Bovine β-lactoglobulin acts as an acid-resistant drug carrier by exploiting its diverse binding regions

Biological Chemistry

Volumn 391, Issue 1, 2010, Pages 21-32

  Barbiroli, Alberto ^a   Beringhelli, Tiziana ^a,b   Bonomi, Francesco ^a   Donghi, Daniela ^a   Ferranti, Pasquale ^c   Galliano, Monica ^d   Iametti, Stefania ^a   Maggioni, Daniela ^a   Rasmussen, Patrizia ^a   Scanu, Sandra ^a   Vilardo, Maria Caterina ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d UNIVERSITY OF PAVIA   (Italy)

Author keywords

lactoglobulin; 19F NMR; Fluorinated drugs; Hydrophobic binding sites; Ligand binding

Indexed keywords

ACID; BETA LACTOGLOBULIN; DRUG CARRIER; FLUINDOSTATIN; FLUORINE DERIVATIVE; FLURBIPROFEN; LIGAND;

ACIDITY; ARTICLE; BINDING KINETICS; BINDING SITE; CIRCULAR DICHROISM; COW; DRUG MIXTURE; DRUG SOLUBILITY; DRUG STABILITY; FLUORINE NUCLEAR MAGNETIC RESONANCE; HETERONUCLEAR NUCLEAR MAGNETIC RESONANCE; HYDROPHOBICITY; MASS SPECTROMETRY; MOLECULE; NUCLEAR MAGNETIC RESONANCE; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; STOICHIOMETRY; TEMPERATURE;

ANIMALS; BINDING SITES; CARRIER PROTEINS; CATTLE; FATTY ACIDS, MONOUNSATURATED; FLUORINE; FLURBIPROFEN; HYDROGEN-ION CONCENTRATION; INDOLES; LACTOGLOBULINS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING;

BOVINAE;

EID: 75149191826     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2010.008     Document Type: Article

References (39)

1. Beringhelli, T., Eberini, I., Galliano, M., Pedoto, A., Perduca, M., Sportiello, A., Fontana, E., Monaco, H.L., and Gianazza, E. (2002). pH and ionic strength dependence of protein (un)folding and ligand binding to bovine b-lactoglobulins A and B. Biochemistry 41, 15415-15422.
2. Brownlow, S., Morais Cabral, J.H., Cooper, R., Flower, D.R., Yewdall, S.J., Polikarpov, I., North, A.C., and Sawyer, L. (1997). Bovine b-lactoglobulin at 1.8 Å resolution: still an enigmatic lipocalin. Structure 5, 481-495.
3. Considine, T., Patel, H.A., Singh, H., and Creamer, L.K. (2005). Influence of binding of sodium dodecyl sulfate, all-trans-retinol, palmitate, and 8-anilino-1-naphthalenesulfonate on the heatinduced unfolding and aggregation of b-lactoglobulin B. J. Agric. Food Chem. 53, 3197-3205. (Pubitemid 40525286)
4. Creamer, L.K., Nilsson, H.C., Paulsson, M.A., Coker, C.J., Hill, J.P., and Jimenez-Flores, R. (2004). Effect of genetic variation on the tryptic hydrolysis of bovine b-lactoglobulin A, B, and C. J. Dairy Sci. 87, 4023-4032.
5. D'Alfonso, L., Collini, M., and Baldini, G. (1999). Evidence of heterogeneous 1-anilinonaphthalene-8-sulfonate binding to blactoglobulin from fluorescence spectroscopy. Biochim. Biophys. Acta 1432, 194-202.
6. Dufour, E. and Haertle, T. (1991). Binding of retinoids and b-carotene to b-lactoglobulin. Influence of protein modifications. Biochim. Biophys. Acta 1079, 316-320.
7. Dufour, E., Marden, M.C., and Haertle, T. (1990). b-Lactoglobulin binds retinol and protoporphyrin IX at two different binding sites. FEBS Lett. 277, 223-226.
8. Eberini, I., Baptista, A.M., Gianazza, E., Fraternali, F., and Beringhelli, T. (2004). Reorganization in apo- and holo-b-lactoglobulin upon protonation of Glu89: molecular dynamics and pKa calculations. Proteins 54, 744-758.
9. Eberini, I., Fantucci, P., Rocco, A.C., Gianazza, E., Galluccio, L., Maggioni, D., Ben, I.D., Galliano, M., Mazzitello, R., Gaiji, N., and Beringhelli, T. (2006). Computational and experimental approaches for assessing the interactions between the model calycin b-lactoglobulin and two antibacterial fluoroquinolones. Proteins 15, 555-567.
10. Eberini, I., Rocco, A.G., Mantegazza, M., Gianazza, E., Baroni, A., Vilardo, M.C., Donghi, D., Galliano, M., and Beringhelli, T. (2008). Computational and experimental approaches assess the interactions between bovine b-lactoglobulin and synthetic compounds of pharmacological interest. J. Mol. Graph. Model. 26, 1004-1013.
11. Fessas, D., Iametti, S., Schiraldi, A., and Bonomi, F. (2001). Thermal unfolding of monomeric and dimeric b-lactoglobulins. Eur. J. Biochem. 268, 5439-5448.
12. Flower, D.R. (1996). The lipocalin protein family: structure and function. Biochem. J. 318, 1-14.
13. Fogolari, F., Ragona, L., Zetta, L., Romagnoli, S., De Kruif, K.G., and Molinari, H. (1998). Monomeric bovine b-lactoglobulin adopts a b-barrel fold at pH 2. FEBS Lett. 436, 149-154.
14. Guo, M.R., Fox, P.F., and Kindstedt, P.S. (1995). Susceptibility of b-lactoglobulin and sodium caseinate to proteolysis by pepsin and trypsin. J. Dairy Sci. 78, 2336-2344.
15. Kinekawa, Y. and Kitabatake, N. (1996). Purification of b-lactoglobulin from whey protein concentrate by pepsin treatment. J. Dairy Sci. 79, 350-356.
16. Konuma, T., Sakurai, K., and Goto, Y. (2007). Promiscuous binding of ligands by b-lactoglobulin involves hydrophobic interactions and plasticity. J. Mol. Biol. 368, 209-218.
17. Kuwata, K., Hoshino, M., Forge, V., Era, S., Batt, C.A., and Goto, Y. (1999). Solution structure and dynamics of bovine b-lactoglobulin A. Protein Sci. 8, 2541-2545.
18. Lozinsky, E., Iametti, S., Barbiroli, A., Likhtenshtein, G.I., Kálai, T., Hideg, K., and Bonomi, F. (2006). Structural features of transiently modified b-lactoglobulin relevant to the stable binding of large hydrophobic molecules. Protein J. 25, 1-15.
19. Mazuel, C. (1991). Analytical Profiles of Drug Substances, Vol.20 (New York, USA: Academic Press), pp. 557-600.
20. McAlpine, A.S. and Sawyer, L. (1990). b-lactoglobulin: a protein drug carrier? Biochem. Soc. Trans. 18, 879.
21. McKenzie, H.A. (1971). b-Lactoglobulins. In: Milk Proteins, H.A. McKenzie, ed. (New York, USA: Academic Press), pp. 257-330.
22. Monaco, H.L., Zanotti, G., Spadon, P., Bolognesi, M., Sawyer, L., and Eliopoulos, E.E. (1987). Crystal structure of the trigonal form of bovine b-lactoglobulin and of its complex with retinol at 2.5 Å resolution. J. Mol. Biol. 197, 695-706.
23. Narayan, M. and Berliner, L.J. (1997). Fatty acids and retinoids bind independently and simultaneously to b-lactoglobulin. Biochemistry 36, 1906-1911.
24. Papiz, M.Z., Sawyer, L., Eliopoulos, E.E., North, A.C., Findlay, J.B., Sivaprasadarao, R., Jones, T.A., Newcomer, M.E., and Kraulis, P.J. (1986). The structure of b-lactoglobulin and its similarity to plasma retinol-binding protein. Nature 324, 383-385.
25. Perez, D.M., Diaz de Villegras, C., Sanchez, L., Aranda, P., Ena, J.M., and Calvo, M. (1989). Interaction of fatty acids with blactoglobulin and albumin from ruminant milk. J. Biochem. 106, 1094-1097.
26. Qin, B.Y., Bewley, M.C., Creamer, L.K., Baker, H.M., Baker, E.N., and Jameson, G.B. (1998). Structural basis of the Tanford transition of bovine b-lactoglobulin. Biochemistry 37, 14014-14023.
27. Ragona, L., Pusterla, F., Zetta, L., Monaco, H.L., and Molinari, H. (1997). Identification of a conserved hydrophobic cluster in partially folded bovine b-lactoglobulin at pH 2. Fold Des. 2, 281-290.
28. Ragona, L., Fogolari, F., Zetta, L., Perez, D.M., Puyol, P., De Kruif, K., Lohr, F., Ruterjans, H., and Molinari, H. (2000). Bovine blactoglobulin: interaction studies with palmitic acid. Protein Sci. 9, 1347-1356.
29. Rasmussen, P., Barbiroli, A., Bonomi, F., Faoro, F., Ferranti, P., Iriti, M., Picariello, G., and Iametti, S. (2007). Formation of structured polymers upon controlled denaturation of b-lactoglobulin with different chaotropes. Biopolymers 86, 57-72.
30. Sakurai, K. and Goto, Y. (2006). Dynamics and mechanism of the Tanford transition of bovine b-lactoglobulin studied using heteronuclear NMR spectroscopy. J. Mol. Biol. 356, 483-496.
31. Sakurai, K. and Goto, Y. (2007). Principal component analysis of the pH-dependent conformational transitions of bovine b-lactoglobulin monitored by heteronuclear NMR. Proc. Natl. Acad. Sci. USA 104, 15346-15351.
32. Sawyer, L. and Kontopidis, G. (2000). The core lipocalin, bovine b-lactoglobulin. Biochim. Biophys. Acta 1482, 136-148.
33. Skerra, A. (2008). Alternative binding proteins: anticalins - harnessing the structural plasticity of the lipocalin ligand pocket to engineer novel binding activities. FEBS J. 275, 2677-2683.
34. Tian, F., Johnson, K., Lesar, A.E., Moseley, H., Ferguson, J., Samuel, I.D., Mazzini, A., and Brancaleon, L. (2006). The pHdependent conformational transition of b-lactoglobulin modulates the binding of protoporphyrin IX. Biochim. Biophys. Acta 1760, 38-46.
35. Uhrinova, S., Uhrin, D., Denton, H., Smith, M., Sawyer, L., and Barlow, P.N. (1998). Complete assignment of 1H, 13C and 15N chemical shifts for bovine b-lactoglobulin: secondary structure and topology of the native state is retained in a partially unfolded form. J. Biomol. NMR 12, 89-107.
36. Urhinova, S., Smith, M.H., Jameson, G.B., Urhin, D., Sawyer, L., and Barlow, P.N. (2000). Structural changes accompanying pHinduced dissociation of the b-lactoglobulin dimer. Biochemistry 39, 3565-3574.
37. Vasskog, T., Berger, U., Samuelsen, P.J., Kallenborn, R., and Jensen, R. (2006). Selective serotonin reuptake inhibitors in sewage influents and effluents from Tromsø, Norway. J. Chromatogr. A 1115, 187-195.
38. Wang, Q., Allen, J.C., and Swaisgood, H.E. (1997). Binding of vitamin D and cholesterol to b-lactoglobulin. J. Dairy Sci. 80, 1054-1059.
39. Yazdanian, M., Briggs, K., Jankovsky, C., and Hawi, A. (2004). The 'High Solubility' definition of the current FDA guidance on biopharmaceutical classification system may be too strict for acidic drugs. Pharm. Res. 21, 293-299.