Cortactin Is a Substrate of Activated Cdc42-Associated Kinase 1 (ACK1) during Ligand-induced Epidermal Growth Factor Receptor Downregulation

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Kelley, Laura C ^a,b   Weed, Scott A ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; ACTIVATED CDC42 ASSOCIATED KINASE 1; CORTACTIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PHOSPHOTRANSFERASE; PROTEIN SH3; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL VACUOLE; CONTROLLED STUDY; ENZYME SUBSTRATE; IN VITRO STUDY; INTERNALIZATION; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR DOWN REGULATION;

CDC42 GTP-BINDING PROTEIN; CORTACTIN; CYTOPLASMIC VESICLES; DOWN-REGULATION; ENZYME ACTIVATION; HUMANS; LIGANDS; PHOSPHORYLATION; PHOSPHOTYROSINE; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEIN-TYROSINE KINASES; PROTEOLYSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SRC HOMOLOGY DOMAINS; SUBSTRATE SPECIFICITY;

EID: 84865606987     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044363     Document Type: Article

References (80)

1. Le Roy C, Wrana JL, (2005) Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 6: 112-126.
2. Sorkin A, Goh LK, (2009) Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 315: 683-696.
3. Jiang X, Huang F, Marusyk A, Sorkin A, (2003) Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol Biol Cell 14: 858-870.
4. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, et al. (1998) c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev 12: 3663-3674.
5. Goh LK, Huang F, Kim W, Gygi S, Sorkin A, (2010) Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J Cell Biol 189: 871-883.
6. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, et al. (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci U S A 102: 2760-2765.
7. Yamazaki T, Zaal K, Hailey D, Presley J, Lippincott-Schwartz J, et al. (2002) Role of Grb2 in EGF-stimulated EGFR internalization. J Cell Sci 115: 1791-1802.
8. Orth JD, Krueger EW, Weller SG, McNiven MA, (2006) A novel endocytic mechanism of epidermal growth factor receptor sequestration and internalization. Cancer Res 66: 3603-3610.
9. Hynes NE, MacDonald G, (2009) ErbB receptors and signaling pathways in cancer. Curr Opin Cell Biol 21: 177-184.
10. Kalyankrishna S, Grandis JR, (2006) Epidermal growth factor receptor biology in head and neck cancer. J Clin Oncol 24: 2666-2672.
11. Ware MF, Tice DA, Parsons SJ, Lauffenburger DA, (1997) Overexpression of cellular Src in fibroblasts enhances endocytic internalization of epidermal growth factor receptor. J Biol Chem 272: 30185-30190.
12. Tanos B, Pendergast AM, (2006) Abl tyrosine kinase regulates endocytosis of the epidermal growth factor receptor. J Biol Chem 281: 32714-32723.
13. Prieto-Echague V, Miller WT, (2011) Regulation of ack-family nonreceptor tyrosine kinases. J Signal Transduct 2011: 742372.
14. Galisteo ML, Yang Y, Urena J, Schlessinger J, (2006) Activation of the nonreceptor protein tyrosine kinase Ack by multiple extracellular stimuli. Proc Natl Acad Sci U S A 103: 9796-9801.
15. Shen F, Lin Q, Gu Y, Childress C, Yang W, (2007) Activated Cdc42-associated kinase 1 is a component of EGF receptor signaling complex and regulates EGF receptor degradation. Mol Biol Cell 18: 732-742.
16. Teo M, Tan L, Lim L, Manser E, (2001) The tyrosine kinase ACK1 associates with clathrin-coated vesicles through a binding motif shared by arrestin and other adaptors. J Biol Chem 276: 18392-18398.
17. Shen H, Ferguson SM, Dephoure N, Park R, Yang Y, et al. (2011) Constitutive activated Cdc42-associated kinase (Ack) phosphorylation at arrested endocytic clathrin-coated pits of cells that lack dynamin. Mol Biol Cell 22: 493-502.
18. Grovdal LM, Johannessen LE, Rodland MS, Madshus IH, Stang E, (2008) Dysregulation of Ack1 inhibits down-regulation of the EGF receptor. Exp Cell Res 314: 1292-1300.
19. Howlin J, Rosenkvist J, Andersson T, (2008) TNK2 preserves epidermal growth factor receptor expression on the cell surface and enhances migration and invasion of human breast cancer cells. Breast Cancer Res 10: R36.
20. Lin Q, Lo CG, Cerione RA, Yang W, (2002) The Cdc42 target ACK2 interacts with sorting nexin 9 (SH3PX1) to regulate epidermal growth factor receptor degradation. J Biol Chem 277: 10134-10138.
21. Chan W, Tian R, Lee YF, Sit ST, Lim L, et al. (2009) Down-regulation of active ACK1 is mediated by association with the E3 ubiquitin ligase Nedd4-2. J Biol Chem 284: 8185-8194.
22. Chua BT, Lim SJ, Tham SC, Poh WJ, Ullrich A, (2010) Somatic mutation in the ACK1 ubiquitin association domain enhances oncogenic signaling through EGFR regulation in renal cancer derived cells. Mol Oncol 4: 323-334.
23. Lin Q, Wang J, Childress C, Sudol M, Carey DJ, et al. (2010) HECT E3 ubiquitin ligase Nedd4-1 ubiquitinates ACK and regulates epidermal growth factor (EGF)-induced degradation of EGF receptor and ACK. Mol Cell Biol 30: 1541-1554.
24. Schafer DA, (2002) Coupling actin dynamics and membrane dynamics during endocytosis. Curr Opin Cell Biol 14: 76-81.
25. Qualmann B, Kessels MM, Kelly RB, (2000) Molecular links between endocytosis and the actin cytoskeleton. J Cell Biol 150: F111-116.
26. Pollard TD, (2007) Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 36: 451-477.
27. Rottner K, Hanisch J, Campellone KG, (2010) WASH, WHAMM and JMY: regulation of Arp2/3 complex and beyond. Trends Cell Biol 20: 650-661.
28. Merrifield CJ, Perrais D, Zenisek D, (2005) Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121: 593-606.
29. Cao H, Orth JD, Chen J, Weller SG, Heuser JE, et al. (2003) Cortactin is a component of clathrin-coated pits and participates in receptor-mediated endocytosis. Mol Cell Biol 23: 2162-2170.
30. Kaksonen M, Peng HB, Rauvala H, (2000) Association of cortactin with dynamic actin in lamellipodia and on endosomal vesicles. J Cell Sci 113 Pt 24: 4421-4426.
31. McNiven MA, Kim L, Krueger EW, Orth JD, Cao H, et al. (2000) Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151: 187-198.
32. Zhu J, Zhou K, Hao JJ, Liu J, Smith N, et al. (2005) Regulation of cortactin/dynamin interaction by actin polymerization during the fission of clathrin-coated pits. J Cell Sci 118: 807-817.
33. Zhu J, Yu D, Zeng XC, Zhou K, Zhan X, (2007) Receptor-mediated endocytosis involves tyrosine phosphorylation of cortactin. J Biol Chem 282: 16086-16094.
34. Cao H, Chen J, Krueger EW, McNiven MA, (2010) SRC-mediated phosphorylation of dynamin and cortactin regulates the "constitutive" endocytosis of transferrin. Mol Cell Biol 30: 781-792.
35. Tehrani S, Tomasevic N, Weed S, Sakowicz R, Cooper JA, (2007) Src phosphorylation of cortactin enhances actin assembly. Proc Natl Acad Sci U S A 104: 11933-11938.
36. Boyle SN, Michaud GA, Schweitzer B, Predki PF, Koleske AJ, (2007) A critical role for cortactin phosphorylation by Abl-family kinases in PDGF-induced dorsal-wave formation. Curr Biol 17: 445-451.
37. Le Clainche C, Pauly BS, Zhang CX, Engqvist-Goldstein AE, Cunningham K, et al. (2007) A Hip1R-cortactin complex negatively regulates actin assembly associated with endocytosis. EMBO J 26: 1199-1210.
38. Stoorvogel W, Kerstens S, Fritzsche I, den Hartigh JC, Oud R, et al. (2004) Sorting of ligand-activated epidermal growth factor receptor to lysosomes requires its actin-binding domain. J Biol Chem 279: 11562-11569.
39. Lynch DK, Winata SC, Lyons RJ, Hughes WE, Lehrbach GM, et al. (2003) A Cortactin-CD2-associated protein (CD2AP) complex provides a novel link between epidermal growth factor receptor endocytosis and the actin cytoskeleton. J Biol Chem 278: 21805-21813.
40. Timpson P, Lynch DK, Schramek D, Walker F, Daly RJ, (2005) Cortactin overexpression inhibits ligand-induced down-regulation of the epidermal growth factor receptor. Cancer Res 65: 3273-3280.
41. Sacks PG, Parnes SM, Gallick GE, Mansouri Z, Lichtner R, et al. (1988) Establishment and characterization of two new squamous cell carcinoma cell lines derived from tumors of the head and neck. Cancer Res 48: 2858-2866.
42. Singh B, Gogineni SK, Sacks PG, Shaha AR, Shah JP, et al. (2001) Molecular cytogenetic characterization of head and neck squamous cell carcinoma and refinement of 3q amplification. Cancer Res 61: 4506-4513.
43. Rothschild BL, Shim AH, Ammer AG, Kelley LC, Irby KB, et al. (2006) Cortactin overexpression regulates actin-related protein 2/3 complex activity, motility, and invasion in carcinomas with chromosome 11q13 amplification. Cancer Res 66: 8017-8025.
44. Olson MF, Pasteris NG, Gorski JL, Hall A, (1996) Faciogenital dysplasia protein (FGD1) and Vav, two related proteins required for normal embryonic development, are upstream regulators of Rho GTPases. Curr Biol 6: 1628-1633.
45. Weed SA, Karginov AV, Schafer DA, Weaver AM, Kinley AW, et al. (2000) Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J Cell Biol 151: 29-40.
46. Du Y, Weed SA, Xiong WC, Marshall TD, Parsons JT, (1998) Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons. Mol Cell Biol 18: 5838-5851.
47. Kelley LC, Ammer AG, Hayes KE, Martin KH, Machida K, et al. (2010) Oncogenic Src requires a wild-type counterpart to regulate invadopodia maturation. J Cell Sci 123: 3923-3932.
48. Kinley AW, Weed SA, Weaver AM, Karginov AV, Bissonette E, et al. (2003) Cortactin interacts with WIP in regulating Arp2/3 activation and membrane protrusion. Curr Biol 13: 384-393.
49. Sheffield P, Garrard S, Derewenda Z, (1999) Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Protein Expr Purif 15: 34-39.
50. Head JA, Jiang D, Li M, Zorn LJ, Schaefer EM, et al. (2003) Cortactin tyrosine phosphorylation requires Rac1 activity and association with the cortical actin cytoskeleton. Mol Biol Cell 14: 3216-3229.
51. Wu H, Reynolds AB, Kanner SB, Vines RR, Parsons JT, (1991) Identification and characterization of a novel cytoskeleton-associated pp60src substrate. Mol Cell Biol 11: 5113-5124.
52. Kelley LC, Hayes KE, Ammer AG, Martin KH, Weed SA, (2010) Cortactin phosphorylated by ERK1/2 localizes to sites of dynamic actin regulation and is required for carcinoma lamellipodia persistence. PLoS One 5: e13847.
53. Manser E, Leung T, Salihuddin H, Tan L, Lim L, (1993) A non-receptor tyrosine kinase that inhibits the GTPase activity of p21cdc42. Nature 363: 364-367.
54. Kato-Stankiewicz J, Ueda S, Kataoka T, Kaziro Y, Satoh T, (2001) Epidermal growth factor stimulation of the ACK1/Dbl pathway in a Cdc42 and Grb2-dependent manner. Biochem Biophys Res Commun 284: 470-477.
55. Yokoyama N, Miller WT, (2003) Biochemical properties of the Cdc42-associated tyrosine kinase ACK1. Substrate specificity, authphosphorylation, and interaction with Hck. J Biol Chem 278: 47713-47723.
56. Ammer AG, Weed SA, (2008) Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil Cytoskeleton 65: 687-707.
57. Oser M, Yamaguchi H, Mader CC, Bravo-Cordero JJ, Arias M, et al. (2009) Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J Cell Biol 186: 571-587.
58. Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC, (2006) Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res 66: 3034-3043.
59. Campbell DH, Sutherland RL, Daly RJ, (1999) Signaling pathways and structural domains required for phosphorylation of EMS1/cortactin. Cancer Res 59: 5376-5385.
60. Martinez-Quiles N, Ho HY, Kirschner MW, Ramesh N, Geha RS, (2004) Erk/Src phosphorylation of cortactin acts as a switch on-switch off mechanism that controls its ability to activate N-WASP. Mol Cell Biol 24: 5269-5280.
61. Eden ER, White IJ, Futter CE, (2009) Down-regulation of epidermal growth factor receptor signalling within multivesicular bodies. Biochem Soc Trans 37: 173-177.
62. Ohashi E, Tanabe K, Henmi Y, Mesaki K, Kobayashi Y, et al. (2011) Receptor Sorting within Endosomal Trafficking Pathway Is Facilitated by Dynamic Actin Filaments. PLoS One 6: e19942.
63. Hussain NK, Jenna S, Glogauer M, Quinn CC, Wasiak S, et al. (2001) Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WASP. Nat Cell Biol 3: 927-932.
64. Huang C, Liu J, Haudenschild CC, Zhan X, (1998) The role of tyrosine phosphorylation of cortactin in the locomotion of endothelial cells. J Biol Chem 273: 25770-25776.
65. Kapus A, Di Ciano C, Sun J, Zhan X, Kim L, et al. (2000) Cell volume-dependent phosphorylation of proteins of the cortical cytoskeleton and cell-cell contact sites. The role of Fyn and FER kinases. J Biol Chem 275: 32289-32298.
66. Crostella L, Lidder S, Williams R, Skouteris GG, (2001) Hepatocyte Growth Factor/scatter factor-induces phosphorylation of cortactin in A431 cells in a Src kinase-independent manner. Oncogene 20: 3735-3745.
67. Huang J, Asawa T, Takato T, Sakai R, (2003) Cooperative roles of Fyn and cortactin in cell migration of metastatic murine melanoma. J Biol Chem 278: 48367-48376.
68. Garcia-Castillo J, Pedersen K, Angelini PD, Bech-Serra JJ, Colome N, et al. (2009) HER2 carboxyl-terminal fragments regulate cell migration and cortactin phosphorylation. J Biol Chem 284: 25302-25313.
69. Kasai A, Shima T, Okada M, (2005) Role of Src family tyrosine kinases in the down-regulation of epidermal growth factor signaling in PC12 cells. Genes Cells 10: 1175-1187.
70. Chan W, Sit ST, Manser E (2011) The Cdc42-associated kinase ACK1 is not auto-inhibited but requires Src for activation. Biochem J.
71. Stuible M, Dube N, Tremblay ML, (2008) PTP1B regulates cortactin tyrosine phosphorylation by targeting Tyr446. J Biol Chem 283: 15740-15746.
72. Yokoyama N, Lougheed J, Miller WT, (2005) Phosphorylation of WASP by the Cdc42-associated kinase ACK1: dual hydroxyamino acid specificity in a tyrosine kinase. J Biol Chem 280: 42219-42226.
73. Weed SA, Parsons JT, (2001) Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20: 6418-6434.
74. Kjaerulff O, Brodin L, Jung A, (2011) The structure and function of endophilin proteins. Cell Biochem Biophys 60: 137-154.
75. Taylor MJ, Perrais D, Merrifield CJ, (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9: e1000604.
76. Schroeder B, Weller SG, Chen J, Billadeau D, McNiven MA, (2010) A Dyn2-CIN85 complex mediates degradative traffic of the EGFR by regulation of late endosomal budding. EMBO J 29: 3039-3053.
77. Eden ER, White IJ, Tsapara A, Futter CE, (2010) Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nat Cell Biol 12: 267-272.
78. Grassart A, Meas-Yedid V, Dufour A, Olivo-Marin JC, Dautry-Varsat A, et al. (2010) Pak1 phosphorylation enhances cortactin-N-WASP interaction in clathrin-caveolin-independent endocytosis. Traffic.
79. van der Horst EH, Degenhardt YY, Strelow A, Slavin A, Chinn L, et al. (2005) Metastatic properties and genomic amplification of the tyrosine kinase gene ACK1. Proc Natl Acad Sci U S A 102: 15901-15906.
80. Weaver AM, (2008) Cortactin in tumor invasiveness. Cancer Lett 265: 157-166.