Distinct roles of Rab11 and Arf6 in the regulation of Rab11-FIP3/arfophilin-1 localization in mitotic cells

Genes to Cells

Volumn 16, Issue 9, 2011, Pages 938-950

  Takahashi, Senye ^a   Takei, Tomomi ^a   Koga, Hiroshi ^a,b   Takatsu, Hiroyuki ^a   Shin, Hye Won ^a   Nakayama, Kazuhisa ^a  

^a KYOTO UNIVERSITY   (Japan)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; FIP3 PROTEIN; FIP4 PROTEIN; RAB11 PROTEIN; UNCLASSIFIED DRUG;

ABSCISSION; ANIMAL CELL; ARTICLE; CELL DIVISION; CYTOKINESIS; DNA TRANSFECTION; FEMALE; GENE CONTROL; HELA CELL; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ADP-RIBOSYLATION FACTORS; CARRIER PROTEINS; CELL DIVISION; CELL LINE, TUMOR; CYTOKINESIS; ENDOSOMES; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; I-KAPPA B KINASE; MICROSCOPY, FLUORESCENCE; MITOSIS; PROTEIN BINDING; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RNA, SMALL INTERFERING; TIME-LAPSE IMAGING;

EID: 80052264931     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/j.1365-2443.2011.01538.x     Document Type: Article

References (49)

1. Boman, A.L., Kuai, J., Zhu, X., Chen, J., Kuriyama, R. & Kahn, R.A. (1999) Arf proteins binds to mitotic kinesin-like protein 1 (MKLP1) in a GTP-dependent fashion. Cell Motil. Cytoskeleton 44, 119-132.
2. D'Souza-Schorey, C. & Chavrier, P. (2006) ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358.
3. Eathiraj, S., Mishra, A., Prekeris, R. & Lambright, D.G. (2006) Structural basis for Rab11-mediated recruitment of FIP3 to recycling endosomes. J. Mol. Biol. 364, 121-135.
4. Fielding, A.B., Schonteich, E., Matheson, J., Wilson, G., Yu, X., Hickson, G.R.X., Srivastava, S., Baldwin, S.A., Prekeris, R. & Gould, G.W. (2005) Rab11-FIP3 and FIP4 interact with Arf6 and the Exocyst to control membrane traffic in cytokinesis. EMBO J. 24, 3389-3399.
5. Gillingham, A.K. & Munro, S. (2007) The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 23, 579-611.
6. Gromley, A., Yeaman, C., Rosa, J., Redick, S., Chen, C.-T., Mirabelle, S., Guha, M., Suillibourne, J. & Doxsey, S.J. (2005) Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123, 75-87.
7. Grosshans, B.L., Ortiz, D. & Novick, P. (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl Acad. Sci. USA 103, 11821-11827.
8. Hayashi, K., Yonemura, S., Matsui, T., Tsukita, S. & Tsukita, S. (1999) Immunofluorescence detection of ezrin/radixin/moesin (ERM) proteins with their carboxyl-terminal threonine phosphorylated in cultured cells and tissues: application of a novel fixation protocol using trichloroacetic acid (TCA) as a fixative. J. Cell Sci. 122, 1149-1158.
9. Hickson, G.R.X., Mateson, J., Riggs, B., Maier, V.H., Fielding, A.B., Prekeris, R., Sullivan, W., Barr, F.A. & Gould, G.W. (2003) Arfophilins are dual Arf/Rab11 binding proteins that regulate recycling endosome distribution and are related to Drosophila nuclear fallout. Mol. Biol. Cell 14, 2908-2920.
10. Horgan, C.P., Oleksy, A., Zhdanov, A.V., Lall, P.Y., White, I.J., Khan, A.R., Futter, C.E., McCaffrey, J.G. & McCaffrey, M.W. (2007) Rab11-FIP3 is critical for the structural integrity of the endosomal-recycling compartment. Traffic 8, 414-430.
11. Horgan, C.P., Walsh, M., Zurawski, T.H. & McCaffrey, M.W. (2004) Rab11-FIP3 localises to a Rab11-positive pericentrosomal compartment during interphase and to the cleavage furrow during cytokinesis. Biochem. Biophys. Res. Commun. 319, 83-94.
12. Hosaka, M., Toda, K., Takatsu, H., Torii, S., Murakami, K. & Nakayama, K. (1996) Structure and intracellular localization of mouse ADP-ribosylation factors type 1 to type 6 (ARF1-ARF6). J. Biochem. 120, 813-819.
13. Jagoe, W.N., Lindsay, A.J., Read, R.J., McCoy, A.J., McCaffrey, M.W. & Khan, A.R. (2006) Crystal structure of Rab11 in complex with Rab11 family interacting protein 2. Structure 14, 1273-1283.
14. Jing, J., Tarbutton, E., Wilson, G. & Prekeris, R. (2009) Rab11-FIP3 is a Rab11-binding protein that regulates breast cancer cell motility by modulating the actin cytoskeleton. Eur. J. Cell Biol. 88, 325-341.
15. Junutula, J.R., Schonteich, E., Wilson, G.M., Peden, A.A., Scheller, R. & Prekeris, R. (2004) Molecular characterization of Rab11 interactions with members of the family of Rab11-interacting proteins. J. Biol. Chem. 279, 33430-33437.
16. Kahn, R.A., Cherfils, J., Elias, M., Lovering, R.C., Munro, S. & Schurmann, A. (2006) Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins. J. Cell Biol. 172, 645-650.
17. Li, J., Peters, P.J., Bai, M., Dai, J., Bos, E., Kirchhausen, T., Kandror, K.V. & Hsu, V.W. (2007) An ACAP1-containing clathrin coat complex for endocytic recycling. J. Cell Biol. 178, 453-464.
18. Low, S.H., Li, X., Miura, M., Kudo, N., Quiñones, B. & Weimbs, T. (2003) Syntaxin 2 and endobrevin are required for the terminal step of cytokinesis in mammalian cells. Dev. Cell 4, 753-759.
19. Mazelova, J., Astuto-Gribble, L., Inoue, H., Tam, B.M., Schonteich, E., Prekeris, R., Moritz, O.L., Randazzo, P.A. & Deretic, D. (2009) Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J. 28, 183-192.
20. Meyers, J.M. & Prekeris, R. (2002) Formation of mutually exclusive Rab11 complexes with members of the family of Rab11-interacting proteins regulates Rab11 endocytic targeting and function. J. Biol. Chem. 277, 49003-49010.
21. Mishima, M., Kaitna, S. & Glotzer, M. (2002) Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell 2, 41-54.
22. Montagnac, G., Echard, A. & Chavrier, P. (2008) Endocytic traffic in animal cell cytokinesis. Curr. Opin. Cell Biol. 20, 454-461.
23. Montagnac, G., Sibarita, J.-B., Loubéry, S., Daviet, L., Romao, M., Raposo, G. & Chavrier, P. (2009) ARF6 interacts with JIP4 to control a motor switch mechanism regulating endosome traffic in cytokinesis. Curr. Biol. 19, 184-195.
24. Moss, J. & Vaughan, M. (1995) Structure and function of ARF proteins: activators of cholera toxin and critical components of intracellular vesicular transport processes. J. Biol. Chem. 270, 12327-12330.
25. Mukai, A., Mizuno, E., Kobayashi, K., Matsumoto, M., Nakayama, K.-I., Kitamura, N. & Komada, M. (2008) Dynamic regulation of ubiquitylation and deubiquitylation at the central spindle during cytokinesis. J. Cell Sci. 121, 1325-1333.
26. Prekeris, R. & Gould, G.W. (2008) Breaking up is hard to do: membrane traffic in cytokinesis. J. Cell Sci. 121, 1569-1576.
27. Prigent, M., Dubois, T., Raposo, G., Derrien, V., Tenza, D., Rossé, C., Camonis, J. & Chavrier, P. (2003) ARF6 controls post-endocytic recycling through its downstream exocyst complex effector. J. Cell Biol. 163, 1111-1121.
28. Riggs, B., Rothwell, W., Mische, S., Hickson, G.R.X., Matheson, J., Hays, T., Gould, G.W. & Sullivan, W. (2003) Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J. Cell Biol. 163, 143-154.
29. Schiel, J.A., Park, K., Morphew, M.K., Reid, E., Hoenger, A. & Prekeris, R. (2011) Endocytic membrane fusion and buckling-induced microtubule severing mediate cell abscission. J. Cell Sci. 124, 1411-1424.
30. Schiel, J.A. & Prekeris, R. (2010) Making the final cut: mechanisms mediating the abscission step of cytokinesis. Scientific World J. 10, 1424-1434.
31. Schonteich, E., Pilli, M., Simon, G.C., Matern, H.T., Junutula, J.R., Sentz, D., Holmes, R.K. & Prekeris, R. (2007) Molecular characterization of Rab11-FIP3 binding to ARF GTPases. Eur. J. Cell Biol. 86, 417-431.
32. Schweitzer, J.K. & D'Souza-Schorey, C. (2005) A requirement for ARF6 during the completion of cytokinesis. Exp. Cell Res. 311, 74-83.
33. Segev, N. (2001) Ypt and Rab GTPases: insight into functions through novel interactions. Curr. Opin. Cell Biol. 13, 500-511.
34. Shaner, N.C., Steinbach, P.A. & Tsien, R.Y. (2005) A guide to choosing fluorescent proteins. Nat. Methods 2, 905-909.
35. Shiba, T., Koga, H., Shin, H.-W., Kawasaki, M., Kato, R., Nakayama, K. & Wakatsuki, S. (2006) Structural basis for Rab11-dependent membrane recruitment of family of Rab11-interacting protein (FIP3)/Arfophilin-1. Proc. Natl Acad. Sci. USA 103, 15416-15421.
36. Shin, H.-W., Kobayashi, H., Kitamura, M., Waguri, S., Suganuma, T., Uchiyama, Y. & Nakayama, K. (2005) Roles of ARFRP1 (ADP-ribosylation factor-related protein 1) in post-Golgi membrane trafficking. J. Cell Sci. 118, 4039-4048.
37. Shin, H.-W., Morinaga, N., Noda, M. & Nakayama, K. (2004) BIG2, a guanine nucleotide exchange factor for ADP-ribosylation factors: its localization to recycling endosomes and implication in the endosome integrity. Mol. Biol. Cell 15, 5283-5294.
38. Shin, H.-W., Shinotsuka, C., Torii, S., Murakami, K. & Nakayama, K. (1997) Identification and subcellular localization of a novel mammalian dynamin-related protein homologous to yeast Vps1p and Dnm1p. J. Biochem. 122, 525-530.
39. Shin, O.-H., Couvillon, A.D. & Exton, J.H. (2001) Arfophilin is a common target of both class II and class III ADP-ribosylation factors. Biochemistry 40, 10846-10852.
40. Simon, G.C., Schonteich, E., Wu, C.C., Piekny, A., Ekiert, D., Yu, X., Gould, G.W., Glotzer, M. & Prekeris, R. (2008) Sequential Cyk-4 binding to ECT2 and FIP3 regulates cleavage furrow ingression and abscission during cytokinesis. EMBO J. 27, 1791-1803.
41. Steigemann, P. & Gerlich, D.W. (2009) Cytokinetic abscission: cellular dynamics at the midbody. Trends Cell Biol. 19, 606-616.
42. Stenmark, H. (2009) Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525.
43. Takahashi, S., Nakagawa, T., Banno, T., Watanabe, T., Murakami, K. & Nakayama, K. (1995) Localization of furin to the trans-Golgi network and recycling from the cell surface involves Ser and Tyr residues within the cytoplasmic domain. J. Biol. Chem. 270, 28397-28401.
44. Takatsu, H., Yoshino, K., Toda, K. & Nakayama, K. (2002) GGA proteins associate with Golgi membranes through interaction between their GGAH domains and ADP-ribosylation factors. Biochem. J. 365, 369-378.
45. Wallace, D.M., Lindsay, A.J., Hedrick, A.G. & McCaffrey, M.W. (2002) The novel Rab11-FIP/Rip/RCP family of proteins displays extensive homo- and hetero-interacting abilities. Biochem. Biophys. Res. Commun. 292, 909-915.
46. Wilson, G.M., Fielding, A.B., Simon, G.C., Yu, X., Andrews, P.D., Hames, R.S., Frey, A.M., Peden, A.A., Gould, G.W. & Prekeris, R. (2005) The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol. Biol. Cell 16, 849-860.
47. Yu, X., Prekeris, R. & Gould, G.W. (2007) Role of endosomal Rab GTPases in cytokinesis. Eur. J. Cell Biol. 86, 25-35.
48. Zerial, M. & McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117.
49. Zhang, X.-M., Ellis, S., Sriratana, A., Mitchell, C.A. & Rowe, T. (2004) Sec15 is an effector for the Rab11 GTPase in mammalian cells. J. Biol. Chem. 279, 43027-43034.