Endophilin A1 induces different membrane shapes using a conformational switch that is regulated by phosphorylation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 19, 2014, Pages 6982-6987

  Ambroso, Mark R ^a   Hegde, Balachandra G ^a,b   Langen, Ralf ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b Post Graduate Department of Physics Rani Channamma University ^*  (India)

Author keywords

Double electron electron resonance; Site directed spin labeling

Indexed keywords

AMPHIPHYSIN; ENDOPHILIN; ENDOPHILIN A1; LEUCINE RICH REPEAT KINASE 2; PROTEIN; PROTEIN BIN; PROTEIN RVS; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; IN VITRO STUDY; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE BINDING; MUTATION; OLIGOMERIZATION; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REGULATORY MECHANISM; SPIN LABELING;

DOUBLE ELECTRON-ELECTRON RESONANCE; SITE-DIRECTED SPIN LABELING;

ACYLTRANSFERASES; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; ELECTRONS; HUMANS; LIPIDS; LIPOSOMES; MEMBRANE PROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; SPIN LABELS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84900520403     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1402233111     Document Type: Article

References (48)

1. Rao Y, Haucke V (2011) Membrane shaping by the Bin/amphiphysin/Rvs (BAR) domain protein superfamily. Cell Mol Life Sci 68(24):3983-3993.
2. McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438(7068):590-596.
3. Qualmann B, Koch D, Kessels MM (2011) Let's go bananas: Revisiting the endocytic BAR code. EMBO J 30(17):3501-3515.
4. Matta S, et al. (2012) LRRK2 controls an EndoA phosphorylation cycle in synaptic endocytosis. Neuron 75(6):1008-1021.
5. Bergmann C, et al. (2003) Oligophrenin 1 (OPHN1) gene mutation causes syndromic X-linked mental retardation with epilepsy, rostral ventricular enlargement and cere-bellar hypoplasia. Brain 126(Pt 7):1537-1544.
6. Nicot A-S, et al. (2007) Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat Genet 39(9):1134-1139.
7. De Camilli P, 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(6): 2219-2223.
8. Meinecke M, et al. (2013) Cooperative recruitment of dynamin and BIN/amphiphysin/Rvs (BAR) domain-containing proteins leads to GTP-dependent membrane scission. J Biol Chem 288(9):6651-6661.
9. Sundborger A, et al. (2011) An endophilin-dynamin complex promotes budding of clathrin-coated vesicles during synaptic vesicle recycling. J Cell Sci 124(pt 1):133-143.
10. Ringstad N, et al. (1999) Endophilin/SH3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis. Neuron 24(1):143-154.
11. Milosevic I, et al. (2011) Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron 72(4):587-601.
12. Soda K, et al. (2012) Role of dynamin, synaptojanin, and endophilin in podocyte foot processes. J Clin Invest 122(12):4401-4411.
13. Schuske KR, et al. (2003) Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40(4):749-762.
14. Verstreken P, et al. (2003) Synaptojanin is recruited by endophilin to promote syn-aptic vesicle uncoating. Neuron 40(4):733-748.
15. Bai J, Hu Z, Dittman JS, Pym ECG, Kaplan JM (2010) Endophilin functions as a membrane-bending molecule and is delivered to endocytic zones by exocytosis. Cell 143(3): 430-441.
16. Farsad K, et al. (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol 155(2):193-200.
17. Gallop JL, et al. (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J 25(12):2898-2910.
18. Masuda M, et al. (2006) Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J 25(12):2889-2897.
19. Ferguson SM, et al. (2009) Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell 17(6):811-822.
20. Drin G, Antonny B (2010) Amphipathic helices and membrane curvature. FEBS Lett 584(9):1840-1847.
21. Stachowiak JC, et al. (2012) Membrane bending by protein-protein crowding. Nat Cell Biol 14(9):944-949.
22. Farsad K, De Camilli P (2003) Mechanisms of membrane deformation. Curr Opin Cell Biol 15(4):372-381.
23. Weissenhorn W (2005) Crystal structure of the endophilin-A1 BAR domain. J Mol Biol 351(3):653-661.
24. Peter BJ, et al. (2004) BAR domains as sensors of membrane curvature: the amphi-physin BAR structure. Science 303(5657):495-499.
25. Blood PD, Swenson RD, Voth GA (2008) Factors influencing local membrane curvature induction by N-BAR domains as revealed by molecular dynamics simulations. Biophys J 95(4):1866-1876.
26. Blood PD, Voth GA (2006) Direct observation of Bin/amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations. Proc Natl Acad Sci USA 103(41):15068-15072.
27. Arkhipov A, Yin Y, Schulten K (2009) Membrane-bending mechanism of amphiphysin N-BAR domains. Biophys J 97(10):2727-2735.
28. Jao CC, et al. (2010) Roles of amphipathic helices and the bin/amphiphysin/rvs (BAR) domain of endophilin in membrane curvature generation. J Biol Chem 285(26): 20164-20170.
29. Bhatia VK, et al. (2009) Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J 28(21):3303-3314.
30. Campelo F, McMahon HT, Kozlov MM (2008) The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys J 95(5):2325-2339.
31. Mim C, Unger VM (2012) Membrane curvature and its generation by BAR proteins. Trends Biochem Sci 37(12):526-533.
32. Jao CC, Hegde BG, Chen J, Haworth IS, Langen R (2008) Structure of membrane-bound alpha-synuclein from site-directed spin labeling and computational refinement. Proc Natl Acad Sci USA 105(50):19666-19671.
33. Varkey J, et al. (2010) Membrane curvature induction and tubulation are common features of synucleins and apolipoproteins. J Biol Chem 285(42):32486-32493.
34. Mizuno N, Jao CC, Langen R, Steven AC (2010) Multiple modes of endophilin-medi-ated conversion of lipid vesicles into coated tubes: Implications for synaptic endocy-tosis. J Biol Chem 285(30):23351-23358.
35. Mim C, et al. (2012) Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149(1):137-145.
36. Cui H, et al. (2013) Understanding the role of amphipathic helices in N-BAR domain driven membrane remodeling. Biophys J 104(2):404-411.
37. Altenbach C, Greenhalgh DA, Khorana HG, Hubbell WL (1994) A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: Application to spin-labeled mutants of bacteriorhodopsin. Proc Natl Acad Sci USA 91(5):1667-1671.
38. Langen R, Oh KJ, Cascio D, Hubbell WL (2000) Crystal structures of spin labeled T4 lysozyme mutants: implications for the interpretation of EPR spectra in terms of structure. Biochemistry 39(29):8396-8405.
39. Zhu C, Das SL, Baumgart T (2012) Nonlinear sorting, curvature generation, and crowding of endophilin N-BAR on tubular membranes. Biophys J 102(8):1837-1845.
40. Sorre B, et al. (2012) Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc Natl Acad Sci USA 109(1):173-178.
41. Lai C-L, et al. (2012) Membrane binding and self-association of the epsin N-terminal homology domain. J Mol Biol 423(5):800-817.
42. Drin G, et al. (2007) A general amphipathic α-helical motif for sensing membrane curvature. Nat Struct Mol Biol 14(2):138-146.
43. Strandberg E, Killian JA (2003) Snorkeling of lysine side chains in transmembrane helices: How easy can it get? FEBS Lett 544(1-3):69-73.
44. Campelo F, Fabrikant G, McMahon HT, Kozlov MM (2010) Modeling membrane shaping by proteins: Focus on EHD2 and N-BAR domains. FEBS Lett 584(9):1830-1839.
45. Boucrot E, et al. (2012) Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149(1):124-136.
46. Lee D-S, Hirashima N, Kirino Y (2000) Rapid transbilayer phospholipid redistribution associated with exocytotic release of neurotransmitters from cholinergic nerve terminals isolated from electric ray Narke japonica. Neurosci Lett 291(1):21-24.
47. Kato N, Nakanishi M, Hirashima N (2002) Transbilayer asymmetry of phospholipids in the plasma membrane regulates exocytotic release in mast cells. Biochemistry 41(25): 8068-8074.
48. Kaneko T, et al. (2005) Rho mediates endocytosis of epidermal growth factor receptor through phosphorylation of endophilin A1 by Rho-kinase. Genes Cells 10(10):973-987.