Tyrosine 394 is phosphorylated in Alzheimer's paired helical filament tau and in fetal tau with c-Abl as the candidate tyrosine kinase

Journal of Neuroscience

Volumn 25, Issue 28, 2005, Pages 6584-6593

  Derkinderen, Pascal ^a,g   Scales, Timothy M E ^a   Hanger, Diane P ^a   Leung, Kit Yi ^a   Byers, Helen L ^a   Ward, Malcolm A ^a   Lenz, Christof ^b   Price, Caroline ^c,h   Bird, Ian N ^c,i   Perera, Timothy ^c,j   Kellie, Stuart ^c,d   Williamson, Ritchie ^a   Noble, Wendy ^a   Van Etten, Richard A ^e   Leroy, Karelle ^f   Brion, Jean Pierre ^f   Reynolds, C Hugh ^a   Anderton, Brian H ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Applied Biosystems   (Germany)

^c Yamanouchi Research Institute   (United Kingdom)

^d UNIVERSITY OF QUEENSLAND   (Australia)

^e TUFTS MEDICAL CENTER   (United States)

^f UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^g NANTES UNIVERSITY HOSPITAL   (France)

^h Current Medicine Group   (United Kingdom)

ⁱ UCB PHARMA   (Belgium)

^j JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

more..

Author keywords

Abl; Alzheimer's disease; Mass spectrometry; Paired helical filaments; Tau; Tyrosine phosphorylation

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ABELSON KINASE; PERVANADATE; PROTEIN TYROSINE KINASE; TAU PROTEIN; TYROSINE;

ALZHEIMER DISEASE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING KINETICS; CONTROLLED STUDY; ENZYME INHIBITION; FETUS; FIBROBLAST; GENETIC TRANSFECTION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; INHIBITION KINETICS; MASS SPECTROMETRY; NEUROBLASTOMA CELL; NEUROFIBRILLARY TANGLE; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

AGED, 80 AND OVER; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BRAIN; BRAIN CHEMISTRY; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; CHO CELLS; COS CELLS; CRICETINAE; CRICETULUS; FEMALE; FETAL PROTEINS; HUMANS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; NEUROBLASTOMA; NEUROFIBRILLARY TANGLES; NEURONS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-ABL; PROTO-ONCOGENE PROTEINS C-FYN; SRC-FAMILY KINASES; TAU PROTEINS; TRANSFECTION; VANADATES;

EID: 22244475384     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1487-05.2005     Document Type: Article

References (67)

1. Alvarez AR, Sandoval PC, Leal NR, Castro PU, Kosik KS (2004) Activation of the neuronal c-Abl tyrosine kinase by amyloid-beta-peptide and reactive oxygen species. Neurobiol Dis 17:326-336.
2. Anderton BH, Betts J, Blackstock WP, Brion JP, Chapman S, Connell J, Dayanandan R, Gallo JM, Gibb G, Hanger DP, Hutton M, Kardalinou E, Leroy K, Lovestone S, Mack T, Reynolds CH, Van Slegtenhorst M (2001) Sites of phosphorylation in tau and factors affecting their regulation. Biochem Soc Symp 67:73-80.
3. Betts JC, Blackstock WP, Ward MA, Anderton BH (1997) Identification of phosphorylation sites on neurofilament proteins by nanoelectrospray mass spectrometry. J Biol Chem 272:12922-12927.
4. 262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding. Neuron 11:153-163.
5. Brandt R, Léger J, Lee G (1995) Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J Cell Biol 131:1327-1340.
6. Brion J-P, Couck A-M, Robertson J, Loviny TLF, Anderton BH (1993) Neurofilament monoclonal antibodies RT97 and 8D8 recognize different modified epitopes in paired helical filament-τ in Alzheimer's disease. J Neurochem 60:1372-1382.
7. Buée L, Bussière T, Buée-Scherrer V, Delacourte A, Hof PR (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Rev 33:95-130.
8. Daley GQ, Van Etten RA, Jackson PK, Bernards A, Baltimore D (1992) Non-myristoylated Abl proteins transform a factor-dependent hematopoietic cell line. Mol Cell Biol 12:1864-1871.
9. Delacourte A, Buée L (2000) Tau pathology: a marker of neurodegenerative disorders. Curr Opin Neurol 371-376.
10. Dente L, Vetriani C, Zucconi A, Pelicci G, Lanfrancone L, Pelicci PG, Cesareni G (1997) Modified phage peptide libraries as a tool to study specificity of phosphorylation and recognition of tyrosine containing peptides. J Mol Biol 269:694-703.
11. Derkinderen P, Girault JA (1997) Protein tyrosine phosphorylation. In: Post translational modifications: techniques and methods. (Boulton AA, Baker GB, Hemmings HC, eds), pp 251-274. Totowa, NJ: Humana.
12. Eidenmuller J, Fath T, Maas T, Pool M, Sontag E, Brandt R (2001) Phosphorylation-mimicking glutamate clusters in the proline-rich region are sufficient to simulate the functional deficiencies of hyperphosphorylated tau protein. Biochem J 357:759-767.
13. Girault J-A (1993) Protein phosphorylation and dephosphorylation in mammalian central nervous system. Neurochem Int 23:1-25.
14. Goedert M, Hasegawa M, Jakes R, Lawler S, Cuenda A, Cohen P (1997) Phosphorylation of microtubule-associated protein tau by stress- activated protein kinases. FEBS Lett 409:57-62.
15. Gordon JA (1991) Use of vanadate as protein-phosphotyrosine phosphatase inhibitor. Methods Enzymol 201:477-482.
16. Hanger DP, Betts JC, Loviny TLF, Blackstock WP, Anderton BH (1998) New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nanoelectrospray mass spectrometry. J Neurochem 71:2465-2476.
17. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok K, Connelly PA (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor-study of Lck- and FynT-dependent T cell activation. J Biol Chem 271:695-701.
18. Hantschel O, Superti-Furga G (2004) Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat Rev Mol Cell Biol 5:33-44.
19. Hunter T (1995) Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80:225-236.
20. Hutton M, Lendon CL, 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 RC, Stevens M, De Graaff E, Wauters E, Van Baren J, et al. (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393:702-705.
21. Huyer G, Liu S, Kelly J, Moffat J, Payette P, Kennedy B, Tsaprailis G, Gresser MJ, Ramachandran C (1997) Mechanism of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate. J Biol Chem 272:843-851.
22. Hwang SC, Jhon DY, Bae YS, Kim JH, Rhee SG (1996) Activation of phospholipase C-gamma by the concerted action of tau proteins and arachidonic acid. J Biol Chem 271:18342-18349.
23. Jackson P, Baltimore D (1989) N-terminal mutations activate the leukemogenic potential of the myristoylated form of c-abl. EMBO J 8:449-456.
24. Jenkins SM, Johnson GVW (1998) Tau complexes with phospholipase C-gamma in situ. NeuroReport 9:67-71.
25. Jones SB, Lu HY, Lu Q (2004) Abl tyrosine kinase promotes dendrogenesis by inducing actin cytoskeletal rearrangements in cooperation with p family small GTPases in hippocampal neurons. J Neurosci 24:8510-8521.
26. Klein C, Kramer EM, Cardine AM, Schraven B, Brandt R, Trotter J (2002) Process outgrowth of oligodendrocytes is promoted by interaction of fyn kinase with the cytoskeletal protein tau. J Neurosci 22:698-707.
27. Koleske AJ, Gifford AM, Scott ML, Nee M, Bronson RT, Miczek KA, Baltimore D (1998) Essential roles for the Abl and Arg tyrosine kinases in neurulation. Neuron 21:1259-1272.
28. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. Lee G, Newman ST, Gard DL, Band H, Panchamoorthy G (1998) Tau interacts with src-family non-receptor tyrosine kinases. J Cell Sci 111:3167-3177.
30. Lee G, Thangavel R, Sharma VM, Litersky JM, Bhaskar K, Fang SM, Do LH, Andreadis A, Van Hoesen G, Ksiezak-Reding H (2004) Phosphorylation of tau by fyn: implications for Alzheimer's disease. J Neurosci 24:2304-2312.
31. Leroy K, Boutajangout A, Authelet M, Woodgett JR, Anderton BH, Brion JP (2002) The active form of glycogen synthase kinase-3beta is associated with granulovacuolar degeneration in neurons in Alzheimer's disease. Acta Neuropathol (Berl) 103:91-99.
32. Liao H, Li YR, Brautigan DL, Gundersen GG (1998) Protein phosphatase 1 is targeted to microtubules by the microtubule-associated protein Tau. J Biol Chem 273:21901-21908.
33. Liu Y, Bishop A, Witucki L, Kraybill B, Shimizu E, Tsien J, Ubersax J, Blethrow J, Morgan DO, Shokat KM (1999) Structural basis for selective inhibition of Src family kinases by PP1. Chem Biol 6:671-678.
34. Lovestone S, Reynolds CH (1997) The phosphorylation of tau: a critical stage in neurodevelopment and neurodegenerative processes. Neuroscience 78:309-324.
35. Lucas JJ, Hernandez F, Gomez-Ramos P, Moran MA, Hen R, Avila J (2001) Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J 20:27-39.
36. Maas T, Eidenmüller J, Brandt R (2000) Interaction of tau with the neural membrane cortex is regulated by phosphorylation at sites that are modified in paired helical filaments. J Biol Chem 275:15733-15740.
37. Maccioni RB, Otth C, Concha II, Muñoz JP (2001) The protein kinase Cdk5-structural aspects, roles in neurogenesis and involvement in Alzheimer's pathology. Eur J Biochem 268:1518-1527.
38. Moresco EM, Koleske AJ (2003) Regulation of neuronal morphogenesis and synaptic function by Abl family kinases. Curr Opin Neurobiol 13:535-544.
39. Morishima-Kawashima M, Hasegawa M, Takio K, Suzuki M, Yoshida H, Titani K, Ihara Y (1995) Proline-directed and non-proline-directed phosphorylation of PHF-tau. J Biol Chem 270:823-829.
40. Mulot SFC, Hughes K, Woodgett JR, Anderton BH, Hanger DP (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-30. FEBS Lett 349:359-364.
41. Nelson PT, Stefansson K, Gulcher J, Saper CB (1996) Molecular evolution of τ protein: implications for Alzheimer's disease. J Neurochem 67:1622-1632.
42. Noble W, Olm V, Takata K, Casey E, Mary O, Meyerson J, Gaynor K, LaFrancois J, Wang L, Kondo T, Davies P, Burns M, Veeranna, Nixon R, Dickson D, Matsuoka Y, Ahlijanian M, Lau LF, Duff K (2003) Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38:555-565.
43. Obenauer JC, Cantley LC, Yaffe MB (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31:3635-3641.
44. Pendergast AM (2002) The Abl family kinases: mechanisms of regulation and signaling. Adv Cancer Res 85:51-100.
45. Plattner R, Kadlec L, DeMali KA, Kazlauskas A, Pendergast AM (1999) c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev 13:2400-2411.
46. Poorkaj P, Bird TD, Wijsman E, Nemens E, Garruto RM, Anderson L, Andreadis A, Wiederholt WC, Raskind M, Schellenberg GD (1998) Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 43:815-825.
47. Rapoport M, Dawson HN, Binder LI, Vitek MP, Ferreira A (2002) Tau is essential to beta-amyloid-induced neurotoxicity. Proc Natl Acad Sci USA 99:6364-6369.
48. Reynolds CH, Utton MA, Gibb GM, Yates A, Anderton BH (1997) Stress-activated protein kinase/c-Jun N-terminal kinase phosphorylates τ protein. J Neurochem 68:1736-1744.
49. Reynolds CH, Betts JC, Blackstock WP, Nebreda AR, Anderton BH (2000) Phosphorylation sites on tau identified by nanoelectrospray mass spectrometry: differences in vitro between the mitogen-activated protein kinases ERK2, c-Jun N-terminal kinase and P38, and glycogen synthase kinase-3β. J Neurochem 74:1587-1595.
50. Roepstorff P, Fohlman J (1984) Proposal for a common nomenclature for sequence ions in mass spectra of peptides. Biomed Mass Spectrom 11:601.
51. Shevchenko A, Chernushevic I, Shevchenko A, Wilm M, Mann M (2002) "De novo" sequencing of peptides recovered from in-gel digested proteins by nanoelectrospray tandem mass spectrometry. Mol Biotechnol 20:107-118.
52. Smith C, Anderton BH (1994) Dorothy Russell memorial lecture. The molecular pathology of Alzheimer's disease: are we any closer to understanding the neurodegenerative process? Neuropathol Appl Neurobiol 20:322-338.
53. Songyang Z, Cantley LC (1995) Recognition and specificity in protein tyrosine kinase-mediated signalling. Trends Biochem Sci 20:470-475.
54. Sontag E, Nunbhakdi-Craig V, Lee G, Brandt R, Kamibayashi C, Kuret J, White III CL, Mumby MC, Bloom GS (1999) Molecular interactions among protein phosphatase 2A, tau, and microtubules-implications for the regulation of tau phosphorylation and the development of tauopathies. J Biol Chem 274:25490-25498.
55. Spillantini MG, Goedert M (1998) Tau protein pathology in neurodegenerative diseases. Trends Neurosci 21:428-433.
56. 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, Van Leuven F (2000) Glycogen synthase kinase-3β 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.
57. Tatton L, Morley GM, Chopra R, Khwaja A (2003) The Src-selective kinase inhibitor PP1 also inhibits Kit and Bcr-Abl tyrosine kinases. J Biol Chem 278:4847-4853.
58. Traxler P, Bold G, Frei J, Lang M, Lydon N, Mett H, Buchdunger E, Meyer T, Mueller M, Furet P (1997) Use of a pharmacophore model for the design of EGF-R tyrosine kinase inhibitors: 4-(phenylamino)pyrazolo[3,4-d]pyrimidines. J Med Chem 40:3601-3616.
59. Van Etten RA (1992) Malignant transformation by abl and BCR/ABL. Cancer Treat Res 63:167-192.
60. Van Etten RA (1999) Cycling, stressed-out and nervous: cellular functions of c-Abl. Trends Cell Biol 9:179-186.
61. Van Etten RA (2004) Mechanisms of transformation by the BCR-ABL oncogene: new perspectives in the post-imatinib era. Leuk Res 28 [Suppl 1]:S21-S28.
62. Van Etten RA, Jackson PK, Baltimore D, Sanders MC, Matsudaira PT, Janmey PA (1994) The COOH terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains with bundling activity. J Cell Biol 124:325-340.
63. Warmuth M, Simon N, Mitina O, Mathes R, Fabbro D, Manley PW, Buchdunger E, Forster K, Moarefi I, Hallek M (2003) Dual-specific Src and Abl kinase inhibitors, PP1 and CGP76030, inhibit growth and survival of cells expressing imatinib mesylate-resistant Bcr-Abl kinases. Blood 101:664-672.
64. Williamson R, Scales T, Clark BR, Gibb G, Reynolds CH, Kellie S, Bird IN, Varndell IM, Sheppard PW, Everall I, Anderton BH (2002) Rapid tyrosine phosphorylation of neuronal proteins including tau and focal adhesion kinase in response to amyloid-β peptide exposure: involvement of Src family protein kinases. J Neurosci 22:10-20.
65. Woodring PJ, Litwack ED, O'Leary DD, Lucero GR, Wang JY, Hunter T (2002) Modulation of the F-actin cytoskeleton by c-Abl tyrosine kinase in cell spreading and neurite extension. J Cell Biol 156:879-892.
66. Wu JJ, Afar DE, Phan H, Witte ON, Lam KS (2002) Recognition of multiple substrate motifs by the c-ABL protein tyrosine kinase. Comb Chem High Throughput Screen 5:83-91.
67. Zukerberg LR, Patrick GN, Nikolic M, Humbert S, Wu CL, Lanier LM, Gertler FB, Vidal M, Van Etten RA, Tsai LH (2000) Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 26:633-646.