Interactions between EHD proteins and Rab11-FIP2: A role for EHD3 in early endosomal transport

Molecular Biology of the Cell

Volumn 17, Issue 1, 2006, Pages 163-177

  Naslavsky, Naava ^a   Rahajeng, Juliati ^a   Sharma, Mahak ^a   Jović, Marko ^a   Caplan, Steve ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY ENDOSOMAL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR PATHWAY SUBSTRATE 15; EPS15 HOMOLOGY DOMAIN 1 PROTEIN; EPS15 HOMOLOGY DOMAIN 3 PROTEIN; EPS15 HOMOLOGY DOMAIN PROTEIN; MEMBRANE PROTEIN; NUCLEOTIDE; RAB PROTEIN; RAB11 FIP2 PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; INTERNALIZATION; KNOCKOUT GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARALOGY; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RECYCLING;

BIOLOGICAL TRANSPORT; CARRIER PROTEINS; ENDOSOMES; HELA CELLS; HUMANS; NUCLEOTIDES; PROTEIN BINDING; RAB GTP-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; TIME FACTORS; TRANSCRIPTION FACTOR TFIIIA;

EID: 30044449424     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-05-0466     Document Type: Article

References (63)

1. Benmerah, A. (2004). Endocytosis: signaling from endocytic membranes to the nucleus. Curr. Biol. 14, R314-316.
2. Berger, B., Wilson, D. B., Wolf, E., Tonchev, T., Milla, M., and Kim, P. S. (1995). Predicting coiled coils by use of pairwise residue correlations. Proc. Natl. Acad. Sci. USA 92, 8259-8263.
3. Braun, A., Agelet, R.P.I., Dahlhaus, R., Koch, D., Fonarev, P., Grant, B. D., Kessels, M. M., and Qualmann, B. (2005). EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol. Biol. Cell 16, 3642-3658.
4. Caplan, S., Hartnell, L. M., Aguilar, R. C., Naslavsky, N., and Bonifacino, J. S. (2001). Human Vam6p promotes lysosome clustering and fusion in vivo. J. Cell Biol. 154, 109-122.
5. 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.
6. Conner, S. D., and Schmid, S. L. (2003). Regulated portals of entry into the cell. Nature 422, 37-44.
7. Cullis, D. N., Philip, B., Baleja, J. D., and Feig, L. A. (2002). Rab11-FIP2, an adaptor protein connecting cellular components involved in internalization and recycling of epidermal growth factor receptors. J. Biol. Chem. 277, 49158-49166.
8. Daro, E., van der Sluijs, P., Galli, T., and Mellman, I. (1996). Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling. Proc. Natl. Acad. Sci. USA 93, 9559-9564.
9. de Beer, T., Carter, R. E., Lobel-Rice, K. E., Sorkin, A., and Overduin, M. (1998). Structure and Asn-Pro-Phe binding pocket of the Eps15 homology domain. Science 281, 1357-1360.
10. de Beer, T., Hoofnagle, A. N., Enmon, J. L., Bowers, R. C., Yamabhai, M., Kay, B. K., and Overduin, M. (2000). Molecular mechanism of NPF recognition by EH domains. Nat. Struct. Biol. 7, 1018-1022.
11. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498.
12. Fan, G. H., Lapierre, L. A., Goldenring, J. R., Sai, J., and Richmond, A. (2004). Rab11-family interacting protein 2 and myosin Vb are required for CXCR2 recycling and receptor-mediated chemotaxis. Mol. Biol. Cell 101, 2115-2124.
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., Zhang, Y., Paupard, M. C., Lin, S. X., Hall, D. H., and Hirsh, D. (2001). Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat. Cell Biol. 3, 573-579.
15. Gruenberg, J., and Maxfield, F. R. (1995). Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7, 552-563.
16. Guilherme, A., Soriano, N. A., Bose, S., Holik, J., Bose, A., Pomerleau, D. P., Furcinitti, P., Leszyk, J., Corvera, S., and Czech, M. P. (2004a). EHD2 and the novel EH domain binding protein EHBP1 couple endocytosis to the actin cytoskeleton. J. Biol. Chem. 279, 10593-10605.
17. Guilherme, A., Soriano, N. A., Furcinitti, P. S., and Czech, M. P. (2004b). Role of EHD1 and EHBP1 in perinuclear sorting and insulin-regulated GLUT4 recycling in 3T3-L1 adipocytes. J. Biol. Chem. 279, 40062-40075.
18. Hales, C. M., Griner, R., Hobdy-Henderson, K. C., Dorn, M. C., Hardy, D., Kumar, R., Navarre, J., Chan, E. K., Lapierre, L. A., and Goldenring, J. R. (2001). Identification and characterization of a family of Rab11-interacting proteins. J. Biol. Chem. 276, 39067-39075.
19. Hales, C. M., Vaerman, J. P., and Goldenring, J. R. (2002). Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J. Biol. Chem. 277, 50415-50421.
20. Hao, M., and Maxfield, F. R. (2000). Characterization of rapid membrane internalization and recycling. J. Biol. Chem. 275, 15279-15286.
21. Hirst, J., Borner, G. H., Harbour, M., and Robinson, M. S. (2005). The aftiphilin/p200/gamma-synergin complex. Mol. Biol. Cell 16, 2554-2565.
22. Hopkins, C. R., and Trowbridge, I. S. (1983). Internalization and processing of transferrin and the transferrin receptor in human carcinoma A431 cells. J. Cell Biol. 97, 508-521.
23. Jacobson, G. R., and Rosenbusch, J. P. (1976). ATP binding to a protease-resistant core of actin. Proc. Natl. Acad. Sci. USA 73, 2742-2746.
24. Kinosian, H. J., Selden, L. A., Estes, J. E., and Gershman, L. C. (1993). Nucleotide binding to actin. Cation dependence of nucleotide dissociation and exchange rates. J. Biol. Chem. 268, 8683-8691.
25. Lapierre, L. A., Dorn, M. C., Zimmerman, C. F., Navarre, J., Burnette, J. O., and Goldenring, J. R. (2003). Rab11b resides in a vesicular compartment distinct from Rab11a in parietal cells and other epithelial cells. Exp. Cell Res. 290, 322-331.
26. Lee, D. W., Zhao, X., Scarselletta, S., Schweinsberg, P. J., Eisenberg, E., Grant, B. D., and Greene, L. E. (2005). ATP Binding regulates oligomerization and endosome association of RME-1 family proteins. J. Biol. Chem. 280, 17213-17220.
27. 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.
28. Lindsay, A. J., Hendrick, A. G., Cantalupo, G., Senic-Matuglia, F., Goud, B., Bucci, C., and McCaffrey, M. W. (2002). Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein. J. Biol. Chem. 277, 12190-12199.
29. Lindsay, A. J., and McCaffrey, M. W. (2002). Rab11-FIP2 functions in transferrin recycling and associates with endosomal membranes via its COOH-terminal domain. J. Biol. Chem. 277, 27193-27199.
30. Lindsay, A. J., and McCaffrey, M. W. (2004a). The C2 domains of the class I Rab11 family of interacting proteins target recycling vesicles to the plasma membrane. J. Cell Sci. 117, 4365-4375.
31. Lindsay, A. J., and McCaffrey, M. W. (2004b). Characterisation of the Rab binding properties of Rab coupling protein (RCP) by site-directed mutagenesis. FEBS Lett. 571, 86-92.
32. Maxfield, F. R., and McGraw, T. E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell. Biol. 5, 121-132.
33. Mellman, I. (1996). Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12, 575-625.
34. Miliaras, N. B., and Wendland, B. (2004). EH proteins: multivalent regulators of endocytosis (and other pathways). Cell Biochem. Biophys. 41, 295-318.
35. Mintz, L., Galperin, E., Pasmanik-Chor, M., Tulzinsky, S., Bromberg, Y., Kozak, C. A., Joyner, A., Fein, A., and Horowitz, M. (1999). EHD1-an EH-domain-containing protein with a specific expression pattern. Genomics 59, 66-76.
36. Naslavsky, N., Boehm, M., Backlund, P. S., Jr., and Caplan, S. (2004a). Rabenosyn-5 and EHD1 interact and sequentially regulate protein recycling to the plasma membrane. Mol. Biol. Cell 15, 2410-2422.
37. Naslavsky, N., and Caplan, S. (2005). C-terminal EH-domain containing proteins: consensus for a role in endocytic trafficking, EH? J. Cell Sci. 118, 4093-4101.
38. Naslavsky, N., Weigert, R., and Donaldson, J. G. (2004b). Characterization of a non-clathrin endocytic pathway: membrane cargo and lipid requirements. Mol. Biol. Cell 15, 3542-3552.
39. Nichols, B. J., and Lippincott-Schwartz, J. (2001). Endocytosis without clathrin coats. Trends Cell Biol. 11, 406-412.
40. Nielsen, E., Christoforidis, S., Uttenweiler-Joseph, S., Miaczynska, M., Dewitte, F., Wilm, M., Hoflack, B., and Zerial, M. (2000). Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J. Cell Biol. 151, 601-612.
41. Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A., and Ehlers, M. D. (2004a). Recycling endosomes supply AMPA receptors for LTP. Science 305, 1972-1975.
42. Park, S. Y., Ha, B. G., Choi, G. H., Ryu, J., Kim, B., Jung, C. Y., and Lee, W. (2004b). EHD2 interacts with the insulin-responsive glucose transporter (GLUT4) in rat adipocytes and may participate in insulin-induced GLUT4 recruitment. Biochemistry 43, 7552-7562.
43. Peden, A. A., Schonteich, E., Chun, J., Junutula, J. R., Scheller, R. H., and Prekeris, R. (2004). The RCP-Rab11 complex regulates endocytic protein sorting. Mol. Biol. Cell 15, 3530-3541.
44. Picciano, J. A., Ameen, N., Grant, B. D., and Bradbury, N. A. (2003). Rme-1 regulates the recycling of the cystic fibrosis transmembrane conductance regulator. Am. J. Physiol. 285, C1009-C1018.
45. Polo, S., Confalonieri, S., Salcini, A. E., and Di Fiore, P. P. (2003). EH and UIM: endocytosis and more. Sci. STKE 2003, re17.
46. Prekeris, R. (2003). Rabs, Rips, FIPs, and endocytic membrane traffic. Scientific World Journal 3, 870-880.
47. Prekeris, R., Davies, J. M., and Scheller, R. H. (2001). Identification of a novel Rab11/25 binding domain present in Eferin and Rip proteins. J. Biol. Chem. 276, 38966-38970.
48. Ren, M., Xu, G., Zeng, J., De Lemos-Chiarandini, C., Adesnik, M., and Sabatini, D. D. (1998). Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc. Natl. Acad. Sci. USA 95, 6187-6192.
49. Rotem-Yehudar, R., Galperin, E., and Horowitz, M. (2001). Association of insulin-like growth factor 1 receptor with EHD1 and SNAP29. J. Biol. Chem. 276, 33054-33060.
50. Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
51. Salcini, A. E., Confalonieri, S., Doria, M., Santolini, E., Tassi, E., Minenkova, O., Cesareni, G., Pelicci, P. G., and Di Fiore, P. P. (1997). Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev. 11, 2239-2249.
52. Santolini, E., Salcini, A. E., Kay, B. K., Yamabhai, M., and Di Fiore, P. P. (1999). The EH network. Exp. Cell Res. 253, 186-209.
53. Shao, Y., Akmentin, W., Toledo-Aral, J. J., Rosenbaum, J., Valdez, G., Cabot, J. B., Hilbush, B. S., and Halegoua, S. (2002). Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes. J. Cell Biol. 157, 679-691.
54. Sheff, D., Pelletier, L., O'Connell, C. B., Warren, G., and Mellman, I. (2002). Transferrin receptor recycling in the absence of perinuclear recycling endosomes. J. Cell Biol. 156, 797-804.
55. Sheff, D. R., Daro, E. A., Hull, M., and Mellman, I. (1999). The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell Biol. 145, 123-139.
56. Smith, C. A., Dho, S. E., Donaldson, J., Tepass, U., and McGlade, C. J. (2004). The cell fate determinant Numb interacts with EHD/Rme-1 family proteins and has a role in endocytic recycling. Mol. Biol. Cell 15, 3698-3708.
57. Sonnichsen, B., De Renzis, S., Nielsen, E., Rietdorf, J., and Zerial, M. (2000). Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149, 901-914.
58. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M., and Parton, R. G. (1996). Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924.
59. van Dam, E. M., Ten Broeke, T., Jansen, K., Spijkers, P., and Stoorvogel, W. (2002). Endocytosed transferrin receptors recycle via distinct dynamin and phosphatidylinositol 3-kinase-dependent pathways. J. Biol. Chem. 277, 48876-48883.
60. van der Sluijs, P., Hull, M., Webster, P., Male, P., Goud, B., and Mellman, I. (1992). The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70, 729-740.
61. Xu, Y., Shi, H., Wei, S., Wong, S. H., and Hong, W. (2004). Mutually exclusive interactions of EHD1 with GS32 and Syndapin H. Mol. Membr. Biol. 21, 269-277.
62. Yamashiro, D. J., Tycko, B., Fluss, S. R., and Maxfield, F. R. (1984). Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37, 789-800.
63. Zeng, J., et al. (1999). Identification of a putative effector protein for rab11 that participates in transferrin recycling. Proc. Natl. Acad. Sci. USA 96, 2840-2845.