Rab coupling protein is selectively degraded by calpain in a Ca 2+-dependent manner

Biochemical Journal

Volumn 389, Issue 1, 2005, Pages 223-231

  Marie, Nicolas ^a   Lindsay, Andrew J ^a   McCaffrey, Mary W ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Calpain; Endocytic recycling compartment; Glu and Ser Thr rich motif (PEST motif); Pro; Rab coupling protein; Rab11

Indexed keywords

BIODEGRADATION; BIOLOGICAL MEMBRANES; CALCIUM; ENZYME INHIBITION;

ENDOCYTOSIS; PLASMA MEMBRANES; PROTEOLYTIC DEGRADATION; RAB COUPLING PROTEINS (RCP);

PROTEINS;

CALCIUM; CALPAIN; RAB PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CANCER CELL; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CELL MEMBRANE; CLONING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; WESTERN BLOTTING; WILD TYPE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CALPAIN; CARRIER PROTEINS; CELL LINE, TUMOR; CELL MEMBRANE; CONSERVED SEQUENCE; DIPEPTIDES; HUMANS; MEMBRANE PROTEINS; MICE; SECRETORY VESICLES; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 22144475413     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20042116     Document Type: Article

References (49)

1. Zerial, M. and McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117
2. van der Sluijs, P., Hull, M., Webster, P., Male, P., Goud, B. and Mellman, I. (1992) The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70, 729-740
3. Van Der Sluijs, P., Hull, M., Zahraoui, A., Tavitian, A., Goud, B. and Mellman, I. (1991) The small GTP-binding protein rab4 is associated with early endosomes. Proc. Natl. Acad. Sci. U.S.A. 88, 6313-6317
4. McCaffrey, M. W., Bielli, A., Cantalupo, G., Mora, S., Roberti, V., Santillo, M., Drummond, F. and Bucci, C. (2001) Rab4 affects both recycling and degradative endosomal trafficking. FEBS Lett. 495, 21-30
5. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M. and Parton, R. G. (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924
6. Urbe, S., Huber, L. A., Zerial, M., Tooze, S. A. and Parton, R. G. (1993) Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett. 334, 175-182
7. Ren, M., Xu, G., Zeng, J., De Lemos-Chiarandini, C., Adesnik, M. and Sabatini, D. D. (1998) Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc. Natl. Acad. Sci. U.S.A. 95, 6187-6192
8. Wilcke, M., Johannes, L., Galli, T., Mayau, V., Goud, B. and Salamero, J. (2000) Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J. Cell Biol. 151, 1207-1220
9. Zeng, J., Ren, M., Gravotta, D., De Lemos-Chiarandini, C., Lui, M., Erdjument-Bromage, H., Tempst, P., Xu, G., Shen, T. H., Morimoto, T. et al. (1999) Identification of a putative effector protein for rab11 that participates in transferrin recycling. Proc. Natl. Acad. Sci. U.S.A. 96, 2840-2845
10. Mammoto, A., Ohtsuka, T., Hotta, I., Sasaki, T. and Takai, Y. (1999) Rab11BP/Rabphilin-11, a downstream target of rab11 small G protein implicated in vesicle recycling. J. Biol. Chem. 274, 25517-25524
11. Lapierre, L. A., Kumar, R., Hales, C. M., Navarre, J., Bhartur, S. G., Burnette, J. O., Provance, Jr, D. W., Mercer, J. A., Bahler, M. and Goldenring, J. R. (2001) Myosin Vb is associated with plasma membrane recycling systems. Mol. Biol. Cell 12, 1843-1857
12. Prekeris, R., Klumperman, J. and Scheller, R. H. (2000) A Rab11/Rip11 protein complex regulates apical membrane trafficking via recycling endosomes. Mol. Cell 6, 1437-1448
13. Prekeris, R., Davies, J. M. and Scheller, R. H. (2001) Identification of a novel Rab11/25 binding domain present in Eferin and Rip proteins. J. Biol. Chem. 276, 38966-38970
14. Lindsay, A. J., Hendrick, A. G., Cantalupo, G., Senic-Matuglia, F., Goud, B., Bucci, C. and McCaffrey, M. W. (2002) Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein. J. Biol. Chem. 277, 12190-12199
15. Hales, C. M., Griner, R., Hobdy-Henderson, K. C., Dorn, M. C., Hardy, D., Kumar, R., Navarre, J., Chan, E. K., Lapierre, L. A. and Goldenring, J. R. (2001) Identification and characterization of a family of Rab11-interacting proteins. J. Biol. Chem. 276, 39067-39075
16. Wallace, D. M. E., Lindsay, A. J., Hendrick, A. G. and McCaffrey, M. W. (2002) Rab11-FIP4 interacts with Rab11 in a GTP-dependent manner and its overexpression condenses the Rab11 positive compartment in HeLa cells. Biochem. Biophys. Res. Commun. 299, 770-779
17. Meyers, J. M. and 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
18. Wallace, D. M., Lindsay, A. J., Hendrick, A. G. and 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
19. Horgan, C. P., Walsh, M., Zurawski, T. H. and 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
20. Hickson, G. R., Matheson, J., Riggs, B., Maier, V. H., Fielding, A. B., Prekeris, R., Sullivan, W., Barr, F. A. and Gould, G. W. (2003) Arfophilins are dual Arf/Rab 11 binding proteins that regulate recycling endosome distribution and are related to Drosophila nuclear fallout. Mol. Biol. Cell 14, 2908-2920
21. Shin, O. H., Couvillon, A. D. and Exton, J. H. (2001) Arfophilin is a common target of both class II and class III ADP-ribosylation factors. Biochemistry 40, 10846-10852
22. Shin, O. H., Ross, A. H., Mihai, I. and Exton, J. H. (1999) Identification of arfophilin, a target protein for GTP-bound class II ADP-ribosylation factors. J. Biol. Chem. 274, 36609-36615
23. 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. and 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
24. Lindsay, A. J. and McCaffrey, M. W. (2004) The C2 domains of the class I Rab11 family of interacting proteins target recycling vesicles to the plasma membrane. J. Cell Sci. 117, 4365-4375
25. Hales, C. M., Vaerman, J.-P. and Goldenring, J. R. (2002) Rab11 family interacting protein 2 associates with myosin Vb and regulates plasma membrane recycling. J. Biol. Chem. 277, 50415-50421
26. Lindsay, A. J. and McCaffrey, M. W. (2002) Rab11-FIP2 functions in transferrin recycling and associates with endosomal membranes via its COOH-terminal domain. J. Biol. Chem. 277, 27193-27199
27. Fan, G.-H., Lapierre, L. A., Goldenring, J. R., Sai, J. and Richmond, A. (2004) Rab11-family interacting protein 2 and myosin Vb Are required for CXCR2 recycling and receptor-mediated chemotaxis. Mol. Biol. Cell 15, 2456-2469
28. Damiani, M. T., Pavarotti, M., Leiva, N., Lindsay, A. J., McCaffrey, M. W. and Colombo, M. I. (2004) Rab coupling protein associates with phagosomes and regulates recycling from the phagosomal compartment. Traffic 5, 785-797
29. Peden, A. A., Schonteich, E., Chun, J., Junutula, J. R., Scheller, R. H. and Prekeris, R. (2004) The RCP-Rab11 complex regulates endocytic protein sorting. Mol. Biol. Cell 15, 3530-3541
30. Dice, J. F. (1987) Molecular determinants of protein half-lives in eukaryotic cells. FASEB J. 1, 349-357
31. Tompa, P., Buzder-Lantos, P., Tantos, A., Farkas, A., Szilagyi, A., Banoczi, Z., Hudecz, F. and Friedrich, P. (2004) On the sequential determinants of calpain cleavage. J. Biol. Chem. 279, 20775-20785
32. Rechsteiner, M. and Rogers, S. W. (1996) PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21, 267-271
33. Shumway, S. D., Maki, M. and Miyamoto, S. (1999) The PEST domain of IκBα is necessary and sufficient for in vitro degradation by μ-calpain. J. Biol. Chem. 274, 30874-30881
34. Fukuda, M. and Itoh, T. (2004) Slac2-a/Melanophilin contains multiple PEST-like sequences that are highly sensitive to proteolysis. J. Biol. Chem. 279, 22314-22321
35. Allaman-Pillet, N., Storling, J., Oberson, A., Roduit, R., Negri, S., Sauser, C., Nicod, P., Beckmann, J. S., Schorderet, D. F., Mandrup-Poulsen, T. and Bonny, C. (2003) Calcium- and proteasome-dependent degradation of the JNK scaffold protein islet-brain 1. J. Biol. Chem. 278, 48720-48726
36. Spencer, M. L., Theodosiou, M. and Noonan, D. J. (2004) NPDC-1, a novel regulator of neuronal proliferation, is degraded by the ubiquitin/proteasome system through a PEST degradation motif. J. Biol. Chem. 279, 37069-37078
37. Tang, F., Kauffman, E. J., Novak, J. L., Nau, J. J., Catlett, N. L. and Weisman, L. S. (2003) Regulated degradation of a class V myosin receptor directs movement of the yeast vacuole. Nature (London) 422, 87-92
38. Glading, A., Bodnar, R. J., Reynolds, I. J., Shiraha, H., Satish, L., Potter, D. A., Blair, H. C. and Wells, A. (2004) Epidermal growth factor activates M-calpain (calpain II), at least in part, by extracellular signal-regulated kinase-mediated phosphorylation. Mol. Cell. Biol. 24, 2499-2512
39. Wang, X., Kumar, R., Navarre, J., Casanova, J. E. and Goldenring, J. R. (2000) Regulation of vesicle trafficking in Madin-Darby canine kidney cells by Rab11a nd Rab25. J. Biol. Chem. 275, 29138-29146
40. Cullis, D. N., Philip, B., Baleja, J. D. and Feig, L. A. (2002) Rab11-FIP2, an adaptor protein connecting cellular components involved in internalization and recycling of epidermal growth factor receptors. J. Biol. Chem. 277, 49158-49166
41. Dayton, W. R., Schollmeyer, J. V., Lepley, R. A. and Cortes, L. R. (1981) A calcium-activated protease possibly involved in myofibrillar protein turnover: isolation of a low-calcium-requiring form of the protease. Biochim. Biophys. Acta 659, 48-61
42. Goll, D. E., Thompson, V. F., Li, H, Wei, W. and Cong, J. (2003) The calpain system. Physiol. Rev. 83, 731-801
43. Suzuki, K., Sorimachi, H., Yoshizawa, T., Kinbara, K. and Ishiura, S. (1995) Calpain: novel family members, activation, and physiologic function. Biol. Chem. Hoppe Seyler 376, 523-529
44. Kakkar, R., Raju, R. V. and Sharma, R. K. (1998) In vitro generation of an active calmodulin-independent phosphodiesterase from brain calmodulin-dependent phosphodiesterase (PDE1A2) by M-calpain. Arch. Biochem. Biophys. 358, 320-328
45. Kubbutat, M. and Vousden, K. (1997) Proteolytic cleavage of human p53 by calpain: a potential regulator of protein stability. Mol. Cell. Biol. 17, 460-468
46. Pariat, M., Carillo, S., Molinari, M., Salvat, C., Debussche, L., Bracco, L., Milner, J. and Piechaczyk, M. (1997) Proteolysis by calpains: a possible contribution to degradation of p53. Mol. Cell. Biol. 17, 2806-2815
47. Gonen, H., Shkedy, D., Barnoy, S., Kosower, N. S. and Ciechanover, A. (1997) On the involvement of calpains in the degradation of the tumor suppressor protein p53. FEBS Lett. 406, 17-22
48. Bordone, L. and Campbell, C. (2002) DNA ligase III is degraded by calpain during cell death induced by DNA-damaging agents. J. Biol. Chem. 277, 26673-26680
49. Lindsay, A. J. and McCaffrey, M. W. (2004) Characterisation of the Rab binding properties of Rab coupling protein (RCP) by site-directed mutagenesis. FEBS Lett. 571, 86-92