Hydrolysis of Dicaffeoylquinic Acids from Ilex kudingcha Happens in the Colon by Intestinal Microbiota

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 51, 2016, Pages 9624-9630

  Xie, Minhao ^a   Chen, Guijie ^a   Hu, Bing ^a   Zhou, Li ^a   Ou, Shiyi ^b   Zeng, Xiaoxiong ^a   Sun, Yi ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b JINAN UNIVERSITY   (China)

Author keywords

dicaffeoylquinic acid; digestion in vitro; intestinal microbiota; kudingcha

Indexed keywords

ANAEROBIC DIGESTION; BODY FLUIDS; DATA HANDLING; FERMENTATION;

ANAEROBIC FERMENTATION; ARTIFICIAL SALIVA; DICAFFEOYLQUINIC ACIDS; IN-VITRO; KUDINGCHA; MICROBIAL COMPOSITION; MICROBIOTAS; SMALL INTESTINE;

HYDROLYSIS;

CAFFEOYLQUINIC ACID; PLANT EXTRACT; QUINIC ACID;

ANALOGS AND DERIVATIVES; BACTERIUM; CACO-2 CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; COLON; HUMAN; HYDROLYSIS; ILEX; INTESTINE FLORA; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY;

BACTERIA; CACO-2 CELLS; COLON; GASTROINTESTINAL MICROBIOME; HUMANS; HYDROLYSIS; ILEX; MOLECULAR STRUCTURE; PLANT EXTRACTS; QUINIC ACID;

EID: 85008625511     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b04710     Document Type: Article

References (52)

1. Zhu, F.; Cai, Y. Z.; Sun, M.; Ke, J. X.; Lu, D. Y.; Corke, H. Comparison of major phenolic constituents and in vitro antioxidant activity of diverse kudingcha genotypes from Ilex kudingcha, Ilex cornuta, and Ligustrum robustum J. Agric. Food Chem. 2009, 57, 6082-6089 10.1021/jf901020h
2. Fan, J. L.; Wu, Z. W.; Zhao, T. H.; Sun, Y.; Ye, H.; Xu, R. J.; Zeng, X. X. Characterization, antioxidant and hepatoprotective activities of polysaccharides from Ilex latifolia Thunb Carbohydr. Polym. 2014, 101, 990-997 10.1016/j.carbpol.2013.10.037
3. Li, L.; Xu, L. J.; Ma, G. Z.; Dong, Y. M.; Peng, Y.; Xiao, P. G. The large-leaved kudingcha (Ilex latifolia Thunb and Ilex kudingcha C.J. Tseng): a traditional Chinese tea with plentiful secondary metabolites and potential biological activities J. Nat. Med. 2013, 67, 425-437 10.1007/s11418-013-0758-z
4. Zhu, K.; Li, G.; Sun, P.; Wang, R.; Qian, Y.; Zhao, X. In vitro and in vivo anti-cancer activities of kuding tea (Ilex kudingcha C.J. Tseng) against oral cancer Exp. Ther. Med. 2014, 7, 709-715 10.3892/etm.2013.1450
5. Song, J. L.; Qian, Y.; Li, G. J.; Zhao, X. Anti-inflammatory effects of kudingcha methanol extract (Ilex kudingcha C.J. Tseng) in dextran sulfate sodium-induced ulcerative colitis Mol. Med. Rep. 2013, 8, 1256-1262 10.3892/mmr.2013.1635
6. Zhao, X.; Wang, Q.; Qian, Y.; Song, J. L. Ilex kudingcha C.J. Tseng (Kudingcha) has in vitro anticancer activities in MCF-7 human breast adenocarcinoma cells and exerts anti-metastatic effects in vivo Oncol. Lett. 2013, 5, 1744-1748 10.3892/ol.2013.1253
7. Zhao, X.; Wang, Q.; Qian, Y.; Song, J. L. Ilex kudingcha C.J. Tseng (kudingcha) prevents HCl/ethanol-induced gastric injury in Sprague-Dawley rats Mol. Med. Rep. 2013, 7, 1613-1616 10.3892/mmr.2013.1402
8. Fan, S. J.; Zhang, Y.; Hu, N.; Sun, Q. H.; Ding, X. B.; Li, G. W.; Zheng, B.; Gu, M.; Huang, F. S.; Sun, Y. Q.; Zhou, Z. Q.; Lu, X.; Huang, C.; Ji, G. Extract of kuding tea prevents high-fat diet-induced metabolic disorders in C57BL/6 mice via liver X receptor (LXR) β antagonism PLoS One 2012, 7 ( 12 ) e51007 10.1371/journal.pone.0051007
9. Song, C. W.; Xie, C.; Zhou, Z. W.; Yu, S. G.; Fang, N. B. Antidiabetic effect of an active components group from Ilex kudingcha and its chemical composition Evidence-Based Complement. Altern. Med. 2012, 2012, 423690 10.1155/2012/423690
10. Kim, J. Y.; Jeong, H. Y.; Lee, H. K.; Yoo, J. K.; Bae, K.; Seong, Y. H. Protective effect of Ilex latifolia, a major component of kudingcha, against transient focal ischemia-induced neuronal damage in rats J. Ethnopharmacol. 2011, 133, 558-564 10.1016/j.jep.2010.10.037
11. Hu, T.; He, X. W.; Jiang, J. G.; Xu, X. L. Efficacy evaluation of a Chinese bitter tea (Ilex latifolia Thunb.) via analyses of its main components Food Funct. 2014, 5, 876-881 10.1039/c3fo60603a
12. Wang, Q. C.; Zhang, X.; Zhang, W. Q.; Sun, X. Q.; Hu, B.; Sun, Y.; Zeng, X. X. Purification and HPLC analysis of caffeoylquinic acids from kudingcha made from Ilex kudingcha C.J. Tseng Food Sci. 2013, 34 ( 22 ) 119-122 (in Chinese)
13. Hu, T.; He, X. W.; Jiang, J. G. Functional analyses on antioxidant, anti-inflammatory, and antiproliferative effects of extracts and compounds from Ilex latifolia Thunb., a Chinese bitter tea J. Agric. Food Chem. 2014, 62, 8608-8615 10.1021/jf501670v
14. Lima, J. D.; Farah, A.; King, B.; de Paulis, T.; Martin, P. R. Distribution of major chlorogenic acids and related compounds in Brazilian green and toasted Ilex paraguariensis (Mate) leaves J. Agric. Food Chem. 2016, 64, 2361-2370 10.1021/acs.jafc.6b00276
15. Dugo, P.; Cacciola, F.; Donato, P.; Jacques, R. A.; Caramão, E. B.; Mondello, L. High efficiency liquid chromatography techniques coupled to mass spectrometry for the characterization of mate extracts J. Chromatogr. A 2009, 1216, 7213-7221 10.1016/j.chroma.2009.08.030
16. n of the chlorogenic acids and hydroxycinnamoylshikimate esters in Mate (Ilex paraguariensis) J. Agric. Food Chem. 2010, 58, 5471-5484 10.1021/jf904537z
17. Xu, D. L.; Wang, Q. C.; Zhang, W. Q.; Hu, B.; Zhou, L.; Zeng, X. X.; Sun, Y. Inhibitory activities of caffeoylquinic acid derivatives from Ilex kudingcha C.J. Tseng on α-glucosidase from Saccharomyces cerevisiae J. Agric. Food Chem. 2015, 63, 3694-3703 10.1021/acs.jafc.5b00420
18. Sun, Y.; Zhang, X.; Zhang, W. Q.; Zeng, X. X.; Hu, Q. H. Purification and structural identification of polyphenols in kudingcha Food Sci. 2011, 32 ( 11 ) 60-63 (in Chinese)
19. Liu, L. X.; Sun, Y.; Laura, T.; Liang, X. F.; Ye, H.; Zeng, X. X. Determination of polyphenolic content and antioxidant activity of kudingcha made from Ilex kudingcha C.J. Tseng Food Chem. 2009, 112, 35-41 10.1016/j.foodchem.2008.05.038
20. IUPAC. Nomenclature of cyclitols. Biochem. J. 1976, 153, 23-31 10.1042/bj1530023.
21. Markovic, S.; Tosovic, J. Comparative study of the antioxidative activities of caffeoylquinic and caffeic acids Food Chem. 2016, 210, 585-592 10.1016/j.foodchem.2016.05.019
22. Bajko, E.; Kalinowska, M.; Borowski, P.; Siergiejczyk, L.; Lewandowski, W. 5-O-Caffeoylquinic acid: a spectroscopic study and biological screening for antimicrobial activity LWT-Food Sci. Technol. 2016, 65, 471-479 10.1016/j.lwt.2015.08.024
23. Huang, K.; Liang, X. C.; Zhong, Y. L.; He, W. Y.; Wang, Z. 5-Caffeoylquinic acid decreases diet-induced obesity in rats by modulating PPARα and LXRα transcription J. Sci. Food Agric. 2015, 95, 1903-1910 10.1002/jsfa.6896
24. Liu, S. L.; Peng, B. J.; Zhong, Y. L.; Liu, Y. L.; Song, Z.; Wang, Z. Effect of 5-caffeoylquinic acid on the NF-κB signaling pathway, peroxisome proliferator-activated receptor gamma 2, and macrophage infiltration in high-fat diet-fed Sprague-Dawley rat adipose tissue Food Funct. 2015, 6, 2779-2786 10.1039/C5FO00626K
25. Tong, J.; Ma, B. X.; Ge, L. L.; Mo, Q. G.; Zhou, G.; He, J. S.; Wang, Y. W. Dicaffeoylquinic acid-enriched fraction of Cichorium glandulosum seeds attenuates experimental type 1 diabetes via multipathway protection J. Agric. Food Chem. 2015, 63, 10791-10802 10.1021/acs.jafc.5b04552
26. Stalmach, A.; Steiling, H.; Williamson, G.; Crozier, A. Bioavailability of chlorogenic acids following acute ingestion of coffee by humans with an ileostomy Arch. Biochem. Biophys. 2010, 501, 98-105 10.1016/j.abb.2010.03.005
27. Stalmach, A.; Mullen, W.; Barron, D.; Uchida, K.; Yokota, T.; Cavin, C.; Steiling, H.; Williamson, G.; Crozier, A. Metabolite profiling of hydroxycinnamate derivatives in plasma and urine after the ingestion of coffee by humans: identification of biomarkers of coffee consumption Drug Metab. Dispos. 2009, 37, 1749-1758 10.1124/dmd.109.028019
28. Lafay, S.; Gil-Izquierdo, A.; Manach, C.; Morand, C.; Besson, C.; Scalbert, A. Chlorogenic acid is absorbed in its intact form in the stomach of rats J. Nutr. 2006, 136, 1192-1197
29. Erk, T.; Hauser, J.; Williamson, G.; Renouf, M.; Steiling, H.; Dionisi, F.; Richling, E. Structure-and dose-absorption relationships of coffee polyphenols Biofactors 2014, 40, 103-112 10.1002/biof.1101
30. da Encarnacao, J. A.; Farrell, T. L.; Ryder, A.; Kraut, N. U.; Williamson, G. In vitro enzymic hydrolysis of chlorogenic acids in coffee Mol. Nutr. Food Res. 2015, 59, 231-239 10.1002/mnfr.201400498
31. Ludwig, I. A.; de Pena, M. P.; Cid, C.; Crozier, A. Catabolism of coffee chlorogenic acids by human colonic microbiota Biofactors 2013, 39, 623-632 10.1002/biof.1124
32. Luo, Q.; Boom, R. M.; Janssen, A. E. M. Digestion of protein and protein gels in simulated gastric environment LWT-Food Sci. Technol. 2015, 63, 161-168 10.1016/j.lwt.2015.03.087
33. Hu, J. L.; Nie, S. P.; Min, F. F.; Xie, M. Y. Artificial simulated saliva, gastric and intestinal digestion of polysaccharide from the seeds of Plantago asiatica L Carbohydr. Polym. 2013, 92, 1143-1150 10.1016/j.carbpol.2012.10.072
34. Farrell, T. L.; Gomez-Juaristi, M.; Poquet, L.; Redeuil, K.; Nagy, K.; Renouf, M.; Williamson, G. Absorption of dimethoxycinnamic acid derivatives in vitro and pharmacokinetic profile in human plasma following coffee consumption Mol. Nutr. Food Res. 2012, 56, 1413-1423 10.1002/mnfr.201200021
35. Zhou, L.; Wang, W.; Huang, J.; Ding, Y.; Pan, Z.; Zhao, Y.; Zhang, R.; Hu, B.; Zeng, X. X. In vitro extraction and fermentation of polyphenols from grape seeds (Vitis vinifera) by human intestinal microbiota Food Funct. 2016, 7, 1959-1967 10.1039/C6FO00032K
36. Zhang, X.; Yang, Y.; Wu, Z.; Weng, P. The modulatory effect of anthocyanins from purple sweet potato on human intestinal microbiota in vitro J. Agric. Food Chem. 2016, 64, 2582-2590 10.1021/acs.jafc.6b00586
37. Thuong, P. T.; Su, N. D.; Ngoc, T. M.; Hung, T. M.; Dang, N. H.; Thuan, N. D.; Bae, K. H.; Oh, W. K. Antioxidant activity and principles of Vietnam bitter tea Ilex kudingcha Food Chem. 2009, 113, 139-145 10.1016/j.foodchem.2008.07.041
38. Ekbatan, S. S.; Sleno, L.; Sabally, K.; Khairallah, J.; Azadi, B.; Rodes, L.; Prakash, S.; Donnelly, D. J.; Kubow, S. Biotransformation of polyphenols in a dynamic multistage gastrointestinal model Food Chem. 2016, 204, 453-462 10.1016/j.foodchem.2016.02.140
39. Mosele, J. I.; Macia, A.; Romero, M. P.; Motilva, M. J. Stability and metabolism of Arbutus unedo bioactive compounds (phenolics and antioxidants) under in vitro digestion and colonic fermentation Food Chem. 2016, 201, 120-130 10.1016/j.foodchem.2016.01.076
40. Hu, B.; Cui, F.; Yin, F.; Zeng, X. X.; Sun, Y.; Li, Y. Q. Caffeoylquinic acids competitively inhibit pancreatic lipase through binding to the catalytic triad Int. J. Biol. Macromol. 2015, 80, 529-535 10.1016/j.ijbiomac.2015.07.031
41. Naish, M.; Clifford, M. N.; Birch, G. G. Sensory astringency of 5-O-caffeoylquinic acid, tannic acid and grape-seed tannin by a time-intensity procedure J. Sci. Food Agric. 1993, 61, 57-64 10.1002/jsfa.2740610110
42. Deshpande, S.; Jaiswal, R.; Matei, M. F.; Kuhnert, N. Investigation of acyl migration in mono-and dicaffeoylquinic acids under aqueous basic, aqueous acidic, and dry roasting conditions J. Agric. Food Chem. 2014, 62, 9160-9170 10.1021/jf5017384
43. Li, Y.-J.; Zhang, C.-F.; Ding, G.; Huang, W.-Z.; Wang, Z.-Z.; Bi, Y.-A.; Xiao, W. Investigating the thermal stability of six caffeoylquinic acids employing rapid-resolution liquid chromatography with quadrupole time-of-flight tandem mass spectrometry Eur. Food Res. Technol. 2015, 240, 1225-1234 10.1007/s00217-015-2425-y
44. Matei, M. F.; Jaiswal, R.; Kuhnert, N. Investigating the chemical changes of chlorogenic acids during coffee brewing: conjugate addition of water to the olefinic moiety of chlorogenic acids and their quinides J. Agric. Food Chem. 2012, 60, 12105-12115 10.1021/jf3028599
45. Xie, C.; Yu, K.; Zhong, D.; Yuan, T.; Ye, F.; Jarrell, J. A.; Millar, A.; Chen, X. Investigation of isomeric transformations of chlorogenic acid in buffers and biological matrixes by ultraperformance liquid chromatography coupled with hybrid quadrupole/ion mobility/orthogonal acceleration time-of-flight mass spectrometry J. Agric. Food Chem. 2011, 59, 11078-11087 10.1021/jf203104k
46. Rastogi, H.; Jana, S. Evaluation of physicochemical properties and intestinal permeability of six dietary polyphenols in human intestinal colon adenocarcinoma Caco-2 cells Eur. J. Drug Metab. Pharmacokinet. 2016, 41, 33-43 10.1007/s13318-014-0234-5
47. David, L. A.; Maurice, C. F.; Carmody, R. N.; Gootenberg, D. B.; Button, J. E.; Wolfe, B. E.; Ling, A. V.; Devlin, A. S.; Varma, Y.; Fischbach, M. A.; Biddinger, S. B.; Dutton, R. J.; Turnbaugh, P. J. Diet rapidly and reproducibly alters the human gut microbiome Nature 2014, 505, 559-563 10.1038/nature12820
48. van Duynhoven, J.; Vaughan, E. E.; Jacobs, D. M.; Kemperman, R. A.; van Velzen, E. J. J.; Gross, G.; Roger, L. C.; Possemiers, S.; Smilde, A. K.; Dore, J.; Westerhuis, J. A.; Van de Wiele, T. Metabolic fate of polyphenols in the human superorganism Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 4531-4538 10.1073/pnas.1000098107
49. Mosele, J. I.; Macia, A.; Motilva, M. J. Metabolic and microbial modulation of the large intestine ecosystem by non-absorbed diet phenolic compounds: a review Molecules 2015, 20, 17429-17468 10.3390/molecules200917429
50. Chen, H. D.; Sang, S. M. Biotransformation of tea polyphenols by gut microbiota J. Funct. Foods 2014, 7, 26-42 10.1016/j.jff.2014.01.013
51. Low, D. Y.; Hodson, M. P.; Williams, B. A.; D’Arcy, B. R.; Gidley, M. J. Microbial biotransformation of polyphenols during in vitro colonic fermentation of masticated mango and banana Food Chem. 2016, 207, 214-222 10.1016/j.foodchem.2016.03.108
52. Barroso, E.; Cueva, C.; Peláez, C.; Martínez-Cuesta, M. C.; Requena, T. Development of human colonic microbiota in the computer-controlled dynamic SIMulator of the GastroIntestinal tract SIMGI LWT-Food Sci. Technol. 2015, 61, 283-289 10.1016/j.lwt.2014.12.014