Requirement for Plk2 in Orchestrated Ras and Rap Signaling, Homeostatic Structural Plasticity, and Memory

Neuron

Volumn 69, Issue 5, 2011, Pages 957-973

  Lee, Kea Joo ^a   Lee, Yeunkum ^a   Rozeboom, Aaron ^a   Lee, Ji Yun ^a   Udagawa, Noriko ^a   Hoe, Hyang Sook ^a   Pak, Daniel T S ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLO LIKE KINASE; RAP PROTEIN; RAS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; DOWN REGULATION; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE SILENCING; HOMEOSTASIS; IMMUNOPRECIPITATION; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; BLOTTING, WESTERN; DENDRITIC SPINES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HIPPOCAMPUS; MEMORY; MICE; NEURONAL PLASTICITY; NEURONS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN KINASES; RAP GTP-BINDING PROTEINS; RAS PROTEINS; RECEPTORS, AMPA; SIGNAL TRANSDUCTION;

EID: 79952237532     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.02.004     Document Type: Article

References (45)

1. Arendt T., Gärtner U., Seeger G., Barmashenko G., Palm K., Mittmann T., Yan L., Hümmeke M., Behrbohm J., Brückner M.K., et al. Neuronal activation of Ras regulates synaptic connectivity. Eur. J. Neurosci. 2004, 19:2953-2966.
2. Biou V., Bhattacharyya S., Malenka R.C. Endocytosis and recycling of AMPA receptors lacking GluR2/3. Proc. Natl. Acad. Sci. USA 2008, 105:1038-1043.
3. Brambilla R., Gnesutta N., Minichiello L., White G., Roylance A.J., Herron C.E., Ramsey M., Wolfer D.P., Cestari V., Rossi-Arnaud C., et al. A role for the Ras signalling pathway in synaptic transmission and long-term memory. Nature 1997, 390:281-286.
4. Buchsbaum R., Telliez J.B., Goonesekera S., Feig L.A. The N-terminal pleckstrin, coiled-coil, and IQ domains of the exchange factor Ras-GRF act cooperatively to facilitate activation by calcium. Mol. Cell. Biol. 1996, 16:4888-4896.
5. Chen H.J., Rojas-Soto M., Oguni A., Kennedy M.B. A synaptic Ras-GTPase activating protein (p135 SynGAP) inhibited by CaM kinase II. Neuron 1998, 20:895-904.
6. de Rooij J., Bos J.L. Minimal Ras-binding domain of Raf1 can be used as an activation-specific probe for Ras. Oncogene 1997, 14:623-625.
7. de Rooij J., Boenink N.M., van Triest M., Cool R.H., Wittinghofer A., Bos J.L. PDZ-GEF1, a guanine nucleotide exchange factor specific for Rap1 and Rap2. J. Biol. Chem. 1999, 274:38125-38130.
8. Evers D.M., Matta J.A., Hoe H.S., Zarkowsky D., Lee S.H., Isaac J.T., Pak D.T. Plk2 attachment to NSF induces homeostatic removal of GluA2 during chronic overexcitation. Nat. Neurosci. 2010, 13:1199-1207.
9. Fu Z., Lee S.H., Simonetta A., Hansen J., Sheng M., Pak D.T. Differential roles of Rap1 and Rap2 small GTPases in neurite retraction and synapse elimination in hippocampal spiny neurons. J. Neurochem. 2007, 100:118-131.
10. Heumann R., Goemans C., Bartsch D., Lingenhöhl K., Waldmeier P.C., Hengerer B., Allegrini P.R., Schellander K., Wagner E.F., Arendt T., et al. Transgenic activation of Ras in neurons promotes hypertrophy and protects from lesion-induced degeneration. J. Cell Biol. 2000, 151:1537-1548.
11. Inglis K.J., Chereau D., Brigham E.F., Chiou S.S., Schöbel S., Frigon N.L., Yu M., Caccavello R.J., Nelson S., Motter R., et al. Polo-like kinase 2 (PLK2) phosphorylates alpha-synuclein at serine 129 in central nervous system. J. Biol. Chem. 2009, 284:2598-2602.
12. Kauselmann G., Weiler M., Wulff P., Jessberger S., Konietzko U., Scafidi J., Staubli U., Bereiter-Hahn J., Strebhardt K., Kuhl D. The polo-like protein kinases Fnk and Snk associate with a Ca(2+)- and integrin-binding protein and are regulated dynamically with synaptic plasticity. EMBO J. 1999, 18:5528-5539.
13. Kim J.H., Liao D., Lau L.F., Huganir R.L. SynGAP: A synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron 1998, 20:683-691.
14. Kim J.H., Lee H.K., Takamiya K., Huganir R.L. The role of synaptic GTPase-activating protein in neuronal development and synaptic plasticity. J. Neurosci. 2003, 23:1119-1124.
15. Komiyama N.H., Watabe A.M., Carlisle H.J., Porter K., Charlesworth P., Monti J., Strathdee D.J., O'Carroll C.M., Martin S.J., Morris R.G., et al. SynGAP regulates ERK/MAPK signaling, synaptic plasticity, and learning in the complex with postsynaptic density 95 and NMDA receptor. J. Neurosci. 2002, 22:9721-9732.
16. Krapivinsky G., Krapivinsky L., Manasian Y., Ivanov A., Tyzio R., Pellegrino C., Ben-Ari Y., Clapham D.E., Medina I. The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1. Neuron 2003, 40:775-784.
17. Lalonde R. The neurobiological basis of spontaneous alternation. Neurosci. Biobehav. Rev. 2002, 26:91-104.
18. Lee K.S., Grenfell T.Z., Yarm F.R., Erikson R.L. Mutation of the polo-box disrupts localization and mitotic functions of the mammalian polo kinase Plk. Proc. Natl. Acad. Sci. USA 1998, 95:9301-9306.
19. Lénárt P., Petronczki M., Steegmaier M., Di Fiore B., Lipp J.J., Hoffmann M., Rettig W.J., Kraut N., Peters J.M. The small-molecule inhibitor BI 2536 reveals novel insights into mitotic roles of polo-like kinase 1. Curr. Biol. 2007, 17:304-315.
20. Liao Y., Kariya K., Hu C.D., Shibatohge M., Goshima M., Okada T., Watari Y., Gao X., Jin T.G., Yamawaki-Kataoka Y., Kataoka T. RA-GEF, a novel Rap1A guanine nucleotide exchange factor containing a Ras/Rap1A-associating domain, is conserved between nematode and humans. J. Biol. Chem. 1999, 274:37815-37820.
21. Ma S., Charron J., Erikson R.L. Role of Plk2 (Snk) in mouse development and cell proliferation. Mol. Cell. Biol. 2003, 23:6936-6943.
22. Ma S., Liu M.A., Yuan Y.L., Erikson R.L. The serum-inducible protein kinase Snk is a G1 phase polo-like kinase that is inhibited by the calcium- and integrin-binding protein CIB. Mol. Cancer Res. 2003, 1:376-384.
23. Manabe T., Aiba A., Yamada A., Ichise T., Sakagami H., Kondo H., Katsuki M. Regulation of long-term potentiation by H-Ras through NMDA receptor phosphorylation. J. Neurosci. 2000, 20:2504-2511.
24. Martone M.E., Pollock J.A., Jones Y.Z., Ellisman M.H. Ultrastructural localization of dendritic messenger RNA in adult rat hippocampus. J. Neurosci. 1996, 16:7437-7446.
25. Mayford M., Bach M.E., Huang Y.Y., Wang L., Hawkins R.D., Kandel E.R. Control of memory formation through regulated expression of a CaMKII transgene. Science 1996, 274:1678-1683.
26. Mazzucchelli C., Brambilla R. Ras-related and MAPK signalling in neuronal plasticity and memory formation. Cell. Mol. Life Sci. 2000, 57:604-611.
27. Morozov A., Muzzio I.A., Bourtchouladze R., Van-Strien N., Lapidus K., Yin D., Winder D.G., Adams J.P., Sweatt J.D., Kandel E.R. Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 2003, 39:309-325.
28. Ohtsuka T., Hata Y., Ide N., Yasuda T., Inoue E., Inoue T., Mizoguchi A., Takai Y. nRap GEP: A novel neural GDP/GTP exchange protein for rap1 small G protein that interacts with synaptic scaffolding molecule (S-SCAM). Biochem. Biophys. Res. Commun. 1999, 265:38-44.
29. Pak D.T., Sheng M. Targeted protein degradation and synapse remodeling by an inducible protein kinase. Science 2003, 302:1368-1373.
30. Pak D.T., Yang S., Rudolph-Correia S., Kim E., Sheng M. Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 2001, 31:289-303.
31. Pozo K., Goda Y. Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 2010, 66:337-351.
32. Ryu J., Futai K., Feliu M., Weinberg R., Sheng M. Constitutively active Rap2 transgenic mice display fewer dendritic spines, reduced extracellular signal-regulated kinase signaling, enhanced long-term depression, and impaired spatial learning and fear extinction. J. Neurosci. 2008, 28:8178-8188.
33. Seeburg D.P., Sheng M. Activity-induced Polo-like kinase 2 is required for homeostatic plasticity of hippocampal neurons during epileptiform activity. J. Neurosci. 2008, 28:6583-6591.
34. Seeburg D.P., Feliu-Mojer M., Gaiottino J., Pak D.T., Sheng M. Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity. Neuron 2008, 58:571-583.
35. Shepherd J.D., Huganir R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 2007, 23:613-643.
36. Thiagarajan T.C., Piedras-Renteria E.S., Tsien R.W. alpha- and betaCaMKII. Inverse regulation by neuronal activity and opposing effects on synaptic strength. Neuron 2002, 36:1103-1114.
37. Turrigiano G.G. The self-tuning neuron: Synaptic scaling of excitatory synapses. Cell 2008, 135:422-435.
38. Vazquez L.E., Chen H.J., Sokolova I., Knuesel I., Kennedy M.B. SynGAP regulates spine formation. J. Neurosci. 2004, 24:8862-8872.
39. Winkles J.A., Alberts G.F. Differential regulation of polo-like kinase 1, 2, 3, and 4 gene expression in mammalian cells and tissues. Oncogene 2005, 24:260-266.
40. Woolfrey K.M., Srivastava D.P., Photowala H., Yamashita M., Barbolina M.V., Cahill M.E., Xie Z., Jones K.A., Quilliam L.A., Prakriya M., Penzes P. Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat. Neurosci. 2009, 12:1275-1284.
41. Wu G.Y., Deisseroth K., Tsien R.W. Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat. Neurosci. 2001, 4:151-158.
42. Ye X., Carew T.J. Small G protein signaling in neuronal plasticity and memory formation: The specific role of ras family proteins. Neuron 2010, 68:340-361.
43. Zhu J.J., Qin Y., Zhao M., Van Aelst L., Malinow R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 2002, 110:443-455.
44. Zhu Y., Pak D., Qin Y., McCormack S.G., Kim M.J., Baumgart J.P., Velamoor V., Auberson Y.P., Osten P., van Aelst L., et al. Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 2005, 46:905-916.
45. Zwartkruis F.J., Wolthuis R.M., Nabben N.M., Franke B., Bos J.L. Extracellular signal-regulated activation of Rap1 fails to interfere in Ras effector signalling. EMBO J. 1998, 17:5905-5912.