Probiotic bacteria grown with chestnut honey enhance in vitro cytotoxicity on breast and colon cancer cells
Keywords:auto-aggregation, chestnut honey, cytotoxicity, Lactobacillus, MCF-7 cell line, Caco-2 cell line, surface hydrophobicity
- Probiotics can exert health benefits and with other food constituents their health effects can be improved. This study investigated the effects of chestnut honey on probiotic bacteria, and the in vitro cytotoxic effects on breast and colon cancer cells.
- Auto-aggregation and surface hydrophobicity tests for Lactobacillus acidophilus LA-5 and Lactobacillus rhamnosus GG were performed, and viabilities of MCF-7 and Caco-2 cells were examined by the MTT assay.
- Chestnut honey positively modulated the probiotic properties. Probiotics grown on honey exhibited cytotoxic effects on breast and colon cancer cells.
- Combinations of honey and probiotics have the potential to formulate new nutraceuticals.
Abstract: Chestnut honey has been used as ethnomedicine. Probiotics are defined as live microorganisms that can provide a health benefit, impeding the development of several health conditions and diseases, including cancer. This study aims to investigate the effects of chestnut honey on probiotic bacteria and the in vitro cytotoxic effects of the combination of probiotics and chestnut honey on cancer cells. First, the effects of chestnut honey on the growth of bacteria were examined, followed by its effects on the probiotic properties of Lactobacillus acidophilus LA-5 and Lactobacillus rhamnosus GG. Once the bacteria had grown on chestnut honey, the in vitro cytotoxic effects on breast and colon cancer cell lines, MCF-7 and Caco-2, respectively, and a non-cancerous breast epithelial cell line, MCF-10A, were investigated. Chestnut honey positively affected the probiotic bacteria by increasing the growth and modulating probiotic properties such as autoaggregation and surface hydrophobicity. Furthermore, probiotics grown on chestnut honey had more cytotoxic effects on the cancer cell lines than probiotics or honey alone. The present study showed that new combinations of honey and probiotics have the potential to formulate new nutraceuticals.
Received: June 14, 2020; Revised: June 19, 2020; Accepted: June 20, 2020; Published online: June 23, 2020
How to cite this article: Celebioglu HU. Probiotic bacteria grown with chestnut honey enhance in vitro cytotoxicity on breast and colon cancer cells. Arch Biol Sci. 2020;72(3):329-38.
Can Z, Yildiz O, Sahin H, Akyuz Turumtay E, Silici S, Kolayli S. An investigation of Turkish honeys: Their physico-chemical properties, antioxidant capacities and phenolic profiles. Food Chem. 2015;180:133-41.
Hellner M, Winter D, Von Georgi R, Munstedt K. Apitherapy: Usage and experience in German beekeepers. Evidence-based Complement Altern Med. 2008;5(4):475-9.
Sahinler N, Sahinler S, Gul A. Biochemical composition of honeys produced in Turkey. J Apic Res. 2004;43(2):53-6.
Kucuk M, Kolayli S, Karaoglu S, Ulusoy E, Baltaci C, Candan F. Biological activities and chemical composition of three honeys of different types from Anatolia. Food Chem. 2007;100(2):526-34.
Sahin H, Aliyazicioglu R, Yildiz O, Kolayli S, Innocenti A, Supuran CT. Honey, pollen, and propolis extracts show potent inhibitory activity against the zinc metalloenzyme carbonic anhydrase. J Enzyme Inhib Med Chem. 2011;26(3):440-4.
Tezcan F, Kolayli S, Ulusoy HSE, Erim FB. Evaluation of organic acid, saccharide composition and antioxidant properties of some authentic Turkish honeys. J Food Nutr Res. 2011;50(1):33-40.
Robin C, Morel O, Vettraino AM, Perlerou C, Diamandis S, Vannini A. Genetic variation in susceptibility to Phytophthora cambivora in European chestnut (Castanea sativa). For Ecol Manage. 2006;226(1-3):199-207.
Sarikaya AO, Ulusoy E, OztUrk N, Tuncel M, Kolayli S. Antioxidant activity and phenolic acid constituents of chestnut (Castania Sativa Mill.) Honey and Propolis. J Food Biochem. 2009;33(4):470-81.
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11:506-14.
González-Rodríguez I, Ruiz L, Gueimonde M, Margolles A, Sánchez B. Factors involved in the colonization and survival of bifidobacteria in the gastrointestinal tract. FEMS Microbiol Lett. 2013;340(1):1-10.
Capurso L. Thirty years of Lactobacillus rhamnosus GG A Review. J Clin Gastroenterol. 2019;53:S1-41.
Gill H, Prasad J. Probiotics, immunomodulation, and health benefits. Adv Exp Med Biol. 2008;606:423-54.
Korotkyi O, Vovk A, Galenova T, Vovk T, Dvorschenko K, Luzza F, Abenavoli L, Kobyliak N, Falalyeyeva T, Ostapchenko L. Effect of probiotic on serum cytokines and matrix metalloproteinases profiles during monoiodoacetate-induced osteoarthritis in rats. Minerva Biotecnol. 2019;31(2):68-73.
Darsanaki RK, Ghaemi N, Mirpour M. Antimutagenic activity of Lactobacillus spp. isolated from commercial yoghurt versus sodium azide, acrylic amide, potassium permanganate and 2-nitrofluorene. Minerva Biotecnol. 2017;29(1):24-9.
Górska A, Przystupski D, Niemczura MJ, Kulbacka J. Probiotic Bacteria: A promising pool in cancer prevention and therapy. Curr Microbiol. 2019;76:939-49.
Harbeck N, Penault-Llorca F, Cortes J, Gnant M, Houssami N, Poortmans P, Ruddy K, Tsang J, Cardoso F. Breast cancer. Nat Rev Dis Prim. 2019;5(1):66.
Chuah LO, Foo HL, Loh TC, Mohammed Alitheen NB, Yeap SK, Abdul Mutalib NE, Abdul Rahim R, Yusoff K. Postbiotic metabolites produced by Lactobacillus plantarum strains exert selective cytotoxicity effects on cancer cells. BMC Complement Altern Med. 2019;19(1):114.
Scott AJ, Merrifield CA, Younes JA, Pekelharing EP. Pre-, pro- and synbiotics in cancer prevention and treatment—a review of basic and clinical research. Ecancermedicalscience. 2018;12:869.
Brandt AL, Castillo A, Harris KB, Keeton JT, Hardin MD, Taylor TM. Inhibition of Listeria monocytogenes by food antimicrobials applied singly and in combination. J Food Sci. 2010;75(9):M557-63.
Celebioglu HU, Delsoglio M, Brix S, Pessione E, Svensson B. Plant polyphenols stimulate adhesion to intestinal mucosa and induce proteome changes in the probiotic Lactobacillus acidophilus NCFM. Mol Nutr Food Res. 2018;62(4):1-11.
Celebioglu HU, Ejby M, Majumder A, Købler C, Goh YJ, Thorsen K, Schmidt B, O’Flaherty S, Abou Hachem M, Lahtinen SJ, Jacobsen S, Klaenhammer TR, Brix S, Mølhave K, Svensson B. Differential proteome and cellular adhesion analyses of the probiotic bacterium Lactobacillus acidophilus NCFM grown on raffinose - an emerging prebiotic. Proteomics. 2016;16(9):1361-75.
Kos B, Susković J, Vuković S, Simpraga M, Frece J, Matosić S. Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol. 2003;94(6):981-7.
Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1-2):55-63.
Al-Mamary M, Al-Meeri A, Al-Habori M. Antioxidant activities and total phenolics of different types of honey. Nutr Res. 2002;22(9):1041-7.
Çol Ayvaz M, Ömür B, Ertürk E, Kabakçi D. Phenolic profiles, antioxidant, antimicrobial, and DNA damage inhibitory activities of chestnut honeys from Black Sea Region of Turkey. J Food Biochem. 2018;42(3): e12502.
Nasuti C, Gabbianelli R, Falcioni G, Cantalamessa F. Antioxidative and gastroprotective activities of anti-inflammatory formulations derived from chestnut honey in rats. Nutr Res. 2006;26(3):130-7.
Sipahi H, Aydogan G, Helvacioglu S, Charehsaz M, Guzelmeric E, Aydin A. Antioxidant, antiinflammatory and antimutagenic activities of various kinds of Turkish honey. Fabad J Pharm Sci. 2017;42(1):7-13.
Yildiz O, Can Z, Saral O, Yuluǧ E, Ozturk F, Aliyazicioǧlu R, Canpolat S, Kolayli S. Hepatoprotective potential of chestnut bee pollen on carbon tetrachloride-induced hepatic damages in rats. Evidence-based Complement Altern Med. 2013;2013:461478.
Bogdanov S. Nature and origin of the antibacterial substances in honey. LWT - Food Sci Technol. 1997;30(7):748-53.
Collado MC, Meriluoto J, Salminen S. Adhesion and aggregation properties of probiotic and pathogen strains. Eur Food Res Technol 2007;226:1065-73.
Van Tassell ML, Miller MJ. Lactobacillus adhesion to mucus. Nutrients 2011;3:613-36
Servin AL, Coconnier M-H. Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract Res Clin Gastroenterol. 2003;17:741-54.
Buck B, Altermann E, Svingerud T, Klaenhammer TR. Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl Environ Microbiol. 2005;71(12):8344-51.
Pedersen K, Tannock GW. Colonization of the porcine gastrointestinal tract by lactobacilli. Appl Environ Microbiol. 1989;55(2):279-83.
Alp D, Kuleasan H, Korkut Altıntas A. The importance of the S-layer on the adhesion and aggregation ability of lactic acid bacteria. Mol Biol Rep. 2020;47:3449-57.
Boonaert CJP, Rouxhet PG. Surface of lactic acid bacteria: Relationships between chemical composition and physicochemical properties. Appl Environ Microbiol. 2000;66(6):254854.
Schillinger U, Guigas C, Holzapfel WH. In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int Dairy J. 2005;15(12):1289-97.
Krasowska A, Sigler K. How microorganisms use hydrophobicity and what does this mean for human needs? Front Cell Infect Microbiol. 2014;4:112.
Celebioglu H, Svensson B. Dietary nutrients, proteomes, and adhesion of probiotic lactobacilli to mucin and host epithelial cells. Microorganisms 2018;6:90.
Sleytr UB, Beveridge TJ. Bacterial S-layers. Trends Microbiol. 1999;7:253-60.
Hynonen U, Palva A. Lactobacillus surface layer proteins: structure, function and applications. Appl Microbiol Biotechnol 2013;97:5225-43.
Sara M, Sleytr UB. S-Layer Proteins. J Bacteriol 2000;182:859-68.
Sengupta R, Altermann E, Anderson RC, McNabb WC, Moughan PJ, Roy NC. The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediators Inflamm. 2013;237921.
Waśko A, Polak-Berecka M, Kuzdraliński A, Skrzypek T. Variability of S-layer proteins in Lactobacillus helveticus strains. Anaerobe. 2014;25:53-60.
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394-424.
Seyhan MF, Yılmaz E, Timirci-Kahraman O, Saygılı N, Kısakesen Hİ, Eronat AP, Ceviz AB, Bilgic Gazioglu S, Yılmaz-Aydogan H, Ozturk O. Anatolian honey is not only sweet but can also protect from breast cancer: Elixir for women from artemis to present. IUBMB Life. 2017;69(9):677-88.
Spilioti E, Jaakkola M, Tolonen T, Lipponen M, Virtanen V, Chinou I, Kassi E, Karabournioti S, Moutsatsou P. Phenolic acid composition, antiatherogenic and anticancer potential of honeys derived from various regions in Greece. PloS One 2014;9(4):e94860.
Ahmed S, Othman NH. Honey as a potential natural anticancer agent: A review of its mechanisms. Evidence-based Complement Altern Med. 2013;2013:829070.
Tomasin R, Cintra Gomes-Marcondes MC. Oral administration of Aloe vera and honey reduces walker tumour growth by decreasing cell proliferation and increasing apoptosis in tumour tissue. Phyther Res. 2011;25(4):619-23.
Jaganathan SK. Honey Constituents and their apoptotic effect in colon cancer cells. J ApiProduct ApiMedical Sci. 2009;1(2):29-36.
Lee YJ, Kuo HC, Chu CY, Wang CJ, Lin WC, Tseng TH. Involvement of tumor suppressor protein p53 and p38 MAPK in caffeic acid phenethyl ester-induced apoptosis of C6 glioma cells. Biochem Pharmacol. 2003;66(12):2281-9.
Pichichero E, Cicconi R, Mattei M, Muzi MG, Canini A. Acacia honey and chrysin reduce proliferation of melanoma cells through alterations in cell cycle progression. Int J Oncol. 2010;37(4):973-81.