Phosphorylation in the amino terminus of tau prevents inhibition of anterograde axonal transport

Neurobiology of Aging

Volumn 33, Issue 4, 2012, Pages 826.e15-826.e30

  Kanaan, Nicholas M ^a,b   Morfini, Gerardo ^b,c   Pigino, Gustavo ^b,c   LaPointe, Nichole E ^d   Andreadis, Athena ^e   Song, Yuyu ^b,c   Leitman, Ellen ^b   Binder, Lester I ^f   Brady, Scott T ^b,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^f NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Axonal transport; Fyn kinase; Glycogen synthase kinase; Kinesin; Protein phosphatase; Tau filaments; Tauopathy; Tyrosine phosphorylation

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; MONOCLONAL ANTIBODY; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN KINASE FYN; TAU PROTEIN; TYROSINE;

AMINO TERMINAL SEQUENCE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; MOLECULAR EVOLUTION; NERVE FIBER TRANSPORT; NEUROFIBRILLARY TANGLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

EID: 84856954738     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.06.006     Document Type: Article

References (57)

1. Avila J., Hernández F. GSK-3 inhibitors for Alzheimer's disease. Expert Rev. Neurother 2007, 7:1527-1533.
2. Berry R.W., Sweet A.P., Clark F.A., Lagalwar S., Lapin B.R., Wang T., Topgi S., Guillozet-Bongaarts A.L., Cochran E.J., Bigio E.H., Binder L.I. Tau epitope display in progressive supranuclear palsy and corticobasal degeneration. J. Neurocytol 2004, 33:287-295.
3. Bhaskar K., Yen S.H., Lee G. Disease-related modifications in tau affect the interaction between Fyn and Tau. J. Biol. Chem 2005, 280:35119-35125.
4. Biernat J., Mandelkow E.M., Schröter C., Lichtenberg-Kraag B., Steiner B., Berling B., Meyer H., Mercken M., Vandermeeren A., Goedert M., et al. 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 1992, 11:1593-1597.
5. Bosco D.A., Morfini G., Karabacak N.M., Song Y., Gros-Louis F., Pasinelli P., Goolsby H., Fontaine B.A., Lemay N., McKenna-Yasek D., Frosch M.P., Agar J.N., Julien J.P., Brady S.T., Brown R.H. Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat. Neurosci 2010, 13:1396-1403.
6. Braak E., Braak H., Mandelkow E.M. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 1994, 87:554-567.
7. Brady S.T., Richards B.W., Leopold P.L. Assay of vesicle motility in squid axoplasm. Methods Cell Biol 1993, 39:191-202.
8. Carmel G., Mager E.M., Binder L.I., Kuret J. The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J. Biol. Chem 1996, 271:32789-32795.
9. Cohen P.T. Protein phosphatase 1-targeted in many directions. J. Cell Sci 2002, 115:241-256.
10. Dessi F., Colle M.A., Hauw J.J., Duyckaerts C. Accumulation of SNAP-25 immunoreactive material in axons of Alzheimer's disease. Neuroreport 1997, 8:3685-3689.
11. Ebneth A., Godemann R., Stamer K., Illenberger S., Trinczek B., Mandelkow E. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J. Cell Biol 1998, 143:777-794.
12. Gamblin T.C., King M.E., Dawson H., Vitek M.P., Kuret J., Berry R.W., Binder L.I. In vitro polymerization of tau protein monitored by laser light scattering: method and application to the study of FTDP-17 mutants. Biochemistry 2000, 39:6136-6144.
13. Giannakopoulos P., Herrmann F.R., Bussière T., Bouras C., Kövari E., Perl D.P., Morrison J.H., Gold G., Hof P.R. Tangle and neuron numbers, but not amyloid load, predict cognitive status in Alzheimer's disease. Neurology 2003, 60:1495-1500.
14. Goedert M., Jakes R. Mutations causing neurodegenerative tauopathies. Biochim. Biophys. Acta 2005, 1739:240-250.
15. Goedert M., Jakes R., Vanmechelen E. Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine. Neurosci. Lett 1995, 205:189. 167-169.
16. Hasegawa M., Morishima-Kawashima M., Takio K., Suzuki M., Titani K., Ihara Y. Protein sequence and mass spectrometric analyses of tau in the Alzheimer's disease brain. J. Biol. Chem 1992, 267:17047-17054.
17. Ho G.J., Hashimoto M., Adame A., Izu M., Alford M.F., Thal L.J., Hansen L.A., Masliah E. Altered p59Fyn kinase expression accompanies disease progression in Alzheimer's disease: implications for its functional role. Neurobiol. Aging 2005, 26:625-635.
18. Horowitz P.M., LaPointe N., Guillozet-Bongaarts A.L., Berry R.W., Binder L.I. N-terminal fragments of tau inhibit full-length tau polymerization in vitro. Biochemistry 2006, 45:12859-12866.
19. Horowitz P.M., Patterson K.R., Guillozet-Bongaarts A.L., Reynolds M.R., Carroll C.A., Weintraub S.T., Bennett D.A., Cryns V.L., Berry R.W., Binder L.I. Early N-terminal changes and caspase-6 cleavage of tau in Alzheimer's disease. J. Neurosci 2004, 24:7895-7902.
20. Iqbal K., Alonso A. Del C., Chen S., Chohan M.O., El-Akkad E., Gong C.X., Khatoon S., Li B., Liu F., Rahman A., Tanimukai H., Grundke-Iqbal I. Tau pathology in Alzheimer disease and other tauopathies. Biochim. Biophys. Acta 2005, 1739:198-210.
21. Ittner L.M., Ke Y.D., Delerue F., Bi M., Gladbach A., van Eersel J., Wölfing H., Chieng B.C., Christie M.J., Napier I.A., Eckert A., Staufenbiel M., Hardeman E., Götz J. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010, 142:387-397.
22. Jeganathan S., Hascher A., Chinnathambi S., Biernat J., Mandelkow E.M., Mandelkow E. Proline-directed pseudo-phosphorylation at AT8 and PHF1 epitopes induces a compaction of the paperclip folding of Tau and generates a pathological (MC-1) conformation. J. Biol. Chem 2008, 283:32066-32076.
23. Jeganathan S., von Bergen M., Brutlach H., Steinhoff H.J., Mandelkow E. Global hairpin folding of tau in solution. Biochemistry 2006, 45:2283-2293.
24. Kanaan N.M., Kordower J.H., Collier T.J. Age-related accumulation of Marinesco bodies and lipofuscin in rhesus monkey midbrain dopamine neurons: relevance to selective neuronal vulnerability. J. Comp. Neurol 2007, 502(5):683-700.
25. Kanaan N.M., Morfini G.A., Lapointe N.E., Pigino G.F., Patterson K.R., Song Y., Andreadis A., Fu Y., Brady S.T., Binder L.I. Pathogenic Forms of Tau Inhibit Kinesin-Dependent Axonal Transport through a Mechanism Involving Activation of Axonal Phosphotransferases. The Journal of neuroscience: the official journal of the Society for Neuroscience 2011, 31(27):9858-9868. 10.1523/JNEUROSCI.0560-11.2011.
26. King M.E., Ahuja V., Binder L.I., Kuret J. Ligand-dependent tau filament formation: implications for Alzheimer's disease progression. Biochemistry 1999, 38:14851-14859.
27. LaPointe N.E., Morfini G., Pigino G., Gaisina I.N., Kozikowski A.P., Binder L.I., Brady S.T. The amino terminus of tau inhibits kinesin-dependent axonal transport: implications for filament toxicity. J. Neurosci. Res 2009, 87:440-451.
28. Lebouvier T., Scales T.M., Williamson R., Noble W., Duyckaerts C., Hanger D.P., Reynolds C.H., Anderton B.H., Derkinderen P. The microtubule-associated protein tau is also phosphorylated on tyrosine. J. Alzheimers Dis 2009, 18:1-9.
29. Lee G. Tau and src family tyrosine kinases. Biochim. Biophys. Acta 2005, 1739:323-330.
30. Lee G., Newman S.T., Gard D.L., Band H., Panchamoorthy G. Tau interacts with src-family non-receptor tyrosine kinases. J. Cell Sci 1998, 111:3167-3177.
31. Lee G., Thangavel R., Sharma V.M., Litersky J.M., Bhaskar K., Fang S.M., Do L.H., Andreadis A., Van Hoesen G., Ksiezak-Reding H. Phosphorylation of tau by fyn: implications for Alzheimer's disease. J. Neurosci 2004, 24:2304-2312.
32. Luo M.H., Tse S.W., Memmott J., Andreadis A. Novel isoforms of tau that lack the microtubule-binding domain. J. Neurochem 2004, 90:340-351.
33. Mandelkow E.M., Stamer K., Vogel R., Thies E., Mandelkow E. Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses. Neurobiol. Aging 2003, 24:1079-1085.
34. Morfini G., Pigino G., Beffert U., Busciglio J., Brady S.T. Fast axonal transport misregulation and Alzheimer's disease. Neuromol. Med 2002, 2:89-99.
35. Morfini G., Pigino G., Mizuno N., Kikkawa M., Brady S.T. Tau binding to microtubules does not directly affect microtubule-based vesicle motility. J. Neurosci. Res 2007, 85:2620-2630.
36. Morfini G., Pigino G., Opalach K., Serulle Y., Moreira J.E., Sugimori M., Llinas R.R., Brady S.T. 1-Methyl-4-phenylpyridinium affects fast axonal transport by activation of caspase and protein kinase C. Proc. Natl. Acad. Sci. U. S. A 2007, 104:2442-2447.
37. Morfini G., Szebenyi G., Brown H., Pant H.C., Pigino G., DeBoer S., Beffert U., Brady S.T. A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. EMBO J 2004, 23:2235-2245.
38. Morfini G., Szebenyi G., Elluru R., Ratner N., Brady S.T. Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J 2002, 21:281-293.
39. Morfini G.A., Burns M., Binder L.I., Kanaan N.M., LaPointe N., Bosco D.A., Brown R.H., Brown H., Tiwari A., Hayward L., Edgar J., Nave K.A., Garberrn J., Atagi Y., Song Y., Pigino G., Brady S.T. Axonal transport defects in neurodegenerative diseases. J. Neurosci 2009, 29:12776-12786.
40. Morfini G.A., You Y.M., Pollema S.L., Kaminska A., Liu K., Yoshioka K., Bjorkblom B., Coffey E.T., Bagnato C., Han D., Huang C.F., Banker G., Pigino G., Brady S.T. Pathogenic huntingtin inhibits fast axonal transport by activating JNK3 and phosphorylating kinesin. Nat. Neurosci 2009, 12:864-871.
41. Morsch R., Simon W., Coleman P.D. Neurons may live for decades with neurofibrillary tangles. J. Neuropathol. Exp. Neurol 1999, 58:188-197.
42. Pigino G., Morfini G., Atagi Y., Deshpande A., Yu C., Jungbauer L., LaDu M., Busciglio J., Brady S. Disruption of fast axonal transport is a pathogenic mechanism for intraneuronal amyloid beta. Proc. Natl. Acad. Sci. U. S. A 2009, 106:5907-5912.
43. Pollock N.J., Mirra S.S., Binder L.I., Hansen L.A., Wood J.G. Filamentous aggregates in Pick's disease, progressive supranuclear palsy, and Alzheimer's disease share antigenic determinants with microtubule-associated protein, tau. Lancet 1986, 2:1211.
44. Praprotnik D., Smith M.A., Richey P.L., Vinters H.V., Perry G. Filament heterogeneity within the dystrophic neurites of senile plaques suggests blockage of fast axonal transport in Alzheimer's disease. Acta Neuropathol 1996, 91:226-235.
45. Price D.L., Wong P.C., Borchelt D.R., Pardo C.A., Thinakaran G., Doan A.P., Lee M.K., Martin L.J., Sisodia S.S. Amyotrophic lateral sclerosis and Alzheimer disease. Lessons from model systems. Rev. Neurol. (Paris) 1997, 153:484-495.
46. Reyes J.F., Reynolds M.R., Horowitz P.M., Fu Y., Guillozet-Bongaarts A.L., Berry R., Binder L.I. A possible link between astrocyte activation and tau nitration in Alzheimer's disease. Neurobiol. Dis 2008, 31:198-208.
47. Reynolds M.R., Berry R.W., Binder L.I. Site-specific nitration and oxidative dityrosine bridging of the tau protein by peroxynitrite: implications for Alzheimer's disease. Biochemistry 2005, 44:1690-1700.
48. Reynolds M.R., Reyes J.F., Fu Y., Bigio E.H., Guillozet-Bongaarts A.L., Berry R.W., Binder L.I. Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer's disease and other tauopathies. J. Neurosci 2006, 26:10636-10645.
49. Robinson D.R., Wu Y.M., Lin S.F. The protein tyrosine kinase family of the human genome. Oncogene 2000, 19:5548-5557.
50. Rovelet-Lecrux A., Lecourtois M., Thomas-Anterion C., Le Ber I., Brice A., Frebourg T., Hannequin D., Campion D. Partial deletion of the MAPT gene: a novel mechanism of FTDP-17. Hum. Mutat 2009, 30:E591-E602.
51. Roy S., Zhang B., Lee V.M., Trojanowski J.Q. Axonal transport defects: a common theme in neurodegenerative diseases. Acta Neuropathol 2005, 109:5-13.
52. Shirazi S.K., Wood J.G. The protein tyrosine kinase, fyn, in Alzheimer's disease pathology. Neuroreport 1993, 4:435-437.
53. Solowska J.M., Morfini G., Falnikar A., Himes B.T., Brady S.T., Huang D., Baas P.W. Quantitative and functional analyses of spastin in the nervous system: implications for hereditary spastic paraplegia. J. Neurosci 2008, 28:2147-2157.
54. Stokin G.B., Lillo C., Falzone T.L., Brusch R.G., Rockenstein E., Mount S.L., Raman R., Davies P., Masliah E., Williams D.S., Goldstein L.S. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 2005, 307:1282-1288.
55. Sun Q., Gamblin T.C. Pseudohyperphosphorylation causing AD-like changes in tau has significant effects on its polymerization. Biochemistry 2009, 48:6002-6011.
56. Suzuki K., Terry R.D. Fine structural localization of acid phosphatase in senile plaques in Alzheimer's presenile dementia. Acta Neuropathol 1967, 8:276-284.
57. Vershinin M., Carter B.C., Razafsky D.S., King S.J., Gross S.P. Multiple-motor based transport and its regulation by Tau. Proc. Natl. Acad. Sci. U. S. A 2007, 104:87-92.