, P.L. and Tsai, L.H. (2001) Cdk5 on the brain. Cell Growth Differ., 12, 277-283.
32. Tsai, L.H., Delalle, I., Caviness, V.S. Jr, Chae, T. and Harlow, E. (1994) p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature, 371, 419-423.
33. Dias-Santagata, D., Fulga, T.A., Duttaroy, A. and Feany, M.B. (2007) Oxidative stress mediates tau-induced neurodegeneration in Drosophila. J. Clin. Invest., 117, 236-245.
34. Li, B., Chohan, M.O., Grundke-Iqbal, I. and Iqbal, K. (2007) Disruption of microtubule network by Alzheimer abnormally hyperphosphorylated tau. Acta Neuropathol., 113, 501-511.
35. Paudel, H.K., Lew, J., Ali, Z. and Wang, J.H. (1993) Brain proline-directed protein kinase phosphorylates tau on sites that are abnormally phosphorylated in tau associated with Alzheimer's paired helical filaments. J. Biol. Chem., 268, 23512-23518.
36. Chee, F.C., Mudher, A., Cuttle, M.F., Newman, T.A., MacKay, D., Lovestone, S. and Shepherd, D. (2005) Over-expression of tau results in defective synaptic transmission in Drosophila neuromuscular junctions. Neurobiol. Dis., 20, 918-928.
37. Mudher, A., Shepherd, D., Newman, T.A., Mildren, P., Jukes, J.P., Squire, A., Mears, A., Drummond, J.A., Berg, S., MacKay, D. et al. (2004) GSK-3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol. Psychiatry, 9, 522-530.
38. Yuan, A., Kumar, A., Peterhoff, C., Duff, K. and Nixon, R.A. (2008) Axonal transport rates in vivo are unaffected by tau deletion or overexpression in mice. J. Neurosci., 28, 1682-1687.
39. Karsten, S.L., Sang, T.K., Gehman, L.T., Chatterjee, S., Liu, J., Lawless, G.M., Sengupta, S., Berry, R.W., Pomakian, J., Oh, H.S. et al. (2006) A genomic screen for modifiers of tauopathy identifies puromycin-sensitive aminopeptidase as an inhibitor of tau-induced neurodegeneration. Neuron, 51, 549-560.
40. Shulman, J.M. and Feany, M.B. (2003) Genetic modifiers of tauopathy in Drosophila. Genetics, 165, 1233-1242.
41. Ghosh, S. and Feany, M.B. (2004) Comparison of pathways controlling toxicity in the eye and brain in Drosophila models of human neurodegenerative diseases. Hum. Mol. Genet., 13, 2011-2018.
42. Fulga, T.A., Elson-Schwab, I., Khurana, V., Steinhilb, M.L., Spires, T.L., Hyman, B.T. and Feany, M.B. (2007) Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo. Nat. Cell Biol., 9, 139-148.
43. Dermaut, B., Norga, K.K., Kania, A., Verstreken, P., Pan, H., Zhou, Y., Callaerts, P. and Bellen, H.J. (2005) Aberrant lysosomal carbohydrate storage accompanies endocytic defects and neurodegeneration in Drosophila benchwarmer. J. Cell Biol., 170, 127-139.
44. Chen, X., Li, Y., Huang, J., Cao, D., Yang, G., Liu, W., Lu, H. and Guo, A. (2007) Study of tauopathies by comparing Drosophila and human tau in Drosophila. Cell Tissue Res., 329, 169-178.
45. Blard, O., Feuillette, S., Bou, J., Chaumette, B., Frebourg, T., Campion, D. and Lecourtois, M. (2007) Cytoskeleton proteins are modulators of mutant tau-induced neurodegeneration in Drosophila. Hum. Mol. Genet., 16, 555-566.
46. Chau, K.W., Chan, W.Y., Shaw, P.C. and Chan, H.Y. (2006) Biochemical investigation of Tau protein phosphorylation status and its solubility properties in Drosophila. Biochem. Biophys. Res. Commun., 346 150-159.
47. Jackson, G.R., Salecker, I., Dong, X., Yao, X., Arnheim, N., Faber, P.W., MacDonald, M.E. and Zipursky, S.L. (1998) Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron, 21, 633-642.
48. Sang, T.K., Li, C., Liu, W., Rodriguez, A., Abrams, J.M., Zipursky, S.L. and Jackson, G.R. (2005) Inactivation of Drosophila Apaf-1 related killer suppresses formation of polyglutamine aggregates and blocks polyglutamine pathogenesis. Hum. Mol. Genet., 14, 357-372.
49. Steffan, J.S., Bodai, L., Pallos, J., Poelman, M., McCampbell, A., Apostol, B.L., Kazantsev, A., Schmidt, E., Zhu, Y.Z., Greenwald, M. et al. (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature, 413, 739-743.
50. Romero, E., Cha, G.H., Verstreken, P., Ly, C.V., Hughes, R.E., Bellen, H.J. and Botas, J. (2008) Suppression of neurodegeneration and increased neurotransmission caused by expanded full-length huntingtin accumulating in the cytoplasm. Neuron, 57, 27-40.
51. Branco, J., Al-Ramahi, I., Ukani, L., Perez, A.M., Fernandez-Funez, P., Rincon-Limas, D. and Botas, J. (2008) Comparative analysis of genetic modifiers in Drosophila points to common and distinct mechanisms of pathogenesis among polyglutamine diseases. Hum. Mol. Genet., 17, 376-390.
52. Baki, L., Shioi, J., Wen, P., Shao, Z., Schwarzman, A., Gama-Sosa, M., Neve, R. and Robakis, N.K. (2004) PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: Effects of FAD mutations. EMBO J., 23, 2586-2596.
53. Greenberg, S.G. and Davies, P. (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc. Natl Acad. Sci. USA, 87, 5827-5831.
54. Oddo, S., Caccamo, A., Cheng, D., Jouleh, B., Torp, R. and LaFerla, F.M. (2007) Genetically augmenting tau levels does not modulate the onset or progression of Abeta pathology in transgenic mice. J. Neurochem., 102, 1053-1063.
55. Harada, A., Oguchi, K., Okabe, S., Kuno, J., Terada, S., Ohshima, T., Sato-Yoshitake, R., Takei, Y., Noda, T. and Hirokawa, N. (1994) Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature, 369, 488-491.
56. Gotz, J., Chen, F., Barmettler, R. and Nitsch, R.M. (2001) Tau filament formation in transgenic mice expressing P301L tau. J. Biol. Chem., 276, 529-534.
57. Ishihara, T., Zhang, B., Higuchi, M., Yoshiyama, Y., Trojanowski, J.Q. and Lee, V.M. (2001) Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mice. Am. J. Pathol. 158, 555-562.
58. Spittaels, K., Van den Haute, C., Van Dorpe, J., Geerts, H., Mercken, M., Bruynseels, K., Lasrado, R., Vandezande, K., Laenen, I., Boon, T. et al. (2000) Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J. Biol. Chem., 275, 41340-41349.
59. Gamblin, T.C., Berry, R.W. and Binder, L.I. (2003) Tau polymerization: role of the amino terminus. Biochemistry, 42, 2252-2257.
60. Morfini, G., Pigino, G., Mizuno, N., Kikkawa, M. and Brady, S.T. (2007) Tau binding to microtubules does not directly affect microtubule-based vesicle motility. J. Neurosci. Res., 85, 2620-2630.
61. Ollmann, M., Young, L.M., Di Como, C.J., Karim, F., Belvin, M., Robertson, S., Whittaker, K., Demsky, M., Fisher, W.W., Buchman, A. et al. (2000) Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell, 101, 91-101.
62. Brand, A.H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401-415.
63. Steitz, M.C., Wickenheisser, J.K. and Siegfried, E. (1998) Overexpression of zeste white 3 blocks wingless signaling in the Drosophila embryonic midgut. Dev. Biol., 197, 218-233.
64. Connell-Crowley, L., Le Gall, M., Vo, D.J. and Giniger, E. (2000) The cyclin-dependent kinase Cdk5 controls multiple aspects of axon patterning in vivo. Curr. Biol., 10, 599-602.
65. Hay, B.A., Wassarman, D.A. and Rubin, G.M. (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell, 83, 1253-1262.
66. Yamaguchi, M., Hirose, F., Inoue, Y.H., Shiraki, M., Hayashi, Y., Nishi, Y. and Matsukage, A. (1999) Ectopic expression of human p53 inhibits entry into S phase and induces apoptosis in the Drosophila eye imaginal disc. Oncogene, 18, 6767-6775.
67. Lantz, V.A. and Miller, K.G. (1998) A class VI unconventional myosin is associated with a homologue of a microtubule-binding protein, cytoplasmic linker protein-170, in neurons and at the posterior pole of Drosophila embryos. J. Cell Biol., 140, 897-910.
68. Sun, T.Q., Lu, B., Feng, J.J., Reinhard, C., Jan, Y.N., Fantl, W.J. and Williams, L.T. (2001) PAR-1 is a dishevelled-associated kinase and a positive regulator of Wnt signalling. Nat. Cell Biol., 3, 628-636.