Spatiotemporal regulation of the ubiquitinated cargo-binding activity of Rabex-5 in the endocytic pathway

Journal of Biological Chemistry

Volumn 287, Issue 48, 2012, Pages 40586-40597

  Aikawa, Yoshikatsu ^a   Hirakawa, Hideki ^b   Lee, Sangho ^c  

^a DOSHISHA UNIVERSITY   (Japan)

^b KAZUSA DNA RESEARCH INSTITUTE   (Japan)

^c Sungkyunkwan University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC EFFICIENCIES; ENDOCYTIC PATHWAYS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MEMBRANE PROTEINS; NEURAL CELL ADHESION MOLECULES; REGULATORY MECHANISM; SPATIO-TEMPORAL DYNAMICS; UBIQUITIN;

BIOLOGICAL MEMBRANES; MOLECULAR BIOLOGY; MOLECULAR RECOGNITION; PROTEINS;

ENZYME ACTIVITY;

BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MUTANT PROTEIN; PROTEIN RABEX 5; RAB PROTEIN; UBIQUITIN; UBIQUITIN BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; HINGE REGION; HUMAN; HUMAN CELL; INTERNALIZATION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; STRUCTURE ACTIVITY RELATION; UBIQUITINATION;

ENDOCYTOSIS; ENDOSOMES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HUMANS; NEURAL CELL ADHESION MOLECULE L1; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RAB5 GTP-BINDING PROTEINS; UBIQUITINATION;

EID: 84870051144     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.411793     Document Type: Article

References (42)

1. Mukhopadhyay, D., and Riezman, H. (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315, 201-205 (Pubitemid 46166358)
2. Raiborg, C., and Stenmark, H. (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452
3. Hicke, L., Schubert, H. L., and Hill, C. P. (2005) Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 6, 610-621 (Pubitemid 41081265)
4. Hurley, J. H., Lee, S., and Prag, G. (2006) Ubiquitin-binding domains. Biochem. J. 399, 361-372 (Pubitemid 44672627)
5. Traub, L. M., and Lukacs, G. L. (2007) Decoding ubiquitin sorting signals for clathrin-dependent endocytosis by CLASPs. J. Cell Sci. 120, 543-553 (Pubitemid 46437889)
6. Dikic, I., Wakatsuki, S., and Walters, K. J. (2009) Ubiquitin-binding domains. From structures to functions. Nat. Rev. Mol. Cell Biol. 10, 659-671
7. Polo, S., Sigismund, S., Faretta, M., Guidi, M., Capua, M. R., Bossi, G., Chen, H., De Camilli, P., and Di Fiore, P. P. (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 28, 451-455 (Pubitemid 34272882)
8. Woelk, T., Oldrini, B., Maspero, E., Confalonieri, S., Cavallaro, E., Di Fiore, P. P., and Polo, S. (2006) Molecular mechanisms of coupled monoubiquitination. Nat. Cell. Biol. 8, 1246-1254 (Pubitemid 44660589)
9. Hoeller, D., Crosetto, N., Blagoev, B., Raiborg, C., Tikkanen, R., Wagner, S., Kowanetz, K., Breitling, R., Mann, M., Stenmark, H., and Dikic, I. (2006) Regulation of ubiquitin-binding proteins by monoubiquitination. Nat. Cell. Biol. 8, 163-169
10. Mattera, R., and Bonifacino, J. S. (2008) Ubiquitin binding and conjugation regulate the recruitment of Rabex-5 to early endosomes. EMBO J. 27, 2484-2494
11. Harper, J. W., and Schulman, B. A. (2006) Structural complexity in ubiquitin recognition. Cell 124, 1133-1136
12. Raiborg, C., Slagsvold, T., and Stenmark, H. (2006) A new side to ubiquitin. Trends Biochem. Sci. 31, 541-544 (Pubitemid 44436936)
13. Lee, S., Tsai, Y. C., Mattera, R., Smith, W. J., Kostelansky, M. S., Weissman, A. M., Bonifacino, J. S., and Hurley, J. H. (2006) Structural basis for ubiquitin recognition and autoubiquitination by Rabex-5. Nat. Struct. Mol. Biol. 13, 264-271 (Pubitemid 43348513)
14. Penengo, L., Mapelli, M., Murachelli, A. G., Confalonieri, S., Magri, L., Musacchio, A., Di Fiore, P. P., Polo, S., and Schneider, T. R. (2006) Crystal structure of the ubiquitin binding domains of Rabex-5 reveals two modes of interaction with ubiquitin. Cell 124, 1183-1195
15. Mattera, R., Tsai, Y. C., Weissman A. M., and Bonifacino, J. S. (2006) The Rab5 guanine nucleotide exchange factor Rabex-5 binds ubiquitin (Ub) and functions as a Ub ligase through an atypical Ub-interacting motif and a zinc finger domain. J. Biol. Chem. 281, 6874-6883 (Pubitemid 43847623)
16. Kalesnikoff, J., Rios, E. J., Chen, C. C., Alejandro Barbieri, M., Tsai, M., Tam, S. Y., and Galli, S. J. (2007) Roles of RabGEF1/Rabex-5 domains in regulating Fcε RI surface expression and Fcε RI-dependent responses in mast cells. Blood 109, 5308-5317 (Pubitemid 46890552)
17. Yan, H., Jahanshahi, M., Horvath, E. A., Liu, H. Y., and Pfleger, C. M. (2010) Rabex-5 ubiquitin ligase activity restricts Ras signaling to establish pathway homeostasis in Drosophila. Curr. Biol. 20, 1378-1382
18. Aikawa, Y. (2012) Rabex-5 protein regulates the endocytic trafficking pathway of ubiquitinated neural cell adhesion molecule l1. J. Biol. Chem. 287, 32312-32323
19. Horiuchi, H., Lippé, R., McBride, H. M., Rubino, M., Woodman, P., Stenmark, H., Rybin, V., Wilm, M., Ashman, K., Mann, M., and Zerial, M. (1997)Anovel Rab5 GDP/GTP exchange to effector complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 19, 1149-1159 (Pubitemid 27408528)
20. Gorvel, J. P., Chavrier, P., Zerial, M., and Gruenberg, J. (1991) rab5 controls early endosome fusion in vitro. Cell 64, 915-925 (Pubitemid 121001179)
21. Bucci, C., Parton, R. G., Mather, I. H., Stunnenberg, H., Simons, K., Hoflack, B., and Zerial, M. (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70, 715-728
22. Li, G., Barbieri, M. A., Colombo, M. I., and Stahl, P. D. (1994) Structural features of the GTP-binding defective Rab5 mutants required for their inhibitory activity on endocytosis. J. Biol. Chem. 269, 14631-14635 (Pubitemid 24194024)
23. Zerial, M., and McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117 (Pubitemid 33674039)
24. Donaldson, K. M., Yin, H., Gekakis, N., Supek, F., and Joazeiro, C. A. (2003) Ubiquitin signals protein trafficking via interaction with a novel ubiquitin binding domain in the membrane fusion regulator, Vps9p. Curr. Biol. 13, 258-262 (Pubitemid 36178306)
25. Le, T. L., Yap, A. S., and Stow, J. L. (1999) Recycling of E-cadherin. A potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146, 219-232 (Pubitemid 29349976)
26. Delprato, A., Merithew, E., and Lambright, D. G. (2004) Structure, exchange determinants, and family-wide rab specificity of the tandem helical bundle and Vps9 domains of Rabex-5. Cell 118, 607-617 (Pubitemid 39179713)
27. Wang, J., Cieplak, P., and Kollman, P. A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21, 1049-1074
28. Pearlman, D. A., Case, D. A., Caldwell, J. W., Ross, W. S., Cheatham, T. E., DeBolt, S., Ferguson, D., Seibel, G., and Kollman, P. (1995) AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comp. Phys. Commun. 91, 1-41
29. Stenmark, H., Parton, R. G., Steele-Mortimer, O., Lütcke, A., Gruenberg, J., and Zerial, M. (1994) Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296 (Pubitemid 24090209)
30. Tall, G. G., Barbieri, M. A., Stahl, P. D., and Horazdovsky, B. F. (2001) Ras-activated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev. Cell 1, 73-82 (Pubitemid 33586070)
31. Ali, B. R., and Seabra, M. C. (2005) Targeting of Rab GTPases to cellular membranes. Biochem. Soc. Trans. 33, 652-656 (Pubitemid 41160831)
32. Esters, H., Alexandrov, K., Constantinescu, A. T., Goody, R. S., and Scheidig, A. J. (2001) Vps9, Rabex-5, and DSS4. Proteins with weak but distinct nucleotide-exchange activities for Rab proteins. J. Mol. Biol. 29, 141-156 (Pubitemid 32619958)
33. Delprato, A., and Lambright, D. G. (2007) Structural basis for Rab GTPase activation by VPS9 domain exchange factors. Nat. Struct. Mol. Biol. 14, 406-412 (Pubitemid 46685882)
34. Lippé, R., Miaczynska, M., Rybin, V., Runge, A., and Zerial, M. (2001) Functional synergy between Rab5 effector Rabaptin-5 and exchange factor Rabex-5 when physically associated in a complex. Mol. Biol. Cell 12, 2219-2228 (Pubitemid 33049711)
35. Carney, D. S., Davies, B. A., and Horazdovsky, B. F. (2006) Vps9 domain-containing proteins. Activators of Rab5 GTPases from yeast to neurons. Trends Cell Biol. 16, 27-35 (Pubitemid 43077092)
36. Zhu, H., Liang, Z., and Li, G. (2009) Rabex-5 is a Rab22 effector and mediates a Rab22-Rab5 signaling cascade in endocytosis. Mol. Biol. Cell 20, 4720-4729
37. Han, L., Wong, D., Dhaka, A., Afar, D., White, M., Xie, W., Herschman, H., Witte, O., and Colicelli, J. (1997) Protein binding and signaling properties of RIN1 suggest a unique effector function. Proc. Natl. Acad. Sci. U.S.A. 94, 4954-4959 (Pubitemid 27214717)
38. Faesen, A. C., Dirac, A. M., Shanmugham, A., Ovaa, H., Perrakis, A., and Sixma, T. K. (2011) Mechanism of USP7/HAUSP activation by its C-terminal ubiquitin-like domain and allosteric regulation by GMP-synthetase. Mol. Cell 7, 147-159
39. 2+-dependent decrease of protein ubiquitination at synapses. Proc. Natl. Acad. Sci. U.S.A. 100, 14908-14913
40. Williams, E. J., Doherty, P., Turner, G., Reid, R. A., Hemperly, J. J., and Walsh, F. S. (1992) Calcium influx into neurons can solely account for cell contact-dependent neurite outgrowth stimulated by transfected L1. J. Cell Biol. 119, 883-892
41. Archer, F. R., Doherty, P., Collins, D., and Bolsover, S. R. (1999) CAMs and FGF cause a local submembrane calcium signal promoting axon outgrowth without a rise in bulk calcium concentration. Eur. J. Neurosci. 11, 3565-3573 (Pubitemid 29484253)
42. Keren-Kaplan, T., Attali, I., Motamedchaboki, K., Davis, B. A., Tanner, N., Reshef, Y., Laudon, E., Kolot, M., Levin-Kravets, O., Kleifeld, O., Glickman, M., Horazdovsky, B. F., Wolf, D. A., and Praq, G. (2011) Synthetic biology approach to reconstituting the ubiquitylation cascade in bacteria. EMBO J. 11, 378-390