An isoform-specific role of FynT tyrosine kinase in Alzheimer's disease

Journal of Neurochemistry

Volumn 136, Issue 3, 2016, Pages 637-650

  Lee, Chingli ^a,b   Low, Clara Y B ^b   Francis, Paul T ^c   Attems, Johannes ^d   Wong, Peter T H ^a   Lai, Mitchell K P ^a,c   Tan, Michelle G K ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b SINGAPORE GENERAL HOSPITAL   (Singapore)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Alzheimer's disease; dementia; Fyn tyrosine kinase; neurofibrillary tangle; reactive astrogliosis

Indexed keywords

FYNB TYROSINE KINASE; FYNT TYROSINE KINASE; PROTEIN KINASE FYN; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (25-35); ISOPROTEIN; NERVE PROTEIN; PEPTIDE FRAGMENT; PROTEIN TYROSINE KINASE;

ALTERNATIVE RNA SPLICING; ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN CELL CULTURE; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; HUMAN; HUMAN TISSUE; MALE; NEOCORTEX; NEUROFIBRILLARY TANGLE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; UPREGULATION; ANIMAL; CELL CULTURE; COCULTURE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; GLIA; METABOLISM; MOLECULAR GENETICS; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELLS, CULTURED; COCULTURE TECHNIQUES; FEMALE; HUMANS; MALE; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; PEPTIDE FRAGMENTS; PREFRONTAL CORTEX; PROTEIN ISOFORMS; PROTEIN-TYROSINE KINASES; RATS; UP-REGULATION;

EID: 84955345215     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13429     Document Type: Article

References (51)

1. Aschner M., (1998) Astrocytes as mediators of immune and inflammatory responses in the CNS. Neurotoxicology 19, 269-281.
2. Bhaskar K., Yen S. H., and, Lee G., (2005) Disease-related modifications in tau affect the interaction between Fyn and Tau. J. Biol. Chem. 280, 35119-35125.
3. Braak H., and, Braak E., (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82, 239-259.
4. Brignatz C., Paronetto M. P., Opi S., et al,. (2009) Alternative splicing modulates autoinhibition and SH3 accessibility in the Src kinase Fyn. Mol. Cell. Biol. 29, 6438-6448.
5. Chaimowitz N. S., Falanga Y. T., Ryan J. J., and, Conrad D. H., (2013) Fyn kinase is required for optimal humoral responses. PLoS ONE 8, e60640.
6. Chin J., Palop J. J., Yu G. Q., Kojima N., Masliah E., and, Mucke L., (2004) Fyn kinase modulates synaptotoxicity, but not aberrant sprouting, in human amyloid precursor protein transgenic mice. J. Neurosci. 24, 4692-4697.
7. Chin J., Palop J. J., Puolivali J., Massaro C., Bien-Ly N., Gerstein H., Scearce-Levie K., Masliah E., and, Mucke L., (2005) Fyn kinase induces synaptic and cognitive impairments in a transgenic mouse model of Alzheimer's disease. J. Neurosci. 25, 9694-9703.
8. Cooke M. P., and, Perlmutter R. M., (1989) Expression of a novel form of the fyn proto-oncogene in hematopoietic cells. New Biol. 1, 66-74.
9. fyn). Cell 65, 281-291.
10. Davidson D., Chow L. M., Fournel M., and, Veillette A., (1992) Differential regulation of T cell antigen responsiveness by isoforms of the src-related tyrosine protein kinase p59fyn. J. Exp. Med. 175, 1483-1492.
11. Davidson D., Viallet J., and, Veillette A., (1994) Unique catalytic properties dictate the enhanced function of p59fynT, the hemopoietic cell-specific isoform of the Fyn tyrosine protein kinase, in T cells. Mol. Cell. Biol. 14, 4554-4564.
12. Davidson D., Shi X., Zhang S., Wang H., Nemer M., Ono N., Ohno S., Yanagi Y., and, Veillette A., (2004) Genetic evidence linking SAP, the X-linked lymphoproliferative gene product, to Src-related kinase FynT in TH2 cytokine regulation. Immunity 21, 707-717.
13. Farina C., Aloisi F., and, Meinl E., (2007) Astrocytes are active players in cerebral innate immunity. Trends Immunol. 28, 138-145.
14. Folstein M. F., Folstein S. E., and, McHugh P. R., (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12, 189-198.
15. Fuller S., Münch G., and, Steele M., (2009) Activated astrocytes: a therapeutic target in Alzheimer's disease? Expert Rev. Neurother. 9, 1585-1594.
16. Glatz D. C., Rujescu D., Tang Y., et al,. (2006) The alternative splicing of tau exon 10 and its regulatory proteins CLK2 and TRA2-BETA1 changes in sporadic Alzheimer's disease. J. Neurochem. 96, 635-644.
17. Haass C., and, Mandelkow E., (2010) Fyn-tau-amyloid: a toxic triad. Cell 142, 356-358.
18. Ho G. J., Hashimoto M., Adame A., Izu M., Alford M. F., Thal L. J., Hansen L. A., and, Masliah E., (2005) Altered p59Fyn kinase expression accompanies disease progression in Alzheimer's disease: implications for its functional role. Neurobiol. Aging 26, 625-635.
19. Huang D. W., Sherman B. T., and, Lempicki R. A., (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13.
20. Huang D. W., Sherman B. T., and, Lempicki R. A., (2009b) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
21. Ittner L. M., Ke Y. D., Delerue F., et al,. (2010) Dendritic function of tau mediates amyloid-b toxicity in Alzheimer's disease mouse models. Cell 142, 387-397.
22. 25-35. Exp. Neurol. 221, 26-37.
23. Kosik K. S., and, Finch E. A., (1987) MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: an immunocytochemical study of cultured rat cerebrum. J. Neurosci. 7, 3142-3153.
24. Lai M. K., Lai O. F., Keene J., Esiri M. M., Francis P. T., Hope T., and, Chen C. P., (2001) Psychosis of Alzheimer's disease is associated with elevated muscarinic M2 binding in the cortex. Neurology 57, 805-811.
25. Lai M. K., Esiri M. M., and, Tan M. G., (2014) Genome-wide profiling of alternative splicing in Alzheimer's disease. Genomics Data, 2, 290-292.
26. Lambert M. P., Barlow A. K., Chromy B. A., et al,. (1998) Diffusible, nonfibrillar ligands derived from Aß1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95, 6448-6453.
27. c-Fyn couples human oligomeric Ab with pathological tau changes in Alzheimer's disease. J. Neurosci. 32, 16857-16871.
28. Lee G., Thangavel R., Sharma V. M., et al,. (2004) Phosphorylation of tau by fyn: implications for Alzheimer's disease. J. Neurosci. 24, 2304-2312.
29. Medeiros R., and, LaFerla F. M., (2013) Astrocytes: conductors of the Alzheimer disease neuroinflammatory symphony. Exp. Neurol. 239, 133-138.
30. Mirra S. S., Heyman A., McKeel D., et al,. (1991) The consortium to establish a registry for Alzheimer's disease (CERAD). Part II. standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41, 479-486.
31. Perrin R. J., Fagan A. M., and, Holtzman D. M., (2009) Multimodal techniques for diagnosis and prognosis of Alzheimer's disease. Nature 461, 916-922.
32. Pike C. J., Cummings B. J., and, Cotman C. W., (1992) b-Amyloid induces neuritic dystrophy in vitro: similarities with Alzheimer pathology. NeuroReport 3, 769-772.
33. Pike C. J., Cummings B. J., Monzavi R., and, Cotman C. W., (1994) b-amyloid-induced changes in cultured astrocytes parallel reactive astrocytosis associated with senile plaques in Alzheimer's disease. Neuroscience 63, 517-531.
34. Pike C. J., Vaughan P. J., Cunningham D. D., and, Cotman C. W., (1996) Thrombin attenuates neuronal cell death and modulates astrocyte reactivity induced by beta-amyloid in vitro. J. Neurochem. 66, 1374-1382.
35. Pooler A. M., Usardi A., Evans C. J., Philpott K. L., Noble W., and, Hanger D. P., (2012) Dynamic association of tau with neuronal membranes is regulated by phosphorylation. Neurobiol. Aging 33, 431, e427-e438.
36. Reitz C., (2012) Alzheimer's disease and the amyloid cascade hypothesis: a critical review. Int. J. Alzheimers Dis. 2012, 369808.
37. Resh M. D., (1998) Fyn, a Src family tyrosine kinase. Int. J. Biochem. Cell Biol. 30, 1159-1162.
38. Roberson E. D., Halabisky B., Yoo J. W., et al,. (2011) Amyloid-b/Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease. J. Neurosci. 31, 700-711.
39. Selkoe D. J., (2002) Alzheimer's disease is a synaptic failure. Science 298, 789-791.
40. Shirazi S. K., and, Wood J. G., (1993) The protein tyrosine kinase, fyn, in Alzheimer's disease pathology. NeuroReport 4, 435-437.
41. Steele M. L., and, Robinson S. R., (2012) Reactive astrocytes give neurons less support: implications for Alzheimer's disease. Neurobiol. Aging 33, 423, e421-e413.
42. Supek F., Bošnjak M., Škunca N., and, Šmuc T., (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6, e21800.
43. Tan M. G., Chua W. T., Esiri M. M., Smith A. D., Vinters H. V., and, Lai M. K., (2010) Genome wide profiling of altered gene expression in the neocortex of Alzheimer's disease. J. Neurosci. Res. 88, 1157-1169.
44. Tollervey J. R., Wang Z., Hortobagyi T., et al,. (2011) Analysis of alternative splicing associated with aging and neurodegeneration in the human brain. Genome Res. 21, 1572-1582.
45. Um J. W., Nygaard H. B., Heiss J. K., Kostylev M. A., Stagi M., Vortmeyer A., Wisniewski T., Gunther E. C., and, Strittmatter S. M., (2012) Alzheimer amyloid-b oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat. Neurosci. 15, 1227-1235.
46. Usardi A., Pooler A. M., Seereeram A., Reynolds C. H., Derkinderen P., Anderton B., Hanger D. P., Noble W., and, Williamson R., (2011) Tyrosine phosphorylation of tau regulates its interactions with Fyn SH2 domains, but not SH3 domains, altering the cellular localization of tau. FEBS J. 278, 2927-2937.
47. Wang H., Ren C. H., Gunawardana C. G., and, Schmitt-Ulms G., (2013) Overcoming barriers and thresholds-signaling of oligomeric Ab through the prion protein to Fyn. Mol. Neurodegener. 8, 24.
48. Whitehouse P. J., Price D. L., Struble R. G., Clark A. W., Coyle J. T., and, Delon M. R., (1982) Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215, 1237-1239.
49. Xia D., and, Götz J., (2014) Premature lethality, hyperactivity, and aberrant phosphorylation in transgenic mice expressing a constitutively active form of Fyn. Front. Mol. Neurosci. 7, 40.
50. Yang K., Belrose J., Trepanier C. H., Lei G., Jackson M. F., and, MacDonald J. F., (2011) Fyn, a potential target for Alzheimer's disease. J. Alzheimers Dis. 27, 243-252.
51. Zamanian J. L., Xu L., Foo L. C., Nouri N., Zhou L., Giffard R. G., and, Barres B. A., (2012) Genomic analysis of reactive astrogliosis. J. Neurosci. 32, 6391-6410.