Solid-state NMR analysis of membrane proteins and protein aggregates by proton detected spectroscopy

Journal of Biomolecular NMR

Volumn 54, Issue 3, 2012, Pages 291-305

  Zhou, Donghua H ^a   Nieuwkoop, Andrew J ^b,c   Berthold, Deborah A ^b   Comellas, Gemma ^b   Sperling, Lindsay J ^b,d   Tang, Ming ^b   Shah, Gautam J ^b   Brea, Elliott J ^b   Lemkau, Luisel R ^b   Rienstra, Chad M ^b  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Chemical assignment; Magic angle spinning; Proton detection; Solid state NMR

Indexed keywords

ALPHA SYNUCLEIN; BACTERIAL PROTEIN; DSBA PROTEIN; MEMBRANE PROTEIN; PROTEIN DSBB; PROTEIN GB1; UNCLASSIFIED DRUG;

ARTICLE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; SENSITIVITY ANALYSIS; SOLID STATE;

ALPHA-SYNUCLEIN; BACTERIAL PROTEINS; DEUTERIUM; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN DISULFIDE-ISOMERASES; PROTONS;

EID: 84868214420     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-012-9672-z     Document Type: Article

References (78)

1. Akbey U, Lange S, Franks TW, Linser R, Rehbein K, Diehl A, van Rossum B-J, Reif B, Oschkinat H (2010) Optimum levels of exchangeable protons in perdeuterated proteins for proton detection in MAS solid-state NMR spectroscopy. J Biomol NMR 46:67-73
2. Bennett AE, OK JH, Griffin RG, Vega S (1992) Chemical shift correlation spectroscopy in rotating solids: Radio frequencydriven dipolar recoupling and longitudinal exchange. J Chem Phys 96:8624-8627
3. Bertini I, Bhaumik A, De Paepe G, Griffin RG, Lelli M, Lewandowski JR, Luchinat C (2010) High-resolution solid-state NMR structure of a 17.6 kDa protein. J Am Chem Soc 132:1032-1040
4. Blois TM, Bowie JU (2009) G-protein-coupled receptor structures were not built in a day. Prot Sci 18:1335-1342
5. 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 463:689-692
6. Castellani F, Rossum BV, Diehl A, Schubert M, Rehbein K, Oschkinat H (2002) Structure of a protein determined by solid-state magicangle-spinning NMR spectroscopy. Nature 420:98-102 (Pubitemid 35291447)
7. Chevelkov V, van Rossum BJ, Castellani F, Rehbein K, Diehl A, Hohwy M, Steuernagel S, Engelke F, Oschkinat H, Reif B (2003) 1H detection in MAS solid-state NMR spectroscopy of biomacromolecules employing pulsed field gradients for residual solvent suppression. J Am Chem Soc 125:7788-7789 (Pubitemid 36782141)
8. Chevelkov V, Rehbein K, Diehl A, Reif B (2006) Ultra-high resolution in proton solid-state NMR spectroscopy at high levels of deuteration. Angew Chem Int Ed 45:3878-3881 (Pubitemid 44098947)
9. Comellas G, Lemkau LR, Nieuwkoop AJ, Kloepper KD, Ladror DT, Ebisu R, Woods WS, Lipton AS, George JM, Rienstra CM (2011) Structured regions of a-synuclein fibrils include the earlyonset parkinson's disease mutation sites. J Mol Biol 411:881-895
10. Couprie J, Remerowski ML, Bailleul A, Courcon M, Gilles N, Quemeneur E, Jamin N (1998) Differences between the electronic environments of reduced and oxidized Escherichia coli DsbA inferred from heteronuclear magnetic resonance spectroscopy. Protein Sci 7:2065-2080 (Pubitemid 28495793)
11. Detken A, Hardy EH, Ernst M, Kainosho M, Kawakami T, Aimoto S, Meier BH (2001) Methods for sequential resonance assignment in solid, uniformly 13C, 15 N labelled peptides: Quantification and application to antamanide. J Biomol NMR 20:203-221 (Pubitemid 32747187)
12. Ernst M, Meier MA, Tuherm T, Samoson A, Meier BH (2004) Lowpower high-resolution solid-state NMR of peptides and proteins. J Am Chem Soc 126:4764-4765 (Pubitemid 38490128)
13. Ferguson N, Becker J, Tidow H, Tremmel S, Sharpe TD, Krause G, Flinders J, Petrovich M, Berriman J, Oschkinat H, Fersht AR (2006) General structural motifs of amyloid protofilaments. Proc Natl Acad Sci USA 103:16248-16253 (Pubitemid 44715182)
14. Filmore D (2004) It's a GPCR world: Cell-based screening assays and structural studies are fueling G-protein coupled receptors as one of the most popular classes of investigational drug targets. Mod Drug Discov 7:24-28
15. Fossi M, Castellani F, Nilges M, Oschkinat H, van Rossum B-J (2005) SOLARIA: A protocol for automated cross-peak assignment and structure calculation for solid-state magic-angle spinning NMR spectroscopy. Angew Chem Int Ed 44:6151-6154 (Pubitemid 41394102)
16. Franks WT, Zhou DH, Wylie BJ, Money BG, Graesser DT, Frericks HL, Sahota G, Rienstra CM (2005) Magic-angle spinning solidstate NMR spectroscopy of the b1 immunoglobin binding domain of protein G (GB1): 15N and 13C chemical shift assignments and conformational analysis. J Am Chem Soc 127:12291-12305 (Pubitemid 41279253)
17. Franks WT, Wylie BJ, Frericks Schmidt HL, Nieuwkoop AJ, Mayrhofer RM, Shah GJ, Graesser DT, Rienstra CM (2008) Dipole tensor-based refinement for atomic-resolution structure determination of a nanocrystalline protein by solid-state NMR spectroscopy. Proc Natl Acad Sci USA 105:4621-4626 (Pubitemid 351753796)
18. Gronenborn AM, Filpula DR, Essig NZ, Achari A, Whitlow M, Wingfield PT, Clore GM (1991) A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G. Science 253:657-661 (Pubitemid 21917198)
19. Grzesiek S, Bax A (1992a) An efficient experiment for sequential backbone assignment of medium-sized isotopically enriched proteins. J Magn Reson 99:201-207
20. Grzesiek S, Bax A (1992b) Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J Am Chem Soc 114:6291-6293
21. Grzesiek S, Bax A (1992c) Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein. J Magn Reson 96:432-440
22. Habenstein B, Wasmer C, Bousset L, Sourigues Y, Schütz A, Loquet A, Meier B, Melki R, Böckmann A (2011) Extensive de novo solid-state NMR assignments of the 33 kDa C-terminal domain of the Ure2 prion. J Biomol NMR 51:235-243
23. Hansen PE (2000) Isotope effects on chemical shifts of proteins and peptides. Magn Reson Chem 38:1-10
24. Hediger S, Meier BH, Kurur ND, Bodenhausen G, Ernst RR (1994) NMR cross polarization by adiabatic passage through the Hartmann-Hahn condition (APHH). Chem Phys Lett 223:283-288
25. Heise H, Hoyer W, Becker S, Andronesi OC, Riedel D, Baldus M (2005) Molecular-level secondary structure, polymorphism, and dynamics of full-length alpha-synuclein fibrils studied by solidstate NMR. Proc Natl Acad Sci USA 102:15871-15876 (Pubitemid 41552835)
26. Hong M (2007) Structure, topology, and dynamics of membrane peptides and proteins from solid-state NMR spectroscopy. J Phys Chem B 111:10340-10351 (Pubitemid 47441837)
27. Huber M, Hiller S, Schanda P, Ernst M, Böckmann A, Verel R, Meier BH (2011) A proton-detected 4D solid-state NMR experiment for protein structure determination. Chem Phys Chem 12:915-918
28. Ikura M, Kay LE, Bax A (1990) A novel approach for sequential assignment of 1H, 13C, and 15 N spectra of larger proteins: Heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry 29:4659-4667 (Pubitemid 20172684)
29. Inaba K, Ito K (2008) Structure and mechanisms of the DsbB-DsbA disulfide bond generation machine. Biochim Biophys Acta 1783:520-529
30. Ishii Y, Yesinowski JP, Tycko R (2001) Sensitivity enhancement in solid-state 13C NMR of synthetic polymers and biopolymers by 1H NMR detection with high-speed magic angle spinning. J Am Chem Soc 123:2921-2922 (Pubitemid 32910734)
31. Iwata K, Fujiwara T, Matsuki Y, Akutsu H, Takahashi S, Naiki H, Goto Y (2006) 3D structure of amyloid protofilaments of beta2-microglobulin fragment probed by solid-state NMR. Proc Natl Acad Sci USA 103:18119-18124 (Pubitemid 44871622)
32. 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 101:711-716 (Pubitemid 38121022)
33. Jehle S, Rajagopal P, Bardiaux B, Markovic S, Kuhne R, Stout JR, Higman VA, Klevit RE, van Rossum B-J, Oschkinat H (2010) Solid-state NMR and SAXS studies provide a structural basis for the activation of aB-crystallin oligomers. Nat Struct Mol Biol 17:1037-1042
34. Kay LE, Ikura M, Tschudin R, Bax A (1990) Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins. J Magn Reson 89:496-514
35. Kloepper KD, Woods WS, Winter KA, George JM, Rienstra CM (2006) Preparation of a-synuclein fibrils for solid-state NMR: Expression, purification, and incubation of wild-type and mutant forms. Protein Express Purif 48:112-117 (Pubitemid 43782618)
36. Kloepper K, Zhou D, Li Y, Winter K, George J, Rienstra C (2007) Temperature-dependent sensitivity enhancement of solid-state NMR spectra of a-synuclein fibrils. J Biomol NMR 39:197-211 (Pubitemid 47617504)
37. Knight MJ, Webber AL, Pell AJ, Guerry P, Barbet-Massin E, Bertini I, Felli IC, Gonnelli L, Pierattelli R, Emsley L, Lesage A, Herrmann T, Pintacuda G (2011) Fast resonance assignment and fold determination of human superoxide dismutase by highresolution proton-detected solid-state MAS NMR spectroscopy. Angew Chem Int Ed 50:11697-11701
38. Lange A, Becker S, Seidel K, Pongs O, Baldus M (2005) A concept for rapid protein-structure determination by solid-state NMR spectroscopy. Angew Chem Int Ed 44:2089-2092
39. Lewandowski JzR, Dumez J-N, Akbey Um, Lange S, Emsley L, Oschkinat H (2011) Enhanced resolution and coherence lifetimes in the solid-state NMR spectroscopy of perdeuterated proteins under ultrafast magic-angle spinning. J Phys Chem Lett 2:2205-2211
40. Li Y, Berthold DA, Frericks HL, Gennis RB, Rienstra CM (2007) Partial 13C and 15 N chemical-shift assignments of the disulfide-bond-forming enzyme DsbB by 3D magic-angle spinning NMR spectroscopy. Chem Bio Chem 8:434-442 (Pubitemid 47183662)
41. Li Y, Berthold DA, Gennis RB, Rienstra CM (2008) Chemical shift assignment of the transmembrane helices of DsbB, a 20-kDa integral membrane enzyme, by 3D magic-angle spinning NMR spectroscopy. Prot Sci 17:199-204 (Pubitemid 351171832)
42. Linser R (2012) Backbone assignment of perdeuterated proteins using long-range H/C-dipolar transfers. J. Biolmol. NMR 52:151-158
43. Linser R, Fink U, Reif B (2008) Proton-detected scalar coupling based assignment strategies in MAS solid-state NMR spectroscopy applied to perdeuterated proteins. J Magn Reson 193:89-93
44. Linser R, Fink U, Reif B (2010a) Assignment of dynamic regions in biological solids enabled by spin-state selective NMR experiments. J Am Chem Soc 132:8891-8893
45. Linser R, Fink U, Reif B (2010b) Narrow carbonyl resonances in proton-diluted proteins facilitate NMR assignments in the solidstate. J Biomol NMR 47:1-6
46. Linser R, Bardiaux B, Higman V, Fink U, Reif B (2011a) Structure calculation from unambiguous long-range amide and methyl 1H-1H distance restraints for a microcrystalline protein with MAS solid-state NMR spectroscopy. J Am Chem Soc 133:5905-5912
47. Linser R, Dasari M, Hiller M, Higman V, Fink U, LopezdelAmo J-M, Markovic S, Handel L, Kessler B, Schmieder P, Oesterhelt D, Oschkinat H, Reif B (2011b) Proton-detected solid-state NMR spectroscopy of fibrillar and membrane proteins. Angew Chem Int Ed 50:4508-4512
48. Loquet A, Bardiaux B, Gardiennet C, Blanchet C, Baldus M, Nilges M, Malliavin T, Bockmann A (2008) 3D Structure determination of the Crh protein from highly ambiguous solid-state NMR restraints. J Am Chem Soc 130:3579-3589 (Pubitemid 351456062)
49. Mani R, Tang M, Wu X, Buffy JJ, Waring AJ, Sherman MA, Hong M (2006) Membrane-bound dimer structure of a beta-hairpin antimicrobial peptide from rotational-echo double-resonance solid-state NMR. Biochemistry 45:8341-8349 (Pubitemid 44036540)
50. Manolikas T, Herrmann T, Meier BH (2008) Protein structure determination from 13C spin-diffusion solid-state NMR spectroscopy. J Am Chem Soc 130:3959-3966 (Pubitemid 351429863)
51. Nielsen JT, Bjerring M, Jeppesen MD, Pedersen RO, Pedersen JM, Hein KL, Vosegaard T, Skrydstrup T, Otzen DE, Nielsen NC (2009) Unique identification of supramolecular structures in amyloid fibrils by solid-state NMR spectroscopy. Angew Chem Int Ed 48:2118-2121
52. Nietlispach D (2004) A selective intra-HN(CA)CO experiment for the backbone assignment of deuterated proteins. J Biomol NMR 28:131-136 (Pubitemid 38232792)
53. Nietlispach D, Ito Y, Laue ED (2002) A novel approach for the sequential backbone assignment of larger proteins: Selective intra-HNCA and DQ-HNCA. J Am Chem Soc 124:11199-11207 (Pubitemid 35025679)
54. Nieuwkoop AJ, Rienstra CM (2010) Supramolecular protein structure determination by site-specific long-range intermolecular solid state NMR spectroscopy. J Am Chem Soc 132:7570-7571
55. Otzen DE (2003) Folding of DsbB in mixed micelles: A kinetic analysis of the stability of a bacterial membrane protein. J Mol Biol 330:641-649
56. Paulson EK, Morcombe CR, Gaponenko V, Dancheck B, Byrd RA, Zilm KW (2003) Sensitive high resolution inverse detection NMR spectroscopy of proteins in the solid state. J Am Chem Soc 125:15831-15836 (Pubitemid 37553700)
57. Permi P, Annila A (2004) Coherence transfer in proteins. Prog Nucl Magn Reson Spectrosc 44:97-137
58. Reif B, Jaroniec CP, Rienstra CM, Hohwy M, Griffin RG (2001) H-1-H-1 MAS correlation spectroscopy and distance measurements in a deuterated peptide. J Magn Reson 151:320-327
59. Schuetz A, Wasmer C, Habenstein B, Verel R, Greenwald J, Riek R, Böckmann A, Meier BH (2010) Protocols for the sequential solid-state NMR spectroscopic assignment of a uniformly labeled 25 kDa protein: HET-s(1-227). Chem Bio Chem 11:1543-1551
60. Shi L, Lake EMR, Ahmed MAM, Brown LS, Ladizhansky V (2009) Solid-state NMR study of proteorhodopsin in the lipid environment: Secondary structure and dynamics. Biochim Biophys Acta 1788:2563-2574
61. Sperling LJ, Berthold DA, Sasser TL, Jeisy-Scott V, Rienstra CM (2010) Assignment strategies for large proteins by magic-angle spinning NMR: The 21-kDa disulfide bond forming enzyme DsbA. J Mol Biol 399:268-282
62. Spillantini MG, Schmidt ML, Lee VMY, Trojanowski JQ, Jakes R, Goedert M (1997) alpha-Synuclein in Lewy bodies. Nature 388:839-840
63. Tang M, Berthold DA, Rienstra CM (2011a) Solid-state NMR of a large membrane protein by paramagnetic relaxation enhancement. J Phys Chem Lett 2:1836-1841
64. Tang M, Sperling L, Berthold D, Schwieters C, Nesbitt A, Nieuwkoop A, Gennis R, Rienstra C (2011b) High-resolution membrane protein structure by joint calculations with solid-state NMR and X-ray experimental data. J Biomol NMR 51:227-233
65. Tang M, Sperling LJ, Berthold DA, Nesbitt AE, Gennis RB, Rienstra CM (2011c) Solid-state NMR study of the charge-transfer complex between ubiquinone-8 and disulfide bond generating membrane protein DsbB. J Am Chem Soc 133:4359-4366
66. Tossavainen H, Permi P (2004) Optimized pathway selection in intraresidual triple-resonance experiments. J Magn Reson 170:244-251
67. Verel R, Baldus M, Ernst M, Meier BH (1998) A homonuclear spinpair filter for solid-state NMR based on adiabatic-passage techniques. Chem Phys Lett 287:421-428 (Pubitemid 128183917)
68. Ward ME, Shi L, Lake E, Krishnamurthy S, Hutchins H, Brown LS, Ladizhansky V (2011) Proton-detected solid-state NMR reveals intramembrane polar networks in a seven-helical transmembrane protein proteorhodopsin. J Am Chem Soc 133:17434-17443
69. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319:1523-1526 (Pubitemid 351398180)
70. Wittekind M, Mueller L (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha-and beta-carbon resonances in proteins. J. Magn. Reson. B 101:201-205
71. Zhou DH, Rienstra CM (2008a) High-performance solvent suppression for proton-detected solid-state NMR. J Magn Reson 192: 167-172
72. Zhou DH, Rienstra CM (2008b) Rapid analysis of organic compounds by proton-detected heteronuclear correlation NMR spectroscopy at 40 kHz magic-angle spinning. Angew Chem Int Ed 47: 7328-7331
73. Zhou D, Kloepper K, Winter K, Rienstra C (2006a) Band-selective 13C homonuclear 3D spectroscopy for solid proteins at high field with rotor-synchronized soft pulses. J Biomol NMR 34:245-257
74. Zhou DH, Graesser DT, Franks WT, Rienstra CM (2006b) Sensitivity and resolution in proton solid-state NMR at intermediate deuteration levels: Quantitative linewidth characterization and applications to correlation spectroscopy. J Magn Reson 178: 297-307 (Pubitemid 43107936)
75. Zhou DH, Shah G, Cormos M, Mullen C, Sandoz D, Rienstra CM (2007a) Proton-detected solid-state NMR spectroscopy of fully protonated proteins at 40 kHz magic-angle spinning. J Am Chem Soc 129:11791-11801 (Pubitemid 47479927)
76. Zhou DH, Shea JJ, Nieuwkoop AJ, Franks WT, Wylie BJ, Mullen C, Sandoz D, Rienstra CM (2007b) Solid-state protein-structure determination with proton-detected triple-resonance 3D magicangle-spinning NMR spectroscopy. Angew Chem Int Ed 46: 8380-8383 (Pubitemid 350114943)
77. Zhou Y, 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 31:896-908
78. Zhou DH, Shah G, Mullen C, Sandoz D, Rienstra CM (2009) Protondetected solid-state NMR of natural abundance peptide and protein pharmaceuticals. Angew Chem Int Ed 48:1253-1256