Rab35 establishes the EHD1-association site by coordinating two distinct effectors during neurite outgrowth

Journal of Cell Science

Volumn 126, Issue 11, 2013, Pages 2424-2435

  Kobayashi, Hotaka ^a   Fukuda, Mitsunori ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

ACAP2; Arf6; Centaurin 2; EHD1; Endocytic recycling; MICAL L1; Neurite outgrowth; Rab35

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CELL PROTEIN; CENTAURIN BETA2; EHD1 PROTEIN; MICAL L1 PROTEIN; NERVE GROWTH FACTOR; RAB PROTEIN; RAB35 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL MIGRATION; CELL STIMULATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; NERVE FIBER GROWTH; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

ACAP2; ARF6; CENTAURIN-Β2; EHD1; ENDOCYTIC RECYCLING; MICAL-L1; NEURITE OUTGROWTH; RAB35;

ADP-RIBOSYLATION FACTORS; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOSOMES; GTPASE-ACTIVATING PROTEINS; NERVE TISSUE PROTEINS; NEURITES; PC12 CELLS; RAB GTP-BINDING PROTEINS; RATS; VESICULAR TRANSPORT PROTEINS;

EID: 84880018040     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.117846     Document Type: Article

References (39)

1. Allaire, P. D., Marat, A. L., Dall'Armi, C., Di Paolo, G., McPherson, P. S. and Ritter, B. (2010). The Connecdenn DENN domain: a GEF for Rab35 mediating cargo-specific exit from early endosomes. Mol. Cell 37, 370-382.
2. Barr, F. and Lambright, D. G. (2010). Rab GEFs and GAPs. Curr. Opin. Cell Biol. 22, 461-470.
3. Brown, F. D., Rozelle, A. L., Yin, H. L., Balla, T. and Donaldson, J. G. (2001). Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J. Cell Biol. 154, 1007-1018.
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. Chevallier, J., Koop, C., Srivastava, A., Petrie, R. J., Lamarche-Vane, N. and Presley, J. F. (2009). Rab35 regulates neurite outgrowth and cell shape. FEBS Lett. 583, 1096-1101.
6. Dambournet, D., Machicoane, M., Chesneau, L., Sachse, M., Rocancourt, M., El Marjou, A., Formstecher, E., Salomon, R., Goud, B. and Echard, A. (2011). Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nat. Cell Biol. 13, 981-988.
7. de Curtis, I. (2001). Cell migration: GAPs between membrane traffic and the cytoskeleton. EMBO Rep. 2, 277-281.
8. Donaldson, J. G. (2003). Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J. Biol. Chem. 278, 41573-41576.
9. Fukuda, M. (2002). Synaptotagmin-like protein (Slp) homology domain 1 of Slac2-a/ melanophilin is a critical determinant of GTP-dependent specific binding to Rab27A. J. Biol. Chem. 277, 40118-40124.
10. Fukuda, M. (2008). Regulation of secretory vesicle traffic by Rab small GTPases. Cell. Mol. Life Sci. 65, 2801-2813.
11. Fukuda, M. and Kanno, E. (2005). Analysis of the role of Rab27 effector Slp4-a/ granuphilin-a in dense-core vesicle exocytosis. Methods Enzymol. 403, 445-457.
12. Fukuda, M., Kanno, E. and Mikoshiba, K. (1999). Conserved N-terminal cysteine motif is essential for homo- and heterodimer formation of synaptotagmins III, V, VI, and X. J. Biol. Chem. 274, 31421-31427.
13. Fukuda, M., Kanno, E., Ishibashi, K. and Itoh, T. (2008). Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity. Mol. Cell. Proteomics 7, 1031-1042.
14. Fukuda, M., Kobayashi, H., Ishibashi, K. and Ohbayashi, N. (2011). Genome-wide investigation of the Rab binding activity of RUN domains: development of a novel tool that specifically traps GTP-Rab35. Cell Struct. Funct. 36, 155-170.
15. Grant, B. D. and Donaldson, J. G. (2009). Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10, 597-608.
16. Grant, B. and Hirsh, D. (1999). Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10, 4311-4326.
17. Hancock, J. F., Cadwallader, K., Paterson, H. and Marshall, C. J. (1991). A CAAX or a CAAL motif and a second signal are sufficient for plasma membrane targeting of ras proteins. EMBO J. 10, 4033-4039.
18. Jackson, T. R., Brown, F. D., Nie, Z., Miura, K., Foroni, L., Sun, J., Hsu, V. W., Donaldson, J. G. and Randazzo, P. A. (2000). ACAPs are arf6 GTPase-activating proteins that function in the cell periphery. J. Cell Biol. 151, 627-638.
19. Jović, M., Naslavsky, N., Rapaport, D., Horowitz, M. and Caplan, S. (2007). EHD1 regulates b1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J. Cell Sci. 120, 802-814.
20. Jović, M., Kieken, F., Naslavsky, N., Sorgen, P. L. and Caplan, S. (2009). Eps15 homology domain 1-associated tubules contain phosphatidylinositol-4-phosphate and phosphatidylinositol-(4,5)-bisphosphate and are required for efficient recycling. Mol. Biol. Cell 20, 2731-2743.
21. Kanno, E., Ishibashi, K., Kobayashi, H., Matsui, T., Ohbayashi, N. and Fukuda, M. (2010). Comprehensive screening for novel Rab-binding proteins by GST pulldown assay using 60 different mammalian Rabs. Traffic 11, 491-507.
22. Kobayashi, H. and Fukuda, M. (2012). Rab35 regulates Arf6 activity through centaurin-b2 (ACAP2) during neurite outgrowth. J. Cell Sci. 125, 2235-2243.
23. Kouranti, I., Sachse, M., Arouche, N., Goud, B. and Echard, A. (2006). Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr. Biol. 16, 1719-1725.
24. Kuroda, T. S. and Fukuda, M. (2004). Rab27A-binding protein Slp2-a is required for peripheral melanosome distribution and elongated cell shape in melanocytes. Nat. Cell Biol. 6, 1195-1203.
25. Lin, S. X., Grant, B., Hirsh, D. and Maxfield, F. R. (2001). Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat. Cell Biol. 3, 567-572.
26. Maxfield, F. R. and McGraw, T. E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132.
27. Montagnac, G. and Chavrier, P. (2008). Endosome positioning during cytokinesis. Biochem. Soc. Trans. 36, 442-443.
28. Naslavsky, N. and Caplan, S. (2011). EHD proteins: key conductors of endocytic transport. Trends Cell Biol. 21, 122-131.
29. Patino-Lopez, G., Dong, X., Ben-Aissa, K., Bernot, K. M., Itoh, T., Fukuda, M., Kruhlak, M. J., Samelson, L. E. and Shaw, S. (2008). Rab35 and its GAP EPI64C in T cells regulate receptor recycling and immunological synapse formation. J. Biol. Chem. 283, 18323-18330.
30. Rahajeng, J., Giridharan, S. S. P., Cai, B., Naslavsky, N. and Caplan, S. (2012). MICAL-L1 is a tubular endosomal membrane hub that connects Rab35 and Arf6 with Rab8a. Traffic 13, 82-93.
31. Sann, S., Wang, Z., Brown, H. and Jin, Y. (2009). Roles of endosomal trafficking in neurite outgrowth and guidance. Trends Cell Biol. 19, 317-324.
32. Sato, M., Sato, K., Liou, W., Pant, S., Harada, A. and Grant, B. D. (2008). Regulation of endocytic recycling by C. elegans Rab35 and its regulator RME-4, a coated-pit protein. EMBO J. 27, 1183-1196.
33. Scita, G. and Di Fiore, P. P. (2010). The endocytic matrix. Nature 463, 464-473.
34. Sharma, M., Giridharan, S. S. P., 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.
35. Shim, J., Lee, S. M., Lee, M. S., Yoon, J., Kweon, H. S. and Kim, Y. J. (2010). Rab35 mediates transport of Cdc42 and Rac1 to the plasma membrane during phagocytosis. Mol. Cell. Biol. 30, 1421-1433.
36. Sorkin, A. and von Zastrow, M. (2009). Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622.
37. Stenmark, H. (2009). Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525.
38. van Ijzendoorn, S. C. D. (2006). Recycling endosomes. J. Cell Sci. 119, 1679-1681.
39. Zerial, M. and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117.