Efficient resonance assignment of proteins in MAS NMR by simultaneous intra- and inter-residue 3D correlation spectroscopy

Journal of Biomolecular NMR

Volumn 55, Issue 3, 2013, Pages 257-265

  Daviso, Eugenio ^a,b   Eddy, Matthew T ^b   Andreas, Loren B ^b   Griffin, Robert G ^b   Herzfeld, Judith ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

3D MAS NMR; DARR; Sidechain backbone correlation; TEDOR

Indexed keywords

ALANINE; ARGININE; CARBON 13; GB1 PROTEIN; GVPA PROTEIN; LYSINE; NITROGEN 15; PROLINE; PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; ATOM; CARBOXY TERMINAL SEQUENCE; MAGIC ANGLE SPINNING NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLARIZATION; PRIORITY JOURNAL; RADIOFREQUENCY;

CARBON ISOTOPES; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEINS;

EID: 84877920130     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-013-9707-0     Document Type: Article

References (62)

1. Ader C, Pongs O, Becker S, Baldus M (2010) Protein dynamics detected in a membrane-embedded potassium channel using two-dimensional solid-state NMR spectroscopy. Biochim Biophys Acta-Biomembranes 1798(2):286-290. doi: 10.1016/j.bbamem.2009.06.023
2. Andreas LB, Eddy MT, Pielak RM, Chou J, Griffin RG (2010) Magic angle spinning NMR investigation of influenza A M2(18-60): support for an allosteric mechanism of inhibition. J Am Chem Soc 132(32):10958-10960. doi: 10.1021/ja101537p
3. Andreas LB, Eddy MT, Chou JJ, Griffin RG (2012) Magic-angle-spinning NMR of the drug resistant S31N M2 proton transporter from influenza A. J Am Chem Soc 134(17):7215-7218. doi: 10.1021/ja3003606
4. Bajaj VS, van der Wel PCA, Griffin RG (2009) Observation of a low-temperature, dynamically driven structural transition in a polypeptide by solid-state NMR spectroscopy. J Am Chem Soc 131(1):118-128. doi: 10.1021/ja8045926
5. 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(6):1197-1207. doi: 10.1080/002689798166215
6. Bateman DA, Tycko R, Wickner RB (2011) Experimentally derived structural constraints for amyloid fibrils of wild-type transthyretin. Biophys J 101(10):2485-2492. doi: 10.1016/j.bpj.2011.10.009
7. Bayro MJ, Maly T, Birkett NR, MacPhee CE, Dobson CM, Griffin RG (2010) High-resolution MAS NMR analysis of PI3-SH3 amyloid fibrils: backbone conformation and implications for protofilament assembly and structure. Biochemistry 49(35):7474-7484. doi: 10.1021/bi100864t
8. Bayro MJ, Debelouchina GT, Eddy MT, Birkett NR, MacPhee CE, Rosay M, Maas WE, Dobson CM, Griffin RG (2011) Intermolecular structure determination of amyloid fibrils with magic-angle spinning and dynamic nuclear polarization NMR. J Am Chem Soc 133(35):13967-13974. doi: 10.1021/ja203756x
9. Bayro MJ, Daviso E, Belenky M, Griffin RG, Herzfeld J (2012) An amyloid organelle, solid-state NMR evidence for cross-beta assembly of gas vesicles. J Biol Chem 287(5):3479-3484. doi: 10.1074/jbc.M111.313049
10. Bennett AE, Becerra LR, Griffin RG (1994) Frequency-selective heteronuclear recoupling in rotating solids. J Chem Phys 100(2):812-814. doi: 10.1063/1.466563
11. Bernstein FC, Koetzle TF, Williams GJB, Meyer EF, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M (1977) Protein data bank - computer-based archival file for macromolecular structures. J Mol Biol 112(3):535-542. doi: 10.1016/s0022-2836(77)80200-3
12. Bhate MP, Wylie BJ, Tian L, McDermott AE (2010) Conformational dynamics in the selectivity filter of KcsA in response to potassium ion concentration. J Mol Biol 401(2):155-166. doi: 10.1016/j.jmb.2010.06.031
13. Bockmann A (2008) 3D protein structures by solid-state NMR spectroscopy: ready for high resolution. Angew Chem Int Ed 47(33):6110-6113. doi: 10.1002/anie.200801352
14. Brinkmann A, Levitt MH (2001) Symmetry principles in the nuclear magnetic resonance of spinning solids: heteronuclear recoupling by generalized Hartmann-Hahn sequences. J Chem Phys 115(1):357-384. doi: 10.1063/1.1377031
15. Comellas G, Lemkau LR, Zhou DH, George JM, Rienstra CM (2012) Structural intermediates during alpha-synuclein fibrillogenesis on phospholipid vesicles. J Am Chem Soc 134(11):5090-5099. doi: 10.1021/ja209019s
16. Debelouchina GT, Platt GW, Bayro MJ, Radford SE, Griffin RG (2010a) Intermolecular alignment in beta(2)-microglobulin amyloid fibrils. J Am Chem Soc 132(48):17077-17079. doi: 10.1021/ja1079871
17. Debelouchina GT, Platt GW, Bayro MJ, Radford SE, Griffin RG (2010b) Magic angle spinning NMR analysis of beta(2)-microglobulin amyloid fibrils in two distinct morphologies. J Am Chem Soc 132(30):10414-10423. doi: 10.1021/ja102775u
18. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) Nmrpipe - a multidimensional spectral processing system based on unix pipes. J Biomol NMR 6(3):277-293. doi: 10.1007/bf00197809
19. Eddy MT, Ong T-C, Clark L, Teijido O, van der Wel PCA, Garces R, Wagner G, Rostovtseva TK, Griffin RG (2012a) Lipid dynamics and protein-lipid interactions in 2D crystals formed with the beta-barrel integral membrane protein VDAC1. J Am Chem Soc 134(14):6375-6387. doi: 10.1021/ja300347v
20. Eddy MT, Ruben D, Griffin RG, Herzfeld J (2012b) Deterministic schedules for robust and reproducible non-uniform sampling in multidimensional NMR. J Magn Reson 214:296-301. doi: 10.1016/j.jmr.2011.12.002
21. Franks WT, Zhou DH, Wylie BJ, Money BG, Graesser DT, Frericks HL, Sahota G, Rienstra CM (2005) Magic-angle spinning solid-state NMR spectroscopy of the beta 1 immunoglobulin binding domain of protein G (GB1): N-15 and C-13 chemical shift assignments and conformational analysis. J Am Chem Soc 127(35):12291-12305. doi: 10.1021/ja044497e
22. Fu RQ, Smith SA, Bodenhausen G (1997) Recoupling of heteronuclear dipolar interactions in solid state magic-angle spinning NMR by simultaneous frequency and amplitude modulation. Chem Phys Lett 272(5-6):361-369. doi: 10.1016/s0009-2614(97)00537-x
23. Gullion T, Schaefer J (1989) Rotational-echo double-resonance nmr. J Magn Reson 81(1):196-200. doi: 10.1016/0022-2364(89)90280-1
24. Hansen JO, Kehlet C, Bjerring M, Vosegaard T, Glaser SJ, Khaneja N, Nielsen NC (2007) Optimal control based design of composite dipolar recoupling experiments by analogy to single-spin inversion pulses. Chem Phys Lett 447(1-3):154-161. doi: 10.1016/j.cplett.2007.08.072
25. Helmus JJ, Nadaud PS, Hofer N, Jaroniec CP (2008) Determination of methyl C-13-N-15 dipolar couplings in peptides and proteins by three-dimensional and four-dimensional magic-angle spinning solid-state NMR spectroscopy. J Chem Phys 128 (5):052314/1-16. doi: 10.1063/1.2817638
26. Higman VA, Flinders J, Hiller M, Jehle S, Markovic S, Fiedler S, van Rossum B-J, Oschkinat H (2009) Assigning large proteins in the solid state: a MAS NMR resonance assignment strategy using selectively and extensively C-13-labelled proteins. J Biomol NMR 44(4):245-260. doi: 10.1007/s10858-009- 9338-7
27. Higman VA, Varga K, Aslimovska L, Judge PJ, Sperling LJ, Rienstra CM, Watts A (2011) The Conformation of bacteriorhodopsin loops in purple membranes resolved by solid-state MAS NMR spectroscopy. Angew Chem Int Ed 50(36):8432-8435. doi: 10.1002/anie.201100730
28. Hing AW, Vega S, Schaefer J (1992) Transferred-echo double-resonance NMR. J Magn Reson 96(1):205-209. doi: 10.1016/0022-2364(92)90305-q
29. Hu K-N, McGlinchey RP, Wickner RB, Tycko R (2011) Segmental polymorphism in a functional amyloid. Biophys J 101(9):2242-2250. doi: 10.1016/j.bpj.2011.09. 051
30. Jaroniec CP, MacPhee CE, Astrof NS, Dobson CM, Griffin RG (2002a) Molecular conformation of a peptide fragment of transthyretin in an amyloid fibril. Proc Natl Acad Sci USA 99(26):16748-16753. doi: 10.1073/pnas.252625999
31. Jaroniec CP, Filip C, Griffin RG (2002b) 3D TEDOR NMR experiments for the simultaneous measurement of multiple carbon-nitrogen distances in uniformly C-13, N-15-labeled solids. J Am Chem Soc 124(36):10728-10742. doi: 10.1021/ja026385y
32. Kehlet C, Bjerring M, Sivertsen AC, Kristensen T, Enghild JJ, Glaser SJ, Khaneja N, Nielsen NC (2007) Optimal control based NCO and NCA experiments for spectral assignment in biological solid-state NMR spectroscopy. J Magn Reson 188(2):216-230. doi: 10.1016/j.jmr.2007.06.011
33. Kryndushkin DS, Wickner RB, Tycko R (2011) The Core of Ure2p Prion fibrils is formed by the N-terminal segment in a parallel cross-beta structure: evidence from solid-state NMR. J Mol Biol 409(2):263-277. doi: 10.1016/j.jmb.2011.03.067
34. Lemkau LR, Comellas G, Kloepper KD, Woods WS, George JM, Rienstra CM (2012) Mutant protein A30P alpha-synuclein adopts wild-type fibril structure, despite slower fibrillation kinetics. J Biol Chem 287(14):11526-11532. doi: 10.1074/jbc.M111.306902
35. Lewandowski JR, De Paepe G, Griffin RG (2007) Proton assisted insensitive nuclei cross polarization. J Am Chem Soc 129(4):728-729. doi: 10.1021/ja0650394
36. 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. Protein Sci 17(2):199-204. doi: 10.1110/ps.073225008
37. 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
38. Long JR, Sun BQ, Bowen A, Griffin RG (1994) Molecular dynamics and magic-angle-spinning NMR. J Am Chem Soc 116(26):11950-11956. doi: 10.1021/ja00105a039
39. Lv G, Kumar A, Giller K, Orcellet ML, Riedel D, Fernandez CO, Becker S, Lange A (2012) Structural comparison of mouse and human alpha-synuclein amyloid fibrils by solid-state NMR. J Mol Biol 420(1-2):99-111. doi: 10.1016/j.jmb.2012.04.009
40. Matsuki Y, Eddy MT, Herzfeld J (2009) Spectroscopy by integration of frequency and time domain information for fast acquisition of high-resolution dark spectra. J Am Chem Soc 131(13):4648-4656. doi: 10.1021/ja807893k
41. Matsuki Y, Eddy MT, Griffin RG, Herzfeld J (2010) Rapid three-dimensional MAS NMR spectroscopy at critical sensitivity. Angew Chem Int Ed 49(48):9215-9218. doi: 10.1002/anie.201003329
42. Maus DC, Copie V, Sun BQ, Griffiths JM, Griffin RG, Luo SF, Schrock RR, Liu AH, Seidel SW, Davis WM, Grohmann A (1996) A solid-state NMR study of tungsten methyl group dynamics in W(eta(5)-C(5)Me(5))Me(4) PF6. J Am Chem Soc 118(24):5665-5671. doi: 10.1021/ja960248h
43. 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
44. Nieuwkoop AJ, Rienstra CM (2010) Supramolecular protein structure determination by site-specific long-range intermolecular solid state NMR Spectroscopy. J Am Chem Soc 132(22):7570-7571. doi: 10.1021/ja100992y
45. Paravastu AK, Leapman RD, Yau W-M, 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
46. Paravastu AK, Qahwash I, Leapman RD, Meredith SC, Tycko R (2009) Seeded growth of beta-amyloid fibrils from Alzheimer's brain-derived fibrils produces a distinct fibril structure. Proc Natl Acad Sci USA 106(18):7443-7448. doi: 10.1073/pnas.0812033106
47. Qiang W, Yau W-M, Luo Y, Mattson MP, Tycko R (2012) Antiparallel beta-sheet architecture in Iowa-mutant beta-amyloid fibrils. Proc Natl Acad Sci USA 109(12):4443-4448. doi: 10.1073/pnas.1111305109
48. Renault M, Bos MP, Tommassen J, Baldus M (2011) Solid-State NMR on a large multidomain integral membrane protein: the outer membrane protein assembly factor BamA. J Am Chem Soc 133(12):4175-4177. doi: 10.1021/ja109469c
49. Riedel K, Leppert J, Ohlenschlager O, Gorlach M, Ramachandran R (2005) TEDOR with adiabatic inversion pulses: resonance assignments of C-13/N-15 labelled RNAs. J Biomol NMR 31(1):49-57. doi: 10.1007/s10858-004-6066-x
50. Rienstra CM, Hohwy M, Hong M, Griffin RG (2000) 2D and 3D N-15-C-13-C-13 NMR chemical shift correlation spectroscopy of solids: assignment of MAS spectra of peptides. J Am Chem Soc 122(44):10979-10990. doi: 10.1021/ja001092v
51. Schaefer J, McKay RA, Stejskal EO (1979) Double-cross-polarization nmr of solids. J Magn Reson 34(2):443-447. doi: 10.1016/0022-2364(79)90022-2
52. Schmidt HLF, Sperling LJ, Gao YG, Wylie BJ, Boettcher JM, Wilson SR, Rienstra CA (2007) Crystal polymorphism of protein GB1 examined by solid-state NMR spectroscopy and X-ray diffraction. J Phys Chem B 111(51):14362-14369. doi: 10.1021/jp075531p
53. Sivanandam VN, Jayaraman M, Hoop CL, Kodali R, Wetzel R, van der Wel PCA (2011) The aggregation-enhancing Huntingtin N-terminus is helical in amyloid fibrils. J Am Chem Soc 133(12):4558-4566. doi: 10.1021/ja110715f
54. Sivertsen AC, Bayro MJ, Belenky M, Griffin RG, Herzfeld J (2009) Solid-State NMR evidence for inequivalent GvpA subunits in gas vesicles. J Mol Biol 387(4):1032-1039. doi: 10.1016/j.jmb.2009.02.015
55. Sivertsen AC, Bayro MJ, Belenky M, Griffin RG, Herzfeld J (2010) Solid-state NMR characterization of gas vesicle structure. Biophys J 99(6):1932-1939. doi: 10.1016/j.bpj.2010.06.041
56. 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(2):268-282. doi: 10.1016/j.jmb.2010.04.012
57. Sun BQ, Costa PR, Kocisko D, Lansbury PT, Griffin RG (1995) Internuclear distance measurements in solid-state nuclear-magnetic-resonance - dipolar recoupling via rotor synchronized spin locking. J Chem Phys 102(2):702-707. doi: 10.1063/1.469182
58. Van Melckebeke H, Wasmer C, Lange A, Ab E, Loquet A, Bockmann A, Meier BH (2010) Atomic-resolution three-dimensional structure of HET-s(218-289) amyloid fibrils by solid-state NMR spectroscopy. J Am Chem Soc 132(39):13765-13775. doi: 10.1021/ja104213J
59. Varga K, Tian L, McDermott AE (2007) Solid-state NMR study and assignments of the KcsA potassium ion channel of S. lividans. Biochim Biophys Acta-Prot Proteom 1774(12):1604-1613. doi: 10.1016/j.bbapap.2007.08.029
60. Warschawski D (2011) Proteins of known structure determined by solid-State NMR. http://www.drorlist.com/nmr/SPNMR.html
61. 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(5869):1523-1526. doi: 10.1126/science.1151839
62. Zhao X, Eden M, Levitt MH (2001) Recoupling of heteronuclear dipolar interactions in solid-state NMR using symmetry-based pulse sequences. Chem Phys Lett 342(3-4):353-361. doi: 10.1016/s0009-2614(01)00593-0