Genome-wide investigation of the rab binding activity of RUN domains: Development of a novel tool that specifically traps GTP-rab35

Cell Structure and Function

Volumn 36, Issue 2, 2011, Pages 155-170

  Fukuda, Mitsunori ^a   Kobayashi, Hotaka ^a   Ishibashi, Koutaro ^a   Ohbayashi, Norihiko ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Rab effector domain; Rab35; RUN and FYVE domain containing (RUFY); RUN and SH3 domain containing 2 (RUSC2); RUN domain

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PROTEIN DENND5A; PROTEIN DENND5B; PROTEIN PLEKHM2; PROTEIN RAB1; PROTEIN RAB1A; PROTEIN RAB33; PROTEIN RAB35; PROTEIN RAB41; PROTEIN RAB6A; PROTEIN RAB6B; PROTEIN RUFY2; PROTEIN RUFY3; PROTEIN RUSC2; RAB BINDING DOMAIN SPECIFIC FOR RAB35; RAB PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL STRAIN; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; MOLECULAR CLONING; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; RUN DOMAIN;

ANIMALS; CARRIER PROTEINS; GENOME; GENOME-WIDE ASSOCIATION STUDY; GUANOSINE TRIPHOSPHATE; HUMANS; MICE; NEURITES; NUCLEAR PROTEINS; PC12 CELLS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RATS; RECOMBINANT PROTEINS;

EID: 80052741612     PISSN: 03867196     EISSN: 13473700     Source Type: Journal    
DOI: 10.1247/csf.11001     Document Type: Article

References (51)

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. Bayer, M., Fischer, J., Kremerskothen, J., Ossendorf, E., Matanis, T., Konczal, M., Weide, T., and Barnekow, A. 2005. Identification and characterization of Iporin as a novel interaction partner for rab1. BMC Cell Biol., 6: 15.
3. Bernards, A. 2003. GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila. Biochim. Biophys. Acta, 1603: 47-82.
4. Bock, J.B., Matern, H.T., Peden, A.A., and Scheller, R.H. 2001. A genomic perspective on membrane compartment organization. Nature, 409: 839-841.
5. Callebaut, I., de Gunzburg, J., Goud, B., and Mornon, J.P. 2001. RUN domains: a new family of domains involved in Ras-like GTPase signaling. Trends Biochem. Sci., 26: 79-83.
6. 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.
7. Cormont, M., Mari, M., Galmiche, A., Hofman, P., and Le Marchand-Brustel, Y. 2001. A FYVE-finger-containing protein, Rabip4, is a Rab4 effector involved in early endosomal traffic. Proc. Natl. Acad. Sci. USA, 98: 1637-1642.
8. 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.
9. Fukuda, M. and Mikoshiba, K. 2000. Expression of synaptotagmin I or II promotes neurite outgrowth in PC12 cells. Neurosci. Lett., 295: 33-36.
10. Fukuda, M. 2003. Distinct Rab binding specificity of Rim1, Rim2, rabphilin, and Noc2: identification of a critical determinant of Rab3A/Rab27A recognition by Rim2. J. Biol. Chem., 278: 15373-15380.
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. 2008. Regulation of secretory vesicle traffic by Rab small GTPases. Cell. Mol. Life Sci., 65: 2801-2813.
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. 2010. How can mammalian Rab small GTPases be comprehensively analyzed?: Development of new tools to comprehensively analyze mammalian Rabs in membrane traffic. Histol. Histopathol., 25: 1473-1480.
15. Fukuda, M. 2011. TBC proteins: GAPs for mammalian small GTPase Rab? Biosci. Reports, 31: 159-168.
16. Crosshans, B.L., Ortiz, D., and Novick, P. 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. USA, 103: 11821-11827.
17. Haas, A.K., Fuchs, E., Kopajtich, R., and Barr, F.A. 2005. A GTPase-activating protein controls Rab5 function in endocytic trafficking. Nat. Cell Biol., 7: 887-893.
18. Holt, O., Kanno, E., Bossi, G., Booth, S., Daniele, T., Santoro, A., Arico, M., Saegusa, C., Fukuda, M., and Griffiths, G.M. 2008. Slp1 and Slp2-a localize to the plasma membrane of CTL and contribute to secretion from the immunological synapse. Traffic, 9: 446-457.
19. Hsu, C., Morohashi, Y., Yoshimura, S., Manrique-Hoyos, N., Jung, S., Lauterbach, M.A., Bakhti, M., Grønborg, M., Möbius, W., Rhee, J., Barr, F.A., and Simons, M. 2010. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J. Cell Biol., 189: 223-232.
20. Imai, A., Yoshie, S., Nashida, T., Fukuda, M., and Shimomura, H. 2009. Redistribution of small GTP-binding protein, Rab27B, in rat parotid acinar cells after stimulation with isoproterenol. Eur. J. Oral Sci., 117: 224-230.
21. Itoh, T. and Fukuda, M. 2006. Identification of EPI64 as a GTPase-activating protein specific for Rab27A. J. Biol. Chem., 281: 31823-31831.
22. Itoh, T., Satoh, M., Kanno, E., and Fukuda, M. 2006. Screening for target Rabs of TBC (Tre-2/Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity. Genes Cells, 11: 1023-1037.
23. Itoh, T., Fujita, N., Kanno, E., Yamamoto, A., Yoshimori, T., and Fukuda, M. 2008. Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol. Biol. Cell, 19: 2916-2925.
24. James, P., Halladay, J., and Craig, E.A. 1996. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics, 144: 1425-1436.
25. Janoueix-Lerosey, I., Pasheva, E., de Tand, M.F., Tavitian, A., and de Gunzburg, J. 1998. Identification of a specific effector of the small GTP-binding protein Rap2. Eur. J. Biochem., 252: 290-298.
26. Kanno, E., Ishibashi, K., Kobayashi, H., Matsui, T., Ohbayashi, N., and Fukuda, M. 2010. Comprehensive screening for novel Rab-binding proteins by GST pull-down assay using 60 different mammalian Rabs. Traffic, 11: 491-507.
27. 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.
28. Kukimoto-Niino, M., Takagi, T., Akasaka, R., Murayama, K., Uchikubo-Kamo, T., Terada, T., Inoue, M., Watanabe, S., Tanaka, A., Hayashizaki, Y., Kigawa, T., Shirouzu, M., and Yokoyama, S. 2006. Crystal structure of the RUN domain of the RAP2-interacting protein x. J. Biol. Chem., 281: 31843-31853.
29. Kuroda, T.S., Ariga, H., and Fukuda, M. 2003. The actin-binding domain of Slac2-a/melanophilin is required for melanosome distribution in melanocytes. Mol. Cell. Biol., 23: 5245-5255.
30. Levivier, E., Goud, B., Souchet, M., Calmels, T.P.G., Mornon, J.P., and Callebaut, I. 2001. uDENN, DENN, and dDENN: Indissociable domains in Rab and MAP kinases signaling pathways. Biochem. Biophys. Res. Commun., 287: 688-695.
31. Marat, A.L. and McPherson, P.S. 2010. The connecdenn family, Rab35 guanine nucleotide exchange factors interfacing with the clathrin machinery. J. Biol. Chem., 285: 10627-10637.
32. Mari, M., Macia, E., Le Marchand-Brustel, Y., and Cormont, M. 2001. Role of the FYVE finger and the RUN domain for the subcellular localization of Rabip4. J. Biol. Chem., 276: 42501-42508.
33. Matsuda, S., Miyazaki, K., Ichigotani, Y., Kurata, H., Takenouchi, Y., Yamamoto, T., Nimura, Y., Irimura, T., Nakatsugawa, S., and Hamaguchi, M. 2000. Molecular cloning and characterization of a novel human gene (NESCA) which encodes a putative adapter protein containing SH3. Biochim. Biophys. Acta., 1491: 321-326.
34. Mori, T., Wada, T., Suzuki, T., Kubota, Y., and Inagaki, N. 2007. Singar1, a novel RUN domain-containing protein, suppresses formation of surplus axons for neuronal polarity. J. Biol. Chem., 282: 19884-19893.
35. Ogura, K., Shirakawa, M., Barnes, T.M., Hekimi, S., and Ohshima, Y. 1997. The UNC-14 protein required for axonal elongation and guidance in Caenorhabditis elegans interacts with the serine/threonine kinase UNC-51. Genes Dev., 11: 1801-1811.
36. Pankiv, S., Alemu, E.A., Brech, A., Bruun, J.A., Lamark, T., Overvatn, A., Bjørkøy, G., and Johansen, T. 2010. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J. Cell Biol., 188: 253-269.
37. 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.
38. Pereira-Leal, J.B. and Seabra, M.C. 2001. Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol., 313: 889-901.
39. Recacha, R., Boulet, A., Jollivet, F., Monier, S., Houdusse, A., Goud, B., and Khan, A.R. 2009. Structural basis for recruitment of Rab6-interacting protein 1 to Golgi via a RUN domain. Structure, 17: 21-30.
40. 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.
41. Schwartz, S.L., Cao, C., Pylypenko, O., Rak, A., and Wandinger-Ness, A. 2007. Rab GTPases at a glance. J. Cell Sci., 120: 3905-3910.
42. 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.
43. Stenmark, H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol., 10: 513-525.
44. Tabata, K., Matsunaga, K., Sakane, A., Sasaki, T., Noda, T., and Yoshimori, T. 2010. Rubicon and PLEKHM1 negatively regulate the endocytic/autophagic pathway via a novel Rab7-binding domain. Mol. Biol. Cell, 21: 4162-4172.
45. Takai, Y., Sasaki, T., and Matozaki, T. 2001. Small GTP-binding proteins. Physiol. Rev., 81: 153-208.
46. Tamura, K., Ohbayashi, N., Maruta, Y., Kanno, E., Itoh, T., and Fukuda, M. 2009. Varp is a novel Rab32/38-binding protein that regulates Tyrp1 trafficking in melanocytes. Mol. Biol. Cell, 20: 2900-2908.
47. Yamamoto, H., Koga, H., Katoh, Y., Takahashi, S., Nakayama, K., and Shin, H.W. 2010. Functional cross-talk between Rab14 and Rab4 through a dual effector, RUFY1/Rabip4. Mol. Biol. Cell, 21: 2746-2755.
48. Yang, H., Sasaki, T., Minoshima, S., and Shimizu, N. 2007. Identification of three novel proteins (SGSM1, 2, 3) which modulate small G protein (RAP and RAB)-mediated signaling pathway. Genomics, 90: 249-260.
49. Yoshimura, S.I., Gerondopoulos, A., Linford, A., Rigden, D.J., and Barr, F.A. 2010. Family-wide characterization of the DENN domain Rab GDP-GTP exchange factors. J. Cell Biol., 191: 367-381.
50. Zerial, M. and McBride, H. 2001. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol., 2: 107-117.
51. Zhang, J., Fonovic, M., Suyama, K., Bogyo, M., and Scott, M.P. 2009. Rab35 controls actin bundling by recruiting fascin as an effector protein. Science, 325: 1250-1254.