αvβ3-integrin-mediated adhesion is regulated through an AAK1L- and EHD3-dependent rapid-recycling pathway

Journal of Cell Science

Volumn 126, Issue 16, 2013, Pages 3593-3601

  Waxmonsky, Nicole C ^a   Conner, Sean D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

AAK1L; EHD3; Integrin recycling

Indexed keywords

AAK1L PROTEIN; EHD3 PROTEIN; INTEGRIN; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

ARTICLE; CELL ADHESION; CELL SURFACE; CELL VIABILITY; CONTROLLED STUDY; ENDOSOME; FOCAL ADHESION; HUMAN; HUMAN CELL; MOLECULAR IMAGING; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

AAK1L; EHD3; INTEGRIN RECYCLING;

ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL ADHESION; CELL MEMBRANE; ENDOSOMES; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; INTEGRIN ALPHAVBETA3; MICE; PROTEIN-SERINE-THREONINE KINASES; TRANSFECTION;

EID: 84883441205     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.122465     Document Type: Article

References (49)

1. Ballana, E., Pauls, E., Senserrich, J., Clotet, B., Perron-Sierra, F., Tucker, G. C. and Esté, J. A. (2009). Cell adhesion through alphaV-containing integrins is required for efficient HIV-1 infection in macrophages. Blood 113, 1278-1286.
2. Blume, J. J., Halbach, A., Behrendt, D., Paulsson, M. and Plomann, M. (2007). EHD proteins are associated with tubular and vesicular compartments and interact with specific phospholipids. Exp. Cell Res. 313, 219-231.
3. Case, L. B. and Waterman, C. M. (2011). Adhesive F-actin waves: a novel integrin-mediated adhesion complex coupled to ventral actin polymerization. PLoS ONE 6, e26631.
4. Caswell, P. T. and Norman, J. C. (2006). Integrin trafficking and the control of cell migration. Traffic 7, 14-21.
5. Caswell, P. T., Spence, H. J., Parsons, M., White, D. P., Clark, K., Cheng, K. W., Mills, G. B., Humphries, M. J., Messent, A. J., Anderson, K. I. et al. (2007). Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments. Dev. Cell 13, 496-510.
6. Conner, S. D. and Schmid, S. L. (2002). Identification of an adaptor-associated kinase, AAK1, as a regulator of clathrin-mediated endocytosis. J. Cell Biol. 156, 921-929.
7. Conner, S. D. and Schmid, S. L. (2003). Differential requirements for AP-2 in clathrinmediated endocytosis. J. Cell Biol. 162, 773-780.
8. Conner, S. D., Schröter, T. and Schmid, S. L. (2003). AAK1-mediated micro2 phosphorylation is stimulated by assembled clathrin. Traffic 4, 885-890.
9. Cope, M. J., Yang, S., Shang, C. and Drubin, D. G. (1999). Novel protein kinases Ark1p and Prk1p associate with and regulate the cortical actin cytoskeleton in budding yeast. J. Cell Biol. 144, 1203-1218.
10. Daumke, O., Lundmark, R., Vallis, Y., Martens, S., Butler, P. J. and McMahon, H. T. (2007). Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449, 923-927.
11. Engqvist-Goldstein, A. E. and Drubin, D. G. (2003). Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19, 287-332.
12. Fang, Z., Takizawa, N., Wilson, K. A., Smith, T. C., Delprato, A., Davidson, M. W., Lambright, D. G. and Luna, E. J. (2010). The membrane-associated protein, supervillin, accelerates F-actin-dependent rapid integrin recycling and cell motility. Traffic 11, 782-799.
13. Galperin, E., Benjamin, S., Rapaport, D., Rotem-Yehudar, R., Tolchinsky, S. and Horowitz, M. (2002). EHD3: a protein that resides in recycling tubular and vesicular membrane structures and interacts with EHD1. Traffic 3, 575-589.
14. Grant, B. D. and Caplan, S. (2008). Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 9, 2043-2052.
15. Grant, B. D. and Donaldson, J. G. (2009). Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10, 597-608.
16. Gudmundsson, H., Hund, T. J., Wright, P. J., Kline, C. F., Snyder, J. S., Qian, L., Koval, O. M., Cunha, S. R., George, M., Rainey, M. A. et al. (2010). EH domain proteins regulate cardiac membrane protein targeting. Circ. Res. 107, 84-95.
17. Harburger, D. S. and Calderwood, D. A. (2009). Integrin signalling at a glance. J. Cell Sci. 122, 159-163.
18. Henderson, D. M. and Conner, S. D. (2007). A novel AAK1 splice variant functions at multiple steps of the endocytic pathway. Mol. Biol. Cell 18, 2698-2706.
19. Henry, K. R., D'Hondt, K., Chang, J. S., Nix, D. A., Cope, M. J., Chan, C. S., Drubin, D. G. and Lemmon, S. K. (2003). The actin-regulating kinase Prk1p negatively regulates Scd5p, a suppressor of clathrin deficiency, in actin organization and endocytosis. Curr. Biol. 13, 1564-1569.
20. Humphries, M. J. (2001). Cell adhesion assays. Mol. Biotechnol. 18, 57-61.
21. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687.
22. 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.
23. Lampson, M. A., Schmoranzer, J., Zeigerer, A., Simon, S. M. and McGraw, T. E. (2001). Insulin-regulated release from the endosomal recycling compartment is regulated by budding of specialized vesicles. Mol. Biol. Cell 12, 3489-3501.
24. Lau, A. W. and Chou, M. M. (2008). The adaptor complex AP-2 regulates post-endocytic trafficking through the non-clathrin Arf6-dependent endocytic pathway. J. Cell Sci. 121, 4008-4017.
25. Margadant, C., Monsuur, H. N., Norman, J. C. and Sonnenberg, A. (2011). Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 23, 607-614.
26. Maxfield, F. R. and McGraw, T. E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132.
27. McGill, M. A., Dho, S. E., Weinmaster, G. and McGlade, C. J. (2009). Numb regulates post-endocytic trafficking and degradation of Notch1. J. Biol. Chem. 284, 26427-26438.
28. Meredith, J. E. J., Jr and Schwartz, M. A. (1997). Integrins, adhesion and apoptosis. Trends Cell Biol. 7, 146-150.
29. Millman, E. E., Zhang, H., Zhang, H., Godines, V., Bean, A. J., Knoll, B. J. and Moore, R. H. (2008). Rapid recycling of beta-adrenergic receptors is dependent on the actin cytoskeleton and myosin Vb. Traffic 9, 1958-1971.
30. Naslavsky, N. and Caplan, S. (2011). EHD proteins: key conductors of endocytic transport. Trends Cell Biol. 21, 122-131.
31. Naslavsky, N., Boehm, M., Backlund, P. S. J., Jr and Caplan, S. (2004). Rabenosyn-5 and EHD1 interact and sequentially regulate protein recycling to the plasma membrane. Mol. Biol. Cell 15, 2410-2422.
32. Naslavsky, N., Rahajeng, J., Sharma, M., Jovic, M. and Caplan, S. (2006). Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport. Mol. Biol. Cell 17, 163-177.
33. Naslavsky, N., Rahajeng, J., Chenavas, S., Sorgen, P. L. and Caplan, S. (2007). EHD1 and Eps15 interact with phosphatidylinositols via their Eps15 homology domains. J. Biol. Chem. 282, 16612-16622.
34. Naslavsky, N., McKenzie, J., Altan-Bonnet, N., Sheff, D. and Caplan, S. (2009). EHD3 regulates early-endosome-to-Golgi transport and preserves Golgi morphology. J. Cell Sci. 122, 389-400.
35. Nishimura, T. and Kaibuchi, K. (2007). Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13, 15-28.
36. Pagano, A., Crottet, P., Prescianotto-Baschong, C. and Spiess, M. (2004). In vitro formation of recycling vesicles from endosomes requires adaptor protein-1/clathrin and is regulated by rab4 and the connector rabaptin-5. Mol. Biol. Cell 15, 4990-5000.
37. Roberts, M., Barry, S., Woods, A., van der Sluijs, P. and Norman, J. (2001). PDGF-regulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11, 1392-1402.
38. Roberts, M. S., Woods, A. J., Dale, T. C., Van Der Sluijs, P. and Norman, J. C. (2004). Protein kinase B/Akt acts via glycogen synthase kinase 3 to regulate recycling of alpha v beta 3 and alpha 5 beta 1 integrins. Mol. Cell. Biol. 24, 1505-1515.
39. Sekiya-Kawasaki, M., Groen, A. C., Cope, M. J., Kaksonen, M., Watson, H. A., Zhang, C., Shokat, K. M., Wendland, B., McDonald, K. L., McCaffery, J. M. et al. (2003). Dynamic phosphoregulation of the cortical actin cytoskeleton and endocytic machinery revealed by real-time chemical genetic analysis. J. Cell Biol. 162, 765-772.
40. Shin, S., Wolgamott, L. and Yoon, S. O. (2012). Integrin trafficking and tumor progression. Int. J. Cell Biol. 2012, 516789.
41. Sorensen, E. B. and Conner, S. D. (2008). AAK1 regulates Numb function at an early step in clathrin-mediated endocytosis. Traffic 9, 1791-1800.
42. Sorensen, E. B. and Conner, S. D. (2010). c-secretase-dependent cleavage initiates notch signaling from the plasma membrane. Traffic 11, 1234-1245.
43. Teckchandani, A., Toida, N., Goodchild, J., Henderson, C., Watts, J., Wollscheid, B. and Cooper, J. A. (2009). Quantitative proteomics identifies a Dab2/integrin module regulating cell migration. J. Cell Biol. 186, 99-111.
44. Tsuruta, D., Gonzales, M., Hopkinson, S. B., Otey, C., Khuon, S., Goldman, R. D. and Jones, J. C. (2002). Microfilament-dependent movement of the beta3 integrin subunit within focal contacts of endothelial cells. FASEB J. 16, 866-868.
45. van der Flier, A. and Sonnenberg, A. (2001). Function and interactions of integrins. Cell Tissue Res. 305, 285-298.
46. Watson, H. A., Cope, M. J., Groen, A. C., Drubin, D. G. and Wendland, B. (2001). In vivo role for actin-regulating kinases in endocytosis and yeast epsin phosphorylation. Mol. Biol. Cell 12, 3668-3679.
47. White, D. P., Caswell, P. T. and Norman, J. C. (2007). alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration. J. Cell Biol. 177, 515-525.
48. Woods, A. J., White, D. P., Caswell, P. T. and Norman, J. C. (2004). PKD1/PKCmu promotes alphavbeta3 integrin recycling and delivery to nascent focal adhesions. EMBO J. 23, 2531-2543.
49. Yan, Q., Sun, W., Kujala, P., Lotfi, Y., Vida, T. A. and Bean, A. J. (2005). CART: an Hrs/actinin-4/BERP/myosin V protein complex required for efficient receptor recycling. Mol. Biol. Cell 16, 2470-2482.