Role of Histone Deacetylase 3 in Ankylosing Spondylitis Via Negative Feedback Loop with MicroRNA-130a and Enhancement of Tumor Necrosis Factor-1α Expression in Peripheral Blood Mononuclear Cells

Overview

Journal Mol Med Rep

Specialty Molecular Biology

Date 2015 Nov 5

PMID 26531724

Citations 21

Authors

Ya Jiang

Lin Wang

Affiliations

Soon will be listed here.

Abstract

The present study was performed to investigate the molecular mechanism of ankylosing spondylitis (AS). The interaction between micro (mi)RNA‑130a and its target tumor necrosis factor (TNF)‑1α and histone deactylase (HDAC)3 was assessed in peripheral blood mononuclear cells (PBMCs) from AS patients. Increased HDAC3 and decreased miRNA‑130a levels were observed in PBMCs from AS patients. HDAC3 knockdown or HDAC3 inhibition promoted the expression of miRNA‑130a, and HDAC3 was recruited to the promoter region of the gene encoding miRNA‑130a in PBMCs. In addition, miR‑130a overexpression led to a decrease, whereas miR‑130a inhibition led to an increase of TNF‑1α expression in PBMCs. Furthermore, HDAC3 knockdown or HDAC3 inhibition was associated with simultaneous upregulation of the expression of miR‑130a and downregulation of the expression of TNF‑1α in PBMCs. These results indicated that HDAC3 was involved in the regulation of the underlying molecular mechanism of AS by forming a negative feedback loop with miR-130a and enhancement of TNF-1α expression.

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References

Fenix-Caballero S, Alegre-Del Rey E, Castano-Lara R, Puigventos-Latorre F, Borrero-Rubio J, Lopez-Vallejo J . Direct and indirect comparison of the efficacy and safety of adalimumab, etanercept, infliximab and golimumab in psoriatic arthritis. J Clin Pharm Ther. 2013; 38(4):286-93. DOI: 10.1111/jcpt.12045. View

Han K, Kang H, Lee J, Yoo L, Im E, Hong A . Histone deacetylase 3 promotes RCAN1 stability and nuclear translocation. PLoS One. 2014; 9(8):e105416. PMC: 4140772. DOI: 10.1371/journal.pone.0105416. View

Zhu S, Pan W, Song X, Liu Y, Shao X, Tang Y . The microRNA miR-23b suppresses IL-17-associated autoimmune inflammation by targeting TAB2, TAB3 and IKK-α. Nat Med. 2012; 18(7):1077-86. DOI: 10.1038/nm.2815. View

Fabbroni M, Cantarini L, Caso F, Costa L, Pagano V, Frediani B . Drug retention rates and treatment discontinuation among anti-TNF-α agents in psoriatic arthritis and ankylosing spondylitis in clinical practice. Mediators Inflamm. 2014; 2014:862969. PMC: 4119698. DOI: 10.1155/2014/862969. View

Meng S, Cao J, Zhang X, Fan Y, Fang L, Wang C . Downregulation of microRNA-130a contributes to endothelial progenitor cell dysfunction in diabetic patients via its target Runx3. PLoS One. 2013; 8(7):e68611. PMC: 3709913. DOI: 10.1371/journal.pone.0068611. View

Kim N, Sun H, Youn M, Yoo J . IL-1β-specific recruitment of GCN5 histone acetyltransferase induces the release of PAF1 from chromatin for the de-repression of inflammatory response genes. Nucleic Acids Res. 2013; 41(8):4495-506. PMC: 3632138. DOI: 10.1093/nar/gkt156. View

Lai N, Yu H, Chen H, Yu C, Huang H, Lu M . Aberrant expression of microRNAs in T cells from patients with ankylosing spondylitis contributes to the immunopathogenesis. Clin Exp Immunol. 2013; 173(1):47-57. PMC: 3694534. DOI: 10.1111/cei.12089. View

Gillespie J, Savic S, Wong C, Hempshall A, Inman M, Emery P . Histone deacetylases are dysregulated in rheumatoid arthritis and a novel histone deacetylase 3-selective inhibitor reduces interleukin-6 production by peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Rheum. 2011; 64(2):418-22. DOI: 10.1002/art.33382. View

Zhang J, Kalkum M, Chait B, Roeder R . The N-CoR-HDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol Cell. 2002; 9(3):611-23. DOI: 10.1016/s1097-2765(02)00468-9. View

10.

Choi J, Oh S, Kang M, Kwon H, Oh G, Kim D . Trichostatin A attenuates airway inflammation in mouse asthma model. Clin Exp Allergy. 2005; 35(1):89-96. DOI: 10.1111/j.1365-2222.2004.02006.x. View

11.

Grausenburger R, Bilic I, Boucheron N, Zupkovitz G, El-Housseiny L, Tschismarov R . Conditional deletion of histone deacetylase 1 in T cells leads to enhanced airway inflammation and increased Th2 cytokine production. J Immunol. 2010; 185(6):3489-97. PMC: 3175530. DOI: 10.4049/jimmunol.0903610. View

12.

Lu M, Yu C, Chen H, Yu H, Huang H, Lai N . Increased miR-223 expression in T cells from patients with rheumatoid arthritis leads to decreased insulin-like growth factor-1-mediated interleukin-10 production. Clin Exp Immunol. 2014; 177(3):641-51. PMC: 4137848. DOI: 10.1111/cei.12374. View

13.

Costa L, Caso F, Atteno M, Del Puente A, Darda M, Caso P . Impact of 24-month treatment with etanercept, adalimumab, or methotrexate on metabolic syndrome components in a cohort of 210 psoriatic arthritis patients. Clin Rheumatol. 2013; 33(6):833-9. DOI: 10.1007/s10067-013-2369-1. View

14.

Toussirot E, Wendling D, Herbein G . Biological treatments given in patients with rheumatoid arthritis or ankylosing spondylitis modify HAT/HDAC (histone acetyltransferase/histone deacetylase) balance. Joint Bone Spine. 2014; 81(6):544-5. DOI: 10.1016/j.jbspin.2014.02.011. View

15.

Pauley K, Satoh M, Chan A, Bubb M, Reeves W, Chan E . Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res Ther. 2008; 10(4):R101. PMC: 2575615. DOI: 10.1186/ar2493. View

16.

Mahlknecht U, Will J, Varin A, Hoelzer D, Herbein G . Histone deacetylase 3, a class I histone deacetylase, suppresses MAPK11-mediated activating transcription factor-2 activation and represses TNF gene expression. J Immunol. 2004; 173(6):3979-90. DOI: 10.4049/jimmunol.173.6.3979. View

17.

Bendinelli P, Matteucci E, Maroni P, Desiderio M . NF-kappaB activation, dependent on acetylation/deacetylation, contributes to HIF-1 activity and migration of bone metastatic breast carcinoma cells. Mol Cancer Res. 2009; 7(8):1328-41. DOI: 10.1158/1541-7786.MCR-08-0548. View

18.

Strietholt S, Maurer B, Peters M, Pap T, Gay S . Epigenetic modifications in rheumatoid arthritis. Arthritis Res Ther. 2008; 10(5):219. PMC: 2592785. DOI: 10.1186/ar2500. View

19.

Zhang X, Chen X, Lin J, Lwin T, Wright G, Moscinski L . Myc represses miR-15a/miR-16-1 expression through recruitment of HDAC3 in mantle cell and other non-Hodgkin B-cell lymphomas. Oncogene. 2011; 31(24):3002-3008. PMC: 3982396. DOI: 10.1038/onc.2011.470. View

20.

Katto J, Engel N, Abbas W, Herbein G, Mahlknecht U . Transcription factor NFκB regulates the expression of the histone deacetylase SIRT1. Clin Epigenetics. 2013; 5(1):11. PMC: 3727996. DOI: 10.1186/1868-7083-5-11. View