Journal Home > Volume 13 , Issue 3
Food Science and Human Wellness 2024, 13(3): 1279-1291 https://doi.org/10.26599/FSHW.2022.9250107
Research Article | Open Access | Issue | Published: 08 February 2024

Elaidic acid-induced intestinal barrier damage led to gut-liver axis derangement and triggered NLRP3 inflammasome in the liver of SD rats

Show Author's Information Hui Liua,b,  Xuenan Lia,  Lu Lia,  Yucai Lia,  Haiyang Yana,  Yong Panga,  Wenliang Lia,  Yuan Yuana,( )
College of Food Science and Engineering, Jilin University, Changchun 130062, China
School of Public Health, Jining Medical University, Jining 272067, China

Peer review under responsibility of Tsinghua University Press.

Keywords:
Gut microbiota, Intestinal barrier, NLRP3 inflammasome, Elaidic acid (EA), Gut-liver axis, TLR4-MyD88-NF-κB/MAPK pathways
Cite this article:
Liu H, Li X, Li L, et al. Elaidic acid-induced intestinal barrier damage led to gut-liver axis derangement and triggered NLRP3 inflammasome in the liver of SD rats. Food Science and Human Wellness, 2024, 13(3): 1279-1291. https://doi.org/10.26599/FSHW.2022.9250107
Download citation
EndNote(RIS)
BibTeX

488

Views

113

Downloads

Citations

0

Crossref

0

WoS

0

Scopus

0

CSCD

Abstract Full text About this article

Previous studies have shown that trans fatty acids (TFA) are associated with several chronic diseases, the gut microbiota is directly influenced by dietary components and linked to chronic diseases. Our research investigated the effects of elaidic acid (EA), a typical TFA, on the gut microbiota to understand the underlying mechanisms of TFA-related chronic diseases. 16S rDNA gene sequencing on faecal samples from Sprague-Dawley rats were performed to explore the composition change of the gut microbiota by EA gavage for 4 weeks. The results showed that the intake of EA increased the abundance of well-documented harmful bacteria, such as Proteobacteria, Anaerotruncus, Oscillibacter and Desulfovibrionaceae. Plus, EA induced translocation of lipopolysaccharides (LPS) and the above pathogenic bacteria, disrupted the intestinal barrier, led to gut-liver axis derangement and TLR4 pathway activation in the liver. Overall, EA induced intestinal barrier damage and regulated TLR4-MyD88-NF-κB/MAPK pathways in the liver of SD rats, leading to the activation of NLRP3 inflammasome and inflammatory liver damage.


menu
Abstract
Full text
Outline
About this article

Elaidic acid-induced intestinal barrier damage led to gut-liver axis derangement and triggered NLRP3 inflammasome in the liver of SD rats

Show Author's information Hui Liua,b, Xuenan Lia, Lu Lia, Yucai Lia, Haiyang Yana, Yong Panga, Wenliang Lia, Yuan Yuana,( )
College of Food Science and Engineering, Jilin University, Changchun 130062, China
School of Public Health, Jining Medical University, Jining 272067, China

Peer review under responsibility of Tsinghua University Press.

Abstract

Previous studies have shown that trans fatty acids (TFA) are associated with several chronic diseases, the gut microbiota is directly influenced by dietary components and linked to chronic diseases. Our research investigated the effects of elaidic acid (EA), a typical TFA, on the gut microbiota to understand the underlying mechanisms of TFA-related chronic diseases. 16S rDNA gene sequencing on faecal samples from Sprague-Dawley rats were performed to explore the composition change of the gut microbiota by EA gavage for 4 weeks. The results showed that the intake of EA increased the abundance of well-documented harmful bacteria, such as Proteobacteria, Anaerotruncus, Oscillibacter and Desulfovibrionaceae. Plus, EA induced translocation of lipopolysaccharides (LPS) and the above pathogenic bacteria, disrupted the intestinal barrier, led to gut-liver axis derangement and TLR4 pathway activation in the liver. Overall, EA induced intestinal barrier damage and regulated TLR4-MyD88-NF-κB/MAPK pathways in the liver of SD rats, leading to the activation of NLRP3 inflammasome and inflammatory liver damage.

Keywords: Gut microbiota, Intestinal barrier, NLRP3 inflammasome, Elaidic acid (EA), Gut-liver axis, TLR4-MyD88-NF-κB/MAPK pathways

References(55)

[1]

Y. Hirata, A. Inoue, S. Suzuki, et al., Trans-fatty acids facilitate DNA damage-induced apoptosis through the mitochondrial JNK-Sab-ROS positive feedback loop, Sci. Rep. 10(1) (2020) 2743. https://doi.org/10.1038/S41598-020-59636-6.
DOI Google Scholar
[2]

N. Gotoh, S. Kagiono, K. Yoshinaga, et al., Study of trans fatty acid formation in oil by heating using model compounds, J. Oleo Sci. 67(3) (2018) 273-281. https://doi.org/10.5650/jos.ess17209.
DOI Google Scholar
[3]

A.B. Oteng, S. Kersten, Mechanisms of action of trans fatty acids, Adv. Nutr. 11(3) (2020) 697-708. https://doi.org/10.1093/advances/nmz125.
DOI Google Scholar
[4]

A.B. Oteng, A. Bhattacharya, S. Brodesser, et al., Feeding Angptl4-/- mice trans fat promotes foam cell formation in mesenteric lymph nodes without leading to ascites, J. Lipid Res. 58(6) (2017) 1100-1113. https://doi.org/10.1194/jlr.M074278.
DOI Google Scholar
[5]

A. Sauvat, G. Chen, K. Muller, et al., Trans-fats inhibit autophagy induced by saturated fatty acids, EBioMedicine 30 (2018) 261-272. https://doi.org/10.1016/j.ebiom.2018.03.028.
DOI Google Scholar
[6]

H. Ka, B. Yi, M.J. Kim, et al., Effects of cis oleic and trans elaidic acids on oxidative stability in riboflavin and chlorophyll photosensitized oil-in-water emulsions, Food Sci. Food Biotechnol. 24(5) (2015) 1645-1648. https://doi.org/10.1007/s10068-015-0213-x.
DOI Google Scholar
[7]

K. Kuhnt, M. Baehr, C. Rohrer, et al., Trans fatty acid isomers and the trans-9/trans-11 index in fat containing foods, Eur. J. Lipid Sci. Technol.113(10) (2011) 1281-1292. https://doi.org/10.1002/ejlt.201100037.
DOI Google Scholar
[8]

R. Ganguly, R. LaVallee, T.G. Maddaford, et al., Ruminant and industrial trans-fatty acid uptake in the heart, J. Nutr. Biochem. 31 (2016) 60-66. https://doi.org/10.1016/j.jnutbio.2015.12.018.
DOI Google Scholar
[9]

I.A. Brouwer, A.J. Wanders, M.B. Katan, Effect of animal and industrial trans fatty acids on HDL and LDL cholesterol levels in humans-a quantitative review, PLoS One 5(3) (2010) e9434. https://doi.org/10.1371/journal.pone.0009434.
DOI Google Scholar
[10]

T. Okamura, Y. Hashimoto, S. Majima, et al., Trans fatty acid intake induces intestinal inflammation and impaired glucose tolerance, Front. Immunol. 12(2021) 669672. https://doi.org/10.3389/fimmu.2021.669672.
DOI Google Scholar
[11]

Y. Ge, W. Liu, H. Tao, et al., Effect of industrial trans-fatty acids-enriched diet on gut microbiota of C57BL/6 mice, Eur. J. Nutr. 58(7) (2019) 2625-2638. https://doi.org/10.1007/s00394-018-1810-2.
DOI Google Scholar
[12]

R.G. Visschers, M.D. Luyer, F.G. Schaap, et al., The gut-liver axis, Curr. Opin. Clin. Nutr. Metab. Care 16(5) (2013) 576-581. https://doi.org/10.1097/MCO.0b013e32836410a4.
DOI Google Scholar
[13]

K. Allen, H. Jaeschke, B.L. Copple, Bile acids induce inflammatory genes in hepatocytes: a novel mechanism of inflammation during obstructive cholestasis, Am. J. Pathol. 178(1) (2011) 175-186. https://doi.org/10.1016/j.ajpath.2010.11.026.
DOI Google Scholar
[14]

N.P. Woodcock, J. Robertson, D.R. Morgan, et al., Bacterial translocation and immunohistochemical measurement of gut immune function, J. Clin.Pathol. 54(8) (2001) 619-623. https://doi.org/10.1136/jcp.54.8.619.
DOI Google Scholar
[15]

S. de Minicis, C. Rychlicki, L. Agostinelli, et al., Dysbiosis contributes to fibrogenesis in the course of chronic liver injury in mice, Hepatology 59(5)(2014) 1738-1749. https://doi.org/10.1002/hep.26695.
DOI Google Scholar
[16]

J. Sabino, S. Vieira-Silva, K. Machiels, et al., Primary sclerosing cholangitis is characterised by intestinal dysbiosis independent from IBD, Gut 65(10)(2016) 1681-1689. https://doi.org/10.1136/gutjnl-2015-311004.
DOI Google Scholar
[17]

N. Akhter, A. Hasan, S. Shenouda, et al., TLR4/MyD88-mediated CCL2 production by lipopolysaccharide (endotoxin): implications for metabolic inflammation, J. Diabetes Metab. Disord. 17(1) (2018) 77-84. https://doi.org/10.1007/s40200-018-0341-y.
DOI Google Scholar
[18]

J. Henao-Mejia, E. Elinav, C. Jin, et al., Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity, Nature 482(7384) (2012) 179-185. https://doi.org/10.1038/nature10809.
DOI Google Scholar
[19]

A. Wree, M.D. McGeough, M.E. Inzaugarat, et al., NLRP3 inflammasome driven liver injury and fibrosis: roles of IL-17 and TNF in mice, Hepatology 67(2) (2018) 736-749. https://doi.org/10.1002/hep.29523.
DOI Google Scholar
[20]

K. Schroder, J. Tschopp, The inflammasomes, Cell 140(6) (2010) 821-832. https://doi.org/10.1016/j.cell.2010.01.040.
DOI Google Scholar
[21]

M. Minemura, Y. Shimizu, Gut microbiota and liver diseases, World J. Gastroenterol. 21(6) (2015) 1691-1702. https://doi.org/10.3748/wjg.v21.i6.1691.
DOI Google Scholar
[22]

P. Chen, P. Starkel, J.R. Turner, et al., Dysbiosis-induced intestinal inflammation activates tumor necrosis factor receptor I and mediates alcoholic liver disease in mice, Hepatology 61(3) (2015) 883-894. https://doi.org/10.1002/hep.27489.
DOI Google Scholar
[23]

L. de Brito Medeiros, S. Alves, R. de Bessa, et al., Ruminant fat intake improves gut microbiota, serum inflammatory parameter and fatty acid profile in tissues of Wistar rats, Sci. Rep. 11(1) (2021) 18963. https://doi.org/10.1038/s41598-021-98248-6.
DOI Google Scholar
[24]

H. Liu, B. Nan, C. Yang, et al., Elaidic acid induced NLRP3 inflammasome activation via ERS-MAPK signaling pathways in kupffer cells, Biochim.Biophys. Acta. Mol. Cell Biol. Lipids 1867(1) (2022) 159061. https://doi.org/10.1016/j.bbalip.2021.159061.
DOI Google Scholar
[25]

S.H. Luo, W. Xiao, X.J. Wei, et al., In vitro evaluation of cytotoxicity of silver-containing borate bioactive glass, J. Biomed. Mater. Res. Part B 95(2)(2010) 441-448. https://doi.org/10.1002/jbm.b.31735.
DOI Google Scholar
[26]

T.P. Bui, J. Ritari, S. Boeren, et al., Production of butyrate from lysine and the amadori product fructoselysine by a human gut commensal, Nat. Commun. 6 (2015) 10062. https://doi.org/10.1038/ncomms10062.
DOI Google Scholar
[27]

H.Z. Zhu, Y.D. Liang, Q.Y. Ma, et al., Xiaoyaosan improves depressive-like behavior in rats with chronic immobilization stress through modulation of the gut microbiota, Biomed. Pharmacother. 112 (2019) 108621. https://doi.org/10.1016/J.Biopha.2019.108621.
DOI Google Scholar
[28]

F.R. Ponziani, S. Bhoori, C. Castelli, et al., Hepatocellular carcinoma is associated with gut microbiota profile and inflammation in nonalcoholic fatty liver disease, Hepatology 69(1) (2019) 107-120. https://doi.org/10.1002/hep.30036.
DOI Google Scholar
[29]

F.D. Urnov, A path to efficient gene editing, Nat. Med. 24(7) (2018) 899-900. https://doi.org/10.1038/s41591-018-0110-y.
DOI Google Scholar
[30]

B.D. Needham, S.M. Carroll, D.K. Giles, et al., Modulating the innate immune response by combinatorial engineering of endotoxin, Proc. Natl. Acad. Sci. U.S.A. 110(4) (2013) 1464-1469. https://doi.org/10.1073/pnas.1218080110.
DOI Google Scholar
[31]

T. Vatanen, A.D. Kostic, E. d’Hennezel, et al., Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans, Cell 165(6) (2016) 1551. https://doi.org/10.1016/j.cell.2016.05.056.
DOI Google Scholar
[32]

Y. Litvak, M.X. Byndloss, R.M. Tsolis, et al., Dysbiotic proteobacteria expansion: a microbial signature of epithelial dysfunction, Curr. Opin. Microbiol. 39 (2017) 1-6. https://doi.org/10.1016/j.mib.2017.07.003.
DOI Google Scholar
[33]

Z.P. Gao, H. Wu, K.Q. Zhang, et al., Protective effects of grape seed procyanidin extract on intestinal barrier dysfunction induced by a long-term high-fat diet, J. Funct. Foods 64 (2020) 103663. https://doi.org/10.1016/J.Jff.2019.103663.
DOI Google Scholar
[34]

C.S. Wang, W.B. Li, H.Y. Wang, et al., VSL#3 can prevent ulcerative colitis-associated carcinogenesis in mice, World J. Gastroenterol. 24(37)(2018) 4254-4262. https://doi.org/10.3748/wjg.v24.i37.4254.
DOI Google Scholar
[35]

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(3) (2012) e34233. https://doi.org/10.1371/journal.pone.0034233.
DOI Google Scholar
[36]

Y. Hua, R. Fan, L. Zhao, et al., Trans-fatty acids alter the gut microbiota in high-fat-diet-induced obese rats, Br. J. Nutr. 124(12) (2020) 1251-1263. https://doi.org/10.1017/S0007114520001841.
DOI Google Scholar
[37]

Q. Zhang, H. Yu, X. Xiao, et al., Inulin-type fructan improves diabetic phenotype and gut microbiota profiles in rats, PeerJ 6 (2018) e4446. https://doi.org/10.7717/peerj.4446.
DOI Google Scholar
[38]

V.R. Figliuolo, L.M. Dos Santos, A. Abalo, et al., Sulfate-reducing bacteria stimulate gut immune responses and contribute to inflammation in experimental colitis, Life Sci. 189 (2017) 29-38. https://doi.org/10.1016/j.lfs.2017.09.014.
DOI Google Scholar
[39]

C. Petersen, R. Bell, K.A. Kiag, et al., T cell-mediated regulation of the microbiota protects against obesity, Science 365(6451) (2019) eaat9351. https://doi.org/10.1126/science.aat9351.
DOI Google Scholar
[40]

A. Miranda-Ribera, M. Ennamorati, G. Serena, et al., Exploiting the zonulin mouse model to establish the role of primary impaired gut barrier function on microbiota composition and immune profiles, Front. Immunol. 10 (2019) 2233. https://doi.org/10.3389/fimmu.2019.02233.
DOI Google Scholar
[41]

C. Zhang, M. Zhang, X. Pang, et al., Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations, ISME J. 6(10)(2012) 1848-1857. https://doi.org/10.1038/ismej.2012.27.
DOI Google Scholar
[42]

C. Li, Y.H. Zhang, Y.T. Ge, et al., Comparative transcriptome and microbiota analyses provide new insights into the adverse effects of industrial trans fatty acids on the small intestine of C57BL/6 mice, Eur. J.Nutr. 60(2) (2021) 975-987. https://doi.org/10.1007/s00394-020-02297-y.
DOI Google Scholar
[43]

H. Zeng, J. Liu, M.I. Jackson, et al., Fatty liver accompanies an increase in lactobacillus species in the hind gut of C57BL/6 mice fed a high-fat diet, J.Nutr. 143(5) (2013) 627-631. https://doi.org/10.3945/jn.112.172460.
DOI Google Scholar
[44]

M. Centanni, S. Turroni, S. Rampelli, et al., Bifidobacterium animalis ssp.lactis BI07 modulates the tumor necrosis factor alpha-dependent imbalances of the enterocyte-associated intestinal microbiota fraction, FEMS Microbiol. Lett. 357(2) (2014) 157-163. https://doi.org/10.1111/1574-6968.12515.
DOI Google Scholar
[45]

A. Albillos, A. de Gottardi, M. Rescigno, The gut-liver axis in liver disease:pathophysiological basis for therapy, J. Hepatol. 72(3) (2020) 558-577. https://doi.org/10.1016/j.jhep.2019.10.003.
DOI Google Scholar
[46]

W. Jiang, N. Wu, X. Wang, et al., Dysbiosis gut microbiota associated with inflammation and impaired mucosal immune function in intestine of humans with non-alcoholic fatty liver disease, Sci. Rep. 5 (2015) 8096. https://doi.org/10.1038/srep08096.
DOI Google Scholar
[47]

I. Hritz, P. Mandrekar, A. Velayudham, et al., The critical role of toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88, Hepatology 48(4) (2008) 1224-1231. https://doi.org/10.1002/hep.22470.
DOI Google Scholar
[48]

N. Qin, F. Yang, A. Li, et al., Alterations of the human gut microbiome in liver cirrhosis, Nature 513(7516) (2014) 59-64. https://doi.org/10.1038/nature13568.
DOI Google Scholar
[49]

D. Feng, H. Zhang, X. Jiang, et al., Bisphenol a exposure induces gut microbiota dysbiosis and consequent activation of gut-liver axis leading to hepatic steatosis in CD-1 mice, Environ. Pollut. 265(Pt A) (2020) 114880. https://doi.org/10.1016/j.envpol.2020.114880.
DOI Google Scholar
[50]

S.H. Lee, Intestinal permeability regulation by tight junction: implication on inflammatory bowel diseases, Intest. Res. 13(1) (2015) 11-18. https://doi.org/10.5217/ir.2015.13.1.11.
DOI Google Scholar
[51]

Q. Zhang, M.J. Lenardo, D. Baltimore, 30 years of NF-κB: a blossoming of relevance to human pathobiology, Cell 168(1/2) (2017) 37-57. https://doi.org/10.1016/j.cell.2016.12.012.
DOI Google Scholar
[52]

R.H. Du, J. Tan, N. Yan, et al., Kir6.2 knockout aggravates lipopolysaccharide-induced mouse liver injury via enhancing NLRP3 inflammasome activation, J. Gastroenterol. 49(4) (2014) 727-736. https://doi.org/10.1007/s00535-013-0823-0.
DOI Google Scholar
[53]

H.B. Yu, B.B. Finlay, The caspase-1 inflammasome: a pilot of innate immune responses, Cell Host Microbe. 4(3) (2008) 198-208. https://doi.org/10.1016/j.chom.2008.08.007.
DOI Google Scholar
[54]

Z. Dong, Q. Zhuang, M. Ning, et al., Palmitic acid stimulates NLRP3 inflammasome activation through TLR4-NF-κB signal pathway in hepatic stellate cells, Ann. Transl. Med. 8(5) (2020) 168. https://doi.org/10.21037/atm.2020.02.21.
DOI Google Scholar
[55]

J. Wang, R. Dong, S. Zheng, Roles of the inflammasome in the gut-liver axis (review), Mol. Med. Rep. 19(1) (2019) 3-14. https://doi.org/10.3892/mmr.2018.9679.
DOI Google Scholar
Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 21 April 2022
Revised: 24 September 2022
Accepted: 04 December 2022
Published: 08 February 2024
Issue date: May 2024

Copyright

© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

Acknowledgements

This work was supported by fund from the National Natural Science Foundation of China (32172322), Shandong Provincial Natural Science Foundation（ZR2023QC291), and Shandong Traditional Chinese Medicine Technology Project (Q-2023130). The authors gratefully acknowledge the fund support.

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