Ellagic acid identified through metabolomic analysis is an active metabolite in strawberry ('Seolhyang') regulating lipopolysaccharide-induced inflammation

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 18, 2014, Pages 3954-3962

  Lee, Jaehoo ^a   Kim, Sugyeong ^a   Namgung, Hyeju ^a   Jo, Young Hee ^a   Bao, Cheng ^a   Choi, Hyung Kyoon ^a   Auh, Joong Hyuck ^a   Lee, Hong Jin ^a  

^a Chung Ang University   (South Korea)

Author keywords

ellagic acid; inflammation; metabolomics; murine macrophage cells; strawberry

Indexed keywords

DISCRIMINANT ANALYSIS; FRUITS; MACROPHAGES; PATHOLOGY; LEAST SQUARES APPROXIMATIONS;

ANTI-INFLAMMATORY ACTIVITY; INFLAMMATION; METABOLOMICS; MITOGEN ACTIVATED PROTEIN KINASE; MURINE MACROPHAGES; PARTIAL LEAST SQUARES - DISCRIMINANT ANALYSIS; STRAWBERRY; TUMOR NECROSIS FACTORS;

ELLAGIC ACID;

FRAGARIA X ANANASSA; MURINAE;

ANTIINFLAMMATORY AGENT; CYCLOOXYGENASE 2; ELLAGIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; PLANT EXTRACT; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; CHEMISTRY; DRUG EFFECTS; FRAGARIA; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATION; MACROPHAGE; MOUSE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CYCLOOXYGENASE 2; ELLAGIC ACID; FRAGARIA; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NF-KAPPA B; PLANT EXTRACTS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84900327414     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf4038503     Document Type: Article

References (49)

1. Pajk, T.; Rezar, V.; Levart, A.; Salobir, J. Efficiency of apples, strawberries, and tomatoes for reduction of oxidative stress in pigs as a model for humans Nutrition 2006, 22, 376-384
2. Zafra-Stone, S.; Yasmin, T.; Bagchi, M.; Chatterjee, A.; Vinson, J. A.; Bagchi, D. Berry anthocyanins as novel antioxidants in human health and disease prevention Mol. Nutr. Food Res. 2007, 51, 675-683
3. Liu, C. J.; Lin, J. Y. Anti-inflammatory and anti-apoptotic effects of strawberry and mulberry fruit polysaccharides on lipopolysaccharide-stimulated macrophages through modulating pro-/anti-inflammatory cytokines secretion and Bcl-2/Bak protein ratio Food Chem. Toxicol. 2012, 50, 3032-3039
4. Zunino, S. J.; Parelman, M. A.; Freytag, T. L.; Stephensen, C. B.; Kelley, D. S.; Mackey, B. E.; Woodhouse, L. R.; Bonnel, E. L. Effects of dietary strawberry powder on blood lipids and inflammatory markers in obese human subjects Br. J. Nutr. 2012, 108, 900-909
5. Basu, A.; Rhone, M.; Lyons, T. J. Berries: emerging impact on cardiovascular health Nutr. Rev. 2010, 68, 168-177
6. Huntley, A. L. The health benefits of berry flavonoids for menopausal women: cardiovascular disease, cancer and cognition Maturitas 2009, 63, 297-301
7. Mink, P. J.; Scrafford, C. G.; Barraj, L. M.; Harnack, L.; Hong, C. P.; Nettleton, J. A.; Jacobs, D. R., Jr. Flavonoid intake and cardiovascular disease mortality: a prospective study in postmenopausal women Am. J. Clin. Nutr. 2007, 85, 895-909
8. Parelman, M. A.; Storms, D. H.; Kirschke, C. P.; Huang, L.; Zunino, S. J. Dietary strawberry powder reduces blood glucose concentrations in obese and lean C57BL/6 mice, and selectively lowers plasma C-reactive protein in lean mice Br. J. Nutr. 2012, 108, 1789-1799
9. da Silva Pinto, M.; Kwon, Y. I.; Apostolidis, E.; Lajolo, F. M.; Genovese, M. I.; Shetty, K. Functionality of bioactive compounds in Brazilian strawberry (Fragaria × ananassa Duch.) cultivars: evaluation of hyperglycemia and hypertension potential using in vitro models J. Agric. Food Chem. 2008, 56, 4386-4392
10. 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
11. Pinto Mda, S.; de Carvalho, J. E.; Lajolo, F. M.; Genovese, M. I.; Shetty, K. Evaluation of antiproliferative, anti-type 2 diabetes, and antihypertension potentials of ellagitannins from strawberries (Fragaria × ananassa Duch.) using in vitro models J. Med. Food 2010, 13, 1027-1035
12. Carlton, P. S.; Kresty, L. A.; Siglin, J. C.; Morse, M. A.; Lu, J.; Morgan, C.; Stoner, G. D. Inhibition of N -nitrosomethylbenzylamine-induced tumorigenesis in the rat esophagus by dietary freeze-dried strawberries Carcinogenesis 2001, 22, 441-446
13. Li, J.; Zhang, D.; Stoner, G. D.; Huang, C. Differential effects of black raspberry and strawberry extracts on BaPDE-induced activation of transcription factors and their target genes Mol. Carcinog. 2008, 47, 286-294
14. Seeram, N. P.; Adams, L. S.; Zhang, Y.; Lee, R.; Sand, D.; Scheuller, H. S.; Heber, D. Blackberry, black raspberry, blueberry, cranberry, red raspberry, and strawberry extracts inhibit growth and stimulate apoptosis of human cancer cells in vitro J. Agric. Food Chem. 2006, 54, 9329-9339
15. Wang, S. Y.; Feng, R.; Lu, Y.; Bowman, L.; Ding, M. Inhibitory effect on activator protein-1, nuclear factor-κB, and cell transformation by extracts of strawberries (Fragaria × ananassa Duch.) J. Agric. Food Chem. 2005, 53, 4187-4193
16. Wedge, D. E.; Meepagala, K. M.; Magee, J. B.; Smith, S. H.; Huang, G.; Larcom, L. L. Anticarcinogenic activity of strawberry, blueberry, and raspberry extracts to breast and cervical cancer cells J. Med. Food 2001, 4, 49-51
17. Zhang, Y.; Seeram, N. P.; Lee, R.; Feng, L.; Heber, D. Isolation and identification of strawberry phenolics with antioxidant and human cancer cell antiproliferative properties J. Agric. Food Chem. 2008, 56, 670-675
18. William Allwood, J.; Ellis, D. I.; Goodacre, R. Metabolomic technologies and their application to the study of plants and plant-host interactions Physiol. Plant. 2007, 132, 117-135
19. German, J. B.; Hammock, B. D.; Watkins, S. M. Metabolomics: building on a century of biochemistry to guide human health Metabolomics 2005, 1, 3-9
20. Schauer, N.; Fernie, A. R. Plant metabolomics: towards biological function and mechanism Trends Plant Sci. 2006, 11, 508-516
21. Heo, S.; Lee, D. Y.; Choi, H. K.; Lee, J.; Kim, J. H.; Cho, S. M.; Lee, H. J.; Auh, J. H. Metabolite fingerprinting of bokbunja (Rubus coreanus Miquel) by UPLC-qTOF-MS Food Sci. Biotechnol. 2011, 20, 567-570
22. Schauer, N.; Zamir, D.; Fernie, A. R. Metabolic profiling of leaves and fruit of wild species tomato: a survey of the Solanum lycopersicum complex J. Exp. Bot. 2005, 56, 297-307
23. Sato, S.; Soga, T.; Nishioka, T.; Tomita, M. Simultaneous determination of the main metabolites in rice leaves using capillary electrophoresis mass spectrometry and capillary electrophoresis diode array detection Plant J. 2004, 40, 151-163
24. Hamzehzarghani, H.; Kushalappa, A. C.; Dion, Y.; Rioux, S.; Comeau, A.; Yaylayan, V.; Marshall, W. D.; Mather, D. E. Metabolic profiling and factor analysis to discriminate quantitative resistance in wheat cultivars against fusarium head blight Physiol. Mol. Plant 2005, 66, 119-133
25. Hagel, J. M.; Facchini, P. J. Plant metabolomics: analytical platforms and integration with functional genomics Phytochem. Rev. 2012, 7, 479-497
26. Seger, C.; Sturm, S. Analytical aspects of plant metabolite profiling platforms: current standings and future aims J. Proteome Res. 2007, 6, 480-497
27. Maatta-Riihinen, K. R.; Kamal-Eldin, A.; Torronen, A. R. Identification and quantification of phenolic compounds in berries of Fragaria and Rubus species (family Rosaceae) J. Agric. Food Chem. 2004, 52, 6178-6187
28. Chan, E. D.; Riches, D. W. IFN-γ + LPS induction of iNOS is modulated by ERK, JNK/SAPK, and p38(mapk) in a mouse macrophage cell line Am. J. Physiol. Cell Physiol. 2001, 280, C441-C450
29. Wang, S. Y.; Zheng, W.; Galletta, G. J. Cultural system affects fruit quality and antioxidant capacity in strawberries J. Agric. Food Chem. 2002, 50, 6534-6542
30. Rothwell, J. A.; Urpi-Sarda, M.; Boto-Ordonez, M.; Knox, C.; Llorach, R.; Eisner, R.; Cruz, J.; Neveu, V.; Wishart, D.; Manach, C.; Andres-Lacueva, C.; Scalbert, A. Phenol-Explorer 2.0: a major update of the Phenol-Explorer database integrating data on polyphenol metabolism and pharmacokinetics in humans and experimental animals Database 2012, 2012, bas031
31. Medzhitov, R. Origin and physiological roles of inflammation Nature 2008, 454, 428-435
32. Jimenez-Garcia, S. N.; Guevara-Gonzalez, R. G.; Miranda-Lopez, R.; Feregrino-Perez, A. A.; Torres-Pacheco, I.; Vazquez-Cruz, M. A. Functional properties and quality characteristics of bioactive compounds in berries: biochemistry, biotechnology, and genomics Food Res. Int. 2013, 54, 1195-1207
33. Lee, D. Y.; Heo, S.; Kim, S. G.; Choi, H.-K.; Lee, H. J.; Cho, S.-M.; Auh, J.-H. Metabolomic characterization of the region- and maturity-specificity of Rubus coreanus Miquel (Bokbunja) Food Res. Int. 2013, 54, 508-515
34. Lee, H. N.; Na, H. K.; Surh, Y. J. Resolution of inflammation as a novel chemopreventive strategy Semin. Immunopathol. 2013, 35, 151-161
35. Lin, J. Y.; Tang, C. Y. Strawberry, loquat, mulberry, and bitter melon juices exhibit prophylactic effects on LPS-induced inflammation using murine peritoneal macrophages Food Chem. 2008, 107, 1587-1596
36. Liu, C. J.; Lin, J. Y. Anti-inflammatory effects of phenolic extracts from strawberry and mulberry fruits on cytokine secretion profiles using mouse primary splenocytes and peritoneal macrophages Int. Immunopharmacol. 2013, 16, 165-170
37. Maurya, M. R.; Gupta, S.; Li, X.; Fahy, E.; Dinasarapu, A. R.; Sud, M.; Brown, H. A.; Glass, C. K.; Murphy, R. C.; Russell, D. W.; Dennis, E. A.; Subramaniam, S. Analysis of inflammatory and lipid metabolic networks across RAW264.7 and thioglycolate-elicited macrophages J. Lipid Res. 2013, 54, 2525-2542
38. Marin, M.; Maria Giner, R.; Rios, J. L.; Carmen Recio, M. Intestinal anti-inflammatory activity of ellagic acid in the acute and chronic dextrane sulfate sodium models of mice colitis J. Ethnopharmacol. 2013, 10.1016/j.jep.2013.09.030
39. Rosillo, M. A.; Sanchez-Hidalgo, M.; Cardeno, A.; Aparicio-Soto, M.; Sanchez-Fidalgo, S.; Villegas, I.; de la Lastra, C. A. Dietary supplementation of an ellagic acid-enriched pomegranate extract attenuates chronic colonic inflammation in rats Pharmacol. Res. 2012, 66, 235-242
40. Rosillo, M. A.; Sanchez-Hidalgo, M.; Cardeno, A.; de la Lastra, C. A. Protective effect of ellagic acid, a natural polyphenolic compound, in a murine model of Crohn's disease Biochem. Pharmacol. 2011, 82, 737-745
41. Karlsson, S.; Nanberg, E.; Fjaeraa, C.; Wijkander, J. Ellagic acid inhibits lipopolysaccharide-induced expression of enzymes involved in the synthesis of prostaglandin E2 in human monocytes Br. J. Nutr. 2010, 103, 1102-1109
42. Lee, W. J.; Ou, H. C.; Hsu, W. C.; Chou, M. M.; Tseng, J. J.; Hsu, S. L.; Tsai, K. L.; Sheu, W. H. Ellagic acid inhibits oxidized LDL-mediated LOX-1 expression, ROS generation, and inflammation in human endothelial cells J. Vasc. Surg. 2010, 52, 1290-1300
43. Cordenunsi, B. R.; Oliveira do Nascimento, J. R.; Genovese, M. I.; Lajolo, F. M. Influence of cultivar on quality parameters and chemical composition of strawberry fruits grown in Brazil J. Agric. Food Chem. 2002, 50, 2581-2586
44. Espin, J. C.; Gonzalez-Barrio, R.; Cerda, B.; Lopez-Bote, C.; Rey, A. I.; Tomas-Barberan, 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
45. Larrosa, M.; Tomas-Barberan, F. A.; Espin, J. C. The dietary hydrolysable tannin punicalagin releases ellagic acid that induces apoptosis in human colon adenocarcinoma Caco-2 cells by using the mitochondrial pathway J. Nutr. Biochem. 2006, 17, 611-625
46. Gonzalez-Barrio, R.; Borges, G.; Mullen, W.; Crozier, A. Bioavailability of anthocyanins and ellagitannins following consumption of raspberries by healthy humans and subjects with an ileostomy J. Agric. Food Chem. 2010, 58, 3933-3939
47. Cerda, B.; Tomas-Barberan, F. A.; Espin, J. C. Metabolism of antioxidant and chemopreventive ellagitannins from strawberries, raspberries, walnuts, and oak-aged wine in humans: identification of biomarkers and individual variability J. Agric. Food Chem. 2005, 53, 227-235
48. Espin, J. C.; Larrosa, M.; Garcia-Conesa, M. T.; Tomas-Barberan, F. Biological significance of urolithins, the gut microbial ellagic acid-derived metabolites: the evidence so far. Evidence-Based Complement. Alternat. Med. 2013, DOI: 10.1155/2013/270418.
49. Gimenez-Bastida, J. A.; Larrosa, M.; Gonzalez-Sarrias, A.; Tomas-Barberan, F.; Espin, 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