Let's go bananas: Revisiting the endocytic BAR code

EMBO Journal

Volumn 30, Issue 17, 2011, Pages 3501-3515

  Qualmann, Britta ^a   Koch, Dennis ^a   Kessels, Michael Manfred ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

BAR domain superfamily proteins; BAR hypothesis; clathrin mediated endocytosis; curvature; vesicle formation

Indexed keywords

AMPHIPHYSIN; AMPHIPHYSIN I; BIN1 PROTEIN; CIP4 PROTEIN; CLATHRIN; DIMER; LIPID BINDING PROTEIN; MEMBRANE PROTEIN; PROTEIN INTERACTING WITH PROTEIN KINASE C; RVS161P PROTEIN; RVS167P PROTEIN; SCAFFOLD PROTEIN; SNX9 PROTEIN; SYNDAPIN; TOCA 1 PROTEIN; UNCLASSIFIED DRUG;

CELL MEMBRANE; CELL VACUOLE; CRYSTAL STRUCTURE; ENDOCYTOSIS; HUMAN; HYDROPHOBICITY; HYPOTHESIS; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MEMBRANE RESISTANCE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW;

ANIMALS; CELL MEMBRANE; CLATHRIN; ENDOCYTOSIS; HUMANS; MEMBRANE PROTEINS; MICE; NERVE TISSUE PROTEINS; PROTEIN STRUCTURE, TERTIARY; TRANSPORT VESICLES;

EID: 80052194357     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.266     Document Type: Review

References (141)

1. Andersson F Jakobsson J Low P Shupliakov O Brodin L (2008) Perturbation of syndapin/PACSIN impairs synaptic vesicle recycling evoked by intense stimulation. J Neurosci 28: 3925-3933
2. Andersson F Low P Brodin L (2010) Selective perturbation of the BAR domain of endophilin impairs synaptic vesicle endocytosis. Synapse 64: 556-560
3. Anggono V Smillie KJ Graham ME Valova VA Cousin MA Robinson PJ (2006) Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nat Neurosci 9: 752-760
4. Aspenström P (1997) A Cdc42 target protein with homology to the non-kinase domain of FER has a potential role in regulating the actin cytoskeleton. Curr Biol 7: 479-487 (Pubitemid 27308971)
5. Ayton GS Blood PD Voth GA (2007) Membrane remodeling from N-BAR domain interactions: insights from multi-scale simulation. Biophys J 92: 3595-3602 (Pubitemid 46698648)
6. Bai J Hu Z Dittman JS Pym EC Kaplan JM (2010) Endophilin functions as a membrane-bending molecule and is delivered to endocytic zones by exocytosis. Cell 143: 430-441
7. Batchelder EM Yarar D (2010) Differential requirements for cla-thrin-dependent endocytosis at sites of cell-substrate adhesion. Mol Biol Cell 21: 3070-3079
8. 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 (Pubitemid 41149914)
9. Bertaso F Zhang C Scheschonka A de Bock F Fontanaud P Marin P Huganir RL Betz H Bockaert J Fagni L Lerner-Natoli M (2008) PICK1 uncoupling from mGluR7a causes absence-like seizures. Nat Neurosci 11 : 940-948
10. Bhatia VK Madsen KL Bolinger PY Kunding A Hedegard P Gether U Stamou D (2009) Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J 28: 3303-3314
11. Billuart P Bienvenu T Ronce N des Portes V Vinet MC Zemni R Roest Crollius H Carrie A Fauchereau F Cherry M Briault S Hamel B Fryns JP Beldjord C Kahn A Moraine C Chelly J (1998) Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Nature 392: 923-926 (Pubitemid 28232063)
12. Boumil RM Letts VA Roberts MC Lenz C Mahaffey CL Zhang ZW Moser T Frankel WN (2010) A missense mutation in a highly conserved alternate exon of dynamin-1 causes epilepsy in fitful mice. PLoS Genet 6: e1001046
13. Braun A Pinyol R Dahlhaus R Koch D Fonarev P Grant BD Kessels MM Qualmann B (2005) EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol Biol Cell 16: 3642-3658 (Pubitemid 41078817)
14. Casal E Federici L Zhang W Fernandez-Recio J Priego EM Miguel RN DuHadaway JB Prendergast GC Luisi BF Laue ED (2006) The crystal structure of the BAR domain from human Bin1/amphiphysin II and its implications for molecular recognition. Biochemistry 45: 12917-12928 (Pubitemid 44763415)
15. Chang L Adams RD Saltiel AR (2002) The TC10-interacting protein CIP4/2 is required for insulin-stimulated Glut4 trans-location in 3T3L1 adipocytes. Proc Natl Acad Sci USA 99: 12835-12840
16. Chang-Ileto B Frere SG Chan RB Voronov SV Roux A Di Paolo G (2011) Synaptojanin 1-mediated PI(45)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. Dev Cell 20: 206-218
17. Chial HJ Wu R Ustach CV McPhail LC Mobley WC Chen YQ (2008) Membrane targeting by APPL1 and APPL2: dynamic scaffolds that oligomerize and bind phosphoinositides. Traffic 9: 215-229
18. Citri A Bhattacharyya S Ma C Morishita W Fang S Rizo J Malenka RC (2010) Calcium binding to PICK1 is essential for the intracellular retention of AMPA receptors underlying long-term depression. J Neurosci 30: 16437-16452
19. Clayton EL Anggono V Smillie KJ Chau N Robinson PJ Cousin MA (2009) The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synap-tic vesicles. J Neurosci 29: 7706-7717
20. David C McPherson PS Mundigl O de Camilli P (1996) A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc Natl Acad Sci USA 93: 331-335 (Pubitemid 26038153)
21. David C Solimena M De Camilli P (1994) Autoimmunity in stiff-Man syndrome with breast cancer is targeted to the C-terminal region of human amphiphysin a protein similar to the yeast proteins Rvs167 and Rvs161. FEBS Lett 351: 73-79
22. Dev KK Henley JM (2006) The schizophrenic faces of PICK1. Trends Pharmacol Sci 27: 574-579 (Pubitemid 44604302)
23. Dharmalingam E Haeckel A Pinyol R Schwintzer L Koch D Kessels MM Qualmann B (2009) F-BAR proteins of the syndapin family shape the plasma membrane and are crucial for neuro-morphogenesis. J Neurosci 29: 13315-13327
24. Di Paolo G Sankaranarayanan S Wenk MR Daniell L Perucco E Caldarone BJ Flavell R Picciotto MR Ryan TA Cremona O De Camilli P (2002) Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout mice. Neuron 33: 789-804 (Pubitemid 34219249)
25. Dislich B Than ME Lichtenthaler SF (2010) Specific amino acids in the BAR domain allow homodimerization and prevent hetero-dimerization of sorting nexin 33. Biochem J 433: 75-83
26. Doherty GJ McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78: 857-902
27. Ehrlich M Boll W Van Oijen A Hariharan R Chandran K Nibert ML Kirchhausen T (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118: 591-605 (Pubitemid 39179712)
28. Erdmann KS Mao Y McCrea HJ Zoncu R Lee S Paradise S Modregger J Biemesderfer D Toomre D De Camilli P (2007) A role of the Lowe syndrome protein OCRL in early steps of the endocytic pathway. Dev Cell 13: 377-390 (Pubitemid 47321603)
29. Evergren E Marcucci M Tomilin N Low P Slepnev V Andersson F Gad H Brodin L De Camilli P Shupliakov O (2004) Amphiphysin is a component of clathrin coats formed during synaptic vesicle recycling at the lamprey giant synapse. Traffic 5: 514-528 (Pubitemid 38923178)
30. Farsad K Ringstad N Takei K Floyd SR Rose K De Camilli P (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol 155: 193-200 (Pubitemid 34289294)
31. Feng Y Hartig SM Bechill JE Blanchard EG Caudell E Corey SJ (2010) The Cdc42-interacting protein-4 (CIP4) gene knock-out mouse reveals delayed and decreased endocytosis. J Biol Chem 285: 4348-4354
32. Ferguson SM Brasnjo G Hayashi M Wolfel M Collesi C Giovedi S Raimondi A Gong LW Ariel P Paradise S O0Toole E Flavell R Cremona O Miesenbock G Ryan TA De Camilli P (2007) A selective activity-dependent requirement for dynamin 1 in synap-tic vesicle endocytosis. Science 316: 570-574 (Pubitemid 46683137)
33. Fricke R Gohl C Dharmalingam E Grevelhorster A Zahedi B Harden N Kessels M Qualmann B Bogdan S (2009) Droso-phila Cip4/Toca-1 integrates membrane trafficking and actin dynamics through WASP and SCAR/WAVE. Curr Biol 19: 1429-1437
34. Frost A Perera R Roux A Spasov K Destaing O Egelman EH De Camilli P Unger VM (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132: 807-817 (Pubitemid 351320580)
35. Frost A Unger VM De Camilli P (2009) The BAR domain super-family: membrane-molding macromolecules. Cell 137: 191-196
36. Gad H Ringstad N Low P Kjaerulff O Gustafsson J Wenk M Di Paolo G Nemoto Y Crun J Ellisman MH De Camilli P Shupliakov O Brodin L (2000) Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27: 301-312
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 (Pubitemid 129495002)
38. Gallop JL Jao CC Kent HM Butler PJ Evans PR Langen R McMahon HT (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J 25: 2898-2910 (Pubitemid 43980396)
39. Gallop JL McMahon HT (2005) BAR domains and membrane curvature: bringing your curves to the BAR. Biochem Soc Symp 72: 223-231 (Pubitemid 44804748)
40. Giuliani C Troglio F Bai Z Patel FB Zucconi A Malabarba MG Disanza A Stradal TB Cassata G Confalonieri S Hardin JD Soto MC Grant BD Scita G (2009) Requirements for F-BAR proteins TOCA-1 and TOCA-2 in actin dynamics and membrane trafficking during Caenorhabditis elegans oocyte growth and embryonic epidermal morphogenesis. PLoS Genet 5: e1000675
41. Guerrier S Coutinho-Budd J Sassa T Gresset A Jordan NV Chen K Jin WL Frost A Polleux F (2009) The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138: 990-1004
42. Haberg K Lundmark R Carlsson SR (2008) SNX18 is an SNX9 paralog that acts as a membrane tubulator in AP-1-positive endosomal trafficking. J Cell Sci 121: 1495-1505 (Pubitemid 351936314)
43. Hartig SM Ishikura S Hicklen RS Feng Y Blanchard EG Voelker KA Pichot CS Grange RW Raphael RM Klip A Corey SJ (2009) The F-BAR protein CIP4 promotes GLUT4 endocytosis through bidirectional interactions with N-WASp and Dynamin-2. J Cell Sci 122: 2283-2291
44. Heiseke A Schobel S Lichtenthaler SF Vorberg I Groschup MH Kretzschmar H Schatzl HM Nunziante M (2008) The novel sorting nexin SNX33 interferes with cellular PrP formation by modulation of PrP shedding. Traffic 9: 1116-1129 (Pubitemid 351916887)
45. Henne WM Boucrot E Meinecke M Evergren E Vallis Y Mittal R McMahon HT (2010) FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328: 1281-1284
46. Henne WM Kent HM Ford MG Hegde BG Daumke O Butler PJ Mittal R Langen R Evans PR McMahon HT (2007) Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure 15: 839-852 (Pubitemid 47042426)
47. Ho HY Rohatgi R Lebensohn AM Le M Li J Gygi SP Kirschner MW (2004) Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118: 203-216 (Pubitemid 38962576)
48. 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 (Pubitemid 41724107)
49. Itoh T Takenawa T (2009) Mechanisms of membrane deformation by lipid-binding domains. Prog Lipid Res 48: 298-305
50. Jung AG Labarrera C Jansen AM Qvortrup K Wild K Kjaerulff O (2010) A mutational analysis of the endophilin-A N-BAR domain performed in living flies. PLoS One 5: e9492
51. Kamioka Y Fukuhara S Sawa H Nagashima K Masuda M Matsuda M Mochizuki N (2004) A novel dynamin-associating molecule formin-binding protein 17 induces tubular membrane invaginations and participates in endocytosis. J Biol Chem 279: 40091-40099 (Pubitemid 39258284)
52. Kessels MM Qualmann B (2002) Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J 21 : 6083-6094 (Pubitemid 35422657)
53. Kessels MM Qualmann B (2006) Syndapin oligomers interconnect the machineries for endocytic vesicle formation and actin polymerization. J Biol Chem 281: 13285-13299 (Pubitemid 43862164)
54. 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 (Pubitemid 38445898)
55. Khelfaoui M Denis C van Galen E de Bock F Schmitt A Houbron C Morice E Giros B Ramakers G Fagni L Chelly J Nosten-Bertrand M Billuart P (2007) Loss of X-linked mental retardation gene oligophrenin1 in mice impairs spatial memory and leads to ventricular enlargement and dendritic spine immaturity. J Neurosci 27: 9439-9450 (Pubitemid 47358207)
56. Kirchhausen T (2009) Imaging endocytic clathrin structures in living cells. Trends Cell Biol 19: 596-605
57. Kumar V Alla SR Krishnan KS Ramaswami M (2009a) Syndapin is dispensable for synaptic vesicle endocytosis at the Drosophila larval neuromuscular junction. Mol Cell Neurosci 40: 234-241
58. Kumar V Fricke R Bhar D Reddy-Alla S Krishnan KS Bogdan S Ramaswami M (2009b) Syndapin promotes formation of a postsynaptic membrane system in Drosophila. Mol Biol Cell 20 (8): 2254-2264
59. Leibfried A Fricke R Morgan MJ Bogdan S Bellaiche Y (2008) Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr Biol 18: 1639-1648
60. Li J Mao X Dong LQ Liu F Tong L (2007) Crystal structures of the BAR-PH and PTB domains of human APPL1. Structure 15: 525-533 (Pubitemid 46702684)
61. Loerke D Mettlen M Yarar D Jaqaman K Jaqaman H Danuser G Schmid SL (2009) Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol 7: e57
62. 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 (Pubitemid 37452256)
63. Lundmark R Carlsson SR (2004) Regulated membrane recruitment of dynamin-2 mediated by sorting nexin 9. J Biol Chem 279: 42694-42702 (Pubitemid 39372155)
64. Lundmark R Carlsson SR (2009) SNX9-a prelude to vesicle release. J Cell Sci 122: 5-11
65. Mani M Lee SY Lucast L Cremona O Di Paolo G De Camilli P Ryan TA (2007) The dual phosphatase activity of synaptojanin1 is required for both efficient synaptic vesicle endocytosis and reavailability at nerve terminals. Neuron 56: 1004-1018 (Pubitemid 350251112)
66. Masuda M Mochizuki N (2010) Structural characteristics of BAR domain superfamily to sculpt the membrane. Semin Cell Dev Biol 21: 391-398
67. Masuda M Takeda S Sone M Ohki T Mori H Kamioka Y Mochizuki N (2006) Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J 25: 2889-2897 (Pubitemid 43980395)
68. Mattila PK Pykalainen A Saarikangas J Paavilainen VO Vihinen H Jokitalo E Lappalainen P (2007) Missing-in-metasta-sis and IRSp53 deform PI(45)P2-rich membranes by an inverse BAR domain-like mechanism. J Cell Biol 176: 953-964 (Pubitemid 46506969)
69. McMahon HT Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438: 590-596 (Pubitemid 41740562)
70. McMahon HT Wigge P Smith C (1997) Clathrin interacts specifically with amphiphysin and is displaced by dynamin. FEBS Lett 413: 319-322 (Pubitemid 27353292)
71. Merrifield CJ (2004) Seeing is believing: imaging actin dynamics at single sites of endocytosis. Trends Cell Biol 14: 352-358 (Pubitemid 38891704)
72. 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 (Pubitemid 40720012)
73. 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 (Pubitemid 38455602)
74. Mettlen M Stoeber M Loerke D Antonescu CN Danuser G Schmid SL (2009) Endocytic accessory proteins are functionally distinguished by their differential effects on the maturation of clathrin-coated pits. Mol Biol Cell 20: 3251-3260
75. Miaczynska M Christoforidis S Giner A Shevchenko A Uttenweiler-Joseph S Habermann B Wilm M Parton RG Zerial M (2004) APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116: 445-456 (Pubitemid 38366320)
76. Millard TH Bompard G Heung MY Dafforn TR Scott DJ Machesky LM Futterer K (2005) Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. EMBO J 24: 240-250 (Pubitemid 40216129)
77. Modregger J Ritter B Witter B Paulsson M Plomann M (2000) All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J Cell Sci 113: 4511-4521 (Pubitemid 32117911)
78. Muller AJ Baker JF DuHadaway JB Ge K Farmer G Donover PS Meade R Reid C Grzanna R Roach AH Shah N Soler AP Prendergast GC (2003) Targeted disruption of the murine Bin1/Amphiphysin II gene does not disable endocytosis but results in embryonic cardiomyopathy with aberrant myofibril formation. Mol Cell Biol 23: 4295-4306 (Pubitemid 36666431)
79. Nadif Kasri N Nakano-Kobayashi A Malinow R Li B Van Aelst L (2009) The Rho-linked mental retardation protein oligophrenin-1 controls synapse maturation and plasticity by stabilizing AMPA receptors. Genes Dev 23: 1289-1302
80. Nakano-Kobayashi A Kasri NN Newey SE Van Aelst L (2009) The Rho-linked mental retardation protein OPHN1 controls synaptic vesicle endocytosis via endophilin A1. Curr Biol 19: 1133-1139
81. Otsuki M Itoh T Takenawa T (2003) Neural Wiskott-Aldrich syndrome protein is recruited to rafts and associates with en-dophilin A in response to epidermal growth factor. J Biol Chem 278: 6461-6469 (Pubitemid 36800906)
82. Pan L Wu H Shen C Shi Y Jin W Xia J Zhang M (2007) Clustering and synaptic targeting of PICK1 requires direct interaction between the PDZ domain and lipid membranes. EMBO J 26: 4576-4587 (Pubitemid 350036623)
83. Pant S Sharma M Patel K Caplan S Carr CM Grant BD (2009) AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in en-docytic recycling. Nat Cell Biol 11 : 1399-1410
84. Park J Kim Y Lee S Park JJ Park ZY Sun W Kim H Chang S (2010) SNX18 shares a redundant role with SNX9 and modulates endocytic trafficking at the plasma membrane. J Cell Sci 123: 1742-1750
85. Perera RM Zoncu R Lucast L De Camilli P Toomre D (2006) Two synaptojanin 1 isoforms are recruited to clathrin-coated pits at different stages. Proc Natl Acad Sci USA 103: 19332-19337 (Pubitemid 46026032)
86. Peter BJ Kent HM Mills IG Vallis Y Butler PJ Evans PR McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303: 495-499 (Pubitemid 38120842)
87. 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 (Pubitemid 34246477)
88. Pylypenko O Lundmark R Rasmuson E Carlsson SR Rak A (2007) The PX-BAR membrane-remodeling unit of sorting nexin 9. EMBO J 26: 4788-4800 (Pubitemid 350126794)
89. Qualmann B Kelly RB (2000) Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J Cell Biol 148: 1047-1062
90. Qualmann B Roos J DiGregorio PJ Kelly RB (1999) Syndapin I a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol Biol Cell 10 : 501-513 (Pubitemid 29156487)
91. Quinones GA Jin J Oro AE (2010) I-BAR protein antagonism of endocytosis mediates directional sensing during guided cell migration. J Cell Biol 189: 353-367
92. Ramjaun AR Micheva KD Bouchelet I McPherson PS (1997) Identification and characterization of a nerve terminal-enriched amphiphysin isoform. J Biol Chem 272: 16700-16706 (Pubitemid 27276504)
93. Rao Y Ma Q Vahedi-Faridi A Sundborger A Pechstein A Puchkov D Luo L Shupliakov O Saenger W Haucke V (2010) Molecular basis for SH3 domain regulation of F-BAR-mediated membrane deformation. Proc Natl Acad Sci USA 107 : 8213-8218
94. Rappoport JZ (2008) Focusing on clathrin-mediated endocytosis. Biochem J 412: 415-423 (Pubitemid 351846407)
95. Razzaq A Robinson IM McMahon HT Skepper JN Su Y Zelhof AC Jackson AP Gay NJ O0Kane CJ (2001) Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles but not for synaptic vesicle endocytosis in Drosophila. Genes Dev 15: 2967-2979 (Pubitemid 33078947)
96. Reider A Barker SL Mishra SK Im YJ Maldonado-Baez L Hurley JH Traub LM Wendland B (2009) Syp1 is a conserved endocytic adaptor that contains domains involved in cargo selection and membrane tubulation. EMBO J 28: 3103-3116
97. Ringstad N Gad H Low P Di Paolo G Brodin L Shupliakov O De Camilli P (1999) Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24: 143-154 (Pubitemid 29466154)
98. Ringstad N Nemoto Y De Camilli P (1997) The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc Natl Acad Sci USA 94: 8569-8574 (Pubitemid 27335079)
99. Ringstad N Nemoto Y De Camilli P (2001) Differential expression of endophilin 1 and 2 dimers at central nervous system synapses. J Biol Chem 276: 40424-40430
100. Roberts-Galbraith RH Gould KL (2010) Setting the F-BAR: functions and regulation of the F-BAR protein family. Cell Cycle 9: 4091-4097
101. Rocca DL Martin S Jenkins EL Hanley JG (2008) Inhibition of Arp2/3-mediated actin polymerization by PICK1 regulates neu-ronal morphology and AMPA receptor endocytosis. Nat Cell Biol 10: 259-271 (Pubitemid 351331013)
102. Saarikangas J Zhao H Pykalainen A Laurinmaki P Mattila PK Kinnunen PK Butcher SJ Lappalainen P (2009) Molecular mechanisms of membrane deformation by I-BAR domain proteins. Curr Biol 19: 95-107
103. Saffarian S Cocucci E Kirchhausen T (2009) Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 7: e1000191
104. Schmid SL Frolov VA (2011) Dynamin: functional design of a membrane fission catalyst. Annu Rev Cell Dev Biol (advance online publication; doi:10.1146/annurev-cellbio-100109-104016)
105. Schöbel S Neumann S Hertweck M Dislich B Kuhn PH Kremmer E Seed B Baumeister R Haass C Lichtenthaler SF (2008) A novel sorting nexin modulates endocytic trafficking and alpha-secretase cleavage of the amyloid precursor protein. J Biol Chem 283: 14257-14268
106. Schuske KR Richmond JE Matthies DS Davis WS Runz S Rube DA van der Bliek AM Jorgensen EM (2003) Endophilin is required for synaptic vesicle endocytosis by localizing synapto-janin. Neuron 40: 749-762 (Pubitemid 37431035)
107. Schwintzer L Koch N Ahuja R Grimm J Kessels MM Qualmann B (2011) The functions of the actin nucleator Cobl in cellular morphogenesis critically depend on syndapin I. EMBO J 30: 3147-3159
108. Shimada A Niwa H Tsujita K Suetsugu S Nitta K Hanawa-Suetsugu K Akasaka R Nishino Y Toyama M Chen L Liu ZJ Wang BC Yamamoto M Terada T Miyazawa A et al (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129: 761-772 (Pubitemid 46813111)
109. Shimada A Takano K Shirouzu M Hanawa-Suetsugu K Terada T Toyooka K Umehara T Yamamoto M Yokoyama S Suetsugu S (2010) Mapping of the basic amino-acid residues responsible for tubulation and cellular protrusion by the EFC/F-BAR domain of pacsin2/Syndapin II. FEBS Lett 584: 1111-1118
110. Shin N Lee S Ahn N Kim SA Ahn SG YongPark Z Chang S (2007) Sorting nexin 9 interacts with dynamin 1 and N-WASP and coordinates synaptic vesicle endocytosis. J Biol Chem 282: 28939-28950 (Pubitemid 47606053)
111. Shupliakov O Low P Grabs D Gad H Chen H David C Takei K De Camilli P Brodin L (1997) Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276: 259-263 (Pubitemid 27172685)
112. Sinha S Chunder N Mukherjee N Alam N Roy A Roychoudhury S Kumar Panda C (2008) Frequent deletion and methylation in SH3GL2 and CDKN2A loci are associated with early-and late-onset breast carcinoma. Ann Surg Oncol 15: 1070-1080
113. Slepnev VI Ochoa GC Butler MH De Camilli P (2000) Tandem arrangement of the clathrin and AP-2 binding domains in amphiphysin 1 and disruption of clathrin coat function by amphiphysin fragments comprising these sites. J Biol Chem 275: 17583-17589 (Pubitemid 30430803)
114. 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 (Pubitemid 34246476)
115. 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 (Pubitemid 40471971)
116. Steinberg JP Takamiya K Shen Y Xia J Rubio ME Yu S Jin W Thomas GM Linden DJ Huganir RL (2006) Targeted in vivo mutations of the AMPA receptor subunit GluR2 and its interacting protein PICK1 eliminate cerebellar long-term depression. Neuron 49: 845-860 (Pubitemid 43376082)
117. Suetsugu S Murayama K Sakamoto A Hanawa-Suetsugu K Seto A Oikawa T Mishima C Shirouzu M Takenawa T Yokoyama S (2006) The RAC binding domain/IRSp53-MIM homology domain of IRSp53 induces RAC-dependent membrane deformation. J Biol Chem 281: 35347-35358 (Pubitemid 46036573)
118. Suetsugu S Toyooka K Senju Y (2010) Subcellular membrane curvature mediated by the BAR superfamily proteins. Semin Cell Dev Biol 21 : 340-349
119. 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
120. Takei K McPherson PS Schmid SL De Camilli P (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374: 186-190
121. Takei K Slepnev VI Haucke V De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1: 33-39 (Pubitemid 129495007)
122. Tan TC Valova VA Malladi CS Graham ME Berven LA Jupp OJ Hansra G McClure SJ Sarcevic B Boadle RA Larsen MR Cousin MA Robinson PJ (2003) Cdk5 is essential for synaptic vesicle endocytosis. Nat Cell Biol 5: 701-710 (Pubitemid 36986777)
123. Tarricone C Xiao B Justin N Walker PA Rittinger K Gamblin SJ Smerdon SJ (2001) The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways. Nature 411 : 215-219 (Pubitemid 32455183)
124. Taylor MJ Perrais D Merrifield CJ (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9: e1000604
125. 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 (Pubitemid 43112973)
126. Turnbull J Lohi H Kearney JA Rouleau GA Delgado-Escueta AV Meisler MH Cossette P Minassian BA (2005) Sacred disease secrets revealed: the genetics of human epilepsy. Hum Mol Genet 14: 2491-2500 (Pubitemid 41236062)
127. Van Weering JR Verkade P Cullen PJ (2010) SNX-BAR proteins in phosphoinositide-mediated tubular-based endosomal sorting. Semin Cell Dev Biol 21: 371-380
128. Verstreken P Kjaerulff O Lloyd TE Atkinson R Zhou Y Meinertzhagen IA Bellen HJ (2002) Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109: 101-112 (Pubitemid 34327520)
129. Verstreken P Koh TW Schulze KL Zhai RG Hiesinger PR Zhou Y Mehta SQ Cao Y Roos J Bellen HJ (2003) Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 13: 733-748 (Pubitemid 37431034)
130. Wang Q Kaan HY Hooda RN Goh SL Sondermann H (2008) Structure and plasticity of Endophilin and Sorting Nexin 9. Structure 16: 1574-1587
131. Wang Q Navarro MV Peng G Molinelli E Goh SL Judson BL Rajashankar KR Sondermann H (2009) Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin. Proc Natl Acad Sci USA 106: 12700-12705
132. Weissenhorn W (2005) Crystal structure of the endophilin-A1 BAR domain. J Mol Biol 351: 653-661 (Pubitemid 41021947)
133. Wu M Huang B Graham M Raimondi A Heuser JE Zhuang X De Camilli P (2010) Coupling between clathrin-dependent endocytic budding and F-BAR-dependent tubulation in a cell-free system. Nat Cell Biol 12: 902-908
134. Xia J Zhang X Staudinger J Huganir RL (1999) Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22: 179-187 (Pubitemid 29070104)
135. Yamada H Padilla-Parra S Park SJ Itoh T Chaineau M Monaldi I Cremona O Benfenati F De Camilli P Coppey-Moisan M Tramier M Galli T Takei K (2009) Dynamic interaction of amphiphysin with N-WASP regulates actin assembly. J Biol Chem 284: 34244-34256
136. 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 (Pubitemid 46972030)
137. Yoshida Y Kinuta M Abe T Liang S Araki K Cremona O Di Paolo G Moriyama Y Yasuda T De Camilli P Takei K (2004) The stimulatory action of amphiphysin on dynamin function is dependent on lipid bilayer curvature. EMBO J 23: 3483-3491 (Pubitemid 39265538)
138. Zhao H Pykalainen A Lappalainen P (2011) I-BAR domain proteins: linking actin and plasma membrane dynamics. Curr Opin Cell Biol 23: 14-21
139. Zhu G Chen J Liu J Brunzelle JS Huang B Wakeham N Terzyan S Li X Rao Z Li G Zhang XC (2007) Structure of the APPL1 BAR-PH domain and characterization of its interaction with Rab5. EMBO J 26: 3484-3493 (Pubitemid 47123536)
140. Zimmerberg J Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7: 9-19 (Pubitemid 43361568)
141. Zoncu R Perera RM Balkin DM Pirruccello M Toomre D De Camilli P (2009) A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136: 1110-1121