Arf1-GTP-induced Tubule Formation Suggests a Function of Arf Family Proteins in Curvature Acquisition at Sites of Vesicle Budding

Overview

Journal J Biol Chem

Specialty Biochemistry

Date 2008 Aug 12

PMID 18693248

Citations 61

Authors

Michael Krauss

Jun-Yong Jia

Aurelien Roux

Rainer Beck

Felix T Wieland

Pietro De Camilli

Volker Haucke

Affiliations

Soon will be listed here.

Abstract

ADP-ribosylation factor (Arf) and related small GTPases play crucial roles in membrane traffic within the exo- and endocytic pathways. Arf proteins in their GTP-bound state are associated with curved membrane buds and tubules, frequently together with effector coat proteins to which they bind. Here we report that Arf1 is found on membrane tubules originating from the Golgi complex where it colocalizes with COPI and GGA1 vesicle coat proteins. Arf1 also induces tubulation of liposomes in vitro. Mutations within the amino-terminal amphipathic helix (NTH) of Arf1 affect the number of Arf1-positive tubules in vivo and its property to tubulate liposomes. Moreover, hydrophilic substitutions within the hydrophobic part of its NTH impair Arf1-catalyzed budding of COPI vesicles in vitro. Our data indicate that GTP-controlled local induction of high curvature membranes is an important property of Arf1 that might be shared by a subgroup of Arf/Arl family GTPases.

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References

Polishchuk R, San Pietro E, Di Pentima A, Tete S, Bonifacino J . Ultrastructure of long-range transport carriers moving from the trans Golgi network to peripheral endosomes. Traffic. 2006; 7(8):1092-103. DOI: 10.1111/j.1600-0854.2006.00453.x. View

Antonny B . Membrane deformation by protein coats. Curr Opin Cell Biol. 2006; 18(4):386-94. DOI: 10.1016/j.ceb.2006.06.003. View

Robinson M . Adaptable adaptors for coated vesicles. Trends Cell Biol. 2004; 14(4):167-74. DOI: 10.1016/j.tcb.2004.02.002. View

Yahara N, Ueda T, Sato K, Nakano A . Multiple roles of Arf1 GTPase in the yeast exocytic and endocytic pathways. Mol Biol Cell. 2001; 12(1):221-38. PMC: 30579. DOI: 10.1091/mbc.12.1.221. View

Farsad K, De Camilli P . Mechanisms of membrane deformation. Curr Opin Cell Biol. 2003; 15(4):372-81. DOI: 10.1016/s0955-0674(03)00073-5. View

Takei K, Slepnev V, Haucke V, De Camilli P . Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol. 1999; 1(1):33-9. DOI: 10.1038/9004. View

Gillingham A, Munro S . The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol. 2007; 23:579-611. DOI: 10.1146/annurev.cellbio.23.090506.123209. View

Cai H, Reinisch K, Ferro-Novick S . Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell. 2007; 12(5):671-82. DOI: 10.1016/j.devcel.2007.04.005. View

Gallop J, Jao C, Kent H, Butler P, Evans P, Langen R . Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 2006; 25(12):2898-910. PMC: 1500843. DOI: 10.1038/sj.emboj.7601174. View

10.

Peter B, Kent H, Mills I, Vallis Y, Butler P, Evans P . BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science. 2003; 303(5657):495-9. DOI: 10.1126/science.1092586. View

11.

Rothman J . Lasker Basic Medical Research Award. The machinery and principles of vesicle transport in the cell. Nat Med. 2002; 8(10):1059-62. DOI: 10.1038/nm770. View

12.

Roux A, Uyhazi K, Frost A, De Camilli P . GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature. 2006; 441(7092):528-31. DOI: 10.1038/nature04718. View

13.

Bos J, Rehmann H, Wittinghofer A . GEFs and GAPs: critical elements in the control of small G proteins. Cell. 2007; 129(5):865-77. DOI: 10.1016/j.cell.2007.05.018. View

14.

Randazzo P . Functional interaction of ADP-ribosylation factor 1 with phosphatidylinositol 4,5-bisphosphate. J Biol Chem. 1997; 272(12):7688-92. View

15.

Caplan S, Naslavsky N, Hartnell L, Lodge R, Polishchuk R, Donaldson J . A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J. 2002; 21(11):2557-67. PMC: 126039. DOI: 10.1093/emboj/21.11.2557. View

16.

Losonczi J, Prestegard J . Nuclear magnetic resonance characterization of the myristoylated, N-terminal fragment of ADP-ribosylation factor 1 in a magnetically oriented membrane array. Biochemistry. 1998; 37(2):706-16. DOI: 10.1021/bi9717791. View

17.

Itoh T, Erdmann K, Roux A, Habermann B, Werner H, De Camilli P . Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell. 2005; 9(6):791-804. DOI: 10.1016/j.devcel.2005.11.005. View

18.

Lee M, Orci L, Hamamoto S, Futai E, Ravazzola M, Schekman R . Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell. 2005; 122(4):605-17. DOI: 10.1016/j.cell.2005.07.025. View

19.

Kahn R, Cherfils J, Elias M, Lovering R, Munro S, Schurmann A . Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins. J Cell Biol. 2006; 172(5):645-50. PMC: 2063696. DOI: 10.1083/jcb.200512057. View

20.

Sun Z, Anderl F, Frohlich K, Zhao L, Hanke S, Brugger B . Multiple and stepwise interactions between coatomer and ADP-ribosylation factor-1 (Arf1)-GTP. Traffic. 2007; 8(5):582-93. DOI: 10.1111/j.1600-0854.2007.00554.x. View