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
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Food Science and Human Wellness Article
PDF (14.9 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Surfactin alleviated hyperglycaemia in mice with type 2 diabetes induced by a high-fat diet and streptozotocin

Xiaoyu Chena, Hongyuan Zhaoa, Fanqiang Menga, Libang Zhoua, Zhaoxin Lua( ), Yingjian Lub( )
College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
College of Food Science and Engineering, Nanjing University of Finance and Economics, Nanjing 210023, China

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

Show Author Information

Abstract

Type 2 diabetes mellitus (T2DM) is associated with liver dysfunction and intestinal dysbiosis. Bioactive peptides (BAPs) have been reported to ameliorate T2DM by preventing oxidative damage to the liver. Bacillus amyloliquefaciens fmb50 produces the lipopeptide surfactin with a wide range of biological activities. The effects of surfactin on T2DM, on the other hand, have not been studied. In the present study, 80 mg/kg body weight surfactin supplementation lowered fasting blood glucose (FBG) levels by 21.05 % and insulin resistance (IR) by 18.18 % compared with those in the T2DM group, reduced inflammation, and increased antioxidant activity in mice with T2DM induced by a high-fat diet (HFD) and streptozotocin (STZ). According to further research, surfactin administration reduced Firmicutes-to-Bacteroidetes ratios while increasing Bifidobacterium abundance by 20 times and the level of the tight junction protein Occludin by 18.38 % and ZO-1 by 66.60 %. Furthermore, surfactin also improved hepatic glucose metabolism by activating the adenosine monophosphate-activated protein kinase (AMPK) signalling pathway, increasing glycogen synthesis and glucose transporter 2 (GLUT2) protein expression while reducing glucose-6-phosphatase (G6Pase) protein expression. In addition, the increased Bifidobacterium abundance indirectly reduced the liver burden of the metabolic products indole, cresol and amine produced by saprophytic bacteria. All of these findings revealed that surfactin not only ameliorated HFD/STZ-induced gut dysbiosis and preserved intestinal barrier integrity but also enhanced hepatic glucose metabolism and detoxification function in T2DM mice. The gut microbiota appeared to be important in controlling glucose metabolism, IR, fat accumulation, inflammation and antioxidation, according to Spearman’s correlation coefficients. All data indicated that surfactin alleviated hyperglycaemia in mice with T2DM induced by HFD/STZ.

Keywords

Gut microbiotaGlucose metabolismInsulin resistanceSurfactinType 2 diabetes mellitus (T2DM)

References

[1]

G. Wu, Z. Bai, Y. Wan, et al., Antidiabetic effects of polysaccharide from azuki bean (Vigna angularis) in type 2 diabetic rats via insulin/PI3K/Akt signaling pathway, Food Hydrocoll. 101 (2020) 105456. https://doi.org/10.1016/j.foodhyd.2019.105456.
Crossref Google Scholar
[2]

F. Valenzuela Zamudio, M.R. Segura Campos, Amaranth, quinoa and chia bioactive peptides: a comprehensive review on three ancient grains and their potential role in management and prevention of Type 2 diabetes, Crit. Rev. Food Sci. Nutr. 62 (2020) 2707-2721. https://doi.org/10.1080/10408398.2020.1857683.
Crossref Google Scholar
[3]

P. Saeedi, I. Petersohn, P. Salpea, et al., IDF Diabetes Atlas Committee 1. global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation Diabetes Atlas, Diabetes. Res. Clin. Pr. 157 (2019) 107843. https://doi.org/10.1016/j.diabres.2019.107843.
Crossref Google Scholar
[4]
International Diabetes Federation, IDF Diabetes Atlas 8th Edition, http://www.diabetesatlas.org.
[5]

American Diabetes Association, Classification and diagnosis of diabetes: standards of medical care in diabetes-2020, Diabetes Care 43 (2020) S14-S31. https://doi.org/10.2337/dc20-S002.
Crossref Google Scholar
[6]

S.C. Palmer, D. Mavridis, A. Nicolucci, et al., Comparison of clinical outcomes and adverse events associated with glucose-lowering drugs in patients with type 2 diabetes: a meta-analysis, JAMA 316 (2016) 313-324. https://doi.org/10.1001/jama.2016.9400.
Crossref Google Scholar
[7]

D.P. Monjiote, E.E.M. Leo, M.R.S. Campos, Functional and biological potential of bioactive compounds in foods for the dietary treatment of type 2 diabetes mellitus, in: M.C. Tecnalia (Ed.), Functional food: improve health through adequate food, 2017. https://doi.org/10.5772/intechopen.68788.
Crossref Google Scholar
[8]

C. Wang, L. Zheng, G. Su, et al., Evaluation and exploration of potentially bioactive peptides in casein hydrolysates against liver oxidative damage in STZ/HFD-induced diabetic rats, J. Agr. Food Chem. 68 (2020) 2393-2405. https://doi.org/10.1021/acs.jafc.9b07687.
Crossref Google Scholar
[9]

M.K. Salgaço, L.G.S. Oliveira, G.N. Costa, et al., Relationship between gut microbiota, probiotics, and type 2 diabetes mellitus, Appl. Biochem. Biotechnol. 103 (2019) 9229-9238. https://doi.org/1007/s00253-019-10156-y.
Crossref Google Scholar
[10]
V. Chauhan, S.S. Kanwar, Bioactive peptides: synthesis, functions and biotechnological applications, in: M.L. Verma, A.K. Chandel (Ed.), biotechnological production of bioactive Compounds, Elsevier, 2020. https://doi.org/10.1016/B978-0-444-64323-0.00004-7.
Crossref
[11]

E.B.M. Daliri, D.H. Oh, B.H. Lee, Bioactive peptides, Foods 6 (2017) 32. https://doi.org/10.3390/foods6050032.
Crossref Google Scholar
[12]

R. Zouari, A.K. Ben, K. Hamden, et al., Assessment of the antidiabetic and antilipidemic properties of Bacillus subtilis SPB1 biosurfactant in alloxan-induced diabetic rats, Pept. Sci. 104 (2015) 764-774. https://doi.org/10.1002/bip.22705.
Crossref Google Scholar
[13]

Z.Q. Gao, X.Y. Zhao, T. Yang, et al., Immunomodulation therapy of diabetes by oral administration of a surfactin lipopeptide in NOD mice, Vaccine 32 (2014) 6812-6819. https://doi.org/10.1016/j.vaccine.2014.08.082.
Crossref Google Scholar
[14]

Y. Wang, J.H. Tian, F.F. Shi, et al., Protective effect of surfactin against copper sulfate-induced inflammation, oxidative stress and hepatic injury in zebrafish, Microbiol. Immunol. 65 (2021) 410-421. https://doi.org/10.1111/1348-0421.12924.10.
Crossref Google Scholar
[15]

X.Y. Chen, H.Y. Zhao, F.Q. Meng, et al., Ameliorated effects of a lipopeptide surfactin on insulin resistance in vitro and in vivo, Food Sci. Nutr. 10 (2022) 2455-2469. https://doi.org/10.1002/fsn3.2852.
Crossref Google Scholar
[16]

C. Sivapathasekaran, P. Das, S. Mukherjee, et al., Marine bacterium derived lipopeptides: characterization and cytotoxic activity against cancer cell lines, Int. J. Pept. Res. T. 16 (2010) 215-222. https://doi.org/10.1007/s10989-010-9212-1.
Crossref Google Scholar
[17]

X.H. Cao, Z.Y. Liao, C.L. Wang, et al., Evaluation of a lipopeptide biosurfactant from Bacillus natto TK-1 as a potential source of anti-adhesive, antimicrobial and antitumor activities, Braz. J. Microbiol. 40 (2009) 373-379. https://doi.org/10.1590/s1517-838220090002000030.
Crossref Google Scholar
[18]

Y.H. Hwang, M.S. Kim, I.B. Song, et al., Subacute (28 day) toxicity of surfactin C, a lipopeptide produced by Bacillus subtilis, in rats, J. Health Sci. 55 (2009) 351-355. https://doi.org/10.1248/jhs.55.351.
Crossref Google Scholar
[19]

L.J. Sun, Y.L. Wang, H.M. Liu, et al., Hemolytic and mice acute oral toxicity evaluation of a new antimicrobial peptide APNT-6, Journal of Fisheries of China 36 (2012) 974-978. https://doi.org/10.3724/SP.J.1231.2012.27759.
Crossref Google Scholar
[20]

S. Chakrabarti, S. Guha, K. Majumder, Food-derived bioactive peptides in human health: challenges and opportunities, Nutrients 10 (2018) 1738. https://doi.org/10.3390/nu10111738.
Crossref Google Scholar
[21]

X.Y. Chen, H.Y. Zhao, Z.X. Lu, Research progress in biosynthesis and application of surfactin, Journal of Nanjing Agricultural University 44 (2021) 1024-1034. https://doi.org/10.7685/jnau.202012015.
Crossref Google Scholar
[22]

X.Y. Chen, Y.J. Lu, M.Y. Shan, et al., A mini-review: mechanism of antimicrobial action and application of surfactin, World J. Microb. and Biot. 38 (2022) 143. https://doi.org/10.1007/s11274-022-03323-3.
Crossref Google Scholar
[23]

J.F. Zhao, Y.H. Li, C. Zhang, et al., Genome shuffling of Bacillus amyloliquefaciens for improving antimicrobial lipopeptide production and an analysis of relative gene expression using FQ RT-PCR, J. Ind. Microbiol. Biot. 39 (2012) 889-896. https://doi.org/10.1007/s10295-012-1098-9.
Crossref Google Scholar
[24]

D.L. Zhang, Y.F. Wang, Y.J. Lu, et al., An efficient method for separation of surfactin from Bacillus amyloliquefaciens fmb50 broth by flocculation, Proces. Biochem. 49 (2014) 1182-1188. https://doi.org/10.1016/j.procbio.2014.03.021.
Crossref Google Scholar
[25]

S.L. Yao, S.M. Zhao, Z.X. Lu, et al., Control of agitation and aeration rates in the production of surfactin in foam overflowing fed-batch culture with industrial fermentation, Rev. Argent. Microbiol. 47 (2015) 344-349. https://doi.org/10.1016/j.ram.2015.09.003.
Crossref Google Scholar
[26]
Z.X. Lu, W. Tang, F.X. Lv, et al., A production method of biosurfactant, China, Jiangsu Province: CN105695543B, 2019-06-04.
[27]

C. Dai, F.F. Guo, Z.X. Lu, et al., Emulsifying properties of lipopeptide biosurfactant surfactin, Food Sci. 36 (2015) 40-44. https://doi.org/10.7506/spkx1002-6630-201515009.
Crossref Google Scholar
[28]

X.Y. Lv, J. Li, M. Zhang, et al., Enhancement of sodium caprate on intestine absorption and antidiabetic action of berberine, AAPS Pharmscitech. 11 (2010) 372-382. https://doi.org/10.1208/s12249-010-9386-z.
Crossref Google Scholar
[29]

J.L. Hu, S.P. Nie, C. Li, et al., In vitro fermentation of polysaccharide from the seeds of Plantago asiatica L. by human fecal microbiota, Food Hydrocoll. 33 (2013) 384-392. https://doi.org/10.1016/j.foodhyd.2013.04.006.
Crossref Google Scholar
[30]

R. Xie, P. Jiang, L. Lin, et al., Oral treatment with Lactobacillus reuteri attenuates depressive-like behaviors and serotonin metabolism alterations induced by chronic social defeat stress, J. Psychiatr. Res. 122 (2020) 70-78. https://doi.org/10.1016/j.jpsychires.2019.12.013.
Crossref Google Scholar
[31]

J.J. Wu, Y.B. Xu, J. Su, et al., Roles of gut microbiota and metabolites in a homogalacturonan-type pectic polysaccharide from Ficus pumila Linn. fruits mediated amelioration of obesity, Carbohyd. Polym. 248 (2020) 116780. https://doi.org/10.1016/j.carbpol.2020.116780.
Crossref Google Scholar
[32]

X.L. Wang, Z.M. Yang, X. Xu, et al., Odd-numbered agaro-oligosaccharides alleviate type 2 diabetes mellitus and related colonic microbiota dysbiosis in mice, Carbohyd. Polym. 240 (2020) 116261. https://doi.org/10.1016/j.carbpol.2020.116261.
Crossref Google Scholar
[33]

J.N. Sun, X.Y. Yu, B. Hou, et al., Vaccarin enhances intestinal barrier function in type 2 diabetic mice, Eur. J. Pharmacol. 908 (2021) 174375. https://doi.org/10.1016/J.EJPHAR.2021.174375.
Crossref Google Scholar
[34]

S. Wu, J. Zuo, Y. Cheng, et al., Ethanol extract of Sargarsum fusiforme alleviates HFD/STZ-induced hyperglycemia in association with modulation of gut microbiota and intestinal metabolites in type 2 diabetic mice, Food Res. Int. 147 (2021) 110550. https://doi.org/10.1016/j.foodres.2021.110550.
Crossref Google Scholar
[35]

Z.Q. Chen, W.W. Li, Q.W. Guo, et al., Anthocyanins from dietary black soybean potentiate glucose uptake in L6 rat skeletal muscle cells via up-regulating phosphorylated Akt and GLUT4, J. Funct. Foods 52 (2019) 663-669. https://doi.org/10.1016/j.jff.2018.11.049.
Crossref Google Scholar
[36]

J. Yin, A. Zuberi, Z.G. Gao, et al., Shilianhua extract inhibits GSK-3beta and promotes glucose metabolism, American Journal of Physiology. Endocrinology and Metabolism 294 (2009) E148-E156. https://doi.org/10.1152/ajpendo.00092.2009.
Crossref Google Scholar
[37]

J.R. Hall, C.E. Short, W.R. Driedzic, Sequence of Atlantic cod (Gadus morhua) GLUT4, GLUT2 and GPDH: developmental stage expression, tissue expression and relationship to starvation-induced changes in blood glucose, J. Exp. Biol. 209 (2006) 4490-4502. https://doi.org/10.1242/jeb.02532.
Crossref Google Scholar
[38]

M. Mueckler, B. Thorens, The SLC2 (GLUT) family of membrane transporters, Mol. Aspects. Med. 34 (2013) 121-138. https://doi.org/10.1016/j.mam.2012.07.001.
Crossref Google Scholar
[39]

H. Sun, S. Ling, D. Zhao, et al., Panax quinquefolium saponin attenuates cardiac remodeling induced by simulated microgravity. Phytomedicine 56 (2019) 83-93. https://doi.org/10.1016/j.phymed.2018.08.007.
Crossref Google Scholar
[40]

Z.H. Ren, Z.F. Xie, D.N. Cao, et al., C-Phycocyanin inhibits hepatic gluconeogenesis and increases glycogen synthesis via activating Akt and AMPK in insulin resistance hepatocytes, Food Funct. 95 (2018) 2829-2939. https://doi.org/10.1039/c8fo00257f.
Crossref Google Scholar
[41]

X. Wei, B. Yang, X. Chen, et al., Zanthoxylum alkylamides ameliorate protein metabolism in type 2 diabetes mellitus rats by regulating multiple signaling pathways, Food Funct. 12 (2021) 3740-3753. https://doi.org/10.1039/d0fo02695f.
Crossref Google Scholar
[42]

H.S. Liu, X.Y. Qi, K.K. Yu, et al., AMPK activation is involved in hypoglycemic and hypolipidemic activities of mogroside-rich extract from Siraitia grosvenorii (Swingle) fruits on high-fat diet/streptozotocin-induced diabetic mice, Food Funct. 10 (2019) 151-162. https://doi.org/10.1039/c8fo01486h.
Crossref Google Scholar
[43]

A.C. Archer, S.P. Muthukumar, P.M. Halami, Lactobacillus fermentum MCC2759 and MCC2760 alleviate inflammation and intestinal function in high-fat diet-fed and streptozotocin-induced diabetic rats, Probiotics. Antimicro. 13 (2021) 1-13. https://doi.org/10.1007/S12602-021-09744-0.
Crossref Google Scholar
[44]

L.X. Gong, T.T. Wen, J. Wang, Role of the microbiome in mediating health effects of dietary components, J. Agri. Food Chem. 68 (2020) 12820-12835. https://doi.org/10.1021/acs.jafc.9b08231.
Crossref Google Scholar
[45]

Y.L. Zhang, T. Wu, W. Li, et al., Lactobacillus casei LC89 exerts antidiabetic effects through regulating hepatic glucagon response and gut microbiota in type 2 diabetic mice, Food Funct. 12 (2021) 8288-8299. https://doi.org/10.1039/D1FO00882J.
Crossref Google Scholar
[46]

S.S. Qiao, L. Bao, K. Wang, et al. Activation of a specific gut Bacteroides-folate-liver axis benefits for the alleviation of nonalcoholic hepatic steatosis, Cell Rep. 32 (2020) 108005. https://doi.org/10.1016/j.celrep.2020.108005.
Crossref Google Scholar
[47]

A.M. El-Baz, A.E. Khodir, M.M. El-Sokkary, et al., The protective effect of Lactobacillus versus 5-aminosalicylic acid in ulcerative colitis model by modulation of gut microbiota and Nrf2/Ho-1 pathway, Life. Sci. 256 (2020) 117027. https://doi.org/10.1016/j.lfs.2020.117927.
Crossref Google Scholar
[48]

A. Gopal, Bile tolerance, taurocholate deconjugation cholesterol removal by Lactobacillus acidophilus and Bifidobacterium spp., Milchwissenschaft-Milk Science International 51 (1996) 619-623.
Google Scholar
[49]

A.M. El-Baz, A. Shata, H.M. Hassan, et al., The therapeutic role of Lactobacillus and montelukast in combination with metformin in diabetes mellitus complications through modulation of gut microbiota and suppression of oxidative stress, Int. Immunopharm. 96 (2021) 107757. https://doi.org/10.1016/J.INTIMP.2021.107757.
Crossref Google Scholar
[50]

G.M. Barlow, A. Yu, R. Mathur. Role of the gut microbiome in obesity and diabetes mellitus, Nutr. Clin. Pract. 30 (2015) 787-797. https://doi.org/10.1177/0884533615609896.
Crossref Google Scholar
[51]

Y. Yamaguchi, K. Adachi, T. Sugiyama, et al., Association of intestinal microbiota with metabolic markers and dietary habits in patients with Type 2 diabetes, Digestion 94 (2016) 66-72. https://doi.org/10.1159/000447690.
Crossref Google Scholar
[52]

S.M. Jeon, Regulation and function of AMPK in physiology and diseases, Exp. Mol. Med. 48 (2016) e245. https://doi.org/10.1038/emm.2016.81.
Crossref Google Scholar
[53]

K. Sabbir, J. Gopabandhu, The role of butyrate, a histone deacetylase inhibitor in diabetes mellitus: experimental evidence for therapeutic intervention, Epigenomics 7 (2015) 669-680. https://doi.org/10.2217/epi.15.20.
Crossref Google Scholar
[54]

N.M. Delzenne, P.D. Cani, A. Everard, et al., Gut microorganisms as promising targets for the management of type 2 diabetes, Diabetologia 58 (2015) 2206-2217. https://doi.org/10.1007/s00125-015-3712-7.
Crossref Google Scholar
[55]

S. Shoji, Y. Toshimasa, O. Yoshifumi, et al., Acetic acid activates hepatic AMPK and reduces hyperglycemia in diabetic KK-A(y) mice, Biochem. Bioph. Res. Co. 344 (2006) 597-604. https://doi.org/10.1016/j.bbrc.2006.03.176.
Crossref Google Scholar
[56]

K. Yazawa, N. Suegara, Y. Kawai, Intestinal microflora and aging: age-related change of enzymes in the liver and the small intestine of germ-free and conventional rats, Mech. Ageing and Dev. 17 (1981) 173-182. https://doi.org/10.1016/0047-6374(81)90083-X.
Crossref Google Scholar
[57]

F. He, A.C. Ouwehand, H. Hashimoto, et al., Adhesion of Bifidobacterium spp. to human intestinal mucus, Microbiol. Immunol. 45 (2001) 259-262. https://doi.org/10.1111/j.1348-0421.2001.tb02615.x.
Crossref Google Scholar
[58]

J.P. Zheng, X.B. Yuan, G. Cheng, et al., Chitosan oligosaccharides improve the disturbance in glucose metabolism and reverse the dysbiosis of gut microbiota in diabetic mice, Carbohyd. Polym. 190 (2018) 77-86. https://doi.org/10.1016/j.carbpol.2018.02.058.
Crossref Google Scholar
[59]

I.S. Larsen, B.A. Jensen, E. Bonazzi, et al., Fungal lysozyme leverages the gut microbiota to curb DSS-induced colitis, Gut Microbes. 13 (2021) 1988836. https://doi.org/10.1080/19490976.2021.1988836.
Crossref Google Scholar
[60]

P.D. Cani, Human gut microbiome: hopes, threats and promises, Gut 67 (2018) 1716-1725. https://doi.org/10.1136/gutjnl-2018-316723.
Crossref Google Scholar
[61]

A. Ghafouri, G. Hajiluian, S.J. Karegar, et al., The effect of Aqueous, Ethanolic extracts of Rheum ribeson insulin sensitivity, inflammation, oxidative stress in patients with type 2 diabetes mellitus: a randomized, double-blind, placebo-controlled trial, J. Herb. Med. 24 (2021) 100389. https://doi.org/10.1016/J.HERMED.2020.100389.
Crossref Google Scholar
Food Science and Human Wellness
Volume 12 Issue 6,
November 2023
Pages 2095-2110
DOI: 10.1016/j.fshw.2023.03.012
Cite this article:
Chen X, Zhao H, Meng F, et al. Surfactin alleviated hyperglycaemia in mice with type 2 diabetes induced by a high-fat diet and streptozotocin. Food Science and Human Wellness, 2023, 12(6): 2095-2110. https://doi.org/10.1016/j.fshw.2023.03.012

582

Views

34

Downloads

10

Crossref

8

Web of Science

8

Scopus

0

CSCD

Altmetrics
Received: 20 February 2022
Revised: 10 March 2022
Accepted: 23 March 2022
Published: 04 April 2023
© 2023 Beijing Academy of Food Sciences.

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