Oriented Sample Solid-State NMR Spectroscopy Stanley J. Opella University of California, San Diego
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1 Winter School 2016 Oriented Sample Solid-State NMR Spectroscopy Stanley J. Opella University of California, San Diego
2 Introduction.
3 Contents of an Escherichia coli cell is enclosed by its plasma membrane, a phospholipid bilayer. soluble proteins membrane proteins
4 1972
5 IL-8 immobilized upon interaction with CXCR1 in phospholipid bilayers. 15 N IL-8 membrane protein IL-8:CXCR1 (1:1) in bilayers 15 N IL-8 soluble protein IL-8 alone in solution solution 1 H NMR spectra of amide hydrogens of IL-8 (66 residues)
6 Solution NMR of a membrane protein in membrane-like environments. uniformly 15 N labeled MerF (80 residues) q = DMPC / DHPC
7 Basic requirements of an NMR approach to membrane proteins. Solve the correlation time problem. High sensitivity. High resolution. Determine protein structures. Resolve resonances. Assign resonances. Measure frequencies. Extract orientation and/or distance constraints. Calculate structures.
8 1972
9 Dissecting solid-state NMR.
10 Separated Local Field Spectroscopy
11 Selecting the correct power lines.
12 Untangling the power lines: homonuclear decoupling.
13 1968
14 Boosting the power lines: cross-polarization.
15 Untangling the power lines: heteronuclear decoupling.
16 1972
17 Selecting the correct power lines: separated local field spectroscopy.
18 Attenuation of dipole-dipole couplings when the 1 H nuclei are abundant.
19 1965
20 Dipolar oscillations during CP build-up. 1974
21 Dipolar oscillations during CP build-up under Lee-Goldburg irradiation analyzed by Fourier transformation. 1975
22 Separated Local Field Spectroscopy. 1 H- 13 C Dipolar Coupling 13 C Chemical Shift Separation by: 1) chemical shifts of the dilute spins 2) homonuclear decoupling of the abundant spins 1976
23 1 H - 1 H spins in water in gypsum. 1 H are dilute by space. θ H N r Δν (3 cos 2 θ - 1) r 3
24
25 1 H - 15 N spins in peptide bond. 15 N is dilute by space. 1 H is abundant in large bath. θ H N r Δν (3 cos 2 θ - 1) r 3
26 The dipole-dipole interaction is anisotropic. Powder pattern. Single crystal rotation pattern. 1948
27 The chemical shift interaction is anisotropic. 13 C is dilute by isotopic composition. There are no 1 H. 1958
28 Separated local field spectra of a uniaxially aligned polymer. 1977
29 Separated local field spectrum of a specifically 15 N labeled protein aligned and immobilized within a virus particle. 1983
30 Separated local field spectra of selectively and uniformly 15 N proteins aligned and immobilized in a virus particle. 1985
31 PISEMA. 1994
32 Improvements in solid-state NMR spectra of proteins
33 Orientationally-dependent frequencies provide high resolution and map the structure onto the spectra of aligned bilayer samples. 1 TM 2 TM 3 TM 7 TM Two-dimensional Separated Local Field (SAMPI4) spectra of uniformly 15 N labeled membrane proteins in magnetically-aligned phospholipid bilayers.
34 Resolved signals from CXCR1 in aligned bilayers. One-dimensional Bo Two-dimensional
35 Resolution from higher dimensions.
36 Orientationally-dependent frequencies provide high resolution and map the structure onto the spectra of aligned bilayer samples. 1 TM 2 TM 3 TM 7 TM Two-dimensional Separated Local Field (SAMPI4) spectra of uniformly 15 N labeled membrane proteins in magnetically-aligned phospholipid bilayers.
37
38 PISA Wheels: Polarity Index Slant Angle. 2000
39 PISA wheels. Slant Angle Polarity Index
40 Structure determination
41 α-helix geometry and periodicity. H-N bond is 15 tilted away from the helix axis f(θ av,φ av,ρ 0 )
42 Dipolar Waves: La Jolla Cove.
43 Dipolar Waves. fd coat protein
44 Sample alignment.
45 The effects of lipid assemblies on protein reorientation rates. micelles bicelles bilayers
46 2004
47 Trans-membrane domain of channel-forming viral membrane protein Vpu.
48 MerFt (60 aa)
49 Rotational sample alignment.
50 10 6 sec -1 R. A. Cone, Rotational diffusion of rhodopsin in the visual receptor membrane, Nature (N.B.) 236, 35 (1972) M. Edidin, Rotational and translational diffusion in membranes, Ann Rev Biophys Bioeng, 3, 179 (1974)
51 Principle used in our current approach to structure determination of membrane proteins: spinnin. And you know that tilt-a-whirl down on the south beach drag I got on it last night and my shirt got caught And that joey kept me spinnin I didn t think I d ever get off" Springsteen, B. (1973) 4 th of July, Asbury Park / Sandy
52 Background for the method. The effect of rotational diffusion on chemical shift powder patterns was among the first topics studied by high-resolution solid-state NMR. The angular constraints measured from mechanically, magnetically, and rotationally aligned samples are equivalent. The principal values of static and motionally averaged powder patterns can be determined from unoriented samples using MAS solid-state NMR. Uniformly 13 C and 15 N labeled proteins are readily expressed and purified from E. coli. 13 C-detection improves sensitivity. Assignment schemes that walk down the backbone. All backbone and side chain sites accessible for complete structure determination.
53 The basic principle is the effect of rotational diffusion on powder patterns: the sign of axial symmetry and reduction in frequency span are determined by the angle of rotation. dipole- dipole coupling chemical shi1 anisotropy Structural Investigations by Means of Nuclear Magnetism. II. Hindered Rotation of Solids H Gutowsky G Pake, J Chem Phys 18, 162 (1950) 19 F Shielding Tensors from Coherently Narrowed NMR Powder Spectra M Mehring R Griffin J Waugh, J Chem Phys 55, 746 (1971)
54 Rotational Alignment of membrane proteins in proteoliposomes Unoriented DMPC 3 o C gel phase...line shape can be interpreted in terms of the orientation of the groups with respect to the diffusion axis...similar to that obtained from oriented samples o C liq crys phase
55 15 N powder patterns in unoriented samples
56 Orientational parameters from unoriented samples.
57 Rotational alignment of phospholipids and proteins P NMR 15 N NMR N NMR Unoriented DPPC/chol Oriented DPPC/chol
58 2010 Vpu TM One Site Two Sites fd coat protein 5 o C unoriented unoriented 25 o C mechanically aligned parallel mechanically aligned parallel *magnetically aligned parallel *scaled for order parameter
59 Magic Angle Spinning.
60 Cross-polarization magic angle spinning: CPMAS.
61 Stationary vs. MAS 13 C NMR spectra of CXCR1 in bilayers. 10 khz MAS stationary
62 Membrane proteins undergo fast rotational diffusion about the bilayer normal in liquid crystalline phospholipid bilayers. n 62
63 Unoriented proteoliposomes. n n n n 63
64 Unoriented proteoliposomes. n n θ O 13 C n n n rota6onal averaging of 13 C CSA in a trans- membrane helix
65 Magic angle sample spinning and rotational diffusion of proteins. n 13 C CSA recoupled from 11 khz MAS n n Bo 13 C CSA sidebands from 5 khz MAS n experimental 55 o simulated
66 One-dimensional MAS solid-state NMR to verify that protein is rotationally aligned: at 25 C but not 10 C. simulated 13 C NMR experimental 13 C NMR stationary 5 khz MAS stationary 5 khz MAS rotating 25 o C immobile 10 o C
67 Temperature dependence of rotational diffusion of MerFt monitored by 13 C Chemical Shift Anisotropy. Ratio of center band to side band
68 Membrane protein structure.
69 Biological mechanism. G-protein coupled receptors (GPCRs). Activated by specific signals (drug). Protein changes conformation. Triggers activation of G-proteins and signaling. GPCRs as structure targets. Receptors for 50% of drugs. $60 billion/year market. Hundreds of drug receptors in the human genome. GPCRs as proteins. 7 TM membrane proteins. > 350 residues. CXCR1 as example.
70 Global dynamics of CXCR1 in phospholipid bilayers from rotational averaging of 13 C carbonyl CSA powder patterns. 25 o C 5 o C
71 Local motions of CXCR1: MAS solid-state INEPT shows mobile termini in bilayers.
72 Two-dimensional NMR of CXCR1 in phospholipid bilayers. 13 C chemical shift / 13 C chemical shift correlation spectrum. Carbonyl Aromatic Aliphatic C α
73 Three-dimensional MAS 1 H- 15 N DC/ 15 N Shift/ 13 Cα Shift Correlation: two-dimensional 1 H- 15 N DC/ 13 Cα Shift planes. U- 13 C, 15 N CXCR1 in DMPC liposomes
74 Three-dimensional spectra of CXCR1 in phospholipid bilayers. 3D 13 C-detected R HNCαCO HN SLF HαCα SLF
75 Two-dimensional MAS 1 H- 13 C DC/ 13 C Shift Correlation of CXCR1. 30 o C with rota6onal diffusion 5 o C sta6c 0.5 DC U- 13 C, 15 N CXCR1 in DMPC liposomes
76 Planes from three-dimensional SLF spectra of CXCR1. 1 H- 13 C 1 H- 15 N
77 1 H- 15 N heteronuclear dipolar coupling as a function of residue number for CXCR1 in bilayers.
78 Angles between H-Cα bond vectors and bilayer normal are determined from rotationally-averaged 1 H- 13 Cα Pake doublets. bilayer normal n parallel static 45.0 khz 152 o parallel recoupled 28.8 khz 14.4 khz experimental 48 o parallel recoupled 7.2 khz 3.6 khz experimental
79 Sidechain structure and dynamics from dipolar couplings.
80 13 C chemical shifts show that two disulfide bonds are intact.
81 Three-dimensional structure of CXCR1 in phospholipid bilayers.
82 Global motions of CXCR1: rotational diffusion in a liquid crystalline phospholipid bilayer.
83 Advantages of this NMR method for determining the structures of membrane proteins. The protein resides in a native environment of liquid crystalline phospholipid bilayers under physiological conditions of temperature and ph. Unmodified protein sequence; no truncations, mutations, or insertion of foreign proteins. Protein is active under the experimental conditions. Can vary composition of lipids, add cholesterol, etc. No stabilizing small molecules or antibody fragments. Atomic resolution structures. Can add drugs, effectors, antibody fragments, etc. by adding them to the proteoliposome sample for direct spectroscopic comparisons.
84 Biological membranes at UCSD : The Fluid Mosaic Model of a Membrane to the Structure of the Chemokine Receptor CXCR1 in Phospholipid Bilayers.
85 Acknowledgements GPCR project Spectroscopy and other projects Sang Ho Park Albert Wu Jasmina Radoicic Bibhuti Das Anna De Angelis Ratan Rai Zheng Long Mignon Chu Sabrina Berkamp Francesca Marassi Vivian Wang Hanna Pavlova Supported by the National Institute of Health RO1EB P41EB UCSD NMR resource website:
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