Excited protein states of human tear lipocalin for low- and high-affinity ligand binding revealed by functional AB loop motion

Biophysical Chemistry

Volumn 149, Issue 1-2, 2010, Pages 47-57

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

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JULES STEIN EYE INSTITUTE   (United States)

Author keywords

Excited protein states; FRET; Ligand binding; Protein dynamics; Tear lipocalin

Indexed keywords

GLUTAMINE; LIPOCALIN 1; LYSINE; TRYPTOPHAN;

ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; LIGAND BINDING; NONHUMAN; PH MEASUREMENT; PLASTICITY; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTON TRANSPORT; SITE DIRECTED MUTAGENESIS;

CIRCULAR DICHROISM; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; HYDROGEN-ION CONCENTRATION; LIGANDS; LIPOCALIN 1; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS;

EID: 77952672523     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2010.03.017     Document Type: Article

References (66)

1. Flower D.R. The lipocalin protein family: structure and function. Biochem. J. 1996, 318(Pt 1):1-14.
2. Gasymov O.K., Abduragimov A.R., Yusifov T.N., Glasgow B.J. Site-directed tryptophan fluorescence reveals the solution structure of tear lipocalin: evidence for features that confer promiscuity in ligand binding. Biochemistry 2001, 40:14754-14762.
3. Breustedt D.A., Korndorfer I.P., Redl B., Skerra A. The 1.8-A crystal structure of human tear lipocalin reveals an extended branched cavity with capacity for multiple ligands. J. Biol. Chem. 2005, 280:484-493.
4. Glasgow B.J., Abduragimov A.R., Farahbakhsh Z.T., Faull K.F., Hubbell W.L. Tear lipocalins bind a broad array of lipid ligands. Curr. Eye Res. 1995, 14:363-372.
5. Gasymov O.K., Abduragimov A.R., Gasimov E.O., Yusifov T.N., Dooley A.N., Glasgow B.J. Tear lipocalin: potential for selective delivery of rifampin. Biochim. Biophys. Acta 2004, 1688:102-111.
6. Gasymov O.K., Abduragimov A.R., Prasher P., Yusifov T.N., Glasgow B.J. Tear lipocalin: evidence for a scavenging function to remove lipids from the human corneal surface. Invest. Ophthalmol. Vis. Sci. 2005, 46:3589-3596.
7. Gasymov O.K., Abduragimov A.R., Yusifov T.N., Glasgow B.J. Binding studies of tear lipocalin: the role of the conserved tryptophan in maintaining structure, stability and ligand affinity. Biochim. Biophys. Acta 1999, 1433:307-320.
8. Glasgow B.J., Marshall G., Gasymov O.K., Abduragimov A.R., Yusifov T.N., Knobler C.M. Tear lipocalins: potential lipid scavengers for the corneal surface. Invest. Ophthalmol. Vis. Sci. 1999, 40:3100-3107.
9. Glasgow B.J., Gasymov O.K., Abduragimov A.R., Engle J.J., Casey R.C. Tear lipocalin captures exogenous lipid from abnormal corneal surfaces. Invest. Ophthalmol. Vis. Sci. 2009.
10. Selsted M.E., Martinez R.J. Isolation and purification of bactericides from human tears. Exp. Eye Res. 1982, 34:305-318.
11. Fluckinger M., Haas H., Merschak P., Glasgow B.J., Redl B. Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores. Antimicrob. Agents Chemother. 2004, 48:3367-3372.
12. van't Hof W., Blankenvoorde M.F., Veerman E.C., Amerongen A.V. The salivary lipocalin von Ebner's gland protein is a cysteine proteinase inhibitor. J. Biol. Chem. 1997, 272:1837-1841.
13. Blaker M., Kock K., Ahlers C., Buck F., Schmale H. Molecular cloning of human von Ebner's gland protein, a member of the lipocalin superfamily highly expressed in lingual salivary glands. Biochim. Biophys. Acta 1993, 1172:131-137.
14. Redl B., Holzfeind P., Lottspeich F. cDNA cloning and sequencing reveals human tear prealbumin to be a member of the lipophilic-ligand carrier protein superfamily. J. Biol. Chem. 1992, 267:20282-20287.
15. Lechner M., Wojnar P., Redl B. Human tear lipocalin acts as an oxidative-stress-induced scavenger of potentially harmful lipid peroxidation products in a cell culture system. Biochem. J. 2001, 356:129-135.
16. Glasgow B.J., Abduragimov A.R., Gassymov O.K., Yusifov T.N., Ruth E.C., Faull K.F. Vitamin E associated with the lipocalin fraction of human tears. Adv. Exp. Med. Biol. 2002, 506:567-572.
17. Yusifov T.N., Abduragimov A.R., Gasymov O.K., Glasgow B.J. Endonuclease activity in lipocalins. Biochem. J. 2000, 347(Pt 3):815-819.
18. Yusifov T.N., Abduragimov A.R., Narsinh K., Gasymov O.K., Glasgow B.J. Tear lipocalin is the major endonuclease in tears. Mol. Vis. 2008, 14:180-188.
19. Skerra A. Anticalins as alternative binding proteins for therapeutic use. Curr. Opin. Mol. Ther. 2007, 9:336-344.
20. Skerra A. Lipocalins as a scaffold. Biochim. Biophys. Acta 2000, 1482:337-350.
21. Schlehuber S., Skerra A. Duocalins: engineered ligand-binding proteins with dual specificity derived from the lipocalin fold. Biol. Chem. 2001, 382:1335-1342.
22. Gasymov O.K., Abduragimov A.R., Yusifov T.N., Glasgow B.J. Resolution of ligand positions by site-directed tryptophan fluorescence in tear lipocalin. Protein Sci. 2000, 9:325-331.
23. Glasgow B.J., Gasymov O.K., Abduragimov A.R., Yusifov T.N., Altenbach C., Hubbell W.L. Side chain mobility and ligand interactions of the G strand of tear lipocalins by site-directed spin labeling. Biochemistry 1999, 38:13707-13716.
24. Gasymov O.K., Abduragimov A.R., Glasgow B.J. Ligand binding site of tear lipocalin: contribution of a trigonal cluster of charged residues probed by 8-anilino-1-naphthalenesulfonic acid. Biochemistry 2008, 47:1414-1424.
25. Millar T.J., Mudgil P., Butovich I.A., Palaniappan C.K. Adsorption of human tear lipocalin to human meibomian lipid films. Invest. Ophthalmol. Vis. Sci. 2009, 50:140-151.
26. Mudgil P., Millar T.J. Adsorption of apo- and holo-tear lipocalin to a bovine Meibomian lipid film. Exp. Eye Res. 2008, 86:622-628.
27. Gasymov O.K., Abduragimov A.R., Glasgow B.J. Intracavitary ligand distribution in tear lipocalin by site-directed tryptophan fluorescence. Biochemistry 2009, 48:7219-7228.
28. Breustedt D.A., Chatwell L., Skerra A. 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. 2009, 65:1118-1125.
29. Calderone V., Berni R., Zanotti G. High-resolution structures of retinol-binding protein in complex with retinol: pH-induced protein structural changes in the crystal state. J. Mol. Biol. 2003, 329:841-850.
30. Newcomer M.E., Ong D.E. Plasma retinol binding protein: structure and function of the prototypic lipocalin. Biochim. Biophys. Acta 2000, 1482:57-64.
31. Roberts S.A., Weichsel A., Qiu Y., Shelnutt J.A., Walker F.A., Montfort W.R. Ligand-induced heme ruffling and bent no geometry in ultra-high-resolution structures of nitrophorin 4. Biochemistry 2001, 40:11327-11337.
32. Hwang P.M., Choy W.Y., Lo E.I., Chen L., Forman-Kay J.D., Raetz C.R., Prive G.G., Bishop R.E., Kay L.E. Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13560-13565.
33. Gasymov O.K., Abduragimov A.R., Glasgow B.J. Molten globule state of tear lipocalin: ANS binding restores tertiary interactions. Biochem. Biophys. Res. Commun. 2007, 357:499-504.
34. Gasymov O.K., Abduragimov A.R., Yusifov T.N., Glasgow B.J. Interstrand loops CD and EF act as pH-dependent gates to regulate fatty acid ligand binding in tear lipocalin. Biochemistry 2004, 43:12894-12904.
35. Gasymov O.K., Abduragimov A.R., Yusifov T.N., Glasgow B.J. Structural changes in human tear lipocalins associated with lipid binding. Biochim. Biophys. Acta 1998, 1386:145-156.
36. Prats M., Teissie J., Tocanne J.F. Nature 1986, 322:756-758.
37. Fogolari F., Moroni E., Wojciechowski M., Baginski M., Ragona L., Molinari H. MM/PBSA analysis of molecular dynamics simulations of bovine beta-lactoglobulin: free energy gradients in conformational transitions?. Proteins 2005, 59:91-103.
38. Gasymov O.K., Abduragimov A.R., Glasgow B.J. pH-dependent conformational changes in tear lipocalin by site-directed tryptophan fluorescence. Biochemistry 2010, 49:582-590.
39. Glasgow B.J., Heinzmann C., Kojis T., Sparkes R.S., Mohandas T., Bateman J.B. Assignment of tear lipocalin gene to human chromosome 9q34-9qter. Curr. Eye Res. 1993, 12:1019-1023.
40. Glasgow B.J. Tissue expression of lipocalins in human lacrimal and von Ebner's glands: colocalization with lysozyme. Graefes Arch. Clin. Exp. Ophthalmol. 1995, 233:513-522.
41. Cormack B. In Current Protocol in Molecular Biology 1987, Greene Pub. Associates and Wiley-Interscience, New York, N.Y.
42. Sreerama N., Woody R.W. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 2000, 287:252-260.
43. Lehrer S.S. Solute perturbation of protein fluorescence. The quenching of the tryptophyl fluorescence of model compounds and of lysozyme by iodide ion. Biochemistry 1971, 10:3254-3263.
44. Sillen A., Engelborghs Y. The correct use of "average" fluorescence parameters. Photochem. Photobiol. 1998, 67:475-486.
45. Lakowicz J.R. Principles of Fluorescence Spectroscopy 2006, Springer, New York. Third ed.
46. Kuppens S., Hellings M., Jordens J., Verheyden S., Engelborghs Y. 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. 2003, 12:930-938.
47. Förster T. Ann. Phys. 1948, 2:55-75.
48. Woody R.W. Theory of circular dichroism of proteins. Circular Dichroism and the Conformational Analysis of Biomolecules 1996, 55. Plenum Press, New York. G.D. Fasman (Ed.).
49. Chothia C. Conformation of twisted beta-pleated sheets in proteins. J. Mol. Biol. 1973, 75:295-302.
50. Pan C.P., Callis P.R., Barkley M.D. Dependence of tryptophan emission wavelength on conformation in cyclic hexapeptides. J. Phys. Chem. B 2006, 110:7009-7016.
51. Vivian J.T., Callis P.R. Mechanisms of tryptophan fluorescence shifts in proteins. Biophys. J. 2001, 80:2093-2109.
52. Engelborghs Y. The analysis of time resolved protein fluorescence in multi-tryptophan proteins. Spectrochim. Acta A Mol. Biomol. Spectrosc. 2001, 57:2255-2270.
53. Pan C.P., Barkley M.D. Conformational effects on tryptophan fluorescence in cyclic hexapeptides. Biophys. J. 2004, 86:3828-3835.
54. Chen Y., Liu B., Yu H.T., Barkley M.D. The peptide bond quenches indole fluorescence. J. Am. Chem. Soc. 1996, 118:9271-9278.
55. Glasgow B.J., Abduragimov A.R., Yusifov T.N., Gasymov O.K., Horwitz J., Hubbell W.L., Faull K.F. A conserved disulfide motif in human tear lipocalins influences ligand binding. Biochemistry 1998, 37:2215-2225.
56. Chen Y., Barkley M.D. Toward understanding tryptophan fluorescence in proteins. Biochemistry 1998, 37:9976-9982.
57. Boehr D.D., Nussinov R., Wright P.E. The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 2009, 5:789-796.
58. Hammes G.G., Chang Y.C., Oas T.G. Conformational selection or induced fit: a flux description of reaction mechanism. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13737-13741.
59. Tokuriki N., Tawfik D.S. Protein dynamism and evolvability. Science 2009, 324:203-207.
60. Weikl T.R., von Deuster C. Selected-fit versus induced-fit protein binding: kinetic differences and mutational analysis. Proteins 2009, 75:104-110.
61. Okazaki K., Takada S. Dynamic energy landscape view of coupled binding and protein conformational change: induced-fit versus population-shift mechanisms. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11182-11187.
62. Frauenfelder H., Fenimore P.W., Young R.D. Protein dynamics and function: insights from the energy landscape and solvent slaving. IUBMB Life 2007, 59:506-512.
63. Vincent F., Spinelli S., Ramoni R., Grolli S., Pelosi P., Cambillau C., Tegoni M. Complexes of porcine odorant binding protein with odorant molecules belonging to different chemical classes. J. Mol. Biol. 2000, 300:127-139.
64. Sakurai K., Konuma T., Yagi M., Goto Y. Structural dynamics and folding of beta-lactoglobulin probed by heteronuclear NMR. Biochim. Biophys. Acta 2009, 1790:527-537.
65. Ragona L., Fogolari F., Catalano M., Ugolini R., Zetta L., Molinari H. EF loop conformational change triggers ligand binding in beta-lactoglobulins. J. Biol. Chem. 2003, 278:38840-38846.
66. Bosshard H.R. Molecular recognition by induced fit: how fit is the concept?. News Physiol. Sci. 2001, 16:171-173.