Abstract
The Bin–Amphiphysin–Rvs (BAR) domain is a membrane lipid binding domain present in a wide variety of proteins, often proteins with a role in Rho-regulated signaling pathways. BAR domains do not only confer binding to lipid bilayers, they also possess a membrane sculpturing ability and thereby directly control the topology of biomembranes. BAR domain-containing proteins participate in a plethora of physiological processes but the common denominator is their capacity to link membrane dynamics to actin dynamics and thereby integrate processes such as endocytosis, exocytosis, vesicle trafficking, cell morphogenesis and cell migration. The Rho family of small GTPases constitutes an important bridging theme for many BAR domain-containing proteins. This review article will focus predominantly on the role of BAR proteins as regulators or effectors of Rho GTPases and it will only briefly discuss the structural and biophysical function of the BAR domains.
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References
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(7):479–487
Aspenström P (2009) Roles of F-BAR/PCH proteins in the regulation of membrane dynamics and actin reorganization. Int Rev Cell Mol Biol 272:1–31. https://doi.org/10.1016/S1937-6448(08)01601-8
Aspenström P (2018) Fast-cycling Rho GTPases. Small GTPases 29:1–8. https://doi.org/10.1080/21541248.2017.1391365
Aspenström P, Richnau N, Johansson AS (2006) The diaphanous-related formin DAAM1 collaborates with the Rho GTPases RhoA and Cdc42, CIP4 and Src in regulating cell morphogenesis and actin dynamics. Exp Cell Res 312(12):2180–2194
Baek JI, Kwon SH, Zuo X, Choi SY, Kim SH, Lipschutz JH (2016) Dynamin binding protein (Tuba) deficiency inhibits ciliogenesis and nephrogenesis in vitro and in vivo. J Biol Chem 291(16):8632–8643. https://doi.org/10.1074/jbc.M115.688663
Bai X, Lenhart KC, Bird KE, Suen AA, Rojas M, Kakoki M, Li F, Smithies O, Mack CP, Taylor JM (2013) The smooth muscle-selective RhoGAP GRAF3 is a critical regulator of vascular tone and hypertension. Nat Commun 4:2910. https://doi.org/10.1038/ncomms3910
Ballard MS, Hinck L (2012) A roundabout way to cancer. Adv Cancer Res 114:187–235. https://doi.org/10.1016/B978-0-12-386503-8.00005-3
Bedford MT, Chan DC, Leder P (1997) FBP WW domains and the Abl SH3 domain bind to a specific class of proline-rich ligands. EMBO J 16(9):2376–2383
Billuart P, Bienvenu T, Ronce N, des Portes V, Vinet MC, Zemni R, Roest Crollius H, Carrié 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(6679):923–926
Bompard G, Sharp SJ, Freiss G, Machesky LM (2005) Involvement of Rac in actin cytoskeleton rearrangements induced by MIM-B. J Cell Sci 118(Pt 22):5393–5403
Bryant DM, Datta A, Rodríguez-Fraticelli AE, Peränen J, Martín-Belmonte F, Mostov KE (2010) A molecular network for de novo generation of the apical surface and lumen. Nat Cell Biol 12(11):1035–1045. https://doi.org/10.1038/ncb2106
Bu W, Lim KB, Yu YH, Chou AM, Sudhaharan T, Ahmed S (2010) Cdc42 interaction with N-WASP and Toca-1 regulates membrane tubulation, vesicle formation and vesicle motility: implications for endocytosis. PLoS One 5(8):e12153. https://doi.org/10.1371/journal.pone
Carnahan RH, Gould KL (2003) The PCH family protein, Cdc15p, recruits two F-actin nucleation pathways to coordinate cytokinetic actin ring formation in Schizosaccharomyces pombe. J Cell Biol 162(5):851–862
Cerqueira OL, Truesdell P, Baldassarre T, Vilella-Arias SA, Watt K, Meens J, Chander H, Osório CA, Soares FA, Reis EM, Craig AW (2015) CIP4 promotes metastasis in triple-negative breast cancer and is associated with poor patient prognosis. Oncotarget 6(11):9397–9408
Chang L, Adams RD, Saltiel AR (2002) The TC10-interacting protein CIP4/2 is required for insulin-stimulated Glut4 translocation in 3T3L1 adipocytes. Proc Natl Acad Sci U S A 99(20):12835–12840
Chen H, Wu X, Pan ZK, Huang S (2010) Integrity of SOS1/EPS8/ABI1 tri-complex determines ovarian cancer metastasis. Cancer Res 70(23):9979–9990. https://doi.org/10.1158/0008-5472.CAN-10-2394
Chesarone MA, DuPage AG, Goode BL (2010) Unleashing formins to remodel the actin and microtubule cytoskeleton. Nat Rev Mol Cell Biol 11(1):62–74. https://doi.org/10.1038/nrm2816
Chiang SH, Baumann CA, Kanzaki M, Thurmond DC, Watson RT, Neudauer CL, Macara IG, Pessin JE, Saltiel AR (2001) Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 410(6831):944–948
Cicchetti P, Mayer BJ, Thiel G, Baltimore D (1992) Identification of a protein that binds to the SH3 region of Abl and is similar to Bcr and GAP-rho. Science 257(5071):803–806. https://doi.org/10.1126/science.1379745
Connolly BA, Rice J, Feig LA, Buchsbaum RJ (2005) Tiam1-IRSp53 complex formation directs specificity of rac-mediated actin cytoskeleton regulation. Mol Cell Biol 25(11):4602–4614. Erratum in: Mol Cell Biol 25(17):7928
Cook DR, Rossman KL, Der CJ (2014) Rho guanine nucleotide exchange factors: regulators of Rho GTPase activity in development and disease. Oncogene 33(31):4021–4035. https://doi.org/10.1038/onc.2013.362
Coutinho-Budd J, Ghukasyan V, Zylka MJ, Polleux F (2012) The F-BAR domains from srGAP1, srGAP2 and srGAP3 regulate membrane deformation differently. J Cell Sci 125(Pt 14):3390–3401. https://doi.org/10.1242/jcs.098962
Csépányi-Kömi R, Sáfár D, Grósz V, Tarján ZL, Ligeti E (2013) In silico tissue-distribution of human Rho family GTPase activating proteins. Small GTPases 4(2):90–101. https://doi.org/10.4161/sgtp.23708
Dawson JC, Bruche S, Spence HJ, Braga VM, Machesky LM (2012) Mtss1 promotes cell-cell junction assembly and stability through the small GTPase Rac1. PLoS One 7(3):e31141. https://doi.org/10.1371/journal.pone.0031141
de Kreuk BJ, Nethe M, Fernandez-Borja M, Anthony EC, Hensbergen PJ, Deelder AM, Plomann M, Hordijk PL (2011) The F-BAR domain protein PACSIN2 associates with Rac1 and regulates cell spreading and migration. J Cell Sci 124(Pt 14):2375–2388. https://doi.org/10.1242/jcs.080630
de Kreuk BJ, Schaefer A, Anthony EC, Tol S, Fernandez-Borja M, Geerts D, Pool J, Hambach L, Goulmy E, Hordijk PL (2013) The human minor histocompatibility antigen1 is a RhoGAP. PLoS One 8(9):e73962. https://doi.org/10.1371/journal.pone.0073962 eCollection 2013
DerMardirossian C, Bokoch GM (2005) GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol 15(7):356–363
Disanza A, Mantoani S, Hertzog M, Gerboth S, Frittoli E, Steffen A, Berhoerster K, Kreienkamp HJ, Milanesi F, Di Fiore PP, Ciliberto A, Stradal TE, Scita G (2006) Regulation of cell shape by Cdc42 is mediated by the synergic actin-bundling activity of the Eps8-IRSp53 complex. Nat Cell Biol 8(12):1337–1347
Doherty GJ, Åhlund MK, Howes MT, Morén B, Parton RG, McMahon HT, Lundmark R (2011) The endocytic protein GRAF1 is directed to cell-matrix adhesion sites and regulates cell spreading. Mol Biol Cell 22(22):4380–4389. https://doi.org/10.1091/mbc.E10-12-0936
DuHadaway JB, Du W, Donover S, Baker J, Liu AX, Sharp DM, Muller AJ, Prendergast GC (2003) Transformation-selective apoptotic program triggered by farnesyltransferase inhibitors requires Bin1. Oncogene 22(23):3578–3588
Elbediwy A, Zihni C, Terry SJ, Clark P, Matter K, Balda MS (2012) Epithelial junction formation requires confinement of Cdc42 activity by a novel SH3BP1 complex. J Cell Biol 198(4):677–693. https://doi.org/10.1083/jcb.201202094
Endris V, Wogatzky B, Leimer U, Bartsch D, Zatyka M, Latif F, Maher ER, Tariverdian G, Kirsch S, Karch D, Rappold GA (2002) The novel Rho-GTPase activating gene MEGAP/srGAP3 has a putative role in severe mental retardation. Proc Natl Acad Sci U S A 99(18):11754–11759
Foletta VC, Brown FD, Young WS 3rd (2002) Cloning of rat ARHGAP4/C1, a RhoGAP family member expressed in the nervous system that colocalizes with the Golgi complex and microtubules. Brain Res Mol Brain Res 107(1):65–79
Francis MK, Holst MR, Vidal-Quadras M, Henriksson S, Santarella-Mellwig R, Sandblad L, Lundmark R (2015) Endocytic membrane turnover at the leading edge is driven by a transient interaction between Cdc42 and GRAF1. J Cell Sci 128(22):4183–4195. https://doi.org/10.1242/jcs.174417
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(5):807–817. https://doi.org/10.1016/j.cell.2007.12.041
Funato Y, Terabayashi T, Suenaga N, Seiki M, Takenawa T, Miki H (2004) IRSp53/Eps8 complex is important for positive regulation of Rac and cancer cell motility/invasiveness. Cancer Res 64(15):5237–5244
Goh WI, Lim KB, Sudhaharan T, Sem KP, Bu W, Chou AM, Ahmed S (2012) mDia1 and WAVE2 proteins interact directly with IRSp53 in filopodia and are involved in filopodium formation. J Biol Chem 287(7):4702–4714. https://doi.org/10.1074/jbc.M111.305102
Govek EE, Newey SE, Akerman CJ, Cross JR, Van der Veken L, Van Aelst L (2004) The X-linked mental retardation protein oligophrenin-1 is required for dendritic spine morphogenesis. Nat Neurosci 7(4):364–372
Govind S, Kozma R, Monfries C, Lim L, Ahmed S (2001) Cdc42Hs facilitates cytoskeletal reorganization and neurite outgrowth by localizing the 58-kD insulin receptor substrate to filamentous actin. J Cell Biol 152(3):579–594
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(5):990–1004. https://doi.org/10.1016/j.cell.2009.06.047
Harada A, Furuta B, Takeuchi K, Itakura M, Takahashi M, Umeda M (2000) Nadrin, a novel neuron-specific GTPase-activating protein involved in regulated exocytosis. J Biol Chem 275(47):36885–36891
Hatzoglou A, Ader I, Splingard A, Flanders J, Saade E, Leroy I, Traver S, Aresta S, de Gunzburg J (2007) Gem associates with Ezrin and acts via the Rho-GAP protein Gmip to down-regulate the Rho pathway. Mol Biol Cell 18(4):1242–1252
Herrington KA, Trinh AL, Dang C, O’Shaughnessy E, Hahn KM, Gratton E, Digman MA, Sütterlin C (2017) Spatial analysis of Cdc42 activity reveals a role for plasma membrane-associated Cdc42 in centrosome regulation. Mol Biol Cell 28(15):2135–2145. https://doi.org/10.1091/mbc
Hildebrand JD, Taylor JM, Parsons JT (1996) An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol Cell Biol 16(6):3169–3178
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(2):203–216
Holst MR, Vidal-Quadras M, Larsson E, Song J, Hubert M, Blomberg J, Lundborg M, Landström M, Lundmark R (2017) Clathrin-independent endocytosis suppresses cancer cell blebbing and invasion. Cell Rep 20(8):1893–1905. https://doi.org/10.1016/j.celrep.2017.08.006
Hou JC, Pessin JE (2007) Ins (endocytosis) and outs (exocytosis) of GLUT4 trafficking. Curr Opin Cell Biol 19(4):466–473
Houy S, Estay-Ahumada C, Croisé P, Calco V, Haeberlé AM, Bailly Y, Billuart P, Vitale N, Bader MF, Ory S, Gasman S (2015) Oligophrenin-1 connects Exocytotic fusion to compensatory endocytosis in neuroendocrine cells. J Neurosci 35(31):11045–11055. https://doi.org/10.1523/JNEUROSCI.4048-14.2015
Hu J, Troglio F, Mukhopadhyay A, Everingham S, Kwok E, Scita G, Craig AW (2009) F-BAR-containing adaptor CIP4 localizes to early endosomes and regulates epidermal growth factor receptor trafficking and downregulation. Cell Signal 21(11):1686–1697. https://doi.org/10.1016/j.cellsig.2009.07.007
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(6):791–804
Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269
Jarius S, Wildemann B, Stöcker W, Moser A, Wandinger KP (2015) Psychotic syndrome associated with anti-Ca/ARHGAP26 and voltage-gated potassium channel antibodies. J Neuroimmunol 286:79–82. https://doi.org/10.1016/j.jneuroim.2015.07.009
Johnson JL, Monfregola J, Napolitano G, Kiosses WB, Catz SD (2012) Vesicular trafficking through cortical actin during exocytosis is regulated by the Rab27a effector JFC1/Slp1 and the RhoA-GTPase-activating protein gem-interacting protein. Mol Biol Cell 23(10):1902–1916. https://doi.org/10.1091/mbc.E11-12-1001
Khelfaoui M, Pavlowsky A, Powell AD, Valnegri P, Cheong KW, Blandin Y, Passafaro M, Jefferys JG, Chelly J, Billuart P (2009) Inhibition of RhoA pathway rescues the endocytosis defects in Oligophrenin1 mouse model of mental retardation. Hum Mol Genet 18(14):2575–2583. https://doi.org/10.1093/hmg/ddp189
Kodani A, Kristensen I, Huang L, Sütterlin C (2009) GM130-dependent control of Cdc42 activity at the Golgi regulates centrosome organization. Mol Biol Cell 20(4):1192–1200. https://doi.org/10.1091/mbc.E08-08-0834
Koeppel MA, McCarthy CC, Moertl E, Jakobi R (2004) Identification and characterization of PS-GAP as a novel regulator of caspase-activated PAK-2. J Biol Chem 279(51):53653–53664
Kovacs EM, Makar RS, Gertler FB (2006) Tuba stimulates intracellular N-WASP-dependent actin assembly. J Cell Sci 119(Pt 13):2715–2726
Kovacs EM, Verma S, Thomas SG, Yap AS (2011) Tuba and N-WASP function cooperatively to position the central lumen during epithelial cyst morphogenesis. Cell Adhes Migr 5(4):344–350
Krugmann S, Jordens I, Gevaert K, Driessens M, Vandekerckhove J, Hall A (2001) Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Curr Biol 11(21):1645–1655
Lee SY, Kim H, Kim K, Lee H, Lee S, Lee D (2016) Arhgap17, a RhoGTPase activating protein, regulates mucosal and epithelial barrier function in the mouse colon. Sci Rep 6:26923. https://doi.org/10.1038/srep26923
Lenhart KC, Becherer AL, Li J, Xiao X, McNally EM, Mack CP, Taylor JM (2014) GRAF1 promotes ferlin-dependent myoblast fusion. Dev Biol 393(2):298–311. https://doi.org/10.1016/j.ydbio.2014.06.025
Liu F, Guo H, Ou M, Hou X, Sun G, Gong W, Jing H, Tan Q, Xue W, Dai Y, Sui W (2016) ARHGAP4 mutated in a Chinese intellectually challenged family. Gene 578(2):205–209. https://doi.org/10.1016/j.gene.2015.12.035
Lodhi IJ, Chiang SH, Chang L, Vollenweider D, Watson RT, Inoue M, Pessin JE, Saltiel AR (2007) Gapex-5, a Rab31 guanine nucleotide exchange factor that regulates Glut4 trafficking in adipocytes. Cell Metab 5(1):59–72
Lucken-Ardjomande Häsler S, Vallis Y, Jolin HE, McKenzie AN, McMahon HT (2014) GRAF1a is a brain-specific protein that promotes lipid droplet clustering and growth, and is enriched at lipid droplet junctions. J Cell Sci 127(Pt 21):4602–4619. https://doi.org/10.1242/jcs.147694
Lundmark R, Doherty GJ, Howes MT, Cortese K, Vallis Y, Parton RG, McMahon HT (2008) The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr Biol 18(22):1802–1808. https://doi.org/10.1016/j.cub.2008.10.044
Luo N, Guo J, Chen L, Yang W, Qu X, Cheng Z (2016) ARHGAP10, downregulated in ovarian cancer, suppresses tumorigenicity of ovarian cancer cells. Cell Death Dis 7:e2157. https://doi.org/10.1038/cddis.2015.401
Luo W, Janoštiak R, Tolde O, Ryzhova LM, Koudelková L, Dibus M, Brábek J, Hanks SK, Rosel D (2017) ARHGAP42 is activated by Src-mediated tyrosine phosphorylation to promote cell motility. J Cell Sci 130(14):2382–2393. https://doi.org/10.1242/jcs.197434
Ma Y, Mi YJ, Dai YK, Fu HL, Cui DX, Jin WL (2013) The inverse F-BAR domain protein srGAP2 acts through srGAP3 to modulate neuronal differentiation and neurite outgrowth of mouse neuroblastoma cells. PLoS One 8(3):e57865. https://doi.org/10.1371/journal.pone.0057865
Madaule P, Axel R (1985) A novel Ras-related gene family. Cell 41(1):31–40. https://doi.org/10.1016/0092-8674(85)90058-3
Madura T, Yamashita T, Kubo T, Tsuji L, Hosokawa K, Tohyama M (2004) Changes in mRNA of Slit-Robo GTPase-activating protein 2 following facial nerve transection. Brain Res Mol Brain Res 123(1–2):76–80
Mattila PK, Pykäläinen A, Saarikangas J, Paavilainen VO, Vihinen H, Jokitalo E, Lappalainen P (2007) Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J Cell Biol 176(7):953–964
Meng DF, Xie P, Peng LX, Sun R, Luo DH, Chen QY, Lv X, Wang L, Chen MY, Mai HQ, Guo L, Guo X, Zheng LS, Cao L, Yang JP, Wang MY, Mei Y, Qiang YY, Zhang ZM, Yun JP, Huang BJ, Qian CN (2017) CDC42-interacting protein 4 promotes metastasis of nasopharyngeal carcinoma by mediating invadopodia formation and activating EGFR signaling. Exp Clin Cancer Res 36(1):21. https://doi.org/10.1186/s13046-016-0483-z. Erratum in: J Exp Clin Cancer Res 36(1):33
Miki H, Yamaguchi H, Suetsugu S, Takenawa T (2000) IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408(6813):732–735
Millard TH, Bompard G, Heung MY, Dafforn TR, Scott DJ, Machesky LM, Fütterer K (2005) Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. EMBO J 24(2):240–250
Millard TH, Dawson J, Machesky LM (2007) Characterisation of IRTKS, a novel IRSp53/MIM family actin regulator with distinct filament bundling properties. J Cell Sci 120(Pt 9):1663–1672
Mim C, Cui H, Gawronski-Salerno JA, Frost A, Lyman E, Voth GA, Unger VM (2012) Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149(1):137–145. https://doi.org/10.1016/j.cell.2012.01.048
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(13):1133–1139. https://doi.org/10.1016/j.cub.2009.05.022
Otani T, Ichii T, Aono S, Takeichi M (2006) Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells. J Cell Biol 175(1):135–146
Parrini MC, Sadou-Dubourgnoux A, Aoki K, Kunida K, Biondini M, Hatzoglou A, Poullet P, Formstecher E, Yeaman C, Matsuda M, Rossé C, Camonis J (2011) SH3BP1, an exocyst-associated RhoGAP, inactivates Rac1 at the front to drive cell motility. Mol Cell 42(5):650–661. https://doi.org/10.1016/j.molcel.2011.03.032
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(5657):495–499
Post A, Pannekoek WJ, Ross SH, Verlaan I, Brouwer PM, Bos JL (2013) Rasip1 mediates Rap1 regulation of Rho in endothelial barrier function through ArhGAP29. Proc Natl Acad Sci U S A 110(28):11427–121432. https://doi.org/10.1073/pnas.1306595110
Post A, Pannekoek WJ, Ponsioen B, Vliem MJ, Bos JL (2015) Rap1 spatially controls ArhGAP29 to inhibit Rho signaling during endothelial barrier regulation. Mol Cell Biol 35(14):2495–2502. https://doi.org/10.1128/MCB.01453-14
Pykäläinen A, Boczkowska M, Zhao H, Saarikangas J, Rebowski G, Jansen M, Hakanen J, Koskela EV, Peränen J, Vihinen H, Jokitalo E, Salminen M, Ikonen E, Dominguez R, Lappalainen P (2011) Pinkbar is an epithelial-specific BAR domain protein that generates planar membrane structures. Nat Struct Mol Biol 18(8):902–907. https://doi.org/10.1038/nsmb.2079
Qiao Y, Chen J, Lim YB, Finch-Edmondson ML, Seshachalam VP, Qin L, Jiang T, Low BC, Singh H, Lim CT, Sudol M (2017) YAP regulates actin dynamics through ARHGAP29 and promotes metastasis. Cell Rep 19(8):1495–1502. https://doi.org/10.1016/j.celrep.2017.04.075
Qin Y, Meisen WH, Hao Y, Macara IG (2010) Tuba, a Cdc42 GEF, is required for polarized spindle orientation during epithelial cyst formation. J Cell Biol 189(4):661–669. https://doi.org/10.1083/jcb.201002097
Qualmann B, Koch D, Kessels MM (2011) Let’s go bananas: revisiting the endocytic BAR code. EMBO J 30(17):3501–3515. https://doi.org/10.1038/emboj.2011.266
Raynaud F, Janossy A, Dahl J, Bertaso F, Perroy J, Varrault A, Vidal M, Worley PF, Boeckers TM, Bockaert J, Marin P, Fagni L, Homburger V (2013) Shank3-Rich2 interaction regulates AMPA receptor recycling and synaptic long-term potentiation. J Neurosci 33(23):9699–9715. https://doi.org/10.1523/JNEUROSCI.2725-12.2013
Raynaud F, Moutin E, Schmidt S, Dahl J, Bertaso F, Boeckers TM, Homburger V, Fagni L (2014) Rho-GTPase-activating protein interacting with Cdc-42-interacting protein 4 homolog 2 (Rich2): a new Ras-related C3 botulinum toxin substrate 1 (Rac1) GTPase-activating protein that controls dendritic spine morphogenesis. J Biol Chem 289(5):2600–2609. https://doi.org/10.1074/jbc.M113.534636
Ren R, Mayer BJ, Cicchetti P, Baltimore D (1993) Identification of a ten-amino acid proline-rich SH3 binding site. Science 259(5098):1157–1161. https://doi.org/10.1126/science.8438166
Ren XR, Du QS, Huang YZ, Ao SZ, Mei L, Xiong WC (2001) Regulation of CDC42 GTPase by proline-rich tyrosine kinase 2 interacting with PSGAP, a novel pleckstrin homology and Src homology 3 domain containing rhoGAP protein. J Cell Biol 152(5):971–984
Richnau N, Aspenström P (2001) Rich, a rho GTPase-activating protein domain-containing protein involved in signaling by Cdc42 and Rac1. J Biol Chem 276(37):35060–35070
Rodal AA, Motola-Barnes RN, Littleton JT (2008) Nervous wreck and Cdc42 cooperate to regulate endocytic actin assembly during synaptic growth. J Neurosci 28(33):8316–8325. https://doi.org/10.1523/JNEUROSCI.2304-08.2008
Rollason R, Korolchuk V, Hamilton C, Jepson M, Banting G (2009) A CD317/tetherin-RICH2 complex plays a critical role in the organization of the subapical actin cytoskeleton in polarized epithelial cells. J Cell Biol 184(5):721–736. https://doi.org/10.1083/jcb.200804154
Rotty JD, Wu C, Bear JE (2013) New insights into the regulation and cellular functions of the ARP2/3 complex. Nat Rev Mol Cell Biol 14(1):7–12. https://doi.org/10.1038/nrm3492
Saengsawang W, Mitok K, Viesselmann C, Pietila L, Lumbard DC, Corey SJ, Dent EW (2012) The F-BAR protein CIP4 inhibits neurite formation by producing lamellipodial protrusions. Curr Biol 22(6):494–501. https://doi.org/10.1016/j.cub.2012.01.038
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. https://doi.org/10.1038/ng0996-69
Salazar MA, Kwiatkowski AV, Pellegrini L, Cestra G, Butler MH, Rossman KL, Serna DM, Sondek J, Gertler FB, De Camilli P (2003) Tuba, a novel protein containing bin/amphiphysin/Rvs and Dbl homology domains, links dynamin to regulation of the actin cytoskeleton. J Biol Chem 278(49):49031–49043
Salzer U, Kostan J, Djinović-Carugo K (2017) Deciphering the BAR code of membrane modulators. Cell Mol Life Sci 74(13):2413–2438. https://doi.org/10.1007/s00018-017-2478-0
Saras J, Franzén P, Aspenström P, Hellman U, Gonez LJ, Heldin CH (1997) A novel GTPase-activating protein for Rho interacts with a PDZ domain of the protein-tyrosine phosphatase PTPL1. J Biol Chem 272(39):24333–24338
Sarowar T, Grabrucker S, Föhr K, Mangus K, Eckert M, Bockmann J, Boeckers TM, Grabrucker AM (2016) Enlarged dendritic spines and pronounced neophobia in mice lacking the PSD protein RICH2. Mol Brain 9:28. https://doi.org/10.1186/s13041-016-0206-6
Savastano CP, Brito LA, Faria ÁC, Setó-Salvia N, Peskett E, Musso CM, Alvizi L, Ezquina SA, James C, GOSgene, Beales P, Lees M, Moore GE, Stanier P, Passos-Bueno MR (2017) Impact of rare variants in ARHGAP29 to the etiology of oral clefts: role of loss-of-function vs missense variants. Clin Genet 91(5):683–689. https://doi.org/10.1111/cge.12823
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, Tanaka A, Sugano S, Shirouzu M, Nagayama K, Takenawa T, Yokoyama S (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129(4):761–772
Simionescu-Bankston A, Leoni G, Wang Y, Pham PP, Ramalingam A, DuHadaway JB, Faundez V, Nusrat A, Prendergast GC, Pavlath GK (2013) The N-BAR domain protein, Bin3, regulates Rac1- and Cdc42-dependent processes in myogenesis. Dev Biol 382(1):160–171. https://doi.org/10.1016/j.ydbio.2013.07.004
Soderling SH, Binns KL, Wayman GA, Davee SM, Ong SH, Pawson T, Scott JD (2002) The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nat Cell Biol 4(12):970–975
Soderling SH, Guire ES, Kaech S, White J, Zhang F, Schutz K, Langeberg LK, Banker G, Raber J, Scott JD (2007) A WAVE-1 and WRP signaling complex regulates spine density, synaptic plasticity, and memory. J Neurosci 27(2):355–365
Sousa S, Cabanes D, Archambaud C, Colland F, Lemichez E, Popoff M, Boisson-Dupuis S, Gouin E, Lecuit M, Legrain P, Cossart P (2005) ARHGAP10 is necessary for alpha-catenin recruitment at adherens junctions and for Listeria invasion. Nat Cell Biol 7(10):954–960
Sudhaharan T, Sem KP, Liew HF, Yu YH, Goh WI, Chou AM, Ahmed S (2016) The Rho GTPase Rif signals through IRTKS, Eps8 and WAVE2 to generate dorsal membrane ruffles and filopodia. J Cell Sci 129(14):2829–2840. https://doi.org/10.1242/jcs.179655
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(46):35347–33558
Sweitzer SM, Hinshaw JE (1998) Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93(6):1021–1029
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(21):2817–2828. https://doi.org/10.1038/emboj.2008.216
Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1(1):33–39
Taylor MJ, Perrais D, Merrifield CJ (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9(3):e1000604. https://doi.org/10.1371/journal.pbio.1000604
Tcherkezian J, Lamarche-Vane N (2007) Current knowledge of the large RhoGAP family of proteins. Biol Cell 99(2):67–86
Toguchi M, Richnau N, Ruusala A, Aspenström P (2010) Members of the CIP4 family of proteins participate in the regulation of platelet-derived growth factor receptor-beta-dependent actin reorganization and migration. Biol Cell 102(4):215–230. https://doi.org/10.1042/BC20090033
Tonucci FM, Hidalgo F, Ferretti A, Almada E, Favre C, Goldenring JR, Kaverina I, Kierbel A, Larocca MC (2015) Centrosomal AKAP350 and CIP4 act in concert to define the polarized localization of the centrosome and Golgi in migratory cells. J Cell Sci 128(17):3277–3289. https://doi.org/10.1242/jcs.170878
Truesdell P, Ahn J, Chander H, Meens J, Watt K, Yang X, Craig AW (2015) CIP4 promotes lung adenocarcinoma metastasis and is associated with poor prognosis. Oncogene 34(27):3527–3535. https://doi.org/10.1038/onc.2014.280
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(2):269–279
Tsujita K, Takenawa T, Itoh T (2015) Feedback regulation between plasma membrane tension and membrane-bending proteins organizes cell polarity during leading edge formation. Nat Cell Biol 17(6):749–758. https://doi.org/10.1038/ncb3162
Vidal-Quadras M, Holst MR, Francis MK, Larsson E, Hachimi M, Yau WL, Peränen J, Martín-Belmonte F, Lundmark R (2017) Endocytic turnover of Rab8 controls cell polarization. J Cell Sci 130(6):1147–1157. https://doi.org/10.1242/jcs.195420
Vogt DL, Gray CD, Young WS 3rd, Orellana SA, Malouf AT (2007) ARHGAP4 is a novel RhoGAP that mediates inhibition of cell motility and axon outgrowth. Mol Cell Neurosci 36(3):332–342
Wakita Y, Kakimoto T, Katoh H, Negishi M (2011) The F-BAR protein Rapostlin regulates dendritic spine formation in hippocampal neurons. J Biol Chem 286(37):32672–32683. https://doi.org/10.1074/jbc.M111.236265
Wallwitz U, Brock S, Schunck A, Wildemann B, Jarius S, Hoffmann F (2017) From dizziness to severe ataxia and dysarthria: new cases of anti-Ca/ARHGAP26 autoantibody-associated cerebellar ataxia suggest a broad clinical spectrum. J Neuroimmunol 309:77–81. https://doi.org/10.1016/j.jneuroim.2017.05.011
Waltereit R, Leimer U, von Bohlen Und Halbach O, Panke J, Hölter SM, Garrett L, Wittig K, Schneider M, Schmitt C, Calzada-Wack J, Neff F, Becker L, Prehn C, Kutscherjawy S, Endris V, Bacon C, Fuchs H, Gailus-Durner V, Berger S, Schönig K, Adamski J, Klopstock T, Esposito I, Wurst W, de Angelis MH, Rappold G, Wieland T, Bartsch D (2012) Srgap3-/- mice present a neurodevelopmental disorder with schizophrenia-related intermediate phenotypes. FASEB J 26(11):4418–4428. https://doi.org/10.1096/fj.11-202317
Watson JR, Fox HM, Nietlispach D, Gallop JL, Owen D, Mott HR (2016) Investigation of the interaction between Cdc42 and its effector TOCA1: handover of cdc42 to the actin regulator N-WASP is facilitated by differential binding affinities. J Biol Chem 291(26):13875–13890. https://doi.org/10.1074/jbc.M116.724294
Wells CD, Fawcett JP, Traweger A, Yamanaka Y, Goudreault M, Elder K, Kulkarni S, Gish G, Virag C, Lim C, Colwill K, Starostine A, Metalnikov P, Pawson T (2006) A Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells. Cell 125(3):535–548
Wong K, Ren XR, Huang YZ, Xie Y, Liu G, Saito H, Tang H, Wen L, Brady-Kalnay SM, Mei L, Wu JY, Xiong WC, Rao Y (2001) Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 107(2):209–221
Yamagishi A, Masuda M, Ohki T, Onishi H, Mochizuki N (2004) A novel actin bundling/filopodium-forming domain conserved in insulin receptor tyrosine kinase substrate p53 and missing in metastasis protein. J Biol Chem 279(15):14929–14936
Yan S, Lv Z, Winterhoff M, Wenzl C, Zobel T, Faix J, Bogdan S, Grosshans J (2013) The F-BAR protein Cip4/Toca-1 antagonizes the formin diaphanous in membrane stabilization and compartmentalization. J Cell Sci 126(Pt 8):1796–1805. https://doi.org/10.1242/jcs.118422
Yao F, Kausalya JP, Sia YY, Teo AS, Lee WH, Ong AG, Zhang Z, Tan JH, Li G, Bertrand D, Liu X, Poh HM, Guan P, Zhu F, Pathiraja TN, Ariyaratne PN, Rao J, Woo XY, Cai S, Mulawadi FH, Poh WT, Veeravalli L, Chan CS, Lim SS, Leong ST, Neo SC, Choi PS, Chew EG, Nagarajan N, Jacques PÉ, So JB, Ruan X, Yeoh KG, Tan P, Sung WK, Hunziker W, Ruan Y, Hillmer AM (2015) Recurrent fusion genes in gastric cancer: CLDN18-ARHGAP26 induces loss of epithelial integrity. Cell Rep 12(2):272–285. https://doi.org/10.1016/j.celrep.2015.06.020
Yi C, Troutman S, Fera D, Stemmer-Rachamimov A, Avila JL, Christian N, Persson NL, Shimono A, Speicher DW, Marmorstein R, Holmgren L, Kissil JL (2011) A tight junction-associated Merlin-angiomotin complex mediates Merlin’s regulation of mitogenic signaling and tumor suppressive functions. Cancer Cell 19(4):527–540. https://doi.org/10.1016/j.ccr.2011.02.017
Zhao H, Pykäläinen A, Lappalainen P (2011) I-BAR domain proteins: linking actin and plasma membrane dynamics. Curr Opin Cell Biol 23(1):14–21. https://doi.org/10.1016/j.ceb.2010.10.005
Zhao H, Michelot A, Koskela EV, Tkach V, Stamou D, Drubin DG, Lappalainen P (2013) Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep 4(6):1213–1223. https://doi.org/10.1016/j.celrep.2013.08.024
Zheng D, Niu S, Yu D, Zhan XH, Zeng X, Cui B, Chen Y, Yoon J, Martin SS, Lu X, Zhan X (2010) Abba promotes PDGF-mediated membrane ruffling through activation of the small GTPase Rac1. Biochem Biophys Res Commun 401(4):527–532. https://doi.org/10.1016/j.bbrc.2010.09.087
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PA has been supported by grants from the Swedish Cancer Society and Karolinska Institutet.
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Aspenström, P. (2018). BAR Domain Proteins Regulate Rho GTPase Signaling. In: Atassi, M. (eds) Protein Reviews – Purinergic Receptors. Advances in Experimental Medicine and Biology(), vol 1111. Springer, Cham. https://doi.org/10.1007/5584_2018_259
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