Conformational investigation of peptides using solid-state NMR spectroscopy-A study of polymorphism of β-turn peptides containing diprolines.
Journal
Chemical biology & drug design
ISSN: 1747-0285
Titre abrégé: Chem Biol Drug Des
Pays: England
ID NLM: 101262549
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
27
09
2019
revised:
02
11
2019
accepted:
16
11
2019
pubmed:
23
11
2019
medline:
19
5
2021
entrez:
23
11
2019
Statut:
ppublish
Résumé
The construction of complex protein folds relies on the precise conversion of a linear polypeptide chain into a compact 3-dimensional structure. In this context, study of isolated secondary structural modules containing short stretches of amino acids assumes significance. Additionally, peptides, both natural and synthetic, play a major role as potential drugs. With a view to understand the local conformations adopted by peptides in the solid state, we propose a multinuclear NMR approach utilizing spectra of nuclei in their natural isotopic abundance. Various solid-state NMR experiments have been utilized for assignment of the spectra. Additionally, the gauge-including projector augmented-wave (GIPAW) calculations were used to confirm the assignments. Particularly, the utility of the double-quantum-single-quantum correlation experiments is highlighted for the purpose of assignment and for inferring the conformation across the peptide bond. The methodology is illustrated for the case of designed peptides containing diproline residues occurring at the β-turns for identifying their cis-trans conformational polymorphism. The proposed method promises to be of use in the study of conformations of small- to medium-sized peptides such as antimicrobial peptides and in the study of polymorphism leading to applications in drug development protocols.
Substances chimiques
Peptides
0
Proline
9DLQ4CIU6V
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
394-407Informations de copyright
© 2019 John Wiley & Sons A/S.
Références
Agarwal, V., Penzel, S., Szekely, K., Cadalbert, R., Testori, E., Oss, A., … Meier, B. H. (2014). De novo 3D structure determination from sub-milligram protein samples by solid-state 100 kHz MAS NMR spectroscopy. Angewandte Chemie International Edition, 53(45), 12253-12256. https://doi.org/10.1002/anie.201405730
Andreotti, A. H. (2003). Native state proline isomerization: An intrinsic molecular switch. Biochemistry, 42(32), 9515-9524. https://doi.org/10.1021/bi0350710
Brown, S. P., Lesage, A., Elena, B., & Emsley, L. (2004). Probing proton−proton proximities in the solid state: High-resolution two-dimensional 1H−H double-quantum CRAMPS NMR spectroscopy. Journal of the American Chemical Society, 126(41), 13230-13231. https://doi.org/10.1021/ja045461p
Burum, D. P., Grant, D. M., & Harris, R. K. (1996). Encyclopedia of nuclear magnetic resonance (pp. 2323-2329). New York, NY: John Wiley & Sons.
Castellani, F., van Rossum, B., Diehl, A., Schubert, M., Rehbein, K., & Oschkinat, H. (2002). Structure of a protein determined by solid-state magic-angle-spinning NMR spectroscopy. Nature, 420(6911), 99-102. https://doi.org/10.1038/nature01070
Chatterjee, B., Saha, I., Raghothama, S., Aravinda, S., Rai, R., Shamala, N., & Balaram, P. (2008). Designed peptides with homochiral and heterochiral diproline templates as conformational constraints. Chemistry-A European Journal, 14(20), 6192-6204. https://doi.org/10.1002/chem.200702029
De Paëpe, G., Lewandowski, J. R., Loquet, A., Böckmann, A., & Griffin, R. G. (2008). Proton assisted recoupling and protein structure determination. The Journal of Chemical Physics, 129(24), 245101. https://doi.org/10.1063/1.3036928
Deschamps, M., Fayon, F., Cadars, S., Rollet, A.-L., & Massiot, D. (2011). 1H and 19F ultra-fast MAS double-quantum single-quantum NMR correlation experiments using three-spin terms of the dipolar homonuclear Hamiltonian. Physical Chemistry Chemical Physics, 13(17), 8024-8030. https://doi.org/10.1039/C0CP02202K
Elena, B., Lesage, A., Steuernagel, S., Böckmann, A., & Emsley, L. (2005). Proton to carbon-13 INEPT in solid-state NMR spectroscopy. Journal of the American Chemical Society, 127(49), 17296-17302. https://doi.org/10.1021/ja054411x
Feng, X., Lee, Y. K., Sandstrom, D., Eden, M., Maisel, H., Sebald, A., & Levitt, M. H. (1996). Direct determination of a molecular torsional angle by solid-state NMR. Chemical Physics Letters, 257(3-4), 314-320. https://doi.org/10.1016/0009-2614(96)00558-1
Giannozzi, P., Baroni, S., Bonini, N., Calandra, M., Car, R., Cavazzoni, C., … Wentzcovitch, R. M. (2009). QUANTUM ESPRESSO: A modular and open-source software project for quantum simulations of materials. Journal of Physics: Condensed Matter, 21(39), 395502. https://doi.org/10.1088/0953-8984/21/39/395502
Guichou, J.-F., Patiny, L., & Mutter, M. (2002). Pseudo-prolines (ΨPro): Direct insertion of ΨPro systems into cysteine containing peptides. Tetrahedron Letters, 43(24), 4389-4390. https://doi.org/10.1016/S0040-4039(02)00755-4
Gunasekaran, K., Ramakrishnan, C., & Balaram, P. (1997). Beta-hairpins in proteins revisited: Lessons for de novo design. Protein Engineering, 10(10), 1131-1141. https://doi.org/10.1093/protein/10.10.1131
Ishii, Y., Terao, T., & Kainosho, M. (1996). Relayed anisotropy correlation NMR: Determination of dihedral angles in solids. Chemical Physics Letters, 256(1-2), 133-140. https://doi.org/10.1016/0009-2614(96)00426-5
Judge, P. J., & Watts, A. (2011). Recent contributions from solid-state NMR to the understanding of membrane protein structure and function. Current Opinion in Chemical Biology, 15(5), 690-695. https://doi.org/10.1016/j.cbpa.2011.07.021
Kantharaju, R. S., Raghavender, U. S., Aravinda, S., Shamala, N., & Balaram, P. (2009). Conformations of heterochiral and homochiral proline-pseudoproline segments in peptides: Context dependent cis-trans peptide bond isomerization. Biopolymers, 92(5), 405-416. https://doi.org/10.1002/bip.21207
Keller, M., Sager, C., Dumy, P., Schutkowski, M., Fischer, G. S., & Mutter, M. (1998). Enhancing the proline effect: Pseudo-prolines for tailoring cis/trans isomerization. Journal of the American Chemical Society, 120(12), 2714-2720. https://doi.org/10.1021/ja973966s
Knight, M. J., Felli, I. C., Pierattelli, R., Emsley, L., & Pintacuda, G. (2013). Magic angle spinning NMR of paramagnetic proteins. Accounts of Chemical Research, 46(9), 2108-2116. https://doi.org/10.1021/ar300349y
Lange, A., Luca, S., & Baldus, M. (2002). Structural constraints from proton-mediated rare-spin correlation spectroscopy in rotating solids. Journal of the American Chemical Society, 124(33), 9704-9705. https://doi.org/10.1021/ja026691b
Leppert, J., Ohlenschläger, O., Görlach, M., & Ramachandran, R. (2004). Adiabatic TOBSY in rotating solids. Journal of Biomolecular NMR, 29(2), 167-173. https://doi.org/10.1023/B:JNMR.0000019248.48726.ff
Lesage, A., Emsley, L., Penin, F., & Böckmann, A. (2006). Investigation of dipolar-mediated water- protein interactions in microcrystalline Crh by solid-state NMR spectroscopy. Journal of the American Chemical Society, 128(25), 8246-8255. https://doi.org/10.1021/ja060866q
Lesage, A., Sakellariou, D., Steuernagel, S., & Emsley, L. (1998). Carbon-proton chemical shift correlation in solid-state NMR by through- bond multiple-quantum spectroscopy. Journal of the American Chemical Society, 120(50), 13194-13201. https://doi.org/10.1021/ja983048+
Lesage, A., Steuernagel, S., & Emsley, L. (1998). Carbon-13 spectral editing in solid-state NMR using heteronuclear scalar couplings. Journal of the American Chemical Society, 120(28), 7095-7100. https://doi.org/10.1021/ja981019t
Monkhorst, H. J., & Pack, J. D. (1976). Special points for Brillouin-zone integrations. Physical Review B, 13(12), 5188. https://doi.org/10.1103/PhysRevB.13.5188
Morcombe, C. R., Gaponenko, V., Byrd, R. A., & Zilm, K. W. (2004). Diluting abundant spins by isotope edited radio frequency field assisted diffusion. Journal of the American Chemical Society, 126(23), 7196-7197. https://doi.org/10.1021/ja047919t
Naito, A., Nishimura, K., Kimura, S., Tuzi, S., Aida, M., Yasuoka, N., & Saitô, H. (1996). Determination of the three-dimensional structure of a new crystalline form of N-Acetyl-Pro-Gly-Phe as revealed by 13C REDOR, X-ray diffraction, and molecular dynamics calculation. The Journal of Physical Chemistry, 100(36), 14995-15004. https://doi.org/10.1021/jp960179t
Nishiyama, Y. (2016). Fast magic-angle sample spinning solid-state NMR at 60-100 kHz for natural abundance samples. Solid State Nuclear Magnetic Resonance, 78, 24-36. https://doi.org/10.1016/j.ssnmr.2016.06.002
Nishiyama, Y., Endo, Y., Nemoto, T., Utsumi, H., Yamauchi, K., Hioka, K., & Asakura, T. (2011). Very fast magic angle spinning 1H-14N 2D solid-state NMR: Sub-micro-liter sample data collection in a few minutes. Journal of Magnetic Resonance, 208(1), 44-48. https://doi.org/10.1016/j.jmr.2010.10.001
Opella, S. J., & Frey, M. H. (1979). Selection of nonprotonated carbon resonances in solid-state nuclear magnetic resonance. Journal of the American Chemical Society, 101(19), 5854-5856. https://doi.org/10.1021/ja00513a079
Pack, J. D., & Monkhorst, H. J. (1977). “ Special points for Brillouin-zone integrations”-a reply. Physical Review B, 16(4), 1748. https://doi.org/10.1103/PhysRevB.16.1748
Paëpe, G. D., Lewandowski, J. R., Loquet, A., Eddy, M., Megy, S., Böckmann, A., & Griffin, R. G. (2011). Heteronuclear proton assisted recoupling. The Journal of Chemical Physics, 134(9), 95101. https://doi.org/10.1063/1.3541251
Pal, D., & Chakrabarti, P. (1999). Cis peptide bonds in proteins: Residues involved, their conformations, interactions and locations1. Journal of Molecular Biology, 294(1), 271-288. https://doi.org/10.1006/jmbi.1999.3217
Patel, H. R., Pithadia, A. S., Brender, J. R., Fierke, C. A., & Ramamoorthy, A. (2014). In search of aggregation pathways of IAPP and other amyloidogenic proteins: Finding answers through NMR spectroscopy. The Journal of Physical Chemistry Letters, 5(11), 1864-1870. https://doi.org/10.1021/jz5001775
Pickard, C. J., & Mauri, F. (2001). All-electron magnetic response with pseudopotentials: NMR chemical shifts. Physical Review B, 63(24), 245101. https://doi.org/10.1103/PhysRevB.63.245101
Quinn, C. M., & Polenova, T. (2017). Structural biology of supramolecular assemblies by magic-angle spinning NMR spectroscopy. Quarterly Reviews of Biophysics, 50, 1-44. https://doi.org/10.1017/S0033583516000159
Rai, R., Aravinda, S., Kanagarajadurai, K., Raghothama, S., Shamala, N., & Balaram, P. (2006). Diproline templates as folding nuclei in designed peptides. Conformational analysis of synthetic peptide helices containing amino terminal Pro-Pro segments. Journal of the American Chemical Society, 128(24), 7916-7928. https://doi.org/10.1021/ja060674v
Reddy, Y. J., Agarwal, V., Lesage, A., Emsley, L., & Ramanathan, K. V. (2014). Heteronuclear proton double quantum-carbon single quantum scalar correlation in solids. Journal of Magnetic Resonance, 245, 31-37. https://doi.org/10.1016/j.jmr.2014.05.004
Retel, J. S., Nieuwkoop, A. J., Hiller, M., Higman, V. A., Barbet-Massin, E., Stanek, J., … Oschkinat, H. (2017). Structure of outer membrane protein G in lipid bilayers. Nature Communications, 8(1), 2073. https://doi.org/10.1038/s41467-017-02228-2
Sakellariou, D., Lesage, A., & Emsley, L. (2001). Spectral editing in solid-state NMR using scalar multiple quantum filters. Journal of Magnetic Resonance, 151(1), 40-47. https://doi.org/10.1006/jmre.2001.2338
Sarkar, P., Reichman, C., Saleh, T., Birge, R. B., & Kalodimos, C. G. (2007). Proline cis-trans isomerization controls autoinhibition of a signaling protein. Molecular Cell, 25(3), 413-426. https://doi.org/10.1016/j.molcel.2007.01.004
Schmidt-Rohr, K. (1996). Torsion angle determination in solid 13C-labeled amino acids and peptides by separated-local-field double-quantum NMR. Journal of the American Chemical Society, 118(32), 7601-7603. https://doi.org/10.1021/ja9605782
Schubert, M., Labudde, D., Oschkinat, H., & Schmieder, P. (2002). A software tool for the prediction of Xaa-Pro peptide bond conformations in proteins based on 13C chemical shift statistics. Journal of Biomolecular NMR, 24(2), 149-154. https://doi.org/10.1023/A:1020997118364
Sibanda, B. L., & Thornton, J. M. (1985). β-Hairpin families in globular proteins. Nature, 316(6024), 170-174. https://doi.org/10.1038/316170a0
Suter, D., & Ernst, R. R. (1985). Spin diffusion in resolved solid-state NMR spectra. Physical Review B, 32(9), 5608-5627. https://doi.org/10.1103/PhysRevB.32.5608
Takegoshi, K., Nakamura, S., & Terao, T. (2001). 13C-1H dipolar-assisted rotational resonance in magic-angle spinning NMR. Chemical Physics Letters, 344(5), 631-637. https://doi.org/10.1016/S0009-2614(01)00791-6
Tang, M., Comellas, G., & Rienstra, C. M. (2013). Advanced solid-state NMR approaches for structure determination of membrane proteins and amyloid fibrils. Accounts of Chemical Research, 46(9), 2080-2088. https://doi.org/10.1021/ar4000168
van Beek, J. D., & Meier, B. H. (2006). A DOQSY approach for the elucidation of torsion angle distributions in biopolymers: Application to silk. Journal of Magnetic Resonance, 178(1), 106-120. https://doi.org/10.1016/j.jmr.2005.09.004
Venkatachalam, C. M. (1968). Stereochemical criteria for polypeptides and proteins. V. Conformation of a system of three linked peptide units. Biopolymers: Original Research on Biomolecules, 6(10), 1425-1436. https://doi.org/10.1002/bip.1968.360061006
Venkatraman, J., Shankaramma, S. C., & Balaram, P. (2001). Design of folded peptides. Chemical Reviews, 101(10), 3131-3152. https://doi.org/10.1021/cr000053z
Webber, A. L., Elena, B., Griffin, J. M., Yates, J. R., Pham, T. N., Mauri, F., … Brown, S. P., 2010). Complete 1H resonance assignment of β-maltose from 1H-1H DQ-SQ CRAMPS and 1H (DQ-DUMBO)-13C SQ refocused INEPT 2D solid-state NMR spectra and first principles GIPAW calculations. Physical Chemistry Chemical Physics, 12(26), 6970-6983. https://doi.org/10.1039/c001290dothers
Wöhr, T., Wahl, F., Nefzi, A., Rohwedder, B., Sato, T., Sun, X., & Mutter, M. (1996). Pseudo-prolines as a solubilizing, structure-disrupting protection technique in peptide synthesis. Journal of the American Chemical Society, 118(39), 9218-9227. https://doi.org/10.1021/ja961509q
Xiao, Y., Ma, B., McElheny, D., Parthasarathy, S., Long, F., Hoshi, M., … Ishii, Y. (2015). Aβ (1-42) fibril structure illuminates self-recognition and replication of amyloid in Alzheimer's disease. Nature Structural & Molecular Biology, 22(6), 499-505. https://doi.org/10.1038/nsmb.2991
Yarava, J. R., Sonti, R., Kantharaju, K., Raghothama, S., & Ramanathan, K. V. (2017). Solid-state NMR at natural isotopic abundance for the determination of conformational polymorphism-the case of designed β-turn peptides containing di-prolines. Chemical Communications, 53, 1317-1320. https://doi.org/10.1039/c6cc08676d
Yates, J. R., Pickard, C. J., & Mauri, F. (2007). Calculation of NMR chemical shifts for extended systems using ultrasoft pseudopotentials. Physical Review B, 76(2), 24401. https://doi.org/10.1103/PhysRevB.76.024401
Zech, S. G., Wand, A. J., & McDermott, A. E. (2005). Protein structure determination by high-resolution solid-state NMR spectroscopy: Application to microcrystalline ubiquitin. Journal of the American Chemical Society, 127(24), 8618-8626. https://doi.org/10.1021/ja0503128
Zhang, R., He, X., Fu, W., Chen, T., Sun, P., Li, B., & Ding, D. (2011). Efficient identification of different types of carbons in organic solids by 2D solid-state NMR spectroscopy. The Journal of Physical Chemistry A, 115(42), 11665-11670. https://doi.org/10.1021/jp2071293
Zhou, D. H., Shea, J. J., Nieuwkoop, A. J., Franks, W. T., Wylie, B. J., Mullen, C., … Rienstra, C. M. (2007). Solid-state protein-structure determination with proton-detected triple-resonance 3D magic-angle-spinning NMR spectroscopy. Angewandte Chemie International Edition, 46(44), 8380-8383. https://doi.org/10.1002/anie.200702905