Diversity and plasticity in Rab GTPase nucleotide release mechanism has consequences for Rab activation and inactivation

eLife

Volumn 2014, Issue 3, 2014, Pages

  Langemeyer, Lars ^a   Bastos, Ricardo Nunes ^a   Cai, Yiying ^b   Itzen, Aymelt ^c   Reinisch, Karin M ^b   Barr, Francis A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; GLUTAMINE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; NUCLEOTIDE; RAB PROTEIN; SHIGA TOXIN;

ARTICLE; CONTROLLED STUDY; FLUORESCENCE IMAGING; FRACTIONATION; HUMAN; HUMAN CELL; HYDROLYSIS; MUTANT; MUTATION; PLASTICITY; PROTEIN PURIFICATION;

EID: 84898756626     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01623.001     Document Type: Article

References (40)

1. Ahmadian MR, Stege P, Scheffzek K, Wittinghofer A. 1997. Confirmation of the arginine-finger hypothesis for the GAP-stimulated GTP-hydrolysis reaction of Ras. Nature Structural Biology 4:686-689. doi: 10.1038/nsb0997-686.
2. Barr F, Lambright DG. 2010. Rab GEFs and GAPs. Current Opinion Cell Biology 22:461-470. doi: 10.1016/j.ceb.2010.04.007.
3. Barr FA. 2013. Rab GTPases and membrane identity: causal or inconsequential? The Journal of Cell Biology 202:191-199. doi: 10.1083/jcb.201306010.
4. Boriack-Sjodin PA, Margarit SM, Bar-Sagi D, Kuriyan J. 1998. The structural basis of the activation of Ras by Sos. Nature 394:337-343. doi: 10.1038/28548.
5. Bos JL, Rehmann H, Wittinghofer A. 2007. GEFs and GAPs: critical elements in the control of small G proteins. Cell 129:865-877. doi: 10.1016/j.cell.2007.05.018.
6. Cai Y, Chin HF, Lazarova D, Menon S, Fu C, Cai H, Sclafani A, Rodgers DW, De La Cruz EM, Ferro-Novick S, Reinisch KM. 2008. The structural basis for activation of the Rab Ypt1p by the TRAPP membrane-tethering complexes. Cell 133:1202-1213. doi: 10.1016/j.cell.2008.04.049.
7. Chin HF, Cai Y, Menon S, Ferro-Novick S, Reinisch KM, De La Cruz EM. 2009. Kinetic analysis of the guanine nucleotide exchange activity of TRAPP, a multimeric Ypt1p exchange factor. Journal of Molecular Biology 389:275-288. doi: 10.1016/j.jmb.2009.03.068.
8. Clark BS, Winter M, Cohen AR, Link BA. 2011. Generation of Rab-based transgenic lines for in vivo studies of endosome biology in zebrafish. Developmental Dynamics 240:2452-2465. doi: 10.1002/dvdy.22758.
9. Dambournet D, Machicoane M, Chesneau L, Sachse M, Rocancourt M, El Marjou A, Formstecher E, Salomon R, Goud B, Echard A. 2011. Rab35 GTPase and OCRL phosphatase remodel lipids and F-actin for successful cytokinesis. Nature Cell Biology 13:981-988. doi: 10.1038/ncb2279.
10. De Antoni A, Schmitzova J, Trepte HH, Gallwitz D, Albert S. 2002. Significance of GTP hydrolysis in Ypt1p-regulated endoplasmic reticulum to Golgi transport revealed by the analysis of two novel Ypt1-GAPs. The Journal of Biological Chemistry 277:41023-41031. doi: 10.1074/jbc.M205783200.
11. Del Conte-Zerial P, Brusch L, Rink JC, Collinet C, Kalaidzidis Y, Zerial M, Deutsch A. 2008. Membrane identity and GTPase cascades regulated by toggle and cut-out switches. Molecular Systems Biology 4:206. doi: 10.1038/msb.2008.45.
12. Delprato A, Lambright DG. 2007. Structural basis for Rab GTPase activation by VPS9 domain exchange factors. Nature Structural & Molecular Biology 14:406-412. doi: 10.1038/nsmb1232.
13. Delprato A, Merithew E, Lambright DG. 2004. Structure, exchange determinants, and family-wide rab specificity of the tandem helical bundle and Vps9 domains of Rabex-5. Cell 118:607-617. doi: 10.1016/j.cell.2004.08.009.
14. Fuchs E, Haas AK, Spooner RA, Yoshimura S, Lord JM, Barr FA. 2007. Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways. The Journal of Cell Biology 177:1133-1143. doi: 10.1083/jcb.200612068.
15. Gallegos ME, Balakrishnan S, Chandramouli P, Arora S, Azameera A, Babushekar A, Bargoma E, Bokhari A, Chava SK, Das P, Desai M, Decena D, Saramma SD, Dey B, Doss AL, Gor N, Gudiputi L, Guo C, Hande S, Jensen M, Jones S, Jones N, Jorgens D, Karamchedu P, Kamrani K, Kolora LD, Kristensen L, Kwan K, Lau H, Maharaj P, Mander N, Mangipudi K, Menakuru H, Mody V, Mohanty S, Mukkamala S, Mundra SA, Nagaraju S, Narayanaswamy R, Ndungu-Case C, Noorbakhsh M, Patel J, Patel P, Pendem SV, Ponakala A, Rath M, Robles MC, Rokkam D, Roth C, Sasidharan P, Shah S, Tandon S, Suprai J, Truong TQ, Uthayaruban R, Varma A, Ved U, Wang Z, Yu Z. 2012. The C. elegans rab family: identification, classification and toolkit construction. PLOS ONE 7:e49387. doi: 10.1371/journal.pone.0049387.
16. Gasper R, Thomas C, Ahmadian MR, Wittinghofer A. 2008. The role of the conserved switch II glutamate in guanine nucleotide exchange factor-mediated nucleotide exchange of GTP-binding proteins. Journal of Molecular Biology 379:51-63. doi: 10.1016/j.jmb.2008.03.011.
17. Gavriljuk K, Gazdag EM, Itzen A, Kotting C, Goody RS, Gerwert K. 2012. Catalytic mechanism of a mammalian Rab. RabGAP complex in atomic detail. Proceedings of the National Academy of Sciences of the United States of America 109:21348-21353. doi: 10.1073/pnas.1214431110.
18. Haas AK, Fuchs E, Kopajtich R, Barr FA. 2005. A GTPase-activating protein controls Rab5 function in endocytic trafficking. Nature Cell Biology 7:887-893. doi: 10.1038/ncb1290.
19. Haas AK, Yoshimura S, Stephens DJ, Preisinger C, Fuchs E, Barr FA. 2007. Analysis of GTPase-activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells. Journal of Cell Science 120:2997-3010. doi: 10.1242/jcs.014225.
20. Ishida M, Ohbayashi N, Maruta Y, Ebata Y, Fukuda M. 2012. Functional involvement of Rab1A in microtubule-dependent anterograde melanosome transport in melanocytes. Journal of Cell Science 125:5177-5187. doi: 10.1242/jcs.109314.
21. John J, Rensland H, Schlichting I, Vetter I, Borasio GD, Goody RS, Wittinghofer A. 1993. Kinetic and structural analysis of the Mg(2+)-binding site of the guanine nucleotide-binding protein p21H-ras. The Journal of Biological Chemistry 268:923-929.
22. Klopper TH, Kienle N, Fasshauer D, Munro S. 2012. Untangling the evolution of Rab G proteins: implications of a comprehensive genomic analysis. BMC Biology 10:71. doi: 10.1186/1741-7007-10-71.
23. Nottingham RM, Ganley IG, Barr FA, Lambright DG, Pfeffer SR. 2011. RUTBC1 protein, a Rab9A effector that activates GTP hydrolysis by Rab32 and Rab33B proteins. The Journal of Biological Chemistry 286:33213-33222. doi: 10.1074/jbc.M111.261115.
24. Pai EF, Kabsch W, Krengel U, Holmes KC, John J, Wittinghofer A. 1989. Structure of the guanine-nucleotide-binding domain of the Ha-ras oncogene product p21 in the triphosphate conformation. Nature 341:209-214. doi: 10.1038/341209a0.
25. Palamidessi A, Frittoli E, Ducano N, Offenhauser N, Sigismund S, Kajiho H, Parazzoli D, Oldani A, Gobbi M, Serini G, Di Fiore PP, Scita G, Lanzetti L. 2013. The GTPase-activating protein RN-tre controls focal adhesion turnover and cell migration. Current biology: CB 23:2355-2364. doi: 10.1016/j.cub.2013.09.060.
26. Pan X, Eathiraj S, Munson M, Lambright DG. 2006. TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism. Nature 442:303-306. doi: 10.1038/nature04847.
27. Pfeffer S, Aivazian D. 2004. Targeting Rab GTPases to distinct membrane compartments. Nature Reviews Molecular Cell Biology 5:886-896. doi: 10.1038/nrm1500.
28. Richardson CJ, Jones S, Litt RJ, Segev N. 1998. GTP hydrolysis is not important for Ypt1 GTPase function in vesicular transport. Molecular and Cellular Biology 18:827-838.
29. Rojas AM, Fuentes G, Rausell A, Valencia A. 2012. The Ras protein superfamily: evolutionary tree and role of conserved amino acids. The Journal of Cell Biology 196:189-201. doi: 10.1083/jcb.201103008.
30. Rybin V, Ullrich O, Rubino M, Alexandrov K, Simon I, Seabra MC, Goody R, Zerial M. 1996. GTPase activity of Rab5 acts as a timer for endocytic membrane fusion. Nature 383:266-269. doi: 10.1038/383266a0.
31. Scheffzek K, Ahmadian MR, Kabsch W, Wiesmuller L, Lautwein A, Schmitz F, Wittinghofer A. 1997. The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277:333-338. doi: 10.1126/science.277.5324.333.
32. Schoebel S, Oesterlin LK, Blankenfeldt W, Goody RS, Itzen A. 2009. RabGDI displacement by DrrA from Legionella is a consequence of its guanine nucleotide exchange activity. Molecular Cell 36:1060-1072. doi: 10.1016/j.molcel.2009.11.014.
33. Stenmark H, Parton RG, Steele-Mortimer O, Lutcke A, Gruenberg J, Zerial M. 1994. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. The EMBO Journal 13:1287-1296.
34. Suh HY, Lee DW, Lee KH, Ku B, Choi SJ, Woo JS, Kim YG, Oh BH. 2010. Structural insights into the dual nucleotide exchange and GDI displacement activity of SidM/DrrA. The EMBO Journal 29:496-504. doi: 10.1038/emboj.2009.347.
35. Thomas C, Fricke I, Scrima A, Berken A, Wittinghofer A. 2007. Structural evidence for a common intermediate in small G protein-GEF reactions. Molecular Cell 25:141-149. doi: 10.1016/j.molcel.2006.11.023.
36. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. The Journal of Cell Biology 135:913-924. doi: 10.1083/jcb.135.4.913.
37. Wu X, Bradley MJ, Cai Y, Kummel D, De La Cruz EM, Barr FA, Reinisch KM. 2011. Insights regarding guanine nucleotide exchange from the structure of a DENN-domain protein complexed with its Rab GTPase substrate. Proceedings of the National Academy of Sciences of the United States of America 108:18672-18677. doi: 10.1073/pnas.1110415108.
38. Xiong B, Bayat V, Jaiswal M, Zhang K, Sandoval H, Charng WL, Li T, David G, Duraine L, Lin YQ, Neely GG, Yamamoto S, Bellen HJ. 2012. Crag is a GEF for Rab11 required for rhodopsin trafficking and maintenance of adult photoreceptor cells. PLOS Biology 10:e1001438. doi: 10.1371/journal.pbio.1001438.
39. Yoshimura S, Gerondopoulos A, Linford A, Rigden DJ, Barr FA. 2010. Family-wide characterization of the DENN domain Rab GDP-GTP exchange factors. The Journal of Cell Biology 191:367-381. doi: 10.1083/jcb.201008051.
40. Zerial M, McBride H. 2001. Rab proteins as membrane organizers. Nature Reviews Molecular Cell Biology 2:107-117. doi: 10.1038/35052055.