Efficient cellular solid-state NMR of membrane proteins by targeted protein labeling

Journal of Biomolecular NMR

Volumn 62, Issue 2, 2015, Pages 199-208

  Baker, Lindsay A ^a,b   Daniëls, Mark ^a   Van Der Cruijsen, Elwin A W ^a   Folkers, Gert E ^a   Baldus, Marc ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cellular membranes; Membrane protein; Protein expression; Solid state NMR

Indexed keywords

MEMBRANE PROTEIN; RECOMBINANT PROTEIN; RIFAMPICIN; BACTERIAL PROTEIN; CARRIER PROTEIN; ESCHERICHIA COLI PROTEIN; POTASSIUM CHANNEL; PROKARYOTIC POTASSIUM CHANNEL; PROTEOLIPID; PROTEOLIPOSOMES; YIDC PROTEIN, E COLI;

ARTICLE; BACTERIAL OUTER MEMBRANE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL MEMBRANE; CONTROLLED STUDY; ESCHERICHIA COLI; INNER MEMBRANE; ISOTOPE LABELING; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLID STATE; SOLID STATE NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; MOLECULAR CLONING; NUCLEAR MAGNETIC RESONANCE; PROCEDURES; PROTEIN CONFORMATION; SENSITIVITY AND SPECIFICITY; STREPTOMYCES LIVIDANS;

BACTERIAL PROTEINS; CLONING, MOLECULAR; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; POTASSIUM CHANNELS; PROTEIN CONFORMATION; PROTEOLIPIDS; RECOMBINANT PROTEINS; RIFAMPIN; SENSITIVITY AND SPECIFICITY; STREPTOMYCES LIVIDANS;

EID: 84930381299     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-015-9936-5     Document Type: Article

References (56)

1. Almeida FC, Amorim GC, Moreau VH et al (2001) Selectively labeling the heterologous protein in Escherichia coli for NMR studies: a strategy to speed up NMR spectroscopy. J Magn Reson 148:142-146
2. Andronesi OC, Becker S, Seidel K et al (2005) Determination of membrane protein structure and dynamics by magic-angle-spinning solid-state NMR spectroscopy. J Am Chem Soc 127:574-581
3. Baker LA, Baldus M (2014) Characterization of membrane protein function by solid-state NMR spectroscopy. Curr Opin Struct Biol 27:48-55
4. Baker LA, Folkers GE, Sinnige T, et al (2015) Magic-angle-spinning solid-state NMR of membrane proteins. Methods Enzymol Ion Channels Part B 557:307-328. doi: 10.1016/bs.mie.2014.12.023
5. Baldus M (2015) A solid view of membrane proteins in situ. Biophys J 108:1585-1586. doi: 10.1016/j.bpj.2015.02.019
6. Baldus M, Petkova AT, Herzfeld J, Griffin RG (1998) Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems. Mol Phys 95:1197-1207
7. Burz DS, Dutta K, Cowburn D, Shekhtman A (2006) Mapping structural interactions using in-cell NMR spectroscopy (STINT-NMR). Nat Methods 3:91-93
8. Caffrey M, Li D, Dukkipati A (2012) Membrane protein structure determination using crystallography and lipidic mesophases: recent advances and successes. Biochemistry 51:6266-6288
9. Campbell E, Korzheva N, Mustaev A et al (2001) Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104:901-912
10. Cruzeiro-Silva C, Albernaz F, Valente A, Almeida F (2006) In-Cell NMR spectroscopy: inhibition of autologous protein expression reduces Escherichia coli lysis. Cell Biochem Biophys 44:497-502. doi: 10.1385/CBB:44:3:497
11. Das B, Nothnagel H, Lu G et al (2012) Structure determination of a membrane protein in proteoliposomes. J Am Chem Soc 134:2047-2056
12. De Jong RN, Daniëls MA, Kaptein R, Folkers GE (2006) Enzyme free cloning for high throughput gene cloning and expression. J Struct Funct Genomics 7:109-118. doi: 10.1007/s10969-006-9014-z
13. Dedmon MM, Patel CN, Young GB, Pielak GJ (2002) FlgM gains structure in living cells. Proc Natl Acad Sci USA 99:12681-12684
14. Dick-Perez M, Wang T, Salazar A et al (2012) Multidimensional solid-state NMR studies of the structure and dynamics of pectic polysaccharides in uniformly 13C-labeled Arabidopsis primary cell walls. Magn Reson Chem 50:539-550. doi: 10.1002/mrc.3836
15. Dick-Pérez M, Zhang Y, Hayes J et al (2011) Structure and interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry 50:989-1000. doi: 10.1021/bi101795q
16. Etzkorn M, Martell S, Andronesi OC et al (2007) Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angew Chem Int Ed Engl 46:459-462. doi: 10.1002/anie.200602139
17. Etzkorn M, Raschle T, Hagn F et al (2013) Cell-free expressed bacteriorhodopsin in different soluble membrane mimetics: biophysical properties and NMR accessibility. Structure 21:394-401
18. Folkers GE, van Buuren BNM, Kaptein R (2004) Expression screening, protein purification and NMR analysis of human protein domains for structural genomics. J Struct Funct Genomics 5:119-131. doi: 10.1023/B:JSFG.0000029200.66197.0c
19. Fu R, Wang X, Li C et al (2011) In situ structural characterization of a recombinant protein in native Escherichia coli membranes with solid-state magic-angle-spinning NMR. J Am Chem Soc 133:12370-12373. doi: 10.1021/ja204062v
20. Fung BM, Khitrin AK, Ermolaev K (2000) An improved broadband decoupling sequence for liquid crystals and solids. J Magn Reson 142:97-101
21. Goddard T.D.,Kneller D.G. 2008
22. Gradmann S, Ader C, Heinrich I et al (2012) Rapid prediction of multi-dimensional NMR data sets. J Biomol NMR 54:377-387
23. Harris RK, Becker ED, Cabral de Menezes SM et al (2008) Further conventions for NMR shielding and chemical shifts (IUPAC Recommendations 2008). Pure Appl Chem 80:59-84
24. Hubbard JA, MacLachlan LK, King GW et al (2003) Nuclear magnetic resonance spectroscopy reveals the functional state of the signalling protein CheY in vivo in Escherichia coli. Mol Microbiol 49:1191-1200
25. Jacso T, Franks WT, Rose H et al (2012) Characterization of membrane proteins in isolated native cellular membranes by dynamic nuclear polarization solid-state NMR spectroscopy without purification and reconstitution. Angew Chem Int Ed Engl 51:432-435. doi: 10.1002/anie.201104987
26. Kaplan M, Cukkemane A, van Zundert GCP et al (2015) Probing a cell-embedded Megadalton protein complex by DNP-supported solid-state NMR. Nat Methods (in press)
27. Koers EJ, van der Cruijsen EAW, Rosay M et al (2014) NMR-based structural biology enhanced by dynamic nuclear polarization at high magnetic field. J Biomol NMR. doi: 10.1007/s10858-014-9865-8
28. Kulminskaya NV, Pedersen MØ, Bjerring M et al (2012) Insitu solid-state NMR spectroscopy of protein in heterogeneous membranes: the baseplate antenna complex of Chlorobaculum tepidum. Angew Chem Int Ed Engl 51:6891-6895. doi: 10.1002/anie.201201160
29. Kumazaki K, Kishimoto T, Furukawa A, et al (2014) Crystal structure of Escherichia coli YidC, a membrane protein chaperone and insertase. Sci Rep 4:7299
30. Lange A, Giller K, Hornig S et al (2006) Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440:959-962. doi: 10.1038/nature04649
31. Mao L, Inoue K, Tao Y et al (2011) Suppression of phospholipid biosynthesis by cerulenin in the condensed single-protein-production (cSPP) system. J Biomol NMR 49:131-137
32. Miao Y, Cross TA (2013) Solid state NMR and protein-protein interactions in membranes. Curr Opin Struct Biol 23:919-928
33. Miao Y, Qin H, Fu R et al (2012) 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. doi: 10.1002/anie.201204666
34. Neal S, Nip AM, Zhang H, Wishart DS (2003) Rapid and accurate calculation of protein 1H, 13C and 15N chemical shifts. J Biomol NMR 26:215-240
35. Renault M, Pawsey S, Bos MP et al (2012a) Solid-state NMR spectroscopy on cellular preparations enhanced by dynamic nuclear polarization. Angew Chem Int Ed Engl 51:2998-3001
36. Renault M, Tommassen-van Boxtel R, Bos MP et al (2012b) Cellular solid-state nuclear magnetic resonance spectroscopy. Proc Natl Acad Sci USA 109:4863-4868
37. Schneider R, Ader C, Lange A et al (2008) Solid-state NMR spectroscopy applied to a chimeric potassium channel in lipid bilayers. J Am Chem Soc 130:7427-7435. doi: 10.1021/ja800190c
38. Serber Z, Ledwidge R, Miller S, Dötsch V (2001) Evaluation of parameters critical to observing proteins inside living Escherichia coli by in-cell NMR spectroscopy. J Am Chem Soc 123:8895-8901. doi: 10.1021/ja0112846
39. Shi L, Kawamura I, Jung K et al (2011) Conformation of a seven-helical transmembrane photosensor in the lipid environment. Angew Chem Int Ed Engl 50:1302-1305
40. Sinnige T, Houben K, Pritisanac I et al (2015) Insight into the conformational stability of membrane-embedded BamA using a combined solution and solid-state NMR approach. J Biomol NMR 61:321-332. doi: 10.1007/s10858-014-9891-6
41. Stenberg F, Chovanec P, Maslen SL et al (2005) Protein complexes of the Escherichia coli cell envelope. J Biol Chem 280:34409-34419. doi: 10.1074/jbc.M506479200
42. Suzuki M, Zhang J, Liu M et al (2005) Single protein production in living cells facilitated by an mRNA interferase. Mol Cell 18:253-261
43. Takahashi H, Ayala I, Bardet M et al (2013) Solid-state NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization. J Am Chem Soc 3:1-9. doi: 10.1021/ja312501d
44. Van Dalen A, Schrempf H, Killian JA, de Kruijff B (2000) Efficient membrane assembly of the KcsA potassium channel in Escherichia coli requires the protonmotive force. EMBO Rep 1:340-346. doi: 10.1093/embo-reports/kvd067
45. Van der Cruijsen EAW, Nand D, Weingarth M et al (2013) Importance of lipid-pore loop interface for potassium channel structure and function. Proc Natl Acad Sci USA 110:13008-13013. doi: 10.1073/pnas.1305563110
46. Wang T, Zabotina O, Hong M (2012) Pectin-cellulose interactions in the Arabidopsis primary cell wall from two-dimensional magic-angle-spinning solid-state nuclear magnetic resonance. Biochemistry 51:9846-9856. doi: 10.1021/bi3015532
47. Wang S, Munro RA, Shi L et al (2013a) Solid-state NMR spectroscopy structure determination of a lipid-embedded heptahelical membrane protein. Nat Methods 10:1007-1012
48. 15N resonance assignments of a seven-transmembrane helical protein Anabaena Sensory Rhodopsin. Biomol NMR Assign 7:253-256
49. Wang T, Salazar A, Zabotina OA, Hong M (2014) Structure and dynamics of Brachypodium primary cell wall polysaccharides from two-dimensional (13)C solid-state nuclear magnetic resonance spectroscopy. Biochemistry 53:2840-2854. doi: 10.1021/bi500231b
50. Ward ME, Wang S et al (2015) In situ structural studies of Anabaena Sensory Rhodopsin in the E. coli membrane. Biophys J 108:1683-1696
51. Wei Y, de Dios AC, McDermott AE (1999) Solid-state 15N NMR chemical shift anisotropy of histidines: experimental and theoretical studies of hydrogen bonding. J Am Chem Soc 121:10389-10394
52. Weingarth M, Baldus M (2013) Solid-state NMR-based approaches for supramolecular structure elucidation. Acc Chem Res 46:2037-2046. doi: 10.1021/ar300316e
53. Weingarth M, Demco DE, Bodenhausen G, Tekely P (2009) Improved magnetization transfer in solid-state NMR with fast magic angle spinning. Chem Phys Lett 469:342-348
54. Weingarth M, Prokofyev A, van der Cruijsen EAW et al (2013) Structural determinants of specific lipid binding to potassium channels. J Am Chem Soc 135:3983-3988. doi: 10.1021/ja3119114
55. Yamamoto K, Caporini MA, Im S-C et al (2014) Cellular solid-state NMR investigation of a membrane protein using dynamic nuclear polarization. Biochim Biophys Acta. doi: 10.1016/j.bbamem.2014.07.008
56. Zhou H-X, Cross TA (2013) Influences of membrane mimetic environments on membrane protein structures. Annu Rev Biophys 42:361-392