The Anti-inflammatory Effects of Dietary Anthocyanins against Ulcerative Colitis

Shiyu Li, Binning Wu, Wenyi Fu, Lavanya Reddivari, Shiyu Li, Binning Wu, Wenyi Fu, Lavanya Reddivari

Abstract

Ulcerative colitis (UC), which is a major form of inflammatory bowel disease (IBD), is a chronic relapsing disorder of the gastrointestinal tract affecting millions of people worldwide. Alternative natural therapies, including dietary changes, are being investigated to manage or treat UC since current treatment options have serious negative side effects. There is growing evidence from animal studies and human clinical trials that diets rich in anthocyanins, which are pigments in fruits and vegetables, protect against inflammation and increased gut permeability as well as improve colon health through their ability to alter bacterial metabolism and the microbial milieu within the intestines. In this review, the structure and bioactivity of anthocyanins, the role of inflammation and gut bacterial dysbiosis in UC pathogenesis, and their regulation by the dietary anthocyanins are discussed, which suggests the feasibility of dietary strategies for UC mitigation.

Keywords: anthocyanins; anti-inflammatory; colitis; colonic inflammation.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
The basic structure of anthocyanin.
Figure 2
Figure 2
Structures of six major anthocyanidins.
Figure 3
Figure 3
The mechanisms through which anthocyanins act as anti-inflammatory agents. Inflammatory signaling pathways including NF-kB, MAPKs (P38, ERK, JNK), and STATs were activated by ligand binding of the pro-inflammatory cytokines TNF-α, LPS, IL, and IFN, which eventually leads to the translocation of transcription factors to the nucleus, transcriptional activation, and cytokine production. Anthocyanins attenuated the cascade of inflammatory responses by inhibiting the translocation of transcription factors (P50 and P65), the phosphorylation of IRAK1, NIK, IKK, STAT1, STAT3, P38, ERK, and JNK, the secretion of inflammatory cytokines (IL-6, IL-1β, TNF-α, iNOS, COX-2, and IFN-γ), and activation of NF-kB, MAPK, and STAT inflammatory signaling pathways.

References

    1. Wallace T.C., Giusti M.M. Anthocyanins. Adv. Nutr. 2015;6:620–622. doi: 10.3945/an.115.009233.
    1. Andersen O.M., Markham K.R. Flavonoids: Chemistry, biochemistry and applications. CRC Press; Boca Raton, FL, USA: 2005.
    1. McGhie T.K., Walton M.C. The bioavailability and absorption of anthocyanins: Towards a better understanding. Mol. Nutr. Food Res. 2007;51:702–713. doi: 10.1002/mnfr.200700092.
    1. Borges G.D.S.C., Vieira F.G.K., Copetti C., Gonzaga L.V., Zambiazi R.C., Mancini Filho J., Fett R. Chemical characterization, bioactive compounds, and antioxidant capacity of jussara (euterpe edulis) fruit from the atlantic forest in southern brazil. Food Res. Int. 2011;44:2128–2133. doi: 10.1016/j.foodres.2010.12.006.
    1. Sui X., Zhang Y., Zhou W. Bread fortified with anthocyanin-rich extract from black rice as nutraceutical sources: Its quality attributes and in vitro digestibility. Food Chem. 2016;196:910–916. doi: 10.1016/j.foodchem.2015.09.113.
    1. Morais C.A., de Rosso V.V., Estadella D., Pisani L.P. Anthocyanins as inflammatory modulators and the role of the gut microbiota. J. Nutr. Biochem. 2016;33:1–7. doi: 10.1016/j.jnutbio.2015.11.008.
    1. Pojer E., Mattivi F., Johnson D., Stockley C.S. The case for anthocyanin consumption to promote human health: A review. Compr. Rev. Food Sci. Food Saf. 2013;12:483–508. doi: 10.1111/1541-4337.12024.
    1. Welch C.R., Wu Q., Simon J.E. Recent advances in anthocyanin analysis and characterization. Curr. Anal. Chem. 2008;4:75–101. doi: 10.2174/157341108784587795.
    1. Pérez-Gregorio R.M., García-Falcón M.S., Simal-Gándara J., Rodrigues A.S., Almeida D.P. Identification and quantification of flavonoids in traditional cultivars of red and white onions at harvest. J. Food Compos. Anal. 2010;23:592–598. doi: 10.1016/j.jfca.2009.08.013.
    1. Woodward G., Kroon P., Cassidy A., Kay C. Anthocyanin stability and recovery: Implications for the analysis of clinical and experimental samples. J. Agric. Food Chem. 2009;57:5271–5278. doi: 10.1021/jf900602b.
    1. Khoo H.E., Azlan A., Tang S.T., Lim S.M. Anthocyanidins and anthocyanins: Colored pigments as food, pharmaceutical ingredients, and the potential health benefits. Food Nutr. Res. 2017;61:1361779. doi: 10.1080/16546628.2017.1361779.
    1. Brouillard R. Chemical structure of anthocyanins. Volume 1 Academic Press; New York, NY, USA: 1982.
    1. He J., Giusti M.M. Anthocyanins: Natural colorants with health-promoting properties. Annu. Rev. Food Sci. Technol. 2010;1:163–187. doi: 10.1146/annurev.food.080708.100754.
    1. Wrolstad R.E., Durst R.W., Lee J. Tracking color and pigment changes in anthocyanin products. Trends Food Sci. Technol. 2005;16:423–428. doi: 10.1016/j.tifs.2005.03.019.
    1. Samadi A.K., Bilsland A., Georgakilas A.G., Amedei A., Amin A., Bishayee A., Azmi A.S., Lokeshwar B.L., Grue B., Panis C. A Multi-Targeted Approach to Suppress Tumor-Promoting Inflammation. Elsevier; Amsterdam, The Netherlands: 2015. Seminars in cancer biology; pp. S151–S184.
    1. Andersen Ø.M., Jordheim M. Basic anthocyanin chemistry and dietary sources. Anthocyanins Health Dis. 2013;1:13–89.
    1. Smeriglio A., Barreca D., Bellocco E., Trombetta D. Chemistry, pharmacology and health benefits of anthocyanins. Phytother. Res. 2016;30:1265–1286. doi: 10.1002/ptr.5642.
    1. de Pascual-Teresa S., Sanchez-Ballesta M.T. Anthocyanins: From plant to health. Phytochem. Rev. 2008;7:281–299. doi: 10.1007/s11101-007-9074-0.
    1. Fang J. Bioavailability of anthocyanins. Drug Metab. Rev. 2014;46:508–520. doi: 10.3109/03602532.2014.978080.
    1. Kong J.-M., Chia L.-S., Goh N.-K., Chia T.-F., Brouillard R. Analysis and biological activities of anthocyanins. Phytochemistry. 2003;64:923–933. doi: 10.1016/S0031-9422(03)00438-2.
    1. Nayak C.A., Srinivas P., Rastogi N.K. Characterisation of anthocyanins from garcinia indica choisy. Food Chem. 2010;118:719–724. doi: 10.1016/j.foodchem.2009.05.052.
    1. da Silva F.L., Escribano-Bailón M.T., Alonso J.J.P., Rivas-Gonzalo J.C., Santos-Buelga C. Anthocyanin pigments in strawberry. Lwt-Food Sci. Technol. 2007;40:374–382. doi: 10.1016/j.lwt.2005.09.018.
    1. Böhm H.G. Mazza und E. Miniati: Anthocyanins in Fruits, Vegetables and Grains. 362 Seiten, zahlr. Abb. und Tab. CRC Press: Boca Raton, Ann Arbor, London, Tokyo 1993. Preis: 144—£. Food Nahrung. 1994;38:343. doi: 10.1002/food.19940380317.
    1. Zamora-Ros R., Knaze V., Luján-Barroso L., Slimani N., Romieu I., Touillaud M., Kaaks R., Teucher B., Mattiello A., Grioni S. Estimation of the intake of anthocyanidins and their food sources in the european prospective investigation into cancer and nutrition (epic) study. Br. J. Nutr. 2011;106:1090–1099. doi: 10.1017/S0007114511001437.
    1. Sebastian R.S., Wilkinson Enns C., Goldman J.D., Martin C.L., Steinfeldt L.C., Murayi T., Moshfegh A.J. A new database facilitates characterization of flavonoid intake, sources, and positive associations with diet quality among us adults. J. Nutr. 2015;145:1239–1248. doi: 10.3945/jn.115.213025.
    1. Yousuf B., Gul K., Wani A.A., Singh P. Health benefits of anthocyanins and their encapsulation for potential use in food systems: A review. Crit. Rev. Food Sci. Nutr. 2016;56:2223–2230. doi: 10.1080/10408398.2013.805316.
    1. Yi W., Akoh C.C., Fischer J., Krewer G. Absorption of anthocyanins from blueberry extracts by caco-2 human intestinal cell monolayers. J. Agric. Food Chem. 2006;54:5651–5658. doi: 10.1021/jf0531959.
    1. Tsuda T., Shiga K., Ohshima K., Kawakishi S., Osawa T. Inhibition of lipid peroxidation and the active oxygen radical scavenging effect of anthocyanin pigments isolated from phaseolus vulgaris l. Biochem. Pharmacol. 1996;52:1033–1039. doi: 10.1016/0006-2952(96)00421-2.
    1. Zhang Y., Vareed S.K., Nair M.G. Human tumor cell growth inhibition by nontoxic anthocyanidins, the pigments in fruits and vegetables. Life Sci. 2005;76:1465–1472. doi: 10.1016/j.lfs.2004.08.025.
    1. Milbury P.E., Cao G., Prior R.L., Blumberg J. Bioavailablility of elderberry anthocyanins. Mech. Ageing Dev. 2002;123:997–1006. doi: 10.1016/S0047-6374(01)00383-9.
    1. Talavera S., Felgines C., Texier O., Besson C., Lamaison J.-L., Rémésy C. Anthocyanins are efficiently absorbed from the stomach in anesthetized rats. J. Nutr. 2003;133:4178–4182. doi: 10.1093/jn/133.12.4178.
    1. Matuschek M.C., Hendriks W.H., McGhie T.K., Reynolds G.W. The jejunum is the main site of absorption for anthocyanins in mice. J. Nutr. Biochem. 2006;17:31–36. doi: 10.1016/j.jnutbio.2005.04.005.
    1. Czank C., Cassidy A., Zhang Q., Morrison D.J., Preston T., Kroon P.A., Botting N.P., Kay C.D. Human metabolism and elimination of the anthocyanin, cyanidin-3-glucoside: A 13c-tracer study. Am. Clin. Nutr. 2013;97:995–1003. doi: 10.3945/ajcn.112.049247.
    1. Felgines C., Krisa S., Mauray A., Besson C., Lamaison J.-L., Scalbert A., Mérillon J.-M., Texier O. Radiolabelled cyanidin 3-o-glucoside is poorly absorbed in the mouse. Br. J. Nutr. 2010;103:1738–1745. doi: 10.1017/S0007114510000061.
    1. Bub A., Watzl B., Heeb D., Rechkemmer G., Briviba K. Malvidin-3-glucoside bioavailability in humans after ingestion of red wine, dealcoholized red wine and red grape juice. Eur. J. Nutr. 2001;40:113–120. doi: 10.1007/s003940170011.
    1. 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. doi: 10.1021/jf001246q.
    1. Manach C., Williamson G., Morand C., Scalbert A., Rémésy C. Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am. J. Clin. Nutr. 2005;81:230S–242S. doi: 10.1093/ajcn/81.1.230S.
    1. Aura A.-M., Martin-Lopez P., O’Leary K.A., Williamson G., Oksman-Caldentey K.-M., Poutanen K., Santos-Buelga C. In vitro metabolism of anthocyanins by human gut microflora. Eur. J. Nutr. 2005;44:133–142. doi: 10.1007/s00394-004-0502-2.
    1. Keppler K., Humpf H.-U. Metabolism of anthocyanins and their phenolic degradation products by the intestinal microflora. Bioorganic Med. Chem. 2005;13:5195–5205. doi: 10.1016/j.bmc.2005.05.003.
    1. Vamanu E., Gatea F., Sârbu I., Pelinescu D. An in vitro study of the influence of curcuma longa extracts on the microbiota modulation process, in patients with hypertension. Pharmaceutics. 2019;11:191. doi: 10.3390/pharmaceutics11040191.
    1. Fleschhut J., Kratzer F., Rechkemmer G., Kulling S.E. Stability and biotransformation of various dietary anthocyanins in vitro. Eur. J. Nutr. 2006;45:7–18. doi: 10.1007/s00394-005-0557-8.
    1. Forester S.C., Waterhouse A.L. Identification of cabernet sauvignon anthocyanin gut microflora metabolites. J. Agric. Food Chem. 2008;56:9299–9304. doi: 10.1021/jf801309n.
    1. Salyer J., Park S., Ricke S., Lee S. Analysis of microbial populations and metabolism of anthocyanins by mice gut microflora fed with blackberry powder. J. Nutr. Food Sci. 2013;3:1–5. doi: 10.4172/2155-9600.1000178.
    1. Hidalgo M., Oruna-Concha M.J., Kolida S., Walton G.E., Kallithraka S., Spencer J.P., de Pascual-Teresa S. Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth. J. Agric. Food Chem. 2012;60:3882–3890. doi: 10.1021/jf3002153.
    1. Chen Y., Li Q., Zhao T., Zhang Z., Mao G., Feng W., Wu X., Yang L. Biotransformation and metabolism of three mulberry anthocyanin monomers by rat gut microflora. Food Chem. 2017;237:887–894. doi: 10.1016/j.foodchem.2017.06.054.
    1. Zielińska M., Lewandowska U., Podsędek A., Cygankiewicz A.I., Jacenik D., Sałaga M., Kordek R., Krajewska W.M., Fichna J. Orally available extract from brassica oleracea var. Capitata rubra attenuates experimental colitis in mouse models of inflammatory bowel diseases. J. Funct. Foods. 2015;17:587–599. doi: 10.1016/j.jff.2015.05.046.
    1. Sugata M., Lin C.-Y., Shih Y.-C. Anti-inflammatory and anticancer activities of taiwanese purple-fleshed sweet potatoes (ipomoea batatas l. Lam) extracts. Biomed. Res. Int. 2015;2015:768093. doi: 10.1155/2015/768093.
    1. Medda R., Lyros O., Schmidt J.L., Jovanovic N., Nie L., Link B.J., Otterson M.F., Stoner G.D., Shaker R., Rafiee P. Anti inflammatory and anti angiogenic effect of black raspberry extract on human esophageal and intestinal microvascular endothelial cells. Microvasc. Res. 2015;97:167–180. doi: 10.1016/j.mvr.2014.10.008.
    1. Youdim K.A., Shukitt-Hale B., Joseph J.A. Flavonoids and the brain: Interactions at the blood–brain barrier and their physiological effects on the central nervous system. Free Radic. Biol. Med. 2004;37:1683–1693. doi: 10.1016/j.freeradbiomed.2004.08.002.
    1. Cassidy A., Mukamal K.J., Liu L., Franz M., Eliassen A.H., Rimm E.B. High anthocyanin intake is associated with a reduced risk of myocardial infarction in young and middle-aged women. Circulation. 2013;127:188–196. doi: 10.1161/CIRCULATIONAHA.112.122408.
    1. 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. doi: 10.1093/ajcn/85.3.895.
    1. Vendrame S., Del Bo C., Ciappellano S., Riso P., Klimis-Zacas D. Berry fruit consumption and metabolic syndrome. Antioxidants. 2016;5:34. doi: 10.3390/antiox5040034.
    1. Overall J., Bonney S., Wilson M., Beermann A., Grace M., Esposito D., Lila M., Komarnytsky S. Metabolic effects of berries with structurally diverse anthocyanins. Int. J. Mol. Sci. 2017;18:422. doi: 10.3390/ijms18020422.
    1. J Thoppil R., Bhatia D., F Barnes K., Haznagy-Radnai E., Hohmann J., S Darvesh A., Bishayee A. Black currant anthocyanins abrogate oxidative stress through nrf2-mediated antioxidant mechanisms in a rat model of hepatocellular carcinoma. Curr. Cancer Drug Targets. 2012;12:1244–1257.
    1. Wu X., Prior R.L. Systematic identification and characterization of anthocyanins by hplc-esi-ms/ms in common foods in the united states: Fruits and berries. J. Agric. Food Chem. 2005;53:2589–2599. doi: 10.1021/jf048068b.
    1. Khoo C., Falk M. Polyphenols in human health and disease. Elsevier; Amsterdam, The Netherlands: 2014. Cranberry polyphenols: Effects on cardiovascular risk factors; pp. 1049–1065.
    1. Rothenberg D.O., Yang H., Chen M., Zhang W., Zhang L. Metabolome and transcriptome sequencing analysis reveals anthocyanin metabolism in pink flowers of anthocyanin-rich tea (camellia sinensis) Molecules. 2019;24:1064. doi: 10.3390/molecules24061064.
    1. Tsutsumi A., Horikoshi Y., Fushimi T., Saito A., Koizumi R., Fujii Y., Hu Q.Q., Hirota Y., Aizawa K., Osakabe N. Acylated anthocyanins derived from purple carrot (daucus carota l.) induce elevation of blood flow in rat cremaster arteriole. Food Funct. 2019;10:1726–1735. doi: 10.1039/C8FO02125B.
    1. Wongwichai T., Teeyakasem P., Pruksakorn D., Kongtawelert P., Pothacharoen P. Anthocyanins and metabolites from purple rice inhibit il-1beta-induced matrix metalloproteinases expression in human articular chondrocytes through the nf-kappab and erk/mapk pathway. Biomed. Pharmacother. 2019;112:108610. doi: 10.1016/j.biopha.2019.108610.
    1. Jayaprakasam B., Vareed S.K., Olson L.K., Nair M.G. Insulin secretion by bioactive anthocyanins and anthocyanidins present in fruits. J. Agric. Food Chem. 2005;53:28–31. doi: 10.1021/jf049018+.
    1. Amini A.M., Muzs K., Spencer J.P., Yaqoob P. Pelargonidin-3-o-glucoside and its metabolites have modest anti-inflammatory effects in human whole blood cultures. Nutr. Res. 2017;46:88–95. doi: 10.1016/j.nutres.2017.09.006.
    1. Tsuda T. Dietary anthocyanin-rich plants: Biochemical basis and recent progress in health benefits studies. Mol. Nutr. Food Res. 2012;56:159–170. doi: 10.1002/mnfr.201100526.
    1. Rodriguez-Mateos A., Heiss C., Borges G., Crozier A. Berry (poly) phenols and cardiovascular health. J. Agric. Food Chem. 2013;62:3842–3851. doi: 10.1021/jf403757g.
    1. Stushnoff C., Holm D., Thompson M.D., Jiang W., Thompson H.J., Joyce N.I., Wilson P. Antioxidant properties of cultivars and selections from the colorado potato breeding program. Am. J. Potato Res. 2008;85:267. doi: 10.1007/s12230-008-9032-4.
    1. Nankar A.N., Dungan B., Paz N., Sudasinghe N., Schaub T., Holguin F.O., Pratt R.C. Quantitative and qualitative evaluation of kernel anthocyanins from southwestern united states blue corn. J. Sci Food Agric. 2016;96:4542–4552. doi: 10.1002/jsfa.7671.
    1. Bognar E., Sarszegi Z., Szabo A., Debreceni B., Kalman N., Tucsek Z., Sumegi B., Gallyas F., Jr. Antioxidant and anti-inflammatory effects in raw264. 7 macrophages of malvidin, a major red wine polyphenol. PLoS ONE. 2013;8:e65355. doi: 10.1371/journal.pone.0065355.
    1. Moriwaki S., Suzuki K., Muramatsu M., Nomura A., Inoue F., Into T., Yoshiko Y., Niida S. Delphinidin, one of the major anthocyanidins, prevents bone loss through the inhibition of excessive osteoclastogenesis in osteoporosis model mice. PLoS ONE. 2014;9:e97177. doi: 10.1371/journal.pone.0097177.
    1. Hafeez B.B., Siddiqui I.A., Asim M., Malik A., Afaq F., Adhami V.M., Saleem M., Din M., Mukhtar H. 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. doi: 10.1158/0008-5472.CAN-08-2232.
    1. Spilmont M., Léotoing L., Davicco M.J., Lebecque P., Miot-Noirault E., Pilet P., Rios L., Wittrant Y., Coxam V. Pomegranate peel extract prevents bone loss in a preclinical model of osteoporosis and stimulates osteoblastic differentiation in vitro. Nutrients. 2015;7:9265–9284. doi: 10.3390/nu7115465.
    1. Lao F., Sigurdson G.T., Giusti M.M. Health benefits of purple corn (zea mays l.) phenolic compounds. Compr. Rev. Food Sci. Food Saf. 2017;16:234–246. doi: 10.1111/1541-4337.12249.
    1. Muche B.M., Speers R.A., Rupasinghe H.P.V. Storage temperature impacts on anthocyanins degradation, color changes and haze development in juice of "merlot" and "ruby" grapes (vitis vinifera) Front. Nutr. 2018;5:100. doi: 10.3389/fnut.2018.00100.
    1. Tang P., Giusti M.M. Black goji as a potential source of natural color in a wide ph range. Food Chem. 2018;269:419–426. doi: 10.1016/j.foodchem.2018.07.034.
    1. Rocha-Parra D., Chirife J., Zamora C., de Pascual-Teresa S. Chemical characterization of an encapsulated red wine powder and its effects on neuronal cells. Molecules. 2018;23:842. doi: 10.3390/molecules23040842.
    1. Kalita D., Holm D.G., LaBarbera D.V., Petrash J.M., Jayanty S.S. Inhibition of alpha-glucosidase, alpha-amylase, and aldose reductase by potato polyphenolic compounds. PLoS ONE. 2018;13:e0191025. doi: 10.1371/journal.pone.0191025.
    1. Lopez-Cobo A., Verardo V., Diaz-de-Cerio E., Segura-Carretero A., Fernandez-Gutierrez A., Gomez-Caravaca A.M. Use of hplc- and gc-qtof to determine hydrophilic and lipophilic phenols in mango fruit (mangifera indica l.) and its by-products. Food Res. Int. 2017;100:423–434. doi: 10.1016/j.foodres.2017.02.008.
    1. Fu X., Cheng S., Liao Y., Huang B., Du B., Zeng W., Jiang Y., Duan X., Yang Z. Comparative analysis of pigments in red and yellow banana fruit. Food Chem. 2018;239:1009–1018. doi: 10.1016/j.foodchem.2017.07.046.
    1. Aguilera Y., Mojica L., Rebollo-Hernanz M., Berhow M., de Mejia E.G., Martin-Cabrejas M.A. Black bean coats: New source of anthocyanins stabilized by beta-cyclodextrin copigmentation in a sport beverage. Food Chem. 2016;212:561–570. doi: 10.1016/j.foodchem.2016.06.022.
    1. Adams S.M., Bornemann P.H. Ulcerative colitis. Am. Fam. Physician. 2013;87:699–705.
    1. Burisch J., Pedersen N., Čuković-Čavka S., Brinar M., Kaimakliotis I., Duricova D., Shonová O., Vind I., Avnstrøm S., Thorsgaard N. East–west gradient in the incidence of inflammatory bowel disease in europe: The ecco-epicom inception cohort. Gut. 2014;63:588–597. doi: 10.1136/gutjnl-2013-304636.
    1. Cosnes J., Gower–Rousseau C., Seksik P., Cortot A. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology. 2011;140:1785–1794. e4. doi: 10.1053/j.gastro.2011.01.055.
    1. Jess T., Simonsen J., Nielsen N.M., Jørgensen K.T., Bager P., Ethelberg S., Frisch M. Enteric salmonella or campylobacter infections and the risk of inflammatory bowel disease. Gut. 2011;60:318–324. doi: 10.1136/gut.2010.223396.
    1. Sahami S., Kooij I., Meijer S., Van den Brink G., Buskens C., Te Velde A. The link between the appendix and ulcerative colitis: Clinical relevance and potential immunological mechanisms. Am. J. Gastroenterol. 2016;111:163. doi: 10.1038/ajg.2015.301.
    1. Hou J.K., Abraham B., El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: A systematic review of the literature. Am. J. Gastroenterol. 2011;106:563. doi: 10.1038/ajg.2011.44.
    1. Ananthakrishnan A.N., Higuchi L.M., Huang E.S., Khalili H., Richter J.M., Fuchs C.S., Chan A.T. Aspirin, nonsteroidal anti-inflammatory drug use, and risk for crohn disease and ulcerative colitis: A cohort study. Ann. Intern. Med. 2012;156:350–359. doi: 10.7326/0003-4819-156-5-201203060-00007.
    1. Khalili H., Higuchi L.M., Ananthakrishnan A.N., Manson J.E., Feskanich D., Richter J.M., Fuchs C.S., Chan A.T. Hormone therapy increases risk of ulcerative colitis but not crohn’s disease. Gastroenterology. 2012;143:1199–1206. doi: 10.1053/j.gastro.2012.07.096.
    1. Ungaro R., Bernstein C.N., Gearry R., Hviid A., Kolho K.-L., Kronman M.P., Shaw S., Van Kruiningen H., Colombel J.-F., Atreja A. Antibiotics associated with increased risk of new-onset crohn’s disease but not ulcerative colitis: A meta-analysis. Am. J. Gastroenterol. 2014;109:1728. doi: 10.1038/ajg.2014.246.
    1. Chen L., Zhou Z., Yang Y., Chen N., Xiang H. Therapeutic effect of imiquimod on dextran sulfate sodium-induced ulcerative colitis in mice. PLoS ONE. 2017;12:e0186138. doi: 10.1371/journal.pone.0186138.
    1. Reddivari L., Wang T., Wu B., Li S. Potato: An Anti-Inflammatory Food. Am. J. Potato Res. 2019;96:164–169. doi: 10.1007/s12230-018-09699-z.
    1. Johansson M.E., Gustafsson J.K., Sjöberg K.E., Petersson J., Holm L., Sjövall H., Hansson G.C. Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. PLoS ONE. 2010;5:e12238. doi: 10.1371/journal.pone.0012238.
    1. Zhao L., Zhang Y., Liu G., Hao S., Wang C., Wang Y. Black rice anthocyanin-rich extract and rosmarinic acid, alone and in combination, protect against dss-induced colitis in mice. Food Funct. 2018;9:2796–2808. doi: 10.1039/C7FO01490B.
    1. Minaiyan M., Ghannadi A., Mahzouni P., Jaffari-Shirazi E. Comparative study of berberis vulgaris fruit extract and berberine chloride effects on acetic acid-induced colitis in rats. Iran. J. Pharm. Res. Ijpr. 2011;10:97.
    1. Atreya R., Mudter J., Finotto S., Müllberg J., Jostock T., Wirtz S., Schütz M., Bartsch B., Holtmann M., Becker C. Blockade of interleukin 6 trans signaling suppresses t-cell resistance against apoptosis in chronic intestinal inflammation: Evidence in crohn disease and experimental colitis in vivo. Nat. Med. 2000;6:583. doi: 10.1038/75068.
    1. Neurath M.F. Cytokines in inflammatory bowel disease. Nat. Rev. Immunol. 2014;14:329. doi: 10.1038/nri3661.
    1. Su L., Nalle S.C., Shen L., Turner E.S., Singh G., Breskin L.A., Khramtsova E.A., Khramtsova G., Tsai P.Y., Fu Y.X. Tnfr2 activates mlck-dependent tight junction dysregulation to cause apoptosis-mediated barrier loss and experimental colitis. Gastroenterology. 2013;145:407–415. doi: 10.1053/j.gastro.2013.04.011.
    1. Hernández-Chirlaque C., Aranda C.J., Ocón B., Capitán-Cañadas F., Ortega-González M., Carrero J.J., Suárez M.D., Zarzuelo A., Sánchez de Medina F., Martínez-Augustin O. Germ-free and antibiotic-treated mice are highly susceptible to epithelial injury in dss colitis. J. Crohn’s Colitis. 2016;10:1324–1335. doi: 10.1093/ecco-jcc/jjw096.
    1. Bernardo D., Vallejo-Díez S., Mann E.R., Al-Hassi H.O., Martínez-Abad B., Montalvillo E., Tee C.T., Murugananthan A.U., Núñez H., Peake S.T. Il-6 promotes immune responses in human ulcerative colitis and induces a skin-homing phenotype in the dendritic cells and t cells they stimulate. Eur. J. Immunol. 2012;42:1337–1353. doi: 10.1002/eji.201142327.
    1. Ono Y., Kanai T., Sujino T., Nemoto Y., Kanai Y., Mikami Y., Hayashi A., Matsumoto A., Takaishi H., Ogata H. T-helper 17 and interleukin-17–producing lymphoid tissue inducer-like cells make different contributions to colitis in mice. Gastroenterology. 2012;143:1288–1297. doi: 10.1053/j.gastro.2012.07.108.
    1. Wu Y.-D., Zhou B. Tnf-α/nf-κb/snail pathway in cancer cell migration and invasion. Br. J. Cancer. 2010;102:639. doi: 10.1038/sj.bjc.6605530.
    1. Hunter C.A., Jones S.A. Il-6 as a keystone cytokine in health and disease. Nat. Immunol. 2015;16:448. doi: 10.1038/ni.3153.
    1. Stumhofer J.S., Silver J.S., Laurence A., Porrett P.M., Harris T.H., Turka L.A., Ernst M., Saris C.J., O’Shea J.J., Hunter C.A. Interleukins 27 and 6 induce stat3-mediated t cell production of interleukin 10. Nat. Immunol. 2007;8:1363. doi: 10.1038/ni1537.
    1. Heller F., Florian P., Bojarski C., Richter J., Christ M., Hillenbrand B., Mankertz J., Gitter A.H., Bürgel N., Fromm M. Interleukin-13 is the key effector th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology. 2005;129:550–564. doi: 10.1016/j.gastro.2005.05.002.
    1. Pickert G., Neufert C., Leppkes M., Zheng Y., Wittkopf N., Warntjen M., Lehr H.-A., Hirth S., Weigmann B., Wirtz S. Stat3 links il-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 2009;206:1465–1472. doi: 10.1084/jem.20082683.
    1. Ordas I., Eckmann L., Talamini M., Baumgart D.C., Sandborn W.J. Ulcerative colitis. Lancet. 2012;380:1606–1619. doi: 10.1016/S0140-6736(12)60150-0.
    1. Liu T., Zhang L., Joo D., Sun S.C. Nf-kappab signaling in inflammation. Signal. Transduct Target. 2017:2.
    1. Quigley E.M. Gut bacteria in health and disease. Gastroenterol. Hepatol. 2013;9:560.
    1. Mazmanian S.K., Round J.L., Kasper D.L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453:620. doi: 10.1038/nature07008.
    1. Lindemann R.K., Gabrielli B., Johnstone R.W. Histone-deacetylase inhibitors for the treatment of cancer. Cell Cycle. 2004;3:777–786. doi: 10.4161/cc.3.6.927.
    1. Smith P.M., Howitt M.R., Panikov N., Michaud M., Gallini C.A., Bohlooly-y M., Glickman J.N., Garrett W.S. The microbial metabolites, short-chain fatty acids, regulate colonic treg cell homeostasis. Science. 2013;341:569–573. doi: 10.1126/science.1241165.
    1. Matsuoka K., Uemura Y., Kanai T., Kunisaki R., Suzuki Y., Yokoyama K., Yoshimura N., Hibi T. Efficacy of bifidobacterium breve fermented milk in maintaining remission of ulcerative colitis. Dig. Dis. Sci. 2018;63:1910–1919. doi: 10.1007/s10620-018-4946-2.
    1. Tamaki H., Nakase H., Inoue S., Kawanami C., Itani T., Ohana M., Kusaka T., Uose S., Hisatsune H., Tojo M. Efficacy of probiotic treatment with bifidobacterium longum 536 for induction of remission in active ulcerative colitis: A randomized, double-blinded, placebo-controlled multicenter trial. Dig. Endosc. 2016;28:67–74. doi: 10.1111/den.12553.
    1. Zocco M., Dal Verme L.Z., Cremonini F., Piscaglia A., Nista E., Candelli M., Novi M., Rigante D., Cazzato I., Ojetti V. Efficacy of lactobacillus gg in maintaining remission of ulcerative colitis. Aliment. Pharmacol. Ther. 2006;23:1567–1574. doi: 10.1111/j.1365-2036.2006.02927.x.
    1. Shen Z.-H., Zhu C.-X., Quan Y.-S., Yang Z.-Y., Wu S., Luo W.-W., Tan B., Wang X.-Y. Relationship between intestinal microbiota and ulcerative colitis: Mechanisms and clinical application of probiotics and fecal microbiota transplantation. World J. Gastroenterol. 2018;24:5. doi: 10.3748/wjg.v24.i1.5.
    1. Ott S., Musfeldt M., Wenderoth D., Hampe J., Brant O., Fölsch U., Timmis K., Schreiber S. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53:685–693. doi: 10.1136/gut.2003.025403.
    1. Morgan X.C., Tickle T.L., Sokol H., Gevers D., Devaney K.L., Ward D.V., Reyes J.A., Shah S.A., LeLeiko N., Snapper S.B. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13:R79. doi: 10.1186/gb-2012-13-9-r79.
    1. Sokol H., Lepage P., Seksik P., Dore J., Marteau P. Temperature gradient gel electrophoresis of fecal 16s rrna reveals active escherichia coli in the microbiota of patients with ulcerative colitis. J. Clin. Microbiol. 2006;44:3172–3177. doi: 10.1128/JCM.02600-05.
    1. Obiso R., Azghani A.O., Wilkins T.D. The bacteroides fragilis toxin fragilysin disrupts the paracellular barrier of epithelial cells. Infect. Immun. 1997;65:1431–1439.
    1. Wells C.L., Van de Westerlo E., Jechorek R.P., Feltis B., Wilkins T., Erlandsen S. Bacteroides fragilis enterotoxin modulates epithelial permeability and bacterial internalization by ht-29 enterocytes. Gastroenterology. 1996;110:1429–1437. doi: 10.1053/gast.1996.v110.pm8613048.
    1. Akiyama S., Nesumi A., Maeda-Yamamoto M., Uehara M., Murakami A. Effects of anthocyanin-rich tea “sunrouge” on dextran sodium sulfate-induced colitis in mice. BioFactors. 2012;38:226–233. doi: 10.1002/biof.1008.
    1. Biedermann L., Mwinyi J., Scharl M., Frei P., Zeitz J., Kullak-Ublick G.A., Vavricka S.R., Fried M., Weber A., Humpf H.-U. Bilberry ingestion improves disease activity in mild to moderate ulcerative colitis—an open pilot study. J. Crohn’s Colitis. 2013;7:271–279. doi: 10.1016/j.crohns.2012.07.010.
    1. Kim J.-M., Kim J.-S., Yoo H., Choung M.-G., Sung M.-K. Effects of black soybean [glycine max (l.) merr.] seed coats and its anthocyanidins on colonic inflammation and cell proliferation in vitro and in vivo. J. Agric. Food Chem. 2008;56:8427–8433. doi: 10.1021/jf801342p.
    1. Monk J.M., Wu W., Hutchinson A.L., Pauls P., Robinson L.E., Power K.A. Navy and black bean supplementation attenuates colitis-associated inflammation and colonic epithelial damage. J. Nutr. Biochem. 2018;56:215–223. doi: 10.1016/j.jnutbio.2018.02.013.
    1. Bibi S., Kang Y., Du M., Zhu M.-J. Dietary red raspberries attenuate dextran sulfate sodium-induced acute colitis. J. Nutr. Biochem. 2018;51:40–46. doi: 10.1016/j.jnutbio.2017.08.017.
    1. Turksen K., Troy T.-C. Barriers built on claudins. J. Cell Sci. 2004;117:2435–2447. doi: 10.1242/jcs.01235.
    1. Morita K., Furuse M., Fujimoto K., Tsukita S. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc. Natl. Acad. Sci. USA. 1999;96:511–516. doi: 10.1073/pnas.96.2.511.
    1. Al-Asmakh M., Hedin L. Microbiota and the control of blood-tissue barriers. Tissue Barriers. 2015;3:e1039691. doi: 10.1080/21688370.2015.1039691.
    1. Feldman G.J., Mullin J.M., Ryan M.P. Occludin: Structure, function and regulation. Adv. Drug Deliv. Rev. 2005;57:883–917. doi: 10.1016/j.addr.2005.01.009.
    1. Umeda K., Matsui T., Nakayama M., Furuse K., Sasaki H., Furuse M., Tsukita S. Establishment and characterization of cultured epithelial cells lacking expression of zo-1. J. Biol. Chem. 2004;279:44785–44794. doi: 10.1074/jbc.M406563200.
    1. Groschwitz K.R., Hogan S.P. Intestinal barrier function: Molecular regulation and disease pathogenesis. J. Allergy Clin. Immunol. 2009;124:3–20. doi: 10.1016/j.jaci.2009.05.038.
    1. Sun X., Du M., Navarre D.A., Zhu M.J. Purple potato extract promotes intestinal epithelial differentiation and barrier function by activating amp-activated protein kinase. Mol. Nutr. Food Res. 2018;62:1700536. doi: 10.1002/mnfr.201700536.
    1. Zhang C., Monk J.M., Lu J.T., Zarepoor L., Wu W., Liu R., Pauls K.P., Wood G.A., Robinson L., Tsao R. Cooked navy and black bean diets improve biomarkers of colon health and reduce inflammation during colitis. Br. J. Nutr. 2014;111:1549–1563. doi: 10.1017/S0007114513004352.
    1. Shan Q., Zheng Y., Lu J., Zhang Z., Wu D., Fan S., Hu B., Cai X., Cai H., Liu P. Purple sweet potato color ameliorates kidney damage via inhibiting oxidative stress mediated nlrp3 inflammasome activation in high fat diet mice. Food Chem. Toxicol. 2014;69:339–346. doi: 10.1016/j.fct.2014.04.033.
    1. Triebel S., Trieu H.-L., Richling E. Modulation of inflammatory gene expression by a bilberry (vaccinium myrtillus l.) extract and single anthocyanins considering their limited stability under cell culture conditions. J. Agric. Food Chem. 2012;60:8902–8910. doi: 10.1021/jf3028842.
    1. Fischer J.G., Keirsey K.I., Kirkland R., Lee S., Grunewald Z.I., de La Serre C.B. Blueberry supplementation influences the gut microbiota, inflammation, and insulin resistance in high-fat-diet–fed rats. J. Nutr. 2018;148:209–219.
    1. Wu L.H., Xu Z.L., Dong D., He S.A., Yu H. Protective effect of anthocyanins extract from blueberry on tnbs-induced ibd model of mice. Evid.-Based Complementary Altern. Med. Ecam. 2011;2011:525462. doi: 10.1093/ecam/neq040.
    1. Chen T., Hu S., Zhang H., Guan Q., Yang Y., Wang X. Anti-inflammatory effects of dioscorea alata l. Anthocyanins in a tnbs-induced colitis model. Food Funct. 2017;8:659–669. doi: 10.1039/C6FO01273F.
    1. Boussenna A., Cholet J., Goncalves-Mendes N., Joubert-Zakeyh J., Fraisse D., Vasson M.P., Texier O., Felgines C. Polyphenol-rich grape pomace extracts protect against dextran sulfate sodium-induced colitis in rats. J. Sci. Food Agric. 2016;96:1260–1268. doi: 10.1002/jsfa.7214.
    1. Choe M.-R., Ji Hye K., Yoo H., Yang C.-H., Kim M.-O., Yu R.-N., Choe S.-Y. Cyanidin and cyanidin-3-o-β-d-glucoside suppress the inflammatory responses of obese adipose tissue by inhibiting the release of chemokines mcp-1 and mrp-2. J. Food Sci. Nutr. 2007;12:148–153.
    1. Lee H.H., Lee S.G., Shin J.S., Lee H.Y., Yoon K., Ji Y.W., Jang D.S., Lee K.T. P-coumaroyl anthocyanin mixture isolated from tuber epidermis of solanum tuberosum attenuates reactive oxygen species and pro-inflammatory mediators by suppressing nf-kappab and stat1/3 signaling in lps-induced raw264.7 macrophages. Biol. Pharm. Bull. 2017;40:1894–1902. doi: 10.1248/bpb.b17-00362.
    1. Le Phuong Nguyen T., Fenyvesi F., Remenyik J., Homoki J.R., Gogolak P., Bacskay I., Feher P., Ujhelyi Z., Vasvari G., Vecsernyes M., et al. Protective effect of pure sour cherry anthocyanin extract on cytokine-induced inflammatory caco-2 monolayers. Nutrients. 2018;10:861. doi: 10.3390/nu10070861.
    1. Jung S.K., Lim T.-G., Seo S.G., Lee H.J., Hwang Y.-S., Choung M.-G., Lee K.W. Cyanidin-3-o-(2″-xylosyl)-glucoside, an anthocyanin from siberian ginseng (acanthopanax senticosus) fruits, inhibits uvb-induced cox-2 expression and ap-1 transactivation. Food Sci. Biotechnol. 2013;22:507–513. doi: 10.1007/s10068-013-0108-7.
    1. Li L., Wang L., Wu Z., Yao L., Wu Y., Huang L., Liu K., Zhou X., Gou D. Anthocyanin-rich fractions from red raspberries attenuate inflammation in both raw264.7 macrophages and a mouse model of colitis. Sci. Rep. 2014;4:6234. doi: 10.1038/srep06234.
    1. Pereira S.R., Pereira R., Figueiredo I., Freitas V., Dinis T.C., Almeida L.M. Comparison of anti-inflammatory activities of an anthocyanin-rich fraction from portuguese blueberries (vaccinium corymbosum l.) and 5-aminosalicylic acid in a tnbs-induced colitis rat model. PLoS ONE. 2017;12:e0174116. doi: 10.1371/journal.pone.0174116.
    1. Roth S., Spalinger M.R., Gottier C., Biedermann L., Zeitz J., Lang S., Weber A., Rogler G., Scharl M. Bilberry-derived anthocyanins modulate cytokine expression in the intestine of patients with ulcerative colitis. PLoS ONE. 2016;11:e0154817. doi: 10.1371/journal.pone.0154817.
    1. Faria A., Fernandes I., Norberto S., Mateus N., Calhau C.A.O. Interplay between anthocyanins and gut microbiota. J. Agric. Food Chem. 2014;62:6898–6902. doi: 10.1021/jf501808a.
    1. Ley R.E., Peterson D.A., Gordon J.I. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124:837–848. doi: 10.1016/j.cell.2006.02.017.
    1. Pan P., Lam V., Salzman N., Huang Y.-W., Yu J., Zhang J., Wang L.-S. Black raspberries and their anthocyanin and fiber fractions alter the composition and diversity of gut microbiota in f-344 rats. Nutr. Cancer. 2017;69:943–951. doi: 10.1080/01635581.2017.1340491.
    1. Cassidy A., Minihane A.M. The role of metabolism (and the microbiome) in defining the clinical efficacy of dietary flavonoids. Am. J. Clin. Nutr. 2017;105:10–22. doi: 10.3945/ajcn.116.136051.
    1. Selma M.V., Espin J.C., Tomas-Barberan F.A. Interaction between phenolics and gut microbiota: Role in human health. J. Agric. Food Chem. 2009;57:6485–6501. doi: 10.1021/jf902107d.
    1. Farombi E.O., Adedara I.A., Awoyemi O.V., Njoku C.R., Micah G.O., Esogwa C.U., Owumi S.E., Olopade J.O. Dietary protocatechuic acid ameliorates dextran sulphate sodium-induced ulcerative colitis and hepatotoxicity in rats. Food Funct. 2016;7:913–921. doi: 10.1039/C5FO01228G.
    1. Parkar S.G., Trower T.M., Stevenson D.E. Fecal microbial metabolism of polyphenols and its effects on human gut microbiota. Anaerobe. 2013;23:12–19. doi: 10.1016/j.anaerobe.2013.07.009.
    1. Molan A.-L., Liu Z., Kruger M. The ability of blackcurrant extracts to positively modulate key markers of gastrointestinal function in rats. World J. Microbiol. Biotechnol. 2010;26:1735–1743. doi: 10.1007/s11274-010-0352-4.
    1. Bialonska D., Ramnani P., Kasimsetty S.G., Muntha K.R., Gibson G.R., Ferreira D. The influence of pomegranate by-product and punicalagins on selected groups of human intestinal microbiota. Int. J. Food Microbiol. 2010;140:175–182. doi: 10.1016/j.ijfoodmicro.2010.03.038.
    1. Gibson G., Wang X. Regulatory effects of bifidobacteria on the growth of other colonic bacteria. J. Appl. Bacteriol. 1994;77:412–420. doi: 10.1111/j.1365-2672.1994.tb03443.x.
    1. Miao M., Jiang H., Jiang B., Zhang T., Cui S.W., Jin Z. Phytonutrients for controlling starch digestion: Evaluation of grape skin extract. Food Chem. 2014;145:205–211. doi: 10.1016/j.foodchem.2013.08.056.
    1. Camelo-Méndez G.A., Agama-Acevedo E., Sanchez-Rivera M.M., Bello-Pérez L.A. Effect on in vitro starch digestibility of mexican blue maize anthocyanins. Food Chem. 2016;211:281–284. doi: 10.1016/j.foodchem.2016.05.024.
    1. Magallanes-Cruz P.A., Flores-Silva P.C., Bello-Perez L.A. Starch structure influences its digestibility: A review. J. Food Sci. 2017;82:2016–2023. doi: 10.1111/1750-3841.13809.
    1. Immerstrand T., Andersson K.E., Wange C., Rascon A., Hellstrand P., Nyman M., Cui S.W., Bergenståhl B., Trägårdh C., Öste R. Effects of oat bran, processed to different molecular weights of β-glucan, on plasma lipids and caecal formation of scfa in mice. Br. J. Nutr. 2010;104:364–373. doi: 10.1017/S0007114510000553.
    1. Immerstrand T. Cholesterol-lowering properties of oats: Effects of processing and the role of oat components. Division of Applied Nutrition and Food Chemistry, Lund University; Lund, Sweden: 2010.
    1. Dostal A., Fehlbaum S., Chassard C., Zimmermann M.B., Lacroix C. Low iron availability in continuous in vitro colonic fermentations induces strong dysbiosis of the child gut microbial consortium and a decrease in main metabolites. Fems Microbiol. Ecol. 2013;83:161–175. doi: 10.1111/j.1574-6941.2012.01461.x.
    1. Xie Y., Zhu X., Li Y., Wang C. Analysis of the ph-dependent fe (iii) ion chelating activity of anthocyanin extracted from black soybean [glycine max (l.) merr.] coats. J. Agric. Food Chem. 2018;66:1131–1139. doi: 10.1021/acs.jafc.7b04719.
    1. Buchweitz M., Brauch J., Carle R., Kammerer D. Application of ferric anthocyanin chelates as natural blue food colorants in polysaccharide and gelatin based gels. Food Res. Int. 2013;51:274–282. doi: 10.1016/j.foodres.2012.11.030.
    1. Serobatse K.R., Kabanda M.M. Antioxidant and antimalarial properties of butein and homobutein based on their ability to chelate iron (ii and iii) cations: A dft study in vacuo and in solution. Eur. Food Res. Technol. 2016;242:71–90. doi: 10.1007/s00217-015-2520-0.

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