Proton-detected polarization optimized experiments (POE) using ultrafast magic angle spinning solid-state NMR: Multi-acquisition of membrane protein spectra

Journal of Magnetic Resonance - Tập 310 - Trang 106664 - 2020
T. Gopinath1, Gianluigi Veglia2,3
1Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, MN 55455, United States
2Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, Minneapolis, MN 55455, United States
3Department of Chemistry, University of Minnesota, Minneapolis, MN 55455, United States

Tài liệu tham khảo

Hu, 2010, Mechanisms of proton conduction and gating in influenza M2 proton channels from solid-state NMR, Science, 330, 505, 10.1126/science.1191714 Quinn, 2018, Dynamic regulation of HIV-1 capsid interaction with the restriction factor TRIM5alpha identified by magic-angle spinning NMR and molecular dynamics simulations, Proc. Natl. Acad. Sci. USA, 115, 11519, 10.1073/pnas.1800796115 Zhou, 2013, Influences of membrane mimetic environments on membrane protein structures, Annu. Rev. Biophys., 42, 361, 10.1146/annurev-biophys-083012-130326 Baldus, 2018, GPCR: Lock and key become flexible, Nat. Chem. Biol., 14, 201, 10.1038/nchembio.2567 Fitzpatrick, 2013, Atomic structure and hierarchical assembly of a cross-beta amyloid fibril, Proc. Natl. Acad. Sci. USA, 110, 5468, 10.1073/pnas.1219476110 Watt, 2014, Recent advances in solid-state nuclear magnetic resonance techniques to quantify biomolecular dynamics, Anal. Chem., 86, 58, 10.1021/ac403956k Qiang, 2017, Structural variation in amyloid-beta fibrils from Alzheimer's disease clinical subtypes, Nature, 541, 217, 10.1038/nature20814 Park, 2012, Structure of the chemokine receptor CXCR1 in phospholipid bilayers, Nature, 491, 779, 10.1038/nature11580 Gopinath, 2017, Probing the conformationally excited states of membrane proteins via 1H-detected MAS solid-state NMR spectroscopy, J. Phys. Chem. B, 121, 4456, 10.1021/acs.jpcb.7b03268 Gustavsson, 2013, Allosteric regulation of SERCA by phosphorylation-mediated conformational shift of phospholamban, Proc. Natl. Acad. Sci. USA, 110, 17338, 10.1073/pnas.1303006110 Ha, 2012, Tuning the structural coupling between the transmembrane and cytoplasmic domains of phospholamban to control sarcoplasmic reticulum Ca(2+)-ATPase (SERCA) function, J. Muscle Res. Cell. Motil., 33, 485, 10.1007/s10974-012-9319-4 Fusco, 2014, Direct observation of the three regions in alpha-synuclein that determine its membrane-bound behaviour, Nat. Commun., 5, 3827, 10.1038/ncomms4827 Castellani, 2002, Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy, Nature, 420, 98, 10.1038/nature01070 Wang, 2016, Structure and dynamics of extracellular loops in human aquaporin-1 from solid-state NMR and molecular dynamics, J. Phys. Chem. B, 120, 9887, 10.1021/acs.jpcb.6b06731 Wasmer, 2008, Amyloid fibrils of the HET-s(218–289) prion form a beta solenoid with a triangular hydrophobic core, Science, 319, 1523, 10.1126/science.1151839 Zhang, 2010, Resonance assignment and three-dimensional structure determination of a human alpha-defensin, HNP-1, by solid-state NMR, J. Mol. Biol., 397, 408, 10.1016/j.jmb.2010.01.030 Franks, 2007, Four-dimensional heteronuclear correlation experiments for chemical shift assignment of solid proteins, J Biomol. NMR, 39, 107, 10.1007/s10858-007-9179-1 J. Cavanagh, W. J. Fairbrother, A. G. Palmer, M. Rance, N. J. Skelton, Protein NMR Spectroscopy: Principles and Practice, second edi. Protein Nmr Spectroscopy: Principles and Practice, 2007, 1–888. Paulson, 2003, Sensitive high resolution inverse detection NMR spectroscopy of proteins in the solid state, J. Am. Chem. Soc., 125, 15831, 10.1021/ja037315+ Chevelkov, 2015, Perspectives for sensitivity enhancement in proton-detected solid-state NMR of highly deuterated proteins by preserving water magnetization, J. Biomol. NMR, 61, 151, 10.1007/s10858-015-9902-2 Zhou, 2007, Proton-detected solid-state NMR spectroscopy of fully protonated proteins at 40 kHz magic-angle spinning, J. Am. Chem. Soc., 129, 11791, 10.1021/ja073462m Zhou, 2007, Solid-state protein-structure determination with proton-detected triple-resonance 3D magic-angle-spinning NMR spectroscopy, Angew. Chem. Int. Ed. Engl., 46, 8380, 10.1002/anie.200702905 Loquet, 2018, 3D structure determination of amyloid fibrils using solid-state NMR spectroscopy, Methods, 138–139, 26, 10.1016/j.ymeth.2018.03.014 Fricke, 2017, Backbone assignment of perdeuterated proteins by solid-state NMR using proton detection and ultrafast magic-angle spinning, Nat. Protoc., 12, 764, 10.1038/nprot.2016.190 Zhang, 2017, Proton-based ultrafast magic angle spinning solid-state NMR spectroscopy, ACC Chem. Res., 50, 1105, 10.1021/acs.accounts.7b00082 Wang, 2015, Nano-mole scale side-chain signal assignment by 1H-detected protein solid-state NMR by ultra-fast magic-angle spinning and stereo-array isotope labeling, PLoS ONE, 10, e0122714, 10.1371/journal.pone.0122714 Chipot, 2018, Perturbations of native membrane protein structure in alkyl phosphocholine detergents: a critical assessment of NMR and biophysical studies, Chem. Rev., 118, 3559, 10.1021/acs.chemrev.7b00570 Gopinath, 2017, (1)H-detected MAS solid-state NMR experiments enable the simultaneous mapping of rigid and dynamic domains of membrane proteins, J. Magn. Reson., 285, 101, 10.1016/j.jmr.2017.09.003 Gopinath, 2012, Dual acquisition magic-angle spinning solid-state NMR-spectroscopy: simultaneous acquisition of multidimensional spectra of biomacromolecules, Angew. Chem. Int. Ed. Engl., 51, 2731, 10.1002/anie.201108132 Gopinath, 2012, 3D DUMAS: simultaneous acquisition of three-dimensional magic angle spinning solid-state NMR experiments of proteins, J. Magn. Reson., 220, 79, 10.1016/j.jmr.2012.04.006 Gopinath, 2013, Orphan spin operators enable the acquisition of multiple 2D and 3D magic angle spinning solid-state NMR spectra, J. Chem. Phys., 138, 184201, 10.1063/1.4803126 Gopinath, 2016, Orphan spin polarization: a catalyst for high-throughput solid-state NMR spectroscopy of proteins, Annu. Rep. NMR Spectrosc., 89, 103, 10.1016/bs.arnmr.2016.04.003 Gopinath, 2016, Multiple acquisitions via sequential transfer of orphan spin polarization (MAeSTOSO): How far can we push residual spin polarization in solid-state NMR?, J. Magn. Reson., 267, 1, 10.1016/j.jmr.2016.03.001 Gopinath, 2018, Experimental aspects of polarization optimized experiments (POE) for magic angle spinning solid-state NMR of microcrystalline and membrane-bound proteins, Methods Mol.Biol., 1688, 37, 10.1007/978-1-4939-7386-6_2 Mote, 2013, Determination of structural topology of a membrane protein in lipid bilayers using polarization optimized experiments (POE) for static and MAS solid state NMR spectroscopy, J. Biomol. NMR, 57, 91, 10.1007/s10858-013-9766-2 Nelson, 2018, Effects of the Arg9Cys and Arg25Cys mutations on phospholamban's conformational equilibrium in membrane bilayers, Biochim. Biophys. Acta, 1860, 1335, 10.1016/j.bbamem.2018.02.030 Kupce, 2017, NOAH: NMR supersequences for small molecule analysis and structure elucidation, Angew. Chem. Int. Ed. Engl., 56, 11779, 10.1002/anie.201705506 Gopinath, 2015, Multiple acquisition of magic angle spinning solid-state NMR experiments using one receiver: application to microcrystalline and membrane protein preparations, J. Magn. Reson., 253, 143, 10.1016/j.jmr.2015.01.001 Nielsen, 2012, Simultaneous acquisition of PAR and PAIN spectra, J. Biomol. NMR, 52, 283, 10.1007/s10858-012-9616-7 Stringer, 2005, Reduction of RF-induced sample heating with a scroll coil resonator structure for solid-state NMR probes, J. Magn. Reson., 173, 40, 10.1016/j.jmr.2004.11.015 Gor'kov, 2007, Using low-E resonators to reduce RF heating in biological samples for static solid-state NMR up to 900 MHz, J. Magn. Reson., 185, 77, 10.1016/j.jmr.2006.11.008 Das, 2016, Simultaneous cross polarization to (13)C and (15)N with (1)H detection at 60kHz MAS solid-state NMR, J. Magn. Reson., 262, 20, 10.1016/j.jmr.2015.12.004 Bellstedt, 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, 325, 10.1007/s10858-012-9680-z Sharma, 2016, A suite of pulse sequences based on multiple sequential acquisitions at one and two radiofrequency channels for solid-state magic-angle spinning NMR studies of proteins, J. Biomol. NMR, 65, 127, 10.1007/s10858-016-0043-z Zhang, 2016, Hybridizing cross-polarization with NOE or refocused-INEPT enhances the sensitivity of MAS NMR spectroscopy, J. Magn. Reson., 266, 59, 10.1016/j.jmr.2016.03.006 Gopinath, 2018, Probing membrane protein ground and conformationally excited states using dipolar- and J-coupling mediated MAS solid state NMR experiments, Methods, 148, 115, 10.1016/j.ymeth.2018.07.003 Gopinath, 2019, Hybridization of TEDOR and NCX MAS solid-state NMR experiments for simultaneous acquisition of heteronuclear correlation spectra and distance measurements, J. Biomol. NMR, 73, 141, 10.1007/s10858-019-00237-5 Fung, 2000, An improved broadband decoupling sequence for liquid crystals and solids, J. Magn. Reson., 142, 97, 10.1006/jmre.1999.1896 Shaka, 1983, An improved sequence for broadband decoupling: WALTZ-16, J. Magn. Reson., 52, 335 Hartmann, 1962, Nuclear double resonance in the rotating frame, Phys. Rev., 128, 2042, 10.1103/PhysRev.128.2042 Zhou, 2008, High-performance solvent suppression for proton detected solid-state NMR, J. Magn. Reson., 192, 167, 10.1016/j.jmr.2008.01.012 Baldus, 1998, Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems, Mol. Phys., 95, 1197, 10.1080/00268979809483251 Bennett, 1995, Heteronuclear decoupling in rotating solids, J. Chem. Phys., 103, 6951, 10.1063/1.470372 Delaglio, 1995, NMRPipe: A multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR, 6, 277, 10.1007/BF00197809 Xue, 2017, Limits of resolution and sensitivity of proton detected MAS solid-state NMR experiments at 111 kHz in deuterated and protonated Proteins, Sci. Rep., 7, 7444, 10.1038/s41598-017-07253-1 Wang, 2015, Nano-mole scale sequential signal assignment by (1)H-detected protein solid-state NMR, Chem. Commun. (Camb), 51, 15055, 10.1039/C5CC04618A Lalli, 2017, Proton-based structural analysis of a heptahelical transmembrane protein in lipid bilayers, J. Am. Chem. Soc., 139, 13006, 10.1021/jacs.7b05269 Zhang, 2015, A novel high-resolution and sensitivity-enhanced three-dimensional solid-state NMR experiment under ultrafast magic angle spinning conditions, Sci. Rep., 5, 11810, 10.1038/srep11810 Wittmann, 2016, Accelerating proton spin diffusion in perdeuterated proteins at 100 kHz MAS, J. Biomol. NMR, 66, 233, 10.1007/s10858-016-0071-8 Zhang, 2017, 3D double-quantum/double-quantum exchange spectroscopy of protons under 100 kHz magic angle spinning, J. Phys. Chem. B, 121, 5944, 10.1021/acs.jpcb.7b03480 Saalwachter, 2011, BaBa-xy16: robust and broadband homonuclear DQ recoupling for applications in rigid and soft solids up to the highest MAS frequencies, J. Magn. Reson., 212, 204, 10.1016/j.jmr.2011.07.001 Demers, 2015, Recovery of bulk proton magnetization and sensitivity enhancement in ultrafast magic-angle spinning solid-state NMR, J. Phys. Chem. B, 119, 2908, 10.1021/jp511987y Pines, 1973, Proton-enhanced NMR of dilute spins in solids, J. Chem. Phys, 59, 569, 10.1063/1.1680061 Andreas, 2016, Structure of fully protonated proteins by proton-detected magic-angle spinning NMR, Proc. Natl. Acad. Sci. USA, 113, 9187, 10.1073/pnas.1602248113 Maly, 2008, Dynamic nuclear polarization at high magnetic fields, J. Chem. Phys., 128, 052211, 10.1063/1.2833582 Wickramasinghe, 2009, Nanomole-scale protein solid-state NMR by breaking intrinsic 1HT1 boundaries, Nat. Methods, 6, 215, 10.1038/nmeth.1300 Suiter, 2014, Sensitivity gains, linearity, and spectral reproducibility in nonuniformly sampled multidimensional MAS NMR spectra of high dynamic range, J. Biomol. NMR, 59, 57, 10.1007/s10858-014-9824-4 Lecoq, 2019, 100 kHz MAS proton-detected NMR spectroscopy of hepatitis B virus capsids, Front. Mol. Biosci., 6, 58, 10.3389/fmolb.2019.00058 Penzel, 2019, Spinning faster: protein NMR at MAS frequencies up to 126 kHz, J. Biomol. NMR, 73, 19, 10.1007/s10858-018-0219-9 Agarwal, 2014, De novo 3D structure determination from sub-milligram protein samples by solid-state 100 kHz MAS NMR spectroscopy, Angew. Chem. Int. Ed. Engl., 53, 12253, 10.1002/anie.201405730 Banigan, 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, 7138, 10.1021/jp303269m Gallo, 2019, A suite of solid-state NMR experiments to utilize orphaned magnetization for assignment of proteins using parallel high and low gamma detection, J. Magn. Reson., 305, 219, 10.1016/j.jmr.2019.07.006 Viegas, 2016, UTOPIA NMR: activating unexploited magnetization using interleaved low-gamma detection, J. Biomol. NMR, 64, 9, 10.1007/s10858-015-0008-7