Chemical feasibility of the general acid/base mechanism of glmS ribozyme self‐cleavage
dc.contributor.author | Dubecký, Matúš | en_US |
dc.contributor.author | Walter, Nils G. | en_US |
dc.contributor.author | Šponer, Jiří | en_US |
dc.contributor.author | Otyepka, Michal | en_US |
dc.contributor.author | Banáš, Pavel | en_US |
dc.date.accessioned | 2015-08-05T16:47:17Z | |
dc.date.available | 2016-12-01T14:33:05Z | en |
dc.date.issued | 2015-10 | en_US |
dc.identifier.citation | Dubecký, Matúš ; Walter, Nils G.; Šponer, Jiří ; Otyepka, Michal; Banáš, Pavel (2015). "Chemical feasibility of the general acid/base mechanism of glmS ribozyme selfâ cleavage." Biopolymers 103(10): 550-562. | en_US |
dc.identifier.issn | 0006-3525 | en_US |
dc.identifier.issn | 1097-0282 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/112240 | |
dc.description.abstract | In numerous Gram‐positive bacteria, the glmS ribozyme or catalytic riboswitch regulates the expression of glucosamine‐6‐phosphate (GlcN6P) synthase via site‐specific cleavage of its sugar‐phosphate backbone in response to GlcN6P ligand binding. Biochemical data have suggested a crucial catalytic role for an active site guanine (G40 in Thermoanaerobacter tengcongensis, G33 in Bacillus anthracis). We used hybrid quantum chemical/molecular mechanical (QM/MM) calculations to probe the mechanism where G40 is deprotonated and acts as a general base. The calculations suggest that the deprotonated guanine G40− is sufficiently reactive to overcome the thermodynamic penalty arising from its rare protonation state, and thus is able to activate the A‐1(2′‐OH) group toward nucleophilic attack on the adjacent backbone. Furthermore, deprotonation of A‐1(2′‐OH) and nucleophilic attack are predicted to occur as separate steps, where activation of A‐1(2′‐OH) precedes nucleophilic attack. Conversely, the transition state associated with the rate‐determining step corresponds to concurrent nucleophilic attack and protonation of the G1(O5′) leaving group by the ammonium moiety of the GlcN6P cofactor. Overall, our calculations help to explain the crucial roles of G40 (as a general base) and GlcN6P (as a general acid) during glmS ribozyme self‐cleavage. In addition, we show that the QM/MM description of the glmS ribozyme self‐cleavage reaction is significantly more sensitive to the size of the QM region and the quality of the QM‐MM coupling than that of other small ribozymes. © 2015 Wiley Periodicals, Inc. Biopolymers 103: 550–562, 2015. | en_US |
dc.publisher | University of California | en_US |
dc.publisher | Wiley Periodicals, Inc. | en_US |
dc.subject.other | ribozyme | en_US |
dc.subject.other | RNA catalysis | en_US |
dc.subject.other | QM/MM | en_US |
dc.subject.other | riboswitch | en_US |
dc.subject.other | glmS | en_US |
dc.title | Chemical feasibility of the general acid/base mechanism of glmS ribozyme self‐cleavage | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Materials Science and Engineering | en_US |
dc.subject.hlbsecondlevel | Chemical Engineering | en_US |
dc.subject.hlbsecondlevel | Chemistry | en_US |
dc.subject.hlbtoplevel | Engineering | en_US |
dc.subject.hlbtoplevel | Science | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/112240/1/bip22657.pdf | |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/112240/2/bip22657-sup-0004-suppinfo04.pdf | |
dc.identifier.doi | 10.1002/bip.22657 | en_US |
dc.identifier.source | Biopolymers | en_US |
dc.identifier.citedreference | Aqvist, J. J Phys Chem‐Us 1990, 94, 8021 – 8024. | en_US |
dc.identifier.citedreference | Hampel, K. J.; Tinsley, M. M. Biochemistry‐Us 2006, 45, 7861 – 7871. | en_US |
dc.identifier.citedreference | Mlynsky, V.; Kuhrova, P.; Zgarbova, M.; Jurecka, P.; Walter, N. G.; Otyepka, M.; Sponer, J.; Banas, P. J Phys Chem B, 2015, 119, 4220 – 4229. | en_US |
dc.identifier.citedreference | Cheatham, T. E.; Case, D. A. Biopolymers 2013, 99, 969 – 977. | en_US |
dc.identifier.citedreference | Sponer, J.; Banas, P.; Jurecka, P.; Zgarbova, M.; Kuhrova, P.; Havrila, M.; Krepl, M.; Stadlbauer, P.; Otyepka, M. J Phys Chem Lett 2014, 5, 1771 – 1782. | en_US |
dc.identifier.citedreference | Case, D. A.; Babin, V.; Berryman, J. T.; Betz, R. M.; Cai, Q.; Cerutti, D. S.; Cheatham III, T. E.; Darden, T. A.; Duke, R. E.; Gohlke, H.; Goetz, A. W.; Gusarov, S.; Homeyer, N.; Janowski, P.; Kaus, J.; Kolossváry, I.; Kovalenko, A.; Lee, T. S.; LeGrand, S.; Luchko, T.; Luo, R.; Madej, B.; Merz, K. M.; Paesani, F.; Roe, D. R.; Roitberg, A.; Sagui, C.; Salomon‐Ferrer, R.; Seabra, G.; Simmerling, C. L.; Smith, W.; Swails, J.; Walker, R. C.; Wang, J.; Wolf, R. M.; Wu, X.; Kollman, P. A. AMBER 12; University of California: San Francisco, 2014.. | en_US |
dc.identifier.citedreference | Salomon‐Ferrer, R.; Gotz, A. W.; Poole, D.; Le Grand, S.; Walker, R. C. J Chem Theory Comput 2013, 9, 3878 – 3888. | en_US |
dc.identifier.citedreference | Bayly, C. I.; Cieplak, P.; Cornell, W. D.; Kollman, P. A. J Phys Chem‐Us 1993, 97, 10269 – 10280. | en_US |
dc.identifier.citedreference | Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. J Am Chem Soc 1996, 118, 2309 – 2309. | en_US |
dc.identifier.citedreference | Perez, A.; Marchan, I.; Svozil, D.; Sponer, J.; Cheatham, T. E.; Laughton, C. A.; Orozco, M. Biophys J 2007, 92, 3817 – 3829. | en_US |
dc.identifier.citedreference | Zgarbova, M.; Otyepka, M.; Sponer, J.; Mladek, A.; Banas, P.; Cheatham, T. E.; Jurecka, P. J Chem Theory Comput 2011, 7, 2886 – 2902. | en_US |
dc.identifier.citedreference | Banas, P.; Hollas, D.; Zgarbova, M.; Jurecka, P.; Orozco, M.; Cheatham, T. E.; Sponer, J.; Otyepka, M. J Chem Theory Comput 2010, 6, 3836 – 3849. | en_US |
dc.identifier.citedreference | Joung, I. S.; Cheatham, T. E. J Phys Chem B 2008, 112, 9020 – 9041. | en_US |
dc.identifier.citedreference | Fedor, M. J. Annu Rev Biophys 2009, 38, 271 – 299. | en_US |
dc.identifier.citedreference | Gresh, N.; Sponer, J. E.; Spackova, N.; Leszczynski, J.; Sponer, J. J Phys Chem B 2003, 107, 8669 – 8681. | en_US |
dc.identifier.citedreference | Banas, P.; Jurecka, P.; Walter, N. G.; Sponer, J.; Otyepka, M. Methods 2009, 49, 202 – 216. | en_US |
dc.identifier.citedreference | Ditzler, M. A.; Otyepka, M.; Sponer, J.; Walter, N. G. Acc Chem Res 2010, 43, 40 – 47. | en_US |
dc.identifier.citedreference | Svensson, M.; Humbel, S.; Froese, R. D. J.; Matsubara, T.; Sieber, S.; Morokuma, K. J Phys Chem‐Us 1996, 100, 19357 – 19363. | en_US |
dc.identifier.citedreference | Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery Jr., J. A.; Peralta, J. E.; Ogliaro, F.; Bearpark, M. J.; Heyd, J.; Brothers, E. N.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A. P.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, N. J.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, Ö.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian09; Gaussian: Wallingford, CT, 2009. | en_US |
dc.identifier.citedreference | Salahub, D. R.; de la Lande, A.; Goursot, A.; Zhang, R.; Zhang, Y. Struct Bond 2013, 150, 1 – 64. | en_US |
dc.identifier.citedreference | Lynch, B. J.; Truhlar, D. G. J Phys Chem A 2001, 105, 2936 – 2941. | en_US |
dc.identifier.citedreference | Lynch, B. J.; Fast, P. L.; Harris, M.; Truhlar, D. G. J Phys Chem A 2000, 104, 4811 – 4815. | en_US |
dc.identifier.citedreference | Mlynsky, V.; Banas, P.; Sponer, J.; van der Kamp, M. W.; Mulholland, A. J.; Otyepka, M. J Chem Theory Comput 2014, 10, 1608 – 1622. | en_US |
dc.identifier.citedreference | Zirbel, C. L.; Sponer, J. E.; Sponer, J.; Stombaugh, J.; Leontis, N. B. Nucleic Acids Res 2009, 37, 4898 – 4918. | en_US |
dc.identifier.citedreference | Banas, P.; Rulisek, L.; Hanosova, V.; Svozil, D.; Walter, N. G.; Sponer, J.; Otyepka, M. J Phys Chem B 2008, 112, 11177 – 11187. | en_US |
dc.identifier.citedreference | Mlynsky, V.; Walter, N. G.; Sponer, J.; Otyepka, M.; Banas, P. Phys Chem Chem Phys 2015, 17, 670 – 679. | en_US |
dc.identifier.citedreference | Hu, L. H.; Soderhjelm, P.; Ryde, U. J Chem Theory Comput 2011, 7, 761 – 777. | en_US |
dc.identifier.citedreference | Vreven, T.; Byun, K. S.; Komaromi, I.; Dapprich, S.; Montgomery, J. A.; Morokuma, K.; Frisch, M. J. J Chem Theory Comput 2006, 2, 815 – 826. | en_US |
dc.identifier.citedreference | Zhang, S.; Ganguly, A.; Goyal, P.; Bingaman, J. L.; Bevilacqua, P. C.; Hammes‐Schiffer, S. J Am Chem Soc 2015, 137, 784 – 798. | en_US |
dc.identifier.citedreference | Barrick, J. E.; Breaker, R. R. Genome Biol 2007, 8: R239. | en_US |
dc.identifier.citedreference | Batey, R. T.; Gilbert, S. D.; Montange, R. K. Nature 2004, 432, 411 – 415. | en_US |
dc.identifier.citedreference | Coppins, R. L.; Hall, K. B.; Groisman, E. A. Curr Opin Microbiol 2007, 10, 176 – 181. | en_US |
dc.identifier.citedreference | Corbino, K. A.; Barrick, J. E.; Lim, J.; Welz, R.; Tucker, B. J.; Puskarz, I.; Mandal, M.; Rudnick, N. D.; Breaker, R. R. Genome Biol 2005, 6. | en_US |
dc.identifier.citedreference | Grundy, F. J.; Henkin, T. M. Crit Rev Biochem Mol 2006, 41, 329 – 338. | en_US |
dc.identifier.citedreference | Henkin, T. M. Gene Dev 2008, 22, 3383 – 3390. | en_US |
dc.identifier.citedreference | Mandal, M.; Boese, B.; Barrick, J. E.; Winkler, W. C.; Breaker, R. R. Cell 2003, 113, 577 – 586. | en_US |
dc.identifier.citedreference | Tucker, B. J.; Breaker, R. R. Curr Opin Struct Biol 2005, 15, 342 – 348. | en_US |
dc.identifier.citedreference | Winkler, W. C. Curr Opin Chem Biol 2005, 9, 594 – 602. | en_US |
dc.identifier.citedreference | Winkler, W. C.; Breaker, R. R. Annu Rev Microbiol 2005, 59, 487 – 517. | en_US |
dc.identifier.citedreference | Deigan, K. E.; Ferre‐D'Amare, A. R. Acc Chem Res 2011, 44, 1329 – 1338. | en_US |
dc.identifier.citedreference | Blount, K. F.; Breaker, R. R. Nat Biotechnol 2006, 24, 1558 – 1564. | en_US |
dc.identifier.citedreference | Barrick, J. E.; Corbino, K. A.; Winkler, W. C.; Nahvi, A.; Mandal, M.; Collins, J.; Lee, M.; Roth, A.; Sudarsan, N.; Jona, I.; Wickiser, J. K.; Breaker, R. R. Proc Natl Acad Sci USA 2004, 101, 6421 – 6426. | en_US |
dc.identifier.citedreference | Winkler, W. C.; Nahvi, A.; Roth, A.; Collins, J. A.; Breaker, R. R. Nature 2004, 428, 281 – 286. | en_US |
dc.identifier.citedreference | Milewski, S. Bba‐Protein Struct M 2002, 1597, 173 – 192. | en_US |
dc.identifier.citedreference | Tinsley, R. A.; Furchak, J. R. W.; Walter, N. G. RNA 2007, 13, 468 – 477. | en_US |
dc.identifier.citedreference | McCarthy, T. J.; Plog, M. A.; Floy, S. A.; Jansen, J. A.; Soukup, J. K.; Soukup, G. A. Chem Biol 2005, 12, 1221 – 1226. | en_US |
dc.identifier.citedreference | Collins, J. A.; Irnov, I.; Baker, S.; Winkler, W. C. Gene Dev 2007, 21, 3356 – 3368. | en_US |
dc.identifier.citedreference | Lau, M. W. L.; Ferre‐D'Amare, A. R. Nat Chem Biol 2013, 9, 805 ‐+. | en_US |
dc.identifier.citedreference | Bevilacqua, P. C.; Yajima, R. Curr Opin Chem Biol 2006, 10, 455 – 464. | en_US |
dc.identifier.citedreference | Lilley, D. M. J. Trends Biochem Sci 2003, 28, 495 – 501. | en_US |
dc.identifier.citedreference | Roth, A.; Nahvi, A.; Lee, M.; Jona, I.; Breaker, R. R. RNA 2006, 12, 607 – 619. | en_US |
dc.identifier.citedreference | Gong, B.; Klein, D. J.; Ferre‐D'Amare, A. R.; Carey, P. R. J Am Chem Soc 2011, 133, 14188 – 14191. | en_US |
dc.identifier.citedreference | Viladoms, J.; Fedor, M. J. J Am Chem Soc 2012, 134, 19043 – 19049. | en_US |
dc.identifier.citedreference | Davis, J. H.; Dunican, B. F.; Strobel, S. A. Biochemistry‐Us 2011, 50, 7236 – 7242. | en_US |
dc.identifier.citedreference | Xin, Y.; Hamelberg, D. RNA 2010, 16, 2455 – 2463. | en_US |
dc.identifier.citedreference | Viladoms, J.; Scott, L. G.; Fedor, M. J. J Am Chem Soc 2011, 133, 18388 – 18396. | en_US |
dc.identifier.citedreference | Brooks, K. M.; Hampel, K. J. Biochemistry‐Us 2011, 50, 2424 – 2433. | en_US |
dc.identifier.citedreference | Klein, D. J.; Been, M. D.; Ferre‐D'Amare, A. R. J Am Chem Soc 2007, 129, 14858 – 14859. | en_US |
dc.identifier.citedreference | Klein, D. J.; Wilkinson, S. R.; Been, M. D.; Ferre‐D'Amare, A. R. J Mol Biol 2007, 373, 178 – 189. | en_US |
dc.identifier.citedreference | Klein, D. J.; Ferre‐D'Amare, A. R. Science 2006, 313, 1752 – 1756. | en_US |
dc.identifier.citedreference | Cochrane, J. C.; Lipchock, S. V.; Strobel, S. A. Chem Biol 2007, 14, 97 – 105. | en_US |
dc.identifier.citedreference | Cochrane, J. C.; Strobel, S. A. Acc Chem Res 2008, 41, 1027 – 1035. | en_US |
dc.identifier.citedreference | Banas, P.; Walter, N. G.; Sponer, J.; Otyepka, M. J Phys Chem B 2010, 114, 8701 – 8712. | en_US |
dc.identifier.citedreference | Sripathi, K. N.; Tay, W. W.; Banas, P.; Otyepka, M.; Poner, J. S.; Walter, N. S. RNA 2014, 20, 1112 – 1128. | en_US |
dc.identifier.citedreference | Mlynsky, V.; Banas, P.; Hollas, D.; Reblova, K.; Walter, N. G.; Sponer, J.; Otyepka, M. J Phys Chem B 2010, 114, 6642 – 6652. | en_US |
dc.identifier.citedreference | Mlynsky, V.; Banas, P.; Walter, N. G.; Sponer, J.; Otyepka, M. J Phys Chem B 2011, 115, 13911 – 13924. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
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