Biomolecules & Therapeutics

  • 제28권5호
  • /
  • Pages.405-413
  • /
  • 2020
  • /
  • 1976-9148(pISSN)
  • /
  • 2005-4483(eISSN)
한국응용약물학회 (The Korean Society of Applied Pharmacology)
권호 표지
DOI QR코드

DOI QR Code

Synovial Cell Migration is Associated with B Cell Activating Factor Expression Increased by TNFα or Decreased by KR33426

  • Lee, Jiyoung (Department of Bioscience and Biotechnology, Sejong University) ;
  • Yoon, Sung Sik (Department of Bioscience and Biotechnology, Sejong University) ;
  • Thuy, Pham Xuan (Department of Bioscience and Biotechnology, Sejong University) ;
  • Moon, Eun-Yi (Department of Bioscience and Biotechnology, Sejong University)
  • 투고 : 2020.06.26
  • 심사 : 2020.07.13
  • 발행 : 2020.09.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Fibroblast-like synoviocytes (FLS) play a crucial role in initiating rheumatoid arthritis. B-cell activating factor (BAFF) plays a role in FLS survival as well as in B cell maturation and maintenance. Here, we investigated whether tumor necrosis factor (TNF)-α-induced BAFF expression controls FLS migration and whether BAFF expression in FLS could be regulated by KR33426 which is the inhibitor of BAFF binding to BAFF receptors (BAFF-R) by using MH7A synovial cells transfected with the SV40 T antigen. More TNF-α-treated cells migrated compared to the control. TNF-α increased BAFF expression in FLS, significantly. FLS migration was inhibited by the transfection with BAFF-siRNA. KR33426 also inhibited BAFF expression increased by TNF-α treatment in FLS as judged by western blotting, PCR, and transcriptional activity assay. Kinases including JNK, p38 and Erk were activated by TNF-α treatment. While JNK and p38 were inhibited by KR33426 treatment, no changes in Erk were observed. Transcription factors including p65, c-Fos, CREB and SP1 were enhanced by TNF-α treatment. Among them, c-Fos was inhibited by KR33426 treatment. Small interference(si)-RNA of c-fos decreased BAFF transcriptional activity. FLS migration induced by TNF-α was inhibited by the transfection with BAFF-siRNA. KR33426 increased Twist, Snail, Cadherin-11 and N-Cadherin. In contrast, KR33426 decreased E-cadherin and TNF-α-enhanced CCL2. Taken together, our results demonstrate that synovial cell migration via CCL2 expression could be regulated by BAFF expression which is decreased by KR33426 and c-Fos-siRNA. It suggests for the first time that the role of BAFF-siRNA on FLS migration might be matched in the effect of KR33426 on BAFF expression.

키워드

참고문헌

  1. Abraham, D. J., Eckes, B., Rajkumar, V. and Krieg, T. (2007) New developments in fibroblast and myofibroblast biology: implications for fibrosis and scleroderma. Curr. Rheumatol. Rep. 9, 136-143. https://doi.org/10.1007/s11926-007-0008-z
  2. Agarwal, S. K., Lee, D. M., Kiener, H. P. and Brenner, M. B. (2008) Coexpression of two mesenchymal cadherins, cadherin 11 and N-cadherin, on murine fibroblast-like synoviocytes. Arthritis Rheum. 58, 1044-1054. https://doi.org/10.1002/art.23369
  3. Di Carlo, E., D'Antuono, T., Pompa, P., Giuliani, R., Rosini, S., Stuppia, L., Musiani, P. and Sorrentino, C. (2009) The lack of epithelial interleukin-7 and BAFF/BLyS gene expression in prostate cancer as a possible mechanism of tumor escape from immunosurveillance. Clin. Cancer Res. 15, 2979-2987. https://doi.org/10.1158/1078-0432.CCR-08-1951
  4. Di Giovine, F. S., Nuki, G. and Duff, G. W. (1988) Tumour necrosis factor in synovial exudates. Ann. Rheum. Dis. 47, 768-772. https://doi.org/10.1136/ard.47.9.768
  5. Feldmann, M. and Maini, R. N. (2001) Anti-TNF alpha therapy of rheumatoid arthritis: what have we learned? Annu. Rev. Immunol. 19, 163-196. https://doi.org/10.1146/annurev.immunol.19.1.163
  6. Firestein, G. S. (1996) Invasive fibroblast-like synoviocytes in rheumatoid arthritis. Passive responders or transformed aggressors? Arthritis Rheum. 39, 1781-1790.
  7. Firestein, G. S. (2003) Evolving concepts of rheumatoid arthritis. Nature 423, 356-361. https://doi.org/10.1038/nature01661
  8. Huber, L. C., Distler, O., Tarner, I., Gay, R. E., Gay, S. and Pap, T. (2006) Synovial fibroblasts: key players in rheumatoid arthritis. Rheumatology (Oxford) 45, 669-675. https://doi.org/10.1093/rheumatology/kel065
  9. Ittah, M., Miceli-Richard, C., Eric Gottenberg, J., Lavie, F., Lazure, T., Ba, N., Sellam, J., Lepajolec, C. and Mariette, X. (2006) B cell-activating factor of the tumor necrosis factor family (BAFF) is expressed under stimulation by interferon in salivary gland epithelial cells in primary Sjogren's syndrome. Arthritis Res. Ther. 8, R51. https://doi.org/10.1186/ar1912
  10. Ittah, M., Miceli-Richard, C., Gottenberg, J. E., Sellam, J., Eid, P., Lebon, P., Pallier, C., Lepajolec, C. and Mariette, X. (2008) Viruses induce high expression of BAFF by salivary gland epithelial cells through TLR- and type-I IFN-dependent and -independent pathways. Eur. J. Immunol. 38, 1058-1064. https://doi.org/10.1002/eji.200738013
  11. Iwamoto, T., Okamoto, H., Toyama, Y. and Momohara, S. (2008) Molecular aspects of rheumatoid arthritis: chemokines in the joints of patients. FEBS J. 275, 4448-4455. https://doi.org/10.1111/j.1742-4658.2008.06580.x
  12. Kato, A., Truong-Tran, A. Q., Scott, A. L., Matsumoto, K. and Schleimer, R. P. (2006) Airway epithelial cells produce B cell-activating factor of TNF family by an IFN-beta-dependent mechanism. J. Immunol. 177, 7164-7172. https://doi.org/10.4049/jimmunol.177.10.7164
  13. Kiener, H. P., Watts, G. F., Cui, Y., Wright, J., Thornhill, T. S., Skold, M., Behar, S. M., Niederreiter, B., Lu, J., Cernadas, M., Coyle, A. J., Sims, G. P., Smolen, J., Warman, M. L., Brenner, M. B. and Lee, D. M. (2010) Synovial fibroblasts self-direct multicellular lining architecture and synthetic function in three-dimensional organ culture. Arthritis Rheum. 62, 742-752. https://doi.org/10.1002/art.27285
  14. Lee, D. M. (2010) Synovial fibroblasts self-direct multicellular lining architecture and synthetic function in three-dimensional organ culture. Arthritis Rheum. 62, 742-752. https://doi.org/10.1002/art.27285
  15. Lauzier, A., Lavoie, R. R., Charbonneau, M., Gouin-Boisvert, B., Harper, K. and Dubois, C. M. (2016) Snail is a critical mediator of invadosome formation and joint degradation in arthritis. Am. J. Pathol. 186, 359-374. https://doi.org/10.1016/j.ajpath.2015.10.021
  16. Lee, D. M., Kiener, H. P., Agarwal, S. K., Noss, E. H., Watts, G. F., Chisaka, O., Takeichi, M. and Brenner, M. B. (2007) Cadherin-11 in synovial lining formation and pathology in arthritis. Science 315, 1006-1010. https://doi.org/10.1126/science.1137306
  17. Lee, G. H., Lee, J., Lee, J. W., Choi, W. S. and Moon, E. Y. (2013) B cell activating factor-dependent expression of vascular endothelial growth factor in MH7A human synoviocytes stimulated with tumor necrosis factor-alpha. Int. Immunopharmacol. 17, 142-147. https://doi.org/10.1016/j.intimp.2013.04.026
  18. Lee, G. H., Lee, M. H., Yoon, Y. D., Kang, J. S., Pyo, S. and Moon, E. Y. (2012) Protein kinase C stimulates human B cell activating factor gene expression through reactive oxygen species-dependent c-Fos in THP-1 pro-monocytic cells. Cytokine 59, 115-123. https://doi.org/10.1016/j.cyto.2012.03.017
  19. Lee, G. H., Oh, J. M., Kim, H. S., Yoon, W. K., Yi, K. Y., Yang, Y., Han, S. H., Lee, S. and Moon, E. Y. (2011) KR33426, [2-(2,5-dichlorophenyl)-5-methyloxazol-4yl]carbonylguanidine, is a novel compound to be effective on mouse systemic lupus erythematosus. Eur. J. Pharmacol. 668, 459-466. https://doi.org/10.1016/j.ejphar.2011.07.026
  20. Lee, J. W., Lee, J., Um, S. H. and Moon, E. Y. (2017) Synovial cell death is regulated by TNF-alpha-induced expression of B-cell activating factor through an ERK-dependent increase in hypoxiainducible factor-1alpha. Cell Death Dis. 8, e2727. https://doi.org/10.1038/cddis.2017.26
  21. Lee, S., Yi, K. Y., Youn, S. J., Lee, B. H. and Yoo, S. E. (2009) (2-Aryl5-methylimidazol-4-ylcarbonyl)guanidines and (2-aryl-5-methyloxazol-4-ylcarbonyl)guanidines as NHE-1 inhibitors. Bioorg. Med. Chem. Lett. 19, 1329-1331. https://doi.org/10.1016/j.bmcl.2009.01.060
  22. Lettesjo, H., Nordstrom, E., Strom, H., Nilsson, B., Glinghammar, B., Dahlstedt, L. and Moller, E. (1998) Synovial fluid cytokines in patients with rheumatoid arthritis or other arthritic lesions. Scand. J. Immunol. 48, 286-292. https://doi.org/10.1046/j.1365-3083.1998.00399.x
  23. Li, G., Zhang, Y., Qian, Y., Zhang, H., Guo, S., Sunagawa, M., Hisamitsu, T. and Liu, Y. (2013) Interleukin-17A promotes rheumatoid arthritis synoviocytes migration and invasion under hypoxia by increasing MMP2 and MMP9 expression through NF-kappaB/HIF-1alpha pathway. Mol. Immunol. 53, 227-236. https://doi.org/10.1016/j.molimm.2012.08.018
  24. Lipsky, P. E. (2007) Why does rheumatoid arthritis involve the joints? N. Engl. J. Med. 356, 2419-2420. https://doi.org/10.1056/NEJMcibr070846
  25. Liu, S. C., Hsu, C. J., Fong, Y. C., Chuang, S. M. and Tang, C. H. (2013) CTGF induces monocyte chemoattractant protein-1 expression to enhance monocyte migration in human synovial fibroblasts. Biochim. Biophys. Acta 1833, 1114-1124. https://doi.org/10.1016/j.bbamcr.2012.12.014
  26. Mackay, F. and Browning, J. L. (2002) BAFF: a fundamental survival factor for B cells. Nat. Rev. Immunol. 2, 465-475. https://doi.org/10.1038/nri844
  27. Mackay, F. and Kalled, S. L. (2002) TNF ligands and receptors in autoimmunity: an update. Curr. Opin. Immunol. 14, 783-790. https://doi.org/10.1016/S0952-7915(02)00407-7
  28. Mackay, F., Schneider, P., Rennert, P. and Browning, J. (2003) BAFF AND APRIL: a tutorial on B cell survival. Annu. Rev. Immunol. 21, 231-264. https://doi.org/10.1146/annurev.immunol.21.120601.141152
  29. Miyazawa, K., Mori, A. and Okudaira, H. (1998) Establishment and characterization of a novel human rheumatoid fibroblast-like synoviocyte line, MH7A, immortalized with SV40 T antigen. J. Biochem. 124, 1153-1162. https://doi.org/10.1093/oxfordjournals.jbchem.a022233
  30. Moon, E. Y., Lee, J. H., Lee, J. W., Song, J. H. and Pyo, S. (2011a) ROS/Epac1-mediated Rap1/NF-kappaB activation is required for the expression of BAFF in Raw264.7 murine macrophages. Cell. Signal. 23, 1479-1488. https://doi.org/10.1016/j.cellsig.2011.05.001
  31. Moon, E. Y., Lee, J. H., Oh, S. Y., Ryu, S. K., Kim, H. M., Kwak, H. S. and Yoon, W. K. (2006) Reactive oxygen species augment B-cell-activating factor expression. Free Radic. Biol. Med. 40, 2103-2111. https://doi.org/10.1016/j.freeradbiomed.2006.02.007
  32. Moon, E. Y., Lee, Y. S., Choi, W. S. and Lee, M. H. (2011b) Toll-like receptor 4-mediated cAMP production up-regulates B-cell activating factor expression in Raw264.7 macrophages. Exp. Cell Res. 317, 2447-2455. https://doi.org/10.1016/j.yexcr.2011.07.003
  33. Moon, E. Y. and Park, H. (2007) B cell activating factor (BAFF) gene promoter activity depends upon co-activator, p300. Immunobiology 212, 637-645. https://doi.org/10.1016/j.imbio.2007.06.002
  34. Moon, E. Y., Yi, K. Y. and Lee, S. (2011c) An increase in B cell apoptosis by interfering BAFF-BAFF-R interaction with small synthetic molecules. Int. Immunopharmacol. 11, 1523-1533. https://doi.org/10.1016/j.intimp.2011.05.009
  35. Nakajima, K., Itoh, K., Nagatani, K., Okawa-Takatsuji, M., Fujii, T., Kuroki, H., Katsuragawa, Y., Aotsuka, S. and Mimori, A. (2007) Expression of BAFF and BAFF-R in the synovial tissue of patients with rheumatoid arthritis. Scand. J. Rheumatol. 36, 365-372. https://doi.org/10.1080/03009740701286615
  36. Nanki, T., Nagasaka, K., Hayashida, K., Saita, Y. and Miyasaka, N. (2001) Chemokines regulate IL-6 and IL-8 production by fibroblast-like synoviocytes from patients with rheumatoid arthritis. J. Immunol. 167, 5381-5385. https://doi.org/10.4049/jimmunol.167.9.5381
  37. Ng, L. G., Sutherland, A. P., Newton, R., Qian, F., Cachero, T. G., Scott, M. L., Thompson, J. S., Wheway, J., Chtanova, T., Groom, J., Sutton, I. J., Xin, C., Tangye, S. G., Kalled, S. L., Mackay, F. and Mackay, C. R. (2004) B cell-activating factor belonging to the TNF family (BAFF)-R is the principal BAFF receptor facilitating BAFF costimulation of circulating T and B cells. J. Immunol. 173, 807-817. https://doi.org/10.4049/jimmunol.173.2.807
  38. O'Hayre, M., Salanga, C. L., Handel, T. M. and Allen, S. J. (2008) Chemokines and cancer: migration, intracellular signalling and intercellular communication in the microenvironment. Biochem. J. 409, 635-649. https://doi.org/10.1042/BJ20071493
  39. Ohata, J., Zvaifler, N. J., Nishio, M., Boyle, D. L., Kalled, S. L., Carson, D. A. and Kipps, T. J. (2005) Fibroblast-like synoviocytes of mesenchymal origin express functional B cell-activating factor of the TNF family in response to proinflammatory cytokines. J. Immunol. 174, 864-870. https://doi.org/10.4049/jimmunol.174.2.864
  40. Ryu, Y. K., Lee, J. W. and Moon, E. Y. (2015) Thymosin beta-4, actinsequestering protein regulates vascular endothelial growth factor expression via hypoxia-inducible nitric oxide production in hela cervical cancer cells. Biomol. Ther. (Seoul) 23, 19-25. https://doi.org/10.4062/biomolther.2014.101
  41. Ryu, Y. K., Lee, Y. S., Lee, G. H., Song, K. S., Kim, Y. S. and Moon, E. Y. (2012) Regulation of glycogen synthase kinase-3 by thymosin beta-4 is associated with gastric cancer cell migration. Int. J. Cancer 131, 2067-2077. https://doi.org/10.1002/ijc.27490
  42. Suurmond, J. and Diamond, B. (2015) Autoantibodies in systemic autoimmune diseases: specificity and pathogenicity. J. Clin. Invest. 125, 2194-2202. https://doi.org/10.1172/JCI78084
  43. Tan, S. M., Xu, D., Roschke, V., Perry, J. W., Arkfeld, D. G., Ehresmann, G. R., Migone, T. S., Hilbert, D. M. and Stohl, W. (2003) Local production of B lymphocyte stimulator protein and APRIL in arthritic joints of patients with inflammatory arthritis. Arthritis Rheum. 48, 982-992. https://doi.org/10.1002/art.10860
  44. Trollmo, C., Nilsson, I. M., Sollerman, C. and Tarkowski, A. (1996) Expression of the mucosal lymphocyte integrin alpha E beta 7 and its ligand E-cadherin in the synovium of patients with rheumatoid arthritis. Scand. J. Immunol. 44, 293-298.
  45. Wahren-Herlenius, M. and Dorner, T. (2013) Immunopathogenic mechanisms of systemic autoimmune disease. Lancet 382, 819-831. https://doi.org/10.1016/S0140-6736(13)60954-X
  46. Woo, S. J., Im, J., Jeon, J. H., Kang, S. S., Lee, M. H., Yun, C. H., Moon, E. Y., Song, M. K., Kim, H. H. and Han, S. H. (2013) Induction of BAFF expression by IFN-gamma via JAK/STAT signaling pathways in human intestinal epithelial cells. J. Leukoc. Biol. 93, 363-368. https://doi.org/10.1189/jlb.0412210
  47. Xing, R., Jin, Y., Sun, L., Yang, L., Li, C., Li, Z., Liu, X. and Zhao, J. (2016) Interleukin-21 induces migration and invasion of fibroblast-like synoviocytes from patients with rheumatoid arthritis. Clin. Exp. Immunol. 184, 147-158. https://doi.org/10.1111/cei.12751
  48. You, S., Yoo, S. A., Choi, S., Kim, J. Y., Park, S. J., Ji, J. D., Kim, T. H., Kim, K. J., Cho, C. S., Hwang, D. and Kim, W. U. (2014) Identification of key regulators for the migration and invasion of rheumatoid synoviocytes through a systems approach. Proc. Natl. Acad. Sci. U.S.A. 111, 550-555. https://doi.org/10.1073/pnas.1311239111
  49. Zhu, D., Zhao, J., Lou, A., Huang, Q., OuYang, Q., Zhu, J., Fan, M., He, Y., Ren, H. and Yang, M. (2019) Transforming growth factor beta1 promotes fibroblast-like synoviocytes migration and invasion via TGF-beta1/Smad signaling in rheumatoid arthritis. Mol. Cell. Biochem. 459, 141-150. https://doi.org/10.1007/s11010-019-03557-0
  50. Zvaifler, N. J. (2006) Relevance of the stroma and epithelial-mesenchymal transition (EMT) for the rheumatic diseases. Arthritis Res. Ther. 8, 210. https://doi.org/10.1186/ar1963

피인용 문헌

  1. Evaluation of Villus Synovium From Unaffected Metacarpophalangeal Joints of Adult and Juvenile Horses vol.102, 2021, https://doi.org/10.1016/j.jevs.2021.103637
  2. B Cell Adhesion to Fibroblast-Like Synoviocytes Is Up-Regulated by Tumor Necrosis Factor-Alpha via Expression of Human Vascular Cell Adhesion Molecule-1 Mediated by B Cell-Activating Factor vol.22, pp.13, 2020, https://doi.org/10.3390/ijms22137166
  3. LW1497, an Inhibitor of Malate Dehydrogenase, Suppresses TGF-β1-Induced Epithelial-Mesenchymal Transition in Lung Cancer Cells by Downregulating Slug vol.10, pp.11, 2021, https://doi.org/10.3390/antiox10111674