Structural elucidation and biological fate of two glucuronyl metabolites of pelargonidin 3-O β-d-glucopyranoside in rats

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 3, 2013, Pages 569-578

  Ichiyanagi, Takashi ^a,d   Kashiwada, Yoshiki ^b   Shida, Yasuo ^c   Sekiya, Michiko ^a   Hatano, Yoshihiko ^a   Takaishi, Yoshihisa ^b   Ikeshiro, Yasumasa ^a  

^a NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

^c TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^d NIIGATA INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

anthocyanin; bioavailability; metabolic fate; pelargonidin 3 O D glucopyranoside; pelargonidin 3 O D glucuronide

Indexed keywords

BIOAVAILABILITY; BIOLOGICAL PROPERTIES; BLOOD PLASMA; GLUCURONIDES; HETERONUCLEAR; IN-VIVO; METABOLIC FATE; PELARGONIDIN; STRAWBERRY FRUITS; STRUCTURAL ELUCIDATION; URINE SAMPLE;

BIOCHEMISTRY; BIOMOLECULES; FRUITS; METABOLITES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; RATS;

ANTHOCYANINS;

ANTHOCYANIN; GLUCURONIDE; PELARGONIDIN; PELARGONIDIN 3 GLUCOSIDE; PELARGONIDIN-3-GLUCOSIDE;

ABSORPTION; ANIMAL; ARTICLE; BIOAVAILABILITY; BLOOD; CHEMISTRY; DOSE RESPONSE; FRAGARIA; FRUIT; MALE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ORAL DRUG ADMINISTRATION; RAT; URINE; WISTAR RAT;

ABSORPTION; ADMINISTRATION, ORAL; ANIMALS; ANTHOCYANINS; BIOLOGICAL AVAILABILITY; DOSE-RESPONSE RELATIONSHIP, DRUG; FRAGARIA; FRUIT; GLUCURONIDES; MAGNETIC RESONANCE SPECTROSCOPY; MALE; RATS; RATS, WISTAR;

FRAGARIA X ANANASSA; MAMMALIA; RATTUS;

EID: 84872855880     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf3032793     Document Type: Article

References (45)

1. Hyson, D. A. A comprehensive review of apples and apple components and their relationship to human health Adv. Nutr. 2011, 2, 408-420
2. Hamer, M.; Chida, Y. Intake of fruit, vegetables, and antioxidants and risk of type 2 diabetes: systematic review and meta-analysis J. Hypertens. 2007, 25, 2361-2369
3. Zhou, J. R. Soy and the prevention of lifestyle-related diseases Clin. Exp. Pharmacol. Physiol. 2004, 31, 14S-19S
4. Chen, Z. Y.; Jiao, R.; Ma, K. Y. Cholesterol-lowering nutraceuticals and functional foods J. Agric. Food Chem. 2008, 56, 8761-8773
5. Arts, I. C.; Hollman, P. C. Polyphenols and disease risk in epidemiologic studies Am. J. Clin. Nutr. 2005, 81, 317S-325S
6. Lecour, S.; Lamont, K. T. Natural polyphenols and cardioprotection Mini Rev. Med. Chem. 2011, 11, 1191-1199
7. Matsumoto, H.; Hanamura, S.; Kawakami, T.; Sato, Y.; Hirayama, M. Preparative-scale isolation of four anthocyanin components of black currant (Ribes nigrum L.) fruits J. Agric. Food Chem. 2001, 49, 1541-1545
8. Garcia-Viguera, C.; Zafrilla, P.; Tomas-Barveran, A. The use of acetone as extraction solvent for anthocyanins from strawberry fruit Phytochem. Anal. 1998, 9, 274-277
9. Wu, X.; Prior, R. L. Identification and characterization of anthocyanins by high-performance liquid chromatography-electrospray ionization-tandem mass spectrometry in common foods in the United States: vegetables, nuts, and grains J. Agric. Food Chem. 2005, 53, 3101-3113
10. Ichiyanagi, T.; Kashiwada, Y.; Shida, Y.; Ikeshiro, Y. Nasunin from eggplant consists of cis-trans isomers of delphinidin 3-[4-(p -coumaroyl)- l -rhamnosyl (1→6)glucopyranoside]-5-glucopyranoside J. Agric. Food Chem. 2000, 148, 119-123
11. Wu, X.; Beecher, G.; Holden, J. M.; Haytowitz, D. B.; Prior, R. L. Concentration of anthocyanins in common foods in the United States and estimation of normal consumption J. Agric. Food Chem. 2006, 54, 4069-4075
12. Chen, P. N.; Chu, S. C.; Chiou, H. L.; Chiang, C. L.; Yang, S. F.; Hsieh, Y. S. Cyanidin 3-glucoside and peonidin 3-glucoside inhibit tumor cell growth and induce apoptosis in vitro and suppress tumor growth in vivo Nutr. Cancer 2005, 53, 232-243
13. Hafeez, B. B.; Siddiqui, I. A.; Asim, M.; Malik, A.; Afaq, F.; Adhami, V. M.; Saleem, M.; Din, M.; Mukhtar, H. A. A dietary anthocyanidin delphinidin induces apoptosis of human prostate cancer PC3 cells in vitro and in vivo: involvement of nuclear factor-κB signaling Cancer Res. 2008, 68, 8564-8572
14. Iida, H.; Nakamura, Y.; Matsumoto, H.; Takeuchi, Y.; Harano, S.; Ishihara, M.; Katsumi, O. Effect of black-currant extract on negative lens-induced ocular growth in chicks Ophthalmic Res. 2010, 44, 242-250
15. Rahman, M. M.; Ichiyanagi, T.; Komiyama, T.; Sato, S.; Konishi, T. Effects of anthocyanins on psychological stress-induced oxidative stress and neurotransmitter status J. Agric. Food Chem. 2008, 56, 7545-7550
16. Wei, X.; Wang, D.; Yang, Y.; Xia, M.; Li, D.; Li, G.; Zhu, Y.; Xiao, Y.; Ling, W. Cyanidin-3- O -β-glucoside improves obesity and triglyceride metabolism in KK-Ay mice by regulating lipoprotein lipase activity J. Sci. Food Agric. 2011, 91, 1006-1013
17. Scazzocchio, B.; Varì, R.; Filesi, C.; D'Archivio, M.; Santangelo, C.; Giovannini, C.; Iacovelli, A.; Silecchia, G.; Li Volti, G.; Galvano, F.; Masella, R. Cyanidin-3- O -β-glucoside and protocatechuic acid exert insulin-like effects by upregulating PPARγ activity in human omental adipocytes Diabetes 2011, 60, 2234-2244
18. Ichiyanagi, T.; Terahara, N.; Rahman, M. M.; Konishi, T. Gastrointestinal uptake of nasunin, acylated anthocyanin in eggplant J. Agric. Food Chem. 2006, 54, 5306-5312
19. Ichiyanagi, T.; Shida, Y.; Rahman, M. M.; Hatano, Y.; Konishi, T. Bioavailability and tissue distribution of anthocyanins in bilberry (Vaccinium myrtillus L.) extract in rats J. Agric. Food Chem. 2006, 54, 6578-6587
20. Matsumoto, H.; Inaba, H.; Kishi, M.; Tominaga, S.; Hirayama, M.; Tsuda, T. Orally administered delphinidin 3-rutinoside and cyanidin 3-rutinoside are directly absorbed in rats and humans and appear in the blood as the intact forms J. Agric. Food Chem. 2001, 49, 1546-1551
21. Wu, X.; Cao, G.; Prior, R. L. Absorption and metabolism of anthocyanins in elderly women after consumption of elderberry or blueberry J. Nutr. 2002, 132, 1865-1871
22. Matsumoto, H.; Ichiyanagi, T.; Iida, H.; Ito, K.; Tsuda, T.; Hirayama, M.; Konishi, T. Ingested delphinidin-3-rutinoside is primarily excreted to urine as the intact form and to bile as the methylated form in rats J. Agric. Food Chem. 2006, 54, 578-582
23. Ichiyanagi, T.; Rahman, M. M.; Hatano, Y.; Konishi, T.; Ikeshiro, Y. Protocatechuic acid is not the major metabolite in rat blood plasma after oral administration of cyanidin 3- O -β- d -glucopyranoside Food Chem. 2007, 105, 1032-1039
24. Okushio, K.; Suzuki, M.; Matsumoto, N.; Nanjo, F.; Hara, Y. Identification of (-)-epicatechin metabolites and their metabolic fate in the rat Drug Metab. Dispos. 1999, 27, 309-316
25. Ichiyanagi, T.; Rahman, M. M.; Kashiwada, K.; Ikeshiro, Y.; Shida, Y.; Hatano, Y.; Matsumoto, H.; Hirayama, M.; Tsuda, T.; Konishi, T. Absorption and metabolism of delphinidin 3- O -β- d -glucopyranoside in rats Free Radical Biol. Med. 2004, 36, 930-937
26. Ichiyanagi, T.; Shida, Y.; Rahman, M. M.; Hatano, Y.; Matsumoto, H.; Hirayama, M.; Konishi, T. Metabolic pathway of cyanidin 3- O -β- d -glucopyranoside in rats J. Agric. Food Chem. 2005, 53, 145-150
27. Piskula, M. K.; Terao, J. Accumulation of (-)-epicatechin metabolites in rat plasma after oral administration and distribution of conjugation enzymes in rat tissues J. Nutr. 1998, 128, 1172-1178
28. Sesink, A. L.; O'Leary, K. A.; Hollman, P. C. Quercetin glucuronides but not glucosides are present in human plasma after consumption of quercetin-3-glucoside or quercetin-4′-glucoside J. Nutr. 2001, 131, 1938-1941
29. Ichiyanagi, T.; Shida, Y.; Rahman, M. M.; Hatano, Y.; Konishi, T. Extended glucuronidation is another major path of cyanidin 3- O -β- d -glucopyranoside metabolism in rats J. Agric. Food Chem. 2005, 53, 7312-7319
30. Felgines, C.; Talavera, S.; Gothier, M. P.; Texier, O.; Scalbert, A.; Lamaison, J. I.; Remesy, C. Strawberry anthocyanins are recovered in urine as glucuoro-and sulfoconjugates in humans J. Nutr. 2003, 133, 1296-1301
31. Mullen, W.; Edwards, C. A.; Serafini, M.; Crozier, A. Bioavailability of pelargonidin-3- O -glucoside and its metabolites in humans following the ingestion of strawberries with and without cream J. Agric. Food Chem. 2008, 56, 713-719
32. Carkeet, C.; Clevidence, B. A.; Novotny, J. A. Anthocyanin excretion by human increases linearly with increasing strawberry dose J. Nutr. 2008, 138, 897-902
33. Felgines, C.; Texier, O.; Besson, C.; Lyan, B.; Lamaison, J. L.; Scalbert, A. Strawberry pelargonidin glycosides are excreted in urine as intact glycosides and glucuronidated pelargonidin derivatives in rats Br. J. Nutr. 2007, 96, 1-6
34. Ichiyanagi, T.; Hatano, Y.; Matsugo, S.; Konishi, T. Structural dependence of HPLC separation pattern of anthocyanins from bilberry (Vaccinium myrtillus L.) Chem. Pharm. Bull. 2004, 52, 628-630
35. Moon, J. H.; Tsushida, T.; Nakahara, K.; Terao, J. Identification of quercetin 3- O -β- d -glucuronide as an antioxidative metabolite in rat plasma after oral administration of quercetin Free Radical Biol. Med. 2001, 30, 1274-1285
36. Natsume, M.; Osakabe, N.; Oyama, M.; Sasaki, M.; Baba, S.; Nakamura, Y.; Osawa, T.; Terao, J. Structure of (-)-epicatechin glucuronide identified from plasma and urine after oral ingestion of (-)-epicatechin: differences between human and rat Free Radical Biol. Med. 2003, 34, 840-849
37. Ichiyanagi, T.; Shida, Y.; Rahman, M. M.; Sekiya, M.; Hatano, Y.; Matsumoto, H.; Hirayama, M.; Konishi, T.; Ikeshiro, Y. Effect on both aglycone and sugar moiety towards phase II metabolism of anthocyanins Food Chem. 2008, 106, 493-500
38. DuPont, M. S.; Day, A. J.; Bennett, R. N.; Mellon, F. A.; Kroon, P. A. Absorption of kaempferol from endive, a source of kaempferol-3-glucuronide, in humans Eur. J. Clin. Nutr. 2004, 58, 947-954
39. Rhaman, M. M.; Ichiyanagi, T.; Komiyama, T.; Hatano, Y.; Konishi, T. Superoxide radical-and peroxynitrite-scavenging activity of anthocyanins; structure-activity relationship and their synergism Free Radical Res. 2006, 40, 993-1002
40. Katsube, N.; Iwashita, K.; Tsushida, T.; Yamaki, K.; Kobori, M. Induction of apoptosis in cancer cells by bilberry (Vaccinium myrtillus) and the anthocyanins J. Agric. Food Chem. 2003, 51, 68-75
41. Cao, G.; Muccitelli, H. U.; Sanchez-Moreno, C.; Prior, R. L. Anthocyanins are absorbed in glycated forms in elderly women: a pharmacokinetic study Am. J. Clin. Nutr. 2001, 73, 920-926
42. Matsumoto, H.; Ito, K.; Yonekura, K.; Tsuda, T.; Ichiyanagi, T.; Hirayama, M.; Konishi, T. Enhanced absorption of anthocyanins after oral administration of phytic acid in rats and humans J. Agric. Food Chem. 2007, 55, 2489-2496
43. Spencer, J. P. E.; Schroeter, H.; Kuhnle, G.; Srai, S. K. S.; Tyrrell, R. M.; Hahn, U.; Rice-Evans, C. Epicatechin and its in vivo metabolite, 3′- O -methyl epicatechin, protect human fibroblasts from oxidative stress-induced cell death involving caspase-3 activation Biochem. J. 2001, 354, 493-500
44. Angeloni, C.; Spencer, J. P.; Leoncini, E.; Biagi, P. L.; Hrelia, S. Role of quercetin and its in vivo metabolites in protecting H9c2 cells against oxidative stress Biochimie 2007, 89, 73-82
45. Edirisinghe, I.; Banaszewski, K.; Cappozzo, J.; Sandhya, K.; Ellis, C. L.; Tadapaneni, R.; Kappagoda, C. T.; Burton-Freeman, B. M. Strawberry anthocyanin and its association with postprandial inflammation and insulin Br. J. Nutr. 2011, 106, 913-922