Peptides from water buffalo cheese whey induced senescence cell death via ceramide secretion in human colon adenocarcinoma cell line

Molecular Nutrition and Food Research

Volumn 55, Issue 2, 2011, Pages 229-238

  De Simone, Carmela ^a   Ferranti, Pasquale ^a   Picariello, Gianluca ^b   Scognamiglio, Ilaria ^c   Dicitore, Alessandra ^c   Addeo, Francesco ^a   Chianese, Lina ^a   Stiuso, Paola ^c  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CNR   (Italy)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Antioxidant; Human epithelial colon cancer; Mozzarella cheese whey; MS; Sphingolipids

Indexed keywords

BIOLOGICAL MARKER; CERAMIDE; CYCLIN A; HEAT SHOCK PROTEIN; MILK PROTEIN; OXIDIZING AGENT; PEPTIDE; PROTECTIVE AGENT; WHEY PROTEIN;

ANIMAL; ARTICLE; BUFFALO; CELL CYCLE; CELL DEATH; CELL STRAIN CACO 2; CHEMISTRY; DIET SUPPLEMENTATION; DRUG EFFECT; ECONOMICS; FEMALE; FOOD INDUSTRY; HUMAN; INDUSTRIAL WASTE; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; METABOLISM; OXIDATIVE STRESS; SECRETION;

ANIMALS; BIOLOGICAL MARKERS; BUFFALOES; CACO-2 CELLS; CELL CYCLE; CELL DEATH; CERAMIDES; CYCLIN A; DIETARY SUPPLEMENTS; FEMALE; FOOD-PROCESSING INDUSTRY; HEAT-SHOCK PROTEINS; HUMANS; INDUSTRIAL WASTE; INTESTINAL MUCOSA; MILK PROTEINS; OXIDANTS; OXIDATIVE STRESS; PEPTIDES; PROTECTIVE AGENTS;

BUBALUS;

EID: 79551536213     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201000074     Document Type: Article

References (62)

1. Miller, D. L., Hanson, W., Schedl, H. P., Osborne, J. W., Proliferation rate and transit time of mucosal cells in small intestine of the diabetic rat. Gastroenterology 1977, 7, 1326-1332.
2. Tak, Y. A., Molecular and cellular responses to oxidative stress and changes in oxidation-reduction imbalance in the intestine. Am. J. Clin. Nutr. 1999, 70, 557-565.
3. Ames, B., Dietary carcinogens and anticarcinogens. Science 1983, 221, 1256-1263.
4. Hoidal, J. R., Reactive oxygen species and cell signaling. Am. J. Respir. Cell. Mol. Biol. 2001, 25, 661-663.
5. Cepinskas, G., Kvietys, P. R., Aw, T. Y., The cytotoxicity of peroxidized omega-3 lipids on cultured human epithelial cells is related to the development of cellular GSH-dependent antioxidant systems. Gastroenterology 1994, 107, 80-86.
6. Tak, Y. A., Molecular and cellular responses to oxidative stress and changes in oxidation-reduction imbalance in the intestine. Am. J. Clin. Nutr. 1999, 70, 557-565.
7. Musch, M. W., Kaplan, B., Chang, E. B., Role of increased basal expression of heat shock protein 72 in colonic epithelial c2BBE adenocarcinoma cells. Cell Growth Differ. 2001, 12, 419-426.
8. Beere, H. M., Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J. Clin. Invest. 2005, 115, 2633-2639.
9. Kondo, T., Matsuda, T., Kitano, T., Takahashi, A. et al., Role of c-jun expression increased by heat shock- and ceramide-activated caspase-3 in HL-60 cell apoptosis. Possible involvement of ceramide in heat shock-induced apoptosis. J. Biol. Chem. 2000, 275, 7668-7676.
10. Bose, R., Verheij, M., Haimovitz-Friedman, A., Scotto, K. et al., Ceramide synthase mediates daunorubicin-induced apoptosis: an alternative mechanism for generating death signals. Cell 1995, 3, 405-414.
11. Senchenkov, A., Litvak, D. A., Cabot, M. C., Targeting ceramide metabolism - a strategy for overcoming drug resistance. J. Natl. Cancer Inst. 2001, 5, 347-357.
12. von Haefen, C., Wieder, T., Gillissen, B., Stärck, L. et al., Ceramide induces mitochondrial activation and apoptosis via a Bax-dependent pathway in human carcinoma cells. Oncogene 2002, 25, 4009-4019.
13. Jones, B. E., Lo, C. R., Srinivasan, A., Valentino, K. L. et al., Ceramide induces caspase-independent apoptosis in rat hepatocytes sensitized by inhibition of RNA synthesis. Hepatology 1999, 1, 215-222.
14. Ping, S. E., Barrett, G. L., Ceramide can induce cell death in sensory neurons, whereas ceramide analogues and sphingosine promote survival. J. Neurosci. Res. 1998, 2, 206-213.
15. Selzner, M., Bielawska, A., Morse, M. A., Rüdiger, H. A. et al., Induction of apoptotic cell death and prevention of tumor growth by ceramide analogues in metastatic human colon cancer. Cancer Res. 2001, 3, 1233-1240.
16. Lim, C. S., Campisi, J., Recent advances in cellular senescence, cancer and aging. Biotechnol. Bioprocess Eng. 2001, 6, 231-236.
17. Di Leonardo, A., Linke, S. P., Clarkin, K., Wahl, G. M., DNA damage triggers a prolonged p53-dependent G1 arrest and long-termed induction of Cip1 in normal human fobroblast. Genes Dev. 1994, 8, 2540-2551.
18. Johnson, I. T., Anticarcinogenic effects of diet-related apoptosis in the colorectal mucosa. Food Chem. Toxicol. 2002, 40, 1171-1178.
19. Ruemmele, F. M., Schwartz, S., Seidman, E. G., Dionne, S. et al., Butyrate induced Caco-2 cell apoptosis is mediated via the mitochondrial pathway. Gut 2003, 52, 94-100.
20. Buda, A., Qualtrough, D., Jepson, M. A., Martines, D. et al., Butyrate downregulates alpha2beta1 integrin: a possible role in the induction of apoptosis in colorectal cancer cell lines. Gut 2003, 52, 729-734.
21. Yang, K., Lamprecht, S. A., Lui, Y., Shinozaki, H. et al., Chemoprevention studies of the flavonoids quercetin and rutin in normal and azoxymethane-treated mouse colon. Carcinogenesis 2000, 21, 1655-1660.
22. Smith, T. K., Mithen, R., Johnson, I. T., Effects of Brassica vegetable juice on the induction of apoptosis and aberrant crypt foci in rat colonic mucosal crypts in vivo. Carcinogenesis 2003, 24, 491-495.
23. Silva, S. V., Xavier Malcata, F., Caseins as source of bioactive peptides. Int. Dairy J. 2005, 15, 1-15.
24. Cervato, G., Cazzola, R., Cestaro, B., Studies on the antioxidant activity of milk caseins. Int. J. Food Sci. Nutr. 1999, 50, 291-296.
25. Chen, J., Lindmark- Mánsson, H., Gorton, L., Akesson, B., Antioxidant capacity of bovine milk as assayed by spectrophotometric and amperometric methods. Int. Dairy J. 2003, 13, 927-935.
26. Suetsuna, K., Ukeda, H., Ochi, H., Isolation and characterization of free radical scavenging activities peptides derived from casein. J. Nutr. Biochem. 2000, 11, 128-131.
27. Pñea-Ramos, E. A., Xiong, Y. L., Arteaga, G. E., Fractionation and characterisation for antioxidant activity of hydrolysed whey protein. J. Sci. Food Agric. 2004, 84, 1908-1918.
28. Rival, S. G., Fornaroli, S., Boeriu, C. G., Wichers, H. J., Caseins casein hydrolysates. 1. Lipoxygenase inhibitory properties. J. Agric. Food Chem. 2001, 49, 287-294.
29. Roy, M. K., Wanatabe, Y., Tamai, Y., Induction of apoptosis in HL-60 cells by skimmed milk digested with a proteolytic enzyme from the yeast Saccharomyces cerevisiae. J. Biosci. Bioeng. 1999, 88, 426-432.
30. Svensson, M., Hakansson, A., Mosseberg, A. K., Linse, S. et al., Conversion of α-lactoalbumin to a protein inducing apoptosis. Proc. Natl. Acad. Sci. USA 2000, 97, 4221-4226.
31. Roy, M. K., Kuwabara, Y., Hara, K., Wanatabe, Y. et al., Peptides from the N-terminal end of bovine lactoferrin induce apoptosis in human leukemic (HL-60) cells. J. Dairy Sci. 2002, 85, 2065-2074.
32. De Simone, C., Picariello, G., Mamone, G., Stiuso, P. et al., Characterisation and cytomodulatory properties of peptides from Mozzarella di Bufala Campana cheese whey. J. Pept. Sci. 2009, 15, 251-258.
33. Herz, F., Scherner, A., Halwer, M., Bogart, L. H., Alkaline phospatase in HT-29, a human colon cancer cell line: influence of sodium butyrate and hyperosmolality. Arch. Biochem. Biophys. 1981, 210, 581-591.
34. Musch, M. W., Kaplan, B., Chang, E. B., Role of increased basal expression of heat shock protein 72 in colonic epithelial c2BBE adenocarcinoma cells. Cell Growth Differ. 2001, 12, 419-426.
35. Obeid, L. M., Linardic, C. M., Karolak, L. A., Hannun, Y. A., Programmed cell death induced by ceramide. Science 1993, 259, 1769-1771.
36. Motta, S., Monti, M., Sesana, S., Caputo, R. et al., Ceramide composition of the psoriatic scale. Biochim. Biophyis. Acta 1993, 1182, 147-151.
37. Yamb, C. H., Funga, T. K., Poon, R. Y. C., Cyclin A in cell cycle control and cancer. Cell Mol. Life Sci. 2002, 59, 1317-1326.
38. Campisi, J., The biology of replicative senescence. Eur. J. Cancer 1997, 33, 703-709.
39. Levy, E., Mehran, M., Seidman, E., Caco-2 cells as a model for intestinal lipoprotein synthesis and secretion. FASEB J. 1995, 9, 626-635.
40. Fruman, D. A., Meyers, R. E., Cantley, L. C., Phosphoinositide kinases. Annu. Rev. Biochem. 1998, 67, 481-507.
41. Vanhaesebroeck, B., Waterfield, M. D., Signaling by distinct classes of phosphoinositide 3-kinases. Exp Cell Res. 1999, 253, 239-254.
42. Semba, S., Itoh, N., Ito, M., Youssef, E. M. et al., Down-regulation of PI3KCG, a catalytic subunit of phosphoinositol 3-OH kinase, by CpG hypermethylation in human colorectal carcinoma. Clin. Cancer Res. 2002, 8, 3824-3831.
43. Roy, H. K., Olusola, B. F., Clemens, D. L., Karolski, W. J. et al., AKT proto-oncogene overexpression is an early event during sporadic colon carcinoma. Carcinogenesis 2002, 23, 201-205.
44. Khaleghpour, K., Li, Y., Banville, D., Yu, Z. et al., Involvement of the PI 3-kinase signaling pathway in progression of colon adenocarcinoma. Carcinogenesis 2004, 25, 241-248.
45. Itoh, N., Semba, S., Ito, M., Takeda, H. et al., Phosphorylation of Akt/PKB is required for suppression of cancer cell apoptosis and tumor progression in human colorectal carcinoma. Cancer 2002, 94, 3127-3134.
46. Nicolas, M., Tritton, T. R., Laurent, G., Jaffrézou, J. P., Cell surface-directed interaction of anthracyclines leads to cytotoxicity and nuclear factor κB activation but not apoptosis signaling. Cancer Res. 2001, 61, 2558-2561.
47. El-Assaad, W., Kozhaya, L., Araysi, S., Panjarian, S. et al., Ceramide and glutathione define two independently regulated pathways of cell death initiated by p53 in Molt-4 leukaemia cells. Biochem. J. 2003, 376, 725-732.
48. Oh, W. J., Kim, W. H., Kang, K. H., Kim, T. Y. et al., Induction of p21 during ceramide-mediated apoptosis in human hepatocarcinoma cells. Cancer Lett. 1998, 129, 215-222.
49. Itoh, M., Kitano, T., Watanabe, M., Kondo, T. et al., Possible role of ceramide as an indicator of chemoresistance: decrease of the ceramide content via activation of glucosylceramide synthase and sphingomyelin synthase in chemoresistant leukemia. Clin. Cancer Res. 2003, 9, 415-423.
50. Hannun, Y. A., Functions of ceramide in coordinating cellular response to stress. Science 1996, 274, 1855-1859.
51. Witty, J. P., Bridgham, J. T., Johnson, A., Induction of apoptotic cell death in hen granulosa cells by ceramide. Endocrinology 1996, 137, 5269-5277.
52. Hannun, Y. A., Obeid, L. M., Ceramide: an intracellular signal for apoptosis. Trends Biochem. Sci. 1995, 20, 73-77.
53. Roninson, I. B., Dokmanovic, M., Induction of senescence-associated growth inhibitors in the tumor-suppressive function of retinoids. J. Cell. Biochem. 2003, 88, 83-94.
54. Meisel, H., Biochemical properties of peptides encrypted in bovine milk proteins. Curr. Med. Chem. 2005, 12, 1915-1919.
55. Meisel, H., FitzGerald, J., Biofunctional peptides from milk proteins: mineral binding and cytomodulatory effects. Curr. Pharm. Des. 2003, 9, 1289-9125.
56. Ferranti, P., Traisci, M. V., Picariello, G., Nasi, A. et al., Casein proteolysis in human milk: tracing the pattern of casein breakdown and the formation of potential bioactive peptides. J. Dairy Res. 2004, 71, 74-87.
57. Onishi, J., Roy, M. K., Juneja, L. R., Wanatabe, Y. et al., 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). J. Pept. Sci. 2008, 14, 1032-1038.
58. Bodana, A. R., Rao, D. R., Antimutagenic activity of milk fermented by Streptococcus thermophilus and Lactobacillus bulgaricus. J. Dairy Sci. 1990, 73, 3379-3384.
59. Hosoda, M., Hashimoto, H., Morita, H., Chiba, M. et al., Antimutagenicity of milk cultured with lactic acid bacteria against N-methyl-N'-nitro-N-nitrosoguanidine. J. Dairy Sci. 1992, 75, 976-981.
60. Maneckjee, R., Biswas, R., Vonderhaar, B. K., Binding of opioids to human MCF-7 breast cancer cells, and their effects on growth. Cancer Res. 1990, 50, 2234-2238.
61. Hatzglou, A., Bakogeorgou, E., Castanas, E., The antiproliferative effect of opioid agonists on the T47D human breast cancer cell line, is partially mediated through opioid receptors. Eur. J. Pharmacol. 1996, 296, 199-207.
62. Reubi, J. C., Laiussue, J., Waser, B., Horisberger, U. et al., Expression of somatostatin receptors in normal, inflamed, and neoplastic human gastrointestinal tissues. Ann. NY Acad. Sci. 1994, 733, 122-137.