The synergistic effect of cell wall extracted from probiotic biomass containing Lactobacillus acidophilus CL1285, L. casei LBC80R, and L. rhamnosus CLR2 on the anticancer activity of cranberry juice—HPLC fractions
Kerlynn Desrouillères
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Search for more papers by this authorMathieu Millette
Bio-K Plus International Inc., Laval, QC, Canada
Search for more papers by this authorLeila Bagheri
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Search for more papers by this authorBehnoush Maherani
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Search for more papers by this authorMajid Jamshidian
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Search for more papers by this authorCorresponding Author
Monique Lacroix
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Correspondence
Monique Lacroix, Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, 531 Blvd. des Prairies, Laval, Quebec, H7V 1B7, Canada
Email: [email protected]
Search for more papers by this authorKerlynn Desrouillères
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Search for more papers by this authorMathieu Millette
Bio-K Plus International Inc., Laval, QC, Canada
Search for more papers by this authorLeila Bagheri
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Search for more papers by this authorBehnoush Maherani
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Search for more papers by this authorMajid Jamshidian
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Search for more papers by this authorCorresponding Author
Monique Lacroix
Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, Laval, QC, Canada
Correspondence
Monique Lacroix, Research Laboratories in Sciences Applied to Food, Canadian Irradiation Center, INRS, Armand-Frappier, Health and Biotechnology Center, Institute of Nutraceutical and Functional Foods, 531 Blvd. des Prairies, Laval, Quebec, H7V 1B7, Canada
Email: [email protected]
Search for more papers by this authorAbstract
Anticancer effects were evaluated on three HPLC fractions obtained from a concentrated cranberry juice and cell wall constituents extracted from a probiotic biomass containing Lactobacillus acidophilus CL1285, Lactobacillus casei LBC80R, and Lactobacillus rhamnosus CLR2. The samples were tested at increasing concentrations for the antiproliferative assay using HT-29 cells' line and for the quinone reductase (QR) assay using Hepa-1c1c7 murine hepatoma cells. Fraction 1 (F1) which is highly concentrated with phenolic acids inhibited the growth of the HT-29 cells' line with IC50 values of 14.80 µg Gallic acid equivalent (GAE)/ml. The fraction 3 (F3) which is highly concentrated in flavonols had potency as QR inducer. Furthermore, the results showed that all cranberry fractions combined with cell wall constituents extracted from the probiotic biomass were more effective in inhibiting the growth of HT-29 as compared to the cranberry fractions tested alone, indicating a possible synergy effect between these bio-functional compounds.
Practical applications
This study strongly evidenced that cranberry juice fractions combined with cell wall constituents extracted from the probiotic biomass can be used as a potent preventive functional compound against colorectal cancer. Therefore, this research proposes a natural dietary compound to prevent mutagenesis and carcinogenesis of colorectal cancer. Furthermore, the industry can formulae products containing probiotic and phenolic compounds as colon cancer cell growth preventive and anticancer products.
CONFLICT OF INTEREST
The authors declare no conflict of interest in this study.
REFERENCES
- Bagheri, L., Madadlou, A., Yarmand, M., & Mousavi, M. E. (2013). Nanoencapsulation of date palm pit extract in whey protein particles generated via desolvation method. Food Research International, 51(2), 866–871. https://doi.org/10.1016/j.foodres.2013.01.058
- Zhang, Caillet, S., Lorenzo, G., Côté, J., Doyon, G., Sylvain, J.-F., & Lacroix, M. (2012). Cancer chemopreventive effect of fractions from cranberry products. Food Research International, 45(1), 320–330. https://doi.org/10.1016/j.foodres.2011.09.011
- Chang, J.-H., Shim, Y. Y., Cha, S.-K., & Chee, K. M. (2010). Probiotic characteristics of lactic acid bacteria isolated from kimchi. Journal of Applied Microbiology, 109(1), 220–230. https://doi.org/10.1111/j.1365-2672.2009.04648.x
- Chen, X.-L., & Kunsch, C. (2004). Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: A new therapeutic approach for the treatment of inflammatory diseases. Current Pharmaceutical Design, 10(8), 879–891.
- Choi, S., Kim, Y., Han, K., You, S., Oh, S., & Kim, S. H. (2006). Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Letters in Applied Microbiology, 42(5), 452–458. https://doi.org/10.1111/j.1472-765X.2006.01913.x
- Côté, J., Caillet, S., Doyon, G., Dussault, D., Sylvain, J.-F., & Lacroix, M. (2011). Antimicrobial effect of cranberry juice and extracts. Food Control, 22(8), 1413–1418. https://doi.org/10.1016/j.foodcont.2011.02.024
- Côté, J., Caillet, S., Doyon, G., Sylvain, J.-F., & Lacroix, M. (2010). Bioactive compounds in cranberries and their biological properties. Critical Reviews in Food Science and Nutrition, 50(7), 666–679. https://doi.org/10.1080/10408390903044107
- D'Aimmo, M. R., Modesto, M., & Biavati, B. (2007). Antibiotic resistance of lactic acid bacteria and Bifidobacterium spp. isolated from dairy and pharmaceutical products. International Journal of Food Microbiology, 115(1), 35–42. https://doi.org/10.1016/j.ijfoodmicro.2006.10.003
- Desrouillères, K., Millette, M., Jamshidian, M., Maherani, B., Fortin, O., & Lacroix, M. (2016). Cancer preventive effect of a specific probiotic fermented milk components and cell walls extracted from a biomass containing L. acidophilus CL1285, L. casei LBC80R, and L. rhamnosus CLR2 on male F344 rats treated with 1,2-dimethylhydrazine. Journal of Functional Foods, 26, 373–384. https://doi.org/10.1016/j.jff.2016.08.005
- Desrouillères, K., Millette, M., Vu, K. D., Touja, R., & Lacroix, M. (2015). Cancer preventive effects of a specific probiotic fermented milk containing Lactobacillus acidophilus CL1285, L. casei LBC80R and L. rhamnosus CLR2 on male F344 rats treated with 1, 2-dimethylhydrazine. Journal of Functional Foods, 17, 816–827. https://doi.org/10.1016/j.jff.2015.06.035
- Ewaschuk, J. B., Walker, J. W., Diaz, H., & Madsen, K. L. (2006). Bioproduction of conjugated linoleic acid by probiotic bacteria occurs in vitro and in vivo in mice. The Journal of Nutrition, 136(6), 1483–1487. https://doi.org/10.1093/jn/136.6.1483
- Fiuza, S., Gomes, C., Teixeira, L., Da Cruz, M. G., Cordeiro, M., Milhazes, N., … Marques, M. (2004). Phenolic acid derivatives with potential anticancer properties––A structure-activity relationship study. Part 1: Methyl, propyl and octyl esters of caffeic and gallic acids. Bioorganic & Medicinal Chemistry, 12(13), 3581–3589. https://doi.org/10.1016/j.bmc.2004.04.026
- Flis, S., Jastrzebski, Z., Namiesnik, J., Arancibia-Avila, P., Toledo, F., Leontowicz, H., … Gorinstein, S. (2012). Evaluation of inhibition of cancer cell proliferation in vitro with different berries and correlation with their antioxidant levels by advanced analytical methods. Journal of Pharmaceutical and Biomedical Analysis, 62, 68–78. https://doi.org/10.1016/j.jpba.2012.01.005
- Haggar, F. A., & Boushey, R. P. (2009). Colorectal cancer epidemiology: Incidence, mortality, survival, and risk factors. Clinics in Colon and Rectal Surgery, 22(04), 191–197. https://doi.org/10.1055/s-0029-1242458
- Hervert-Hernández, D., Pintado, C., Rotger, R., & Goñi, I. (2009). Stimulatory role of grape pomace polyphenols on Lactobacillus acidophilus growth. International Journal of Food Microbiology, 136(1), 119–122. https://doi.org/10.1016/j.ijfoodmicro.2009.09.016
- Hill, C., Guarner, F., Reid, G., Gibson, G. R., Merenstein, D. J., Pot, B., … Sanders, M. E. (2014). The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nature Reviews Gastroenterology & Hepatology, 11(8), 506–514. https://doi.org/10.1038/nrgastro.2014.66
- Hirayama, K., & Rafter, J. (2000). The role of probiotic bacteria in cancer prevention. Microbes and Infection, 2(6), 681–686. https://doi.org/10.1016/S1286-4579(00)00357-9
- Howell, A. B., Botto, H., Combescure, C., Blanc-Potard, A.-B., Gausa, L., Matsumoto, T., … Lavigne, J. P. (2010). Dosage effect on uropathogenic Escherichia coli anti-adhesion activity in urine following consumption of cranberry powder standardized for proanthocyanidin content: A multicentric randomized double blind study. BMC Infectious Diseases, 10(1), 94. https://doi.org/10.1186/1471-2334-10-94
- Janicke, B., Önning, G., & Oredsson, S. M. (2005). Differential effects of ferulic acid and p-coumaric acid on S phase distribution and length of S phase in the human colonic cell line Caco-2. Journal of Agricultural and Food Chemistry, 53(17), 6658–6665. https://doi.org/10.1021/jf0504891
- Kahkonen, M. P., Hopia, A. I., & Heinonen, M. (2001). Berry phenolics and their antioxidant activity. Journal of Agriculture and Food Chemistry, 49(8), 4076–4082. https://doi.org/10.1021/jf010152t
- Kaminogawa, S., & Nanno, M. (2004). Modulation of immune functions by foods. Evidence-Based Complementary and Alternative Medicine, 1(3), 241–250. https://doi.org/10.1093/ecam/neh042
- Kang, Y.-H., & Pezzuto, J. M. (2004). Induction of quinone reductase as a primary screen for natural product anticarcinogens. In H. Sies & L. Packer (Eds), Methods in enzymology (Vol. 382, pp. 380–414). Elsevier. https://doi.org/10.1016/S0076-6879(04)82021-4
- Karp, G. (2009). Cell and molecular biology: Concepts and experiments. New Jersey: John Wiley & Sons.
- Kim, J. Y., Woo, H. J., Kim, Y.-S., & Lee, H. J. (2002). Screening for antiproliferative effects of cellular components from lactic acid bacteria against human cancer cell lines. Biotechnology Letters, 24(17), 1431–1436.
- Kolling, Y., Salva, S., Villena, J., Marranzino, G., & Alvarez, S. (2015). Non-viable immunobiotic Lactobacillus rhamnosus CRL1505 and its peptidoglycan improve systemic and respiratory innate immune response during recovery of immunocompromised-malnourished mice. International Immunopharmacology, 25(2), 474–484. https://doi.org/10.1016/j.intimp.2015.02.006
- Lacombe, A., Wu, V. C. H., Tyler, S., & Edwards, K. (2010). Antimicrobial action of the American cranberry constituents; phenolics, anthocyanins, and organic acids, against Escherichia coli O157:H7. International Journal of Food Microbiology, 139(1), 102–107. https://doi.org/10.1016/j.ijfoodmicro.2010.01.035
- Li, W., Du, B., Wang, T., Wang, S., & Zhang, J. (2009). Kaempferol induces apoptosis in human HCT116 colon cancer cells via the ataxia-telangiectasia mutated-p53 pathway with the involvement of p53 upregulated modulator of apoptosis. Chemico-Biological Interactions, 177(2), 121–127. https://doi.org/10.1016/j.cbi.2008.10.048
- Millette, M., Luquet, F. M., & Lacroix, M. (2007). In vitro growth control of selected pathogens by Lactobacillus acidophilus- and Lactobacillus casei-fermented milk. Letters in Applied Microbiology, 44(3), 314–319. https://doi.org/10.1111/j.1472-765X.2006.02060.x
- Murad, L. D., Soares, N. D. C. P., Brand, C., Monteiro, M. C., & Teodoro, A. J. (2015). Effects of caffeic and 5-caffeoylquinic acids on cell viability and cellular uptake in human colon adenocarcinoma cells. Nutrition and Cancer, 67(3), 532–542. https://doi.org/10.1080/01635581.2015.1004736
- Murphy, B. T., MacKinnon, S. L., Yan, X., Hammond, G. B., Vaisberg, A. J., & Neto, C. C. (2003). Identification of triterpene hydroxycinnamates with in vitro antitumor activity from whole cranberry fruit (Vaccinium macrocarpon). Journal of Agricultural and Food Chemistry, 51(12), 3541–3545. https://doi.org/10.1021/jf034114g
- Ngamdee, P., Jiamyangyuen, S., & Parkin, K. L. (2016). Phase II enzyme induction and anti-inflammatory effects of crude extracts and secondary fractions obtained from bran from five black glutinous rice cultivars. International Journal of Food Science & Technology, 51(2), 333–341. https://doi.org/10.1111/ijfs.12967
- Paredes-López, O., Cervantes-Ceja, M. L., Vigna-Pérez, M., & Hernández-Pérez, T. (2010). Berries: Improving human health and healthy aging, and promoting quality life—A review. Plant Foods for Human Nutrition, 65(3), 299–308. https://doi.org/10.1007/s11130-010-0177-1
- Peres, C. M., Hernandez-Mendonza, A., Bronze, M. R., Peres, C., & Malcata, F. X. (2015). Synergy of olive bioactive phytochemicals and probiotic strain in control of Escherichia coli. LWT - Food Science and Technology, 64(2), 938–945. https://doi.org/10.1016/j.lwt.2015.06.074
- Pezzuto, J. (1995). Phytochemistry of medicinal plants. In R. M. J. Arnason & J. Romeo (Eds.), Recent advances in phytochemistry ( 29th ed., pp. 19–44). New York, NY: Plenum Press.
- Rasool, S., Kadla, S. A., Rasool, V., & Ganai, B. A. (2013). A comparative overview of general risk factors associated with the incidence of colorectal cancer. Tumor Biology, 34(5), 2469–2476. https://doi.org/10.1007/s13277-013-0876-y
- Saad, N., Delattre, C., Urdaci, M., Schmitter, J.-M., & Bressollier, P. (2013). An overview of the last advances in probiotic and prebiotic field. LWT-Food Science and Technology, 50(1), 1–16. https://doi.org/10.1016/j.lwt.2012.05.014
- Sambi, M., Bagheri, L., & Szewczuk, M. R. (2019). Current challenges in cancer immunotherapy: Multimodal approaches to improve efficacy and patient response rates. Journal of Oncology, 2019, 12. https://doi.org/10.1155/2019/4508794
- Seeram, N. P., Adams, L. S., Hardy, M. L., & Heber, D. (2004). Total cranberry extract versus its phytochemical constituents: Antiproliferative and synergistic effects against human tumor cell lines. Journal of Agricultural and Food Chemistry, 52(9), 2512–2517. https://doi.org/10.1021/jf0352778
- Shen, X. J., Rawls, J. F., Randall, T. A., Burcall, L., Mpande, C., Jenkins, N., … Keku, T. O. (2010). Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes, 1(3), 138–147. https://doi.org/10.4161/gmic.1.3.12360
- Shih, C.-H., Siu, S. O., Ng, R., Wong, E., Chiu, L. C. M., Chu, I. K., & Lo, C. (2007). Quantitative analysis of anticancer 3-deoxyanthocyanidins in infected sorghum seedlings. Journal of Agricultural and Food Chemistry, 55(2), 254–259. https://doi.org/10.1021/jf062516t
- Shoemaker, R. H. (2006). The NCI60 human tumour cell line anticancer drug screen. Nature Reviews Cancer, 6(10), 813–823. https://doi.org/10.1038/nrc1951
- Siegel, R., Ma, J., Zou, Z., & Jemal, A. (2014). Cancer statistics, 2014. CA: A Cancer Journal for Clinicians, 64(1), 9–29. https://doi.org/10.3322/caac.21208
- Signoretto, C., Boaretti, M., & Canepari, P. (1998). Peptidoglycan synthesis by Enterococcus faecalis penicillin binding protein 5. Archives of Microbiology, 170(3), 185–190. https://doi.org/10.1007/s002030050632
- Singleton, V. L., & Rossi, J. A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16(3), 144–158.
- Sobhani, I., Tap, J., Roudot-Thoraval, F., Roperch, J. P., Letulle, S., Langella, P., … Furet, J. P. (2011). Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS ONE, 6(1), e16393. https://doi.org/10.1371/journal.pone.0016393
- Sreekumar, O., & Hosono, A. (1998). Antimtagenicity and the influence of physical factors in binding lactobacillus gasseri and bifidobacterium longum cells t amino acid pyrolysates. Journal of Dairy Science, 81(6), 1508–1516. https://doi.org/10.3168/jds.S0022-0302(98)75716-9
- Srivastava, A., Akoh, C. C., Fischer, J., & Krewer, G. (2007). Effect of anthocyanin fractions from selected cultivars of Georgia-Grown blueberries on apoptosis and phase II enzymes. Journal of Agricultural and Food Chemistry, 55(8), 3180–3185. https://doi.org/10.1021/jf062915o
- Stoner, G. D., Wang, L. S., & Casto, B. C. (2008). Laboratory and clinical studies of cancer chemoprevention by antioxidants in berries. Carcinogenesis, 29(9), 1665–1674. https://doi.org/10.1093/carcin/bgn142
- Su, B.-N., Gu, J.-Q., Kang, Y.-H., Park, E.-J., Pezzuto, J. M., & Kinghorn, A. D. (2004). Induction of the phase II enzyme, quinone reductase, by withanolides and norwithanolides from solanaceous species. Mini-Reviews in Organic Chemistry, 1(1), 115–123.
- Tabasco, R., Sánchez-Patán, F., Monagas, M., Bartolomé, B., Victoria Moreno-Arribas, M., Peláez, C., & Requena, T. (2011). Effect of grape polyphenols on lactic acid bacteria and bifidobacteria growth: Resistance and metabolism. Food Microbiology, 28(7), 1345–1352. https://doi.org/10.1016/j.fm.2011.06.005
- Tahmourespour, A., & Kermanshahi, R. K. (2011). The effect of a probiotic strain (Lactobacillus acidophilus) on the plaque formation of oral Streptococci. Bosnian Journal of Basic Medical Sciences, 11(1), 37–40. https://doi.org/10.17305/bjbms.2011.2621
- Talalay, P. (2000). Chemoprotection against cancer by induction of phase 2 enzymes. BioFactors, 12(1–4), 5–11. https://doi.org/10.1002/biof.5520120102
- Uccello, M., Malaguarnera, G., Basile, F., D’agata, V., Malaguarnera, M., Bertino, G., … Biondi, A. (2012). Potential role of probiotics on colorectal cancer prevention. BMC Surgery, 12(1), S35. https://doi.org/10.1186/1471-2482-12-S1-S35
- Uda, Y., Price, K. R., Williamson, G., & Rhodes, M. J. C. (1997). Induction of the anticarcinogenic marker enzyme, quinone reductase, in murine hepatoma cells in vitro by flavonoids. Cancer Letters, 120(2), 213–216. https://doi.org/10.1016/S0304-3835(97)00311-X
- Vistica, D. T., Skehan, P., Scudiero, D., Monks, A., Pittman, A., & Boyd, M. R. (1991). Tetrazolium-based assays for cellular viability: A critical examination of selected parameters affecting formazan production. Cancer Research, 51(10), 2515–2520.
- Vu, K. D., Carlettini, H., Bouvet, J., Côté, J., Doyon, G., Sylvain, J.-F., & Lacroix, M. (2012). Effect of different cranberry extracts and juices during cranberry juice processing on the antiproliferative activity against two colon cancer cell lines. Food Chemistry, 132(2), 959–967. https://doi.org/10.1016/j.foodchem.2011.11.078
- Yang, J., & Liu, R. H. (2009). Induction of phase II enzyme, quinone reductase, in murine hepatoma cells in vitro by grape extracts and selected phytochemicals. Food Chemistry, 114(3), 898–904. https://doi.org/10.1016/j.foodchem.2008.10.045
- Yang, T., Owen, J. L., Lightfoot, Y. L., Kladde, M. P., & Mohamadzadeh, M. (2013). Microbiota impact on the epigenetic regulation of colorectal cancer. Trends in Molecular Medicine, 19(12), 714–725. https://doi.org/10.1016/j.molmed.2013.08.005
- Zhang, H., Zhang, M., Yu, L., Zhao, Y., He, N., & Yang, X. (2012). Antitumor activities of quercetin and quercetin-5′, 8-disulfonate in human colon and breast cancer cell lines. Food and Chemical Toxicology, 50(5), 1589–1599. https://doi.org/10.1016/j.fct.2012.01.025
- Zhang, Y., Chen, A. Y., Li, M., Yao, Q., & Chen, C. J. (2008). QS302. Ginkgo Biloba extract kaempferol inhibits cell proliferation and induces apoptosis in panceratic cancer cells. Journal of Surgical Research, 144(2), 17–23.
- Zuo, Y., Wang, C., & Zhan, J. (2002). Separation, characterization, and quantitation of benzoic and phenolic antioxidants in American cranberry fruit by GC−MS. Journal of Agricultural and Food Chemistry, 50(13), 3789–3794. https://doi.org/10.1021/jf020055f