Substitutions of Thr30 provide mechanistic insight into tryptophan-mediated activation of TRAP binding to RNA

Nucleic Acids Research

Volumn 34, Issue 10, 2006, Pages 2933-2942

  Payal, Vandana ^a   Gollnick, Paul ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; RNA; THREONINE; THROMBIN RECEPTOR ACTIVATING PEPTIDE; TRYPTOPHAN; VALINE; BACTERIAL PROTEIN; RNA BINDING PROTEIN; TRYPSIN;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS SUBTILIS; BETA CHAIN; BINDING ASSAY; BINDING KINETICS; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; BIOSYNTHESIS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OPERON; PROTEIN BINDING;

BACILLUS SUBTILIS;

AMINO ACID SUBSTITUTION; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; GENE EXPRESSION REGULATION, BACTERIAL; OPERON; PROTEIN BINDING; RNA; RNA-BINDING PROTEINS; THREONINE; TRYPSIN; TRYPTOPHAN; VALINE;

EID: 33745156497     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl383     Document Type: Article

References (41)

1. Babitzke,P. (1997) Regulation of tryptophan biosynthesis: Trp-ing the TRAP or how Bacillus subtilis reinvented the wheel. Mol. Microbiol., 26, 1-9.
2. Gollnick,P. (1994) Regulation of the Bacillus subtilis trp operon by an RNA-binding protein. Mol. Microbiol., 11, 991-997.
3. Chen,X., Antson,A.A., Yang,M., Li,P., Baumann,C., Dodson,E.J., Dodson,G.G. and Gollnick,P. (1999) Regulatory features of the trp operon and the crystal structure of the trp RNA-binding attenuation protein from Bacillus stearothermophilus. J. Mol. Biol., 289, 1003-1016.
4. Antson,A.A., Otridge,J., Brzozowski,A.M., Dodson,E.J., Dodson,G.G., Wilson,K.S., Smith,T.M., Yang,M., Kurecki,T. and Gollnick,P. (1995) The structure of trp RNA-binding attenuation protein. Nature, 374, 693-700.
5. Otridge,J. and Gollnick,P. (1993) MtrB from Bacillus subtilis binds specifically to trp leader RNA in a tryptophan-dependent manner. Proc. Natl Acad. Sci. USA, 90, 128-132.
6. Babitzke,P., Stults,J.T., Shire,S.J. and Yanofsky,C. (1994) TRAP, the trp RNA-binding attenuation protein of Bacillus subtilis, is a multisubunit complex that appears to recognize G/UAG repeats in the trpEDCFBA and trpG transcripts. J. Biol. Chem., 269, 16597-16604.
7. Baumann,C., Xirasagar,S. and Gollnick,P. (1997) The trp RNA-binding attenuation protein (TRAP) from Bacillus subtilis binds to unstacked trp leader RNA. J. Biol. Chem., 272, 19863-19869.
8. Babitzke,P., Yealy,J. and Campanelli,D. (1996) Interaction of the trp RNA-binding attenuation protein (TRAP) of Bacillus subtilis with RNA: effects of the number of GAG repeats, the nucleotides separating adjacent repeats, and RNA secondary structure. J. Bacteriol., 178, 5159-5163.
9. Babitzke,P., Bear,D.G. and Yanofsky,C. (1995) TRAP, the trp RNA-binding attenuation protein of Bacillus subtilis, is a toroid-shaped molecule that binds transcripts containing GAG or UAG repeats separated by two nucleotides. Proc. Natl Acad. Sci. USA, 92, 7916-7920.
10. Hopcroft,N.H., Manfredo,A., Wendt,A.L., Brzozowski,A.M., Gollnick,P. and Antson,A.A. (2004) The interaction of RNA with TRAP: The role of triplet repeats and separating spacer nucleotides. J. Mol. Biol., 338, 43-53.
11. Antson,A.A., Dodson,E.J., Dodson,G., Greaves,R.B., Chen,X. and Gollnick,P. (1999) Structure of the trp RNA-binding attenuation protein, TRAP, bound to RNA. Nature, 401, 235-242.
12. Yang,M., Chen,X., Militello,K., Hoffman,R., Fernandez,B., Baumann,C. and Gollnick,P. (1997) Alanine-scanning mutagenesis of Bacillus subtilis trp RNA-binding attenuation protein (TRAP) reveals residues involved in tryptophan binding and RNA binding. J. Mol. Biol., 270, 696-710.
13. Snyder,D., Lary,J., Chen,Y., Gollnick,P. and Cole,J.L. (2004) Interaction of the trp RNA-binding attenuation protein (TRAP) with anti-TRAP. J. Mol. Biol., 338, 669-682.
14. Li,P.T., Scott,D.J. and Gollnick,P. (2002) Creating hetero-11-mers composed of wild-type and mutant subunits to study RNA binding to TRAP. J. Biol. Chem., 277, 11838-11844.
15. McElroy,C., Manfredo,A., Wendt,A., Gollnick,P. and Foster,M. (2002) TROSY-NMR studies of the 91kDa TRAP protein reveal allosteric control of a gene regulatory protein by ligand-altered flexibility. J. Mol. Biol., 323, 463-473.
16. Yakhnin,A.V., Trimble,J.J., Chiaro,C.R. and Babitzke,P. (2000) Effects of mutations in the L-tryptophan binding pocket of the Trp RNA-binding attenuation protein of Bacillus subtilis. J. Biol. Chem., 275, 4519-4524.
17. Li,P.T. and Gollnick,P. (2004) Characterization of a trp RNA-binding attenuation protein (TRAP) mutant with tryptophan independent RNA binding activity. J. Mol. Biol., 335, 707-722.
18. Xirasagar,S., Elliott,M.B., Bartolini,W., Gollnick,P. and Gottlieb,P.A. (1998) RNA structure inhibits the TRAP (trp RNA-binding attenuation protein)-RNA interaction. J. Biol. Chem., 273, 27146-27153.
19. Tabor,S. and Richardson,C.C. (1985) A bacteriophage T7 RNA polymerase/ promoter system for controlled exclusive expression of specific genes. Proc. Natl Acad. Sci. USA, 82, 1074-1078.
20. Yang,M., de Saizieu,A., van Loon,A.P. and Gollnick,P. (1995) Translation of trpG in Bacillus subtilis is regulated by the trp RNA-binding attenuation protein (TRAP). J. Bacteriol., 177, 4272-4278.
21. Kuroda,M.I., Henner,D. and Yanofsky,C. (1988) cis-acting sites in the transcript of the Bacillus subtilis trp operon regulate expression of the operon. J. Bacteriol., 170, 3080-3088.
22. van der Vossen,J.M., van der Lelie,D. and Venema,G. (1987) Isolation and characterization of Streptococcus cremoris Wg2-specific promoters. Appl. Environ. Microbiol., 53, 2452-2457.
23. Guerout-Fleury,A.M., Shazand,K., Frandsen,N. and Stragier,P. (1995) Antibiotic-resistance cassettes for Bacillus subtilis. Gene, 167, 335-336.
24. Gollnick,P., Ishino,S., Kuroda,M.I., Henner,D.J. and Yanofsky,C. (1990) The mtr locus is a two-gene operon required for transcription attenuation in the trp operon of Bacillus subtilis. Proc. Natl Acad. Sci. USA, 87, 8726-8730.
25. Antson,A.A., Brzozowski,A.M., Dodson,E.J., Dauter,Z., Wilson,K.S., Kurecki,T., Otridge,J. and Gollnick,P. (1994) 11-fold symmetry of the trp RNA-binding attenuation protein (TRAP) from Bacillus subtilis determined by X-ray analysis. J. Mol. Biol., 244, 1-5.
26. Baumann,C., Otridge,J. and Gollnick,P. (1996) Kinetic and thermodynamic analysis of the interaction between TRAP (trp RNA-binding attenuation protein) of Bacillus subtilis and trp leader RNA. J. Biol. Chem., 271, 12269-12274.
27. Li,P.T. and Gollnick,P. (2002) Using hetero-11-mers composed of wild type and mutant subunits to study tryptophan binding to TRAP and its role in activating RNA binding. J. Biol. Chem., 277, 35567-35573.
28. Hopcroft,N.H., Wendt,A.L., Gollnick,P. and Antson,A.A. (2002) Specificity of TRAP-RNA interactions: Crystal structures of two complexes with different RNA sequences. Acta Crystallogr. D Biol. Crystallogr., 58, 615-621.
29. Betts,M.J. and Russels,R.B. (2003) Amino acid properties and consequences of substitution. In Barnes,M.R. and Gray,I.C. (eds), Bioinformatics for Genetecists. John Wiley and Sons Ltd, pp. 289-316.
30. Creighton,T.E. (1993) Proteins, Structures and Molecular Properties, 2nd edn. Freeman and Company, NY.
31. Gollnick,P., Babitzke,P., Antson,A. and Yanofsky,C. (2005) Complexity in regulation of tryptophan biosynthesis in Bacillus subtilis. Annu Rev Genet., 39, 47-68.
32. Steinberg,W. (1974) Temperature-induced derepression of tryptophan biosynthesis in a tryptophanyl-transfer ribonucleic acid synthetase mutant of Bacillus subtilis. J. Bacteriol., 117, 1023-1034.
33. TT charging and regulates expression of the genes of tryptophan biosynthesis. Proc. Natl Acad. Sci. USA, 97, 2656-2661.
34. Valbuzzi,A. and Yanofsky,C. (2001) Inhibition of the B.subtilis regulatory protein TRAP by the TRAP-inhibitory protein, AT. Science, 293, 2057-2059.
35. Valbuzzi,A., Gollnick,P., Babitzke,P. and Yanofsky,C. (2002) The anti-trp RNA-binding attenuation protein (Anti-TRAP), AT, recognizes the tryptophan-activated RNA binding domain of the TRAP regulatory protein. J. Biol. Chem., 277, 10608-10613.
36. Somerville,R. (1992) The Trp repressor, a ligand-activated regulatory protein. Prog. Nucleic Acid. Res. Mol. Biol., 42, 1-38.
37. Zhao,D., Arrowsmith,C.H., Jia,X. and Jardetzky,O. (1993) Refined solution structures of the Escherichia coli trp holo- and aporepressor. J. Mol. Biol., 229, 735-746.
38. Schevitz,R.W., Otwinowski,Z., Joachimiak,A., Lawson,C.L. and Sigler,P.B. (1985) The three-dimensional structure of trp repressor. Nature, 317, 782-786.
39. Kelley,R.L. and Yanofsky,C. (1985) Mutational studies with the trp repressor of Escherichia coli support the helix-turn-helix model of repressor recognition of operator DNA. Proc. Natl Acad. Sci. USA, 82, 483-487.
40. Luisi,B.F. and Sigler,P.B. (1990) The stereochemistry and biochemistry of the trp repressor-operator complex. Biochim. Biophys. Acta, 1048, 113-126.
41. Mechuram,T., Fayat,G. and Blanquet,S. (1983) Sequence of the Escherichia coli pheST operon and identification of the himA gene. J. Bacteriol., 163, 787-791.