Rabex-5 protein regulates the endocytic trafficking pathway of ubiquitinated neural cell adhesion molecule L1

Journal of Biological Chemistry

Volumn 287, Issue 39, 2012, Pages 32312-32323

  Aikawa, Yoshikatsu ^a  

^a DOSHISHA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEINS; CELL ADHESION MOLECULES; CELL SURFACE PROTEINS; DEPHOSPHORYLATIONS; ENDOCYTIC PATHWAYS; ENDOCYTIC SORTING; ENDOSOMES; EUKARYOTIC CELLS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HOMOPHILIC BINDING; INTEGRAL MEMBRANE PROTEINS; LYSINE RESIDUES; LYSOSOMAL DEGRADATION; MAXIMAL RATES; NEURAL CELL ADHESION MOLECULES; POST-TRANSLATIONAL MODIFICATIONS; PROTEASOMES; TYROSINE-BASED MOTIFS; UBIQUITIN; UBIQUITINATION; ZINC FINGER DOMAINS;

AMINO ACIDS; ANTIBODIES; ASSOCIATION REACTIONS; BIOMOLECULES; RNA;

CELL MEMBRANES;

BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; IMMUNOGLOBULIN; LYSINE; NERVE CELL ADHESION MOLECULE L1; PROTEASOME; RAB PROTEIN; RAB5 PROTEIN; RABEX 5 PROTEIN; UBIQUITIN; UBIQUITIN BINDING PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DEPHOSPHORYLATION; EMBRYO; ENDOCYTOSIS; ENDOSOME; GENE; GENE SILENCING; HUMAN; HUMAN CELL; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; RABEX 5 GENE; REGULATORY MECHANISM; RNA INTERFERENCE; UBIQUITINATION;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; ENDOCYTOSIS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HUMANS; LYSOSOMES; MICE; MUTATION, MISSENSE; NEURAL CELL ADHESION MOLECULE L1; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEOLYSIS; UBIQUITINATED PROTEINS; UBIQUITINATION; ZINC FINGERS;

EUKARYOTA;

EID: 84866555797     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.374322     Document Type: Article

References (47)

1. Maness, P. F., and Schachner, M. (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 10, 19-26 (Pubitemid 46026522)
2. Schmid, R. S., and Maness, P. F. (2008) L1 and NCAM adhesion molecules as signaling coreceptors in neuronal migration and process outgrowth. Curr. Opin. Neurobio1. 18, 245-250
3. Kamiguchi, H., Long, K. E., Pendergast, M., Schaefer, A. W., Rapoport, I., Kirchhausen, T., and Lemmon, V. (1998) The neural cell adhesion molecule L1 interacts with the AP-2 adaptor and is endocytosed via the clathrin-mediated pathway. J. Neurosci. 18, 5311-5321 (Pubitemid 28311948)
4. Kamiguchi, H., and Lemmon, V. (2000) Recycling of the cell adhesion molecule L1 in axonal growth cones. J. Neurosci. 20, 3676-3686 (Pubitemid 30266230)
5. Kamiguchi, H., and Yoshihara, F. (2001) The role of endocytic l1 trafficking in polarized adhesion and migration of nerve growth cones. J. Neurosci. 21, 9194-9203 (Pubitemid 33096863)
6. Wisco, D., Anderson, E. D., Chang, M. C., Norden, C., Boiko, T., Fölsch, H., and Winckler, B. (2003) Uncovering multiple axonal targeting pathways in hippocampal neurons. J. Cell Biol. 162, 1317-1328 (Pubitemid 37210887)
7. Yap, C. C., Nokes, R. L., Wisco, D., Anderson, E., Fölsch, H., and Winckler, B. (2008) Pathway selection to the axon depends on multiple targeting signals in NgCAM. J. Cell Sci. 121, 1514-1525 (Pubitemid 351936316)
8. Yap, C. C., Wisco, D., Kujala, P., Lasiecka, Z. M., Cannon, J. T., Chang, M. C., Hirling, H., Klumperman, J., and Winckler, B. (2008) The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM. J. Cell Biol. 180, 827-842 (Pubitemid 351397781)
9. Schaefer, A. W., Kamei, Y., Kamiguchi, H., Wong, E. V., Rapoport, I., Kirchhausen, T., Beach, C. M., Landreth, G., Lemmon, S. K., and Lemmon, V. (2002) L1 endocytosis is controlled by a phosphorylation-dephosphorylation cycle stimulated by outside-in signaling by L1. J. Cell Biol. 157, 1223-1232 (Pubitemid 34847792)
10. Dequidt, C., Danglot, L., Alberts, P., Galli, T., Choquet, D., and Thoumine, O. (2007) Fast turnover of L1 adhesions in neuronal growth cones involving both surface diffusion and exo/endocytosis of L1 molecules. Mol. Biol. Cell 18, 3131-3143 (Pubitemid 47235317)
11. Hicke, L., Schubert, H. L., and Hill, C. P. (2005) Ubiquitin-binding domains. Nat. Rev. Mol. Cell Biol. 6, 610-621 (Pubitemid 41081265)
12. Mukhopadhyay, D., and Riezman, H. (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315, 201-205 (Pubitemid 46166358)
13. Raiborg, C., and Stenmark, H. (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452
14. 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)
15. Dikic, I., Wakatsuki, S., and Walters, K. J. (2009) Ubiquitin-binding domains: from structures to functions. Nat. Rev. Mol. Cell Biol. 10, 659-671
16. Haglund, K., and Dikic, I. (2012) The role of ubiquitylation in receptor endocytosis and endosomal sorting. J. Cell Sci. 125, 265-275
17. 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) A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90, 1149-1159 (Pubitemid 27408528)
18. 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)
19. 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)
20. 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)
21. 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)
22. 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)
23. Haglund, K., Sigismund, S., Polo, S., Szymkiewicz, I., Di Fiore, P. P., and Dikic, I. (2003) Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5, 461-466 (Pubitemid 36592270)
24. Long, K. E., Asou, H., Snider, M. D., and Lemmon, V. (2001) The role of endocytosis in regulating L1-mediated adhesion. J. Biol. Chem. 276, 1285-1290 (Pubitemid 32096557)
25. Diestel, S., Schaefer, D., Cremer, H., and Schmitz, B. (2007) NCAM is ubiquitylated, endocytosed, and recycled in neurons. J. Cell Sci. 120, 4035-4049 (Pubitemid 350269409)
26. Thelen, K., Georg, T., Bertuch, S., Zelina, P., and Pollerberg, G. E. (2008) Ubiquitination and endocytosis of cell adhesion molecule DM-GRASP regulate its cell surface presence and affect its role for axon navigation. J. Biol. Chem. 283, 32792-32801
27. Schäfer, M. K., Schmitz, B., and Diestel, S. (2010) L1CAM ubiquitination facilitates its lysosomal degradation. FEBS Lett. 584, 4475-4480
28. Damke, H., Baba, T., Warnock, D. E., and Schmid, S. L. (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934 (Pubitemid 24355982)
29. Sakurai, T., Gil, O. D., Whittard, J. D., Gazdoiu, M., Joseph, T., Wu, J., Waksman, A., Benson, D. L., Salton, S. R., and Felsenfeld, D. P. (2008) Interactions between the L1 cell adhesion molecule and ezrin support traction-force generation and can be regulated by tyrosine phosphorylation. J. Neurosci. Res. 86, 2602-2614
30. 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)
31. Volpicelli, L. A., Lah, J. J., and Levey, A. I. (2001) Rab5-dependent trafficking of the m4 muscarinic acetylcholine receptor to the plasma membrane, early endosomes, and multivesicular bodies. J. Biol. Chem. 276, 47590-47598
32. Dinneen, J. L., and Ceresa, B. P. (2004) Continual expression of Rab5(Q79L) causes a ligand-independent EGFR internalization and diminishes EGFR activity. Traffic 5, 606-615 (Pubitemid 39144490)
33. 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
34. Geetha, T., Jiang, J., and Wooten, M. W. (2005) Lysine 63 polyubiquitination of the nerve growth factor receptor TrkA directs internalization and signaling. Mol. Cell 20, 301-312 (Pubitemid 41484174)
35. Duncan, L. M., Piper, S., Dodd, R. B., Saville, M. K., Sanderson, C. M., Luzio, J. P., and Lehner, P. J. (2006) Lysine 63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J. 25, 1635-1645
36. Kumar, K. G., Barriere, H., Carbone, C. J., Liu, J., Swaminathan, G., Xu, P., Li, Y., Baker, D. P., Peng, J., Lukacs, G. L., and Fuchs, S. Y. (2007) Site-specific ubiquitination exposes a linear motif to promote interferon-α receptor endocytosis. J. Cell Biol. 179, 935-950 (Pubitemid 350223490)
37. Huang, F., Kirkpatrick, D., Jiang, X., Gygi, S., and Sorkin, A. (2006) Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol. Cell 21, 737-748 (Pubitemid 43376125)
38. Barriere, H., Nemes, C., Lechardeur, D., Khan-Mohammad M., Fruh, K., and Lukacs, G. L. (2006) Molecular basis of oligoubiquitin-dependent internalization of membrane proteins in mammalian cells. Traffic 7, 282-297 (Pubitemid 43323956)
39. Hawryluk, M. J., Keyel, P. A., Mishra, S. K., Watkins, S. C., Heuser, J. E., and Traub, L. M. (2006) Epsin 1 is a polyubiquitin-selective clathrin-associated sorting protein. Traffic 7, 262-281 (Pubitemid 43323955)
40. Traub, L. M. (2009) Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 10, 583-596
41. Sorkina, T., Miranda, M., Dionne, K. R., Hoover, B. R., Zahniser, N. R., and Sorkin, A. (2006) RNA interference screen reveals an essential role of Nedd4-2 in dopamine transporter ubiquitination and endocytosis. J. Neurosci. 26, 8195-8205 (Pubitemid 44315144)
42. Jakobsson, J., Gad, H., Andersson, F., Löw, P., Shupliakov, O., and Brodin, L. (2008) Role of epsin 1 in synaptic vesicle endocytosis. Proc. Natl. Acad. Sci. U.S.A. 105, 6445-6450 (Pubitemid 351758365)
43. Sigismund, S., Woelk, T., Puri, C., Maspero, E., Tacchetti, C., Transidico, P., Di Fiore, P. P., and Polo, S. (2005) Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. U.S.A. 102, 2760-2765 (Pubitemid 40299866)
44. 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)
45. 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)
46. 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
47. 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