Lipid bilayer preparations of membrane proteins for oriented and magic-angle spinning solid-state NMR samples

Nature Protocols

Volumn 8, Issue 11, 2013, Pages 2256-2270

  Das, Nabanita ^a,b   Murray, Dylan T ^b   Cross, Timothy A ^a,b  

^a FLORIDA STATE UNIVERSITY   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DETERGENT; LIPOSOME; MEMBRANE PROTEIN; PROTEIN CRGA; PROTEIN RV1861; PROTEOLIPOSOME; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL PROCEDURES; CLINICAL PROTOCOL; LIPID BILAYER; MYCOBACTERIUM TUBERCULOSIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SAMPLING; SOLID STATE;

BACTERIAL PROTEINS; CLONING, MOLECULAR; LIPID BILAYERS; LIPOSOMES; MEMBRANE PROTEINS; MEMBRANES, ARTIFICIAL; MYCOBACTERIUM TUBERCULOSIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; TRANSCRIPTION FACTORS;

EID: 84887005994     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2013.129     Document Type: Article

References (73)

1. Page, R.C., Li, C., Hu, J., Gao, F.P. & Cross, T.A. Lipid bilayers: An essential environment for the understanding of membrane proteins. Magn. Reson. Chem. 45, S2-S11 (2007).
2. Dong, H., Sharma, M., Zhou, H.X. & Cross, T.A. Glycines: role in ?-helical membrane protein structures and a potential indicator of native conformation. Biochemistry 51, 4779-4789 (2012).
3. Zhou, H.X. & Cross, T.A. Influences of membrane mimetic environments on membrane protein structures. Annu. Rev. Biophys. 42, 361-392 (2013).
4. Anfinsen, C.B. Principles that govern the folding of protein chains. Science 181, 223-230 (1973).
5. Korepanova, A. et al. Cloning and expression of multiple integral membrane proteins from Mycobacterium tuberculosis in Escherichia coli. Protein Sci. 14, 148-158 (2005). (Pubitemid 40054126)
6. Caffrey, M. Crystallizing membrane proteins for structure determination: use of lipidic mesophases. Annu. Rev. Biophys. 38, 29-51 (2009).
7. Separovic, F., Killian, J.A., Cotten, M., Busath, D.D. & Cross, T.A. Modeling the membrane environment for membrane proteins. Biophys. J. 100, 2073-2074 (2011).
8. Li, D. et al. Crystal structure of the integral membrane diacylglycerol kinase. Nature 497, 521-524 (2013).
9. Chou, J.J., Kaufman, J.D., Stahl, S.J., Wingfield, P.T. & Bax, A. Micelle-induced curvature in a water-insoluble HIV-1 Env peptide revealed by NMR dipolar coupling measurement in stretched polyacrylamide gel. J. Am. Chem. Soc. 124, 2450-2451 (2002). (Pubitemid 34251754)
10. Van Horn, W.D. et al. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 324, 1726-1729 (2009).
11. Griffin, R.G. Dipolar recoupling in MAS spectra of biological solids. Nat. Struct. Biol. 5, 508-512 (1998).
12. Tang, W., Knox, R.W. & Nevzorov, A.A. A spectroscopic assignment technique for membrane proteins reconstituted in magnetically aligned bicelles. J. Biomol. NMR 54, 307-316 (2012).
13. Ketchem, R.R., Hu, W., Tian, F. & Cross, T.A. Structure and dynamics from solid state NMR spectroscopy. Structure 2, 699-701 (1994).
14. Sharma, M. et al. Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer. Science 330, 509-512 (2010).
15. Mote, K.R. et al. Multidimensional oriented solid-state NMR experiments enable the sequential assignment of uniformly 15N labeled integral membrane proteins in magnetically aligned lipid bilayers. Journal of Biomolecular NMR 51, 339-346 (2011).
16. Nevzorov, A.A. & Opella, S.J. Selective averaging for high-resolution solid-state NMR spectroscopy of aligned samples. J. Magn. Reson. 185, 59-70 (2007). (Pubitemid 46484391)
17. Can, T.V. et al. Magic angle spinning and oriented sample solid-state NMR structural restraints combine for influenza A M2 protein functional insights. J. Am. Chem. Soc. 134, 9022-9025 (2012).
18. Murray, D.T., Das, N. & Cross, T.A. Solid-state NMR strategy for characterizing native membrane protein structures. Accounts Chem. Res. 46, 2172-2181 (2013).
19. Plocinski, P. et al. Mycobacterium tuberculosis CwsA interacts with CrgA and Wag31, and the CrgA-CwsA complex is involved in peptidoglycan synthesis and cell shape determination. J. Bacteriol. 194, 6398-6409 (2012).
20. Plocinski, P. et al. Characterization of CrgA, a new partner of the Mycobacterium tuberculosis peptidoglycan polymerization complexes. J. Bacteriol. 193, 3246-3256 (2011).
21. Li, C. et al. Uniformly aligned full-length membrane proteins in liquid crystalline bilayers for structural characterization. J. Am. Chem. Soc. 129, 5304-5305 (2007). (Pubitemid 46697586)
22. Su, P.C., Si, W., Baker, D.L. & Berger, B.W. High-yield membrane protein expression from E. coli using an engineered outer membrane protein F fusion. Protein Sci. 22, 434-443 (2013).
23. Grisshammer, R. Understanding recombinant expression of membrane proteins. Curr. Opin. Biotechnol. 17, 337-340 (2006). (Pubitemid 44177667)
24. Zoonens, M. & Miroux, B. Expression of membrane proteins at the Escherichia coli membrane for structural studies. Methods Mol. Biol. 601, 49-66 (2010).
25. Hu, J., Qin, H., Gao, F.P. & Cross, T.A. A systematic assessment of mature MBP in membrane protein production: overexpression, membrane targeting and purification. Protein Expr. Purif. 80, 34-40 (2011).
26. Mouillac, B. & Baneres, J.L. Mammalian membrane receptors expression as inclusion bodies in Escherichia coli. Methods Mol. Biol. 601, 39-48 (2010).
27. Qin, H. et al. Construction of a series of vectors for high throughput cloning and expression screening of membrane proteins from Mycobacterium tuberculosis. BMC Biotechnol. 8, 51 (2008).
28. Kiefer, H. et al. Expression of an olfactory receptor in Escherichia coli: Purification, reconstitution, and ligand binding. Biochemistry 35, 16077-16084 (1996). (Pubitemid 27044069)
29. Aslanidis, C. & de Jong, P.J. Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res. 18, 6069-6074 (1990).
30. Korepanova, A. et al. Expression of membrane proteins from Mycobacterium tuberculosis in Escherichia coli as fusions with maltose binding protein. Protein Expr. Purif. 53, 24-30 (2007). (Pubitemid 46283455)
31. Seddon, A.M., Curnow, P. & Booth, P.J. Membrane proteins, lipids and detergents: not just a soap opera. Biochim. Biophys. Acta 1666, 105-117 (2004). (Pubitemid 39425201)
32. Rigaud, J.L., Pitard, B. & Levy, D. Reconstitution of membrane proteins into liposomes: Application to energy-transducing membrane proteins. Biochim. Biophys. Acta 1231, 223-246 (1995).
33. Rigaud, J.L. & Levy, D. Reconstitution of membrane proteins into liposomes. Methods Enzymol. 372, 65-86 (2003). (Pubitemid 37337801)
34. Signorell, G.A., Kaufmann, T.C., Kukulski, W., Engel, A. & Remigy, H.W. Controlled 2D crystallization of membrane proteins using methyl-beta-cyclodextrin. J. Struct. Biol. 157, 321-328 (2007). (Pubitemid 46109330)
35. DeGrip, W.J., VanOostrum, J. & Bovee-Geurts, P.H.M. Selective detergent-extraction from mixed detergent/lipid/protein micelles, using cyclodextrin inclusion compounds: A novel generic approach for the preparation of proteoliposomes. Biochem. J. 330, 667-674 (1998). (Pubitemid 28111960)
36. Rigaud, J.L., Levy, D., Mosser, G. & Lambert, O. Detergent removal by non-polar polystyrene beads-applications to membrane protein reconstitution and two-dimensional crystallization. Eur. Biophy. J. Biophys. Lett. 27, 305-319 (1998). (Pubitemid 28319741)
37. Rigaud, J.L., Mosser, G., Lacapere, J.J., Olofsson, A., Levy, D. & Ranck, J.L. Bio-Beads: An efficient strategy for two-dimensional crystallization of membrane proteins. J. Struct. Biol. 118, 226-235 (1997). (Pubitemid 27239877)
38. Kimura, T. et al. Recombinant cannabinoid type 2 receptor in liposome model activates G protein in response to anionic lipid constituents. J. Biol. Chem. 287, 4076-4087 (2012).
39. Park, S.H. et al. Optimization of purification and refolding of the human chemokine receptor CXCR1 improves the stability of proteoliposomes for structure determination. Biochim. Biophys. Acta 1818, 584-591 (2012).
40. van den Brink-van der Laan, E., Killian, J.A. & de Kruijff, B. Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile. Biochim. Biophys. Acta 1666, 275-288 (2004). (Pubitemid 39425210)
41. Miao, Y.M. et al. M2 proton channel structural validation from full-length protein samples in synthetic bilayers and E. coli membranes. Angew. Chem. Int. Ed. Engl. 51, 8383-8386 (2012).
42. Cady, S., Wang, T. & Hong, M. Membrane-dependent effects of a cytoplasmic helix on the structure and drug binding of the influenza virus M2 protein. J. Am. Chem. Soc. 133, 11572-11579 (2011).
43. Bhate, M.P., Wylie, B.J., Tian, L. & McDermott, A.E. Conformational dynamics in the selectivity filter of KcsA in response to potassium ion concentration. J. Mol. Biol. 401, 155-166 (2010).
44. Peterson, E. et al. Functional reconstitution of influenza A M2(22-62). Biochim. Biophys. Acta 1808, 516-521 (2011).
45. Nagy, J.K. & Sanders, C.R. Destabilizing mutations promote membrane protein misfolding. Biochemistry 43, 19-25 (2004). (Pubitemid 38055938)
46. Wallace, B.A., Lees, J.G., Orry, A.J., Lobley, A. & Janes, R.W. Analyses of circular dichroism spectra of membrane proteins. Protein Sci. 12, 875-884 (2003). (Pubitemid 36348474)
47. Andreas, L.B., Eddy, M.T., Pielak, R.M., Chou, J. & Griffin, R.G. Magic angle spinning NMR investigation of influenza A M2(18-60): support for an allosteric mechanism of inhibition. J. Am. Chem Soc. 132, 10958-10960 (2010).
48. Ketchem, R.R., Hu, W. & Cross, T.A. High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. Science 261, 1457-1460 (1993). (Pubitemid 23334269)
49. De Angelis, A.A. & Opella, S.J. Bicelle samples for solid-state NMR of membrane proteins. Nat. Protoc. 2, 2332-2338 (2007).
50. Cevc, G. & Marsh, D. Phospholipid Bilayers: Physical Principles and Models Vol. 5 (John Wiley & Sons, 1987).
51. Baldus, M. Solid-state nuclear magnetic resonance. In Comprehensive Biophysics Vol. 1 (ed. Engleman, E.) 160-181 (Academic Press, 2012).
52. Lakatos, A., Mors, K. & Glaubitz, C. How to investigate interactions between membrane proteins and ligands by solid-state NMR. Methods Mol. Biol. 914, 65-86 (2012).
53. Wu, C.H., Ramamoorthy, A. & Opella, S.J. High resolution heteronuclear dipolar solid-state NMR spectroscopy. J. Magn. Reson. A 109, 270-272 (1994).
54. Wang, J. et al. Imaging membrane protein helical wheels. J. Magn. Reson. 144, 162-167 (2000).
55. Marassi, F.M. & Opella, S.J.A solid-state NMR index of helical membrane protein structure and topology. J. Magn. Reson. 144, 150-155 (2000).
56. Murray, D.T., Lu, Y.T., Cross, T.A. & Quine, J.R. Geometry of kinked protein helices from NMR data. J. Magn. Reson. 210, 82-89 (2011).
57. Opella, S.J. et al. Structures of the M2 channel-lining segments from nicotinic acetylcholine and NMDA receptors by NMR spectroscopy. Nat. Struct. Biol. 6, 374-379 (1999). (Pubitemid 29166487)
58. Park, S.H., De Angelis, A.A., Nevzorov, A.A., Wu, C.H. & Opella, S.J. Three-dimensional structure of the transmembrane domain of Vpu from HIV-1 in aligned phospholipid bicelles. Biophys. J. 91, 3032-3042 (2006). (Pubitemid 44526493)
59. Verardi, R., Shi, L., Traaseth, N.J., Walsh, N. & Veglia, G. Structural topology of phospholamban pentamer in lipid bilayers by a hybrid solution and solid-state NMR method. Proc. Natl. Acad. Sci. USA 108, 9101-9106 (2011).
60. Zech, S.G., Wand, A.J. & McDermott, A.E. Protein structure determination by high-resolution solid-state NMR spectroscopy: Application to microcrystalline ubiquitin. J. Am. Chem. Soc. 127, 8618-8626 (2005). (Pubitemid 40868243)
61. McDermott, A. Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR. Annu. Rev. Biophys. 38, 385-403 (2009).
62. Castellani, F. et al. Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 420, 98-102 (2002). (Pubitemid 35291447)
63. Park, S.H. et al. Structure of the chemokine receptor CXCR1 in phospholipid bilayers. Nature 491, 779-783 (2012).
64. Das, B.B. et al. Structure determination of a membrane protein in proteoliposomes. J. Am. Chem. Soc. 134, 2047-2056 (2012).
65. Park, S.H., Das, B.B., De Angelis, A.A., Scrima, M. & Opella, S.J. Mechanically, magnetically, and ?rotationally aligned? membrane proteins in phospholipid bilayers give equivalent angular constraints for NMR structure determination. J. Phys. Chem. B 114, 13995-14003 (2010).
66. Opella, S.J. Structure determination of membrane proteins in their native phospholipid bilayer environment by rotationally aligned solid-state NMR spectroscopy. Accounts Chem. Res. 46, 2145-2153 (2013).
67. Cady, S.D. et al. Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463, 689-692 (2010).
68. Massotte, D. G protein-coupled receptor overexpression with the baculovirus-insect cell system: A tool for structural and functional studies. Biochim. Biophys. Acta 1610, 77-89 (2003). (Pubitemid 36173999)
69. McCusker, E.C., Bane, S.E., O?Malley, M.A. & Robinson, A.S. Heterologous GPCR expression: A bottleneck to obtaining crystal structures. Biotechnol. Prog. 23, 540-547 (2007). (Pubitemid 46911176)
70. Shi, L. & Ladizhansky, V. Magic-angle spinning solid-state NMR experiments for structural characterization of proteins. Methods Mol. Biol. 895, 153-165 (2012).
71. Gor?kov, P.L. et al. Using low-E resonators to reduce RF heating in biological samples for static solid-state NMR up to 900 MHz. J. Magn. Reson. 185, 77-93 (2007).
72. Quine, J.R. et al. Intensity and mosaic spread analysis from PISEMA tensors in solid-state NMR. J. Magn. Reson. 179, 190-198 (2006).
73. Page, R.C. et al. Comprehensive evaluation of solution nuclear magnetic resonance spectroscopy sample preparation for helical integral membrane proteins. J. Struct. Funct. Genomics 7, 51-64 (2006). (Pubitemid 44273863)