Czech J. Food Sci., 2019, 37(1):29-35 | DOI: 10.17221/221/2018-CJFS

In vitro cytotoxic and genotoxic effects of donkey milk on lung cancer and normal cells linesFood Microbiology and Safety

Cetin Akca, Ozgur Vatan, Dilek Yilmaz, Huzeyfe Huriyet, Nilüfer Cinkilic, Tolga Cavas*
Department of Biology, Cell Culture and Genetic Toxicology Laboratory, Faculty of Arts and Sciences, Uludag University, Bursa, Turkey

In vitro cytotoxic and genotoxic effects of donkey milk on cancer (A549) and normal (BEAS-2B) lung cell lines were investigated. The XTT and WST-1 tests as well as clonogenic assays were used to evaluate cytotoxicity. The comet assay and micronucleus test were used as genotoxicity endpoints. Donkey milk showed lower cytotoxic effects against normal lung cell line BEAS-2B in comparison to the tumor cell line A549. Genotoxicity experiments revealed dose dependent increases in the frequencies of micronuclei and single stranded DNA breaks in A549 cells whereas no significant damage was observed in BEAS-2B cells. The results indicate that donkey milk has anti-proliferative and genotoxic effects on lung cancer cells at concentrations which are non-toxic to normal lung cells.

Keywords: anti-cancer; cytotoxicity; jenny milk; genotoxicity; in vitro

Published: February 28, 2019  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Akca C, Vatan O, Yilmaz D, Huriyet H, Cinkilic N, Cavas T. In vitro cytotoxic and genotoxic effects of donkey milk on lung cancer and normal cells lines. Czech J. Food Sci.. 2019;37(1):29-35. doi: 10.17221/221/2018-CJFS.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Al Ahmad M., Al Natour Z., Mustafa F., Rizvi T. (2018): Electrical characterization of normal and cancer cells. IEEE Access, 6: 25979-25986. doi: 10.1109/ACCESS.2018.2830883 Go to original source...
    2. Amati L., Marzulli M., Martulli M., Tafaro A., Jirillo F., Pugliese V., Martemucci G., D'Alesandro A.G., Jirillo E. (2010): Donkey and goat milk intake and modulation of the human aged immune response. Current Pharmaceutical Design, 16: 864-869. Go to original source... Go to PubMed...
    3. Anandhini B., Palaniswamy M. (2013): Anticancer effect of goat milk fermented by Lactobacillus plantarum and Lactobacillus paracasei. International Journal of Pharmacy and Pharmaceutical Sciences, 5(3): 813-828.
    4. Araya C., Lomonte B. (2007): Antitumor effects of cationic synthetic peptides derived from Lys49 phospholipase A2 homologues of snake venoms. Cell Biology International, 31: 263-268. Go to original source... Go to PubMed...
    5. Cavas T., Cinkilic N., Vatan O., Yilmaz D. (2014): Effects of fullerenol nanoparticles on acetamiprid induced cytoxicity and genotoxicity in cultured human lung fibroblasts. Pesticide Biochemistry and Physiology, 114: 1-7. Go to original source... Go to PubMed...
    6. Chiofalo B., Dugo P., Bonaccorsi I.L., Mondello L. (2011): Comparison of major lipid components in human and donkey milk: new perspectives for a hypoallergenic diet in humans. Immunopharmacology and Immunotoxicology, 33: 633-644. Go to original source... Go to PubMed...
    7. Clementi E.A., Wilhelm K.R., Schleucher J., MorozovaRoche L.A., Hakansson A.P. (2013): A complex of equine lysozyme and oleic acid with bactericidal activity against Streptococcus pneumoniae. PLoS ONE, 8: e80649. doi: 10.1371/journal.pone.0080649 Go to original source... Go to PubMed...
    8. Cunsolo V., Saletti R., Muccilli V., Foti S. (2007): Characterization of the protein profile of donkey's milk whey fraction. Journal of Mass Spectrometry, 42: 1162-1174. Go to original source... Go to PubMed...
    9. Ertel A., Verghese A., Byers S.W., Ochs M., Tozeren A. (2006): Pathway-specific differences between tumor cell lines and normal and tumor tissue cells. Molecular Cancer, 5: 55. Go to original source... Go to PubMed...
    10. Fang B., Zhang M., Tian M., Jiang L., Guo H.Y., Ren F.Z. (2014): Bovine lactoferrin binds oleic acid to form an anti-tumor complex similar to HAMLET. Biochimica et Biophysica Acta. 1841: 535-453. Go to original source... Go to PubMed...
    11. Fantuz F., Vincenzetti S., Polidori P., Vita A., Polidori F., Salimei E. (2001): Study on the protein fractions of donkey milk. In: Proceedings of the XIV A.S.P.A. Congress. Firenze, Italy: 635-637.
    12. Furlong S.J., Mader J.S., Hoskin D.W. (2010): 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, 88: 371-375. Go to original source... Go to PubMed...
    13. Ganjam L.S., Thornton W.H., Marshall R.T., McDolands R.S. (1997): Antiproliferative effects of yogurt fractions obtained by membrane dialysis on cultured mammalian intestinal cells. Journal of Dairy Science, 80: 2325-2329. Go to original source... Go to PubMed...
    14. Gill H.S., Cross M.L. (2000): Anticancer properties of bovine milk. British Journal of Nutrition, 84: 161-166. Go to original source... Go to PubMed...
    15. Habib H.M., Ibrahim W.H., Schneider-Stock R., Hassan H.M. (2013): Camel milk lactoferrin reduces the proliferation of colorectal cancer cells and exerts antioxidant and DNA damage inhibitory activities. Food Chemistry, 141: 148-152. Go to original source... Go to PubMed...
    16. Host A. (2002): Frequency of cow's milk allergy in childhood. Annals of Allergy, Asthma & Immunology, 89: 33-337. Go to original source... Go to PubMed...
    17. Huang Y., Feng Q.I., Yan Q., Hao X., Chen Y. (2015): Alpha-helical cationic anticancer peptides: a promising candidate for novel anticancer drugs. Mini Reviews in Medicinal Chemistry, 15: 73-81. Go to original source... Go to PubMed...
    18. Korashy H.M., Maayah Z.H., Abd-Allah A.R., El-Kadi A.O.S., Alhaider A.A. (2012): Camel milk triggers apoptotic signaling pathways in human hepatoma HepG2 and breast cancer MCF7 cell lines through transcriptional mechanism. Journal of Biomedicine and Biotechnology, 593195. doi: 10.1155/2012/593195. Go to original source... Go to PubMed...
    19. Kumbicak U., Cavaº T., Cinkiliç N., Kumbiçak Z., Vatan O., Yilmaz D. (2014): Evaluation of in vitro cytotoxicity and genotoxicity of copper-zinc alloy nanoparticles in human lung epithelial cells. Food and Chemical Toxicology, 73: 105-112. Go to original source... Go to PubMed...
    20. Laursen I., Briand P., Lykkesfeldt A.E. (1990): Serum albumin as a modulator on growth of the human breast cancer cell line MCF-7. Anticancer Research, 10: 343-351.
    21. Lionetti L., Cavaliere G., Bergamo P., Trinchese G., De Filippo C., Gifuni G., Gaita M., Pignalosa A., Donizzetti I., Putti R., Di Palo R., Barletta A., Mollica M.P. (2012): Diet supplementation with donkey milk upregulates liver mitochondrial uncoupling, reduces energy efficiency and improves antioxidant and anti-inflammatory defenses in rats. Molecular Nutrition & Food Research, 56: 1596-1600. Go to original source... Go to PubMed...
    22. Lopez-Exposito I., Recio I. (2008): Protective effect of milk peptides: Antibacterial and antitumor proteins. Advances in Experimental Medicine and Biology, 606: 271-293. Go to original source... Go to PubMed...
    23. Ma J., Guan R., Shen H., Lu F., Xiai C., Liu M., Kang T. (2013): Comparison of anticancer activity between lactoferrinnanoliposome and lactoferrin in Caco-2 cells in vitro. Food and Chemical Toxicology, 59: 72-77. Go to original source... Go to PubMed...
    24. Mader J.S., Salsman J., Conrad D.M., Hoskin D.W. (2005): Bovine lactoferricin selectively induces apoptosis in human leukemia and carcinoma cell lines. Molecular Cancer Therapeutics, 4: 612-624. Go to original source... Go to PubMed...
    25. Mahanta S., Paul S. (2015): Stable self-assembly of bovine α-lactalbuminexhibits target-specific antiproliferativeactivity in multiple cancer cells. ACS Applied Materials and Interfaces, 7: 28177-28187. Go to original source... Go to PubMed...
    26. Malihe Shariatikia M., Behbahani M., Mohabatkar H. (2017): Anticancer activity of cow, sheep, goat, mare, donkey and camel milks and their caseins and whey proteins and in silico comparison of the caseins. Molecular Biology Research Communications, 6: 57-64.
    27. Mao X., Gu J., Sun Y., Xu S., Zhang X., Yang H., Ren F. (2009): Anti-proliferative and anti-tumor effect of active components in donkey milk on A549 human lung cancer cells. International Dairy Journal, 19: 703-708. Go to original source...
    28. Nielsen S.B., Wilhelm K., Vad B., Schleucher J., Morozova-Roche L.A., Otzen D. (2010): The interaction of equine lysozyme:oleic acid complexes with lipid membranes suggests a cargo off-loading mechanism. Journal of Molecular Biology, 398: 351-361. Go to original source... Go to PubMed...
    29. Parodi P.W. (2007): A role for milk proteins and their peptides in cancer prevention. Current Pharmaceutical Design, 13: 813-828. Go to original source... Go to PubMed...
    30. Pepe G., Tenore G.C., Mastrocinque R., Stusio P., Campiglia P. (2013): Potential Anticarcinogenic peptides from bovine milk. Journal of Amino Acids. vol. 2013, Article ID 939804, 7 pages. doi 10.1155/2013/939804 Go to original source... Go to PubMed...
    31. Polidori P., Vincenzetti S. (2012): Protein profile characterization of donkey milk. In: Hurley W. (ed.): Milk Protein. IntechOpen: 215-232. Go to original source...
    32. Praveesh B.V., Angayarkanni J., Palaniswamy M. (2011): Antihypertensive and anticancer effect of cow milk fermented by Lactobacillus plantarum and Lactobacillus paracasei. International Journal of Pharmacy and Pharmaceutical Sciences, 3: 452-456.
    33. Quita Salwa M., Kurdi Lina A.F. (2010): Antigenotoxic and anticytotoxic effect of camel milk in mice treated with cisplatin. Saudi Journal of Biological Sciences, 17: 159-166. Go to original source... Go to PubMed...
    34. Rahmat A., Rosli R., Hoon T.M., Umar-Tsafe N., Ali A.M., Abu Bakar M.F. (2006): Comparative evaluation of cytotoxic effects of milk from various species on leukemia cell lines. Malaysian Journal Of Medicine And Health Sciences, 2: 1-10.
    35. Sah B.N.P., Vasiljevic T., McKechnie S., Donkot O.N. (2015): Identification of anticancer peptides from bovine milk proteins and their potential roles in management of Cancer: A critical review. Comprehensive Reviews in Food Science and Food Safety, 14: 123-138. Go to original source... Go to PubMed...
    36. Sternhagen L.G., Allen J.C. (2001): Growth rates of a human colon adenocarcinoma cell line are regulated by the milk protein alpha-lactalbumin. Advances in Experimental Medicine and Biology, 50: 115-120. Go to original source... Go to PubMed...
    37. Singh N.P., McCoy M.T., Tice R.R., Schneider E.L. (1988): A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research, 175: 184-191. Go to original source... Go to PubMed...
    38. Svensson M., Sabharwal H., Hakansson A., Mossberg A.K., Lipniunas P., Leffler H., Svanborg C., Linse S. (1999): Molecular characterization of a-lactalbumin folding variants that induce apoptosis in tumor cells. The Journal of Biological Chemistry. 274: 6388-6396. Go to original source... Go to PubMed...
    39. Szachowicz-Petelska B., Dobrzynska I., Sulkowski S., Figaszewski Z.A. (2010): Characterization of the cell membrane during cancer transformation. Journal of Environmental Biology, 31: 845-850.
    40. Wilhelm K., Darinskas A., Noppe W., Duchardt E., Mok K.H., Vukojevic V., Schleucher J., Morozova-Roche L.A. (2009): Protein oligomerization induced by oleic acid at the solid- liquid interface: equine lysozyme cytotoxic complexes. The FEBS Journal, 276: 3975-3989. Go to original source... Go to PubMed...
    41. Wise S.S., Holmes A.L., Qin Q., Hong X., Katsifis S.P., Thompson W.D., Wise Sr J.P. (2010): Comparative genotoxicity and cytotoxicity of four hexavalent chromium compounds in human bronchial cells. Chemical Research in Toxicology, 23: 365-372. Go to original source... Go to PubMed...
    42. Yoo Y.C., Watanabe R., Koike Y., Mitobe M., Shimazaki K., Watanabe S., Azuma I. (1997): Apoptosis in human leukemic cells induced by lactoferricin, a bovine milk protein-derived peptide: involvement of reactive oxygen species. Biochemical and Biophysical Research Communications, 237: 624-628. Go to original source... Go to PubMed...
    43. Zhang Y., Lima C.F., Rodrigues L.R. (2015): In vitro evaluation of bovine lactoferrin potential as an anticancer agent. Indian Journal of Dairy Science, 40: 6-15. Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content