Journal Home > Volume 12 , Issue 6

Theasinensin A (TSA), a dimer of epigallocatechin gallate, has been preliminarily demonstrated to have hypoglycemia and anti-inflammatory effects. However, little information is available on its potential mechanisms of anti-diabetes. Therefore, the present study aimed to investigate the influence of TSA on glucose and lipid metabolism and gut microbiota in high-fat-diet/streptozotocin-induced diabetic mice. As result, TSA improved polydipsia, polyphagia and impaired glucose tolerance of diabetic mice, declined the fasting blood glucose and hepatic triglyceride level, and enhanced the expression at mRNA level of insulin receptor substrate, phosphoinositide 3-kinase, protein kinase B and glucagon-like peptide 1 receptor (GLP-1R) in the diabetic liver. Moreover, TSA could restore the disorder of gut microbiota of diabetic mice. High-dose (100 mg/kg) TSA showed better beneficial effects from the blood biochemical parameters, hepatic function and gut microbiota. In general, high-dose TSA significantly modulated gut microbiota by increasing the relative abundance of Akkermansia and decreasing the relative abundances of Acetatifactor, Anaerotruncus, Pseudoflavonifactor, Oscillibacter and Clostridium clusters. The results indicated that TSA could exert an anti-diabetes effect in diabetic mice through restoring glucose homeostasis, declining hepatic steatosis, activating insulin and GLP-1 signaling pathways, and ameliorating gut microbiota dysbiosis.


menu
Abstract
Full text
Outline
About this article

Theasinensin A attenuated diabetic development by restoring glucose homeostasis, improving hepatic steatosis and modulating gut microbiota in high-fat-diet/streptozotocin-induced diabetic mice

Show Author's information Weiqi XuaYujie HuangaWangting ZhouaYujia PengaXuhui KanaWei DongaGuijie ChenaXiaoxiong Zenga( )Zhonghua Liub,c( )
College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
Key Laboratory of Ministry of Education for Tea Science, Hunan Agricultural University, Changsha 410128, China
National Research Center of Engineering Technology for Utilization of Botanical Functional Ingredients, Changsha 410128, China

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

Abstract

Theasinensin A (TSA), a dimer of epigallocatechin gallate, has been preliminarily demonstrated to have hypoglycemia and anti-inflammatory effects. However, little information is available on its potential mechanisms of anti-diabetes. Therefore, the present study aimed to investigate the influence of TSA on glucose and lipid metabolism and gut microbiota in high-fat-diet/streptozotocin-induced diabetic mice. As result, TSA improved polydipsia, polyphagia and impaired glucose tolerance of diabetic mice, declined the fasting blood glucose and hepatic triglyceride level, and enhanced the expression at mRNA level of insulin receptor substrate, phosphoinositide 3-kinase, protein kinase B and glucagon-like peptide 1 receptor (GLP-1R) in the diabetic liver. Moreover, TSA could restore the disorder of gut microbiota of diabetic mice. High-dose (100 mg/kg) TSA showed better beneficial effects from the blood biochemical parameters, hepatic function and gut microbiota. In general, high-dose TSA significantly modulated gut microbiota by increasing the relative abundance of Akkermansia and decreasing the relative abundances of Acetatifactor, Anaerotruncus, Pseudoflavonifactor, Oscillibacter and Clostridium clusters. The results indicated that TSA could exert an anti-diabetes effect in diabetic mice through restoring glucose homeostasis, declining hepatic steatosis, activating insulin and GLP-1 signaling pathways, and ameliorating gut microbiota dysbiosis.

Keywords: Gut microbiota, Diabetes, Tea, Glucose homeostasis, Hepatic steatosis, Theasinensin A

References(87)

[1]

P. Saeedi, I. Petersohn, P. Salpea, et al., Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation Diabetes Atlas, 9th edition, Diabetes Res. Clin. Pract. 157 (2019) 107843. http://doi.org/10.1016/j.diabres.2019.107843.

[2]

R.A. DeFronzo, E. Ferrannini, L. Groop, et al., Type 2 diabetes mellitus, Nat. Rev. Dis. Primers 1 (2015) 15019. http://doi.org/10.1038/nrdp.2015.19.

[3]

N. Kietsiriroje, S. Pearson, M. Campbell, et al., Double diabetes: a distinct high-risk group?, Diabetes Obes. Metab. 21 (2019) 2609-2618. http://doi.org/10.1111/dom.13848.

[4]

M. Roden, G.I. Shulman, The integrative biology of type 2 diabetes, Nature 576 (2019) 51-60. http://doi.org/10.1038/s41586-019-1797-8.

[5]

F.M. Gribble, F. Reimann, Metabolic messengers: glucagon-like peptide 1, Nat. Metab. 3 (2021) 142-148. http://doi.org/10.1038/s42255-020-00327-x.

[6]

D.J. Drucker, Mechanisms of action and therapeutic application of glucagon-like peptide-1, Cell Metab. 27 (2018) 740-756. http://doi.org/10.1016/j.cmet.2018.03.001.

[7]

M.S. Abd El Aziz, M. Kahle, J.J. Meier, et al., A meta-analysis comparing clinical effects of short- or long-acting GLP-1 receptor agonists versus insulin treatment from head-to-head studies in type 2 diabetic patients, Diabetes Obes. Metab. 19 (2017) 216-227. http://doi.org/10.1111/dom.12804.

[8]

J. Rosenstock, A. Nino, J. Soffer, et al., Impact of a weekly glucagon-like peptide 1 receptor agonist, albiglutide, on glycemic control and on reducing prandial insulin use in type 2 diabetes inadequately controlled on multiple insulin therapy: a randomized trial, Diabetes Care 43 (2020) 2509-2518. http://doi.org/10.2337/dc19-2316.

[9]

M.S. Desai, A.M. Seekatz, N.M. Koropatkin, et al., A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility, Cell 167 (2016) 1339-1353. http://doi.org/10.1016/j.cell.2016.10.043.

[10]

J.L. Sonnenburg, F. Bäckhed, Diet-microbiota interactions as moderators of human metabolism, Nature 535 (2016) 56-64. http://doi.org/10.1038/nature18846.

[11]

Y. Fan, O. Pedersen, Gut microbiota in human metabolic health and disease, Nat. Rev. Microbiol. 19 (2021) 55-71. http://doi.org/10.1038/s41579-020-0433-9.

[12]

C. Chevalier, O. Stojanović, D.J. Colin, et al., Gut microbiota orchestrates energy homeostasis during Cold, Cell 163 (2015) 1360-1374. http://doi.org/10.1016/j.cell.2015.11.004.

[13]

S.V. Lynch, O. Pedersen, The human intestinal microbiome in health and disease, N. Engl. J. Med. 375 (2016) 2369-2379. http://doi.org/10.1056/NEJMra1600266.

[14]

K.H. Allin, V. Tremaroli, R. Caesar, et al., Aberrant intestinal microbiota in individuals with prediabetes, Diabetologia 61 (2018) 810-820. http://doi.org/10.1007/s00125-018-4550-1.

[15]

H. Zhong, H. Ren, Y. Lu, et al., Distinct gut metagenomics and metaproteomics signatures in prediabetics and treatment-naïve type 2 diabetics, Ebiomedicine 47 (2019) 373-383. http://doi.org/10.1016/j.ebiom.2019.08.048.

[16]

L.A. David, C.F. Maurice, R.N. Carmody, et al., Diet rapidly and reproducibly alters the human gut microbiome, Nature 505 (2014) 559-563. http://doi.org/10.1038/nature12820.

[17]

J. Zhu, M. Wu, H. Zhou, et al., Liubao brick tea activates the PI3K-Akt signaling pathway to lower blood glucose, metabolic disorders and insulin resistance via altering the intestinal flora, Food Res. Int. 148 (2021) 110594. http://doi.org/10.1016/j.foodres.2021.110594.

[18]

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) e1801064. http://doi.org/10.1002/mnfr.201801064.

[19]

G. Nonaka, O. Kawahara, I. Nishioka, Tannins and related compounds. XV. a new class of dimeric flavan-3-ol gallates, theasinensins A and B, and proanthocyanidin gallates from green tea leaf, Chem. Pharm. Bull. 31 (1983) 3906-3914. https://doi.org/10.1248/cpb.31.3906.

[20]

T. Tanaka, C. Mine, S. Watarumi, et al., Accumulation of epigallocatechin quinone dimers during tea fermentation and formation of theasinensins, J. Nat. Prod. 65 (2002) 1582-1587. http://doi.org/10.1021/np020245k.

[21]

T. Tanaka, S. Watarumi, Y. Matsuo, et al., Production of theasinensins A and D, epigallocatechin gallate dimers of black tea, by oxidation-reduction dismutation of dehydrotheasinensin A, Tetrahedron 59 (2003) 7939-7947. http://doi.org/10.1016/j.tet.2003.08.025.

[22]

Z. Liu, W.J.C. de Bruijn, M.G. Sanders, et al., Insights in the recalcitrance of theasinensin A to human gut microbial degradation, J. Agric. Food Chem. 69 (2021) 2477-2484. http://doi.org/10.1021/acs.jafc.1c00727.

[23]

Z. Liu, W.J.C. de Bruijn, M.E. Bruins, et al., Microbial metabolism of theaflavin-3, 3'-digallate and its gut microbiota composition modulatory effects, J. Agric. Food Chem. 69 (2021) 232-245. http://doi.org/10.1021/acs.jafc.0c06622.

[24]

Q. Yang, X. Wei, Y. Fang, et al., Nanochemoprevention with therapeutic benefits: an updated review focused on epigallocatechin gallate delivery, Crit. Rev. Food Sci. Nutr. 60 (2020) 1243-1264. http://doi.org/10.1080/10408398.2019.1565490.

[25]

M. Weerawatanakorn, W. Hung, M. Pan, et al., Chemistry and health beneficial effects of oolong tea and theasinensins, Food Sci. Human Wellness 4 (2015) 133-146. http://doi.org/10.1016/j.fshw.2015.10.002.

[26]

Y. Miyata, S. Tamaru, T. Tanaka, et al., Theflavins and theasinensin A derived from fermented tea have antihyperglycemic and hypotriacylglycerolemic effects in KK-Ay mice and Sprague-Dawley rats, J. Agric. Food Chem. 61 (2013) 9366-9372. http://doi.org/10.1021/jf400123y.

[27]

T. Shii, M. Miyamoto, Y. Matsuo, et al., Biomimetic one-pot preparation of a black tea polyphenol theasinensin A from epigallocatechin gallate by treatment with copper(II) chloride and ascorbic acid, Chem. Pharm. Bull. 59 (2011) 1183-1185. http://doi.org/10.1248/cpb.59.1183.

[28]

S. Tao, G. Chen, W. Xu, et al., Preparation of theasinensin A and theasinensin B and exploration of their inhibitory mechanism on α-glucosidase, Food Funct. 11 (2020) 3527-3538. http://doi.org/10.1039/c9fo03054a.

[29]

C. Lin, J. Wu, J. Jian, et al., (−)-Epicatechin-3-O-β-D-allopyranoside from davallia formosana prevents diabetes and dyslipidemia in streptozotocin-induced diabetic mice, PLoS One 12 (2017) e0173984. http://doi.org/10.1371/journal.pone.0173984.

[30]

S. Neschen, M. Scheerer, A. Seelig, et al., Metformin supports the antidiabetic effect of a sodium glucose cotransporter 2 inhibitor by suppressing endogenous glucose production in diabetic mice, Diabetes 64 (2015) 284-290. http://doi.org/10.2337/db14-0393.

[31]
Food Drug Administration. Guidance for industry: estimating the maximum safe starting dose in initial clinical trials for therapeutics in adult healthy volunteers, 2005. https://www.fda.gov/media/72309/download.
[32]

Y. Peng, Y. Yan, P. Wan, et al., Gut microbiota modulation and anti-inflammatory 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://doi.org/10.1016/j.freeradbiomed.2019.04.005.

[33]

Y. Cao, S. Zou, H. Xu, et al., Hypoglycemic activity of the baker's yeast β-glucan in obese/type 2 diabetic mice and the underlying mechanism, Mol. Nutr. Food Res. 60 (2016) 2678-2690. http://doi.org/10.1002/mnfr.201600032.

[34]

S.M. Poucher, S. Cheetham, J. Francis, et al., Effects of saxagliptin and sitagliptin on glycaemic control and pancreatic β-cell mass in a streptozotocin-induced mouse model of type 2 diabetes, Diabetes Obes. Metab. 14 (2012) 918-926. http://doi.org/10.1111/j.1463-1326.2012.01619.x.

[35]

J. Luo, J. Quan, J. Tsai, et al., Nongenetic mouse models of non-insulin-dependent diabetes mellitus, Metabolism 47 (1998) 663-668. http://doi.org/10.1016/s0026-0495(98)90027-0.

[36]

A.M. McKillop, B.M. Moran, Y.H. Abdel-Wahab, et al., Metabolic effects of orally administered small-molecule agonists of GPR55 and GPR119 in multiple low-dose streptozotocin-induced diabetic and incretin-receptor-knockout mice, Diabetologia 59 (2016) 2674-2685. http://doi.org/10.1007/s00125-016-4108-z.

[37]

Y. Kupriyanova, O.P. Zaharia, P. Bobrov, et al., Early changes in hepatic energy metabolism and lipid content in recent-onset type 1 and 2 diabetes mellitus, J. Hepatol. 74 (2021) 1028-1037. http://doi.org/10.1016/j.jhep.2020.11.030.

[38]

B. Teupe, K. Bergis, Epidemiological evidence for "double diabetes", Lancet 337 (1991) 361-362. http://doi.org/10.1016/0140-6736(91)90988-2.

[39]

S.J. Cleland, Cardiovascular risk in double diabetes mellitus--when two worlds collide, Nat. Rev. Endocrinol. 8 (2012) 476-485. http://doi.org/10.1038/nrendo.2012.47.

[40]

W.L. Hung, G. Yang, Y.C. Wang, et al., Protective effects of theasinensin A against carbon tetrachloride-induced liver injury in mice, Food Funct. 8 (2017) 3276-3287. http://doi.org/10.1039/c7fo00700k.

[41]

Y. Yamashita, L. Wang, Z. Tinshun, et al., Fermented tea improves glucose intolerance in mice by enhancing translocation of glucose transporter 4 in skeletal muscle, J. Agric. Food Chem. 60 (2012) 11366-11371. http://doi.org/10.1021/jf303597c.

[42]

J. Qiu, Y. Kitamura, Y. Miyata, et al., Transepithelial transport of theasinensins through Caco-2 cell monolayers and their absorption in sprague-dawley rats after oral administration, J. Agric. Food Chem. 60 (2012) 8036-8043. http://doi.org/10.1021/jf302242n.

[43]

C.N. Lumeng, A.R. Saltiel, Inflammatory links between obesity and metabolic disease, J. Clin. Invest. 121 (2011) 2111-2117. http://doi.org/10.1172/JCI57132.

[44]

S. Nishimura, I. Manabe, M. Nagasaki, et al., CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity, Nat. Med. 15 (2009) 914-920. http://doi.org/10.1038/nm.1964.

[45]

G.S. Hotamisligil, N.S. Shargill, B.M. Spiegelman, Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance, Science 259 (1993) 87-91. http://doi.org/10.1126/science.7678183.

[46]

A.D. Pradhan, J.E. Manson, N. Rifai, et al., C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus, J. Am. Med. Assoc. 286 (2001) 327-334. http://doi.org/10.1001/jama.286.3.327.

[47]

X. Wang, W. Bao, J. Liu, et al., Inflammatory markers and risk of type 2 diabetes: a systematic review and meta-analysis, Diabetes Care 36 (2012) 166-175. http://doi.org/10.2337/dc12-0702.

[48]

F. Magkos, X. Su, D. Bradley, et al., Intrahepatic diacylglycerol content is associated with hepatic insulin resistance in obese subjects, Gastroenterology 142 (2012) 1444-1446. http://doi.org/10.1053/j.gastro.2012.03.003.

[49]

P.K. Luukkonen, Y. Zhou, S. Sadevirta, et al., Hepatic ceramides dissociate steatosis and insulin resistance in patients with non-alcoholic fatty liver disease, J. Hepatol. 64 (2016) 1167-1175. http://doi.org/10.1016/j.jhep.2016.01.002.

[50]

J. Mauer, B. Chaurasia, L. Plum, et al., Myeloid cell-restricted insulin receptor deficiency protects against obesity-induced inflammation and systemic insulin resistance, PLoS Genet. 6 (2010) e1000938. http://doi.org/10.1371/journal.pgen.1000938.

[51]

H. Shi, M.V. Kokoeva, K. Inouye, et al., TLR4 links innate immunity and fatty acid-induced insulin resistance, J. Clin. Invest. 116 (2006) 3015-3025. http://doi.org/10.1172/JCI28898.

[52]

N.A. Gupta, J. Mells, R.M. Dunham, et al., Glucagon-like peptide-1 receptor is present on human hepatocytes and has a direct role in decreasing hepatic steatosis in vitro by modulating elements of the insulin signaling pathway, Hepatology 51 (2010) 1584-1592. http://doi.org/10.1002/hep.23569.

[53]

D. Zhou, Y. Chen, Z. Zhao, et al., Sodium butyrate reduces high-fat diet-induced non-alcoholic steatohepatitis through upregulation of hepatic GLP-1R expression, Exp. Mol. Med. 50 (2018) 1-12. http://doi.org/10.1038/s12276-018-0183-1.

[54]

R.A. Saleh, T.F. Eissa, D.M. Abdallah, et al., Peganum harmala enhanced GLP-1 and restored insulin signaling to alleviate AlCl3-induced alzheimer-like pathology model, Sci. Rep. 11 (2021) 12040. http://doi.org/10.1038/s41598-021-90545-4.

[55]

A. Chadt, H. Al-Hasani, Glucose transporters in adipose tissue, liver, and skeletal muscle in metabolic health and disease, Pflugers Arch. 472 (2020) 1273-1298. http://doi.org/10.1007/s00424-020-02417-x.

[56]

J. Qiu, Y. Kitamura, Y. Miyata, et al., Transepithelial transport of theasinensins through Caco-2 cell monolayers and their absorption in sprague-dawley rats after oral Administration, J. Agric. Food Chem. 60 (2012) 8036-8043. http://doi.org/10.1021/jf302242n.

[57]

Y. Que, M. Cao, J. He, et al., Gut bacterial characteristics of patients with type 2 diabetes mellitus and the application potential, Front. Immunol. 12 (2021) 3218. http://doi.org/10.3389/fimmu.2021.722206.

[58]

M. Knip, H. Siljander, The role of the intestinal microbiota in type 1 diabetes mellitus, Nat. Rev. Endocrinol. 12 (2016) 154-167. http://doi.org/10.1038/nrendo.2015.218.

[59]

S.M. Henning, J. Yang, M. Hsu, et al., Decaffeinated green and black tea polyphenols decrease weight gain and alter microbiome populations and function in diet-induced obese mice, Eur. J. Nutr. 57 (2018) 2759-2769. http://doi.org/10.1007/s00394-017-1542-8.

[60]

T. Hatano, M. Kusuda, M. Hori, et al., Theasinensin A, a tea polyphenol formed from (−)-epigallocatechin gallate, suppresses antibiotic resistance of methicillin-resistant Staphylococcus aureus, Planta Med. 69 (2003) 984-989. http://doi.org/10.1055/s-2003-45142.

[61]

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. http://doi.org/10.1038/nature05414.

[62]

P.J. Turnbaugh, M. Hamady, T. Yatsunenko, et al., A core gut microbiome in obese and lean twins, Nature 457 (2009) 480-484. http://doi.org/10.1038/nature07540.

[63]

M. Remely, F. Ferk, S. Sterneder, et al., EGCG prevents high fat diet-induced changes in gut microbiota, decreases of DNA strand breaks, and changes in expression and DNA methylation of dnmt1 and MLH1 in C57BL/6J male mice, Oxid. Med. Cell Longev. 2017 (2017) 3079148. http://doi.org/10.1155/2017/3079148.

[64]

H. Lee, G. Ko, Effect of metformin on metabolic improvement and gut microbiota, Appl. Environ. Microbiol. 80 (2014) 5935-5943. http://doi.org/10.1128/AEM.01357-14.

[65]

K. Gao, R. Yang, J. Zhang, et al., Effects of qijian mixture on type 2 diabetes assessed by metabonomics, gut microbiota and network pharmacology, Pharmacol. Res. 130 (2018) 93-109. http://doi.org/10.1016/j.phrs.2018.01.011.

[66]

P.M. Ryan, E. Patterson, I. Carafa, et al., Metformin and dipeptidyl peptidase-4 inhibitor differentially modulate the intestinal microbiota and plasma metabolome of metabolically dysfunctional mice, Can. J. Diabetes 44 (2020) 146-155. http://doi.org/10.1016/j.jcjd.2019.05.008.

[67]

C. Lee, S.N. Hong, N.Y. Paik, et al., CD1d modulates colonic inflammation in NOD2−/− mice by altering the intestinal microbial composition comprising Acetatifactor muris, J. Crohns Colitis 13 (2019) 1081-1091. http://doi.org/10.1093/ecco-jcc/jjz025.

[68]

I. Lagkouvardos, D. Joseph, M. Kapfhammer, et al., IMNGS: a comprehensive open resource of processed 16S rRNA microbial profiles for ecology and diversity studies, Sci. Rep. 6 (2016) 33721. http://doi.org/10.1038/srep33721.

[69]

A. Everard, V. Lazarevic, M. Derrien, et al., Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice, Diabetes 60 (2011) 2775-2786. http://doi.org/10.2337/db11-0227.

[70]

D. Liu, J. Huang, Y. Luo, et al., Fuzhuan brick tea attenuates high-fat diet-induced obesity and associated metabolic disorders by shaping gut microbiota, J. Agric. Food Chem. 67 (2019) 13589-13604. http://doi.org/10.1021/acs.jafc.9b05833.

[71]

J.M. Natividad, B. Lamas, H.P. Pham, et al., Bilophila wadsworthia aggravates high fat diet induced metabolic dysfunctions in mice, Nat. Commun. 9 (2018) 1-15. http://doi.org/10.1038/s41467-018-05249-7.

[72]

Y.Y. Lam, C.W. Ha, C.R. Campbell, et al., Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice, PLoS One 7 (2012) e34233. http://doi.org/10.1371/journal.pone.0034233.

[73]

Y.C. Tung, Z.R. Liang, M.J. Yang, et al., Oolong tea extract alleviates weight gain in high-fat diet-induced obese rats by regulating lipid metabolism and modulating gut microbiota, Food Funct. 13 (2022) 2846-2856. http://doi.org/10.1039/d1fo03356e.

[74]

Y. Wang, M. Ouyang, X. Gao, et al., Phocea, Pseudoflavonifractor and Lactobacillus intestinalis: three potential biomarkers of gut microbiota that affect progression and complications of obesity-induced type 2 diabetes mellitus, Diabetes Metab. Syndr. Obes. 13 (2020) 835-850. http://doi.org/10.2147/DMSO.S240728.

[75]

M. Yassour, M.Y. Lim, H.S. Yun, et al., Sub-clinical detection of gut microbial biomarkers of obesity and type 2 diabetes, Genome Med. 8 (2016) 1-14. http://doi.org/10.1186/s13073-016-0271-6.

[76]

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

[77]

H. Plovier, A. Everard, C. Druart, et al., A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice, Nat. Med. 23 (2017) 107-113. http://doi.org/10.1038/nm.4236.

[78]

C. Depommier, M. van Hul, A. Everard, et al., Pasteurized Akkermansia muciniphila increases whole-body energy expenditure and fecal energy excretion in diet-induced obese mice, Gut Microbes 11 (2020) 1231-1245. http://doi.org/10.1080/19490976.2020.1737307.

[79]

H.S. Yoon, C.H. Cho, M.S. Yun, et al., Akkermansia muciniphila secretes a glucagon-like peptide-1-inducing protein that improves glucose homeostasis and ameliorates metabolic disease in mice, Nat. Microbiol. 6 (2021) 563-573. http://doi.org/10.1038/s41564-021-00880-5.

[80]

H. Zheng, P. Xu, Q. Jiang, et al., Depletion of acetate-producing bacteria from the gut microbiota facilitates cognitive impairment through the gut-brain neural mechanism in diabetic mice, Microbiome 9 (2021) 1-19. http://doi.org/10.1186/s40168-021-01088-9.

[81]

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. http://doi.org/10.1038/nature18309.

[82]

K.R. Freeland, T.M.S. Wolever, Acute effects of intravenous and rectal acetate on glucagon-like peptide-1, peptide YY, ghrelin, adiponectin and tumour necrosis factor-α, Br. J. Nutr. 103 (2010) 460-466. http://doi.org/10.1017/S0007114509991863.

[83]

L. Zhao, F. Zhang, X. Ding, et al., Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes, Science 359 (2018) 1151-1156. http://doi.org/10.1126/science.aao5774.

[84]

J. Qin, Y. Li, Z. Cai, et al., A metagenome-wide association study of gut microbiota in type 2 diabetes, Nature 490 (2012) 55-60. http://doi.org/10.1038/nature11450.

[85]

T. Unno, M. Sakuma, S. Mitsuhashi, Effect of dietary supplementation of (−)-epigallocatechin gallate on gut microbiota and biomarkers of colonic fermentation in rats, J. Nutr. Sci. Vitaminol. 60 (2014) 213-219. http://doi.org/10.3177/jnsv.60.213.

[86]

E. Mezhibovsky, K.A. Knowles, Q. He, et al., Grape polyphenols attenuate diet-induced obesity and hepatic steatosis in mice in association with reduced butyrate and increased markers of intestinal carbohydrate oxidation, Front. Nutr. 8 (2021) 317. http://doi.org/10.3389/fnut.2021.675267.

[87]

M.C. de Goffau, K. Luopajarvi, M. Knip, et al., Fecal microbiota composition differs between children with β-cell autoimmunity and those without, Diabetes 62 (2013) 1238-1244. http://doi.org/10.2337/db12-0526.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 30 December 2021
Revised: 07 February 2022
Accepted: 01 March 2022
Published: 04 April 2023
Issue date: November 2023

Copyright

© 2023 Beijing Academy of Food Sciences.

Acknowledgements

The study was supported by the Key Technology R&D Program of Jiangsu Province (BE2020341) and the Priority Academic Program Development of Jiangsu Higher Education Institutions.

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