Identification of endosomal epidermal growth factor receptor signaling targets by functional organelle proteomics

Molecular and Cellular Proteomics

Volumn 6, Issue 5, 2007, Pages 908-922

  Stasyk, Taras ^a   Schiefermeier, Natalia ^a   Skvortsov, Sergej ^b   Zwierzina, Heinz ^b   Peränen, Johan ^c   Bonn, Guenther K ^d   Hubeer, Lukas A ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 8; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; GEFITINIB; GUANOSINE TRIPHOSPHATASE; INTEGRIN; LIGAND; MOESIN; MYOSIN; MYOSIN LIGHT CHAIN; PHOSPHOPROTEIN; PROTEIN CAPZ; RAS PROTEIN; SEPTIN;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL ORGANELLE; CELL SURVIVAL; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ENDOSOME; FLUORESCENCE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEOMICS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

CELL CULTURE TECHNIQUES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENDOSOMES; EPIDERMAL GROWTH FACTOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; PROTEINS; PROTEOMICS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 34249706373     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M600463-MCP200     Document Type: Article

References (60)

1. Hoeller, D., Volarevic, S., and Dikic, I. (2005) Compartmentalization of growth factor receptor signalling. Curr. Opin. Cell Biol. 17, 107-111
2. Dard, N., and Peter, M. (2006) Scaffold proteins in MAP kinase signaling: more than simple passive activating platforms. BioEssays 28, 146-156
3. Teis, D., and Huber, L. A. (2003) The odd couple: signal transcluction and endocytosis. Cell. Mol. Life. Sci. 60, 2020-2033
4. Muller, J., Ory, S., Copeland, T., Piwnica-Worms, H., and Morrison, D. K. (2001) C-TAK1 regulates Ras signaling by phosphorylating the MAPK scaffold, KSR1. Mol. Cell 8, 983-993
5. Kurzbauer, R., Teis, D., de Araujo M. E., Maurer-Stroh, S., Eisenhaber, F., Bourenkov, G. P., Bartunik, H. D., Hekman, M., Rapp, U. R., Huber, L. A., and Clausen, T. (2004) Crystal structure of the p14/MP1 scaffolding complex: how a twin couple attaches mitogen-activated protein kinase signaling to late endosomes. Proc. Natl. Acad. Sci. U. S. A. 101, 10984-10989
6. Wunderlich, W., Fialka, I., Teis, D., Alpi, A., Pfeifer, A., Parton, R. G., Lottspeich, F., and Huber, L. A. (2001) A novel 14-kilodalton protein interacts with the mitogen-activated protein kinase scaffold mpi on a late endosomal/lysosomal compartment. J. Cell Biol. 152, 765-776
7. Teis, D., Wunderlich, W., and Huber, L. A. (2002) Localization of the MP1-MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. Dev. Cell 3, 803-814
8. Miaczynska, M., Christoforidis, S., Giner, A., Shevchenko, A., Uttenweiler-Joseph, S., Habermann, B., Wilm, M., Parton, R. G., and Zerial, M. (2004) APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116, 445-456
9. Blagoev, B., Ong, S. E., Kratchmarova, I., and Mann, M. (2004) Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat. Biotechnol. 22, 1139-1145
10. Zhang, Y., Wolf-Yadlin, A., Ross, P. L., Pappin, D. J., Rush, J., Lauffenburger, D. A., and White, F. M. (2005) Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol. Cell. Proteomics 4, 1240-1250
11. Wu, S. L., Kim, J., Bandle, R. W., Liotta, L., Petricoin, E., and Karger, B. L. (2006) Dynamic profiling of the post-translational modifications and interaction partners of epidermal growth factor receptor signaling after stimulation by epidermal growth factor using extended range proteomic analysis (ERPA). Mol. Cell. Proteomics 5, 1610-1627
12. Kratchmarova, I., Blagoev, B., Haack-Sorensen, M., Kassem, M., and Mann, M. (2005) Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 308, 1472-1477
13. Yoon, S,, and Seger, R. (2006) The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 24, 21-44
14. Stasyk, T., Morandell, S., Bakry, R., Feuerstein, I., Huck, C. W., Stecher, G., Bonn, G. K., and Huber, L. A. (2005) Quantitative detection of phosphoproteins by combination of two-dimensional difference gel electrophoresis and phosphospecific fluorescent staining. Electrophoresis 26, 2850-2854
15. Reichmann, E., Schwarz, H., Deiner, E. M., Leitner, I., Eilers, M., Berger, J Busslinger, M., and Beug, H. (1992) Activation of an inducible c-FosER fusion protein causes loss of epithelial polarity and triggers epithelial-fibroblastoid cell conversion. Cell 71, 1103-1116
16. Huber, L. A., Pfaller, K., and Vietor, I. (2003) Organelle proteomics: implications for subcellular fractionation in proteomics. Circ. Res. 92, 962-968
17. Fialka, I., Pasquali, C., Lottspeich, F., Ahorn, H., and Huber, L. A. (1997) Subcellular fractionation of polarized epithelial cells and identification of organelle-specific proteins by two-dimensional gel electrophoresis. Electrophoresis 18, 2582-2590
18. Araujo, M. E. G., and Huber, L. A. (2006) Subcellular fractionation, in Cardiovascular Proteomics: Methods and Protocols, pp. 73-85, Humana Press Inc., Totowa, NJ
19. Fialka, I., Pasquali, C., Kurzbauer, R., Lottspeich, F., and Huber, L. A. (1999) Loss of epithelial polarity is accompanied by differential association of proteins with intracellular membranes. Electrophoresis 20, 331-343
20. Wessel, D., and Flugge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143
21. Wilkins, M. R., Appel, R. D., Van Eyk, J. E., Chung, M. C., Gorg, A., Hecker, M., Huber, L. A., Langen, H., Link, A. J., Pak, Y. K., Patterson, S. D., Pennington, S. R., Rabilloud, T., Simpson, R. J., Weiss, W., and Dunn, M. J. (2006) Guidelines for the next 10 years of proteomics. Proteomics 6, 4-8
22. Rabilloud, T., Strub, J. M., Luche, S., van Dorsselaer, A., and Lunardi, J. (2001) A comparison between Sypro Ruby and ruthenium II tris (bathophenanthroline disulfonate) as fluorescent stains for protein detection in gels. Proteomics 1, 699-704
23. Lamanda, A., Zahn, A., Roder, D., and Langen, H. (2004) Improved ruthenium II tris (bathophenantroline disulfonate) staining and destaining protocol for a better signal-to-background ratio and improved baseline resolution. Proteomics 4, 599-608
24. Hellman, U. (2000) Sample preparation by SDS/PAGE and in-gel digestion. EXS 43-54
25. Furuhjelm, J., and Peranen, J. (2003) The C-terminal end of R-Ras contains a focal adhesion targeting signal. J. Cell Sci. 116, 3729-3738
26. Poupon, V., Stewart, A., Gray, S. R., Piper, R. C., and Luzio, J. P. (2003) The role of mVps18p in clustering, fusion, and intracellular localization of late endocytic organelles. Mol. Biol. Cell 14, 4015-4027
27. Cabezas, A., Bache, K. G., Brech, A., and Stenmark, H. (2005) Alix regulates cortical actin and the spatial distribution of endosomes. J. Cell Sci. 118, 2625-2635
28. Harder, T., Kellner, R., Parton, R. G., and Gruenberg, J. (1997) Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol. Biol. Cell 8, 533-545
29. Liu, L., and McKeehan, W. L. (2002) Sequence analysis of LRPPRC and its SEC1 domain interaction partners suggests roles in cytoskeletal organization, vesicular trafficking, nucleocytosolic shuttling, and chromosome activity. Genomics 79, 124-136
30. Spiliotis, E. T., and Nelson, W. J. (2006) Here come the septins: novel polymers that coordinate intracellular functions and organization. J. Cell Sci. 119, 4-10
31. Takayama, S., Xie, Z., and Reed, J. C. (1999) An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J. Biol. Chem. 274, 781-786
32. Ku, N. O., and Omary, M. B. (1997) Phosphorylation of human keratin 8 in vivo at conserved head domain serine 23 and at epidermal growth factor-stimulated tail domain serine 431. J. Biol. Chem. 272, 7556-7564
33. Blagoev, B., Kratchmarova, I., Ong, S. E., Nielsen, M., Foster, L. J, and Mann, M. (2003) A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat. Biotechnol. 21, 315-318
34. Klemke, R. L., Cal, S., Giannini, A. L., Gallagher, P. J., de Lanerolle, P., and Cheresh, D. A. (1997) Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137, 481-492
35. Marklund, U., Brattsand, G., Shingler, V., and Gullberg, M. (1993) Serine 25 of oncoprotein 18 is a major cytosolic target for the mitogen-activated protein kinase. J. Biol. Chem. 268, 15039-15047
36. Habelhah, H., Shah, K., Huang, L., Ostareck-Lederer, A., Burlingame, A. L., Shokat, K. M., Hentze, M. W., and Ronai, Z. (2001) ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nat. Cell Biol. 3, 325-330
37. Loeffler-Ragg, J., Skvortsov, S., Sarg, B., Skvortsova, I., Witsch-Baumgartner, M., Mueller, D., Lindner, H., and Zwierzina, H. (2005) Gefitinib-responsive EGFR-positive colorectal cancers have different proteome profiles from non-responsive cell lines. Eur. J. Cancer 41, 2338-2346
38. Zhang, Z., Vuori, K., Wang, H., Reed, J. C., and Ruoslahti, E. (1996) Integrin activation by R-ras. Cell 85, 61-69
39. Self, A. J., Caron, E., Paterson, H. F., and Hall, A. (2001) Analysis of R-Ras signalling pathways. J. Cell Sci. 114, 1357-1366
40. Foster, L. J., de Hoog, C. L., Zhang, Y., Zhang, Y., Xie, X., Mootha, V. K., and Mann, M. (2006) A mammalian organelle map by protein correlation profiling. Cell 125, 187-199
41. Andersen, J. S., and Mann, M. (2006) Organellar proteomics: turning inventories into insights. EMBO Rep. 7, 874-879
42. Andersen, J. S., Lam, Y. W., Leung, A. K., Ong, S. E., Lyon, C. E., Lamond, A. I., and Mann, M. (2005) Nucleolar proteome dynamics. Nature 433, 77-83
43. Pasquali, C., Fialka, I., and Huber, L. A. (1997) Preparative two-dimensional gel electrophoresis of membrane proteins. Electrophoresis 18, 2573-2581
44. Huber, L. A. (2003) Is proteomics heading in the wrong direction. Nat. Rev. Mol. Cell. Biol. 4, 74-80
45. Hong, O. K., Suh, S. H., Kwon, H. S., Ko, S. H., Choi, Y. H., Moon, S.D., Yoo, S. J., Son, H. Y., Park, K. S., Lee, I. K., and Yoon, K. H. (2005) Proteomic analysis of differential protein expression in response to epidermal growth factor in neonatal porcine pancreatic cell monolayers. J. Cell. Biochem. 95, 769-781
46. Weinman, E. J., Hall, R. A., Friedman, P. A., Liu-Chen, L. Y., and Shenolikar, S. (2006) The association of NHERF adaptor proteins with g protein-coupled receptors and receptor tyrosine kinases. Annu. Rev. Physiol. 68, 491-505
47. + exchanger regulatory factor stabilizes epidermal growth factor receptors at the cell surface. Mol. Biol. Cell 15, 5470-5480
48. Cao, T. T., Deacon, H. W., Reczek, D., Bretscher, A., and von Zastrow, M. (1999) A kinase-regulated PDZ-domain interaction controls endocytic sorting of the β2-adrenergic receptor. Nature 401, 286-290
49. Fialka, I., Steinlein, P., Ahorn, H., Bock, G., Burbelo, P. D., Haberfellner, M., Lottspeich, F., Paiha, K., Pasquali, C., and Huber, L. A. (1999) Identification of syntenin as a protein of the apical early endocytic compartment in Madin-Darby canine kidney cells. J. Biol. Chem. 274, 26233-26239
50. Ito, H., Iwamoto, I., Morishita, R., Nozawa, Y., Narumiya, S., Asano, T., and Nagata, K. I. (2005) Possible role of Rho/Rhotekin signaling in mammalian septin organization. Oncogene 24, 7064-7072
51. She, Y. M., Huang, Y. W., Zhang, L., and Trimble, W. S. (2004) Septin 2 phosphorylation: theoretical and mass spectrometric evidence for the existence of a single phosphorylation site in vivo. Rapid Commun. Mass Spectrom. 18, 1123-1130
52. Bukau, B., and Horwich, A. L. (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366
53. Doong, H., Price, J., Kim, Y. S., Gasbarre, C., Probst, J., Liotta, L. A., Blanchette, J., Rizzo, K., and Kohn, E. (2000) CAIR-1/BAG-3 forms an EGF-regulated ternary complex with phospholipase C-γ and Hsp70/ Hsc70. Oncogene 19, 4385-4395
54. Nylandsted, J., Gyrd-Hansen, M., Danielewicz, A., Fehrenbacher, N., Lademlien, U., Hoyer-Hansen, M., Weber, E., Multhoff, G., Rohde, M., and Jaattela, M. (2004) Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J. Exp. Med. 200, 425-435
55. Mili, S., Shu, H. J., Zhao, Y., and Piñol-Roma, S. (2001) Distinct RNP complexes of shuttling hnRNP proteins with pre-mRNA and mRNA: candidate intermediates in formation and export of mRNA. Mol. Cell. Biol. 21, 7307-7319
56. Gao, J., Li, J., Chen, Y., and Ma, L. (2005) Activation of tyrosine kinase of EGFR induces Gβγ-dependent GRK-EGFR complex formation. FEBS Lett. 579, 122-126
57. Zheng, B., Lavoie, C., Tang, T. D., Ma, P., Meerloo, T., Beas, A., and Farquhar, M. G. (2004) Regulation of epidermal growth factor receptor degradation by heterotrimeric Gαs protein. Mol. Biol. Cell 15, 5538-5550
58. Sethi, T., Ginsberg, M. H., Downward, J., and Hughes, P. E. (1999) The small GTP-binding protein R-Ras can influence integrin activation by antagonizing a Ras/Raf-initiated integrin suppression pathway. Mol. Biol. Cell 10, 1799-1809
59. Bagshaw, R. D., Mahuran, D. J., and Callahan, J. W. (2005) A proteomic analysis of lysosomal integral membrane proteins reveals the diverse composition of the organelle. Mol. Cell. Proteomics 4, 133-143
60. Harden, T. K., and Sondek, J. (2006) Regulation of phospholipase C isozymes by ras superfamily GTPases. Annu. Rev. Pharmacol. Toxicol. 46, 335-379