Intraarticular treatment with integrin α10β1-selected mesenchymal stem cells affects microRNA expression in experimental post-traumatic osteoarthritis in horses.
Abstract: Osteoarthritis (OA) remains a major cause of lameness in horses, which leads to lost days of training and early retirement. Still, the underlying pathological processes are poorly understood. MicroRNAs (miRNAs) are small non-coding RNAs that serve as regulators of many biological processes including OA. Analysis of miRNA expression in diseased joint tissues such as cartilage and synovial membrane may help to elucidate OA pathology. Since integrin α10β1-selected mesenchymal stem cell (integrin α10-MSC) have shown mitigating effect on equine OA we here investigated the effect of integrin α10-MSCs on miRNA expression. Cartilage and synovial membrane was harvested from the middle carpal joint of horses with experimentally induced, untreated OA, horses with experimentally induced OA treated with allogeneic adipose-derived MSCs selected for the marker integrin α10-MSCs, and from healthy control joints. miRNA expression in cartilage and synovial membrane was established by quantifying 70 pre-determined miRNAs by qPCR. Differential expression of the miRNAs was evaluated by comparing untreated OA and control, untreated OA and MSC-treated OA, and joints with high and low pathology score. A total of 60 miRNAs were successfully quantified in the cartilage samples and 55 miRNAs were quantified in the synovial membrane samples. In cartilage, miR-146a, miR-150 and miR-409 had significantly higher expression in untreated OA joints than in control joints. Expression of miR-125a-3p, miR-150, miR-200c, and miR-499-5p was significantly reduced in cartilage from MSC-treated OA joints compared to the untreated OA joints. Expression of miR-139-5p, miR-150, miR-182-5p, miR-200a, miR-378, miR-409-3p, and miR-7177b in articular cartilage reflected pathology score. Several of these miRNAs are known from research in human patients with OA and from murine OA models. Our study shows that these miRNAs are also differentially expressed in experimental equine OA, and that expression depends on OA severity. Moreover, MSC treatment, which resulted in less severe OA, also affected miRNA expression in cartilage.
Copyright © 2024 Andersen, Walters, Bundgaard, Berg, Vonk, Lundgren-Åkerlund, Henriksen, Lindegaard, Skovgaard and Jacobsen.
Publication Date: 2024-03-26 PubMed ID: 38596460PubMed Central: PMC11002141DOI: 10.3389/fvets.2024.1374681Google Scholar: Lookup
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Summary
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The research explores the effect of mesenchymal stem cells (MSCs) selected for the marker integrin α10 on microRNA (miRNA) expression in horses with osteoarthritis. The study found that specific miRNAs show different levels of expression in joints from horses with untreated osteoarthritis versus those treated with MSCs, suggesting that MSC treatment can influence miRNA expression.
Introduction
- The research is centered on osteoarthritis (OA), a significant cause of lameness in horses, contributing to lost training days and early retirement. Unfortunately, the underlying pathological processes remain poorly understood.
- miRNAs are small non-coding RNAs that regulate numerous biological processes, including OA. It is believed that analyzing miRNA expression in diseased joint tissues like cartilage and synovial membrane could enlighten us about the pathology of OA.
Experimentation and Methodology
- In the study, cartilage and synovial membrane were harvested from various horses: those with experimentally induced, untreated OA; those with experimentally induced OA treated with allogeneic adipose-derived MSCs selected for the marker integrin α10-MSCs, and from healthy control joints.
- miRNA expression in cartilage and synovial membrane was established by quantifying 70 pre-determined miRNAs using quantitative PCR (qPCR). The differential expression of the miRNAs was evaluated by comparing various scenarios, such as untreated OA and control, untreated OA and MSC-treated OA, and joints with high and low pathology scores.
Findings and Conclusions
- They found a total of 60 miRNAs quantified in the cartilage samples and 55 miRNAs in the synovial membrane samples. miRNAs like miR-146a, miR-150, and miR-409 had significantly higher expression in untreated OA joints than in control joints.
- The expression of particular miRNAs was drastically reduced in cartilage from MSC-treated OA joints compared to the untreated OA joints. This suggests that MSC treatment affects miRNA expression in a way that potentially reduces OA severity.
- The expression of certain miRNAs in articular cartilage also reflected the pathology score. These findings show that the miRNAs known from research in human patients with OA and from murine OA models are also differentially expressed in experimental equine OA, and their expression depends on OA severity.
Cite This Article
APA
Andersen C, Walters M, Bundgaard L, Berg LC, Vonk LA, Lundgren-Åkerlund E, Henriksen BL, Lindegaard C, Skovgaard K, Jacobsen S.
(2024).
Intraarticular treatment with integrin α10β1-selected mesenchymal stem cells affects microRNA expression in experimental post-traumatic osteoarthritis in horses.
Front Vet Sci, 11, 1374681.
https://doi.org/10.3389/fvets.2024.1374681 Publication
Researcher Affiliations
- Department of Veterinary Clinical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Taastrup, Denmark.
- Department of Veterinary Clinical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Taastrup, Denmark.
- Department of Veterinary Clinical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Taastrup, Denmark.
- Department of Veterinary Clinical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Taastrup, Denmark.
- Xintela AB, Lund, Sweden.
- Xintela AB, Lund, Sweden.
- Department of Biotechnology and Biomedicine, Technical University of Denmark, Lyngby, Denmark.
- Department of Veterinary Clinical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Taastrup, Denmark.
- Department of Biotechnology and Biomedicine, Technical University of Denmark, Lyngby, Denmark.
- Department of Veterinary Clinical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Taastrup, Denmark.
Conflict of Interest Statement
Authors EL-Å and LV were employed by the company Xintela AB. Author EL-Å is the CEO and CSO of Xintela AB, holds stock in the company, is an inventor of a patent related to this study. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
This article includes 98 references
- Murray RC, Walters JM, Snart H, Dyson SJ, Parkin TDH. Identification of risk factors for lameness in dressage horses. Vet J (2010) 184:27–36.
- Egenvall A, Tranquille CA, Lönnell AC, Bitschnau C, Oomen A, Hernlund E. Days-lost to training and competition in relation to workload in 263 elite show-jumping horses in four European countries. Prev Vet Med (2013) 112:387–400.
- Rossdale PD, Hopes R, Digby NJ, Offord K. Epidemiological study of wastage among racehorses 1982 and 1983. Vet Rec (1985) 116:66–9.
- Schlueter AE, Orth MW. Equine osteoarthritis: a brief review of the disease and its causes. Equine Comp Exer Physiol (2004) 1:221–31.
- McIlwraith CW, Frisbie DD, Kawcak CE. The horse as a model of naturally occurring osteoarthritis. Bone Joint Res (2012) 1:297–309.
- Sophia Fox AJ, Bedi A, Rodeo SA. The basic science of articular cartilage: structure, composition, and function. Sports Health (2009) 1:461–8.
- Roseti L, Desando G, Cavallo C, Petretta M, Grigolo B. Articular Cartilage Regeneration in Osteoarthritis. Cells (2019) 8:1305.
- Loeser RF, Goldring SR, Scanzello CR, Goldring MB. Osteoarthritis: a disease of the joint as an organ. Arthritis Rheum (2012) 64:1697–707.
- Barley RDC, Adesida AB, Bagnall KM, Jomha NM. Immunohistochemical characterization of reparative tissue present in human osteoarthritic tissue. Virchows Archiv (2010) 456:561–9.
- Evans CH. Advances in regenerative orthopedics. Mayo Clin Proc (2013) 88:1323–39.
- McIlwraith CW, Frisbie DD, Rodkey WG, Kisiday JD, Werpy NM, Kawcak CE. Evaluation of intra-articular mesenchymal stem cells to augment healing of microfractured chondral defects. Arthroscopy (2011) 27:1552–61.
- Wilke MM, Nydam DV, Nixon AJ. Enhanced early chondrogenesis in articular defects following arthroscopic mesenchymal stem cell implantation in an equine model. J Orthop Res (2007) 25:913–25.
- Delco ML, Goodale M, Talts JF, Pownder SL, Koff MF, Miller AD. Integrin α10β1-selected mesenchymal stem cells mitigate the progression of osteoarthritis in an equine talar impact model. Am J Sports Med (2020) 48:612–23.
- Barrachina L, Remacha AR, Romero A, Vitoria A, Albareda J, Prades M. Assessment of effectiveness and safety of repeat administration of proinflammatory primed allogeneic mesenchymal stem cells in an equine model of chemically induced osteoarthritis. BMC Vet Res (2018) 14:241–17.
- Colbath AC, Dow SW, Hopkins LS, Phillips JN, McIlwraith CW, Goodrich LR. Allogeneic vs. autologous intra-articular mesenchymal stem cell injection within normal horses: Clinical and cytological comparisons suggest safety. Equine Vet J (2020) 52:144–51.
- Broeckx SY, Seys B, Suls M, Vandenberghe A, Mariën T, Adriaensen E. Equine allogeneic chondrogenic induced mesenchymal stem cells are an effective treatment for degenerative joint disease in horses. Stem Cells Dev (2019) 28:410–22.
- Frisbie DD, Kisiday JD, Kawcak CE, Werpy NM, McIlwraith CW. Evaluation of adipose-derived stromal vascular fraction or bone marrow-derived mesenchymal stem cells for treatment of osteoarthritis. J Orthop Res (2009) 27:1675–80.
- Fortier LA, Potter HG, Rickey EJ, Schnabel LV, Foo LF, Chong LR. Concentrated bone marrow aspirate improves full-thickness cartilage repair compared with microfracture in the equine model. J Bone Joint Surg A (2010) 92:1927–37.
- Ferris DJ, Frisbie DD, Kisiday JD, McIlwraith CW, Hague BA, Major MD. Clinical outcome after intra-articular administration of bone marrow derived mesenchymal stem cells in 33 horses with stifle injury. Vet Surg (2014) 43:255–65.
- Mariñas-Pardo L, García-Castro J, Rodríguez-Hurtado I, Rodríguez-García MI, Núñez-Naveira L, Hermida-Prieto M. Allogeneic adipose-derived mesenchymal stem cells (Horse Allo 20) for the treatment of osteoarthritis-associated lameness in horses: characterization, safety, and efficacy of intra-articular treatment. Stem Cells Dev (2018) 27:1147–60.
- Broeckx SY, Martens AM, Bertone AL, Brantegem LVAN, Duchateau L. The use of equine chondrogenic-induced mesenchymal stem cells as a treatment for osteoarthritis: a randomised, double-blinded, placebo-controlled proof-of-concept study. Equine Vet J (2019) 51:787–94.
- Broeckx S, Suls M, Beerts C, Vandenberghe A, Seys B, Wuertz-Kozak K. Allogenic mesenchymal stem cells as a treatment for equine degenerative joint disease: a pilot study. Curr Stem Cell Res Ther (2014) 9:497–503.
- Krampera M, Franchini M, Pizzolo G, Aprili G. Mesenchymal stem cells: from biology to clinical use. Blood Transf (2007) 5:120–9.
- Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD. Multilineage potential of adult human mesenchymal stem cells. Science (1999) 284:143–7.
- Andersen C, Uvebrant K, Mori Y, Aarsvold S, Jacobsen S, Berg LC. Human integrin α10β1-selected mesenchymal stem cells home to cartilage defects in the rabbit knee and assume a chondrocyte-like phenotype. Stem Cell Res Ther (2022) 13:206–15.
- Zhao X, Zhao Y, Sun X, Xing Y, Wang X, Yang Q. Immunomodulation of MSCs and MSC-derived extracellular vesicles in osteoarthritis. Front Bioeng Biotechnol (2020) 8:1–14.
- Li K, Yan G, Huang H, Zheng M, Ma K, Cui X. Anti-inflammatory and immunomodulatory effects of the extracellular vesicles derived from human umbilical cord mesenchymal stem cells on osteoarthritis via M2 macrophages. J Nanobiotechnol (2022) 20:38–20.
- Jiang S, Tian G, Yang Z, Gao X, Wang F, Li J. Enhancement of acellular cartilage matrix scaffold by Wharton’s jelly mesenchymal stem cell-derived exosomes to promote osteochondral regeneration. Bioact Mater (2021) 6:2711–28.
- Matsukawa T, Sakai T, Yonezawa T, Hiraiwa H, Hamada T, Nakashima M. MicroRNA-125b regulates the expression of aggrecanase-1 (ADAMTS-4) in human osteoarthritic chondrocytes. Arthritis Res Ther (2013) 15:R28–11.
- McLeod CM, Mauck RL. On the origin and impact of mesenchymal stem cell heterogeneity: new insights and emerging tools for single cell analysis. Eur Cell Mater (2017) 34:217–31.
- Johal KS, Lees VC, Reid AJ. Adipose-derived stem cells: selecting for translational success. Regen Med (2015) 10:79–96.
- Nielsen FM, Riis SE, Andersen JI, Lesage R, Fink T, Pennisi CP. Discrete adipose-derived stem cell subpopulations may display differential functionality after in vitro expansion despite convergence to a common phenotype distribution. Stem Cell Res Ther (2016) 7:1–13.
- Varas L, Ohlsson LB, Honeth G, Olsson A, Bengtsson T, Wiberg C. α 10 integrin expression is up-regulated on fibroblast growth factor-2-treated mesenchymal stem cells with improved chondrogenic differentiation potential. Stem Cells Dev (2007) 16:965–78.
- Uvebrant K, Rasmusson LR, Talts JF, Alberton P, Aszodi A, Lundgren-Akerlund E. Integrin α10β1 selected equine MSCs have improved chondrogenic differentiation immunomodulatory and cartilage adhesion capacity. Ann Stem Cell Res (2019) 2:1–5.
- Andersen C, Jacobsen S, Uvebrant K, Griffin JF IV, Vonk LA, Walters M. Integrin α10β1-selected mesenchymal stem cells reduce pain and cartilage degradation and increase immunomodulation in an equine osteoarthritis model. Cartilage (2023):1–15.
- Cong L, Zhu Y, Tu G. A bioinformatic analysis of microRNAs role in osteoarthritis. Osteoarthritis Cartilage (2017) 25:1362–71.
- Adams BD, Parsons C, Walker L, Zhang WC, Slack FJ. Targeting noncoding RNAs in disease. J Clin Inves (2017) 127:761–71.
- Lara-Barba E, Araya MJ, Hill CN, Bustamante-Barrientos FA, Ortloff A, García C. Role of microRNA shuttled in small extracellular vesicles derived from mesenchymal stem/stromal cells for osteoarticular disease treatment. Front Immunol (2021) 12:1–13.
- Castanheira C, Balaskas P, Falls C, Ashraf-Kharaz Y, Clegg P, Burke K. Equine synovial fluid small non-coding RNA signatures in early osteoarthritis. BMC Vet Res (2021) 17:26–12.
- Li YH, Tavallaee G, Tokar T, Nakamura A, Sundararajan K, Weston A. Identification of synovial fluid microRNA signature in knee osteoarthritis: differentiating early- and late-stage knee osteoarthritis. Osteoarthritis Cartilage (2016) 24:1577–86.
- Castanheira CIGD, Anderson JR, Fang Y, Milner PI, Goljanek-Whysall K, House L. Mouse microRNA signatures in joint ageing and post-traumatic osteoarthritis. Osteoarthr Cartil Open (2021) 3:100186.
- Ma Y, Wu Y, Chen J, Huang K, Ji B, Chen Z. miR-10a-5p promotes chondrocyte apoptosis in osteoarthritis by targeting HOXA1. Mol Ther Nucleic Acids (2019) 14:398–409.
- Makki MS, Haqqi TM. miR-139 modulates MCPIP1/IL-6 expression and induces apoptosis in human OA chondrocytes. Exp Mol Med (2015) 47:e189–9.
- 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) 474:296–302.
- Liu DH, Jheng YC, Chen PY, Yarmishyn AA, Huang SE, Chien CS. Frontier review of the roles of exosomes in osteoarthritis. J Chin Med Assoc (2021) 84:754–6.
- Malemud CJ. MicroRNAs and osteoarthritis. Cells (2018) 7:1–10.
- Endisha H, Rockel J, Jurisica I, Kapoor M. The complex landscape of microRNAs in articular cartilage: biology, pathology, and therapeutic targets. JCI Insight (2018) 3:1–15.
- Shen P, Yang Y, Liu G, Chen W, Chen J, Wang Q. CircCDK14 protects against osteoarthritis by sponging miR-125a-5p and promoting the expression of Smad2. Theranostics (2020) 10:9113–31.
- Feng L, Feng C, Wang CX, Xu DY, Chen JJ, Huang JF. Circulating microRNA let–7e is decreased in knee osteoarthritis, accompanied by elevated apoptosis and reduced autophagy. Int J Mol Med (2020) 45:1464–76.
- Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ. Combinatorial microRNA target predictions. Nat Genet (2005) 37:495–500.
- Glinge C, Clauss S, Boddum K, Jabbari R, Jabbari J, Risgaard B. Stability of circulating blood-based microRNAs-Pre-analytic methodological considerations. PLoS One (2017) 12:1–16.
- López AG, Brogaard L, Heegaard PMH, Cirera S, Skovgaard K. AU content in the microRNA sequence influences its stability after heat treatment. MicroRNA (2019) 8:216–22.
- Zhang Z, Qin YW, Brewer G, Jing Q. MicroRNA degradation and turnover: regulating the regulators. Wiley Interdiscip Rev RNA (2012) 3:593–600.
- Aryani A, Denecke B. In vitro application of ribonucleases: comparison of the effects on mRNA and miRNA stability. BMC Res Notes (2015) 8:1–9.
- Foland JW, McIlwraith CW, Trotter GW, Powers BE, Lamar CH. Effect of betamethasone and exercise on equine carpal joints with osteochondral fragments. Vet Surg (1994) 23:369–76.
- FRISBIE DD, KAWCAK CE, TROTTER GW, POWERS BE, WALTON RM, McILWRAITH CW. Effects of triamcinolone acetonide on an in vivo equine osteochondral fragment exercise model. Equine Vet J (1997) 29:349–59.
- Frisbie DD, Kawcak CE, Werpy NM, Park RD, McIlwraith CW. Clinical, biochemical, and histologic effects of intra-articular administration of autologous conditioned serum in horses with experimentally induced osteoarthritis. Am J Vet Res (2007) 68:290–6.
- Frisbie DD, Al-Sobayil F, Billinghurst RC, Kawcak CE, McIlwraith CW. Changes in synovial fluid and serum biomarkers with exercise and early osteoarthritis in horses. Osteoarthritis Cartilage (2008) 16:1196–204.
- Frisbie DD, Kawcak CE, Baxter GM, Trotter GW, Powers BE, Lassen ED. Effects of 6α-methylprednisolone acetate on an equine osteochondral fragment exercise model. Am J Vet Res (1998) 59:1619–28.
- McIlwraith CW, Frisbie DD, Kawcak CE. Evaluation of intramuscularly administered sodium pentosan polysulfate for treatment of experimentally induced osteoarthritis in horses. Am J Vet Res (2012) 73:628–33.
- Frisbie DD, Ghivizzani SC, Robbins PD, Evans CH, McIlwraith CW. Treatment of experimental equine osteoarthritis by in vivo delivery of the equine interleukin-1 receptor antagonist gene. Gene Ther (2002) 9:12–20.
- Kawcak CE, Frisbie DD, Werpy NM, Park RD, McIlwraith CW. Effects of exercise vs experimental osteoarthritis on imaging outcomes. Osteoarthritis Cartilage (2008) 16:1519–25.
- Andersen C, Walters M, Jacobsen S, Lindegaard C. A detailed macroscopic scoring system for experimental post-traumatic osteoarthritis in the equine middle carpal joint. BMC Res Notes (2022) 15:1–7.
- Balcells I, Cirera S, Busk PK. Specific and sensitive quantitative RT-PCR of miRNAs with DNA primers. BMC Biotechnol (2011) 11:70.
- Busk PK. A tool for design of primers for microRNA-specific quantitative RT-qPCR. BMC Bioinformatics (2014) 15:1–9.
- Zhang H, Zheng W, Li D, Zheng J. miR-146a-5p promotes chondrocyte apoptosis and inhibits autophagy of osteoarthritis by targeting NUMB. Cartilage (2021) 13:1467S–77S.
- Shao J, Ding Z, Peng J, Zhou R, Li L, Qian Q. MiR-146a-5p promotes IL-1β-induced chondrocyte apoptosis through the TRAF6-mediated NF-kB pathway. Inflam Res (2020) 69:619–30.
- Liu JN, Lu S, Fu CM. MiR-146a expression profiles in osteoarthritis in different tissue sources: a meta-analysis of observational studies. J Orthop Surg Res (2022) 17:148–10.
- Jin L, Zhao J, Jing W. Role of miR-146a in human chondrocyte apoptosis in response to mechanical pressure injury in vitro. Int J Mol Med (2014) 34:451–63.
- Ntoumou E, Tzetis M, Braoudaki M, Lambrou G, Poulou M, Malizos K. Serum microRNA array analysis identifies miR-140-3p, miR-33b-3p and miR-671-3p as potential osteoarthritis biomarkers involved in metabolic processes. Clin Epigenet (2017) 9:127–15.
- Jiang M, Xu K, Ren H, Wang M, Hou X, Cao J. Role of lincRNA-Cox2 targeting miR-150 in regulating the viability of chondrocytes in osteoarthritis. Exp Ther Med (2021) 22:800–9.
- Liu X, Zhou F, Yang Y, Wang W, Niu L, Zuo D. MiR-409-3p and MiR-1896 co-operatively participate in IL-17-induced inflammatory cytokine production in astrocytes and pathogenesis of EAE mice via targeting SOCS3/STAT3 signaling. Glia (2019) 67:101–12.
- He L, Tian L. Downregulation of miR-409-3p suppresses LPS-induced inflammation in human bronchial epithelial cells through SOCS3/JAK1/STAT3 signaling: the implication for bronchopneumonia. Mol Med Rep (2021) 23:1–10.
- Yamasaki K, Nakasa T, Miyaki S, Ishikawa M, Deie M, Adachi N. Expression of microRNA-146 in osteoarthritis cartilage. Arthr Rheumat (2009) 60:1035–41.
- Jones SW, Watkins G, le Good N, Roberts S, Murphy CL, Brockbank SMV. The identification of differentially expressed microRNA in osteoarthritic tissue that modulate the production of TNF-α and MMP13. Osteoarthritis Cartilage (2009) 17:464–72.
- Krejci P, Prochazkova J, Bryja V, Jelinkova P, Pejchalova K, Kozubik A. Fibroblast growth factor inhibits interferon gamma-STAT1 and interleukin 6-STAT3 signaling in chondrocytes. Cell Signal (2009) 21:151–60.
- de Andrés MC, Imagawa K, Hashimoto K, Gonzalez A, Goldring MB, Roach HI. Suppressors of cytokine signalling (SOCS) are reduced in osteoarthritis. Biochem Biophys Res Commun (2011) 407:54–9.
- van de Loo FAJ, Veenbergen S, van den Brand B, Bennink MB, Blaney-Davidson E, Arntz OJ. Enhanced suppressor of cytokine signaling 3 in arthritic cartilage dysregulates human chondrocyte function. Arthritis Rheum (2012) 64:3313–23.
- Gao A, Van Dyke TE. Role of suppressors of cytokine signaling 3 in bone inflammatory responses. Front Immunol (2013) 4:506.
- Koskinen-Kolasa A, Vuolteenaho K, Korhonen R, Moilanen T, Moilanen E. Catabolic and proinflammatory effects of leptin in chondrocytes are regulated by suppressor of cytokine signaling-3. Arthritis Res Ther (2016) 18:215–3.
- Zhang Y, Wang F, Chen G, He R, Yang L. LncRNA MALAT1 promotes osteoarthritis by modulating miR-150-5p/AKT3 axis. Cell Biosci (2019) 9:54–12.
- Wang H, Shu J, Zhang C, Wang Y, Shi R, Yang F. Extracellular vesicle-mediated miR-150-3p delivery in joint homeostasis: a potential treatment for osteoarthritis?. Cells (2022) 11:2766.
- Churov AV, Oleinik EK, Knip M. MicroRNAs in rheumatoid arthritis: altered expression and diagnostic potential. Autoimmun Rev (2015) 14:1029–37.
- Niimoto T, Nakasa T, Ishikawa M, Okuhara A, Izumi B, Deie M. MicroRNA-146a expresses in interleukin-17 producing T cells in rheumatoid arthritis patients. BMC Musculoskelet Disord (2010) 11:209.
- Payet M, Dargai F, Gasque P, Guillot X. Epigenetic regulation (Including micro-rnas, dna methylation and histone modifications) of rheumatoid arthritis: a systematic review. Int J Mol Sci (2021) 22:12170.
- Weishaupt MA, Wiestner T, Hogg HP, Jordan P, Auer JA. Compensatory load redistribution of horses with induced weight-bearing forelimb lameness trotting on a treadmill. Vet J (2006) 171:135–46.
- Kelmer G, Keegen KG, Kramer J, Wilson DA, Pai FP, Singh P. Computer-assisted kinematic evaluation of induced compensatory movements resembling lameness in horses trotting on a treadmill. Am J Vet Res (2005) 66:646–55.
- Yin CM, Suen WCW, Lin S, Wu XM, Li G, Pan XH. Dysregulation of both miR-140-3p and miR-140-5p in synovial fluid correlate with osteoarthritis severity. Bone Joint Res (2017) 6:612–8.
- 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) 9:2852–64.
- Shang G, Wang Y, Xu Y, Zhang S, Sun X, Guan H. Long non-coding RNA TCONS_00041960 enhances osteogenesis and inhibits adipogenesis of rat bone marrow mesenchymal stem cell by targeting miR-204-5p and miR-125a-3p. J Cell Physiol (2018) 233:6041–51.
- Tu XM, Gu YL, Ren GQ. miR-125a-3p targetedly regulates GIT1 expression to inhibit osteoblastic proliferation and differentiation. Exp Ther Med (2016) 12:4099–106.
- Kung LHW, Ravi V, Rowley L, Bell KM, Little CB, Bateman JF. Comprehensive expression analysis of microRNAs and mRNAs in synovial tissue from a mouse model of early post-traumatic osteoarthritis. Sci Rep (2017) 7:17701–12.
- Walters M, Skovgaard K, Heegaard PMH, Peffers MJ, Fang Y, Bundgaard L. Identification and characterization of temporal expression of microRNAs in synovial fluid obtained from an experimental equine model of osteoarthritis. Equine Vet J .
- Van Den Boom R, Van De Lest CHA, Bull S, Brama PAJ, Van Weeren PR, Barneveld A. Influence of repeated arthrocentesis and exercise on synovial fluid concentrations of nitric oxide, prostaglandin E2 and glycosaminoglycans in healthy equine joints. Equine Vet J (2005) 37:250–6.
- Van Den Boom R, Brama PAJ, Kiers GH, DeGroot J, Barneveld A, Van Weeren PR. The influence of repeated arthrocentesis and exercise on matrix metalloproteinase and tumour necrosis factor α activities in normal equine joints. Equine Vet J (2004) 36:155–9.
- Yassin AM, AbuBakr HO, Abdelgalil AI, Farid OA, El-Behairy AM, Gouda EM. Circulating miR-146b and miR-27b are efficient biomarkers for early diagnosis of Equidae osteoarthritis. Sci Rep (2023) 13:7966–11.
- Anderson JR, Jacobsen S, Walters M, Bundgaard L, Diendorfer A, Hackl M. Small non-coding RNA landscape of extracellular vesicles from a post-traumatic model of equine osteoarthritis. Front Vet Sci (2022) 9.
- Baker ME, Lee S, Clinton M, Hackl M, Castanheira C, Peffers MJ. Investigation of microRNA biomarkers in equine distal interphalangeal joint osteoarthritis. Int J Mol Sci (2022) 23.
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