Decoy receptor 3 regulates the expression of various genes in rheumatoid arthritis synovial fibroblasts

Fukuda,Koji; Miura,Yasushi; Maeda,Toshihisa; Takahashi,Masayasu; Hayashi,Shinya; Kurosaka,Masahiro

doi:10.3892/ijmm.2013.1461

Decoy receptor 3 regulates the expression of various genes in rheumatoid arthritis synovial fibroblasts

Authors:
- Koji Fukuda
- Yasushi Miura
- Toshihisa Maeda
- Masayasu Takahashi
- Shinya Hayashi
- Masahiro Kurosaka
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Affiliations: Department of Orthopaedic Surgery, Kobe University Graduate School of Medicine, Chuo, Kobe, Hyogo 650-0017, Japan, Division of Orthopaedic Science, Department of Rehabilitation Science, Kobe University Graduate School of Health Sciences, Suma, Kobe, Hyogo 654-0142, Japan, Department of Orthopaedic Surgery, Kohnan Hospital, Higashinada, Kobe, Hyogo 658-0064, Japan
Published online on: August 1, 2013 https://doi.org/10.3892/ijmm.2013.1461
Pages: 910-916

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Abstract

Decoy receptor 3 (DcR3), a member of the tumor necrosis factor (TNF) receptor (TNFR) superfamily, lacks the transmembrane domain of conventional TNFRs in order to be a secreted protein. DcR3 competitively binds and inhibits members of the TNF family, including Fas ligand (FasL), LIGHT and TNF-like ligand 1A (TL1A). We previously reported that TNFα-induced DcR3 overexpression in rheumatoid arthritis fibroblast-like synoviocytes (RA-FLS) protects cells from Fas-induced apoptosis. Previous studies have suggested that DcR3 acting as a ligand directly induces the differentiation of macrophages into osteoclasts. Furthermore, we reported that DcR3 induces very late antigen-4 (VLA-4) expression in THP-1 macrophages, inhibiting cycloheximide-induced apoptosis and that DcR3 binds to membrane-bound TL1A expressed on RA-FLS, resulting in the negative regulation of cell proliferation induced by inflammatory cytokines. In the current study, we used cDNA microarray to search for genes in RA-FLS whose expression was regulated by the ligation of DcR3. The experiments revealed the expression profiles of genes in RA-FLS regulated by DcR3. The profiles showed that among the 100 genes most significantly regulated by DcR3, 45 were upregulated and 55 were downregulated. The upregulated genes were associated with protein complex assembly, cell motility, regulation of transcription, cellular protein catabolic processes, cell membrane, nucleotide binding and glycosylation. The downregulated genes were associated with transcription regulator activity, RNA biosynthetic processes, cytoskeleton, zinc finger region, protein complex assembly, phosphate metabolic processes, mitochondrion, ion transport, nucleotide binding and cell fractionation. Further study of the genes detected in the current study may provide insight into the pathogenesis and treatment of rheumatoid arthritis by DcR3-TL1A signaling.

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1	Chou CT, Yang JS and Lee MR: Apoptosis in rheumatoid arthritis - expression of Fas, Fas-L, p53, and Bcl-2 in rheumatoid synovial tissues. J Pathol. 193:110–116. 2001. View Article : Google Scholar : PubMed/NCBI
2	Tak PP, Zvaifler NJ, Green DR and Firestein GS: Rheumatoid arthritis and p53: how oxidative stress might alter the course of inflammatory diseases. Immunol Today. 21:78–82. 2000. View Article : Google Scholar : PubMed/NCBI
3	Yamanishi Y, Boyle DL, Rosengren S, Green DR, Zvaifler NJ and Firestein GS: Regional analysis of p53 mutations in rheumatoid arthritis synovium. Proc Natl Acad Sci USA. 99:10025–10030. 2002. View Article : Google Scholar : PubMed/NCBI
4	Hayashi S, Miura Y, Nishiyama T, et al: Decoy receptor 3 expressed in rheumatoid synovial fibroblasts protects the cells against Fas-induced apoptosis. Arthritis Rheum. 56:1067–1075. 2007. View Article : Google Scholar : PubMed/NCBI
5	Pitti RM, Marsters SA, Lawrence DA, et al: Genomic amplification of a decoy receptor for Fas ligand in lung and colon cancer. Nature. 396:699–703. 1998. View Article : Google Scholar : PubMed/NCBI
6	Bai C, Connolly B, Metzker ML, et al: Overexpression of M68/DcR3 in human gastrointestinal tract tumors independent of gene amplification and its location in a four-gene cluster. Proc Natl Acad Sci USA. 97:1230–1235. 2000. View Article : Google Scholar : PubMed/NCBI
7	Ohshima K, Haraoka S, Sugihara M, et al: Amplification and expression of a decoy receptor for fas ligand (DcR3) in virus (EBV or HTLV-I) associated lymphomas. Cancer Lett. 160:89–97. 2000. View Article : Google Scholar : PubMed/NCBI
8	Chen J, Zhang L and Kim S: Quantification and detection of DcR3, a decoy receptor in TNFR family. J Immunol Methods. 285:63–70. 2004. View Article : Google Scholar : PubMed/NCBI
9	Shi G, Wu Y, Zhang J and Wu J: Death decoy receptor TR6/DcR3 inhibits T cell chemotaxis in vitro and in vivo. J Immunol. 171:3407–3414. 2003. View Article : Google Scholar : PubMed/NCBI
10	Tsuji S, Hosotani R, Yonehara S, et al: Endogenous decoy receptor 3 blocks the growth inhibition signals mediated by Fas ligand in human pancreatic adenocarcinoma. Int J Cancer. 106:17–25. 2003. View Article : Google Scholar : PubMed/NCBI
11	Yu KY, Kwon B, Ni J, Zhai Y, Ebner R and Kwon BS: A newly identified member of tumor necrosis factor receptor superfamily (TR6) suppresses LIGHT-mediated apoptosis. J Biol Chem. 274:13733–13736. 1999. View Article : Google Scholar : PubMed/NCBI
12	Migone TS, Zhang J, Luo X, et al: TL1A is a TNF-like ligand for DR3 and TR6/DcR3 and functions as a T cell costimulator. Immunity. 16:479–492. 2002. View Article : Google Scholar : PubMed/NCBI
13	Yang CR, Wang JH, Hsieh SL, Wang SM, Hsu TL and Lin WW: Decoy receptor 3 (DcR3) induces osteoclast formation from monocyte/macrophage lineage precursor cells. Cell Death Differ. 11(Suppl 1): S97–S107. 2004. View Article : Google Scholar : PubMed/NCBI
14	Hsu MJ, Lin WW, Tsao WC, et al: Enhanced adhesion of monocytes via reverse signaling triggered by decoy receptor 3. Exp Cell Res. 292:241–251. 2004. View Article : Google Scholar : PubMed/NCBI
15	Tateishi K, Miura Y, Hayashi S, Takahashi M and Kurosaka M: DcR3 protects THP-1 macrophages from apoptosis by increasing integrin alpha4. Biochem Biophys Res Commun. 389:593–598. 2009. View Article : Google Scholar : PubMed/NCBI
16	Takahashi M, Miura Y, Hayashi S, Tateishi K, Fukuda K and Kurosaka M: DcR3-TL1A signalling inhibits cytokine-induced proliferation of rheumatoid synovial fibroblasts. Int J Mol Med. 28:423–427. 2011.PubMed/NCBI
17	Arnett FC, Edworthy SM, Bloch DA, et al: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 31:315–324. 1988. View Article : Google Scholar : PubMed/NCBI
18	Kamada N, Hisamatsu T, Honda H, et al: TL1A produced by lamina propria macrophages induces Th1 and Th17 immune responses in cooperation with IL-23 in patients with Crohn’s disease. Inflamm Bowel Dis. 16:568–575. 2010.PubMed/NCBI
19	Bamias G, Martin C III, Marini M, et al: Expression, localization, and functional activity of TL1A, a novel Th1-polarizing cytokine in inflammatory bowel disease. J Immunol. 171:4868–4874. 2003. View Article : Google Scholar : PubMed/NCBI
20	Prehn JL, Mehdizadeh S, Landers CJ, et al: Potential role for TL1A, the new TNF-family member and potent costimulator of IFN-gamma, in mucosal inflammation. Clin Immunol. 112:66–77. 2004. View Article : Google Scholar : PubMed/NCBI
21	Papadakis KA, Zhu D, Prehn JL, et al: Dominant role for TL1A/DR3 pathway in IL-12 plus IL-18-induced IFN-gamma production by peripheral blood and mucosal CCR9⁺ T lymphocytes. J Immunol. 174:4985–4990. 2005. View Article : Google Scholar : PubMed/NCBI
22	Cassatella MA, Pereira-da-Silva G, Tinazzi I, et al: Soluble TNF-like cytokine (TL1A) production by immune complexes stimulated monocytes in rheumatoid arthritis. J Immunol. 178:7325–7333. 2007. View Article : Google Scholar : PubMed/NCBI
23	Prehn JL, Thomas LS, Landers CJ, Yu QT, Michelsen KS and Targan SR: The T cell costimulator TL1A is induced by FcgammaR signaling in human monocytes and dendritic cells. J Immunol. 178:4033–4038. 2007. View Article : Google Scholar : PubMed/NCBI
24	Zhang J, Wang X, Fahmi H, et al: Role of TL1A in the pathogenesis of rheumatoid arthritis. J Immunol. 183:5350–5357. 2009. View Article : Google Scholar : PubMed/NCBI
25	Sethi G, Sung B and Aggarwal BB: Therapeutic potential of VEGI/TL1A in autoimmunity and cancer. Adv Exp Med Biol. 647:207–215. 2009. View Article : Google Scholar : PubMed/NCBI
26	Bamias G, Siakavellas S, Stamatelopoulos K, Chryssochoou E, Papamichael C and Sfikakis P: Circulating levels of TNF-like cytokine 1A (TL1A) and its decoy receptor 3 (DcR3) in rheumatoid arthritis. Clin Immunol. 129:249–255. 2008. View Article : Google Scholar : PubMed/NCBI
27	Edwards JR, Sun SG, Locklin R, et al: LIGHT (TNFSF14), a novel mediator of bone resorption, is elevated in rheumatoid arthritis. Arthritis Rheum. 54:1451–1462. 2006. View Article : Google Scholar : PubMed/NCBI
28	Khan J, Simon R, Bittner M, et al: Gene expression profiling of alveolar rhabdomyosarcoma with cDNA microarrays. Cancer Res. 58:5009–5013. 1998.PubMed/NCBI
29	Espinosa I, Catasus L, Canet B, D’Angelo E, Munoz J and Prat J: Gene expression analysis identifies two groups of ovarian high-grade serous carcinomas with different prognosis. Mod Pathol. 24:846–854. 2011. View Article : Google Scholar : PubMed/NCBI
30	Chang YC, Chen TC, Lee CT, et al: Epigenetic control of MHC class II expression in tumor-associated macrophages by decoy receptor 3. Blood. 111:5054–5063. 2008. View Article : Google Scholar : PubMed/NCBI
31	Li J, Yang S, Lu S, et al: Differential gene expression profile associated with the abnormality of bone marrow mesenchymal stem cells in aplastic anemia. PLoS One. 7:e477642012. View Article : Google Scholar : PubMed/NCBI
32	Whitney LW, Becker KG, Tresser NJ, et al: Analysis of gene expression in mutiple sclerosis lesions using cDNA microarrays. Ann Neurol. 46:425–428. 1999. View Article : Google Scholar : PubMed/NCBI
33	Heller RA, Schena M, Chai A, et al: Discovery and analysis of inflammatory disease-related genes using cDNA microarrays. Proc Natl Acad Sci USA. 94:2150–2155. 1997. View Article : Google Scholar : PubMed/NCBI
34	Lee SK, Jeon EK, Kim YJ, et al: A global gene expression analysis of the peripheral blood mononuclear cells reveals the gene expression signature in psoriasis. Ann Dermatol. 21:237–242. 2009. View Article : Google Scholar : PubMed/NCBI
35	van der Pouw Kraan TC, van Gaalen FA, Kasperkovitz PV, et al: Rheumatoid arthritis is a heterogeneous disease: evidence for differences in the activation of the STAT-1 pathway between rheumatoid tissues. Arthritis Rheum. 48:2132–2145. 2003.PubMed/NCBI
36	Akitaya T and Bronner-Fraser M: Expression of cell adhesion molecules during initiation and cessation of neural crest cell migration. Dev Dyn. 194:12–20. 1992. View Article : Google Scholar : PubMed/NCBI
37	Kashima T, Nakamura K, Kawaguchi J, et al: Overexpression of cadherins suppresses pulmonary metastasis of osteosarcoma in vivo. Int J Cancer. 104:147–154. 2003. View Article : Google Scholar : PubMed/NCBI
38	Marie PJ: Role of N-cadherin in bone formation. J Cell Physiol. 190:297–305. 2002. View Article : Google Scholar : PubMed/NCBI
39	Nonomura Y, Mizoguchi F, Suzuki A, et al: Hypoxia-induced abrogation of contact-dependent inhibition of rheumatoid arthritis synovial fibroblast proliferation. J Rheumatol. 36:698–705. 2009. View Article : Google Scholar
40	Hasko G and Szabo C: IL-12 as a therapeutic target for pharmacological modulation in immune-mediated and inflammatory diseases: regulation of T helper 1/T helper 2 responses. Br J Pharmacol. 127:1295–1304. 1999. View Article : Google Scholar : PubMed/NCBI
41	Paradowska-Gorycka A, Grzybowska-Kowalczyk A, Wojtecka-Lukasik E and Maslinski S: IL-23 in the pathogenesis of rheumatoid arthritis. Scand J Immunol. 71:134–145. 2010. View Article : Google Scholar
42	Swaak AJ, van den Brink HG and Aarden LA: Cytokine production in whole blood cell cultures of patients with rheumatoid arthritis. Ann Rheum Dis. 56:693–695. 1997. View Article : Google Scholar : PubMed/NCBI
43	Liu FL, Chen CH, Chu SJ, et al: Interleukin (IL)-23 p19 expression induced by IL-1beta in human fibroblast-like synoviocytes with rheumatoid arthritis via active nuclear factor-kappaB and AP-1 dependent pathway. Rheumatology (Oxford). 46:1266–1273. 2007. View Article : Google Scholar
44	Kim HR, Cho ML, Kim KW, et al: Up-regulation of IL-23p19 expression in rheumatoid arthritis synovial fibroblasts by IL-17 through PI3-kinase-, NF-kappaB- and p38 MAPK-dependent signalling pathways. Rheumatology (Oxford). 46:57–64. 2007. View Article : Google Scholar : PubMed/NCBI
45	Kular L, Pakradouni J, Kitabgi P, Laurent M and Martinerie C: The CCN family: a new class of inflammation modulators? Biochimie. 93:377–388. 2011. View Article : Google Scholar : PubMed/NCBI
46	Yadav VK and Ducy P: Lrp5 and bone formation. Ann NY Acad Sci. 1192:103–109. 2010. View Article : Google Scholar : PubMed/NCBI
47	Gustafsson BI, Thommesen L, Stunes AK, et al: Serotonin and fluoxetine modulate bone cell function in vitro. J Cell Biochem. 98:139–151. 2006. View Article : Google Scholar : PubMed/NCBI
48	Ducy P and Karsenty G: The two faces of serotonin in bone biology. J Cell Biol. 191:7–13. 2010. View Article : Google Scholar : PubMed/NCBI
49	Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA and Mann M: Proteomic characterization of the human centrosome by protein correlation profiling. Nature. 426:570–574. 2003. View Article : Google Scholar : PubMed/NCBI
50	Doxsey S, Zimmerman W and Mikule K: Centrosome control of the cell cycle. Trends Cell Biol. 15:303–311. 2005. View Article : Google Scholar : PubMed/NCBI
51	Shi X, Sun X, Liu M, Li D, Aneja R and Zhou J: CEP70 protein interacts with gamma-tubulin to localize at the centrosome and is critical for mitotic spindle assembly. J Biol Chem. 286:33401–33408. 2011. View Article : Google Scholar : PubMed/NCBI
52	Shi X, Wang J, Yang Y, Ren Y, Zhou J and Li D: Cep70 promotes microtubule assembly in vitro by increasing microtubule elongation. Acta Biochim Biophys Sin (Shanghai). 44:450–454. 2012. View Article : Google Scholar : PubMed/NCBI
53	Leon O and Roth M: Zinc fingers: DNA binding and protein-protein interactions. Biol Res. 33:21–30. 2000. View Article : Google Scholar : PubMed/NCBI