The Crystal Structure of the BAR Domain from Human Bin1/amphiphysin II and Its Implications for Molecular Recognition

Overview

Journal Biochemistry

Specialty Biochemistry

Date 2006 Oct 25

PMID 17059209

Citations 41

Authors

Eva Casal

Luca Federici

Wei Zhang

Juan Fernandez-Recio

Eva-Maria Priego

Ricardo Nunez Miguel

James B DuHadaway

George C Prendergast

Ben F Luisi

Ernest D Laue

Affiliations

Soon will be listed here.

Abstract

BAR domains are found in proteins that bind and remodel membranes and participate in cytoskeletal and nuclear processes. Here, we report the crystal structure of the BAR domain from the human Bin1 protein at 2.0 A resolution. Both the quaternary and tertiary architectures of the homodimeric Bin1BAR domain are built upon "knobs-into-holes" packing of side chains, like those found in conventional left-handed coiled-coils, and this packing governs the curvature of a putative membrane-engaging concave face. Our calculations indicate that the Bin1BAR domain contains two potential sites for protein-protein interactions on the convex face of the dimer. Comparative analysis of structural features reveals that at least three architectural subtypes of the BAR domain are encoded in the human genome, represented by the Arfaptin, Bin1/Amphiphysin, and IRSp53 BAR domains. We discuss how these principal groups may differ in their potential to form regulatory heterotypic interactions.

Citing Articles

Dynamics of membrane tubulation coupled with fission by a two-component module.

Bhattacharyya S, Pucadyil T Proc Natl Acad Sci U S A. 2024; 121(20):e2402180121.

PMID: 38717859 PMC: 11098101. DOI: 10.1073/pnas.2402180121.

BIN1 in the Pursuit of Ousting the Alzheimer's Reign: Impact on Amyloid and Tau Neuropathology.

Kaur I, Behl T, Sundararajan G, Panneerselvam P, Vijayakumar A, Senthilkumar G Neurotox Res. 2023; 41(6):698-707.

PMID: 37847429 DOI: 10.1007/s12640-023-00670-3.

Syndapin and GTPase RAP-1 control endocytic recycling via RHO-1 and non-muscle myosin II.

Rodriguez-Polanco W, Norris A, Velasco A, Gleason A, Grant B Curr Biol. 2023; 33(22):4844-4856.e5.

PMID: 37832552 PMC: 10841897. DOI: 10.1016/j.cub.2023.09.051.

Centronuclear Myopathy Caused by Defective Membrane Remodelling of Dynamin 2 and BIN1 Variants.

Fujise K, Noguchi S, Takeda T Int J Mol Sci. 2022; 23(11).

PMID: 35682949 PMC: 9181712. DOI: 10.3390/ijms23116274.

Unfolding Mechanisms and Conformational Stability of the Dimeric Endophilin N-BAR Domain.

Jin R, Grasso M, Zhou M, Marmorstein R, Baumgart T ACS Omega. 2021; 6(32):20790-20803.

PMID: 34423187 PMC: 8374900. DOI: 10.1021/acsomega.1c01905.

References

Murshudov G, Vagin A, Lebedev A, Wilson K, Dodson E . Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr D Biol Crystallogr. 1999; 55(Pt 1):247-55. DOI: 10.1107/S090744499801405X. View

Razzaq A, Su Y, Mehren J, Mizuguchi K, Jackson A, Gay N . Characterisation of the gene for Drosophila amphiphysin. Gene. 1999; 241(1):167-74. DOI: 10.1016/s0378-1119(99)00451-5. View

Pandit J, Danley D, Schulte G, Mazzalupo S, Pauly T, Hayward C . Crystal structure of human squalene synthase. A key enzyme in cholesterol biosynthesis. J Biol Chem. 2000; 275(39):30610-7. DOI: 10.1074/jbc.M004132200. View

Vagin A, Teplyakov A . An approach to multi-copy search in molecular replacement. Acta Crystallogr D Biol Crystallogr. 2000; 56(Pt 12):1622-4. DOI: 10.1107/s0907444900013780. View

Miki H, Yamaguchi H, Suetsugu S, Takenawa T . IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature. 2000; 408(6813):732-5. DOI: 10.1038/35047107. View

Walshaw J, Woolfson D . Socket: a program for identifying and analysing coiled-coil motifs within protein structures. J Mol Biol. 2001; 307(5):1427-50. DOI: 10.1006/jmbi.2001.4545. View

Tarricone C, Xiao B, Justin N, Walker P, Rittinger K, Gamblin S . The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways. Nature. 2001; 411(6834):215-9. DOI: 10.1038/35075620. View

Shi J, Blundell T, Mizuguchi K . FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol. 2001; 310(1):243-57. DOI: 10.1006/jmbi.2001.4762. View

Farsad K, Ringstad N, Takei K, Floyd S, Rose K, De Camilli P . Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol. 2001; 155(2):193-200. PMC: 2198845. DOI: 10.1083/jcb.200107075. View

10.

Razzaq A, ROBINSON I, McMahon H, Skepper J, Su Y, Zelhof A . Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila. Genes Dev. 2001; 15(22):2967-79. PMC: 312829. DOI: 10.1101/gad.207801. View

11.

Leventis P, Chow B, Stewart B, Iyengar B, Campos A, Boulianne G . Drosophila Amphiphysin is a post-synaptic protein required for normal locomotion but not endocytosis. Traffic. 2001; 2(11):839-50. DOI: 10.1034/j.1600-0854.2001.21113.x. View

12.

Zelhof A, Bao H, Hardy R, Razzaq A, Zhang B, Doe C . Drosophila Amphiphysin is implicated in protein localization and membrane morphogenesis but not in synaptic vesicle endocytosis. Development. 2001; 128(24):5005-15. DOI: 10.1242/dev.128.24.5005. View

13.

Zhang B, Zelhof A . Amphiphysins: raising the BAR for synaptic vesicle recycling and membrane dynamics. Bin-Amphiphysin-Rvsp. Traffic. 2002; 3(7):452-60. DOI: 10.1034/j.1600-0854.2002.30702.x. View

14.

Lee E, Marcucci M, Daniell L, Pypaert M, Weisz O, Farsad K . Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science. 2002; 297(5584):1193-6. DOI: 10.1126/science.1071362. View

15.

Leprince C, Le Scolan E, Meunier B, Fraisier V, Brandon N, de Gunzburg J . Sorting nexin 4 and amphiphysin 2, a new partnership between endocytosis and intracellular trafficking. J Cell Sci. 2003; 116(Pt 10):1937-48. DOI: 10.1242/jcs.00403. View

16.

Muller A, Baker J, DuHadaway J, Ge K, Farmer G, Donover P . 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. 2003; 23(12):4295-306. PMC: 156129. DOI: 10.1128/MCB.23.12.4295-4306.2003. View

17.

Canutescu A, Shelenkov A, Dunbrack Jr R . A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci. 2003; 12(9):2001-14. PMC: 2323997. DOI: 10.1110/ps.03154503. View

18.

Kajiho H, Saito K, Tsujita K, Kontani K, Araki Y, Kurosu H . RIN3: a novel Rab5 GEF interacting with amphiphysin II involved in the early endocytic pathway. J Cell Sci. 2003; 116(Pt 20):4159-68. DOI: 10.1242/jcs.00718. View

19.

Owen D, Lowe P, Nietlispach D, Brosnan C, Chirgadze D, Parker P . Molecular dissection of the interaction between the small G proteins Rac1 and RhoA and protein kinase C-related kinase 1 (PRK1). J Biol Chem. 2003; 278(50):50578-87. DOI: 10.1074/jbc.M304313200. View

20.

Peter B, Kent H, Mills I, Vallis Y, Butler P, Evans P . BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science. 2003; 303(5657):495-9. DOI: 10.1126/science.1092586. View