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Original Article

Rab1a and Rab5a preferentially bind to binary lipid compositions with higher stored curvature elastic energy

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Pages 303-314 | Received 22 May 2013, Accepted 17 Jun 2013, Published online: 02 Jul 2013

References

  • Aivazian D, Serrano RL, Pfeffer S. 2006. TIP47 is a key effector for Rab9 localization. J Cell Biol 173:917–926.
  • Akavia UD, Litvin O, Kim J, Sanchez-Garcia F, Kotliar D, Causton HC, et al. 2010. An integrated approach to uncover drivers of cancer. Cell 143:1005–1017.
  • Alexandrov K, Simon I, Iakovenko A, Holz B, Goody RS, Scheidig AJ. 1998. Moderate discrimination of REP-1 between Rab7 × GDP and Rab7 × GTP arises from a difference of an order of magnitude in dissociation rates. FEBS Lett 425:460–464.
  • Ali BR, Wasmeier C, Lamoreux L, Strom M, Seabra MC. 2004. Multiple regions contribute to membrane targeting of Rab GTPases. J Cell Sci 117:6401–6412.
  • Attard GS, Smith WS, Templer RH, Hunt AN, Jackowski S. 1998. Modulation of CTP:phosphocholine cytidylyltransferase by membrane torque tension. Biochem Soc Trans 26:S230.
  • Attard GS, Templer RH, Smith WS, Hunt AN, Jackowski S. 2000. Modulation of CTP:phosphocholine cytidylyltransferase by membrane curvature elastic stress. PNAS 97:9032–9036.
  • Barral DC, Ramalho JS, Anders R, Hume AN, Knapton HJ, Tolmachova T, et al. 2002. Functional redundancy of Rab27 proteins and the pathogenesis of Griscelli syndrome. J Clin Invest 110:247–257.
  • Beck R, Sun Z, Adolf F, Rutz C, Bassler J, Wild K, et al. 2008. Membrane curvature induced by Arf1-GTP is essential for vesicle formation. PNAS 105:11731–11736.
  • 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.
  • Booth PJ. 2000. Unravelling the folding of bacteriorhodopsin. Biochim Biophys Acta 1460:4–14.
  • Booth PJ, Clarke J. 2010. Membrane protein folding makes the transition. PNAS 107:3947–3948.
  • Catz SD, Johnson JL, Babior BM. 2002. The C2A domain of JFC1 binds to 3′-phosphorylated phosphoinositides and directs plasma membrane association in living cells. PNAS 99:11652–11657.
  • Charalambous K, Miller D, Curnow P, Booth PJ. 2008. Lipid bilayer composition influences small multidrug transporters. BMC Biochem 9:31.
  • Chernomordik LV, Kozlov MM. 2003. Protein-lipid interplay in fusion and fission of biological membranes. Annu Rev Biochem 72:175–207.
  • Costigan SC, Booth PJ, Templer RH. 2000. Estimations of lipid bilayer geometry in fluid lamellar phases. Biochim Biophys Acta 1468:41–54.
  • Curnow P, Lorch M, Charalambous K, Booth PJ. 2004. The reconstitution and activity of the small multidrug transporter EmrE is modulated by non-bilayer lipid composition. J Mol Biol 343:213–222.
  • Dirac-Svejstrup AB, Sumizawa T, Pfeffer SR. 1997. Identification of a GDI displacement factor that releases endosomal Rab GTPases from Rab-GDI. Embo J 16:465–472.
  • Ganley IG, Pfeffer SR. 2006. Cholesterol accumulation sequesters Rab9 and disrupts late endosome function in NPC1-deficient cells. J Biol Chem 281:17890–17899.
  • Hendrix A, Maynard D, Pauwels P, Braems G, Denys H, Van den Broecke R, et al. 2010. Effect of the secretory small GTPase Rab27B on breast cancer growth, invasion, and metastasis. J Natl Cancer Inst 102:866–880.
  • Hong H, Tamm LK. 2004. Elastic coupling of integral membrane protein stability to lipid bilayer forces. PNAS 101:4065–4070.
  • Horiuchi H, Ullrich O, Bucci C, Zerial M. 1995. Purification of posttranslationally modified and unmodified Rab5 protein expressed in Spodoptera frugiperda cells. Meth Enzymol 257:9–15.
  • Hutagalung AH, Novick PJ. 2011. Role of rab GTPases in membrane traffic and cell physiology. Physiol Rev 91:119–149.
  • Jancic C, Savina A, Wasmeier C, Tolmachova T, El-Benna J, Dang PM-C, et al. 2007. Rab27a regulates phagosomal pH and NADPH oxidase recruitment to dendritic cell phagosomes. Nat Cell Biol 9:367–378.
  • Johnson JL, Brzezinska AA, Tolmachova T, Munafo DB, Ellis BA, Seabra MC, et al. 2010. Rab27a and Rab27b regulate neutrophil azurophilic granule exocytosis and NADPH oxidase activity by independent mechanisms. Traffic 11:533–547.
  • Kozlov MM, Leikin S, Rand RP. 1994. Bending, hydration and interstitial energies quantitatively account for the hexagonal-lamellar-hexagonal reentrant phase transition in dioleoylphosphatidylethanolamine. Biophys J 67:1603–1611.
  • Lee MCS, Orci L, Hamamoto S, Futai E, Ravazzola M, Schekman R. 2005. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122:605–617.
  • Lewis JR, Cafiso DS. 1999. Correlation between the free energy of a channel-forming voltage-gated peptide and the spontaneous curvature of bilayer lipids. Biochemistry 38:5932–5938.
  • Lipinski AR, Heymann J, Meissner C, Karlas A, Brinkmann V, Meyer TF, et al. 2009. Rab6 and Rab11 regulate chlamydia trachomatis development and Golgin-84-dependent Golgi fragmentation. PLoS Pathogens 5:12.
  • Lipowsky R. 1991. The conformation of membranes. Nature 349:475–481.
  • Lombardi D, Soldati T, Riederer MA, Goda Y, Zerial M, Pfeffer SR. 1993. Rab9 functions in transport between late endosomes and the trans Golgi network. Embo J 12:677–682.
  • Machner MP, Isberg RR. 2007. A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318:974–977.
  • Marsh D. 2006. Elastic curvature constants of lipid monolayers and bilayers. Chem Phys Lipids 144:146–159.
  • McAdara Berkowitz JK, Catz SD, Johnson JL, Ruedi JM, Thon V, Babior BM. 2001. JFC1, a novel tandem C2 domain-containing protein associated with the leukocyte NADPH oxidase. J Biol Chem 276:18855–18862.
  • Miller D, Charalambous K, Rotem D, Schuldiner S, Curnow P, Booth PJ. 2009. In vitro unfolding and refolding of the small multidrug transporter EmrE. J Mol Biol 393:815–832.
  • Mizuno K, Tolmachova T, Ushakov DS, Romao M, Abrink M, Ferenczi MA, et al. 2007. Rab27b regulates mast cell granule dynamics and secretion. Traffic 8:883–892.
  • Nagy JK, Lonzer WL, Sanders CR. 2001. Kinetic study of folding and misfolding of diacylglycerol kinase in model membranes. Biochemistry 40:8971–8980.
  • Nishimura N, Nakamura H, Takais Y. 1994. Molecular cloning and characterization of two rab GDI species from rat brain: Brain- specific and ubiquitous types. Biochemistry 269:14191–14198.
  • Pereira-Leal JB, Seabra MC. 2000. 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 301:1077–1087.
  • Pereira-Leal JB, Seabra MC. 2001. Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 313:889–901.
  • Pfeffer S. 2005. A model for Rab GTPase localization. Biochem Soc Trans 33:627–630.
  • Pfeffer S, Aivazian D. 2004. Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol 5:886–896.
  • Seabra MC, Brown MS, Goldstein JL. 1993. Retinal degeneration in choroideremia: Deficiency of rab geranylgeranyl transferase. Science 259:377–381.
  • Seabra MC, Wasmeier C. 2004. Controlling the location and activation of Rab GTPases. Curr Opin Cell Biol 16:451–457.
  • Seddon AM, Lorch M, Ces O, Templer RH, Macrae F, Booth PJ. 2008. Phosphatidylglycerol lipids enhance folding of an alpha helical membrane protein. J Mol Biol 380:548–556.
  • Shapiro AD, Pfeffer SR. 1995. Quantitative analysis of the interactions between prenyl Rab9, GDP dissociation inhibitor-alpha, and guanine nucleotides. J Biol Chem 270:11085–11090.
  • Shearman GC, Ces O, Templer RH, Seddon JM. 2006. Inverse lyotropic phases of lipids and membrane curvature. J Phys Condens Matt 18:S1105–S1124.
  • Sivars U, Aivazian D, Pfeffer SR. 2003. Yip3 catalyses the dissociation of endosomal Rab-GDI complexes. Nature 425:856–859.
  • Soldati T, Shapiro AD, Svejstrup AB, Pfeffer SR. 1994. Membrane targeting of the small GTPase Rab9 is accompanied by nucleotide exchange. Nature 369:76–78.
  • Strom M, Hume AN, Tarafder AK, Barkagianni E, Seabra MC. 2002. A family of Rab27-binding proteins. Melanophilin links Rab27a and myosin Va function in melanosome transport. J Biol Chem 277:25423–25430.
  • Tarafder AK, Wasmeier C, Figueiredo AC, Booth AEG, Orihara A, Ramalho JS, et al. 2011. Rab27a targeting to melanosomes requires nucleotide exchange but not effector binding. Traffic 12:1056–1066.
  • Templer RH, Castle SJ, Curran AR, Rumbles G, Klug DR. 1998. Sensing isothermal changes in the lateral pressure in model membranes using di-pyrenyl phosphatidylcholine. Faraday Discuss 41–78.
  • Tortorella D, Ulbrandt ND, London E. 1993. Simple centrifugation method for efficient pelleting of both small and large unilamellar vesicles that allows convenient measurement of protein binding. Biochemistry 32:9181–9188.
  • Ullrich O, Horiuchi H, Bucci C, Zerial M. 1994. Membrane association of Rab5 mediated by GDP-dissociation inhibitor and accompanied by GDP/GTP exchange. Nature 368: 157–160.
  • Ullrich O, Stenmark H, Alexandrov K, Huber LA, Kaibuchi K, Sasaki T, et al. 1993. Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins. J Biol Chem 268:18143–18150.
  • Winterhalter M, Helfrich W. 1988. Effect of surface charge on the curvature elasticity of membranes. J Phys Chem 92:6865–6867.
  • Wu Y-W, Oesterlin LK, Tan K-T, Waldmann H, Alexandrov K, Goody RS. 2010. Membrane targeting mechanism of Rab GTPases elucidated by semisynthetic protein probes. Nat Chem Biol 6:689.
  • Wu Y-W, Tan K-T, Waldmann H, Goody RS, Alexandrov K. 2007. Interaction analysis of prenylated Rab GTPase with Rab escort protein and GDP dissociation inhibitor explains the need for both regulators. PNAS 104:12294–12299.
  • Yokoyama K, Kaji H, He J, Tanaka C, Hazama R, Kamigaki T, et al. 2011. Rab27a negatively regulates phagocytosis by prolongation of the actin-coating stage around phagosomes. J Biol Chem 286:5375–5382.
  • Zerial M, McBride H. 2001. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107–117.

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