Structural basis for Arf6-MKLP1 complex formation on the Flemming body responsible for cytokinesis

EMBO Journal

Volumn 31, Issue 11, 2012, Pages 2590-2603

  Makyio, Hisayoshi ^a   Ohgi, Minako ^b   Takei, Tomomi ^b   Takahashi, Senye ^b   Takatsu, Hiroyuki ^b   Katoh, Yohei ^b   Hanai, Ayako ^b   Ueda, Tomoko ^b   Kanaho, Yasunori ^c   Xie, Yong ^d   Shin, Hye Won ^b   Kamikubo, Hironari ^e   Kataoka, Mikio ^e   Kawasaki, Masato ^a   Kato, Ryuichi ^a   Wakatsuki, Soichi ^a   Nakayama, Kazuhisa ^b  

^a INSTITUTE OF MATERIALS STRUCTURE SCIENCE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

^d INSTITUTE OF MEDICINAL PLANT DEVELOPMENT   (China)

^e NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Arf6; cytokinesis; Flemming body; MKLP1; X ray crystallography

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ALPHA TUBULIN; BETA TUBULIN; GUANOSINE TRIPHOSPHATASE; HOMODIMER; KINESIN; PROTEIN MKLP1; SMALL INTERFERING RNA; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; BIOACCUMULATION; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOKINESIS; FLEMMING BODY; MEMBRANE MODEL; MICROTUBULE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SPINDLE POLE BODY;

ADP-RIBOSYLATION FACTORS; ANIMALS; CRYSTALLOGRAPHY, X-RAY; CYTOKINESIS; HELA CELLS; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; PROTEIN BINDING;

EID: 84861846404     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.89     Document Type: Article

References (59)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D 66: 213-221
2. Balasubramanian MK, Bi E, Glotzer M (2004) Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr Biol 14: R806-R818 (Pubitemid 39239356)
3. Boman AL, Kuai J, Zhu X, Chen J, Kuriyama R, Kahn RA (1999) Arf proteins binds to mitotic kinesin-like protein 1 (MKLP1) in a GTP-dependent fashion. Cell Motil Cytoskeleton 44: 119-132 (Pubitemid 29480307)
4. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 50: 760-763
5. Chavrier P, Ménétrey J (2010) Toward a structural understanding of Arf family: effector specificity. Structure 18: 1552-1558
6. Chen VB, Arendall III WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D 66: 12-21
7. Derrien V, Couillault C, Franco M, Martineau S, Montcourrier P, Houlgatte R, Chavrier P (2002) A conserved C-terminal domain of EFA6-family ARF6-guanine nucleotide exchange factors induces lengthening of microvilli-like membrane protrusions. J Cell Sci 115: 2867-2879
8. D'Souza-Schorey C, Chavrier P (2006) ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 7: 347-358
9. Dyer N, Rebollo E, Dominguez P, Elkhatib N, Chavrier P, Daviet L, González C, González-Gaitán M (2007) Spermatocyte cytokinesis requires rapid membrane addition mediated by ARF6 on central spindle recycling endosomes. Development 134: 4437-4447
10. Emoto K, Inadome H, Kanaho Y, Narumiya S, Umeda M (2005) Local change in phospholipid composition at the cleavage furrow is essential for completion of cytokinesis. J Biol Chem 280: 37901-37907 (Pubitemid 41642402)
11. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D 66: 486-501
12. Field SJ, Madson N, Kerr ML, Galbraith KAA, Kennedy CE, Tahiliani M, Wilkins A, Cantley LC (2005) PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr Biol 15: 1407-1412 (Pubitemid 41097546)
13. Fielding AB, Schonteich E, Matheson J, Wilson G, Yu X, Hickson GRX, Srivastava S, Baldwin SA, Prekeris R, Gould GW (2005) Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J 24: 3389-3399 (Pubitemid 41486777)
14. Glotzer M (2005) The molecular requirements for cytokinesis. Science 307: 1735-1739
15. Guinier A, Fournet G (1955) Small-angle scattering of X-rays. New York: Wiley
16. Hanzal-Bayer M, Renault L, Roversi P, Wittinghofer A, Hillig RC (2002) The complex of Arl2-GTP and PDE delta: from structure to function. EMBO J 21: 2095-2106 (Pubitemid 34516768)
17. Hiraki M, Kato R, Nagai M, Satoh T, Hirano S, Ihara K, Kudo N, Nagae M, Kobayashi M, Inoue M, Uejima T, Oda S, Chavas LM, Akutsu M, Yamada Y, Kawasaki M, Matsugaki N, Igarashi N, Suzuki M, Wakatsuki S (2006) Development of an automated large-scale protein-crystallization and monitoring system for high-throughput protein-structure analyses. Acta Crystallogr D 62: 1058-1065 (Pubitemid 44337380)
18. Holm L, Rosenström P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38((Web Server issue)): W545-W549
19. Honda A, Nogami M, Yokozeki T, Yamazaki M, Nakamura H, Watanabe H, Kawamoto K, Nakayama K, Morris AJ, Frohman MA, Kanaho Y (1999) Phosphatidylinositol 4-phosphate 5-kinase a is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99: 521-532
20. Isabet T, Montagnac G, Regazzoni K, Raynal B, El Khadali F, England P, Franco M, Chavrier P, Houdusse A, Ménétrey J (2009) The structural basis of Arf effector specificity: the crystal structure of ARF6 in a complex with JIP4. EMBO J 28: 2835-2845
21. Ishizaki R, Shin H-W, Mitsuhashi H, Nakayama K (2008) Redundant roles of BIG2 and BIG1, guanine-nucleotide exchange factors for ADP-ribosylation factors in membrane traffic between the trans-Golgi network and endosomes. Mol Biol Cell 19: 2650-2660
22. Kahn RA, Cherfils J, Elias M, Lovering RC, Munro S, Schurmann A (2006) Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins. J Cell Biol 172: 645-650
23. Kawasaki M, Nakayama K, Wakatsuki S (2005) Membrane recruitment of effector proteins by Arf and Rab GTPases. Curr Opin Struct Biol 15: 681-689 (Pubitemid 41668525)
24. Klarlund JK, Tsiaras W, Holik JJ, Chawla A, Czech MP (2000) Distinct phosphoinositide binding selectivities for pleckstrin homology domains of GRP1-like proteins based on diglycine versus triglycine motifs. J Biol Chem 275: 32816-32821
25. Kraulis P (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946-950
26. Macia E, Luton F, Partisani M, Cherfils J, Chardin P, Franco M (2004) The GDP-bound form of Arf6 is located at the plasma membrane. J Cell Sci 117: 2389-2398 (Pubitemid 38807505)
27. Man Z, Kondo Y, Koga H, Umino H, Nakayama K, Shin H-W (2011) Arfaptins are localized to the trans-Golgi by interaction with Arl1, but not Arfs. J Biol Chem 286: 11569-11578
28. Matuliene J, Kuriyama R (2002) Kinesin-like protein CHO1 is required for the formation of midbody matrix and the completion of cytokinesis in mammalian cells. Mol Biol Cell 13: 1832-1845 (Pubitemid 34651475)
29. Ménétrey J, Macia E, Pasqualato S, Franco M, Cherfils J (2000) Structure of Arf6-GDP suggests a basis for guanine nucleotide exchange factors specificity. Nat Struct Biol 7: 466-469 (Pubitemid 30414466)
30. Ménétrey J, Perderiset M, Cicolari J, Dubois T, Elkhatib N, El Khadali F, Franco M, Chavrier P, Houdusse A (2007) Structural basis for ARF1-mediated recruitment of ARHGAP21 to Golgi membranes. EMBO J 26: 1953-1962 (Pubitemid 46624047)
31. Merithew E, Hatherly S, Dumas JJ, Lawe DC, Heller-Harrison R, Lambright DG (2001) Structural plasticity of an invariant hydrophobic triad in the switch regions of Rab GTPases is a determinant of effector recognition. J Biol Chem 276: 13982-13988
32. Merritt EA, Bacon DJ (1997) Raster3D: photorealistic molecular graphics. Methods Enzymol 277: 505-524 (Pubitemid 27390937)
33. Mishima M, Kaitna S, Glotzer M (2002) Central spindle assembly and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev Cell 2: 41-54 (Pubitemid 34065905)
34. Montagnac G, Sibarita J-B, Loubéry S, Daviet L, Romao M, Raposo G, Chavrier P (2009) ARF6 interacts with JIP4 to control a motor switch mechanism regulating endosome traffic in cytokinesis. Curr Biol 19: 184-195
35. Neto H, Collins LL, Gould GW (2011) Vesicle trafficking and membrane remodelling in cytokinesis. Biochem J 437: 13-24
36. O'Neal CJ, Jobling MG, Holmes RK, Hol WG (2005) Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 309: 1093-1096
37. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326 (Pubitemid 27085611)
38. Painter J, Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D 62: 439-450
39. Panic B, Perisic O, Veprintsev DB, Williams RL, Munro S (2003) Structural basis for Arl1-dependent targeting of homodimeric GRIP domains to the Golgi apparatus. Mol Cell 12: 863-874 (Pubitemid 37352780)
40. Pasqualato S, Menetrey J, Franco M, Cherfils J (2001) The structural GDP/GTP cycle of human Arf6. EMBO Rep 2: 234-238 (Pubitemid 32273303)
41. Pasqualato S, Renault L, Cherfils J (2002) Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for 'front-back' communication. EMBO Rep 3: 1035-1041 (Pubitemid 35469894)
42. Potterton L, McNicholas S, Krissinel E, Gruber J, Cowtan K, Emsley P, Murshudov GN, Cohen S, Perrakis A, Noble M (2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr D 60: 2288-2294
43. Prekeris R, Gould GW (2008) Breaking up is hard to do: membrane traffic in cytokinesis. J Cell Sci 121: 1569-1576 (Pubitemid 351911813)
44. Schiel JA, Park K,Morphew MK, Reid E, Hoenger A, Prekeris R (2011) Endocytic membrane fusion and buckling-induced microtubule severing mediate cell abscission. J Cell Sci 124: 1411-1424
45. Schonteich E, Pilli M, Simon GC, Matern HT, Junutula JR, Sentz D, Holmes RK, Prekeris R (2007) Molecular characterization of Rab11-FIP3 binding to ARF GTPases. Eur J Cell Biol 86: 417-431 (Pubitemid 47099509)
46. Schrodinger LLC (2010; The PyMOL Molecular Graphics System, Version 1.3r1.
47. Schuermann JP, Tanner JJ (2003) MRSAD: using anomalous dispersion from S atoms collected at Cu Kalpha wavelength in molecular- replacement structure determination. Acta Crystallogr D 59: 1731-1736 (Pubitemid 37245125)
48. Schweitzer JK, D'Souza-Schorey C (2002) Localization and activation of the ARF6 GTPase during cleavage furrow ingression and cytokinesis. J Biol Chem 277: 27210-27216 (Pubitemid 34951737)
49. Schweitzer JK, D'Souza-Schorey C (2005) A requirement for ARF6 during the completion of cytokinesis. Exp Cell Res 311: 74-83 (Pubitemid 41527176)
50. Shiba T, Kawasaki M, Takatsu H, Nogi T, Matsugaki N, Igarashi N, Suzuki M, Kato R, Nakayama K, Wakatsuki S (2003) Molecular mechanism of membrane recruitment of GGA by ARF in lysosomal protein transport. Nat Struct Biol 10: 386-393 (Pubitemid 36523274)
51. Shiba T, Koga H, Shin H-W, Kawasaki M, Kato R, Nakayama K, Wakatsuki S (2006) Structural basis for Rab11-dependent membrane recruitment of family of Rab11-interacting protein (FIP3)/ Arfophilin-1. Proc Natl Acad Sci USA 103: 15416-15421 (Pubitemid 44625606)
52. Shin H-W, Morinaga N, Noda M, Nakayama K (2004) BIG2, a guanine nucleotide exchange factor for ADP-ribosylation factors: its localization to recycling endosomes and implication in the endosome integrity. Mol Biol Cell 15: 5283-5294 (Pubitemid 39564724)
53. Steigemann P, Gerlich DW (2009) Cytokinetic abscission: cellular dynamics at the midbody. Trends Cell Biol 19: 606-616
54. Suzuki T, Kanai Y, Hara T, Sasaki J, Sasaki T, Kohara M, Maehama T, Taya C, Shitara H, Yonekawa H, Frohman MA, Yokozeki T, Kanaho Y (2006) Crucial role of the small GTPase ARF6 in hepatic cord formation during liver development. Mol Cell Biol 26: 6149-6156 (Pubitemid 44204533)
55. Takahashi S, Takei T, Koga H, Takatsu H, Shin H-W, Nakayama K (2011) Distinct roles of Rab11 and Arf6 in the regulation of Rab11- FIP3/Arfophilin-1 localization in mitotic cells. Genes Cells 16: 938-950
56. Takatsu H, Yoshino K, Toda K, Nakayama K (2002) GGA proteins associate with Golgi membranes through interaction between their GGAH domains and ADP-ribosylation factors. Biochem J 365: 369-378 (Pubitemid 36135309)
57. Yu X, Prekeris R, Gould GW (2007) Role of endosomal Rab GTPases in cytokinesis. Eur J Cell Biol 86: 25-35 (Pubitemid 44896971)
58. Zhang T, Li S, Zhang Y, Zhong C, Lai Z, Ding J (2009) Crystal structure of the ARL2-GTP-BART complex reveals a novel recognition and binding mode of small GTPase with effector. Structure 17: 602-610
59. Zhu C, Bossy-Metzel E, Jiang W (2005) Recruitment of MKLP1 to the spindle midzone/midbody by INCENP is essential for midbody formation and completion of cytokinesis in human cells. Biochem J 389: 373-381 (Pubitemid 41021140)