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Structure of Rab11-FIP3-Rabin8 reveals simultaneous binding of FIP3 and Rabin8 effectors to Rab11.

Vetter M, Stehle R, Basquin C, Lorentzen E
Nat Struct Mol Biol 22 695-702 (2015)
Related entries: 4uj3, 4uj5

Cited: 33 times
EuropePMC logo PMID: 26258637

Abstract

The small GTPase Rab11 and its effectors FIP3 and Rabin8 are essential to membrane-trafficking pathways required for cytokinesis and ciliogenesis. Although effector binding is generally assumed to be sequential and mutually exclusive, we show that Rab11 can simultaneously bind FIP3 and Rabin8. We determined crystal structures of human Rab11-GMPPNP-Rabin8 and Rab11-GMPPNP-FIP3-Rabin8. The structures reveal that the C-terminal domain of Rabin8 adopts a previously undescribed fold that interacts with Rab11 at an unusual effector-binding site neighboring the canonical FIP3-binding site. We show that Rab11-GMPPNP-FIP3-Rabin8 is more stable than Rab11-GMPPNP-Rabin8, owing to direct interaction between Rabin8 and FIP3 within the dual effector-bound complex. The data allow us to propose a model for how membrane-targeting complexes assemble at the trans-Golgi network and recycling endosomes, through multiple weak interactions that create high-avidity complexes.

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  1. The substrate specificity of the human TRAPPII complex's Rab-guanine nucleotide exchange factor activity. Jenkins ML, Harris NJ, Dalwadi U, Fleming KD, Ziemianowicz DS, Rafiei A, Martin EM, Schriemer DC, Yip CK, Burke JE. Commun Biol 3 735 (2020)


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  1. Rab GTPases and their interacting protein partners: Structural insights into Rab functional diversity. Pylypenko O, Hammich H, Yu IM, Houdusse A. Small GTPases 9 22-48 (2018)
  2. The intraflagellar transport machinery in ciliary signaling. Mourão A, Christensen ST, Lorentzen E. Curr Opin Struct Biol 41 98-108 (2016)
  3. ARF family GTPases with links to cilia. Fisher S, Kuna D, Caspary T, Kahn RA, Sztul E. Am J Physiol Cell Physiol 319 C404-C418 (2020)
  4. Regulation of ciliary membrane protein trafficking and signalling by kinesin motor proteins. Morthorst SK, Christensen ST, Pedersen LB. FEBS J 285 4535-4564 (2018)
  5. Novel topography of the Rab11-effector interaction network within a ciliary membrane targeting complex. Vetter M, Wang J, Lorentzen E, Deretic D. Small GTPases 6 165-173 (2015)
  6. Ciliogenesis membrane dynamics and organization. Zhao H, Khan Z, Westlake CJ. Semin Cell Dev Biol 133 20-31 (2023)
  7. Dynamic structural biology at the protein membrane interface. Burke JE. J Biol Chem 294 3872-3880 (2019)

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  1. Rabin8 regulates neurite outgrowth in both GEF activity-dependent and -independent manners. Homma Y, Fukuda M. Mol Biol Cell 27 2107-2118 (2016)
  2. The G2019S variant of leucine-rich repeat kinase 2 (LRRK2) alters endolysosomal trafficking by impairing the function of the GTPase RAB8A. Rivero-Ríos P, Romo-Lozano M, Madero-Pérez J, Thomas AP, Biosa A, Greggio E, Hilfiker S. J Biol Chem 294 4738-4758 (2019)
  3. Akt Regulates a Rab11-Effector Switch Required for Ciliogenesis. Walia V, Cuenca A, Vetter M, Insinna C, Perera S, Lu Q, Ritt DA, Semler E, Specht S, Stauffer J, Morrison DK, Lorentzen E, Westlake CJ. Dev Cell 50 229-246.e7 (2019)
  4. SCD1 and SCD2 Form a Complex That Functions with the Exocyst and RabE1 in Exocytosis and Cytokinesis. Mayers JR, Hu T, Wang C, Cárdenas JJ, Tan Y, Pan J, Bednarek SY. Plant Cell 29 2610-2625 (2017)
  5. Multivalent Rab interactions determine tether-mediated membrane fusion. Lürick A, Gao J, Kuhlee A, Yavavli E, Langemeyer L, Perz A, Raunser S, Ungermann C. Mol Biol Cell 28 322-332 (2017)
  6. Transport of fungal RAB11 secretory vesicles involves myosin-5, dynein/dynactin/p25, and kinesin-1 and is independent of kinesin-3. Peñalva MA, Zhang J, Xiang X, Pantazopoulou A. Mol Biol Cell 28 947-961 (2017)
  7. Rab22A recruits BLOC-1 and BLOC-2 to promote the biogenesis of recycling endosomes. Shakya S, Sharma P, Bhatt AM, Jani RA, Delevoye C, Setty SR. EMBO Rep 19 e45918 (2018)
  8. Using hydrogen deuterium exchange mass spectrometry to engineer optimized constructs for crystallization of protein complexes: Case study of PI4KIIIβ with Rab11. Fowler ML, McPhail JA, Jenkins ML, Masson GR, Rutaganira FU, Shokat KM, Williams RL, Burke JE. Protein Sci 25 826-839 (2016)
  9. Sequential recruitment of Rab GTPases during early stages of phagocytosis. Yeo JC, Wall AA, Luo L, Stow JL. Cell Logist 6 e1140615 (2016)
  10. Structural determinants of Rab11 activation by the guanine nucleotide exchange factor SH3BP5. Jenkins ML, Margaria JP, Stariha JTB, Hoffmann RM, McPhail JA, Hamelin DJ, Boulanger MJ, Hirsch E, Burke JE. Nat Commun 9 3772 (2018)
  11. A non-canonical GTPase interaction enables ORP1L-Rab7-RILP complex formation and late endosome positioning. Ma X, Liu K, Li J, Li H, Li J, Liu Y, Yang C, Liang H. J Biol Chem 293 14155-14164 (2018)
  12. Rab32 interacts with SNX6 and affects retromer-dependent Golgi trafficking. Waschbüsch D, Hübel N, Ossendorf E, Lobbestael E, Baekelandt V, Lindsay AJ, McCaffrey MW, Khan AR, Barnekow A. PLoS One 14 e0208889 (2019)
  13. The Arf GEF GBF1 and Arf4 synergize with the sensory receptor cargo, rhodopsin, to regulate ciliary membrane trafficking. Wang J, Fresquez T, Kandachar V, Deretic D. J Cell Sci 130 3975-3987 (2017)
  14. An interaction network between the SNARE VAMP7 and Rab GTPases within a ciliary membrane-targeting complex. Kandachar V, Tam BM, Moritz OL, Deretic D. J Cell Sci 131 jcs222034 (2018)
  15. The ins and outs of the Arf4-based ciliary membrane-targeting complex. Deretic D, Lorentzen E, Fresquez T. Small GTPases 12 1-12 (2021)
  16. Allosteric binding sites in Rab11 for potential drug candidates. Kumar AP, Lukman S. PLoS One 13 e0198632 (2018)
  17. Conformational control of small GTPases by AMPylation. Barthelmes K, Ramcke E, Kang HS, Sattler M, Itzen A. Proc Natl Acad Sci U S A 117 5772-5781 (2020)
  18. Eps15 homology domain 1 promotes the evolution of papillary thyroid cancer by regulating endocytotic recycling of epidermal growth factor receptor. Liu Y, Liang Y, Li M, Liu D, Tang J, Yang W, Tong D, Jin X. Oncol Lett 16 4263-4270 (2018)
  19. Purification and crystal structure of human ODA16: Implications for ciliary import of outer dynein arms by the intraflagellar transport machinery. Wang J, Taschner M, Petriman NA, Andersen MB, Basquin J, Bhogaraju S, Vetter M, Wachter S, Lorentzen A, Lorentzen E. Protein Sci 29 1502-1510 (2020)
  20. Crystal structure of tetrameric human Rabin8 GEF domain. Vetter M, Boegholm N, Christensen A, Bhogaraju S, Andersen MB, Lorentzen A, Lorentzen E. Proteins 86 405-413 (2018)
  21. The type V myosin-containing complex HUM is a RAB11 effector powering movement of secretory vesicles. Pinar M, Alonso A, de Los Ríos V, Bravo-Plaza I, de la Gandara Á, Galindo A, Arias-Palomo E, Peñalva MÁ. iScience 25 104514 (2022)
  22. Molecular basis for the recruitment of the Rab effector protein WDR44 by the GTPase Rab11. Thibodeau MC, Harris NJ, Jenkins ML, Parson MAH, Evans JT, Scott MK, Shaw AL, Pokorný D, Leonard TA, Burke JE. J Biol Chem 299 102764 (2023)
  23. Regulation of podocalyxin trafficking by Rab small GTPases in epithelial cells. Mrozowska PS, Fukuda M. Small GTPases 7 231-238 (2016)
  24. Crystal structure of Arabidopsis thaliana RabA1a. Yun JS, Ha SC, Kim S, Kim YG, Kim H, Chang JH. J Integr Plant Biol 61 93-109 (2019)
  25. The IFT81-IFT74 complex acts as an unconventional RabL2 GTPase-activating protein during intraflagellar transport. Boegholm N, Petriman NA, Loureiro-López M, Wang J, Vela MIS, Liu B, Kanie T, Ng R, Jackson PK, Andersen JS, Lorentzen E. EMBO J 42 e111807 (2023)


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