Resveratrol Attenuates Ankylosing Spondylitis in Mice by Inhibiting the TLR4/NF-κB/NLRP3 Pathway and Regulating Gut Microbiota

References

• Alcon-Giner C, Caim S, Mitra S, Ketskemety J, Wegmann U, Wain J, Belteki G, Clarke P, Hall LJ. 2017. Optimisation of 16S rRNA gut microbiota profiling of extremely low birth weight infants. BMC Genomics. 18(1):841.
   PubMedGoogle Scholar
• Babaie F, Hasankhani M, Mohammadi H, Safarzadeh E, Rezaiemanesh A, Salimi R, Baradaran B, Babaloo Z. 2018. The role of gut microbiota and IL-23/IL-17 pathway in ankylosing spondylitis immunopathogenesis: new insights and updates. Immunol Lett. 196:52–62.
   PubMed Web of Science ®Google Scholar
• Baeten D, Sieper J, Braun J, Baraliakos X, Dougados M, Emery P, Deodhar A, Porter B, Martin R, Andersson M, et al. 2015. Secukinumab, an interleukin-17A inhibitor, in ankylosing spondylitis. N Engl J Med. 373(26):2534–48.
   PubMed Web of Science ®Google Scholar
• Bellaver B, Souza DG, Souza DO, Quincozes-Santos A. 2014. Resveratrol increases antioxidant defenses and decreases proinflammatory cytokines in hippocampal astrocyte cultures from newborn, adult and aged Wistar rats. Toxicol In Vitro. 28(4):479–84.
   PubMed Web of Science ®Google Scholar
• Bleil J, Maier R, Hempfing A, Sieper J, Appel H, Syrbe U. 2016. Granulation tissue eroding the subchondral bone also promotes new bone formation in ankylosing spondylitis. Arthritis Rheumatol. 68(10):2456–65.
   PubMed Web of Science ®Google Scholar
• Bleil J, Sieper J, Maier R, Schlichting U, Hempfing A, Syrbe U, Appel H. 2015. Cartilage in facet joints of patients with ankylosing spondylitis (AS) shows signs of cartilage degeneration rather than chondrocyte hypertrophy: implications for joint remodeling in as. Arthritis Res Ther. 17(1):170.
   PubMedGoogle Scholar
• Chedea VS, Vicas SI, Sticozzi C, Pessina F, Frosini M, Maioli E, Valacchi G. 2017. Resveratrol: from diet to topical usage. Food Funct. 8(11):3879–92.
   PubMed Web of Science ®Google Scholar
• Cui W, Sun C, Ma Y, Wang S, Wang X, Zhang Y. 2020. Inhibition of TLR4 induces M2 microglial polarization and provides neuroprotection via the NLRP3 inflammasome in alzheimer’s disease. Front Neurosci. 14:444.
   PubMed Web of Science ®Google Scholar
• Ding SJ, Xu S, Ma Y, Liu G, Jang HM, Fang J. 2019. Modulatory mechanisms of the NLRP3 inflammasomes in diabetes. Biomolecules. 9(12): undefined. doi:10.3390/biom9120850.
   Web of Science ®Google Scholar
• Donovan C, Liu G, Shen S, Marshall JE, Kim RY, Alemao CA, Budden KF, Choi JP, Kohonen-Corish M, El-Omar EM, et al. 2020. The role of the microbiome and the NLRP3 inflammasome in the gut and lung. J Leukoc Biol. 108(3):925–35.
   PubMed Web of Science ®Google Scholar
• Garcia-Hernandez V, Quiros M, Nusrat A. 2017. Intestinal epithelial claudins: expression and regulation in homeostasis and inflammation. Ann N Y Acad Sci. 1397(1):66–79.
   PubMed Web of Science ®Google Scholar
• Gill T, Asquith M, Rosenbaum JT, Colbert RA. 2015. The intestinal microbiome in spondyloarthritis. Curr Opin Rheumatol. 27(4):319–25.
   PubMed Web of Science ®Google Scholar
• Glant TT, Mikecz K, Arzoumanian A, Poole AR. 1987. Proteoglycan-induced arthritis in BALB/c mice. Clinical features and histopathology. Arthritis Rheum. 30(2):201–12.
   PubMedGoogle Scholar
• Grasberger H, Gao J, Nagao-Kitamoto H, Kitamoto S, Zhang M, Kamada N, Eaton KA, El-Zaatari M, Shreiner AB, Merchant JL, et al. 2015. Increased Expression of DUOX2 is an epithelial response to mucosal dysbiosis required for immune homeostasis in mouse intestine. Gastroenterology. 149:1849–59.
   PubMed Web of Science ®Google Scholar
• Haynes KR, Pettit AR, Duan R, Tseng HW, Glant TT, Brown MA, Thomas GP. 2012. Excessive bone formation in a mouse model of ankylosing spondylitis is associated with decreases in Wnt pathway inhibitors. Arthritis Res Ther. 14(6):R253.
   PubMed Web of Science ®Google Scholar
• Ishikawa LL, Colavite PM, da Rosa LC, Balbino B, Franca TG, Zorzella-Pezavento SF, Chiuso-Minicucci F, Sartori A. 2014. Commercial bovine proteoglycan is highly arthritogenic and can be used as an alternative antigen source for PGIA model. Biomed Res Int. 2014:148594.
   PubMed Web of Science ®Google Scholar
• Ishikawa J, Takahashi N, Matsumoto T, Yoshioka Y, Yamamoto N, Nishikawa M, Hibi H, Ishigro N, Ueda M, Furukawa K, et al. 2016. Factors secreted from dental pulp stem cells show multifaceted benefits for treating experimental rheumatoid arthritis. Bone. 83:210–19.
   PubMed Web of Science ®Google Scholar
• Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D. 2015. Role of the normal gut microbiota. World J Gastroenterol. 21(29):8787–803.
   PubMed Web of Science ®Google Scholar
• Kim SK, Cho YJ, Choe JY. 2018. NLRP3 inflammasomes and NLRP3 inflammasome-derived proinflammatory cytokines in peripheral blood mononuclear cells of patients with ankylosing spondylitis. Clin Chim Acta. 486:269–74.
   PubMed Web of Science ®Google Scholar
• Landy J, Ronde E, English N, Clark SK, Hart AL, Knight SC, Ciclitira PJ, Al-Hassi HO. 2016. Tight junctions in inflammatory bowel diseases and inflammatory bowel disease associated colorectal cancer. World J Gastroenterol. 22(11):3117–26.
   PubMed Web of Science ®Google Scholar
• Li X, Chen XX, Xu Y, Xu XB, Wu WF, Zhao Q, Hu JN. 2022. Construction of glycogen-based nanoparticles loaded with resveratrol for the alleviation of high-fat diet-induced nonalcoholic fatty liver disease. Biomacromolecules. 23(1):409–23.
   PubMed Web of Science ®Google Scholar
• Li H, Liu X, Chen F, Zuo K, Wu C, Yan Y, Chen W, Lin W, Xie Q. 2018. Avian influenza virus subtype H9N2 affects intestinal microbiota, barrier structure injury, and inflammatory intestinal disease in the chicken ileum. Viruses. 10(5):270.
   PubMed Web of Science ®Google Scholar
• Liu B, Ding ZH, Xiong JH, Heng X, Wang HF, Chu WH. 2022. Gut microbiota and inflammatory cytokine changes in patients with ankylosing spondylitis. Biomed Res Int. 2022(undefined):1005111.
   PubMedGoogle Scholar
• Liu M, Xie J, Sun Y. 2020. Tlr4/myd88/nf-κB-mediated inflammation contributes to cardiac dysfunction in rats of PTSD. Cell Mol Neurobiol. 40(6):1029–35.
   PubMed Web of Science ®Google Scholar
• Lories RJ, Haroon N. 2014. Bone formation in axial spondyloarthritis. Best Pract Res Clin Rheumatol. 28(5):765–77.
   PubMed Web of Science ®Google Scholar
• Lu JM, Jin GN, Lu YN, Zhao XD, Lan HW, Mu SR, Shen XY, Xu GH, Jin CH, Ma J, et al. 2021. Resveratrol modulates toxoplasma gondii infection induced liver injury by intervening in the HMGB1/TLR4/NF-kappaB signaling pathway. Eur J Pharmacol. 910:174497.
   PubMed Web of Science ®Google Scholar
• Lv LX, Hu XJ, Qian GR, Zhang H, Lu HF, Zheng BW, Jiang L, Li LJ. 2014. Administration of lactobacillus salivarius LI01 or pediococcus pentosaceus LI05 improves acute liver injury induced by D-galactosamine in rats. Appl Microbiol Biotechnol. 98(12):5619–32.
   PubMed Web of Science ®Google Scholar
• Maloy KJ, Powrie F. 2011. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 474:298–306.
   PubMed Web of Science ®Google Scholar
• Mir H, Meena AS, Chaudhry KK, Shukla PK, Gangwar R, Manda B, Padala MK, Shen L, Turner JR, Dietrich P, et al. 2016. Occludin deficiency promotes ethanol-induced disruption of colonic epithelial junctions, gut barrier dysfunction and liver damage in mice. Biochim Biophys Acta. 1860(4):765–74.
   PubMed Web of Science ®Google Scholar
• Molto A, Granger B, Wendling D, Dougados M, Gossec L. 2017. Use of nonsteroidal anti-inflammatory drugs in early axial spondyloarthritis in daily practice: data from the DESIR cohort. Joint Bone Spine. 84:79–82.
   PubMed Web of Science ®Google Scholar
• Neerinckx B, Lories R. 2017. Mechanisms, impact and prevention of pathological bone regeneration in spondyloarthritis. Curr Opin Rheumatol. 29(4):287–92.
   PubMed Web of Science ®Google Scholar
• Poulsen MM, Fjeldborg K, Ornstrup MJ, Kjaer TN, Nohr MK, Pedersen SB. 2015. Resveratrol and inflammation: challenges in translating pre-clinical findings to improved patient outcomes. Biochim Biophys Acta. 1852(6):1124–36.
   PubMed Web of Science ®Google Scholar
• Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE Jr., Balish E, Taurog JD, Hammer RE, Wilson KH, Sartor RB. 1996. Normal luminal bacteria, especially bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J Clin Invest. 98(4):945–53.
   PubMed Web of Science ®Google Scholar
• Rezaiemanesh A, Abdolmaleki M, Abdolmohammadi K, Aghaei H, Pakdel FD, Fatahi Y, Soleimanifar N, Zavvar M, Nicknam MH. 2018. Immune cells involved in the pathogenesis of ankylosing spondylitis. Biomed Pharmacother. 100:198–204.
   PubMed Web of Science ®Google Scholar
• Song X, Liu L, Peng SW, Liu T, Chen YQ, Jia RY, Zou YF, Li LX, Zhao XH, Liang XX, et al. 2022. Resveratrol regulates intestinal barrier function in cyclophosphamide-induced immunosuppressed mice. J Sci Food Agric. 102(3):1205–15.
   PubMed Web of Science ®Google Scholar
• Takaoka M. 1939. Resveratrol, a new phenolic compound, from veratrum grandiflorum. Nippon Kagaku Kaishi. 60(11):1090–100.
   Google Scholar
• Tian ZG, Yao M, Chen J. 2020. Micheliolide alleviates ankylosing spondylitis (AS) by suppressing the activation of the NLRP3 inflammasome and maintaining the balance of Th1/Th2 via regulating the NF-κB signaling pathway. Ann Transl Med. 8(16):991.
   PubMed Web of Science ®Google Scholar
• Tong W, Chen X, Song X, Chen Y, Jia R, Zou Y, Li L, Yin L, He C, Liang X, et al. 2020. Resveratrol inhibits LPS-induced inflammation through suppressing the signaling cascades of TLR4-NF-kappaB/mapks/irf3. Exp Ther Med. 19:1824–34.
   PubMed Web of Science ®Google Scholar
• Van Praet L, Jans L, Carron P, Jacques P, Glorieus E, Colman R, Cypers H, Mielants H, De Vos M, Cuvelier C, et al. 2014. Degree of bone marrow oedema in sacroiliac joints of patients with axial spondyloarthritis is linked to gut inflammation and male sex: results from the GIANT cohort. Ann Rheum Dis. 73(6):1186–89.
   PubMed Web of Science ®Google Scholar
• Van Praet L, Van den Bosch FE, Jacques P, Carron P, Jans L, Colman R, Glorieus E, Peeters H, Mielants H, De Vos M, et al. 2013. Microscopic gut inflammation in axial spondyloarthritis: a multiparametric predictive model. Ann Rheum Dis. 72(3):414–17.
   PubMed Web of Science ®Google Scholar
• Wang J, Fan SM, Zhang J. 2019. Epigallocatechin-3-gallate ameliorates lipopolysaccharide-induced acute lung injury by suppression of TLR4/NF-κB signaling activation. Braz J Med Biol Res. 52(7):e8092.
   PubMed Web of Science ®Google Scholar
• Wang G, Hu Z, Fu Q, Song X, Cui Q, Jia R, Zou Y, He C, Li L, Yin Z. 2017. Resveratrol mitigates lipopolysaccharide-mediated acute inflammation in rats by inhibiting the TLR4/NF-κBp65/MAPKs signaling cascade. Sci Rep. 7:45006. https://doi.org/10.1038/srep45006
   Google Scholar
• Wen C, Zheng Z, Shao T, Liu L, Xie Z, Le Chatelier E, He Z, Zhong W, Fan Y, Zhang L, et al. 2017. Quantitative metagenomics reveals unique gut microbiome biomarkers in ankylosing spondylitis. Genome Biol. 18(1):142.
   PubMedGoogle Scholar
• Wu X, Xu W, Feng X, He Y, Liu X, Gao Y, Yang S, Shao Z, Yang C, Ye Z. 2015. TNF-a mediated inflammatory macrophage polarization contributes to the pathogenesis of steroid-induced osteonecrosis in mice. Int J Immunopathol Pharmacol. 28(3):351–61.
   PubMed Web of Science ®Google Scholar
• Wu LY, Ye ZN, Zhuang Z, Gao Y, Tang C, Zhou CH, Wang CX, Zhang XS, Xie GB, Liu JP, et al. 2018. Biochanin a reduces inflammatory injury and neuronal apoptosis following subarachnoid hemorrhage via suppression of the TLRs/TIRAP/MyD88/NF-kappaB pathway. Behav Neurol. 2018:1960106.
   PubMed Web of Science ®Google Scholar
• Yang Y, Dai M. 2015. Expression of PADI4 in patients with ankylosing spondylitis and its role in mediating the effects of TNF-α on the proliferation and osteogenic differentiation of human mesenchymal stem cells. Int J Mol Med. 36(2):565–70.
   PubMed Web of Science ®Google Scholar
• Yuan Q, Zhang X, Liu Z, Song S, Xue P, Wang J, Ruan J. 2013. Ethanol extract of Adiantum capillus-veneris L. suppresses the production of inflammatory mediators by inhibiting NF-κB activation. J Ethnopharmacol. 147(3):603–11.
   PubMed Web of Science ®Google Scholar
• Yu Z, Zhang Y, Gao N, Yong K. 2015. Suppression of development of ankylosing spondylitis through soluble flt-1. Cell Physiol Biochem. 37(6):2135–42.
   PubMedGoogle Scholar
• Zhang XN, Yu ZL, Chen JY, Li XY, Wang ZP, Wu M, Liu LT. 2022. The crosstalk between NLRP3 inflammasome and gut microbiome in atherosclerosis. Pharmacol Res. 181:106289.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Zeng J, Li Y, Liao Q, Huang D, Zou Y, Liu G. 2021. Tail suspension delays ectopic ossification in proteoglycan-induced ankylosing spondylitis in mice via miR-103/DKK1. Exp Ther Med. 22(3):965.
   PubMed Web of Science ®Google Scholar
• Zhang C, Zhao XH, Yang L, Chen XY, Jiang RS, Jin SH, Geng ZY. 2017. Resveratrol alleviates heat stress-induced impairment of intestinal morphology, microflora, and barrier integrity in broilers. Poult Sci. 96(12):4325–32.
   PubMed Web of Science ®Google Scholar
• Zhao X, Xu J, Song X, Jia R, Yin Z, Cheng A, Jia R, Zou Y, Li L, Yin L, et al. 2016. Antiviral effect of resveratrol in ducklings infected with virulent duck enteritis virus. Antiviral Res. 130:93–100.
   PubMed Web of Science ®Google Scholar
• Zhou L, Xiao X, Zhang Q, Zheng J, Deng M. 2019. Deciphering the anti-obesity benefits of resveratrol: the “Gut microbiota-adipose tissue” axis. Front Endocrinol (Lausanne). 10:413.
   PubMed Web of Science ®Google Scholar
• Zhu W, He X, Cheng K, Zhang L, Chen D, Wang X, Qiu G, Cao X, Weng X. 2019. Ankylosing spondylitis: etiology, pathogenesis, and treatments. Bone Res. 7(1):22.
   PubMedGoogle Scholar