Tau phosphorylated at tyrosine 394 is found in Alzheimer's disease tangles and can be a product of the abl-related kinase, Arg

Journal of Alzheimer's Disease

Volumn 19, Issue 2, 2010, Pages 721-733

  Tremblay, Matthew A ^a   Acker, Christopher M ^a   Davies, Peter ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Abl2; Alzheimer's disease; Arg; Phosphorylation; Tangle; Tau; Tyrosine

Indexed keywords

ABELSON KINASE; ARGININE; PROTEIN KINASE FYN; PROTEIN KINASE SYK; TAU PROTEIN; TYROSINE;

ALZHEIMER DISEASE; ARTICLE; GENETIC TRANSFECTION; HUMAN; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NEUROFIBRILLARY TANGLE; OXIDATIVE STRESS; PAIRED HELICAL FILAMENT; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; TAUOPATHY;

EID: 77049126656     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-1271     Document Type: Article

References (43)

1. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA (1989) Multiple isoforms of human microtubuleassociated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3, 519-526.
2. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83, 4913-4917.
3. Kosik KS, Joachim CL, Selkoe DJ (1986) Microtubuleassociated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc Natl Acad Sci USA 83, 4044-4048.
4. Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW (1975) A protein factor essential for microtubule assembly. Proc Natl Acad Sci USA 72, 1858-1862.
5. Biernat J, Gustke N, Drewes G, Mandelkow EM, Mandelkow E (1993) Phosphorylation of Ser262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding. Neuron 11, 153-163.
6. Johnson GV, Stoothoff WH (2004) Tau phosphorylation in neuronal cell function and dysfunction. J Cell Sci 117, 5721-5729.
7. Cripps D, Thomas SN, Jeng Y, Yang F, Davies P, Yang AJ (2006) Alzheimer disease-specific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation. J Biol Chem 281, 10825-10838.
8. Vega IE, Cui L, Propst JA, Hutton ML, Lee G, Yen SH (2005) Increase in tau tyrosine phosphorylation correlates with the formation of tau aggregates. Brain Res Mol Brain Res 138, 135-144.
9. Derkinderen P, Scales TM, Hanger DP, Leung KY, Byers HL, Ward MA, Lenz C, Price C, Bird IN, Perera T, Kellie S, Williamson R, Noble W, Van Etten RA, Leroy K, Brion JP, Reynolds CH, Anderton BH (2005) Tyrosine 394 is phosphorylated in Alzheimer's paired helical filament tau and in fetal tau with c-Abl as the candidate tyrosine kinase. J Neurosci 25, 6584-6593.
10. 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.
11. De Felice FG, Wu D, Lambert MP, Fernandez SJ, Velasco PT, Lacor PN, Bigio EH, Jerecic J, Acton PJ, Shughrue PJ, Chen-Dodson E, Kinney GG, Klein WL (2008) Alzheimer's disease-type neuronal tau hyperphosphorylation induced by Abeta oligomers. Neurobiol Aging 29, 1334-1347.
12. 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-beta peptide exposure: involvement of Src family protein kinases. J Neurosci 22, 10-20.
13. 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.
14. Lebouvier T, Scales TM, Hanger DP, Geahlen RL, Lardeux B, Reynolds CH, Anderton BH, Derkinderen P (2007) The microtubule-associated protein tau is phosphorylated by Syk. Biochim Biophys Acta. 1783, 188-192.
15. Kruh GD, Perego R, Miki T, Aaronson SA (1990) The complete coding sequence of arg defines the Abelson subfamily of cytoplasmic tyrosine kinases. Proc Natl Acad Sci USA 87, 5802-5806.
16. Perego R, Ron D, Kruh GD (1991) Arg encodes a widely expressed 145 kDa protein-tyrosine kinase. Oncogene 6, 1899-1902.
17. Koleske AJ, Gifford AM, Scott ML, Nee M, Bronson RT, Miczek KA, BaltimoreD(1998) Essential roles for the Abl and Arg tyrosine kinases in neurulation. Neuron 21, 1259-1272.
18. Moresco EM, Donaldson S,Williamson A, Koleske AJ (2005) Integrin-mediated dendrite branch maintenance requires Abelson (Abl) family kinases. J Neurosci 25, 6105-6118.
19. Moresco EM, Koleske AJ (2003) Regulation of neuronal morphogenesis and synaptic function by Abl family kinases. Curr Opin Neurobiol 13, 535-544.
20. Moresco EM, Scheetz AJ, Bornmann WG, Koleske AJ, Fitzsimonds RM (2003) Abl family nonreceptor tyrosine kinases modulate short-term synaptic plasticity. J Neurophysiol 89, 1678-1687.
21. Sfakianos MK, Eisman A, Gourley SL, Bradley WD, Scheetz AJ, Settleman J, Taylor JR, Greer CA,Williamson A, Koleske AJ (2007) Inhibition of Rho via Arg and p190RhoGAP in the postnatal mouse hippocampus regulates dendritic spine maturation, synapse and dendrite stability, and behavior. J Neurosci 27, 10982-10992.
22. Cao C, Leng Y, Huang W, Liu X, Kufe D (2003) Glutathione peroxidase 1 is regulated by the c-Abl and Arg tyrosine kinases. J Biol Chem 278, 39609-39614.
23. Cao C, Leng Y, Kufe D (2003) Catalase activity is regulated by c-Abl and Arg in the oxidative stress response. J Biol Chem 278, 29667-29675.
24. Cao C, Leng Y, Li C, Kufe D (2003) Functional interaction between the c-Abl and Arg protein-tyrosine kinases in the oxidative stress response. J Biol Chem 278, 12961-12967. (Pubitemid 36800062)
25. Cao C, Leng Y, Liu X, Yi Y, Li P, Kufe D (2003) Catalase is regulated by ubiquitination and proteosomal degradation. Role of the c-Abl and Arg tyrosine kinases. Biochemistry 42, 10348-10353.
26. Cao C, Li Y, Leng Y, Li P,Ma Q, Kufe D (2005) Ubiquitination and degradation of the Arg tyrosine kinase is regulated by oxidative stress. Oncogene 24, 2433-2440.
27. Cao C, Ren X, Kharbanda S, Koleske A, Prasad KV, Kufe D (2001) The ARG tyrosine kinase interacts with Siva-1 in the apoptotic response to oxidative stress. J Biol Chem 276, 11465-11468.
28. Davies P (1999) Characterization and use of monoclonal antibodies to tau and PHF-tau. Alzheimer's Disease: Methods and Protocols. Methods in Molecular Medicine, 361-374.
29. Otvos L, Jr., Feiner L, Lang E, Szendrei GI, Goedert M, Lee VM (1994) Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. J Neurosci Res 39, 669-673.
30. Khatoon S, Grundke-Iqbal I, Iqbal K (1992) Brain levels of microtubule-associated protein tau are elevated in Alzheimer's disease: a radioimmuno-slot-blot assay for nanograms of the protein. J Neurochem 59, 750-753.
31. Nishimura N, Furukawa Y, Sutheesophon K, Nakamura M, Kishi K, Okuda K, SatoY, KanoY(2003) Suppression ofARG kinase activity by STI571 induces cell cycle arrest through upregulation of CDK inhibitor p18/INK4c. Oncogene 22, 4074-4082.
32. Okuda K, Weisberg E, Gilliland DG, Griffin JD (2001) ARG tyrosine kinase activity is inhibited by STI571. Blood 97, 2440-2448.
33. Liu WH, Makrigiorgos GM (2003) Sensitive and quantitative detection of mutations associated with clinical resistance to STI-571. Leuk Res 27, 979-982.
34. Yamamoto M, Kurosu T, Kakihana K, Mizuchi D, Miura O (2004) The two major imatinib resistance mutations E255K and T315I enhance the activity of BCR/ABL fusion kinase. Biochem Biophys Res Commun 319, 1272-1275.
35. Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S, Zimmermann J, Lydon NB (1996) Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 2, 561-566.
36. Jing Z, Caltagarone J, Bowser R (2009) Altered Subcellular Distribution of c-Abl in Alzheimer's Disease. J Alzheimers Dis 17, 409-422.
37. Lin H, Lin TY, Juang JL (2007) Abl deregulates Cdk5 kinase activity and subcellular localization in Drosophila neurodegeneration. Cell Death Differ 14, 607-615.
38. Tanis KQ, Veach D, Duewel HS, Bornmann WG, Koleske AJ (2003) Two distinct phosphorylation pathways have additive effects on Abl family kinase activation. Mol Cell Biol 23, 3884-3896.
39. Perkinton MS, Standen CL, Lau KF, Kesavapany S, Byers HL, Ward M, McLoughlin DM, Miller CC (2004) The c-Abl tyrosine kinase phosphorylates the Fe65 adaptor protein to stimulate Fe65/amyloid precursor protein nuclear signaling. J Biol Chem 279, 22084-22091.
40. Zambrano N, Bruni P, Minopoli G, Mosca R, Molino D, Russo C, Schettini G, Sudol M, Russo T (2001) The beta-amyloid precursor protein APP is tyrosine-phosphorylated in cells expressing a constitutively active form of the Abl protoncogene. J Biol Chem 276, 19787-19792.
41. Netzer WJ, Dou F, Cai D, Veach D, Jean S, Li Y, Bornmann WG, Clarkson B, Xu H, Greengard P (2003) Gleevec inhibits beta-amyloid production but not Notch cleavage. Proc Natl Acad Sci USA 100, 12444-12449.
42. Markesbery WR (1997) Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med 23, 134-147.
43. Sun X, Majumder P, Shioya H,Wu F, Kumar S,Weichselbaum R, Kharbanda S, Kufe D (2000) Activation of the cytoplasmic c-Abl tyrosine kinase by reactive oxygen species. J Biol Chem 275, 17237-17240. (Pubitemid 30430754)