The conserved disulfide bond of human tear lipocalin modulates conformation and lipid binding in a ligand selective manner

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 5, 2011, Pages 671-683

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

^a JULES STEIN EYE INSTITUTE   (United States)

Author keywords

Disulfide motive; FRET; Ligand binding; Lipocalin 1; Protein dynamic; Tear lipocalin; Time resolved fluorescence

Indexed keywords

CHOLESTEROL; LIPOCALIN; PALMITIC ACID; DISULFIDE; LIGAND; LIPOCALIN 1;

ARTICLE; CIRCULAR DICHROISM; DISULFIDE BOND; FLUORESCENCE SPECTROSCOPY; KINETICS; LACRIMAL FLUID; LIGAND BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE; CHEMISTRY; ELECTRON SPIN RESONANCE; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; SPECTROFLUOROMETRY;

CIRCULAR DICHROISM; DISULFIDES; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; LIGANDS; LIPOCALIN 1; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SPECTROMETRY, FLUORESCENCE;

EID: 79960659887     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.03.017     Document Type: Article

References (65)

1. O.K. Gasymov, A.R. Abduragimov, T.N. Yusifov, B.J. Glasgow, Site-directed tryptophan fluorescence reveals the solution structure of tear lipocalin: evidence for features that confer promiscuity in ligand binding, Biochemistry 40 (2001) 14754-14762. (Pubitemid 33136095)
2. D.A. Breustedt, LP. Korndorfer, B. Redi, A. Skerra, The 1.8-A crystal structure of human tear lipocalin reveals an extended branched cavity with capacity for multiple ligands, J. Biol. Chem. 280 (2005) 484-493. (Pubitemid 40165013)
3. B.J. Glasgow, C. Marshall, O.K. Gasymov, A.R. Abduragimov, T.N. Yusifov, C.M. Knobler, Tear lipocalins: potential lipid scavengers for the corneal surface, Invest. Ophthalmol. Vis. Sci. 40 (1999) 3100-3107.
4. M.E. Selsted, R.J. Martinez, Isolation and purification of bactericides from human tears, Exp. Eye Res. 34 (1982) 305-318. (Pubitemid 12138160)
5. ] M. Fluckinger, H. Haas, P. Merschak, B.J. Glasgow, B. Redi, Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores, Antimicrob. Agents Chemother. 48 (2004) 3367-3372. (Pubitemid 39129332)
6. W. van't Hof, M.F. Blankenvoorde, E.C. Veerman, A.V. Amerongen, The salivary lipocalin von Ebner's gland protein is a cysteine proteinase inhibitor, J. Biol. Chem. (1997) 1837-1841.
7. ] M. Blaker, K. Kock, C. Ahlers, F. Buck, H. Schmale, 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 (1993) 131-137. (Pubitemid 23065789)
8. ] B. Redi, P. Holzfeind, F. Lottspeich, cDNA cloning and sequencing reveals human tear prealbumin to be a member of the lipophilic-ligand carrier protein superfamily, J. Biol. Chem. 267 (1992) 20282-20287.
9. M. Lechner, P. Wojnar, B. Redi, Human tear lipocalin acts as an oxidative-stressinduced scavenger of potentially harmful lipid peroxidation products in a cell culture system, Biochem. J. 356 (2001) 129-135. (Pubitemid 34275714)
10. BJ. Glasgow, A.R. Abduragimov, O.K. Gassymov, T.N. Yusifov, E.C. Ruth, K.F. Faull, Vitamin E associated with the lipocalin fraction of human tears, Adv. Exp. Med. Biol. 506 (2002) 567-572. (Pubitemid 36307721)
11. T.N. Yusifov, A.R. Abduragimov, O.K. Gasymov, B.J. Glasgow, Endonuclease activity in lipocalins, Biochem. J. 347 (Pt 3) (2000) 815-819. (Pubitemid 30260973)
12. B.J. Glasgow, A.R. Abduragimov, Z.T. Farahbakhsh, K.F. Faull, W.L. Hubbell, Tear lipocalins bind a broad array of lipid ligands, Curr. Eye Res. 14 (1995) 363-372.
13. O.K. Gasymov, A.R. Abduragimov, E.O. Gasimov, T.N. Yusifov, A.N. Dooley, B.J. Glasgow, Tear lipocalin: potential for selective delivery of rifampin, Biochim. Biophys. Acta 1688 (2004) 102-111. (Pubitemid 38264404)
14. O.K. Gasymov, A.R. Abduragimov, P. Prasher, T.N. Yusifov, B.J. Glasgow, Tear lipocalin: evidence for a scavenging function to remove lipids from the human corneal surface, Invest. Ophthalmol. Vis. Sci. 46 (2005) 3589-3596. (Pubitemid 44264661)
15. O.K. Gasymov, A.R. Abduragimov, T.N. Yusifov, B.J. Glasgow, Binding studies of tear lipocalin: the role of the conserved tryptophan in maintaining structure, stability and ligand affinity, Biochim. Biophys. Acta 1433 (1999) 307-320. (Pubitemid 29369065)
16. O.K. Gasymov, A.R. Abduragimov, B.J. Glasgow, Ligand binding site of tear lipocalin: contribution of a trigonal cluster of charged residues probed by 8anilino-1-naphthalenesulfonic acid, Biochemistry 47 (2008) 1414-1424.
17. T.J. Millar, P. Mudgil, L.A. Butovich, C.K. Palaniappan, Adsorption of human tear lipocalin to human meibomian lipid films, Invest. Ophthalmol. Vis. Sci. 50 (2009) 140-151.
18. B. Nagyova, J.M. Tiffany, Components responsible for the surface tension of human tears, Curr. Eye Res. 19 (1999) 4-11. (Pubitemid 29308823)
19. O.K. Gasymov, A.R. Abduragimov, B.J. Glasgow, Intracavitary ligand distribution in tear lipocalin by site-directed tryptophan fluorescence, Biochemistry 48 (2009) 7219-7228.
20. D.A. Breustedt, L Chatwell, A. Skerra, A new crystal form of human tear lipocalin reveals high flexibility in the loop region and induced fit in the ligand cavity, Acta Crystallogr. D Biol. Crystallogr. 65 (2009) 1118-1125.
21. O.K. Gasymov, A.R. Abduragimov, B.J. Glasgow, pH-dependent conformational changes in tear lipocalin by site-directed tryptophan fluorescence, Biochemistry 49 (2010) 582-590.
22. B.J. Glasgow, A.R. Abduragimov, T.N. Yusifov, O.K. Gasymov, J. Horwitz, W.L. Hubbell, K.F. Faull, A conserved disulfide motif in human tear lipocalins influences ligand binding, Biochemistry 37 (1998) 2215-2225. (Pubitemid 28119294)
23. B. Redi, P. Merschak, B. Abt, P. Wojnar, Phage display reveals a novel interaction of human tear lipocalin and thioredoxin which is relevant for ligand binding, FEBS Lett. 460 (1999) 182-186. (Pubitemid 29479267)
24. B.J. Glasgow, C Heinzmann, T. Kojis, R.S. Sparkes, T. Mohandas, J.B. Bateman, Assignment of tear lipocalin gene to human chromosome 9q34-9qter, Curr. Eye Res. 12 (1993) 1019-1023. (Pubitemid 23348313)
25. B.J. Glasgow, Tissue expression of lipocalins in human lacrimal and von Ebner's glands: colocalization with lysozyme, Graefes Arch. Clin. Exp. Ophthalmol. 233 (1995) 513-522.
26. B. Cormack, In Current Protocol in Molecular Biology, Greene Pub. Associates and Wiley- Interscience, New York, N.Y., 1987.
27. B.J. Glasgow, O.K. Gasymov, A.R. Abduragimov, T.N. Yusifov, C Altenbach, W.L. Hubbell, Side chain mobility and ligand interactions of the C strand of tear lipocalins by site-directed spin labeling, Biochemistry 38 (1999) 13707-13716.
28. O.K. Gasymov, A.R. Abduragimov, T.N. Yusifov, B.J. Glasgow, Interstrand loops CD and EF act as pH-dependent gates to regulate fatty acid ligand binding in tear lipocalin, Biochemistry 43 (2004) 12894-12904. (Pubitemid 39331809)
29. F.A.O. Marston, The Purification of Eukaryotic Polypeptides Expresses in Escherichia coli, in: D.M. Glover (Ed.), DNA Cloning: A Practical Approach, Vol. Ill, Chap. 4, IRL Press, Oxford, England, 1987, pp. 59-88.
30. D. Bozimowski, J.D. Artiss, B. Zak, The variable reagent blank: protein determination as a model, J. Clin. Chem. Clin. Biochem. 23 (1985) 683-689. (Pubitemid 16242100)
31. G.L. Peterson, A simplification of the protein assay method of Lowry et al. which is more generally applicable, Anal. Biochem. 83 (1977) 346-356. (Pubitemid 8269786)
32. S.S. Lehrer, Solute perturbation of protein fluorescence. The quenching of the tryptophyl fluorescence of model compounds and of lysozyme by iodide ion, Biochemistry 10 (1971) 3254-3263.
33. L Tcatchoff, C Nespoulous, J.C. Pernollet, L Briand, A single lysyl residue defines the binding specificity of a human odorant-binding protein for aldehydes, FEBS Lett. 580 (2006) 2102-2108.
34. J.R. Lakowicz, Principles of Fluorescence Spectroscopy, Springer, New York, 2006, p. 166.
35. A. Sillen, Y. Engelborghs, The correct use of "average" fluorescence parameters, Photochem. Photobiol. 67 (1998) 475-486.
36. J.R. Lakowicz, Principles of Fluorescence Spectroscopy, Third ed. Springer, New York, 2006.
37. M.R Eftink, C.A. Chiron, Exposure of tryptophanyl residues in proteins. Quantitative determination by fluorescence quenching studies, Biochemistry 15 (1976) 672-680
38. T. Förster, Intermolecular energy migration and fluorescence, Ann. Phys. 2 (1948) 55-75.
39. M.M. Santoro, D.W. Bolen, Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alphachymotrypsin using different denaturants, Biochemistry 27 (1988) 8063-8068.
40. S. Tsukamoto, K. Fujiwara, M. Ikeguchi, Fatty acids bound to recombinant tear lipocalin and their role in structural stabilization, J. Biochem. 146 (2009) 343-350.
41. O.K. Gasymov, A.R. Abduragimov, P. Merschak, B. Redi, B.J. Glasgow, Oligomeric state of lipocalin-1 (LCNl) by multiangle laser light scattering and fluorescence anisotropy decay, Biochim. Biophys. Acta 1774 (2007) 1307-1315. (Pubitemid 47484294)
42. O.K. Gasymov, A.R. Abduragimov, T.N. Yusifov, B.J. Glasgow, Structural changes in human tear lipocalins associated with lipid binding, Biochim. Biophys. Acta 1386 (1998) 145-156. (Pubitemid 29333226)
43. D.A. Breustedt, D.L. Schonfeld, A. Skerra, Comparative ligand-binding analysis of ten human lipocalins, Biochim. Biophys. Acta 1764 (2006) 161-173.
44. O.K. Gasymov, A.R. Abduragimov, T.N. Yusifov, B.J. Glasgow, Relaxation of betastructure in tear lipocalin and enhancement of retinoid binding, Invest. Ophthalmol. Vis. Sci. 43 (2002) 3165-3173.
45. S.C. Gill, P.H. von Hippel, Calculation of protein extinction coefficients from amino acid sequence data, Anal. Biochem. 182 (1989) 319-326. (Pubitemid 19277112)
46. S. Tsukamoto, T. Yamashita, Y. Yamada, K. Fujiwara, K. Maki, K. Kuwajima, Y. Matsumura, H. Kihara, H. Tsuge, M. Ikeguchi, Non-native alpha-helix formation is not necessary for folding of lipocalin: comparison of burst-phase folding between tear lipocalin and beta-lactoglobulin, Proteins 76 (2009) 226-236.
47. C.N. Pace, F. Vajdos, L Fee, G. Grimsley, T. Gray, How to measure and predict the molar absorption coefficient of a protein, Protein Sci. 4 (1995) 2411-2423.
48. E.H. Strickland, Aromatic contributions to circular dichroism spectra of proteins, CRC Crit. Rev. Biochem. 2 (1974) 113-175.
49. J. Horwitz, E.H. Strickland, C Billups, Analysis of the vibrational structure in the near-ultraviolet circular dichroism and absorption spectra of tyrosine derivatives and ribonuclease-A at 77°K, J. Am. Chem. Soc. 92 (1970) 2119-2129.
50. O.K. Gasymov, A.R. Abduragimov, B.J. Glasgow, Site-directed circular dichroism of proteins: ILb bands of Trp resolve position-specific features in tear lipocalin, Anal. Biochem. 374 (2008) 386-395.
51. Y. Chen, M.D. Barkley, Toward understanding tryptophan fluorescence in proteins, Biochemistry 37 (1998) 9976-9982. (Pubitemid 28366351)
52. Y. Chen, B. Liu, H.T. Yu, M.D. Barkley, The peptide bond quenches indole fluorescence, J. Am. Chem. Soc. 118 (1996) 9271-9278. (Pubitemid 26355121)
53. J.K. Myers, C.N. Pace, J.M. Scholtz, Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding, Protein Sci. 4 (1995)2138-2148.
54. D. Shortle, Staphylococcal nuclease: a showcase of m-value effects, Adv. Protein Chem. 46 (1995) 217-247.
55. D.C. Wilton, The fatty acid analogue 11(dansylamino)undecanoic acid is a fluorescent probe for the bilirubin-binding sites of albumin and not for the highaffinity fatty acid-binding sites, Biochem. J. 270 (1990) 163-166. (Pubitemid 20275591)
56. Y. Yamada, K. Nakagawa, T. Yajima, K. Saito, A. Tokushima, K. Fujiwara, M. Ikeguchi, Structural and thermodynamic consequences of removal of a conserved disulfide bond from equine beta-lactoglobulin, Proteins 63 (2006) 595-602.
57. J. Liu, C Guo, Y. Yao, D. Lin, Effects of removing a conserved disulfide bond on the biological characteristics of rat lipocalin-type prostaglandin D synthase, Biochimie 90 (2008) 1637-1646.
58. M. Parisi, A. Mazzini, R. Tibor Sorbi, R. Ramoni, S. Grolli, R. Favilla, Role of the disulphide bridge in folding, stability and function of porcine odorant binding protein: spectroscopic equilibrium studies on C63A/C155A double mutant, Biochim. Biophys. Acta 1750 (2005) 30-39. (Pubitemid 40797724)
59. G. del VaI, B.C. Yee, R.M. Lozano, B.B. Buchanan, R.W. Ermel, Y.M. Lee, O.L. Frick, Thioredoxin treatment increases digestibility and lowers allergenicity of milk, J. Allergy Clin. Immunol. 103 (1999) 690-697.
60. F. Scalfari, M. Castagna, B. Fattori, I. Andreini, C Maremmani, P. Pelosi, Expression of a lipocalin in human nasal mucosa, Comp. Biochem. Physiol. 118B (1997) 819-824. (Pubitemid 28088028)
61. ] E. Lacazette, A.M. Gachon, G. Pitiot, A novel human odorant-binding protein gene family resulting from genomic duplicons at 9q34: differential expression in the oral and genital spheres, Hum. Mol. Genet. 9 (2000) 289-301. (Pubitemid 30052753)
62. B. Redi, Human tear lipocalin, Biochim. Biophys. Acta 1482 (2000) 241-248. [63] P. Wojnar, S. Dirnhofer, P. Ladurner, P. Berger, B. Redi, Human lipocalin-1, a physiological scavenger of lipophilic compounds, is produced by corticotrophs of the pituitary gland, J. Histochem. Cytochem. 50 (2002) 433-435.
63. P.A. Jordan, J.M. Gibbins, Extracellular disulfide exchange and the regulation of cellular function, Antioxid. Redox Signal. 8 (2006) 312-324. (Pubitemid 43741302)
64. U. Schwertassek,Y. Balmer, M.Gutscher,LWeingarten,M. Preuss.J. Engelhard,M. Winkler, T.P. Dick, Selective redox regulation of cytokine receptor signaling by extracellular thioredoxin-1, EMBO J. 26 (2007) 3086-3097. (Pubitemid 47057486)
65. C Sotozono, S. Ermis, K. Yamasaki, H. Nakamura,J. Yodoi, S.S. Kinoshita, Thioredoxin in human tears, Invest. Ophthalmol. Vis. Sci. 46 (2005) E-Abstract 2818.