The non-catalytic carboxyl-terminal domain of ARFGAP1 regulates actin cytoskeleton reorganization by antagonizing the activation of Rac1

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Siu, Ka Yu ^a   Yu, Mei Kuen ^a   Wu, Xinggang ^a   Zong, Min ^a   Roth, Michael G ^b   Chan, Hsiao Chang ^a   Yu, Sidney ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1 GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR;

ANIMAL CELL; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL MEMBRANE; CELL MIGRATION; CELL SPREADING; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; ENZYME ACTIVE SITE; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; BIOCATALYSIS; CELL SHAPE; CELL STRAIN HEK293; CHEMISTRY; CHO CELL; CRICETULUS; ENZYME ACTIVATION; GENE DELETION; GENETICS; HAMSTER; HELA CELL; METABOLISM; PROTEIN TERTIARY STRUCTURE;

MAMMALIA;

ACTINS; ADP-RIBOSYLATION FACTORS; ANIMALS; BIOCATALYSIS; CELL SHAPE; CHO CELLS; CRICETINAE; CRICETULUS; CYTOSKELETON; ENZYME ACTIVATION; GTPASE-ACTIVATING PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; PROTEIN STRUCTURE, TERTIARY; RAC1 GTP-BINDING PROTEIN; SEQUENCE DELETION;

EID: 79953685463     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018458     Document Type: Article

References (63)

1. Roth MG, (2000) Arf. GTPases 24, In: Hall A, editors. Oxford University Press pp. 176-197.
2. D'Souza-Schorey C, Chavrier P, (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7: 347-358.
3. Shome K, Nie Y, Romero G, (1998) ADP-ribosylation Factor Proteins Mediate Agonist-induced Activation of Phospholipase D. Journal of Biological Chemistry 273: 30836-30841.
4. Miura K, Jacques KM, Stauffer S, Kubosaki A, Zhu K, et al. (2002) ARAP1: a point of convergence for Arf and Rho signaling. Mol Cell 9: 109-119.
5. Krugmann S, Anderson KE, Ridley SH, Risso N, McGregor A, et al. (2002) Identification of ARAP3, a novel PI3K effector regulating both Arf and Rho GTPases, by selective capture on phosphoinositide affinity matrices. Mol Cell 9: 95-108.
6. Klarlund JK, Guilherme A, Holik JJ, Virbasius JV, Chawla A, et al. (1997) Signaling by phosphoinositide-3,4,5-trisphosphate through proteins containing pleckstrin and Sec7 homology domains. Science 275: 1927-1930.
7. Kahn RA, Gilman AG, (1986) The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP binding protein. J Biol Chem 261: 7906-7911.
8. Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, et al. (1999) Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99: 521-532.
9. Hiroki I, Paul AR, (2007) Arf GAPs and Their Interacting Proteins. Traffic 8: 1465-1475.
10. Hammonds-Odie LP, Jackson TR, Profit AA, Blader IJ, Turck CW, et al. (1996) Identification and cloning of centaurin-alpha. A novel phosphatidylinositol 3,4,5-trisphosphate-binding protein from rat brain. J Biol Chem 271: 18859-18868.
11. Cockcroft S, Thomas GM, Fensome A, Geny B, Cunningham E, et al. (1994) Phospholipase D: a downstream effector of ARF in granulocytes. Science 263: 523-526.
12. Brown HA, Gutowski S, Moomaw CR, Slaughter C, Sternweis PC, (1993) ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell 75: 1137-1144.
13. Kahn RA, Bruford E, Inoue H, Logsdon JM, Nie Z, et al. (2008) Consensus nomenclature for the human ArfGAP domain-containing proteins. The Journal of Cell Biology 182: 1039-1044.
14. Cukierman E, Huber I, Rotman M, Cassel D, (1995) The ARF1 GTPase-activating protein: zinc finger motif and Golgi complex localization. Science 270: 1999-2002.
15. Poon PP, Wang X, Rotman M, Huber I, Cukierman E, et al. (1996) Saccharomyces cerevisiae Gcs1 is an ADP-ribosylation factor GTPase-activating protein. Proc Natl Acad Sci U S A 93: 10074-10077.
16. Aoe T, Cukierman E, Lee A, Cassel D, Peters PJ, et al. (1997) The KDEL receptor, ERD2, regulates intracellular traffic by recruiting a GTPase-activating protein for ARF1. Embo J 16: 7305-7316.
17. Yu S, Roth MG, (2002) Casein Kinase I Regulates Membrane Binding by ARF GAP1. Mol Biol Cell 13: 2559-2570.
18. Bigay J, Casella J-F, Drin G, Mesmin B, Antonny B, (2005) ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO J 24: 2244-2253.
19. Robinson M, Poon PP, Schindler C, Murray LE, Kama R, et al. (2006) The Gcs1 Arf-GAP Mediates Snc1,2 v-SNARE Retrieval to the Golgi in Yeast. Mol Biol Cell 17: 1845-1858.
20. Poon PP, Nothwehr SF, Singer RA, Johnston GC, (2001) The Gcs1 and Age2 ArfGAP proteins provide overlapping essential function for transport from the yeast trans-Golgi network. J Cell Biol 155: 1239-1250.
21. Blader IJ, Cope MJ, Jackson TR, Profit AA, Greenwood AF, et al. (1999) GCS1, an Arf guanosine triphosphatase-activating protein in Saccharomyces cerevisiae, is required for normal actin cytoskeletal organization in vivo and stimulates actin polymerization in vitro. Mol Biol Cell 10: 581-596.
22. Yang S, Cope MJTV, Drubin DG, (1999) Sla2p Is Associated with the Yeast Cortical Actin Cytoskeleton via Redundant Localization Signals. Mol Biol Cell 10: 2265-2283.
23. Pruyne D, Bretscher A, (2000) Polarization of cell growth in yeast. J Cell Sci 113: 571-585.
24. Nobes CD, Hall A, (1995) Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81: 53-62.
25. Kozma R, Ahmed S, Best A, Lim L, (1995) The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol 15: 1942-1952.
26. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A, (1992) The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70: 401-410.
27. Ridley AJ, Hall A, (1992) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70: 389-399.
28. Song J, Khachikian Z, Radhakrishna H, Donaldson J, (1998) Localization of endogenous ARF6 to sites of cortical actin rearrangement and involvement of ARF6 in cell spreading. J Cell Sci 111: 2257-2267.
29. Radhakrishna H, Klausner RD, Donaldson JG, (1996) Aluminum fluoride stimulates surface protrusions in cells overexpressing the ARF6 GTPase. The Journal of Cell Biology 134: 935-947.
30. Radhakrishna H, Al-Awar O, Khachikian Z, Donaldson J, (1999) ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J Cell Sci 112: 855-866.
31. Boshans RL, Szanto S, van Aelst L, D'Souza-Schorey C, (2000) ADP-ribosylation factor 6 regulates actin cytoskeleton remodeling in coordination with Rac1 and RhoA. Mol Cell Biol 20: 3685-3694.
32. Aoe T, Huber I, Vasudevan C, Watkins SC, Romero G, et al. (1999) The KDEL receptor regulates a GTPase-activating protein for ADP-ribosylation factor 1 by interacting with its non-catalytic domain. J Biol Chem 274: 20545-20549.
33. Frank S, Upender S, Hansen SH, Casanova JE, (1998) ARNO is a guanine nucleotide exchange factor for ADP-ribosylation factor 6. J Biol Chem 273: 23-27.
34. Zhao Z-s, Manser E, Loo T-H, Lim L, (2000) Coupling of PAK-Interacting Exchange Factor PIX to GIT1 Promotes Focal Complex Disassembly. Mol Cell Biol 20: 6354-6363.
35. Turner CE, Brown MC, Perrotta JA, Riedy MC, Nikolopoulos SN, et al. (1999) Paxillin LD4 Motif Binds PAK and PIX through a Novel 95-kD Ankyrin Repeat, ARF-GAP Protein: A Role in Cytoskeletal Remodeling. The Journal of Cell Biology 145: 851-863.
36. Nishiya N, Kiosses WB, Han J, Ginsberg MH, (2005) An [alpha]4 integrin-paxillin-Arf-GAP complex restricts Rac activation to the leading edge of migrating cells. Nat Cell Biol 7: 343-352.
37. Bagrodia S, Bailey D, Lenard Z, Hart M, Guan JL, et al. (1999) A Tyrosine-phosphorylated Protein That Binds to an Important Regulatory Region on the Cool Family of p21-activated Kinase-binding Proteins. Journal of Biological Chemistry 274: 22393-22400.
38. Oshiro T, Koyama S, Sugiyama S, Kondo A, Onodera Y, et al. (2002) Interaction of POB1, a Downstream Molecule of Small G Protein Ral, with PAG2, a Paxillin-binding Protein, Is Involved in Cell Migration. Journal of Biological Chemistry 277: 38618-38626.
39. Onodera Y, Hashimoto S, Hashimoto A, Morishige M, Mazaki Y, et al. (2005) Expression of AMAP1, an ArfGAP, provides novel targets to inhibit breast cancer invasive activities. EMBO J 24: 963-973.
40. Oda A, Wada I, Miura K, Okawa K, Kadoya T, et al. (2003) CrkL Directs ASAP1 to Peripheral Focal Adhesions. Journal of Biological Chemistry 278: 6456-6460.
41. Liu Y, Yerushalmi GM, Grigera PR, Parsons JT, (2005) Mislocalization or Reduced Expression of Arf GTPase-activating Protein ASAP1 Inhibits Cell Spreading and Migration by Influencing Arf1 GTPase Cycling. Journal of Biological Chemistry 280: 8884-8892.
42. Chen J-L, Fucini RV, Lacomis L, Erdjument-Bromage H, Tempst P, et al. (2005) Coatomer-bound Cdc42 regulates dynein recruitment to COPI vesicles. The Journal of Cell Biology 169: 383-389.
43. D'Souza-Schorey C, Boshans RL, McDonough M, Stahl PD, Van Aelst L, (1997) A role for POR1, a Rac1-interacting protein, in ARF6-mediated cytoskeletal rearrangements. Embo J 16: 5445-5454.
44. Shin O, Exton JH, William E, Balch CJDaAH, (2005) Assays and Properties of Arfaptin 2 Binding to Rac1 and ADP[hyphen (true graphic)]Ribosylation Factors (Arfs). Methods in Enzymology Academic Press pp. 359-367.
45. Valderrama F, Luna A, Babi T, Martinez-Menarguez JA, Ballesta J, et al. (2000) The Golgi-associated COPI-coated buds and vesicles contain beta/gamma-actin. Proceedings of the National Academy of Sciences of the United States of America 97: 1560-1565.
46. Valderrama F, Duran JM, Babia T, Barth H, Renau-Piqueras J, et al. (2001) Actin Microfilaments Facilitate the Retrograde Transport from the Golgi Complex to the Endoplasmic Reticulum in Mammalian Cells. Traffic 2: 717-726.
47. Heimann K, Percival JM, Weinberger R, Gunning P, Stow JL, (1999) Specific isoforms of actin-binding proteins on distinct populations of Golgi-derived vesicles. J Biol Chem 274: 10743-10750.
48. Fucini RV, Navarrete A, Vadakkan C, Lacomis L, Erdjument-Bromage H, et al. (2000) Activated ADP-ribosylation factor assembles distinct pools of actin on golgi membranes. J Biol Chem 275: 18824-18829.
49. Fucini RV, Chen JL, Sharma C, Kessels MM, Stamnes M, (2002) Golgi vesicle proteins are linked to the assembly of an actin complex defined by mAbp1. Mol Biol Cell 13: 621-631.
50. Jones DH, Morris JB, Morgan CP, Kondo H, Irvine RF, et al. (2000) Type I phosphatidylinositol 4-phosphate 5-kinase directly interacts with ADP-ribosylation factor 1 and is responsible for phosphatidylinositol 4,5-bisphosphate synthesis in the golgi compartment. J Biol Chem 275: 13962-13966.
51. Roth MG, Bi K, Ktistakis NT, Yu S, (1999) Phospholipase D as an effector for ADP-ribosylation factor in the regulation of vesicular traffic. Chemistry and Physics of Lipids 98: 141-152.
52. Rein U, Andag U, Duden R, Schmitt HD, Spang A, (2002) ARF-GAP mediated interaction between the ER-Golgi v-SNAREs and the COPI coat. The Journal of Cell Biology 157: 395-404.
53. Lanoix J, Ouwendijk J, Stark A, Szafer E, Cassel D, et al. (2001) Sorting of Golgi resident proteins into different subpopulations of COPI vesicles: a role for ArfGAP1. J Cell Biol 155: 1199-1212.
54. Jou TS, Leung SM, Fung LM, Ruiz WG, Nelson WJ, et al. (2000) Selective alterations in biosynthetic and endocytic protein traffic in Madin-Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol Biol Cell 11: 287-304.
55. Yoshimori T, Keller P, Roth MG, Simons K, (1996) Different biosynthetic transport routes to the plasma membrane in BHK and CHO cells. The Journal of Cell Biology 133: 247-256.
56. Stow JL, Fath KR, Burgess DR, (1998) Budding roles for myosin II on the Golgi. Trends in Cell Biology 8: 138-141.
57. Rozelle AL, Machesky LM, Yamamoto M, Driessens MHE, Insall RH, et al. (2000) Phosphatidylinositol 4,5-bisphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Current Biology 10: 311-320.
58. Merrifield CJ, Feldman ME, Wan L, Almers W, (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4: 691-698.
59. Lorra C, Huttner WB, (1999) The mesh hypothesis of Golgi dynamics. Nat Cell Biol 1: E113-115.
60. Godbey W, Wu K, Hirasaki G, Mikos A, (1999) Improved packing of poly(ethylenimine)/DNA complexes increases transfection efficiency. Gene Theraphy 6: 1380-1388.
61. Burbelo PD, Drechsel D, Hall A, (1995) A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J Biol Chem 270: 29071-29074.
62. Ren X-D, Schwartz MA, Balch CJD WE, Alan H, (2000) Determination of GTP loading on Rho. Methods in Enzymology Academic Press pp. 264-272.
63. Puertollano R, Randazzo PA, Presley JF, Hartnell LM, Bonifacino JS, (2001) The GGAs Promote ARF-Dependent Recruitment of Clathrin to the TGN. Cell 105: 93-102.