Chemical Genetic Identification of NDR1/2 Kinase Substrates AAK1 and Rabin8 Uncovers Their Roles in Dendrite Arborization and Spine Development

Neuron

Volumn 73, Issue 6, 2012, Pages 1127-1142

  Ultanir, Sila K ^a   Hertz, Nicholas T ^a,b   Li, Guangnan ^b   Ge, Woo Ping ^a   Burlingame, Alma L ^a   Pleasure, Samuel J ^b   Shokat, Kevan M ^a,b   Jan, Lily Yeh ^a,b   Jan, Yuh Nung ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; PHOSPHOTRANSFERASE; PROTEIN AP 2 ASSOCIATED KINASE; PROTEIN RABIN8; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; ENZYME SUBSTRATE; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE MUTATION; GENE TARGETING; IN VIVO STUDY; MARKER GENE; NDR 1 KINASE GENE; NDR 2 KINASE GENE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RAT; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TRANSPORT VESICLE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; AUTOANTIGENS; CELLS, CULTURED; DENDRITES; DENDRITIC SPINES; ELECTROPORATION; EMBRYO, MAMMALIAN; EXCITATORY POSTSYNAPTIC POTENTIALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HIPPOCAMPUS; HUMANS; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTATION; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, LONG-EVANS; RNA, SMALL INTERFERING; SYNAPSES; TRANSFECTION;

EID: 84863347402     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.01.019     Document Type: Article

References (59)

1. Allen J.J., Li M., Brinkworth C.S., Paulson J.L., Wang D., Hübner A., Chou W.H., Davis R.J., Burlingame A.L., Messing R.O., et al. A semisynthetic epitope for kinase substrates. Nat. Methods 2007, 4:511-516.
2. Bichsel S.J., Tamaskovic R., Stegert M.R., Hemmings B.A. Mechanism of activation of NDR (nuclear Dbf2-related) protein kinase by the hMOB1 protein. J. Biol. Chem. 2004, 279:35228-35235.
3. Bishop A.C., Ubersax J.A., Petsch D.T., Matheos D.P., Gray N.S., Blethrow J., Shimizu E., Tsien J.Z., Schultz P.G., Rose M.D., et al. A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 2000, 407:395-401.
4. Blethrow J.D., Glavy J.S., Morgan D.O., Shokat K.M. Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc. Natl. Acad. Sci. USA 2008, 105:1442-1447.
5. Brondyk W.H., McKiernan C.J., Fortner K.A., Stabila P., Holz R.W., Macara I.G. Interaction cloning of Rabin3, a novel protein that associates with the Ras-like GTPase Rab3A. Mol. Cell. Biol. 1995, 15:1137-1143.
6. Brown T.C., Correia S.S., Petrok C.N., Esteban J.A. Functional compartmentalization of endosomal trafficking for the synaptic delivery of AMPA receptors during long-term potentiation. J. Neurosci. 2007, 27:13311-13315.
7. Cong J., Geng W., He B., Liu J., Charlton J., Adler P.N. The furry gene of Drosophila is important for maintaining the integrity of cellular extensions during morphogenesis. Development 2001, 128:2793-2802.
8. Conner S.D., Schmid S.L. Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J. Cell Biol. 2002, 156:921-929.
9. Conner S.D., Schmid S.L. Differential requirements for AP-2 in clathrin-mediated endocytosis. J. Cell Biol. 2003, 162:773-779.
10. Cornils H., Stegert M.R., Hergovich A., Hynx D., Schmitz D., Dirnhofer S., Hemmings B.A. Ablation of the kinase NDR1 predisposes mice to the development of T cell lymphoma. Sci. Signal. 2010, 3:ra47.
11. Cornils H., Kohler R.S., Hergovich A., Hemmings B.A. Human NDR kinases control G(1)/S cell cycle transition by directly regulating p21 stability. Mol. Cell. Biol. 2011, 31:1382-1395.
12. De Matteis M.A., Di Campli A., Godi A. The role of the phosphoinositides at the Golgi complex. Biochim. Biophys. Acta 2005, 1744:396-405.
13. Devroe E., Erdjument-Bromage H., Tempst P., Silver P.A. Human Mob proteins regulate the NDR1 and NDR2 serine-threonine kinases. J. Biol. Chem. 2004, 279:24444-24451.
14. Emoto K., He Y., Ye B., Grueber W.B., Adler P.N., Jan L.Y., Jan Y.N. Control of dendritic branching and tiling by the Tricornered-kinase/Furry signaling pathway in Drosophila sensory neurons. Cell 2004, 119:245-256.
15. Emoto K., Parrish J.Z., Jan L.Y., Jan Y.N. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 2006, 443:210-213.
16. Fiala J.C., Feinberg M., Popov V., Harris K.M. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 1998, 18:8900-8911.
17. Gallegos M.E., Bargmann C.I. Mechanosensory neurite termination and tiling depend on SAX-2 and the SAX-1 kinase. Neuron 2004, 44:239-249.
18. Geng W., He B., Wang M., Adler P.N. The tricornered gene, which is required for the integrity of epidermal cell extensions, encodes the Drosophila nuclear DBF2-related kinase. Genetics 2000, 156:1817-1828.
19. Gerges N.Z., Backos D.S., Esteban J.A. Local control of AMPA receptor trafficking at the postsynaptic terminal by a small GTPase of the Rab family. J. Biol. Chem. 2004, 279:43870-43878.
20. Gupta-Rossi N., Ortica S., Meas-Yedid V., Heuss S., Moretti J., Olivo-Marin J.C., Israël A. The adaptor-associated kinase 1, AAK1, is a positive regulator of the Notch pathway. J. Biol. Chem. 2011, 286:18720-18730.
21. Han C., Wang D., Soba P., Zhu S., Lin X., Jan L.Y., Jan Y.N. Integrins regulate repulsion-mediated dendritic patterning of drosophila sensory neurons by restricting dendrites in a 2D space. Neuron 2012, 73:64-78.
22. Harris K.M. Structure, development, and plasticity of dendritic spines. Curr. Opin. Neurobiol. 1999, 9:343-348.
23. Hattula K., Furuhjelm J., Arffman A., Peränen J. A Rab8-specific GDP/GTP exchange factor is involved in actin remodeling and polarized membrane transport. Mol. Biol. Cell 2002, 13:3268-3280.
24. Henderson D.M., Conner S.D. A novel AAK1 splice variant functions at multiple steps of the endocytic pathway. Mol. Biol. Cell 2007, 18:2698-2706.
25. Hergovich A., Stegert M.R., Schmitz D., Hemmings B.A. NDR kinases regulate essential cell processes from yeast to humans. Nat. Rev. Mol. Cell Biol. 2006, 7:253-264.
26. Hertz N.T., Wang B.T., Allen J.J., Zhang C., Dar A.C., Burlingame A.L., Shokat K.M. Chemical genetic approach for kinase-substrate mapping by covalent capture of thiophosphopeptides and analysis by mass spectrometry. Curr Protoc Chem Biol. 2010, V2:15-36.
27. Horgan C.P., McCaffrey M.W. The dynamic Rab11-FIPs. Biochem. Soc. Trans. 2009, 37:1032-1036.
28. Horton A.C., Rácz B., Monson E.E., Lin A.L., Weinberg R.J., Ehlers M.D. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 2005, 48:757-771.
29. Jan Y.N., Jan L.Y. Branching out: mechanisms of dendritic arborization. Nat. Rev. Neurosci. 2010, 11:316-328.
30. Jansen J.M., Wanless A.G., Seidel C.W., Weiss E.L. Cbk1 regulation of the RNA-binding protein Ssd1 integrates cell fate with translational control. Curr. Biol. 2009, 19:2114-2120.
31. Koike-Kumagai M., Yasunaga K., Morikawa R., Kanamori T., Emoto K. The target of rapamycin complex 2 controls dendritic tiling of Drosophila sensory neurons through the Tricornered kinase signalling pathway. EMBO J. 2009, 28:3879-3892.
32. Konur S., Yuste R. Developmental regulation of spine and filopodial motility in primary visual cortex: reduced effects of activity and sensory deprivation. J. Neurobiol. 2004, 59:236-246.
33. Kuai L., Ong S.E., Madison J.M., Wang X., Duvall J.R., Lewis T.A., Luce C.J., Conner S.D., Pearlman D.A., Wood J.L., et al. AAK1 identified as an inhibitor of neuregulin-1/ErbB4-dependent neurotrophic factor signaling using integrative chemical genomics and proteomics. Chem. Biol. 2011, 18:891-906.
34. Kuo C.T., Zhu S., Younger S., Jan L.Y., Jan Y.N. Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 2006, 51:283-290.
35. Kurischko C., Kuravi V.K., Wannissorn N., Nazarov P.A., Husain M., Zhang C., Shokat K.M., McCaffery J.M., Luca F.C. The yeast LATS/Ndr kinase Cbk1 regulates growth via Golgi-dependent glycosylation and secretion. Mol. Biol. Cell 2008, 19:5559-5578.
36. Li Z., Jo J., Jia J.M., Lo S.C., Whitcomb D.J., Jiao S., Cho K., Sheng M. Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 2010, 141:859-871.
37. MacVicar B.A., Thompson R.J. Non-junction functions of pannexin-1 channels. Trends Neurosci. 2010, 33:93-102.
38. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2001, 4:1086-1092.
39. Mazanka E., Alexander J., Yeh B.J., Charoenpong P., Lowery D.M., Yaffe M., Weiss E.L. The NDR/LATS family kinase Cbk1 directly controls transcriptional asymmetry. PLoS Biol. 2008, 6:e203.
40. Millward T.A., Hess D., Hemmings B.A. Ndr protein kinase is regulated by phosphorylation on two conserved sequence motifs. J. Biol. Chem. 1999, 274:33847-33850.
41. Nelson B., Kurischko C., Horecka J., Mody M., Nair P., Pratt L., Zougman A., McBroom L.D., Hughes T.R., Boone C., Luca F.C. RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. Mol. Biol. Cell 2003, 14:3782-3803.
42. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annu. Rev. Physiol. 2002, 64:313-353.
43. Penzes P., Cahill M.E., Jones K.A., VanLeeuwen J.E., Woolfrey K.M. Dendritic spine pathology in neuropsychiatric disorders. Nat. Neurosci. 2011, 14:285-293.
44. Ramocki M.B., Zoghbi H.Y. Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 2008, 455:912-918.
45. Robinson M.S. Adaptable adaptors for coated vesicles. Trends Cell Biol. 2004, 14:167-174.
46. Sekiya-Kawasaki M., Groen A.C., Cope M.J., Kaksonen M., Watson H.A., Zhang C., Shokat K.M., Wendland B., McDonald K.L., McCaffery J.M., Drubin D.G. Dynamic phosphoregulation of the cortical actin cytoskeleton and endocytic machinery revealed by real-time chemical genetic analysis. J. Cell Biol. 2003, 162:765-772.
47. Shah K., Liu Y., Deirmengian C., Shokat K.M. Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates. Proc. Natl. Acad. Sci. USA 1997, 94:3565-3570.
48. Stegert M.R., Tamaskovic R., Bichsel S.J., Hergovich A., Hemmings B.A. Regulation of NDR2 protein kinase by multi-site phosphorylation and the S100B calcium-binding protein. J. Biol. Chem. 2004, 279:23806-23812.
49. Stegert M.R., Hergovich A., Tamaskovic R., Bichsel S.J., Hemmings B.A. Regulation of NDR protein kinase by hydrophobic motif phosphorylation mediated by the mammalian Ste20-like kinase MST3. Mol. Cell. Biol. 2005, 25:11019-11029.
50. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 2009, 10:513-525.
51. Stork O., Zhdanov A., Kudersky A., Yoshikawa T., Obata K., Pape H.C. Neuronal functions of the novel serine/threonine kinase Ndr2. J. Biol. Chem. 2004, 279:45773-45781.
52. Toshima J., Toshima J.Y., Martin A.C., Drubin D.G. Phosphoregulation of Arp2/3-dependent actin assembly during receptor-mediated endocytosis. Nat. Cell Biol. 2005, 7:246-254.
53. Vichalkovski A., Gresko E., Cornils H., Hergovich A., Schmitz D., Hemmings B.A. NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis. Curr. Biol. 2008, 18:1889-1895.
54. Wang Z., Edwards J.G., Riley N., Provance D.W., Karcher R., Li X.D., Davison I.G., Ikebe M., Mercer J.A., Kauer J.A., Ehlers M.D. Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 2008, 135:535-548.
55. Williams D.W., Kondo S., Krzyzanowska A., Hiromi Y., Truman J.W. Local caspase activity directs engulfment of dendrites during pruning. Nat. Neurosci. 2006, 9:1234-1236.
56. Yang W.K., Peng Y.H., Li H., Lin H.C., Lin Y.C., Lai T.T., Suo H., Wang C.H., Lin W.H., Ou C.Y., et al. Nak regulates localization of clathrin sites in higher-order dendrites to promote local dendrite growth. Neuron 2011, 72:285-299.
57. Ye B., Zhang Y., Song W., Younger S.H., Jan L.Y., Jan Y.N. Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 2007, 130:717-729.
58. Yuste R., Bonhoeffer T. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat. Rev. Neurosci. 2004, 5:24-34.
59. Zhang C., Kenski D.M., Paulson J.L., Bonshtien A., Sessa G., Cross J.V., Templeton D.J., Shokat K.M. A second-site suppressor strategy for chemical genetic analysis of diverse protein kinases. Nat. Methods 2005, 2:435-441.