Constitutive activated Cdc42-associated kinase (Ack) phosphorylation at arrested endocytic clathrin-coated pits of cells that lack dynamin

In cells in which clathrin-mediated endocytosis is arrested before fission by depleting dynamin, the major change in tyrosine phosphorylation is the increased phosphorylation/activation of Ack, a tyrosine kinase. Our finding reveals a link between the progression of clathrin-coated pits to endocytic vesicles and an activation-deactivation cycle of Ack.

[1]  A. Dautry‐Varsat,et al.  Receptor-mediated endocytosis: the intracellular journey of transferrin and its receptor. , 1986, Biochimie.

[2]  S. Antonarakis,et al.  Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WASP , 2001, Nature Cell Biology.

[3]  M. von Zastrow,et al.  Structure of an Arrestin2-Clathrin Complex Reveals a Novel Clathrin Binding Domain That Modulates Receptor Trafficking* , 2009, The Journal of Biological Chemistry.

[4]  L. Pelkmans,et al.  Not just a sink: endosomes in control of signal transduction. , 2004, Current opinion in cell biology.

[5]  Matthias Mann,et al.  Mass spectrometric-based approaches in quantitative proteomics. , 2003, Methods.

[6]  P. Camilli,et al.  Endocytosis and Signaling An Inseparable Partnership , 2001, Cell.

[7]  Michael K. Rosen,et al.  Autoinhibition and activation mechanisms of the Wiskott–Aldrich syndrome protein , 2000, Nature.

[8]  J. Kyriakis,et al.  Gene 33 Is an Endogenous Inhibitor of Epidermal Growth Factor (EGF) Receptor Signaling and Mediates Dexamethasone-induced Suppression of EGF Function* , 2005, Journal of Biological Chemistry.

[9]  W. Miller,et al.  Biochemical Properties of the Cdc42-associated Tyrosine Kinase ACK1 , 2003, Journal of Biological Chemistry.

[10]  J. Heuser,et al.  Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation , 1989, The Journal of cell biology.

[11]  A. Miele,et al.  Two distinct interaction motifs in amphiphysin bind two independent sites on the clathrin terminal domain β-propeller , 2004, Nature Structural &Molecular Biology.

[12]  Duilio Cascio,et al.  Regulation of clathrin adaptor function in endocytosis: novel role for the SAM domain , 2010, The EMBO journal.

[13]  R. Cerione,et al.  Cloning and Characterization of a Novel Cdc42-associated Tyrosine Kinase, ACK-2, from Bovine Brain* , 1997, The Journal of Biological Chemistry.

[14]  P. De Camilli,et al.  Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. , 2009, Developmental cell.

[15]  E. C. Dell'Angelica,et al.  Clathrin-binding proteins: got a motif? Join the network! , 2001, Trends in cell biology.

[16]  S. Brenner,et al.  Genetic alterations in the tyrosine kinase transcriptome of human cancer cell lines. , 2007, Cancer research.

[17]  R. Cerione,et al.  The Cdc42 Target ACK2 Directly Interacts with Clathrin and Influences Clathrin Assembly* , 2001, The Journal of Biological Chemistry.

[18]  A. Ullrich,et al.  Mig-6 Is a Negative Regulator of the Epidermal Growth Factor Receptor Signal , 2001, Biological chemistry.

[19]  Wange Lu,et al.  Structure of PAK1 in an Autoinhibited Conformation Reveals a Multistage Activation Switch , 2000, Cell.

[20]  Iva Greenwald,et al.  Crosstalk Between the EGFR and LIN-12/Notch Pathways in C. elegans Vulval Development , 2004, Science.

[21]  P. De Camilli,et al.  Tuba, a Novel Protein Containing Bin/Amphiphysin/Rvs and Dbl Homology Domains, Links Dynamin to Regulation of the Actin Cytoskeleton* , 2003, Journal of Biological Chemistry.

[22]  J. Schlessinger,et al.  Activation of the nonreceptor protein tyrosine kinase Ack by multiple extracellular stimuli. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[23]  P. Mak,et al.  Crystal Structures of the Phosphorylated and Unphosphorylated Kinase Domains of the Cdc42-associated Tyrosine Kinase ACK1* , 2004, Journal of Biological Chemistry.

[24]  E. Peles,et al.  Protein tyrosine kinase PYK2 involved in Ca2+-induced regulation of ion channel and MAP kinase functions , 1995, Nature.

[25]  L. Lim,et al.  A non-receptor tyrosine kinase that inhibits the GTPase activity of p21cdc42 , 1993, Nature.

[26]  Donald Huddler,et al.  Drosophila Ack Targets Its Substrate, the Sorting Nexin DSH3PX1, to a Protein Complex Involved in Axonal Guidance* , 2002, The Journal of Biological Chemistry.

[27]  E. Laue,et al.  Structure of the small G protein Cdc42 bound to the GTPase-binding domain of ACK , 1999, Nature.

[28]  A. Sorkin,et al.  Inhibition of the receptor‐binding function of clathrin adaptor protein AP‐2 by dominant‐negative mutant μ2 subunit and its effects on endocytosis , 1999, The EMBO journal.

[29]  S. Powers,et al.  Metastatic properties and genomic amplification of the tyrosine kinase gene ACK1. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[30]  P. De Camilli,et al.  Tuba, a GEF for CDC42, links dynamin to actin regulatory proteins. , 2005, Methods in enzymology.

[31]  Ron Bose,et al.  Inhibition of the EGF Receptor by Binding to an Activating Kinase Domain Interface , 2007, Nature.

[32]  A. Sorkin,et al.  Endocytosis and signalling: intertwining molecular networks , 2009, Nature Reviews Molecular Cell Biology.

[33]  P. De Camilli,et al.  A PH domain within OCRL bridges clathrin‐mediated membrane trafficking to phosphoinositide metabolism , 2009, The EMBO journal.

[34]  P. Sternberg,et al.  ARK-1 inhibits EGFR signaling in C. elegans. , 2000, Molecular cell.

[35]  Guillermo Ayala,et al.  Loss of endocytic clathrin-coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate , 2007, Proceedings of the National Academy of Sciences.

[36]  S. Schmid,et al.  Regulation of signal transduction by endocytosis. , 2000, Current opinion in cell biology.

[37]  M. Teo,et al.  The Tyrosine Kinase ACK1 Associates with Clathrin-coated Vesicles through a Binding Motif Shared by Arrestin and Other Adaptors* , 2001, The Journal of Biological Chemistry.

[38]  Steven P Gygi,et al.  A probability-based approach for high-throughput protein phosphorylation analysis and site localization , 2006, Nature Biotechnology.

[39]  S. Gygi,et al.  Large-scale identification and evolution indexing of tyrosine phosphorylation sites from murine brain. , 2008, Journal of proteome research.

[40]  T. Kirchhausen,et al.  Role of lipids and actin in the formation of clathrin-coated pits. , 2006, Experimental cell research.

[41]  E. Maspero,et al.  A two-tiered mechanism of EGFR inhibition by RALT/MIG6 via kinase suppression and receptor degradation , 2010, The Journal of cell biology.

[42]  J. Schlessinger Cell Signaling by Receptor Tyrosine Kinases , 2000, Cell.

[43]  M. Sudol,et al.  HECT E3 Ubiquitin Ligase Nedd4-1 Ubiquitinates ACK and Regulates Epidermal Growth Factor (EGF)-Induced Degradation of EGF Receptor and ACK , 2010, Molecular and Cellular Biology.

[44]  Chen Huiping,et al.  Loss of RALT/MIG-6 expression in ERBB2-amplified breast carcinomas enhances ErbB-2 oncogenic potency and favors resistance to Herceptin , 2005, Oncogene.

[45]  L. Lim,et al.  Down-regulation of Active ACK1 Is Mediated by Association with the E3 Ubiquitin Ligase Nedd4-2* , 2009, Journal of Biological Chemistry.

[46]  H. Stenmark,et al.  Endocytosis and signaling. , 2011, Current opinion in cell biology.

[47]  J. Yates,et al.  An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database , 1994, Journal of the American Society for Mass Spectrometry.

[48]  Steven P Gygi,et al.  Signaling networks assembled by oncogenic EGFR and c-Met , 2008, Proceedings of the National Academy of Sciences.

[49]  R. Cerione,et al.  The Cdc42 Target ACK2 Interacts with Sorting Nexin 9 (SH3PX1) to Regulate Epidermal Growth Factor Receptor Degradation* , 2002, The Journal of Biological Chemistry.