Comprehensive screening for novel rab-binding proteins by GST pull-down assay using 60 different mammalian rabs

Traffic

Volumn 11, Issue 4, 2010, Pages 491-507

  Kanno, Eiko ^a   Ishibashi, Koutaro ^a   Kobayashi, Hotaka ^a   Matsui, Takahide ^a   Ohbayashi, Norihiko ^a   Fukuda, Mitsunori ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Comprehensive screening; Effector; GTPase activating protein; Membrane traffic; Rab; Tre 2 Bub2 Cdc16 domain

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ANKYRIN; ARF PROTEIN; BINDING PROTEIN; GLUTATHIONE TRANSFERASE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RAB BINDING PROTEIN; RAB PROTEIN; RAB22 BINDING PROTEIN; RAB35 BINDING PROTEIN; RAB36 BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL LYSATE; CELL MEMBRANE; CELL STRAIN; CELL STRAIN 3T3; CONTROLLED STUDY; ENZYME ASSAY; GENE INACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MAMMAL; MASS SPECTROMETRY; MEMBRANE TRANSPORT; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

ADP-RIBOSYLATION FACTORS; ANIMALS; ANKYRIN REPEAT; GLUTATHIONE TRANSFERASE; GTPASE-ACTIVATING PROTEINS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MONOMERIC GTP-BINDING PROTEINS; NEURITES; PC12 CELLS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RAB GTP-BINDING PROTEINS; RATS;

EID: 77951754492     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2010.01038.x     Document Type: Article

References (53)

1. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001, 2:107-117.
2. Pfeffer SR. Rab GTPases: specifying and deciphering organelle identity and function. Trends Cell Biol 2001, 11:487-491.
3. Pereira-Leal JB, Seabra MC. Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 2001, 313:889-901.
4. Bock JB, Matern HT, Peden AA, Scheller RH. A genomic perspective on membrane compartment organization. Nature 2001, 409:839-841.
5. Itoh T, Satoh M, Kanno E, Fukuda M. Screening for target Rabs of TBC (Tre-2 /Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity. Genes Cells 2006, 11:1023-1037.
6. Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci USA 2006, 103:11821-11827.
7. Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A. Rab GTPases at a glance. J Cell Sci 2007, 120:3905-3910.
8. Fukuda M, Kanno E, Ishibashi K, Itoh T. Large scale screening for novel Rab effectors reveals unexpected broad Rab binding specificity. Mol Cell Proteomics 2008, 7:1031-1042.
9. Bernards A. GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila. Biochim Biophys Acta 2003, 1603:47-82.
10. Randazzo PA, Hirsch DS. Arf GAPs: multifunctional proteins that regulate membrane traffic and actin remodelling. Cell Signal 2004, 16:401-413.
11. Cuif MH, Possmayer F, Zander H, Bordes N, Jollivet F, Couedel-Courteille A, Janoueix-Lerosey I, Langsley G, Bornens M, Goud B. Characterization of GAPCenA, a GTPase activating protein for Rab6, part of which associates with the centrosome. EMBO J 1999, 18:1772-1782.
12. Kuroda TS, Fukuda M. Identification and biochemical analysis of Slac2-c/MyRIP as a Rab27A-, myosin Va/VIIa-, and actin-binding protein. Methods Enzymol 2005, 403:431-444.
13. Alory C, Balch WE. Organization of the Rab-GDI/CHM superfamily: the functional basis for choroideremia disease. Traffic 2001, 2:532-543.
14. Seabra MC, Wasmeier C. Controlling the location and activation of Rab GTPases. Curr Opin Cell Biol 2004, 16:451-457.
15. Fukuda M. Distinct Rab binding specificity of Rim1, Rim2, rabphilin, and Noc2: identification of a critical determinant of Rab3A/Rab27A recognition by Rim2. J Biol Chem 2003, 278:15373-15380.
16. Fukuda M, Kanno E, Yamamoto A. Rabphilin and Noc2 are recruited to dense-core vesicles through specific interaction with Rab27A in PC12 cells. J Biol Chem 2004, 279:13065-13075.
17. Hoffenberg S, Liu X, Nikolova L, Hall HS, Dai W, Baughn RE, Dickey BF, Barbieri MA, Aballay A, Stahl PD, Knoll BJ. A novel membrane-anchored Rab5 interacting protein required for homotypic endosome fusion. J Biol Chem 2000, 275:24661-24669.
18. Matanis T, Akhmanova A, Wulf P, Del Nery E, Weide T, Stepanova T, Galjart N, Grosveld F, Goud B, De Zeeuw CI, Barnekow A, Hoogenraad CC. Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex. Nat Cell Biol 2002, 4:986-992.
19. Johansson M, Rocha N, Zwart W, Jordens I, Janssen L, Kuijl C, Olkkonen VM, Neefjes J. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor βIII spectrin. J Cell Biol 2007, 176:459-471.
20. Junutula JR, Schonteich E, Wilson GM, Peden AA, Scheller RH, Prekeris R. Molecular characterization of Rab11 interactions with members of the family of Rab11-interacting proteins. J Biol Chem 2004, 279:33430-33437.
21. Eathiraj S, Pan X, Ritacco C, Lambright DG. Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature 2005, 436:415-419.
22. Itoh T, Fujita N, Kanno E, Yamamoto A, Yoshimori T, Fukuda M. Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell 2008, 19:2916-2925.
23. Han SY, Park DY, Park SD, Hong SH. Identification of Rab6 as an N-ethylmaleimide-sensitive fusion protein-binding protein. Biochem J 2000, 352:165-173.
24. Zhang Y, Grant B, Hirsh D. RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol Biol Cell 2001, 12:2011-2021.
25. Chang HC, Hull M, Mellman I. The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila. J Cell Biol 2004, 164:1055-1064.
26. Girard M, Poupon V, Blondeau F, McPherson PS. The DnaJ-domain protein RME-8 functions in endosomal trafficking. J Biol Chem 2005, 280:40135-40143.
27. Fujibayashi A, Taguchi T, Misaki R, Ohtani M, Dohmae N, Takio K, Yamada M, Gu J, Yamakami M, Fukuda M, Waguri S, Uchiyama Y, Yoshimori T, Sekiguchi K. Human RME-8 is involved in membrane trafficking through early endosomes. Cell Struct Funct 2008, 33:35-50.
28. Haas AK, Fuchs E, Kopajtich R, Barr FA. A GTPase-activating protein controls Rab5 function in endocytic trafficking. Nat Cell Biol 2005, 7:887-893.
29. Fuchs E, Haas AK, Spooner RA, Yoshimura S, Lord JM, Barr FA. Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways. J Cell Biol 2007, 177:1133-1143.
30. Itoh T, Fukuda M. Identification of EPI64 as a GTPase-activating protein specific for Rab27A. J Biol Chem 2006, 281:31823-31831.
31. Ishibashi K, Kanno E, Itoh T, Fukuda M. Identification and characterization of a novel Tre-2 /Bub2/Cdc16 (TBC) protein that possesses Rab3A-GAP activity. Genes Cells 2009, 14:41-52.
32. Simonsen A, Lippé R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 1998, 394:494-498.
33. Patino-Lopez G, Dong X, Ben-Aissa K, Bernot KM, Itoh T, Fukuda M, Kruhlak MJ, Samelson LE, Shaw S. Rab35 and its GAP EPI64C in T cells regulate receptor recycling and immunological synapse formation. J Biol Chem 2008, 283:18323-18330.
34. Jackson TR, Brown FD, Nie Z, Miura K, Foroni L, Sun J, Hsu VW, Donaldson JG, Randazzo PA. ACAPs are arf6 GTPase-activating proteins that function in the cell periphery. J Cell Biol 2000, 151:627-638.
35. Chevallier J, Koop C, Srivastava A, Petrie RJ, Lamarche-Vane N, Presley JF. Rab35 regulates neurite outgrowth and cell shape. FEBS Lett 2009, 583:1096-1101.
36. Dell'Angelica EC, Puertollano R, Mullins C, Aguilar RC, Vargas JD, Hartnell LM, Bonifacino JS. GGAs: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex. J Cell Biol 2000, 149:81-94.
37. Santy LC, Casanova JE. Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J Cell Biol 2001, 154:599-610.
38. Hyvola N, Diao A, McKenzie E, Skippen A, Cockcroft S, Lowe M. Membrane targeting and activation of the Lowe syndrome protein OCRL1 by Rab GTPases. EMBO J 2006, 25:3750-3761.
39. Williams C, Choudhury R, McKenzie E, Lowe M. Targeting of the type II inositol polyphosphate 5-phosphatase INPP5B to the early secretory pathway. J Cell Sci 2007, 120:3941-3951.
40. Rivera-Molina FE, Novick PJ. A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc Natl Acad Sci USA 2009, 106:14408-14413.
41. D'Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 2006, 7:347-358.
42. Kouranti I, Sachse M, Arouche N, Goud B, Echard A. Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 2006, 16:1719-1725.
43. Fukuda M, Aruga J, Niinobe M, Aimoto S, Mikoshiba K. Inositol-1,3,4,5-tetrakisphosphate binding to C2B domain of IP4BP/synaptotagmin II. J Biol Chem 1994, 269:29206-29211.
44. Fukuda M, Kanno E, Mikoshiba K. Conserved N-terminal cysteine motif is essential for homo- and heterodimer formation of synaptotagmins III, V, VI, and X. J Biol Chem 1999, 274:31421-31427.
45. Fukuda M, Kuroda TS, Mikoshiba K. Slac2-a/melanophilin, the missing link between Rab27 and myosin Va: implications of a tripartite protein complex for melanosome transport. J Biol Chem 2002, 277:12432-12436.
46. Fukuda M, Kojima T, Aruga J, Niinobe M, Mikoshiba K. Functional diversity of C2 domains of synaptotagmin family: mutational analysis of inositol high polyphosphate binding domain. J Biol Chem 1995, 270:26523-26527.
47. Tsuboi T, Fukuda M. Rab3A and Rab27A cooperatively regulate the docking step of dense-core vesicle exocytosis in PC12 cells. J Cell Sci 2006, 119:2196-2203.
48. Fukuda M, Kanno E. Analysis of the role of Rab27 effector Slp4-a/granuphilin-a in dense-core vesicle exocytosis. Methods Enzymol 2005, 403:445-457.
49. Tamura K, Ohbayashi N, Maruta Y, Kanno E, Itoh T, Fukuda M. Varp is a novel Rab32/38-binding protein that regulates Tyrp1 trafficking in melanocytes. Mol Biol Cell 2009, 20:2900-2908.
50. James P, Halladay J, Craig EA. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 1996, 144:1425-1436.
51. Kuroda TS, Ariga H, Fukuda M. The actin-binding domain of Slac2-a/melanophilin is required for melanosome distribution in melanocytes. Mol Cell Biol 2003, 23:5245-5255.
52. Ibata K, Fukuda M, Hamada T, Kabayama H, Mikoshiba K. Synaptotagmin IV is present at the Golgi and distal parts of neurites. J Neurochem 2000, 74:518-526.
53. Fukuda M, Mikoshiba K. Expression of synaptotagmin I or II promotes neurite outgrowth in PC12 cells. Neurosci Lett 2000, 295:33-36.