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Annual Review of Cell and Developmental Biology

Volume 35, 2019

Curving Cells Inside and Out: Roles of BAR Domain Proteins in Membrane Shaping and Its Cellular Implications

Abstract

Many cellular processes rely on precise and timely deformation of the cell membrane. While many proteins participate in membrane reshaping and scission, usually in highly specialized ways, Bin/amphiphysin/Rvs (BAR) domain proteins play a pervasive role, as they not only participate in many aspects of cell trafficking but also are highly versatile membrane remodelers. Subtle changes in the shape and size of the BAR domain can greatly impact the way in which BAR domain proteins interact with the membrane. Furthermore, the activity of BAR domain proteins can be tuned by external physical parameters, and so they behave differently depending on protein surface density, membrane tension, or membrane shape. These proteins can form 3D structures that mold the membrane and alter its liquid properties, even promoting scission under various circumstances.As such, BAR domain proteins have numerous roles within the cell. Endocytosis is among the most highly studied processes in which BAR domain proteins take on important roles. Over the years, a more complete picture has emerged in which BAR domain proteins are tied to almost all intracellular compartments; examples include endosomal sorting and tubular networks in the endoplasmic reticulum and T-tubules. These proteins also have a role in autophagy, and their activity has been linked with cancer. Here, we briefly review the history of BAR domain protein discovery, discuss the mechanisms by which BAR domain proteins induce curvature, and attempt to settle important controversies in the field. Finally, we review BAR domain proteins in the context of a cell, highlighting their emerging roles in cell signaling and organelle shaping.

Keyword(s): amphipathic helices, BAR domain proteins, curvature, membrane traffic, scaffold, scission
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2019-10-06
2024-04-19
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Literature Cited

  1. Almeida-Souza L, Frank RAW, Garcia-Nafria J, Colussi A, Gunawardana N et al. 2018. A flat BAR protein promotes actin polymerization at the base of clathrin-coated pits. Cell 174:325–37.e14
     [Google Scholar]
  2. Ambroggio E, Sorre B, Bassereau P, Goud B, Manneville JB, Antonny B 2010. ArfGAP1 generates an Arf1 gradient on continuous lipid membranes displaying flat and curved regions. EMBO J 29:292–303
     [Google Scholar]
  3. Ambroso MR, Hegde BG, Langen R 2014. Endophilin A1 induces different membrane shapes using a conformational switch that is regulated by phosphorylation. PNAS 111:6982–87
     [Google Scholar]
  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. 7:479–87
     [Google Scholar]
  5. Baldassarre T, Watt K, Truesdell P, Meens J, Schneider MM et al. 2015. Endophilin A2 promotes TNBC cell invasion and tumor metastasis. Mol. Cancer Res. 13:1044–55
     [Google Scholar]
  6. Barbieri E, Di Fiore PP, Sigismund S 2016. Endocytic control of signaling at the plasma membrane. Curr. Opin. Cell Biol. 39:21–27
     [Google Scholar]
  7. Bassereau P, Sorre B, Levy A 2014. Bending lipid membranes: experiments after W. Helfrich's model. Adv. Colloid Interface Sci. 208:47–57
     [Google Scholar]
  8. Bauer F, Urdaci M, Aigle M, Crouzet M 1993. Alteration of a yeast Sh3 protein leads to conditional viability with defects in cytoskeletal and budding patterns. Mol. Cell. Biol. 13:5070–84
     [Google Scholar]
  9. Baumgart T, Capraro BR, Zhu C, Das SL 2011. Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu. Rev. Phys. Chem. 62:483–506
     [Google Scholar]
  10. Bhatia VK, Madsen KL, Bolinger PY, Kunding A, Hedegard P et al. 2009. Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J 28:3303–14
     [Google Scholar]
  11. Bickel T, Jeppesen C, Marques CM 2001. Local entropic effects of polymers grafted to soft interfaces. Eur. Phys. J. E 4:33–43
     [Google Scholar]
  12. Billcliff PG, Noakes CJ, Mehta ZB, Yan G, Mak L et al. 2016. OCRL1 engages with the F-BAR protein pacsin 2 to promote biogenesis of membrane-trafficking intermediates. Mol. Biol. Cell 27:90–107
     [Google Scholar]
  13. Blood PD, Voth GA. 2006. Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations. PNAS 103:15068–72
     [Google Scholar]
  14. Boucrot E, Ferreira AP, Almeida-Souza L, Debard S, Vallis Y et al. 2015. Endophilin marks and controls a clathrin-independent endocytic pathway. Nature 517:460–65
     [Google Scholar]
  15. Boucrot E, Pick A, Camdere G, Liska N, Evergren E et al. 2012. Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149:124–36
     [Google Scholar]
  16. Breidenich M, Netz RR, Lipowsky R 2000. The shape of polymer-decorated membranes. Europhys. Lett. 49:431–37
     [Google Scholar]
  17. Burd C, Cullen PJ. 2014. Retromer: a master conductor of endosome sorting. Cold Spring Harb. Perspect. Biol. 6:a016774
     [Google Scholar]
  18. Busch DJ, Houser JR, Hayden CC, Sherman MB, Lafer EM, Stachowiak JC 2015. Intrinsically disordered proteins drive membrane curvature. Nat. Commun. 6:7875
     [Google Scholar]
  19. Butler MH, David C, Ochoa GC, Freyberg Z, Daniell L et al. 1997. Amphiphysin II (SH3P9; BIN1), a member of the amphiphysin/Rvs family, is concentrated in the cortical cytomatrix of axon initial segments and nodes of Ranvier in brain and around T tubules in skeletal muscle. J. Cell Biol. 137:1355–67
     [Google Scholar]
  20. Callan-Jones A, Bassereau P. 2013. Curvature-driven membrane lipid and protein distribution. Curr. Opin. Solid State Mater. Sci. 17:143–50
     [Google Scholar]
  21. Campelo F, McMahon HT, Kozlov MM 2008. The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys. J. 95:2325–39
     [Google Scholar]
  22. Canham PB. 1970. The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. J. Theor. Biol. 26:61–81
     [Google Scholar]
  23. Capraro BR, Yoon Y, Cho W, Baumgart T 2010. Curvature sensing by the epsin N-terminal homology domain measured on cylindrical lipid membrane tethers. J. Am. Chem. Soc. 132:1200–1
     [Google Scholar]
  24. Chen Z, Atefi E, Baumgart T 2016a. Membrane shape instability induced by protein crowding. Biophys. J. 111:1823–26
     [Google Scholar]
  25. Chen Z, Zhu C, Kuo CJ, Robustelli J, Baumgart T 2016b. The N-terminal amphipathic helix of endophilin does not contribute to its molecular curvature generation capacity. J. Am. Chem. Soc. 138:14616–22
     [Google Scholar]
  26. 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 9:215–29 Erratum. 2008. Traffic 9:623–24
    [Google Scholar]
  27. Chou T, Kim KS, Oster G 2001. Statistical thermodynamics of membrane bending-mediated protein–protein attractions. Biophys. J. 80:1075–87
     [Google Scholar]
  28. Crouzet M, Urdaci M, Dulau L, Aigle M 1991. Yeast mutant affected for viability upon nutrient starvation: characterization and cloning of the RVS161 gene. Yeast 7:727–43
     [Google Scholar]
  29. Cui H, Lyman E, Voth GA 2011. Mechanism of membrane curvature sensing by amphipathic helix containing proteins. Biophys. J. 100:1271–79
     [Google Scholar]
  30. Dai Y, Ren D, Yang Q, Cui Y, Guo W et al. 2017. The TGF-β signalling negative regulator PICK1 represses prostate cancer metastasis to bone. Br. J. Cancer 117:685–94
     [Google Scholar]
  31. 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. PNAS 93:331–35
     [Google Scholar]
  32. De Camilli P, Thomas A, Cofiell R, Folli F, Lichte B et al. 1993. The synaptic vesicle-associated protein amphiphysin is the 128-kD autoantigen of Stiff-Man syndrome with breast cancer. J. Exp. Med. 178:2219–23
     [Google Scholar]
  33. De Matteis MA, Staiano L, Emma F, Devuyst O 2017. The 5-phosphatase OCRL in Lowe syndrome and Dent disease 2. Nat. Rev. Nephrol. 13:455–70
     [Google Scholar]
  34. Delage E, Cervantes DC, Penard E, Schmitt C, Syan S et al. 2016. Differential identity of Filopodia and Tunneling Nanotubes revealed by the opposite functions of actin regulatory complexes. Sci. Rep. 6:39632
     [Google Scholar]
  35. Di Fiore PP, von Zastrow M 2014. Endocytosis, signaling, and beyond. Cold Spring Harb. Perspect. Biol. 6:a016865
     [Google Scholar]
  36. Diggins NL, Webb DJ. 2017. APPL1 is a multifunctional endosomal signaling adaptor protein. Biochem. Soc. Trans. 45:771–79
     [Google Scholar]
  37. Dommersnes PG, Fournier JB. 1999. N-body study of anisotropic membrane inclusions: membrane mediated interactions and ordered aggregation. Eur. Phys. J. B 12:9–12
     [Google Scholar]
  38. Dong R, Saheki Y, Swarup S, Lucast L, Harper JW, De Camilli P 2016. Endosome-ER contacts control actin nucleation and retromer function through VAP-dependent regulation of PI4P. Cell 166:408–23
     [Google Scholar]
  39. Drin G, Antonny B. 2010. Amphipathic helices and membrane curvature. FEBS Lett 584:1840–47
     [Google Scholar]
  40. 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
     [Google Scholar]
  41. Frost A, Perera R, Roux A, Spasov K, Destaing O et al. 2008. Structural basis of membrane invagination by F-BAR domains. Cell 132:807–17
     [Google Scholar]
  42. Giachino C, Lantelme E, Lanzetti L, Saccone S, Bella Valle G, Migone N 1997. A novel SH3-containing human gene family preferentially expressed in the central nervous system. Genomics 41:427–34
     [Google Scholar]
  43. Goulian M, Bruinsma R, Pincus P 1993. Long-range forces in heterogeneous fluid membranes. Europhys. Lett. 22:145–50
     [Google Scholar]
  44. Heinrich MC, Capraro BR, Tian A, Isas JM, Langen R, Baumgart T 2010. Quantifying membrane curvature generation of Drosophila amphiphysin N-BAR domains. J. Phys. Chem. Lett. 1:3401–6
     [Google Scholar]
  45. Helfrich W. 1973. Elastic properties of lipid bilayers: theory and possible experiments. Z. Nat. C 28:693–703
     [Google Scholar]
  46. 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 15:839–52
     [Google Scholar]
  47. Hu J, Ye F, Cui M, Lee P, Wei C et al. 2016. Protein profiling of bladder urothelial cell carcinoma. PLOS ONE 11:e0161922
     [Google Scholar]
  48. Huang L-Y, Wang X, Cui XF, Li H, Zhao J et al. 2018. IRTKS is correlated with progression and survival time of patients with gastric cancer. Gut 67:1400–9
     [Google Scholar]
  49. Huang T, Zhou Y, Zhang J, Wong CC, Li W et al. 2018. SRGAP1, a crucial target of miR-340 and miR-124, functions as a potential oncogene in gastric tumorigenesis. Oncogene 37:1159–74
     [Google Scholar]
  50. Isas JM, Ambroso MR, Hegde PB, Langen J, Langen R 2015. Tubulation by amphiphysin requires concentration-dependent switching from wedging to scaffolding. Structure 23:873–81
     [Google Scholar]
  51. 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
     [Google Scholar]
  52. Johnson IR, Parkinson-Lawrence EJ, Keegan H, Spillane CD, Barry-O'Crowley J et al. 2015. Endosomal gene expression: a new indicator for prostate cancer patient prognosis. Oncotarget 6:37919–29
     [Google Scholar]
  53. Kalaidzidis I, Miaczynska M, Brewińska-Olchowik M, Hupalowska A, Ferguson C et al. 2015. APPL endosomes are not obligatory endocytic intermediates but act as stable cargo-sorting compartments. J. Cell Biol. 211:123–44
     [Google Scholar]
  54. Lee E, Marcucci M, Daniell L, Pypaert M, Weisz OA et al. 2002. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297:1193–96
     [Google Scholar]
  55. Leibler S, Andelman D. 1987. Ordered and curved meso-structures in membranes and amphiphilic films. J. Phys. 48:2013–18
     [Google Scholar]
  56. Lichte B, Veh RW, Meyer HE, Kilimann MW 1992. Amphiphysin, a novel protein associated with synaptic vesicles. EMBO J 11:2521–30
     [Google Scholar]
  57. Lipowsky R. 2013. Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Faraday Discuss 161:305–31
     [Google Scholar]
  58. Lu W, Khatri L, Ziff EB 2014. Trafficking of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPA) receptor subunit GluA2 from the endoplasmic reticulum is stimulated by a complex containing Ca2+/calmodulin-activated kinase II (CaMKII) and PICK1 protein and by release of Ca2+ from internal stores. J. Biol. Chem. 289:19218–30
     [Google Scholar]
  59. Madsen KL, Bhatia V, Gether U, Stamou D 2010. BAR domains, amphipathic helices and membrane‐anchored proteins use the same mechanism to sense membrane curvature. FEBS Lett 584:1848–55
     [Google Scholar]
  60. Mattila PK, Pykäläinen A, Saarikangas J, Paavilainen VO, Vihinen H et al. 2007. Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J. Cell Biol. 176:953–64
     [Google Scholar]
  61. McMahon HT, Boucrot E. 2011. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12:517–33
     [Google Scholar]
  62. Mellman I, Yarden Y. 2013. Endocytosis and cancer. Cold Spring Harb. Perspect. Biol. 5:a016949
     [Google Scholar]
  63. Mesarec L, Góźdź W, Kralj S, Fošnarič M, Penič S et al. 2017. On the role of external force of actin filaments in the formation of tubular protrusions of closed membrane shapes with anisotropic membrane components. Eur. Biophys. J. 46:705–18
     [Google Scholar]
  64. Millard TH, Bompard G, Heung MY, Dafforn TR, Scott DJ et al. 2005. Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. EMBO J 24:240–50
     [Google Scholar]
  65. Mim C, Cui H, Gawronski-Salerno JA, Frost A, Lyman E et al. 2012. Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149:137–45
     [Google Scholar]
  66. Neefjes J, Jongsma MML, Berlin I 2017. Stop or go? Endosome positioning in the establishment of compartment architecture, dynamics, and function. Trends Cell Biol 27:580–94
     [Google Scholar]
  67. Netz RR, Pincus P. 1995. Inhomogeneous fluid membranes: segregation, ordering, and effective rigidity. Phys. Rev. E 52:4114–28
     [Google Scholar]
  68. Nikolov V, Lipowsky R, Dimova R 2007. Behavior of giant vesicles with anchored DNA molecules. Biophys. J. 92:4356–68
     [Google Scholar]
  69. Nishimura T, Morone N, Suetsugu S 2018. Membrane re-modelling by BAR domain superfamily proteins via molecular and non-molecular factors. Biochem. Soc. Trans. 46:379–89
     [Google Scholar]
  70. Noguchi H. 2014. Two- or three-step assembly of banana-shaped proteins coupled with shape transformation of lipid membranes. Europhys. Lett. 108:48001
     [Google Scholar]
  71. Noguchi H. 2016. Membrane tubule formation by banana-shaped proteins with or without transient network structure. Sci. Rep. 6:20935
     [Google Scholar]
  72. Ogi S, Fujita H, Kashihara M, Yamamoto C, Sonoda K et al. 2013. Sorting nexin 2-mediated membrane trafficking of c-Met contributes to sensitivity of molecular-targeted drugs. Cancer Sci 104:573–83
     [Google Scholar]
  73. Pang X, Fan J, Zhang Y, Zhang K, Gao B et al. 2014. A PH domain in ACAP1 possesses key features of the BAR domain in promoting membrane curvature. Dev. Cell 31:73–86
     [Google Scholar]
  74. Park JM, Lubensky TC. 1996. Interactions between membrane inclusions on fluctuating membranes. J. Phys. I 6:1217–35
     [Google Scholar]
  75. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJG et al. 2004. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495–99
     [Google Scholar]
  76. Pinheiro NA, Caballero OL, Soares F, Reis LF, Simpson AJ 2001. Significant overexpression of oligophrenin-1 in colorectal tumors detected by cDNA microarray analysis. Cancer Lett 172:67–73
     [Google Scholar]
  77. Prevost C, Zhao H, Manzi J, Lemichez E, Lappalainen P et al. 2015. IRSp53 senses negative membrane curvature and phase separates along membrane tubules. Nat. Commun. 6:8529
     [Google Scholar]
  78. Pykäläinen A, Boczkowska M, Zhao HX, Saarikangas J, Rebowski G et al. 2011. Pinkbar is an epithelial-specific BAR domain protein that generates planar membrane structures. Nat. Struct. Mol. Biol. 18:902–7
     [Google Scholar]
  79. Qualmann B, Koch D, Kessels MM 2011. Let's go bananas: revisiting the endocytic BAR code. EMBO J 30:3501–15
     [Google Scholar]
  80. Ramakrishnan N, Sunil Kumar PB, Ipsen JH 2013. Membrane-mediated aggregation of curvature-inducing nematogens and membrane tubulation. Biophys. J. 104:1018–28
     [Google Scholar]
  81. Ramesh P, Baroji YF, Reihani SN, Stamou D, Oddershede LB, Bendix PM 2013. FBAR syndapin 1 recognizes and stabilizes highly curved tubular membranes in a concentration dependent manner. Sci. Rep. 3:1565
     [Google Scholar]
  82. Renard HF, Simunovic M, Lemiere J, Boucrot E, Garcia-Castillo MD et al. 2015. Endophilin-A2 functions in membrane scission in clathrin-independent endocytosis. Nature 517:493–96
     [Google Scholar]
  83. Rosselli-Murai LK, Yates JA, Yoshida S, Bourg J, Ho KKY et al. 2018. Loss of PTEN promotes formation of signaling-capable clathrin-coated pits. J. Cell Sci. 131:jcs208926
     [Google Scholar]
  84. Sakamuro D, Elliott KJ, Wechsler-Reya R, Prendergast GC 1996. BIN1 is a novel MYC-interacting protein with features of a tumour suppressor. Nat. Genet. 14:69–77
     [Google Scholar]
  85. Saric A, Cacciuto A. 2012. Mechanism of membrane tube formation induced by adhesive nanocomponents. Phys. Rev. Lett. 109:188101
     [Google Scholar]
  86. Sathe M, Muthukrishnan G, Rae J, Disanza A, Thattai M et al. 2018. Small GTPases and BAR domain proteins regulate branched actin polymerisation for clathrin and dynamin-independent endocytosis. Nat. Commun. 9:1835
     [Google Scholar]
  87. Scharaw S, Iskar M, Ori A, Boncompain G, Laketa V et al. 2016. The endosomal transcriptional regulator RNF11 integrates degradation and transport of EGFR. J. Cell Biol. 215:543–58
     [Google Scholar]
  88. Schmid SL. 2017. Reciprocal regulation of signaling and endocytosis: implications for the evolving cancer cell. J. Cell Biol. 216:2623–32
     [Google Scholar]
  89. Schweitzer Y, Kozlov MM. 2015. Membrane-mediated interaction between strongly anisotropic protein scaffolds. PLOS Comput. Biol. 11:e1004054
     [Google Scholar]
  90. Shi Z, Baumgart T. 2015. Membrane tension and peripheral protein density mediate membrane shape transitions. Nat. Commun. 6:5974
     [Google Scholar]
  91. Simunovic M, Evergren E, Golushko I, Prevost C, Renard HF et al. 2016a. How curvature-generating proteins build scaffolds on membrane nanotubes. PNAS 113:11226–31
     [Google Scholar]
  92. Simunovic M, Manneville JB, Renard HF, Evergren E, Raghunathan K et al. 2017a. Friction mediates scission of tubular membranes scaffolded by BAR proteins. Cell 170:172–84.e11
     [Google Scholar]
  93. Simunovic M, Mim C, Marlovits TC, Resch G, Unger VM, Voth GA 2013a. Protein-mediated transformation of lipid vesicles into tubular networks. Biophys. J. 105:711–19
     [Google Scholar]
  94. Simunovic M, Prevost C, Callan-Jones A, Bassereau P 2016b. Physical basis of some membrane shaping mechanisms. Philos. Trans. R. Soc. A 374:20160034
     [Google Scholar]
  95. Simunovic M, Saric A, Henderson JM, Lee KYC, Voth GA 2017b. Long-range organization of membrane-curving proteins. ACS Cent. Sci. 3:1246–53
     [Google Scholar]
  96. Simunovic M, Srivastava A, Voth GA 2013b. Linear aggregation of proteins on the membrane as a prelude to membrane remodeling. PNAS 110:20396–401
     [Google Scholar]
  97. Simunovic M, Voth GA. 2015. Membrane tension controls the assembly of curvature-generating proteins. Nat. Commun. 6:7219
     [Google Scholar]
  98. Simunovic M, Voth GA, Callan-Jones A, Bassereau P 2015. When physics takes over: BAR proteins and membrane curvature. Trends Cell Biol 25:780–92
     [Google Scholar]
  99. Sorre B, Callan-Jones A, Manzi J, Goud B, Prost J et al. 2012. Nature of curvature coupling of amphiphysin with membranes depends on its bound density. PNAS 109:173–78
     [Google Scholar]
  100. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, Sasaki DY et al. 2012. Membrane bending by protein–protein crowding. Nat. Cell Biol. 14:944–49
     [Google Scholar]
  101. Sundborger A, Soderblom C, Vorontsova O, Evergren E, Hinshaw JE, Shupliakov O 2011. An endophilin-dynamin complex promotes budding of clathrin-coated vesicles during synaptic vesicle recycling. J. Cell Sci. 124:133–43
     [Google Scholar]
  102. Takeda T, Kozai T, Yang H, Ishikuro D, Seyama K et al. 2018. Dynamic clustering of dynamin-amphiphysin helices regulates membrane constriction and fission coupled with GTP hydrolysis. eLife 7:e30246
     [Google Scholar]
  103. 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
     [Google Scholar]
  104. Tarricone C, Xiao B, Justin N, Walker PA, Rittinger K et al. 2001. The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways. Nature 411:215–19
     [Google Scholar]
  105. van Weering JR, Sessions RB, Traer CJ, Kloer DP, Bhatia VK et al. 2012. Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO J 31:4466–80
     [Google Scholar]
  106. Wang J, Jia Y, Zhao S, Zhang X, Wang X et al. 2017. BIN1 reverses PD-L1-mediated immune escape by inactivating the c-MYC and EGFR/MAPK signaling pathways in non-small cell lung cancer. Oncogene 36:6235–43
     [Google Scholar]
  107. Wu T, Shi Z, Baumgart T 2014. Mutations in BIN1 associated with centronuclear myopathy disrupt membrane remodeling by affecting protein density and oligomerization. PLOS ONE 9:e93060
     [Google Scholar]
  108. Xiao GY, Mohanakrishnan A, Schmid SL 2018. Role for ERK1/2-dependent activation of FCHSD2 in cancer cell-selective regulation of clathrin-mediated endocytosis. PNAS 115:E9570–79
     [Google Scholar]
  109. Zemel A, Ben-Shaul A, May S 2008. Modulation of the spontaneous curvature and bending rigidity of lipid membranes by interfacially adsorbed amphipathic peptides. J. Phys. Chem. B 112:6988–96
     [Google Scholar]
  110. Zhu C, Das SL, Baumgart T 2012. Nonlinear sorting, curvature generation, and crowding of endophilin N-BAR on tubular membranes. Biophys. J. 102:1837–45
     [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100617-060558
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Curving Cells Inside and Out: Roles of BAR Domain Proteins in Membrane Shaping and Its Cellular Implications
Annual Review of Cell and Developmental Biology 35, 111 (2019); https://doi.org/10.1146/annurev-cellbio-100617-060558
/content/journals/10.1146/annurev-cellbio-100617-060558
/content/journals/10.1146/annurev-cellbio-100617-060558
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