Characterization of PXK as a protein involved in epidermal growth factor receptor trafficking

Molecular and Cellular Biology

Volumn 30, Issue 7, 2010, Pages 1689-1702

  Takeuchi, Hiroshi ^a   Takeuchi, Takako ^a   Gao, Jing ^a   Cantley, Lewis C ^b,c   Hirata, Masato ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PROTEIN PXK; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; INTERNALIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA INTERFERENCE; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CYSTEINE PROTEINASE INHIBITORS; FEMALE; HUMANS; INTRACELLULAR MEMBRANES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEUPEPTINS; MACROLIDES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NERVE TISSUE PROTEINS; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; SEQUENCE ALIGNMENT; TISSUE DISTRIBUTION;

MAMMALIA;

EID: 77949381391     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01105-09     Document Type: Article

References (75)

1. Ago, T., F. Kuribayashi, H. Hiroaki, R. Takeya, T. Ito, D. Kohda, and H. Sumimoto. 2003. Phosphorylation of p47phox directs phox homology domain from SH3 domain toward phosphoinositides, leading to phagocyte NADPH oxidase activation. Proc. Natl. Acad. Sci. U. S. A. 100:4474-4479.
2. Alwan, H. A., E. J. van Zoelen, and J. E. van Leeuwen. 2003. Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. J. Biol. Chem. 278:35781-35790.
3. Arighi, C. N., L. M. Hartnell, R. C. Aguilar, C. R. Haft, and J. S. Bonifacino. 2004. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165:123-133.
4. Badour, K., M. K. McGavin, J. Zhang, S. Freeman, C. Vieira, D. Filipp, M. Julius, G. B. Mills, and K. A. Siminovitch. 2007. Interaction of the Wiskott-Aldrich syndrome protein with sorting nexin 9 is required for CD28 endocytosis and cosignaling in T cells. Proc. Natl. Acad. Sci. U. S. A. 104:1593-1598.
5. Boudeau, J., D. Miranda-Saavedra, G. J. Barton, and D. R. Alessi. 2006. Emerging roles of pseudokinases. Trends Cell Biol. 16:443-452.
6. Bravo, J., D. Karathanassis, C. M. Pacold, M. E. Pacold, C. D. Ellson, K. E. Anderson, P. J. Butler, I. Lavenir, O. Perisic, P. T. Hawkins, L. Stephens, and R. L. Williams. 2001. The crystal structure of the PX domain from p40(phox) bound to phosphatidylinositol 3-phosphate. Mol. Cell 8:829-839.
7. Carlton, J., M. Bujny, B. J. Peter, V. M. Oorschot, A. Rutherford, H. Mellor, J. Klumperman, H. T. McMahon, and P. J. Cullen. 2004. Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high-curvature membranes and 3-phosphoinositides. Curr. Biol. 14:1791-1800.
8. Carlton, J., M. Bujny, A. Rutherford, and P. Cullen. 2005. Sorting nexins - unifying trends and new perspectives. Traffic 6:75-82.
9. Choi, J. H., W. P. Hong, M. J. Kim, J. H. Kim, S. H. Ryu, and P. G. Suh. 2004. Sorting nexin 16 regulates EGF receptor trafficking by phosphatidylinositol-3-phosphate interaction with the Phox domain. J. Cell Sci. 117:4209-4218.
10. Dumas, J. J., E. Merithew, E. Sudharshan, D. Rajamani, S. Hayes, D. Lawe, S. Corvera, and D. G. Lambright. 2001. Multivalent endosome targeting by homodimeric EEA1. Mol. Cell 8:947-958.
11. Ellson, C. D., S. Andrews, L. R. Stephens, and P. T. Hawkins. 2002. The PX domain: a new phosphoinositide-binding module. J. Cell Sci. 115:1099-1105.
12. Engqvist-Goldstein, A. E., and D. G. Drubin. 2003. Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19:287-332.
13. Fernandez-Borja, M., L. Janssen, D. Verwoerd, P. Hordijk, and J. Neefjes. 2005. RhoB regulates endosome transport by promoting actin assembly on endosomal membranes through Dia1. J. Cell Sci. 118:2661-2670.
14. Fukuda, M., and T. S. Kuroda. 2002. Slac2-c (synaptotagmin-like protein homologue lacking C2 domains-c), a novel linker protein that interacts with Rab27, myosin Va/VIIa, and actin. J. Biol. Chem. 277:43096-43103.
15. Gaullier, J. M., A. Simonsen, A. D'Arrigo, B. Bremnes, H. Stenmark, and R. Aasland. 1998. FYVE fingers bind PtdIns(3)P. Nature 394:432-433.
16. Giot, L., J. S. Bader, C. Brouwer, A. Chaudhuri, B. Kuang, Y. Li, Y. L. Hao, C. E. Ooi, B. Godwin, E. Vitols, G. Vijayadamodar, P. Pochart, H. Machineni, M. Welsh, Y. Kong, B. Zerhusen, R. Malcolm, Z. Varrone, A. Collis, M. Minto, S. Burgess, L. McDaniel, E. Stimpson, F. Spriggs, J. Williams, K. Neurath, N. Ioime, M. Agee, E. Voss, K. Furtak, R. Renzulli, N. Aanensen, S. Carrolla, E. Bickelhaupt, Y. Lazovatsky, A. DaSilva, J. Zhong, C. A. Stanyon, R. L. Finley, Jr., K. P. White, M. Braverman, T. Jarvie, S. Gold, M. Leach, J. Knight, R. A. Shimkets, M. P. McKenna, J. Chant, and J. M. Rothberg. 2003. A protein interaction map of Drosophila melanogaster. Science 302:1727-1736.
17. Gruenberg, J. 2001. The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2:721-730.
18. Haft, C. R., M. de la Luz Sierra, R. Bafford, M. A. Lesniak, V. A. Barr, and S. I. Taylor. 2000. Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol. Biol. Cell 11:4105-4116.
19. Haft, C. R., M. de la Luz Sierra, V. A. Barr, D. H. Haft, and S. I. Taylor. 1998. Identification of a family of sorting nexin molecules and characterization of their association with receptors. Mol. Cell. Biol. 18:7278-7287.
20. Haglund, K., S. Sigismund, S. Polo, I. Szymkiewicz, P. P. Di Fiore, and I. Dikic. 2003. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5:461-466.
21. Hanks, S. K., and T. Hunter. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9:576-596.
22. Hanson, B. J., and W. Hong. 2003. Evidence for a role of SNX16 in regulating traffic between the early and later endosomal compartments. J. Biol. Chem. 278:34617-34630.
23. Harley, J. B., M. E. Alarcon-Riquelme, L. A. Criswell, C. O. Jacob, R. P. Kimberly, K. L. Moser, B. P. Tsao, T. J. Vyse, C. D. Langefeld, S. K. Nath, J. M. Guthridge, B. L. Cobb, D. B. Mirel, M. C. Marion, A. H. Williams, J. Divers, W. Wang, S. G. Frank, B. Namjou, S. B. Gabriel, A. T. Lee, P. K. Gregersen, T. W. Behrens, K. E. Taylor, M. Fernando, R. Zidovetzki, P. M. Gaffney, J. C. Edberg, J. D. Rioux, J. O. Ojwang, J. A. James, J. T. Merrill, G. S. Gilkeson, M. F. Seldin, H. Yin, E. C. Baechler, Q. Z. Li, E. K. Wakeland, G. R. Bruner, K. M. Kaufman, and J. A. Kelly. 2008. Genomewide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat. Genet. 40:204-210.
24. Hayakawa, A., S. J. Hayes, D. C. Lawe, E. Sudharshan, R. Tuft, K. Fogarty, D. Lambright, and S. Corvera. 2004. Structural basis for endosomal targeting by FYVE domains. J. Biol. Chem. 279:5958-5966.
25. Hayashi, S., T. Okada, N. Igarashi, T. Fujita, S. Jahangeer, and S. Nakamura. 2002. Identification and characterization of RPK118, a novel sphingosine kinase-1-binding protein. J. Biol. Chem. 277:33319-33324.
26. Hertzog, M., C. van Heijenoort, D. Didry, M. Gaudier, J. Coutant, B. Gigant, G. Didelot, T. Preat, M. Knossow, E. Guittet, and M. F. Carlier. 2004. The beta-thymosin/WH2 domain; structural basis for the switch from inhibition to promotion of actin assembly. Cell 117:611-623.
27. Hoepfner, S., F. Severin, A. Cabezas, B. Habermann, A. Runge, D. Gillooly, H. Stenmark, and M. Zerial. 2005. Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121:437-450.
28. Holt, M. R., and A. Koffer. 2001. Cell motility: proline-rich proteins promote protrusions. Trends Cell Biol. 11:38-46.
29. Huang, F., L. K. Goh, and A. Sorkin. 2007. EGF receptor ubiquitination is not necessary for its internalization. Proc. Natl. Acad. Sci. U. S. A. 104:16904-16909.
30. Huang, F., D. Kirkpatrick, X. Jiang, S. Gygi, and A. Sorkin. 2006. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol. Cell 21:737-748.
31. Ikonomov, O. C., D. Sbrissa, M. Foti, J. L. Carpentier, and A. Shisheva. 2003. PIKfyve controls fluid phase endocytosis but not recycling/degradation of endocytosed receptors or sorting of procathepsin D by regulating multivesicular body morphogenesis. Mol. Biol. Cell 14:4581-4591.
32. Irie, H. Y., R. V. Pearline, D. Grueneberg, M. Hsia, P. Ravichandran, N. Kothari, S. Natesan, and J. S. Brugge. 2005. Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition. J. Cell Biol. 171:1023-1034.
33. Jang, I. H., S. Lee, J. B. Park, J. H. Kim, C. S. Lee, E. M. Hur, I. S. Kim, K. T. Kim, H. Yagisawa, P. G. Suh, and S. H. Ryu. 2003. The direct interaction of phospholipase C-gamma 1 with phospholipase D2 is important for epidermal growth factor signaling. J. Biol. Chem. 278:18184-18190.
34. Jeng, R. L., and M. D. Welch. 2001. Cytoskeleton: actin and endocytosis - no longer the weakest link. Curr. Biol. 11:R691-694.
35. Kaksonen, M., C. P. Toret, and D. G. Drubin. 2006. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7:404-414.
36. Kanai, F., H. Liu, S. J. Field, H. Akbary, T. Matsuo, G. E. Brown, L. C. Cantley, and M. B. Yaffe. 2001. The PX domains of p47phox and p40phox bind to lipid products of PI(3)K. Nat. Cell Biol. 3:675-678.
37. Katzmann, D. J., G. Odorizzi, and S. D. Emr. 2002. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3:893-905.
38. Kurten, R. C., D. L. Cadena, and G. N. Gill. 1996. Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science 272:1008-1010.
39. Lee, C. S., I. S. Kim, J. B. Park, M. N. Lee, H. Y. Lee, P. G. Suh, and S. H. Ryu. 2006. The phox homology domain of phospholipase D activates dynamin GTPase activity and accelerates EGFR endocytosis. Nat. Cell Biol. 8:477-484.
40. Lin, J., J. Liu, Y. Wang, J. Zhu, K. Zhou, N. Smith, and X. Zhan. 2005. Differential regulation of cortactin and N-WASP-mediated actin polymerization by missing in metastasis (MIM) protein. Oncogene 24:2059-2066.
41. Lin, Q., C. G. Lo, R. A. Cerione, and W. Yang. 2002. The Cdc42 target ACK2 interacts with sorting nexin 9 (SH3PX1) to regulate epidermal growth factor receptor degradation. J. Biol. Chem. 277:10134-10138.
42. Liu, L., C. Yang, J. Yuan, X. Chen, J. Xu, Y. Wei, J. Yang, G. Lin, and L. Yu. 2005. RPK118, a PX domain-containing protein, interacts with peroxiredoxin-3 through pseudo-kinase domains. Mol. Cells 19:39-45.
43. Lundmark, R., and S. R. Carlsson. 2003. Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. J. Biol. Chem. 278:46772-46781.
44. Lunn, M. L., R. Nassirpour, C. Arrabit, J. Tan, I. McLeod, C. M. Arias, P. E. Sawchenko, J. R. Yates III, and P. A. Slesinger. 2007. A unique sorting nexin regulates trafficking of potassium channels via a PDZ domain interaction. Nat. Neurosci. 10:1249-1259.
45. Mao, H., T. S. Ferguson, S. M. Cibulsky, M. Holmqvist, C. Ding, H. Fei, and I. B. Levitan. 2005. MONaKA, a novel modulator of the plasma membrane Na, K-ATPase. J. Neurosci. 25:7934-7943.
46. McPherson, P. S. 1999. Regulatory role of SH3 domain-mediated protein-protein interactions in synaptic vesicle endocytosis. Cell Signal. 11:229-238.
47. Mellman, I. 1996. Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12:575-625.
48. Merino-Trigo, A., M. C. Kerr, F. Houghton, A. Lindberg, C. Mitchell, R. D. Teasdale, and P. A. Gleeson. 2004. Sorting nexin 5 is localized to a subdomain of the early endosomes and is recruited to the plasma membrane following EGF stimulation. J. Cell Sci. 117:6413-6424.
49. Paavilainen, V. O., E. Bertling, S. Falck, and P. Lappalainen. 2004. Regulation of cytoskeletal dynamics by actin-monomer-binding proteins. Trends Cell Biol. 14:386-394.
50. Parks, W. T., D. B. Frank, C. Huff, C. Renfrew Haft, J. Martin, X. Meng, M. P. de Caestecker, J. G. McNally, A. Reddi, S. I. Taylor, A. B. Roberts, T. Wang, and R. J. Lechleider. 2001. Sorting nexin 6, a novel SNX, interacts with the transforming growth factor-beta family of receptor serine-threonine kinases. J. Biol. Chem. 276:19332-19339.
51. Patki, V., D. C. Lawe, S. Corvera, J. V. Virbasius, and A. Chawla. 1998. A functional PtdIns(3)P-binding motif. Nature 394:433-434.
52. Paunola, E., P. K. Mattila, and P. Lappalainen. 2002. WH2 domain: a small, versatile adapter for actin monomers. FEBS Lett. 513:92-97.
53. Ponting, C. P. 1996. Novel domains in NADPH oxidase subunits, sorting nexins, and PtdIns 3-kinases: binding partners of SH3 domains? Protein Sci. 5:2353-2357.
54. Sato, T. K., M. Overduin, and S. D. Emr. 2001. Location, location, location: membrane targeting directed by PX domains. Science 294:1881-1885.
55. Schafer, D. A. 2002. Coupling actin dynamics and membrane dynamics during endocytosis. Curr. Opin. Cell Biol. 14:76-81.
56. Scheeff, E. D., and P. E. Bourne. 2005. Structural evolution of the protein kinase-like superfamily. PLoS Comput. Biol. 1:e49.
57. Schopperle, W. M., M. H. Holmqvist, Y. Zhou, J. Wang, Z. Wang, L. C. Griffith, I. Keselman, F. Kusinitz, D. Dagan, and I. B. Levitan. 1998. Slob, a novel protein that interacts with the Slowpoke calcium-dependent potassium channel. Neuron 20:565-573.
58. Schulze, W. X., and M. Mann. 2004. A novel proteomic screen for peptideprotein interactions. J. Biol. Chem. 279:10756-10764.
59. Seet, L. F., and W. Hong. 2006. The Phox (PX) domain proteins and membrane traffic. Biochim. Biophys. Acta 1761:878-896.
60. Slagsvold, T., A. Marchese, A. Brech, and H. Stenmark. 2006. CISK attenuates degradation of the chemokine receptor CXCR4 via the ubiquitin ligase AIP4. EMBO J. 25:3738-3749.
61. Sorkin, A., and L. K. Goh. 2009. Endocytosis and intracellular trafficking of ErbBs. Exp. Cell Res. 315:683-696.
62. Soulet, F., D. Yarar, M. Leonard, and S. L. Schmid. 2005. SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol. Biol. Cell 16:2058-2067.
63. Stenmark, H., and D. J. Gillooly. 2001. Intracellular trafficking and turnover of phosphatidylinositol 3-phosphate. Semin. Cell Dev. Biol. 12:193-199.
64. Vergarajauregui, S., A. San Miguel, and R. Puertollano. 2006. Activation of p38 mitogen-activated protein kinase promotes epidermal growth factor receptor internalization. Traffic 7:686-698.
65. Worby, C. A., and J. E. Dixon. 2002. Sorting out the cellular functions of sorting nexins. Nat. Rev. Mol. Cell Biol. 3:919-931.
66. Xing, Y., D. Liu, R. Zhang, A. Joachimiak, Z. Songyang, and W. Xu. 2004. Structural basis of membrane targeting by the Phox homology domain of cytokine-independent survival kinase (CISK-PX). J. Biol. Chem. 279:30662-30669.
67. Xu, Y., L. F. Seet, B. Hanson, and W. Hong. 2001. The Phox homology (PX) domain, a new player in phosphoinositide signalling. Biochem. J. 360:513-530.
68. Yarar, D., C. M. Waterman-Storer, and S. L. Schmid. 2007. SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev. Cell 13:43-56.
69. Yeow-Fong, L., L. Lim, and E. Manser. 2005. SNX9 as an adaptor for linking synaptojanin-1 to the Cdc42 effector ACK1. FEBS Lett. 579:5040-5048.
70. Zeng, H., H. Fei, and I. B. Levitan. 2004. The slowpoke channel binding protein Slob from Drosophila melanogaster exhibits regulatable protein kinase activity. Neurosci. Lett. 365:33-38.
71. Zheng, B., C. Lavoie, T. D. Tang, P. Ma, T. Meerloo, A. Beas, and M. G. Farquhar. 2004. Regulation of epidermal growth factor receptor degradation by heterotrimeric Galphas protein. Mol. Biol. Cell 15:5538-5550.
72. Zheng, B., Y. C. Ma, R. S. Ostrom, C. Lavoie, G. N. Gill, P. A. Insel, X. Y. Huang, and M. G. Farquhar. 2001. RGS-PX1, a GAP for GalphaS and sorting nexin in vesicular trafficking. Science 294:1939-1942.
73. Zhong, Q., C. S. Lazar, H. Tronchere, T. Sato, T. Meerloo, M. Yeo, Z. Songyang, S. D. Emr, and G. N. Gill. 2002. Endosomal localization and function of sorting nexin 1. Proc. Natl. Acad. Sci. U. S. A. 99:6767-6772.
74. Zhong, Q., M. J. Watson, C. S. Lazar, A. M. Hounslow, J. P. Waltho, and G. N. Gill. 2005. Determinants of the endosomal localization of sorting nexin 1. Mol. Biol. Cell 16:2049-2057.
75. Zou, X., G. Qiu, C. Chen, M. Wu, Y. Hu, H. Zheng, X. Li, S. Gu, C. Ji, and Y. Mao. 2005. Expression pattern and subcellular localization of five splice isoforms of human PXK. Int. J. Mol. Med. 16:701-707.