Rab11 is phosphorylated by classical and novel protein kinase C isoenzymes upon sustained phorbol ester activation

Biology of the Cell

Volumn 104, Issue 2, 2012, Pages 102-115

  Pavarotti, Martín ^a   Capmany, Anahí ^a   Vitale, Nicolas ^b   Colombo, María Isabel ^a   Damiani, María Teresa ^a  

^a School of Medicine University of Cuyo ^*  (Argentina)

^b Institut des Neurosciences Cellulaires et Intégratives UPR3212   (France)

Author keywords

Phosphorylation; PKC; Rab GTPases; Rab11; Transferrin recycling

Indexed keywords

PHORBOL 12 ACETATE 13 MYRISTATE; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA I; PROTEIN KINASE C BETA II; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C ETA; PROTEIN KINASE C ZETA; PROTEIN SERINE THREONINE KINASE; RAB11 PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; BIOINFORMATICS; CELL COMPARTMENTALIZATION; CELL MIGRATION; CYTOSOL; ENZYME ACTIVATION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROBABILITY; PROTEIN EXPRESSION; PROTEIN PROCESSING; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS;

COMPUTATIONAL BIOLOGY; CYTOSOL; ENDOSOMES; HELA CELLS; HUMANS; ISOENZYMES; MASS SPECTROMETRY; PHOSPHORYLATION; PLASMIDS; PROTEIN KINASE C; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS; SERINE; SUBSTRATE SPECIFICITY; TETRADECANOYLPHORBOL ACETATE; TRANSFECTION; TRANSFERRIN;

EID: 84861378550     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1111/boc.201100062     Document Type: Article

References (47)

1. Audebert, S., Navarro, C., Nourry, C., Chasserot-Golaz, S., Lécine, P., Bellaiche, Y., Dupont, J.L., Premont, R.T., Sempéré, C., Strub, J.M., Van Dorsselaer, A., Vitale, N. and Borg, J.P. (2004) Mammalian scribble forms a tight complex with the betaPIX exchange factor. Curr. Biol. 14, 987-995.
2. Bailly, E., McCaffrey, M., Touchot, N., Zahraoui, A., Goud, B. and Bornens, M. (1991) Phosphorylation of two small GTP-binding proteins of the Rab family by p34cdc2. Nature 350, 715-718.
3. Bao, J., Alroy, I., Waterman, H., Schejter, E.D., Brodie, C., Gruenberg, J. and Yarden, Y. (2000) Threonine phosphorylation diverts internalized epidermal growth factor receptors from a degradative pathway to the recycling endosome. J. Biol. Chem. 275, 26178-26186.
4. Becker, K.P. and Hannun, Y.A. (2003) cPKC-dependent sequestration of membrane-recycling components in a subset of recycling endosomes. J. Biol. Chem. 278, 52747-52754.
5. Béglé, A., Tryoen-Tóth, P., de Barry, J., Bader, M.F., Vitale, N. (2009) ARF6 regulates the synthesis of fusogenic lipids for calcium-regulated exocytosis in neuroendocrine cells. J. Biol Chem. 284, 4836-4845.
6. Bolte, S. and Cordelieres, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232.
7. Bond, A.E., Dudley, E., Tuytten, R., Lemiere, F., Smith, C.J., Esmans, E.L. and Newton, R.P. (2007) Mass spectrometric identification of Rab23 phosphorylation as a response to challenge by cytidine 3′, 5′-cyclic monophosphate in mouse brain. Rapid Commun. Mass Spectrom. 21, 2685-2692.
8. Chamberlain, M.D., Oberg, J.C., Furber, L.A., Poland, S.F., Hawrysh, A.D., Knafelc, S.M., McBride, H.M. and Anderson, D.H. (2010) Deregulation of Rab5 and Rab4 proteins in p85R274A-expressing cells alters PDGFR trafficking. Cell Signal. 22, 1562-1575.
9. Chappell, D.S., Patel, N.A., Jiang, K., Li, P., Watson, J.E., Byers, D.M. and Cooper, D.R. (2009) Functional involvement of protein kinase C-betaII and its substrate, myristoylated alanine-rich C-kinase substrate (MARCKS), in insulin-stimulated glucose transport in L6 rat skeletal muscle cells. Diabetologia 52, 901-911.
10. Chen, Y.W., Lang, M.L. and Wade, W.F. (2004) Protein kinase C-alpha and -delta are required for FcalphaR (CD89) trafficking to MHC class II compartments and FcalphaR-mediated antigen presentation. Traffic 5, 577-594.
11. Chiariello, M., Bruni, C.B. and Bucci, C. (1999) The small GTPases Rab5a, Rab5b and Rab5c are differentially phosphorylated in vitro. FEBS Lett. 453, 20-24.
12. Cramm-Behrens, C.I., Dienst, M. and Jacob, R. (2008) Apical cargo traverses endosomal compartments on the passage to the cell surface. Traffic 9, 2206-2220.
13. 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.
14. Ducharme, N.A., Hales, C.M., Lapierre, L.A., Ham, A.J., Oztan, A., Apodaca, G. and Goldenring, J.R. (2006) MARK2/EMK1/Par-1Balpha phosphorylation of Rab11-family interacting protein 2 is necessary for the timely establishment of polarity in Madin-Darby canine kidney cells. Mol. Biol. Cell 17, 3625-3637.
15. Fitzgerald, M.L. and Reed, G.L. (1999) Rab6 is phosphorylated in thrombin-activated platelets by a protein kinase C-dependent mechanism: Effects on GTP/GDP binding and cellular distribution. Biochem. J. 342, 353-360.
16. Hiragaki, S., Uno, T. and Takeda, M. (2009) Putative regulatory mechanism of prothoracicotropic hormone (PTTH) secretion in the American cockroach, Periplaneta americana as inferred from co-localization of Rab8, PTTH, and protein kinase C in neurosecretory cells. Cell Tissue Res. 335, 607-615.
17. Idkowiak-Baldys, J., Becker, K.P., Kitatani, K. and Hannun, Y.A. (2006) Dynamic sequestration of the recycling compartment by classical protein kinase C. J. Biol. Chem. 281, 22321-22331.
18. Idkowiak-Baldys, J., Baldys, A., Raymond, J.R. and Hannun, Y.A. (2009) Sustained receptor stimulation leads to sequestration of recycling endosomes in a classical protein kinase C- and phospholipase D-dependent manner. J. Biol. Chem. 284, 22322-22331.
19. Jagoe, W.N., Lindsay, A., Read, R., McCoy, A., McCaffrey, M. and Khan, A. (2006) Purification, crystallization and preliminary X-ray diffraction studies of Rab11 in complex with Rab11-FIP2. Structure 14, 1273-1283.
20. Jones, B.W. and Hinkle, P.M. (2009) Subcellular trafficking of the TRH receptor: Effect of phosphorylation. Mol. Endocrinol. 23, 1466-1478.
21. Karniguian, A., Zahraoui, A. and Tavitian, A. (1993) Identification of small GTP-binding rab proteins in human platelets: Thrombin-induced phosphorylation of rab3B, rab6, and rab8 proteins. Proc. Natl. Acad. Sci. U. S. A. 90, 7647-7651.
22. Kelley, L.A. and Sternberg, M.J. (2009) Protein structure prediction on the Web: A case study using the Phyre server. Nat. Protoc. 4, 363-371.
23. Kleiman, E., Carter, G., Ghansah, T., Patel, N.A. and Cooper, D.R. (2009) Developmentally spliced PKCbetaII provides a possible link between mTORC2 and Akt kinase to regulate 3T3-L1 adipocyte insulin-stimulated glucose transport. Biochem. Biophys. Res. Commun. 388, 554-559.
24. Leiva, N., Pavarotti, M., Colombo, M.I. and Damiani, M.T. (2006) Reconstitution of recycling from the phagosomal compartment in streptolysin O-permeabilized macrophages: Role of Rab11. Exp. Cell Res. 312, 1843-1855.
25. 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.
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. Llado, A., Tebar, F., Calvo, M., Moreto, J., Sorkin, A. and Enrich, C. (2004) Protein kinase C delta-calmodulin crosstalk regulates epidermal growth factor receptor exit from early endosomes. Mol. Biol. Cell 15, 4877-4891.
28. Otani, T., Oshima, K., Onishi, S., Takeda, M., Shinmyozu, K., Yonemura, S. and Hayashi, S. (2011) IKKepsilon regulates cell elongation through recycling endosome shuttling. Dev. Cell 20, 219-232.
29. Parker, P.J. and Murray-Rust, J. (2004) PKC at a glance. J. Cell Sci. 117, 131-132.
30. Pasqualato, S., Senic-Matuglia, F., Renault, L., Goud, B., Salamero, J. and Cherfils, J. (2004) The structural GDP/GTP cycle of Rab11 reveals a novel interface involved in the dynamics of recycling endosomes. J. Biol. Chem. 279, 11480-11488.
31. Pfeffer, S. (2005) A model for Rab GTPase localization. Biochem. Soc. Trans. 33, 627-630.
32. 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.
33. Prekeris, R. (2003) Rabs, Rips, FIPs, and endocytic membrane traffic. ScientificWorld J. 3, 870-880.
34. Savina, A., Fader, C.M., Damiani, M.T. and Colombo, M.I. (2005) Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner. Traffic 6, 131-143.
35. Scheper, W., Zwart, R. and Baas, F. (2004) Rab6 membrane association is dependent of Presenilin 1 and cellular phosphorylation events. Brain Res. Mol. Brain Res. 122, 17-23.
36. Shiba, T., Koga, H., Shin, H.W., Kawasaki, M., Kato, R., Nakayama, K. and Wakatsuki, S. (2006) Structural basis for Rab11-dependent membrane recruitment of a family of Rab11-interacting protein 3 (FIP3)/Arfophilin-1. Proc. Natl. Acad. Sci. U. S. A 103, 15416-15421.
37. Su, T., Bryant, D.M., Luton, F., Vergés, M., Ulrich, S.M., Hansen, K.C., Datta, A., Eastburn, D.J., Burlingame, A.L., Shokat, K.M. and Mostov, K.E. (2010) A kinase cascade leading to Rab11-FIP5 controls transcytosis of the polymeric immunoglobulin receptor. Nat. Cell Biol. 12, 1143-1153.
38. Sugawara, K., Shibasaki, T., Mizoguchi, A., Saito, T. and Seino, S. (2009) Rab11 and its effector Rip11 participate in regulation of insulin granule exocytosis. Genes Cells 14, 445-456.
39. Thong, F.S., Bilan, P.J. and Klip, A. (2007) The Rab GTPase-activating protein AS160 integrates Akt, protein kinase C, and AMP-activated protein kinase signals regulating GLUT4 traffic. Diabetes 56, 414-423.
40. Tisdale, E.J. (2000) Rab2 requires PKC iota/lambda to recruit beta-COP for vesicle formation. Traffic 1, 702-712.
41. 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.
42. Uno, T., Nakada, T., Okamaoto, S., Nakamura, M., Matsubara, M., Imaishi, H., Yamagata, H., Kanamaru, K. and Takagi, M. (2007) Determination of phosphorylated amino acid residues of Rab8 from Bombyx mori. Arch. Insect Biochem. Physiol 66, 89-97.
43. van der Sluijs, P., Hull, M., Huber, L.A., Male, P., Goud, B and Mellman, I. (1992) Reversible phosphorylation-dephosphorylation determines the localization of rab4 during the cell cycle. EMBO J. 11, 4379-4389.
44. Wang, F., Chen, X., Zhang, X. and Ma, L. (2008) Phosphorylation state of mu-opioid receptor determines the alternative recycling of receptor via Rab4 or Rab11 pathway. Mol. Endocrinol. 22, 1881-1892.
45. Ward, E.S., Martinez, C., Vaccaro, C., Zhou, J., Tang, Q. and Ober, R.J. (2005) From sorting endosomes to exocytosis: Association of Rab4 and Rab11 GTPases with the Fc receptor, FcRn, during recycling. Mol. Biol. Cell 16, 2028-2038.
46. 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.
47. 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.