In vitro bioaccessibility, human gut microbiota metabolites and hepatoprotective potential of chebulic ellagitannins: A case of padma Hepaten® formulation

Nutrients

Volumn 7, Issue 10, 2015, Pages 8456-8477

  Olennikov, Daniil N ^a   Kashchenko, Nina I ^a   Chirikova, Nadezhda K ^b  

^a INSTITUTE OF GENERAL AND EXPERIMENTAL BIOLOGY   (Russian Federation)

^b NORTH EASTERN FEDERAL UNIVERSITY   (Russian Federation)

Author keywords

Bioaccessibility; Bras Bu; Chebulic ellagitannins; Hepatoprotective activity; Human gut microbiota; Padma Hepaten; Tibetan medicine; Triphala; Urolithins

Indexed keywords

1,6 DI O GALLOYL D GLUCOSE; 3,4,6 TRI O GALLOYL D GLUCOSE; ALPHA PUNICALAGIN; BETA PUNICALAGIN; CHEBULAGIC ACID; CHEBULANIN; CHEBULIC ACID; CHEBULINIC ACID; CORILAGIN; ELLAGIC ACID; ELLAGITANNIN; ESTER; GALLIC ACID; GLUCOGALLIN; LACTATE DEHYDROGENASE; MALONALDEHYDE; POLYPHENOL DERIVATIVE; TERT BUTYL HYDROPEROXIDE; UNCLASSIFIED DRUG; UROLITHIN; UROLITHIN B; UROLITHIN C; 3,8-DIHYDROXY-6H-DIBENZO(B,D)PYRAN-6-ONE; BENZOPYRAN DERIVATIVE; COUMARIN DERIVATIVE; PADMA HEPATEN; PLANT EXTRACT; TANNIN; UROLITHIN D;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL ACTIVITY; CELL VIABILITY ASSAY; CHEMICAL COMPOSITION; CONTROLLED STUDY; CYTOTOXICITY; DIALYSIS; DIGESTION; FECES ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IN VITRO STUDY; INTESTINE FLORA; LIVER CELL DAMAGE; LIVER PROTECTION; LIVER TOXICITY; METABOLITE; MTT ASSAY; NONHUMAN; QUANTITATIVE ANALYSIS; RAT; SIMULATION; STOMACH JUICE; TIBETAN MEDICINE; ULTRAVIOLET SPECTROPHOTOMETRY; ANIMAL; BIOAVAILABILITY; CELL CULTURE; CELL SURVIVAL; DRUG EFFECTS; GASTROINTESTINAL TRACT; LIVER CELL; LIVER DISEASES; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANIMALS; BENZOPYRANS; BIOLOGICAL AVAILABILITY; CELL SURVIVAL; CELLS, CULTURED; COUMARINS; DIGESTION; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HEPATOCYTES; HUMANS; HYDROLYZABLE TANNINS; LIVER DISEASES; OXIDATION-REDUCTION; PLANT EXTRACTS; RATS; TERT-BUTYLHYDROPEROXIDE;

EID: 84944463822     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu7105406     Document Type: Article

References (52)

1. Heaney, R.P. Factors influencing the measurement of bioavailability, taking calcium as a model. J. Nutr. 2001, 131, 1344–1348.
2. Carbonell-Capella, J.M.; Buniowska, M.; Barba, F.J.; Esteve, M.J.; Frígola, A. Analytical methods for determining bioavailability and bioaccessibility of bioactive compounds from fruits and vegetables: A review. Comp. Rev. Food Sci. Food Saf. 2014, 13, 155–171. [CrossRef]
3. Alminger, M.; Aura, A.M.; Bohn, T.; Dufour, C.; El, S.N.; Gomes, A.; Karakaya, S.; Martínez-Cuesta, M.C.; McDougall, G.J.; Requena, T. et al. In vitro models for studying secondary plant metabolite digestion and bioaccessibility. Compr. Rev. Food Sci. Food Saf. 2014, 13, 413–436. [CrossRef]
4. Chen, J.; Gaikwad, V.; Holmes, M.; Murray, B.; Povey, M.; Wang, Y.; Zhang, Y. Development of a simple model device for in vitro gastric digestion investigation. Food Funct. 2011, 2, 174–182. [CrossRef] [PubMed]
5. McClements, D.J.; Li, Y. Review of in vitro digestion models for rapid screening of emulsion-based systems. Food Funct. 2010, 1, 32–59. [CrossRef] [PubMed]
6. Courraud, J.; Berger, J.; Cristol, J.P.; Avallone, S. Stability and bioaccessibility of different forms of carotenoids and vitamin A during in vitro digestion. Food Chem. 2013, 136, 871–877. [CrossRef]
7. Garret, D.A.; Faila, M.L.; Sarama, R.J. Estimation of carotenoids bioavailability from fresh stir-fried vegetables using an in vitro digestion/Caco-2 cell culture model. J. Nutr. Biochem. 2000, 49, 1035–1041. [CrossRef]
8. Stanisavljević, N.; Samardžić, J.; Janković, T.; Šavikin, K.; Mojsin, M.; Topalović, V.; Stevanović, M. Antioxidant and antiproliferative activity of chokeberry juice phenolics during in vitro simulated digestion in the presence of food matrix. Food Chem. 2015, 175, 516–522. [CrossRef]
9. Bouayed, J.; Hoffmann, L.; Bohn, T. Total phenolics, flavonoids, anthocyanins and antioxidant activity following simulated gastro-intestinal digestion and dialysis of apple varieties: Bioaccessibility and potentional uptake. Food Chem. 2011, 128, 14–21. [CrossRef]
10. Kern, S.M.; Bennett, R.N.; Needs, P.W.; Mellon, F.A.; Kroon, P.A.; Garcia-Conesa, M.T. Characterization of metabolites of hydroxycinnamates in the in vitro model of human small intestinal epithelium Caco-2 cells. J. Agric. Food Chem. 2003, 51, 7884–7891. [CrossRef] [PubMed]
11. Saleem, A.; Husheem, M.; Härkönen, P.; Pihlaya, K. Inhibition of cancer cell growth by crude extract and the phenolics of Terminalia chebula retz. fruit. J. Ethnopharmacol. 2002, 81, 327–336. [CrossRef]
12. Cho, H.; Jung, H.; Lee, H.; Yi, H.C.; Kwak, H.-K.; Hwang, K.I. Chemopreventive activity of ellagitannins and their derivatives from black raspberry seeds on HT-29 colon cancer cells. Food Funct. 2015, 6, 1675–1683. [CrossRef]
13. Yamagata, K.; Tagami, M.; Yamori, Y. Dietary polyphenols regulate endothelial function and prevent cardiovascular disease. Nutrition 2015, 31, 28–37. [CrossRef]
14. Li, A.N.; Li, S.; Zhang, Y.J.; Xu, X.R.; Chen, Y.M.; Li, H.B. Resources and biological activities of natural polyphenols. Nutrients 2014, 6, 6020–6047. [CrossRef]
15. Baliga, M.S.; Meera, S.; Mathai, B.; Rai, M.P.; Pawar, V.; Palatty, P.L. Scientific validation of the ethnomedicinal properties of the Ayurvedic drug Triphala: A review. Chin. J. Integr. Med. 2012, 18, 946–954. [CrossRef]
16. Bhatnagar, S.; Rani, A.; Kumari, R. Therapeutic potential of Triphala against human diseases. Int. J. Pharm. Sci. Rev. Res. 2015, 31, 5–13.
17. Balasubramani, S.P.; Venkatasubramanian, P.; Kukkupuni, S.K.; Patwardhan, B. Plant-based Rasayana drugs from Ayurveda. Chin. J. Integr. Med. 2011, 17, 88–94. [CrossRef]
18. Pfundstein, B.; el Desouky, S.K.; Hull, W.E.; Haubner, R.; Erben, G.; Owen, R.W. Polyphenolic compounds in the fruits of Egyptian medicinal plants (Terminalia bellerica, Terminalia chebula and Terminalia horrida): Characterization, quantitation and determination of antioxidant capacities. Phytochemistry 2010, 71, 1132–1148. [CrossRef]
19. Rathinamoorthy, R.; Thilagavathi, G. Terminalia chebula—Review on pharmacological and biochemical studies. Int. J. PharmTech Res. 2014, 6, 97–116.
20. Saraswathi Motamarri, N.; Karthikeyan, M.; Kannan, M.; Rajasekar, S. Terminalia belerica Roxb.—A phytopharmacological review. Int. J. Res. Pharm. Biomed. Sci. 2012, 3, 96–99.
21. Espín, J.C.; González-Barrio, R.; Cerdá, B.; López-Bote, C.; Rey, A.I.; Tomás-Barberán, F.A. Iberian pig as a model to clarify obscure points in the bioavailability and metabolism of ellagitannins in humans. J. Agric. Food Chem. 2007, 55, 10476–10485. [CrossRef]
22. Espín, J.C.; Larrosa, M.; García-Conesa, M.T.; Tomás-Barberán, F. Biological significance of urolithins, the gut microbial ellagic acid-derived metabolites: The evidence so far. Evid. Based Complement. Altern. Med. 2013. [CrossRef]
23. Seeram, N.P.; Henning, S.M.; Zhang, Y.; Suchard, M.; Li, Z.; Heber, D. Pomegranate juice ellagitannin metabolites are present in human plasma and some persist in urine for up to 48 h. J. Nutr. 2006, 136, 2481–2485. [PubMed]
24. Dell’agli, M.; Galli, G.V.; Bulgari, M.; Basilico, N.; Romeo, S.; Bhattacharya, D.; Taramelli, D.; Bosisio, M. Ellagitannins of the fruit rind of the pomegranate (Punica granatum) antagonize in vitro the host inflammatory response mechanism involved in the onset of malaria. Malar. J. 2010, 9, 208. [CrossRef]
25. Gimenez-Bastida, J.A.; Gonzalez-Sarrias, A.; Larrosa, M.; Tomás-Barberán, F.; Espín, J.C.; Garcia-Conesa, M.T. Ellagitannin metabolites, urolithin A glucuronide and its aglycone urolithin A, ameliorate TNF-alpha-induced inflammation and associated molecular markers in human aortic endothelial cells. Mol. Nutr. Food Res. 2012, 56, 784–796. [CrossRef] [PubMed]
26. Gimenez-Bastida, J.A.; Larrosa, M.; Gonzalez-Sarrias, A.; Tomás-Barberán, F.; Espín, J.C.; Garcia-Conesa, M.T. Intestinal ellagitannin metabolites ameliorate cytokine-induced inflammation and associated molecular markers in human colon fibroblasts. J. Agric. Food Chem. 2012, 60, 8866–8876. [CrossRef]
27. Bialonska, D.; Kasimsetty, S.G.; Khan, S.I.; Ferreira, D. Urolithins, intestinal microbial metabolites of pomegranate ellagitannins, exhibit potent antioxidant activity in a cell-based assay. J. Agric. Food Chem. 2009, 57, 10181–10186. [CrossRef]
28. Verzelloni, E.; Pellacani, C.; Tagliazucchi, D.; Tagliaferri, S.; Calani, L.; Costa, L.G.; Brighenti, F.; Borges, G.; Crozier, A.; Conte, A. et al. Antiglycative and neuroprotective activity of colon-derived polyphenol catabolites. Mol. Nutr. Food Res. 2011, 55, S35–S43. [CrossRef]
29. Gonzalez-Sarrias, A.; Larrosa, M.; Tomas-Barberan, F.A.; Dolara, P.; Espin, J.C. NF-kappaB-dependent anti-inflammatory activity of urolithins, gut microbiota ellagic acid-derived metabolites, in human colonic fibroblasts. Br. J. Nutr. 2010, 104, 503–512. [CrossRef] [PubMed]
30. Kiss, A.K.; Granica, S.; Stolarczyk, M.; Melzig, M.F. Epigenetic modulation of mechanisms involved in inflammation: Influence of selected polyphenolic substances on histone acetylation state. Food Chem. 2012, 131, 1015–1020. [CrossRef]
31. Piwowarski, J.P.; Granica, S.; Zwierzyńska, M.; Stefańska, J.; Schopohl, P.; Melzig, M.F.; Kiss, A.K. Role of human gut microbiota metabolism in the anti-inflammatory effect of traditionally used ellagitannin-rich plant material. J. Ethnopharmacol. 2014, 155, 801–809. [CrossRef]
32. PADMA: Tibetische Arzneimittel Seit 1969: PADMA Hepaten. Available online: http://www.padma.at/produkte/padma-hepaten (accessed on 15 May 2011).
33. Ginsburg, I.; Koren, E.; Horani, A.; Mahamid, M.; Doron, S.; Muhanna, N.; Amer, J.; Safadi, R. Amelioration of hepatic fibrosis via Padma Hepaten is associated with altered natural killer T lymphocytes. Clin. Exp. Immun. 2009, 157, 155–164. [CrossRef]
34. United States Pharmacopeia. Simulated Gastric Fluid and Simulated Intestinal Fluid. In The United States Pharmacopeia 23, the National Formulary 18; The United States Pharmacopeial Convention, Inc.: Rockville, MD, USA, 1995; p. 2053.
35. Marambe, H.K.; Shand, P.J.; Wanasundara, J.P.D. Release of angiotensin I-converting enzyme inhibitory peptides from flaxseed (Linum usitatissimum L.) protein under simulated gastrointestinal digestion. J. Agric. Food Chem. 2011, 59, 9596–9604. [CrossRef] [PubMed]
36. Oomen, A.G.; Rompelberg, C.J.M.; Bruil, M.A.; Dobbe, C.J.G.; Pereboom, D.P.K.H.; Sips, A.J.A.M. Development of an in vitro digestion model for estimating the bioaccessibility of soil contaminants. Arch. Environ. Contam. Toxicol. 2003, 44, 281–287. [CrossRef]
37. Savoie, L.; Gauthier, S.F. Dialysis cell for the in vitro measurement of the protein digestibility. J. Food Sci. 1986, 51, 494–498. [CrossRef]
38. Lee, H.S.; Won, N.H.; Kim, K.H.; Lee, H.; Jun, W.; Lee, K.W. Antioxidant effects of aqueous extract of Terminalia chebula in vivo and in vitro. Biol. Pharm. Bull. 2005, 28, 1639–1644. [CrossRef] [PubMed]
39. Tseng, T.H.; Wang, C.J.; Kao, E.S.; Chu, H.Y. Hibiscus protocatechuic acid protects against oxidative damage induced by tert-butylhydroperoxide in rat primary hepatocytes. Chem. Biol. Interact. 1996, 101, 137–148. [CrossRef]
40. Yagi, K. Lipid peroxides and human diseases. Chem. Phys. Lipids 1987, 45, 337–351. [CrossRef]
41. Olennikov, D.N.; Kashchenko, N.I.; Schwabl, H.; Vennos, C.; Loepfe, C. New gallates of mucic acid from Phyllanthus emblica. Chem. Nat. Compd. 2015, 51, 612–617. [CrossRef]
42. Olennikov, D.N.; Kashchenko, N.I.; Schwabl, H.; Vennos, C. Application of MC-RP-HPLC-UV for the rapid and sensitive analysis of phenolic compounds in Terminalia species. Pharm. Chem. J. 2015. in press.
43. Anand, K.K.; Singh, B.; Saxena, A.K.; Chandan, B.K.; Gupta, V.N.; Bhardwaj, V. 3,4,5-Trihydroxy benzoic acid (gallic acid), the hepatoprotective principle in the fruits of Terminalia belerica-bioassay guided activity. Pharmacol. Res. 1997, 36, 315–321. [CrossRef] [PubMed]
44. Bouayed, J.; Deußer, H.; Hoffmann, L.; Bohn, T. Bioaccessible and dialysable polyphenols in selected apple varieties following in vitro digestion vs. their native patterns. Food Chem. 2012, 131, 1466–1472. [CrossRef]
45. Manach, C.; Scalbert, A.; Morand, C.; Rémésy, C.; Jiménez, L. Polyphenols: Food sources and bioavailability. Am. J. Clin. Nutr. 2004, 79, 727–747. [PubMed]
46. Shahrzad, S.; Bitsch, I. Determination of gallic acid and its metabolites in human plasma and urine by high-performance liquid chromatography. J. Chrom. B 1998, 705, 87–95. [CrossRef]
47. Shahrzad, S.; Aoyagi, K.; Winter, A.; Koyama, A.; Bitsch, I. Pharmacokinetics of gallic acid and its relative bioavailability from tea in healthy humans. J. Nutr. 2001, 131, 1207–1210. [PubMed]
48. Mertens-Talcott, S.U.; Jilma-Stohlawetz, P.; Rios, J.; Hingorani, L.; Derendorf, H. Absorption, metabolism, and antioxidant effects of pomegranate (Punica granatum L.) polyphenols after ingestion of a standardized extract in healthy human volunteers. J. Agric. Food Chem. 2006, 54, 8956–8961. [CrossRef]
49. Crozier, A.; Jaganath, I.B.; Clifford, M.N. Dietary phenolics: Chemistry, bioavailability and effects on health. Nat. Prod. Rep. 2009, 26, 1001–1043. [CrossRef] [PubMed]
50. Lei, F.; Xing, D.M.; Xiang, L.; Zhao, Y.N.; Wang, W.; Zhang, L.J.; Du, L.J. Pharmacokinetic study of ellagic acid in rat after oral administration of pomegranate leaf extract. J. Chrom. B 2003, 796, 189–194. [CrossRef]
51. Haidara, K.; Morel, I.; Abaléa, V.; Barré, M.G.; Denizeau, F. Mechanism of tert-butylhydroperoxide induced apoptosis in rat hepatocytes: Involvement of mitochondria and endoplasmic reticulum. Biochim. Biophys. Acta 2002, 1542, 173–185. [CrossRef]
52. Pfundstein, B.; Haubner, R.; Würtele, G.; Gehres, N.; Ulrich, C.M.; Owen, R.W. Pilot walnut intervention study of urolithin bioavailability in human volunteers. J. Agric. Food Chem. 2014, 62, 10264–10273. [CrossRef] [PubMed]