P61A mutation in the factor for inversion stimulation results in a thermostable dimeric intermediate

Biochemistry

Volumn 44, Issue 45, 2005, Pages 14715-14724

  Meinhold, Derrick ^a   Boswell, Sarah ^a,b   Colón, Wilfredo ^a  

^a Research Rensselaer Polytechnic Institute   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CROSSLINKING; PROTEINS; SELF ASSEMBLY; UREA;

INVERSION STIMULATION; PROTEOLYTIC RESISTANCE;

DIMERS;

ALANINE; BACTERIAL PROTEIN; DIMER; FACTOR FOR INVERSION STIMULATION; GLUTARALDEHYDE; PROLINE; TRANSCRIPTION FACTOR; UREA;

ALPHA HELIX; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CONCENTRATION RESPONSE; CONFORMATIONAL TRANSITION; HEAT TREATMENT; MUTATION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEIN STRUCTURE; REACTION INTERMEDIATE; THERMAL DENATURATION; THERMOSTABILITY;

ALANINE; AMINO ACID SUBSTITUTION; CROSS-LINKING REAGENTS; DIMERIZATION; FACTOR FOR INVERSION STIMULATION PROTEIN; GLUTARAL; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MUTATION; PROLINE; PROTEIN DENATURATION; TEMPERATURE; UREA;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE;

EID: 27744446562     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050640k     Document Type: Article

References (44)

1. Johnson, R. C., Bruist, M. F., and Simon, M. I. (1986) Host protein requirements for in vitro site-specific DNA inversion. Cell 46, 531-539.
2. Koch, C., and Kahmann, R. (1986) Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu, J. Biol. Chem. 261, 15673-15678.
3. Ball, C. A., Osuna, R., Ferguson, K. C., and Johnson, R. C. (1992) Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli, J. Bacteriol. 174, 8043-8056.
4. Xu, J., and Johnson, R. C. (1995) Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli, J. Bacteriol. 177, 938-947.
5. Bruist, M. F., Glasgow, A. C., Johnson, R. C., and Simon, M. I. (1987) Fis binding to the recombinational enhancer of the Hin DNA inversion system, Genes Dev. 1, 762-772.
6. Hobart, S. A., Ilin, S., Moriarty, D. F., Osuna, R., and Colon, W. (2002) Equilibrium denaturation studies of the E. coli factor for inversion stimulation: implications for in vivo function, Protein Sci. 11, 1671-1680.
7. 61 Ala illustrates that the kink within the long α-helix is not due to the presence of the proline residue, J. Biol. Chem. 269, 28947-28954.
8. Boswell, S. A., Mathew, J., Beach, M., Osuna, R., and Colón, W. (2004) Variable contributions of tyrosine residues to the structural and spectroscopic properties of the factor for inversion stimulation, Biochemistry 43, 2964-2977.
9. Richardson, J. S., and Richardson, D. C. (1988) Amino acid preferences for specific locations at the ends of alpha helices, Science 240, 1648-1652.
10. Hobart, S. A., Meinhold, D. W., Osuna, R., and Colon, W. (2002) From two-state to three-state: Effect of P61A mutation on the dynamics and stability of the factor for inversion stimulation results in an altered equilibrium denaturation mechanism, Biochemistry 41, 13744-13754.
11. Park, Y. C, and Bedouelle, H. (1998) Dimeric tyrosyl-tRNA synthetase from Bacillus stearothermophilits unfolds through a monomeric intermediate. A quantitative analysis under equilibrium conditions, J. Biol. Chem. 273, 18052-18059.
12. Zolkiewski, M., Redowicz, M. J., Korn, E. D., Hammer, J. A., III, and Ginsburg, A. (1997) Two-state thermal unfolding of a long dimeric coiled-coil: the Acanthamoeba myosin II rod, Biochemistry 36, 7876-7883.
13. Steif, C., Weber, P., Hinz, H.-J., Flossdorf, J., Cesareni, G., and Kokkinidis, M. (1993) Subunit interaction provide a significant contribution to the stability of the dimeric four-alpha-helical-bundle protein ROP, Biochemistry 32, 3867-3876.
14. Kretschmar, M., and Jaenicke, R. (1999) Stability of a homodimeric Ca(2+)-binding member of the beta gamma-crystallin superfamily: DSC measurements on spherulin 3a from Physarum polycephalum, J. Mol. Biol. 291, 1147-1153.
15. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding, Protein Sci. 4, 2138-2148.
16. Soulages, J. L. (1998) Chemical denaturation: potential impact of undetected intermediates in the free energy of unfolding and m-values obtained from a two-state assumption. Biophys. J. 75, 484-492.
17. Swint, L., and Robertson, A. D. (1993) Thermodynamics of unfolding for turkey ovomucoid third domain: thermal and chemical denaturation, Protein Sci. 2, 2037-2049.
18. Kuroda, Y., Kidokoro, S., and Wada, A. (1992) Thermodynamic characterization of cytochrome c at low pH, J. Mol. Biol. 223, 1139-1153.
19. Nishii, I., Kataoka, M., and Goto, Y. (1995) Thermodynamic stability of the molten globule states of apomyoglobin, J. Mol. Biol. 250, 223-238.
20. Haynie, D. T., and Freire, E. (1993) Structural energetics of the molten globule state, Proteins: Struct., Funct., Genet. 16, 115-140.
21. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling, Electrophoresis 18, 2714-2723.
22. Suhre, K., and Claverie, J. M. (2003) Genomic correlates of hyperthermostability, an update, J. Biol. Chem. 278, 17198-17202.
23. Chakravarty, S., and Varadarajan, R. (2002) Elucidation of factors responsible for enhanced thermal stability of proteins: a structural genomics study, Biochemistry 41, 8152-8161.
24. Vetriani, C., Maeder, D. L., Tolliday, N., Yip, K. S., Stillman, T. J., Britton, K. L., Rice, D. W., Klump, H. H., and Robb, F. T. (1998) Protein thermostability above 100 °C: a key role for ionic interactions, Proc. Natl. Acad. Sci. U.S.A. 95, 12300-12305.
25. Merz, A., Knochel, T., Jansonius, J. N., and Kirschner, K. (1999) The hyperthermostable indoleglycerol phosphate synthase from Thermotoga maritima is destabilized by mutational disruption of two solvent-exposed salt bridges, J. Mol. Biol. 288, 753-763.
26. Biro, J., Fabry, S., Dietmaier, W., Bogedain, C., and Hensel, R. (1990) Engineering thermostability in archaebacterial glyceraldehyde-3-phosphate dehydrogenase. Hints for the important role of interdomain contacts in stabilizing protein conformation, FEBS Lett. 275, 130-134.
27. Kirino, H., Aoki, M., Aoshima, M., Hayashi, Y., Ohba, M., Yamagishi, A., Wakagi, T., and Oshima, T. (1994) Hydrophobic interaction at the subunit interface contributes to the thermostability of 3-isopropylmalate dehydrogenase from an extreme thermophile, Thermus thermophilus, Eur. J. Biochem. 220, 275-281.
28. Toth-Zsamboki, E., Oury, C., Watanabe, H., Nilius, B., Vermylen, J., and Hoylaerts, M. F. (2002) The intracellular tyrosine residues of the ATP-gated P2X1 ion channel are essential for its function, FEBS Lett. 524, 15-19.
29. Zhou, H. X. (2002) Towards the physical basis of thermophilic proteins: linking of enriched polar interactions and reduced heat capacity of unfolding, Biophys. J. 83, 3126-3133.
30. Hardy, F., Vriend, G., van der Vinne, B., Frigerio, F., Grandi, G., Venema, G., and Eijsink, V. G. (1994) The effect of engineering surface loops on the thermal stability of Bacillus subtilis neutral protease, Protein Eng. 7, 425-430.
31. Torrez, M., Schultehenrich, M., and Livesay, D. R. (2003) Conferring thermostability to mesophilic proteins through optimized electrostatic surfaces, Biophys. J. 85, 2845-2853.
32. Kumar, S., Tsai, C. J., and Nussinov, R. (2000) Factors enhancing protein thermostability, Protein Eng. 13, 179-191.
33. Jaenicke, R. (2000) Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity?, Proc. Natl. Acad. Sci. U.S.A. 97, 2962-2964.
34. Thomas, A. S., and Elcock, A. H. (2004) Molecular simulations suggest protein salt bridges are uniquely suited to life at high temperatures, J. Am. Chem. Soc. 126, 2208-2214.
35. a values of the carboxyl and imidazole groups in Bacillus circulans xylanase, Protein Sci. 6, 2667-2670.
36. Georgescu, R. E., Alexov, E. G., and Gunner, M. R. (2002) Combining conformational flexibility and continuum electrostatics for calculating pK(a)s in proteins, Biophys. J. 83, 1731-1748.
37. Finkel, S. E., and Johnson, R. C. (1992) The Fis Protein: it's not just for DNA inversion anymore, Mol. Microbiol. 6, 3257-3265.
38. Ali Azam, T., Iwata, A., Nishimura, A., Ueda, S., and Ishihama, A. (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid, J. Bacteriol. 181, 6361-6370.
39. Beach, M. B., and Osuna, R. (1998) Identification and characterization of the fis operon in enteric bacteria, J. Bacteriol. 180, 5932-5946.
40. Harbury, P. B., Zhang, T., Kim, P. S., and Alber, T. (1993) A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants, Science 262, 1401-1407.
41. Potekhin, S. A., Medvedkin, V. N., Kashparov, I. A., and Venyaminov, S. (1994) Synthesis and properties of the peptide corresponding to the mutant form of the leucine zipper of the transcriptional activator GCN4 from yeast, Protein Eng. 7, 1097-1101.
42. Lumb, K. J., and Kim, P. S. (1995) A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil, Biochemistry 34, 8642-8648.
43. Hardy, J. A., and Nelson, H. C. (2000) Proline in alpha-helical kink is required for folding kinetics but not for kinked structure, function, or stability of heat shock transcription factor, Protein Sci. 9, 2128-2141.
44. Richardson, J. S., and Richardson, D. C. (2002) Natural beta-sheet proteins use negative design to avoid edge-to-edge aggregation, Proc. Natl. Acad. Sci. U.S.A. 99, 2754-2759.