Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2016, Article ID 7123587, 12 pages
http://dx.doi.org/10.1155/2016/7123587
Research Article

β-Lactoglobulin Influences Human Immunity and Promotes Cell Proliferation

1Department and College of Biological Science and Technology, National Chiao Tung University, Hsinchu, Taiwan
2Institute of Molecular Medicine and Bioengineering, National Chiao Tung University, Hsinchu, Taiwan

Received 17 April 2016; Accepted 1 August 2016

Academic Editor: Frederick D. Quinn

Copyright © 2016 Chun San Tai et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Marshall, “Therapeutic applications of whey protein,” Alternative Medicine Review, vol. 9, no. 2, pp. 136–156, 2004. View at Google Scholar · View at Scopus
  2. A. A. Perez, R. B. Andermatten, A. C. Rubiolo, and L. G. Santiago, “β-Lactoglobulin heat-induced aggregates as carriers of polyunsaturated fatty acids,” Food Chemistry, vol. 158, pp. 66–72, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Sava, I. Van der Plancken, W. Claeys, and M. Hendrickx, “Heat-induced changes in thiol availability of beta-lactoglobulin,” Communications in Agricultural and Applied Biological Sciences, vol. 69, no. 2, pp. 243–246, 2004. View at Google Scholar · View at Scopus
  4. W. L. Chen, M. T. Hwang, C. Y. Liau, J. C. Ho, K. C. Hong, and S. J. T. Mao, “β-Lactoglobulin is a thermal marker in processed milk as studied by electrophoresis and circular dichroic spectra,” Journal of Dairy Science, vol. 88, no. 5, pp. 1618–1630, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. M.-C. Yang, H.-H. Guan, M.-Y. Liu et al., “Crystal structure of a secondary vitamin D3 binding site of milk β-lactoglobulin,” Proteins: Structure, Function, and Bioinformatics, vol. 71, no. 3, pp. 1197–1210, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. M. D. Pérez and M. Calvo, “Interaction of beta-lactoglobulin with retinol and fatty acids and its role as a possible biological function for this protein: a review,” Journal of Dairy Science, vol. 78, no. 5, pp. 978–988, 1995. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Kontopidis, C. Holt, and L. Sawyer, “Invited review: β-lactoglobulin: binding properties, structure, and function,” Journal of Dairy Science, vol. 87, no. 4, pp. 785–796, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Y. Song, W. L. Chen, M. C. Yang, J. P. Huang, and S. J. Mao, “Epitope mapping of a monoclonal antibody specific to bovine dry milk: involvement of residues 66–76 of strand D in thermal denatured β-lactoglobulin,” The Journal of Biological Chemistry, vol. 280, no. 5, pp. 3574–3582, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. M. C. Yang, N. C. Chen, C.-J. Chen, C. Y. Wu, and S. J. T. Mao, “Evidence for β-lactoglobulin involvement in vitamin D transport in vivo—role of the γ-turn (Leu-Pro-Met) of β-lactoglobulin in vitamin D binding,” The FEBS Journal, vol. 276, no. 8, pp. 2251–2265, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. L. H. Riihimaki-Lampen, M. J. Vainio, M. Vahermo et al., “The binding of synthetic retinoids to lipocalin beta-lactoglobulins,” Journal of Medicinal Chemistry, vol. 53, no. 1, pp. 514–518, 2010. View at Publisher · View at Google Scholar
  11. A. Barbiroli, T. Beringhelli, F. Bonomi et al., “Bovine β-lactoglobulin acts as an acid-resistant drug carrier by exploiting its diverse binding regions,” Biological Chemistry, vol. 391, no. 1, pp. 21–32, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. D. E. W. Chatterton, G. Smithers, P. Roupas, and A. Brodkorb, “Bioactivity of β-lactoglobulin and α-lactalbumin—technological implications for processing,” International Dairy Journal, vol. 16, no. 11, pp. 1229–1240, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Rovoli, O. Gortzi, S. Lalas, and G. Kontopidis, “β-Lactoglobulin improves liposome's encapsulation properties for vitamin E delivery,” Journal of Liposome Research, vol. 24, no. 1, pp. 74–81, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Brealey, M. Brand, I. Hargreaves et al., “Association between mitochondrial dysfunction and severity and outcome of septic shock,” The Lancet, vol. 360, no. 9328, pp. 219–223, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. F. B. Mayr, S. Yende, and D. C. Angus, “Epidemiology of severe sepsis,” Virulence, vol. 5, no. 1, pp. 4–11, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. D. C. Angus and T. van der Poll, “Severe sepsis and septic shock,” The New England Journal of Medicine, vol. 369, no. 9, pp. 840–851, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Rocha, R. Herance, S. Rovira, A. Hernández-Mijares, and V. M. Víctor, “Mitochondrial dysfunction and antioxidant therapy in sepsis,” Infectious Disorders—Drug Targets, vol. 12, no. 2, pp. 161–178, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Kumar, “Optimizing antimicrobial therapy in sepsis and septic shock,” Critical Care Nursing Clinics of North America, vol. 23, no. 1, pp. 79–97, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. M. M. Berger and R. L. Chioléro, “Antioxidant supplementation in sepsis and systemic inflammatory response syndrome,” Critical Care Medicine, vol. 35, no. 9, supplement, pp. S584–S590, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. O. Power, P. Jakeman, and R. J. FitzGerald, “Antioxidative peptides: enzymatic production, in vitro and in vivo antioxidant activity and potential applications of milk-derived antioxidative peptides,” Amino Acids, vol. 44, no. 3, pp. 797–820, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Hernández-Ledesma, I. Recio, and L. Amigo, “β-Lactoglobulin as source of bioactive peptides,” Amino Acids, vol. 35, no. 2, pp. 257–265, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Chaneton, J. M. Pérez Sáez, and L. E. Bussmann, “Antimicrobial activity of bovine β-lactoglobulin against mastitis-causing bacteria,” Journal of Dairy Science, vol. 94, no. 1, pp. 138–145, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. D. K. Heyland, R. Dhaliwal, U. Suchner, and M. M. Berger, “Antioxidant nutrients: a systematic review of trace elements and vitamins in the critically ill patient,” Intensive Care Medicine, vol. 31, no. 3, pp. 327–337, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. H. C. Liu, W. L. Chen, and S. J. T. Mao, “Antioxidant nature of bovine milk β-lactoglobulin,” Journal of Dairy Science, vol. 90, no. 2, pp. 547–555, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Y. Savcun, E. Özkan, E. Dulundu et al., “Antioxidant and anti-inflammatory effects of curcumin against hepatorenal oxidative injury in an experimental sepsis model in rats,” Ulusal Travma ve Acil Cerrahi Dergisi, vol. 19, no. 6, pp. 507–515, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Li, Y. Ma, and M. O. Ngadi, “Binding of curcumin to β-lactoglobulin and its effect on antioxidant characteristics of curcumin,” Food Chemistry, vol. 141, no. 2, pp. 1504–1511, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. J.-M. Yoo, Y. W. Park, S. Y. Yoon et al., “Thymic stromal lymphopoietin induction is mediated by the major whey proteins α-lactalbumin and β-lactoglobulin through the NF-κB pathway in immune cells,” Journal of Agricultural and Food Chemistry, vol. 63, no. 50, pp. 10803–10810, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. G. W. Krissansen, “Emerging health properties of whey proteins and their clinical implications,” Journal of the American College of Nutrition, vol. 26, no. 6, pp. 713S–723S, 2007. View at Google Scholar · View at Scopus
  29. F. J. Pérez-Cano, S. Marín-Galén, M. Castell et al., “Bovine whey protein concentrate supplementation modulates maturation of immune system in suckling rats,” British Journal of Nutrition, vol. 98, no. 1, pp. S80–S84, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. G. Badr, H. Ebaid, M. Mohany, and A. S. Abuelsaad, “Modulation of immune cell proliferation and chemotaxis towards CC chemokine ligand (CCL)-21 and CXC chemokine ligand (CXCL)-12 in undenatured whey protein-treated mice,” Journal of Nutritional Biochemistry, vol. 23, no. 12, pp. 1640–1646, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. D. A. Belford, M.-L. Rogers, G. O. Regester et al., “Milk-derived growth factors as serum supplements for the growth of fibroblast and epithelial cells,” In Vitro Cellular & Developmental Biology—Animal, vol. 31, no. 10, pp. 752–760, 1995. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Pakkanen, A. Kanttinen, L. Satama, and J. Aalto, “Bovine colostrum fraction as a serum substitute for the cultivation of mouse hybridomas,” Applied Microbiology and Biotechnology, vol. 37, no. 4, pp. 451–456, 1992. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Capiaumont, S. Ostrovidov, C. Legrand, F. Belleville, and P. Nabet, “Bovine whey: a substitute for FBS in CHO-K1 cell cultures,” In Vitro Cellular & Developmental Biology—Animal, vol. 32, no. 1, pp. 8–12, 1996. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Beaulieu, C. Dupont, and P. Lemieux, “Whey proteins and peptides: beneficial effects on immune health,” Therapy, vol. 3, no. 1, pp. 69–78, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Fleming, K. A. Thompson-Crispi, D. C. Hodgins, F. Miglior, M. Corredig, and B. A. Mallard, “Short communication: variation of total immunoglobulin G and β-lactoglobulin concentrations in colostrum and milk from Canadian Holsteins classified as high, average, or low immune responders,” Journal of Dairy Science, vol. 99, no. 3, pp. 2358–2363, 2016. View at Publisher · View at Google Scholar · View at Scopus
  36. W. L. Chen, M. T. Huang, H. C. Liu, C. W. Li, and S. J. T. Mao, “Distinction between dry and raw milk using monoclonal antibodies prepared against dry milk proteins,” Journal of Dairy Science, vol. 87, no. 8, pp. 2720–2729, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. W. L. Chen, W. T. Liu, M. C. Yang, M. T. Hwang, J. H. Tsao, and S. J. T. Mao, “A novel conformation-dependent monoclonal antibody specific to the native structure of β-lactoglobulin and its application,” Journal of Dairy Science, vol. 89, no. 3, pp. 912–921, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. C. F. Tseng, C. C. Lin, H. Y. Huang, H. C. Liu, and S. J. T. Mao, “Antioxidant role of human haptoglobin,” Proteomics, vol. 4, no. 8, pp. 2221–2228, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Alberts, J. Ranger-Moore, J. Einspahr et al., “Safety and efficacy of dose-intensive oral vitamin A in subjects with sun-damaged skin,” Clin Cancer Res, vol. 10, no. 6, pp. 1875–1880, 2004. View at Publisher · View at Google Scholar
  40. R. Zange, Y. Li, and T. Kissel, “Biocompatibility testing of ABA triblock copolymers consisting of poly(L-lactic-co-glycolic acid) A blocks attached to a central poly(ethylene oxide) B block under in vitro conditions using different L929 mouse fibroblasts cell culture models,” Journal of Controlled Release, vol. 56, no. 1–3, pp. 249–258, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. J. L. Pariente, B. S. Kim, and A. Atala, “In vitro biocompatibility assessment of naturally derived and synthetic biomaterials using normal human urothelial cells,” Journal of Biomedical Materials Research, vol. 55, no. 1, pp. 33–39, 2001. View at Google Scholar
  42. D. J. Oldfield, H. Singh, and M. W. Taylor, “Kinetics of heat-induced whey protein denaturation and aggregation in skim milks with adjusted whey protein concentration,” Journal of Dairy Research, vol. 72, no. 3, pp. 369–378, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Patel, “Functional food relevance of whey protein: a review of recent findings and scopes ahead,” Journal of Functional Foods, vol. 19, pp. 308–319, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Xu, Y. Sugiura, S. Nagaoka, and Y. Kanamaru, “IEC-6 intestinal cell death induced by bovine milk α-lactalbumin,” Bioscience, Biotechnology and Biochemistry, vol. 69, no. 6, pp. 1082–1089, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Knowles and H. S. Gill, “Immunomodulation by dairy ingredients: potential for improving health,” in Handbook of Functional Dairy Products, pp. 125–153, 2004. View at Google Scholar
  46. H. Meisel, “Biochemical properties of peptides encrypted in bovine milk proteins,” Current Medicinal Chemistry, vol. 12, no. 16, pp. 1905–1919, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. D. M. Barbano and J. M. Lynch, “Major advances in testing of dairy products: milk component and dairy product attribute testing,” Journal of Dairy Science, vol. 89, no. 4, pp. 1189–1194, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. A. S. Yalçin, “Emerging therapeutic potential of whey proteins and peptides,” Current Pharmaceutical Design, vol. 12, no. 13, pp. 1637–1643, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Rytkönen, T. J. Karttunen, R. Karttunen et al., Effect of Heat Denaturation of Bovine Milk Beta-Lactoglobulin on Its Epithelial Transport and Allergenicity, University of Oulu, 2006.
  50. D. B. Fathy, S. A. Mathis, T. Leeb, and L. M. F. Leeb-Lundberg, “A single position in the third transmembrane domains of the human B1 and B2 bradykinin receptors is adjacent to and discriminates between the C-terminal residues of subtype-selective ligands,” The Journal of Biological Chemistry, vol. 273, no. 20, pp. 12210–12218, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. D. R. Flower, “Beyond the superfamily: the lipocalin receptors,” Biochimica et Biophysica Acta (BBA)—Protein Structure and Molecular Enzymology, vol. 1482, no. 1-2, pp. 327–336, 2000. View at Publisher · View at Google Scholar · View at Scopus
  52. K. W. Rodenburg and D. J. Van der Horst, “Lipoprotein-mediated lipid transport in insects: analogy to the mammalian lipid carrier system and novel concepts for the functioning of LDL receptor family members,” Biochimica et Biophysica Acta (BBA)—Molecular and Cell Biology of Lipids, vol. 1736, no. 1, pp. 10–29, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. X. Arias-Moreno, A. Velazquez-Campoy, J. C. Rodríguez, M. Pocoví, and J. Sancho, “Mechanism of low density lipoprotein (LDL) release in the endosome: implications of the stability and Ca2+ affinity of the fifth binding module of the LDL receptor,” The Journal of Biological Chemistry, vol. 283, no. 33, pp. 22670–22679, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Casartelli, G. Cermenati, S. Rodighiero, F. Pennacchio, and B. Giordana, “A megalin-like receptor is involved in protein endocytosis in the midgut of an insect (Bombyx mori, Lepidoptera),” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 295, no. 4, pp. R1290–R1300, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. J. J. Mond and M. Brunswick, “UNIT 3.10 proliferative assays for B cell function,” in Current Protocols in Immunology, chapter 3, 2003. View at Publisher · View at Google Scholar
  56. D. Depoil, S. Fleire, B. L. Treanor et al., “CD19 is essential for B cell activation by promoting B cell receptor-antigen microcluster formation in response to membrane-bound ligand,” Nature Immunology, vol. 9, no. 1, pp. 63–72, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. D. Depoil, M. Weber, B. Treanor et al., “Early events of B cell activation by antigen,” Science Signaling, vol. 2, no. 63, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. S. C. Wilde, J. K. Keppler, K. Palani, and K. Schwarz, “β-Lactoglobulin as nanotransporter—part I: binding of organosulfur compounds,” Food Chemistry, vol. 197, pp. 1015–1021, 2016. View at Publisher · View at Google Scholar · View at Scopus
  59. Z. Teng, Y. Luo, Y. Li, and Q. Wang, “Cationic beta-lactoglobulin nanoparticles as a bioavailability enhancer: effect of surface properties and size on the transport and delivery in vitro,” Food Chemistry, vol. 204, pp. 391–399, 2016. View at Publisher · View at Google Scholar
  60. S. C. Wilde, C. Treitz, J. K. Keppler et al., “β-Lactoglobulin as nanotransporter—part II: characterization of the covalent protein modification by allicin and diallyl disulfide,” Food Chemistry, vol. 197, pp. 1022–1029, 2016. View at Publisher · View at Google Scholar · View at Scopus