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Role of Long Intergenic Nonprotein-Coding RNA 00511 in Nod-Like Receptor Protein Pyrin Domain 3-Induced Chondrocyte Pyroptosis via the MicroRNA-9-5p/FUT1 Axis

  • Tianjun Zhai (School of Rehabilitation Science, Shanghai University of Traditional Chinese Medicine) ;
  • Zengqiao Zhang (Tuina Department of Yueyang Hospital of Integrated Traditional Chinese and Western Medicine Affiliated to Shanghai University of Traditional Chinese Medicine) ;
  • Xiaoshen Hu (School of Health Preservation and Rehabilitation, Chengdu University of Traditional Chinese Medicine) ;
  • Dongyi He (Rheumatoid Internal Medicine in Shanghai Guanghua Hospital of Integrated Traditional Chinese and Western Medicine) ;
  • Wei Feng (School of Rehabilitation Science, Shanghai University of Traditional Chinese Medicine)
  • Received : 2023.12.12
  • Accepted : 2024.03.29
  • Published : 2024.07.28

Abstract

This study aimed to determine the function of LINC00511 in Nod-Like Receptor Pyrin Domain 3 inflammasome-mediated chondrocyte pyroptosis via the regulation of miR-9-5p and FUT 1. Chondrocyte inflammatory injury was induced by treating chondrocytes with LPS. Afterwards, the levels of IL-1β and IL-18, the expression of NLRP3, ASC, Caspase-1, and GSDMD, cell viability, and LDH activity in chondrocytes were assessed. LINC00511 expression in LPS-treated chondrocytes was detected, and LINC00511 was subsequently silenced to analyse its role in chondrocyte pyroptosis. The subcellular localization of LINC00511 was predicted and verified. Furthermore, the binding relationships between LINC00511 and miR-9-5p and between miR-9-5p and FUT1 were validated. LINC00511 regulated NLRP3 inflammasome-mediated chondrocyte pyroptosis through the miR-9-5p/FUT1 axis. LPS-treated ATDC5 cells exhibited elevated levels of inflammatory injury; increased levels of NLRP3, ASC, Caspase-1, and GSDMD; reduced cell viability; increased LDH activity; and increased LINC00511 expression, while LINC00511 silencing inhibited the NLRP3 inflammasome to restrict LPS-induced chondrocyte pyroptosis. Next, LINC00511 sponged miR-9-5p, which targeted FUT1. Silencing LINC00511 suppressed FUT1 by upregulating miR-9-5p. Additionally, downregulation of miR-9-5p or overexpression of FUT1 neutralized the suppressive effect of LINC00511 knockdown on LPS-induced chondrocyte pyroptosis. Silencing LINC00511 inhibited the NLRP3 inflammasome to quench Caspase-1-dependent chondrocyte pyroptosis in OA by promoting miR-9-5p and downregulating FUT1.

Keywords

Acknowledgement

This work was supported by the Scientific Research Fund of the National Natural Science Foundation of China (81873328, 82205239) and the China Postdoctoral Science Foundation (No. 2021MD703797).

References

  1. Yan Z, Qi W, Zhan J, Lin Z, Lin J, Xue X, et al. 2020. Activating Nrf2 signalling alleviates osteoarthritis development by inhibiting inflammasome activation. J. Cell. Mol. Med. 24: 13046-13057.
  2. Glyn-Jones S, Palmer AJ, Agricola R, Price AJ, Vincent TL, Weinans H, et al. 2015. Osteoarthritis. Lancet 386: 376-387.
  3. Nelson AE. 2018. Osteoarthritis year in review 2017: clinical. Osteoarthritis Cartilage 26: 319-325.
  4. Pereira D, Ramos E, Branco J. 2015. Osteoarthritis. Acta Med. Port. 28: 99-106.
  5. Ali Syeda Z, Langden SSS, Munkhzul C, Lee M, Song SJ. 2020. Regulatory mechanism of microRNA expression in cancer. Int. J. Mol. Sci. 21: 1723.
  6. Geyer M, Schonfeld C. 2018. Novel Insights into the pathogenesis of osteoarthritis. Curr. Rheumatol. Rev. 14: 98-107.
  7. Liu G, Wang Y, Zhang M, Zhang Q. 2019. Long noncoding RNA THRIL promotes LPS-induced inflammatory injury by downregulating microRNA-125b in ATDC5 cells. Int. Immunopharmacol. 66: 354-361.
  8. Hu P, Cui H, Lei T, Li S, Mai E, Jia F. 2019. Linc00511 Indicates a poor prognosis of liver hepatocellular carcinoma. Onco Targets Ther. 12: 9367-9376.
  9. Mao BD, Xu P, Xu P, Zhong Y, Ding WW, Meng QZ. 2019. LINC00511 knockdown prevents cervical cancer cell proliferation and reduces resistance to paclitaxel. J. Biosci. 44: 44.
  10. Rozi R, Zhou Y, Rong K, Chen P. 2022. miR-124-3p sabotages lncRNA MALAT1 stability to repress chondrocyte pyroptosis and relieve cartilage injury in osteoarthritis. J. Orthop. Surg. Res. 17: 453.
  11. Gao Y, Zhao H, Li Y. 2019. LncRNA MCM3AP-AS1 regulates miR-142-3p/HMGB1 to promote LPS-induced chondrocyte apoptosis. BMC Musculoskelet. Disord. 20: 605.
  12. Zhang Y, Dong Q, Sun X. 2020. Positive feedback loop LINC00511/miR-150-5p/SP1 modulates chondrocyte apoptosis and proliferation in osteoarthritis. DNA Cell Biol. 39: 1506-1512.
  13. Chen Z, Wu H, Zhang Z, Li G, Liu B. 2019. LINC00511 accelerated the process of gastric cancer by targeting miR-625-5p/NFIX axis. Cancer Cell Int. 19: 351.
  14. Lu G, Li Y, Ma Y, Lu J, Chen Y, Jiang Q, et al. 2018. Long noncoding RNA LINC00511 contributes to breast cancer tumourigenesis and stemness by inducing the miR-185-3p/E2F1/Nanog axis. J. Exp. Clin. Cancer Res. 37: 289.
  15. Swingler TE, Niu L, Smith P, Paddy P, Le L, Barter MJ, et al. 2019. The function of microRNAs in cartilage and osteoarthritis. Clin. Exp. Rheumatol. 37 Suppl 120: 40-47.
  16. Chen H, Yang J, Tan Z. 2019. Upregulation of microRNA-9-5p inhibits apoptosis of chondrocytes through downregulating Tnc in mice with osteoarthritis following tibial plateau fracture. J. Cell. Physiol. 234: 23326-23336.
  17. Tang H, Han X, Feng Y, Hao Y. 2020. linc00968 inhibits the tumorigenesis and metastasis of lung adenocarcinoma via serving as a ceRNA against miR-9-5p and increasing CPEB3. Agng (Albany NY) 12: 22582-22598.
  18. Xie CH, Cao YM, Huang Y, Shi QW, Guo JH, Fan ZW, et al. 2016. Long non-coding RNA TUG1 contributes to tumorigenesis of human osteosarcoma by sponging miR-9-5p and regulating POU2F1 expression. Tumour Biol. 37: 15031-15041.
  19. Isozaki T, Amin MA, Ruth JH, Campbell PL, Tsou PS, Ha CM, et al. 2014. Fucosyltransferase 1 mediates angiogenesis in rheumatoid arthritis. Arthritis Rheumatol. 66: 2047-2058.
  20. Li Z, Wang J, Yang J. 2020. TUG1 knockdown promoted viability and inhibited apoptosis and cartilage ECM degradation in chondrocytes via the miR-17-5p/FUT1 pathway in osteoarthritis. Exp. Ther. Med. 20: 154.
  21. Wang L, Shen S, Xiao H, Ding F, Wang M, Li G, et al. 2020. ARHGAP24 inhibits cell proliferation and cell cycle progression and induces apoptosis of lung cancer via a STAT6-WWP2-p27 axis. Carcinogenesis 41: 711-721.
  22. Poh L, Kang SW, Baik SH, Ng GYQ, She DT, Balaganapathy P, et al. 2019. Evidence that NLRC4 inflammasome mediates apoptotic and pyroptotic microglial death following ischemic stroke. Brain Behav. Immun. 75: 34-47.
  23. Chen X, Chen RX, Wei WS, Li YH, Feng ZH, Tan L, et al. 2018. PRMT5 Circular RNA promotes metastasis of urothelial carcinoma of the bladder through sponging miR-30c to induce epithelial-mesenchymal transition. Clin. Cancer Res. 24: 6319-6330.
  24. Abramoff B, Caldera FE. 2020. Osteoarthritis: Pathology, diagnosis, and treatment options. Med. Clin. North Am. 104: 293-311.
  25. Fang Y, Tian S, Pan Y, Li W, Wang Q, Tang Y, et al. 2020. Pyroptosis: A new frontier in cancer. Biomed. Pharmacother. 121: 109595.
  26. Agbana YL, Abi ME, Ni Y, Xiong G, Chen J, Yun F, et al. 2020. LINC00511 as a prognostic biomarker for human cancers: a systematic review and meta-analysis. BMC Cancer 20: 682.
  27. Zu Y, Mu Y, Li Q, Zhang ST, Yan HJ. 2019. Icariin alleviates osteoarthritis by inhibiting NLRP3-mediated pyroptosis. J. Orthop. Surg. Res. 14: 307.
  28. Hu PF, Chen WP, Bao JP, Wu LD. 2018. Paeoniflorin inhibits IL-1beta-induced chondrocyte apoptosis by regulating the Bax/Bcl-2/ caspase-3 signaling pathway. Mol. Med. Rep. 17: 6194-6200.
  29. Li J, Li Y, Meng F, Fu L, Kong C. 2018. Knockdown of long non-coding RNA linc00511 suppresses proliferation and promotes apoptosis of bladder cancer cells Wnt/beta-catenin signaling pathway. Biosci. Rep. 38: BSR20171701.
  30. Wang RP, Jiang J, Jiang T, Wang Y, Chen LX. 2019. Increased long noncoding RNA LINC00511 is correlated with poor prognosis and contributes to cell proliferation and metastasis by modulating miR-424 in hepatocellular carcinoma. Eur. Rev. Med. Pharmacol. Sci. 23: 3291-3301.
  31. Yu CL, Xu XL, Yuan F. 2019. LINC00511 is associated with the malignant status and promotes cell proliferation and motility in cervical cancer. Biosci. Rep. 39: BSR20190903.
  32. Yan L, Wu X, Liu Y, Xian W. 2018. LncRNA Linc00511 promotes osteosarcoma cell proliferation and migration through sponging miR-765. J. Cell. Biochem. 120: 7248-7256.
  33. Zhang J, Zhou M, Zhao X, Wang G, Li J. 2020. Long noncoding RNA LINC00173 is downregulated in cervical cancer and inhibits cell proliferation and invasion by modulating the miR-182-5p/FBXW7 axis. Pathol. Res. Pract. 216: 152994.
  34. Li F, Dai B, Ni X. 2020. Long non-coding RNA cancer susceptibility candidate 2 (CASC2) alleviates the high glucose-induced injury of CIHP-1 cells via regulating miR-9-5p/PPARgamma axis in diabetes nephropathy. Diabetol. Metab. Syndr. 12: 68.
  35. Zhao J, Pu J, Hao B, Huang L, Chen J, Hong W, et al. 2020. LncRNA RP11-86H7.1 promotes airway inflammation induced by TRAPM2.5 by acting as a ceRNA of miRNA-9-5p to regulate NFKB1 in HBECS. Sci. Rep. 10: 11587.
  36. Jin Z, Ren J, Qi S. 2020. Exosomal miR-9-5p secreted by bone marrow-derived mesenchymal stem cells alleviates osteoarthritis by inhibiting syndecan-1. Cell Tissue Res. 381: 99-114.
  37. Roshanravan N, Alamdari NM, Jafarabadi MA, Mohammadi A, Shabestari BR, Nasirzadeh N, et al. 2020. Effects of oral butyrate and inulin supplementation on inflammation-induced pyroptosis pathway in type 2 diabetes: A randomized, double-blind, placebo-controlled trial. Cytokine 131: 155101.
  38. Ou M, Zhang Y, Cui S, Zhao S, Tu J. 2019. Upregulated MiR-9-5p protects against inflammatory response in rats with deep vein thrombosis via inhibition of NF-kappaB p50. Inflammation 42: 1925-1938.
  39. Chi L, Jiao D, Nan G, Yuan H, Shen J, Gao Y. 2019. miR-9-5p attenuates ischemic stroke through targeting ERMP1-mediated endoplasmic reticulum stress. Acta Histochem. 121: 151438.
  40. Jiang HY, Wang ZJ. 2020. ADPGK-AS1 promotes the progression of colorectal cancer via sponging miR-525 to upregulate FUT1. Eur. Rev. Med. Pharmacol. Sci. 24: 2380-2386.
  41. Wang Z, Hu J, Pan Y, Shan Y, Jiang L, Qi X, et al. 2018. miR-140-5p/miR-149 affects chondrocyte proliferation, apoptosis, and autophagy by targeting FUT1 in osteoarthritis. Inflammation 41: 959-971.
  42. Amin MA, Campbell PL, Ruth JH, Isozaki T, Rabquer BJ, Alex Stinson W, et al. 2015. A key role for Fut1-regulated angiogenesis and ICAM-1 expression in K/BxN arthritis. Ann. Rheum. Dis. 74: 1459-1466.
  43. Isozaki T, Ruth JH, Amin MA, Campbell PL, Tsou PS, Ha CM, et al. 2014. Fucosyltransferase 1 mediates angiogenesis, cell adhesion and rheumatoid arthritis synovial tissue fibroblast proliferation. Arthritis Res. Ther. 16: R28.