NMR Studies Reveal the Role of Biomembranes in Modulating Ligand Binding and Release by Intracellular Bile Acid Binding Proteins

Journal of Molecular Biology

Volumn 394, Issue 5, 2009, Pages 852-863

  Pedò, Massimo ^a   Löhr, Frank ^b   D'Onofrio, Mariapina ^a   Assfalg, Michael ^a   Dötsch, Volker ^b   Molinari, Henriette ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

lipid transport; liposomes; liver bile acid binding protein; NMR; protein membrane interaction

Indexed keywords

BILE ACID BINDING PROTEIN; LIPID BINDING PROTEIN; LIPOSOME; NITROGEN 15; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE PERMEABILITY; CELL POLARITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; LIGAND BINDING; LIPID TRANSPORT; MEMBRANE; MEMBRANE BINDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECRETION;

EID: 70449672175     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.10.014     Document Type: Article

References (34)

1. Alrefai W.A., and Gill R.K. Bile acid transporters: structure, function, regulation and pathophysiological implications. Pharm. Res. 24 (2007) 1803-1823
2. Chiang J.Y. Bile acids: regulation of synthesis. J. Lipid Res. 50 (2009) 1955-1966
3. Pellicciari R., Camaioni E., Costantino G., Formentini L., Sabbatini P., Venturoni F., et al. On the way to selective PARP-2 inhibitors. Design, synthesis, and preliminary evaluation of a series of isoquinolinone derivatives. ChemMedChem 3 (2008) 914-923
4. Kosters A., and Karpen S.J. Bile acid transporters in health and disease. Xenobiotica 38 (2008) 1043-1071
5. Kullak-Ublick G.A., Stieger B., and Meier P.J. Enterohepatic bile salt transporters in normal physiology and liver disease. Gastroenterology 126 (2004) 322-342
6. Weisiger R.A. When is a carrier not a membrane carrier? The cytoplasmic transport of amphipathic molecules. Hepatology 24 (1996) 1288-1295
7. Pielak G.J., Li C., Miklos A.C., Schlesinger A.P., Slade K.M., Wang G.F., and Zigoneanu I.G. Protein nuclear magnetic resonance under physiological conditions. Biochemistry 48 (2009) 226-234
8. Selenko P., and Wagner G. Looking into live cells with in-cell NMR spectroscopy. J. Struct. Biol. 158 (2007) 244-253
9. Serber Z., Selenko P., Hansel R., Reckel S., Lohr F., Ferrell Jr. J.E., et al. Investigating macromolecules inside cultured and injected cells by in-cell NMR spectroscopy. Nat. Protoc. 1 (2006) 2701-2709
10. Xu Y., Yushmanov V.E., and Tang P. NMR studies of drug interaction with membranes and membrane-associated proteins. Biosci. Rep. 22 (2002) 175-196
11. Vasile F., Ragona L., Catalano M., Zetta L., Perduca M., Monaco H., and Molinari H. Solution structure of chicken liver basic fatty acid binding protein. J. Biomol. NMR 25 (2003) 157-160
12. Eliseo T., Ragona L., Catalano M., Assfalg M., Paci M., Zetta L., et al. Structural and dynamic determinants of ligand binding in the ternary complex of chicken liver bile acid binding protein with two bile salts revealed by NMR. Biochemistry 46 (2007) 12557-12567
13. Nichesola D., Perduca M., Capaldi S., Carrizo M.E., Righetti P.G., and Monaco H.L. Crystal structure of chicken liver basic fatty acid-binding protein complexed with cholic acid. Biochemistry 43 (2004) 14072-14079
14. Ragona L., Catalano M., Luppi M., Cicero D., Eliseo T., Foote J., et al. NMR dynamic studies suggest that allosteric activation regulates ligand binding in chicken liver bile acid-binding protein. J. Biol. Chem. 281 (2006) 9697-9709
15. Tomaselli S., Ragona L., Zetta L., Assfalg M., Ferranti P., Longhi R., et al. NMR-based modeling and binding studies of a ternary complex between chicken liver bile acid binding protein and bile acids. Proteins: Struct. Funct. Genet. 69 (2007) 177-191
16. Villarreal M.A., Perduca M., Monaco H.L., and Montich G.G. Binding and interactions of L-BABP to lipid membranes studied by molecular dynamic simulations. Biochim. Biophys. Acta 1778 (2008) 1390-1397
17. Galassi V., Nolan V., Villarreal M.A., Perduca M., Monaco H.L., and Montich G.G. Kinetics of lipid-membrane binding and conformational change of L-BABP. Biochem. Biophys. Res. Commun. 382 (2009) 771-775
18. Decca M.B., Perduca M., Monaco H.L., and Montich G.G. Conformational changes of chicken liver bile acid-binding protein bound to anionic lipid membrane are coupled to the lipid phase transitions. Biochim. Biophys. Acta 1768 (2007) 1583-1591
19. Nolan V., Perduca M., Monaco H.L., Maggio B., and Montich G.G. Interactions of chicken liver basic fatty acid-binding protein with lipid membranes. Biochim. Biophys. Acta 1611 (2003) 98-106
20. Pedò M., D'Onofrio M., Ferranti P., Molinari H., and Assfalg M. Towards the elucidation of molecular determinants of cooperativity in the liver bile acid binding protein. Proteins: Struct. Funct. Genet. 77 (2009) 718-731
21. Schneider M.F., Marsh D., Jahn W., Kloesgen B., and Heimburg T. Network formation of lipid membranes: triggering structural transitions by chain melting. Proc. Natl Acad. Sci. USA 96 (1999) 14312-14317
22. D'Onofrio M., Ragona L., Fessas D., Signorelli M., Ugolini R., Pedo M., et al. NMR unfolding studies on a liver bile acid binding protein reveal a global two-state unfolding and localized singular behaviors. Arch. Biochem. Biophys. 481 (2009) 21-29
23. Storch J., and Bass N.M. Transfer of fluorescent fatty acids from liver and heart fatty acid-binding proteins to model membranes. J. Biol. Chem. 265 (1990) 7827-7831
24. Kim H.K., and Storch J. Free fatty acid transfer from rat liver fatty acid-binding protein to phospholipid vesicles. Effect of ligand and solution properties. J. Biol. Chem. 267 (1992) 77-82
25. Kim H.K., and Storch J. Mechanism of free fatty acid transfer from rat heart fatty acid-binding protein to phospholipid membranes. Evidence for a collisional process. J. Biol. Chem. 267 (1992) 20051-20056
26. Cassio D., Macias R.I., Grosse B., Marin J.J., and Monte M.J. Expression, localization, and inducibility by bile acids of hepatobiliary transporters in the new polarized rat hepatic cell lines, Can 3-1 and Can 10. Cell Tissue Res. 330 (2007) 447-460
27. Tomaselli S., Zanzoni S., Ragona L., Gianolio E., Aime S., Assfalg M., and Molinari H. Solution structure of the supramolecular adduct between a liver cytosolic bile acid binding protein and a bile acid-based gadolinium(III)-chelate, a potential hepatospecific magnetic resonance imaging contrast agent. J. Med. Chem. 51 (2008) 6782-6792
28. Tochtrop G.P., Richter K., Tang C., Toner J.J., Covey D.F., and Cistola D.P. Energetics by NMR: site-specific binding in a positively cooperative system. Proc. Natl Acad. Sci. USA 99 (2002) 1847-1852
29. Davies J.K., Thumser A.E., and Wilton D.C. Binding of recombinant rat liver fatty acid-binding protein to small anionic phospholipid vesicles results in ligand release: a model for interfacial binding and fatty acid targeting. Biochemistry 38 (1999) 16932-16940
30. Hagan R.M., Worner-Gibbs J., and Wilton D.C. The interaction of liver fatty-acid-binding protein (FABP) with anionic phospholipid vesicles: is there extended phospholipid anchorage under these conditions?. Biochem. J. 410 (2008) 123-129
31. Tuominen E.K., Wallace C.J., and Kinnunen P.K. Phospholipid-cytochrome c interaction: evidence for the extended lipid anchorage. J. Biol. Chem. 277 (2002) 8822-8826
32. Kramer W., Girbig F., Gutjahr U., Kowalewski S., Jouvenal K., Muller G., et al. Intestinal bile acid absorption. Na(+)-dependent bile acid transport activity in rabbit small intestine correlates with the coexpression of an integral 93-kDa and a peripheral 14-kDa bile acid-binding membrane protein along the duodenum-ileum axis. J. Biol. Chem. 268 (1993) 18035-18046
33. Nakahara M., Furuya N., Takagaki K., Sugaya T., Hirota K., Fukamizu A., et al. Ileal bile acid-binding protein, functionally associated with the farnesoid X receptor or the ileal bile acid transporter, regulates bile acid activity in the small intestine. J. Biol. Chem. 280 (2005) 42283-42289
34. Pervushin K., Riek R., Wider G., and Wuthrich K. Attenuated T2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc. Natl Acad. Sci. USA 94 (1997) 12366-12371