Interstrand loops CD and EF act as pH-dependent gates to regulate fatty acid ligand binding in tear lipocalin

Biochemistry

Volumn 43, Issue 40, 2004, Pages 12894-12904

  Gasymov, Oktay K ^a   Abduragimov, Adil R ^a   Yusifov, Taleh N ^a   Glasgow, Ben J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENERGY TRANSFER; FLUORESCENCE; IONIZATION; MUTAGENESIS; PH EFFECTS; PHASE TRANSITIONS; RESONANCE; TITRATION;

CIRCULAR DICHROISM SPECTROSCOPY; ELECTROSTATIC INTERACTIONS; LIGAND BINDING; PALMITIC ACIDS; TEAR LIPOCALIN (TL);

FATTY ACIDS;

16 (9 ANTHROYLOXY)PALMITIC ACID; 8 ANILINO 1 NAPHTHALENESULFONIC ACID; ACRYLAMIDE; FATTY ACID; LIGAND; LIPOCALIN; PALMITIC ACID DERIVATIVE; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; ENERGY TRANSFER; FLUORESCENCE; IONIZATION; LACRIMAL FLUID; LIGAND BINDING; PH; PRIORITY JOURNAL;

CARRIER PROTEINS; CIRCULAR DICHROISM; FATTY ACIDS; HUMANS; HYDROGEN-ION CONCENTRATION; LIGANDS; MUTATION; PALMITIC ACIDS; PROTEIN STRUCTURE, SECONDARY; SPECTROMETRY, FLUORESCENCE; TEARS; TRYPTOPHAN;

CALYX;

EID: 4944239351     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049076o     Document Type: Article

References (45)

1. Glasgow, B. J., Abduragimov, A. R., Farahbakhsh, Z. T., Faull, K. F., and Hubbell, W. L. (1995) Tear lipocalins bind a broad array of lipid ligands, Curr. Eye Res. 14, 363-372.
2. Glasgow, B. J., Marshall, G., Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Knobler, C. M. (1999) Tear lipocalins: potential lipid scavengers for the corneal surface, Invest. Ophthalmol. Visual Sci. 40, 3100-3107.
3. Selsted, M. E., and Martinez, R. J. (1982) Isolation and purification of bactericides from human tears, Exp. Eye. Res. 34, 305-318.
4. van't Hof, W., Blankenvoorde, M. F., Veerman, E. C., and Amerongen, A. V. (1997) The salivary lipocalin von Ebner's gland protein is a cysteine proteinase inhibitor, J. Biol. Chem. 272, 1837-1841.
5. Blaker, M., Kock, K., Ahlers, C., Buck, F., and Schmale, H. (1993) Molecular cloning of human von Ebner's gland protein, a member of the lipocalin superfamily highly expressed in lingual salivary glands, Biochim. Biophys. Acta 1172, 131-137.
6. Redl, B., Holzfeind, P., and Lottspeich, F. (1992) cDNA cloning and sequencing reveals human tear prealbumin to be a member of the lipophilic-ligand carrier protein superfamily, J. Biol. Chem. 267, 20282-20287.
7. Lechner, M., Wojnar, P., and Redl, B. (2001) Human tear lipocalin acts as an oxidative-stress-induced scavenger of potentially harmful lipid peroxidation products in a cell culture system, Biochem. J. 356, 129-135.
8. Glasgow, B. J., Abduragimov, A. R., Gassymov, O. K., Yusifov, T. N., Ruth, E. C., and Faull, K. F. (2002) Vitamin E associated with the lipocalin fraction of human tears, Adv. Exp. Med. Biol. 506, 567-572.
9. Yusifov, T. N., Abduragimov, A. R., Gasymov, O. K., and Glasgow, B. J. (2000) Endonuclease activity in lipocalins, Biochem. J. 347 Pt 3, 815-819.
10. Flower, D. R. (1996) The lipocalin protein family: structure and function, Biochem. J. 318 (Part 1), 1-14.
11. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (2000) Resolution of ligand positions by site-directed tryptophan fluorescence in tear lipocalin, Protein Sci. 9, 325-331.
12. Glasgow, B. J., Abduragimov, A. R., Yusifov, T. N., Gasymov, O. K., Horwitz, J., Hubbell, W. L., and Faull, K. F. (1998) A conserved disulfide motif in human tear lipocalins influences ligand binding, Biochemistry 37, 2215-2225.
13. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (2002) RET and anisotropy measurements establish the proximity of the conserved Trp17 to I1e98 and Phe99 of tear lipocalin, Biochemistry 41, 8837-8848.
14. Kennedy, M. W., Brass, A., McCruden, A. B., Price, N. C., Kelly, S. M., and Cooper, A. (1995) The ABA-1 allergen of the parasitic nematode Ascaris suum: fatty acid and retinoid binding function and structural characterization, Biochemistry 34, 6700-6710.
15. Narayan, M., and Berliner, L. J. (1997) Fatty acids and retinoids bind independently and simultaneously to beta-lactoglobulin, Biochemistry 36, 1906-1911.
16. Abduragimov, A. R., Gasymov, O. K., Yusifov, T. N., and Glasgow, B. J. (2000) Functional cavity dimensions of tear lipocalin, Curr. Eye Res. 21, 824-832.
17. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (2001) Site-directed tryptophan fluorescence reveals the solution structure of tear lipocalin: evidence for features that confer promiscuity in ligand binding, Biochemistry 40, 14754-14762.
18. Gasymov, O. K., Abduragimov, A. R., Gasimov, E. O., Yusifov, T. N., Dooley, A. N., and Glasgow, B. J. (2004) Tear lipocalin: potential for selective delivery of rifampin, Biochim. Biophys. Acta 1688, 102-111.
19. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (1998) Structural changes in human tear lipocalins associated with lipid binding, Biochim. Biophys. Acta 1386, 145-156.
20. Prats, M., Teissie, J., Tocanne J. F. (1986) Lateral proton conduction at lipid-water interfaces and its implications for the chemiosmotic-coupling hypothesis, Nature 322, 756-758.
21. Ragona, L., Fogolari, F., Catalano, M., Ugolini, R., Zetta, L., and Molinari, H. (2003) EF loop conformational change triggers ligand binding in beta-lactoglobulins, J. Biol. Chem. 278, 38840-38846.
22. Tanford, C. (1959) The reversible transformation of B-lactoglobulin at pH 7.5, J. Am. Chem. Soc. 81, 4032-4036.
23. Eberini, I., Baptista, A. M., Gianazza, E., Fraternali, F., and Beringhelli, T. (2004) Reorganization in apo- and holo-beta-lactoglobulin upon protonation of Glu89: molecular dynamics and pKa calculations, Proteins 54, 744-758.
24. Collini, M., D'Alfonso, L., Molinari, H., Ragona, L., Catalano, M., and Baldini, G. (2003) Competitive binding of fatty acids and the fluorescent probe 1-8-anilinonaphthalene sulfonate to bovine beta-lactoglobulin, Protein Sci. 12, 1596-1603.
25. Calderone, V., Berni, R., and Zanotti, G. (2003) High-resolution structures of retinol-binding protein in complex with retinol: pH-induced protein structural changes in the crystal state, J. Mol. Biol. 329, 841-850.
26. Clore, G. M., and Gronenborn, A. M. (1997) NMR structures of proteins and protein complexes beyond 20,000 M(r), Nat. Struct. Biol. 4 (Suppl.), 849-853.
27. Glasgow, B. J., Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., Altenbach, C., and Hubbell, W. L. (1999) Side chain mobility and ligand interactions of the G strand of tear lipocalins by site-directed spin labeling, Biochemistry 38, 13707-13716.
28. Bychkova, V. E., Berni, R., Rossi, G. L., Kutyshenko, V. P., and Ptitsyn, O. B. (1992) Retinol-binding protein is in the molten globule state at low pH, Biochemistry 31, 7566-7571.
29. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (1997) Solution structure by site directed tryptophan fluorescence in tear lipocalin, Biochem. Biophys. Res. Commun. 239, 191-196.
30. Adams, P. D., Chen, Y., Ma, K., Zagorski, M. G., Sonnichsen, F. D., McLaughlin, M. L., and Barkley, M. D. (2002) Intramolecular quenching of tryptophan fluorescence by the peptide bond in cyclic hexapeptides, J. Am. Chem. Soc. 124, 9278-9286.
31. Chen, Y., and Barkley, M. D. (1998) Toward understanding tryptophan fluorescence in proteins, Biochemistry 37, 9976-9982.
32. Glasgow, B. J., Heinzmann, C., Kojis, T., Sparkes, R. S., Mohandas, T., and Bateman, J. B. (1993) Assignment of tear lipocalin gene to human chromosome 9q34-9qter, Curr. Eye Res. 12, 1019-1023.
33. Glasgow, B. J. (1995) Tissue expression of lipocalins in human lacrimal and von Ebner's glands: colocalization with lysozyme, Graefe's Arch. Clin. Exp. Ophthalmol. 233, 513-522.
34. Cormack, B. (1987) Current Protocol in Molecular Biology, Vol. Suppl. 15, Greene Publishing Associates and Wiley-Interscience, New York.
35. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (1999) Binding studies of tear lipocalin: the role of the conserved tryptophan in maintaining structure, stability and ligand affinity, Biochim. Biophys. Acta 1433, 307-320.
36. Marston, F. A. O. (1987) A Practical Approach. In DNA Cloning, Vol. III, IRL Press, Oxford, England.
37. Bozimowski, D., Artiss, J. D., and Zak, B. (1985) The variable reagent blank: protein determination as a model, J. Clin. Chem. Clin. Biochem. 23, 683-689.
38. Cogan, U., Kopelman, M., Mokady, S., and Shinitzky, M. (1976) Binding affinities of retinol and related compounds to retinol binding proteins, Eur. J. Biochem. 65, 71-78.
39. Eftink, M. R., and Ghiron, C. A. (1976) Exposure of tryptophanyl residues in proteins. Quantitative determination by fluorescence quenching studies, Biochemistry 15, 672-680.
40. Kuppens, S., Hellings, M., Jordens, J., Verheyden, S., and Engelborghs, Y. (2003) Conformational states of the switch I region of Ha-ras-p21 in hinge residue mutants studied by fluorescence lifetime and fluorescence anisotropy measurements, Protein Sci. 12, 930-938.
41. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (2003) Resolving near-ultraviolet circular dichroism spectra of single trp mutants in tear lipocalin, Anal. Biochem. 318, 300-308.
42. Strickland, E. H. (1974) Aromatic contributions to circular dichroism spectra of proteins, CRC Crit. Rev. Biochem. 2, 113-175.
43. Vivian, J. T., and Callis, P. R. (2001) Mechanisms of tryptophan fluorescence shifts in proteins, Biophys. J. 80, 2093-2109.
44. Chen, Y. L. B., Yu, H. T., Barkley, M. D. (1996) J. Am. Chem. Soc. 118, 9271-9278.
45. Kuppens, S., Diaz, J. F., and Engelborghs, Y. (1999) Characterization of the hinges of the effector loop in the reaction pathway of the activation of ras-proteins. Kinetics of binding of beryllium trifluoride to V29G and I36G mutants of Ha-ras-p21, Protein Sci. 8, 1860-1866.