Skip to main content
SpringerLink
Log in

Functions of actin in endocytosis

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Endocytosis is a fundamental eukaryotic process required for remodelling plasma-membrane lipids and protein to ensure appropriate membrane composition. Increasing evidence from a number of cell types reveals that actin plays an active, and often essential, role at key endocytic stages. Much of our current mechanistic understanding of the endocytic process has come from studies in budding yeast and has been facilitated by yeast’s genetic amenability and by technological advances in live cell imaging. While endocytosis in metazoans is likely to be subject to a greater array of regulatory signals, recent reports indicate that spatiotemporal aspects of vesicle formation requiring actin are likely to be conserved across eukaryotic evolution. In this review we focus on the ‘modular’ model of endocytosis in yeast before highlighting comparisons with other cell types. Our discussion is limited to endocytosis involving clathrin as other types of endocytosis have not been demonstrated in yeast.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Roth TF, Porter KR (1964) Yolk protein uptake in the oocyte of the mosquito Aedes aegypti L. J Cell Biol 20:313–332

    PubMed  CAS  Google Scholar 

  2. Perrais D, Merrifield CJ (2005) Dynamics of endocytic vesicle creation. Dev Cell 9:581–592

    PubMed  CAS  Google Scholar 

  3. Roth MG (2006) Clathrin-mediated endocytosis before fluorescent proteins. Nat Rev Mol Cell Biol 7:63–68

    PubMed  CAS  Google Scholar 

  4. Ungewickell EJ, Hinrichsen L (2007) Endocytosis: clathrin-mediated membrane budding. Curr Opin Cell Biol 19:417–425

    PubMed  CAS  Google Scholar 

  5. Adams AEM, Pringle JR (1984) Relationship to actin and tubulin distribution to bud growth in wild type and morphogenetic mutant Saccharomyces cerevisiae. J Cell Biol 98:934–945

    PubMed  CAS  Google Scholar 

  6. Munn AL, Riezman H (1994) Endocytosis is required for the growth of vacuolar H+-ATPase-defective yeast—identification of 6 new End genes. J Cell Biol 127:373–386

    PubMed  CAS  Google Scholar 

  7. Munn AL, Stevenson BJ, Geli MI, Riezman H (1995) End5, End6, and End7—mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol Biol Cell 6:1721–1742

    PubMed  CAS  Google Scholar 

  8. Raths S, Rohrer J, Crausaz F, Riezman H (1993) end3 and end4: two mutants defective in receptor-mediated endocytosis in Saccharomyces cerevisiae. J Cell Biol 120:55–65

    PubMed  CAS  Google Scholar 

  9. Wendland B, McCaffery JM, Xiao Q, Emr SD (1996) A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15. J Cell Biol 135:1485–1500

    PubMed  CAS  Google Scholar 

  10. Benedetti H, Raths S, Crausaz F, Riezman H (1994) The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol Biol Cell 5:1023–1037

    PubMed  CAS  Google Scholar 

  11. Kübler E, Riezman H (1993) Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J 12:2855–2862

    PubMed  Google Scholar 

  12. Geli MI, Riezman H (1996) Role of type I myosins in receptor-mediated endocytosis in yeast. Science 272:533–535

    PubMed  CAS  Google Scholar 

  13. Ayscough KR, Stryker J, Pokala N, Sanders M, Crews P, Drubin DG (1997) High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J Cell Biol 137:399–416

    PubMed  CAS  Google Scholar 

  14. Kaksonen M, Toret CP, Drubin DG (2005) A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123:305–320

    PubMed  CAS  Google Scholar 

  15. Newpher TM, Smith RP, Lemmon V, Lemmon SK (2005) In vivo dynamics of clathrin and its adaptor-dependent recruitment to the actin-based endocytic machinery in yeast. Dev Cell 9:87–98

    PubMed  CAS  Google Scholar 

  16. Ayscough KR (2000) Endocytosis and the development of cell polarity in yeast require a dynamic F-actin cytoskeleton. Curr Biol 10:1587–1590

    PubMed  CAS  Google Scholar 

  17. Doyle T, Botstein D (1996) Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc Natl Acad Sci USA 93:3886–3891

    PubMed  CAS  Google Scholar 

  18. Waddle J, Karpova T, Waterson R, Cooper J (1996) Movement of cortical actin patches in yeast. J Cell Biol 132:861–870

    PubMed  CAS  Google Scholar 

  19. Warren DT, Andrews PD, Gourlay CG, Ayscough KR (2002) Sla1p couples the yeast endocytic machinery to proteins regulating actin dynamics. J Cell Sci 115:1703–1715

    PubMed  CAS  Google Scholar 

  20. Kaksonen M, Sun Y, Drubin DG (2003) A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115:475–487

    PubMed  CAS  Google Scholar 

  21. Galletta BJ, Chuang DY, Cooper JA (2008) Distinct roles for Arp2/3 regulators in actin assembly and endocytosis. PLoS Biol 6:72–85

    CAS  Google Scholar 

  22. Gheorghe DM, Aghamohammadzadeh S, Rooij L, Allwood EG, Winder SJ, Ayscough KR (2008) Interactions between the yeast SM22 homologue Scp1 and actin demonstrate the importance of actin bundling in endocytosis. J Biol Chem 283:15037–15046

    PubMed  CAS  Google Scholar 

  23. Jonsdottir GA, Li R (2004) Dynamics of yeast myosin I: evidence for a possible role in scission of endocytic vesicles. Curr Biol 14:1604–1609

    PubMed  CAS  Google Scholar 

  24. Soulard A, Friant S, Fitterer C, Orange C, Kaneva G, Mirey G, Winsor B (2005) The WASP/Las17p-interacting protein Bzz1p functions with Myo5p in an early stage of endocytosis. Protoplasma 226:89–101

    PubMed  CAS  Google Scholar 

  25. Sun YD, Martin AC, Drubin DG (2006) Endocytic internalization in budding yeast requires coordinated actin nucleation and myosin motor activity. Dev Cell 11:33–46

    PubMed  CAS  Google Scholar 

  26. Gagny B, Wiederkehr A, Dumoulin P, Winsor B, Riezman H, Haguenauer-Tsapis R (2000) A novel EH domain protein of Saccharomyces cerevisiae, Ede1p, involved in endocytosis. J Cell Sci 113:3309–3319

    PubMed  CAS  Google Scholar 

  27. Swanson KA, Hicke L, Radhakrishnan I (2006) Structural basis for monoubiquitin recognition by the Ede1 UBA domain. J Mol Biol 358:713–724

    PubMed  CAS  Google Scholar 

  28. Aguilar RC, Watson HA, Wendland B (2003) The yeast epsin Ent1 is recruited to membranes through multiple independent interactions. J Biol Chem 278:10737–10743

    PubMed  CAS  Google Scholar 

  29. Howard JP, Hutton JL, Olson JM, Payne GS (2002) Sla1p serves as the targeting signal recognition factor for NPFX(1,2)D-mediated endocytosis. J Cell Biol 157:315–326

    PubMed  CAS  Google Scholar 

  30. Liu K, Hua ZL, Nepute JA, Graham TR (2007) Yeast P4-ATPases Drs2p and Dnf1p are essential cargos of the NPFXD/Sla1p endocytic pathway. Mol Biol Cell 18:487–500

    PubMed  CAS  Google Scholar 

  31. Sun Y, Kaksonen M, Maddenr DT, Schekman R, Drubin DG (2005) Interaction of Sla2p’s ANTH domain with PtdIns(4,5)P-2 is important for actin-dependent endocytic internalization. Mol Biol Cell 16:717–730

    PubMed  CAS  Google Scholar 

  32. Sun YD, Carroll S, Kaksonen M, Toshima JY, Drubin DG (2007) Ptdlns(4,5)P-2 turnover is required for multiple stages during clathrin- and actin-dependent endocytic internalization. J Cell Biol 177:355–367

    PubMed  CAS  Google Scholar 

  33. Wendland B, Steece KE, Emr SD (1999) Yeast epsins contain an essential N-terminal ENTH domain, bind clathrin and are required for endocytosis. EMBO J 18:4383–4393

    PubMed  CAS  Google Scholar 

  34. Idrissi FZ, Grotsch H, Fernandez-Golbano IM, Presciatto-Baschong C, Riezman H, Geli MI (2008) Distinct acto/myosin-I structures associate with endocytic profiles at the plasma membrane. J Cell Biol 180:1219–1232

    PubMed  CAS  Google Scholar 

  35. Wesp A, Hicke L, Palecek J, Lombardi R, Aust T, Munn AL, Riezman H (1997) End4p/Sla2p interacts with actin-associated proteins for endocytosis in Saccharomyces cerevisiae. Mol Biol Cell 8:2291–2306

    PubMed  CAS  Google Scholar 

  36. Newpher TM, Lemmon SK (2006) Clathrin is important for normal actin dynamics and progression of Sla2p-containing patches during endocytosis in yeast. Traffic 7:574–588

    PubMed  CAS  Google Scholar 

  37. Gourlay CW, Dewar H, Warren DT, Costa R, Satish N, Ayscough KR (2003) An interaction between Sla1p and Sla2p plays a role in regulating actin dynamics and endocytosis in budding yeast. J Cell Sci 116:2551–2564

    PubMed  CAS  Google Scholar 

  38. Ayscough KR, Eby JJ, Lila T, Dewar H, Kozminski KG, Drubin DG (1999) Sla1p is a functionally modular component of the yeast cortical actin cytoskeleton required for correct localization of both Rho1p-GTPase and Sla2p, a protein with talin homology. Mol Biol Cell 10:1061–1075

    PubMed  CAS  Google Scholar 

  39. Holtzman DA, Yang S, Drubin DG (1993) Synthetic-lethal interactions identify two novel genes, SLA1 and SLA2, that control membrane cytoskeleton assembly in Saccharomyces cerevisiae. J Cell Biol 122:635–644

    PubMed  CAS  Google Scholar 

  40. Rodal AA, Manning AL, Goode BL, Drubin DG (2003) Negative regulation of yeast WASp by two SH3 domain-containing proteins. Curr Biol 13:1000–1008

    PubMed  CAS  Google Scholar 

  41. Kim K, Galletta BJ, Schmidt KO, Chang FS, Blumer KJ, Cooper JA (2006) Actin-based motility during endocytosis in budding yeast. Mol Biol Cell 17:1354–1363

    PubMed  CAS  Google Scholar 

  42. Evangelista M, Klebl BM, Tong AHY, Webb BA, Leeuw T, Leberer E, Whiteway M, Thomas DY, Boone C (2000) A role for myosin-I in actin assembly through interactions with Vrp1p, Bee1p, and the Arp2/3 complex. J Cell Biol 148:353–362

    PubMed  CAS  Google Scholar 

  43. Geli MI, Lombardi R, Schmelzl B, Riezman H (2000) An intact SH3 domain is required for myosin I-induced actin polymerization. EMBO J 19:4281–4291

    PubMed  CAS  Google Scholar 

  44. Thanabalu T, Rajmohan R, Meng L, Ren G, Vajjhala PR, Munn AL (2007) Verprolin function in endocytosis and actin organization—roles of the Las17p (yeast WASP)-binding domain and a novel C-terminal actin-binding domain. FEBS J 274:4103–4125

    PubMed  CAS  Google Scholar 

  45. Duncan MC, Cope M, Goode BL, Wendland B, Drubin DG (2001) Yeast Eps15-like endocytic protein, Pan1p, activates the Arp2/3 complex. Nat Cell Biol 3:687–690

    PubMed  CAS  Google Scholar 

  46. Goode BL, Rodal AA, Barnes G, Drubin DG (2001) Activation of the Arp2/3 complex by the actin filament binding protein Abp1p. J Cell Biol 153:627–634

    PubMed  CAS  Google Scholar 

  47. Chang FS, Han GS, Carman GM, Blumer KJ (2005) A WASp-binding type II phosphatidylinositol 4-kinase required for actin polymerization-driven endosome motility. J Cell Biol 171:133–142

    PubMed  CAS  Google Scholar 

  48. Dewar H, Warren DT, Gardiner FC, Gourlay CG, Satish N, Richardson MR, Andrews PD, Ayscough KR (2002) Novel proteins linking the actin cytoskeleton to the endocytic machinery in Saccharomyces cerevisiae. Mol Biol Cell 13:3646–3661

    PubMed  CAS  Google Scholar 

  49. Madania A, Dumoulin P, Grava S, Kitamoto H, Scharer-Brodbeck C, Soulard A, Moreau V, Winsor B (1999) The Saccharomyces cerevisiae homologue of human Wiskott–Aldrich syndrome protein Las17p interacts with the Arp2/3 complex. Mol Biol Cell 10:3521–3538

    PubMed  CAS  Google Scholar 

  50. Robertson AS, Allwood EG, Smith AP, Gardiner FC, Costa R, Winder SJ, Ayscough KR (2009) The WASP homolog Las17 activates the novel actin-regulatory activity of Ysc84 to promote endocytosis in yeast. Mol Biol Cell 20:1618–1628

    PubMed  CAS  Google Scholar 

  51. Huckaba TM, Gay AC, Pantalena LF, Yang HC, Pon LA (2004) Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae. J Cell Biol 167:519–530

    PubMed  CAS  Google Scholar 

  52. Okreglak V, Drubin DG (2007) Cofilin recruitment and function during actin-mediated endocytosis dictated by actin nucleotide state. J Cell Biol 178:1251–1264

    PubMed  CAS  Google Scholar 

  53. Amatruda JF, Cannon JF, Tatchell K, Hug C, Cooper JA (1990) Disruption of the actin cytoskeleton in yeast capping protein mutants. Nature 344:352–354

    PubMed  CAS  Google Scholar 

  54. Adams AEM, Botstein D, Drubin DG (1991) Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature 354:404–408

    PubMed  CAS  Google Scholar 

  55. Goodman A, Goode BL, Matsudaira P, Fink GR (2003) The Saccharomyces cerevisiae calponin/transgelin homolog Scp1 functions with fimbrin to regulate stability and organization of the actin cytoskeleton. Mol Biol Cell 14:2617–2629

    PubMed  CAS  Google Scholar 

  56. Winder SJ, Jess T, Ayscough KR (2003) SCP1 encodes an actin-bundling protein in yeast. Biochem J 375:287–295

    PubMed  CAS  Google Scholar 

  57. Lappalainen P, Fedorov EV, Fedorov AA, Almo SC, Drubin DG (1997) Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO J 16:5520–5530

    PubMed  CAS  Google Scholar 

  58. Moon AL, Janmey PA, Louie A, Drubin DG (1993) Cofilin is an essential component of the yeast cortical actin cytoskeleton. J Cell Biol 120:421–435

    PubMed  CAS  Google Scholar 

  59. Balcer HI, Goodman AL, Rodal AA, Smith E, Kugler J, Heuser JE, Goode BL (2003) Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aip1. Curr Biol 13:2159–2169

    PubMed  CAS  Google Scholar 

  60. Song BD, Schmid SL (2003) A molecular motor or a regulator? Dynamin’s in a class of its own. Biochemistry 42:1369–1376

    PubMed  CAS  Google Scholar 

  61. Yu XW, Cai MJ (2004) The yeast dynamin-related GTPase Vps1p functions in the organization of the actin cytoskeleton via interaction with Sla1p. J Cell Sci 117:3839–3853

    PubMed  CAS  Google Scholar 

  62. Gammie AE, Kurihara LJ, Vallee RB, Rose MD (1995) Dnm1, a Dynamin-related gene, participates in endosomal trafficking in yeast. J Cell Biol 130:553–566

    PubMed  CAS  Google Scholar 

  63. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJG, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495–499

    PubMed  CAS  Google Scholar 

  64. Drees BL, Sundin B, Brazeau E, Caviston JP, Chen GC, Guo W, Kozminski KG, Lau MW, Moskow JJ, Tong A, Schenkman LR, McKenzie A, Brennwald P, Longtine M, Bi E, Chan C, Novick P, Boone C, Pringle JR, Davis TN, Fields S, Drubin DG (2001) A protein interaction map for cell polarity development. J Cell Biol 154:549–571

    PubMed  CAS  Google Scholar 

  65. Lombardi R, Riezman H (2001) Rvs161p and Rvs167p, the two yeast amphiphysin homologs, function together in vivo. J Biol Chem 276:6016–6022

    PubMed  CAS  Google Scholar 

  66. Girao H, Geli MI, Idrissi FZ (2008) Actin in the endocytic pathway: from yeast to mammals. FEBS Lett 582:2112–2119

    PubMed  CAS  Google Scholar 

  67. Mulholland J, Preuss D, Moon A, Wong A, Drubin D, Botstein D (1994) Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J Cell Biol 125:381–391

    PubMed  CAS  Google Scholar 

  68. Smythe E, Ayscough KR (2003) The Ark1/Prk1 family of protein kinases—regulators of endocytosis and the actin cytoskeleton. EMBO Rep 4:246–251

    PubMed  CAS  Google Scholar 

  69. Cope M, Yang S, Shang C, Drubin DG (1999) Novel protein kinases Ark1p and Prk1p associate with and regulate the cortical actin cytoskeleton in budding yeast. J Cell Biol 144:1203–1218

    PubMed  CAS  Google Scholar 

  70. Watson HA, Cope M, Groen AC, Drubin DG, Wendland B (2001) In vivo role for actin-regulating kinases in endocytosis and yeast epsin phosphorylation. Mol Biol Cell 12:3668–3679

    PubMed  CAS  Google Scholar 

  71. Zeng GH, Yu XW, Cai MJ (2001) Regulation of yeast actin cytoskeleton-regulatory complex Pan1p/Sla1p/End3p by serine/threonine kinase Prk1p. Mol Biol Cell 12:3759–3772

    PubMed  CAS  Google Scholar 

  72. Stefan CJ, Padilla SM, Audhya A, Emr SD (2005) The phosphoinositide phosphatase Sjl2 is recruited to cortical actin patches in the control of vesicle formation and fission during endocytosis. Mol Cell Biol 25:2910–2923

    PubMed  CAS  Google Scholar 

  73. Toshima J, Toshima JY, Martin AC, Drubin DG (2005) Phosphoregulation of Arp2/3-dependent actin assembly during receptor-mediated endocytosis. Nat Cell Biol 7:246–254

    PubMed  CAS  Google Scholar 

  74. Toret CP, Lee L, Sekiya-Kawasaki M, Drubin DG (2008) Multiple pathways regulate endocytic coat disassembly in Saccharomyces cerevisiae for optimal downstream trafficking. Traffic 9:848–859

    PubMed  CAS  Google Scholar 

  75. Lambrechts A, Gevaert K, Cossart P, Vandekerckhove J, Van Troys M (2008) Listeria comet tails: the actin-based motility machinery at work. Trends Cell Biol 18:220–227

    PubMed  CAS  Google Scholar 

  76. Toshima JY, Toshima J, Kaksonen M, Martin AC, King DS, Drubin DG (2006) Spatial dynamics of receptor-mediated endocytic trafficking in budding yeast revealed by using fluorescent alpha-factor derivatives. Proc Natl Acad Sci USA 103:5793–5798

    PubMed  CAS  Google Scholar 

  77. Yoshiuchi S, Yamamoto T, Sakane H, Kadota J, Mochida J, Asaka M, Tanaka K (2006) Identification of novel mutations in ACT1 and SLA2 that suppress the actin-cable-overproducing phenotype caused by overexpression of a dominant active form of Bni1p in Saccharomyces cerevisiae. Genetics 173:527–539

    PubMed  CAS  Google Scholar 

  78. Aikawa Y, Martin TFJ (2005) GTPases regulating membrane dynamics, vol 404. Academic Press, London, pp 422-431

    Google Scholar 

  79. Klein S, Franco M, Chardin P, Luton F (2006) Role of the Arf6 GDP/GTP cycle and Arf6 GTPase-activating proteins in actin remodeling and intracellular transport. J Biol Chem 281:12352–12361

    PubMed  CAS  Google Scholar 

  80. Gillingham AK, Munro S (2007) Identification of a guanine nucleotide exchange factor for Arf3, the yeast orthologue of mammalian Arf6. PLoS ONE 2:e842

    PubMed  Google Scholar 

  81. Smaczynska-de Rooij II, Costa R, Ayscough KR (2008) Yeast Arf3p modulates plasma membrane Ptdlns(4,5)P2 levels to facilitate endocytosis. Traffic 9:559–573

    PubMed  CAS  Google Scholar 

  82. Lambert AA, Perron MP, Lavoie E, Pallotta D (2007) The Saccharomyces cerevisiae Arf3 protein is involved in actin cable and cortical patch formation. FEMS Yeast Res 7:782–795

    PubMed  CAS  Google Scholar 

  83. Qualmann B, Kessels MM (2002) Endocytosis and the cytoskeleton. Int Rev Cytol 220:93–144

    PubMed  CAS  Google Scholar 

  84. Shupliakov O, Bloom O, Gustafsson JS, Kjaerulff O, Low P, Tomilin N, Pieribone VA, Greengard P, Brodin L (2002) Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc Natl Acad Sci USA 99:14476–14481

    PubMed  CAS  Google Scholar 

  85. Fujimoto LM, Roth R, Heuser JE, Schmid SL (2000) Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 1:161–171

    PubMed  CAS  Google Scholar 

  86. Merrifield CJ (2004) Seeing is believing: imaging actin dynamics at single sites of endocytosis. Trends Cell Biol 14:352–358

    PubMed  CAS  Google Scholar 

  87. Merrifield CJ, Feldman ME, Wan L, Almers W (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4:691–698

    PubMed  CAS  Google Scholar 

  88. Merrifield CJ, Perrais D, Zenisek D (2005) Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121:593–606

    PubMed  CAS  Google Scholar 

  89. Schmid SL, Smythe E (1991) Stage-specific assays for coated pit formation and coated vesicle budding in vitro. J Cell Biol 114:869–880

    PubMed  CAS  Google Scholar 

  90. Yarar D, Waterman-Storer CM, Schmid SL (2005) A dynamic actin cytoskeleton functions at multiple stages of clathrin-mediated endocytosis. Mol Biol Cell 16:964–975

    PubMed  CAS  Google Scholar 

  91. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, De Camilli P (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell 9:791–804

    PubMed  CAS  Google Scholar 

  92. Tsujita K, Suetsugu S, Sasaki N, Furutani M, Oikawa T, Takenawa T (2006) Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J Cell Biol 172:269–279

    PubMed  CAS  Google Scholar 

  93. Takano K, Toyooka K, Suetsugu S (2008) EFC/F-BAR proteins and the N-WASP-WIP complex induce membrane curvature-dependent actin polymerization. EMBO J 27:2817–2828

    PubMed  CAS  Google Scholar 

  94. Rocca DL, Martin S, Jenkins EL, Hanley JG (2008) Inhibition of Arp2/3-mediated actin polymerization by PICK1 regulates neuronal morphology and AMPA receptor endocytosis. Nat Cell Biol 10:259–271

    PubMed  CAS  Google Scholar 

  95. Kessels MM, Engqvist-Goldstein AE, Drubin DG, Qualmann B (2001) Mammalian Abp1, a signal-responsive F-actin-binding protein, links the actin cytoskeleton to endocytosis via the GTPase dynamin. J Cell Biol 153:351–366

    PubMed  CAS  Google Scholar 

  96. Han J, Shui JW, Zhang X, Zheng B, Han S, Tan TH (2005) HIP-55 is important for T-cell proliferation, cytokine production, and immune responses. Mol Cell Biol 25:6869–6878

    PubMed  CAS  Google Scholar 

  97. Connert S, Wienand S, Thiel C, Krikunova M, Glyvuk N, Tsytsyura Y, Hilfiker-Kleiner D, Bartsch JW, Klingauf J, Wienands J (2006) SH3P7/mAbp1 deficiency leads to tissue and behavioral abnormalities and impaired vesicle transport. EMBO J 25:1611–1622

    PubMed  CAS  Google Scholar 

  98. Engqvist-Goldstein AE, Drubin DG (2003) Actin assembly and endocytosis: from yeast to mammals. Annu Rev Cell Dev Biol 19:287–332

    PubMed  CAS  Google Scholar 

  99. Chen CY, Brodsky FM (2005) Huntingtin-interacting protein 1 (Hip1) and Hip1-related protein (Hip1R) bind the conserved sequence of clathrin light chains and thereby influence clathrin assembly in vitro and actin distribution in vivo. J Biol Chem 280:6109–6117

    PubMed  CAS  Google Scholar 

  100. Legendre-Guillemin V, Metzler M, Lemaire JF, Philie J, Gan L, Hayden MR, McPherson PS (2005) Huntingtin interacting protein 1 (HIP1) regulates clathrin assembly through direct binding to the regulatory region of the clathrin light chain. J Biol Chem 280:6101–6108

    PubMed  CAS  Google Scholar 

  101. Engqvist-Goldstein AE, Zhang CX, Carreno S, Barroso C, Heuser JE, Drubin DG (2004) RNAi-mediated Hip1R silencing results in stable association between the endocytic machinery and the actin assembly machinery. Mol Biol Cell 15:1666–1679

    PubMed  CAS  Google Scholar 

  102. Wilbur JD, Chen CY, Manalo V, Hwang PK, Fletterick RJ, Brodsky FM (2008) Actin binding by Hip1 (Huntingtin-interacting protein 1) and Hip1R (Hip1-related protein) is regulated by clathrin light chain. J Biol Chem 283:32870–32879

    PubMed  CAS  Google Scholar 

  103. Ammer AG, Weed SA (2008) Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil Cytoskeleton 65:687–707

    PubMed  CAS  Google Scholar 

  104. Le Clainche C, Pauly BS, Zhang CX, Engqvist-Goldstein AE, Cunningham K, Drubin DG (2007) A Hip1R-cortactin complex negatively regulates actin assembly associated with endocytosis. EMBO J 26:1199–1210

    PubMed  Google Scholar 

  105. Zhu J, Yu D, Zeng XC, Zhou K, Zhan X (2007) Receptor-mediated endocytosis involves tyrosine phosphorylation of cortactin. J Biol Chem 282:16086–16094

    PubMed  CAS  Google Scholar 

  106. Merrifield CJ, Qualmann B, Kessels MM, Almers W (2004) Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited to sites of clathrin-mediated endocytosis in cultured fibroblasts. Eur J Cell Biol 83:13–18

    PubMed  CAS  Google Scholar 

  107. Benesch S, Polo S, Lai FP, Anderson KI, Stradal TE, Wehland J, Rottner K (2005) N-WASP deficiency impairs EGF internalization and actin assembly at clathrin-coated pits. J Cell Sci 118:3103–3115

    PubMed  CAS  Google Scholar 

  108. Innocenti M, Gerboth S, Rottner K, Lai FP, Hertzog M, Stradal TE, Frittoli E, Didry D, Polo S, Disanza A, Benesch S, Di Fiore PP, Carlier MF, Scita G (2005) Abi1 regulates the activity of N-WASP and WAVE in distinct actin-based processes. Nat Cell Biol 7:969–976

    PubMed  CAS  Google Scholar 

  109. Kessels MM, Qualmann B (2006) Syndapin oligomers interconnect the machineries for endocytic vesicle formation and actin polymerization. J Biol Chem 281:13285–13299

    PubMed  CAS  Google Scholar 

  110. Shin N, Ahn N, Chang-Ileto B, Park J, Takei K, Ahn SG, Kim SA, Di Paolo G, Chang S (2008) SNX9 regulates tubular invagination of the plasma membrane through interaction with actin cytoskeleton and dynamin 2. J Cell Sci 121:1252–1263

    PubMed  CAS  Google Scholar 

  111. Yarar D, Waterman-Storer CM, Schmid SL (2007) SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev Cell 13:43–56

    PubMed  CAS  Google Scholar 

  112. Kochubey O, Majumdar A, Klingauf J (2006) Imaging clathrin dynamics in Drosophila melanogaster hemocytes reveals a role for actin in vesicle fission. Traffic 7:1614–1627

    PubMed  CAS  Google Scholar 

  113. Sokac AM, Wieschaus E (2008) Local actin-dependent endocytosis is zygotically controlled to initiate Drosophila cellularization. Dev Cell 14:775–786

    PubMed  CAS  Google Scholar 

  114. Bruck S, Huber TB, Ingham RJ, Kim K, Niederstrasser H, Allen PM, Pawson T, Cooper JA, Shaw AS (2006) Identification of a novel inhibitory actin capping protein binding motif in CD2 associated protein. J Biol Chem 281(28):19196–19203

    PubMed  CAS  Google Scholar 

  115. Dikic I (2002) CIN85/CMS family of adaptor molecules. FEBS Lett 529:110–115

    PubMed  CAS  Google Scholar 

  116. Kowanetz K, Husnjak K, Holler D, Kowanetz M, Soubeyran P, Hirsch D, Schmidt MH, Pavelic K, De Camilli P, Randazzo PA, Dikic I (2004) CIN85 associates with multiple effectors controlling intracellular trafficking of epidermal growth factor receptors. Mol Biol Cell 15:3155–3166

    PubMed  CAS  Google Scholar 

  117. Cormont M, Meton I, Mari M, Monzo P, Keslair F, Gaskin C, McGraw TE, Le Marchand-Brustel Y (2003) CD2AP/CMS regulates endosome morphology and traffic to the degradative pathway through its interaction with Rab4 and c-Cbl. Traffic 4:97–112

    PubMed  CAS  Google Scholar 

  118. Hutchings NJ, Clarkson N, Chalkley R, Barclay AN, Brown MH (2003) Linking the T cell surface protein CD2 to the actin-capping protein CAPZ via CMS and CIN85. J Biol Chem 278:22396–22403

    PubMed  CAS  Google Scholar 

  119. Petrelli A, Gilestro GF, Lanzardo S, Comoglio PM, Migone N, Giordano S (2002) The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature 416:187–190

    PubMed  CAS  Google Scholar 

  120. Soubeyran P, Kowanetz K, Szymkiewicz I, Langdon WY, Dikic I (2002) Cbl-CIN85-endophilin complex mediates ligand-induced downregulation of EGF receptors. Nature 416:183–187

    PubMed  CAS  Google Scholar 

  121. Lynch DK, Winata SC, Lyons RJ, Hughes WE, Lehrbach GM, Wasinger V, Corthals G, Cordwell S, Daly RJ (2003) A Cortactin-CD2-associated protein (CD2AP) complex provides a novel link between epidermal growth factor receptor endocytosis and the actin cytoskeleton. J Biol Chem 278:21805–21813

    PubMed  CAS  Google Scholar 

  122. Sabharanjak S, Sharma P, Parton RG, Mayor S (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2:411–423

    PubMed  CAS  Google Scholar 

  123. Gauthier NC, Monzo P, Gonzalez T, Doye A, Oldani A, Gounon P, Ricci V, Cormont M, Boquet P (2007) Early endosomes associated with dynamic F-actin structures are required for late trafficking of H. pylori VacA toxin. J Cell Biol 177:343–354

    PubMed  CAS  Google Scholar 

  124. Chadda R, Howes MT, Plowman SJ, Hancock JF, Parton RG, Mayor S (2007) Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 8:702–717

    PubMed  CAS  Google Scholar 

  125. Soulet F, Yarar D, Leonard M, Schmid SL (2005) SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol Biol Cell 16:2058–2067

    PubMed  CAS  Google Scholar 

  126. Lundmark R, Carlsson SR (2003) Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. J Biol Chem 278:46772–46781

    PubMed  CAS  Google Scholar 

  127. Lladó A, Timpson P, Vilà de Muga S, Moretó J, Pol A, Grewal T, Daly RJ, Enrich C, Tebar F (2008) Protein kinase Cdelta and calmodulin regulate epidermal growth factor receptor recycling from early endosomes through Arp2/3 complex and cortactin. Mol Biol Cell 19:17–29

    PubMed  Google Scholar 

  128. Rodal AA, Motola-Barnes RN, Littleton JT (2008) Nervous wreck and Cdc42 cooperate to regulate endocytic actin assembly during synaptic growth. J Neurosci 28:8316–8325

    PubMed  CAS  Google Scholar 

  129. Maldonado-Baez L, Dores MR, Perkins EM, Drivas TG, Hicke L, Wendland B (2008) Interaction between epsin/Yap180 adaptors and the scaffolds Ede1/Pan1 is required for endocytosis Mol. Biol Cell 19:2936–2948

    CAS  Google Scholar 

  130. Wendland B, Emr SD (1998) Pan1p, yeast eps15, functions as a multivalent adaptor that coordinates protein-protein interactions essential for endocytosis. J Cell Biol 141:71–84

    PubMed  CAS  Google Scholar 

  131. Cope M, Yang S, Shang C, Drubin DG (1999) Novel protein kinases Ark1p and Prk1p associate with and regulate the cortical actin cytoskeleton in budding yeast J. Cell Biol 144:1203–1218

    CAS  Google Scholar 

  132. Zeng GS, Cai MJ (1999) Regulation of the actin cytoskeleton organization in yeast by a novel serine/threonine kinase Prk1p J. Cell Biol 144:71–82

    CAS  Google Scholar 

  133. Hussain NK, Jenna S, Glogauer M, Quinn CC, Wasiak S, Guipponi M, Antonarakis SE, Kay BK, Stossel TP, Lamarche-Vane N, McPherson PS (2001) Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WASP. Nat Cell Biol 3:927–932

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Soheil Aghamohammadzadeh and Alison Motley for critical reading of the manuscript. AR is supported by a BBSRC studentship, work in the ES lab is supported by a programme grant from the MRC (G0300452). KRA is a senior MRC non-clinical fellow (G0601600).

Author information

Authors and Affiliations

  1. Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Court, Western Bank, Sheffield, S10 2TN, UK

    Alastair S. Robertson & Kathryn R. Ayscough

  2. Department of Biomedical Science, University of Sheffield, Firth Court, Western Bank, Sheffield, S10 2TN, UK

    Elizabeth Smythe

Authors
  1. Alastair S. Robertson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elizabeth Smythe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kathryn R. Ayscough
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kathryn R. Ayscough.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Robertson, A.S., Smythe, E. & Ayscough, K.R. Functions of actin in endocytosis. Cell. Mol. Life Sci. 66, 2049–2065 (2009). https://doi.org/10.1007/s00018-009-0001-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-009-0001-y

Keywords

Search

Navigation