A saposin-lipoprotein nanoparticle system for membrane proteins

Nature Methods

Volumn 13, Issue 4, 2016, Pages 345-351

  Frauenfeld, Jens ^a,h   Löving, Robin ^a   Armache, Jean Paul ^b   Sonnen, Andreas F P ^c,d   Guettou, Fatma ^a   Moberg, Per ^a   Zhu, Lin ^a,e   Jegerschöld, Caroline ^a,e   Flayhan, Ali ^f   Briggs, John A G ^c,d   Garoff, Henrik ^a   Löw, Christian ^a,f   Cheng, Yifan ^b,g   Nordlund, Pär ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^e ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^f EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h Salipro Biotech AB   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; LIPOPROTEIN; MEMBRANE PROTEIN; MOLECULAR SCAFFOLD; NANOPARTICLE; SCAFFOLD PROTEIN; SPHINGOLIPID ACTIVATOR PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; BACTERIAL PROTEIN; COTRANSPORTER; GLYCOPROTEIN GP 120; HYDROGEN-COUPLED OLIGOPEPTIDE TRANSPORTER PEPT2; LIPID;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRITICAL MICELLE CONCENTRATION; FLUOROMETRY; HUMAN IMMUNODEFICIENCY VIRUS 1; LIPID TRANSPORT; MOLECULAR WEIGHT; NONHUMAN; PARTICLE SIZE; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN RECONSTITUTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SOLUBILIZATION; STOICHIOMETRY; THERMOSTABILITY; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS SPIKE; CHEMISTRY; CRYOELECTRON MICROSCOPY; HUMAN; METABOLISM; PROCEDURES; PROTEIN CONFORMATION;

BACTERIAL PROTEINS; CRYOELECTRON MICROSCOPY; HIV ENVELOPE PROTEIN GP120; HUMANS; LIPIDS; MEMBRANE PROTEINS; NANOPARTICLES; PROTEIN CONFORMATION; SAPOSINS; SYMPORTERS;

EID: 84960194524     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.3801     Document Type: Article

References (58)

1. Wallin, E. & von Heijne, G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 7, 1029-1038 (1998).
2. Overington, J.P., Al-Lazikani, B. & Hopkins, A. How many drug targets are there? Nat. Rev. Drug Discov. 5, 993-996 (2006).
3. Tate, C.G. Practical considerations of membrane protein instability during purifcation and crystallisation. Methods Mol. Biol. 601, 187-203 (2010).
4. Breyton, C., Pucci, B. & Popot, J.L. Amphipols and fuorinated surfactants: two alternatives to detergents for studying membrane proteins in vitro. Methods Mol. Biol. 601, 219-245 (2010).
5. Raschle, T., Hiller, S., Etzkorn, M. & Wagner, G. Nonmicellar systems for solution NMR spectroscopy of membrane proteins. Curr. Opin. Struct. Biol. 20, 471-479 (2010).
6. Rigaud, J.L. & Levy, D. Reconstitution of membrane proteins into liposomes. Methods Enzymol. 372, 65-86 (2003).
7. Bayburt, T.H., Carlson, J.W. & Sligar, S.G. Reconstitution and imaging of a membrane protein in a nanometer-size phospholipid bilayer. J. Struct. Biol. 123, 37-44 (1998).
8. Wang, L. & Sigworth, F.J. Structure of the BK potassium channel in a lipid membrane from electron cryomicroscopy. Nature 461, 292-295 (2009).
9. Frauenfeld, J. et al. Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nat. Struct. Mol. Biol. 18, 614-621 (2011).
10. Efremov, R.G., Leitner, A., Aebersold, R. & Raunser, S. Architecture and conformational switch mechanism of the ryanodine receptor. Nature 517, 39-43 (2015).
11. Bruhn, H. A short guided tour through functional and structural features of saposin-like proteins. Biochem. J. 389, 249-257 (2005).
12. Olmeda, B., Garcia-Alvarez, B. & Perez-Gil, J. Structure-function correlations of pulmonary surfactant protein SP-B and the saposin-like family of proteins. Eur. Biophys. J. 42, 209-222 (2013).
13. Ahn, V.E., Faull, K.F., Whitelegge, J.P., Fluharty, A.L. & Prive, G.G. Crystal structure of saposin B reveals a dimeric shell for lipid binding. Proc. Natl. Acad. Sci. USA 100, 38-43 (2003).
14. Hawkins, C.A., de Alba, E. & Tjandra, N. Solution structure of human saposin C in a detergent environment. J. Mol. Biol. 346, 1381-1392 (2005).
15. Rossmann, M. et al. Crystal structures of human saposins C and D: implications for lipid recognition and membrane interactions. Structure 16, 809-817 (2008).
16. Popovic, K., Holyoake, J., Pomes, R. & Prive, G.G. Structure of saposin A lipoprotein discs. Proc. Natl. Acad. Sci. USA 109, 2908-2912 (2012).
17. Löw, C. et al. Nanobody mediated crystallization of an archeal mechanosensitive channel. PLoS ONE 8, e77984 (2013).
18. Guettou, F. et al. Structural insights into substrate recognition in proton-dependent oligopeptide transporters. EMBO Rep. 14, 804-810 (2013).
19. Guettou, F. et al. Selectivity mechanism of a bacterial homolog of the human drug-peptide transporters PepT1 and PepT2. Nat. Struct. Mol. Biol. 21, 728-731 (2014).
20. Alexander, C.G. et al. Novel microscale approaches for easy, rapid determination of protein stability in academic and commercial settings. Biochim. Biophys. Acta 1844, 2241-2250 (2014).
21. Cyrklaff, M., Adrian, M. & Dubochet, J. Evaporation during preparation of unsupported thin vitrifed aqueous layers for cryo-electron microscopy. J. Electron Microsc. Tech. 16, 351-355 (1990).
22. Li, X. et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10, 584-590 (2013).
23. Scheres, S.H. & Chen, S. Prevention of overftting in cryo-EM structure determination. Nat. Methods 9, 853-854 (2012).
24. Plotkin, S.A. & Plotkin, S.L. The development of vaccines: how the past led to the future. Nat. Rev. Microbiol. 9, 889-893 (2011).
25. Agrawal, N. et al. Functional stability of unliganded envelope glycoprotein spikes among isolates of human immunodefciency virus type 1 (HIV-1). PLoS ONE 6, e21339 (2011).
26. Leaman, D.P. & Zwick, M.B. Increased functional stability and homogeneity of viral envelope spikes through directed evolution. PLoS Pathog. 9, e1003184 (2013).
27. Löving, R., Sjoberg, M., Wu, S.R., Binley, J.M. & Garoff, H. Inhibition of the HIV-1 spike by single-PG9/16-antibody binding suggests a coordinated-activation model for its three protomeric units. J. Virol. 87, 7000-7007 (2013).
28. Julien, J.P. et al. Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc. Natl. Acad. Sci. USA 110, 4351-4356 (2013).
29. Walker, L.M. et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289 (2009).
30. Kwong, P.D. et al. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393, 648-659 (1998).
31. Thali, M. et al. Characterization of conserved human immunodefciency virus type 1 gp120 neutralization epitopes exposed upon gp120-CD4 binding. J. Virol. 67, 3978-3988 (1993).
32. Hagn, F., Etzkorn, M., Raschle, T. & Wagner, G. Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins. J. Am. Chem. Soc. 135, 1919-1925 (2013).
33. Knowles, T.J. et al. Membrane proteins solubilized intact in lipid containing nanoparticles bounded by styrene maleic acid copolymer. J. Am. Chem. Soc. 131, 7484-7485 (2009).
34. McGregor, C.L. et al. Lipopeptide detergents designed for the structural study of membrane proteins. Nat. Biotechnol. 21, 171-176 (2003).
35. Park, S.H. et al. Nanodiscs versus macrodiscs for NMR of membrane proteins. Biochemistry 50, 8983-8985 (2011).
36. Schafmeister, C.E., Miercke, L.J. & Stroud, R.M. Structure at 2.5 Å of a designed peptide that maintains solubility of membrane proteins. Science 262, 734-738 (1993).
37. Tao, H. et al. Engineered nanostructured β-sheet peptides protect membrane proteins. Nat. Methods 10, 759-761 (2013).
38. Tribet, C., Audebert, R. & Popot, J.L. Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc. Natl. Acad. Sci. USA 93, 15047-15050 (1996).
39. Wang, X., Mu, Z., Li, Y., Bi, Y. & Wang, Y. Smaller nanodiscs are suitable for studying protein lipid interactions by solution NMR. Protein J. 34, 205-211 (2015).
40. Paulsen, C.E., Armache, J.P., Gao, Y., Cheng, Y. & Julius, D. Structure of the TRPA1 ion channel suggests regulatory mechanisms. Nature 520, 511-517 (2015).
41. Rollauer, S.E. et al. Structure of the TatC core of the twin-arginine protein transport system. Nature 492, 210-214 (2012).
42. Bayburt, T.H. & Sligar, S.G. Membrane protein assembly into Nanodiscs. FEBS Lett. 584, 1721-1727 (2010).
43. Haynes, B.F. & Verkoczy, L. AIDS/HIV. Host controls of HIV neutralizing antibodies. Science 344, 588-589 (2014).
44. Kwong, P.D., Mascola, J.R. & Nabel, G.J. Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat. Rev. Immunol. 13, 693-701 (2013).
45. Huang, J. et al. Broad and potent neutralization of HIV-1 by a gp41-specifc human antibody. Nature 491, 406-412 (2012).
46. Muster, T. et al. A conserved neutralizing epitope on gp41 of human immunodefciency virus type 1. J. Virol. 67, 6642-6647 (1993).
47. Rujas, E. et al. Structural and thermodynamic basis of epitope binding by neutralizing and nonneutralizing forms of the anti-HIV-1 antibody 4e10. J. Virol. 89, 11975-11989 (2015).
48. Zanetti, G., Briggs, J.A., Grunewald, K., Sattentau, Q.J. & Fuller, S.D. Cryo-electron tomographic structure of an immunodefciency virus envelope complex in situ. PLoS Pathog. 2, e83 (2006).
49. Kucukelbir, A., Sigworth, F.J. & Tagare, H.D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63-65 (2014).
50. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
51. Liao, M., Cao, E., Julius, D. & Cheng, Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504, 107-112 (2013).
52. Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. bioRxiv doi:10.1101/020917 (13 August 2015).
53. Scheres, S.H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
54. Elmlund, D. & Elmlund, H. SIMPLE: software for ab initio reconstruction of heterogeneous single-particles. J. Struct. Biol. 180, 420-427 (2012).
55. Pettersen, E.F. et al. UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
56. Moore, P.L. et al. Nature of nonfunctional envelope proteins on the surface of human immunodefciency virus type 1. J. Virol. 80, 2515-2528 (2006).
57. Wu, S.R. et al. Single-particle cryoelectron microscopy analysis reveals the HIV-1 spike as a tripod structure. Proc. Natl. Acad. Sci. USA 107, 18844-18849 (2010).
58. Löving, R., Wu, S.R., Sjoberg, M., Lindqvist, B. & Garoff, H. Maturation cleavage of the murine leukemia virus Env precursor separates the transmembrane subunits to prime it for receptor triggering. Proc. Natl. Acad. Sci. USA 109, 7735-7740 (2012).