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Journal of Amino Acids
Volume 2013 (2013), Article ID 939804, 7 pages
http://dx.doi.org/10.1155/2013/939804
Review Article

Potential Anticarcinogenic Peptides from Bovine Milk

1Dipartimento di Scienze Farmaceutiche e Biomediche, Università degli Studi di Salerno, Via Ponte Don Melillo, 84084 Fisciano, Italy
2Dipartimento di Chimica Farmaceutica e Tossicologica, Università di Napoli “Federico II,” Via D. Montesano 49, 80131 Napoli, Italy
3Dipartimento di Biochimica e Biofisica, Seconda Università di Napoli, Via L. De Crecchio 7, 80138 Napoli, Italy

Received 21 December 2012; Accepted 28 January 2013

Academic Editor: Michele Caraglia

Copyright © 2013 Giacomo Pepe 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. I. Lopez-Exposito and I. Recio, “Protective effect of milk peptides: antibacterial and antitumor properties,” Advances in Experimental Medicine and Biology, vol. 606, pp. 271–293, 2008. View at Publisher · View at Google Scholar
  2. P. W. Parodi, “A role for milk proteins and their peptides in cancer prevention,” Current Pharmaceutical Design, vol. 13, no. 8, pp. 813–828, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Tellez, M. Corredig, L. Y. Brovko, and M. W. Griffiths, “Characterization of immune-active peptides obtained from milk fermented by Lactobacillus helveticus,” Journal of Dairy Research, vol. 77, no. 2, pp. 129–136, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Sasaki and H. Kume, “Nutritional and physiological effects of peptides from whey: milk whey proteins/peptides, natural beneficial modulators of inflammation,” Bulletin of the International Dairy Federation, vol. 417, pp. 43–50, 2007.
  5. L. Sawyer, “β-lactoglobulin,” in Advanced Dairy Chemistry I, P. F. Fox and P. McSweeney, Eds., pp. 319–386, Kluwer, Amsterdam, The Netherlands, 3rd edition, 2003.
  6. A. Henschen, F. Lottspeich, V. Brantl, and H. Teschemacher, “Novel opioid peptides derived from casein (β-casomorphins). II. Structure of active components from bovine casein peptone,” Hoppe-Seyler's Zeitschrift fur Physiologische Chemie, vol. 360, no. 9, pp. 1217–1224, 1979. View at Scopus
  7. Z. Sun, Z. Zhang, X. Wang, R. Cade, Z. Elmir, and M. Fregly, “Relation of β-casomorphin to apnea in sudden infant death syndrome,” Peptides, vol. 24, no. 6, pp. 937–943, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. F. Jänicke, M. Schmitt, L. Pache et al., “Urokinase (uPA) and its inhibitor PAI-1 are strong and independent prognostic factors in node-negative breast cancer,” Breast Cancer Research and Treatment, vol. 24, no. 3, pp. 195–208, 1992. View at Publisher · View at Google Scholar · View at Scopus
  9. A. K. Tandon, G. M. Clark, G. C. Chamness, J. M. Chirgwin, and W. L. McGuire, “Cathepsin D and prognosis in breast cancer,” New England Journal of Medicine, vol. 322, no. 5, pp. 297–302, 1990. View at Scopus
  10. A. Hatzoglou, E. Bakogeorgou, C. Hatzoglou, P. M. Martin, and E. Castanas, “Antiproliferative and receptor binding properties of α- and β-casomorphins in the T47D human breast cancer cell line,” European Journal of Pharmacology, vol. 310, no. 2-3, pp. 217–223, 1996. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Loukas, D. Varoucha, and C. Zioudrou, “Opioid activities and structures of α-casein-derived exorphins,” Biochemistry, vol. 22, no. 19, pp. 4567–4573, 1983. View at Scopus
  12. H. Teschemacher, “Opioid receptor ligands derived from food proteins,” Current Pharmaceutical Design, vol. 9, no. 16, pp. 1331–1344, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Kampa, S. Loukas, A. Hatzoglou, P. Martin, P. M. Martin, and E. Castanas, “Identification of a novel opioid peptide (Tyr-Val-Pro-Phe-Pro) derived from human αs1 casein (αs1-casomorphin, and αs1-casomorphin amide),” Biochemical Journal, vol. 319, no. 3, pp. 903–908, 1996. View at Scopus
  14. C. De Simone, P. Ferranti, G. Picariello et al., “Peptides from water buffalo cheese whey induced senescence cell death via ceramide secretion in human colon adenocarcinoma cell line,” Molecular Nutrition and Food Research, vol. 55, no. 2, pp. 229–238, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. C. De Simone, G. Picariello, G. Mamone et al., “Characterisation and cytomodulatory properties of peptides from Mozzarella di Bufala Campana cheese whey,” Journal of Peptide Science, vol. 15, no. 3, pp. 251–258, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Berrocal, S. Chanton, M. A. Juillerat, B. Pavillard, J. C. Scherz, and R. Jost, “Tryptic phosphopeptides from whole casein. II. Physicochemical properties related to the solubilization of calcium,” Journal of Dairy Research, vol. 56, no. 3, pp. 335–341, 1989. View at Scopus
  17. A. Zawadzki, Q. Liu, Y. Wang, A. Melander, B. Jeppsson, and H. Thorlacius, “Verapamil inhibits L-type calcium channel mediated apoptosis in human colon cancer cells,” Diseases of the Colon and Rectum, vol. 51, no. 11, pp. 1696–1702, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Perego, S. Cosentino, A. Fiorilli, G. Tettamanti, and A. Ferraretto, “Casein phosphopeptides modulate proliferation and apoptosis in HT-29 cell line through their interaction with voltage-operated L-type calcium channels,” The Journal of Nutritional Biochemistry, vol. 23, no. 7, pp. 808–816, 2012. View at Publisher · View at Google Scholar
  19. K. Brew, F. J. Castellino, T. C. Vanaman, and R. L. Hill, “The complete amino acid sequence of bovine alpha-lactalbumin,” Journal of Biological Chemistry, vol. 245, no. 17, pp. 4570–4582, 1970. View at Scopus
  20. P. F. Fox, “The milk protein system,” in Developments of Dairy Chemistry-4-Functional Peptides, P. F. Fox, Ed., pp. 35–45, Elsevier Applied Science Publishers, London, UK, 1989.
  21. J. Fast, A. K. Mossberg, H. Nilsson, C. Svanborg, M. Akke, and S. Linse, “Compact oleic acid in HAMLET,” FEBS Letters, vol. 579, no. 27, pp. 6095–6100, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Svensson, J. Fast, A. K. Mossberg et al., “α-lactalbumin unfolding is not sufficient to cause apoptosis, but is required for the conversion to HAMLET (human α-lactalbumin made lethal to tumor cells),” Protein Science, vol. 12, no. 12, pp. 2794–2804, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Håkansson, B. Zhivotovsky, S. Orrenius, H. Sabharwal, and C. Svanborget, “Apoptosis induced by a human milk protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 17, pp. 8064–8068, 1995. View at Publisher · View at Google Scholar
  24. E. A. Permyakov and L. J. Berliner, “α-Lactalbumin: structure and function,” FEBS Letters, vol. 473, no. 3, pp. 269–274, 2000. View at Publisher · View at Google Scholar · View at Scopus
  25. L. G. Sternhagen and J. C. Allen, “Growth rates of a human colon adenocarcinoma cell line are regulated by the milk protein alpha-lactalbumin,” Advances in Experimental Medicine and Biology, vol. 501, pp. 115–120, 2001. View at Scopus
  26. A. S. Goldman, R. M. Goldblum, and L. A. Hanson, “Anti-inflammatory systems in human milk,” in Antioxidant Nutrients and Immune Functions, A. Bendich, M. Phillips, and R. P. Tengerdy, Eds., pp. 69–76, Plenum Press, New York, NY, USA, 1990.
  27. 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
  28. J. E. Kinsella and D. M. Whitehead, “Proteins in whey: chemical, physical, and functional properties,” Advances in Food and Nutrition Research, vol. 33, no. C, pp. 343–438, 1989. View at Publisher · View at Google Scholar · View at Scopus
  29. J. N. de Wit, “Functional properties of whey proteins,” in Developments of Dairy Chemistry-4-Functional Peptides, P. F. Fox, Ed., pp. 285–322, Elsevier Applied Science Publishers, London, UK, 1989.
  30. I. Laursen, P. Briand, and A. E. Lykkesfeldt, “Serum albumin as a modulator on growth of the human breast cancer cell line, MCF-7,” Anticancer Research A, vol. 10, no. 2, pp. 343–351, 1990. View at Scopus
  31. I. E. M. Bosselaers, P. W. J. R. Caessens, M. A. J. S. Van Boekel, and G. M. Alink, “Differential effects of milk proteins, BSA and soy protein on 4NQO- or MNNG-induced SCEs in V79 cells,” Food and Chemical Toxicology, vol. 32, no. 10, pp. 905–909, 1994. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Hauer, W. Voetsh, and F. A. Anderer, “Identification of a mannose-acetate-specific 87-kDa receptor responsible for human NK and LAK activity,” Immunology Letters, vol. 42, no. 1-2, pp. 7–12, 1994. View at Publisher · View at Google Scholar
  33. T. Zagulski, P. Lipinski, A. Zagulska, S. Broniek, and Z. Jarzabek, “Lactoferrin can protect mice against a lethal dose of Escherichia coli in experimental infection in vivo,” British Journal of Experimental Pathology, vol. 70, no. 6, pp. 697–704, 1989. View at Scopus
  34. J. He and P. Furmanski, “Sequence specificity and transcriptional activation in the binding of lactoferrin to DNA,” Nature, vol. 373, no. 6516, pp. 721–724, 1995. View at Publisher · View at Google Scholar · View at Scopus
  35. P. E. Florian, M. Trif, R. W. Evans, and A. Roşeanu, “An overview on the antiviral activity of Lactoferrin,” Romanian Journal of Biochemistry, vol. 46, no. 2, pp. 187–197, 2009.
  36. M. Tomita, W. Bellamy, M. Takase, K. Yamauchi, H. Wakabayashi, and K. Kawase, “Potent antibacterial peptides generated by pepsin digestion of bovine lactoferrin,” Journal of Dairy Science, vol. 74, no. 12, pp. 4137–4142, 1991. View at Publisher · View at Google Scholar · View at Scopus
  37. W. Bellamy, M. Takase, K. Yamauchi, H. Wakabayashi, K. Kawase, and M. Tomita, “Identification of the bactericidal domain of lactoferrin,” Biochimica et Biophysica Acta, vol. 1112, no. 1-2, pp. 130–136, 1992.
  38. Y. C. Yoo, R. Watanabe, Y. Koike et al., “Apoptosis in human leukemic cells induced by lactoferricin, a bovine milk protein-devived peptide: involvement of reactive oxygen species,” Biochemical and Biophysical Research Communications, vol. 237, no. 3, pp. 624–628, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. L. T. Eliassen, G. Berge, B. Sveinbjørnsson, J. S. Svendsen, L. H. Vorland, and Ø. Rekdal, “Evidence for a direct antitumor mechanism of action of bovine lactoferricin,” Anticancer Research, vol. 22, no. 5, pp. 2703–2710, 2002. View at Scopus
  40. J. S. Mader, J. Salsman, D. M. Conrad, and D. W. Hoskin, “Bovine lactoferricin selectively induces apoptosis in human leukemia and carcinoma cell lines,” Molecular Cancer Therapeutics, vol. 4, no. 4, pp. 612–624, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. L. T. Eliassen, G. Berge, A. Leknessund et al., “The antimicrobial peptide, Lactoferricin B, is cytotoxic to neuroblastoma cells in vitro and inhibits xenograft growth in vivo,” International Journal of Cancer, vol. 119, no. 3, pp. 493–500, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. S. J. Furlong, J. S. Mader, and D. W. Hoskin, “Lactoferricin-induced apoptosis in estrogen-nonresponsive MDA-MB-435 breast cancer cells is enhanced by C6 ceramide or tamoxifen,” Oncology reports., vol. 15, no. 5, pp. 1385–1390, 2006. View at Scopus
  43. M. D. Burdick, A. Harris, C. J. Reid, T. Iwamura, and M. A. Hollingsworth, “Oligosaccharides expressed on MUC1 by pancreatic and colon tumor cell lines,” Journal of Biological Chemistry, vol. 272, no. 39, pp. 20202–24198, 1997.
  44. J. W. Dennis, “N-linked oligosaccharide processing and tumor cell biology,” Seminars in Cancer Biology, vol. 2, no. 6, pp. 411–420, 1991.
  45. T. Utsugi, A. J. Schroit, J. Connor, C. D. Bucana, and I. J. Fidler, “Elevated expression of phosphatidylserine in the outer membrane leaflet of human tumor cells and recognition by activated human blood monocytes,” Cancer Research, vol. 51, no. 11, pp. 3062–3066, 1991. View at Scopus
  46. I. Dobrzyńska, B. Szachowicz-Petelska, S. Sulkowski, and Z. Figaszewski, “Changes in electric charge and phospholipids composition in human colorectal cancer cells,” Molecular and Cellular Biochemistry, vol. 276, no. 1-2, pp. 113–119, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. W. H. Yoon, H. D. Park, K. Lim, and B. D. Hwang, “Effect of O-glycosylated mucin on invasion and metastasis of HM7 human colon cancer cells,” Biochemical and Biophysical Research Communications, vol. 222, no. 3, pp. 694–699, 1996. View at Publisher · View at Google Scholar · View at Scopus
  48. L. T. Eliassen, B. E. Haug, G. Berge, and Ø. Rekdal, “Enhanced antitumour activity of 15-residue bovine lactoferricin derivatives containing bulky aromatic amino acids and lipophilic N-terminal modifications,” Journal of Peptide Science, vol. 9, no. 8, pp. 510–517, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. N. Yang, M. B. Strøm, S. M. Mekonnen, J. S. Svendsen, and Ø. Rekdal, “The effects of shortening lactoferrin derived peptides against tumour cells, bacteria and normal human cells,” Journal of Peptide Science, vol. 10, no. 1, pp. 37–46, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. J. L. Gifford, H. N. Hunter, and H. J. Vogel, “Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties,” Cellular and Molecular Life Sciences, vol. 62, no. 22, pp. 2588–2598, 2005. View at Publisher · View at Google Scholar
  51. S. Riedl, B. Rinner, S. Tumer, H. Schaider, K. Lohner, and D. Zweytick, “Targeting the cancer cell membrane specifically with human lactoferricin derivatives,” Annals of Oncology, vol. 22, pp. 31–34, 2011. View at Publisher · View at Google Scholar
  52. E. Staudegger, E. J. Prenner, M. Kriechbaum et al., “X-ray studies on the interaction of the antimicrobial peptide gramicidin S with microbial lipid extracts: evidence for cubic phase formation,” Biochimica et Biophysica Acta, vol. 1468, no. 1-2, pp. 213–230, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Willumeit, M. Kumpugdee, S. S. Funari et al., “Structural rearrangement of model membranes by the peptide antibiotic NK-2,” Biochimica et Biophysica Acta, vol. 1669, no. 2, pp. 125–134, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Hickel, S. Danner-Pongratz, H. Amenitsch et al., “Influence of antimicrobial peptides on the formation of nonlamellar lipid mesophases,” Biochimica et Biophysica Acta, vol. 1778, no. 10, pp. 2325–2333, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Zweytick, S. Tumer, S. E. Blondelle, and K. Lohner, “Membrane curvature stress and antibacterial activity of lactoferricin derivatives,” Biochemical and Biophysical Research Communications, vol. 369, no. 2, pp. 395–400, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Zweytick, G. Deutsch, J. Andrä et al., “Studies on Lactoferricin-derived Escherichia coli membrane-active peptides reveal differences in the mechanism of N-acylated versus nonacylated peptides,” Journal of Biological Chemistry, vol. 286, no. 24, pp. 21266–21276, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. J. S. Mader, A. Richardson, J. Salsman et al., “Bovine lactoferricin causes apoptosis in Jurkat T-leukemia cells by sequential permeabilization of the cell membrane and targeting of mitochondria,” Experimental Cell Research, vol. 313, no. 12, pp. 2634–2650, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Onishi, M. K. Roy, L. R. Juneja, Y. Watanabe, and Y. Tamai, “A lactoferrin-derived peptide with cationic residues concentrated in a region of its helical structure induces necrotic cell death in a leukemic cell line (HL-60),” Journal of Peptide Science, vol. 14, no. 9, pp. 1032–1038, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. S. J. Furlong, J. S. Mader, and D. W. Hoskin, “Bovine lactoferricin induces caspase-independent apoptosis in human B-lymphoma cells and extends the survival of immune-deficient mice bearing B-lymphoma xenografts,” Experimental and Molecular Pathology, vol. 88, no. 3, pp. 371–375, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. J. S. Mader, D. Smyth, J. Marshall, and D. W. Hoskin, “Bovine lactoferricin inhibits basic fibroblast growth factor- and vascular endothelial growth factor165-induced angiogenesis by competing for heparin-like binding sites on endothelial cells,” American Journal of Pathology, vol. 169, no. 5, pp. 1753–1766, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. D. W. Hoskin and A. Ramamoorthy, “Studies on anticancer activities of antimicrobial peptides,” Biochimica et Biophysica Acta, vol. 1778, no. 2, pp. 357–375, 2008. View at Publisher · View at Google Scholar