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There are a number of health benefits of Mesona chinensis Benth polysaccharide (MP), but little is known about its hepatoprotective effect and effect on gut microbiota composition in mice with liver damage induced by cyclophosphamide (CTX). This study indicated that MP supplementation effectively inhibited the production of serum aspartate aminotransferase (AST) and alanine aminotransferase (ALT), enhanced liver antioxidant capacity and repaired liver damage in mice caused by CTX. The release of inflammatory cytokines in liver and the concentration of lipopolysaccharide (LPS) in serum were decreased, and the level of short chain fatty acids (SCFAs) in colon was increased after MP administration. Those effects may be correlated with the regulation of the gut microbiota. Importantly, MP restrained liver inflammatory responses induced by CTX may via increasing the SCFAs-producing bacteria family Ruminococcaceae and reduced LPS-producing bacteria genus Bacteroides. In short, the prevention of CTX-induced liver injury by supplementing MP is achieved at least in part by regulating the community structure of the gut microbiota, and MP is expected to be a potential prebiotic to treat and prevent liver diseases.


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Mesona chinensis Benth polysaccharides alleviates liver injury by beneficial regulation of gut microbiota in cyclophosphamide-induced mice

Show Author's information Yuzhen HongMingyue ShenLixin HuangTing WuJianhua Xie( )
State Key Laboratory of Food Science and Technology, Nanchang University, Nanchang 330047, China

Abstract

There are a number of health benefits of Mesona chinensis Benth polysaccharide (MP), but little is known about its hepatoprotective effect and effect on gut microbiota composition in mice with liver damage induced by cyclophosphamide (CTX). This study indicated that MP supplementation effectively inhibited the production of serum aspartate aminotransferase (AST) and alanine aminotransferase (ALT), enhanced liver antioxidant capacity and repaired liver damage in mice caused by CTX. The release of inflammatory cytokines in liver and the concentration of lipopolysaccharide (LPS) in serum were decreased, and the level of short chain fatty acids (SCFAs) in colon was increased after MP administration. Those effects may be correlated with the regulation of the gut microbiota. Importantly, MP restrained liver inflammatory responses induced by CTX may via increasing the SCFAs-producing bacteria family Ruminococcaceae and reduced LPS-producing bacteria genus Bacteroides. In short, the prevention of CTX-induced liver injury by supplementing MP is achieved at least in part by regulating the community structure of the gut microbiota, and MP is expected to be a potential prebiotic to treat and prevent liver diseases.

Keywords: Gut microbiota, Oxidative stress, Polysaccharide, Liver damage

References(45)

[1]

A. Emadi, R.J. Jones, R.A. Brodsky, Cyclophosphamide and cancer: golden annivers ary, Nat. Rev. Clin. Oncol. 6 (2009) 638-647. https://doi.org/10.1038/nrclinonc.2009.146.

[2]

P.D. King, M.C. Perry, Hepatotoxicity of chemotherapy, Oncologist 6 (2001) 162-176. https://doi.org/10.1634/theoncologist.6-2-162.

[3]

M.T. Madondo, M. Quinn, M. Plebanski, Low dose cyclophosphamide: mechanisms of T cell modulation, Cancer Treat Rev. 42 (2016) 3-9. https://doi.org/10.1016/j.ctrv.2015.11.005.

[4]

P. Vitaglione, F. Morisco, N. Caporaso, et al., Dietary antioxidant compounds and liver health, Crit. Rev. Food. Sci. Nutr. 44 (2004) 575-586. https://doi.org/10.1080/10408690490911701.

[5]

S.K. Asrani, H. Devarbhavi, J. Eaton, et al., Burden of liver diseases in the world, J. Hepatol. 70 (2019) 151-171. https://doi.org/10.1016/j.jhep.2018.09.014.

[6]

M.O. Germoush, Diosmin protects against cyclophosphamide-induced liver injury through attenuation of oxidative stress, inflammation and apoptosis, Int. J. Pharmacol. 12 (2016) 644-654. https://doi.org/10.3923/ijp.2016.644.654.

[7]

M. Zarei, T. Shivanandappa, Amelioration of cyclophosphamide-induced hepatotoxicity by the root extract of Decalepis hamiltonii in mice, Food. Chem. Toxicol. 57 (2013) 179-184. https://doi.org/10.1016/j.fct.2013.03.028.

[8]

Y. Yu, M.Y. Shen, Q.Q. Song, et al., Biological activities and pharmaceutical applications of polysaccharide from natural resources: a review, Carbohydr. Polym. 183 (2018) 91-101. https://doi.org/10.1016/j.carbpol.2017.12.009.

[9]

J.H. Xie, M.Y. Xie, S.P. Nie, et al., Isolation, chemical composition and antioxidant activities of a water-soluble polysaccharide from Cyclocarya paliurus (Batal.) Iljinskaja, Food. Chem. 119 (2010) 1626-1632. https://doi.org/10.1016/j.foodchem.2009.09.055.

[10]

J. Luo, C. Zhang, R. Liu, et al., Ganoderma lucidum polysaccharide alleviating colorectal cancer by alteration of special gut bacteria and regulation of gene expression of colonic epithelial cells, J. Funct. Foods. 47 (2018) 127-135. https://doi.org/10.1016/j.jff.2018.05.041.

[11]

X. Xu, J. Yang, Z. Ning, et al., Lentinula edodes-derived polysaccharide rejuvenates mice in terms of immune responses and gut microbiota, Food. Funct. 6 (2015) 2653-2663. https://doi.org/10.1039/C5FO00689A.

[12]

J. Xie, M. Jin, G.A. Morris, et al., Advances on bioactive polysaccharides from medicinal plants, Crit. Rev. Food. Sci. Nutr. 56(sup1) (2015) S60-S84. https://doi.org/10.1080/10408398.2015.1069255.

[13]

S. Lin, G. Hao, M. Long, et al., Oyster (Ostrea plicatula Gmelin) polysaccharides intervention ameliorates cyclophosphamide-Induced genotoxicity and hepatotoxicity in mice via the Nrf2-ARE pathway, Biomed. Pharmacother. 95 (2017) 1067-1071. https://doi.org/10.1016/j.biopha.2017.08.058.

[14]

L. Huang, M. Huang, M. Shen, et al., Sulfated modification enhanced the antioxidant activity of Mesona chinensis Benth polysaccharide and its protective effect on cellular oxidative stress, Int. J. Biol. Macromol. 136 (2019) 1000-1006. https://doi.org/10.1016/j.ijbiomac.2019.06.199.

[15]

L.H. Lin, J.H. Xie, S.C. Liu, et al., Polysaccharide from Mesona chinensis: extraction optimization, physicochemical characterizations and antioxidant activities, Int. J. Biol. Macromol. 99 (2017) 665-673. https://doi.org/10.1016/j.ijbiomac.2017.03.040.

[16]

L.X. Huang, M.Y. Shen, X.W. Zhang, et al., Effect of high-pressure microfluidization treatment on the physicochemical properties and antioxidant activities of polysaccharide from Mesona chinensis Benth, Carbohydr. Polym. 200 (2018) 191-199. https://doi.org/10.1016/j.carbpol.2018.07.087.

[17]

W. Wang, L. Jiang, Y. Ren, et al., Characterizations and hepatoprotective effect of polysaccharides from Mesona blumes against tetrachloride-induced acute liver injury in mice, Int. J. Biol. Macromol. 124 (2019) 788-795. https://doi.org/10.1016/j.ijbiomac.2018.11.260.

[18]

F. Backhed, R.E. Ley, J.L. Sonnenburg, et al., Host-bacterial mutualism in the human intestine, Science 307 (2005) 1915-1920. https://doi.org/10.1126/science.1104816.

[19]

G.A. Cresci, B. Glueck, M.R. McMullen, et al., Prophylactic tributyrin treatment mitigates chronic-binge ethanol-induced intestinal barrier and liver injury, J. Gastroenterol. Hepatol. 32 (2017) 1587-1597. https://doi.org/10.1111/jgh.13731.

[20]

P.A. van Leeuwen, M.A. Boermeester, A.P. Houdijk, et al., Clinical significance of translocation, Gut 35 (1994) S28-S34. https://doi.org/10.1136/gut.35.1_suppl.s28.

[21]

X.C. Peng, S.T. Li, J.M. Luo, et al., Effects of dietary fibers and their mixtures on short chain fatty acids and microbiota in mice guts, Food. Funct. 4 (2013) 932-938. https://doi.org/10.1039/c3fo60052a.

[22]

H.J. Flint, K.P. Scott, P. Louis, et al., The role of the gut microbiota in nutrition and health, Nat. Rev. Gastroenterol. Hepatol. 9 (2012) 577-589. https://doi.org/10.1038/nrgastro.2012.156.

[23]

R. Zhao, Q. Hu, G. Ma, et al., Effects of Flammulina velutipes polysaccharide on immune response and intestinal microbiota in mice, J. Funct. Foods. 56 (2019) 255-264. https://doi.org/10.1016/j.jff.2019.03.031.

[24]

Y. Xia, T. Wang, S. Yu, et al., Structural characteristics and hepatoprotective potential of Aralia elata root bark polysaccharides and their effects on SCFAs produced by intestinal flora metabolism, Carbohydr. Polym. 207 (2019) 256-265. https://doi.org/10.1016/j.carbpol.2018.11.097.

[25]

J. Wu, H. Shao, J. Zhang, et al., Mussel polysaccharide alpha-D-glucan (MP-A) protects against non-alcoholic fatty liver disease via maintaining the homeostasis of gut microbiota and regulating related gut-liver axis signaling pathways, Int. J. Biol. Macromol. 130 (2019) 68-78. https://doi.org/10.1016/j.ijbiomac.2019.02.097.

[26]

D. Hou, Q. Zhao, L. Yousaf, et al., Consumption of mung bean (Vigna radiata L.) attenuates obesity, ameliorates lipid metabolic disorders and modifies the gut microbiota composition in mice fed a high-fat diet, J. Funct. Foods. 64 (2020) 1756-4646. https://doi.org/10.1016/j.jff.2019.103687.

[27]

S.R. Fahmy, A.I. Amien, F.M. Abd-Elgleel, et al., Antihepatotoxic efficacy of Mangifera indica L. polysaccharides against cyclophosphamide in rats, Chem. Biol. Interact. 244 (2016) 113-120. https://doi.org/10.1016/j.cbi.2015.11.009.

[28]

Y.V. Yuan, D.E. Bone, M.F. Carrington, Antioxidant activity of dulse (Palmaria palmata) extract evaluated in vitro, Food. Chem. 91 (2015) 485-494. https://doi.org/10.1016/j.foodchem.2004.04.039.

[29]

D.H. Mak, S.P. Ip, P.C. Li, et al., Alterations in tissue glutathione antioxidant system in streptozotocin-induced diabetic rats, Mol. Cell. Biochem. 162 (1996) 153-158. https://doi.org/10.1007/BF00227543.

[30]

R.K. Nitharwal, H. Patel, M.S. Karchuli, et al., Chemoprotective potential of Coccinia indica against cyclophosphamide-induced toxicity, Indian. J. Pharmacol. 45 (2013) 502-507. https://doi.org/10.4103/0253-7613.117783.

[31]

G. Malaguarnera, M. Giordano, G. Nunnari, et al., Gut microbiota in alcoholic liver disease: pathogenetic role and therapeutic perspectives, World. J. Gastroenterol. 20 (2014) 16639-16648. https://doi.org/10.3748/wjg.v20.i44.16639.

[32]

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

[33]

J.S. Park, E.J. Lee, J.C. Lee, et al., Anti-inflammatory effects of short chain fatty acids in IFN-gamma-stimulated RAW 264.7 murine macrophage cells: involvement of NF-kappaB and ERK signaling pathways, Int. Immunopharmacol. 7 (2007) 70-77. https://doi.org/10.1016/j.intimp.2006.08.015.

[34]

X. Xu, P. Xu, C. Ma, et al., Gut microbiota, host health, and polysaccharides, Biotechnol. Adv. 31 (2013) 318-337.https://doi.org/10.1016/j.biotechadv.2012.12.009.

[35]

J. Hu, S. 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.

[36]

I. Sekirov, S.L. Russell, L.C. Antunes, et al., Gut microbiota in health and disease, Physiol. Rev. 90 (2010) 859-904. https://doi.org/10.1152/physrev.00045.2009.

[37]

M.K. Takanori Kana, The gut microbiota and inflammatory bowel disease, Semin. Immunopathol. 37 (2015) 47-55. https://doi.org/10.1007/s00281-014-0454-4.

[38]

M. Lyu, Y.F. Wang, G.W. Fan, et al., Balancing herbal medicine and functional food for prevention and treatment of cardiometabolic diseases through modulating gut microbiota, Front. Microbiol. 8 (2017) 2146. https://doi.org/10.3389/fmicb.2017.02146.

[39]

Q. Shang, X. Shan, C. Cai, et al., Dietary fucoidan modulates the gut microbiota in mice by increasing the abundance of Lactobacillus and Ruminococcaceae, Food. Funct. 7 (2016) 3224-3232. https://doi.org/10.1039/C6FO00309E.

[40]

C.J. Zheng, R. Liu, B. Xue, et al., Impact and consequences of polyphenols and fructooligosaccharide interplay on gut microbiota in rats, Food. Funct. 8 (2017) 1925-1932. https://doi.org/10.1039/C6FO01783E.

[41]

H. Wang, Y. Li, X. Feng, et al., Dysfunctional gut microbiota and relative co-abundance network in infantile eczema, Gut Pathog. 8 (2016) 36. https://doi.org/10.1186/s13099-016-0118-0.

[42]

F.F. Anhe, R.T. Nachbar, T.V. Varin, et al., Treatment with camu camu (Myrciaria dubia) prevents obesity by altering the gut microbiota and increasing energy expenditure in diet-induced obese mice, Gut 68 (2019) 453-464. https://doi.org/10.1136/gutjnl-2017-315565.

[43]

D.L. Chen, C.Q. Zheng, J. Yang, et al., Immunomodulatory activities of a fungal protein extracted from Hericium erinaceus through regulating the gut microbiota, Front. Immunol. 8 (2017) 666. https://doi.org/10.3389/fimmu.2017.00666.

[44]

L. Zhang, Y.N. Wu, T. Chen, et al., Relationship between intestinal microbial dysbiosis and primary liver cancer, Hepatobiliary. Pancreat. Dis. Int. 18 (2019) 149-157. https://doi.org/10.1016/j.hbpd.2019.01.002.

[45]

T. Liu, J. Li, Y. Liu, et al., Short-chain fatty acids suppress lipopolysaccharide-induced production of nitric oxide and proinflammatory cytokines through inhibition of NF-kappaB pathway in RAW264.7 cells, Inflammation 35 (2012) 1676-1684. https://doi.org/10.1007/s10753-012-9484-z.

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Publication history

Received: 31 March 2020
Revised: 05 June 2020
Accepted: 10 June 2020
Published: 11 September 2021
Issue date: January 2022

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© 2021 Beijing Academy of Food Sciences. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co., Ltd.

Acknowledgements

Acknowledgement

This study was supported by grants from the National Natural Science Foundation of China (21566024), and the Natural Science Foundation of Jiangxi province, China (20181ACB20013).

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

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