Biochemical investigation of Tau protein phosphorylation status and its solubility properties in Drosophila

Biochemical and Biophysical Research Communications

Volumn 346, Issue 1, 2006, Pages 150-159

  Chau, Katy Wing Kam ^a   Chan, Wood Yee ^a   Shaw, Pang Chui ^a   Chan, Ho Yin Edwin ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Alzheimer's disease; Cdk5; GSK3 ; PHF; Pre tangles

Indexed keywords

CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE; TAU PROTEIN;

AGING; ARTICLE; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; MEDICAL INFORMATICS; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; TRANSGENIC ANIMAL;

AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CYCLIN-DEPENDENT KINASE 5; DROSOPHILA; DROSOPHILA PROTEINS; EYE; GENE EXPRESSION PROFILING; GLYCOGEN SYNTHASE KINASE 3; HUMANS; LITHIUM CHLORIDE; PHOSPHORYLATION; SOLUBILITY; TAU PROTEINS; WING;

EID: 33744994326     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.05.112     Document Type: Article

References (46)

1. Drubin D.G., and Kirschner M.W. Tau protein function in living cells. J. Cell. Biol. 103 (1986) 2739-2746
2. Goedert M. Filamentous nerve cell inclusions in neurodegenerative diseases: tauopathies and alpha-synucleinopathies. Philos. Trans. R Soc. Lond. B Biol. Sci. 354 (1999) 1101-1118
3. Lee V.M., Kenyon T.K., and Trojanowski J.Q. Transgenic animal models of tauopathies. Biochim. Biophys. Acta 1739 (2005) 251-259
4. Gustke N., Steiner B., Mandelkow E.M., Biernat J., Meyer H.E., Goedert M., and Mandelkow E. The Alzheimer-like phosphorylation of tau protein reduces microtubule binding and involves Ser-Pro and Thr-Pro motifs. FEBS Lett. 307 (1992) 199-205
5. Lauckner J., Frey P., and Geula C. Comparative distribution of tau phosphorylated at Ser262 in pre-tangles and tangles. Neurobiol. Aging 24 (2003) 767-776
6. Hutton M., Lendon C.L., Rizzu P., Baker M., Froelich S., Houlden H., Pickering-Brown S., Chakraverty S., Isaacs A., Grover A., Hackett J., Adamson J., Lincoln S., Dickson D., Davies P., Petersen R.C., Stevens M., de Graaff E., Wauters E., van Baren J., Hillebrand M., Joosse M., Kwon J.M., Nowotny P., Che L.K., Norton J., Morris J.C., Reed L.A., Trojanowski J., Basun H., Lannfelt L., Neystat M., Fahn S., Dark F., Tannenberg T., Dodd P.R., Hayward N., Kwok J.B., Schofield P.R., Andreadis A., Snowden J., Craufurd D., Neary D., Owen F., Oostra B.A., Hardy J., Goate A., van Swieten J., Mann D., Lynch T., and Heutink P. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393 (1998) 702-705
7. Spillantini M.G., Murrell J.R., Goedert M., Farlow M.R., Klug A., and Ghetti B. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc. Natl. Acad. Sci. USA 95 (1998) 7737-7741
8. Lau L.F., Schachter J.B., Seymour P.A., and Sanner M.A. Tau protein phosphorylation as a therapeutic target in Alzheimer's disease. Curr. Top Med. Chem. 2 (2002) 395-415
9. Stoothoff W.H., and Johnson G.V. Tau phosphorylation: physiological and pathological consequences. Biochim. Biophys. Acta 1739 (2005) 280-297
10. Anderton B.H., Betts J., Blackstock W.P., Brion J.P., Chapman S., Connell J., Dayanandan R., Gallo J.M., Gibb G., Hanger D.P., Hutton M., Kardalinou E., Leroy K., Lovestone S., Mack T., Reynolds C.H., and Van Slegtenhorst M. Sites of phosphorylation in tau and factors affecting their regulation. Biochem. Soc. Symp. (2001) 73-80
11. Pei J.J., Braak E., Braak H., Grundke-Iqbal I., Iqbal K., Winblad B., and Cowburn R.F. Distribution of active glycogen synthase kinase 3beta (GSK-3beta) in brains staged for Alzheimer disease neurofibrillary changes. J. Neuropathol. Exp. Neurol. 58 (1999) 1010-1019
12. Yamaguchi H., Ishiguro K., Uchida T., Takashima A., Lemere C.A., and Imahori K. Preferential labeling of Alzheimer neurofibrillary tangles with antisera for tau protein kinase (TPK) I/glycogen synthase kinase-3 beta and cyclin-dependent kinase 5, a component of TPK II. Acta Neuropathol. (Berlin) 92 (1996) 232-241
13. Ferrer I., Pastor P., Rey M.J., Munoz E., Puig B., Pastor E., Oliva R., and Tolosa E. Tau phosphorylation and kinase activation in familial tauopathy linked to deln296 mutation. Neuropathol. Appl. Neurobiol. 29 (2003) 23-34
14. Ferrer I., Barrachina M., and Puig B. Glycogen synthase kinase-3 is associated with neuronal and glial hyperphosphorylated tau deposits in Alzheimer's disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Acta Neuropathol. (Berlin) 104 (2002) 583-591
15. Smith M.A., Siedlak S.L., Richey P.L., Nagaraj R.H., Elhammer A., and Perry G. Quantitative solubilization and analysis of insoluble paired helical filaments from Alzheimer disease. Brain Res. 717 (1996) 99-108
16. Schweers O., Mandelkow E.M., Biernat J., and Mandelkow E. Oxidation of cysteine-322 in the repeat domain of microtubule-associated protein tau controls the in vitro assembly of paired helical filaments. Proc. Natl. Acad. Sci. USA 92 (1995) 8463-8467
17. Mori H., Kondo J., and Ihara Y. Ubiquitin is a component of paired helical filaments in Alzheimer's disease. Science 235 (1987) 1641-1644
18. Hernandez F., Perez M., Lucas J.J., and Avila J. Sulfo-glycosaminoglycan content affects PHF-tau solubility and allows the identification of different types of PHFs. Brain Res. 935 (2002) 65-72
19. Kraemer B.C., Zhang B., Leverenz J.B., Thomas J.H., Trojanowski J.Q., and Schellenberg G.D. Neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proc. Natl. Acad. Sci. USA 100 (2003) 9980-9985
20. Zabrocki P., Pellens K., Vanhelmont T., Vandebroek T., Griffioen G., Wera S., Van Leuven F., and Winderickx J. Characterization of alpha-synuclein aggregation and synergistic toxicity with protein tau in yeast. FEBS J. 272 (2005) 1386-1400
21. Jackson G.R., Wiedau-Pazos M., Sang T.K., Wagle N., Brown C.A., Massachi S., and Geschwind D.H. Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 34 (2002) 509-519
22. Mudher A., Shepherd D., Newman T.A., Mildren P., Jukes J.P., Squire A., Mears A., Berg S., MacKay D., Asuni A.A., Bhat R., and Lovestone S. GSK-3beta inhibition reverses axonal transport defects and behavioural phenotypes in Drosophila. Mol. Psychiatry 9 (2004) 522-530
23. Nishimura I., Yang Y., and Lu B. PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila. Cell 116 (2004) 671-682
24. Shulman J.M., and Feany M.B. Genetic modifiers of tauopathy in Drosophila. Genetics 165 (2003) 1233-1242
25. Williams D.W., Tyrer M., and Shepherd D. Tau and tau reporters disrupt central projections of sensory neurons in Drosophila. J. Comp. Neurol. 428 (2000) 630-640
26. Wittmann C.W., Wszolek M.F., Shulman J.M., Salvaterra P.M., Lewis J., Hutton M., and Feany M.B. Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 293 (2001) 711-714
27. Mershin A., Pavlopoulos E., Fitch O., Braden B.C., Nanopoulos D.V., and Skoulakis E.M. Learning and memory deficits upon TAU accumulation in Drosophila mushroom body neurons. Learn Mem. 11 (2004) 277-287
28. Feuillette S., Blard O., Lecourtois M., Frebourg T., Campion D., and Dumanchin C. Tau is not normally degraded by the proteasome. J. Neurosci. Res. 80 (2005) 400-405
29. Wong S.L., Chen Y., Chan C.M., Chan C.S., Chan P.K., Chui Y.L., Fung K.P., Waye M.M., Tsui S.K., and Chan H.Y. In vivo functional characterization of the SARS-Coronavirus 3a protein in Drosophila. Biochem. Biophys. Res. Commun. 337 (2005) 720-729
30. Huen N.Y., and Chan H.Y. Dynamic regulation of molecular chaperone gene expression in polyglutamine disease. Biochem. Biophys. Res. Commun. 334 (2005) 1074-1084
31. Bourouis M. Targeted increase in shaggy activity levels blocks wingless signaling. Genesis 34 (2002) 99-102
32. Imahori K., and Uchida T. Physiology and pathology of tau protein kinases in relation to Alzheimer's disease. J. Biochem. (Tokyo) 121 (1997) 179-188
33. Morgan D.O. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13 (1997) 261-291
34. Ishihara T., Zhang B., Higuchi M., Yoshiyama Y., Trojanowski J.Q., and Lee V.M. Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mice. Am. J. Pathol. 158 (2001) 555-562
35. Zhang B., Higuchi M., Yoshiyama Y., Ishihara T., Forman M.S., Martinez D., Joyce S., Trojanowski J.Q., and Lee V.M. Retarded axonal transport of R406W mutant tau in transgenic mice with a neurodegenerative tauopathy. J. Neurosci. 24 (2004) 4657-4667
36. Zhukareva V., Shah K., Uryu K., Braak H., Del Tredici K., Sundarraj S., Clark C., Trojanowski J.Q., and Lee V.M.-Y. Biochemical analysis of {tau} proteins in argyrophilic grain disease, Alzheimer's disease, and Pick's disease: a comparative study. Am. J. Pathol. 161 (2002) 1135-1141
37. Lewis J., McGowan E., Rockwood J., Melrose H., Nacharaju P., Van Slegtenhorst M., Gwinn-Hardy K., Paul Murphy M., Baker M., Yu X., Duff K., Hardy J., Corral A., Lin W.L., Yen S.H., Dickson D.W., Davies P., and Hutton M. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat. Genet. 25 (2000) 402-405
38. Schneider A., Wright Araujo G., Trajkovic K., Herrmann M.M., Merkler D., Mandelkow E.-M., Weissert R., and Simons M. Hyperphosphorylation and aggregation of tau in experimental autoimmune encephalomyelitis. J. Biol. Chem. (2004) 55833-55839
39. Spittaels K., Van den Haute C., Van Dorpe J., Geerts H., Mercken M., Bruynseels K., Lasrado R., Vandezande K., Laenen I., Boon T., Van Lint J., Vandenheede J., Moechars D., Loos R., and Van Leuven F. 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 (2000) 41340-41349
40. Munoz-Montano J.R., Moreno F.J., Avila J., and Diaz-Nido J. Lithium inhibits Alzheimer's disease-like tau protein phosphorylation in neurons. FEBS Lett. 411 (1997) 183-188
41. 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., and Duff K. Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc. Natl. Acad. Sci. USA 102 (2005) 6990-6995
42. Perez M., Hernandez F., Lim F., Diaz-Nido J., and Avila J. Chronic lithium treatment decreases mutant tau protein aggregation in a transgenic mouse model. J. Alzheimers Dis. 5 (2003) 301-308
43. Trojanowski J.Q., and Lee V.M. Transgenic models of tauopathies and synucleinopathies. Brain Pathol. 9 (1999) 733-739
44. Goedert M., Jakes R., Crowther R.A., Cohen P., Vanmechelen E., Vandermeeren M., and Cras P. Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: identification of phosphorylation sites in tau protein. Biochem. J. 301 Pt 3 (1994) 871-877
45. Weaver C.L., Espinoza M., Kress Y., and Davies P. Conformational change as one of the earliest alterations of tau in Alzheimer's disease. Neurobiol. Aging 21 (2000) 719-727
46. Micchelli C.A., Esler W.P., Kimberly W.T., Jack C., Berezovska O., Kornilova A., Hyman B.T., Perrimon N., and Wolfe M.S. Gamma-secretase/presenilin inhibitors for Alzheimer's disease phenocopy Notch mutations in Drosophila. FASEB J. 17 (2003) 79-81