A GDP-bound of rab1 inhibits protein export from the endoplasmic reticulum and transport between Golgi compartments

doi:10.1083/jcb.125.2.225

This Article

	Full Text (PDF, 3215K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Nuoffer, C.
	Articles by Balch, W. E.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Nuoffer, C.
	Articles by Balch, W. E.


Social Bookmarking

	What's this?

ARTICLES

A GDP-bound of rab1 inhibits protein export from the endoplasmic reticulum and transport between Golgi compartments

C Nuoffer, HW Davidson, J Matteson, J Meinkoth and WE Balch
Department of Cell Biology, Scripps Research Institute, La Jolla, California 92037.

Rab1 is a small GTPase regulating vesicular traffic between early compartments of the secretory pathway. To explore the role of rab1 we have analyzed the function of a mutant (rab1a[S25N]) containing a substitution which perturbs Mg2+ coordination and reduces the affinity for GTP, resulting in a form which is likely to be restricted to the GDP-bound state. The rab1a(S25N) mutant led to a marked reduction in protein export from the ER in vivo and in vitro, indicating that a guanine nucleotide exchange protein (GEP) is critical for the recruitment of rab1 during vesicle budding. The mutant protein required posttranslational isoprenylation for inhibition and behaved as a competitive inhibitor of wild-type rab1 function. Both rab1a and rab1b (92% identity) were able to antagonize the inhibitory activity of the rab1a(S25N) mutant, suggesting that these two isoforms are functionally interchangeable. The rab1 mutant also inhibited transport between Golgi compartments and resulted in an apparent loss of the Golgi apparatus, suggesting that Golgi integrity is coupled to rab1 function in vesicular traffic.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Patel, N., Singh, S. B., Basu, S. K., Mukhopadhyay, A. (2008). Leishmania requires Rab7-mediated degradation of endocytosed hemoglobin for their growth. Proc. Natl. Acad. Sci. USA 105: 3980-3985 [Abstract] [Full Text]
Sklan, E. H., Serrano, R. L., Einav, S., Pfeffer, S. R., Lambright, D. G., Glenn, J. S. (2007). TBC1D20 Is a Rab1 GTPase-activating Protein That Mediates Hepatitis C Virus Replication. J. Biol. Chem. 282: 36354-36361 [Abstract] [Full Text]
Brumell, J. H., Scidmore, M. A. (2007). Manipulation of Rab GTPase Function by Intracellular Bacterial Pathogens. Microbiol. Mol. Biol. Rev. 71: 636-652 [Abstract] [Full Text]
Machner, M. P., Isberg, R. R. (2007). A Bifunctional Bacterial Protein Links GDI Displacement to Rab1 Activation. Science 318: 974-977 [Abstract] [Full Text]
Beske, O., Reichelt, M., Taylor, M. P., Kirkegaard, K., Andino, R. (2007). Poliovirus infection blocks ERGIC-to-Golgi trafficking and induces microtubule-dependent disruption of the Golgi complex. J. Cell Sci. 120: 3207-3218 [Abstract] [Full Text]
Saraste, J., Goud, B. (2007). Functional Symmetry of Endomembranes. Mol. Biol. Cell 18: 1430-1436 [Abstract] [Full Text]
Dupre, D. J., Robitaille, M., Ethier, N., Villeneuve, L. R., Mamarbachi, A. M., Hebert, T. E. (2006). Seven Transmembrane Receptor Core Signaling Complexes Are Assembled Prior to Plasma Membrane Trafficking. J. Biol. Chem. 281: 34561-34573 [Abstract] [Full Text]
Chen, C. Y., Balch, W. E. (2006). The Hsp90 Chaperone Complex Regulates GDI-dependent Rab Recycling. Mol. Biol. Cell 17: 3494-3507 [Abstract] [Full Text]
Ren, G., Vajjhala, P., Lee, J. S., Winsor, B., Munn, A. L. (2006). The BAR Domain Proteins: Molding Membranes in Fission, Fusion, and Phagy. Microbiol. Mol. Biol. Rev. 70: 37-120 [Abstract] [Full Text]
Derre, I., Isberg, R. R. (2005). LidA, a Translocated Substrate of the Legionella pneumophila Type IV Secretion System, Interferes with the Early Secretory Pathway. Infect. Immun. 73: 4370-4380 [Abstract] [Full Text]
Cleator, J. H., Ravenell, R., Kurtz, D. T., Hildebrandt, J. D. (2004). A Dominant Negative G{alpha}s Mutant That Prevents Thyroid-stimulating Hormone Receptor Activation of cAMP Production and Inositol 1,4,5-Trisphosphate Turnover: COMPETITION BY DIFFERENT G PROTEINS FOR ACTIVATION BY A COMMON RECEPTOR. J. Biol. Chem. 279: 36601-36607 [Abstract] [Full Text]
Wu, G., Zhao, G., He, Y. (2003). Distinct Pathways for the Trafficking of Angiotensin II and Adrenergic Receptors from the Endoplasmic Reticulum to the Cell Surface: Rab1-INDEPENDENT TRANSPORT OF A G PROTEIN-COUPLED RECEPTOR. J. Biol. Chem. 278: 47062-47069 [Abstract] [Full Text]
Alvarez, C., Garcia-Mata, R., Brandon, E., Sztul, E. (2003). COPI Recruitment Is Modulated by a Rab1b-dependent Mechanism. Mol. Biol. Cell 14: 2116-2127 [Abstract] [Full Text]
Vernoud, V., Horton, A. C., Yang, Z., Nielsen, E. (2003). Analysis of the Small GTPase Gene Superfamily of Arabidopsis. Plant Physiol. 131: 1191-1208 [Abstract] [Full Text]
Mohrmann, K., Gerez, L., Oorschot, V., Klumperman, J., van der Sluijs, P. (2002). rab4 Function in Membrane Recycling from Early Endosomes Depends on a Membrane to Cytoplasm Cycle. J. Biol. Chem. 277: 32029-32035 [Abstract] [Full Text]
Cheung, A. Y., Chen, C. Y.-h., Glaven, R. H., de Graaf, B. H. J., Vidali, L., Hepler, P. K., Wu, H.-m. (2002). Rab2 GTPase Regulates Vesicle Trafficking between the Endoplasmic Reticulum and the Golgi Bodies and Is Important to Pollen Tube Growth. Plant Cell 14: 945-962 [Abstract] [Full Text]
Mesa, R., Salomon, C., Roggero, M., Stahl, P. D., Mayorga, L. S. (2002). Rab22a affects the morphology and function of the endocytic pathway. J. Cell Sci. 114: 4041-4049 [Abstract] [Full Text]
Tisdale, E. J. (2002). Glyceraldehyde-3-phosphate Dehydrogenase Is Phosphorylated by Protein Kinase Ciota /lambda and Plays a Role in Microtubule Dynamics in the Early Secretory Pathway. J. Biol. Chem. 277: 3334-3341 [Abstract] [Full Text]
Huang, M., Weissman, J. T., Beraud-Dufour, S., Luan, P., Wang, C., Chen, W., Aridor, M., Wilson, I. A., Balch, W. E. (2001). Crystal structure of Sar1-GDP at 1.7 A resolution and the role of the NH2 terminus in ER export. JCB 155: 937-948 [Abstract] [Full Text]
Takai, Y., Sasaki, T., Matozaki, T. (2001). Small GTP-Binding Proteins. Physiol. Rev. 81: 153-208 [Abstract] [Full Text]
Wilcke, M., Johannes, L., Galli, T., Mayau, V., Goud, B., Salamero, J. (2000). Rab11 Regulates the Compartmentalization of Early Endosomes Required for Efficient Transport from Early Endosomes to the Trans-Golgi Network. JCB 151: 1207-1220 [Abstract] [Full Text]
Echard, A., Opdam, F. J.M., de Leeuw, H. J.P.C., Jollivet, F., Savelkoul, P., Hendriks, W., Voorberg, J., Goud, B., Fransen, J. A.M. (2000). Alternative Splicing of the Human Rab6A Gene Generates Two Close but Functionally Different Isoforms. Mol. Biol. Cell 11: 3819-3833 [Abstract] [Full Text]
Allan, B. B., Moyer, B. D., Balch, W. E. (2000). Rab1 Recruitment of p115 into a cis-SNARE Complex: Programming Budding COPII Vesicles for Fusion. Science 289: 444-448 [Abstract] [Full Text]
Erdman, R. A., Shellenberger, K. E., Overmeyer, J. H., Maltese, W. A. (2000). Rab24 Is an Atypical Member of the Rab GTPase Family. DEFICIENT GTPase ACTIVITY, GDP DISSOCIATION INHIBITOR INTERACTION, AND PRENYLATION OF Rab24 EXPRESSED IN CULTURED CELLS. J. Biol. Chem. 275: 3848-3856 [Abstract] [Full Text]
Opdam, F., Echard, A, Croes, H., van den Hurk, J., van de Vorstenbosch, R., Ginsel, L., Goud, B, Fransen, J. (2000). The small GTPase Rab6B, a novel Rab6 subfamily member, is cell-type specifically expressed and localised to the Golgi apparatus. J. Cell Sci. 113: 2725-2735 [Abstract]
Knight, J. B., Cao, K. T., Gibson, G. V., Olson, A. L. (2000). Expression of a Prenylation-Deficient Rab4 Interferes with Propagation of Insulin Signaling through Insulin Receptor Substrate-1. Endocrinology 141: 208-218 [Abstract] [Full Text]
Somsel Rodman, J, Wandinger-Ness, A (2000). Rab GTPases coordinate endocytosis. J. Cell Sci. 113: 183-192 [Abstract]
Alvarez, C., Fujita, H., Hubbard, A., Sztul, E. (1999). ER to Golgi Transport: Requirement for P115 at a Pre-Golgi Vtc Stage. JCB 147: 1205-1222 [Abstract] [Full Text]
Chung, S.-H., Joberty, G., Gelino, E. A., Macara, I. G., Holz, R. W. (1999). Comparison of the Effects on Secretion in Chromaffin and PC12 Cells of Rab3 Family Members and Mutants. EVIDENCE THAT INHIBITORY EFFECTS ARE INDEPENDENT OF DIRECT INTERACTION WITH RABPHILIN3. J. Biol. Chem. 274: 18113-18120 [Abstract] [Full Text]
Tisdale, E. J. (1999). A Rab2 Mutant with Impaired GTPase Activity Stimulates Vesicle Formation from Pre-Golgi Intermediates. Mol. Biol. Cell 10: 1837-1849 [Abstract] [Full Text]
Luan, P., Balch, W. E., Emr, S. D., Burd, C. G. (1999). Molecular Dissection of Guanine Nucleotide Dissociation Inhibitor Function in Vivo. Rab-INDEPENDENT BINDING TO MEMBRANES AND ROLE OF RAB RECYCLING FACTORS. J. Biol. Chem. 274: 14806-14817 [Abstract] [Full Text]
del Valle, M, Robledo, Y, Sandoval, I. (1999). Membrane flow through the Golgi apparatus: specific disassembly of the cis-Golgi network by ATP depletion. J. Cell Sci. 112: 4017-4029 [Abstract]
Field, H, Ali, B., Sherwin, T, Gull, K, Croft, S., Field, M. (1999). TbRab2p, a marker for the endoplasmic reticulum of Trypanosoma brucei, localises to the ERGIC in mammalian cells. J. Cell Sci. 112: 147-156 [Abstract]
Wu, S.-K., Luan, P., Matteson, J., Zeng, K., Nishimura, N., Balch, W. E. (1998). Molecular Role for the Rab Binding Platform of Guanine Nucleotide Dissociation Inhibitor in Endoplasmic Reticulum to Golgi Transport. J. Biol. Chem. 273: 26931-26938 [Abstract] [Full Text]
Jones, S., Richardson, C. J., Litt, R. J., Segev, N. (1998). Identification of Regulators for Ypt1 GTPase Nucleotide Cycling. Mol. Biol. Cell 9: 2819-2837 [Abstract] [Full Text]
Ren, M., Xu, G., Zeng, J., De Lemos-Chiarandini, C., Adesnik, M., 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. USA 95: 6187-6192 [Abstract] [Full Text]
Aridor, M., Weissman, J., Bannykh, S., Nuoffer, C., Balch, W. E. (1998). Cargo Selection by the COPII Budding Machinery during Export from the ER. JCB 141: 61-70 [Abstract] [Full Text]
Yoon, Y., Pitts, K. R., Dahan, S., McNiven, M. A. (1998). A Novel Dynamin-like Protein Associates with Cytoplasmic Vesicles and Tubules of the Endoplasmic Reticulum in Mammalian Cells. JCB 140: 779-793 [Abstract] [Full Text]
Peter, F, Wong, S., Subramaniam, V., Tang, B., Hong, W (1998). Alpha-SNAP but not gamma-SNAP is required for ER-Golgi transport after vesicle budding and the Rab1-requiring step but before the EGTA-sensitive step. J. Cell Sci. 111: 2625-2633 [Abstract]
Yang, W., Storrie, B. (1998). Scattered Golgi Elements during Microtubule Disruption Are Initially Enriched in Trans-Golgi Proteins. Mol. Biol. Cell 9: 191-207 [Abstract] [Full Text]
Ivessa, N. E., Gravotta, D., De Lemos-Chiarandini, C., Kreibich, G. (1997). Functional Protein Prenylation Is Required for the Brefeldin A-dependent Retrograde Transport from the Golgi Apparatus to the Endoplasmic Reticulum. J. Biol. Chem. 272: 20828-20834 [Abstract] [Full Text]
Turner, M. D., Plutner, H., Balch, W. E. (1997). A Rab GTPase Is Required for Homotypic Assembly of the Endoplasmic Reticulum. J. Biol. Chem. 272: 13479-13483 [Abstract] [Full Text]
Mukhopadhyay, A., Funato, K., Stahl, P. D. (1997). Rab7 Regulates Transport from Early to Late Endocytic Compartments in Xenopus Oocytes. J. Biol. Chem. 272: 13055-13059 [Abstract] [Full Text]
Mukhopadhyay, A., Barbieri, A. M., Funato, K., Roberts, R., Stahl, P. D. (1997). Sequential Actions of Rab5 and Rab7 Regulate Endocytosis in the Xenopus Oocyte. JCB 136: 1227-1237 [Abstract] [Full Text]
Martinez, O., Antony, C., Pehau-Arnaudet, G., Berger, E. G., Salamero, J., Goud, B. (1997). GTP-bound forms of rab6 induce the redistribution of Golgi proteins into the�endoplasmic�reticulum. Proc. Natl. Acad. Sci. USA 94: 1828-1833 [Abstract] [Full Text]
Satoh, A, Tokunaga, F, Kawamura, S, Ozaki, K (1997). In situ inhibition of vesicle transport and protein processing in the dominant negative Rab1 mutant of Drosophila. J. Cell Sci. 110: 2943-2953 [Abstract]
Jin, M., Saucan, L., Farquhar, M. G., Palade, G. E. (1996). Rab1a and Multiple Other Rab Proteins Are Associated with the Transcytotic Pathway in Rat Liver. J. Biol. Chem. 271: 30105-30113 [Abstract] [Full Text]
Tisdale, E. J., Balch, W. E. (1996). Rab2 Is Essential for the Maturation of Pre-Golgi Intermediates. J. Biol. Chem. 271: 29372-29379 [Abstract] [Full Text]
Mayer, T., Touchot, N., Elazar, Z. (1996). Transport between cis and medial Golgi Cisternae Requires the Function of the Ras-related Protein Rab6. J. Biol. Chem. 271: 16097-16103 [Abstract] [Full Text]
Wilson, A. L., Erdman, R. A., Maltese, W. A. (1996). Association of Rab1B with GDP-dissociation Inhibitor (GDI) Is Required for Recycling but Not Initial Membrane Targeting of the Rab Protein. J. Biol. Chem. 271: 10932-10940 [Abstract] [Full Text]
Pan, J. Y., Sanford, J. C., Wessling-Resnick, M. (1996). Influence of Mg[IMAGE] on the Structure and Function of Rab5. J. Biol. Chem. 271: 1322-1328 [Abstract] [Full Text]
McConlogue, L., Castellano, F., deWit, C., Schenk, D., Maltese, W. A. (1996). Differential Effects of a Rab6 Mutant on Secretory Versus Amyloidogenic Processing of Alzheimer's beta-Amyloid Precursor Protein. J. Biol. Chem. 271: 1343-1348 [Abstract] [Full Text]
Lowe, S., Wong, S., Hong, W (1996). The mammalian ARF-like protein 1 (Arl1) is associated with the Golgi complex. J. Cell Sci. 109: 209-220 [Abstract]
Simpson, J. C., Dascher, C., Roberts, L. M., Lord, J. M., Balch, W. E. (1995). Ricin Cytotoxicity Is Sensitive to Recycling between the Endoplasmic Reticulum and the Golgi Complex. J. Biol. Chem. 270: 20078-20083 [Abstract] [Full Text]
Chung, S.-H., Takai, Y., Holz, R. W. (1995). Evidence That the Rab3a-binding Protein, Rabphilin3a, Enhances Regulated Secretion. J. Biol. Chem. 270: 16714-16718 [Abstract] [Full Text]
Janoueix-Lerosey, I., Jollivet, F., Camonis, J., Marche, P. N., Goud, B. (1995). Two-hybrid System Screen with the Small GTP-binding Protein Rab6. J. Biol. Chem. 270: 14801-14808 [Abstract] [Full Text]
Dugan, J. M., deWit, C., McConlogue, L., Maltese, W. A. (1995). The Ras-related GTP-binding Protein, Rab1B, Regulates Early Steps in Exocytic Transport and Processing of [IMAGE]-Amyloid Precursor Protein. J. Biol. Chem. 270: 10982-10989 [Abstract] [Full Text]
Saraste, J, Lahtinen, U, Goud, B (1995). Localization of the small GTP-binding protein rab1p to early compartments of the secretory pathway. J. Cell Sci. 108: 1541-1552 [Abstract]
Bannykh, S., Aridor, M., Plutner, H., Rowe, T., Balch, W.E. (1995). Regulated Export of Cargo from the Endoplasmic Reticulum of Mammalian Cells. Cold Spring Harb Symp Quant Biol 60: 127-137 [Abstract]
Maltese, W. A., Wilson, S., Tan, Y., Suomensaari, S., Sinha, S., Barbour, R., McConlogue, L. (2001). Retention of the Alzheimer's Amyloid Precursor Fragment C99 in the Endoplasmic Reticulum Prevents Formation of Amyloid beta -Peptide. J. Biol. Chem. 276: 20267-20279 [Abstract] [Full Text]
Overmeyer, J. H., Wilson, A. L., Maltese, W. A. (2001). Membrane Targeting of a Rab GTPase That Fails to Associate with Rab Escort Protein (REP) or Guanine Nucleotide Dissociation Inhibitor (GDI)*. J. Biol. Chem. 276: 20379-20386 [Abstract] [Full Text]
Wu, G., Yussman, M. G., Barrett, T. J., Hahn, H. S., Osinska, H., Hilliard, G. M., Wang, X., Toyokawa, T., Yatani, A., Lynch, R. A., Robbins, J., Dorn, G. W. II (2001). Increased Myocardial Rab GTPase Expression: A Consequence and Cause of Cardiomyopathy. Circ. Res. 89: 1130-1137 [Abstract] [Full Text]