Structural and functional analysis of FIP2 binding to the endosome-localised Rab25 GTPase

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 12, 2013, Pages 2679-2690

  Lall, Patrick ^a   Horgan, Conor P ^b   Oda, Shunichiro ^a   Franklin, Edward ^a   Sultana, Azmiri ^a   Hanscom, Sara R ^b   McCaffrey, Mary W ^b   Khan, Amir R ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Cancer; Crystal structure; Endosome; FIP2; Rab11; Rab25

Indexed keywords

AUREOBASIDIN A; FIP2 PROTEIN; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; RAB25 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BIOLOGICAL ACTIVITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA SEQUENCE; ENDOSOME; ENTHALPY; FEMALE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; ISOTHERMAL TITRATION CALORIMETRY; OVARY CANCER; PLASMID; PRENYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS; TWO HYBRID SYSTEM; WESTERN BLOTTING; X RAY CRYSTALLOGRAPHY;

EUKARYOTA;

EID: 84885353097     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.09.005     Document Type: Article

References (79)

1. E.E. Kelly, C.P. Horgan, B. Goud, and M.W. McCaffrey The Rab family of proteins: 25 years on Biochem. Soc. Trans. 40 2012 1337 1347
2. D.A. Andres, M.C. Seabra, M.S. Brown, S.A. Armstrong, T.E. Smeland, F.P. Cremers, and J.L. Goldstein cDNA cloning of component A of Rab geranylgeranyl transferase and demonstration of its role as a Rab escort protein Cell 73 1993 1091 1099 (Pubitemid 23180484)
3. A. Bernards GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila Biochim. Biophys. Acta 1603 2003 47 82 (Pubitemid 36262941)
4. R.S. Goody, A. Rak, and K. Alexandrov The structural and mechanistic basis for recycling of Rab proteins between membrane compartments Cell. Mol. Life Sci. 62 2005 1657 1670 (Pubitemid 41176048)
5. F.A. Barr Rab GTPases and membrane identity: causal or inconsequential? J. Cell Biol. 202 2013 191 199
6. S.R. Pfeffer Rab GTPase regulation of membrane identity Curr. Opin. Cell Biol. 25 2013 414 419
7. J. Blumer, Y.W. Wu, R.S. Goody, and A. Itzen Specific localization of Rabs at intracellular membranes Biochem. Soc. Trans. 40 2012 1421 1425
8. A.E. Booth, M.C. Seabra, and A.N. Hume Rab27a and melanosomes: a model to investigate the membrane targeting of Rabs Biochem. Soc. Trans. 40 2012 1383 1388
9. J.E. Walker, M. Saraste, M.J. Runswick, and N.J. Gay Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold EMBO J. 1 1982 945 951
10. M. Saraste, P.R. Sibbald, and A. Wittinghofer The P-loop - a common motif in ATP- and GTP-binding proteins Trends Biochem. Sci. 15 1990 430 434
11. I.R. Vetter, and A. Wittinghofer The guanine nucleotide-binding switch in three dimensions Science 294 2001 1299 1304 (Pubitemid 33063089)
12. C. Stroupe, and A.T. Brunger Crystal structures of a Rab protein in its inactive and active conformations J. Mol. Biol. 304 2000 585 598 (Pubitemid 32006192)
13. E. Merithew, S. Hatherly, J.J. Dumas, D.C. Lawe, R. Heller-Harrison, and D.G. Lambright Structural plasticity of an invariant hydrophobic triad in the switch regions of Rab GTPases is a determinant of effector recognition J. Biol. Chem. 276 2001 13982 13988
14. J.B. Pereira-Leal, and M.C. Seabra The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily J. Mol. Biol. 301 2000 1077 1087
15. A.S. Burguete, T.D. Fenn, A.T. Brunger, and S.R. Pfeffer Rab and Arl GTPase family members cooperate in the localization of the Golgin GCC185 Cell 132 2008 286 298 (Pubitemid 351181231)
16. H. Fernandes, E. Franklin, and A.R. Khan Crystallization of an engineered RUN domain of Rab6-interacting protein 1/DENND5 Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67 2011 556 560
17. S. Eathiraj, X. Pan, C. Ritacco, and D.G. Lambright Structural basis of family-wide Rab GTPase recognition by rabenosyn-5 Nature 436 2005 415 419 (Pubitemid 41059053)
18. M.T. Lee, A. Mishra, and D.G. Lambright Structural mechanisms for regulation of membrane traffic by rab GTPases Traffic 10 2009 1377 1389
19. A.R. Khan, and J. Menetrey Structural biology of Arf and Rab GTPases' effector recruitment and specificity Structure 21 2013 1284 1297
20. X. Hou, N. Hagemann, S. Schoebel, W. Blankenfeldt, R.S. Goody, K.S. Erdmann, and A. Itzen A structural basis for Lowe syndrome caused by mutations in the Rab-binding domain of OCRL1 EMBO J. 30 2011 1659 1670
21. M. Kukimoto-Niino, A. Sakamoto, E. Kanno, K. Hanawa-Suetsugu, T. Terada, M. Shirouzu, M. Fukuda, and S. Yokoyama Structural basis for the exclusive specificity of Slac2-a/melanophilin for the Rab27 GTPases Structure 16 2008 1478 1490
22. L.M. Chavas, K. Ihara, M. Kawasaki, S. Torii, T. Uejima, R. Kato, T. Izumi, and S. Wakatsuki Elucidation of Rab27 recruitment by its effectors: structure of Rab27a bound to Exophilin4/Slp2-a Structure 16 2008 1468 1477
23. C. Ostermeier, and A.T. Brunger Structural basis of Rab effector specificity: crystal structure of the small G protein Rab3A complexed with the effector domain of rabphilin-3A Cell 96 1999 363 374 (Pubitemid 29077590)
24. W.N. Jagoe, A.J. Lindsay, R.J. Read, A.J. McCoy, M.W. McCaffrey, and A.R. Khan Crystal structure of rab11 in complex with rab11 family interacting protein 2 Structure 14 2006 1273 1283 (Pubitemid 44177808)
25. A. Mishra, S. Eathiraj, S. Corvera, and D.G. Lambright Structural basis for Rab GTPase recognition and endosome tethering by the C2H2 zinc finger of early endosomal autoantigen 1 (EEA1) Proc. Natl. Acad. Sci. U. S. A. 107 2010 10866 10871
26. M. Fukuda Distinct Rab27 binding affinities of Slp2-a and Slac2-a/melanophilin: hierarchy of Rab27A effectors Biochem. Biophys. Res. Commun. 343 2006 666 674
27. J.R. Goldenring, K.R. Shen, H.D. Vaughan, and I.M. Modlin Identification of a small GTP-binding protein, Rab25, expressed in the gastrointestinal mucosa, kidney, and lung J. Biol. Chem. 268 1993 18419 18422 (Pubitemid 23273765)
28. E.E. Kelly, C.P. Horgan, and M.W. McCaffrey Rab11 proteins in health and disease Biochem. Soc. Trans. 40 2012 1360 1367
29. C.P. Horgan, and M.W. McCaffrey The dynamic Rab11-FIPs Biochem. Soc. Trans. 37 2009 1032 1036
30. S. Mitra, K.W. Cheng, and G.B. Mills Rab25 in cancer: a brief update Biochem. Soc. Trans. 40 2012 1404 1408
31. K.W. Cheng, J.P. Lahad, W.L. Kuo, A. Lapuk, K. Yamada, N. Auersperg, J. Liu, K. Smith-McCune, K.H. Lu, D. Fishman, J.W. Gray, and G.B. Mills The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers Nat. Med. 10 2004 1251 1256 (Pubitemid 39540444)
32. P.T. Caswell, H.J. Spence, M. Parsons, D.P. White, K. Clark, K.W. Cheng, G.B. Mills, M.J. Humphries, A.J. Messent, K.I. Anderson, M.W. McCaffrey, B.W. Ozanne, and J.C. Norman Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments Dev. Cell 13 2007 496 510 (Pubitemid 47514517)
33. M.A. Dozynkiewicz, N.B. Jamieson, I. Macpherson, J. Grindlay, P.V. van den Berghe, A. von Thun, J.P. Morton, C. Gourley, P. Timpson, C. Nixon, C.J. McKay, R. Carter, D. Strachan, K. Anderson, O.J. Sansom, P.T. Caswell, and J.C. Norman Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression Dev. Cell 22 2012 131 145
34. P. Amornphimoltham, K. Rechache, J. Thompson, A. Masedunskas, K. Leelahavanichkul, V. Patel, A. Molinolo, J.S. Gutkind, and R. Weigert Rab25 regulates invasion and metastasis in head and neck cancer Clin. Cancer Res. 19 2013 1375 1388
35. J.M. Cheng, M. Ding, A. Aribi, P. Shah, and K. Rao Loss of RAB25 expression in breast cancer Int. J. Cancer 118 2006 2957 2964
36. J.M. Cheng, L. Volk, D.K. Janaki, S. Vyakaranam, S. Ran, and K.A. Rao Tumor suppressor function of Rab25 in triple-negative breast cancer Int. J. Cancer 126 2010 2799 2812
37. K.T. Nam, H.J. Lee, J.J. Smith, L.A. Lapierre, V.P. Kamath, X. Chen, B.J. Aronow, T.J. Yeatman, S.G. Bhartur, B.C. Calhoun, B. Condie, N.R. Manley, R.D. Beauchamp, R.J. Coffey, and J.R. Goldenring Loss of Rab25 promotes the development of intestinal neoplasia in mice and is associated with human colorectal adenocarcinomas J. Clin. Invest. 120 2010 840 849
38. J.R. Goldenring, and K.T. Nam Rab25 as a tumour suppressor in colon carcinogenesis Br. J. Cancer 104 2011 33 36
39. M. Tong, K.W. Chan, J.Y. Bao, K.Y. Wong, J.N. Chen, P.S. Kwan, K.H. Tang, L. Fu, Y.R. Qin, S. Lok, X.Y. Guan, and S. Ma Rab25 is a tumor suppressor gene with anti-angiogenic and anti-invasive activities in esophageal squamous cell carcinoma Cancer Res. 72 2012 6024 6035
40. T. Shiba, H. Koga, H.W. Shin, M. Kawasaki, R. Kato, K. Nakayama, and S. Wakatsuki Structural basis for Rab11-dependent membrane recruitment of a family of Rab11-interacting protein 3 (FIP3)/Arfophilin-1 Proc. Natl. Acad. Sci. U. S. A. 103 2006 15416 15421 (Pubitemid 44625606)
41. S. Eathiraj, A. Mishra, R. Prekeris, and D.G. Lambright Structural basis for Rab11-mediated recruitment of FIP3 to recycling endosomes J. Mol. Biol. 364 2006 121 135 (Pubitemid 44647251)
42. E.E. Kelly, C.P. Horgan, C. Adams, T.M. Patzer, D.M. Ni Shuilleabhain, J.C. Norman, and M.W. McCaffrey Class I Rab11-family interacting proteins are binding targets for the Rab14 GTPase Biol. Cell 102 2010 51 62
43. A.J. Lindsay, and M.W. McCaffrey Rab11-FIP2 functions in transferrin recycling and associates with endosomal membranes via its COOH-terminal domain J. Biol. Chem. 277 2002 27193 27199 (Pubitemid 34951735)
44. A.J. Lindsay, A.G. Hendrick, G. Cantalupo, F. Senic-Matuglia, B. Goud, C. Bucci, and M.W. McCaffrey Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein J. Biol. Chem. 277 2002 12190 12199 (Pubitemid 34952785)
45. W.N. Jagoe, S.R. Jackson, A.J. Lindsay, M.W. McCaffrey, and A.R. Khan Purification, crystallization and preliminary X-ray diffraction studies of Rab11 in complex with Rab11-FIP2 Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62 2006 692 694
46. M.T. Damiani, M. Pavarotti, N. Leiva, A.J. Lindsay, M.W. McCaffrey, and M.I. Colombo Rab coupling protein associates with phagosomes and regulates recycling from the phagosomal compartment Traffic 5 2004 785 797 (Pubitemid 39307262)
47. C.P. Horgan, S.R. Hanscom, R.S. Jolly, C.E. Futter, and M.W. McCaffrey Rab11-FIP3 links the Rab11 GTPase and cytoplasmic dynein to mediate transport to the endosomal-recycling compartment J. Cell Sci. 123 2010 181 191
48. C.P. Horgan, S.R. Hanscom, and M.W. McCaffrey Dynein LIC1 localizes to the mitotic spindle and midbody and LIC2 localizes to spindle poles during cell division Cell. Biol. Int. 35 2011 171 178
49. C.P. Horgan, S.R. Hanscom, E.E. Kelly, and M.W. McCaffrey Tumor susceptibility gene 101 (TSG101) is a novel binding-partner for the class II Rab11-FIPs PLoS One 7 2012 e32030
50. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674 (Pubitemid 47080256)
51. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D: Biol. Crystallogr. 66 2010 486 501
52. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, A. McCoy, S.J. McNicholas, G.N. Murshudov, N.S. Pannu, E.A. Potterton, H.R. Powell, R.J. Read, A. Vagin, and K.S. Wilson Overview of the CCP4 suite and current developments Acta Crystallogr. D: Biol. Crystallogr. 67 2011 235 242
53. C.M. Hales, R. Griner, K.C. Hobdy-Henderson, M.C. Dorn, D. Hardy, R. Kumar, J. Navarre, E.K. Chan, L.A. Lapierre, and J.R. Goldenring Identification and characterization of a family of Rab11-interacting proteins J. Biol. Chem. 276 2001 39067 39075
54. A. Echard, F. Jollivet, O. Martinez, J.J. Lacapere, A. Rousselet, I. Janoueix-Lerosey, and B. Goud Interaction of a Golgi-associated kinesin-like protein with Rab6 Science 279 1998 580 585 (Pubitemid 28067290)
55. A.R. Moorhead, K.A. Rzomp, and M.A. Scidmore The Rab6 effector bicaudal D1 associates with Chlamydia trachomatis inclusions in a biovar-specific manner Infect. Immun. 75 2007 781 791 (Pubitemid 46203441)
56. A. Ignatev, S. Kravchenko, A. Rak, R.S. Goody, and O. Pylypenko A structural model of the GDP dissociation inhibitor rab membrane extraction mechanism J. Biol. Chem. 283 2008 18377 18384
57. X. Wu, M.J. Bradley, Y. Cai, D. Kummel, E.M. De La Cruz, F.A. Barr, and K.M. Reinisch Insights regarding guanine nucleotide exchange from the structure of a DENN-domain protein complexed with its Rab GTPase substrate Proc. Natl. Acad. Sci. U. S. A. 108 2011 18672 18677
58. J. Jing, J.R. Junutula, C. Wu, J. Burden, H. Matern, A.A. Peden, and R. Prekeris FIP1/RCP binding to Golgin-97 regulates retrograde transport from recycling endosomes to the trans-Golgi network Mol. Biol. Cell 21 2010 3041 3053
59. A.R. Khan Oligomerization of rab/effector complexes in the regulation of vesicle trafficking Prog. Mol. Biol. Transl. Sci. 117 2013 579 614
60. Z. Wang, J.G. Edwards, N. Riley, D.W. Provance Jr., R. Karcher, X.D. Li, I.G. Davison, M. Ikebe, J.A. Mercer, J.A. Kauer, and M.D. Ehlers Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity Cell 135 2008 535 548
61. C.P. Horgan, and M.W. McCaffrey Endosomal trafficking in animal cytokinesis Front. Biosci. (Schol. Ed.) 4 2012 547 555
62. C.P. Horgan, T.H. Zurawski, and M.W. McCaffrey Purification and functional properties of Rab11-FIP3 Methods Enzymol. 403 2005 499 512 (Pubitemid 43216935)
63. C.P. Horgan, M. Walsh, T.H. Zurawski, and M.W. McCaffrey Rab11-FIP3 localises to a Rab11-positive pericentrosomal compartment during interphase and to the cleavage furrow during cytokinesis Biochem. Biophys. Res. Commun. 319 2004 83 94 (Pubitemid 38670165)
64. S.G. Addinall, P.S. Mayr, S. Doyle, J.K. Sheehan, P.G. Woodman, and V.J. Allan Phosphorylation by cdc2-CyclinB1 kinase releases cytoplasmic dynein from membranes J. Biol. Chem. 276 2001 15939 15944
65. M. Chiariello, C.B. Bruni, and C. Bucci The small GTPases Rab5a, Rab5b and Rab5c are differentially phosphorylated in vitro FEBS Lett. 453 1999 20 24 (Pubitemid 29335465)
66. J. Ding, G. Soule, J.H. Overmeyer, and W.A. Maltese Tyrosine phosphorylation of the Rab24 GTPase in cultured mammalian cells Biochem. Biophys. Res. Commun. 312 2003 670 675 (Pubitemid 37468223)
67. E. Bailly, M. McCaffrey, N. Touchot, A. Zahraoui, B. Goud, and M. Bornens Phosphorylation of two small GTP-binding proteins of the Rab family by p34cdc2 Nature 350 1991 715 718 (Pubitemid 21912305)
68. A. Karniguian, A. Zahraoui, and A. Tavitian Identification of small GTP-binding rab proteins in human platelets: thrombin-induced phosphorylation of rab3B, rab6, and rab8 proteins Proc. Natl. Acad. Sci. U. S. A. 90 1993 7647 7651 (Pubitemid 23250007)
69. P. van der Sluijs, M. Hull, L.A. Huber, P. Male, B. Goud, and I. Mellman Reversible phosphorylation-dephosphorylation determines the localization of rab4 during the cell cycle EMBO J. 11 1992 4379 4389
70. N.A. Ducharme, C.M. Hales, L.A. Lapierre, A.J. Ham, A. Oztan, G. Apodaca, and J.R. Goldenring MARK2/EMK1/Par-1Balpha phosphorylation of Rab11-family interacting protein 2 is necessary for the timely establishment of polarity in Madin-Darby canine kidney cells Mol. Biol. Cell 17 2006 3625 3637 (Pubitemid 44156454)
71. L.A. Lapierre, K.M. Avant, C.M. Caldwell, A. Oztan, G. Apodaca, B.C. Knowles, J.T. Roland, N.A. Ducharme, and J.R. Goldenring Phosphorylation of Rab11-FIP2 regulates polarity in MDCK cells Mol. Biol. Cell 23 2012 2302 2318
72. L.L. Collins, G. Simon, J. Matheson, C. Wu, M.C. Miller, T. Otani, X. Yu, S. Hayashi, R. Prekeris, and G.W. Gould Rab11-FIP3 is a cell cycle-regulated phosphoprotein BMC Cell Biol. 13 2012 4
73. E. Mizuno-Yamasaki, F. Rivera-Molina, and P. Novick GTPase networks in membrane traffic Annu. Rev. Biochem. 81 2012 637 659
74. J.T. Dabbeekeh, S.L. Faitar, C.P. Dufresne, and J.K. Cowell The EVI5 TBC domain provides the GTPase-activating protein motif for RAB11 Oncogene 26 2007 2804 2808 (Pubitemid 46663836)
75. C. Laflamme, G. Assaker, D. Ramel, J.F. Dorn, D. She, P.S. Maddox, and G. Emery Evi5 promotes collective cell migration through its Rab-GAP activity J. Cell Biol. 198 2012 57 67
76. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797 (Pubitemid 47321791)
77. A.G.W. Leslie Integration of macromolecular diffraction data Acta Cryst. D55 1999 1696 1702 (Pubitemid 29504424)
78. P.R. Evans Scaling and assessment of data quality Acta Cryst. D62 2006 72 82
79. B.W. Matthews, Solvent content of protein crystals, J. Mol. Biol. 33 (1968) 491-497.