Serine-arginine protein kinases: New players in neurodegenerative diseases?

Reviews in the Neurosciences

Volumn 24, Issue 4, 2013, Pages 401-413

  Chan, Chi Bun ^a   Ye, Keqiang ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alternative splicing; Cell cycle; Neurodegenerative disease; Neuron; SRPK; Tauopathy

Indexed keywords

ARGININE KINASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CASEIN KINASE II; CASPASE 9; CELL CYCLE PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIN B1; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 5; FIBRONECTIN; GLUTAMATE RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN E2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN E3; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN G; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; N METHYL DEXTRO ASPARTIC ACID; PROTEIN 14 3 3; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN SERINE KINASE; S6 KINASE; SERINE ARGININE RICH PROTEIN; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; STRESS ACTIVATED PROTEIN KINASE; TAU PROTEIN; TAU TUBULIN KINASE 1; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BRAIN CELL CULTURE; CELL CYCLE CHECKPOINT; CELL CYCLE PROGRESSION; CELL STRESS; CELL SURVIVAL; DEGENERATIVE DISEASE; DENDRITIC SPINE; FRONTOTEMPORAL DEMENTIA; HIPPOCAMPUS; HUMAN; HUNTINGTON CHOREA; LONG TERM POTENTIATION; MEMORY; MICROTUBULE; MILD COGNITIVE IMPAIRMENT; NERVE CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PICK PRESENILE DEMENTIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; RNA PROCESSING; RNA SPLICING; SYNAPTIC TRANSMISSION; TAUOPATHY;

ALTERNATIVE SPLICING; ANIMALS; BRAIN; CELL CYCLE; HUMANS; MUTATION; NEURODEGENERATIVE DISEASES; NEURONS; PROTEIN-SERINE-THREONINE KINASES;

EID: 84888173055     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/revneuro-2013-0014     Document Type: Article

References (146)

1. Allen, J.W., Eldadah, B.A., Huang, X., Knoblach, S.M., and Faden, A.I. (2001). Multiple caspases are involved in beta-amyloidinduced neuronal apoptosis. J. Neurosci. Res. 65, 45-53.
2. Auffret, A., Gautheron, V., Mattson, M.P., Mariani, J., and Rovira, C. (2010). Progressive age-related impairment of the late long-term potentiation in Alzheimer's disease presenilin-1 mutant knock-in mice. J. Alzheimers Dis. 19, 1021-1033.
3. Baloyannis, S.J. (2009). Dendritic pathology in Alzheimer's disease. J. Neurol. Sci. 283, 153-157.
4. Baumann, K., Mandelkow, E.M., Biernat, J., Piwnica-Worms, H., and Mandelkow, E. (1993). Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett. 336, 417-424.
5. Behl, C., Davis, J.B., Lesley, R., and Schubert, D. (1994). Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 77, 817-827.
6. Bell, K.F., Bennett, D.A., and Cuello, A.C. (2007). Paradoxical upregulation of glutamatergic presynaptic boutons during mild cognitive impairment. J. Neurosci. 27, 10810-10817.
7. Bhaskar, K., Miller, M., Chludzinski, A., Herrup, K., Zagorski, M., and Lamb, B.T. (2009). The PI3K-Akt-mTOR pathway regulates Abeta oligomer induced neuronal cell cycle events. Mol. Neurodegener. 4, 14.
8. Black, M.M., Slaughter, T., Moshiach, S., Obrocka, M., and Fischer, I. (1996). Tau is enriched on dynamic microtubules in the distal region of growing axons. J. Neurosci. 16, 3601-3619.
9. Blaustein, M., Pelisch, F., Tanos, T., Munoz, M.J., Wengier, D., Quadrana, L., Sanford, J.R., Muschietti, J.P., Kornblihtt, A.R., Caceres, J.F., et al. (2005). Concerted regulation of nuclear and cytoplasmic activities of SR proteins by AKT. Nat. Struct. Mol. Biol. 12, 1037-1044.
10. Busser, J., Geldmacher, D.S., and Herrup, K. (1998). Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J. Neurosci. 18, 2801-2807.
11. Chun, J., Kwon, T., Lee, E.J., Kim, C.H., Han, Y.S., Hong, S.K., Hyun, S., and Kang, S.S. (2004). 14-3-3 Protein mediates phosphorylation of microtubule-associated protein tau by serum- and glucocorticoid-induced protein kinase 1. Mol. Cells 18, 360-368.
12. Correas, I., Diaz-Nido, J., and Avila, J. (1992). Microtubuleassociated protein tau is phosphorylated by protein kinase C on its tubulin binding domain. J. Biol. Chem. 267, 15721-15728.
13. Currais, A., Hortobagyi, T., and Soriano, S. (2009). The neuronal cell cycle as a mechanism of pathogenesis in Alzheimer's disease. Aging (Albany NY) 1, 363-371.
14. D'Souza, I. and Schellenberg, G.D. (2006). Arginine/serine-rich protein interaction domain-dependent modulation of a tau exon 10 splicing enhancer: altered interactions and mechanisms for functionally antagonistic FTDP-17 mutations Delta280K AND N279K. J. Biol. Chem. 281, 2460-2469.
15. Daniilidou, M., Tsolaki, M., Giannakouros, T., and Nikolakaki, E. (2011). Detection of elevated antibodies against SR protein kinase 1 in the serum of Alzheimer's disease patients. J. Neuroimmunol. 238, 67-72.
16. de Silva, R., Lashley, T., Gibb, G., Hanger, D., Hope, A., Reid, A., Bandopadhyay, R., Utton, M., Strand, C., Jowett, T., et al. (2003). Pathological inclusion bodies in tauopathies contain distinct complements of tau with three or four microtubulebinding repeat domains as demonstrated by new specific monoclonal antibodies. Neuropathol. Appl. Neurobiol. 29, 288-302.
17. Del Bo, R., Ghezzi, S., Scarpini, E., Bresolin, N., and Comi, G.P. (2009). VEGF genetic variability is associated with increased risk of developing Alzheimer's disease. J. Neurol. Sci. 283, 66-68.
18. Delisle, M.B., Murrell, J.R., Richardson, R., Trofatter, J.A., Rascol, O., Soulages, X., Mohr, M., Calvas, P., and Ghetti, B. (1999). A mutation at codon 279 (N279K) in exon 10 of the Tau gene causes a tauopathy with dementia and supranuclear palsy. Acta. Neuropathol. 98, 62-77.
19. Dephoure, N., Zhou, C., Villen, J., Beausoleil, S.A., Bakalarski, C.E., Elledge, S.J., and Gygi, S.P. (2008). A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105, 10762-10767.
20. Ding, J.H., Zhong, X.Y., Hagopian, J.C., Cruz, M.M., Ghosh, G., Feramisco, J., Adams, J.A., and Fu, X.D. (2006). Regulated cellular partitioning of SR protein-specific kinases in mammalian cells. Mol. Biol. Cell 17, 876-885.
21. Drechsel, D.N., Hyman, A.A., Cobb, M.H., and Kirschner, M.W. (1992). Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol. Biol. Cell 3, 1141-1154.
22. Drewes, G., Trinczek, B., Illenberger, S., Biernat, J., Schmitt-Ulms, G., Meyer, H.E., Mandelkow, E.M., and Mandelkow, E. (1995). Microtubule-associated protein/microtubule affinity-regulating kinase (p110mark). A novel protein kinase that regulates tau-microtubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site serine 262. J. Biol. Chem. 270, 7679-7688.
23. Eckert, A., Steiner, B., Marques, C., Leutz, S., Romig, H., Haass, C., and Muller, W.E. (2001). Elevated vulnerability to oxidative stress-induced cell death and activation of caspase-3 by the Swedish amyloid precursor protein mutation. J. Neurosci. Res. 64, 183-192.
24. Edmond, V., Moysan, E., Khochbin, S., Matthias, P., Brambilla, C., Brambilla, E., Gazzeri, S., and Eymin, B. (2011). Acetylation and phosphorylation of SRSF2 control cell fate decision in response to cisplatin. EMBO J. 30, 510-523.
25. Erdo, F., Trapp, T., Mies, G., and Hossmann, K.A. (2004). Immunohistochemical analysis of protein expression after middle cerebral artery occlusion in mice. Acta Neuropathol. 107, 127-136.
26. Esmaeli-Azad, B., McCarty, J.H., and Feinstein, S.C. (1994). Sense and antisense transfection analysis of tau function: tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J. Cell Sci. 107 (Pt 4), 869-879.
27. Falke, E., Nissanov, J., Mitchell, T.W., Bennett, D.A., Trojanowski, J.Q., and Arnold, S.E. (2003). Subicular dendritic arborization in Alzheimer's disease correlates with neurofibrillary tangle density. Am. J. Pathol. 163, 1615-1621.
28. Forstl, H. and Kurz, A. (1999). Clinical features of Alzheimer's disease. Eur. Arch. Psychiatry Clin. Neurosci. 249, 288-290.
29. Freeman, R.S., Estus, S., and Johnson, E.M., Jr. (1994). Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of Cyclin D1 during programmed cell death. Neuron 12, 343-355.
30. Fukuhara, T., Hosoya, T., Shimizu, S., Sumi, K., Oshiro, T., Yoshinaka, Y., Suzuki, M., Yamamoto, N., Herzenberg, L.A., and Hagiwara, M. (2006). Utilization of host SR protein kinases and RNA-splicing machinery during viral replication. Proc. Natl. Acad. Sci. USA 103, 11329-11333.
31. Gao, L., Wang, J., Wang, Y., and Andreadis, A. (2007). SR protein 9G8 modulates splicing of tau exon 10 via its proximal downstream intron, a clustering region for frontotemporal dementia mutations. Mol. Cell. Neurosci. 34, 48-58.
32. Gengler, S., Hamilton, A., and Holscher, C. (2010). Synaptic plasticity in the hippocampus of a APP/PS1 mouse model of Alzheimer's disease is impaired in old but not young mice. PLoS One 5, e9764.
33. Ghosh, G. and Adams, J.A. (2011). Phosphorylation mechanism and structure of serine-arginine protein kinases. FEBS J. 278, 587-597.
34. Goedert, M., Cohen, E.S., Jakes, R., and Cohen, P. (1992). p42 MAP kinase phosphorylation sites in microtubule-associated protein tau are dephosphorylated by protein phosphatase 2A1. Implications for Alzheimer's disease [corrected]. FEBS Lett. 312, 95-99.
35. Greenwood, J.A., Scott, C.W., Spreen, R.C., Caputo, C.B., and Johnson, G.V. (1994). Casein kinase II preferentially phosphorylates human tau isoforms containing an amino-terminal insert. Identification of threonine 39 as the primary phosphate acceptor. J. Biol. Chem. 269, 4373-4380.
36. Grundke-Iqbal, I., Iqbal, K., Tung, Y.C., Quinlan, M., Wisniewski, H.M., and Binder, L.I. (1986). Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA 83, 4913-4917.
37. Gu, Z., Liu, W., and Yan, Z. (2009). {beta}-Amyloid impairs AMPA receptor trafficking and function by reducing Ca2 + /calmodulindependent protein kinase II synaptic distribution. J. Biol. Chem. 284, 10639-10649.
38. Gu, J., Shi, J., Wu, S., Jin, N., Qian, W., Zhou, J., Iqbal, I.G., Iqbal, K., Gong, C.X., and Liu, F. (2012). Cyclic AMP-dependent protein kinase regulates 9G8-mediated alternative splicing of tau exon 10. FEBS Lett. 586, 2239-2244.
39. Gui, J.F., Lane, W.S., and Fu, X.D. (1994). A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 369, 678-682.
40. Hanger, D.P., Hughes, K., Woodgett, J.R., Brion, J.P., and Anderton, B.H. (1992). Glycogen synthase kinase-3 induces Alzheimer's disease-like phosphorylation of tau: generation of paired helical filament epitopes and neuronal localisation of the kinase. Neurosci. Lett. 147, 58-62.
41. Hartmann, A.M., Rujescu, D., Giannakouros, T., Nikolakaki, E., Goedert, M., Mandelkow, E.M., Gao, Q.S., Andreadis, A., and Stamm, S. (2001). Regulation of alternative splicing of human tau exon 10 by phosphorylation of splicing factors. Mol. Cell. Neurosci. 18, 80-90.
42. Hensley, K., Carney, J.M., Mattson, M.P., Aksenova, M., Harris, M., Wu, J.F., Floyd, R.A., and Butterfield, D.A. (1994). A model for beta-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease. Proc. Natl. Acad. Sci. USA 91, 3270-3274.
43. Hernandez, F., Perez, M., Lucas, J.J., Mata, A.M., Bhat, R., and Avila, J. (2004). Glycogen synthase kinase-3 plays a crucial role in tau exon 10 splicing and intranuclear distribution of SC35. Implications for Alzheimer's disease. J. Biol. Chem. 279, 3801-3806.
44. Herrup, K. and Busser, J.C. (1995). The induction of multiple cell cycle events precedes target-related neuronal death. Development 121, 2385-2395.
45. Hoglinger, G.U., Breunig, J.J., Depboylu, C., Rouaux, C., Michel, P.P., Alvarez-Fischer, D., Boutillier, A.L., Degregori, J., Oertel, W.H., Rakic, P., et al. (2007). The pRb/E2F cell-cycle pathway mediates cell death in Parkinson's disease. Proc. Natl. Acad. Sci. USA 104, 3585-3590.
46. Hong, Y., Jang, S.W., and Ye, K. (2011). The N-terminal fragment from caspase-cleaved serine/arginine protein-specific kinase2 (SRPK2) translocates into the nucleus and promotes apoptosis. J. Biol. Chem. 286, 777-786.
47. Hong, Y., Chan, C.B., Kwon, I.S., Li, X., Song, M., Lee, H.P., Liu, X., Sompol, P., Jin, P., Lee, H.G., et al. (2012). SRPK2 phosphorylates tau and mediates the cognitive defects in Alzheimer's disease. J. Neurosci. 32, 17262-17272.
48. Hoover, B.R., Reed, M.N., Su, J., Penrod, R.D., Kotilinek, L.A., Grant, M.K., Pitstick, R., Carlson, G.A., Lanier, L.M., Yuan, L.L., et al. (2010). Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron 68, 1067-1081.
49. Hsieh, H., Boehm, J., Sato, C., Iwatsubo, T., Tomita, T., Sisodia, S., and Malinow, R. (2006). AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52, 831-843.
50. Hutton, M., Lendon, C.L., Rizzu, P., Baker, M., Froelich, S., Houlden, H., Pickering-Brown, S., Chakraverty, S., Isaacs, A., Grover, A., et al. (1998). Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393, 702-705.
51. Illenberger, S., Zheng-Fischhofer, Q., Preuss, U., Stamer, K., Baumann, K., Trinczek, B., Biernat, J., Godemann, R., Mandelkow, E.M., and Mandelkow, E. (1998). The endogenous and cell cycle-dependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease. Mol. Biol. Cell 9, 1495-1512.
52. Jang, S.W., Yang, S.J., Ehlen, A., Dong, S., Khoury, H., Chen, J., Persson, J.L., and Ye, K. (2008). Serine/arginine proteinspecific kinase 2 promotes leukemia cell proliferation by phosphorylating acinus and regulating cyclin A1. Cancer Res. 68, 4559-4570.
53. Jang, S.W., Liu, X., Fu, H., Rees, H., Yepes, M., Levey, A., and Ye, K. (2009). Interaction of Akt-phosphorylated SRPK2 with 14-3-3 mediates cell cycle and cell death in neurons. J. Biol. Chem. 284, 24512-24525.
54. Jankovic, J. (2008). Parkinson's disease: clinical features and diagnosis. J. Neurol. Neurosurg. Psychiatry 79, 368-376.
55. Jordan-Sciutto, K.L., Dorsey, R., Chalovich, E.M., Hammond, R.R., and Achim, C.L. (2003). Expression patterns of retinoblastoma protein in Parkinson disease. J. Neuropathol. Exp. Neurol. 62, 68-74.
56. Kalsotra, A. and Cooper, T.A. (2011). Functional consequences of developmentally regulated alternative splicing. Nat. Rev. Genet. 12, 715-729.
57. Kamachi, M., Le, T.M., Kim, S.J., Geiger, M.E., Anderson, P., and Utz, P.J. (2002). Human autoimmune sera as molecular probes for the identification of an autoantigen kinase signaling pathway. J. Exp. Med. 196, 1213-1225.
58. Kar, A., Havlioglu, N., Tarn, W.Y., and Wu, J.Y. (2006). RBM4 interacts with an intronic element and stimulates tau exon 10 inclusion. J. Biol. Chem. 281, 24479-24488.
59. Kashani, A., Lepicard, E., Poirel, O., Videau, C., David, J.P., Fallet-Bianco, C., Simon, A., Delacourte, A., Giros, B., Epelbaum, J., et al. (2008). Loss of VGLUT1 and VGLUT2 in the prefrontal cortex is correlated with cognitive decline in Alzheimer disease. Neurobiol. Aging 29, 1619-1630.
60. Kim, I., Park, E.J., Seo, J., Ko, S.J., Lee, J., and Kim, C.H. (2011). Zinc stimulates tau S214 phosphorylation by the activation of Raf/ mitogen-activated protein kinase-kinase/extracellular signalregulated kinase pathway. NeuroReport 22, 839-844.
61. Kitamura, Y., Shimohama, S., Kamoshima, W., Ota, T., Matsuoka, Y., Nomura, Y., Smith, M.A., Perry, G., Whitehouse, P.J., and Taniguchi, T. (1998). Alteration of proteins regulating apoptosis, Bcl-2, Bcl-x, Bax, Bak, Bad, ICH-1 and CPP32, in Alzheimer's disease. Brain Res. 780, 260-269.
62. Koizumi, J., Okamoto, Y., Onogi, H., Mayeda, A., Krainer, A.R., and Hagiwara, M. (1999). The subcellular localization of SF2/ ASF is regulated by direct interaction with SR protein kinases (SRPKs). J. Biol. Chem. 274, 11125-11131.
63. Kornblihtt, A.R., Schor, I.E., Allo, M., Dujardin, G., Petrillo, E., and Munoz, M.J. (2013). Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. Cell Biol. 14, 153-165.
64. Kranenburg, O., van der Eb, A.J., and Zantema, A. (1996). Cyclin D1 is an essential mediator of apoptotic neuronal cell death. EMBO J. 15, 46-54.
65. Kruman, II, Wersto, R.P., Cardozo-Pelaez, F., Smilenov, L., Chan, S.L., Chrest, F.J., Emokpae, R. Jr., Gorospe, M., and Mattson, M.P. (2004). Cell cycle activation linked to neuronal cell death initiated by DNA damage. Neuron 41, 549-561.
66. Ksiezak-Reding, H., Pyo, H.K., Feinstein, B., and Pasinetti, G.M. (2003). Akt/PKB kinase phosphorylates separately Thr212 and Ser214 of tau protein in vitro. Biochim. Biophys. Acta 1639, 159-168.
67. Kuroyanagi, H., Kimura, T., Wada, K., Hisamoto, N., Matsumoto, K., and Hagiwara, M. (2000). SPK-1, a C. elegans SR protein kinase homologue, is essential for embryogenesis and required for germline development. Mech. Dev. 99, 51-64.
68. Kurt, M.A., Davies, D.C., Kidd, M., Duff, K., Rolph, S.C., Jennings, K.H., and Howlett, D.R. (2001). Neurodegenerative changes associated with beta-amyloid deposition in the brains of mice carrying mutant amyloid precursor protein and mutant presenilin-1 transgenes. Exp. Neurol. 171, 59-71.
69. Kyoung Pyo, H., Lovati, E., Pasinetti, G.M., and Ksiezak-Reding, H. (2004). Phosphorylation of tau at THR212 and SER214 in human neuronal and glial cultures: the role of AKT. Neuroscience 127, 649-658.
70. Lambrechts, D., Storkebaum, E., Morimoto, M., Del-Favero, J., Desmet, F., Marklund, S.L., Wyns, S., Thijs, V., Andersson, J., van Marion, I., et al. (2003). VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat. Genet. 34, 383-394.
71. Lee, G., Cowan, N., and Kirschner, M. (1988). The primary structure and heterogeneity of tau protein from mouse brain. Science 239, 285-288.
72. Lee, G., Newman, S.T., Gard, D.L., Band, H., and Panchamoorthy, G. (1998). Tau interacts with src-family non-receptor tyrosine kinases. J. Cell Sci. 111 (Pt 21), 3167-3177.
73. Leroy, A., Landrieu, I., Huvent, I., Legrand, D., Codeville, B., Wieruszeski, J.M., and Lippens, G. (2010). Spectroscopic studies of GSK3 { beta } phosphorylation of the neuronal tau protein and its interaction with the N-terminal domain of apolipoprotein E. J. Biol. Chem. 285, 33435-33444.
74. Lindwall, G. and Cole, R.D. (1984). Phosphorylation affects the ability of tau protein to promote microtubule assembly. J. Biol. Chem. 259, 5301-5305.
75. Loh, B.J., Cullen, C.F., Vogt, N., and Ohkura, H. (2012). The conserved kinase SRPK regulates karyosome formation and spindle microtubule assembly in Drosophila oocytes. J. Cell Sci. 125, 4457-4462.
76. Loo, D.T., Copani, A., Pike, C.J., Whittemore, E.R., Walencewicz, A.J., and Cotman, C.W. (1993). Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955.
77. Ma, H.T. and Poon, R.Y. (2011). How protein kinases co-ordinate mitosis in animal cells. Biochem. J. 435, 17-31.
78. Manczak, M., Anekonda, T.S., Henson, E., Park, B.S., Quinn, J., and Reddy, P.H. (2006). Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression. Hum. Mol. Genet. 15, 1437-1449.
79. Martin, L., Latypova, X., and Terro, F. (2011). Post-translational modifications of tau protein: implications for Alzheimer's disease. Neurochem. Int. 58, 458-471.
80. Mathew, R., Hartmuth, K., Mohlmann, S., Urlaub, H., Ficner, R., and Luhrmann, R. (2008). Phosphorylation of human PRP28 by SRPK2 is required for integration of the U4/U6-U5 tri-snRNP into the spliceosome. Nat. Struct. Mol. Biol. 15, 435-443.
81. Menalled, L.B. (2005). Knock-in mouse models of Huntington's disease. NeuroRx 2, 465-470.
82. Mills, J.D. and Janitz, M. (2012). Alternative splicing of mRNA in the molecular pathology of neurodegenerative diseases. Neurobiol. Aging 33, 1012 e1011-1024.
83. Misteli, T., Caceres, J.F., and Spector, D.L. (1997). The dynamics of a pre-mRNA splicing factor in living cells. Nature 387, 523-527.
84. Momeni, P., Pittman, A., Lashley, T., Vandrovcova, J., Malzer, E., Luk, C., Hulette, C., Lees, A., Revesz, T., Hardy, J., et al. (2009). Clinical and pathological features of an Alzheimer's disease patient with the MAPT Delta K280 mutation. Neurobiol. Aging 30, 388-393.
85. Mosch, B., Morawski, M., Mittag, A., Lenz, D., Tarnok, A., and Arendt, T. (2007). Aneuploidy and DNA replication in the normal human brain and Alzheimer's disease. J. Neurosci. 27, 6859-6867.
86. Mullaart, E., Boerrigter, M.E., Ravid, R., Swaab, D.F., and Vijg, J. (1990). Increased levels of DNA breaks in cerebral cortex of Alzheimer's disease patients. Neurobiol. Aging 11, 169-173.
87. Mylonis, I. and Giannakouros, T. (2003). Protein kinase CK2 phosphorylates and activates the SR protein-specific kinase 1. Biochem. Biophys. Res. Commun. 301, 650-656.
88. Mytilinaios, D.G., Tsamis, K.I., Nikolakaki, E., and Giannakouros, T. (2012). Distribution of SRPK1 in human brain. J. Chem. Neuroanat. 43, 20-27.
89. Nagy, Z., Esiri, M.M., Cato, A.M., and Smith, A.D. (1997). Cell cycle markers in the hippocampus in Alzheimer's disease. Acta Neuropathol. 94, 6-15.
90. Nakagawa, O., Arnold, M., Nakagawa, M., Hamada, H., Shelton, J.M., Kusano, H., Harris, T.M., Childs, G., Campbell, K.P., Richardson, J.A., et al. (2005). Centronuclear myopathy in mice lacking a novel muscle-specific protein kinase transcriptionally regulated by MEF2. Genes Dev. 19, 2066-2077.
91. Ngo, J.C., Gullingsrud, J., Giang, K., Yeh, M.J., Fu, X.D., Adams, J.A., McCammon, J.A., and Ghosh, G. (2007). SR protein kinase 1 is resilient to inactivation. Structure 15, 123-133.
92. Niblock, M. and Gallo, J.M. (2012). Tau alternative splicing in familial and sporadic tauopathies. Biochem. Soc. Trans. 40, 677-680.
93. Nikolakaki, E., Kohen, R., Hartmann, A.M., Stamm, S., Georgatsou, E., and Giannakouros, T. (2001). Cloning and characterization of an alternatively spliced form of SR protein kinase 1 that interacts specifically with scaffold attachment factor-B. J. Biol. Chem. 276, 40175-40182.
94. Nowak, D.G., Amin, E.M., Rennel, E.S., Hoareau-Aveilla, C., Gammons, M., Damodoran, G., Hagiwara, M., Harper, S.J., Woolard, J., Ladomery, M.R., et al. (2010). Regulation of vascular endothelial growth factor (VEGF) splicing from pro-angiogenic to anti-angiogenic isoforms: a novel therapeutic strategy for angiogenesis. J. Biol. Chem. 285, 5532-5540.
95. Oddo, S., Caccamo, A., Shepherd, J.D., Murphy, M.P., Golde, T.E., Kayed, R., Metherate, R., Mattson, M.P., Akbari, Y., and LaFerla, F.M. (2003). Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39, 409-421.
96. Ogunshola, O.O., Antic, A., Donoghue, M.J., Fan, S.Y., Kim, H., Stewart, W.B., Madri, J.A., and Ment, L.R. (2002). Paracrine and autocrine functions of neuronal vascular endothelial growth factor (VEGF) in the central nervous system. J. Biol. Chem. 277, 11410-11415.
97. Park, D.S., Morris, E.J., Stefanis, L., Troy, C.M., Shelanski, M.L., Geller, H.M., and Greene, L.A. (1998). Multiple pathways of neuronal death induced by DNA-damaging agents, NGF deprivation, and oxidative stress. J. Neurosci. 18, 830-840.
98. Pei, J.J., An, W.L., Zhou, X.W., Nishimura, T., Norberg, J., Benedikz, E., Gotz, J., and Winblad, B. (2006). P70 S6 kinase mediates tau phosphorylation and synthesis. FEBS Lett. 580, 107-114.
99. Qian, W., Iqbal, K., Grundke-Iqbal, I., Gong, C.X., and Liu, F. (2011a). Splicing factor SC35 promotes tau expression through stabilization of its mRNA. FEBS Lett. 585, 875-880.
100. Qian, W., Liang, H., Shi, J., Jin, N., Grundke-Iqbal, I., Iqbal, K., Gong, C.X., and Liu, F. (2011b). Regulation of the alternative splicing of tau exon 10 by SC35 and Dyrk1A. Nucleic Acids Res. 39, 6161-6171.
101. Ranganathan, S. and Bowser, R. (2003). Alterations in G(1) to S phase cell-cycle regulators during amyotrophic lateral sclerosis. Am. J. Pathol. 162, 823-835.
102. Rhind, N. and Russell, P. (2012). Signaling pathways that regulate cell division. Cold Spring Harbor Perspect. Biol. 4, a005942.
103. Risso, G., Pelisch, F., Quaglino, A., Pozzi, B., and Srebrow, A. (2012). Regulating the regulators: serine/arginine-rich proteins under scrutiny. IUBMB Life 64, 809-816.
104. Robertson, J., Loviny, T.L., Goedert, M., Jakes, R., Murray, K.J., Anderton, B.H., and Hanger, D.P. (1993). Phosphorylation of tau by cyclic-AMP-dependent protein kinase. Dementia 4, 256-263.
105. Ryoo, S.R., Jeong, H.K., Radnaabazar, C., Yoo, J.J., Cho, H.J., Lee, H.W., Kim, I.S., Cheon, Y.H., Ahn, Y.S., Chung, S.H., et al. (2007). DYRK1A-mediated hyperphosphorylation of Tau. A functional link between Down syndrome and Alzheimer disease. J. Biol. Chem. 282, 34850-34857.
106. Samsonov, A., Yu, J.Z., Rasenick, M., and Popov, S.V. (2004). Tau interaction with microtubules in vivo. J. Cell Sci. 117, 6129-6141.
107. Sato, S., Cerny, R.L., Buescher, J.L., and Ikezu, T. (2006). Tau-tubulin kinase 1 (TTBK1), a neuron-specific tau kinase candidate, is involved in tau phosphorylation and aggregation. J. Neurochem. 98, 1573-1584.
108. Scheff, S.W., Price, D.A., Schmitt, F.A., and Mufson, E.J. (2006). Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging 27, 1372-1384.
109. Scheff, S.W., Price, D.A., Schmitt, F.A., DeKosky, S.T., and Mufson, E.J. (2007). Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 68, 1501-1508.
110. Schmetsdorf, S., Gartner, U., and Arendt, T. (2007). Constitutive expression of functionally active cyclin-dependent kinases and their binding partners suggests noncanonical functions of cell cycle regulators in differentiated neurons. Cereb. Cortex 17, 1821-1829.
111. Schwartz, G.K. and Shah, M.A. (2005). Targeting the cell cycle: a new approach to cancer therapy. J. Clin. Oncol. 23, 9408-9421.
112. Schwerk, C., Prasad, J., Degenhardt, K., Erdjument-Bromage, H., White, E., Tempst, P., Kidd, V.J., Manley, J.L., Lahti, J.M., and Reinberg, D. (2003). ASAP, a novel protein complex involved in RNA processing and apoptosis. Mol. Cell. Biol. 23, 2981-2990.
113. Seward, M.E., Swanson, E., Norambuena, A., Reimann, A., Cochran, J.N., Li, R., Roberson, E.D., and Bloom, G.S. (2013). Amyloid-beta signals through tau to drive ectopic neuronal cell cycle re-entry in Alzheimer's disease. J. Cell Sci. 126, 1278-1286.
114. Shi, J., Qian, W., Yin, X., Iqbal, K., Grundke-Iqbal, I., Gu, X., Ding, F., Gong, C.X., and Liu, F. (2011). Cyclic AMP-dependent protein kinase regulates the alternative splicing of tau exon 10: a mechanism involved in tau pathology of Alzheimer disease. J. Biol. Chem. 286, 14639-14648.
115. Shieh, S.Y., Ikeda, M., Taya, Y., and Prives, C. (1997). DNA damageinduced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91, 325-334.
116. Shimohama, S., Tanino, H., and Fujimoto, S. (1999). Changes in caspase expression in Alzheimer's disease: comparison with development and aging. Biochem. Biophys. Res. Commun. 256, 381-384.
117. Shultz, J.C., Goehe, R.W., Wijesinghe, D.S., Murudkar, C., Hawkins, A.J., Shay, J.W., Minna, J.D., and Chalfant, C.E. (2010). Alternative splicing of caspase 9 is modulated by the phosphoinositide 3-kinase/Akt pathway via phosphorylation of SRp30a. Cancer Res. 70, 9185-9196.
118. Siebel, C.W., Feng, L., Guthrie, C., and Fu, X.D. (1999). Conservation in budding yeast of a kinase specific for SR splicing factors. Proc. Natl. Acad. Sci. USA 96, 5440-5445.
119. Smith, D.L., Pozueta, J., Gong, B., Arancio, O., and Shelanski, M. (2009). Reversal of long-term dendritic spine alterations in Alzheimer disease models. Proc. Natl. Acad. Sci. USA 106, 16877-16882.
120. Steiner, B., Mandelkow, E.M., Biernat, J., Gustke, N., Meyer, H.E., Schmidt, B., Mieskes, G., Soling, H.D., Drechsel, D., Kirschner, M.W., et al. (1990). Phosphorylation of microtubule-associated protein tau: identification of the site for Ca2 (+) -calmodulin dependent kinase and relationship with tau phosphorylation in Alzheimer tangles. EMBO J. 9, 3539-3544.
121. Sturrock, A. and Leavitt, B.R. (2010). The clinical and genetic features of Huntington disease. J. Geriatr. Psychiatry Neurol. 23, 243-259.
122. Sumrejkanchanakij, P., Tamamori-Adachi, M., Matsunaga, Y., Eto, K., and Ikeda, M.A. (2003). Role of cyclin D1 cytoplasmic sequestration in the survival of postmitotic neurons. Oncogene 22, 8723-8730.
123. Svensson, B., Peters, M., Konig, H.G., Poppe, M., Levkau, B., Rothermundt, M., Arolt, V., Kogel, D., and Prehn, J.H. (2002). Vascular endothelial growth factor protects cultured rat hippocampal neurons against hypoxic injury via an antiexcitotoxic, caspase-independent mechanism. J. Cereb. Blood Flow Metab. 22, 1170-1175.
124. Szekelyhidi, Z., Pato, J., Waczek, F., Banhegyi, P., Hegymegi-Barakonyi, B., Eros, D., Meszaros, G., Hollosy, F., Hafenbradl, D., Obert, S., et al. (2005). Synthesis of selective SRPK-1 inhibitors: novel tricyclic quinoxaline derivatives. Bioorg. Med. Chem. Lett. 15, 3241-3246.
125. Tang, Z., Yanagida, M., and Lin, R.J. (1998). Fission yeast mitotic regulator Dsk1 is an SR protein-specific kinase. J. Biol. Chem. 273, 5963-5969.
126. Tsianou, D., Nikolakaki, E., Tzitzira, A., Bonanou, S., Giannakouros, T., and Georgatsou, E. (2009). The enzymatic activity of SR protein kinases 1 and 1a is negatively affected by interaction with scaffold attachment factors B1 and 2. FEBS J. 276, 5212-5227.
127. Ueberham, U., Hessel, A., and Arendt, T. (2003). Cyclin C expression is involved in the pathogenesis of Alzheimer's disease. Neurobiol. Aging 24, 427-435.
128. Uetsuki, T., Takemoto, K., Nishimura, I., Okamoto, M., Niinobe, M., Momoi, T., Miura, M., and Yoshikawa, K. (1999). Activation of neuronal caspase-3 by intracellular accumulation of wild-type Alzheimer amyloid precursor protein. J. Neurosci. 19, 6955-6964.
129. van der Putten, H., Wiederhold, K.H., Probst, A., Barbieri, S., Mistl, C., Danner, S., Kauffmann, S., Hofele, K., Spooren, W.P., Ruegg, M.A., et al. (2000). Neuropathology in mice expressing human alpha-synuclein. J. Neurosci. 20, 6021-6029.
130. Varvel, N.H., Bhaskar, K., Patil, A.R., Pimplikar, S.W., Herrup, K., and Lamb, B.T. (2008). Abeta oligomers induce neuronal cell cycle events in Alzheimer's disease. J. Neurosci. 28, 10786-10793.
131. Vincent, I., Jicha, G., Rosado, M., and Dickson, D.W. (1997). Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J. Neurosci. 17, 3588-3598.
132. Virdee, K., Yoshida, H., Peak-Chew, S., and Goedert, M. (2007). Phosphorylation of human microtubule-associated protein tau by protein kinases of the AGC subfamily. FEBS Lett. 581, 2657-2662.
133. Vivarelli, S., Lenzken, S.C., Ruepp, M.D., Ranzini, F., Maffioletti, A., Alvarez, R., Muhlemann, O., and Barabino, S.M. (2013). Paraquat modulates alternative pre-mRNA splicing by modifying the intracellular distribution of SRPK2. PLoS One 8, e61980.
134. Wang, H.Y., Lin, W., Dyck, J.A., Yeakley, J.M., Songyang, Z., Cantley, L.C., and Fu, X.D. (1998). SRPK2: a differentially expressed SR protein-specific kinase involved in mediating the interaction and localization of pre-mRNA splicing factors in mammalian cells. J. Cell Biol. 140, 737-750.
135. Wang, J., Gao, Q.S., Wang, Y., Lafyatis, R., Stamm, S., and Andreadis, A. (2004). Tau exon 10, whose missplicing causes frontotemporal dementia, is regulated by an intricate interplay of cis elements and trans factors. J. Neurochem. 88, 1078-1090.
136. Wang, Y., Gao, L., Tse, S.W., and Andreadis, A. (2010). Heterogeneous nuclear ribonucleoprotein E3 modestly activates splicing of tau exon 10 via its proximal downstream intron, a hotspot for frontotemporal dementia mutations. Gene 451, 23-31.
137. Wang, P., Xie, Z.H., Guo, Y.J., Zhao, C.P., Jiang, H., Song, Y., Zhu, Z.Y., Lai, C., Xu, S.L., and Bi, J.Z. (2011a). VEGF-induced angiogenesis ameliorates the memory impairment in APP transgenic mouse model of Alzheimer's disease. Biochem. Biophys. Res. Commun. 411, 620-626.
138. Wang, Y., Wang, J., Gao, L., Stamm, S., and Andreadis, A. (2011b). An SRp75/hnRNPG complex interacting with hnRNPE2 regulates the 5'splice site of tau exon 10, whose misregulation causes frontotemporal dementia. Gene 485, 130-138.
139. Wei, Z., Song, M.S., MacTavish, D., Jhamandas, J.H., and Kar, S. (2008). Role of calpain and caspase in beta-amyloidinduced cell death in rat primary septal cultured neurons. Neuropharmacology 54, 721-733.
140. Yap, K. and Makeyev, E.V. (2013). Regulation of gene expression in mammalian nervous system through alternative pre-mRNA splicing coupled with RNA quality control mechanisms. Mol. Cell. Neurosci. in press.
141. Yin, X., Jin, N., Gu, J., Shi, J., Zhou, J., Gong, C.X., Iqbal, K., Grundke-Iqbal, I., and Liu, F. (2012). Dual-specificity tyrosine phosphorylation-regulated kinase 1A (Dyrk1A) modulates serine/arginine-rich protein 55 (SRp55)-promoted Tau exon 10 inclusion. J. Biol. Chem. 287, 30497-30506.
142. Yoshida, H. and Goedert, M. (2006). Sequential phosphorylation of tau protein by cAMP-dependent protein kinase and SAPK4/ p38delta or JNK2 in the presence of heparin generates the AT100 epitope. J. Neurochem. 99, 154-164.
143. Yoshida, H., Hastie, C.J., McLauchlan, H., Cohen, P., and Goedert, M. (2004). Phosphorylation of microtubule-associated protein tau by isoforms of c-Jun N-terminal kinase (JNK). J. Neurochem. 90, 352-358.
144. Yuan, A., Kumar, A., Peterhoff, C., Duff, K., and Nixon, R.A. (2008). Axonal transport rates in vivo are unaffected by tau deletion or overexpression in mice. J. Neurosci. 28, 1682-1687.
145. Zhong, X.Y., Ding, J.H., Adams, J.A., Ghosh, G., and Fu, X.D. (2009). Regulation of SR protein phosphorylation and alternative splicing by modulating kinetic interactions of SRPK1 with molecular chaperones. Genes Dev. 23, 482-495.
146. Zhou, Z., Qiu, J., Liu, W., Zhou, Y., Plocinik, R.M., Li, H., Hu, Q., Ghosh, G., Adams, J.A., Rosenfeld, M.G., et al. (2012). The Akt-SRPK-SR axis constitutes a major pathway in transducing EGF signaling to regulate alternative splicing in the nucleus. Mol. Cell 47, 422-433.