Regulation of Src trafficking and activation by the endocytic regulatory proteins MICAL-L1 and EHD1

Journal of Cell Science

Volumn 127, Issue 8, 2014, Pages 1684-1698

  Reinecke, James B ^a   Katafiasz, Dawn ^a   Naslavsky, Naava ^a   Caplan, Steve ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Circular dorsal ruffle; EHD1; Endocytic recycling; Focal adhesion; MICAL L1; Migration; Src

Indexed keywords

EHD1 PROTEIN; MICAL L1 PROTEIN; PLATELET DERIVED GROWTH FACTOR; REGULATOR PROTEIN; SMALL INTERFERING RNA; SRC PROTEIN; UNCLASSIFIED DRUG; VINCULIN; CYTOSKELETON PROTEIN; EHD1 PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR; LIM PROTEIN; MICAL1 PROTEIN, HUMAN; PROTEIN TYROSINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VESICULAR TRANSPORT PROTEIN;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL SPREADING; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOSOME; FIBROBLAST; FLOW CYTOMETRY; FOCAL ADHESION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; STEADY STATE; ANIMAL; CELL MEMBRANE; CELL MOTION; CELL SHAPE; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYMOLOGY; HELA CELL LINE; METABOLISM; MOUSE; PHYSIOLOGY; TRANSPORT VESICLE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL MEMBRANE; CELL MOVEMENT; CELL SHAPE; CYTOSKELETAL PROTEINS; ENDOCYTOSIS; ENDOSOMES; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; FOCAL ADHESIONS; HELA CELLS; HUMANS; LIM DOMAIN PROTEINS; MICE; PLATELET-DERIVED GROWTH FACTOR; PROTEIN TRANSPORT; SRC-FAMILY KINASES; TRANSPORT VESICLES; VESICULAR TRANSPORT PROTEINS;

EID: 84898871888     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.133892     Document Type: Article

References (54)

1. Arias-Salgado, E. G., Lizano, S., Sarkar, S., Brugge, J. S., Ginsberg, M. H. and Shattil, S. J. (2003). Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc. Natl. Acad. Sci. USA 100, 13298-13302.
2. Azimifar, S. B., Böttcher, R. T., Zanivan, S., Grashoff, C., Krüger, M., Legate, K. R., Mann, M. and Fässler, R. (2012). Induction of membrane circular dorsal ruffles requires co-signalling of integrin-ILK-complex and EGF receptor. J. Cell Sci. 125, 435-448.
3. Cai, B., Giridharan, S. S., Zhang, J., Saxena, S., Bahl, K., Schmidt, J. A., Sorgen, P. L., Guo, W., Naslavsky, N. and Caplan, S. (2013). Differential roles of C-terminal Eps15 homology domain proteins as vesiculators and tubulators of recycling endosomes. J. Biol. Chem. 288, 30172-30180.
4. Caplan, S., Naslavsky, N., Hartnell, L. M., Lodge, R., Polishchuk, R. S., Donaldson, J. G. and Bonifacino, J. S. (2002). A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J. 21, 2557-2567.
5. Chang, J. H., Gill, S., Settleman, J. and Parsons, S. J. (1995). c-Src regulates the simultaneous rearrangement of actin cytoskeleton, p190RhoGAP, and p120RasGAP following epidermal growth factor stimulation. J. Cell Biol. 130, 355-368.
6. Cooper, J. A., Gould, K. L., Cartwright, C. A. and Hunter, T. (1986). Tyr527 is phosphorylated in pp60c-src: implications for regulation. Science 231, 1431-1434.
7. Courtneidge, S. A., Levinson, A. D. and Bishop, J. M. (1980). The protein encoded by the transforming gene of avian sarcoma virus (pp60src) and a homologous protein in normal cells (pp60proto-src) are associated with the plasma membrane. Proc. Natl. Acad. Sci. USA 77, 3783-3787.
8. Deramaudt, T. B., Dujardin, D., Hamadi, A., Noulet, F., Kolli, K., De Mey, J., Takeda, K. and Rondé, P. (2011). FAK phosphorylation at Tyr-925 regulates cross-talk between focal adhesion turnover and cell protrusion. Mol. Biol. Cell 22, 964-975.
9. Donepudi, M. and Resh, M. D. (2008). c-Src trafficking and co-localization with the EGF receptor promotes EGF ligand-independent EGF receptor activation and signaling. Cell. Signal. 20, 1359-1367.
10. Ezratty, E. J., Partridge, M. A. and Gundersen, G. G. (2005). Microtubuleinduced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7, 581-590.
11. Feder, D. and Bishop, J. M. (1990). Purification and enzymatic characterization of pp60c-src from human platelets. J. Biol. Chem. 265, 8205-8211.
12. Fichtman, B., Ravid, L., Rapaport, D. and Horowitz, M. (2008). EHDS are serine phosphoproteins: EHD1 phosphorylation is enhanced by serum stimulation. Cell. Mol. Biol. Lett. 13, 632-648.
13. Fincham, V. J. and Frame, M. C. (1998). The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility. EMBO J. 17, 81-92.
14. Fincham, V. J., Brunton, V. G. and Frame, M. C. (2000). The SH3 domain directs acto-myosin-dependent targeting of v-Src to focal adhesions via phosphatidylinositol 3-kinase. Mol. Cell. Biol. 20, 6518-6536.
15. Fra, A. M., Williamson, E., Simons, K. and Parton, R. G. (1994). Detergentinsoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269, 30745-30748.
16. Friedl, P. and Gilmour, D. (2009). Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10, 445-457.
17. Giridharan, S. S., Cai, B., Vitale, N., Naslavsky, N. and Caplan, S. (2013). Cooperation of MICAL-L1, syndapin2, and phosphatidic acid in tubular recycling endosome biogenesis. Mol. Biol. Cell 24, 1776-1790.
18. Gu, Z., Noss, E. H., Hsu, V. W. and Brenner, M. B. (2011). Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. J. Cell Biol. 193, 61-70.
19. Hoon, J. L., Wong, W. K. and Koh, C. G. (2012). Functions and regulation of circular dorsal ruffles. Mol. Cell. Biol. 32, 4246-4257.
20. Huveneers, S. and Danen, E. H. (2009). Adhesion signaling - crosstalk between integrins, Src and Rho. J. Cell Sci. 122, 1059-1069.
21. Jović, M., Naslavsky, N., Rapaport, D., Horowitz, M. and Caplan, S. (2007). EHD1 regulates beta1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J. Cell Sci. 120, 802-814.
22. Kaplan, K. B., Swedlow, J. R., Varmus, H. E. and Morgan, D. O. (1992). Association of p60c-src with endosomal membranes in mammalian fibroblasts. J. Cell Biol. 118, 321-333.
23. Kaplan, K. B., Bibbins, K. B., Swedlow, J. R., Arnaud, M., Morgan, D. O. and Varmus, H. E. (1994). Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527. EMBO J. 13, 4745-4756.
24. Kasahara, K., Nakayama, Y., Kihara, A., Matsuda, D., Ikeda, K., Kuga, T., Fukumoto, Y., Igarashi, Y. and Yamaguchi, N. (2007). Rapid trafficking of c-Src, a non-palmitoylated Src-family kinase, between the plasma membrane and late endosomes/lysosomes. Exp. Cell Res. 313, 2651-2666.
25. Klinghoffer, R. A., Sachsenmaier, C., Cooper, J. A. and Soriano, P. (1999). Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 18, 2459-2471.
26. Koegl, M., Zlatkine, P., Ley, S. C., Courtneidge, S. A. and Magee, A. I. (1994). Palmitoylation of multiple Src-family kinases at a homologous N-terminal motif. Biochem. J. 303, 749-753.
27. Kypta, R. M., Goldberg, Y., Ulug, E. T. and Courtneidge, S. A. (1990). Association between the PDGF receptor and members of the src family of tyrosine kinases. Cell 62, 481-492.
28. Lobert, V. H. and Stenmark, H. (2012). The ESCRT machinery mediates polarization of fibroblasts through regulation of myosin light chain. J. Cell Sci. 125, 29-36.
29. Luttrell, D. K., Lee, A., Lansing, T. J., Crosby, R. M., Jung, K. D., Willard, D., Luther, M., Rodriguez, M., Berman, J. and Gilmer, T. M. (1994). Involvement of pp60c-src with two major signaling pathways in human breast cancer. Proc. Natl. Acad. Sci. USA 91, 83-87.
30. Magdalena, J., Millard, T. H. and Machesky, L. M. (2003). Microtubule involvement in NIH 3T3 Golgi and MTOC polarity establishment. J. Cell Sci. 116, 743-756.
31. Mettlen, M., Platek, A., Van Der Smissen, P., Carpentier, S., Amyere, M., Lanzetti, L., de Diesbach, P., Tyteca, D. and Courtoy, P. J. (2006). Src triggers circular ruffling and macropinocytosis at the apical surface of polarized MDCK cells. Traffic 7, 589-603.
32. Mori, S., Rönnstrand, L., Yokote, K., Engström, A., Courtneidge, S. A., Claesson-Welsh, L. and Heldin, C. H. (1993). Identification of two juxtamembrane autophosphorylation sites in the PDGF beta-receptor involvement in the interaction with Src family tyrosine kinases. EMBO J. 12, 2257-2264.
33. Nada, S., Okada, M., MacAuley, A., Cooper, J. A. and Nakagawa, H. (1991). Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature 351, 69-72.
34. Payne, G., Shoelson, S. E., Gish, G. D., Pawson, T. and Walsh, C. T. (1993). Kinetics of p56lck and p60src Src homology 2 domain binding to tyrosine-phosphorylated peptides determined by a competition assay or surface plasmon resonance. Proc. Natl. Acad. Sci. USA 90, 4902-4906.
35. Rahajeng, J., Giridharan, S. S., Naslavsky, N. and Caplan, S. (2010). Collapsin response mediator protein-2 (Crmp2) regulates trafficking by linking endocytic regulatory proteins to dynein motors. J. Biol. Chem. 285, 31918-31922.
36. Ren, Y., Meng, S., Mei, L., Zhao, Z. J., Jove, R. and Wu, J. (2004). Roles of Gab1 and SHP2 in paxillin tyrosine dephosphorylation and Src activation in response to epidermal growth factor. J. Biol. Chem. 279, 8497-8505.
37. Reuter, C., Findik, D. and Presek, P. (1990). Characterization of purified pp60csrc protein tyrosine kinase from human platelets. Eur. J. Biochem. 190, 343-350.
38. Rohrschneider, L. R. (1979). Immunofluorescence on avian sarcoma virustransformed cells: localization of the src gene product. Cell 16, 11-24.
39. Sandilands, E. and Frame, M. C. (2008). Endosomal trafficking of Src tyrosine kinase. Trends Cell Biol. 18, 322-329.
40. Sandilands, E., Cans, C., Fincham, V. J., Brunton, V. G., Mellor, H., Prendergast, G. C., Norman, J. C., Superti-Furga, G. and Frame, M. C. (2004). RhoB and actin polymerization coordinate Src activation with endosome-mediated delivery to the membrane. Dev. Cell 7, 855-869.
41. Schnatwinkel, C., Christoforidis, S., Lindsay, M. R., Uttenweiler-Joseph, S., Wilm, M., Parton, R. G. and Zerial, M. (2004). The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol. 2, E261.
42. Sharma, M., Giridharan, S. S., Rahajeng, J., Naslavsky, N. and Caplan, S. (2009). MICAL-L1 links EHD1 to tubular recycling endosomes and regulates receptor recycling. Mol. Biol. Cell 20, 5181-5194.
43. Smart, J. E., Oppermann, H., Czernilofsky, A. P., Purchio, A. F., Erikson, R. L. and Bishop, J. M. (1981). Characterization of sites for tyrosine phosphorylation in the transforming protein of Rous sarcoma virus (pp60v-src) and its normal cellular homologue (pp60c-src). Proc. Natl. Acad. Sci. USA 78, 6013-6017.
44. Tanji, M., Ishizaki, T., Ebrahimi, S., Tsuboguchi, Y., Sukezane, T., Akagi, T., Frame, M. C., Hashimoto, N., Miyamoto, S. and Narumiya, S. (2010). mDia1 targets v-Src to the cell periphery and facilitates cell transformation, tumorigenesis, and invasion. Mol. Cell. Biol. 30, 4604-4615.
45. Timpson, P., Jones, G. E., Frame, M. C. and Brunton, V. G. (2001). Coordination of cell polarization and migration by the Rho family GTPases requires Src tyrosine kinase activity. Curr. Biol. 11, 1836-1846.
46. Tu, C., Ortega-Cava, C. F., Winograd, P., Stanton, M. J., Reddi, A. L., Dodge, I., Arya, R., Dimri, M., Clubb, R. J., Naramura, M. et al. (2010). Endosomal-sorting complexes required for transport (ESCRT) pathway-dependent endosomal traffic regulates the localization of active Src at focal adhesions. Proc. Natl. Acad. Sci. USA 107, 16107-16112.
47. Veracini, L., Franco, M., Boureux, A., Simon, V., Roche, S. and Benistant, C. (2006). Two distinct pools of Src family tyrosine kinases regulate PDGF-induced DNA synthesis and actin dorsal ruffles. J. Cell Sci. 119, 2921-2934.
48. Ware, M. F., Tice, D. A., Parsons, S. J. and Lauffenburger, D. A. (1997). Overexpression of cellular Src in fibroblasts enhances endocytic internalization of epidermal growth factor receptor. J. Biol. Chem. 272, 30185-30190.
49. Webb, D. J., Donais, K., Whitmore, L. A., Thomas, S. M., Turner, C. E., Parsons, J. T. and Horwitz, A. F. (2004). FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 6, 154-161.
50. Welham, M. J. and Wyke, J. A. (1988). A single point mutation has pleiotropic effects on pp60v-src function. J. Virol. 62, 1898-1906.
51. Wheeler, D. L., Iida, M. and Dunn, E. F. (2009). The role of Src in solid tumors. Oncologist 14, 667-678.
52. Wilde, A., Beattie, E. C., Lem, L., Riethof, D. A., Liu, S. H., Mobley, W. C., Soriano, P. and Brodsky, F. M. (1999). EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake. Cell 96, 677-687.
53. Wozniak, M. A., Modzelewska, K., Kwong, L. and Keely, P. J. (2004). Focal adhesion regulation of cell behavior. Biochim. Biophys. Acta 1692, 103-119.
54. Xu, W., Doshi, A., Lei, M., Eck, M. J. and Harrison, S. C. (1999). Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3, 629-638.