Abstract:
Rab31, a protein that we cloned from an oligodendrocyte cDNA library, is required for transport of mannose 6-phosphate receptors (MPRs) from the trans-Golgi network (TGN) to endosomes and for Golgi/TGN organization. Here we extend the knowledge of the mechanism of action of Rab31 by demonstrating its interaction with OCRL-1, a phosphatidylinositol 4,5-diphosphate 5-phosphatase (PI(4,5)P2 5-phosphatase) that regulates the levels of PI(4,5)P 2 and PI(4)P, molecules involved in transport and Golgi/TGN organization. We show that Rab31 interacts with OCRL-1 in a yeast two-hybrid system, GST-Rab31 pull-down experiments, and coimmunoprecipitation of OCRL-1 using oligodendrocyte culture lysates. Rab31 and OCRL-1 colocalize in the TGN, post-TGN carriers, and endosomes. Cation-dependent MPR (CD-MPR) is sorted to OCRL-1-containing carriers, but CD63 and vesicular stomatitis virus G (VSVG) are not. siRNA-mediated depletion of endogenous Rab31 causes collapse of the TGN apparatus and markedly decreases the levels of OCRL-1 in the TGN and endosomes. Our observations indicate that the role of Rab31 in the Golgi/TGN structure and transport of MPRs depends on its capability to recruit OCRL-1 to domains of the TGN where the formation of carriers occurs. The importance of our observations is highlighted by the fact that mutation of OCRL-1 causes demyelination in humans. © 2009 Wiley-Liss, Inc.
Registro:
Documento: |
Artículo
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Título: | Interaction of Rab31 and OCRL-1 in oligodendrocytes: Its role in transport of mannose 6-phosphate receptors |
Autor: | Rodriguez-Gabin, A.G.; Ortiz, E.; Demoliner, K.; Si, Q.; Almazan, G.; Larocca, J.N. |
Filiación: | Department of Neurology, Albert Einstein College of Medicine, Yeshiva University, Bronx, NY, United States Departamento de Química Biológica, Instituto de Química Y Fisicoquímica Biológica, UBA-CONICET, Buenos Aires, Argentina Department of Pharmacology and Therapeutics, McGill University, Montreal, QC, Canada Department of Neuroscience, Albert Einstein College of Medicine, Yeshiva University, Bronx, NY, United States
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Palabras clave: | Endosomes; Myelin; Oligodendrocytes; Phosphatidylinositol 4,5-diphosphate 5-phosphatase; Rab proteins; Signaling; Trans-Golgi network; Vesicle transport; cation; CD36 antigen; phosphatase; phosphatidylinositol 4,5 diphosphate 5 phosphatase; Rab protein; small interfering RNA; somatomedin B receptor; unclassified drug; animal cell; animal tissue; article; cell lysate; controlled study; demyelination; endosome; experiment; female; Golgi complex; heterozygote detection; human; human cell; immunoprecipitation; mutation; nerve cell culture; nonhuman; oligodendroglia; priority journal; protein interaction; protein protein interaction; rat; stomatitis; trans Golgi network; two hybrid system; Vesicular stomatitis virus; yeast; Animals; Antigens, CD; Brain; Cations; Cell Membrane; Cells, Cultured; Endosomes; Hela Cells; Humans; Mice; Oligodendroglia; Phosphoric Monoester Hydrolases; Platelet Membrane Glycoproteins; Protein Binding; Protein Conformation; rab GTP-Binding Proteins; Rats; Receptor, IGF Type 2; trans-Golgi Network |
Año: | 2010
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Volumen: | 88
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Número: | 3
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Página de inicio: | 589
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Página de fin: | 604
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DOI: |
http://dx.doi.org/10.1002/jnr.22236 |
Título revista: | Journal of Neuroscience Research
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Título revista abreviado: | J. Neurosci. Res.
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ISSN: | 03604012
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CODEN: | JNRED
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CAS: | phosphatase, 9013-05-2; Antigens, CD; Cations; Cd63 protein, rat; Phosphoric Monoester Hydrolases, 3.1.3.-; Platelet Membrane Glycoproteins; Receptor, IGF Type 2; lysosomal protein GP53; rab GTP-Binding Proteins, 3.6.1.-
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Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03604012_v88_n3_p589_RodriguezGabin |
Referencias:
- Allan, B.B., Moyer, B.D., Balch, W.E., Rab1 recruitment of p115 into a cis-SNARE complex: Programming budding COPII vesicles for fusion [see comments] (2000) Science, 289, pp. 444-448
- Armstrong, J., How do Rab proteins function in membrane traffic? (2000) Int J Biochem Cell Biol, 32, pp. 303-307
- Blewitt, M.E., Gendrel, A.V., Pang, Z., Sparrow, D.B., Whitelaw, N., Craig, J.M., Apedaile, A., Whitelaw, E., SmcHD1, containing a structural-maintenance-of-chromosomes hinge domain, has a critical role in X inactivation (2008) Nat Genet, 40, pp. 663-669
- Bonifacino, J.S., Glick, B.S., The mechanisms of vesicle budding and fusion (2004) Cell, 116, pp. 153-166
- Bonifacino, J.S., Traub, L.M., Signals for sorting of transmembrane proteins to endosomes and lysosomes (2003) Annu Rev Biochem, 72, pp. 395-447
- Bouverat, B.P., Krueger, W.H., Coetzee, T., Bansal, R., Pfeiffer, S.E., Expression of rab GTP-binding proteins during oligodendrocyte differentiation in culture (2000) J Neurosci Res, 59, pp. 446-453
- Brodsky, F.M., Chen, C.Y., Knuehl, C., Towler, M.C., Wakeham, D.E., Biological basket weaving: Formation and function of clathrin-coated vesicles (2001) Annu Rev Cell Dev Biol, 17, pp. 517-568
- Burcelin, R., Rodriguez-Gabin, A.G., Charron, M.J., Almazan, G., Larocca, J.N., Molecular analysis of the monomeric GTP-binding proteins of oligodendrocytes (1997) Brain Res Mol Brain Res, 50, pp. 9-15
- Choudhury, R., Diao, A., Zhang, F., Eisenberg, E., Saint-Pol, A., Williams, C., Konstantakopoulos, A., Lowe, M., Lowe syndrome protein OCRL1 interacts with clathrin and regulates protein trafficking between endosomes and the trans-Golgi network (2005) Mol Biol Cell, 16, pp. 3467-3479
- Cockcroft, S., De Matteis, M.A., Inositol lipids as spatial regulators of membrane traffic (2001) J Membrane Biol, 180, pp. 187-194
- De Matteis, M., Godi, A., Corda, D., Phosphoinositides and the golgi complex (2002) Curr Opin Cell Biol, 14, pp. 434-447
- Dressman, M.A., Olivos-Glander, I.M., Nussbaum, R.L., Suchy, S.F., Ocrl1, a PtdIns(4,5)P2 5-phosphatase, is localized to the trans-Golgi network of fibroblasts and epithelial cells (2000) J Histochem Cytochem, 48, pp. 179-190
- Erdmann, K.S., Mao, Y., McCrea, H.J., Zoncu, R., Lee, S., Paradise, S., Modregger, J., De Camilli, P., A role of the Lowe syndrome protein OCRL in early steps of the endocytic pathway (2007) Dev Cell, 13, pp. 377-390
- Faucherre, A., Desbois, P., Satre, V., Lunardi, J., Dorseuil, O., Gacon, G., Lowe syndrome protein OCRL1 interacts with Rac GTPase in the trans-Golgi network (2003) Hum Mol Genet, 12, pp. 2449-2456
- Godi, A., Santone, I., Pertile, P., Devarajan, P., Stabach, P.R., Morrow, J.S., Di Tullio, G., De Matteis, M.A., ADP ribosylation factor regulates spectrin binding to the Golgi complex (1998) Proc Natl Acad Sci U S A, 95, pp. 8607-8612
- Griffiths, G., Hoflack, B., Simons, K., Mellman, I., Kornfeld, S., The mannose 6-phosphate receptor and the biogenesis of lysosomes (1988) Cell, 52, pp. 329-341
- Habib, R., Bargeton, E., Brissaud, H.E., Raynaud, J., Le Ball, J.C., Constatations anatomiques chez un enfant atteint d'un syndrome de Lowe. (1962) Arch Fr Pediatr, pp. 945-960
- Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., Pease, L.R., Site-directed mutagenesis by overlap extension using the polymerase chain reaction [see comments] (1989) Gene, 77, pp. 51-59
- Huber, L.A., Madison, D.L., Simons, K., Pfeiffer, S.E., Myelin membrane biogenesis by oligodendrocytes. Developmental regulation of low molecular weight GTP-binding proteins (1994) FEBS Lett, 347, pp. 273-278
- 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 (2006) EMBO J, 25, pp. 3750-3761
- Janvier, K., Bonifacino, J.S., Role of the endocytic machinery in the sorting of lysosome-associated membrane proteins (2005) Mol Biol Cell, 16, pp. 4231-4242
- Johnson, J.M., Castle, J., Garrett-Engele, P., Kan, Z., Loerch, P.M., Armour, C.D., Santos, R., Shoemaker, D.D., Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays (2003) Science, 302, pp. 2141-2144
- Larocca, J.N., Almazan, G., Acetylcholine agonists stimulate mitogen-activated protein kinase in oligodendrocyte progenitors by muscarinic receptors (1997) J Neurosci Res, 50, pp. 743-754
- Larocca, J.N., Rodriguez-Gabin, A.G., Myelin biogenesis: Vesicle transport in oligodendrocytes (2002) Neurochem Res, 27, pp. 1313-1329
- Lin, T., Orrison, B.M., Leahey, A.M., Suchy, S.F., Bernard, D.J., Lewis, R.A., Nussbaum, R.L., Spectrum of mutations in the OCRL1 gene in the Lowe oculocerebrorenal syndrome (1997) Am J Hum Genet, 60, pp. 1384-1388
- Madison, D.L., Kruger, W.H., Kim, T., Pfeiffer, S.E., Differential expression of rab3 isoforms in oligodendrocytes and astrocytes (1996) J Neurosci Res, 45, pp. 258-268
- Manders, E.M., Stap, J., Brakenhoff, G.J., van Driel, R., Aten, J.A., Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy (1992) J Cell Sci, 103, pp. 857-862
- McCarthy, K.D., de Vellis, J., Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue (1980) J Cell Biol, 85, pp. 890-902
- Monnier, N., Satre, V., Lerouge, E., Berthoin, F., Lunardi, J., OCRL1 mutation analysis in French Lowe syndrome patients: Implications for molecular diagnosis strategy and genetic counseling (2000) Hum Mutat, 16, pp. 157-165
- Morell, P., Myelin formation, structure, and biochemistry (1994) Basic neuroschemistry: Molecular, cellular, and medical aspects, pp. 147-195. , Siegel B, editor, New York: Raven Press. p
- Mullins, C., Bonifacino, J.S., The molecular machinery for lysosome biogenesis (2001) Bioessays, 23, pp. 333-343
- Nussbaum, R.L., Orrison, B.M., Janne, P.A., Charnas, L., Chinault, A.C., Physical mapping and genomic structure of the Lowe syndrome gene OCRL1 (1997) Hum Genet, 99, pp. 145-150
- Pfeffer, S., A model for Rab GTPase localization (2005) Biochem Soc Trans, 33, pp. 627-630
- Raine, C.S., Morphology of myelin and myelination (1984) Myelination, pp. 1-41. , Morrel P, editor, New York: Plenum Press. p
- Rodriguez-Gabin, A.G., Cammer, M., Almazan, G., Charron, M., Larocca, J.N., Role of rRAB22b, an oligodendrocyte protein, in regulation of transport of vesicles from trans Golgi to endocytic compartments (2001) J Neurosci Res, 66, pp. 1149-1160
- Rodriguez-Gabin, A.G., Almazan, G., Larocca, J.N., Vesicle transport in oligodendrocytes: Probable role of Rab40c protein (2004) J Neurosci Res, 76, pp. 758-770
- Rodriguez-Gabin, A.G., Yin, X., Si, Q., Larocca, J.N., Transport of mannose-6-phosphate receptors from the trans-Golgi network to endosomes requires Rab31 (2009) Exp Cell Res, 315, pp. 2215-2230
- Rouille, Y., Rohn, W., Hoflack, B., Targeting of lysosomal proteins (2000) Semin Cell Dev Biol, 11, pp. 165-171
- Rous, B.A., Reaves, B.J., Ihrke, G., Briggs, J.A., Gray, S.R., Stephens, D.J., Banting, G., Luzio, J.P., Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes (2002) Mol Biol Cell, 13, pp. 1071-1082
- Schneider, J.F., Boltshauser, E., Neuhaus, T.J., Rauscher, C., Martin, E., MRI and proton spectroscopy in Lowe syndrome (2001) Neuropediatrics, 32, pp. 45-48
- Siddhanta, A., Radulescu, A., Stankewich, M.C., Morrow, J.S., Shields, D., Fragmentation of the Golgi apparatus. A role for beta III spectrin and synthesis of phosphatidylinositol 4,5-bisphosphate (2003) J Biol Chem, 278, pp. 1957-1965
- Ungewickell, A.J., Majerus, P.W., Increased levels of plasma lysosomal enzymes in patients with Lowe syndrome (1999) Proc Natl Acad Sci U S A, 96, pp. 13342-13344
- Vicinanza, M., D'Angelo, G., Di Campli, A., De Matteis, M.A., Function and dysfunction of the PI system in membrane trafficking (2008) EMBO J, 27, pp. 2457-2470
- Wang, J., Sun, H.Q., Macia, E., Kirchhausen, T., Watson, H., Bonifacino, J.S., Yin, H.L., PI4P promotes the recruitment of the GGA adaptor proteins to the trans-Golgi network and regulates their recognition of the ubiquitin sorting signal (2007) Mol Biol Cell, 18, pp. 2646-2655
- Zerial, M., McBride, H., Rab proteins as membrane organizers (2001) Nat Rev Mol Cell Biol, 2, pp. 107-117
- Zerial, M., Stenmark, H., Rab GTPases in vesicular transport (1993) Curr Opin Cell Biol, 5, pp. 613-620
- Zhang, X., Jefferson, A.B., Auethavekiat, V., Majerus, P.W., The protein deficient in Lowe syndrome is a phosphatidylinositol-4,5-bisphosphate 5-phosphatase (1995) Proc Natl Acad Sci U S A, 92, pp. 4853-4856
- Zhang, X., Hartz, P.A., Philip, E., Racusen, L.C., Majerus, P.W., Cell lines from kidney proximal tubules of a patient with Lowe syndrome lack OCRL inositol polyphosphate 5-phosphatase and accumulate phosphatidylinositol 4,5-bisphosphate (1998) J Biol Chem, 273, pp. 1574-1582
Citas:
---------- APA ----------
Rodriguez-Gabin, A.G., Ortiz, E., Demoliner, K., Si, Q., Almazan, G. & Larocca, J.N.
(2010)
. Interaction of Rab31 and OCRL-1 in oligodendrocytes: Its role in transport of mannose 6-phosphate receptors. Journal of Neuroscience Research, 88(3), 589-604.
http://dx.doi.org/10.1002/jnr.22236---------- CHICAGO ----------
Rodriguez-Gabin, A.G., Ortiz, E., Demoliner, K., Si, Q., Almazan, G., Larocca, J.N.
"Interaction of Rab31 and OCRL-1 in oligodendrocytes: Its role in transport of mannose 6-phosphate receptors"
. Journal of Neuroscience Research 88, no. 3
(2010) : 589-604.
http://dx.doi.org/10.1002/jnr.22236---------- MLA ----------
Rodriguez-Gabin, A.G., Ortiz, E., Demoliner, K., Si, Q., Almazan, G., Larocca, J.N.
"Interaction of Rab31 and OCRL-1 in oligodendrocytes: Its role in transport of mannose 6-phosphate receptors"
. Journal of Neuroscience Research, vol. 88, no. 3, 2010, pp. 589-604.
http://dx.doi.org/10.1002/jnr.22236---------- VANCOUVER ----------
Rodriguez-Gabin, A.G., Ortiz, E., Demoliner, K., Si, Q., Almazan, G., Larocca, J.N. Interaction of Rab31 and OCRL-1 in oligodendrocytes: Its role in transport of mannose 6-phosphate receptors. J. Neurosci. Res. 2010;88(3):589-604.
http://dx.doi.org/10.1002/jnr.22236