Allosteric Signaling in the Biotin Repressor Occurs via Local Folding Coupled to Global Dampening of Protein Dynamics

Journal of Molecular Biology

Volumn 381, Issue 1, 2008, Pages 89-101

  Laine, Olli ^a   Streaker, Emily D ^a   Nabavi, Maryam ^a   Fenselau, Catherine C ^a   Beckett, Dorothy ^a  

^a Department of Chemistry and Biochemistry   (United States)

Author keywords

allostery; biotin repressor; HDX MS; MALDI ToF MS

Indexed keywords

BIOTIN; DEUTERIUM; HYDROGEN; LIGAND; PEPSIN A; PROTEIN;

ALLOSTERISM; ARTICLE; BINDING SITE; CORRELATION ANALYSIS; DEUTERIUM HYDROGEN EXCHANGE; DYNAMICS; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN BINDING; REPRESSOR GENE; THERMODYNAMICS;

EID: 46649105245     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.05.018     Document Type: Article

References (34)

1. Monod J., Wyman J., and Changeux J.P. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12 (1965) 88-118
2. Koshland Jr. D.E., Nemethy G., and Filmer D. Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5 (1966) 365-385
3. Suel G.M., Lockless S.W., Wall M.A., and Ranganathan R. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nature Struct. Biol. 10 (2003) 59-69
4. Yang J., Garrod S.M., Deal M.S., Anand G.S., Woods Jr. V.L., and Taylor S. Allosteric network of cAMP-dependent protein kinase revealed by mutation of Tyr204 in the P+1 loop. J. Mol. Biol. 346 (2005) 191-201
5. Popovych N., Sun S., Ebright R.H., and Kalodimos C.G. Dynamically driven protein allostery. Nature Struct. Mol. Biol. 13 (2006) 831-838
6. Barker D.F., and Campbell A.M. The birA gene of Escherichia coli encodes a biotin holoenzyme synthetase. J. Mol. Biol. 146 (1981) 451-467
7. Barker D.F., and Campbell A.M. Genetic and biochemical characterization of the birA gene and its product: evidence for a direct role of biotin holoenzyme synthetase in repression of the biotin operon in Escherichia coli. J. Mol. Biol. 146 (1981) 469-492
8. Lane M.D., Rominger K.L., Young D.L., and Lynen F. The enzymatic synthesis of holotranscarboxylase from apotranscarboxylase and (+)-biotin. J. Biol. Chem. 239 (1964) 2865-2871
9. Prakash O., and Eisenberg M.A. Biotinyl 5′-adenylate: corepressor role in the regulation of the biotin genes of Escherichia coli K-12. Proc. Natl Acad. Sci. USA 76 (1979) 5592-5595
10. Streaker E.D., Gupta A., and Beckett D. The biotin repressor: thermodynamic coupling of corepressor binding, protein assembly, and sequence-specific DNA binding. Biochemistry 41 (2002) 14263-14271
11. Streaker E.D., and Beckett D. Coupling of protein assembly and DNA binding: biotin repressor dimerization precedes biotin operator binding. J. Mol. Biol. 325 (2003) 937-948
12. Wilson K.P., Shewchuk L.M., Brennan R.G., Otsuka A.J., and Matthews B.W. Escherichia coli biotin holoenzyme synthetase/bio repressor crystal structure delineates the biotin- and DNA-binding domains. Proc. Natl Acad. Sci. USA 89 (1992) 9257-9261
13. Weaver L.H., Kwon K., Beckett D., and Matthews B.W. Corepressor-induced organization and assembly of the biotin repressor: a model for allosteric activation of a transcriptional regulator. Proc. Natl Acad. Sci. USA 98 (2001) 6045-6050
14. Wood Z.A., Weaver L.H., Brown P.H., Beckett D., and Matthews B.W. Co-repressor induced order and biotin repressor dimerization: a case for divergent followed by convergent evolution. J. Mol. Biol. 357 (2006) 509-523
15. Kwon K., Streaker E.D., Ruparelia S., and Beckett D. Multiple disordered loops function in corepressor-induced dimerization of the biotin repressor. J. Mol. Biol. 304 (2000) 821-833
16. Xu Y., Nenortas E., and Beckett D. Evidence for distinct ligand-bound conformational states of the multifunctional Escherichia coli repressor of biotin biosynthesis. Biochemistry 34 (1995) 16624-16631
17. Naganathan S., and Beckett D. Nucleation of an allosteric response via ligand-induced loop folding. J. Mol. Biol. 373 (2007) 96-111
18. Brown P., Cronan J.E., Grotli M., and Beckett D. The biotin repressor: modulation of allostery by corepressor analogs. J. Mol. Biol. 337 (2004) 857-869
19. Hoofnagle A.N., Resing K.A., and Ahn N.G. Practical methods for deuterium exchange/mass spectrometry. Methods Mol. Biol. 250 (2004) 283-298
20. Zhang Z., and Smith D.L. Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation. Protein Sci. 2 (1993) 522-531
21. Emrick M.A., Lee T., Starkey P.J., Mumby M.C., Resing K.A., and Ahn N.G. The gatekeeper residue controls autoactivation of ERK2 via a pathway of intramolecular connectivity. Proc. Natl Acad. Sci. USA 103 (2006) 18101-18106
22. Koeppe J.R., and Komives E.A. Amide H/2H exchange reveals a mechanism of thrombin activation. Biochemistry 45 (2006) 7724-7732
23. Brock M., Fan F., Mei F.C., Li S., Gessner C., Woods Jr. V.L., and Cheng X. Conformational analysis of Epac activation using amide hydrogen/deuterium exchange mass spectrometry. J. Biol. Chem. 282 (2007) 32256-32263
24. Englander J.J., Del Mar C., Li W., Englander S.W., Kim J.S., Stranz D.D., et al. Protein structure change studied by hydrogen-deuterium exchange, functional labeling, and mass spectrometry. Proc. Natl Acad. Sci. USA 100 (2003) 7057-7062
25. Resing K.A., and Ahn N.G. Deuterium exchange mass spectrometry as a probe of protein kinase activation. Analysis of wild-type and constitutively active mutants of MAP kinase kinase-1. Biochemistry 37 (1998) 463-475
26. Mandell J.G., Falick A.M., and Komives E.A. Measurement of amide hydrogen exchange by MALDI-TOF mass spectrometry. Anal. Chem. 70 (1998) 3987-3995
27. Englander S.W. Hydrogen exchange and mass spectrometry: a historical perspective. J. Am. Soc. Mass Spectrom. 17 (2006) 1481-1489
28. Brown P.H., and Beckett D. Use of binding enthalpy to drive an allosteric transition. Biochemistry 44 (2005) 3112-3121
29. Keramisanou D., Biris N., Gelis I., Sianidis G., Karamanou S., Economou A., and Kalodimos C.G. Disorder-order folding transitions underlie catalysis in the helicase motor of SecA. Nature Struct. Mol. Biol. 13 (2006) 594-602
30. Hilser V.J., and Thompson E.B. Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins. Proc. Natl Acad. Sci. USA 104 (2007) 8311-8315
31. Tsai C.J., Del Sol A., and Nussinov R. Allostery: absence of a change in shape does not imply that allostery is not at play. J. Mol. Biol. (2008) In the press
32. Abbott J., and Beckett D. Cooperative binding of the Escherichia coli repressor of biotin biosynthesis to the biotin operator sequence. Biochemistry 32 (1993) 9649-9656
33. Gill S.C., and von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182 (1989) 319-326
34. Koradi R., Billeter M., and Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14 (1996) 51-55