Schistosoma mansoni fatty acid binding protein: Specificity and functional control as revealed by crystallographic structure

Biochemistry

Volumn 43, Issue 41, 2004, Pages 13000-13011

  Angelucci, Francesco ^a   Johnson, Kenneth A ^a   Baiocco, Paola ^a   Miele, Adriana E ^a   Brunori, Maurizio ^a   Valle, Cristiana ^b   Vigorosi, Fabio ^b   Troiani, Anna Rita ^b   Liberti, Piero ^b   Cioli, Donato ^b   Klinkert, Mo Quen ^c   Bellelli, Andrea ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Institute of Cell Biology   (Italy)

^c BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTALLIZATION; DATA REDUCTION; DISSOCIATION; FATTY ACIDS; HYDROCARBONS; NUTRITION; OPTIMIZATION; RATE CONSTANTS;

ARACHIDONIC ACIDS (ACD); MONITORING DISPLACEMENTS; OLEIC ACIDS (OLA); SCHISTOSOMIASIS;

PROTEINS;

8 ANILINO 1 NAPHTHALENESULFONIC ACID; ARACHIDONIC ACID; ARGININE; CATION; FATTY ACID; FATTY ACID BINDING PROTEIN; HYDROCARBON; LIGAND; OLEIC ACID; PROSTAGLANDIN; PROTEIN SM14; UNCLASSIFIED DRUG; VACCINE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL BOND; CONFORMATION; CONTROLLED STUDY; CRYSTALLIZATION; CRYSTALLOGRAPHY; DISSOCIATION; EXPERIMENT; FATTY ACID SYNTHESIS; FLOW KINETICS; HOST; IMMUNITY; LIGAND BINDING; MEASUREMENT; MONITORING; NONHUMAN; NUTRIENT; PARASITOSIS; PH; PREVALENCE; PRIORITY JOURNAL; PROCESS CONTROL; PROSTAGLANDIN SYNTHESIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; SCHISTOSOMA; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS;

ANIMALS; ARACHIDONIC ACID; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; EPITOPES; FATTY ACID-BINDING PROTEINS; HELMINTH PROTEINS; KINETICS; LIGANDS; MACROMOLECULAR SUBSTANCES; MICE; OLEIC ACID; PROTEIN BINDING; SCHISTOSOMA MANSONI; SPECIES SPECIFICITY; VACCINES, SUBUNIT;

SCHISTOSOMA; SCHISTOSOMA MANSONI; TREMATODA;

EID: 5444234023     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048505f     Document Type: Article

References (46)

1. Brouwers, J. F., Smeenk, I. M., van Golde, L. M., and Tielens, A. G. (1997) The incorporation, modification and turnover of fatty acids in adult Schistosoma mansoni, Mol. Biochem. Parasitol. 88, 175-185.
2. Furlong S. T., and Caulfield J. P. (1989) Schistosoma mansoni: synthesis and release of phospholipids, lysophospholipids, and neutral lipids by schistosomula, Exp. Parasitol. 69, 65-67.
3. McKerrow, J., and Salter, J. (2002) Invasion of skin by schistosoma cercariae, Trends Parasitol. 18, 193-195.
4. Moser, D., Tendler, M., Griffiths, G., and Klinkert, M.-Q. (1991) A 14-kDa Schistosoma mansoni polypeptide is homologous to a gene family of fatty acid binding proteins, J. Biol. Chem. 266, 8447-8454.
5. Brito, C. F., Oliveira, G. C., Oliveira. S. C., Street, M., Riengrojpitak, S., Wilson, R. A., Simpson, A. J., and Correa-Oliveira, R. (2002) Sm14 gene expression in different stages of the Schistosoma mansoni life cycle and immunolocalization of the Sm14 protein within the adult worm, Braz. J. Med. Biol. Res. 35, 377-81.
6. Tendler, M., Brito, C. A., Vilar, M. M., Serra-Freire, N., Diogo, C. M., Almeida, M. S., Delbem, A. C., Da Silva, J. F., Savino, W., Garratt, R. C., Katz, N., and Simpson, A. S. (1996) A Schistosoma mansoni fatty acid-binding protein, Sm14, is the potential basis of a dual-purpose anti-helminth vaccine, Proc. Natl. Acad. Sci. U.S.A. 93, 269-73.
7. Bergquist, N. R., and Colley, D. G. (1998) Schistosomiasis Vaccines: Research to development, Parasitol. Today 14, 99-104.
8. Ferrari, M. L. A., Coelho, P. M. Z., Antunes, C. M. F., Tavares, C. A. P., and da Cunha, A. S. (2003) Efficacy of oxamniquine and praziquantel in the treatment of Schistosoma mansoni infection: a controlled trial, Bull. W.H.O. 83, 190-196.
9. Storch, J., and Thumser, A. E. (2000) The fatty acid transport function of fatty acid binding proteins, Biochim. Biophys. Acta 1486, 28-44.
10. Veerkamp, J. H, Peeters, R. A., and Maatman, R. G. (1991) Structural and functional features of different types of cytoplasmatic fatty acid-binding proteins, Biochim. Biophys. Acta 1081, 1-24.
11. Weisiger, R. A. (2002) Cytosolic fatty acid binding proteins catalyze two distinct steps in intracellular transport of their ligands, Mol. Cell. Biochem. 239, 35-42.
12. Kaikaus, R. M., Bass, N. M., and Okner R. K. (1990) Functions of fatty acid binding protein, Experientia 46, 617-630
13. Murphy, E. J., Barcelo-Coblijn, G., Binas, B., and Glatz, J. F. (2004) Heart fatty acid uptake is decreased in heart-fatty acid binding protein gene-ablated mice, J. Biol. Chem. 279, 34481-34488.
14. Richieri, G. V., Ogata, R. T., Zimmerman, A. W., Veerkamp, J. H., and Kleinfeld, A. M. (2000) Fatty acid binding proteins from different tissues show distinct pattern of fatty acid interactions, Biochemistry 39, 7197-7204.
15. Rumjanek, F. D., and Simpson, A. J. (1980) The incorporation and utilization of radiolabelled lipids by adult Schistosoma mansoni, Mol. Biochem. Parasitol. 1, 31-44.
16. 2 in the inhibition of epidermal Langherans cell migration during schistosomiasis infection, J. Exp. Med. 193, 1135-1147.
17. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
18. Otwinowsky, S., and Minor, W. (1996) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-325.
19. Matthews, B. W. (1968) Solvent content of protein crystals, J. Mol. Biol. 33, 491-497.
20. Navaza, J. (2001) AmoRe: an automated package for molecular replacement, Acta Crystallogr. D57, 1367-1372.
21. Collaborative Computational Project, Number 4 (1994) Acta Crystallogr. D50, 760-763.
22. Zanotti, G., Scapin, G., Spadon, P., Veerkamp, J. H., and Sacchettini, J. C. (1992) Three-dimensional structure of recombinant human muscle fatty acid-binding protein, J. Biol. Chem. 267, 18541.
23. McRee, D. E. (1999) XtalView/Xfit: A versatile program for manipulating atomic coordinates and electron density, J. Struct. Biol. 125, 156-165.
24. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of the macromolecular structures by the maximum-likelihood method, Acta Crystallogr. D54, 1285-1294.
25. Laskowsky, R. A., MacArthur, M. W., Moss, D. S., and Thorntorn, J. (1993) PROCHECK: a program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291
26. Liang, J., Edelsbrunner, H., and Woodward, C. (1998) Anatomy of Protein Pockets and Cavities: Measurement of Binding Site Geometry and Implications for Ligand Design, Protein Sci. 7, 1884-1897.
27. Kirk, R. W., Kurian, E., and Prendergast, F. G. (1996) Characterization of the sources of protein-ligand affinity: 1-sulfonato-8-anilinonaphthalene binding to intestinal fatty acid binding protein, Biophys. J. 70, 69-83.
28. Richieri, G. V., Ogata, R. T., and Kleinfeld A. M. (1992) A fluorescently labeled intestinal fatty acid binding protein, J. Biol. Chem. 267, 23495-23501.
29. Sacchettini, J. C., Gordon, J. I., and Banaszak, L. J. (1989) Crystal structure of rat intestinal fatty acid binding protein. Refinement and analysis of the Escherichia coli-derived protein with bound palmitate, J. Mol. Biol. 208, 327-339.
30. Eads, J., Sacchettini, J. C., Kromminga, A., and Gordon, J. I. (1993) Escherichia coli-derived rat intestinal fatty acid binding protein with bound myristate at 1.5Å resolution and I-FABP Arg106→Gln with bound oleate at 1.74Å resolution, J. Biol. Chem. 268, 26375-26385.
31. Herr, F. H., Aronson, J., and Storch, J. (1996) Role of the portal lysine residues in electrostatic interactions between heart fatty acid binding protein and phospholipid membranes, Biochemistry 35, 11840-11845.
32. Kennedy, M. W., Scott, J. C, Lo, S., Beauchamp, J., and McManus, D. P. (2000) Sj-FABPc fatty-acid binding protein of the human blood fluke Schistosoma japonicum: structural and functional characterization and unusual solvent exposure of a portal-proximal tryptophan residue, Biochem. J. 349, 377-384.
33. Vilar, M. M., Barrientos, F., Almeida, M., Thaumaturgo, N., Simpson, A., Garratt, R., and Tendler, M. (2003) An experimental bivalent peptide vaccine against schistosomiasis and fascioliasis. Vaccine 22, 137-144.
34. Ramos, C. R., Figueredo, R. C., Pertinhez, T. A., Vilar, M. M., do Nascimento, A. L., Tendler, M., Raw, I., Spisni, A., and Ho, P. L. (2003) Gene structure and M20T polymorphism of the Schistosoma mansoni Sm14 fatty acid binding protein, J. Biol. Chem. 278, 12745-12751.
35. Richieri, G. V., Low, P. J., Ogata, R. T., and Kleinfeld, A. M. (1998) Thermodynamics of fatty acid binding protein to engineered mutants of the adipocyte and intestinal fatty acid binding proteins, J. Biol. Chem. 273, 7397-7405.
36. Balendiran, K. G., Schnutgen, F., Scapin, G., Borchers, T., Xhong, N., Lim, K., Godbout, R., Spener, F., and Sacchettini, J. (2000) Crystal structure and thermodynamic analysis of human brain fatty acid binding protein, J. Biol. Chem. 275, 27045-27054
37. 1H exchange, Biochemistry 36, 2278-2290.
38. Kurian, E., Kirk, W. R., and Prendergast, F. G. (1996) Affinity for rRat intestinal fatty acid binding protein: Further examination, Biochemistry 35, 3865-3874.
39. Ory, J. J., and Banaszak, L. J. (1999) Studies of ligand binding reaction of adipocyte lipid binding protein using the fluorescent probe 1,8-anilinonaphthalene-8-sulfonate, Biophys. J. 77, 1107-1116.
40. Alvite, G., Di Pietro, S. M., Santomè, J. A., Ehrlich, R., and Esteves, A. (2001) Binding properties of Echinococcus granulosus fatty acid binding protein, Biochim. Biophys. Acta 1533, 293-302.
41. Esteves, A., Joseph, L., Paulino, M., and Ehrlich, R. (1997) Remarks on the philogeny and structure of fatty acid binding proteins from parasitic platyhelminths, Int. J. Parasitol. 27, 1013-1027.
42. LaLonde, J. M., Levenson, M. A., Roe, J. J., Bernlohr, D. A., and Banaszak, L. J. (1994) Adipocyte lipid-binding protein complexed with arachidonic acid, J. Biol. Chem. 269, 25339-25347.
43. Wootan, M. G., Bernlohr, D. A., and Storch, J. (1993) Mechanism of fluorescent fatty acid transfer from adipocyte fatty acid binding protein to membranes, Biochemistry 32, 8622-8627.
44. Eastman, S. J., Wilschut, J., Cullis, P. R., and Hope, M. J. (1989) Intervesicular exchange of lipids with weak acid and weak base characteristic: influence of transmembrane pH gradients. Biochim. Biophys. Acta 981, 178-184.
45. Richieri, G. V., and Kleinfeld, A. M. (1995) Unbound free fatty acid levels in human serum, J. Lipid Res. 36, 229-240.
46. Fan, J., Gan. J., Yang, W., Liying, S., McManus, D., and Brindley, P. J. (2003) A Schistosoma japonicum very low-density lipoprotein-binding protein, Int. J. Biochem. Cell Biol. 35, 1436-1451.