Combination of 15N reverse labeling and afterglow spectroscopy for assigning membrane protein spectra by magic-angle-spinning solid-state NMR: Application to the multidrug resistance protein EmrE

Journal of Biomolecular NMR

Volumn 55, Issue 4, 2013, Pages 391-399

  Banigan, James R ^a   Gayen, Anindita ^a   Traaseth, Nathaniel J ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

EmrE; Magic angle spinning; Membrane proteins; Sequential acquisition assignment methods; Small multidrug resistance; Solid state NMR

Indexed keywords

MEMBRANE PROTEIN; MULTIDRUG RESISTANCE PROTEIN; PROTEIN EMRE; UNCLASSIFIED DRUG; ANTIPORTER; EMRE PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN;

AMINO ACID ANALYSIS; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; ESCHERICHIA COLI; ISOTOPE LABELING; LIPID BILAYER; LIPID MEMBRANE; MAGIC ANGLE SPINNING NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN TRANSPORT; SOLID STATE; BIOLOGICAL MODEL; CHEMISTRY; METHODOLOGY;

ANTIPORTERS; ESCHERICHIA COLI PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, BIOLOGICAL;

EID: 84877875388     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-013-9724-z     Document Type: Article

References (81)

1. Agarwal V, Fink U, Schuldiner S, Reif B (2007) MAS solid-state NMR studies on the multidrug transporter EmrE. Biochim Biophys Acta 1768(12):3036-3043. doi: 10.1016/j.bbamem.2007.09.012 (Pubitemid 350236098)
2. Akbey Ü, Camponeschi F, van Rossum B-J, Oschkinat H (2011) Triple resonance cross-polarization for more sensitive 13C MAS NMR spectroscopy of deuterated proteins. ChemPhysChem 12(11):2092-2096. doi: 10.1002/cphc.201100084
3. Amadi ST, Koteiche HA, Mishra S, Mchaourab HS (2010) Structure, dynamics, and substrate-induced conformational changes of the multidrug transporter EmrE in liposomes. J Biol Chem 285(34):26710-26718. doi: 10.1074/jbc.M110.132621
4. Baldus M, Geurts DG, Hediger S, Meier BH (1996) Efficient N-15-C-13 polarization transfer by adiabatic-passage Hartmann-Hahn cross polarization. J Magn Reson, Ser A 118(1):140-144 (Pubitemid 126751687)
5. Baldus M, Petkova AT, Herzfeld JH, Griffin RG (1998) Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems. Mol Phys 95:1197-1207 (Pubitemid 128495249)
6. Banigan JR, Traaseth NJ (2012) Utilizing afterglow magnetization from cross-polarization magic-angle-spinning solid-state NMR spectroscopy to obtain simultaneous heteronuclear multidimensional spectra. J Phys Chem B 116(24):7138-7144. doi: 10.1021/jp303269m
7. Bayro MJ, Daviso E, Belenky M, Griffin RG, Herzfeld J (2012) An amyloid organelle, solid-state NMR evidence for cross-β assembly of gas vesicles. J Biol Chem 287(5):3479-3484. doi: 10.1074/jbc.M111.313049
8. Bellstedt P, Herbst C, Häfner S, Leppert J, Görlach M, Ramachandran R (2012) Solid state NMR of proteins at high MAS frequencies: symmetry-based mixing and simultaneous acquisition of chemical shift correlation spectra. J Biomol NMR 54(4):325-335. doi: 10.1007/s10858-012-9680-z
9. Bertini I, Emsley L, Lelli M, Luchinat C, Mao JF, Pintacuda G (2010) Ultrafast MAS solid-state NMR permits extensive C-13 and H-1 detection in paramagnetic metalloproteins. J Am Chem Soc 132(16):5558. doi: 10.1021/Ja100398q
10. Bhate MP, McDermott AE (2012) Protonation state of E71 in KcsA and its role for channel collapse and inactivation. Proc Natl Acad Sci USA 109(38):15265-15270. doi: 10.1073/pnas.1211900109
11. Cady SD, Schmidt-Rohr K, Wang J, Soto CS, DeGrado WF, Hong M (2010) Structure of the amantadine binding site of influenza M2 proton channels in lipid bilayers. Nature 463(7281):689-692. doi: 10.1038/Nature08722
12. Castellani F, van Rossum B, Diehl A, Schubert M, Rehbein K, Oschkinat H (2002) Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature 420(6911):98-102. doi: 10.1038/nature01070 (Pubitemid 35291447)
13. Chen Y-J, Pornillos O, Lieu S, Ma C, Chen AP, Chang G (2007) X-ray structure of EmrE supports dual topology model. Proc Natl Acad Sci 104(48):18999-19004. doi: 10.1073/pnas.0709387104
14. Cross TA, Sharma M, Yi M, Zhou H-X (2011) Influence of solubilizing environments on membrane protein structures. Trends Biochem Sci 36(2):117-125. doi: 10.1016/j.tibs.2010.07.005
15. De Angelis AA, Howell SC, Nevzorov AA, Opella SJ (2006) Structure determination of a membrane protein with two trans-membrane helices in aligned phospholipid bicelles by solid-state NMR spectroscopy. J Am Chem Soc 128(37):12256-12267. doi: 10.1021/ja063640w (Pubitemid 44413857)
16. Durr UHN, Yamamoto K, Im SC, Waskell L, Ramamoorthy A (2007) Solid-state NMR reveals structural and dynamical properties of a membrane-anchored electron-carrier protein, cytochrome b(5). J Am Chem Soc 129(21):6670. doi: 10.1021/Ja069028m (Pubitemid 46847487)
17. Etzkorn M, Martell S, Andronesi OC, Seidel K, Engelhard M, Baldus M (2007) Secondary structure, dynamics, and topology of a seven-helix receptor in native membranes, studied by solid-state NMR spectroscopy. Angew Chem Int Edit 46(3):459-462. doi: 10.1002/anie.200602139 (Pubitemid 46142261)
18. Fleishman SJ, Harrington SE, Enosh A, Halperin D, Tate CG, Ben-Tal N (2006) Quasi-symmetry in the Cryo-EM structure of EmrE provides the key to modeling its transmembrane domain. J Mol Biol 364(1):54-67. doi: 10.1016/j.jmb.2006.08.072 (Pubitemid 44634527)
19. Franks WT, Wylie BJ, Stellfox SA, Rienstra CM (2006) Backbone conformational constraints in a microcrystalline U-N-15-labeled protein by 3D dipolar-shift solid-state NMR spectroscopy. J Am Chem Soc 128(10):3154-3155. doi: 10.1021/Ja058292x
20. Franks WT, Kloepper KD, Wylie BJ, Rienstra CM (2007) Four-dimensional heteronuclear correlation experiments for chemical shift assignment of solid proteins. J Biomol NMR 39(2):107-131. doi: 10.1007/s10858-007-9179-1 (Pubitemid 47377484)
21. Gardiennet C, Loquet A, Etzkorn M, Heise H, Baldus M, Böckmann A (2008) Structural constraints for the Crh protein from solid-state NMR experiments. J Biomol NMR 40(4):239-250. doi: 10.1007/s10858-008-9229-3
22. Giraud N, Böckmann A, Lesage A, Penin F, Blackledge M, Emsley L (2004) Site-specific backbone dynamics from a crystalline protein by solid-state NMR spectroscopy. J Am Chem Soc 126(37):11422-11423. doi: 10.1021/ja046578g (Pubitemid 39244942)
23. Gopinath T, Veglia G (2012) Dual acquisition magic-angle spinning solid-state nmr-spectroscopy: simultaneous acquisition of multidimensional spectra of biomacromolecules. Angew Chem Int Ed 51(11):2731-2735. doi: 10.1002/anie.201108132
24. Gustavsson M, Traaseth NJ, Veglia G (2012) Probing ground and excited states of phospholamban in model and native lipid membranes by magic angle spinning NMR spectroscopy. Biochim Biophys Acta 1818(2):146-153. doi: 10.1016/j.bbamem.2011.07.040
25. Heise H, Hoyer W, Becker S, Andronesi OC, Riedel D, Baldus M (2005) Molecular-level secondary structure, polymorphism, and dynamics of full-length α-synuclein fibrils studied by solid-state NMR. Proc Natl Acad Sci USA 102(44):15871-15876. doi: 10.1073/pnas.0506109102 (Pubitemid 41552835)
26. Herbst C, Riedel K, Ihle Y, Leppert J, Ohlenschläger O, Görlach M, Ramachandran R (2008) MAS solid state NMR of RNAs with multiple receivers. J Biomol NMR 41(3):121-125. doi: 10.1007/s10858-008-9247-1
27. Hiller S, Garces RG, Malia TJ, Orekhov VY, Colombini M, Wagner G (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321(5893):1206-1210. doi: 10.1126/science.1161302
28. Hong M, DeGrado WF (2012) Structural basis for proton conduction and inhibition by the influenza M2 protein. Protein Sci 21(11):1620-1633. doi: 10.1002/pro.2158
29. Hong M, Jakes K (1999) Selective and extensive 13C labeling of a membrane protein for solid-state NMR investigations. J Biomol NMR 14(1):71-74. doi: 10.1023/a:1008334930603 (Pubitemid 29258287)
30. Hong M, Zhang Y, Hu F (2012) Membrane protein structure and dynamics from NMR spectroscopy. Annu Rev Phys Chem 63(1):1-24. doi: 10.1146/annurev-physchem- 032511-143731
31. Igumenova TI, McDermott AE, Zilm KW, Martin RW, Paulson EK, Wand AJ (2004) Assignments of carbon NMR resonances for microcrystalline ubiquitin. J Am Chem Soc 126(21):6720-6727. doi: 10.1021/Ja030547o (Pubitemid 38697371)
32. Jaipuria G, Lobo NP, Shet D, Atreya HS (2012) High resolution methyl selective (1)(3)C-NMR of proteins in solution and solid state. J Biomol NMR 54(1):33-42. doi: 10.1007/s10858-012-9647-0
33. Jaroniec CP, MacPhee CE, Bajaj VS, McMahon MT, Dobson CM, Griffin RG (2004) High-resolution molecular structure of a peptide in an amyloid fibril determined by magic angle spinning NMR spectroscopy. Proc Natl Acad Sci USA 101(3):711-716. doi: 10.1073/pnas.0304849101 (Pubitemid 38121022)
34. Jehle S, Rehbein K, Diehl A, van Rossum BJ (2006) Amino-acid selective experiments on uniformly 13C and 15 N labeled proteins by MAS NMR: filtering of lysines and arginines. J Magn Reson 183(2):324-328. doi: 10.1016/j.jmr.2006.08. 015 (Pubitemid 44739344)
35. Johnson E, Nguyen PT, Yeates TO, Rees DC (2012) Inward facing conformations of the MetNI methionine ABC transporter: implications for the mechanism of transinhibition. Protein Sci 21(1):84-96. doi: 10.1002/pro.765
36. Kim HJ, Howell SC, Van Horn WD, Jeon YH, Sanders CR (2009) Recent advances in the application of solution NMR spectroscopy to multi-span integral membrane proteins. Prog Nucl Magn Reson Spectrosc 55(4):335-360. doi: 10.1016/j.pnmrs.2009.07.002
37. Knox RW, Lu GJ, Opella SJ, Nevzorov AA (2010) A resonance assignment method for oriented-sample solid-state NMR of proteins. J Am Chem Soc 132(24):8255-8257. doi: 10.1021/ja102932n
38. Korkhov VM, Tate CG (2009) An emerging consensus for the structure of EmrE. Acta Crystallogr D 65:186-192. doi: 10.1107/S0907444908036640
39. Krishnamurthy H, Gouaux E (2012) X-ray structures of LeuT in substrate-free outward-open and apo inward-open states. Nature 481 (7382):469-474. http://www.nature.com/nature/journal/v481/n7382/abs/nature10737. html#supplementary-information
40. Krishnarjuna B, Jaipuria G, Thakur A, D'Silva P, Atreya H (2011) Amino acid selective unlabeling for sequence specific resonance assignments in proteins. J Biomol NMR 49(1):39-51. doi: 10.1007/s10858-010-9459-z
41. Lehner I, Basting D, Meyer B, Haase W, Manolikas T, Kaiser C, Karas M, Glaubitz C (2008) The key residue for substrate transport (Glu14) in the EmrE dimer is asymmetric. J Biol Chem 283(6):3281-3288. doi: 10.1074/jbc.M707899200
42. Li J, Hoop CL, Kodali R, Sivanandam VN, van der Wel PCA (2011) Amyloid-like fibrils from a domain-swapping protein feature a parallel, in-register conformation without native-like interactions. J Biol Chem 286(33):28988-28995. doi: 10.1074/jbc.M111.261750
43. Lian L-Y, Middleton DA (2001) Labelling approaches for protein structural studies by solution-state and solid-state NMR. Prog Nucl Magn Reson Spectrosc 39(3):171-190. doi: 10.1016/s0079-6565(01)00034-6 (Pubitemid 32997728)
44. Liang BY, Tamm LK (2007) Structure of outer membrane protein G by solution NMR spectroscopy. Proc Natl Acad Sci USA 104(41):16140-16145. doi: 10.1073/pnas.0705466104 (Pubitemid 350099375)
45. Linden AH, Lange S, Franks WT, Akbey U, Specker E, van Rossum BJ, Oschkinat H (2011) Neurotoxin II bound to acetylcholine receptors in native membranes studied by dynamic nuclear polarization NMR. J Am Chem Soc 133(48):19266-19269. doi: 10.1021/Ja206999c
46. Martin RW, Zilm KW (2003) Preparation of protein nanocrystals and their characterization by solid state NMR. J Magn Reson 165(1):162-174. doi: 10.1016/S1090-7807(03)00253-2
47. Masterson LR, Tonelli M, Markley JL, Veglia G (2008) Simultaneous detection and deconvolution of congested NMR spectra containing three isotopically labeled species. J Am Chem Soc 130(25):7818-7819. doi: 10.1021/ja802701w (Pubitemid 351875045)
48. McDermott A (2009) Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR. Annu Rev Biophys 38(1):385-403. doi: 10.1146/annurev.biophys.050708.133719
49. Morcombe CR, Zilm KW (2003) Chemical shift referencing in MAS solid state NMR. J Magn Reson 162(2):479-486. doi: 10.1016/S1090-7807(03)00082-X
50. Morrison EA, DeKoster GT, Dutta S, Vafabakhsh R, Clarkson MW, Bahl A, Kern D, Ha T, Henzler-Wildman KA (2012) Antiparallel EmrE exports drugs by exchanging between asymmetric structures. Nature 481 (7379):45-50. http://www.nature.com/nature/journal/v481/n7379/abs/nature10703. html#supplementary-information
51. Muller SD, De Angelis AA, Walther TH, Grage SL, Lange C, Opella SJ, Ulrich AS (2007) Structural characterization of the pore forming protein TatA(d) of the twin-arginine translocase in membranes by solid-state N-15-NMR. Biochim Biophys Acta 1768(12):3071-3079. doi: 10.1016/j.bbamem.2007.09.008 (Pubitemid 350236094)
52. Neugebauer D-C, Zingsheim HP, Oesterhelt D (1978) Recrystallization of the purple membrane in vivo and in vitro. J Mol Biol 123(2):247-257. doi: 10.1016/0022-2836(78)90324-8 (Pubitemid 8406692)
53. Paravastu AK, Leapman RD, Yau WM, Tycko R (2008) Molecular structural basis for polymorphism in Alzheimer's beta-amyloid fibrils. Proc Natl Acad Sci USA 105(47):18349-18354. doi: 10.1073/pnas.0806270105
54. Park SH, Prytulla S, De Angelis AA, Brown JM, Kiefer H, Opella SJ (2006) High-resolution NMR spectroscopy of a GPCR in aligned bicelles. J Am Chem Soc 128(23):7402-7403. doi: 10.1021/ja0606632 (Pubitemid 43877489)
55. Rasia RM, Brutscher B, Plevin MJ (2012) Selective isotopic unlabeling of proteins using metabolic precursors: application to NMR assignment of intrinsically disordered proteins. ChemBioChem 13(5):732-739. doi: 10.1002/cbic.201100678
56. Rasmussen SGF, DeVree BT, Zou Y, Kruse AC, Chung KY, Kobilka TS, Thian FS, Chae PS, Pardon E, Calinski D, Mathiesen JM, Shah STA, Lyons JA, Caffrey M, Gellman SH, Steyaert J, Skiniotis G, Weis WI, Sunahara RK, Kobilka BK (2011) Crystal structure of the [bgr]2 adrenergic receptor-Gs protein complex. Nature 477 (7366):549-555. http://www.nature.com/nature/journal/v477/n7366/abs/ nature10361.html#supplementary-information
57. Renault M, Tommassen-van Boxtel R, Bos MP, Post JA, Tommassen J, Baldus M (2012) Cellular solid-state nuclear magnetic resonance spectroscopy. Proc Natl Acad Sci. doi: 10.1073/pnas.1116478109
58. Sackett K, Nethercott MJ, Epand RF, Epand RM, Kindra DR, Shai Y, Weliky DP (2010) Comparative analysis of membrane-associated fusion peptide secondary structure and lipid mixing function of HIV gp41 constructs that model the early pre-hairpin intermediate and final hairpin conformations. J Mol Biol 397(1):301-315. doi: 10.1016/j.jmb.2010.01.018
59. Schmidt-Rohr K, Fritzsching KJ, Liao SY, Hong M (2012) Spectral editing of two-dimensional magic-angle-spinning solid-state NMR spectra for protein resonance assignment and structure determination. J Biomol NMR 54(4):343-353. doi: 10.1007/s10858-012-9676-8
60. Schuetz A, Wasmer C, Habenstein B, Verel R, Greenwald J, Riek R, Bockmann A, Meier BH (2010) Protocols for the sequential solid-state NMR spectroscopic assignment of a uniformly labeled 25 kDa protein: HET-s(1-227). ChemBioChem 11(11):1543-1551. doi: 10.1002/cbic.201000124
61. Schuldiner S (2009) EmrE, a model for studying evolution and mechanism of ion-coupled transporters. Biochim Biophys Acta 1794(5):748-762. doi: 10.1016/j.bbapap.2008.12.018
62. Sengupta I, Nadaud PS, Helmus JJ, Schwieters CD, Jaroniec CP (2012) Protein fold determined by paramagnetic magic-angle spinning solid-state NMR spectroscopy. Nat Chem 4(5):410-417. doi: 10.1038/Nchem.1299
63. Sharma M, Yi MG, Dong H, Qin HJ, Peterson E, Busath DD, Zhou HX, Cross TA (2010) Insight into the mechanism of the influenza A proton channel from a structure in a lipid bilayer. Science 330(6003):509-512. doi: 10.1126/science.1191750
64. Shi L, Ahmed MAM, Zhang W, Whited G, Brown LS, Ladizhansky V (2009) Three-dimensional solid-state NMR study of a seven-helical integral membrane proton pump - structural insights. J Mol Biol 386(4):1078-1093. doi: 10.1016/j.jmb.2009.01.011
65. Takegoshi K, Nakamura S, Terao T (2001) 13C-1H dipolar-assisted rotational resonance in magic-angle spinning NMR. Chem Phys Lett 344:631-637 (Pubitemid 33628408)
66. Tate CG, Kunji ER, Lebendiker M, Schuldiner S (2001) The projection structure of EmrE, a proton-linked multidrug transporter from Escherichia coli, at 7 Å resolution. EMBO J 20:77-81 (Pubitemid 32101423)
67. Toyoshima C, Kanai R, Cornelius F (2011) First crystal structures of Na +, K + -ATPase: new light on the oldest ion pump. Structure 19(12):1732-1738. doi: 10.1016/j.str.2011.10.016
68. Traaseth NJ, Veglia G (2011) Frequency-selective heteronuclear dephasing and selective carbonyl labeling to deconvolute crowded spectra of membrane proteins by magic angle spinning NMR. J Magn Reson 211(1):18-24. doi: 10.1016/j.jmr.2011.03.013
69. Traaseth NJ, Buffy JJ, Zamoon J, Veglia G (2006) Structural dynamics and topology of phospholamban in oriented lipid bilayers using multidimensional solid-state NMR. Biochemistry 45(46):13827-13834. doi: 10.1021/Bi0607610 (Pubitemid 44788751)
70. Traaseth NJ, Shi L, Verardi R, Mullen DG, Barany G, Veglia G (2009) Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach. Proc Natl Acad Sci USA 106(25):10165-10170. doi: 10.1073/pnas.0904290106
71. Tycko R (2011) Solid-state NMR studies of amyloid fibril structure. Annu Rev Phys Chem 62(1):279-299. doi: 10.1146/annurev-physchem-032210-103539
72. Ubarretxena-Belandia I, Baldwin JM, Schuldiner S, Tate CG (2003) Three-dimensional structure of the bacterial multidrug transporter EmrE shows it is an asymmetric homodimer. EMBO J 22(23):6175-6181 (Pubitemid 37522575)
73. Verardi R, Shi L, Traaseth NJ, Walsh N, Veglia G (2011) Structural topology of phospholamban pentamer in lipid bilayers by a hybrid solution and solid-state NMR method. Proc Natl Acad Sci 108(22):9101-9106. doi: 10.1073/pnas.1016535108
74. Verardi R, Traaseth NJ, Masterson LR, Vostrikov VV, Veglia G (2012) Isotope labeling for solution and solid-state NMR spectroscopy of membrane proteins. Adv Exp Med Biol 992:35-62. doi: 10.1007/978-94-007-4954-2-3
75. Vostrikov VV, Daily AE, Greathouse DV, Koeppe RE (2010) Charged or aromatic anchor residue dependence of transmembrane peptide tilt. J Biol Chem 285(41):31723-31730. doi: 10.1074/jbc.M110.152470
76. Vuister GW, Kim S-J, Wu C, Bax A (1994) 2D and 3D NMR study of phenylalanine residues in proteins by reverse isotopic labeling. J Am Chem Soc 116(20):9206-9210. doi: 10.1021/ja00099a041 (Pubitemid 24336954)
77. Wallin E, Heijne GV (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7(4):1029-1038. doi: 10.1002/pro.5560070420 (Pubitemid 28216544)
78. White SH (2009) Biophysical dissection of membrane proteins. Nature 459(7245):344-346
79. Wishart D, Bigam C, Yao J, Abildgaard F, Dyson HJ, Oldfield E, Markley J, Sykes B (1995) 1H, 13C and 15 N chemical shift referencing in biomolecular NMR. J Biomol NMR 6(2):135-140. doi: 10.1007/BF00211777
80. Yang J, Tasayco ML, Polenova T (2008) Magic angle spinning NMR experiments for structural studies of differentially enriched protein interfaces and protein assemblies. J Am Chem Soc 130(17):5798-5807. doi: 10.1021/ja711304e (Pubitemid 351600513)
81. Zhou YP, Cierpicki T, Jimenez RHF, Lukasik SM, Ellena JF, Cafiso DS, Kadokura H, Beckwith J, Bushweller JH (2008) NMR solution structure of the integral membrane enzyme DsbB: functional insights into DsbB-catalyzed disulfide bond formation. Mol Cell 31(6):896-908. doi: 10.1016/j.molcel.2008.08.028