A Linear Correlation between the Energetics of Allosteric Communication and Protein Flexibility in the Escherichia coli Cyclic AMP Receptor Protein Revealed by Mutation-Induced Changes in Compressibility and Amide Hydrogen-Deuterium Exchange

Biochemistry

Volumn 43, Issue 13, 2004, Pages 3844-3852

  Gekko, Kunihiko ^a   Obu, Norihiro ^a   Li, Jianquan ^b   Lee, J Ching ^b  

^a HIROSHIMA UNIVERSITY   (Japan)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTIC WAVE VELOCITY; AMINO ACIDS; BINDING ENERGY; DNA; ELECTRON DENSITY MEASUREMENT; ESCHERICHIA COLI; FOURIER TRANSFORM INFRARED SPECTROSCOPY; MUTAGENESIS; SUBSTITUTION REACTIONS;

ALLOSTERIC COMMUNICATION; CAMP BINDING; CYCLIC AMP RECEPTOR PROTEIN (CRP);

PROTEINS;

AMIDE; CARBON; CYCLIC AMP; CYCLIC AMP BINDING PROTEIN; DEUTERIUM; MUTANT PROTEIN;

ALLOSTERISM; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; DNA BINDING; ENERGY; ESCHERICHIA COLI; INFRARED SPECTROSCOPY; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; WILD TYPE;

ALLOSTERIC REGULATION; AMIDES; BINDING SITES; CIRCULAR DICHROISM; CYCLIC AMP RECEPTOR PROTEIN; DEUTERIUM EXCHANGE MEASUREMENT; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; LINEAR MODELS; MODELS, CHEMICAL; MUTAGENESIS, SITE-DIRECTED; SOLUTIONS; SOLVENTS; SPECTROPHOTOMETRY, ULTRAVIOLET; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 1842539352     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi036271e     Document Type: Article

References (41)

1. de Crombrugghe, B., Busby, S., and Buc, H. (1984) Cyclic AMP receptor protein: role in transcription activation, Science 224, 831-838.
2. Kolb, A., Busby, S., Buc, H., Garges, S., and Adhya, S. (1993) Transcriptional regulation by cAMP and its receptor protein, Annu. Rev. Biochem. 62, 749-795.
3. Busby, S., and Ebright, R. H. (1999) Transcription activation by catabolite activator protein (CAP), J. Mol. Biol. 293, 199-213.
4. Harman, J. G. (2001) Allosteric regulation of the cAMP receptor protein, Biochim. Biophys. Acta 1547, 1-17.
5. McKay, D. B., Weber, I. T., and Steitz, T. A. (1982) Structure of catabolite gene activator protein at 2.9 Å resolution. Incorporation of amino acid sequence and interactions with cyclic AMP, J. Biol. Chem. 251, 9518-9524.
6. Weber, I. T., and Steitz, T. A. (1987) Structure of a Complex of Catabolite Gene Activator Protein and Cyclic AMP Refined at 2.5 Å Resolution, J. Mol. Biol. 198, 311-326.
7. Passner, J. M., Schultz, S. C., and Steitz, T. A. (2000) Modeling the cAMP-induced Allosteric Transition Using the Crystal Structure of CAP-cAMP at 2.1 Å Resolution, J. Mol. Biol. 304, 847-859.
8. Li, J., Cheng, X., and Lee, J. C. (2002) Structure and Dynamics of the Modular Halves of Escherichia coli Cyclic AMP Receptor Protein, Biochemistry 41, 14771-14778.
9. Lin, S.-H., and Lee, J. C. (2002) Communications between the High-Affinity Cyclic Nucleotide Binding Sites in E. coli Cyclic AMP Receptor Protein: Effect of Single Site Mutations, Biochemistry 41, 11857-11867.
10. Lin, S.-H., and Lee, J. C. (2002) Linkage of Multiequilibria in DNA Recognition by the D53H Escherichia coli cAMP Receptor Protein, Biochemistry 41, 14935-14943.
11. Chen, R., and Lee, J. C. (2003) Functional Roles of Loops 3 and 4 in the Cyclic Nucleotide Binding Domain of Cyclic AMP Receptor Protein from Escherichia coli, J. Biol. Chem. 278, 13235-13243.
12. Eilen, E., and Krakow, J. S. (1997) Effects of cyclic nucleotides on the conformational states of the α core of the cyclic AMP receptor protein, Biochim. Biophys. Acta 493, 115-121.
13. Eilen, E., Pampeno, C., and Krakow, J. S. (1978) Functional Roles of Loops 3 and 4 in the Cyclic Nucleotide Binding Domain of Cyclic AMP Receptor Protein from Escherichia coli, Biochemistry 17, 2469-2473.
14. Ebright, R. H., LeGrice, S. F. J., Miller, J. P., and Krakow, J. S. (1985) Analogs of Cyclic AMP that Elicit the Biochemically Defined Conformational Change in Catabolite Gene Activator Protein (CAP) but do not Stimulate Binding to DNA, J. Mol. Biol. 182, 91-107.
15. Kumar, S. A., Murthy, N. S., and Krakow, J. S. (1980) Ligand-induced change in the radius of gyration of cAMP receptor protein from Escherichia coli, FEBS Lett. 109, 121-124.
16. Wu, F. Y.-H., Nath, K., and Wu, C. W. (1974) Conformational Transitions of Cyclic Adenosine Monophosphate Receptor Protein of Escherichia coli. A Fluorescent Probe Study, Biochemistry 13, 2567-2572.
17. DeGrazia, H., Harman, J. G., Tan, G. S., and Wertell, R. M. (1990) Investigation of the cAMP receptor protein secondary structure by Raman spectroscopy, Biochemistry 29, 3557-3562.
18. Tan, G. S., Kelly, P., Kim, J., and Wartell, R. M. (1991) Comparison of cAMP Receptor Protein (CRP) and a cAMP-Independent Form of CRP by Raman Spectroscopy and DNA Binding, Biochemistry 30, 5076-5080.
19. Baichoo, N., and Heyduk, T. (1997) Mapping Conformational Changes in a Protein: Application of a Protein Footprinting Technique to cAMP-Induced Conformational Changes in cAMP Receptor Protein, Biochemistry 36, 10830-10836.
20. Baichoo, N., and Heyduk, T. (1999) Mapping cyclic nucleotide-induced conformational changes in cyclic-AMP receptor protein by a protein footprinting technique using different chemical proteases, Protein Sci. 8, 518-528.
21. Won, H. S., Lee, T. W., Park, S. H., and Lee, B. J. (2002) Stoichiometry and Structural Effect of the Cyclic Nucleotide Binding to Cyclic AMP Receptor Protein, J. Biol. Chem. 277, 11450-11455.
22. Heyduk, T., and Lee, J. C. (1989) Escherichia coli cAMP Receptor Protein: Evidence for Three Protein Conformational States with Different Promoter Binding Affinities, Biochemistry 28, 6914-6924.
23. Pan, H., Lee, J. C., and Hilser, V. J. (2000) Binding sites in Escherichia coli dihydrofolate reductase communicate by modulating the conformational ensemble, Proc. Natl. Acad. Sci. U.S.A. 97, 12020-12025.
24. Karplus, M., and McCammon, J. A. (1981) The internal dynamics of globular proteins, CRC Crit. Rev. Biochem. 9, 293-349.
25. Cooper, A. (1976) Thermodynamic fluctuations in protein molecules, Proc. Natl. Acad. Sci. U.S.A. 73, 2740-2741.
26. Gekko, K., and Noguchi, H. (1979) Compressibility of globular proteins in water at 25 °C, J. Phys. Chem. 83, 2706-2714.
27. Gekko, K., and Hasegawa, Y. (1986) Compressibility-structure relationship of globular proteins, Biochemistry 25, 6563-6571.
28. Taulier, N., and Chalikian, T. V. (2002) Compressibility of protein transitions, Biochim. Biophys. Acta 1595, 48-70.
29. Kamiyama, T., and Gekko, K. (2000) Effect of ligand binding on the flexibility of dihydrofolate reductase as revealed by compressibility, Biochim. Biophys. Acta 1478, 257-266.
30. Gekko, K., Kimoto, A., and Kamiyama, T. (2003) Effects of Disulfide Bonds on Compactness of Protein Molecules Revealed by Volume, Compressibility, and Expansibility Changes during Reduction, Biochemistry 42, 13746-13753.
31. Tamura, Y., and Gekko, K. (1995) Compactness of thermally and chemically denatured ribonuclease A as revealed by volume and compressibility, Biochemistry 34, 1878-1884.
32. Gekko, K., Kamiyama, T., Ohmae, E., and Katayanagi, K. (2000) Single amino acid substitutions in flexible loops can induce large compressibility changes in dihydrofolate reductase, J. Biochem. 128, 21-27.
33. Gekko, K., Tamura, Y., Ohmae, E., Hayashi, H., Kagamiyama, H., and Ueno, H. (1996) A large compressibility change of protein induced by a single amino acid substitution, Protein Sci. 5, 542-545.
34. Kim, K. S., Fuchs, J. A., and Woodward, C. K. (1993) Hydrogen exchange identifies native-state motional domains important in protein folding, Biochemistry 32, 9600-9608.
35. Lin, S.-H., Kovac, L., Chin, A. J., Chin, C. C.-Q., and Lee, J. C. (2002) Ability of E. coli Cyclic AMP Receptor Protein To Differentiate Cyclic Nucleotides: Effects of Single Site Mutations, Biochemistry 41, 2946-2955.
36. Mihalyi, E. (1976) in Handbook of Biochemistry and Molecular Biology (Fasmann, G. D., Ed.) p 189, CRC Press, Boca Raton, FL.
37. Greenspan, M. G., and Tschiegg, C. (1956) Sing-around ultrasonic velocimeter for liquids, Rev. Sci. Instrum. 28, 897-901.
38. Tamura, Y., Suzuki, N., and Mihashi, K. (1993) Adiabatic compressibility of myosin subfragment-1 and heavy meromyosin with or without nucleotide, Biophys. J. 65, 1899-1905.
39. Susi, H., and Byler, D. M. (1983) Protein structure by Fourier transform infrared spectroscopy: second derivative spectra, Biochem. Biophys. Res. Commun. 115, 391-397.
40. de Jongh, H. H., Goormaghtigh, E., and Ruysschaert, J. M. (1995) Tertiary stability of native and methionine-80 modified cytochrome c detected by proton-deuterium exchange using online Fourier transform infrared spectroscopy, Biochemistry 34, 172-179.
41. Kauzmann, W. (1959) Some factors in the interpretation of protein denaturation, Adv. Protein Chem. 14, 1-63.