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Protoplasma

, Volume 249, Issue 3, pp 587–597 | Cite as

The exocyst complex in exocytosis and cell migration

  • Jianglan Liu
  • Wei GuoEmail author
Review Article

Abstract

Exocytosis is a fundamental membrane trafficking event in eukaryotic cells in which membrane proteins or lipids are incorporated into the plasma membrane and vesicle contents are secreted to the exterior of the cell. The exocyst, an evolutionarily conserved octameric protein complex, plays a crucial role in the targeting of secretory vesicles to the plasma membrane during exocytosis. The exocyst has been shown to be involved in diverse cellular processes requiring polarized exocytosis such as yeast budding, epithelial polarity establishment, and neurite outgrowth. Recently, the exocyst has also been implicated in cell migration through mechanisms independent of its role in exocytosis. In this review, we will first summarize our knowledge on the exocyst complex at a molecular and structural level. Then, we will discuss the specific functions of the exocyst in exocytosis in various cell types. Finally, we will review the emerging roles of the exocyst during cell migration and tumor cell invasion.

Keywords

Exocyst Exocytosis Cell migration Arp2/3 complex Small GTPase 

Notes

Acknowledgment

We would like to thank Dr. John Schmidt in the Guo lab for thorough reading of the manuscript prior to submission. The work in Wei Guo’s laboratory has been supported by the National Institutes of Health, Pew Scholars Program in Biomedical Sciences and American Heart Association.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aalto MK, Ronne H, Keranen S (1993) Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport. EMBO J 12:4095–4104PubMedGoogle Scholar
  2. Abe T, Kato M, Miki H, Takenawa T, Endo T (2003) Small GTPase TC10 and its homologue RhoT induce N-WASP-mediated long process formation and neurite outgrowth. J Cell Sci 116:155–168PubMedCrossRefGoogle Scholar
  3. Baek K, Knodler A, Lee SH, Zhang X, Orlando K, Zhang J, Foskett TJ, Guo W, Dominguez R (2010) Structure-function study of the N-terminal domain of exocyst subunit Sec3. J Biol Chem 285:10424–10433PubMedCrossRefGoogle Scholar
  4. Beronja S, Laprise P, Papoulas O, Pellikka M, Sisson J, Tepass U (2005) Essential function of Drosophila Sec6 in apical exocytosis of epithelial photoreceptor cells. J Cell Biol 169:635–646PubMedCrossRefGoogle Scholar
  5. Boeckeler K, Rosse C, Howell M, Parker PJ (2010) Manipulating signal delivery—plasma-membrane ERK activation in aPKC-dependent migration. J Cell Sci 123:2725–2732PubMedCrossRefGoogle Scholar
  6. Brown MD, Sacks DB (2006) IQGAP1 in cellular signaling: bridging the GAP. Trends Cell Biol 16:242–249PubMedCrossRefGoogle Scholar
  7. Brown DL, Heimann K, Lock J, Kjer-Nielsen L, van Vliet C, Stow JL, Gleeson PA (2001) The GRIP domain is a specific targeting sequence for a population of trans-Golgi network derived tubulo-vesicular carriers. Traffic 2:336–344PubMedCrossRefGoogle Scholar
  8. Bryant DM, Datta A, Rodríguez-Fraticelli AE, Peränen J, Martín-Belmonte F, Mostov KE (2010) A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 12(11):1035–1045PubMedCrossRefGoogle Scholar
  9. Brymora A, Valova VA, Larsen MR, Roufogalis BD, Robinson PJ (2001) The brain exocyst complex interacts with RalA in a GTP-dependent manner: identification of a novel mammalian Sec3 gene and a second Sec15 gene. J Biol Chem 276:29792–29797PubMedCrossRefGoogle Scholar
  10. Cavanaugh LF, Chen X, Richardson BC, Ungar D, Pelczer I, Rizo J, Hughson FM (2007) Structural analysis of conserved oligomeric Golgi complex subunit 2. J Biol Chem 282:23418–23426PubMedCrossRefGoogle Scholar
  11. Chen XW, Leto D, Xiao J, Goss J, Wang Q, Shavit JA, Xiong T, Yu G, Ginsburg D, Toomre D, Xu Z, Saltiel AR (2011) Exocyst function is regulated by effector phosphorylation. Nat Cell Biol 13(5):580–588PubMedCrossRefGoogle Scholar
  12. Cole RA, Synek L, Zarsky V, Fowler JE (2005) SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol 138:2005–2018PubMedCrossRefGoogle Scholar
  13. Das A, Guo W (2011) Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol 21(7):383–386PubMedCrossRefGoogle Scholar
  14. Dong G, Hutagalung AH, Fu C, Novick P, Reinisch KM (2005) The structures of exocyst subunit Exo70p and the Exo84p C-terminal domains reveal a common motif. Nat Struct Mol Biol 12:1094–1100PubMedCrossRefGoogle Scholar
  15. Dupraz S, Grassi D, Bernis ME, Sosa L, Bisbal M, Gastaldi L, Jausoro I, Caceres A, Pfenninger KH, Quiroga S (2009) The TC10–Exo70 complex is essential for membrane expansion and axonal specification in developing neurons. J Neurosci 29:13292–13301PubMedCrossRefGoogle Scholar
  16. Elias M, Drdova E, Ziak D, Bavlnka B, Hala M, Cvrckova F, Soukupova H, Zarsky V (2003) The exocyst complex in plants. Cell Biol Int 27(3):199–201PubMedCrossRefGoogle Scholar
  17. Ewart MA, Clarke M, Kane S, Chamberlain LH, Gould GW (2005) Evidence for a role of the exocyst in insulin-stimulated Glut4 trafficking in 3 T3-L1 adipocytes. J Biol Chem 280:3812–3816PubMedCrossRefGoogle Scholar
  18. Feig LA (2003) Ral-GTPases: approaching their 15 minutes of fame. Trends Cell Biol 13:419–425PubMedCrossRefGoogle Scholar
  19. Fukai S, Matern HT, Jagath JR, Scheller RH, Brunger AT (2003) Structural basis of the interaction between RalA and Sec5, a subunit of the sec6/8 complex. EMBO J 22:3267–3278PubMedCrossRefGoogle Scholar
  20. Gerges NZ, Backos DS, Rupasinghe CN, Spaller MR, Esteban JA (2006) Dual role of the exocyst in AMPA receptor targeting and insertion into the postsynaptic membrane. EMBO J 25:1623–1634PubMedCrossRefGoogle Scholar
  21. Goley ED, Welch MD (2006) The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 7:713–726PubMedCrossRefGoogle Scholar
  22. Govindan B, Bowser R, Novick P (1995) The role of Myo2, a yeast class V myosin, in vesicular transport. J Cell Biol 128:1055–1068PubMedCrossRefGoogle Scholar
  23. Grindstaff KK, Yeaman C, Anandasabapathy N, Hsu SC, Rodriguez-Boulan E, Scheller RH, Nelson WJ (1998) Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 93:731–740PubMedCrossRefGoogle Scholar
  24. Grote E, Carr CM, Novick PJ (2000) Ordering the final events in yeast exocytosis. J Cell Biol 151:439–452PubMedCrossRefGoogle Scholar
  25. 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 18:1071–1080PubMedCrossRefGoogle Scholar
  26. Guo W, Sacher M, Barrowman J, Ferro-Novick S, Novick P (2000) Protein complexes in transport vesicle targeting. Trends Cell Biol 10:251–255PubMedCrossRefGoogle Scholar
  27. Guo W, Tamanoi F, Novick P (2001) Spatial regulation of the exocyst complex by Rho1 GTPase. Nat Cell Biol 3(4):353–360PubMedCrossRefGoogle Scholar
  28. Hala M, Cole R, Synek L, Drdova E, Pecenkova T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler JE, Zarsky V (2008) An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20:1330–1345PubMedCrossRefGoogle Scholar
  29. Hamburger ZA, Hamburger AE, West AP Jr, Weis WI (2006) Crystal structure of the S.cerevisiae exocyst component Exo70p. J Mol Biol 356:9–21PubMedCrossRefGoogle Scholar
  30. Hase K, Kimura S, Takatsu H, Ohmae M, Kawano S, Kitamura H, Ito M, Watarai H, Hazelett CC, Yeaman C, Ohno H (2009) M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat Cell Biol 11:1427–1432PubMedCrossRefGoogle Scholar
  31. Hazuka CD, Foletti DL, Hsu SC, Kee Y, Hopf FW, Scheller RH (1999) The sec6/8 complex is located at neurite outgrowth and axonal synapse-assembly domains. J Neurosci 19:1324–1334PubMedGoogle Scholar
  32. He B, Guo W (2009) The exocyst complex in polarized exocytosis. Curr Opin Cell Biol 21:537–542PubMedCrossRefGoogle Scholar
  33. Hsu SC, Ting AE, Hazuka CD, Davanger S, Kenny JW, Kee Y, Scheller RH (1996) The mammalian brain rsec6/8 complex. Neuron 17:1209–1219PubMedCrossRefGoogle Scholar
  34. Hsu SC, Hazuka CD, Roth R, Foletti D, Heuser J, Scheller RH (1998) Subunit composition, protein interactions, and structures of the mammalian brain sec6/8 complex and septin filaments. Neuron 20:1111–1122PubMedCrossRefGoogle Scholar
  35. Hsu SC, Hazuka CD, Foletti DL, Scheller RH (1999) Targeting vesicles to specific sites on the plasma membrane: the role of the sec6/8 complex. Trends Cell Biol 9:150–153PubMedCrossRefGoogle Scholar
  36. Inoue M, Chang L, Hwang J, Chiang SH, Saltiel AR (2003) The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature 422:629–633PubMedCrossRefGoogle Scholar
  37. Inoue M, Chiang SH, Chang L, Chen XW, Saltiel AR (2006) Compartmentalization of the exocyst complex in lipid rafts controls Glut4 vesicle tethering. Mol Biol Cell 17:2303–2311PubMedCrossRefGoogle Scholar
  38. Jin R, Junutula JR, Matern HT, Ervin KE, Scheller RH, Brunger AT (2005) Exo84 and Sec5 are competitive regulatory Sec6/8 effectors to the RalA GTPase. EMBO J 24:2064–2074PubMedCrossRefGoogle Scholar
  39. Kawase K, Nakamura T, Takaya A, Aoki K, Namikawa K, Kiyama H, Inagaki S, Takemoto H, Saltiel AR, Matsuda M (2006) GTP hydrolysis by the Rho family GTPase TC10 promotes exocytic vesicle fusion. Dev Cell 11:411–421PubMedCrossRefGoogle Scholar
  40. Langevin J, Morgan MJ, Sibarita JB, Aresta S, Murthy M, Schwarz T, Camonis J, Bellaiche Y (2005) Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev Cell 9:365–376PubMedCrossRefGoogle Scholar
  41. LeClaire LL 3rd, Baumgartner M, Iwasa JH, Mullins RD, Barber DL (2008) Phosphorylation of the Arp2/3 complex is necessary to nucleate actin filaments. J Cell Biol 182:647–654PubMedCrossRefGoogle Scholar
  42. Lemmon MA (2004) Pleckstrin homology domains: not just for phosphoinositides. Biochem Soc Trans 32:707–711PubMedCrossRefGoogle Scholar
  43. Liu J, Zuo X, Yue P, Guo W (2007) Phosphatidylinositol 4,5-bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells. Mol Biol Cell 18:4483–4492PubMedCrossRefGoogle Scholar
  44. Liu J, Yue P, Artym VV, Mueller SC, Guo W (2009) The role of the exocyst in matrix metalloproteinase secretion and actin dynamics during tumor cell invadopodia formation. Mol Biol Cell 20:3763–3771PubMedCrossRefGoogle Scholar
  45. Lizunov VA, Lisinski I, Stenkula K, Zimmerberg J, Cushman SW (2009) Insulin regulates fusion of GLUT4 vesicles independent of Exo70-mediated tethering. J Biol Chem 284:7914–7919PubMedCrossRefGoogle Scholar
  46. Mattila PK, Pykalainen A, Saarikangas J, Paavilainen VO, Vihinen H, Jokitalo E, Lappalainen P (2007) Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J Cell Biol 176:953–964PubMedCrossRefGoogle Scholar
  47. McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590–596PubMedCrossRefGoogle Scholar
  48. Mendoza MC, Er EE, Zhang W, Ballif BA, Elliott HL, Danuser G, Blenis J (2011) ERK-MAPK drives lamellipodia protrusion by activating the WAVE2 regulatory complex. Mol Cell 41:661–671PubMedCrossRefGoogle Scholar
  49. Moore BA, Robinson HH, Xu Z (2007) The crystal structure of mouse Exo70 reveals unique features of the mammalian exocyst. J Mol Biol 371:410–421PubMedCrossRefGoogle Scholar
  50. Moskalenko S, Henry DO, Rosse C, Mirey G, Camonis JH, White MA (2002) The exocyst is a Ral effector complex. Nat Cell Biol 4:66–72PubMedCrossRefGoogle Scholar
  51. Mott HR, Nietlispach D, Hopkins LJ, Mirey G, Camonis JH, Owen D (2003) Structure of the GTPase-binding domain of Sec5 and elucidation of its Ral binding site. J Biol Chem 278:17053–17059PubMedCrossRefGoogle Scholar
  52. Munson M, Novick P (2006) The exocyst defrocked, a framework of rods revealed. Nat Struct Mol Biol 13:577–581PubMedCrossRefGoogle Scholar
  53. Murthy M, Garza D, Scheller RH, Schwarz TL (2003) Mutations in the exocyst component Sec5 disrupt neuronal membrane traffic, but neurotransmitter release persists. Neuron 37:433–447PubMedCrossRefGoogle Scholar
  54. Noritake J, Watanabe T, Sato K, Wang S, Kaibuchi K (2005) IQGAP1: a key regulator of adhesion and migration. J Cell Sci 118:2085–2092PubMedCrossRefGoogle Scholar
  55. Novick P, Guo W (2002) Ras family therapy: Rab, Rho and Ral talk to the exocyst. Trends Cell Biol 12:247–249PubMedCrossRefGoogle Scholar
  56. Novick P, Schekman R (1979) Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 76:1858–1862PubMedCrossRefGoogle Scholar
  57. Novick P, Field C, Schekman R (1980) Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21:205–215PubMedCrossRefGoogle Scholar
  58. Oztan A, Silvis M, Weisz OA, Bradbury NA, Hsu SC, Goldenring JR, Yeaman C, Apodaca G (2007) Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells. Mol Biol Cell 18:3978–3992PubMedCrossRefGoogle Scholar
  59. Pfeffer SR (1999) Transport-vesicle targeting: tethers before SNAREs. Nat Cell Biol 1:E17–E22PubMedCrossRefGoogle Scholar
  60. Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465PubMedCrossRefGoogle Scholar
  61. Polzin A, Shipitsin M, Goi T, Feig LA, Turner TJ (2002) Ral-GTPase influences the regulation of the readily releasable pool of synaptic vesicles. Mol Cell Biol 22:1714–1722PubMedCrossRefGoogle Scholar
  62. Prigent M, Dubois T, Raposo G, Derrien V, Tenza D, Rosse C, Camonis J, Chavrier P (2003) ARF6 controls post-endocytic recycling through its downstream exocyst complex effector. J Cell Biol 163:1111–1121PubMedCrossRefGoogle Scholar
  63. Riefler GM, Balasingam G, Lucas KG, Wang S, Hsu SC, Firestein BL (2003) Exocyst complex subunit sec8 binds to postsynaptic density protein-95 (PSD-95): a novel interaction regulated by cypin (cytosolic PSD-95 interactor). Biochem J 373:49–55PubMedCrossRefGoogle Scholar
  64. Rosse C, Hatzoglou A, Parrini MC, White MA, Chavrier P, Camonis J (2006) RalB mobilizes the exocyst to drive cell migration. Mol Cell Biol 26:727–734PubMedCrossRefGoogle Scholar
  65. Rosse C, Formstecher E, Boeckeler K, Zhao Y, Kremerskothen J, White MD, Camonis JH, Parker PJ (2009) An aPKC-exocyst complex controls paxillin phosphorylation and migration through localised JNK1 activation. PLoS Biol 7:e1000235PubMedCrossRefGoogle Scholar
  66. Sakurai-Yageta M, Recchi C, Le Dez G, Sibarita JB, Daviet L, Camonis J, D’Souza-Schorey C, Chavrier P (2008) The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J Cell Biol 181:985–998PubMedCrossRefGoogle Scholar
  67. Sans N, Prybylowski K, Petralia RS, Chang K, Wang YX, Racca C, Vicini S, Wenthold RJ (2003) NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nat Cell Biol 5:520–530PubMedCrossRefGoogle Scholar
  68. Scita G, Confalonieri S, Lappalainen P, Suetsugu S (2008) IRSp53: crossing the road of membrane and actin dynamics in the formation of membrane protrusions. Trends Cell Biol 18:52–60PubMedCrossRefGoogle Scholar
  69. Shipitsin M, Feig LA (2004) RalA but not RalB enhances polarized delivery of membrane proteins to the basolateral surface of epithelial cells. Mol Cell Biol 24:5746–5756PubMedCrossRefGoogle Scholar
  70. Sivaram MV, Furgason ML, Brewer DN, Munson M (2006) The structure of the exocyst subunit Sec6p defines a conserved architecture with diverse roles. Nat Struct Mol Biol 13:555–556PubMedCrossRefGoogle Scholar
  71. Spiczka KS, Yeaman C (2008) Ral-regulated interaction between Sec5 and paxillin targets Exocyst to focal complexes during cell migration. J Cell Sci 121:2880–2891PubMedCrossRefGoogle Scholar
  72. Sugihara K, Asano S, Tanaka K, Iwamatsu A, Okawa K, Ohta Y (2002) The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat Cell Biol 4:73–78PubMedCrossRefGoogle Scholar
  73. Svitkina T (2007) Electron microscopic analysis of the leading edge in migrating cells. Methods Cell Biol 79:295–319PubMedCrossRefGoogle Scholar
  74. Synek L, Schlager N, Elias M, Quentin M, Hauser MT, Zarsky V (2006) AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J 48:54–72PubMedCrossRefGoogle Scholar
  75. TerBush DR, Novick P (1995) Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae. J Cell Biol 130:299–312PubMedCrossRefGoogle Scholar
  76. TerBush DR, Maurice T, Roth D, Novick P (1996) The exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J 15:6483–6494PubMedGoogle Scholar
  77. Terbush DR, Guo W, Dunkelbarger S, Novick P (2001) Purification and characterization of yeast exocyst complex. Methods Enzymol 329:100–110PubMedCrossRefGoogle Scholar
  78. Ting AE, Hazuka CD, Hsu SC, Kirk MD, Bean AJ, Scheller RH (1995) rSec6 and rSec8, mammalian homologs of yeast proteins essential for secretion. Proc Natl Acad Sci USA 92:9613–9617PubMedCrossRefGoogle Scholar
  79. Tsuboi T, Ravier MA, Xie H, Ewart MA, Gould GW, Baldwin SA, Rutter GA (2005) Mammalian exocyst complex is required for the docking step of insulin vesicle exocytosis. J Biol Chem 280:25565–25570PubMedCrossRefGoogle Scholar
  80. Vega IE, Hsu SC (2001) The exocyst complex associates with microtubules to mediate vesicle targeting and neurite outgrowth. J Neurosci 21:3839–3848PubMedGoogle Scholar
  81. Walch-Solimena C, Collins RN, Novick PJ (1997) Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J Cell Biol 137:1495–1509PubMedCrossRefGoogle Scholar
  82. Wang S, Liu Y, Adamson CL, Valdez G, Guo W, Hsu SC (2004) The mammalian exocyst, a complex required for exocytosis, inhibits tubulin polymerization. J Biol Chem 279:35958–35966PubMedCrossRefGoogle Scholar
  83. Wang J, Ding Y, Wang J, Hillmer S, Miao Y, Lo SW, Wang X, Robinson DG, Jiang L (2010) EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to cell wall exocytosis in Arabidopsis and tobacco cells. Plant Cell 22(12):4009–4030PubMedCrossRefGoogle Scholar
  84. Waters MG, Hughson FM (2000) Membrane tethering and fusion in the secretory and endocytic pathways. Traffic 1:588–597PubMedCrossRefGoogle Scholar
  85. Wen TJ, Hochholdinger F, Sauer M, Bruce W, Schnable PS (2005) The roothairless1 gene of maize encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol 138:1637–1643PubMedCrossRefGoogle Scholar
  86. Whyte JR, Munro S (2001) The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic. Dev Cell 1:527–537PubMedCrossRefGoogle Scholar
  87. Whyte JR, Munro S (2002) Vesicle tethering complexes in membrane traffic. J Cell Sci 115:2627–2637PubMedGoogle Scholar
  88. Wu S, Mehta SQ, Pichaud F, Bellen HJ, Quiocho FA (2005) Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat Struct Mol Biol 12:879–885PubMedCrossRefGoogle Scholar
  89. Yamashita M, Kurokawa K, Sato Y, Yamagata A, Mimura H, Yoshikawa A, Sato K, Nakano A, Fukai S (2010) Structural basis for the Rho- and phosphoinositide-dependent localization of the exocyst subunit Sec3. Nat Struct Mol Biol 17:180–186PubMedCrossRefGoogle Scholar
  90. Yoshizaki H, Mochizuki N, Gotoh Y, Matsuda M (2007) Akt-PDK1 complex mediates epidermal growth factor-induced membrane protrusion through Ral activation. Mol Biol Cell 18:119–128PubMedCrossRefGoogle Scholar
  91. Zarsky V, Cvrckova F, Potocky M, Hala M (2009) Exocytosis and cell polarity in plants—exocyst and recycling domains. New Phytol 183:255–272PubMedCrossRefGoogle Scholar
  92. Zhang X, Bi E, Novick P, Du L, Kozminski KG, Lipschutz JH, Guo W (2001) Cdc42 interacts with the exocyst and regulates polarized secretion. J Biol Chem 276:46745–46750PubMedCrossRefGoogle Scholar
  93. Zhang XM, Ellis S, Sriratana A, Mitchell CA, Rowe T (2004) Sec15 is an effector for the Rab11 GTPase in mammalian cells. J Biol Chem 279:43027–43034PubMedCrossRefGoogle Scholar
  94. Zhang X, Orlando K, He B, Xi F, Zhang J, Zajac A, Guo W (2008) Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J Cell Biol 180:145–158PubMedCrossRefGoogle Scholar
  95. Zhao Y, Guo W (2009) Sec-ure nanotubes with RalA and exocyst. Nat Cell Biol 11(12):1396–1397PubMedCrossRefGoogle Scholar
  96. Zhao H, Pykalainen A, Lappalainen P (2011) I-BAR domain proteins: linking actin and plasma membrane dynamics. Curr Opin Cell Biol 23:14–21PubMedCrossRefGoogle Scholar
  97. Zuo X, Zhang J, Zhang Y, Hsu SC, Zhou D, Guo W (2006) Exo70 interacts with the Arp2/3 complex and regulates cell migration. Nat Cell Biol 8:1383–1388PubMedCrossRefGoogle Scholar
  98. Zuo X, Guo W, Lipschutz JH (2009) The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol Biol Cell 20:2522–2529PubMedCrossRefGoogle Scholar

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© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA

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