Bacterial toxin RelE: A highly efficient ribonuclease with exquisite substrate specificity using atypical catalytic residues

Biochemistry

Volumn 52, Issue 48, 2013, Pages 8633-8642

  Griffin, Meghan A ^a   Davis, Jared H ^a   Strobel, Scott A ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID COMPOSITIONS; AMINO ACID STARVATIONS; CATALYTIC RESIDUE; CHARGE STABILIZATION; KINETIC ANALYSIS; MOLECULAR MECHANISM; STRUCTURAL INFORMATION; SUBSTRATE SPECIFICITY;

AMINO ACIDS; RATE CONSTANTS; RNA;

MACROMOLECULES;

BACTERIAL TOXIN; BACTERIAL TOXIN RELB; BACTERIAL TOXIN RELE; MESSENGER RNA; RIBONUCLEASE; RNA 16S; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; ARTICLE; CATALYSIS; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION CONSTANT; ENZYME KINETICS; ENZYME SPECIFICITY; KINETICS; KWASHIORKOR; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON TRANSPORT; REACTION ANALYSIS; REACTION TIME; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; RNA CLEAVAGE; SITE DIRECTED MUTAGENESIS; TURNOVER TIME;

EID: 84889257673     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401325c     Document Type: Article

References (58)

1. Yamaguchi, Y., Park, J. H., and Inouye, M. (2011) Toxin-antitoxin systems in bacteria and archaea Annu. Rev. Genet. 45, 61-79
2. Wang, X. and Wood, T. K. (2011) Toxin-antitoxin systems influence biofilm and persister cell formation and the general stress response Appl. Environ. Microbiol. 77, 5577-5583
3. Gerdes, K. and Maisonneuve, E. (2012) Bacterial persistence and toxin-antitoxin loci Annu. Rev. Microbiol. 66, 103-123
4. Gerdes, K. (2000) Toxin-antitoxin modules may regulate synthesis of macromolecules during nutritional stress J. Bacteriol. 182, 561-572 (Pubitemid 30053984)
5. Christensen, S. K., Mikkelsen, M., Pedersen, K., and Gerdes, K. (2001) RelE, a global inhibitor of translation, is activated during nutritional stress Proc. Natl. Acad. Sci. U.S.A. 98, 14328-14333 (Pubitemid 33121391)
6. Overgaard, M., Borch, J., and Gerdes, K. (2009) RelB and RelE of Escherichia coli form a tight complex that represses transcription via the ribbon-helix-helix motif in RelB J. Mol. Biol. 394, 183-196
7. Yamaguchi, Y. and Inouye, M. (2011) Regulation of growth and death in Escherichia coli by toxin-antitoxin systems Nat. Rev. Microbiol. 9, 779-790
8. Guglielmini, J. and Van Melderen, L. (2011) Bacterial toxin-antitoxin systems: Translation inhibitors everywhere Mobile Genetic Elements 1, 283-290
9. Gotfredsen, M. and Gerdes, K. (1998) The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family Mol. Microbiol. 29, 1065-1076 (Pubitemid 28389446)
10. Pedersen, K., Zavialov, A. V., Pavlov, M. Y., Elf, J., Gerdes, K., and Ehrenberg, M. (2003) The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site Cell 112, 131-140 (Pubitemid 36106425)
11. Cherny, I., Overgaard, M., Borch, J., Bram, Y., Gerdes, K., and Gazit, E. (2007) Structural and thermodynamic characterization of the Escherichia coli RelBE toxin-antitoxin system: Indication for a functional role of differential stability Biochemistry 46, 12152-12163 (Pubitemid 350022370)
12. Neubauer, C., Gao, Y. G., Andersen, K. R., Dunham, C. M., Kelley, A. C., Hentschel, J., Gerdes, K., Ramakrishnan, V., and Brodersen, D. E. (2009) The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE Cell 139, 1084-1095
13. Goeders, N., Dreze, P. L., and Van Melderen, L. (2013) Relaxed cleavage specificity within the RelE toxin family J. Bacteriol. 195, 2541-2549
14. Hurley, J. M., Cruz, J. W., Ouyang, M., and Woychik, N. A. (2011) Bacterial toxin RelE mediates frequent codon-independent mRNA cleavage from the 5′ end of coding regions in vivo J. Biol. Chem. 286, 14770-14778
15. Christensen, S. K. and Gerdes, K. (2003) RelE toxins from bacteria and Archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA Mol. Microbiol. 48, 1389-1400 (Pubitemid 36718231)
16. Pedersen, K., Christensen, S. K., and Gerdes, K. (2002) Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins Mol. Microbiol. 45, 501-510 (Pubitemid 34779839)
17. Takagi, H., Kakuta, Y., Okada, T., Yao, M., Tanaka, I., and Kimura, M. (2005) Crystal structure of archaeal toxin-antitoxin RelE-RelB complex with implications for toxin activity and antitoxin effects Nat. Struct. Mol. Biol. 12, 327-331 (Pubitemid 43093087)
18. Yang, W. (2011) Nucleases: Diversity of structure, function and mechanism Q. Rev. Biophys. 44, 1-93
19. Li, G. Y., Zhang, Y., Inouye, M., and Ikura, M. (2009) Inhibitory mechanism of Escherichia coli RelE-RelB toxin-antitoxin module involves a helix displacement near an mRNA interferase active site J. Biol. Chem. 284, 14628-14636
20. Kamada, K. and Hanaoka, F. (2005) Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin Mol. Cell 19, 497-509 (Pubitemid 41140007)
21. Zegers, I., Haikal, A. F., Palmer, R., and Wyns, L. (1994) Crystal structure of RNase T1 with 3′-guanylic acid and guanosine J. Biol. Chem. 269, 127-133 (Pubitemid 24026633)
22. Bauerova-Hlinkova, V., Dvorsky, R., Perecko, D., Povazanec, F., and Sevcik, J. (2009) Structure of RNase Sa2 complexes with mononucleotides: New aspects of catalytic reaction and substrate recognition FEBS J. 276, 4156-4168
23. Mossakowska, D. E., Nyberg, K., and Fersht, A. R. (1989) Kinetic Characterization of the Recombinant Ribonuclease from Bacillus amyloliquefaciens (Barnase) and Investigation of Key Residues in Catalysis by Site-Directed Mutagenesis Biochemistry 28, 3843-3850 (Pubitemid 19125432)
24. Meiering, E. M., Serrano, L., and Fersht, A. R. (1992) Effect of Active-Site Residues in Barnase on Activity and Stability J. Mol. Biol. 225, 585-589
25. Yakovlev, G. I., Mitkevich, V. A., Shaw, K. L., Trevino, S., Newsom, S., Pace, C. N., and Makarov, A. A. (2003) Contribution of active site residues to the activity and thermal stability of ribonuclease Sa Protein Sci. 12, 2367-2373 (Pubitemid 37163371)
26. Shapiro, R., Fox, E. A., and Riordan, J. F. (1989) Role of lysines in human angiogenin: Chemical modification and site-directed mutagenesis Biochemistry 28, 1726-1732 (Pubitemid 19072045)
27. Rodnina, M. V., Fricke, R., Kuhn, L., and Wintermeyer, W. (1995) Codon-Dependent Conformational Change of Elongation-Factor Tu Preceding Gtp Hydrolysis on the Ribosome EMBO J. 14, 2613-2619
28. Ryder, S. P. and Strobel, S. A. (1999) Nucleotide analog interference mapping Methods 18, 38-50 (Pubitemid 29440535)
29. Shanahan, C. A., Gaffney, B. L., Jones, R. A., and Strobel, S. A. (2011) Differential analogue binding by two classes of c-di-GMP riboswitches J. Am. Chem. Soc. 133, 15578-15592
30. Frederiksen, J. K. and Piccirilli, J. A. (2009) Separation of RNA phosphorothioate oligonucleotides by HPLC Methods Enzymol. 468, 289-309
31. Herschlag, D., Piccirilli, J. A., and Cech, T. R. (1991) Ribozyme-catalyzed and nonenzymatic reactions of phosphate diesters: Rate effects upon substitution of sulfur for a nonbridging phosphoryl oxygen atom Biochemistry 30, 4844-4854
32. Herschlag, D. (1994) Ribonuclease Revisited: Catalysis Via the Classical General Acid-Base Mechanism or a Triester-like Mechanism J. Am. Chem. Soc. 116, 11631-11635
33. Loverix, S., Winqvist, A., Stromberg, R., and Steyaert, J. (2000) Mechanism of RNase T-1: Concerted triester-like phosphoryl transfer via a catalytic three-centered hydrogen bond Chem. Biol. 7, 651-658
34. Stivers, J. T. and Nagarajan, R. (2006) Probing enzyme phosphoester interactions by combining mutagenesis and chemical modification of phosphate ester oxygens Chem. Rev. 106, 3443-3467 (Pubitemid 44376944)
35. Kamal, M. Z., Mohammad, T. A. S., Krishnamoorthy, G., and Rao, N. M. (2012) Role of Active Site Rigidity in Activity: MD Simulation and Fluorescence Study on a Lipase Mutant PLoS One 7 e35188
36. Song, H. and Ismagilov, R. F. (2003) Millisecond kinetics on a microfluidic chip using nanoliters of reagents J. Am. Chem. Soc. 125, 14613-14619 (Pubitemid 37452397)
37. Herschlag, D., Eckstein, F., and Cech, T. R. (1993) The Importance of Being Ribose at the Cleavage Site in the Tetrahymena Ribozyme Reaction Biochemistry 32, 8312-8321 (Pubitemid 23265824)
38. Gu, H., Zhang, S., Wong, K. Y., Radak, B. K., Dissanayake, T., Kellerman, D. L., Dai, Q., Miyagi, M., Anderson, V. E., York, D. M., Piccirilli, J. A., and Harris, M. E. (2013) Experimental and computational analysis of the transition state for ribonuclease A-catalyzed RNA 2′-O- transphosphorylation Proc. Natl. Acad. Sci. U.S.A. 110, 13002-13007
39. Wong, K. Y., Gu, H., Zhang, S., Piccirilli, J. A., Harris, M. E., and York, D. M. (2012) Characterization of the reaction path and transition states for RNA transphosphorylation models from theory and experiment Angew. Chem. 51, 647-651
40. a values of catalytic groups in enzyme active sites IUBMB Life 53, 85-98 (Pubitemid 34553129)
41. Mowat, C. G., Moysey, R., Miles, C. S., Leys, D., Doherty, M. K., Taylor, P., Walkinshaw, M. D., Reid, G. A., and Chapman, S. K. (2001) Kinetic and crystallographic analysis of the key active site acid/base arginine in a soluble fumarate reductase Biochemistry 40, 12292-12298 (Pubitemid 32959751)
42. Doherty, M. K., Pealing, S. L., Miles, C. S., Moysey, R., Taylor, P., Walkinshaw, M. D., Reid, G. A., and Chapman, S. K. (2000) Identification of the active site acid/base catalyst in a bacterial fumarate reductase: A kinetic and crystallographic study Biochemistry 39, 10695-10701
43. Bevilacqua, P. C. (2003) Mechanistic considerations for general acid-base catalysis by RNA: Revisiting the mechanism of the hairpin ribozyme Biochemistry 42, 2259-2265 (Pubitemid 36255199)
44. Nakano, S., Chadalavada, D. M., and Bevilacqua, P. C. (2000) General acid-base catalysis in the mechanism of a hepatitis delta virus ribozyme Science 287, 1493-1497 (Pubitemid 30127144)
45. Oivanen, M., Kuusela, S., and Lonnberg, H. (1998) Kinetics and mechanisms for the cleavage and isomerization of the phosphodiester bonds of RNA by Bronsted acids and bases Chem. Rev. 98, 961-990 (Pubitemid 128632233)
46. Sekimoto, T., Matsuyama, T., Fukui, T., and Tanizawa, K. (1993) Evidence for lysine 80 as general base catalyst of leucine dehydrogenase J. Biol. Chem. 268, 27039-27045 (Pubitemid 24006416)
47. Aktas, D. F. and Cook, P. F. (2009) A lysine-tyrosine pair carries out acid-base chemistry in the metal ion-dependent pyridine dinucleotide-linked β-hydroxyacid oxidative decarboxylases Biochemistry 48, 3565-3577
48. Schlippe, Y. V. G. and Hedstrom, L. (2005) A twisted base? The role of arginine in enzyme-catalyzed proton abstractions Arch. Biochem. Biophys. 433, 266-278 (Pubitemid 39586597)
49. Loverix, S., Doumen, J., and Steyaert, J. (1997) Additivity of protein-guanine interactions in ribonuclease T1 J. Biol. Chem. 272, 9635-9639 (Pubitemid 27171622)
50. Francuski, D. and Saenger, W. (2009) Crystal structure of the antitoxin-toxin protein complex RelB-RelE from Methanococcus jannaschii J. Mol. Biol. 393, 898-908
51. Harms, M. J., Schlessman, J. L., Sue, G. R., and Garcia-Moreno, B. (2011) Arginine residues at internal positions in a protein are always charged Proc. Natl. Acad. Sci. U.S.A. 108, 18954-18959
52. Isom, D. G., Castaneda, C. A., Cannon, B. R., and Garcia-Moreno, B. (2011) Large shifts in pKa values of lysine residues buried inside a protein Proc. Natl. Acad. Sci. U.S.A. 108, 5260-5265
53. Baudet, S. and Janin, J. (1991) Crystal-Structure of a Barnase-D(Gpc) Complex at 1.9-Å Resolution J. Mol. Biol. 219, 123-132 (Pubitemid 121003978)
54. Steyaert, J., Hallenga, K., Wyns, L., and Stanssens, P. (1990) Histidine-40 of Ribonuclease-T1 Acts as Base Catalyst When the True Catalytic Base, Glutamic Acid-58, Is Replaced by Alanine Biochemistry 29, 9064-9072 (Pubitemid 20311984)
55. Ruben, E. A., Schwans, J. P., Sonnett, M., Natarajan, A., Gonzalez, A., Tsai, Y., and Herschlag, D. (2013) Ground state destabilization from a positioned general base in the ketosteroid isomerase active site Biochemistry 52, 1074-1081
56. Brown, B. L., Grigoriu, S., Kim, Y., Arruda, J. M., Davenport, A., Wood, T. K., Peti, W., and Page, R. (2009) Three dimensional structure of the MqsR:MqsA complex: A novel TA pair comprised of a toxin homologous to RelE and an antitoxin with unique properties PLoS Pathog. 5, e1000706
57. Inoue-Ito, S., Yajima, S., Fushinobu, S., Nakamura, S., Ogawa, T., Hidaka, M., and Masaki, H. (2012) Identification of the catalytic residues of sequence-specific and histidine-free ribonuclease colicin E5 J. Biochem. 152, 365-372
58. Yajima, S., Inoue, S., Ogawa, T., Nonaka, T., Ohsawa, K., and Masaki, H. (2006) Structural basis for sequence-dependent recognition of colicin E5 tRNase by mimicking the mRNA-tRNA interaction Nucleic Acids Res. 34, 6074-6082 (Pubitemid 44942729)