Facile backbone structure determination of human membrane proteins by NMR spectroscopy

Nature Methods

Volumn 9, Issue 8, 2012, Pages 834-839

  Klammt, Christian ^a,b   Maslennikov, Innokentiy ^a,b   Bayrhuber, Monika ^a,c   Eichmann, Cédric ^a,c   Vajpai, Navratna ^a,c   Chiu, Ellis Jeremy Chua ^a,b   Blain, Katherine Y ^a   Esquivies, Luis ^a   Kwon, June Hyun Jung ^b   Balana, Bartosz ^d   Pieper, Ursula ^e   Sali, Andrej ^e   Slesinger, Paul A ^d   Kwiatkowski, Witek ^a   Riek, Roland ^a,c   Choe, Senyon ^a,b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b Gachon University   (South Korea)

^c ETH ZURICH   (Switzerland)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CHEMICAL LABELING; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

DATABASES, PROTEIN; HUMANS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION;

EID: 84864426351     PISSN: 15487091     EISSN: 15487105     Source Type: Journal    
DOI: 10.1038/nmeth.2033     Document Type: Article

References (55)

1. Klammt, C. et al. High level cell-free expression and specific labeling of integral membrane proteins. Eur. J. Biochem. 271, 568-580 (2004). (Pubitemid 38183631)
2. Wuu, J.J. & Swartz, J.R. High yield cell-free production of integral membrane proteins without refolding or detergents. Biochim. Biophys. Acta 1778, 1237-1250 (2008).
3. Katzen, F. et al. Insertion of membrane proteins into discoidal membranes using a cell-free protein expression approach. J. Proteome Res. 7, 3535-3542 (2008).
4. Kalmbach, R. et al. Functional cell-free synthesis of a seven helix membrane protein: in situ insertion of bacteriorhodopsin into liposomes. J. Mol. Biol. 371, 639-648 (2007). (Pubitemid 47087829)
5. Klammt, C. et al. Evaluation of detergents for the soluble expression of alpha-helical and beta-barrel-type integral membrane proteins by a preparative scale individual cell-free expression system. FEBS J. 272, 6024-6038 (2005). (Pubitemid 41713694)
6. Maslennikov, I. et al. Membrane domain structures of three classes of histidine kinase receptors by cell-free expression and rapid NMR analysis. Proc. Natl. Acad. Sci. USA 107, 10902-10907 (2010).
7. Klammt, C. et al. Polymer-based cell-free expression of ligand-binding family B G-protein coupled receptors without detergents. Protein Sci. 20, 1030-1041 (2011).
8. Junge, F. et al. Modulation of G-protein coupled receptor sample quality by modified cell-free expression protocols: a case study of the human endothelin A receptor. J. Struct. Biol. 172, 94-106 (2010).
9. Keller, T. et al. Cell free expression and functional reconstitution of eukaryotic drug transporters. Biochemistry 47, 4552-4564 (2008). (Pubitemid 351522106)
10. Klammt, C. et al. Functional analysis of cell-free-produced human endothelin B receptor reveals transmembrane segment 1 as an essential area for ET-1 binding and homodimer formation. FEBS J. 274, 3257-3269 (2007). (Pubitemid 47024965)
11. Ishihara, G. et al. Expression of G protein coupled receptors in a cell-free translational system using detergents and thioredoxin-fusion vectors. Protein Expr. Purif. 41, 27-37 (2005). (Pubitemid 40406360)
12. Pervushin, K., Riek, R., Wider, G. & Wuthrich, K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl. Acad. Sci. USA 94, 12366-12371 (1997).
13. Gautier, A. et al. Structure determination of the seven-helix transmembrane receptor sensory rhodopsin II by solution NMR spectroscopy. Nat. Struct. Mol. Biol. 17, 768-774 (2010).
14. Van Horn, W.D. et al. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 324, 1726-1729 (2009).
15. Wang, J., Pielak, R.M., McClintock, M.A. & Chou, J.J. Solution structure and functional analysis of the influenza B proton channel. Nat. Struct. Mol. Biol. 16, 1267-1271 (2009).
16. Hiller, S. et al. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321, 1206-1210 (2008).
17. Bayrhuber, M. et al. Structure of the human voltage-dependent anion channel. Proc. Natl. Acad. Sci. USA 105, 15370-15375 (2008).
18. Page, R.C. et al. Backbone structure of a small helical integral membrane protein: A unique structural characterization. Protein Sci. 18, 134-146 (2009).
19. Liang, B., Bushweller, J.H. & Tamm, L.K. Site-directed parallel spin-labeling and paramagnetic relaxation enhancement in structure determination of membrane proteins by solution NMR spectroscopy. J. Am. Chem. Soc. 128, 4389-4397 (2006).
20. Iwahara, J., Schwieters, C.D. & Clore, G.M. Ensemble approach for NMR structure refinement against (1)H paramagnetic relaxation enhancement data arising from a flexible paramagnetic group attached to a macromolecule. J. Am. Chem. Soc. 126, 5879-5896 (2004). (Pubitemid 38621427)
21. Battiste, J.L. & Wagner, G. Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data. Biochemistry 39, 5355-5365 (2000). (Pubitemid 30257075)
22. Kay, L.E. Solution NMR spectroscopy of supra-molecular systems, why bother? A methyl-TROSY view. J. Magn. Reson. 210, 159-170 (2011).
23. Rual, J.F. et al. Human ORFeome version 1.1: a platform for reverse proteomics. Genome Res. 14, 2128-2135 (2004).
24. Sobhanifar, S. et al. Structural investigation of the C-terminal catalytic fragment of presenilin 1. Proc. Natl. Acad. Sci. USA 107, 9644-9649 (2010).
25. Zhou, Y. et al. NMR solution structure of the integral membrane enzyme DsbB: functional insights into DsbB-catalyzed disulfide bond formation. Mol. Cell 31, 896-908 (2008).
26. Bedo, G. et al. Characterization of hypoxia induced gene 1: expression during rat central nervous system maturation and evidence of antisense RNA expression. Int. J. Dev. Biol. 49, 431-436 (2005). (Pubitemid 41076272)
27. Kasper, L.H. & Brindle, P.K. Mammalian gene expression program resiliency: the roles of multiple coactivator mechanisms in hypoxia-responsive transcription. Cell Cycle 5, 142-146 (2006). (Pubitemid 43131147)
28. Jiang, Z., Gui, S. & Zhang, Y. Analysis of differential gene expression by fiber-optic BeadArray and pathway in prolactinomas. Endocrine 38, 360-368 (2010).
29. Cheriyath, V., Leaman, D.W. & Borden, E.C. Emerging roles of FAM14 family members (G1P3/ISG 6-16 and ISG12/IFI27) in innate immunity and cancer. J. Interferon Cytokine Res. 31, 173-181 (2011).
30. Nilsson, R. et al. Discovery of genes essential for heme biosynthesis through large-scale gene expression analysis. Cell Metab. 10, 119-130 (2009).
31. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291 (1993).
32. Zheng, L., Baumann, U. & Reymond, J.L. An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 32, e115 (2004).
33. Shi, C. et al. Purification and characterization of a recombinant G-protein-coupled receptor, Saccharomyces cerevisiae Ste2p, transiently expressed in HEK293 EBNA1 cells. Biochemistry 44, 15705-15714 (2005). (Pubitemid 41746901)
34. Klammt, C., Schwarz, D., Dotsch, V. & Bernhard, F. Cell-free production of integral membrane proteins on a preparative scale. Methods Mol. Biol. 375, 57-78 (2007). (Pubitemid 350183381)
35. Ichetovkin, I.E., Abramochkin, G. & Shrader, T.E. Substrate recognition by the leucyl/phenylalanyl-tRNA-protein transferase. Conservation within the enzyme family and localization to the trypsin-resistant domain. J. Biol. Chem. 272, 33009-33014 (1997). (Pubitemid 28023640)
36. Savage, D.F. et al. Cell-free complements in vivo expression of the E. coli membrane proteome. Protein Sci. 16, 966-976 (2007). (Pubitemid 46683201)
37. Riek, R. et al. Solution NMR techniques for large molecular and supramolecular structures. J. Am. Chem. Soc. 124, 12144-12153 (2002). (Pubitemid 35154881)
38. Salzmann, M. et al. TROSY in triple-resonance experiments: new perspectives for sequential NMR assignment of large proteins. Proc. Natl. Acad. Sci. USA 95, 13585-13590 (1998). (Pubitemid 28523015)
39. Salzmann, M. et al. TROSY-type triple-resonance experiments for sequential NMR assignments of large proteins. J. Am. Chem. Soc. 121, 844-848 (1999).
40. Diercks, T., Coles, M. & Kessler, H. An efficient strategy for assignment of cross-peaks in 3D heteronuclear NOESY experiments. J. Biomol. NMR 15, 177-180 (1999).
41. Hilty, C., Wider, G., Fernandez, C. & Wuthrich, K. Membrane protein-lipid interactions in mixed micelles studied by NMR spectroscopy with the use of paramagnetic reagents. ChemBioChem 5, 467-473 (2004). (Pubitemid 39257103)
42. Yabuki, T. et al. Dual amino acid-selective and site-directed stable-isotope labeling of the human c-Ha-Ras protein by cell-free synthesis. J. Biomol. NMR 11, 295-306 (1998). (Pubitemid 128511280)
43. Kainosho, M. & Tsuji, T. Assignment of the three methionyl carbonyl carbon resonances in Streptomyces subtilisin inhibitor by a carbon-13 and nitrogen-15 double-labeling technique. A new strategy for structural studies of proteins in solution. Biochemistry 21, 6273-6279 (1982). (Pubitemid 13141631)
44. Van Horn, W.D., Beel, A.J., Kang, C. & Sanders, C.R. The impact of window functions on NMR-based paramagnetic relaxation enhancement measurements in membrane proteins. Biochim. Biophys. Acta 1798, 140-149 (2010).
45. Roosild, T.P. et al. NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science 307, 1317-1321 (2005). (Pubitemid 40299982)
46. Kroncke, B.M., Horanyi, P.S. & Columbus, L. Structural origins of nitroxide side chain dynamics on membrane protein alpha-helical sites. Biochemistry 49, 10045-10060 (2010).
47. Langen, R., Oh, K.J., Cascio, D. & Hubbell, W.L. Crystal structures of spin labeled T4 lysozyme mutants: implications for the interpretation of EPR spectra in terms of structure. Biochemistry 39, 8396-8405 (2000). (Pubitemid 30489936)
48. Clore, G.M., Robien, M.A. & Gronenborn, A.M. Exploring the limits of precision and accuracy of protein structures determined by nuclear magnetic resonance spectroscopy. J. Mol. Biol. 231, 82-102 (1993). (Pubitemid 23186600)
49. Lubingbuhl, P., Szyperski, T. & Wuthrich, K. Statistical basis for the use of 13Ca chemical shifts in protein structure determination. J. Magn. Reson. B. 109, 229-233 (1995).
50. Guntert, P. Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278, 353-378 (2004).
51. Dalton, J.A., Michalopoulos, I. & Westhead, D.R. Calculation of helix packing angles in protein structures. Bioinformatics 19, 1298-1299 (2003). (Pubitemid 36850227)
52. Koradi, R., Billeter, M. & Wuthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55 (1996). (Pubitemid 26152976)
53. Brewer, G.J., Torricelli, J.R., Evege, E.K. & Price, P.J. Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576 (1993). (Pubitemid 23215708)
54. Pieper, U. et al. ModBase, a database of annotated comparative protein structure models, and associated resources. Nucleic Acids Res. 39, D465-D474 (2011).
55. Bairoch, A. et al. The Universal Protein Resource (UniProt). Nucleic Acids Res. 33, D154-D159 (2005). (Pubitemid 40207850)