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Restoring Resolution in Biological Solid-State NMR under Conditions of Off-Magic-Angle Spinning Riddhiman Sarkar, Diana C. Rodriguez Camargo, Guido Pintacuda, and Bernd Reif J. Phys. Chem. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.jpclett.5b02467 • Publication Date (Web): 01 Dec 2015 Downloaded from http://pubs.acs.org on December 2, 2015

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The Journal of Physical Chemistry Letters

Restoring Resolution in Biological Solid-State NMR under Conditions of off-Magic-Angle Spinning

Riddhiman Sarkar,a,b Diana C. Rodriguez Camargo a,b , Guido Pintacudac and Bernd Reifa,b*

December 01, 2015

a

Helmholtz-Zentrum München (HMGU), Deutsches Forschungszentrum für

Gesundheit und Umwelt, Ingolstädter Landstr. 1, 85764 Neuherberg, Germany b

Munich Center for Integrated Protein Science (CIPS-M) at Department Chemie, Technische Universität München (TUM), Lichtenbergstr. 4, 85747 Garching, Germany

c

Université de Lyon, Institut de Sciences Analytiques, Centre de RMN à Très Hauts Champs, 5 rue de la Doua, 69100 Villeurbanne, France

For submission to J. Phys. Chem. Lett. To whom correspondence should be addressed: [email protected]

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Abstract Spin-state-selective excitation (S3E) experiments allow the selection of the most slowly relaxing transition under transverse relaxation. We show that in solid-state, the dipole-dipole interaction (DD) of a anisotropy (CSA) of

15

1

H-15N bond vector and the chemical shift

N in an amide moiety mutually cancel each other for a

particular multiplet component, when the sample is spun off the magic angle (Arctan [√2] = 54.74°). In conventional experiments, the accuracy of the adjustment of the spinning angle is crucial for their performance. We demonstrate that for S3E experiments the requirement to spin the sample exactly at the magic angle is not mandatory. Applications in narrow bore magnets will be facilitated where the adjustment of the magic angle is often difficult. The method opens new perspectives for the development of schemes to determine distances and to quantify dynamics in the solid-state.

Table of Contents Figure

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In the last few years, solid state NMR has emerged as a powerful analytical technique to study the structural properties of non-soluble biomolecules, such as amyloid fibrils,1-2, aggregate-chaperone complexes,3, membrane proteins4-5, or large soluble protein complexes.6-8 In conventional solid-state NMR experiments, high power proton decoupling9-12 and Magic Angle Spinning (MAS)13-14 are two key prerequisites to achieve high resolution and sensitivity. Perdeuteration can be used to chemically dilute the dipolar coupling network among protons and to enhance the resolution in proton detected solid-state NMR experiments.15-17 This approach thus allows bypassing the paradigm of high power decoupling in the solid-state. We show here that also the precondition of accurately setting the spinning angle to the magic angle can be partially overcome for perdeuterated proteins. We present a solid-state NMR approach that employs elements in direct analogy to TROSY and RDC techniques in solution. The development of the TROSY technique is a very important contribution in the development of solution-state NMR,18-20 that allows to study large protein complexes, which were so far not accessible.21-22 Due to interference between the 1H-15N DD and the CSA relaxation mechanisms of the amide nitrogen and proton, respectively, the four single quantum (SQ) transitions in

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H,15N

correlation spectra are associated with the anisotropies of different magnitude, resulting in differential relaxation of the four multiplet components. The crosscorrelated relaxation (CCR) rate23-25 as utilized in TROSY experiments increases as a function of the tumbling correlation times (τc) and the relative magnitude of the CSA and the DD interactions. As such, molecules with a large molecular weight yield a larger differential broadening, since τc is proportional to molecular weight. The TROSY effect reaches a maximum at a magnetic field strength of around 23.5 T (1 GHz 1H Larmor frequency).20, 26 At this magnetic field strength, the magnitude of the 1

H-15N DD matches the

excitation (S3E)

27

15

N CSA of the protein backbone amide. Spin-state-selective

and transfer (S3T) experiments select only the slowest relaxing

transition is selected (corresponding to HβN− → H−Nβ spin state). TROSY is a consequence of relaxation, and thus a second-order effect. A second methodological development that revolutionized solution-state NMR is the exploitation of anisotropic interactions such as Residual Dipolar Couplings (RDCs),28-29 in which proteins are partially aligned, yielding information on the absolute orientation of a bond vector with respect to the alignment tensor. RDCs are first order interactions and are visible as a modulation of the J splitting in the spectra. In the solid-state, spinning the sample off the magic angle results in only partial averaging of anisotropic interactions. In case where decoupling in both dimensions is omitted, the (Hβ/Nβ) component evolves under the influence of the difference of the DD and CSA anisotropies, whereas, the

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(Hα/Nα) component is affected by the sum of the two anisotropies. While TROSY experiments exploit differential relaxation, i.e., the second order effect of crosscorrelation, nuclear spins experience both coherent and incoherent interactions in the solid-state. In case DD and CSA interactions cancel out, off-magic angle spinning will yield spectra spectra of equally high quality. Interference of the 15

15

N CSA and the 1H-

N heteronuclear dipolar coupling was employed recently in aligned peptides,

collagen fibers and membrane proteins to study their backbone conformation.30-31 We show here that S3E experiments exploiting cross-correlation in the solid-state and yield high-resolution spectra under adverse conditions which imply less accurate settings of the spinning angle. In the solid-state, the intensity of a cross peak is affected by coherent and incoherent contributions.32 Coherent effects such as anisotropic interactions are spun out under fast magic angle spinning (60 kHz). Under these conditions, the α/β multiplet intensities in a coupled HSQC are equal as the total intensity accumulates into the center peak of the spinning sideband manifold.33 Only residues, which undergo ns-us timescale motion show a significant amount of differential broadening. Differential broadening is due to relaxation interference which is an incoherent mechanism.34-35 The HβN− component appears to be narrow due to mutual cancellation of DD and CSA interactions. The other multiplet component (HαN−) is linked to the sum of the CSA and DD and shows significant broadening. The experimental implementation of this approach is represented in Figure 1. We emphasize that the observed effect is due to a superposition of the two coherent interactions.

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Figure 1. H, N correlation spectra for a microcrystalline sample of a perdeuterated SH3 domain of α-spectrin. Experiments were recorded without heteronuclear decoupling in both evolution periods. Black and red spectra represent experiments in which the rotor axis was set exactly on the magic angle or was deliberately misadjusted, respectively. The off axis experiment was carried out at a spinning angle of approximately 55.33°. Experiments were 1 performed at 17.6 T (750 MHz for H) and at a rotor spinning frequency of 20 kHz.

For rigid residues in the solid-state, line broadening is proportional to the deviation of the spinning axis from the magic angle, and is illustrated in the simulations shown in Figure 2. Since the CSA interaction scales proportional to the magnetic field strength, a maximum of the DD-CSA cross-correlation effect is expected at a magnetic field strength of 23.5 T.20, 26 When decoupling is applied in both dimensions, the narrow component is mixed with the broad component. Therefore, a decoupled HSQC experiment is expected to perform worse in comparison to a S3E experiment, where only the narrowest component is selected. In Figure 3A, the performance of a decoupled HSQC and a S3E experiments is compared under conditions of off-magic angle spinning at a magnetic field strength of 23.5 T. The spectral quality of the HSQC is significantly compromised, whereas all resonances are observable in the S3E experiment.

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Figure 2. Simulated N spectra (coupled and decoupled HSQC, S3E) as a function of the rotor- spinning angle at an external magnetic field strength of 23.5 T. For the simulations an 1 15 isolated H- N spin pair was chosen assuming standard amide bond parameters (JNH= 95 1 Hz). To achieve decoupling, in the HSQC, an ideal 180° pulse was applied on the H channel in the middle of the evolution period. The MAS frequency was set to 60 kHz to match the 36 experimental conditions. The simulations were performed using the program Simpson.

The efficiency of the S3E approach depend on the deviation of the spinning axis from the magic angle, the local order parameter, the relative orientation between the 1H15

N DD and the

15

N CSA interaction tensors in the Principal Axis System (PAS), the

magnitude of the CSA tensor and the strength of the dipolar interaction network among the surrounding proton spins. Peaks originating from dynamic residues are in principle not affected by mis-adjustment of the spinning angle. As a consequence, these residues yield more intense signals in the off-magic angle experiments (Figure 3B). This is in particular the case for N-terminal residues E3, T4, and G5 and the Cterminal D62 of the SH3 domain. These residues are known to undergo ns-µs motion.35

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15

Figure 3. Selected Regions of (A) decoupled HSQC (left) and S3E experiment (right). H, N correlation spectra recorded at a spinning angle ΔϑRL = 0.14° off the magic angle. The 2 15 13 experiments were recorded at an external field strength of 23.5 T, for a H, N, C labelled microcrystalline sample of the α-spectrin SH3 domain. Exchangeable protons were back substituted with 50% H2O. (B) Dynamic residues such as G5 and T4 that are not detectable in the on-axis HSQC. We have shown previously that these residues undergo motion on a ns-µs 35 timescale. Due to relaxation interference in the HSQC, amides only become visible in the S3E experiments.

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In solid-state NMR probes, the rotor spinning axis is adjusted to the magic angle by turning a screw to mechanically change the orientation of the stator with respect to the direction of the magnetic field. Optimization is achieved by maximizing the number of sidebands (or increasing the intensities of the sidebands) in the spectrum of KBr powder sample. Satellite-transition-MAS (ST-MAS) on

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79

Br

NaNO3 or

Hall effect magnetic flux sensors37 can alternatively be used to properly set the rotorangle. However, ST-MAS cannot be implemented in the commercial solid state NMR probes dedicated for bio-solids applications as they are normally not tuneable to most of the quadrupolar nuclei. Also, the Hall device method is often not available for commercial probes and suffers from a difficult to control temperature sensitivity of its electrical components. To probe the accuracy and robustness of the magic angle adjustment, we compared the standard procedure employed to set the spinning angle involving KBr with a method in which the absolute rotation angle is determined. In the standard experiment, the intensity of the first spinning sideband is maximized with respect to the center band. To determine the absolute spinning angle , we employ a procedure suggested by Pileio et al.38 In brief,

13

CO signal intensities for [1,2]-13C-glycine are

measured as a function of a [τ- (π)13C-τ] echo delay (under high-power

1

H

decoupling). The signal intensities oscillate as a function of the scalar coupling J(Cα,C’), when ΔϑRL = 0° (at the magic angle). However, when ΔϑRL ≠ 0, an additional dipolar coupling term is introduced. ΔϑRL can be fit using the analytical expression provided by Pileio et al.39 To avoid systematic errors, samples were exchanged by unmounting and mounting the probe in the magnet. Also, the sample eject mode which involves a flip of the stator is not employed in these experiments. We find that the spinning angle can change up to ΔϑRL = 0.2° while at the same time the K79Br side band peak heights vary only within 5 % around an average value of 0.11 (Figure 4). Already for smaller deviations (ΔϑRL = 0.14°, Figure 3A), the decoupled HSQC performs much worse in comparison to the S3E experiment. It appears that the adjustment of the rotor-axis using K79Br powder is not quantitative and only sensitive to relatively large mis-settings. In cases where an accurate setting of the spinning angle is difficult, the S3E experiments seem to be an alternative to record high resolution 1H,15N correlations. Such situations arise for solid-state NMR probes that require a flip of the stator for sample exchange. For such a probe, accurate adjustment of the spinning angle using K79Br was not possible beyond ΔϑRL = 0.2° in our hands.

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Figure 4. (A) Estimation of ΔϑRL for subsequent optimizations of the rotor spinning axis. For a 13 quantitative determination of the rotor angle u-[ C]-glycine has been employed, following the 39 procedure described by Pileio et al. . The x-axis in the plot denotes the fitted values for ΔϑRL, whereas the standard errors from the fits are contained in the width of the normal distribution. Curves represented in different color indicate replicate experiments. (B) Intensity 79 ratio between the first spinning sideband and the center band in K Br powder. Identical colours in A and B indicate measurements performed using the same rotor angle setting (left: 79 glycine, right: K Br).

In the past, residual dipolar couplings induced by off-magic angle spinning have been used to estimate carbon, carbon distances.38-40 In deuterated samples, dipolar truncation is less of an issue, as the proton spin system is chemically dilute and enables the measurement of long-range proton-proton contacts.41-43 Off-magic angle conditions will facilitate structure determination, as dipolar couplings are not averaged to zero. This applies in particular to fast MAS experiments where 1H,1H spin diffusion is effectively suppressed. In addition, the scheme might open new perspectives for the quantification of dynamics in the solid-state as mobile and rigid regions in the sample experience differential residual anisotropies and are thus differently affected by off magic angle spinning. We have demonstrated that in the solid-state at high magnetic fields, S3E experiments are more robust with respect to off-magic angle conditions in comparison to HSQC experiments. Since the usual method for rotor angle adjustment is not very reliable, S3E experiments provide a safe alternative that suffers less from off-magic angle conditions. The method holds the potential to quantify order parameters as flexible regions of the sample are unaffected by magic angle mis-settings. In addition, the presented approach will facilitate the measurement of long range proton distances and thus contribute to the repertoire of methods for the determination of the structure of biomolecules in the solid-state.

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Acknowledgement We acknowledge fruitful discussions and experimental help from Dr. Loren Andreas and Tanguy Le Marchand. This work was performed in the framework of the SFB1035 (Project B07; German Research Foundation, DFG). We acknowledge support from the Helmholtz-Gemeinschaft and the Deutsche Forschungsgemeinschaft (Grants Re1435). We are grateful to the Center for Integrated Protein Science Munich (CIPS-M) for financial support.

Supporting Information The Supporting information contains additional details on the employed radiofrequency pulse schemes, as well as notes on the theory of off-axis spinning.

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