AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (9.9 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Open Access

Sugarcane leaves-derived polyphenols alleviate metabolic syndrome and modulate gut microbiota of ob/ob mice

Li Suna,b,1,Tao Wanga,b,1Baosong Chena,bCui Guoa,bShanshan Qiaoa,bJinghan Lina,bHuan Liaoa,bHuanqin Daia,bBin WangcJingzu Suna( )Hongwei Liua,b( )
State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China
Savaid Medicine School, University of Chinese Academy of Sciences, Beijing 100101, China
Guangxi Academy of Sciences, Nanning 530007, China

1 These authors contributed equally.

Peer review under responsibility of Tsinghua University Press.

Show Author Information

Abstract

Sugarcane leaves-derived polyphenols (SLP) have been demonstrated to have diverse health-promoting benefits, but the mechanism of action has not been fully elucidated. This study aimed to investigate the anti-metabolic disease effects of SLP and the underlying mechanisms in mice. In the current study, we prepared the SLP mainly consisting of three flavonoid glycosides, three phenol derivatives, and two lignans including one new compound, and further demonstrated that SLP reduced body weight gain and fat accumulation, improved glucose and lipid metabolism disorders, ameliorated hepatic steatosis, and regulated short-chain fatty acids (SCFAs) production and secondary bile acids metabolism in ob/ob mice. Notably, SLP largely altered the gut microbiota composition, especially enriching the commensal bacteria Akkermansia muciniphila and Bacteroides acidifaciens. Oral gavage with the above two strains ameliorated metabolic syndrome (MetS), regulated secondary bile acid metabolism, and increased the production of SCFAs in high-fat diet (HFD)-induced obese mice. These results demonstrated that SLP could be used as a prebiotic to attenuate MetS via regulating gut microbiota composition and further activating the secondary bile acids-mediated gut-adipose axis.

Electronic Supplementary Material

Download File(s)
fshw-13-2-633_ESM.docx (1.4 MB)

References

[1]

J. Kaur, A comprehensive review on metabolic syndrome, Cardiol. Res. Pract. 2014 (2014) 943162. https://doi.org/10.1155/2014/943162.

[2]

M. Guevara-Cruz, A.G. Flores-Lopez, M. Aguilar-Lopez, et al., Improvement of lipoprotein profile and metabolic endotoxemia by a lifestyle intervention that modifies the gut microbiota in subjects with metabolic syndrome, J. Am. Heart Assoc. 8 (2019) e012401. https://doi.org/10.1161/JAHA.119.012401.

[3]

P.J. Miranda, R.A. Defronzo, R.M. Califf, et al., Metabolic syndrome: definition, pathophysiology, and mechanisms, Am. Heart J. 149 (2005) 33-45.

[4]

G.M. Saklayen, The global epidemic of the metabolic syndrome, Curr. Hypertens 20 (2018) 12. https://doi.org/10.1016/j.ahj.2004.07.013.

[5]

A. Koliada, G. Syzenko, V. Moseiko, et al., Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population, BMC Microbiol. 17 (2017) 120. https://doi.org/10.1186/s12866-017-1027-1.

[6]

P.D. Cani, J. Amar, M.A. Iglesias, et al., Metabolic endotoxemia initiates obesity and insulin resistance, Diabetes 56 (2007) 1761-1772. https://doi.org/10.2337/db06-1491.

[7]

J.G. LeBlanc, F. Chain, R. Martin, et al., Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Micro, Cell Fact. 16 (2017) 79. https://doi.org/10.1186/s12934-017-0691-z.

[8]

S.S. Qiao, K. Wang, C. Liu, et al., The enriched gut commensal Faeciroseburia intestinalis contributes to the anti-metabolic disorders effects of the Ganoderma meroterpene derivative, Food Sci. Food Saf. 11 (2021) 85-96. https://doi.org/10.1016/j.fshw.2021.07.010.

[9]

C. Depommier, A. Everard, C. Druart, et al., Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study, Nat. Med. 25 (2013) 1096. https://doi.org/10.1038/s41591-019-0495-2.

[10]

K. Wang, M. Liao, N. Zhou, et al., Parabacteroides distasonis alleviates obesity and metabolic dysfunctions via production of succinate and secondary bile acids, Cell Rep. 26 (2019) 222-235. https://doi.org/10.1016/j.celrep.2018.12.028.

[11]

H.K. Pedersen, V. Gudmundsdottir, H.B. Nielsen, et al., Human gut microbes impact host serum metabolome and insulin sensitivity, Nature 535 (2016) 376-381. https://doi.org/10.1038/nature18646.

[12]

J. Liu, Z. He, N. Ma, et al., Beneficial effects of dietary polyphenols on high-fat diet-induced obesity linking with modulation of gut microbiota, J. Agri. Food Chem. 68 (2019) 33-47. https://doi.org/10.1021/acs.jafc.9b06817.

[13]

F. Huang, X. Zheng, X. Ma, et al., Theabrownin from pu-erh tea attenuates hypercholesterolemia via modulation of gut microbiota and bile acid metabolism, Nat. Commun. 10 (2019) 4971. https://doi.org/10.1038/s41467-019-12896-x.

[14]

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 Radic. Biol. Med. 156 (2020) 83-98. https://doi.org/10.1016/j.freeradbiomed.2020.04.013.

[15]

G. Matacchione, F. Gurau, S. Baldoni, et al., Pleiotropic effects of polyphenols on glucose and lipid metabolism: focus on clinical trials, Ageing Res. Rev. 61 (2020) 101074. https://doi.org/10.1016/j.arr.2020.101074.

[16]

R.V. Santos, A.R. Evangelista, J.C. Pinto, et al., Chemical composition of sugar cane (Saccharum spp.) and of the silages with different additives at two cutting ages, Cienc. Agrotecnologia 30 (2006) 1184-1189. https://doi.org/10.1590/S1413-70542006000600022.

[17]

Y.T. Xu, C.Y. Li, X.B. Huang, et al., Photoinduced hydroxylation of arylboronic acids with molecular oxygen under photocatalyst-free conditions, Green Chem. 21 (2019) 4971-4975. https://doi.org/10.1039/C9GC02229E.

[18]

S. Moussouni, C.V. Karakousi, P. Tsatalas, et al., Biological studies with phytochemical analysis of cornus mas unripe fruits, Chem. Nat. Compd. 56 (2020) 141-144. https://doi.org/10.1007/s10600-020-02966-8.

[19]

R. Swisłocka, M. Kowczyk-Sadowy, M. Kalinowska, et al., Spectroscopic (FT-IR, FT-Raman, 1H and 13C NMR) and theoretical studies of p-coumaric acid and alkali metalp-coumarates, Spectroscopy 27 (2012) 35-48. https://doi.org/10.3390/molecules20023146.

[20]

J.M. Gieel, I. Serbian, A. Loesche, et al., Substituted cinnamic anhydrides act as selective inhibitors of acetylcholinesterase, Bioorg. Chem. 90 (2019) 103058. https://doi.org/10.1016/j.bioorg.2019.103058.

[21]

J. Shuai, Z. Li, S. Wei, et al., Bioactive constituents of Glycyrrhiza uralensis (Licorice): discovery of the effective components of a traditional herbal medicine, J. Nat. Prod. 79 (2017) 281-292. https://doi.org/10.1021/acs.jnatprod.5b00877.

[22]

T. Deyama, T. Ikawa, S. Nishibe, et al., The constituents of Eucommia ulmoides OLIV. Ⅱ. Isolation and structures of three new lignan glycosides, Chem. Pharm. Bull. 33 (1985) 3651-3657. https://doi.org/10.1248/cpb.33.3651.

[23]

W.X. Sun, X. Li, N. Li, et al., Chemical constituents of the extraction of bamboo leaves from Phyllostachys nigra (Lodd. ex Lindl.) Munro var. henonis (Mitf.) Stepf. ex Rendle, J. Shenyang Pharm. Univ. 25 (2008) 39-43. https://doi.org/10.1631/jzus.B0820047.

[24]

J. Zhang, Y. Wang, X.Q. Zhang, et al., Chemical constituents from the leaves of Lophatherum gracile, Chin. J. Nat. Med. 7 (2010) 428-431. https://doi.org/10.3724/SP.J.1009.2009.00428.

[25]

J. Yang, K.X. Liu, J.M. Qu, et al., The changes induced by cyclophosphamide in intestinal barrier and microflora in mice, Eur. J. Pharmacol. 714 (2013) 120-124. https://doi.org/10.1016/j.ejphar.2013.06.006.

[26]

L. Sun, L. Bao, D. Phurbu, et al., Amelioration of metabolic disorders by a mushroom-derived polyphenols correlates with the reduction of Ruminococcaceae in gut of DIO mice, Food Sci. Hum. Well. 10 (2021) 442-451. https://doi.org/10.1016/j.fshw.2021.04.006.

[27]

Q. Christian, P. Elmar, Y. Pelin, et al., The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nucleic Acids Res. 41 (2012) D590-D596. https://doi.org/10.1093/nar/gks1219.

[28]

R.C. Edgar, MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res. 32 (2004) 1792-1797. https://doi.org/10.2460/ajvr.69.1.82.

[29]

Q. Wang, G.M. Garrity, J.M. Tiedje, et al., Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy, Appl. Environ. Microbiol. 73 (2007) 5261-5267. https://doi.org/10.1128/AEM.00062-07.

[30]

W. Shi, H. Qi, Q. Sun, et al., gcMeta: a global catalogue of metagenomics platform to support the archiving, standardization and analysis of microbiome data, Nucleic Acids Res. 47 (2019) D637-D648. https://doi.org/10.1093/nar/gky1008.

[31]

C. Lapierre, A. Voxeur, S. Boutet, et al., Arabinose conjugates diagnostic of ferulate-ferulate and ferulate-monolignol cross-coupling are released by mild acidolysis of grass cell walls, J. Agri. Food Chem. 67 (2019) 12962-12971. https://doi.org/10.1021/acs.jafc.9b05840.

[32]

H.E. Robert, M.G. Scott, Z.Z. Paul, Metabolic syndrome, Lancet 365 (2005) 1415-1428. https://doi.org/10.1016/S0140-6736(05)66378-7.

[33]

B. Msa, C. Fa, D. Gma et al., Role of polyphenols in combating type 2 diabetes and insulin resistance, Int. J. Biol. Macromol. 206 (2022) 567-579. https://doi.org/10.1016/j.ijbiomac.2022.03.004.

[34]

C.S. Yang, J.S. Zhang, L. Zhang, et al., Mechanisms of body weight reduction and metabolic syndrome alleviation by tea, Mol. Nutr. Food Res. 60 (2016) 160-174. https://doi.org/10.1002/mnfr.201500428.

[35]

C.S. Yang, J. Hong, Prevention of chronic diseases by tea: possible mechanisms and human relevance, Annu. Rev. Nutr. 33 (2013) 161-181. https://doi.org/10.1146/annurev-nutr-071811-150717.

[36]

A. Kashani, A.D. Brejnrod, C. Jin, et al., Impaired glucose metabolism and altered gut microbiome despite calorie restriction of ob/ob mice, Animal Microbiome 1 (2019) 1-16. https://doi.org/10.1186/s42523-019-0007-1.

[37]

C.P. Briscoe, D. Looper, P. Tran, et al., LPS-induced biomarkers in mice: a potential model for identifying insulin sensitizers, Biochem. Bioph. Res. Co. 361 (2007) 140-145. https://doi.org/10.1016/j.bbrc.2007.06.164.

[38]

J.R. Marchesi, D.H. Adams, F. Fava, et al., The gut microbiota and host health, Gut 65 (2015) 330-339. https://doi.org/10.1136/gutjnl-2015-309990.

[39]

J. Zhou, L.L. Tang, C.L. Shen, et al., Green tea polyphenols modify gut-microbiota dependent metabolisms of energy, bile constituents and micronutrients in female sprague-dawley rats, J. Nutr. Biochem. 61 (2018) 68-81. https://doi.org/10.1016/j.jnutbio.2018.07.018.

[40]

T. Chen, A.B. Liu, S. Sun, et al., Green tea polyphenols modify the gut microbiome in db/db mice as co-abundance groups correlating with the blood glucose lowering effect, Mol. Nutr. Food Res. 63 (2019) 1801064. https://doi.org/10.1002/mnfr.201801064.

[41]

J. Tan, C. McKenzie, M. Potamitis, et al., The role of short-chain fatty acids in health and disease, Adv. Immunol. 121 (2014) 91-119. https://doi.org/10.1016/B978-0-12-800100-4.00003-9.

[42]

E.P. Broeders, E.B. Nascimento, B. Havekes, et al., The bile acid chenodeoxycholic acid increases human brown adipose tissue activity, Cell Metab. 22 (2015) 418-426. https://doi.org/10.1016/j.cmet.2015.07.002.

[43]

A. Molinaro, A. Wahlstrom, H.U. Marschall, Role of bile acids in metabolic control, Trends Endocrinol Metab. 29 (2018) 31-41. https://doi.org/10.1016/j.tem.2017.11.002.

[44]

R. Colombo, F.M. Lancas, J.H. Yariwake, et al., Determination of flavonoids in cultivated sugarcane leaves, bagasse, juice and in transgenic sugarcane by liquid chromatography-UV detection, J. Chromatogr. A 1103 (2006) 118-124. https://doi.org/10.1016/j.chroma.2005.11.007.

[45]
C. Sun, Summer-heat relieving flour suitable for eating in summer and preparation method thereof, (2013) CN103349038A.
[46]
S.X. Xu, The invention relates to sugarcane leaves tea beverage and a preparation method thereof, (2012) CN102823677B.
[47]

C.P. Lee, Z.T. Chen, P.Y. Yu, et al., Identification of bioactive compounds and comparison of apoptosis induction of three varieties of sugarcane leaves, J. Funct. Foods 4 (2012) 391-397. https://doi.org/10.1016/j.jff.2012.01.011.

[48]

B.S. Wang, P.D. Duh, S.C. Wu, et al., Effects of the aqueous extract of sugarcane leaves on antimutation and nitric oxide generation, Food Chem. 124 (2010) 495-500. https://doi.org/10.1016/j.foodchem.2010.06.060.

[49]

X.T. Hou, J.G. Deng, A.Y. Li, et al., Study on hypoglycemia activity of the different extracts of sugarcane leaves, West China J. Pharm. Sci. 26 (2011) 451-453. https://doi.org/10.13375/j.cnki.wcjps.2011.05.011.

[50]

X.F. Li, R. Dai, G.H. Li, et al., Anti-platelet aggregation function and acute toxicity of 4-hydroxybenzyl aldehyde(4-HBAL) extracted from Gastrodia elata Blume, Nat. Prod. Res. Dev. 25 (2013) 317-320. https://doi.org/10.16333/j.1001-6880.2013.03.006.

[51]
B. Xiang, S. Liu, Y. Guo, et al., Study of anti-inflammation of p-hydroxybenzaldehyde from Gastrodia elata Blume, Chin. J. Ethnomed. Ethnopharm. 25 (2016) 16-19. https://doi.org/CNKI:SUN:MZMJ.0.2016-09-010.
[52]

A. Abdel-Moneim, A.I. Yousef, S.A. El-Twab, et al., Gallic acid and p-coumaric acid attenuate type 2 diabetes-induced neurodegeneration in rats, Metabolic Brain Disease 32 (2017) 1279-1286. https://doi.org/10.1007/s11011-017-0039-8.

[53]
J.H. Yoon, K. Youn, C.T. Ho, et al., p-Coumaric acid and ursolic acid from Corni Fructus attenuated β-amyloid25–35-induced toxicity through regulation of the NF-κB signaling pathway in PC12 cells, J. Agri. Food Chem. 62 (2014) 4911-6. https://doi.org/10.1021/jf501314g. Epub 2014 May19.
[54]

M. Guven, A.B. Aras, T. Akman, et al., Neuroprotective effect of p-coumaric acid in rat model of embolic cerebral ischemia, Iran. J. Basic Med. Sci. 18 (2015) 356-363.

[55]

S.A. Yoon, K. Seong, S. Hye-Sun, et al., p-Coumaric acid modulates glucose and lipid metabolism via AMP-activated protein kinase in L6 skeletal muscle cells, Biochem. Bioph. Res. Co. 432 (2013) 553-557. https://doi.org/10.1016/j.bbrc.2013.02.067.

[56]

Y.T. Loo, K. Howell, H. Suleria, et al., Sugarcane polyphenol and fiber to affect production of short-chain fatty acids and microbiota composition using in vitro digestion and pig faecal fermentation model, Food Chem. 385 (2022) 132665. https://doi.org/10.1016/j.foodchem.2022.132665.

[57]

P. Paresh, A. Aljada, A. Chaudhuri, et al., Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation, Circulation 111 (2005) 1448-1454. https://doi.org/10.1161/01.CIR.0000158483.13093.9D.

[58]

R. Cancello, K. Clément, Is obesity an inflammatory illness? Role of low-grade inflammation and macrophage infiltration in human white adipose tissue, BJOG 113 (2006) 1141-1147. https://doi.org/10.1111/j.1471-0528.2006.01004.x.

[59]

S.P. Weisberg, D. McCann, M. Desai, et al., Obesity is associated with macrophage accumulation in adipose tissue, J. Clin. Invest. 112 (2003) 1796-1808. https://doi.org/10.1172/JCI19246.

[60]

B. Tva, C. Rn, A. Fa, et al., The metabolic and vascular protective effects of olive (Olea europaea L.) leaf extract in diet-induced obesity in mice are related to the amelioration of gut microbiota dysbiosis and to its immunomodulatory properties, Pharmacol. Res. 150 (2019) 104487. https://doi.org/10.1016/j.phrs.2019.104487.

[61]

D. Berry, B. Stecher, A. Schintlmeister, et al., Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing, P. Natl. Acad. Sci. U.S.A. 110 (2013) 4720-4725. https://doi.org/10.1073/pnas.1219247110.

[62]

D. Berry, E. Mader, T.K. Lee, et al., Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells, P. Natl. Acad. Sci. U.S.A. 112 (2014) 194-203. https://doi.org/10.1073/pnas.1420406112.

[63]

J.Y. Yang, Y.S. Lee, Y. Kim, et al., Gut commensal Bacteroides acidifaciens prevents obesity and improves insulin sensitivity in mice, Mucosal Immunol. 10 (2016) 104-116. https://doi.org/10.1038/mi.2016.42.

[64]

L. Wu, Q. Yan, F. Chen, et al., Bupleuri radix extract ameliorates impaired lipid metabolism in high-fat diet-induced obese mice via gut microbia-mediated regulation of FGF21 signaling pathway, Biomed. Pharmacother. 135 (2021) 111187. https://doi.org/10.1016/j.biopha.2020.111187.

[65]

A. Everard, C. Belzer, L. Geurts, et al., Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity, P. Natl. Acad. Sci. U.S.A. 110 (2013) 9066-9071. https://doi.org/10.1073/pnas.1219451110.

[66]

S.S, Qiao, K. Wang, C. Liu, et al., The enriched gut commensal Faeciroseburia intestinalis contributes to the anti-metabolic disorders effects of the Ganoderma meroterpene derivative, Food Sci. Hum. Well. 11 (2022) 85-96. https://doi.org/10.1016/j.fshw.2021.07.010.

[67]

T. Pols, L.G. Noriega, M. Nomura, et al., The bile acid membrane receptor TGR5: a valuable metabolic target, Digest. Dis. 29 (2011) 37-44. https://doi.org/10.1159/000324126.

[68]

L.A. Velazquez-Villegas, A. Perino, V. Lemos, et al., TGR5 signalling promotes mitochondrial fission and beige remodelling of white adipose tissue, Nat. Commun. 9 (2018) 245. https://doi.org/10.1038/s41467-017-02068-0.

Food Science and Human Wellness
Pages 633-648
Cite this article:
Sun L, Wang T, Chen B, et al. Sugarcane leaves-derived polyphenols alleviate metabolic syndrome and modulate gut microbiota of ob/ob mice. Food Science and Human Wellness, 2024, 13(2): 633-648. https://doi.org/10.26599/FSHW.2022.9250048

2511

Views

554

Downloads

2

Crossref

2

Web of Science

2

Scopus

0

CSCD

Altmetrics

Received: 05 July 2022
Revised: 22 August 2022
Accepted: 21 September 2022
Published: 25 September 2023
© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

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

Return