β-ionone prevents dextran sulfate sodium-induced ulcerative colitis and modulates gut microbiota in mice

Jingjing Fang , Tingting Liu , Yumeng Wang , Seong-Gook Kang , Kunlun Huang , Tao Tong

Food Innovation and Advances ›› 2024, Vol. 3 ›› Issue (4) : 320 -331.

PDF (5938KB)
Food Innovation and Advances ›› 2024, Vol. 3 ›› Issue (4) :320 -331. DOI: 10.48130/fia-0024-0031
ARTICLE
research-article

β-ionone prevents dextran sulfate sodium-induced ulcerative colitis and modulates gut microbiota in mice

Author information +
History +
PDF (5938KB)

Abstract

β-ionone has various biological activities, such as anti-inflammatory, antimicrobial, and anticancer effects. The pathogenesis of ulcerative colitis is correlated with immune dysfunction, intestinal barrier damage, and gut microbiota imbalance. However, whether β-ionone has preventive efficacy against ulcerative colitis is unknown. This study investigated the effect of β-ionone on dextran sulfate sodium-induced ulcerative colitis and the underlying molecular mechanisms involved. The ulcerative colitis mouse model was induced by 1.5% dextran sulfate sodium for 10 d. Meanwhile, 200 mg/kg β-ionone was administrated to the mice. Body weight, colon length, colon tissue pathology, colon tissue inflammatory cytokines, colonic oxidative stress, and barrier function were assessed. The composition and structure of gut microbiota were profiled using 16S rRNA sequencing. The results showed that β-ionone supplementation effectively prevented ulcerative colitis by ameliorating colonic tissue damage, reducing inflammatory phenomena, and protecting the colonic epithelial mucosal barrier. β-ionone also protected mice from dextran sulfate sodium-induced gut microbiota disturbance by modifying the overall structure and function of the gut microbiota community and increasing the relative abundance of beneficial gut microbiota. The Spearman correlation analysis revealed that the changes in abundance of the gut microbiota were correlated with ulcerative colitis-related indicators. Overall, this study demonstrated that β-ionone has a preventive effect on ulcerative colitis in mice, and the underlying mechanism may be associated with the protection of the gut barrier and regulation of the gut microbiota. These results are conducive to promoting clinical trials and product development of β-ionone for the prevention and treatment of ulcerative colitis.

Keywords

Gut microbiota / Intestinal barrier / Ulcerative colitis / β-ionone

Cite this article

Download citation ▾
Jingjing Fang, Tingting Liu, Yumeng Wang, Seong-Gook Kang, Kunlun Huang, Tao Tong. β-ionone prevents dextran sulfate sodium-induced ulcerative colitis and modulates gut microbiota in mice. Food Innovation and Advances, 2024, 3(4): 320-331 DOI:10.48130/fia-0024-0031

登录浏览全文

4963

注册一个新账户 忘记密码

Ethical statement

All experimental procedures were conducted according to the guidelines provided by the Animal Care Committee. The China Agricultural University Laboratory Animal Welfare and Animal Experimental Ethical Committee approved the animal experimental protocol used in this study (AW40702202-4-4).

Author contributions

The authors confirm contribution to the paper as follows: study conception and design: Tong T, Huang K, Kang SG; draft manuscript preparation: Fang J, Wang Y; experiments conduction: Liu T; analysis and interpretation of results: Fang J, Liu T; manuscript revision: Fang J, Tong T. All authors reviewed the results and approved the final version of the manuscript.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Acknowledgments

This research was funded by the Science and Technology project of Xizang Autonomous Region (XZ202401ZY0092) and Chinese Universities Scientific Fund (2024TC083).

Conflict of interest

The authors declare that they have no conflict of interest.

References

[1]

Porter RJ, Kalla R, Ho GT. 2020. Ulcerative colitis: recent advances in the understanding of disease pathogenesis. F1000Research 0:294

[2]

Kobayashi T, Siegmund B, Le Berre C, Wei SC, Ferrante M, et al. 2020. Ulcerative colitis. Nature Reviews Disease Primers 6:74

[3]

Harbord M, Eliakim R, Bettenworth D, Karmiris K, Katsanos K, et al. 2017. Third european evidence-based consensus on diagnosis and management of ulcerative colitis. Part 2: current management. Journal of Crohn's and Colitis 11:769-84

[4]

Sandborn WJ, Panés J, Sands BE, Reinisch W, Su C, et al. 2019. Venous thromboembolic events in the tofacitinib ulcerative colitis clinical development programme. Alimentary Pharmacology & Therapeutics 50:1068-76

[5]

Nishida A, Inoue R, Inatomi O, Bamba S, Naito Y, et al. 2018. Gut microbiota in the pathogenesis of inflammatory bowel disease. Clinical Journal of Gastroenterology 11:1-10

[6]

Zhao Y, Li M, Wang Y, Geng R, Fang J, et al. 2023. Understanding the mechanism underlying the anti-diabetic effect of dietary component: a focus on gut microbiota. Critical Reviews in Food Science and Nutrition 63:7378-98

[7]

Gallimore AM, Godkin A. 2013. Epithelial barriers, microbiota, and colorectal cancer. The New England Journal of Medicine 368:282-84

[8]

Ansari M, Emami S. 2016. β-ionone and its analogs as promising anticancer agents. European Journal of Medicinal Chemistry 123:141-54

[9]

Zhu Q, Tong T. 2023. Research progress on bioactivities of β ionone and structure-function relationship of its derivatives. Journal of Food Safety and Quality 14:101-8

[10]

Kamada K, Yasuda R, Murakami T, Inoue R, Mizushima K, et al. 2020. Tu 1927 the effects of carotenoid ingestion on the expression of tight junction protein in intestine which were correlated with gut microbiota composition. Gastroenterology 158:S1221-S1222

[11]

Ma Y, Guo X, Wang Q, Liu T, Liu Q, et al. 2022. Anti-inflammatory effects of β-ionone-curcumin hybrid derivatives against ulcerative colitis. Chemico-Biological Interactions 367:110189

[12]

Xiong T, Zheng X, Zhang K, Wu H, Dong Y, et al. 2022. Ganluyin ameliorates dss-induced ulcerative colitis by inhibiting the entericorigin LPS/TLR4/NF- κB pathway. Journal of Ethnopharmacology 289:115001

[13]

Wang X, Yang J, Cao Q, Tang J. 2014. Therapeutic efficacy and mechanism of water-soluble extracts of banxiaxiexin decoction on BALB/C mice with oxazolone-induced colitis. Experimental and Therapeutic Medicine 8:1201-4

[14]

Krych Ł, Kot W, Bendtsen KMB, Hansen AK, Vogensen FK, et al. 2018. Have you tried spermine? A rapid and cost-effective method to eliminate dextran sodium sulfate inhibition of PCR and RT-PCR. Journal of Microbiological Methods 144:1-7

[15]

Chassaing B, Koren O, Goodrich JK, Poole AC, Srinivasan S, et al. 2015. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519:92-96

[16]

Nearing JT, Douglas GM, Hayes MG, MacDonald J, Desai DK, et al. 2022. Microbiome differential abundance methods produce different results across 38 datasets. Nature Communications 13:342

[17]

El-Akabawy G, El-Sherif NM. 2019. Zeaxanthin exerts protective effects on acetic acid-induced colitis in rats via modulation of proinflammatory cytokines and oxidative stress. Biomedicine & Pharmacotherapy 111:841-51

[18]

Jeon YD, Lee JH, Lee YM, Kim DK. 2020. Puerarin inhibits inflammation and oxidative stress in dextran sulfate sodium-induced colitis mice model. Biomedicine & Pharmacotherapy 124:109847

[19]

Kwon J, Lee C, Heo S, Kim B, Hyun CK. 2021. Dss-induced colitis is associated with adipose tissue dysfunction and disrupted hepatic lipid metabolism leading to hepatosteatosis and dyslipidemia in mice. Scientific Reports 11:5283

[20]

Pelaseyed T, Bergström JH, Gustafsson JK, Ermund A, Birchenough GMH, et al. 2014. The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunological Reviews 260:8-20

[21]

Gong Y, Li H, Li Y. 2016. Effects of Bacillus subtilis on epithelial tight junctions of mice with inflammatory bowel disease. Journal of Interferon and Cytokine Research 36:75-85

[22]

Dahl C, Stigum H, Valeur J, Iszatt N, Lenters V, et al. 2018. Preterm infants have distinct microbiomes not explained by mode of delivery, breastfeeding duration or antibiotic exposure. International Journal of Epidemiology 47:1658-69

[23]

Hu Y, Ye Z, Wu M, She Y, Li L, et al. 2021. The communication between intestinal microbiota and ulcerative colitis: an exploration of pathogenesis, animal models, and potential therapeutic strategies. Frontiers in Medicine 8:766126

[24]

Peng L, Gao X, Nie L, Xie J, Dai T, et al. 2020. Astragalin attenuates dextran sulfate sodium (DSS)-induced acute experimental colitis by alleviating gut microbiota dysbiosis and inhibiting NF- κB activation in mice. Frontiers in Immunology 11:2058

[25]

Moura FA, de Andrade KQ, de Araújo ORP, Nunes-Souza V, de Farias Santos JC, et al. 2016. Colonic and hepatic modulation by lipoic acid and/or n -acetylcysteine supplementation in mild ulcerative colitis induced by dextran sodium sulfate in rats. Oxidative Medicine and Cellular Longevity 2016:1-18

[26]

Agista AZ, Rusbana TB, Islam J, Ohsaki Y, Sultana H, et al. 2021. Fermented rice bran supplementation prevents the development of intestinal fibrosis due to DSS-induced inflammation in mice. Nutrients 13:1869

[27]

Chen L, Yokoyama W, Alves P, Tan Y, Pan J, et al. 2021. Effect of encapsulation on β-carotene absorption and metabolism in mice. Food Hydrocolloids 121:107009

[28]

Yin M, Li C, Zhang L, Zhang L, Lin J, et al. 2022. Mechanism of antifungal activity and therapeutic action of β-ionone on Aspergillus fumigatus keratitis via suppressing LOX1 and JNK/p38 MAPK activation. International Immunopharmacology 110:108992

[29]

Fukuda T, Majumder K, Zhang H, Turner PV, Matsui T, et al. 2016. Adenine inhibits TNF- α signaling in intestinal epithelial cells and reduces mucosal inflammation in a dextran sodium sulfateinduced colitis mouse model. Journal of Agricultural and Food Chemistry 64:4227-34

[30]

Shan M, Gentile M, Yeiser JR, Walland AC, Bornstein VU, et al. 2013. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 342:447-53

[31]

Wu Y, Jha R, Li A, Liu H, Zhang Z, et al. 2022. Probiotics (Lactobacillus plantarum HNU082) supplementation relieves ulcerative colitis by affecting intestinal barrier functions, immunity-related gene expression, gut microbiota, and metabolic pathways in mice. Microbiology Spectrum 10:e01651-22

[32]

Edelblum KL, Turner JR. 2009. The tight junction in inflammatory disease: communication breakdown. Current Opinion in Pharmacology 9:715-20

[33]

Li Q, Zhou S, Wang Y, Cong J. 2022. Changes of intestinal microbiota and microbiota-based treatments in IBD. Archives of Microbiology 204:442

[34]

Hu S, Ma Y, Xiong K, Wang Y, Liu Y, et al. 2023. Ameliorating effects of vitamin k 2 on dextran sulfate sodium-induced ulcerative colitis in mice. International Journal of Molecular Sciences 24:2986

[35]

Fan Y, Pedersen O. 2021. Gut microbiota in human metabolic health and disease. Nature reviews. Microbiology 19:55-71

[36]

Tian M, Li D, Ma C, Feng Y, Hu X, et al. 2021. Barley leaf insoluble dietary fiber alleviated dextran sulfate sodium-induced mice colitis by modulating gut microbiota. Nutrients 13:846

[37]

Cui L, Guan X, Ding W, Luo Y, Wang W, et al. 2021. Scutellaria baicalensis georgi polysaccharide ameliorates DSS-induced ulcerative colitis by improving intestinal barrier function and modulating gut microbiota. International Journal of Biological Macromolecules 166:1035-45

[38]

Martens EC, Neumann M, Desai MS. 2018. Interactions of commensal and pathogenic microorganisms with the intestinal mucosal barrier. Nature Reviews Microbiology 16:457-70

[39]

Guo J, Li M, Zhao Y, Kang SG, Huang K, et al. 2023. Dietary supplementation of cedryl acetate ameliorates adiposity and improves glucose homeostasis in high-fat diet-fed mice. Nutrients 15:980

[40]

Tong T, Guo J, Wu Y, Sharma D, Sangar M, et al. 2024. Dietary supplementation of ark clams protects gut health and modifies gut microbiota in d-galactose-induced aging rats. Journal of the Science of Food and Agriculture 104:675-685

[41]

Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, et al. 2016. Population-level analysis of gut microbiome variation. Science 352:560-564

[42]

Baldassano SN, Bassett DS. 2016. Topological distortion and reorganized modular structure of gut microbial co-occurrence networks in inflammatory bowel disease. Scientific Reports 6:26087

[43]

Nikolaus S, Schulte B, Al-Massad N, Thieme F, Schulte DM, et al. 2017. Increased tryptophan metabolism is associated with activity of inflammatory bowel diseases. Gastroenterology 153:1504-1516.E2

[44]

Zhang HL, Zhang AH, Miao JH, Sun H, Yan GL, et al. 2019. Targeting regulation of tryptophan metabolism for colorectal cancer therapy: a systematic review. RSC Advances 9:338-72

[45]

Wu L, Tang Z, Chen H, Ren Z, Ding Q, et al. 2021. Mutual interaction between gut microbiota and protein/amino acid metabolism for host mucosal immunity and health. Animal Nutrition 7:11-16

[46]

Feng W, Liu J, Tan Y, Ao H, Wang J, et al. 2020. Polysaccharides from Atractylodes macrocephala koidz. Ameliorate ulcerative colitis via extensive modification of gut microbiota and host metabolism. Food Research International 138:109777

[47]

Winkler ES, Thackray LB. 2019. A long-distance relationship: the commensal gut microbiota and systemic viruses. Current Opinion in Virology 37:44-51

AI Summary AI Mindmap
PDF (5938KB)

88

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/