Role of glycogen synthase kinase-3β in APP hyperphosphorylation induced by NMDA stimulation in cortical neurons

Pharmaceuticals

Volumn 3, Issue 1, 2010, Pages 42-58

  Ploia, Cristina ^a   Sclip, Alessandra ^a   Colombo, Alessio ^a   Repici, Mariaelena ^b   Gardoni, Fabrizio ^c   di Luca, Monica ^c   Forloni, Gianluigi ^a   Antoniou, Xanthi ^a   Borsello, Tiziana ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b Groupe Enzymologie Moléculaire et Fonctionnelle   (France)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

APP; Cdk5; GSK 3 ; JNK; NMDA

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CYCLIN DEPENDENT KINASE 5; GLYCOGEN SYNTHASE KINASE 3BETA; N METHYL DEXTRO ASPARTIC ACID; ROSCOVITINE; STRESS ACTIVATED PROTEIN KINASE; THREONINE;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BRAIN CELL; CELL STIMULATION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; EXCITOTOXICITY; NERVE CELL NECROSIS; NONHUMAN; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

EID: 77951907971     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph3010042     Document Type: Article

References (48)

1. Da Cruz e Silva, E.F.; da Cruz e Silva, O.A. Protein phosphorylation and APP metabolism. Neurochem. Res. 2003, 28, 1553-1561.
2. Tomita, S.; Kirino, Y.; Suzuki, T. A basic amino acid in the cytoplasmic domain of Alzheimer's beta-amyloid precursor protein (APP) is essential for cleavage of APP at the alpha-site. J. Biol. Chem. 1998, 273, 19304-19310.
3. Lee, M.S.; Kao, S.C.; Lemere, C.A.; Xia, W.; Tseng, H.C.; Zhou, Y.; Neve, R.; Ahlijanian, M.K.; Tsai, L.H. APP processing is regulated by cytoplasmic phosphorylation. J. Cell. Biol. 2003, 163, 83-95.
4. Aplin, A.E.; Gibb, G.M.; Jacobsen, J.S.; Gallo, J.M.; Anderton, B.H. In vitro phosphorylation of the cytoplasmic domain of the amyloid precursor protein by glycogen synthase kinase-3beta. J. Neurochem. 1996, 67, 699-707.
5. Iijima, K.; Ando, K.; Takeda, S.; Satoh, Y.; Seki, T.; Itohara, S.; Greengard, P.; Kirino, Y.; Nairn, A.C.; Suzuki, T. Neuron-specific phosphorylation of Alzheimer's beta-amyloid precursor protein by cyclin-dependent kinase 5. J. Neurochem. 2000, 75, 1085-1091.
6. Standen, C.L.; Brownlees, J.; Grierson, A.J.; Kesavapany, S.; Lau, K.F.; McLoughlin, D.M.; Miller, C.C. Phosphorylation of thr(668) in the cytoplasmic domain of the Alzheimer's disease amyloid precursor protein by stress-activated protein kinase 1b (Jun N-terminal kinase-3). J. Neurochem. 2001, 76, 316-320.
7. Muresan, Z.; Muresan, V. c-Jun NH2-terminal kinase-interacting protein-3 facilitates phosphorylation and controls localization of amyloid-beta precursor protein. J. Neurosci. 2005, 25, 3741-3751.
8. Muresan, Z.; Muresan, V. The amyloid-beta precursor protein is phosphorylated via distinct pathways during differentiation, mitosis, stress, and degeneration. Mol. Biol. Cell. 2007, 18, 3835-3844.
9. Gong, X.; Tang, X.; Wiedmann, M.; Wang, X.; Peng, J.; Zheng, D.; Blair, L.A.; Marshall, J.; Mao, Z. Cdk5-mediated inhibition of the protective effects of transcription factor MEF2 in neurotoxicity-induced apoptosis. Neuron 2003, 38, 33-46.
10. Lee, M.S.; Kwon, Y.T.; Li, M.; Peng, J.; Friedlander, R.M.; Tsai, L.H. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 2000, 405, 360-364.
11. Suzuki, T.; Oishi, M.; Marshak, D.R.; Czernik, A.J.; Nairn, A.C.; Greengard, P. Cell cycle- dependent regulation of the phosphorylation and metabolism of the Alzheimer amyloid precursor protein. Embo. J. 1994, 13, 1114-1122.
12. Colombo, A.; Bastone, A.; Ploia, C.; Sclip, A.; Salmona, M.; Forloni, G.; Borsello, T. JNK regulates APP cleavage and degradation in a model of Alzheimer's disease. Neurobiol. Dis. 2009, 33, 518-525.
13. Yang, D.D.; Kuan, C.Y.; Whitmarsh, A.J.; Rincon, M.; Zheng, T.S.; Davis, R.J.; Rakic, P.; Flavell, R.A. Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 1997, 389, 865-870.
14. Centeno, C.; Repici, M.; Chatton, J.Y.; Riederer, B.M.; Bonny, C.; Nicod, P.; Price, M.; Clarke, P.G.; Papa, S.; Franzoso, G.; Borsello, T. Role of the JNK pathway in NMDA-mediated excitotoxicity of cortical neurons. Cell Death Differ. 2007, 14, 240-253.
15. Borsello, T.; Clarke, P.G.; Hirt, L.; Vercelli, A.; Repici, M.; Schorderet, D.F.; Bogousslavsky, J.; Bonny, C. A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat. Med. 2003, 9, 1180-1186.
16. Shoji, M.; Iwakami, N.; Takeuchi, S.; Waragai, M.; Suzuki, M.; Kanazawa, I.; Lippa, C.F.; Ono, S.; Okazawa, H. JNK activation is associated with intracellular beta-amyloid accumulation. Brain Res. Mol. Brain Res. 2000, 85, 221-233.
17. Colombo, A.; Repici, M.; Pesaresi, M.; Santambrogio, S.; Forloni G.; Borsello, T. The TAT-JNK inhibitor peptide interferes with beta amyloid protein stability. Cell Death Differ. 2007, 14, 1845-1848.
18. O'Hare, M.J.; Kushwaha, N.; Zhang, Y.; Aleyasin, H.; Callaghan, S.M.; Slack, R.S.; Albert, P.R.; Vincent, I.; Park, D.S. Differential roles of nuclear and cytoplasmic cyclin-dependent kinase 5 in apoptotic and excitotoxic neuronal death. J. Neurosci. 2005, 25, 8954-8966.
19. Cruz, J.C.; Kim, D.; Moy, L.Y.; Dobbin, M.M.; Sun, X.; Bronson, R.T.; Tsai, L.H. p25/Cyclin-dependent kinase 5 induces production and intraneuronal accumulation of amyloid beta in vivo. J. Neurosci. 2006, 26, 10536-10541.
20. Alvarez, A.; Toro, R.; Caceres, A.; Maccioni, R.B. Inhibition of tau phosphorylating protein kinase cdk5 prevents beta-amyloid-induced neuronal death. FEBS Lett. 1999, 459, 421-426.
21. Patrick, G.N.; Zukerberg, L.; Nikolic, M.; de la Monte, S.; Dikkes, P.; Tsai, L.H. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999, 402, 615-622.
22. Avila, J.; Lucas, J.J.; Perez, M.; Hernandez, F. Role of tau protein in both physiological and pathological conditions. Physiol. Rev. 2004, 84, 361-384.
23. Hanger, D.P.; Hughes, K.; Woodgett, J.R.; Brion, J.P.; Anderton, B.H. 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. 1992, 147, 58-62.
24. Kirschenbaum, F.; Hsu, S.C.; Cordell, B.; McCarthy, J.V. Substitution of a glycogen synthase kinase-3beta phosphorylation site in presenilin 1 separates presenilin function from beta-catenin signaling. J. Biol. Chem. 2001, 276, 7366-7375.
25. Grimes, C.A.; Jope, R.S. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neurobiol. 2001, 65, 391-426.
26. Bhat, R.V.; Budd Haeberlein, S.L.; Avila, J. Glycogen synthase kinase 3: A drug target for CNS therapies. J. Neurochem. 2004, 89, 1313-1317.
27. Takashima, A.; Noguchi, K.; Michel, G.; Mercken, M.; Hoshi, M.; Ishiguro, K.; Imahori, K. Exposure of rat hippocampal neurons to amyloid beta peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase- 3 beta. Neurosci. Lett. 1996, 203, 33-36.
28. Kelly, S.; Zhao, H.; Hua Sun, G.; Cheng, D.; Qiao, Y.; Luo, J.; Martin, K.; Steinberg, G.K.; Harrison, S.D.; Yenari, M.A. Glycogen synthase kinase 3beta inhibitor Chir025 reduces neuronal death resulting from oxygen-glucose deprivation, glutamate excitotoxicity, and cerebral ischemia. Exp. Neurol. 2004, 188, 378-386.
29. Lesne, S.; Ali, C.; Gabriel, C.; Croci, N.; MacKenzie, E.T.; Glabe, C.G.; Plotkine, M.; Marchand- Verrecchia, C.; Vivien, D.; Buisson, A. NMDA receptor activation inhibits alpha-secretase and promotes neuronal amyloid-beta production. J. Neurosci. 2005, 25, 9367-9377.
30. Bain, J.; McLauchlan, H.; Elliott, M.; Cohen, P. The specificities of protein kinase inhibitors: An update. Biochem. J. 2003, 371, 199-204.
31. Plotkin, B.; Kaidanovich, O.; Talior, I.; Eldar-Finkelman, H. Insulin mimetic action of synthetic phosphorylated peptide inhibitors of glycogen synthase kinase-3. J. Pharmacol. Exp. Ther. 2003, 305, 974-980.
32. Hardy, J. A hundred years of Alzheimer's disease research. Neuron 2006, 52, 3-13.
33. Koh, J.Y.; Yang, L.L.; Cotman, C.W. Beta-amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage. Brain. Res. 1990, 533, 315-320.
34. Mattson, M.P.; Cheng, B.; Davis, D.; Bryant, K.; Lieberburg, I.; Rydel, R.E. beta-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 1992, 12, 376-389.
35. Wu, J.; Anwyl, R.; Rowan, M.J. [beta]-Amyloid selectively augments NMDA receptor-mediated synaptic transmission in rat hippocampus. Neuroreport 1995, 6, 2409-2413.
36. Butterfield, D.A.; Pocernich, C.B. The glutamatergic system and Alzheimer's disease: Therapeutic implications. CNS Drugs 2003, 17, 641-652.
37. Rowan, M.J.; Klyubin, I.; Wang, Q.; Anwyl, R. Mechanisms of the inhibitory effects of amyloid beta-protein on synaptic plasticity. Exp. Gerontol. 2004, 39, 1661-1667.
38. Dunah, A.W.; Yasuda, R.P.; Luo, J.; Wang, Y.; Prybylowski, K.L.; Wolfe, B.B. Biochemical studies of the structure and function of the N-methyl-D-aspartate subtype of glutamate receptors. Mol. Neurobiol. 1999, 19, 151-179.
39. Reisberg, B.; Doody, R.; Stoffler, A.; Schmitt, F.; Ferris, S.; Mobius, H.J. Memantine in moderate-to-severe Alzheimer's disease. N. Engl. J. Med. 2003, 348, 1333-1341.
40. Zoladz, P.R.; Campbell, A.M.; Park, C.R.; Schaefer, D.; Danysz, W.; Diamond, D.M. Enhancement of long-term spatial memory in adult rats by the noncompetitive NMDA receptor antagonists, memantine and neramexane. Pharmacol. Biochem. Behav. 2006, 85, 298-306.
41. Szatmari, E.; Habas, A.; Yang, P.; Zheng, J.J.; Hagg, T.; Hetman, M. A positive feedback loop between glycogen synthase kinase 3beta and protein phosphatase 1 after stimulation of NR2B NMDA receptors in forebrain neurons. J. Biol. Chem. 2005, 280, 37526-37535.
42. Kim, J.W.; Lee, J.E.; Kim, M.J.; Cho, E.G.; Cho, S.G.; Choi, E.J. Glycogen synthase kinase 3 beta is a natural activator of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase kinase 1 (MEKK1). J. Biol. Chem. 2003, 278, 13995-14001.
43. 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.
44. Fornoni, A.; Pileggi, A.; Molano, R.D.; Sanabria, N.Y.; Tejada, T.; Gonzalez-Quintana, J.; Ichii, H.; Inverardi, L.; Ricordi, C.; Pastori, R.L. Inhibition of c-jun N terminal kinase (JNK) improves functional beta cell mass in human islets and leads to AKT and glycogen synthase kinase-3 (GSK- 3) phosphorylation. Diabetologia 2008, 51, 298-308.
45. Plattner, F.; Angelo, M.; Giese, K.P. The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J. Biol. Chem. 2006, 281, 25457-25465.
46. Hu, D.; Fang, W.; Han, A.; Gallagher, L.; Davis, R.J.; Xiong, B.; Yang, W. c-Jun N-terminal kinase 1 interacts with and negatively regulates Wnt/beta-catenin signaling through GSK3beta pathway. Carcinogenesis 2008, 29, 2317-2324.
47. Bonny, C.; Oberson, A.; Negri, S.; Sauser, C.; Schorderet, D.F. Cell-permeable peptide inhibitors of JNK: Novel blockers of beta-cell death. Diabetes 2001, 50, 77-82.
48. Hoey, S.E.; Williams, R.J.; Perkinton, M.S. Synaptic NMDA receptor activation stimulates alpha-secretase amyloid precursor protein processing and inhibits amyloid-beta production. J. Neurosci. 2009, 29, 4442-4460.