Effects of forsythin extract in <i>Forsythia</i> leaves on intestinal microbiota and short-chain fatty acids in rats fed a high-fat diet

Lanlan Gui; Shaokang Wang; Jing Wang; Wang Liao; Zitong Chen; Da Pan; Hui Xia; Guiju Sun; Su Tian

doi:10.26599/FSHW.2022.9250055

Food Science and Human Wellness 2024, 13(2): 659-667 https://doi.org/10.26599/FSHW.2022.9250055

Open Access | Issue | Published: 25 September 2023

Effects of forsythin extract in Forsythia leaves on intestinal microbiota and short-chain fatty acids in rats fed a high-fat diet

Show Author's Information Hide Author's Information Lanlan Gui^{^a^,}, Shaokang Wang^{^a}(

), Jing Wang^{^b}, Wang Liao^{^a}, Zitong Chen^{^b}, Da Pan^{^a}, Hui Xia^{^a}, Guiju Sun^{^a}, Su Tian^{^c}

Department of Nutrition and Food Hygiene, School of Public Health, Southeast University, Nanjing 210009, China

Nanjing Municipal Center for Disease Control and Prevention, Nanjing 210003, China

Department of Nutrition and Food Hygiene, School of Public Health, Hebei Medical University, Shijiazhuang 050017, China

Peer review under responsibility of Tsinghua University Press.

Keywords:

Intestinal microbiota, High-fat diet, Forsythin, Short-chain fatty acid (SCFA)

Cite this article:

Gui L, Wang S, Wang J, et al. Effects of forsythin extract in Forsythia leaves on intestinal microbiota and short-chain fatty acids in rats fed a high-fat diet. Food Science and Human Wellness, 2024, 13(2): 659-667. https://doi.org/10.26599/FSHW.2022.9250055

Download citation

EndNote(RIS)

BibTeX

1105

Views

281

Downloads

Citations

Crossref

WoS

Scopus

CSCD

Abstract Full text Electronic supplementary material About this article

Abstract

Forsythia suspensa, belonging to the deciduous shrubs of the Luteaceae family, a traditional Chinese medicine, has effects of alleviating swelling, clearing heat, detoxification and promoting blood circulation. The leaves of F. suspensa contain multiple chemical components and have a long history of use in folk medicines and health foods. The purpose of this study was to explore the effects of forsythin extract from F. suspensa leaves on intestinal microbiota and short-chain fatty acid (SCFA) content in rats with obesity induced by a high-fat diet. Forsythin extract in F. suspensa leaves increased the abundance of the intestinal microbiota, ameliorated intestinal microbiota disorders and inhibited the increase in total SCFA content in the intestinal tract in rats with obesity induced by a high-fat diet. These results suggested that forsythin extract in F. suspensa leaves may slow the development of obesity induced by a high-fat diet; thus, its active components and efficacy are worthy of further study.

Full text

Abstract

Full text

Outline

Electronic supplementary material

About this article

Effects of forsythin extract in Forsythia leaves on intestinal microbiota and short-chain fatty acids in rats fed a high-fat diet

Show Author's information Hide Author's Information Lanlan Gui^{^a^,}, Shaokang Wang^{^a}(

), Jing Wang^{^b}, Wang Liao^{^a}, Zitong Chen^{^b}, Da Pan^{^a}, Hui Xia^{^a}, Guiju Sun^{^a}, Su Tian^{^c}

Department of Nutrition and Food Hygiene, School of Public Health, Southeast University, Nanjing 210009, China

Nanjing Municipal Center for Disease Control and Prevention, Nanjing 210003, China

Department of Nutrition and Food Hygiene, School of Public Health, Hebei Medical University, Shijiazhuang 050017, China

Peer review under responsibility of Tsinghua University Press.

Abstract

Keywords: Intestinal microbiota, High-fat diet, Forsythin, Short-chain fatty acid (SCFA)

References(40)

[1]

K.L. Xiang, R.X. Liu, L. Zhao, et al., Labdane diterpenoids from Forsythia suspensa with anti-inflammatory and anti-viral activities, Phytochemistry 173 (2020) 112298. https://doi.org/10.1016/j.phytochem.2020.112298.

DOI Google Scholar

[2]

N. Guo, Q.Y. Gai, J. Jiao, et al., Antibacterial activity of Fructus forsythia essential oil and the application of EO-loaded nanoparticles to food-borne pathogens, Foods 5 (2016) 73. https://doi.org/10.3390/foods5040073.

DOI Google Scholar

[3]

J. Jiao, Q.Y. Gai, M. Luo, et al., Comparison of main bioactive compounds in tea infusions with different seasonal Forsythia suspensa leaves by liquid chromatography-tandem mass spectrometry and evaluation of antioxidant activity, Food Res. Int. 53 (2013) 857-863. https://doi.org/10.1016/j.foodres.2012.12.018.

DOI Google Scholar

[4]

Y. Cui, Q. Wang, X.W. Shi, et al., Simultaneous quantification of 14 bioactive constituents in Forsythia suspensa by liquid chromatography-electrospray ionisation-mass spectrometry, Phytochem. Anal. 21 (2010) 253-260. https://doi.org/10.1002/pca.1194.

DOI Google Scholar

[5]

L.Q. Chen, L.X. Lin, Z. Dong, et al., Comparison of neuroprotective effect of Forsythia suspensa leaf extract and forsythiaside, one of its metabolites, Nat. Prod. Res. 32 (2018) 2705-2708. https://doi.org/10.1080/14786419.2017.1374266.

DOI Google Scholar

[6]

L.M. Zhao, X. Yan, J. Shi, et al., Ethanol extract of Forsythia suspensa root induces apoptosis of esophageal carcinoma cells via the mitochondrial apoptotic pathway, Mol. Med. Rep. 11 (2015) 871-880. https://doi.org/10.3892/mmr.2014.2874.

DOI Google Scholar

[7]

M. Rosenbaum, R. Knight, R.L. Leibel, The gut microbiota in human energy homeostasis and obesity, Trends Endocrinol. Metab. 26 (2015) 493-501. https://doi.org/10.1016/j.tem.2015.07.002

DOI Google Scholar

[8]

J.A. Santos-Marcos, F. Perez-Jimenez, A. Camargo, The role of diet and intestinal microbiota in the development of metabolic syndrome, J. Nutr. Biochem. 70 (2019) 1-27. https://doi.org/10.1016/j.jnutbio.2019.03.017.

DOI Google Scholar

[9]

P. Wang, J.P. Gao, W.X. Ke, et al., Resveratrol reduces obesity in high-fat diet-fed mice via modulating the composition and metabolic function of the gut microbiota, Free Radic. Biol. Med. 156 (2020) 83-98. https://doi.org/10.1016/j.freeradbiomed.2020.04.013.

DOI Google Scholar

[10]

M.Y. Hu, L. Zhang, Z. Ruan, et al., The regulatory effects of citrus peel powder on liver metabolites and gut flora in mice with non-alcoholic fatty liver disease (NAFLD), Foods 10 (2021) 3022. https://doi.org/10.3390/foods10123022

DOI Google Scholar

[11]

Y.J. Liang, C.L. Lin, S.X. Huang, et al., Traditional Chinese medicine and intestinal microbiota: a complementary and integrative health approach to ameliorate obesity-related diseases, Holist. Nurs. Pract. 33 (2019) 259-265. https://doi.org/10.1097/hnp.0000000000000311.

DOI Google Scholar

[12]

Y.Y. Li, X. Gao, Y.J. Lou, Interactions of tea polyphenols with intestinal microbiota and their implication for cellular signal conditioning mechanism, J. Food Biochem. 43 (2019) e12953. https://doi.org/10.1111/jfbc.12953

DOI Google Scholar

[13]

J.H. Wang, S. Bose, G.C. Kim, Flos Lonicera ameliorates obesity and associated endotoxemia in rats through modulation of gut permeability and intestinal microbiota, PLoS One 9 (2014) e86117. https://doi.org/10.1371/journal.pone.0086117.

DOI Google Scholar

[14]

J.H. Cummings, E.W. Pomare, W.J. Branch, et al., Short chain fatty acids in human large intestine, portal, hepatic and venous blood, Gut 28 (1987) 1221-1227. https://doi.org/10.1136/gut.28.10.1221.

DOI Google Scholar

[15]

E.E. Canfora, J.W. Jocken, E.E. Blaak, Short-chain fatty acids in control of body weight and insulin sensitivity, Nat. Rev. Endocrinol. 11 (2015) 577-591. https://doi.org/10.1038/nrendo.2015.128.

DOI Google Scholar

[16]

J. Tarini, T.M. Wolever, The fermentable fibre inulin increases postprandial serum short-chain fatty acids and reduces free-fatty acids and ghrelin in healthy subjects, Appl. Physiol. Nutr. Metab. 35 (2010) 9-16. https://doi.org/10.1139/h09-119.

DOI Google Scholar

[17]

Q.Q. Ye, Y.R. Wang, W.B. Fang, et al., Study on the regulation effect of 8 herbs on intestinal diagnostic flora growth, Journal of Guangdong Pharmaceutical 32 (2016) 291-294. https://doi.org/10.16809/j.cnki.1006-8783.2016012901.

DOI Google Scholar

[18]

Y.Q. Zhou, Y.H. Zheng, S. Chen, et al., Effects of Forsythiae fructus on Lingnan damp-heat model mice and changes of intestinal flora, Traditional Chinese Drug Research and Clinical Pharmacology 30 (2019) 678-685. https://doi.org/10.19378/j.issn.1003-9783.2019.06.007.

DOI Google Scholar

[19]

D.I. Bolnick, L.K. Snowberg, P.E. Hirsch, et al., Individual diet has sex-dependent effects on vertebrate gut microbiota, Nat. Commun. 5 (2014) 4500. https://doi.org/10.1038/ncomms5500.

DOI Google Scholar

[20]

L.X. Yao, E.A. Davidson, M.W. Shaikh, et al., Quantitative analysis of short-chain fatty acids in human plasma and serum by GC-MS, Anal Bioanal Chem. 414 (2022) 4391-4399. https://doi.org/10.1007/s00216-021-03785-8.

DOI Google Scholar

[21]

J.C. Wu, Study on the in vitro metabolism of total flavonoids in Ziziphi Spinosae Semen by normal human intestinal flora, Shanxi University, China, 2021.

[22]

X.N. Yang, I. Khan, S.C. Kang, Chemical composition, mechanism of antibacterial action and antioxidant activity of leaf essential oil of Forsythia koreana deciduous shrub, Asian Pac. J. Trop. Med. 8 (2015) 694-700. https://doi.org/10.1016/j.apjtm.2015.07.031.

DOI Google Scholar

[23]

J.F. Yuan, X.Q. Liu, J.X. Yang, et al., Forsythia suspense leaves, a plant: extraction, purification and antioxidant activity of main active compounds, Eur. Food Res. Technol. 238 (2014) 527-533. https://doi.org/10.1007/s00217-014-2179-y.

DOI Google Scholar

[24]

S.Bibbò, G. Ianiro, V. Giorgio, et al., The role of diet on gut microbiota composition, Eur. Rev. Med. Pharmacol. Sci. 20 (2016) 4742-4749.

Google Scholar

[25]

J. Lloyd-Price, G. Abu-Ali, C. Huttenhower, The healthy human microbiome, Genome. Med. 8 (2016) 51. https://doi.org/10.1186/s13073-016-0307-y.

DOI Google Scholar

[26]

C.T. Zhi, J.Q. Huang, J. Wang, et al., Connection between gut microbiome and the development of obesity, Eur. J. Clin. Microbiol. Infect. Dis. 38 (2019) 1987-1998. https://doi.org/10.1007/s10096-019-03623-x.

DOI Google Scholar

[27]

P.J. Turnbaugh, R.E. Ley, M.A. Mahowald, et al., An obesity-associated gut microbiome with increased capacity for energy harvest, Nature 444 (2006) 1027-1031. https://doi.org/10.1038/nature05414.

DOI Google Scholar

[28]

P.D. Cani, N.M. Delzenne, Interplay between obesity and associated metabolic disorders: new insights into the gut microbiota, Curr. Opin. Pharmacol. 9 (2009) 737-743. https://doi.org/10.1016/j.coph.2009.06.016.

DOI Google Scholar

[29]

R. Krajmalnik-Brown, Z.E. Ilhan, D.W. Kang, et al., Effects of gut microbes on nutrient absorption and energy regulation, Nutr. Clin. Pract. 27 (2012) 201-214. https://doi.org/10.1177/0884533611436116.

DOI Google Scholar

[30]

J. Fernandez, S. Redondo-Blanco, I. Gutierrez-del-Rio, et al., Colon microbiota fermentation of dietary prebiotics towards short-chain fatty acids and their roles as anti-inflammatory and antitumour agents: a review, J. Funct. Foods 25 (2016) 511-522. https://doi.org/10.1016/j.jff.2016.06.032.

DOI Google Scholar

[31]

M. Li, B.C.A.M. van Esch, G.T.M. Wagenaar, et al., Pro- and anti-inflammatory effects of short chain fatty acids on immune and endothelial cells, Eur. J. Pharmacol. 831 (2018) 52-59. https://doi.org/10.1016/j.ejphar.2018.05.003.

DOI Google Scholar

[32]

M.G. Rooks, W.S. Garrett, Gut microbiota, metabolites and host immunity, Nat. Rev. Immunol. 16 (2016) 341-352. https://doi.org/10.1038/nri.2016.42

DOI Google Scholar

[33]

H. Maruta, Y. Yoshimura, A. Araki, Activation of AMP-activated protein kinase and stimulation of energy metabolism by acetic acid in L6 myotube cells, PLoS One 11 (2016) e0158055. https://doi.org/10.1371/journal.pone.0158055.

DOI Google Scholar

[34]

M.A. Hernández, E.E. Canfora, J.W. Jocken, et al., The short-chain fatty acid acetate in body weight control and insulin sensitivity, Nutrients 11 (2019) 1943. https://doi.org/10.3390/nu11081943.

DOI Google Scholar

[35]

K. Weitkunat, S. Schumann, D. Nickel, et al., Importance of propionate for the repression of hepatic lipogenesis and improvement of insulin sensitivity in high-fat diet-induced obesity, Mol. Nutr. Food Res. 60 (2016) 2611-2621. https://doi.org/10.1002/mnfr.201600305.

DOI Google Scholar

[36]

Z.G. Gao, J. Yin, J. Zhang, et al., Butyrate improves insulin sensitivity and increases energy expenditure in mice, Diabetes 58 (2009) 1509-1517. https://doi.org/10.2337/db08-1637.

DOI Google Scholar

[37]

B.T. Wang, Q.M. Kong, X. Li, et al., A high-fat diet increases gut microbiota biodiversity and energy expenditure due to nutrient difference, Nutrients 12 (2020) 3197. https://doi.org/10.3390/nu12103197.

DOI Google Scholar

[38]

R.J. Perry, L. Peng, N.A. Barry, et al., Acetate mediates a microbiome-brain-β-cell axis to promote metabolic syndrome, Nature 534 (2016) 213-217. https://doi.org/10.1038/nature18309.

DOI Google Scholar

[39]

M. Rau, A. Rehman, M. Dittrich, et al., Fecal SCFAs and SCFA-producing bacteria in gut microbiome of human NAFLD as a putative link to systemic T-cell activation and advanced disease, United Eur. Gastroenterol. J. 6 (2018) 1496-1507. https://doi.org/10.1177/2050640618804444.

DOI Google Scholar

[40]

A. Schwiertz, D. Taras, K. Schäfer, et al., Microbiota and SCFA in lean and overweight healthy subjects, Obesity 18 (2010) 190-195. https://doi.org/10.1038/oby.2009.167.

DOI Google Scholar

Electronic supplementary material

File

fshw-13-2-659_ESM.docx (203.1 KB)

About this article

Publication history

Acknowledgements

Rights and permissions

Publication history

Received: 05 August 2022

Revised: 29 August 2022

Accepted: 02 September 2022

Published: 25 September 2023

Issue date: March 2024

Copyright

Acknowledgements

This study was funded by grants from the National Key R&D Program of China (2016YFD0500604).

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/).