Dominant role of local dipolar interactions in phosphate binding to a receptor cleft with an electronegative charge surface: Equilibrium, kinetic, and crystallographic studies

Protein Science

Volumn 7, Issue 12, 1998, Pages 2550-2559

  Ledvina, Polly S ^a   Tsai, Ah Lim ^b   Wang, Zhongmin ^a   Koehl, Edward ^a   Quiocho, Florante A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Anion binding sites; Electrostatic interaction; Fast kinetics; Hinge bending motion; Noncomplementary surface charge sites; Phosphate binding protein; X ray structure

Indexed keywords

BINDING PROTEIN; PHOSPHATE;

ARTICLE; BINDING KINETICS; CRYSTALLOGRAPHY; ELECTRICITY; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR BINDING;

EID: 0031678068     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560071208     Document Type: Article

References (34)

1. Åqvist J, Luecke J, Quiocho FA. 1991. Dipoles localized at helix termini of proteins stabilize charges. Proc Natl Acad Sci USA 88:2026-2030.
2. Brune M, Hunter JL, Corrie JE, Webb MR. 1994. Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment 1 ATPase. Biochemistry 33:8262-8271.
3. Brünger AT. 1992. X-PLOR. Version 3.1, A system for X-ray crystallography and NMR. New Haven, Connecticut: Yale University.
4. Careaga CL, Sutherland J, Sabeti J, Falke JJ. 1995. Large amplitude twisting motions of an interdomain hinge: A disulfide trapping study of the galactose-glucose binding protein. Biochemistry 34:3048-3055.
5. Cleland WW, Kreevoy MM. 1994. Low-barrier hydrogen bonds and enzymic catalysis. Science 264:1887-1890.
6. Engh RA, Huber R. 1991. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallogr A47:392-400.
7. He JJ, Quiocho FA. 1993. Dominant role of local dipoles in stabilizing uncompensated charges on a sulfate sequestered in a periplasmic active transport protein. Protein Sci 2:1643-1647.
8. Hibbert F, Emsley J. 1990. Hydrogen bonding and chemical reactivity. Adv Phys Org Chem 26:255-379.
9. Jacobson BL, He JJ, Lemon DD, Quiocho FA. 1992. Interdomain salt bridges modulate ligand-induced domain motion of the sulfate receptor protein for active transport. J Mol Biol 223:27-30.
10. Kang CH, Shin WC, Yamagata Y, Gokcen S, Ames GF, Kim SH. 1991. Crystal structure of the lysine-, arginine-, ornithine-bindmg protein (LAO) from Salmonella typhimurium at 2.7 Å resolution. J Biol Chem 266:23893-23899.
11. Kubena BD, Luecke H, Rosenberg H, Quiocho FA. 1986. Crystallization and x-ray diffraction studies of a phosphate-binding protein involved in active transport in Escherichia coli. J Biol Chem 261:7995-7996.
12. Ledvina PS, Yao N, Choudhary A, Quiocho FA. 1996. Negative electrostatic surface potential of protein sites specific for anionic ligands. Proc Natl Acad Sci USA 93:6786-6791.
13. Luecke H, Quiocho FA. 1990. High specificity of a phosphate transport protein determined by hydrogen bonds. Nature 347:402-406.
14. Medveczky N, Rosenberg H. 1970. The phosphate-binding protein of Escherichia coli. Biochim Biophys Acta 211:158-168.
15. Miller DM III, Olson JS, Pflugrath JW, Quiocho FA. 1983. Rates of ligand binding to periplasmic proteins involved in bacterial transport and chemotaxis. J Biol Chem 258:13665-13672.
16. Miller DM III, Olson JS, Quiocho FA. 1980. The mechanism of sugar binding to the periplasmic receptor for galactose chemotaxis and transport in Escherichia coli. J Biol Chem 255:2465-2471.
17. Nicholls A, Bharadwaj R, Honig B. 1993. Grasp: Graphical representation and analysis of surface properties. Biophys J 64:166-170.
18. Nickitenko AV, Trakhanov S, Quiocho FA. 1995. 2 Å resolution structure of DppA, a periplasmic dipeptide transport/chemosensory receptor. Biochemistry 34:16585-16595.
19. Nolte HJ, Rosenberry, TL, Neumann E. 1980. Effective charge on acetylcholinesterase active sites determined from the ionic strength dependence of association rate constants with cationic ligands. Biochemistry 19:3705-3711.
20. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326.
21. Pardee AB. 1966. Purification and properties of a sulfate-binding protein from Salmonella typhimurium. J Biol Chem 241:5886-5892.
22. Pflugrath JW, Quiocho FA. 1985. Sulphate sequestered in the sulfate-binding protein is bound solely by hydrogen bonds. Nature 314:257-260.
23. Quiocho FA. 1991. Atomic structure and function of periplasmic receptors for active transport and chemotaxis. Curr Opin Struct Biol 1:922-933.
24. Quiocho FA, Gilliland GL, Phillips GN Jr. 1977. The 2.8-Å resolution structure of the L-arabinose-binding protein from Escherichia coli. Polypeptide chain folding, domain similarity, and probable location of sugar-binding site. J Biol Chem 252:5142-5149.
25. Quiocho FA, Ledvina PS. 1996. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: Variation of common themes. Mol Microbiol 20:17-25.
26. Quiocho FA, Sack JS, Vyas NK. 1987. Stabilization of charges on isolated charged groups sequestered in proteins by polarized peptide units. Nature 327:561-564.
27. Sack JS, Quiocho FA. 1997. CHAIN - A crystallographic modeling program. Methods Enzymol 277:158-173.
28. Sack JS, Saper MA, Quiocho FA. 1989. Periplasmic binding protein structure and function. Refined X-ray structures of the leucine/isoleucine/valine-binding protein and its complex with leucine. J Mol Biol 206:171-191.
29. Vermersch PS, Tesmer JJ, Lemon DD, Quiocho FA. 1990. A Pro to Gly mutation in the hinge of the arabinose-binding protein enhances binding and alters specificity. Sugar-binding and crystallographic studies. J Biol Chem 265: 16592-16603.
30. Walmsley AR, Shaw JG, Kelly DJ. 1992. The mechanism of ligand binding to the periplasmic C4-dicarboxylale binding protein (DctP) from Rhodobacter capsulatus. J Biol Chem 267:8064-8072.
31. Wang Z, Choudhary A, Ledvina PS, Quiocho FA. 1994. Fine tuning the specificity of the periplasmic phosphate receptor for active transport. Site-directed mutagenesis, ligand binding, and crystallographic studies. J Biol Chem 269:25091-25094.
32. Wang Z, Luecke H, Yao N, Quiocho FA. 1997. A low energy short hydrogen bond in very high resolution structures of protein receptor-phosphate com-plexes. Nat Struct Biol 4:519-522.
33. Yao N, Ledvina PS, Choudhary A, Quiocho FA. 1996. Modulation of a salt link does not affect binding of phosphate to its specific active transport receptor. Biochemistry 35:2079-2085.
34. Yao N, Trakhanov S, Quiocho FA. 1994. Refined 1.89-Å structure of the histidine-binding protein complexed with histidine and its relationship with many other active transport/chemosensory proteins. Biochemistry 33:4769-4779.