The GlcN6P cofactor plays multiple catalytic roles in the glmS ribozyme

Nature Chemical Biology

Volumn 13, Issue 4, 2017, Pages 439-445

  Bingaman, Jamie L ^a   Zhang, Sixue ^b   Stevens, David R ^b   Yennawar, Neela H ^a   Hammes Schiffer, Sharon ^b   Bevilacqua, Philip C ^a,c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APORIBOZYME; GLMS PROTEIN; GLUCOSAMINE; GLUCOSAMINE 6 PHOSPHATE; HOLOENZYME; MAGNESIUM ION; NUCLEIC ACID BASE; NUCLEOPHILE; RIBOZYME; UNCLASSIFIED DRUG; GLUCOSAMINE 6-PHOSPHATE; GLUCOSE 6 PHOSPHATE;

ARTICLE; CALCULATION; CATALYSIS; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME STABILITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTON TRANSPORT; STATIC ELECTRICITY; STEREOSPECIFICITY; ANALOGS AND DERIVATIVES; BIOCATALYSIS; CHEMISTRY; METABOLISM; MOLECULAR DOCKING; MOLECULAR MODEL;

BIOCATALYSIS; GLUCOSAMINE; GLUCOSE-6-PHOSPHATE; MODELS, MOLECULAR; MOLECULAR DOCKING SIMULATION; RNA, CATALYTIC;

EID: 85012261811     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2300     Document Type: Article

References (39)

1. Li, Y. & Breaker, R.R. Kinetics of RNA degradation by specific base catalysis of transesterification involving the 2'-hydroxyl group. J. Am. Chem. Soc. 121, 5364-5372 (1999).
2. Soukup, G.A. & Breaker, R.R. Relationship between internucleotide linkage geometry and the stability of RNA. RNA 5, 1308-1325 (1999).
3. Emilsson, G.M., Nakamura, S., Roth, A. & Breaker, R.R. Ribozyme speed limits. RNA 9, 907-918 (2003).
4. Fersht, A. Structure and Mechanism in Protein Science (W.H. Freeman, 1999).
5. Cech, T.R., Zaug, A.J. & Grabowski, P.J. In vitro splicing of the ribosomal RNA precursor of Tetrahymena: involvement of a guanosine nucleotide in the excision of the intervening sequence. Cell 27, 487-496 (1981).
6. Viladoms, J., Scott, L.G. & Fedor, M.J. An active-site guanine participates in glmS ribozyme catalysis in its protonated state. J. Am. Chem. Soc. 133, 18388-18396 (2011).
7. Soukup, J.K. The structural and functional uniqueness of the glmS ribozyme. Prog. Mol. Biol. Transl. Sci. 120, 173-193 (2013).
8. Zhang, S. et al. Role of the active site guanine in the glmS ribozyme self-cleavage mechanism: quantum mechanical/molecular mechanical free energy simulations. J. Am. Chem. Soc. 137, 784-798 (2015).
9. Klein, D.J. & Ferre-DAmare, A.R. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313, 1752-1756 (2006).
10. Cochrane, J.C., Lipchock, S.V. & Strobel, S.A. Structural investigation of the glmS ribozyme bound to its catalytic cofactor. Chem. Biol. 14, 97-105 (2007).
11. Viladoms, J. & Fedor, M.J. The glmS ribozyme cofactor is a general acid-base catalyst. J. Am. Chem. Soc. 134, 19043-19049 (2012).
12. Klein, D.J., Wilkinson, S.R., Been, M.D. & Ferre-DAmare, A.R. Requirement of helix P2.2 and nucleotide G1 for positioning the cleavage site and cofactor of the glmS ribozyme. J. Mol. Biol. 373, 178-189 (2007).
13. Uhlenbeck, O.C. Keeping RNA happy. RNA 1, 4-6 (1995).
14. Chadalavada, D.M., Senchak, S.E. & Bevilacqua, P.C. The folding pathway of the genomic hepatitis delta virus ribozyme is dominated by slow folding of the pseudoknots. J. Mol. Biol. 317, 559-575 (2002).
15. Brown, T.S., Chadalavada, D.M. & Bevilacqua, P.C. Design of a highly reactive HDV ribozyme sequence uncovers facilitation of RNA folding by alternative pairings and physiological ionic strength. J. Mol. Biol. 341, 695-712 (2004).
16. Roth, A., Nahvi, A., Lee, M., Jona, I. & Breaker, R.R. Characteristics of the glmS ribozyme suggest only structural roles for divalent metal ions. RNA 12, 607-619 (2006).
17. Frederiksen, J.K. & Piccirilli, J.A. Identification of catalytic metal ion ligands in ribozymes. Methods 49, 148-166 (2009).
18. Klawuhn, K., Jansen, J.A., Souchek, J., Soukup, G.A. & Soukup, J.K. Analysis of metal ion dependence in glmS ribozyme self-cleavage and coenzyme binding. ChemBioChem 11, 2567-2571 (2010).
19. Brooks, K.M. & Hampel, K.J. Rapid steps in the glmS ribozyme catalytic pathway: cation and ligand requirements. Biochemistry 50, 2424-2433 (2011).
20. Murray, J.B., Seyhan, A.A., Walter, N.G., Burke, J.M. & Scott, W.G. The hammerhead, hairpin and VS ribozymes are catalytically proficient in monovalent cations alone. Chem. Biol. 5, 587-595 (1998).
21. Perrotta, A.T. & Been, M.D. HDV ribozyme activity in monovalent cations. Biochemistry 45, 11357-11365 (2006).
22. Frederiksen, J.K., Li, N.-S., Das, R., Herschlag, D. & Piccirilli, J.A. Metal-ion rescue revisited: biochemical detection of site-bound metal ions important for RNA folding. RNA 18, 1123-1141 (2012).
23. Hampel, K.J. & Tinsley, M.M. Evidence for preorganization of the glmS ribozyme ligand binding pocket. Biochemistry 45, 7861-7871 (2006).
24. Thaplyal, P., Ganguly, A., Hammes-Schiffer, S. & Bevilacqua, P.C. Inverse thio effects in the hepatitis delta virus ribozyme reveal that the reaction pathway is controlled by metal ion charge density. Biochemistry 54, 2160-2175 (2015).
25. DeRose, V.J. Metal ion binding to catalytic RNA molecules. Curr. Opin. Struct. Biol. 13, 317-324 (2003).
26. Johnson-Buck, A.E., McDowell, S.E. & Walter, N.G. Metal ions: supporting actors in the playbook of small ribozymes. Met. Ions Life Sci. 9, 175-196 (2011).
27. Bevilacqua, P.C. & Yajima, R. Nucleobase catalysis in ribozyme mechanism. Curr. Opin. Chem. Biol. 10, 455-464 (2006).
28. Cochrane, J.C., Lipchock, S.V., Smith, K.D. & Strobel, S.A. Structural and chemical basis for glucosamine 6-phosphate binding and activation of the glmS ribozyme. Biochemistry 48, 3239-3246 (2009).
29. Brooks, K.M. & Hampel, K.J. A rate-limiting conformational step in the catalytic pathway of the glmS ribozyme. Biochemistry 48, 5669-5678 (2009).
30. Scott, E.C. & Uhlenbeck, O.C. A re-investigation of the thio effect at the hammerhead cleavage site. Nucleic Acids Res. 27, 479-484 (1999).
31. Yoshida, A., Sun, S. & Piccirilli, J.A. A new metal ion interaction in the Tetrahymena ribozyme reaction revealed by double sulfur substitution. Nat. Struct. Biol. 6, 318-321 (1999).
32. Ward, W.L. & Derose, V.J. Ground-state coordination of a catalytic metal to the scissile phosphate of a tertiary-stabilized Hammerhead ribozyme. RNA 18, 16-23 (2012).
33. Jencks, W.P. Catalysis in Chemistry and Enzymology (Dover, 1969).
34. Zhang, S. et al. Assessing the potential effects of active site Mg2+ ions in the glmS ribozyme-cofactor complex. J. Phys. Chem. Lett. 7, 3984-3988 (2016).
35. Lau, M.W.L. & Ferre-DAmare, A.R. An in vitro evolved glmS ribozyme has the wild-type fold but loses coenzyme dependence. Nat. Chem. Biol. 9, 805-810 (2013).
36. Chinnapen, D.J.-F. & Sen, D. A deoxyribozyme that harnesses light to repair thymine dimers in DNA. Proc. Natl. Acad. Sci. USA 101, 65-69 (2004).
37. Cernak, P. & Sen, D. A thiamin-utilizing ribozyme decarboxylates a pyruvate-like substrate. Nat. Chem. 5, 971-977 (2013).
38. Poon, L.C.H. et al. Guanine-rich RNAs and DNAs that bind heme robustly catalyze oxygen transfer reactions. J. Am. Chem. Soc. 133, 1877-1884 (2011).
39. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).