Role for Gcs1p in Regulation of Arl1p at Trans-Golgi Compartments

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2005 Jun 25

PMID 15975906

Citations 19

Authors

Ya-Wen Liu

Chun-Fang Huang

Kai-Bin Huang

Fang-Jen S Lee

Affiliations

Soon will be listed here.

Abstract

ADP-ribosylation factor (ARF) and ARF-like (ARL) proteins are members of the ARF family, which are critical components of several different vesicular trafficking pathways. ARFs have little or no detectable GTPase activity without the assistance of a GTPase-activating protein (GAP). Here, we demonstrate that yeast Gcs1p exhibits GAP activity toward Arl1p and Arf1p in vitro, and Arl1p can interact with Gcs1p in a GTP-dependent manner. Arl1p was observed both on trans-Golgi and in cytosol and was recruited from cytosol to membranes in a GTP-dependent manner. In gcs1 mutant cells, the fraction of Arl1p in cytosol relative to trans-Golgi was less than it was in wild-type cells. Increasing Gcs1p levels returned the distribution toward that of wild-type cells. Both Arl1p and Gcs1p influenced the distribution of Imh1p, an Arl1p effector. Our data are consistent with the conclusion that Arl1p moves in a dynamic equilibrium between trans-Golgi and cytosol, and the release of Arl1p from membranes in cells requires the hydrolysis of bound GTP, which is accelerated by Gcs1p.

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References

Donaldson J . Filling in the GAPs in the ADP-ribosylation factor story. Proc Natl Acad Sci U S A. 2000; 97(8):3792-4. PMC: 33976. DOI: 10.1073/pnas.97.8.3792. View

Mitsui K, Yaguchi S, Tsurugi K . The GTS1 gene, which contains a Gly-Thr repeat, affects the timing of budding and cell size of the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1994; 14(8):5569-78. PMC: 359076. DOI: 10.1128/mcb.14.8.5569-5578.1994. View

Bhamidipati A, Lewis S, Cowan N . ADP ribosylation factor-like protein 2 (Arl2) regulates the interaction of tubulin-folding cofactor D with native tubulin. J Cell Biol. 2000; 149(5):1087-96. PMC: 2174823. DOI: 10.1083/jcb.149.5.1087. View

Szafer E, Pick E, Rotman M, Zuck S, Huber I, Cassel D . Role of coatomer and phospholipids in GTPase-activating protein-dependent hydrolysis of GTP by ADP-ribosylation factor-1. J Biol Chem. 2000; 275(31):23615-9. DOI: 10.1074/jbc.M003171200. View

Eugster A, Frigerio G, Dale M, Duden R . COP I domains required for coatomer integrity, and novel interactions with ARF and ARF-GAP. EMBO J. 2000; 19(15):3905-17. PMC: 306616. DOI: 10.1093/emboj/19.15.3905. View

Lin C, Huang P, Liao W, Cheng H, Huang C, Kuo J . ARL4, an ARF-like protein that is developmentally regulated and localized to nuclei and nucleoli. J Biol Chem. 2000; 275(48):37815-23. DOI: 10.1074/jbc.M002470200. View

Coe J, Murray L, Dawes I . Identification of a sporulation-specific promoter regulating divergent transcription of two novel sporulation genes in Saccharomyces cerevisiae. Mol Gen Genet. 1994; 244(6):661-72. DOI: 10.1007/BF00282757. View

Rothman J . Mechanisms of intracellular protein transport. Nature. 1994; 372(6501):55-63. DOI: 10.1038/372055a0. View

Cukierman E, Huber I, Rotman M, Cassel D . The ARF1 GTPase-activating protein: zinc finger motif and Golgi complex localization. Science. 1995; 270(5244):1999-2002. DOI: 10.1126/science.270.5244.1999. View

10.

Ding M, Vitale N, Tsai S, Adamik R, Moss J, Vaughan M . Characterization of a GTPase-activating protein that stimulates GTP hydrolysis by both ADP-ribosylation factor (ARF) and ARF-like proteins. Comparison to the ARD1 gap domain. J Biol Chem. 1996; 271(39):24005-9. DOI: 10.1074/jbc.271.39.24005. View

11.

Wang X, Hoekstra M, DeMaggio A, Dhillon N, Vancura A, Kuret J . Prenylated isoforms of yeast casein kinase I, including the novel Yck3p, suppress the gcs1 blockage of cell proliferation from stationary phase. Mol Cell Biol. 1996; 16(10):5375-85. PMC: 231536. DOI: 10.1128/MCB.16.10.5375. View

12.

Poon P, Wang X, Rotman M, Huber I, Cukierman E, Cassel D . Saccharomyces cerevisiae Gcs1 is an ADP-ribosylation factor GTPase-activating protein. Proc Natl Acad Sci U S A. 1996; 93(19):10074-7. PMC: 38338. DOI: 10.1073/pnas.93.19.10074. View

13.

Lowe S, Wong S, Hong W . The mammalian ARF-like protein 1 (Arl1) is associated with the Golgi complex. J Cell Sci. 1996; 109 ( Pt 1):209-20. DOI: 10.1242/jcs.109.1.209. View

14.

Golemis E, Khazak V . Alternative yeast two-hybrid systems. The interaction trap and interaction mating. Methods Mol Biol. 1997; 63:197-218. DOI: 10.1385/0-89603-481-X:197. View

15.

Randazzo P . Resolution of two ADP-ribosylation factor 1 GTPase-activating proteins from rat liver. Biochem J. 1997; 324 ( Pt 2):413-9. PMC: 1218446. DOI: 10.1042/bj3240413. View

16.

Antonny B, Huber I, Paris S, Chabre M, Cassel D . Activation of ADP-ribosylation factor 1 GTPase-activating protein by phosphatidylcholine-derived diacylglycerols. J Biol Chem. 1998; 272(49):30848-51. DOI: 10.1074/jbc.272.49.30848. View

17.

Lee F, Huang C, Yu W, Buu L, Lin C, Huang M . Characterization of an ADP-ribosylation factor-like 1 protein in Saccharomyces cerevisiae. J Biol Chem. 1998; 272(49):30998-1005. DOI: 10.1074/jbc.272.49.30998. View

18.

Moss J, Vaughan M . Molecules in the ARF orbit. J Biol Chem. 1998; 273(34):21431-4. DOI: 10.1074/jbc.273.34.21431. View

19.

Brown M, Andrade J, Radhakrishna H, Donaldson J, Cooper J, Randazzo P . ASAP1, a phospholipid-dependent arf GTPase-activating protein that associates with and is phosphorylated by Src. Mol Cell Biol. 1998; 18(12):7038-51. PMC: 109286. DOI: 10.1128/MCB.18.12.7038. View

20.

Premont R, Claing A, Vitale N, Freeman J, Pitcher J, Patton W . beta2-Adrenergic receptor regulation by GIT1, a G protein-coupled receptor kinase-associated ADP ribosylation factor GTPase-activating protein. Proc Natl Acad Sci U S A. 1998; 95(24):14082-7. PMC: 24330. DOI: 10.1073/pnas.95.24.14082. View