Transport properties of bovine and reindeer β-lactoglobulin in the Caco-2 cell model

International Journal of Pharmaceutics

Volumn 347, Issue 1-2, 2008, Pages 1-8

  Riihimäki, Laura ^a   Galkin, Anna ^a   Finel, Moshe ^a   Heikura, Jonna ^b   Valkonen, Kaija ^b   Virtanen, Vesa ^b   Laaksonen, Reijo ^a,c   Slotte, J Peter ^d   Vuorela, Pia ^a,d  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF OULU   (Finland)

^c TAMPERE UNIVERSITY HOSPITAL   (Finland)

^d ÅBO AKADEMI UNIVERSITY   (Finland)

Author keywords

Lactoglobulin; Caco 2 monolayer; Ligand; Reindeer; Transport

Indexed keywords

BETA LACTOGLOBULIN; CHOLESTEROL; LIGAND; PALMITIC ACID; RETINOL; TRITIUM;

ANTIBODY LABELING; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE TRANSPORT; CELL STRAIN CACO 2; CONTROLLED STUDY; COW; DRUG TRANSPORT; GENOTYPE; HUMAN; HUMAN CELL; HYDROPHOBICITY; IMMUNOBLOTTING; INTESTINE ABSORPTION; MONOLAYER CULTURE; NONHUMAN; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PROTEIN TRANSPORT; REINDEER; TRANSPORT KINETICS;

ANIMALS; BIOLOGICAL TRANSPORT; CACO-2 CELLS; CARRIER PROTEINS; CATTLE; CELL MEMBRANE; CHOLESTEROL; ELECTRIC IMPEDANCE; HUMANS; LACTOGLOBULINS; LIGANDS; PALMITIC ACID; REINDEER; VITAMIN A;

EID: 36549003218     PISSN: 03785173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2007.06.015     Document Type: Article

References (47)

1. Altmann S.W., Davis Jr. H.R., Zhu L., Yao X., Hoos L.M., Tetzloff G., Iyer S.P.N., Maguine M., Golovko A., Zeng M., Wang L., Murgolo N., and Graziano M.P. Niemann-Pick C1 Like 1 protein is critical for intestinal cholesterol absorption. Science 303 (2004) 1201-1204
2. Artursson P., Palm K., and Luthman K. Caco-2 monolayers in experimental and theoretical predictions of drug transport. Adv. Drug Deliv. Rev. 22 (1996) 67-84
3. Bellovino D., Apreda M., Gragnoli S., Massimi M., and Gaetani S. Vitamin A transport: in vitro models for the study of RBP secretion. Mol. Aspects Med. 24 (2003) 411-420
4. Bernasconi E., Fritsché R., and Corthésy B. Specific effects of denaturation, hydrolysis and exposure to Lactococcus lactis on bovine β-lactoglobulin transepithelial transport, antigenicity and allergenicity. Clin. Exp. Allergy 36 (2006) 803-814
5. Brownlow S., Cabral J.H.M., Cooper R., Flower D.R., Yewdall S.J., Polikarpov I., North A.C.T., and Sawyer L. Bovine β-lactoglobulin at 1.8 Å resolution-still an enigmatic lipocalin. Structure 5 (1997) 481-495
6. Burczynski F.J., Cai Z.S., Moran J.B., and Forker E.L. Palmitate uptake by cultured hepatocytes: albumin binding and stagnant layer phenomena. Am. J. Physiol. 257 (1989) G584-G593
7. Burczynski F.J., Moran J.B., Cai Z.S., and Forker E.L. β-Lactoglobulin enhances the uptake of free palmitate by hepatocyte monolayers: the relative importance of diffusion and facilitated dissociation. Can. J. Physiol. Pharmacol. 68 (1990) 201-206
8. Caillard I., and Tome D. Transport of β-lactoglobulin and α-lactalbumin in enterocyte-like Caco-2 cells. Reprod. Nutr. Dev. 35 (1995) 179-188
9. Davies J.P., Scott C., Oishi K., Liapis A., and Ioannou Y.A. Inactivation of NPC1L1 causes multiple lipid transport defects and protects against diet-induced hypercholesterolemia. J. Biol. Chem. 280 (2005) 12710-12720
10. De Jongh H.H., Groneveld T., and de Groot J. Mild isolation procedure discloses new protein structural properties of β-lactoglobulin. J. Dairy Sci. 84 (2001) 562-571
11. Eberini I., Fantucci P., Rocco A.G., Gianazza E., Galluccio L., Maggioni D., Ben I.D., Galliano M., Mazzinello R., and Gaiji N. Computational and experimental approaches for assessing the interactions between the model calycin β-lactoglobulin and two antibacterial fluoroquinolones. Proteins 65 (2006) 555-567
12. Field F.J., Born E., Murthy S., and Mathur S.N. Transport of cholesterol from the endoplasmic reticulum to the plasma membrane is constitutive in Caco-2 cells and differs from the transport of plasma membrane cholesterol to the endoplasmic reticulum. J. Lipid Res. 39 (1998) 333-343
13. Flower D.R., North A.C.T., and Attwood T.K. Structure and sequence relationships in the lipocalins and related proteins. Protein Sci. 2 (1993) 753-761
14. Heikura J., Suutari T., Rytkönen J., Nieminen M., Virtanen V., and Valkonen K. A new procedure to isolate β-lactoglobulin from reindeer milk. Milchwissenschaft 60 (2005) 388-392
15. Heyman M., and Desjeux J.F. Significance of intestinal food protein transport. J. Pediatr. Gastroenterol. Nutr. 15 (1992) 48-57
16. Laitinen L., Kangas H., Kaukonen A.M., Hakala K., Kotiaho T., Kostiainen R., and Hirvonen J. N-in-one permeability studies of heterogeneous sets of compounds across Caco-2 cell monolayers. Pharm. Res. 20 (2003) 187-197
17. Laitinen L., Tammela P., Galkin A., Vuorela H., Marvola M., and Vuorela P. Effects of extracts of commonly consumed food supplements and food fractions on the permeability of drugs across Caco-2 cell monolayers. Pharm. Res. 21 (2004) 1904-1916
18. Levin M.S., Talkad V.D., Gordon J.I., and Stenson W.F. Trafficking of exogenous fatty acids within Caco-2 cells. J. Lipid Res. 33 (1992) 9-19
19. Levin M.S. Cellular retinol-binding proteins are determinants of retinol uptake and metabolism in stably transfected Caco-2 cells. J. Biol. Chem. 268 (1993) 8267-8276
20. Mansouri A., Guéant J.L., Capiaumont J., Pelosi P., Nabet P., and Haertlé T. Plasma membrane receptor for beta-lactoglobulin and retinol-binding protein in murine hybridomas. Biofactors 7 (1998) 287-298
21. McAlpine A.S., and Sawyer L. β-Lactoglobulin: a protein drug carrier?. Biochem. Soc. Trans. 18 (1990) 879
22. Moncla B.J., Hillier S.L., and Charnetzky W.T. Constitutive uptake and degradation of fatty acids by Yersinia pestis. J. Bacteriol. 153 (1983) 340-344
23. Murthy S., Albright E., Mathur S.N., and Field F.J. Modification of Caco-2 cell membrane fatty acid composition by eicosapentaenoic acid and palmitic acid: effect on cholesterol metabolism. J. Lipid Res. 29 (1988) 773-780
24. Narayan M., and Berliner L.J. Fatty acids and retinoids bind independently and simultaneously to β-lactoglobulin. Biochemistry 36 (1997) 1906-1911
25. Neutra M.R., Mantis N.J., Frey A., and Giannasca P.J. The composition and function of M cell apical membranes: implications for microbial pathogenesis. Semin. Immunol. 11 (1999) 171-181
26. Oksanen E., Jaakola V.P., Tolonen T., Valkonen K., Åkerström B., Kalkkinen N., Virtanen V., and Goldman A. Reindeer β-lactoglobulin crystal structure with pseudo-body-centred noncrystallographic symmetry. Acta Crystallogr. D: Biol. Crystallogr. 62 (2006) 1369-1374
27. Papiz M.Z., Sawyer L., Eliopoulos E.E., North A.C.T., Findlay J.B.C., Sivaprasadarao R., Jones T.A., Newcomer M.E., and Kraulis P.J. The structure of β-lactoglobulin and its similarity to plasma retinol-binding protein. Nature 324 (1986) 383-385
28. Pérez M.D., and Calvo M. Interaction of β-lactoglobulin with retinol and fatty acids and its role as a possible biological function for this protein: a review. J. Dairy Sci. 78 (1995) 978-988
29. Puyol P., Perez M.D., Sanchez L., Ena J.M., and Calvo M. Uptake and passage of β-lactoglobulin, palmitic acid and retinol across the Caco-2 monolayer. Biochim. Biophys. Acta 1236 (1995) 149-154
30. Quick T.C., and Ong D.E. Vitamin A metabolism in the human intestinal Caco-2 cell line. Biochemistry 29 (1990) 11116-11123
31. Riihimäki L., Aitio O., Vahermo M., Heikura J., Valkonen K., Virtanen V., Yli-Kauhaluoma J., and Vuorela P. Microplate screening assay for binding of ligands to bovine or reindeer β-lactoglobulins. J. Biochem. Biophys. Meth. 68 (2006) 75-85
32. Rytkönen J., Alatossava T., Nieminen M., and Valkonen K. Isolation and characterization of β-lactoglobulin from reindeer milk. Milchwissenschaft 57 (2002) 259-261
33. Rytkönen J., Valkonen K.H., Virtanen V., Foxwell R.A., Kyd J.M., Cripps A.W., and Karttunen T.J. Enterocyte and M-Cell transport of native and heat-denatured bovine β-lactoglobulin: significance of heat denaturation. J. Agric. Food Chem. 54 (2006) 1500-1507
34. Sawyer L., and Kontopidis G. The core lipocalin, bovine β-lactoglobulin. Biochim. Biophys. Acta 1482 (2000) 136-148
35. Siissalo, S., Laitinen, L., Koljonen, M., Vellonen, K.S., Kortejärvi, H., Urtti, A., Hirvonen, J., Kaukonen, A.M., in press. Effect of cell differentation and passage number on the expression of efflux proteins in wild type and vinblastine-induced Caco-2 cell lines. Eur. J. Pharm. Biopharm.
36. Suruga K., Mochizuki K., Suzuki R., Goda T., and Takase S. Regulation of cellular retinol-binding protein type II gene expression by arachidonic acid analogue and 9-cis retinoic acid in Caco-2 cells. Eur. J. Biochem. 262 (1999) 70-78
37. Suutari T.J., Valkonen K.H., Karttunen T.J., Ehn B.M., Ekstrand B., Bengtsson U., Virtanen V., Nieminen M., and Kokkonen J. IgE cross reactivity between reindeer and bovine milk β-lactoglobulins in cow's milk allergic patients. J. Investig. Allergol. Clin. Immunol. 16 (2006) 296-302
38. Tanabe S., Tesaki S., Watanabe J., Fukushi E., Sonoyama K., and Kawabata J. Isolation and structural elucidation of a peptide derived from Edam cheese that inhibits β-lactoglobulin transport. J. Dairy Sci. 86 (2003) 464-468
39. Temsamani J., and Vidal P. The use of cell-penetrating peptides for drug delivery. Drug Discov. Today 9 (2004) 1012-1019
40. Trotter P.J., Ho S.Y., and Storch J. Fatty acid uptake by Caco-2 human intestinal cells. J. Lipid Res. 37 (1996) 336-346
41. Trotter P.J., and Storch J. Fatty acid uptake and metabolism in a human intestinal cell line (Caco-2): comparison of apical and basolateral incubation. J. Lipid Res. 32 (1991) 293-304
42. van Greevenbroek M.M.J., Voorhout W.F., Erkelens D.W., van Meer G., and de Bruin T.W.A. Palmitic acid and linoleic acid metabolism in Caco-2 cells: different triglyceride synthesis and lipoprotein secretion. J. Lipid Res. 36 (1995) 13-24
43. Wang Q., Allen J.C., and Swaisgood H.E. Binding of retinoids to β-lactoglobulin isolated by bioselective adsorption. J. Dairy Sci. 80 (1997) 1047-1053
44. Wang Q., Allen J.C., and Swaisgood H.E. Binding of vitamin D and cholesterol to β-lactoglobulin. J. Dairy Sci. 80 (1997) 1054-1059
45. Wu K., Kim H.T., Rodriquez J.L., Hilsenbeck S.G., Mohsin S.K., Xu X.C., Lamph W.W., Kuhn J.G., Green J.E., and Brown P.H. Suppression of mammary tumorigenesis in transgenic mice by the RXR-selective retinoid, LGD1069. Cancer Epidemiol. Biomarkers Prev. 11 (2002) 467-474
46. Wu S.Y., Pérez M.D., Puyol P., and Sawyer L. β-Lactoglobulin binds palmitate within its central cavity. J. Biol. Chem. 274 (1999) 170-174
47. Yamanashi Y., Takada T., and Suzuki H. Niemann-Pick C1-Like 1 overexpression facilitates ezetimibe-sensitive cholesterol and β-sitosterol uptake in Caco-2 cells. J. Pharmacol. Exp. Ther. 320 (2007) 559-564