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Published in: Arthritis Research & Therapy 1/2020

Open Access 01-12-2020 | Knee Osteoarthritis | Research article

Association of circulating microRNAs with prevalent and incident knee osteoarthritis in women: the OFELY study

Authors: Jean-Charles Rousseau, Marjorie Millet, Martine Croset, Elisabeth Sornay-Rendu, Olivier Borel, Roland Chapurlat

Published in: Arthritis Research & Therapy | Issue 1/2020

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Abstract

Objectives

In the context of the scarcity of biomarkers for knee osteoarthritis (OA), we examined the associations of prevalent and incident OA with the expression levels of serum miRNAs in subjects with and without OA.

Methods

With a next-generation sequencing approach, we compared the miRome expression of 10 women with knee OA and 10 age-matched healthy subjects. By real-time qPCR, we analyzed the expression levels of 19 miRNAs at baseline selecting 43 women with prevalent knee OA (Kellgren Lawrence score of 2/3), 23 women with incident knee OA over a 4-year follow-up and 67 healthy subjects without prevalent or incident OA matched for age and body mass index.

Results

Serum miR-146a-5p was significantly increased in the group of prevalent knee OA compared with controls (relative quantification (RQ); median [Interquartile range] 1.12 [0.73; 1.46] vs 0.85 [0.62; 1.03], p = 0.015). The likelihood of prevalent knee OA was significantly increased (odds ratio [95% confidence interval (CI)] 1.83 [1.21–2.77], p = 0.004) for each quartile increase in serum miR-146a-5p. The women with miR-146a-5p levels above the median (0.851) had a higher risk of prevalent knee OA compared to those below the median [95% CI] 4.62 [1.85–11.5], p = 0.001. Moreover, we found a significant association between the baseline level of serum miR-186-5p and the risk of incident knee OA (Q4 vs Q1–3; odds ratio [95% CI] 6.13 [1.14–32.9], p = 0.034).

Conclusion

We showed for the first time that miR-146a-5p and miR-186-5p are significantly associated with prevalent and incident knee OA, respectively.
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Literature
1.
go back to reference Martel-Pelletier J, Barr AJ, Cicuttini FM, Conaghan PG, Cooper C, Goldring MB, et al. Osteoarthritis. Nat Rev Dis Primers. 2016;2:16072.PubMedCrossRef Martel-Pelletier J, Barr AJ, Cicuttini FM, Conaghan PG, Cooper C, Goldring MB, et al. Osteoarthritis. Nat Rev Dis Primers. 2016;2:16072.PubMedCrossRef
3.
go back to reference Shorter E, Sannicandro AJ, Poulet B, Goljanek-Whysall K. Skeletal muscle wasting and its relationship with osteoarthritis: a mini-review of mechanisms and current interventions. Curr Rheumatol Rep. 2019;21(8):40.PubMedPubMedCentralCrossRef Shorter E, Sannicandro AJ, Poulet B, Goljanek-Whysall K. Skeletal muscle wasting and its relationship with osteoarthritis: a mini-review of mechanisms and current interventions. Curr Rheumatol Rep. 2019;21(8):40.PubMedPubMedCentralCrossRef
4.
go back to reference Trachana V, Ntoumou E, Anastasopoulou L, Tsezou A. Studying microRNAs in osteoarthritis: critical overview of different analytical approaches. Mech Ageing Dev. 2018;171:15–23.PubMedCrossRef Trachana V, Ntoumou E, Anastasopoulou L, Tsezou A. Studying microRNAs in osteoarthritis: critical overview of different analytical approaches. Mech Ageing Dev. 2018;171:15–23.PubMedCrossRef
5.
go back to reference Jin L, Zhao J, Jing W, Yan S, Wang X, Xiao C, et al. Role of miR-146a in human chondrocyte apoptosis in response to mechanical pressure injury in vitro. Int J Mol Med. 2014;34(2):451–63.PubMedPubMedCentralCrossRef Jin L, Zhao J, Jing W, Yan S, Wang X, Xiao C, et al. Role of miR-146a in human chondrocyte apoptosis in response to mechanical pressure injury in vitro. Int J Mol Med. 2014;34(2):451–63.PubMedPubMedCentralCrossRef
6.
go back to reference Meng F, Zhang Z, Chen W, Huang G, He A, Hou C, et al. MicroRNA-320 regulates matrix metalloproteinase-13 expression in chondrogenesis and interleukin-1beta-induced chondrocyte responses. Osteoarthr Cartil. 2016;24(5):932–41.CrossRef Meng F, Zhang Z, Chen W, Huang G, He A, Hou C, et al. MicroRNA-320 regulates matrix metalloproteinase-13 expression in chondrogenesis and interleukin-1beta-induced chondrocyte responses. Osteoarthr Cartil. 2016;24(5):932–41.CrossRef
7.
go back to reference Ji Q, Xu X, Xu Y, Fan Z, Kang L, Li L, et al. miR-105/Runx2 axis mediates FGF2-induced ADAMTS expression in osteoarthritis cartilage. J Mol Med (Berl). 2016;94(6):681–94.CrossRef Ji Q, Xu X, Xu Y, Fan Z, Kang L, Li L, et al. miR-105/Runx2 axis mediates FGF2-induced ADAMTS expression in osteoarthritis cartilage. J Mol Med (Berl). 2016;94(6):681–94.CrossRef
8.
go back to reference Mao G, Wu P, Zhang Z, Zhang Z, Liao W, Li Y, et al. MicroRNA-92a-3p regulates Aggrecanase-1 and Aggrecanase-2 expression in chondrogenesis and IL-1beta-induced catabolism in human articular chondrocytes. Cell Physiol Biochem. 2017;44(1):38–52.PubMedCrossRef Mao G, Wu P, Zhang Z, Zhang Z, Liao W, Li Y, et al. MicroRNA-92a-3p regulates Aggrecanase-1 and Aggrecanase-2 expression in chondrogenesis and IL-1beta-induced catabolism in human articular chondrocytes. Cell Physiol Biochem. 2017;44(1):38–52.PubMedCrossRef
10.
go back to reference Hu W, Zhang W, Li F, Guo F, Chen A. miR-139 is up-regulated in osteoarthritis and inhibits chondrocyte proliferation and migration possibly via suppressing EIF4G2 and IGF1R. Biochem Biophys Res Commun. 2016;474(2):296–302.PubMedCrossRef Hu W, Zhang W, Li F, Guo F, Chen A. miR-139 is up-regulated in osteoarthritis and inhibits chondrocyte proliferation and migration possibly via suppressing EIF4G2 and IGF1R. Biochem Biophys Res Commun. 2016;474(2):296–302.PubMedCrossRef
11.
go back to reference Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A. 2011;108(12):5003–8.PubMedPubMedCentralCrossRef Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A. 2011;108(12):5003–8.PubMedPubMedCentralCrossRef
12.
13.
go back to reference Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13(4):423–33.PubMedPubMedCentralCrossRef Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 2011;13(4):423–33.PubMedPubMedCentralCrossRef
14.
go back to reference Murata K, Yoshitomi H, Tanida S, Ishikawa M, Nishitani K, Ito H, et al. Plasma and synovial fluid microRNAs as potential biomarkers of rheumatoid arthritis and osteoarthritis. Arthritis Res Ther. 2010;12(3):R86.PubMedPubMedCentralCrossRef Murata K, Yoshitomi H, Tanida S, Ishikawa M, Nishitani K, Ito H, et al. Plasma and synovial fluid microRNAs as potential biomarkers of rheumatoid arthritis and osteoarthritis. Arthritis Res Ther. 2010;12(3):R86.PubMedPubMedCentralCrossRef
15.
go back to reference Zhang L, Yang M, Marks P, White LM, Hurtig M, Mi QS, et al. Serum non-coding RNAs as biomarkers for osteoarthritis progression after ACL injury. Osteoarthr Cartil. 2012;20(12):1631–7.CrossRef Zhang L, Yang M, Marks P, White LM, Hurtig M, Mi QS, et al. Serum non-coding RNAs as biomarkers for osteoarthritis progression after ACL injury. Osteoarthr Cartil. 2012;20(12):1631–7.CrossRef
16.
go back to reference Okuhara A, Nakasa T, Shibuya H, Niimoto T, Adachi N, Deie M, et al. Changes in microRNA expression in peripheral mononuclear cells according to the progression of osteoarthritis. Mod Rheumatol. 2012;22(3):446–57.PubMedCrossRef Okuhara A, Nakasa T, Shibuya H, Niimoto T, Adachi N, Deie M, et al. Changes in microRNA expression in peripheral mononuclear cells according to the progression of osteoarthritis. Mod Rheumatol. 2012;22(3):446–57.PubMedCrossRef
17.
go back to reference Borgonio Cuadra VM, Gonzalez-Huerta NC, Romero-Cordoba S, Hidalgo-Miranda A, Miranda-Duarte A. Altered expression of circulating microRNA in plasma of patients with primary osteoarthritis and in silico analysis of their pathways. PLoS One. 2014;9(6):e97690.PubMedPubMedCentralCrossRef Borgonio Cuadra VM, Gonzalez-Huerta NC, Romero-Cordoba S, Hidalgo-Miranda A, Miranda-Duarte A. Altered expression of circulating microRNA in plasma of patients with primary osteoarthritis and in silico analysis of their pathways. PLoS One. 2014;9(6):e97690.PubMedPubMedCentralCrossRef
18.
go back to reference Beyer C, Zampetaki A, Lin NY, Kleyer A, Perricone C, Iagnocco A, et al. Signature of circulating microRNAs in osteoarthritis. Ann Rheum Dis. 2015;74(3):e18.PubMedCrossRef Beyer C, Zampetaki A, Lin NY, Kleyer A, Perricone C, Iagnocco A, et al. Signature of circulating microRNAs in osteoarthritis. Ann Rheum Dis. 2015;74(3):e18.PubMedCrossRef
19.
go back to reference Li YH, Tavallaee G, Tokar T, Nakamura A, Sundararajan K, Weston A, et al. Identification of synovial fluid microRNA signature in knee osteoarthritis: differentiating early- and late-stage knee osteoarthritis. Osteoarthr Cartil. 2016;24(9):1577–86.CrossRef Li YH, Tavallaee G, Tokar T, Nakamura A, Sundararajan K, Weston A, et al. Identification of synovial fluid microRNA signature in knee osteoarthritis: differentiating early- and late-stage knee osteoarthritis. Osteoarthr Cartil. 2016;24(9):1577–86.CrossRef
20.
go back to reference Soyocak A, Kurt H, Ozgen M, Turgut Cosan D, Colak E, Gunes HV. miRNA-146a, miRNA-155 and JNK expression levels in peripheral blood mononuclear cells according to grade of knee osteoarthritis. Gene. 2017;627:207–11.PubMedCrossRef Soyocak A, Kurt H, Ozgen M, Turgut Cosan D, Colak E, Gunes HV. miRNA-146a, miRNA-155 and JNK expression levels in peripheral blood mononuclear cells according to grade of knee osteoarthritis. Gene. 2017;627:207–11.PubMedCrossRef
21.
go back to reference Kong R, Gao J, Si Y, Zhao D. Combination of circulating miR-19b-3p, miR-122-5p and miR-486-5p expressions correlates with risk and disease severity of knee osteoarthritis. Am J Transl Res. 2017;9(6):2852–64.PubMedPubMedCentral Kong R, Gao J, Si Y, Zhao D. Combination of circulating miR-19b-3p, miR-122-5p and miR-486-5p expressions correlates with risk and disease severity of knee osteoarthritis. Am J Transl Res. 2017;9(6):2852–64.PubMedPubMedCentral
22.
go back to reference Ntoumou E, Tzetis M, Braoudaki M, Lambrou G, Poulou M, Malizos K, et al. Serum microRNA array analysis identifies miR-140-3p, miR-33b-3p and miR-671-3p as potential osteoarthritis biomarkers involved in metabolic processes. Clin Epigenetics. 2017;9:127.PubMedPubMedCentralCrossRef Ntoumou E, Tzetis M, Braoudaki M, Lambrou G, Poulou M, Malizos K, et al. Serum microRNA array analysis identifies miR-140-3p, miR-33b-3p and miR-671-3p as potential osteoarthritis biomarkers involved in metabolic processes. Clin Epigenetics. 2017;9:127.PubMedPubMedCentralCrossRef
23.
go back to reference Arlot ME, Sornay-Rendu E, Garnero P, Vey-Marty B, Delmas PD. Apparent pre- and postmenopausal bone loss evaluated by DXA at different skeletal sites in women: the OFELY cohort. J Bone Miner Res. 1997;12(4):683–90.PubMedCrossRef Arlot ME, Sornay-Rendu E, Garnero P, Vey-Marty B, Delmas PD. Apparent pre- and postmenopausal bone loss evaluated by DXA at different skeletal sites in women: the OFELY cohort. J Bone Miner Res. 1997;12(4):683–90.PubMedCrossRef
24.
go back to reference Rousseau JC, Sornay-Rendu E, Bertholon C, Garnero P, Chapurlat R. Serum periostin is associated with prevalent knee osteoarthritis and disease incidence/progression in women: the OFELY study. Osteoarthr Cartil. 2015;23(10):1736–42.CrossRef Rousseau JC, Sornay-Rendu E, Bertholon C, Garnero P, Chapurlat R. Serum periostin is associated with prevalent knee osteoarthritis and disease incidence/progression in women: the OFELY study. Osteoarthr Cartil. 2015;23(10):1736–42.CrossRef
25.
go back to reference Peterfy C, Li J, Zaim S, Duryea J, Lynch J, Miaux Y, et al. Comparison of fixed-flexion positioning with fluoroscopic semi-flexed positioning for quantifying radiographic joint-space width in the knee: test-retest reproducibility. Skelet Radiol. 2003;32(3):128–32.CrossRef Peterfy C, Li J, Zaim S, Duryea J, Lynch J, Miaux Y, et al. Comparison of fixed-flexion positioning with fluoroscopic semi-flexed positioning for quantifying radiographic joint-space width in the knee: test-retest reproducibility. Skelet Radiol. 2003;32(3):128–32.CrossRef
26.
go back to reference Garnero P, Sornay-Rendu E, Arlot M, Christiansen C, Delmas PD. Association between spine disc degeneration and type II collagen degradation in postmenopausal women: the OFELY study. Arthritis Rheum. 2004;50(10):3137–44.PubMedCrossRef Garnero P, Sornay-Rendu E, Arlot M, Christiansen C, Delmas PD. Association between spine disc degeneration and type II collagen degradation in postmenopausal women: the OFELY study. Arthritis Rheum. 2004;50(10):3137–44.PubMedCrossRef
28.
go back to reference Gensburger D, Roux JP, Arlot M, Sornay-Rendu E, Ravaud P, Chapurlat R. Influence of blinding sequence of radiographs on the reproducibility and sensitivity to change of joint space width measurement in knee osteoarthritis. Arthritis Care Res (Hoboken). 2010;62(12):1699–705.CrossRef Gensburger D, Roux JP, Arlot M, Sornay-Rendu E, Ravaud P, Chapurlat R. Influence of blinding sequence of radiographs on the reproducibility and sensitivity to change of joint space width measurement in knee osteoarthritis. Arthritis Care Res (Hoboken). 2010;62(12):1699–705.CrossRef
29.
go back to reference Akhtar N, Haqqi TM. MicroRNA-199a* regulates the expression of cyclooxygenase-2 in human chondrocytes. Ann Rheum Dis. 2012;71(6):1073–80.PubMedCrossRef Akhtar N, Haqqi TM. MicroRNA-199a* regulates the expression of cyclooxygenase-2 in human chondrocytes. Ann Rheum Dis. 2012;71(6):1073–80.PubMedCrossRef
30.
go back to reference Ukai T, Sato M, Akutsu H, Umezawa A, Mochida J. MicroRNA-199a-3p, microRNA-193b, and microRNA-320c are correlated to aging and regulate human cartilage metabolism. J Orthop Res. 2012;30(12):1915–22.PubMedCrossRef Ukai T, Sato M, Akutsu H, Umezawa A, Mochida J. MicroRNA-199a-3p, microRNA-193b, and microRNA-320c are correlated to aging and regulate human cartilage metabolism. J Orthop Res. 2012;30(12):1915–22.PubMedCrossRef
31.
go back to reference Le LT, Swingler TE, Crowe N, Vincent TL, Barter MJ, Donell ST, et al. The microRNA-29 family in cartilage homeostasis and osteoarthritis. J Mol Med (Berl). 2016;94(5):583–96.CrossRef Le LT, Swingler TE, Crowe N, Vincent TL, Barter MJ, Donell ST, et al. The microRNA-29 family in cartilage homeostasis and osteoarthritis. J Mol Med (Berl). 2016;94(5):583–96.CrossRef
32.
go back to reference Yamasaki K, Nakasa T, Miyaki S, Ishikawa M, Deie M, Adachi N, et al. Expression of MicroRNA-146a in osteoarthritis cartilage. Arthritis Rheum. 2009;60(4):1035–41.PubMedPubMedCentralCrossRef Yamasaki K, Nakasa T, Miyaki S, Ishikawa M, Deie M, Adachi N, et al. Expression of MicroRNA-146a in osteoarthritis cartilage. Arthritis Rheum. 2009;60(4):1035–41.PubMedPubMedCentralCrossRef
33.
go back to reference Zhang X, Wang C, Zhao J, Xu J, Geng Y, Dai L, et al. miR-146a facilitates osteoarthritis by regulating cartilage homeostasis via targeting Camk2d and Ppp3r2. Cell Death Dis. 2017;8(4):e2734.PubMedPubMedCentralCrossRef Zhang X, Wang C, Zhao J, Xu J, Geng Y, Dai L, et al. miR-146a facilitates osteoarthritis by regulating cartilage homeostasis via targeting Camk2d and Ppp3r2. Cell Death Dis. 2017;8(4):e2734.PubMedPubMedCentralCrossRef
34.
go back to reference Li J, Huang J, Dai L, Yu D, Chen Q, Zhang X, et al. miR-146a, an IL-1beta responsive miRNA, induces vascular endothelial growth factor and chondrocyte apoptosis by targeting Smad4. Arthritis Res Ther. 2012;14(2):R75.PubMedPubMedCentralCrossRef Li J, Huang J, Dai L, Yu D, Chen Q, Zhang X, et al. miR-146a, an IL-1beta responsive miRNA, induces vascular endothelial growth factor and chondrocyte apoptosis by targeting Smad4. Arthritis Res Ther. 2012;14(2):R75.PubMedPubMedCentralCrossRef
35.
go back to reference Zhang F, Wang J, Chu J, Yang C, Xiao H, Zhao C, et al. MicroRNA-146a induced by hypoxia promotes chondrocyte autophagy through Bcl-2. Cell Physiol Biochem. 2015;37(4):1442–53.PubMedCrossRef Zhang F, Wang J, Chu J, Yang C, Xiao H, Zhao C, et al. MicroRNA-146a induced by hypoxia promotes chondrocyte autophagy through Bcl-2. Cell Physiol Biochem. 2015;37(4):1442–53.PubMedCrossRef
36.
go back to reference Wang JH, Shih KS, Wu YW, Wang AW, Yang CR. Histone deacetylase inhibitors increase microRNA-146a expression and enhance negative regulation of interleukin-1beta signaling in osteoarthritis fibroblast-like synoviocytes. Osteoarthr Cartil. 2013;21(12):1987–96.CrossRef Wang JH, Shih KS, Wu YW, Wang AW, Yang CR. Histone deacetylase inhibitors increase microRNA-146a expression and enhance negative regulation of interleukin-1beta signaling in osteoarthritis fibroblast-like synoviocytes. Osteoarthr Cartil. 2013;21(12):1987–96.CrossRef
37.
go back to reference Gu SX, Li X, Hamilton JL, Chee A, Kc R, Chen D, et al. MicroRNA-146a reduces IL-1 dependent inflammatory responses in the intervertebral disc. Gene. 2015;555(2):80–7.PubMedCrossRef Gu SX, Li X, Hamilton JL, Chee A, Kc R, Chen D, et al. MicroRNA-146a reduces IL-1 dependent inflammatory responses in the intervertebral disc. Gene. 2015;555(2):80–7.PubMedCrossRef
38.
go back to reference Zhong JH, Li J, Liu CF, Liu N, Bian RX, Zhao SM, et al. Effects of microRNA-146a on the proliferation and apoptosis of human osteoarthritis chondrocytes by targeting TRAF6 through the NF-kappaB signalling pathway. Biosci Rep. 2017;37(2). Zhong JH, Li J, Liu CF, Liu N, Bian RX, Zhao SM, et al. Effects of microRNA-146a on the proliferation and apoptosis of human osteoarthritis chondrocytes by targeting TRAF6 through the NF-kappaB signalling pathway. Biosci Rep. 2017;37(2).
39.
go back to reference Guan YJ, Li J, Yang X, Du S, Ding J, Gao Y, et al. Evidence that miR-146a attenuates aging- and trauma-induced osteoarthritis by inhibiting Notch1, IL-6, and IL-1 mediated catabolism. Aging Cell. 2018;17(3):e12752.PubMedPubMedCentralCrossRef Guan YJ, Li J, Yang X, Du S, Ding J, Gao Y, et al. Evidence that miR-146a attenuates aging- and trauma-induced osteoarthritis by inhibiting Notch1, IL-6, and IL-1 mediated catabolism. Aging Cell. 2018;17(3):e12752.PubMedPubMedCentralCrossRef
40.
go back to reference Nakasa T, Shibuya H, Nagata Y, Niimoto T, Ochi M. The inhibitory effect of microRNA-146a expression on bone destruction in collagen-induced arthritis. Arthritis Rheum. 2011;63(6):1582–90.PubMedCrossRef Nakasa T, Shibuya H, Nagata Y, Niimoto T, Ochi M. The inhibitory effect of microRNA-146a expression on bone destruction in collagen-induced arthritis. Arthritis Rheum. 2011;63(6):1582–90.PubMedCrossRef
41.
go back to reference Islam F, Gopalan V, Vider J, Wahab R, Ebrahimi F, Lu CT, et al. MicroRNA-186-5p overexpression modulates colon cancer growth by repressing the expression of the FAM134B tumour inhibitor. Exp Cell Res. 2017;357(2):260–70.PubMedCrossRef Islam F, Gopalan V, Vider J, Wahab R, Ebrahimi F, Lu CT, et al. MicroRNA-186-5p overexpression modulates colon cancer growth by repressing the expression of the FAM134B tumour inhibitor. Exp Cell Res. 2017;357(2):260–70.PubMedCrossRef
42.
go back to reference Weber A, Mak SH, Berenbaum F, Sellam J, Zheng YP, Han Y, et al. Association between osteoarthritis and increased risk of dementia: a systemic review and meta-analysis. Medicine (Baltimore). 2019;98(10):e14355.CrossRef Weber A, Mak SH, Berenbaum F, Sellam J, Zheng YP, Han Y, et al. Association between osteoarthritis and increased risk of dementia: a systemic review and meta-analysis. Medicine (Baltimore). 2019;98(10):e14355.CrossRef
43.
go back to reference Satoh J, Kino Y, Niida S. MicroRNA-Seq data analysis pipeline to identify blood biomarkers for Alzheimer’s disease from public data. Biomark Insights. 2015;10:21–31.PubMedPubMedCentralCrossRef Satoh J, Kino Y, Niida S. MicroRNA-Seq data analysis pipeline to identify blood biomarkers for Alzheimer’s disease from public data. Biomark Insights. 2015;10:21–31.PubMedPubMedCentralCrossRef
44.
go back to reference Dimitroulas T, Duarte RV, Behura A, Kitas GD, Raphael JH. Neuropathic pain in osteoarthritis: a review of pathophysiological mechanisms and implications for treatment. Semin Arthritis Rheum. 2014;44(2):145–54.PubMedCrossRef Dimitroulas T, Duarte RV, Behura A, Kitas GD, Raphael JH. Neuropathic pain in osteoarthritis: a review of pathophysiological mechanisms and implications for treatment. Semin Arthritis Rheum. 2014;44(2):145–54.PubMedCrossRef
45.
go back to reference Jiang BC, Cao DL, Zhang X, Zhang ZJ, He LN, Li CH, et al. CXCL13 drives spinal astrocyte activation and neuropathic pain via CXCR5. J Clin Invest. 2016;126(2):745–61.PubMedPubMedCentralCrossRef Jiang BC, Cao DL, Zhang X, Zhang ZJ, He LN, Li CH, et al. CXCL13 drives spinal astrocyte activation and neuropathic pain via CXCR5. J Clin Invest. 2016;126(2):745–61.PubMedPubMedCentralCrossRef
46.
go back to reference Nielen MM, van Sijl AM, Peters MJ, Verheij RA, Schellevis FG, Nurmohamed MT. Cardiovascular disease prevalence in patients with inflammatory arthritis, diabetes mellitus and osteoarthritis: a cross-sectional study in primary care. BMC Musculoskelet Disord. 2012;13:150.PubMedPubMedCentralCrossRef Nielen MM, van Sijl AM, Peters MJ, Verheij RA, Schellevis FG, Nurmohamed MT. Cardiovascular disease prevalence in patients with inflammatory arthritis, diabetes mellitus and osteoarthritis: a cross-sectional study in primary care. BMC Musculoskelet Disord. 2012;13:150.PubMedPubMedCentralCrossRef
47.
go back to reference Wang KJ, Zhao X, Liu YZ, Zeng QT, Mao XB, Li SN, et al. Circulating MiR-19b-3p, MiR-134-5p and MiR-186-5p are promising novel biomarkers for early diagnosis of acute myocardial infarction. Cell Physiol Biochem. 2016;38(3):1015–29.PubMedCrossRef Wang KJ, Zhao X, Liu YZ, Zeng QT, Mao XB, Li SN, et al. Circulating MiR-19b-3p, MiR-134-5p and MiR-186-5p are promising novel biomarkers for early diagnosis of acute myocardial infarction. Cell Physiol Biochem. 2016;38(3):1015–29.PubMedCrossRef
48.
go back to reference Sornay-Rendu E, Munoz F, Duboeuf F, Delmas PD, Study O. Disc space narrowing is associated with an increased vertebral fracture risk in postmenopausal women: the OFELY Study. J Bone Miner Res. 2004;19(12):1994–9.PubMedCrossRef Sornay-Rendu E, Munoz F, Duboeuf F, Delmas PD, Study O. Disc space narrowing is associated with an increased vertebral fracture risk in postmenopausal women: the OFELY Study. J Bone Miner Res. 2004;19(12):1994–9.PubMedCrossRef
49.
go back to reference Sornay-Rendu E, Allard C, Munoz F, Duboeuf F, Delmas PD. Disc space narrowing as a new risk factor for vertebral fracture: the OFELY study. Arthritis Rheum. 2006;54(4):1262–9.PubMedCrossRef Sornay-Rendu E, Allard C, Munoz F, Duboeuf F, Delmas PD. Disc space narrowing as a new risk factor for vertebral fracture: the OFELY study. Arthritis Rheum. 2006;54(4):1262–9.PubMedCrossRef
50.
go back to reference O’Neill TW, McCloskey EV, Kanis JA, Bhalla AK, Reeve J, Reid DM, et al. The distribution, determinants, and clinical correlates of vertebral osteophytosis: a population based survey. J Rheumatol. 1999;26(4):842–8.PubMed O’Neill TW, McCloskey EV, Kanis JA, Bhalla AK, Reeve J, Reid DM, et al. The distribution, determinants, and clinical correlates of vertebral osteophytosis: a population based survey. J Rheumatol. 1999;26(4):842–8.PubMed
51.
go back to reference Liu G, Peacock M, Eilam O, Dorulla G, Braunstein E, Johnston CC. Effect of osteoarthritis in the lumbar spine and hip on bone mineral density and diagnosis of osteoporosis in elderly men and women. Osteoporos Int. 1997;7(6):564–9.PubMedCrossRef Liu G, Peacock M, Eilam O, Dorulla G, Braunstein E, Johnston CC. Effect of osteoarthritis in the lumbar spine and hip on bone mineral density and diagnosis of osteoporosis in elderly men and women. Osteoporos Int. 1997;7(6):564–9.PubMedCrossRef
52.
go back to reference Wu J, Cai H, Xiang YB, Matthews CE, Ye F, Zheng W, et al. Intra-individual variation of miRNA expression levels in human plasma samples. Biomarkers. 2018;23(4):339–46.PubMedPubMedCentralCrossRef Wu J, Cai H, Xiang YB, Matthews CE, Ye F, Zheng W, et al. Intra-individual variation of miRNA expression levels in human plasma samples. Biomarkers. 2018;23(4):339–46.PubMedPubMedCentralCrossRef
53.
Metadata
Title
Association of circulating microRNAs with prevalent and incident knee osteoarthritis in women: the OFELY study
Authors
Jean-Charles Rousseau
Marjorie Millet
Martine Croset
Elisabeth Sornay-Rendu
Olivier Borel
Roland Chapurlat
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2020
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/s13075-019-2086-5

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