Black Currant Anthocyanins Attenuate Weight Gain and Improve Glucose Metabolism in Diet-Induced Obese Mice with Intact, but Not Disrupted, Gut Microbiome

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 27, 2015, Pages 6172-6180

  Esposito, Debora ^a   Damsud, Thanakorn ^a,b   Wilson, Mickey ^a   Grace, Mary H ^a   Strauch, Renee ^a   Li, Xu ^a   Lila, Mary Ann ^a   Komarnytsky, Slavko ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b RAJAMANGALA UNIVERSITY OF TECHNOLOGY SRIVIJAYA   (Thailand)

Author keywords

functional food; gastrointestinal tract; gut microbiome; inflammation; obesity

Indexed keywords

ANTIBIOTICS; BIOCHEMISTRY; BIODEGRADATION; FUNCTIONAL FOOD; GLUCOSE; MAMMALS; METABOLISM; NUTRITION; PATHOLOGY; PHYSIOLOGY;

ANTHOCYANIN CONTENT; GASTROINTESTINAL TRACT; INFLAMMATION; MICROBIAL DEGRADATION; MICROBIOME; OBESITY; PROTECTIVE EFFECTS; PROTOCATECHUIC ACID;

ANTHOCYANINS;

ANIMALIA; MUS; RIBES HUDSONIANUM; RIBES NIGRUM;

ANTHOCYANIN; GLUCOSE; PLANT EXTRACT;

ANIMAL; C57BL MOUSE; CHEMISTRY; DRUG EFFECTS; FRUIT; HUMAN; INTESTINE FLORA; MALE; METABOLISM; MICROBIOLOGY; MOUSE; MOUSE MUTANT; OBESITY; PATHOPHYSIOLOGY; RIBES; WEIGHT GAIN;

ANIMALS; ANTHOCYANINS; FRUIT; GASTROINTESTINAL MICROBIOME; GLUCOSE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; OBESITY; PLANT EXTRACTS; RIBES; WEIGHT GAIN;

EID: 84937064835     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b00963     Document Type: Article

References (39)

1. White, M. F. Insulin signaling in health and disease Science 2003, 302, 1710-1711 10.1126/science.1092952
2. Manco, M.; Putignani, L.; Bottazzo, G. F. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk Endocr. Rev. 2010, 31, 817-844 10.1210/er.2009-0030
3. Tsuda, T. Dietary anthocyanin-rich plants: biochemical basis and recent progress in health benefits studies Mol. Nutr. Food Res. 2012, 56, 159-170 10.1002/mnfr.201100526
4. Tsuda, T.; Horio, F.; Uchida, K.; Aoki, H.; Osawa, T. Dietary cyanidin 3- O -β- d -glucoside-rich purple corn color prevents obesity and ameliorates hyperglycemia in mice J. Nutr. 2003, 133, 2125-2130
5. Kwon, S. H.; Ahn, I. S.; Kim, S. O.; Kong, C. S.; Chung, H. Y.; Do, M. S.; Park, K. Y. Anti-obesity and hypolipidemic effects of black soybean anthocyanins J. Med. Food 2007, 10, 552-556 10.1089/jmf.2006.147
6. Prior, R. L.; Wu, X.; Gu, L.; Hager, T. J.; Hager, A.; Howard, L. R. Whole berries versus berry anthocyanins: interactions with dietary fat levels in the C57BL/6J mouse model of obesity J. Agric. Food Chem. 2008, 56, 647-653 10.1021/jf071993o
7. Qin, B.; Anderson, R. A. An extract of chokeberry attenuates weight gain and modulates insulin, adipogenic and inflammatory signalling pathways in epididymal adipose tissue of rats fed a fructose-rich diet Br. J. Nutr. 2012, 108, 581-587 10.1017/S000711451100599X
8. Hwang, Y. P.; Choi, J. H.; Han, E. H.; Kim, H. G.; Wee, J. H.; Jung, K. O.; Jung, K. H.; Kwon, K. I.; Jeong, T. C.; Chung, Y. C.; Jeong, H. G. Purple sweet potato anthocyanins attenuate hepatic lipid accumulation through activating adenosine monophosphate-activated protein kinase in human HepG2 cells and obese mice Nutr. Res. 2011, 31, 896-906 10.1016/j.nutres.2011.09.026
9. Wu, T.; Qi, X.; Liu, Y.; Guo, J.; Zhu, R.; Chen, W.; Zheng, X.; Yu, T. Dietary supplementation with purified mulberry (Morus australis Poir) anthocyanins suppresses body weight gain in high-fat diet fed C57BL/6 mice Food Chem. 2013, 141, 482-487 10.1016/j.foodchem.2013.03.046
10. Wu, T.; Tang, Q.; Yu, Z.; Gao, Z.; Hu, H.; Chen, W.; Zheng, X.; Yu, T. Inhibitory effects of sweet cherry anthocyanins on the obesity development in C57BL/6 mice Int. J. Food Sci. Nutr. 2014, 65, 351-359 10.3109/09637486.2013.854749
11. Hogan, S.; Canning, C.; Sun, S.; Sun, X.; Zhou, K. Effects of grape pomace antioxidant extract on oxidative stress and inflammation in diet induced obese mice J. Agric. Food Chem. 2010, 58, 11250-11256 10.1021/jf102759e
12. Benn, T.; Kim, B.; Park, Y. K.; Wegner, C. J.; Harness, E.; Nam, T. G.; Kim, D. O.; Lee, J. S.; Lee, J. Y. Polyphenol-rich black currant extract prevents inflammation in diet-induced obese mice J. Nutr. Biochem. 2014, 25, 1019-1025 10.1016/j.jnutbio.2014.05.008
13. Marques, A. Y.; Dragano, N. R.; Lenquiste, S. A.; Batista, A. G.; Palazzo, C. C.; Marostica, M. R., Jr. Freeze-dried jaboticaba peel powder rich in anthocyanins did not reduce weight gain and lipid content in mice and rats Arch. Latinoam. Nutr. 2012, 62, 37-43
14. Prior, R. L.; Wilkes, S.; Rogers, T.; Khanal, R. C.; Wu, X.; Hager, T. J.; Hager, A.; Howard, L. Dietary black raspberry anthocyanins do not alter development of obesity in mice fed an obesogenic high-fat diet J. Agric. Food Chem. 2010, 58, 3977-3983 10.1021/jf9030772
15. van Dam, R. M.; Naidoo, N.; Landberg, R. Dietary flavonoids and the development of type 2 diabetes and cardiovascular diseases: review of recent findings Curr. Opin. Lipidol. 2013, 24, 25-33 10.1097/MOL.0b013e32835bcdff
16. Stull, A. J.; Cash, K. C.; Johnson, W. D.; Champagne, C. M.; Cefalu, W. T. Bioactives in blueberries improve insulin sensitivity in obese, insulin-resistant men and women J. Nutr. 2010, 140, 1764-1768 10.3945/jn.110.125336
17. Karlsen, A.; Retterstol, L.; Laake, P.; Paur, I.; Bohn, S. K.; Sandvik, L.; Blomhoff, R. Anthocyanins inhibit nuclear factor-κB activation in monocytes and reduce plasma concentrations of pro-inflammatory mediators in healthy adults J. Nutr. 2007, 137, 1951-1954
18. Zhu, Y.; Xia, M.; Yang, Y.; Liu, F.; Li, Z.; Hao, Y.; Mi, M.; Jin, T.; Ling, W. Purified anthocyanin supplementation improves endothelial function via NO-cGMP activation in hypercholesterolemic individuals Clin. Chem. 2011, 57, 1524-1533 10.1373/clinchem.2011.167361
19. Hansen, A. S.; Marckmann, P.; Dragsted, L. O.; Finne Nielsen, I. L.; Nielsen, S. E.; Gronbaek, M. Effect of red wine and red grape extract on blood lipids, haemostatic factors, and other risk factors for cardiovascular disease Eur. J. Clin. Nutr. 2005, 59, 449-455 10.1038/sj.ejcn.1602107
20. Curtis, P. J.; Kroon, P. A.; Hollands, W. J.; Walls, R.; Jenkins, G.; Kay, C. D.; Cassidy, A. Cardiovascular disease risk biomarkers and liver and kidney function are not altered in postmenopausal women after ingesting an elderberry extract rich in anthocyanins for 12 weeks J. Nutr. 2009, 139, 2266-2271 10.3945/jn.109.113126
21. Giordano, L.; Coletta, W.; Tamburrelli, C.; D'Imperio, M.; Crescente, M.; Silvestri, C.; Rapisarda, P.; Reforgiato Recupero, G.; De Curtis, A.; Iacoviello, L.; de Gaetano, G.; Rotilio, D.; Cerletti, C.; Donati, M. B. Four-week ingestion of blood orange juice results in measurable anthocyanin urinary levels but does not affect cellular markers related to cardiovascular risk: a randomized cross-over study in healthy volunteers Eur. J. Nutr. 2012, 51, 541-548 10.1007/s00394-011-0237-9
22. Wright, O. R.; Netzel, G. A.; Sakzewski, A. R. A randomized, double-blind, placebo-controlled trial of the effect of dried purple carrot on body mass, lipids, blood pressure, body composition, and inflammatory markers in overweight and obese adults: the QUENCH trial Can. J. Physiol. Pharmacol. 2013, 91, 480-488 10.1139/cjpp-2012-0349
23. Faria, A.; Fernandes, I.; Norberto, S.; Mateus, N.; Calhau, C. Interplay between anthocyanins and gut microbiota J. Agric. Food Chem. 2014, 62, 6898-6902 10.1021/jf501808a
24. Walton, M. C.; Hendriks, W. H.; Broomfield, A. M.; McGhie, T. K. Viscous food matrix influences absorption and excretion but not metabolism of black currant anthocyanins in rats J. Food Sci. 2009, 74, H22-H29 10.1111/j.1750-3841.2008.00996.x
25. Mbeunkui, F.; Grace, M. H.; Yousef, G. G.; Lila, M. A. Isolation and characterization of flavonols from black currant by high-performance counter-current chromatography and electrospray ionization tandem mass spectrometry J. Sep. Sci. 2012, 35, 1682-1689 10.1002/jssc.201200198
26. Keppler, K.; Humpf, H. U. Metabolism of anthocyanins and their phenolic degradation products by the intestinal microflora Bioorg. Med. Chem. 2005, 13, 5195-5205 10.1016/j.bmc.2005.05.003
27. Ellacott, K. L.; Morton, G. J.; Woods, S. C.; Tso, P.; Schwartz, M. W. Assessment of feeding behavior in laboratory mice Cell Metab. 2010, 12, 10-17 10.1016/j.cmet.2010.06.001
28. Wang, Z.; Klipfell, E.; Bennett, B. J.; Koeth, R.; Levison, B. S.; Dugar, B.; Feldstein, A. E.; Britt, E. B.; Fu, X.; Chung, Y. M.; Wu, Y.; Schauer, P.; Smith, J. D.; Allayee, H.; Tang, W. H.; DiDonato, J. A.; Lusis, A. J.; Hazen, S. L. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 2011, 472, 57-63 10.1038/nature09922
29. He, J.; Magnuson, B. A.; Giusti, M. M. Analysis of anthocyanins in rat intestinal contents-impact of anthocyanin chemical structure on fecal excretion J. Agric. Food Chem. 2005, 53, 2859-2966 10.1021/jf0479923
30. Yousef, G. G.; Brown, A. F.; Funakoshi, Y.; Mbeunkui, F.; Grace, M. H.; Ballington, J. R.; Loraine, A.; Lila, M. A. Efficient quantification of the health-relevant anthocyanin and phenolic acid profiles in commercial cultivars and breeding selections of blueberries (Vaccinium spp.) J. Agric. Food Chem. 2013, 61, 4806-4815 10.1021/jf400823s
31. Kuhnau, J. The flavonoids. A class of semi-essential food components: their role in human nutrition World Rev. Nutr. Diet. 1976, 24, 117-191
32. McGhie, T. K.; Ainge, G. D.; Barnett, L. E.; Cooney, J. M.; Jensen, D. J. Anthocyanin glycosides from berry fruit are absorbed and excreted unmetabolized by both humans and rats J. Agric. Food Chem. 2003, 51, 4539-4548 10.1021/jf026206w
33. Hertog, M. G.; Hollman, P. C.; Katan, M. B.; Kromhout, D. Intake of potentially anticarcinogenic flavonoids and their determinants in adults in The Netherlands Nutr. Cancer 1993, 20, 21-29 10.1080/01635589309514267
34. Reagan-Shaw, S.; Nihal, M.; Ahmad, N. Dose translation from animal to human studies revisited FASEB J. 2008, 22, 659-661 10.1096/fj.07-9574LSF
35. Slimestad, R.; Solheim, H. Anthocyanins from black currants (Ribes nigrum L.) J. Agric. Food Chem. 2002, 50, 3228-3231 10.1021/jf011581u
36. Hellstrom, J.; Hietaranta, T.; Karhu, S.; Mattila, P.; Tiirikka, T.; Vetelainen, M. High variability in anthocyanin contents between different blackcurrant varieties NJF Report 2010, 6, 116-118
37. Hosseinian, F. S.; Beta, T. Saskatoon and wild blueberries have higher anthocyanin contents than other Manitoba berries J. Agric. Food Chem. 2007, 55, 10832-10838 10.1021/jf072529m
38. Stuchlikova, E.; Hruskova, J.; Tenorova, M.; Novotna, B.; Komarkova, A.; Riedl, O. Some changes in intermediary metabolism of obese patients Clin. Chim. Acta 1961, 6, 571-577 10.1016/0009-8981(61)90149-8
39. Fleissner, C. K.; Huebel, N.; Abd El-Bary, M. M.; Loh, G.; Klaus, S.; Blaut, M. Absence of intestinal microbiota does not protect mice from diet-induced obesity Br. J. Nutr. 2010, 104, 919-929 10.1017/S0007114510001303