Advertisement

Rab Proteins and the Organization of Organelle Membrane Domains

  • Marnix Wieffer
  • Marisa P. McShane
  • Marino Zerial
Chapter

Abstract

Many critical cellular processes, like vesicular transport and signaling, rely on the establishment and maintenance of membrane domains. Membrane domains consist of a cluster of specific lipids and proteins that provide membranes with a distinct molecular identity. Rab GTPases are one of the main coordinators of membrane domain formation and dynamics. In this chapter, we will give a brief introduction into Rab GTPases and focus on how they create and coordinate membrane domains. This will include an in-depth look into the Rab effectors and binding partners that define membrane domains. Throughout we will highlight how these proteins are regulated such as via feedback and feed-forward loops to create cascades. Finally, we propose that signaling domains on organelles are also coordinated by Rab GTPases.

Keywords

Rab GTPase Endosome Rab effector Membrane domain Signaling 

References

  1. Abankwa D, Gorfe A, Hancock J (2008) Mechanisms of Ras membrane organization and signaling: Ras on a rocker. Cell Cycle 7(17):2667–2673PubMedPubMedCentralGoogle Scholar
  2. Bache KG, Raiborg C, Mehlum A, Madshus IH, Stenmark H (2002) Phosphorylation of Hrs downstream of the epidermal growth factor receptor. Eur J Biochem 269(16):3881–3887PubMedGoogle Scholar
  3. Backer JM (2008) The regulation and function of Class III PI3Ks: novel roles for Vps34. Biochem J 410(1):1–17PubMedGoogle Scholar
  4. Barbero P, Bittova L, Pfeffer SR (2002) Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J Cell Biol 156(3):511–518PubMedPubMedCentralGoogle Scholar
  5. Barr FA (2013) Rab GTPases and membrane identity: causal or inconsequential? J Cell Biol 202(2):191–199PubMedPubMedCentralGoogle Scholar
  6. Barr F, Lambright DG (2010) Rab GEFs and GAPs. Curr Opin Cell Biol 22(4):461–470PubMedPubMedCentralGoogle Scholar
  7. Blümer J, Rey J, Dehmelt L, Mazel T, Wu Y-W, Bastiaens P, Goody RS, Itzen A (2013) RabGEFs are a major determinant for specific Rab membrane targeting. J Cell Biol 200(3):287–300PubMedPubMedCentralGoogle Scholar
  8. Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116(2):153–166PubMedGoogle Scholar
  9. Bonifacino JS, Hierro A (2011) Transport according to GARP: receiving retrograde cargo at the trans-Golgi network. Trends Cell Biol 21(3):159–167PubMedPubMedCentralGoogle Scholar
  10. Brandhorst D, Zwilling D, Rizzoli SO, Lippert U, Lang T, Jahn R (2006) Homotypic fusion of early endosomes: SNAREs do not determine fusion specificity. Proc Natl Acad Sci USA 103(8):2701–2706PubMedPubMedCentralGoogle Scholar
  11. Brandman O, Meyer T (2008) Feedback loops shape cellular signals in space and time. Science 322(5900):390–395PubMedPubMedCentralGoogle Scholar
  12. Bröcker C, Engelbrecht-Vandré S, Ungermann C (2010) Multisubunit tethering complexes and their role in membrane fusion. Curr Biol 20(21):R943–R952PubMedGoogle Scholar
  13. Bröcker C, Kuhlee A, Gatsogiannis C, Kleine Balderhaar HJ, Hönscher C, Engelbrecht-Vandré S, Ungermann C, Raunser S (2012) Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex. Proc Natl Acad Sci USA 109(6):1991–1996PubMedPubMedCentralGoogle Scholar
  14. Cao X, Ballew N, Barlowe C (1998) Initial docking of ER-derived vesicles requires Uso1p and Ypt1p but is independent of SNARE proteins. EMBO J 17(8):2156–2165PubMedPubMedCentralGoogle Scholar
  15. Carlton J, Bujny M, Peter BJ, Oorschot VMJ, Rutherford A, Mellor H, Klumperman J, McMahon HT, Cullen PJ (2004) Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Curr Biol 14(20):1791–1800PubMedGoogle Scholar
  16. Carroll KS, Hanna J, Simon I, Krise J, Barbero P, Pfeffer SR (2001) Role of Rab9 GTPase in facilitating receptor recruitment by TIP47. Science 292(5520):1373–1376PubMedGoogle Scholar
  17. Chan C-C, Scoggin S, Wang D, Cherry S, Dembo T, Greenberg B, Jin EJ, Kuey C, Lopez A, Mehta SQ, Perkins TJ, Brankatschk M, Rothenfluh A, Buszczak M, Hiesinger PR (2011) Systematic discovery of Rab GTPases with synaptic functions in Drosophila. Curr Biol 21(20):1704–1715PubMedPubMedCentralGoogle Scholar
  18. Chen PI, Kong C, Su X, Stahl PD (2009) Rab5 isoforms differentially regulate the trafficking and degradation of epidermal growth factor receptors. J Biol Chem 284(44):30328–30338PubMedPubMedCentralGoogle Scholar
  19. Cherfils J, Zeghouf M (2013) Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol Rev 93(1):269–309PubMedGoogle Scholar
  20. Chesneau L, Dambournet D, Machicoane M, Kouranti I, Fukuda M, Goud B, Echard A (2012) An ARF6/Rab35 GTPase cascade for endocytic recycling and successful cytokinesis. Curr Biol 22(2):147–153PubMedGoogle Scholar
  21. Christoforidis S, McBride HM, Burgoyne RD, Zerial M (1999a) The Rab5 effector EEA1 is a core component of endosome docking. Nature 397(6720):621–625PubMedGoogle Scholar
  22. Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, Yip S-C, Waterfield MD, Backer JM, Zerial M (1999b) Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1(4):249–252PubMedGoogle Scholar
  23. Conibear E, Cleck JN, Stevens TH (2003) Vps51p mediates the association of the GARP (Vps52/53/54) complex with the late golgi t-SNARE Tlg1p. Mol Biol Cell 14(4):1610–1623PubMedPubMedCentralGoogle Scholar
  24. De Renzis S, Sonnichsen B, Zerial M (2002) Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat Cell Biol 4(2):124–133PubMedGoogle Scholar
  25. 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. Mol Syst Biol 4:206PubMedPubMedCentralGoogle Scholar
  26. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443(7112):651–657PubMedGoogle Scholar
  27. Diekmann Y, Seixas E, Gouw M, Tavares-Cadete F, Seabra MC, Pereira-Leal JB (2011) Thousands of Rab GTPases for the cell biologist. PLoS Comput Biol 7(10):e1002217PubMedPubMedCentralGoogle Scholar
  28. 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(3):465–472PubMedPubMedCentralGoogle Scholar
  29. Dong B, Kakihara K, Otani T, Wada H, Hayashi S (2013) Rab9 and retromer regulate retrograde trafficking of luminal protein required for epithelial tube length control. Nat Commun 4:1358PubMedPubMedCentralGoogle Scholar
  30. Dou Z, Pan J-A, Dbouk HA, Ballou LM, DeLeon JL, Fan Y, Chen J-S, Liang Z, Li G, Backer JM, Lin RZ, Zong W-X (2013) Class IA PI3K p110β subunit promotes autophagy through Rab5 small GTPase in response to growth factor limitation. Mol Cell 50(1):29–42PubMedPubMedCentralGoogle Scholar
  31. Eathiraj S, Pan X, Ritacco C, Lambright DG (2005) Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature 436(7049):415–419PubMedPubMedCentralGoogle Scholar
  32. Elias M, Brighouse A, Gabernet-Castello C, Field MC, Dacks JB (2012) Sculpting the endomembrane system in deep time: high resolution phylogenetics of Rab GTPases. J Cell Sci 125(10):2500–2508PubMedPubMedCentralGoogle Scholar
  33. Field MC, Sali A, Rout MP (2011) On a bender-BARs, ESCRTs, COPs, and finally getting your coat. J Cell Biol 193(6):963–972PubMedPubMedCentralGoogle Scholar
  34. Frasa MAM, Koessmeier KT, Ahmadian MR, Braga VMM (2012) Illuminating the functional and structural repertoire of human TBC/RABGAPs. Nat Rev Mol Cell Biol 13(2):67–73PubMedGoogle Scholar
  35. Freisinger T, Klünder B, Johnson J, Müller N, Pichler G, Beck G, Costanzo M, Boone C, Cerione RA, Frey E, Wedlich-Söldner R (2013) Establishment of a robust single axis of cell polarity by coupling multiple positive feedback loops. Nat Commun 4:1807PubMedPubMedCentralGoogle Scholar
  36. Galvez T, Gilleron J, Zerial M, O’Sullivan GA (2012) SnapShot: mammalian Rab proteins in endocytic trafficking. Cell 151(1):234–234.e232PubMedGoogle Scholar
  37. Gould GW, Lippincott-Schwartz J (2009) New roles for endosomes: from vesicular carriers to multi-purpose platforms. Nat Rev Mol Cell Biol 10(4):287–292PubMedPubMedCentralGoogle Scholar
  38. Grecco H, Schmick M, Bastiaens PH (2011) Signaling from the living plasma membrane. Cell 144(6):897–909PubMedGoogle Scholar
  39. Grosshans BL, Andreeva A, Gangar A, Niessen S, Yates JR, Brennwald P, Novick P (2006a) The yeast lgl family member Sro7p is an effector of the secretory Rab GTPase Sec4p. J Cell Biol 172(1):55–66PubMedPubMedCentralGoogle Scholar
  40. Grosshans BL, Ortiz D, Novick P (2006b) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci USA 103(32):11821–11827PubMedPubMedCentralGoogle Scholar
  41. Guo W, Roth D, Walch-Solimena C, Novick P (1999) The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J 18(4):1071–1080PubMedPubMedCentralGoogle Scholar
  42. Gurkan C, Lapp H, Alory C, Su AI, Hogenesch JB, Balch WE (2005) Large-scale profiling of Rab GTPase trafficking networks: the membrome. Mol Biol Cell 16(8):3847–3864PubMedPubMedCentralGoogle Scholar
  43. Gurkan C, Koulov AV, Balch WE (2007) An evolutionary perspective on eukaryotic membrane trafficking. Adv Exp Med Biol 607:73–83PubMedGoogle Scholar
  44. Hales CM, Vaerman J-P, Goldenring JR (2002) Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J Biol Chem 277(52):50415–50421PubMedGoogle Scholar
  45. Hancock JF, Parton RG (2005) Ras plasma membrane signalling platforms. Biochem J 389(1):1–11PubMedPubMedCentralGoogle Scholar
  46. Hensel M, Klingauf J, Piehler J (2013) Imaging the invisible: resolving cellular microcompartments by superresolution microscopy techniques. Biol Chem 394(9):1097–1113PubMedGoogle Scholar
  47. Hoepfner S, Severin F, Cabezas A, Habermann B, Runge A, Gillooly D, Stenmark H, Zerial M (2005) Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121(3):437–450PubMedGoogle Scholar
  48. Horazdovsky BF, Cowles CR, Mustol P, Holmes M, Emr SD (1996) A Novel RING finger protein, Vps8p, functionally interacts with the small GTPase, Vps21p, to facilitate soluble vacuolar protein localization. J Biol Chem 271(52):33607–33615PubMedGoogle Scholar
  49. Horiuchi H, Lippé R, McBride HM, Rubino M, Woodman P, Stenmark H, Rybin V, Wilm M, Ashman K, Mann M, Zerial M (1997) A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90(6):1149–1159PubMedGoogle Scholar
  50. Hunt SD, Stephens DJ (2011) The role of motor proteins in endosomal sorting. Biochem Soc Trans 39(5):1179–1184PubMedGoogle Scholar
  51. Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91(1):119–149PubMedPubMedCentralGoogle Scholar
  52. Hyvola N, Diao A, McKenzie E, Skippen A, Cockcroft S, Lowe M (2006) Membrane targeting and activation of the Lowe syndrome protein OCRL1 by rab GTPases. EMBO J 25(16):3750–3761PubMedPubMedCentralGoogle Scholar
  53. Imamura T, Huang J, Usui I, Satoh H, Bever J, Olefsky JM (2003) Insulin-induced GLUT4 translocation involves protein kinase C-λ-mediated functional coupling between Rab4 and the motor protein kinesin. Mol Cell Biol 23(14):4892–4900PubMedPubMedCentralGoogle Scholar
  54. Jean S, Kiger AA (2012) Coordination between RAB GTPase and phosphoinositide regulation and functions. Nat Rev Mol Cell Biol 13(7):463–470PubMedGoogle Scholar
  55. Jin Y, Sultana A, Gandhi P, Franklin E, Hamamoto S, Khan AR, Munson M, Schekman R, Weisman LS (2011) Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex. Dev Cell 21(6):1156–1170PubMedPubMedCentralGoogle Scholar
  56. Johnson EE, Overmeyer JH, Gunning WT, Maltese WA (2006) Gene silencing reveals a specific function of hVps34 phosphatidylinositol 3-kinase in late versus early endosomes. J Cell Sci 119(7):1219–1232PubMedGoogle Scholar
  57. Jones AT, Clague MJ (1995) Phosphatidylinositol 3-kinase activity is required for early endosome fusion. Biochem J 311(1):31–34PubMedPubMedCentralGoogle Scholar
  58. Kauppi M, Simonsen A, Br B, Vieira A, Callaghan J, Stenmark H, Olkkonen VM (2002) The small GTPase Rab22 interacts with EEA1 and controls endosomal membrane trafficking. J Cell Sci 115(5):899–911PubMedGoogle Scholar
  59. Klöpper T, Kienle N, Fasshauer D, Munro S (2012) Untangling the evolution of Rab G proteins: implications of a comprehensive genomic analysis. BMC Biol 10(1):71PubMedPubMedCentralGoogle Scholar
  60. Kobayashi H, Fukuda M (2013) Rab35 establishes the EHD1-association site by coordinating two distinct effectors during neurite outgrowth. J Cell Sci 126(11):2424–2435PubMedGoogle Scholar
  61. Kouranti I, Sachse M, Arouche N, Goud B, Echard A (2006) Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 16(17):1719–1725PubMedGoogle Scholar
  62. Kozubowski L, Saito K, Johnson JM, Howell AS, Zyla TR, Lew DJ (2008) Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr Biol 18(22):1719–1726PubMedPubMedCentralGoogle Scholar
  63. Krauß M, Haucke V (2007) Phosphoinositides: regulators of membrane traffic and protein function. FEBS Lett 581(11):2105–2111PubMedGoogle Scholar
  64. Kurosu H, Katada T (2001) Association of phosphatidylinositol 3-kinase composed of p110β-catalytic and p85-regulatory subunits with the small GTPase Rab5. J Biochem 130(1):73–78PubMedGoogle Scholar
  65. Lane KT, Beese LS (2006) Thematic review series: lipid posttranslational modifications. Structural biology of protein farnesyltransferase and geranylgeranyltransferase type I. J Lipid Res 47(4):681–699PubMedGoogle Scholar
  66. Lapierre LA, Kumar R, Hales CM, Navarre J, Bhartur SG, Burnette JO, Provance DW, Mercer JA, Bähler M, Goldenring JR (2001) Myosin Vb Is associated with plasma membrane recycling systems. Mol Biol Cell 12(6):1843–1857PubMedPubMedCentralGoogle Scholar
  67. Lawe DC, Chawla A, Merithew E, Dumas J, Carrington W, Fogarty K, Lifshitz L, Tuft R, Lambright D, Corvera S (2002) Sequential roles for phosphatidylinositol 3-phosphate and Rab5 in tethering and fusion of early endosomes via their interaction with EEA1. J Biol Chem 277(10):8611–8617PubMedGoogle Scholar
  68. Li G, D’Souza-Schorey C, Barbieri MA, Roberts RL, Klippel A, Williams LT, Stahl PD (1995) Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. Proc Natl Acad Sci USA 92(22):10207–10211PubMedPubMedCentralGoogle Scholar
  69. Lindsay AJ, Hendrick AG, Cantalupo G, Senic-Matuglia F, Goud B, Bucci C, McCaffrey MW (2002) Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein. J Biol Chem 277(14):12190–12199PubMedGoogle Scholar
  70. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327(5961):46–50PubMedGoogle Scholar
  71. Lipatova Z, Tokarev AA, Jin Y, Mulholland J, Weisman LS, Segev N (2008) Direct interaction between a myosin V motor and the Rab GTPases Ypt31/32 is required for polarized secretion. Mol Biol Cell 19(10):4177–4187PubMedPubMedCentralGoogle Scholar
  72. Lloyd TE, Atkinson R, Wu MN, Zhou Y, Pennetta G, Bellen HJ (2002) Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell 108(2):261–269PubMedGoogle Scholar
  73. Malerød L, Stuffers S, Brech A, Stenmark H (2007) Vps22/EAP30 in ESCRT-II mediates endosomal sorting of growth factor and chemokine receptors destined for lysosomal degradation. Traffic 8(11):1617–1629PubMedGoogle Scholar
  74. Mao X, Kikani CK, Riojas RA, Langlais P, Wang L, Ramos FJ, Fang Q, Christ-Roberts CY, Hong JY, Kim RY, Liu F, Dong LQ (2006) APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat Cell Biol 8(5):516–523PubMedGoogle Scholar
  75. Markgraf DF, Ahnert F, Arlt H, Mari M, Peplowska K, Epp N, Griffith J, Reggiori F, Ungermann C (2009) The CORVET subunit Vps8 cooperates with the Rab5 homolog Vps21 to induce clustering of late endosomal compartments. Mol Biol Cell 20(24):5276–5289PubMedPubMedCentralGoogle Scholar
  76. McBride HM, Rybin V, Murphy C, Giner A, Teasdale R, Zerial M (1999) Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98(3):377–386PubMedGoogle Scholar
  77. Merithew E, Stone C, Eathiraj S, Lambright DG (2003) Determinants of Rab5 interaction with the N terminus of early endosome antigen 1. J Biol Chem 278(10):8494–8500PubMedGoogle Scholar
  78. Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, Wilm M, Parton RG, Zerial M (2004) APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116(3):445–456PubMedGoogle Scholar
  79. Mills IG, Jones AT, Clague MJ (1998) Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr Biol 8(15):881–884PubMedGoogle Scholar
  80. Mitsuuchi Y, Johnson SW, Sonoda G, Tanno S, Golemis EA, Testa JR (1999) Identification of a chromosome 3p14.3-21.1 gene, APPL, encoding an adaptor molecule that interacts with the oncoprotein-serine/threonine kinase AKT2. Oncogene 18(35):4891–4898PubMedGoogle Scholar
  81. Mizuno-Yamasaki E, Medkova M, Coleman J, Novick P (2010) Phosphatidylinositol 4-phosphate controls both membrane recruitment and a regulatory switch of the Rab GEF Sec2p. Dev Cell 18(5):828–840PubMedPubMedCentralGoogle Scholar
  82. Munro S (2011) The golgin coiled-coil proteins of the golgi apparatus. Cold Spring Harb Perspect Biol 3(6):1–14Google Scholar
  83. Murray JT, Panaretou C, Stenmark H, Miaczynska M, Backer JM (2002) Role of Rab5 in the recruitment of hVps34/p150 to the early endosome. Traffic 3(6):416–427PubMedGoogle Scholar
  84. Nielsen E, Severin F, Backer JM, Hyman AA, Zerial M (1999) Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol 1(6):376–382PubMedGoogle Scholar
  85. Nielsen E, Christoforidis S, Uttenweiler-Joseph S, Miaczynska M, Dewitte F, Wilm M, Hoflack B, Zerial M (2000) Rabenosyn-5, a novel Rab5 effector, is complexed with Hvps45 and recruited to endosomes through a FYVE finger domain. J Cell Biol 151(3):601–612PubMedPubMedCentralGoogle Scholar
  86. Nordmann M, Cabrera M, Perz A, Bröcker C, Ostrowicz C, Engelbrecht-Vandré S, Ungermann C (2010) The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr Biol 20(18):1654–1659PubMedGoogle Scholar
  87. Numrich J, Ungermann C (2014) Endocytic Rabs in membrane trafficking and signaling. Biol Chem 395(3):327–333PubMedGoogle Scholar
  88. Ohya T, Miaczynska M, Coskun Ü, Lommer B, Runge A, Drechsel D, Kalaidzidis Y, Zerial M (2009) Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes. Nature 459(7250):1091–1097PubMedGoogle Scholar
  89. Ortiz D, Medkova M, Walch-Solimena C, Novick P (2002) Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J Cell Biol 157(6):1005–1015PubMedPubMedCentralGoogle Scholar
  90. Palfy M, Remenyi A, Korcsmaros T (2012) Endosomal crosstalk: meeting points for signaling pathways. Trends Cell Biol 22(9):447–456PubMedPubMedCentralGoogle Scholar
  91. Peplowska K, Markgraf DF, Ostrowicz CW, Bange G, Ungermann C (2007) The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev Cell 12(5):739–750PubMedGoogle Scholar
  92. Pereira-Leal JB (2008) The Ypt/Rab family and the evolution of trafficking in fungi. Traffic 9(1):27–38PubMedGoogle Scholar
  93. Pérez-Victoria FJ, Schindler C, Magadán JG, Mardones GA, Delevoye C, Romao M, Raposo G, Bonifacino JS (2010) Ang2/fat-free is a conserved subunit of the golgi-associated retrograde protein complex. Mol Biol Cell 21(19):3386–3395PubMedPubMedCentralGoogle Scholar
  94. Pfeffer SR (2013a) A nexus for receptor recycling. Nat Cell Biol 15(5):446–448PubMedGoogle Scholar
  95. Pfeffer SR (2013b) Rab GTPase regulation of membrane identity. Curr Opin Cell Biol 25(4):414–419PubMedPubMedCentralGoogle Scholar
  96. Platta HW, Stenmark H (2011) Endocytosis and signaling. Curr Opin Cell Biol 23(4):393–403PubMedGoogle Scholar
  97. Plemel RL, Lobingier BT, Brett CL, Angers CG, Nickerson DP, Paulsel A, Sprague D, Merz AJ (2011) Subunit organization and Rab interactions of Vps-C protein complexes that control endolysosomal membrane traffic. Mol Biol Cell 22(8):1353–1363PubMedPubMedCentralGoogle Scholar
  98. Polevoy G, Wei H-C, Wong R, Szentpetery Z, Kim YJ, Goldbach P, Steinbach SK, Balla T, Brill JA (2009) Dual roles for the Drosophila PI 4-kinase four wheel drive in localizing Rab11 during cytokinesis. J Cell Biol 187(6):847–858PubMedPubMedCentralGoogle Scholar
  99. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010) Identification of the switch in early-to-late endosome transition. Cell 141(3):497–508PubMedGoogle Scholar
  100. Preuss ML, Schmitz AJ, Thole JM, Bonner HKS, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kβ1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172(7):991–998PubMedPubMedCentralGoogle Scholar
  101. Price A, Wickner W, Ungermann C (2000) Proteins needed for vesicle budding from the golgi complex are also required for the docking step of homotypic vacuole fusion. J Cell Biol 148(6):1223–1230PubMedPubMedCentralGoogle Scholar
  102. Raiborg C, Bache KG, Gillooly DJ, Madshus IH, Stang E, Stenmark H (2002) Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol 4(5):394–398PubMedGoogle Scholar
  103. Raiborg C, Malerød L, Pedersen NM, Stenmark H (2008) Differential functions of Hrs and ESCRT proteins in endocytic membrane trafficking. Exp Cell Res 314(4):801–813PubMedGoogle Scholar
  104. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122(5):735–749PubMedGoogle Scholar
  105. Rivera-Molina FE, Novick PJ (2009) A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc Natl Acad Sci USA 106(34):14408–14413PubMedPubMedCentralGoogle Scholar
  106. Rizo J, Südhof TC (2012) The membrane fusion enigma: SNAREs, Sec1/Munc18 proteins, and their accomplices–guilty as charged? Annu Rev Cell Dev Biol 28(1):279–308PubMedGoogle Scholar
  107. Rojas R, van Vlijmen T, Mardones GA, Prabhu Y, Rojas AL, Mohammed S, Heck AJR, Ga R, van der Sluijs P, Bonifacino JS (2008) Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J Cell Biol 183(3):513–526PubMedPubMedCentralGoogle Scholar
  108. Santiago-Tirado FH, Legesse-Miller A, Schott D, Bretscher A (2011) PI4P and Rab inputs collaborate in myosin-V-dependent transport of secretory compartments in yeast. Dev Cell 20(1):47–59PubMedPubMedCentralGoogle Scholar
  109. Schenck A, Goto-Silva L, Collinet C, Rhinn M, Giner A, Habermann B, Brand M, Zerial M (2008) The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 133(3):486–497PubMedGoogle Scholar
  110. Seaman MNJ (2012) The retromer complex—endosomal protein recycling and beyond. J Cell Sci 125(20):4693–4702PubMedPubMedCentralGoogle Scholar
  111. Shin H-W, Hayashi M, Christoforidis S, Lacas-Gervais S, Hoepfner S, Wenk MR, Modregger J, Uttenweiler-Joseph S, Wilm M, Nystuen A, Frankel WN, Solimena M, De Camilli P, Zerial M (2005) An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J Cell Biol 170(4):607–618PubMedPubMedCentralGoogle Scholar
  112. Simonsen A, Lippé R, Christoforidis S, Gaullier J-M, Brech A, Callaghan J, Toh B-H, Murphy C, Zerial M, Stenmark H (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394(6692):494–498PubMedGoogle Scholar
  113. Simonsen A, Gaullier JM, D’Arrigo A, Stenmark H (1999) The Rab5 effector EEA1 interacts directly with syntaxin-6. J Biochem 274:28857–28860Google Scholar
  114. Simonsen A, Wurmser AE, Emr SD, Stenmark H (2001) The role of phosphoinositides in membrane transport. Curr Opin Cell Biol 13(4):485–492PubMedGoogle Scholar
  115. Siniossoglou S, Pelham HRB (2002) Vps51p links the VFT complex to the SNARE Tlg1p. J Biol Chem 277(50):48318–48324PubMedGoogle Scholar
  116. Sivars U, Aivazian D, Pfeffer SR (2003) Yip3 catalyses the dissociation of endosomal Rab-GDI complexes. Nature 425(6960):856–859PubMedGoogle Scholar
  117. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M (2000) Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149(4):901–914PubMedPubMedCentralGoogle Scholar
  118. Sorkin A, von Zastrow M (2009) Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10(9):609–622PubMedPubMedCentralGoogle Scholar
  119. Stalder D, Mizuno-Yamasaki E, Ghassemian M, Novick PJ (2013) Phosphorylation of the Rab exchange factor Sec2p directs a switch in regulatory binding partners. Proc Natl Acad Sci USA 110(50):19995–20002PubMedPubMedCentralGoogle Scholar
  120. Stein M, Pilli M, Bernauer S, Habermann BH, Zerial M, Wade RC (2012) The interaction properties of the human Rab GTPase family-comparative analysis reveals determinants of molecular binding selectivity. PLoS One 7(4):e34870PubMedPubMedCentralGoogle Scholar
  121. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10(8):513–525PubMedGoogle Scholar
  122. Stenmark H (2012) The Rabs: a family at the root of metazoan evolution. BMC Biol 10:68PubMedPubMedCentralGoogle Scholar
  123. Stenmark H, Vitale G, Ullrich O, Zerial M (1995) Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion. Cell 83(3):423–432PubMedGoogle Scholar
  124. Stroupe C, Collins KM, Fratti RA, Wickner W (2006) Purification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p. EMBO J 25(8):1579–1589PubMedPubMedCentralGoogle Scholar
  125. Suda Y, Kurokawa K, Hirata R, Nakano A (2013) Rab GAP cascade regulates dynamics of Ypt6 in the Golgi traffic. Proc Natl Acad Sci USA 110(47):18976–18981PubMedPubMedCentralGoogle Scholar
  126. Südhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323(5913):474–477PubMedPubMedCentralGoogle Scholar
  127. Suvorova ES, Duden R, Lupashin VV (2002) The Sec34/Sec35p complex, a Ypt1p effector required for retrograde intra-Golgi trafficking, interacts with Golgi SNAREs and COPI vesicle coat proteins. J Cell Biol 157(4):631–643PubMedPubMedCentralGoogle Scholar
  128. Ueno H, Huang X, Tanaka Y, Hirokawa N (2011) KIF16B/Rab14 molecular motor complex is critical for early embryonic development by transporting FGF receptor. Dev Cell 20(1):60–71PubMedGoogle Scholar
  129. 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(6467):157–160PubMedGoogle Scholar
  130. Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, Bilanges B (2010) The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol 11(5):329–341PubMedGoogle Scholar
  131. Vitale G, Rybin V, Christoforidis S, Thornqvist P-O, McCaffrey M, Stenmark H, Zerial M (1998) Distinct Rab-binding domains mediate the interaction of Rabaptin-5 with GTP-bound Rab4 and Rab5. EMBO J 17(7):1941–1951PubMedPubMedCentralGoogle Scholar
  132. Vonderheit A, Helenius A (2005) Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 3(7):e233PubMedPubMedCentralGoogle Scholar
  133. Weigert R, Porat-Shliom N, Amornphimoltham P (2013) Imaging cell biology in live animals: ready for prime time. J Cell Biol 201(7):969–979PubMedPubMedCentralGoogle Scholar
  134. 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(7):534–540PubMedGoogle Scholar
  135. Wurmser AE, Sato TK, Emr SD (2000) New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to snare-dependent docking and fusion. J Cell Biol 151(3):551–562PubMedPubMedCentralGoogle Scholar
  136. Yoo SK, Deng Q, Cavnar PJ, Wu YI, Hahn KM, Huttenlocher A (2010) Differential regulation of protrusion and polarity by PI(3)K during neutrophil motility in live zebrafish. Dev Cell 18(2):226–236PubMedPubMedCentralGoogle Scholar
  137. Yu I-M, Hughson FM (2010) Tethering factors as organizers of intracellular vesicular traffic. Annu Rev Cell Dev Biol 26(1):137–156PubMedGoogle Scholar
  138. Zeigerer A, Gilleron J, Bogorad RL, Marsico G, Nonaka H, Seifert S, Epstein-Barash H, Kuchimanchi S, Peng CG, Ruda VM, Del Conte-Zerial P, Hengstler JG, Kalaidzidis Y, Koteliansky V, Zerial M (2012) Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. Nature 485(7399):465–470PubMedGoogle Scholar
  139. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2(2):107–117PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Max Planck Institute of Molecular Cell Biology and GeneticsDresdenGermany

Personalised recommendations