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http://dx.doi.org/10.6564/JKMRS.2022.26.1.001

Refinement of protein NMR structures using atomistic force field and implicit solvent model: Comparison of the accuracies of NMR structures with Rosetta refinement  

Jee, Jun-Goo (Research Institute of Pharmaceutical Sciences, College of Pharmacy, Kyungpook National University)
Publication Information
Journal of the Korean Magnetic Resonance Society / v.26, no.1, 2022 , pp. 1-9 More about this Journal
Abstract
There are two distinct approaches to improving the quality of protein NMR structures during refinement: all-atom force fields and accumulated knowledge-assisted methods that include Rosetta. Mao et al. reported that, for 40 proteins, Rosetta increased the accuracies of their NMR-determined structures with respect to the X-ray crystal structures (Mao et al., J. Am. Chem. Soc. 136, 1893 (2014)). In this study, we calculated 32 structures of those studied by Mao et al. using all-atom force field and implicit solvent model, and we compared the results with those obtained from Rosetta. For a single protein, using only the experimental NOE-derived distances and backbone torsion angle restraints, 20 of the lowest energy structures were extracted as an ensemble from 100 generated structures. Restrained simulated annealing by molecular dynamics simulation searched conformational spaces with a total time step of 1-ns. The use of GPU-accelerated AMBER code allowed the calculations to be completed in hours using a single GPU computer-even for proteins larger than 20 kDa. Remarkably, statistical analyses indicated that the structures determined in this way showed overall higher accuracies to their X-ray structures compared to those refined by Rosetta (p-value < 0.01). Our data demonstrate the capability of sophisticated atomistic force fields in refining NMR structures, particularly when they are coupled with the latest GPU-based calculations. The straightforwardness of the protocol allows its use to be extended to all NMR structures.
Keywords
NMR structure refinement; all-atom force field; generalized-Born implicit solvent;
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1 P. Guntert, C. Mumenthaler and K. Wuthrich, J. Mol. Biol., 273, 283 (1997)   DOI
2 A. W. Gotz, M. J. Williamson, D. Xu, D. Poole, S. Le Grand and R. C. Walker, J. Chem. Theory Comput., 8, 1542 (2012)   DOI
3 J. Chen and C. L. Brooks, 3rd, Proteins, 67, 922 (2007)   DOI
4 T. J. Ragan, R. H. Fogh, R. Tejero, W. Vranken, G. T. Montelione, A. Rosato and G. W. Vuister, J. Biomol. NMR, 62, 413 (2015)   DOI
5 A. T. Brunger, P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J. S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson and G. L. Warren, Acta Crystallogr. D Biol. Crystallogr., 54, 905 (1998)
6 N. Sekiyama, J.-G. Jee, S. Isogai, K. Akagi, T. H. Huang, M. Ariyoshi, H. Tochio and M. Shirakawa, J. Biomol. NMR, 52, 339 (2012)   DOI
7 J.-G. Jee, Bull. Korean Chem. Soc., 31, 2717 (2010)   DOI
8 A. Ohno, J.-G. Jee, K. Fujiwara, T. Tenno, N. Goda, H. Tochio, H. Kobayashi, H. Hiroaki and M. Shirakawa, Structure, 13, 521 (2005)   DOI
9 R. Das and D. Baker, Annu. Rev. Biochem., 77, 363 (2008)   DOI
10 H. Park, F. DiMaio, and D. Baker, Structure, 23, 1123 (2015)   DOI
11 V. Mirjalili and M. Feig, J. Chem. Theory Comput., 9, 1294 (2013)   DOI
12 S. Lindert, J. Meiler and J. A. McCammon, J. Chem. Theory Comput., 9, 3843 (2013)   DOI
13 R. Salomon-Ferrer, A. W. Gotz, D. Poole, S. Le Grand, R. C. Walker, J Chem Theory Comput, 9, 3878 (2013)   DOI
14 Y. Shen, O. Lange, F. Delaglio, P. Rossi, J. M. Aramini, G. Liu, A. Eletsky, Y. Wu, K. K. Singarapu, A. Lemak, A. Ignatchenko, C. H. Arrowsmith, T. Szyperski, G. T. Montelione, D. Baker and A. Bax, Proc. Natl. Acad. Sci. U. S. A., 105, 4685 (2008)   DOI
15 S. Raman, O. F. Lange, P. Rossi, M. Tyka, X. Wang, J. Aramini, G. Liu, T. A. Ramelot, A. Eletsky, T. Szyperski, M. A. Kennedy, J. Prestegard, G. T. Montelione, D. Baker, Science, 327, 1014 (2010)   DOI
16 C. D. Schwieters, J. J. Kuszewski, N. Tjandra and G. M. Clore, J. Magn. Reson., 160, 65 (2003)   DOI
17 A. Rosato, J. M. Aramini, C. Arrowsmith, A. Bagaria, D. Baker, A. Cavalli, J. F. Doreleijers, A. Eletsky, A. Giachetti, P. Guerry, A. Gutmanas, P. Guntert, Y. He, T. Herrmann, Y. J. Huang, V. Jaravine, H. R. Jonker, M. A. Kennedy, O. F. Lange, G. Liu, T. E. Malliavin, R. Mani, B. Mao, G. T. Montelione, M. Nilges, P. Rossi, G. van der Schot, H. Schwalbe, T. A. Szyperski, M. Vendruscolo, R. Vernon, W. F. Vranken, S. Vries, G. W. Vuister, B. Wu, Y. Yang and A. M. Bonvin, Structure, 20, 227 (2012)   DOI
18 T. Ikeya, J.-G. Jee, Y. Shigemitsu, J. Hamatsu, M. Mishima, Y. Ito, M. Kainosho and P. Guntert, J. Biomol. NMR, 50, 137 (2011)   DOI
19 K. Tunyasuvunakool, J. Adler, Z. Wu, T. Green, M. Zielinski, A. Zidek, A. Bridgland, A. Cowie, C. Meyer, A. Laydon, S. Velankar, G. J. Kleywegt, A. Bateman, R. Evans, A. Pritzel, M. Figurnov, O. Ronneberger, R. Bates, S. A. A. Kohl, A. Potapenko, A. J. Ballard, B. Romera-Paredes, S. Nikolov, R. Jain, E. Clancy, D. Reiman, S. Petersen, A. W. Senior, K. Kavukcuoglu, E. Birney, P. Kohli, J. Jumper and D. Hassabis, Nature, 596, 590 (2021)   DOI
20 J. Jumper, R. Evans, A. Pritzel, T. Green, M. Figurnov, O. Ronneberger, K. Tunyasuvunakool, R. Bates, A. Zidek, A. Potapenko, A. Bridgland, C. Meyer, S. A. A. Kohl, A. J. Ballard, A. Cowie, B. Romera-Paredes, S. Nikolov, R. Jain, J. Adler, T. Back, S. Petersen, D. Reiman, E. Clancy, M. Zielinski, M. Steinegger, M. Pacholska, T. Berghammer, S. Bodenstein, D. Silver, O. Vinyals, A. W. Senior, K. Kavukcuoglu, P. Kohli and D. Hassabis, Nature, 596, 583 (2021)   DOI
21 K. Wuthrich, NMR of Proteins and Nucleic Acids. Wiley, New York (1986)
22 J.-G. Jee, Bull. Korean Chem. Soc., 35, 1944 (2014)   DOI
23 A. Zemla, C. Venclovas, J. Moult and K. Fidelis, Proteins, Suppl 5, 13 (2001)
24 J.-G. Jee, T. Mizuno, K. Kamada, H. Tochio, Y. Chiba, K. Yanagi, G. Yasuda, H. Hiroaki, F. Hanaoka and M. Shirakawa, J. Biol. Chem., 285, 15931 (2010)   DOI
25 J.-G. Jee and H.-C. Ahn, Bull Korean Chem. Soc., 30, 1139 (2009)   DOI
26 K. Fujiwara, T. Tenno, K. Sugasawa, J.-G. Jee, I. Ohki, C. Kojima, H. Tochio, H. Hiroaki, F. Hanaoka and M. Shirakawa, J. Biol. Chem., 279, 4760 (2004)   DOI
27 K. Joo, I. Joung, J. Lee, J. Lee, W. Lee, B. Brooks, S. J. Lee and J. Lee, Proteins, 83, 2251 (2015)   DOI
28 Y. Shen and A. Bax, Nat. Methods, 12, 747 (2015)   DOI
29 O. F. Lange, P. Rossi, N. G. Sgourakis, Y. Song, H. W. Lee, J. M. Aramini, A. Ertekin, R. Xiao, T. B. Acton, G. T. Montelione and D. Baker, Proc. Natl. Acad. Sci. U. S. A., 109, 10873 (2012)   DOI
30 B. Mao, R. Tejero, D. Baker, G. T. and Montelione, J. Am. Chem. Soc., 136, 1893 (2014)   DOI
31 S. Lindert, J. A. and McCammon, J. Chem. Theory Comput., 11, 1337 (2015)   DOI
32 V. Mirjalili, K. Noyes and M. Feig, Proteins, 82 Suppl. 2, 196 (2014)   DOI
33 J. Xu and Y. Zhang, Bioinformatics, 26, 889 (2010)   DOI
34 D. A. Case, T. A. Darden, T. E. Cheatham, I. Simmerling, C.L., J. Wang, R. E. Duke, R. Luo, R. C. Walker, W. Zhang, K. M. Merz, B. Roberts, S. Hayik, A. Roitberg, G. Seabra, J. Swails, A. W. Goetz, I. Kolossvary, K. F. Wong, F. Paesani, J. Vanicek, R. M. Wolf, J. Liu, X. Wu, S. R. Brozell, T. Steinbrecher, H. Gohlke, Q. Cai, X. Ye, J. Wang, M.-J. Hsieh, G. Cui, D. R. Roe, D. H. Mathews, M. G. Seetin, R. Salomon-Ferrer, C. Sagui, V. Babin, T. Luchko, S. Gusarov, A. Kovalenko and P. A. Kollman, University of California, San Francisco (2012)
35 S. Le Grand, A. W. Gotz and R. C. Walker, Computer Physics Communications, 184, 374 (2013)   DOI
36 D. K. Kirchner and P. Guntert, BMC Bioinformatics, 12, 170 (2011)   DOI
37 Y. Zhang and J. Skolnick, Proteins, 57, 702 (2004)   DOI
38 R. J. Read and G. Chavali, Proteins, 69 Suppl 8, 27 (2007)   DOI
39 A. Zemla, C. Venclovas, J. Moult and K. Fidelis, Proteins, Suppl 3, 22 (1999)
40 A. Bhattacharya, R. Tejero and G. T. Montelione, Proteins, 66, 778 (2007)   DOI
41 G. T. Montelione, M. Nilges, A. Bax, P. Guntert, T. Herrmann, J. S. Richardson, C. D. Schwieters, W. F. Vranken, G. W. Vuister, D. S. Wishart, H. M. Berman, G. J. Kleywegt and J. L. Markley, Structure, 21, 1563 (2013)   DOI
42 J.-G. Jee, J. Kor. Mag. Res. Soc., 18, 24 (2014)   DOI
43 J.-G. Jee, J. Kor. Mag. Res. Soc., 18, 69 (2014)   DOI