The role of β-d-mannuronic acid, as a new non-steroidal anti-inflammatory drug on expression of miR-146a, IRAK1, TRAF6, NF-κB and pro-inflammatory cytokines following a clinical trial in rheumatoid arthritis patients

References

• Won S, Cho S-K, Kim D, et al. Update on the prevalence and incidence of rheumatoid arthritis in Korea and an analysis of medical care and drug utilization. Rheumatol Int. 2018;38(4):649–656.
   PubMed Web of Science ®Google Scholar
• Rossini M, Rossi E, Bernardi D, et al. Prevalence and incidence of rheumatoid arthritis in Italy. Rheumatol Int. 2014;34(5):659–664.
   PubMed Web of Science ®Google Scholar
• Deane KD, Demoruelle MK, Kelmenson LB, et al. Genetic and environmental risk factors for rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2017;31(1):3–18.
   PubMed Web of Science ®Google Scholar
• Yap H-Y, Tee S-Y, Wong MM-T, et al. Pathogenic role of immune cells in rheumatoid arthritis: implications in clinical treatment and biomarker development. Cells. 2018;7(10):161.
   PubMed Web of Science ®Google Scholar
• Uhlig T, Moe RH, Kvien TK. The burden of disease in rheumatoid arthritis. Pharmacoeconomics. 2014;32(9):841–851.
   PubMed Web of Science ®Google Scholar
• O’Brien J, Hayder H, Zayed Y, et al. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol. 2018;9:402.
   PubMed Web of Science ®Google Scholar
• Long H, Wang X, Chen Y, et al. Dysregulation of microRNAs in autoimmune diseases: pathogenesis, biomarkers and potential therapeutic targets. Cancer Lett. 2018;428:90–103.
   PubMed Web of Science ®Google Scholar
• Gibbings DJ, Ciaudo C, Erhardt M, et al. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol. 2009;11(9):1143–1149.
   PubMed Web of Science ®Google Scholar
• Boldin MP, Baltimore D. MicroRNAs, new effectors and regulators of NF‐κB. Immunol Rev. 2012;246(1):205–220.
   PubMedGoogle Scholar
• Ghosh S, Hayden MS. New regulators of NF-κB in inflammation. Nat Rev Immunol. 2008;8(11):837–848.
   PubMed Web of Science ®Google Scholar
• Niimoto T, Nakasa T, Ishikawa M, et al. MicroRNA-146a expresses in interleukin-17 producing T cells in rheumatoid arthritis patients. BMC Musculoskelet Disord. 2010;11(1):209.
   PubMedGoogle Scholar
• Nakasa T, Miyaki S, Okubo A, et al. Expression of microRNA‐146 in rheumatoid arthritis synovial tissue. Arthritis Rheum. 2008;58(5):1284–1292.
   PubMed Web of Science ®Google Scholar
• Abou-Zeid A, Saad M, Soliman E. MicroRNA 146a expression in rheumatoid arthritis: association with tumor necrosis factor–alpha and disease activity. Genet Test Mol Biomark. 2011;15(11):807–812.
   PubMed Web of Science ®Google Scholar
• Pauley KM, Satoh M, Chan AL, et al. Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res Ther. 2008;10(4):R101.
   PubMed Web of Science ®Google Scholar
• Taganov KD, Boldin MP, Chang K-J, et al. NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci. 2006;103(33):12481–12486.
   PubMed Web of Science ®Google Scholar
• Liu W, Wu Y-H, Zhang L, et al. MicroRNA-146a suppresses rheumatoid arthritis fibroblast-like synoviocytes proliferation and inflammatory responses by inhibiting the TLR4/NF-kB signaling. Oncotarget. 2018;9(35):23944.
   PubMedGoogle Scholar
• Liu T, Zhang L, Joo D, et al. NF-κB signaling in inflammation. Sig Transduct Target Ther. 2017;2(1):17023.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Khorramizadeh MR, Saadat F, et al. Chemopreventive effect of M2000, a new anti-inflammatory agent. Med Sci Monit. 2004;10(10):PI105–PI109.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Cuzzocrea S, Rehm B, et al. M2000: a revolution in pharmacology. Med Sci Monit. 2005;11(8):PI53–PI63.
   PubMed Web of Science ®Google Scholar
• Fattahi MJ, Abdollahi M, Agha Mohammadi A, et al. Preclinical assessment of β-d-mannuronic acid (M2000) as a non-steroidal anti-inflammatory drug. Immunopharmacol Immunotoxicol. 2015;37(6):535–540.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Taeb M, Mortazavi-Jahromi SS, et al. Introduction of β-d-mannuronic acid (M2000) as a novel NSAID with immunosuppressive property based on COX-1/COX-2 activity and gene expression. Pharmacol Rep. 2017;69(5):1067–1072.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Rehm BH, Sahmani AA, et al. M‐2000, as a new anti‐inflammatory molecule in treatment of experimental nephrosis. Immunopharmacol Immunotoxicol. 2004;26(4):611–619.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Khodadadi A, Rehm B, et al. Sodium alginate as a novel therapeutic option in experimental colitis. Scand J Immunol. 2005;61(4):316–321.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Cuzzocrea S, Rehm B, et al. Treatment of experimental arthritis with M2000, a novel designed non‐steroidal anti‐inflammatory drug. Scand J Immunol. 2005;61(5):435–441.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Borzooy Z, Abhari RS, et al. Treatment of experimental immune complex glomerulonephritis by sodium alginate. Vasc Pharmacol. 2005;43(1):30–35.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Matsuo H, Nakane S, et al. Novel immunosuppressive therapy by M2000 in experimental multiple sclerosis. Immunopharmacol Immunotoxicol. 2005;27(2):255–265.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Rehm B, Sotoude M, et al. Therapeutic approach by a novel designed anti-inflammatory drug, M2000, in experimental immune complex glomerulonephritis. Immunopharmacol Immunotoxicol. 2007;29(1):49–61.
   PubMed Web of Science ®Google Scholar
• Mirshafiey A, Rehm B, Abhari RS, et al. Production of M2000 (β-d-mannuronic acid) and its therapeutic effect on experimental nephritis. Environ Toxicol Pharmacol. 2007;24(1):60–66.
   PubMed Web of Science ®Google Scholar
• Razavi A, Khodadadi A, Eslami MB, et al. Therapeutic effect of sodium alginate in experimental chronic ulcerative colitis. Iran J Allergy Asthma Immunol. 2008;7(1):13–18.
   PubMed Web of Science ®Google Scholar
• Mortazavi-Jahromi SS, Alizadeh S, Javanbakht MH, et al. Cardioprotective effect of β-d-mannuronic acid (M2000) as a novel NSAID on gene expression of oxLDL scavenger receptors in the experimental diabetic model. Immunopharmacol Immunotoxicol. 2018;40(4):284–289.
   PubMed Web of Science ®Google Scholar
• Mortazavi-Jahromi SS, Alizadeh S, Javanbakht MH, et al. Anti-diabetic effect of β-d-mannuronic acid (M2000) as a novel NSAID with immunosuppressive property on insulin production, blood glucose, and inflammatory markers in the experimental diabetes model. Arch Physiol Biochem. 2019;125(5):435–440.
   PubMed Web of Science ®Google Scholar
• Ahmadi H, Jamshidi AR, Gharibdoost F, et al. A phase I/II randomized, controlled, clinical trial for assessment of the efficacy and safety of β-d-mannuronic acid in rheumatoid arthritis patients. Inflammopharmacology. 2018;26(3):737–745.
   PubMed Web of Science ®Google Scholar
• Fattahi MJ, Jamshidi AR, Mahmoudi M, et al. Evaluation of the efficacy and safety of β-d-mannuronic acid in patients with ankylosing spondylitis: a 12-week randomized, placebo-controlled, phase I/II clinical trial. Int Immunopharmacol. 2018;54:112–117.
   PubMed Web of Science ®Google Scholar
• Rezaieyazdi Z, Farooqi A, Soleymani-Salehabadi H, et al. International multicenter randomized, placebo-controlled phase III clinical trial of β-d-mannuronic acid in rheumatoid arthritis patients. Inflammopharmacology. 2019;27(5):911–921.
   PubMed Web of Science ®Google Scholar
• Mortazavi-Jahromi SS, Jamshidi MM, Farazmand A, et al. Pharmacological effects of β-d-mannuronic acid (M2000) on miR-146a, IRAK1, TRAF6 and NF-κB gene expression, as target molecules in inflammatory reactions. Pharmacol Rep. 2017;69(3):479–484.
   PubMed Web of Science ®Google Scholar
• Ye E-A, Steinle JJ. miR-146a attenuates inflammatory pathways mediated by TLR4/NF-κB and TNFα to protect primary human retinal microvascular endothelial cells grown in high glucose. Mediat Inflamm. 2016;2016:3958453.
   PubMed Web of Science ®Google Scholar
• Wu H, Fan H, Shou Z, et al. Extracellular vesicles containing miR-146a attenuate experimental colitis by targeting TRAF6 and IRAK1. Int Immunopharmacol. 2019;68:204–212.
   PubMed Web of Science ®Google Scholar
• Pauley KM, Cha S. miRNA-146a in rheumatoid arthritis: a new therapeutic strategy. Immunotherapy. 2011;3(7):829–831.
   PubMed Web of Science ®Google Scholar
• Xie Q, Wang S-C, Zhong J, et al. MicroRNA-146a, a good biomarker and potential therapeutic target for rheumatoid arthritis. Genet Test Mol Biomark. 2013;17(2):91–92.
   PubMed Web of Science ®Google Scholar
• Stanczyk J, Pedrioli DML, Brentano F, et al. Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum. 2008;58(4):1001–1009.
   PubMed Web of Science ®Google Scholar
• Churov AV, Oleinik EK, Knip M. MicroRNAs in rheumatoid arthritis: altered expression and diagnostic potential. Autoimmun Rev. 2015;14(11):1029–1037.
   PubMed Web of Science ®Google Scholar
• Bogunia-Kubik K, Wysoczańska B, Piątek D, et al. Significance of polymorphism and expression of miR-146a and NFkB1 genetic variants in patients with rheumatoid arthritis. Arch Immunol Ther Exp. 2016;64(S1):131–136.
   PubMedGoogle Scholar
• Brzustewicz E, Bryl E. The role of cytokines in the pathogenesis of rheumatoid arthritis—practical and potential application of cytokines as biomarkers and targets of personalized therapy. Cytokine. 2015;76(2):527–536.
   PubMed Web of Science ®Google Scholar
• Edrees A, Misra S, Abdou N. Anti-tumor necrosis factor (TNF) therapy in rheumatoid arthritis: correlation of TNF-alpha serum level with clinical response and benefit from changing dose or frequency of infliximab infusions. Clin Exp Rheumatol. 2005;23(4):469–474.
   PubMed Web of Science ®Google Scholar
• Dayer J-M, Choy E. Therapeutic targets in rheumatoid arthritis: the interleukin-6 receptor. Rheumatology (Oxford). 2010;49(1):15–24.
   PubMed Web of Science ®Google Scholar
• Yoshida Y, Tanaka T. Interleukin 6 and rheumatoid arthritis. BioMed Res Int. 2014;2014:1–12.
   Web of Science ®Google Scholar
• Houssiau FA, Devogelaer JP, Van Damme J, et al. Interleukin‐6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum. 1988;31(6):784–788.
   PubMedGoogle Scholar
• Kumar P, Banik S. Pharmacotherapy options in rheumatoid arthritis. Clin Med Insights Arthritis Musculoskelet Disord. 2013;6:35–43.
   PubMedGoogle Scholar
• Jahanbakhshi M, Babaloo Z, Mortazavi-Jahromi SS, et al. Modification of sexual hormones in rheumatoid arthritis patients by M2000 (β-d-mannuronic acid) as a novel NSAID with immunosuppressive property. EMIDDT. 2018;18(5):530–536.
   Google Scholar
• Ahmadi H, Mahmoudi M, Gharibdoost F, et al. Targeting of circulating Th17 cells by β-d-mannuronic acid (M2000) as a novel medication in patients with rheumatoid arthritis. Inflammopharmacology. 2018;26(1):57–65.
   PubMed Web of Science ®Google Scholar
• Aletaha S, Haddad L, Roozbehkia M, et al. M2000 (β‐d‐mannuronic acid) as a novel antagonist for blocking the TLR 2 and TLR 4 downstream signalling pathway. Scand J Immunol. 2017;85(2):122–129.
   PubMed Web of Science ®Google Scholar
• Ahmadi H, Jamshidi AR, Mahmoudi M, et al. Hematological improvement of patients with active rheumatoid arthritis by β-d-mannuronic acid (M2000) as a novel NSAID with immunosuppressive property. Iran J Allergy Asthma Immunol. 2017;16(5):433–442.
   PubMed Web of Science ®Google Scholar
• Fattahi MJ, Ahmadi H, Jafarnezhad-Ansariha F, et al. Oral administration effects of β-d-mannuronic acid (M2000) on Th17 and regulatory T cells in patients with ankylosing spondylitis. Biomed Pharmacother. 2018;100:495–500.
   PubMed Web of Science ®Google Scholar
• Rastegari‐Pouyani M, Mostafaie A, Mansouri K, et al. Anti‐angiogenesis effect of β‐d‐mannuronic acid (M2000) as a novel NSAID with immunosuppressive properties under experimental model. Clin Exp Pharmacol Physiol. 2018;45(4):370–376.
   PubMedGoogle Scholar
• Zilahi E, Tarr T, Papp G, et al. Increased microRNA-146a/b, TRAF6 gene and decreased IRAK1 gene expressions in the peripheral mononuclear cells of patients with Sjögren’s syndrome. Immunol Lett. 2012;141(2):165–168.
   PubMed Web of Science ®Google Scholar
• Yousefzadeh N, Alipour MR, Soufi FG. Deregulation of NF-кB-miR-146a negative feedback loop may be involved in the pathogenesis of diabetic neuropathy. J Physiol Biochem. 2015;71(1):51–58.
   PubMed Web of Science ®Google Scholar
• Chatzikyriakidou A, Voulgari PV, Georgiou I, et al. A polymorphism in the 3’-UTR of interleukin-1 receptor-associated kinase (IRAK1), a target gene of miR-146a, is associated with rheumatoid arthritis susceptibility. Joint Bone Spine. 2010;77(5):411–413.
   PubMed Web of Science ®Google Scholar