AAK1 identified as an inhibitor of neuregulin-1/ErbB4-dependent neurotrophic factor signaling using integrative chemical genomics and proteomics

Chemistry and Biology

Volumn 18, Issue 7, 2011, Pages 891-906

  Kuai, Letian ^a   Ong, Shao En ^b   Madison, Jon M ^a   Wang, Xiang ^b   Duvall, Jeremy R ^b   Lewis, Timothy A ^b   Luce, Catherine J ^a   Conner, Sean D ^c   Pearlman, David A ^a   Wood, John L ^d   Schreiber, Stuart L ^b   Carr, Steven A ^b   Scolnick, Edward M ^a   Haggarty, Stephen J ^a,e  

^a Stanley Center for Psychiatric Research   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d Department of Environmental and Radiological Health Sciences   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AAK1 PROTEIN, RAT; CARBAZOLE DERIVATIVE; EPIDERMAL GROWTH FACTOR RECEPTOR; INDOLE ALKALOID; K 252; NERVE GROWTH FACTOR; NEU DIFFERENTIATION FACTOR; PROTEIN SERINE THREONINE KINASE; RECEPTOR TYROSINE PROTEIN KINASE ERBB 4; RECEPTOR TYROSINE-PROTEIN KINASE ERBB-4;

ANIMAL; ARTICLE; CELL STRAIN; CHEMICAL STRUCTURE; GENE SILENCING; GENETICS; GENOMICS; HUMAN; METABOLISM; METHODOLOGY; NEURITE; PROTEOMICS; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CARBAZOLES; GENE KNOCKDOWN TECHNIQUES; GENOMICS; HUMANS; INDOLE ALKALOIDS; MODELS, MOLECULAR; NERVE GROWTH FACTORS; NEUREGULIN-1; NEURITES; PC12 CELLS; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 79960965515     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2011.03.017     Document Type: Article

References (69)

1. R.S. Al-awar, J.E. Ray, K.A. Hecker, S. Joseph, J. Huang, C. Shih, H.B. Brooks, C.D. Spencer, S.A. Watkins, and R.M. Schultz Preparation of novel aza-1,7-annulated indoles and their conversion to potent indolocarbazole kinase inhibitors Bioorg. Med. Chem. Lett. 14 2004 3925 3928 (Pubitemid 38844397)
2. J. Baulida, M.H. Kraus, M. Alimandi, P.P. Di Fiore, and G. Carpenter All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired J. Biol. Chem. 271 1996 5251 5257 (Pubitemid 26075021)
3. M.M. Berg, D.W. Sternberg, L.F. Parada, and M.V. Chao K-252a inhibits nerve growth factor-induced trk proto-oncogene tyrosine phosphorylation and kinase activity J. Biol. Chem. 267 1992 13 16
4. G.D. Borasio Differential effects of the protein kinase inhibitor K-252a on the in vitro survival of chick embryonic neurons Neurosci. Lett. 108 1990 207 212 (Pubitemid 20036457)
5. T.G. Boulton, S.H. Nye, D.J. Robbins, N.Y. Ip, E. Radziejewska, S.D. Morgenbesser, R.A. DePinho, N. Panayotatos, M.H. Cobb, and G.D. Yancopoulos ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF Cell 65 1991 663 675
6. E.M. Bublil, and Y. Yarden The EGF receptor family: spearheading a merger of signaling and therapeutics Curr. Opin. Cell Biol. 19 2007 124 134 (Pubitemid 46386405)
7. A. Buonanno The neuregulin signaling pathway and schizophrenia: from genes to synapses and neural circuits Brain Res. Bull. 83 2010 122 131
8. K.O. Cho, W.C. Skarnes, B. Minsk, S. Palmieri, L. Jackson-Grusby, and J.A. Wagner Nerve growth factor regulates gene expression by several distinct mechanisms Mol. Cell. Biol. 9 1989 135 143 (Pubitemid 19024787)
9. S.D. Conner, and S.L. Schmid Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis J. Cell Biol. 156 2002 921 929 (Pubitemid 34839873)
10. S.D. Conner, T. Schroter, and S.L. Schmid AAK1-mediated micro2 phosphorylation is stimulated by assembled clathrin Traffic 4 2003 885 890 (Pubitemid 37540590)
11. J. Cox, and M. Mann MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 26 2008 1367 1372
12. J.E. Debreczeni, L. Farkas, V. Harmat, C. Hetenyi, I. Hajdu, P. Zavodszky, K. Kohama, and L. Nyitray Structural evidence for non-canonical binding of Ca2+ to a canonical EF-hand of a conventional myosin J. Biol. Chem. 280 2005 41458 41464 (Pubitemid 41832205)
13. M.A. Fabian, W.H. Biggs 3rd, D.K. Treiber, C.E. Atteridge, M.D. Azimioara, M.G. Benedetti, T.A. Carter, P. Ciceri, P.T. Edeen, and M. Floyd A small molecule-kinase interaction map for clinical kinase inhibitors Nat. Biotechnol. 23 2005 329 336 (Pubitemid 41094421)
14. D.L. Falls Neuregulins: functions, forms, and signaling strategies Exp. Cell Res. 284 2003 14 30 (Pubitemid 36335807)
15. D.E. Gingrich, D.R. Reddy, M.A. Iqbal, J. Singh, L.D. Aimone, T.S. Angeles, M. Albom, S. Yang, M.A. Ator, and S.L. Meyer A new class of potent vascular endothelial growth factor receptor tyrosine kinase inhibitors: structure-activity relationships for a series of 9-alkoxymethyl-12-(3- hydroxypropyl)indeno[2,1-a]pyrrolo[3,4-c]carbazole-5- ones and the identification of CEP-5214 and its dimethylglycine ester prodrug clinical candidate CEP-7055 J. Med. Chem. 46 2003 5375 5388 (Pubitemid 37490370)
16. M.A. Glicksman, J.E. Prantner, S.L. Meyer, M.E. Forbes, M. Dasgupta, M.E. Lewis, and N. Neff K-252a and staurosporine promote choline acetyltransferase activity in rat spinal cord cultures J. Neurochem. 61 1993 210 221 (Pubitemid 23175903)
17. M.A. Glicksman, M.E. Forbes, J.E. Prantner, and N.T. Neff K-252a promotes survival and choline acetyltransferase activity in striatal and basal forebrain neuronal cultures J. Neurochem. 64 1995 1502 1512
18. L.A. Greene, and A.S. Tischler Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor Proc. Natl. Acad. Sci. USA 73 1976 2424 2428
19. P.M. Guy, J.V. Platko, L.C. Cantley, R.A. Cerione, and K.L. Carraway 3rd Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity Proc. Natl. Acad. Sci. USA 91 1994 8132 8136
20. T. Harada, T. Morooka, S. Ogawa, and E. Nishida ERK induces p35, a neuron-specific activator of Cdk5, through induction of Egr1 Nat. Cell Biol. 3 2001 453 459 (Pubitemid 32422080)
21. S. Hashimoto K-252a, a potent protein kinase inhibitor, blocks nerve growth factor-induced neurite outgrowth and changes in the phosphorylation of proteins in PC12h cells J. Cell Biol. 107 1988 1531 1539
22. L.E. Heasley, and G.L. Johnson The beta-PDGF receptor induces neuronal differentiation of PC12 cells Mol. Biol. Cell 3 1992 545 553 (Pubitemid 23079755)
23. D.M. Henderson, and S.D. Conner A novel AAK1 splice variant functions at multiple steps of the endocytic pathway Mol. Biol. Cell 18 2007 2698 2706 (Pubitemid 47025734)
24. M. Kaneko, Y. Saito, H. Saito, T. Matsumoto, Y. Matsuda, J.L. Vaught, C.A. Dionne, T.S. Angeles, M.A. Glicksman, and N.T. Neff Neurotrophic 3,9-bis[(alkylthio)methyl]-and-bis(alkoxymethyl)-K-252a derivatives J. Med. Chem. 40 1997 1863 1869 (Pubitemid 27251276)
25. D.R. Kaplan, D. Martin-Zanca, and L.F. Parada Tyrosine phosphorylation and tyrosine kinase activity of the trk proto-oncogene product induced by NGF Nature 350 1991 158 160 (Pubitemid 21912187)
26. D.R. Kaplan, B.L. Hempstead, D. Martin-Zanca, M.V. Chao, and L.F. Parada The trk proto-oncogene product: a signal transducing receptor for nerve growth factor Science 252 1991 554 558 (Pubitemid 121000451)
27. M.W. Karaman, S. Herrgard, D.K. Treiber, P. Gallant, C.E. Atteridge, B.T. Campbell, K.W. Chan, P. Ciceri, M.I. Davis, and P.T. Edeen A quantitative analysis of kinase inhibitor selectivity Nat. Biotechnol. 26 2008 127 132
28. H. Kase, K. Iwahashi, and Y. Matsuda K-252a, a potent inhibitor of protein kinase C from microbial origin J. Antibiot. (Tokyo) 39 1986 1059 1065 (Pubitemid 16046365)
29. B. Knusel, and F. Hefti K-252 compounds: modulators of neurotrophin signal transduction J. Neurochem. 59 1992 1987 1996
30. S. Koizumi, M.L. Contreras, Y. Matsuda, T. Hama, P. Lazarovici, and G. Guroff K-252a: a specific inhibitor of the action of nerve growth factor on PC 12 cells J. Neurosci. 8 1988 715 721 (Pubitemid 18078094)
31. L. Kuai, X. Wang, J.M. Madison, S.L. Schreiber, E.M. Scolnick, and S.J. Haggarty Chemical genetics identifies small-molecule modulators of neuritogenesis involving neuregulin-1/ErbB4 signaling ACS Chem. Neurosci. 1 2010 325 342
32. G.H. Kuo, C. Prouty, A. DeAngelis, L. Shen, D.J. O'Neill, C. Shah, P.J. Connolly, W.V. Murray, B.R. Conway, and P. Cheung Synthesis and discovery of macrocyclic polyoxygenated bis-7-azaindolylmaleimides as a novel series of potent and highly selective glycogen synthase kinase-3beta inhibitors J. Med. Chem. 46 2003 4021 4031 (Pubitemid 37122448)
33. J.C. Latourelle, N. Pankratz, A. Dumitriu, J.B. Wilk, S. Goldwurm, G. Pezzoli, C.B. Mariani, A.L. DeStefano, C. Halter, and J.F. Gusella Genomewide association study for onset age in Parkinson disease BMC Med. Genet. 10 2009 98
34. P. Lazarovici, B.Z. Levi, P.I. Lelkes, S. Koizumi, K. Fujita, Y. Matsuda, K. Ozato, and G. Guroff K-252a inhibits the increase in c-fos transcription and the increase in intracellular calcium produced by nerve growth factor in PC12 cells J. Neurosci. Res. 23 1989 1 8 (Pubitemid 19167317)
35. Y. Liu, Y.M. Tao, R.S. Woo, W.C. Xiong, and L. Mei Stimulated ErbB4 internalization is necessary for neuregulin signaling in neurons Biochem. Biophys. Res. Commun. 354 2007 505 510 (Pubitemid 46161352)
36. M. Longart, M. Chatani-Hinze, C.M. Gonzalez, D. Vullhorst, and A. Buonanno Regulation of ErbB-4 endocytosis by neuregulin in GABAergic hippocampal interneurons Brain Res. Bull. 73 2007 210 219 (Pubitemid 46880055)
37. A.C. Maroney, L. Lipfert, M.E. Forbes, M.A. Glicksman, N.T. Neff, R. Siman, and C.A. Dionne K-252a induces tyrosine phosphorylation of the focal adhesion kinase and neurite outgrowth in human neuroblastoma SH-SY5Y cells J. Neurochem. 64 1995 540 549
38. L. Mei, and W.C. Xiong Neuregulin 1 in neural development, synaptic plasticity and schizophrenia Nat. Rev. Neurosci. 9 2008 437 452 (Pubitemid 351704944)
39. T. Miyasaka, M.V. Chao, P. Sherline, and A.R. Saltiel Nerve growth factor stimulates a protein kinase in PC-12 cells that phosphorylates microtubule-associated protein-2 J. Biol. Chem. 265 1990 4730 4735
40. J. Moffat, D.A. Grueneberg, X. Yang, S.Y. Kim, A.M. Kloepfer, G. Hinkle, B. Piqani, T.M. Eisenhaure, B. Luo, and J.K. Grenier A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen Cell 124 2006 1283 1298
41. A. Morotti, S. Mila, P. Accornero, E. Tagliabue, and C. Ponzetto K252a inhibits the oncogenic properties of Met, the HGF receptor Oncogene 21 2002 4885 4893
42. C. Murakata, M. Kaneko, G. Gessner, T.S. Angeles, M.A. Ator, T.M. O'Kane, B.A. McKenna, B.A. Thomas, J.R. Mathiasen, and M.S. Saporito Mixed lineage kinase activity of indolocarbazole analogues Bioorg. Med. Chem. Lett. 12 2002 147 150 (Pubitemid 34037954)
43. S.H. Nye, S.P. Squinto, D.J. Glass, T.N. Stitt, P. Hantzopoulos, M.J. Macchi, N.S. Lindsay, N.Y. Ip, and G.D. Yancopoulos K-252a and staurosporine selectively block autophosphorylation of neurotrophin receptors and neurotrophin-mediated responses Mol. Biol. Cell 3 1992 677 686 (Pubitemid 23098266)
44. K.K. Ojo, J.R. Gillespie, A.J. Riechers, A.J. Napuli, C.L. Verlinde, F.S. Buckner, M.H. Gelb, M.M. Domostoj, S.J. Wells, and A. Scheer Glycogen synthase kinase 3 is a potential drug target for African trypanosomiasis therapy Antimicrob. Agents Chemother. 52 2008 3710 3717
45. O. Olusanya, P.D. Andrews, J.R. Swedlow, and E. Smythe Phosphorylation of threonine 156 of the mu2 subunit of the AP2 complex is essential for endocytosis in vitro and in vivo Curr. Biol. 11 2001 896 900 (Pubitemid 32532818)
46. S.E. Ong, and M. Mann A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC) Nat. Protoc. 1 2006 2650 2660
47. S.E. Ong, B. Blagoev, I. Kratchmarova, D.B. Kristensen, H. Steen, A. Pandey, and M. Mann Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 1 2002 376 386
48. S.E. Ong, M. Schenone, A.A. Margolin, X. Li, K. Do, M.K. Doud, D.R. Mani, L. Kuai, X. Wang, and J.L. Wood Identifying the proteins to which small-molecule probes and drugs bind in cells Proc. Natl. Acad. Sci. USA 106 2009 4617 4622
49. D. Pearlman Free energy calculations: methods and applications B.G. Rao, The Encyclopedia of Computational Chemistry 1998 John Wiley & Sons New York 1036 1061
50. S. Pollack, L. Young, J. Bilsland, N. Wilkie, S. Ellis, F. Hefti, H. Broughton, and S. Harper The staurosporine-like compound L-753,000 (NB-506) potentiates the neurotrophic effects of neurotrophin-3 by acting selectively at the TrkA receptor Mol. Pharmacol. 56 1999 185 195 (Pubitemid 29309828)
51. J. Rappsilber, M. Mann, and Y. Ishihama Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips Nat. Protoc. 2 2007 1896 1906 (Pubitemid 47308128)
52. D. Ricotta, S.D. Conner, S.L. Schmid, K. von Figura, and S. Honing Phosphorylation of the AP2 mu subunit by AAK1 mediates high affinity binding to membrane protein sorting signals J. Cell Biol. 156 2002 791 795 (Pubitemid 34839862)
53. P.P. Roux, G. Dorval, M. Boudreau, A. Angers-Loustau, S.J. Morris, J. Makkerh, and P.A. Barker K252a and CEP1347 are neuroprotective compounds that inhibit mixed-lineage kinase-3 and induce activation of Akt and ERK J. Biol. Chem. 277 2002 49473 49480 (Pubitemid 36014383)
54. U.T. Ruegg, and G.M. Burgess Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors of protein kinases Trends Pharmacol. Sci. 10 1989 218 220 (Pubitemid 19146392)
55. C. Sanchez, C. Mendez, and J.A. Salas Indolocarbazole natural products: occurrence, biosynthesis, and biological activity Nat. Prod. Rep. 23 2006 1007 1045 (Pubitemid 44808996)
56. N. Schiering, S. Knapp, M. Marconi, M.M. Flocco, J. Cui, R. Perego, L. Rusconi, and C. Cristiani Crystal structure of the tyrosine kinase domain of the hepatocyte growth factor receptor c-Met and its complex with the microbial alkaloid K-252a Proc. Natl. Acad. Sci. USA 100 2003 12654 12659 (Pubitemid 37339954)
57. D.S. Smith, C.S. King, E. Pearson, C.K. Gittinger, and G.E. Landreth Selective inhibition of nerve growth factor-stimulated protein kinases by K-252a and 5′-S-methyladenosine in PC12 cells J. Neurochem. 53 1989 800 806 (Pubitemid 19207376)
58. E. Smythe, and K.R. Ayscough The Ark1/Prk1 family of protein kinases. Regulators of endocytosis and the actin skeleton EMBO Rep. 4 2003 246 251 (Pubitemid 36511719)
59. A. Sorkin, and L.K. Goh Endocytosis and intracellular trafficking of ErbBs Exp. Cell Res. 314 2008 3093 3106
60. B.R. Stockwell Chemical genetics: ligand-based discovery of gene function Nat. Rev. 1 2000 116 125
61. M. Sundvall, A. Korhonen, I. Paatero, E. Gaudio, G. Melino, C.M. Croce, R.I. Aqeilan, and K. Elenius Isoform-specific monoubiquitination, endocytosis, and degradation of alternatively spliced ErbB4 isoforms Proc. Natl. Acad. Sci. USA 105 2008 4162 4167 (Pubitemid 351754351)
62. P. Tapley, F. Lamballe, and M. Barbacid K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors Oncogene 7 1992 371 381
63. S. Traverse, N. Gomez, H. Paterson, C. Marshall, and P. Cohen Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor Biochem. J. 288 1992 351 355
64. E. Tzahar, G. Levkowitz, D. Karunagaran, L. Yi, E. Peles, S. Lavi, D. Chang, N. Liu, A. Yayon, and D. Wen ErbB-3 and ErbB-4 function as the respective low and high affinity receptors of all Neu differentiation factor/heregulin isoforms J. Biol. Chem. 269 1994 25226 25233 (Pubitemid 24311798)
65. X. Wang, B.S. Imber, and S.L. Schreiber Small-molecule reagents for cellular pull-down experiments Bioconjug. Chem. 19 2008 585 587 (Pubitemid 351431387)
66. L. Wen, Y.S. Lu, X.H. Zhu, X.M. Li, R.S. Woo, Y.J. Chen, D.M. Yin, C. Lai, A.V. Terry Jr. , and A. Vazdarjanova Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons Proc. Natl. Acad. Sci. USA 107 2010 1211 1216
67. R.S. Woo, X.M. Li, Y. Tao, E. Carpenter-Hyland, Y.Z. Huang, J. Weber, H. Neiswender, X.P. Dong, J. Wu, and M. Gassmann Neuregulin-1 enhances depolarization-induced GABA release Neuron 54 2007 599 610 (Pubitemid 46756135)
68. X.L. Yang, Y.Z. Huang, W.C. Xiong, and L. Mei Neuregulin-induced expression of the acetylcholine receptor requires endocytosis of ErbB receptors Mol. Cell. Neurosci. 28 2005 335 346 (Pubitemid 40202594)
69. H.C. Zhang, C.K. Derian, D.F. McComsey, K.B. White, H. Ye, L.R. Hecker, J. Li, M.F. Addo, D. Croll, and A.J. Eckardt Novel indolylindazolylmaleimides as inhibitors of protein kinase C-beta: synthesis, biological activity, and cardiovascular safety J. Med. Chem. 48 2005 1725 1728 (Pubitemid 40396306)