Specificity determinants for lipids bound to β-barrel proteins

Journal of Lipid Research

Volumn 45, Issue 2, 2004, Pages 232-243

  Reese, Amy J ^a   Banaszak, Leonard J ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Adipocyte lipid binding protein; Ligand binding; Oleic acid; Protein ligand interaction; Retinoic acid

Indexed keywords

ADIPOCYTE LIPID BINDING PROTEIN; CELLULAR RETINOIC ACID BINDING PROTEIN I; FATTY ACID; FATTY ACID BINDING PROTEIN; LIPID; LIPID BINDING PROTEIN; MUTANT PROTEIN; OLEIC ACID; RETINOID BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ELECTRON; LIGAND BINDING; LIPID TRANSPORT; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LIPID INTERACTION; PROTEIN STABILITY;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CARRIER PROTEINS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; FATTY ACID-BINDING PROTEINS; LIGANDS; MICE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, RETINOIC ACID; RECOMBINANT PROTEINS; SENSITIVITY AND SPECIFICITY; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 1242274646     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M300113-JLR200     Document Type: Article

References (60)

1. Xu, Z., D. A. Bernlohr, and L. J. Banaszak. 1993. The adipocyte lipid-binding protein at 1.6-A resolution. Crystal structures of the apoprotein and with bound saturated and unsaturated fatty acids. J. Biol. Chem. 268: 7874-7884.
2. Kleywegt, G. J., T. Bergors, H. Senn, P. Le Motte, B. Gsell, K. Shudo, and T. A. Jones. 1994. Crystal structures of cellular retinoic acid binding proteins I and II in complex with all-trans-retinoic acid and a synthetic retinoid. Structure. 2: 1241-1258.
3. Banaszak, L., N. Winter, X. Xu, D. A. Bernlohr, S. Cowan, and A. T. Jones. 1994. Lipid-binding proteins: a family of fatty acid and retinoid transport proteins. Adv. Protein Chem. 45: 89-151.
4. Lucke, C., S. Huang, M. Rademacher, and H. Ruterjans. 2002. New insights into intracellular lipid binding proteins: the role of buried water. Protein Sci. 11: 2382-2392.
5. Woolf, T. B. 1997. Molecular dynamics of individual alpha-helices of bacteriorhodopsin in dimyristol phosphatidylcholine. I. Structure and dynamics. Biophys. J. 73: 2376-2392.
6. Lucke, C., D. Fushman, C. Ludwig, J. A. Hamilton, J. C. Sacchettini, and H. Ruterjans. 1997. A comparative study of the backbone dynamics of two closely related lipid binding proteins: bovine heart fatty acid binding protein and porcine ileal fatty acid binding protein. Third Int. Conf. Lipid-Binding Proteins. 14: 1-16.
7. Likic, V. A., and F. G. Prendergast. 2001. Dynamics of internal water in fatty acid binding protein: computer simulations and comparison with experiments. Proteins. 43: 65-72.
8. Krishnan, V. V. 2000. Dynamics of cellular retinoic acid binding protein I on multiple time scales with implications for ligand binding. Biochemistry. 39: 19-29.
9. Constantine, K. L., M. S. Friedrichs, M. Wittekind, H. Jamil, C. H. Chu, R. A. Parker, V. Goldfarb, L. Mueller, and B. T. Farmer II. 1998. Backbone and side chain dynamics of uncomplexed human adipocyte and muscle fatty acid-binding proteins. Biochemistry. 37: 7965-7980.
10. Richieri, G. V., P. J. Low, R. T. Ogata, and A. M. Kleinfeld. 1997. Mutants of rat intestinal fatty acid-binding protein illustrate the critical role played by enthalpy-entropy compensation in ligand binding. J. Biol. Chem. 272: 16737-16740.
11. Richieri, G. V., R. T. Ogata, and A. M. Kleinfeld. 1996. Thermodynamic and kinetic properties of fatty acid interactions with rat liver fatty acid-binding protein. J. Biol. Chem. 271: 31068-31074.
12. Richieri, G. V., P. J. Low, R. T. Ogata, and A. M. Kleinfeld. 1998. Thermodynamics of fatty acid binding to engineered mutants of the adipocyte and intestinal fatty acid-binding proteins. J. BioL Chem. 273: 7397-7405.
13. Kane, C. D., and D. A. Bernlohr. 1996. A simple assay for intracellular lipid-binding proteins using displacement of 1-anilinonaphthalene 8-sulfonic acid. Anal. Biochem. 233: 197-204.
14. Zhang, J., Z. P. Liu, T. A. Jones, L. M. Gierasch, and J. F. Sambrook. 1992. Mutating the charged residues in the binding pocket of cellular retinoic acid-binding protein simultaneously reduces its binding affinity to retinoic acid and increases its thermostability. Proteins. 13: 87-99.
15. Richieri, G. V., R. T. Ogata, and A. M. Kleinfeld. 1995. Thermodynamics of fatty acid binding to fatty acid-binding proteins and fatty acid partition between water and membranes measured using the fluorescent probe ADIFAB. J. Biol. Chem. 270: 15076-15084.
16. Kunkel, T. A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA. 82: 488-492.
17. Ory, J., C. D. Kane, M. A. Simpson, L.J. Banaszak, and D. A. Bernlohr. 1997. Biochemical and crystallographic analyses of a portal mutant of the adipocyte lipid-binding protein. J. Biol. Chem. 272: 9793-9801.
18. Rosenberg, A. H., B. N. Lade, D. Chui, S-W. Lin, J.J. Dunn, and F. W. Studier. 1987. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene. 56: 125-135.
19. Schoepfer, R. 1993. The pRSET family of T7 promoter expression vectors for Escherichia coli. Gene. 124: 83-85.
20. Johnson, B. H., and M. H. Hecht. 1994. Recombinant proteins can be isolated from E. coli cells by repeated cycles of freezing and thawing. Bio/Technology. 12: 1357-1360.
21. Thompson, J. R., J. M. Bratt, and L. J. Banaszak. 1995. Crystal structure of cellular retinoic acid binding protein I shows increased access to the binding cavity due to formation of an intermolecular beta-sheet. J. Mol. Biol. 252: 433-446.
22. Xu, Z. H., M. K. Buelt, L. J. Banaszak, and D. A. Bernlohr. 1991. Expression, purification, and crystallization of the adipocyte lipid binding protein. J. Biol. Chem. 266: 14367-14370.
23. Glatz, J. F. C., and J. H. Veerkamp. 1983. A radiochemical procedure for the assay of fatty acid binding by proteins. Anal. Biochem. 132: 89-95.
24. Glatz, J. F., and J. H. Veerkamp. 1983. Removal of fatty acids from serum albumin by Lipidex 1000 chromatography. J. Biochem. Biophys. Methods. 8: 57-61.
25. LaLonde, J. M., D. A. Bernlohr, and L. J. Banaszak. 1994. X-ray crystallographic structures of adipocyte lipid-binding protein complexed with palmitate and hexadecanesulfonic acid. Properties of cavity binding sites. Biochemistry. 33: 4885-4895.
26. LaLonde, J. M., M. A. Levenson, J. J. Roe, D. A. Bernlohr, and L. J. Banaszak. 1994. Adipocyte lipid-binding protein complexed with arachidonic acid. Titration calorimetry and X-ray crystallographic studies. J. Biol. Chem. 269: 25339-25347.
27. Carter, C. W., Jr., and C. W. Carter. 1979. Protein crystallization using incomplete factorial experiments. J. Biol. Chem. 254: 12219-12223.
28. Howard, A. J., G. L. Gilliland, B. C. Finzel, T. L. Poulos, D. H. Ohlendorf, and F. R. Salemme. 1987. The use of imaging proportional counter in macromolecular crystallography. J. Appl. Crystallogr. 20: 383-387.
29. Rigaku. (1998) Crystal Clear. Version 1.2.2. Rigaku/MSC, The Woodlands, TX.
30. Brünger, A. (1990) X-PLOR: A System for Crystallography and NMR. Version 3.1. Yale University Press, New Haven, CT.
31. Brünger, A. T., P. Adams, M. Clore, P. Gros, M. Nilges, and R. Read. 1998. Crystallography and NMR system. Acta Crystallogr. D54: 905-921.
32. Jones, T. A., J. Y. You, S. W. Cowan, and M. Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogy. A47: 110-119.
33. Kleywegt, G.J., and T. A. Jones. 1996. xdlMAPMAN and xdlDATAMAN - programs for reformatting, analysis and manipulation of biomacromolecular electron-density maps and reflection data sets. Acta Crystallogr D52: 826-828.
34. Brünger, A. T. 1992. The free R value: a novel statistical quantity for assessing the accuracy of crystal structurcs. Nature. 355: 472-474.
35. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stcrcochemical stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
36. Liang, J., H. Edelsbrunner, and C. Woodward. 1998. Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design. Protein Sci. 7: 1884-1897.
37. Buelt, M. K., Z. Xu, L. J. Banaszak, and D. A. Bernlohr. 1992. Structural and functional characterization of the phosphorylated adipocyte lipid-binding protein (pp15). Biochemistry. 31: 3493-3499.
38. Prinsen, C. F., and J. H. Veerkamp. 1996. Fatty acid binding and conformational stability of mutants of human muscle fatty acid-binding protein. Biochem. J. 314: 253-260.
39. Kirk, W. R., E. Kurian, and F. G. Prendergast. 1996. Characterization of the sources of protein-ligand affinity: 1-sulfonato-8-(1′ )anilinonaphthalene binding to intestinal fatty acid binding protein. Biophys. J. 70: 69-83.
40. Ong, D., and F. Chytil. 1978. Cellular retinoic acid-binding protein from rat testis: purification and characterization. J. Biol. Chem. 253: 4551-4554.
41. Synergy Software. (2000) KaleidaGraph: Data Analysis and Graphic Presentation for Business, Science and Engineering. Version 3,5. Synergy Software, Reading, PA.
42. Simpson, M. A., and D. A. Bernlohr. 1998. Analysis of a series of phenylalanine 57 mutants of the adipocyte lipid-binding protein. Biochemistry. 37: 10980-10986.
43. Epps, D. E., T. J. Raub, and F.J. Kedzy. 1995. A general, wide-range spectrofluorometric method for measuring the site-specific affinities of drugs toward human serum albumin. Anal. Biochem. 227: 342-350.
44. MicroCal. 1993. ORIGIN. Version 2.9. MicroCal, Northampton, MA.
45. Brünger, A. T. 1990. Rigid body refinement reference. Acta Crystallogr A46: 46-57.
46. Brünger, A. T. 1988. Crystallographic refinement by simulated annealing. Application to a 2.8 A resolution structure of aspartate aminotransferase. J. Mol. Biol. 203: 803-816.
47. Jiang, J. S., and A. T. Brünger. 1994. Protein hydration observed by X-ray diffraction. Solvation properties of penicillopepsin and neuraminidase crystal structures. J. Mol. Biol. 243: 100-115.
48. Xu, Z., D. A. Bernlohr, and L. J. Banaszak. 1992. Crystal structure of recombinant murine adipocyte lipid-binding protein. Biochemistry. 31: 3484-3492.
49. Ory, J. J., and L. J. Banaszak. 1999. Studies of the ligand binding reaction of adipocyte lipid binding protein using the fluorescent probe 1,8-anilinonaphthalene-8-sulfonate. Biophys. J. 77: 1107-1116.
50. Predki, P. F., V. Agrawal, A. T. Brunger, and L. Regan. 1996. Amino-acid substitutions in a surface turn modulate protein stability. Nat. Struct. Biol. 3: 54-58.
51. Lee, A. Y., P. Zhang, J. Clardy, B. Ganem, J. W. Erickson, and D. Xie. 1998. Thermodynamics of a transition state analogue inhibitor binding to Escherichia coli chorismate mutase: probing the charge state of an active site residue and its role in inhibitor binding and catalysis. Biochemistry. 37: 9052-9057.
52. Mandiyan, V., R. O'Brien, M. Zhou, B. Margolis, M. A. Lemmon, J. M. Sturtevant, and J. Schlessinger. 1996. Thermodynamic studies of SHC phosphotyrosine interaction domain recognition of the NPXpY motif. J. Biol. Chem. 271: 4770-4775.
53. Reddy, S. G., G. Scapin, and J. S. Blanchard. 1996. Interaction of pyridine nucleotide substrates with Escherichia coli dihydrodipicolinate reductase: thermodynamic and structural analysis of binary complexes. Biochemistry. 35: 13294-13302.
54. Balendiran, G. K., F. Schnütgen, G. Scapin, T. Börchers, N. Xhong, K. Lim, R. Godbout, F. Spener, and J. C. Sacchittini. 2000. Crystal structure and thermodynamic analysis of human brain fatty acid-binding protein. J. Biol. Chem. 275: 27045-27054.
55. LiCata, V. J., and D. A. Bernlohr. 1998. Surface properties of adipocyte lipid-binding protein: response to lipid binding, and comparison with homologous proteins. Proteins. 33: 577-589.
56. Bernlohr, D. A., C. W. Angus, M. D. Lane, M. A. Bolanowski, and T. J. Kelly, Jr. 1984. Expression of specific mRNAs during adipose differentiation: identification of an mRNA encoding a homologue of myelin P2 protein. Proc. Natl. Acad. Sci. USA. 81: 5468-5472.
57. Stoner, C. M., and L. J. Gudas. 1989. Mouse cellular retinoic acid binding protein: cloning, complementary DNA sequence, and messenger RNA expression during the retinoic acid-induced differentiation of F9 wild type and RA-3-10 mutant teratocarcinoma cells. Cancer Res. 49: 1497-1504.
58. Evans, S. V. 1993. SETOR: hardware-lighted three-dimensional solid model representations of macro-molecules. J. Mol. Graph. 11: 134-138.
59. Christopher, J. A. 1997. SPOCK. Texas A&M Center for Macromolecular Design, College Station, TX.
60. Wallace, A. C., R. A. Laskowski, and J. M. Thornton. 1995. LIG-PLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8: 127-134.