Biotransformation of cranberry proanthocyanidins to probiotic metabolites by lactobacillus rhamnosus enhances their anticancer activity in HepG2 cells in vitro

Oxidative Medicine and Cellular Longevity

Volumn 2019, Issue , 2019, Pages

  Rupasinghe, H P Vasantha ^a,b   Parmar, Indu ^a   Neir, Sandhya V ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLI; BIOCONVERSION; BIOMOLECULES; CELL PROLIFERATION; CELLS; CYTOLOGY; METABOLITES; PHENOLS; PROBIOTICS; PROPIONIC ACID;

ACTIVE METABOLITES; ANAEROBIC CONDITIONS; ANTICANCER ACTIVITIES; BIOCONVERSION PROCESS; HEPATOCELLULAR CARCINOMA; LACTOBACILLUS RHAMNOSUS; MOLECULAR MECHANISM; PHARMACOLOGICAL ACTIVITY;

FLAVONOIDS;

3 (4 HYDROXYPHENYL)PROPIONIC ACID; 4 HYDROXYPHENYLACETIC ACID; AGLYCONE; ANTHOCYANIN; CAFFEIC ACID; CASPASE 3; CASPASE 7; CATECHIN; CATECHOL; CHALCONE DERIVATIVE; CHLOROGENIC ACID; DRUG METABOLITE; EPICATECHIN; EPICATECHIN GALLATE; EPIGALLOCATECHIN; EPIGALLOCATECHIN GALLATE; FERULIC ACID; FLAVAN DERIVATIVE; FLAVONOL; GALACTOSIDE; GLUCOSIDE; HYDROCINNAMIC ACID; ISOFERULIC ACID; PHENOL DERIVATIVE; POLYPHENOL DERIVATIVE; PROANTHOCYANIDIN; PROBIOTIC AGENT; PYROGALLOL; QUERCETIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; ANTINEOPLASTIC AGENT; HYDROXYBENZOIC ACID DERIVATIVE; PHENOLIC ACID; PLANT EXTRACT; POLYPHENOL;

ANAEROBIC FERMENTATION; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRANBERRY; CYTOTOXICITY; DRUG DECOMPOSITION; DRUG MECHANISM; DRUG POTENTIATION; DRUG TRANSFORMATION; HEP-G2 CELL LINE; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; INCUBATION TIME; LACTOBACILLUS RHAMNOSUS; MITOCHONDRION; NONHUMAN; CELL PROLIFERATION; DRUG EFFECT; FERMENTATION; METABOLISM;

BACTERIA; CELLS; CYTOLOGY; FLAVONOIDS; PHENOLS; PROPIONIC ACID;

ANTINEOPLASTIC AGENTS; CATECHIN; CELL PROLIFERATION; FERMENTATION; HEP G2 CELLS; HUMANS; HYDROXYBENZOATES; LACTOBACILLUS RHAMNOSUS; PLANT EXTRACTS; POLYPHENOLS; PROANTHOCYANIDINS; PROBIOTICS;

EID: 85073890111     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2019/4750795     Document Type: Article

References (45)

1. F. Bray, J. Ferlay, I. Soerjomataram, R. L. Siegel, L. A. Torre, and A. Jemal, "Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries," CA: A Cancer Journal for Clinicians, vol. 68, no. 6, pp. 394-424, 2018.
2. K. S. Bhullar, N. O. Lagarón, E. M. McGowan et al., "Kinasetargeted cancer therapies: Progress, challenges and future directions," Molecular Cancer, vol. 17, no. 1, pp. 48-67, 2018.
3. D. Stagos, G. D. Amoutzias, A. Matakos, A. Spyrou, A. M. Tsatsakis, and D. Kouretas, "Chemoprevention of liver cancer by plant polyphenols," Food and Chemical Toxicology, vol. 50, no. 6, pp. 2155-2170, 2012.
4. S. Thilakarathna and H. P. V. Rupasinghe, "Flavonoid bioavailability and attempts for bioavailability enhancement," Nutrients, vol. 5, no. 9, pp. 3367-3387, 2013.
5. C. Rice-Evans, N. Miller, and G. Paganga, "Antioxidant properties of phenolic compounds," Trends in Plant Science, vol. 2, no. 4, pp. 152-159, 1997.
6. A. M. Aura, "Microbial metabolism of dietary phenolic compounds in the colon," Phytochemistry Reviews, vol. 7, no. 3, pp. 407-429, 2008.
7. W. W. Thilakarathna, M. G. Langille, and H. P. V. Rupasinghe, "Polyphenol-based prebiotics and synbiotics: Potential for cancer chemoprevention," Current Opinion in Food Science, vol. 20, pp. 51-57, 2018.
8. H. P. V. Rupasinghe, S. V. Neir, and I. Parmar, "Polyphenol characterization, anti-oxidant, anti-proliferation and antityrosinase activity of cranberry pomace," Functional Foods in Health and Disease, vol. 6, no. 11, pp. 754-768, 2016.
9. P. J. Ferguson, E. Kurowska, D. J. Freeman, A. F. Chambers, and D. J. Koropatnick, "A flavonoid fraction from cranberry extract inhibits proliferation of human tumor cell lines," Journal of Nutrition, vol. 134, no. 6, pp. 1529-1535, 2004.
10. J. A. Marazza, M. S. Garro, and G. Savoy de Giori, "Aglycone production by Lactobacillus rhamnosus CRL981 during soymilk fermentation," Food Microbiology, vol. 26, no. 3, pp. 333-339, 2009.
11. J. A. Curiel, H. Rodríguez, I. Acebrón, J. M. Mancheño, B. de Las Rivas, and R. Muñoz, "Production and physicochemical properties of recombinant Lactobacillus plantarum tannase," Journal of Agricultural and Food Chemistry, vol. 57, no. 14, pp. 6224-6230, 2009.
12. X. Wang, X. Geng, Y. Egashira, and H. Sanada, "Purification and characterization of a feruloyl esterase from the intestinal bacterium Lactobacillus acidophilus," Applied and Environmental Microbiology, vol. 70, no. 4, pp. 2367-2372, 2004.
13. H. Rodríguez, J. M. Landete, B. Rivas, and R. Muñoz, "Metabolism of food phenolic acids by Lactobacillus plantarum CECT 748T," Food Chemistry, vol. 107, no. 4, pp. 1393-1398, 2008.
14. V. L. Singleton and J. A. Rossi, "Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents," American Journal of Enology and Viticulture, vol. 16, pp. 144-158, 1965.
15. H. P. V. Rupasinghe, G. M. Huber, C. Embree, and P. L. Forsline, "Red-fleshed apple as a source for functional beverages," Canadian Journal of Plant Science, vol. 90, no. 1, pp. 95-100, 2010.
16. C. C. Ratnasooriya, H. P. V. Rupasinghe, and A. R. Jamieson, "Juice quality and polyphenol concentration of fresh fruits and pomace of selected Nova Scotia-grown grape cultivars," Canadian Journal of Plant Science, vol. 90, no. 2, pp. 193-205, 2010.
17. H. P. V. Rupasinghe, L. J. Yu, K. S. Bhullar, and B. Bors, "Short Communication: Haskap (Lonicera caerulea): A new berry crop with high antioxidant capacity," Canadian Journal of Plant Science, vol. 92, no. 7, pp. 1311-1317, 2012.
18. K. S. Bhullar and H. P. V. Rupasinghe, "Antioxidant and cytoprotective properties of partridgeberry polyphenols," Food Chemistry, vol. 168, pp. 595-605, 2015.
19. S. V. G. Nair, Ziaullah, and H. P. V. Rupasinghe, "Fatty acid esters of phloridzin induce apoptosis of human liver cancer cells through altered gene expression," PLoS One, vol. 9, no. 9, article e107149, 2014.
20. F. Sánchez-Patán, R. Tabasco, M. Monagas et al., "Capability of Lactobacillus plantarum IFPL935 to catabolize flavan-3-ol compounds and complex phenolic extracts," Journal of Agricultural and Food Chemistry, vol. 60, no. 29, pp. 7142-7151, 2012.
21. Y. Uekusa, M. Kamihira-Ishijima, O. Sugimoto et al., "Interaction of epicatechin gallate with phospholipid membranes as revealed by solid-state NMR spectroscopy," Biochimica et Biophysica Acta (BBA) - Biomembranes, vol. 1808, no. 6, pp. 1654-1660, 2011.
22. E. Barroso, F. Sánchez-Patán, P. J. Martin-Alvarez et al., "Lactobacillus plantarum IFPL935 favors the initial metabolism of red wine polyphenols when added to a colonic microbiota," Journal of Agricultural and Food Chemistry, vol. 61, no. 42, pp. 10163-10172, 2013.
23. C. Kaneuchi, M. Seki, and K. Komagata, "Production of succinic acid from citric acid and related acids by Lactobacillus Strains," Applied and Environmental Microbiology, vol. 54, no. 12, pp. 3053-3056, 1988.
24. R. R. Scheline, Handbook of Mammalian Metabolism of Plant Compounds, CRC Press, Boca Raton, FL, USA, 1991.
25. J. D. Reed, C. G. Krueger, and M. M. Vestling, "MALDI-TOF mass spectrometry of oligomeric food polyphenols," Phytochemistry, vol. 66, no. 18, pp. 2248-2263, 2005.
26. A. E. Hagerman, K. M. Riedl, G. A. Jones et al., "High molecular weight plant polyphenolics (tannins) as biological antioxidants," Journal of Agricultural and Food Chemistry, vol. 46, no. 5, pp. 1887-1892, 1998.
27. S. Déprez, C. Brezillon, S. Rabot et al., "Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids," Journal of Nutrition, vol. 130, no. 11, pp. 2733-2738, 2000.
28. I. Parmar and H.P.V. Rupasinghe, "Proanthocyanidins in cranberry and grape seeds: Metabolism, bioavailability and biological activity," in Nutraceuticals and Functional Foods: Natural Remedy, S. K. Brar, S. Kaur, and G. S. Dhillon, Eds., pp. 119-145, Nova Science Publishers, 2014.
29. H. Rodríguez, J. A. Curiel, J. M. Landete et al., "Food phenolics and lactic acid bacteria," International Journal of Food Microbiology, vol. 132, no. 2-3, pp. 79-90, 2009.
30. M. P. Gonthier, C. Rémésy, A. Scalbert et al., "Microbial metabolism of caffeic acid and its esters chlorogenic and caftaric acids by human faecal microbiota in vitro," Biomedicine and Pharmacotherapy, vol. 60, no. 9, pp. 536-540, 2006.
31. S. Sang, M. J. Lee, I. Yang, B. Buckley, and C. S. Yang, "Human urinary metabolite profile of tea polyphenols analyzed by liquid chromatography/electrospray ionization tandem mass spectrometry with data-dependent acquisition," Rapid Communications in Mass Spectrometry, vol. 22, no. 10, pp. 1567-1578, 2008.
32. A.-M. Aura, P. Martin-Lopez, K. A. O'Leary et al., "In vitro metabolism of anthocyanins by human gut microflora," European Journal of Nutrition, vol. 44, no. 3, pp. 133-142, 2005.
33. K. Keppler and H. U. Humpf, "Metabolism of anthocyanins and their phenolic degradation products by the intestinal microflora," Bioorganic & Medicinal Chemistry, vol. 13, no. 17, pp. 5195-5205, 2005.
34. J. Fleschhut, F. Kratzer, G. Rechkemmer, and S. E. Kulling, "Stability and bio-transformation of various dietary anthocyanins in vitro," European Journal of Nutrition, vol. 45, no. 1, pp. 7-18, 2006.
35. M. Hidalgo, M. J. Oruna-Concha, S. Kolida et al., "Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth," Journal of Agricultural and Food Chemistry, vol. 60, no. 15, pp. 3882-3890, 2012.
36. J. Winter, L. H. Moore, Dowell VR Jr, and V. D. Bokkenheuser, "C-ring cleavage of flavonoids by human intestinal bacteria," Applied and Environmental Microbiology, vol. 55, no. 5, pp. 1203-1208, 1989.
37. M.-P. Gonthier, V. Cheynier, J. L. Donovan et al., "Microbial aromatic acid metabolites formed in the gut account for a major fraction of the polyphenols excreted in urine of rats fed red wine polyphenols," Journal of Nutrition, vol. 133, no. 2, pp. 461-467, 2003.
38. G. van't Slot and H.-U. Humpf, "Degradation and metabolism of catechin, epigallocatechin-3-gallate (EGCG), and related compounds by the intestinal microbiota in the pig cecum model," Journal of Agricultural and Food Chemistry, vol. 57, no. 17, pp. 8041-8048, 2009.
39. A. R. Rechner, M. A. Smith, G. Kuhnle et al., "Colonic metabolism of dietary polyphenols: Influence of structure on microbial fermentation products," Free Radical Biology and Medicine, vol. 36, no. 2, pp. 212-225, 2004.
40. X. He, Y. Zou, W. B. Yoon, S. J. Park, D. S. Park, and J. Ahn, "Effects of probiotic fermentation on the enhancement of biological and pharmacological activities of Codonopsis lanceolata extracted by high pressure treatment," Journal of Bioscience and Bioengineering, vol. 112, no. 2, pp. 188-193, 2011.
41. H. Jaeschke, G. J. Gores, A. I. Cederbaum, J. A. Hinson, D. Pessayre, and J. J. Lemasters, "Mechanisms of hepatotoxicity," Toxicological Sciences, vol. 65, no. 2, pp. 166-176, 2002.
42. K. D. Vu, H. Carlettini, J. Bouvet et al., "Effect of different cranberry extracts and juices during cranberry juice processing on the antiproliferative activity against two colon cancer cell lines," Food Chemistry, vol. 132, no. 2, pp. 959-967, 2012.
43. D. Ferrari, A. Stepczynska, M. Los, S. Wesselborg, and K. Schulze-Osthoff, "Differential regulation and ATP requirement for caspase-8 and caspase-3 activation during CD95- and anticancer drug-induced apoptosis," Journal of Experimental Medicine, vol. 188, no. 5, pp. 979-984, 1998.
44. R. Sonntag, N. Gassler, J.-M. Bangen, C. Trautwein, and C. Liedtke, "Pro-apoptotic Sorafenib signaling in murine hepatocytes depends on malignancy and is associated with PUMA expression in vitro and in vivo," Cell Death and Disease, vol. 5, no. 1, article e1030, 2014.
45. W. P. D. W. Thilakarathna and H. P. V. Rupasinghe, "Microbial metabolites of proanthocyanidins reduce chemical carcinogen-induced DNA damage in human lung epithelial and fetal hepatic cells in vitro," Food and Chemical Toxicology., vol. 125, pp. 479-493, 2019.