1,335
Views
4
CrossRef citations to date
0
Altmetric
Research Article

Glucocorticoid receptors involved in ginsenoside compound K ameliorate adjuvant arthritis by inhibiting the glycolysis of fibroblast-like synoviocytes via the NF-κB/HIF-1α pathway

, , , , , , , & show all
Pages 1162-1174 | Received 04 Dec 2022, Accepted 22 Jul 2023, Published online: 09 Aug 2023

References

  • Bartok B, Firestein GS. 2010. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev. 233(1):233–255. doi: 10.1111/j.0105-2896.2009.00859.x.
  • Belaiba RS, Bonello S, Zähringer C, Schmidt S, Hess J, Kietzmann T, Görlach A. 2007. Hypoxia up-regulates hypoxia-inducible factor-1α transcription by involving phosphatidylinositol 3-kinase and nuclear factor κB in pulmonary artery smooth muscle cells. Mol Biol Cell. 18(12):4691–4697. doi: 10.1091/mbc.e07-04-0391.
  • Bustamante MF, Oliveira PG, Garcia-Carbonell R, Croft AP, Smith JM, Serrano RL, Sanchez-Lopez E, Liu X, Kisseleva T, Hay N, et al. 2018. Hexokinase 2 as a novel selective metabolic target for rheumatoid arthritis. Ann Rheum Dis. 77(11):1636–1643. doi: 10.1136/annrheumdis-2018-213103.
  • Chen J, Si M, Wang Y, Liu L, Zhang Y, Zhou A, Wei W. 2019. Ginsenoside metabolite compound K exerts anti-inflammatory and analgesic effects via downregulating COX2. Inflammopharmacology. 27(1):157–166. doi: 10.1007/s10787-018-0504-y.
  • Damerau A, Gaber T. 2020. Modeling rheumatoid arthritis in vitro: from experimental feasibility to physiological proximity. Int J Mol Sci. 21:7916. doi: 10.3390/ijms21217916.
  • De Bosscher K, Vanden Berghe W, Beck IM, Van Molle W, Hennuyer N, Hapgood J, Libert C, Staels B, Louw A, Haegeman G. 2005. A fully dissociated compound of plant origin for inflammatory gene repression. Proc Natl Acad Sci U S A. 102(44):15827–15832. doi: 10.1073/pnas.0505554102.
  • de Oliveira PG, Farinon M, Sanchez-Lopez E, Miyamoto S, Guma M. 2019. Fibroblast-like synoviocytes glucose metabolism as a therapeutic target in rheumatoid arthritis. Front Immunol. 10:1743. doi: 10.3389/fimmu.2019.01743.
  • Falconer J, Murphy AN, Young SP, Clark AR, Tiziani S, Guma M, Buckley CD. 2018. Review: synovial cell metabolism and chronic inflammation in rheumatoid arthritis. Arthritis Rheumatol. 70(7):984–999. doi: 10.1002/art.40504.
  • Fearon U, Hanlon MM, Wade SM, Fletcher JM. 2019. Altered metabolic pathways regulate synovial inflammation in rheumatoid arthritis. Clin Exp Immunol. 197(2):170–180. doi: 10.1111/cei.13228.
  • Filer A. 2013. The fibroblast as a therapeutic target in rheumatoid arthritis. Curr Opin Pharmacol. 13(3):413–419. doi: 10.1016/j.coph.2013.02.006.
  • Garcia-Carbonell R, Divakaruni AS, Lodi A, Vicente-Suarez I, Saha A, Cheroutre H, Boss GR, Tiziani S, Murphy AN, Guma M. 2016. Critical role of glucose metabolism in rheumatoid arthritis fibroblast-like synoviocytes. Arthritis Rheumatol. 68(7):1614–1626. doi: 10.1002/art.39608.
  • Hasegawa H. 2004. Proof of the mysterious efficacy of ginseng: basic and clinical trials: metabolic activation of ginsenoside: deglycosylation by intestinal bacteria and esterification with fatty acid. J Pharmacol Sci. 95(2):153–157. doi: 10.1254/jphs.fmj04001x4.
  • Hayden MS, Ghosh S. 2008. Shared principles in NF-κB signaling. Cell. 132(3):344–362. doi: 10.1016/j.cell.2008.01.020.
  • Hayden MS, Ghosh S. 2012. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 26(3):203–234. doi: 10.1101/gad.183434.111.
  • Korb A, Pavenstädt H, Pap T. 2009. Cell death in rheumatoid arthritis. Apoptosis. 14(4):447–454. doi: 10.1007/s10495-009-0317-y.
  • Korbecki J, Simińska D, Gąssowska-Dobrowolska M, Listos J, Gutowska I, Chlubek D, Baranowska-Bosiacka I. 2021. Chronic and cycling hypoxia: drivers of cancer chronic inflammation through HIF-1 and NF-κB activation: a review of the molecular mechanisms. Int J Mol Sci. 22:10701. doi: 10.3390/ijms221910701.
  • Lee JW, Kim MO, Song YN, Min JH, Kim SM, Kang MJ, Oh ES, Lee RW, Jung S, Ro H, et al. 2022. Compound K ameliorates airway inflammation and mucus secretion through the regulation of PKC signaling in vitro and in vivo. J Ginseng Res. 46(3):496–504. doi: 10.1016/j.jgr.2021.12.008.
  • Li J, Zhang J, Xie F, Peng J, Wu X. 2018. Macrophage migration inhibitory factor promotes Warburg effect via activation of the NF‑κB/HIF‑1α pathway in lung cancer. Int J Mol Med. 41(2):1062–1068. doi: 10.3892/ijmm.2017.3277.
  • Li PP, Liu DD, Liu YJ, Song SS, Wang QT, Chang Y, Wu YJ, Chen JY, Zhao WD, Zhang LL, et al. 2012. BAFF/BAFF-R involved in antibodies production of rats with collagen-induced arthritis via PI3K-Akt-mTOR signaling and the regulation of paeoniflorin. J Ethnopharmacol. 141(1):290–300. doi: 10.1016/j.jep.2012.02.034.
  • Liu KK, Wang QT, Yang SM, Chen JY, Wu HX, Wei W. 2014. Ginsenoside compound K suppresses the abnormal activation of T lymphocytes in mice with collagen-induced arthritis. Acta Pharmacol Sin. 35(5):599–612. doi: 10.1038/aps.2014.7.
  • Liu T, Zhu L, Wang L. 2022. A narrative review of the pharmacology of ginsenoside compound K. Ann Transl Med. 10(4):234. doi: 10.21037/atm-22-501.
  • Luan H, Gu W, Li H, Wang Z, Lu L, Ke M, Lu J, Chen W, Lan Z, Xiao Y, et al. 2021. Serum metabolomic and lipidomic profiling identifies diagnostic biomarkers for seropositive and seronegative rheumatoid arthritis patients. J Transl Med. 19(1):500. doi: 10.1186/s12967-021-03169-7.
  • Luo W, Hu H, Chang R, Zhong J, Knabel M, O'Meally R, Cole RN, Pandey A, Semenza GL. 2011. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell. 145(5):732–744. doi: 10.1016/j.cell.2011.03.054.
  • Masoud GN, Li W. 2015. HIF-1α pathway: role, regulation and intervention for cancer therapy. Acta Pharm Sin B. 5(5):378–389. doi: 10.1016/j.apsb.2015.05.007.
  • Masoumi M, Mehrabzadeh M, Mahmoudzehi S, Mousavi MJ, Jamalzehi S, Sahebkar A, Karami J. 2020. Role of glucose metabolism in aggressive phenotype of fibroblast-like synoviocytes: latest evidence and therapeutic approaches in rheumatoid arthritis. Int Immunopharmacol. 89(Pt A):107064. doi: 10.1016/j.intimp.2020.107064.
  • Mathupala SP, Rempel A, Pedersen PL. 2001. Glucose catabolism in cancer cells: identification and characterization of a marked activation response of the type II hexokinase gene to hypoxic conditions. J Biol Chem. 276(46):43407–43412. doi: 10.1074/jbc.M108181200.
  • McGarry T, Biniecka M, Gao W, Cluxton D, Canavan M, Wade S, Wade S, Gallagher L, Orr C, Veale DJ, et al. 2017. Resolution of TLR2-induced inflammation through manipulation of metabolic pathways in rheumatoid arthritis. Sci Rep. 7:43165. doi: 10.1038/srep43165.
  • McGarry T, Orr C, Wade S, Biniecka M, Wade S, Gallagher L, Low C, Veale DJ, Fearon U. 2018. JAK/STAT blockade alters synovial bioenergetics, mitochondrial function, and proinflammatory mediators in rheumatoid arthritis. Arthritis Rheumatol. 70(12):1959–1970. doi: 10.1002/art.40569.
  • Mor A, Abramson SB, Pillinger MH. 2005. The fibroblast-like synovial cell in rheumatoid arthritis: a key player in inflammation and joint destruction. Clin Immunol. 115(2):118–128. doi: 10.1016/j.clim.2004.12.009.
  • Morita M, Sato T, Nomura M, Sakamoto Y, Inoue Y, Tanaka R, Ito S, Kurosawa K, Yamaguchi K, Sugiura Y, et al. 2018. PKM1 confers metabolic advantages and promotes cell-autonomous tumor cell growth. Cancer Cell. 33(3):355–367.e7. doi: 10.1016/j.ccell.2018.02.004.
  • Nygaard G, Firestein GS. 2020. Restoring synovial homeostasis in rheumatoid arthritis by targeting fibroblast-like synoviocytes. Nat Rev Rheumatol. 16(6):316–333. doi: 10.1038/s41584-020-0413-5.
  • Quiñonez-Flores CM, González-Chávez SA, Pacheco-Tena C. 2016. Hypoxia and its implications in rheumatoid arthritis. J Biomed Sci. 23(1):62. doi: 10.1186/s12929-016-0281-0.
  • Schormann N, Hayden KL, Lee P, Banerjee S, Chattopadhyay D. 2019. An overview of structure, function, and regulation of pyruvate kinases. Protein Sci. 28(10):1771–1784. doi: 10.1002/pro.3691.
  • Song G, Lu Q, Fan H, Zhang X, Ge L, Tian R, Wang S, Feng T, Pan J, Feng J, et al. 2019. Inhibition of hexokinases holds potential as treatment strategy for rheumatoid arthritis. Arthritis Res Ther. 21(1):87. doi: 10.1186/s13075-019-1865-3.
  • Song W, Wei L, Du Y, Wang Y, Jiang S. 2018. Protective effect of ginsenoside metabolite compound K against diabetic nephropathy by inhibiting NLRP3 inflammasome activation and NF-κB/p38 signaling pathway in high-fat diet/streptozotocin-induced diabetic mice. Int Immunopharmacol. 63:227–238. doi: 10.1016/j.intimp.2018.07.027.
  • Spencer NY, Stanton RC. 2019. The Warburg effect, lactate, and nearly a century of trying to cure cancer. Semin Nephrol. 39(4):380–393. doi: 10.1016/j.semnephrol.2019.04.007.
  • Sundahl N, Bridelance J, Libert C, De Bosscher K, Beck IM. 2015. Selective glucocorticoid receptor modulation: new directions with non-steroidal scaffolds. Pharmacol Ther. 152:28–41. doi: 10.1016/j.pharmthera.2015.05.001.
  • Taniguchi K, Karin M. 2018. NF-κB, inflammation, immunity and cancer: coming of age. Nat Rev Immunol. 18(5):309–324. doi: 10.1038/nri.2017.142.
  • Wang CW, Huang YC, Chan FN, Su SC, Kuo YH, Huang SF, Hung MW, Lin HC, Chang WL, Chang TC. 2015. A gut microbial metabolite of ginsenosides, compound K, induces intestinal glucose absorption and Na+/glucose cotransporter 1 gene expression through activation of cAMP response element binding protein. Mol Nutr Food Res. 59(4):670–684. doi: 10.1002/mnfr.201400688.
  • Wang D, Chang Y, Wu Y, Zhang L, Yan S, Xie G, Qin Q, Jin J, Wang W, Fang J, et al. 2011. Therapeutic effects of TACI-Ig on rat with adjuvant arthritis. Clin Exp Immunol. 163(2):225–234. doi: 10.1111/j.1365-2249.2010.04293.x.
  • Wang Q, Xu B, Fan K, Wu J, Wang T. 2020. Inflammation suppression by dexamethasone via inhibition of CD147-mediated NF-κB pathway in collagen-induced arthritis rats. Mol Cell Biochem. 473(1-2):63–76. doi: 10.1007/s11010-020-03808-5.
  • Wang Y, Chen J, Luo X, Zhang Y, Si M, Wu H, Yan C, Wei W. 2016. Ginsenoside metabolite compound K exerts joint-protective effect by interfering with synoviocyte function mediated by TNF-α and tumor necrosis factor receptor type 2. Eur J Pharmacol. 771:48–55. doi: 10.1016/j.ejphar.2015.12.019.
  • Wang Y, Xian H, Qi J, Wei F, Cheng X, Li S, Wang Q, Liu Z, Yu Y, Zhou J, et al. 2020. Inhibition of glycolysis ameliorate arthritis in adjuvant arthritis rats by inhibiting synoviocyte activation through AMPK/NF-кB pathway. Inflamm Res. 69(6):569–578. doi: 10.1007/s00011-020-01332-2.
  • Wu H, Chen J, Wang Q, Jia X, Song S, Yuan P, Liu K, Liu L, Zhang Y, Zhou A, et al. 2014. Ginsenoside metabolite compound K attenuates inflammatory responses of adjuvant-induced arthritis rats. Immunopharmacol Immunotoxicol. 36(2):124–129. doi: 10.3109/08923973.2014.880717.
  • Zeng G, Chen F, Xiong X, Liang Q, Chen T, Song W, Huang H. 2013. Effects of ursolic acid on arthritis and bone destruction in collagen-induced CIA rats. J Hunan Univ Chin Med. 33(07):3–7. Chinese.
  • Zhao J, Guo S, Schrodi SJ, He D. 2021. Molecular and cellular heterogeneity in rheumatoid arthritis: mechanisms and clinical implications. Front Immunol. 12:790122. doi: 10.3389/fimmu.2021.790122.
  • Zheng F, Chen J, Zhang X, Wang Z, Chen J, Lin X, Huang H, Fu W, Liang J, Wu W, et al. 2021. The HIF-1α antisense long non-coding RNA drives a positive feedback loop of HIF-1α mediated transactivation and glycolysis. Nat Commun. 12(1):1341. doi: 10.1038/s41467-021-21535-3.
  • Zhou J, Yu Y, Yang X, Wang Y, Song Y, Wang Q, Chen Z, Zong S, Fan M, Meng X, et al. 2019. Berberine attenuates arthritis in adjuvant-induced arthritic rats associated with regulating polarization of macrophages through AMPK/NF-кB pathway. Eur J Pharmacol. 852:179–188. doi: 10.1016/j.ejphar.2019.02.036.
  • Zhou MY, Cai L, Feng XW, Mu YR, Meng B, Liu FY, Li R. 2021. Lentivirus-mediated overexpression or silencing of aquaporin 1 affects the proliferation, migration and invasion of TNF-α-stimulated rheumatoid arthritis fibroblast-like synoviocytes by Wnt/β-Catenin signaling pathway. J Inflamm Res. 14:1945–1957. doi: 10.2147/JIR.S312783.