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Intimate and Facultative? Regulation of Clathrin-Mediated Endocytosis by the Actin Cytoskeleton

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Vesicle Trafficking in Cancer

Abstract

Clathrin-mediated endocytosis (CME) involves the timely coordination of plasma membrane deformation, clathrin coat assembly, and cargo inclusion. CME culminates with vesicle release through membrane scission, followed by internalization and uncoating en route to the endosome. The biochemical and biophysical requirements of CME are supplied by a broad number of regulators, many of which bind actin and/or modify actin dynamics. The multidomain structure of these regulators enables their integration into signal-based cellular programs. The architecture and dynamic nature of the actin cytoskeleton establish its influence on distinct aspects of CME, ranging from membrane compartmentalization and acquisition of membrane curvature to coated pit invagination and vesicle movement. However, in mammalian cells, the regulation of CME by the actin cytoskeleton may be facultative, as CME still occurs, in certain cellular contexts, in the absence of actin polymerization. This chapter addresses the complexity of CME regulation by actin and expands on the role of membrane compartmentalization on the spatial organization of clathrin-coated pits and on the multiplicity of differently structured regulators of actin dynamics at the coated pit.

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References

  1. Scita G, Di Fiore PP (2010) The endocytic matrix. Nature 463:464–473

    Article  PubMed  CAS  Google Scholar 

  2. Le Roy C, Wrana JL (2005) Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 6:112–126

    Article  PubMed  CAS  Google Scholar 

  3. Sigismund S, Confalonieri S, Ciliberto A, Polo S, Scita G et al (2012) Endocytosis and signaling: cell logistics shape the eukaryotic cell plan. Physiol Rev 92:273–366

    Article  PubMed  CAS  Google Scholar 

  4. Pelkmans L, Fava E, Grabner H, Hannus M, Habermann B et al (2005) Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436:78–86

    Article  PubMed  CAS  Google Scholar 

  5. Mosesson Y, Mills GB, Yarden Y (2008) Derailed endocytosis: an emerging feature of cancer. Nat Rev Cancer 8:835–850

    Article  PubMed  CAS  Google Scholar 

  6. Lanzetti L, Di Fiore PP (2008) Endocytosis and cancer: an ‘insider’ network with dangerous liaisons. Traffic 9:2011–2021

    Article  PubMed  CAS  Google Scholar 

  7. Lamaze C, Fujimoto LM, Yin HL, Schmid SL (1997) The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J Biol Chem 272:20332–20335

    Article  PubMed  CAS  Google Scholar 

  8. Gottlieb TA, Ivanov IE, Adesnik M, Sabatini DD (1993) Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol 120:695–710

    Article  PubMed  CAS  Google Scholar 

  9. Jackman MR, Shurety W, Ellis JA, Luzio JP (1994) Inhibition of apical but not basolateral endocytosis of ricin and folate in Caco-2 cells by cytochalasin D. J Cell Sci 107(pt 9): 2547–2556

    PubMed  CAS  Google Scholar 

  10. Altschuler Y, Liu S, Katz L, Tang K, Hardy S et al (1999) ADP-ribosylation factor 6 and endocytosis at the apical surface of Madin-Darby canine kidney cells. J Cell Biol 147:7–12

    Article  PubMed  CAS  Google Scholar 

  11. Shurety W, Bright NA, Luzio JP (1996) The effects of cytochalasin D and phorbol myristate acetate on the apical endocytosis of ricin in polarised Caco-2 cells. J Cell Sci 109(pt 12):2927–2935

    PubMed  CAS  Google Scholar 

  12. Hyman T, Shmuel M, Altschuler Y (2006) Actin is required for endocytosis at the apical surface of Madin-Darby canine kidney cells where ARF6 and clathrin regulate the actin cytoskeleton. Mol Biol Cell 17:427–437

    Article  PubMed  CAS  Google Scholar 

  13. 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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  15. Toret CP, Drubin DG (2006) The budding yeast endocytic pathway. J Cell Sci 119:4585–4587

    Article  PubMed  CAS  Google Scholar 

  16. Robertson AS, Smythe E, Ayscough KR (2009) Functions of actin in endocytosis. Cell Mol Life Sci 66:2049–2065

    Article  PubMed  CAS  Google Scholar 

  17. Taylor MJ, Perrais D, Merrifield CJ (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9:e1000604

    Article  PubMed  CAS  Google Scholar 

  18. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K et al (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118:591–605

    Article  PubMed  CAS  Google Scholar 

  19. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-­mediated endocytosis. Nat Rev Mol Cell Biol 12:517–533

    Article  PubMed  CAS  Google Scholar 

  20. Loerke D, Mettlen M, Yarar D, Jaqaman K, Jaqaman H et al (2009) Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol 7:e57

    Article  PubMed  CAS  Google Scholar 

  21. Cao H, Chen J, Krueger EW, McNiven MA (2010) SRC-mediated phosphorylation of dynamin and cortactin regulates the “constitutive” endocytosis of transferrin. Mol Cell Biol 30:781–792

    Article  PubMed  CAS  Google Scholar 

  22. Doyon JB, Zeitler B, Cheng J, Cheng AT, Cherone JM et al (2011) Rapid and efficient clathrin-­mediated endocytosis revealed in genome-edited mammalian cells. Nat Cell Biol 13:331–337

    Article  PubMed  CAS  Google Scholar 

  23. Kusumi A, Suzuki KG, Kasai RS, Ritchie K, Fujiwara TK (2011) Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem Sci 36:604–615

    Article  PubMed  CAS  Google Scholar 

  24. Ritchie K, Shan XY, Kondo J, Iwasawa K, Fujiwara T et al (2005) Detection of non-­Brownian diffusion in the cell membrane in single molecule tracking. Biophys J 88:2266–2277

    Article  PubMed  CAS  Google Scholar 

  25. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 157:1071–1081

    Article  PubMed  CAS  Google Scholar 

  26. Sako Y, Kusumi A (1995) Barriers for lateral diffusion of transferrin receptor in the plasma membrane as characterized by receptor dragging by laser tweezers: fence versus tether. J Cell Biol 129:1559–1574

    Article  PubMed  CAS  Google Scholar 

  27. Golebiewska U, Kay JG, Masters T, Grinstein S, Im W et al (2011) Evidence for a fence that impedes the diffusion of phosphatidylinositol 4,5-bisphosphate out of the forming phagosomes of macrophages. Mol Biol Cell 22:3498–3507

    Article  PubMed  CAS  Google Scholar 

  28. Chaudhuri A, Bhattacharya B, Gowrishankar K, Mayor S, Rao M (2011) Spatiotemporal regulation of chemical reactions by active cytoskeletal remodeling. Proc Natl Acad Sci U S A 108:14825–14830

    Article  PubMed  CAS  Google Scholar 

  29. Kalay Z, Fujiwara TK, Kusumi A (2012) Confining domains lead to reaction bursts: reaction kinetics in the plasma membrane. PLoS One 7:e32948

    Article  PubMed  CAS  Google Scholar 

  30. Plowman SJ, Muncke C, Parton RG, Hancock JF (2005) H-ras, K-ras, and inner plasma membrane raft proteins operate in nanoclusters with differential dependence on the actin cytoskeleton. Proc Natl Acad Sci U S A 102:15500–15505

    Article  PubMed  CAS  Google Scholar 

  31. Henis YI, Hancock JF, Prior IA (2009) Ras acylation, compartmentalization and signaling nanoclusters (review). Mol Membr Biol 26:80–92

    Article  PubMed  CAS  Google Scholar 

  32. Zhai RG, Bellen HJ (2004) The architecture of the active zone in the presynaptic nerve terminal. Physiology (Bethesda) 19:262–270

    Article  Google Scholar 

  33. Yu HY, Bement WM (2007) Control of local actin assembly by membrane fusion-dependent compartment mixing. Nat Cell Biol 9:149–159

    Article  PubMed  CAS  Google Scholar 

  34. Villanueva J, Torregrosa-Hetland CJ, Garcia-Martinez V, Del Mar Frances M, Viniegra S et al (2012) The F-actin cortex in chromaffin granule dynamics and fusion: a minireview. J Mol Neurosci 48(2):323–327

    Article  PubMed  CAS  Google Scholar 

  35. Walther TC, Brickner JH, Aguilar PS, Bernales S, Pantoja C et al (2006) Eisosomes mark static sites of endocytosis. Nature 439:998–1003

    Article  PubMed  CAS  Google Scholar 

  36. Brach T, Specht T, Kaksonen M (2011) Reassessment of the role of plasma membrane domains in the regulation of vesicular traffic in yeast. J Cell Sci 124:328–337

    Article  PubMed  CAS  Google Scholar 

  37. Gaidarov I, Santini F, Warren RA, Keen JH (1999) Spatial control of coated-pit dynamics in living cells. Nat Cell Biol 1:1–7

    Article  PubMed  CAS  Google Scholar 

  38. Bennett EM, Chen CY, Engqvist-Goldstein AE, Drubin DG, Brodsky FM (2001) Clathrin hub expression dissociates the actin-binding protein Hip1R from coated pits and disrupts their alignment with the actin cytoskeleton. Traffic 2:851–858

    Article  PubMed  CAS  Google Scholar 

  39. 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

    Article  PubMed  CAS  Google Scholar 

  40. Heuser J (1980) Three-dimensional visualization of coated vesicle formation in fibroblasts. J Cell Biol 84:560–583

    Article  PubMed  CAS  Google Scholar 

  41. Bellve KD, Leonard D, Standley C, Lifshitz LM, Tuft RA et al (2006) Plasma membrane domains specialized for clathrin-mediated endocytosis in primary cells. J Biol Chem 281:16139–16146

    Article  PubMed  CAS  Google Scholar 

  42. 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

    Article  PubMed  CAS  Google Scholar 

  43. Boucrot E, Saffarian S, Massol R, Kirchhausen T, Ehrlich M (2006) Role of lipids and actin in the formation of clathrin-coated pits. Exp Cell Res 312:4036–4048

    Article  PubMed  CAS  Google Scholar 

  44. Santini F, Gaidarov I, Keen JH (2002) G protein-coupled receptor/arrestin3 modulation of the endocytic machinery. J Cell Biol 156:665–676

    Article  PubMed  CAS  Google Scholar 

  45. Nunez D, Antonescu C, Mettlen M, Liu A, Schmid SL et al (2011) Hotspots organize clathrin-­mediated endocytosis by efficient recruitment and retention of nucleating resources. Traffic 12:1868–1878

    Article  PubMed  CAS  Google Scholar 

  46. Cao H, Krueger EW, McNiven MA (2011) Hepatocytes internalize trophic receptors at large endocytic “Hot Spots”. Hepatology 54:1819–1829

    Article  PubMed  CAS  Google Scholar 

  47. Maupin P, Pollard TD (1983) Improved preservation and staining of HeLa cell actin filaments, clathrin-coated membranes, and other cytoplasmic structures by tannic acid-­glutaraldehyde-saponin fixation. J Cell Biol 96:51–62

    Article  PubMed  CAS  Google Scholar 

  48. Akisaka T, Yoshida H, Suzuki R, Shimizu K, Takama K (2003) Clathrin sheets on the protoplasmic surface of ventral membranes of osteoclasts in culture. J Electron Microsc (Tokyo) 52:535–543

    Article  CAS  Google Scholar 

  49. Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG (2009) Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 187:733–747

    Article  PubMed  CAS  Google Scholar 

  50. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C et al (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10:839–850

    Article  PubMed  CAS  Google Scholar 

  51. Teckchandani A, Toida N, Goodchild J, Henderson C, Watts J et al (2009) Quantitative proteomics identifies a Dab2/integrin module regulating cell migration. J Cell Biol 186:99–111

    Article  PubMed  CAS  Google Scholar 

  52. Nishimura T, Kaibuchi K (2007) Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev Cell 13:15–28

    Article  PubMed  CAS  Google Scholar 

  53. Chetrit D, Ziv N, Ehrlich M (2009) Dab2 regulates clathrin assembly and cell spreading. Biochem J 418:701–715

    Article  PubMed  CAS  Google Scholar 

  54. Saffarian S, Cocucci E, Kirchhausen T (2009) Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 7:e1000191

    Article  PubMed  CAS  Google Scholar 

  55. Taylor MJ, Lampe M, Merrifield CJ (2012) A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLoS Biol 10:e1001302

    Article  PubMed  CAS  Google Scholar 

  56. 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

    Article  PubMed  CAS  Google Scholar 

  57. 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

    Article  PubMed  CAS  Google Scholar 

  58. Mettlen M, Stoeber M, Loerke D, Antonescu CN, Danuser G et al (2009) Endocytic accessory proteins are functionally distinguished by their differential effects on the maturation of clathrin-coated pits. Mol Biol Cell 20:3251–3260

    Article  PubMed  CAS  Google Scholar 

  59. Janmey PA, Weitz DA (2004) Dealing with mechanics: mechanisms of force transduction in cells. Trends Biochem Sci 29:364–370

    Article  PubMed  CAS  Google Scholar 

  60. Batchelder EM, Yarar D (2010) Differential requirements for clathrin-dependent endocytosis at sites of cell-substrate adhesion. Mol Biol Cell 21:3070–3079

    Article  PubMed  CAS  Google Scholar 

  61. Liu AP, Loerke D, Schmid SL, Danuser G (2009) Global and local regulation of clathrin-­coated pit dynamics detected on patterned substrates. Biophys J 97:1038–1047

    Article  PubMed  CAS  Google Scholar 

  62. Dalby MJ, Berry CC, Riehle MO, Sutherland DS, Agheli H et al (2004) Attempted endocytosis of nano-environment produced by colloidal lithography by human fibroblasts. Exp Cell Res 295:387–394

    Article  PubMed  CAS  Google Scholar 

  63. Aghamohammadzadeh S, Ayscough KR (2009) Differential requirements for actin during yeast and mammalian endocytosis. Nat Cell Biol 11:1039–1042

    Article  PubMed  CAS  Google Scholar 

  64. Boulant S, Kural C, Zeeh JC, Ubelmann F, Kirchhausen T (2011) Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 13:1124–1131

    Article  PubMed  CAS  Google Scholar 

  65. Cureton DK, Massol RH, Saffarian S, Kirchhausen TL, Whelan SP (2009) Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog 5:e1000394

    Article  PubMed  CAS  Google Scholar 

  66. Cureton DK, Massol RH, Whelan SP, Kirchhausen T (2010) The length of vesicular stomatitis virus particles dictates a need for actin assembly during clathrin-dependent endocytosis. PLoS Pathog 6:e1001127

    Article  PubMed  CAS  Google Scholar 

  67. Gauthier NC, Fardin MA, Roca-Cusachs P, Sheetz MP (2011) Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading. Proc Natl Acad Sci U S A 108:14467–14472

    Article  PubMed  CAS  Google Scholar 

  68. Gaidarov I, Keen JH (1999) Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J Cell Biol 146:755–764

    Article  PubMed  CAS  Google Scholar 

  69. Keyel PA, Watkins SC, Traub LM (2004) Endocytic adaptor molecules reveal an endosomal population of clathrin by total internal reflection fluorescence microscopy. J Biol Chem 279:13190–13204

    Article  PubMed  CAS  Google Scholar 

  70. Saarikangas J, Zhao H, Lappalainen P (2010) Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol Rev 90:259–289

    Article  PubMed  CAS  Google Scholar 

  71. Jackson LP, Kelly BT, McCoy AJ, Gaffry T, James LC et al (2010) A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141:1220–1229

    Article  PubMed  CAS  Google Scholar 

  72. 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

    Article  PubMed  CAS  Google Scholar 

  73. Itoh T, Koshiba S, Kigawa T, Kikuchi A, Yokoyama S et al (2001) Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 291:1047–1051

    Article  PubMed  CAS  Google Scholar 

  74. Russo A, O’Bryan JP (2012) Intersectin 1 is required for neuroblastoma tumorigenesis. Oncogene 31(46):4828–4834

    Article  PubMed  CAS  Google Scholar 

  75. Vallis Y, Wigge P, Marks B, Evans PR, McMahon HT (1999) Importance of the pleckstrin homology domain of dynamin in clathrin-mediated endocytosis. Curr Biol 9:257–260

    Article  PubMed  CAS  Google Scholar 

  76. Yun M, Keshvara L, Park CG, Zhang YM, Dickerson JB et al (2003) Crystal structures of the Dab homology domains of mouse disabled 1 and 2. J Biol Chem 278:36572–36581

    Article  PubMed  CAS  Google Scholar 

  77. Ford MG, Pearse BM, Higgins MK, Vallis Y, Owen DJ et al (2001) Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291:1051–1055

    Article  PubMed  CAS  Google Scholar 

  78. Legendre-Guillemin V, Wasiak S, Hussain NK, Angers A, McPherson PS (2004) ENTH/ANTH proteins and clathrin-mediated membrane budding. J Cell Sci 117:9–18

    Article  PubMed  CAS  Google Scholar 

  79. Antonescu CN, Aguet F, Danuser G, Schmid SL (2011) Phosphatidylinositol-(4,5)-bisphosphate regulates clathrin-coated pit initiation, stabilization, and size. Mol Biol Cell 22:2588–2600

    Article  PubMed  CAS  Google Scholar 

  80. Varnai P, Thyagarajan B, Rohacs T, Balla T (2006) Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J Cell Biol 175:377–382

    Article  PubMed  CAS  Google Scholar 

  81. Padron D, Wang YJ, Yamamoto M, Yin H, Roth MG (2003) Phosphatidylinositol phosphate 5-kinase Ibeta recruits AP-2 to the plasma membrane and regulates rates of constitutive endocytosis. J Cell Biol 162:693–701

    Article  PubMed  CAS  Google Scholar 

  82. Zoncu R, Perera RM, Sebastian R, Nakatsu F, Chen H et al (2007) Loss of endocytic clathrin-­coated pits upon acute depletion of phosphatidylinositol 4,5-bisphosphate. Proc Natl Acad Sci U S A 104:3793–3798

    Article  PubMed  CAS  Google Scholar 

  83. Aikawa Y, Martin TF (2003) ARF6 regulates a plasma membrane pool of phosphatidylinositol(4,5)bisphosphate required for regulated exocytosis. J Cell Biol 162:647–659

    Article  PubMed  CAS  Google Scholar 

  84. Wen PJ, Osborne SL, Zanin M, Low PC, Wang HT et al (2011) Phosphatidylinositol(4,5)bisphosphate coordinates actin-mediated mobilization and translocation of secretory vesicles to the plasma membrane of chromaffin cells. Nat Commun 2:491

    Article  PubMed  CAS  Google Scholar 

  85. Gareus R, Di Nardo A, Rybin V, Witke W (2006) Mouse profilin 2 regulates endocytosis and competes with SH3 ligand binding to dynamin 1. J Biol Chem 281:2803–2811

    Article  PubMed  CAS  Google Scholar 

  86. van Rheenen J, Song X, van Roosmalen W, Cammer M, Chen X et al (2007) EGF-induced PIP2 hydrolysis releases and activates cofilin loc.lly in carcinoma cells. J Cell Biol 179:1247–1259

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  88. Qualmann B, Koch D, Kessels MM (2011) Let’s go bananas: revisiting the endocytic BAR code. EMBO J 30:3501–3515

    Article  PubMed  CAS  Google Scholar 

  89. Rao Y, Haucke V (2011) Membrane shaping by the Bin/amphiphysin/Rvs (BAR) domain protein superfamily. Cell Mol Life Sci 68:3983–3993

    Article  PubMed  CAS  Google Scholar 

  90. Kessels MM, Qualmann B (2004) The syndapin protein family: linking membrane trafficking with the cytoskeleton. J Cell Sci 117:3077–3086

    Article  PubMed  CAS  Google Scholar 

  91. Henne WM, Kent HM, Ford MG, Hegde BG, Daumke O et al (2007) Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure 15:839–852

    Article  PubMed  CAS  Google Scholar 

  92. Takenawa T, Suetsugu S (2007) The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 8:37–48

    Article  PubMed  CAS  Google Scholar 

  93. Yamada H, Padilla-Parra S, Park SJ, Itoh T, Chaineau M et al (2009) Dynamic interaction of amphiphysin with N-WASP regulates actin assembly. J Biol Chem 284:34244–34256

    Article  PubMed  CAS  Google Scholar 

  94. Shin N, Lee S, Ahn N, Kim SA, Ahn SG et al (2007) Sorting nexin 9 interacts with dynamin 1 and N-WASP and coordinates synaptic vesicle endocytosis. J Biol Chem 282:28939–28950

    Article  PubMed  CAS  Google Scholar 

  95. Kessels MM, Qualmann B (2002) Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J 21:6083–6094

    Article  PubMed  CAS  Google Scholar 

  96. Hussain NK, Jenna S, Glogauer M, Quinn CC, Wasiak S et al (2001) Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WASP. Nat Cell Biol 3:927–932

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  98. Innocenti M, Gerboth S, Rottner K, Lai FP, Hertzog M et al (2005) Abi1 regulates the activity of N-WASP and WAVE in distinct actin-based processes. Nat Cell Biol 7:969–976

    Article  PubMed  CAS  Google Scholar 

  99. Damke H, Baba T, Warnock DE, Schmid SL (1994) Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127:915–934

    Article  PubMed  CAS  Google Scholar 

  100. Ramachandran R (2011) Vesicle scission: dynamin. Semin Cell Dev Biol 22:10–17

    Article  PubMed  CAS  Google Scholar 

  101. Praefcke GJ, McMahon HT (2004) The dynamin superfamily: universal membrane tabulation and fission molecules? Nat Rev Mol Cell Biol 5:133–147

    Article  PubMed  CAS  Google Scholar 

  102. Stow ell MH, Marks B, Wigge P, McMahon HT (1999) Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat Cell Biol 1:27–32

    Article  CAS  Google Scholar 

  103. Rapp port JZ, Hayman KP, Kendal S, Simon SM (2008) Dynamics of dynamin during clathrin mediated endocytosis in PC12 cells. PLoS One 3:e2416

    Article  CAS  Google Scholar 

  104. Osaka T, Ikeda K (1983) Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J Neurobiology 14:207–225

    Article  Google Scholar 

  105. Damke H, Bins DD, Ueda H, Schmid SL, Baba T (2001) Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol Biol Cell 12:2578–2589

    PubMed  CAS  Google Scholar 

  106. Sweeter SM, Hingham JE (1998) Dynamin undergoes a GTP-dependent conformational change causing gesticulation. Cell 93:1021–1029

    Article  Google Scholar 

  107. Roux A, Oyaizu K, Frost A, De Camille P (2006) GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission. Nature 441:528–531

    Article  PubMed  CAS  Google Scholar 

  108. Bashkiria PV, Asimov SA, Evasive AI, Schmid SL, Zimmer berg J et al (2008) GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission. Cell 135:1276–1286

    Article  CAS  Google Scholar 

  109. Narayanan R, Leonard M, Song BD, Schmid SL, Ram swami M (2005) An internal GAP domain negatively regulates presynaptic dynamin in vivo: a two-step model for dynamin function. J Cell Biol 169:117–126

    Article  PubMed  CAS  Google Scholar 

  110. Liu J, Kaksonen M, Drubin DG, Ouster G (2006) Endocytic vesicle scission by lipid phase boundary forces. Proc Natl Acad Sci U S A 103:10277–10282

    Article  PubMed  CAS  Google Scholar 

  111. Roth JD, Krueger EW, Cao H, McNiven MA (2002) The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc Natl Acad Sci U S A 99:167–172

    Article  CAS  Google Scholar 

  112. Lee E, De Camille P (2002) Dynamin at actin tails. Proc Natl Acad Sci U S A 99:161–166

    Article  PubMed  CAS  Google Scholar 

  113. McNiven MA, Baldassarre M, Buccione R (2004) The role of dynamin in the assembly and function of podosomes and invadopodia. Front Biosci 9:1944–1953

    Article  PubMed  CAS  Google Scholar 

  114. Schafer DA (2004) Regulating actin dynamics at membranes: a focus on dynamin. Traffic 5:463–469

    Article  PubMed  CAS  Google Scholar 

  115. Gu C, Yaddanapudi S, Weins A, Osborn T, Reiser J et al (2010) Direct dynamin-actin interactions regulate the actin cytoskeleton. EMBO J 29:3593–3606

    Article  PubMed  CAS  Google Scholar 

  116. Buday L, Downward J (2007) Roles of cortactin in tumor pathogenesis. Biochim Biophys Acta 1775:263–273

    PubMed  CAS  Google Scholar 

  117. Higgs HN, Pollard TD (2001) Regulation of actin filament network formation through ARP2/3 complex: activation by a diverse array of proteins. Annu Rev Biochem 70:649–676

    Article  PubMed  CAS  Google Scholar 

  118. Kinley AW, Weed SA, Weaver AM, Karginov AV, Bissonette E et al (2003) Cortactin interacts with WIP in regulating Arp2/3 activation and membrane protrusion. Curr Biol 13:384–393

    Article  PubMed  CAS  Google Scholar 

  119. Weaver AM, Heuser JE, Karginov AV, Lee WL, Parsons JT et al (2002) Interaction of cortactin and N-WASp with Arp2/3 complex. Curr Biol 12:1270–1278

    Article  PubMed  CAS  Google Scholar 

  120. McNiven MA, Kim L, Krueger EW, Roth JD, Cao H et al (2000) Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151:187–198

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  123. Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y et al (2001) Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11:370–374

    Article  PubMed  CAS  Google Scholar 

  124. Zhu J, Zhou K, Hao JJ, Liu J, Smith N et al (2005) Regulation of cortactin/dynamin interaction by actin polymerization during the fission of clathrin-coated pits. J Cell Sci 118:807–817

    Article  PubMed  CAS  Google Scholar 

  125. Barroso C, Rodenbusch SE, Welch MD, Drubin DG (2006) A role for cortactin in Listeria monocytogenes invasion of NIH 3T3 cells, but not in its intracellular motility. Cell Motil Cytoskeleton 63:231–243

    Article  PubMed  CAS  Google Scholar 

  126. 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

    Article  PubMed  CAS  Google Scholar 

  127. Mooren OL, Kotova TI, Moore AJ, Schafer DA (2009) Dynamin2 GTPase and cortactin remodel actin filaments. J Biol Chem 284:23995–24005

    Article  PubMed  CAS  Google Scholar 

  128. Engqvist-Goldstein AE, Warren RA, Kessels MM, Keen JH, Heuser J et al (2001) The actin-­binding protein Hip1R associates with clathrin during early stages of endocytosis and promotes clathrin assembly in vitro. J Cell Biol 154:1209–1223

    Article  PubMed  CAS  Google Scholar 

  129. Wilbur JD, Chen CY, Manalo V, Hwang PK, Fletterick RJ et al (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

    Article  PubMed  CAS  Google Scholar 

  130. 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

    Article  PubMed  CAS  Google Scholar 

  131. Engqvist-Goldstein AE, Kessels MM, Chopra VS, Hayden MR, Drubin DG (1999) An actin-­binding protein of the Sla2/Huntingtin interacting protein 1 family is a novel component of clathrin-coated pits and vesicles. J Cell Biol 147:1503–1518

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  133. Poupon V, Girard M, Legendre-Guillemin V, Thomas S, Bourbonniere L et al (2008) Clathrin light chains function in mannose phosphate receptor trafficking via regulation of actin assembly. Proc Natl Acad Sci U S A 105:168–173

    Article  PubMed  CAS  Google Scholar 

  134. Boettner DR, Friesen H, Andrews B, Lemmon SK (2011) Clathrin light chain directs endocytosis by influencing the binding of the yeast Hip1R homologue, Sla2, to F-actin. Mol Biol Cell 22:3699–3714

    Article  PubMed  CAS  Google Scholar 

  135. Galletta BJ, Chuang DY, Cooper JA (2008) Distinct roles for Arp2/3 regulators in actin assembly and endocytosis. PLoS Biol 6:e1

    Article  PubMed  CAS  Google Scholar 

  136. Jung G, Wu X, Hammer JA III (1996) Dictyostelium mutants lacking multiple classic myosin I isoforms reveal combinations of shared and distinct functions. J Cell Biol 133:305–323

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  139. Krendel M, Osterweil EK, Mooseker MS (2007) Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett 581:644–650

    Article  PubMed  CAS  Google Scholar 

  140. Wells AL, Lin AW, Chen LQ, Safer D, Cain SM et al (1999) Myosin VI is an actin-based motor that moves backwards. Nature 401:505–508

    Article  PubMed  CAS  Google Scholar 

  141. Spudich G, Chibalina MV, Au JS, Arden SD, Buss F et al (2007) Myosin VI targeting to clathrin-coated structures and dimerization is mediated by binding to disabled-2 and PtdIns(4,5)P2. Nat Cell Biol 9:176–183

    Article  PubMed  CAS  Google Scholar 

  142. Morris SM, Arden SD, Roberts RC, Kendrick-Jones J, Cooper JA et al (2002) Myosin VI binds to and localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic 3:331–341

    Article  PubMed  CAS  Google Scholar 

  143. Dance AL, Miller M, Seragaki S, Aryal P, White B et al (2004) Regulation of myosin-VI targeting to endocytic compartments. Traffic 5:798–813

    Article  PubMed  CAS  Google Scholar 

  144. Aschenbrenner L, Naccache SN, Hasson T (2004) Uncoated endocytic vesicles require the unconventional myosin, Myo6, for rapid transport through actin barriers. Mol Biol Cell 15:2253–2263

    Article  PubMed  CAS  Google Scholar 

  145. Buss F, Kendrick-Jones J (2008) How are the cellular functions of myosin VI regulated within the cell? Biochem Biophys Res Commun 369:165–175

    Article  PubMed  CAS  Google Scholar 

  146. Hasson T (2003) Myosin VI: two distinct roles in endocytosis. J Cell Sci 116:3453–3461

    Article  PubMed  CAS  Google Scholar 

  147. Avraham KB, Hasson T, Steel KP, Kingsley DM, Russell LB et al (1995) The mouse Snell’s waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nat Genet 11:369–375

    Article  PubMed  CAS  Google Scholar 

  148. Puri C (2009) Loss of myosin VI no insert isoform (NoI) induces a defect in clathrin-­mediated endocytosis and leads to caveolar endocytosis of transferrin receptor. J Biol Chem 284:34998–35014

    Article  PubMed  CAS  Google Scholar 

  149. Dunn TA, Chen S, Faith DA, Hicks JL, Platz EA et al (2006) A novel role of myosin VI in human prostate cancer. Am J Pathol 169:1843–1854

    Article  PubMed  CAS  Google Scholar 

  150. Yoshida H, Cheng W, Hung J, Montell D, Geisbrecht E et al (2004) Lessons from border cell migration in the Drosophila ovary: a role for myosin VI in dissemination of human ovarian cancer. Proc Natl Acad Sci U S A 101:8144–8149

    Article  PubMed  CAS  Google Scholar 

  151. Tsyba L, Nikolaienko O, Dergai O, Dergai M, Novokhatska O et al (2011) Intersectin multidomain adaptor proteins: regulation of functional diversity. Gene 473:67–75

    Article  PubMed  CAS  Google Scholar 

  152. Yamabhai M, Hoffman NG, Hardison NL, McPherson PS, Castagnoli L et al (1998) Intersectin, a novel adaptor protein with two Eps15 homology and five Src homology 3 domains. J Biol Chem 273:31401–31407

    Article  PubMed  CAS  Google Scholar 

  153. Okamoto M, Schoch S, Sudhof TC (1999) EHSH1/intersectin, a protein that contains EH and SH3 domains and binds to dynamin and SNAP-25. A protein connection between exocytosis and endocytosis? J Biol Chem 274:18446–18454

    Article  PubMed  CAS  Google Scholar 

  154. Pechstein A, Bacetic J, Vahedi-Faridi A, Gromova K, Sundborger A et al (2010) Regulation of synaptic vesicle recycling by complex formation between intersectin 1 and the clathrin adaptor complex AP2. Proc Natl Acad Sci U S A 107:4206–4211

    Article  PubMed  CAS  Google Scholar 

  155. Henne WM, Boucrot E, Meinecke M, Evergren E, Vallis Y et al (2011) FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328:1281–1284

    Article  CAS  Google Scholar 

  156. Sengar AS, Wang W, Bishay J, Cohen S, Egan SE (1999) The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. EMBO J 18:1159–1171

    Article  PubMed  CAS  Google Scholar 

  157. Martin NP, Mohney RP, Dunn S, Das M, Scappini E et al (2006) Intersectin regulates epidermal growth factor receptor endocytosis, ubiquitylation, and signaling. Mol Pharmacol 70:1643–1653

    Article  PubMed  CAS  Google Scholar 

  158. Malacombe M, Ceridono M, Calco V, Chasserot-Golaz S, McPherson PS et al (2006) Intersectin-1L nucleotide exchange factor regulates secretory granule exocytosis by activating Cdc42. EMBO J 25:3494–3503

    Article  PubMed  CAS  Google Scholar 

  159. Evergren E, Gad H, Walther K, Sundborger A, Tomilin N et al (2007) Intersectin is a negative regulator of dynamin recruitment to the synaptic endocytic zone in the central synapse. J Neurosci 27:379–390

    Article  PubMed  CAS  Google Scholar 

  160. Klein IK, Predescu DN, Sharma T, Knezevic I, Malik AB et al (2009) Intersectin-2L regulates caveola endocytosis secondary to Cdc42-mediated actin polymerization. J Biol Chem 284:25953–25961

    Article  PubMed  CAS  Google Scholar 

  161. Specht K, Harbeck N, Smida J, Annecke K, Reich U et al (2009) Expression profiling identifies genes that predict recurrence of breast cancer after adjuvant CMF-based chemotherapy. Breast Cancer Res Treat 118:45–56

    Article  PubMed  CAS  Google Scholar 

  162. Kirchhausen T (2000) Three ways to make a vesicle. Nat Rev Mol Cell Biol 1:187–198

    Article  PubMed  CAS  Google Scholar 

  163. Antonny B (2006) Membrane deformation by protein coats. Curr Opin Cell Biol 18: 386–394

    Article  PubMed  CAS  Google Scholar 

  164. Beck R, Sun Z, Adolf F, Rutz C, Bassler J et al (2008) Membrane curvature induced by Arf1-­GTP is essential for vesicle formation. Proc Natl Acad Sci U S A 105:11731–11736

    Article  PubMed  CAS  Google Scholar 

  165. Lee MC, Orci L, Hamamoto S, Futai E, Ravazzola M et al (2005) Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122: 605–617

    Article  PubMed  CAS  Google Scholar 

  166. Ramachandran R, Pucadyil TJ, Liu YW, Acharya S, Leonard M et al (2009) Membrane insertion of the pleckstrin homology domain variable loop 1 is critical for dynamin-catalyzed vesicle scission. Mol Biol Cell 20:4630–4639

    Article  PubMed  CAS  Google Scholar 

  167. Lamaze C, Chuang TH, Terlecky LJ, Bokoch GM, Schmid SL (1996) Regulation of receptor-­mediated endocytosis by Rho and Rac. Nature 382:177–179

    Article  PubMed  CAS  Google Scholar 

  168. Malecz N, McCabe PC, Spaargaren C, Qiu R, Chuang Y et al (2000) Synaptojanin 2, a novel Rac1 effector that regulates clathrin-mediated endocytosis. Curr Biol 10:1383–1386

    Article  PubMed  CAS  Google Scholar 

  169. Paleotti O, Macia E, Luton F, Klein S, Partisani M et al (2005) The small G-protein Arf6GTP recruits the AP-2 adaptor complex to membranes. J Biol Chem 280:21661–21666

    Article  PubMed  CAS  Google Scholar 

  170. Donaldson JG, Porat-Shliom N, Cohen LA (2009) Clathrin-independent endocytosis: a unique platform for cell signaling and PM remodeling. Cell Signal 21:1–6

    Article  PubMed  CAS  Google Scholar 

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Hirschhorn, T., Ehrlich, M. (2013). Intimate and Facultative? Regulation of Clathrin-Mediated Endocytosis by the Actin Cytoskeleton. In: Yarden, Y., Tarcic, G. (eds) Vesicle Trafficking in Cancer. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6528-7_2

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