Journal Home > Volume 12 , Issue 4
Food Science and Human Wellness 2023, 12(4): 1309-1322 https://doi.org/10.1016/j.fshw.2022.10.013
Research Article | Open Access | Issue | Published: 18 November 2022

Lonicera caerulea polyphenols inhibit fat absorption by regulating Nrf2-ARE pathway mediated epithelial barrier dysfunction and special microbiota

Show Author's Information Yuehua Wanga,b,  Ningxuan Gaoa,b,  Andrea Nieto-Velozac,  Lingxi Zhoud,  Xiyun Suna,b,  Xu Sia,b,  Jinlong Tiana,b,  Yang Line,  Xinyao Jiaoa( ),  Bin Lia,b( )
College of Food Science, Shenyang Agricultural University, Shenyang 110161, China
Key Laboratory of Healthy Food Nutrition and Innovative Manufacturing of Liaoning Province, Shenyang 110161, China
Instituto de Ciencia y Tecnología de Alimentos, Universidad Nacional de Colombia, Bogotá 111311, Colombia
Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, Wuxi 214122, China
College of Food Science and Technology, Zhejiang University of Technology, Hangzhou 310014, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Keywords:
Gut microbiota, Oxidative stress, Polyphenols, Lonicera caerulea berries, Intestinal epithelial barrier
Cite this article:
Wang Y, Gao N, Nieto-Veloza A, et al. Lonicera caerulea polyphenols inhibit fat absorption by regulating Nrf2-ARE pathway mediated epithelial barrier dysfunction and special microbiota. Food Science and Human Wellness, 2023, 12(4): 1309-1322. https://doi.org/10.1016/j.fshw.2022.10.013
Download citation
EndNote(RIS)
BibTeX

374

Views

33

Downloads

Citations

4

Crossref

5

WoS

6

Scopus

1

CSCD

Abstract Full text About this article
Scope

High-fat diet (HFD) induces imbalance in the small intestine environment, where fat digestion and absorption mainly take place. This study aimed to elucidate the mechanisms by which Lonicera caerulea polyphenols (LCP) might inhibit fat absorption, from the perspective of small intestine microbiota and epithelial barrier integrity.

Methods and results

Male Sprague-Dawley rats were given HFD with or without co-administration of LCP for 8 weeks. The results showed that LCP supplementation significantly decreased the levels of serum triglycerides (TG), total cholesterol (TC), and low-density lipoprotein cholesterol (LDL-C), and increased the contents of fecal sterols, in HFD rats. LCP also inhibited the dysfunction of the small intestine epithelial barrier, via alleviating the oxidative stress activated by Nrf2-ARE pathway, and by modulating the expressions of pro-inflammatory factors such as tumor necrosis factor-α (TNF-α), interleukin-6 (IL-6), cyclooxygenase-2 (COX-2), nuclear factor kappa-B p65 (NF-κB p65) and inducible nitric oxide synthase (iNOS) in the small intestine. Additionally, LCP administration restored the balance in small intestine microbiota and increased the abundance of the specific bacteria, such as Lactobacillus, involved in fat absorption.

Conclusion

Our results demonstrated that LCP may be beneficial to inhibit fat absorption. The mechanism seems to be associated with the protection of the epithelial barrier integrity and the modulation of specific bacteria in the small intestine.


menu
Abstract
Full text
Outline
About this article

Lonicera caerulea polyphenols inhibit fat absorption by regulating Nrf2-ARE pathway mediated epithelial barrier dysfunction and special microbiota

Show Author's information Yuehua Wanga,b, Ningxuan Gaoa,b, Andrea Nieto-Velozac, Lingxi Zhoud, Xiyun Suna,b, Xu Sia,b, Jinlong Tiana,b, Yang Line, Xinyao Jiaoa( ), Bin Lia,b( )
College of Food Science, Shenyang Agricultural University, Shenyang 110161, China
Key Laboratory of Healthy Food Nutrition and Innovative Manufacturing of Liaoning Province, Shenyang 110161, China
Instituto de Ciencia y Tecnología de Alimentos, Universidad Nacional de Colombia, Bogotá 111311, Colombia
Key Laboratory of Industrial Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, Wuxi 214122, China
College of Food Science and Technology, Zhejiang University of Technology, Hangzhou 310014, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

Scope

High-fat diet (HFD) induces imbalance in the small intestine environment, where fat digestion and absorption mainly take place. This study aimed to elucidate the mechanisms by which Lonicera caerulea polyphenols (LCP) might inhibit fat absorption, from the perspective of small intestine microbiota and epithelial barrier integrity.

Methods and results

Male Sprague-Dawley rats were given HFD with or without co-administration of LCP for 8 weeks. The results showed that LCP supplementation significantly decreased the levels of serum triglycerides (TG), total cholesterol (TC), and low-density lipoprotein cholesterol (LDL-C), and increased the contents of fecal sterols, in HFD rats. LCP also inhibited the dysfunction of the small intestine epithelial barrier, via alleviating the oxidative stress activated by Nrf2-ARE pathway, and by modulating the expressions of pro-inflammatory factors such as tumor necrosis factor-α (TNF-α), interleukin-6 (IL-6), cyclooxygenase-2 (COX-2), nuclear factor kappa-B p65 (NF-κB p65) and inducible nitric oxide synthase (iNOS) in the small intestine. Additionally, LCP administration restored the balance in small intestine microbiota and increased the abundance of the specific bacteria, such as Lactobacillus, involved in fat absorption.

Conclusion

Our results demonstrated that LCP may be beneficial to inhibit fat absorption. The mechanism seems to be associated with the protection of the epithelial barrier integrity and the modulation of specific bacteria in the small intestine.

Keywords: Gut microbiota, Oxidative stress, Polyphenols, Lonicera caerulea berries, Intestinal epithelial barrier

References(64)

[1]

B. Li, Z. Cheng, X. Sun, et al., Lonicera caerulea L. polyphenols alleviate oxidative stress-induced intestinal environment imbalance and lipopolysaccharide-induced liver injury in HFD-fed rats by regulating the Nrf2/HO-1/NQO1 and MAPK pathways, Mol. Nutr. Food Res. 64 (2020)1901315. http://dx.doi.org/10.1002/mnfr.201901315.
DOI Google Scholar
[2]

J. Tulkens, G. Vergauwen, J. van Deun, et al., Increased levels of systemic LPS-positive bacterial extracellular vesicles in patients with intestinal barrier dysfunction, Gut 69 (2020) 191-193. http://dx.doi.org/10.1136/gutjnl-2018-317726.
DOI Google Scholar
[3]

A. Hruby, F.B. Hu, The epidemiology of obesity: a big picture, Pharmacoeconomics 33 (2015) 673-789. http://dx.doi.org/10.1007/s40273-014-0243-x.
DOI Google Scholar
[4]

H. Zhao, N. Cheng, L. He, et al., Antioxidant and hepatoprotective effects of A. cerana honey against acute alcohol-induced liver damage in mice, Food Res. Int. 101 (2017) 35-44. http://dx.doi.org/10.1016/j.foodres.2017.08.014.
DOI Google Scholar
[5]

J.K. Lee, S.H. Jung, S.E. Lee, et al., Alleviation of ascorbic acid-induced gastric high acidity by calcium ascorbate in vitro and in vivo, Korean J. Physiol. Pharmacol. 22 (2018) 35-42. http://dx.doi.org/10.4196/kjpp.2018.22.1.35.
DOI Google Scholar
[6]

P.M. Ferraro, G.C. Curhan, G. Gambaro, et al., Total, dietary, and supplemental vitamin C intake and risk of incident kidney stones, Am. J. Kidney Dis. 67 (2016) 400-407. http://dx.doi.org/10.1053/j.ajkd.2015.09.005.
DOI Google Scholar
[7]

A. Flint, B. Helt, A. Raben, et al., Effects of different dietary fat types on postprandial appetite and energy expenditure, Obes. Res. 11 (2012) 1449-1455. http://dx.doi.org/10.1038/oby.2003.194.
DOI Google Scholar
[8]

Y. Yao, F. Xu, X. Ju, et al., Lipid-lowering effects and intestinal transport of polyphenol extract from digested buckwheat in Caco-2/HepG2 coculture models, J. Agric. Food Chem. 68 (2020) 4205-4214. http://dx.doi.org/10.1021/acs.jafc.0c00321.
DOI Google Scholar
[9]

Y. Wang, J. Zhu, X. Meng, et al., Comparison of polyphenol, anthocyanin and antioxidant capacity in four varieties of Lonicera caerulea berry extracts, Food Chem. 197 (2016) 522-529. http://dx.doi.org/10.1016/j.foodchem.2015.11.006.
DOI Google Scholar
[10]

Y. Wang, B. Li, Y. Ma, et al., Lonicera caerulea berry extract attenuates lipopolysaccharide induced inflammation in BRL-3A cells: oxidative stress, energy metabolism, hepatic function, J. Funct. Foods 24 (2016) 1-10. http://dx.doi.org/10.1016/j.jff.2016.03.023.
DOI Google Scholar
[11]

R. Becker, A. Szakiel, Phytochemical characteristics and potential therapeutic properties of blue honeysuckle Lonicera caerulea L.(Caprifoliaceae), J. Herb Medi. 16 (2019) 100237. http://dx.doi.org/10.1016/j.hermed.2018.10.002.
DOI Google Scholar
[12]

B. Kusznierewicz, A. Piekarska, B. Mrugalska, et al., Phenolic composition and antioxidant properties of Polish blue-berried honeysuckle genotypes by HPLC-DAD-MS, HPLC postcolumn derivatization with ABTS or FC, and TLC with DPPH visualization, J. Agric. Food Chem. 60 (2012) 1755-1763.http://dx.doi.org/10.1021/jf2039839.
DOI Google Scholar
[13]

P. Raudsepp, D. Anton, M. Roasto, et al., The antioxidative and antimicrobial properties of the blue honeysuckle (Lonicera caerulea L.), Siberian rhubarb (Rheum rhaponticum L.) and some other plants, compared to ascorbic acid and sodium nitrite, Food Control 31 (2013) 129-135. http://dx.doi.org/10.1016/j.foodcont.2012.10.007.
DOI Google Scholar
[14]

M.I. Gruia, E. Oprea, I. Gruia, et al., The antioxidant response induced by Lonicera caerulaea berry extracts in animals bearing experimental solid tumors, Molecules 13 (2008) 1195-1206. http://dx.doi.org/10.3390/molecules13051195.
DOI Google Scholar
[15]

J.W. Kim, Y.S. Lee, D.J. Seol, et al., Anti-obesity and fatty liver-preventing activities of Lonicera caerulea in high-fat diet-fed mice, Int. J. Mol. Med. 42(2018) 3047-3064. http://dx.doi.org/10.3892/ijmm.2018.3879.
DOI Google Scholar
[16]

S. Wu, R. Hu, H. Nakano, et al., Modulation of gut microbiota by Lonicera caerulea L. berry polyphenols in a mouse model of fatty liver induced by high fat diet, Molecules 23 (2018) 3213. http://dx.doi.org/10.3390/molecules23123213.
DOI Google Scholar
[17]

T. Jhansyrani, D. Sujatha, K. Bharathi, et al., Ethanolic extract of cashew apple inhibits lipid metabolism and ameliorates obesity in atherogenic dietinduced obese rats, Asian Pac. J. Trop. Bio. 9 (2019) 405-414. http://dx.doi.org/10.4103/2221-1691.269522.
DOI Google Scholar
[18]

L. Gulua, L. Nikolaishvili, M. Jgenti, et al., Polyphenol content, anti-lipase and antioxidant activity of teas made in Georgia, Ann. Agric. Sci. 16 (2018)357-361. http://dx.doi.org/10.1016/j.aasci.2018.06.006.
DOI Google Scholar
[19]

A. Gondoin, D. Grussu, D. Stewart, et al., White and green tea polyphenols inhibit pancreatic lipase in vitro, Food Res. Int. 43 (2010) 1537-1544. http://dx.doi.org/10.1016/j.foodres.2010.04.029.
DOI Google Scholar
[20]

M. Friedrich, K.J. Petzke, D. Raederstorff, et al., Acute effects of epigallocatechin gallate from green tea on oxidation and tissue incorporation of dietary lipids in mice fed a high-fat diet, Int. J. Obes. 36 (2012) 735-743.http://dx.doi.org/10.1038/ijo.2011.136.
DOI Google Scholar
[21]

H. Sugiyama, Y. Akazome, T. Shoji, et al., Oligomeric procyanidins in apple polyphenol are main active components for inhibition of pancreatic lipase and triglyceride absorption, J. Agric. Food Chem. 55 (2007) 4604-4609.http://dx.doi.org/10.1021/jf070569k.
DOI Google Scholar
[22]

F.G. Apaydin, H. Baş, S. Kalender, et al., Bendiocarb induced histopathological and biochemical alterations in rat liver and preventive role of vitamins C and E, Environ. Toxicol. Pharmacol. 49 (2017) 148-155. http://dx.doi.org/10.1016/j.etap.2016.11.018.
DOI Google Scholar
[23]

P.C. Badgujar, N.N. Pawar, G.A. Chandratre, et al., Fipronil induced oxidative stress in kidney and brain of mice: protective effect of vitamin E and vitamin C, Pestic. Biochem. Physiol. 118 (2015) 10-18. http://dx.doi.org/10.1016/j.pestbp.2014.10.013.
DOI Google Scholar
[24]

Y. Wang, B. Li, J. Zhu, et al., Lonicera caerulea berry extract suppresses lipopolysaccharide-induced inflammation via Toll-like receptor and oxidative stress-associated mitogen-activated protein kinase signaling, Food Funct. 7 (2016) 4267-4277. http://dx.doi.org/10.1039/c6fo00627b.
DOI Google Scholar
[25]

S. Liu, Z. Wu, S. Guo, et al., Polyphenol-rich extract from wild Lonicera caerulea berry reduces cholesterol accumulation by mediating the expression of hepatic miR-33 and miR-122, HMGCR, and CYP7A1 in rats, J. Funct.Foods 40 (2018) 648-658. http://dx.doi.org/10.1016/j.jff.2017.11.048.
DOI Google Scholar
[26]

J. Zhao, J. Zang, Y. Lin, et al., Polyphenol-rich blue honeysuckle extract alleviates silica-induced lung fibrosis by modulating Th immune response and Nrf2/HO-1 MAPK signaling, J. Funct. Foods 53 (2019) 176-186. http://dx.doi.org/10.1016/j.jff.2018.12.030.
DOI Google Scholar
[27]

A.A.A. Abdo, C. Zhang, Y. Lin, et al., Xylo-oligosaccharides ameliorate high cholesterol diet induced hypercholesterolemia and modulate sterol excretion and gut microbiota in hamsters, J. Funct. Foods 77 (2021) 104334.http://dx.doi.org/10.1016/j.jff.2020.104334.
DOI Google Scholar
[28]

K.E. Hummer, Blue honeysuckle: a new berry crop for North America, J.Am. Pomol. Soci. 60 (2006) 3-8. http://dx.doi.org/10.1300/J064v27n04_08.
DOI Google Scholar
[29]

G.B. Celli, A. Ghanem, M.S.L. Brooks, Haskap berries (Lonicera caerulea L.)-a critical review of antioxidant capacity and health-related studies for potential value-added products, Food Bioproc. Technol. 7 (2014) 1541-1554.http://dx.doi.org/10.1007/s11947-014-1301-2.
DOI Google Scholar
[30]

I. Palikova, J. Heinrich, P. Bednar, et al., Constituents and antimicrobial properties of blue honeysuckle: a novel source for phenolic antioxidants, J. Agric. Food Chem. 56 (2008) 11883-11889. http://dx.doi.org/10.1021/jf8026233.
DOI Google Scholar
[31]

A. Chaovanalikit, M.M. Thompson, R.E. Wrolstad, Characterization and quantification of anthocyanins and polyphenolics in blue honeysuckle(Lonicera caerulea L.), J. Agric. Food Chem. 52 (2004) 848-852. http://dx.doi.org/10.1021/jf030509o.
DOI Google Scholar
[32]

T. Finkel, N.J. Holbrook, Oxidants, oxidative stress and the biology of ageing, Nature 408 (2000) 239-247. http://dx.doi.org/10.1038/35041687.
DOI Google Scholar
[33]

M. Valko, D. Leibfritz, J. Moncol, et al., Free radicals and antioxidants in normal physiological functions and human disease, Int. J. Biochem. Cell Biol. 39 (2007) 44-84. http://dx.doi.org/10.1016/j.biocel.2006.07.001.
DOI Google Scholar
[34]

L.J. John, M. Fromm, J.D. Schulzke, Epithelial barriers in intestinal inflammation, Antioxid. Redox. Signal. 15 (2011) 1255-1270. http://dx.doi.org/10.1089/ars.2011.3892.
DOI Google Scholar
[35]

T. Hussain, B. Tan, Y. Yin, et al., Oxidative stress and inflammation: what polyphenols can do for us?, Oxid. Med. Cell. Longev. 2016 (2016) 1-9.http://dx.doi.org/10.1155/2016/7432797.
DOI Google Scholar
[36]

J. Tan, Y. Li, D.X. Hou, et al., The effects and mechanisms of cyanidin-3-glucoside and its phenolic metabolites in maintaining intestinal integrity, Antioxidants 8 (2019) 479. http://dx.doi.org/10.3390/antiox8100479.
DOI Google Scholar
[37]

J.Heinrich, K. Valentová, J. Vacek, et al., Metabolic profiling of phenolic acids and oxidative stress markers after consumption of Lonicera caerulea L.fruit, J. Agric. Food Chem. 61 (2013) 4526-4532. http://dx.doi.org/10.1021/jf304150b.
DOI Google Scholar
[38]

J.M. Lee, J.A. Johnson, An important role of Nrf2-ARE pathway in the cellular defense mechanism, J. Biochem. Mol. Biol. 37 (2004) 139-143.http://dx.doi.org/10.5483/BMBRep.2004.37.2.139.
DOI Google Scholar
[39]

S. Singh, S. Vrishni, B.K. Singh, et al., Nrf2-ARE stress response mechanism: a control point in oxidative stress-mediated dysfunctions and chronic inflammatory diseases, Free Radic. Res. 44 (2010) 1267-1288. http://dx.doi.org/10.3109/10715762.2010.507670.
DOI Google Scholar
[40]

H. Kumar, I.S. Kim, S.V. More, et al., Natural product-derived pharmacological modulators of Nrf2/ARE pathway for chronic diseases, Nat.Prod. Rep. 31 (2014) 109-139. http://dx.doi.org/10.1039/c3np70065h.
DOI Google Scholar
[41]

J. Reyes-Ocampo, D. Ramirez-Ortega, G.I.V. Cervantes, et al., Mitochondrial dysfunction related to cell damage induced by 3-hydroxykynurenine and 3-hydroxyanthranilic acid: non-dependent-effect of early reactive oxygen species production, Neurotoxicology 50 (2015) 81-91. http://dx.doi.org/10.1016/j.neuro.2015.08.003.
DOI Google Scholar
[42]

S. Wu, S. Yano, J. Chen, et al., Polyphenols from Lonicera caerulea L. berry inhibit LPS-induced inflammation through dual modulation of inflammatory and antioxidant mediators, J. Agric. Food Chem. 65 (2017) 5133-5141.http://dx.doi.org/10.1021/acs.jafc.7b01599.
DOI Google Scholar
[43]

S.Wu, S. Yano, A. Hisanaga, et al., Polyphenols from Lonicera caerulea L. berry attenuate experimental nonalcoholic steatohepatitis by inhibiting proinflammatory cytokines productions and lipid peroxidation, Mol. Nutr.Food Res. 61 (2017) 1600858. http://dx.doi.org/10.1002/mnfr.201600858.
DOI Google Scholar
[44]

R. Hu, Z. He, M. Liu, et al., Dietary protocatechuic acid ameliorates inflammation and up-regulates intestinal tight junction proteins by modulating gut microbiota in LPS-challenged piglets, J. Anim. Sci.Biotechnol. 11 (2020) 92. http://dx.doi.org/10.1186/s40104-020-00492-9.
DOI Google Scholar
[45]

P.L. Brubaker, Glucagon-like peptide-2 and the regulation of intestinal growth and function, Compr. Physiol. 8 (2018) 1185-1210. http://dx.doi.org/10.1002/cphy.c170055.
DOI Google Scholar
[46]

P.D. Cani, S. Possemiers, T.V. de Wiele, et al., Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability, Gut 58 (2009) 1091-1103. http://dx.doi.org/10.1136/gut.2018.165886.
DOI Google Scholar
[47]

T. Suzuki, H. Hara, Role of flavonoids in intestinal tight junction regulation, J. Nutr. Biochem. 22 (2011) 401-408. http://dx.doi.org/10.1016/j.jnutbio.2010.08.001.
DOI Google Scholar
[48]

U. Etxeberria, N. Arias, N. Boque, et al., Reshaping faecal gut microbiota composition by the intake of trans-resveratrol and quercetin in high-fat sucrose diet-fed rats, J. Nutr. Biochem. 26 (2015) 651-660. http://dx.doi.org/10.1016/j.jnutbio.2015.01.002.
DOI Google Scholar
[49]

S. Bibi, Y. Kang, M. Du, et al., Dietary red raspberries attenuate dextran sulfate sodium-induced acute colitis, J. Nutr. Biochem. 51 (2018) 40-46.http://dx.doi.org/10.1016/j.jnutbio.2017.08.017.
DOI Google Scholar
[50]

Y. Peng, Y. Yan, P. Wan, et al., Gut microbiota modulation and antiinflammatory properties of anthocyanins from the fruits of Lycium ruthenicum Murray in dextran sodium sulfate-induced colitis in mice, Free Radic. Biol. Med. 136 (2019) 96-108. http://dx.doi.org/10.1016/j.freeradbiomed.2019.04.005.
DOI Google Scholar
[51]

P. Wang, D. Li, W. Ke, et al., Resveratrol-induced gut microbiota reduces obesity in high-fat diet-fed mice, Int. J. Obes. 44 (2019) 213-225. http://dx.doi.org/10.1038/s41366-019-0332-1.
DOI Google Scholar
[52]

N.R. Shin, T.W. Whon, J.W. Bae, Proteobacteria: microbial signature of dysbiosis in gut microbiota, Trends Biotechnol. 33 (2015) 496-503. http://dx.doi.org/10.1016/j.tibtech.2015.06.011.
DOI Google Scholar
[53]

A.M.P. Gomes, F.X. Malcata, Bifidobacterium spp. and Lactobacillus acidophilus: biological, biochemical, technological and therapeutical properties relevant for use as probiotics, Trends Food Sci. Technol. 10 (1999)139-157. http://dx.doi.org/10.1016/S0924-2244(99)00033-3.
DOI Google Scholar
[54]

S. Parvez, K.A. Malik, S.A. Kang, et al., Probiotics and their fermented food products are beneficial for health, J. Appl. Microbiol. 100 (2006) 1171-1185.http://dx.doi.org/10.1111/j.1365-2672.2006.02963.x.
DOI Google Scholar
[55]

C. Chelakkot, Y. Choi, D.K. Kim, et al., Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions, Exp. Mol. Med. 50 (2018) e450. http://dx.doi.org/10.1038/emm.2017.282.
DOI Google Scholar
[56]

N.N. Zhang, W.H. Guo, H. Hu, et al., Effect of a polyphenol-rich Canarium album extract on the composition of the gut microbiota of mice fed a high-fat diet, Molecules 23 (2018) 2188. http://dx.doi.org/10.3390/molecules23092188.
DOI Google Scholar
[57]

Y. Ravussin, O. Koren, A. Spor, et al., Responses of gut microbiota to diet composition and weight loss in lean and obese mice, Obesity 20 (2012) 738-747. http://dx.doi.org/10.1038/oby.2011.111.
DOI Google Scholar
[58]

B.W. Parks, E. Nam, E. Org, et al., Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice, Cell Metab. 17 (2013) 141-152. http://dx.doi.org/10.1016/j.cmet.2012.12.007.
DOI Google Scholar
[59]

X. Jiao, Y. Wang, Y. Lin, et al., Blueberry polyphenols extract as a potential prebiotic with anti-obesity effects on C57BL/6 J mice by modulating the gut microbiota, J. Nutr. Biochem. 64 (2018) 88-100. http://dx.doi.org/10.1016/j.jnutbio.2018.07.008.
DOI Google Scholar
[60]

L. Abenavoli, E. Scarpellini, C. Colica, et al., Gut microbiota and obesity: a role for probiotics, Nutrients 11 (2019) 2690. http://dx.doi.org/10.3390/nu11112690.
DOI Google Scholar
[61]

R. Zhao, X. Long, J. Yang, et al., Pomegranate peel polyphenols reduce chronic low-grade inflammatory responses by modulating gut microbiota and decreasing colonic tissue damage in rats fed a high-fat diet, Food Funct.10 (2019) 8273-8285. http://dx.doi.org/10.1039/C9FO02077B.
DOI Google Scholar
[62]

Z. Wang, K.L. Lam, J. Hu, et al., Chlorogenic acid alleviates obesity and modulates gut microbiota in high-fat-fed mice, Food Sci. Nutr. 7 (2019) 579-588. http://dx.doi.org/10.1002/fsn3.868.
DOI Google Scholar
[63]

P. Wang, J. Gao, W. Ke, et al., Resveratrol reduces obesity in high-fat diet-fed mice via modulating the structure and metabolic function of the gut microbiota, Free Radical Bio. Medi. 156 (2020) 83-98. http://dx.doi.org/10.1016/j.freeradbiomed.2020.04.013.
DOI Google Scholar
[64]

L. Monin, S.L. Gaffen, Interleukin 17 family cytokines: signaling mechanisms, biological activities, and therapeutic implications, Cold Spring Harb. Perspect. Biol. 10 (2018) a028522. http://dx.doi.org/10.1101/cshperspect.a028522.
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 21 May 2021
Revised: 17 August 2021
Accepted: 18 November 2021
Published: 18 November 2022
Issue date: July 2023

Copyright

© 2023 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32001685), the Guidance Plan of Liaoning Natural Science Foundation (20180550776), and the Research Initiation Fund of Shenyang Agricultural University (880418026).

Rights and permissions

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Return