Extracellular Vesicles in Joint Disease and Therapy.
Abstract: The use of extracellular vesicles (EVs) as a potential therapy is currently explored for different disease areas. When it comes to the treatment of joint diseases this approach is still in its infancy. As in joint diseases both inflammation and the associated articular tissue destruction are important factors, both the immune-suppressive and the regenerative properties of EVs are potentially advantageous characteristics for future therapy. There is, however, only limited knowledge on the basic features, such as numerical profile and function, of EVs in joint articular tissues in general and their linking medium, the synovial fluid, in particular. Further insight is urgently needed in order to appreciate the full potential of EVs and to exploit these in EV-mediated therapies. Physiologic joint homeostasis is a prerequisite for proper functioning of joints and we postulate that EVs play a key role in the regulation of joint homeostasis and hence can have an important function in re-establishing disturbed joint homeostasis, and, in parallel, in the regeneration of articular tissues. In this mini-review EVs in the joint are explained from a historical perspective in both health and disease, including the potential niche for EVs in articular tissue regeneration. Furthermore, the translational potential of equine models for human joint biology is discussed. Finally, the use of MSC-derived EVs that is recently gaining ground is highlighted and recommendations are given for further EV research in this field.
Publication Date: 2018-11-12 PubMed ID: 30483255PubMed Central: PMC6240615DOI: 10.3389/fimmu.2018.02575Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Research Support
- Non-U.S. Gov't
- Review
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research article discusses the potential therapeutic use of extracellular vesicles (EVs) for joint diseases. Current understanding of EVs’ basic features is limited, particularly in their numerical profile and function in joint articular tissues and synovial fluid. The authors postulate that EVs might play a crucial role in maintaining joint homeostasis and could be significant in re-establishing disturbed joint homeostasis and regenerating articular tissues. The article also discusses the growing use of mesenchymal stem cell (MSC)-derived EVs.
Role of Extracellular Vesicles in Joint Diseases
- Extracellular Vesicles (EVs) have recently come under scrutiny for their potential therapeutic applications in various disease areas. However, their use in the treatment of joint diseases is relatively new and still under exploration.
- Joint diseases are characterized by inflammation and associated articular tissue destruction. Therefore, the immune-suppressive and regenerative properties of EVs could be advantageous for future therapy in this field.
Limited Knowledge on EVs in Joint Articular Tissues
- There is currently limited knowledge on the numerical profile and function of EVs in joint articular tissues and synovial fluid. Exploring these aspects in detail is essential to understand the full potential of EVs and to develop efficacious EV-mediated therapies.
- EVs may play a critical role in maintaining joint homeostasis, a balanced state necessary for proper joint function.
- They could also be instrumental in re-establishing disturbed joint homeostasis and assisting in the regeneration of articular tissues.
EVs in Articular Tissue Regeneration
- This review elaborates on the historical perspective of EVs in joint health and disease, including their potential role in articular tissue regeneration.
- Equine models are suggested to have translational potential for understanding human joint biology. Further research in this direction is encouraged.
Use of Mesenchymal Stem Cell-Derived EVs
- Mesenchymal Stem Cell (MSC)-derived EVs are gaining attention for their potential use in therapeutics.
- The paper highlights this recent development and provides recommendations for further research in the field of EVs, especially in the context of joint diseases.
Cite This Article
APA
Boere J, Malda J, van de Lest CHA, van Weeren PR, Wauben MHM.
(2018).
Extracellular Vesicles in Joint Disease and Therapy.
Front Immunol, 9, 2575.
https://doi.org/10.3389/fimmu.2018.02575 Publication
Researcher Affiliations
- Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, Netherlands.
- Department of Biochemistry & Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, Netherlands.
- Department of Orthopaedics, University Medical Center Utrecht, Utrecht, Netherlands.
- Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, Netherlands.
- Department of Orthopaedics, University Medical Center Utrecht, Utrecht, Netherlands.
- Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, Netherlands.
- Department of Biochemistry & Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, Netherlands.
- Department of Equine Sciences, Faculty of Veterinary Medicine, Utrecht University, Utrecht, Netherlands.
- Department of Biochemistry & Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, Netherlands.
MeSH Terms
- Animals
- Biological Therapy / trends
- Disease Models, Animal
- Extracellular Vesicles / metabolism
- Homeostasis
- Horses
- Humans
- Joint Diseases / metabolism
- Joint Diseases / pathology
- Joint Diseases / therapy
- Joints / pathology
- Mesenchymal Stem Cells / metabolism
- Regeneration
- Stem Cell Niche
Grant Funding
- 647426 / European Research Council
References
This article includes 120 references
- Lunenfeld B, Stratton P. The clinical consequences of an ageing world and preventive strategies.. Best Pract Res Clin Obstet Gynaecol 2013 Oct;27(5):643-59.
- Caron J. Osteoarthritis. In: Ross M, Dyson S, editors. Diagnosis and Management of Lameness in the Horse. Philadelphia, PA: Elsevier Saunders; (2011). p. 655–68.
- Hui AY, McCarty WJ, Masuda K, Firestein GS, Sah RL. A systems biology approach to synovial joint lubrication in health, injury, and disease.. Wiley Interdiscip Rev Syst Biol Med 2012 Jan-Feb;4(1):15-37.
- de Grauw JC. Molecular monitoring of equine joint homeostasis.. Vet Q 2011 Jun;31(2):77-86.
- Goldring MB, Marcu KB. Cartilage homeostasis in health and rheumatic diseases.. Arthritis Res Ther 2009;11(3):224.
- Wojdasiewicz P, Poniatowski ŁA, Szukiewicz D. The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of osteoarthritis.. Mediators Inflamm 2014;2014:561459.
- Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes/microvesicles as a mechanism of cell-to-cell communication.. Kidney Int 2010 Nov;78(9):838-48.
- Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses.. Nat Rev Immunol 2009 Aug;9(8):581-93.
- Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake.. J Extracell Vesicles 2014;3.
- Yáñez-Mó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, Colás E, Cordeiro-da Silva A, Fais S, Falcon-Perez JM, Ghobrial IM, Giebel B, Gimona M, Graner M, Gursel I, Gursel M, Heegaard NH, Hendrix A, Kierulf P, Kokubun K, Kosanovic M, Kralj-Iglic V, Krämer-Albers EM, Laitinen S, Lässer C, Lener T, Ligeti E, Linē A, Lipps G, Llorente A, Lötvall J, Manček-Keber M, Marcilla A, Mittelbrunn M, Nazarenko I, Nolte-'t Hoen EN, Nyman TA, O'Driscoll L, Olivan M, Oliveira C, Pállinger É, Del Portillo HA, Reventós J, Rigau M, Rohde E, Sammar M, Sánchez-Madrid F, Santarém N, Schallmoser K, Ostenfeld MS, Stoorvogel W, Stukelj R, Van der Grein SG, Vasconcelos MH, Wauben MH, De Wever O. Biological properties of extracellular vesicles and their physiological functions.. J Extracell Vesicles 2015;4:27066.
- van Niel G, D'Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles.. Nat Rev Mol Cell Biol 2018 Apr;19(4):213-228.
- Subra C, Grand D, Laulagnier K, Stella A, Lambeau G, Paillasse M, De Medina P, Monsarrat B, Perret B, Silvente-Poirot S, Poirot M, Record M. Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins.. J Lipid Res 2010 Aug;51(8):2105-20.
- Record M, Carayon K, Poirot M, Silvente-Poirot S. Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies.. Biochim Biophys Acta 2014 Jan;1841(1):108-20.
- Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells.. Nat Cell Biol 2007 Jun;9(6):654-9.
- Yoon YJ, Kim OY, Gho YS. Extracellular vesicles as emerging intercellular communicasomes.. BMB Rep 2014 Oct;47(10):531-9.
- Subra C, Laulagnier K, Perret B, Record M. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies.. Biochimie 2007 Feb;89(2):205-12.
- Llorente A, Skotland T, Sylvänne T, Kauhanen D, Róg T, Orłowski A, Vattulainen I, Ekroos K, Sandvig K. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells.. Biochim Biophys Acta 2013 Jul;1831(7):1302-9.
- Solomon DH, Browning JA, Wilkins RJ. Inorganic phosphate transport in matrix vesicles from bovine articular cartilage.. Acta Physiol (Oxf) 2007 Jun;190(2):119-25.
- Kirsch T, Harrison G, Golub EE, Nah HD. The roles of annexins and types II and X collagen in matrix vesicle-mediated mineralization of growth plate cartilage.. J Biol Chem 2000 Nov 10;275(45):35577-83.
- De Toro J, Herschlik L, Waldner C, Mongini C. Emerging roles of exosomes in normal and pathological conditions: new insights for diagnosis and therapeutic applications.. Front Immunol 2015;6:203.
- Nolte-'t Hoen EN, Wauben MH. Immune cell-derived vesicles: modulators and mediators of inflammation.. Curr Pharm Des 2012;18(16):2357-68.
- van der Vlist EJ, Arkesteijn GJ, van de Lest CH, Stoorvogel W, Nolte-'t Hoen EN, Wauben MH. CD4(+) T cell activation promotes the differential release of distinct populations of nanosized vesicles.. J Extracell Vesicles 2012;1.
- Kim JH, Lee J, Park J, Gho YS. Gram-negative and Gram-positive bacterial extracellular vesicles.. Semin Cell Dev Biol 2015 Apr;40:97-104.
- Szempruch AJ, Dennison L, Kieft R, Harrington JM, Hajduk SL. Sending a message: extracellular vesicles of pathogenic protozoan parasites.. Nat Rev Microbiol 2016 Nov;14(11):669-675.
- Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes.. Nat Biotechnol 2011 Apr;29(4):341-5.
- Boukouris S, Mathivanan S. Exosomes in bodily fluids are a highly stable resource of disease biomarkers.. Proteomics Clin Appl 2015 Apr;9(3-4):358-67.
- Verma M, Lam TK, Hebert E, Divi RL. Extracellular vesicles: potential applications in cancer diagnosis, prognosis, and epidemiology.. BMC Clin Pathol 2015;15:6.
- Gámez-Valero A, Lozano-Ramos SI, Bancu I, Lauzurica-Valdemoros R, Borràs FE. Urinary extracellular vesicles as source of biomarkers in kidney diseases.. Front Immunol 2015;6:6.
- Anderson HC. Electron microscopic studies of induced cartilage development and calcification.. J Cell Biol 1967 Oct;35(1):81-101.
- Anderson HC. Vesicles associated with calcification in the matrix of epiphyseal cartilage.. J Cell Biol 1969 Apr;41(1):59-72.
- Bonucci E. Fine structure of early cartilage calcification.. J Ultrastruct Res 1967 Sep;20(1):33-50.
- Hessle L, Johnson KA, Anderson HC, Narisawa S, Sali A, Goding JW, Terkeltaub R, Millan JL. Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization.. Proc Natl Acad Sci U S A 2002 Jul 9;99(14):9445-9.
- Anderson HC. Matrix vesicles and calcification.. Curr Rheumatol Rep 2003 Jun;5(3):222-6.
- Nahar NN, Missana LR, Garimella R, Tague SE, Anderson HC. Matrix vesicles are carriers of bone morphogenetic proteins (BMPs), vascular endothelial growth factor (VEGF), and noncollagenous matrix proteins.. J Bone Miner Metab 2008;26(5):514-9.
- Cui L, Houston DA, Farquharson C, MacRae VE. Characterisation of matrix vesicles in skeletal and soft tissue mineralisation.. Bone 2016 Jun;87:147-58.
- Anderson HC. Molecular biology of matrix vesicles.. Clin Orthop Relat Res 1995 May;(314):266-80.
- Stewart AJ, Roberts SJ, Seawright E, Davey MG, Fleming RH, Farquharson C. The presence of PHOSPHO1 in matrix vesicles and its developmental expression prior to skeletal mineralization.. Bone 2006 Nov;39(5):1000-1007.
- Johnson KA, Hessle L, Vaingankar S, Wennberg C, Mauro S, Narisawa S, Goding JW, Sano K, Millan JL, Terkeltaub R. Osteoblast tissue-nonspecific alkaline phosphatase antagonizes and regulates PC-1.. Am J Physiol Regul Integr Comp Physiol 2000 Oct;279(4):R1365-77.
- Roberts S, Narisawa S, Harmey D, Millán JL, Farquharson C. Functional involvement of PHOSPHO1 in matrix vesicle-mediated skeletal mineralization.. J Bone Miner Res 2007 Apr;22(4):617-27.
- Roberts SJ, Stewart AJ, Sadler PJ, Farquharson C. Human PHOSPHO1 exhibits high specific phosphoethanolamine and phosphocholine phosphatase activities.. Biochem J 2004 Aug 15;382(Pt 1):59-65.
- Iannotti JP, Naidu S, Noguchi Y, Hunt RM, Brighton CT. Growth plate matrix vesicle biogenesis. The role of intracellular calcium.. Clin Orthop Relat Res 1994 Sep;(306):222-9.
- Roach HI, Clarke NM. Physiological cell death of chondrocytes in vivo is not confined to apoptosis. New observations on the mammalian growth plate.. J Bone Joint Surg Br 2000 May;82(4):601-13.
- Morhayim J, Baroncelli M, van Leeuwen JP. Extracellular vesicles: specialized bone messengers.. Arch Biochem Biophys 2014 Nov 1;561:38-45.
- Lefebvre V, Bhattaram P. Vertebrate skeletogenesis.. Curr Top Dev Biol 2010;90:291-317.
- Colnot C. Cellular and molecular interactions regulating skeletogenesis.. J Cell Biochem 2005 Jul 1;95(4):688-97.
- Kobayashi T, Lyons KM, McMahon AP, Kronenberg HM. BMP signaling stimulates cellular differentiation at multiple steps during cartilage development.. Proc Natl Acad Sci U S A 2005 Dec 13;102(50):18023-7.
- Mackie EJ, Ahmed YA, Tatarczuch L, Chen KS, Mirams M. Endochondral ossification: how cartilage is converted into bone in the developing skeleton.. Int J Biochem Cell Biol 2008;40(1):46-62.
- Corrigan L, Redhai S, Leiblich A, Fan SJ, Perera SM, Patel R, Gandy C, Wainwright SM, Morris JF, Hamdy F, Goberdhan DC, Wilson C. BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior.. J Cell Biol 2014 Sep 1;206(5):671-88.
- Wendler F, Bota-Rabassedas N, Franch-Marro X. Cancer becomes wasteful: emerging roles of exosomes(†) in cell-fate determination.. J Extracell Vesicles 2013 Sep 24;2.
- Gross JC, Chaudhary V, Bartscherer K, Boutros M. Active Wnt proteins are secreted on exosomes.. Nat Cell Biol 2012 Oct;14(10):1036-45.
- Hosaka Y, Saito T, Sugita S, Hikata T, Kobayashi H, Fukai A, Taniguchi Y, Hirata M, Akiyama H, Chung UI, Kawaguchi H. Notch signaling in chondrocytes modulates endochondral ossification and osteoarthritis development.. Proc Natl Acad Sci U S A 2013 Jan 29;110(5):1875-80.
- Mirando AJ, Liu Z, Moore T, Lang A, Kohn A, Osinski AM, O'Keefe RJ, Mooney RA, Zuscik MJ, Hilton MJ. RBP-Jκ-dependent Notch signaling is required for murine articular cartilage and joint maintenance.. Arthritis Rheum 2013 Oct;65(10):2623-33.
- Ristorcelli E, Beraud E, Mathieu S, Lombardo D, Verine A. Essential role of Notch signaling in apoptosis of human pancreatic tumoral cells mediated by exosomal nanoparticles.. Int J Cancer 2009 Sep 1;125(5):1016-26.
- Sheldon H, Heikamp E, Turley H, Dragovic R, Thomas P, Oon CE, Leek R, Edelmann M, Kessler B, Sainson RC, Sargent I, Li JL, Harris AL. New mechanism for Notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes.. Blood 2010 Sep 30;116(13):2385-94.
- Berckmans RJ, Nieuwland R, Tak PP, Böing AN, Romijn FP, Kraan MC, Breedveld FC, Hack CE, Sturk A. Cell-derived microparticles in synovial fluid from inflamed arthritic joints support coagulation exclusively via a factor VII-dependent mechanism.. Arthritis Rheum 2002 Nov;46(11):2857-66.
- Berckmans RJ, Nieuwland R, Kraan MC, Schaap MC, Pots D, Smeets TJ, Sturk A, Tak PP. Synovial microparticles from arthritic patients modulate chemokine and cytokine release by synoviocytes.. Arthritis Res Ther 2005;7(3):R536-44.
- Biró E, Nieuwland R, Tak PP, Pronk LM, Schaap MC, Sturk A, Hack CE. Activated complement components and complement activator molecules on the surface of cell-derived microparticles in patients with rheumatoid arthritis and healthy individuals.. Ann Rheum Dis 2007 Aug;66(8):1085-92.
- Boilard E, Nigrovic PA, Larabee K, Watts GF, Coblyn JS, Weinblatt ME, Massarotti EM, Remold-O'Donnell E, Farndale RW, Ware J, Lee DM. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production.. Science 2010 Jan 29;327(5965):580-3.
- Cloutier N, Tan S, Boudreau LH, Cramb C, Subbaiah R, Lahey L, Albert A, Shnayder R, Gobezie R, Nigrovic PA, Farndale RW, Robinson WH, Brisson A, Lee DM, Boilard E. The exposure of autoantigens by microparticles underlies the formation of potent inflammatory components: the microparticle-associated immune complexes.. EMBO Mol Med 2013 Feb;5(2):235-49.
- Duchez AC, Boudreau LH, Naika GS, Bollinger J, Belleannée C, Cloutier N, Laffont B, Mendoza-Villarroel RE, Lévesque T, Rollet-Labelle E, Rousseau M, Allaeys I, Tremblay JJ, Poubelle PE, Lambeau G, Pouliot M, Provost P, Soulet D, Gelb MH, Boilard E. Platelet microparticles are internalized in neutrophils via the concerted activity of 12-lipoxygenase and secreted phospholipase A2-IIA.. Proc Natl Acad Sci U S A 2015 Jul 7;112(27):E3564-73.
- Fourcade O, Simon MF, Viodé C, Rugani N, Leballe F, Ragab A, Fournié B, Sarda L, Chap H. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells.. Cell 1995 Mar 24;80(6):919-27.
- György B, Módos K, Pállinger E, Pálóczi K, Pásztói M, Misják P, Deli MA, Sipos A, Szalai A, Voszka I, Polgár A, Tóth K, Csete M, Nagy G, Gay S, Falus A, Kittel A, Buzás EI. Detection and isolation of cell-derived microparticles are compromised by protein complexes resulting from shared biophysical parameters.. Blood 2011 Jan 27;117(4):e39-48.
- György B, Szabó TG, Turiák L, Wright M, Herczeg P, Lédeczi Z, Kittel A, Polgár A, Tóth K, Dérfalvi B, Zelenák G, Böröcz I, Carr B, Nagy G, Vékey K, Gay S, Falus A, Buzás EI. Improved flow cytometric assessment reveals distinct microvesicle (cell-derived microparticle) signatures in joint diseases.. PLoS One 2012;7(11):e49726.
- Headland SE, Jones HR, Norling LV, Kim A, Souza PR, Corsiero E, Gil CD, Nerviani A, Dell'Accio F, Pitzalis C, Oliani SM, Jan LY, Perretti M. Neutrophil-derived microvesicles enter cartilage and protect the joint in inflammatory arthritis.. Sci Transl Med 2015 Nov 25;7(315):315ra190.
- Junkar I, Sustar V, Frank M, Jansa V, Zavec A, Rozman B. Blood and synovial microparticles as revealed by atomic force and scanning electron microscope. Open Autoimmun J (2009) 1:50–8.
- Martínez-Lorenzo MJ, Anel A, Saez-Gutierrez B, Royo-Cañas M, Bosque A, Alava MA, Piñeiro A, Lasierra P, Asín-Ungría J, Larrad L. Rheumatoid synovial fluid T cells are sensitive to APO2L/TRAIL.. Clin Immunol 2007 Jan;122(1):28-40.
- Matei CI, Boulocher C, Boulé C, Schramme M, Viguier E, Roger T, Berthier Y, Trunfio-Sfarghiu AM, Blanchin MG. Ultrastructural analysis of healthy synovial fluids in three mammalian species.. Microsc Microanal 2014 Jun;20(3):903-11.
- Messer L, Alsaleh G, Freyssinet JM, Zobairi F, Leray I, Gottenberg JE, Sibilia J, Toti-Orfanoudakis F, Wachsmann D. Microparticle-induced release of B-lymphocyte regulators by rheumatoid synoviocytes.. Arthritis Res Ther 2009;11(2):R40.
- Pásztói M, Sódar B, Misják P, Pálóczi K, Kittel Á, Tóth K, Wellinger K, Géher P, Nagy G, Lakatos T, Falus A, Buzás EI. The recently identified hexosaminidase D enzyme substantially contributes to the elevated hexosaminidase activity in rheumatoid arthritis.. Immunol Lett 2013 Jan;149(1-2):71-6.
- Skriner K, Adolph K, Jungblut PR, Burmester GR. Association of citrullinated proteins with synovial exosomes.. Arthritis Rheum 2006 Dec;54(12):3809-14.
- Mustonen AM, Nieminen P, Joukainen A, Jaroma A, Kääriäinen T, Kröger H, Lázaro-Ibáñez E, Siljander PR, Kärjä V, Härkönen K, Koistinen A, Rilla K. First in vivo detection and characterization of hyaluronan-coated extracellular vesicles in human synovial fluid.. J Orthop Res 2016 Nov;34(11):1960-1968.
- Reich N, Beyer C, Gelse K, Akhmetshina A, Dees C, Zwerina J, Schett G, Distler O, Distler JH. Microparticles stimulate angiogenesis by inducing ELR(+) CXC-chemokines in synovial fibroblasts.. J Cell Mol Med 2011 Apr;15(4):756-62.
- Attur MG, Dave M, Akamatsu M, Katoh M, Amin AR. Osteoarthritis or osteoarthrosis: the definition of inflammation becomes a semantic issue in the genomic era of molecular medicine.. Osteoarthritis Cartilage 2002 Jan;10(1):1-4.
- Rahmati M, Mobasheri A, Mozafari M. Inflammatory mediators in osteoarthritis: A critical review of the state-of-the-art, current prospects, and future challenges.. Bone 2016 Apr;85:81-90.
- Domenis R, Zanutel R, Caponnetto F, Toffoletto B, Cifù A, Pistis C, Di Benedetto P, Causero A, Pozzi M, Bassini F, Fabris M, Niazi KR, Soon-Shiong P, Curcio F. Characterization of the Proinflammatory Profile of Synovial Fluid-Derived Exosomes of Patients with Osteoarthritis.. Mediators Inflamm 2017;2017:4814987.
- Kolhe R, Hunter M, Liu S, Jadeja RN, Pundkar C, Mondal AK, Mendhe B, Drewry M, Rojiani MV, Liu Y, Isales CM, Guldberg RE, Hamrick MW, Fulzele S. Gender-specific differential expression of exosomal miRNA in synovial fluid of patients with osteoarthritis.. Sci Rep 2017 May 17;7(1):2029.
- Kato T, Miyaki S, Ishitobi H, Nakamura Y, Nakasa T, Lotz MK, Ochi M. Exosomes from IL-1β stimulated synovial fibroblasts induce osteoarthritic changes in articular chondrocytes.. Arthritis Res Ther 2014 Aug 4;16(4):R163.
- Jüngel A, Distler O, Schulze-Horsel U, Huber LC, Ha HR, Simmen B, Kalden JR, Pisetsky DS, Gay S, Distler JH. Microparticles stimulate the synthesis of prostaglandin E(2) via induction of cyclooxygenase 2 and microsomal prostaglandin E synthase 1.. Arthritis Rheum 2007 Nov;56(11):3564-74.
- Malda J, Boere J, van de Lest CH, van Weeren P, Wauben MH. Extracellular vesicles — new tool for joint repair and regeneration.. Nat Rev Rheumatol 2016 Apr;12(4):243-9.
- Buzas EI, György B, Nagy G, Falus A, Gay S. Emerging role of extracellular vesicles in inflammatory diseases.. Nat Rev Rheumatol 2014 Jun;10(6):356-64.
- Distler JH, Pisetsky DS, Huber LC, Kalden JR, Gay S, Distler O. Microparticles as regulators of inflammation: novel players of cellular crosstalk in the rheumatic diseases.. Arthritis Rheum 2005 Nov;52(11):3337-48.
- Greisen SR, Yan Y, Hansen AS, Venø MT, Nyengaard JR, Moestrup SK, Hvid M, Freeman GJ, Kjems J, Deleuran B. Extracellular Vesicles Transfer the Receptor Programmed Death-1 in Rheumatoid Arthritis.. Front Immunol 2017;8:851.
- Turpin D, Truchetet ME, Faustin B, Augusto JF, Contin-Bordes C, Brisson A, Blanco P, Duffau P. Role of extracellular vesicles in autoimmune diseases.. Autoimmun Rev 2016 Feb;15(2):174-83.
- Fu H, Hu D, Zhang L, Tang P. Role of extracellular vesicles in rheumatoid arthritis.. Mol Immunol 2018 Jan;93:125-132.
- Rhys HI, Dell'Accio F, Pitzalis C, Moore A, Norling LV, Perretti M. Neutrophil Microvesicles from Healthy Control and Rheumatoid Arthritis Patients Prevent the Inflammatory Activation of Macrophages.. EBioMedicine 2018 Mar;29:60-69.
- Hunter W. Of the structure and disease of articular cartilages. Philos Trans R Soc Lond (1742):514–21.
- Smith BD, Grande DA. The current state of scaffolds for musculoskeletal regenerative applications.. Nat Rev Rheumatol 2015 Apr;11(4):213-22.
- Malda J, Visser J, Melchels FP, Jüngst T, Hennink WE, Dhert WJ, Groll J, Hutmacher DW. 25th anniversary article: Engineering hydrogels for biofabrication.. Adv Mater 2013 Sep 25;25(36):5011-28.
- Visser J, Peters B, Burger TJ, Boomstra J, Dhert WJ, Melchels FP, Malda J. Biofabrication of multi-material anatomically shaped tissue constructs.. Biofabrication 2013 Sep;5(3):035007.
- Makris EA, Gomoll AH, Malizos KN, Hu JC, Athanasiou KA. Repair and tissue engineering techniques for articular cartilage.. Nat Rev Rheumatol 2015 Jan;11(1):21-34.
- de Windt TS, Vonk LA, Slaper-Cortenbach IC, van den Broek MP, Nizak R, van Rijen MH, de Weger RA, Dhert WJ, Saris DB. Allogeneic Mesenchymal Stem Cells Stimulate Cartilage Regeneration and Are Safe for Single-Stage Cartilage Repair in Humans upon Mixture with Recycled Autologous Chondrons.. Stem Cells 2017 Jan;35(1):256-264.
- Huleihel L, Hussey GS, Naranjo JD, Zhang L, Dziki JL, Turner NJ, Stolz DB, Badylak SF. Matrix-bound nanovesicles within ECM bioscaffolds.. Sci Adv 2016 Jun;2(6):e1600502.
- Lam J, Lu S, Kasper FK, Mikos AG. Strategies for controlled delivery of biologics for cartilage repair.. Adv Drug Deliv Rev 2015 Apr;84:123-34.
- Proia P, Schiera G, Mineo M, Ingrassia AM, Santoro G, Savettieri G, Di Liegro I. Astrocytes shed extracellular vesicles that contain fibroblast growth factor-2 and vascular endothelial growth factor.. Int J Mol Med 2008 Jan;21(1):63-7.
- Zhang J, Liu X, Li H, Chen C, Hu B, Niu X, Li Q, Zhao B, Xie Z, Wang Y. Exosomes/tricalcium phosphate combination scaffolds can enhance bone regeneration by activating the PI3K/Akt signaling pathway.. Stem Cell Res Ther 2016 Sep 20;7(1):136.
- Toh WS, Lai RC, Hui JHP, Lim SK. MSC exosome as a cell-free MSC therapy for cartilage regeneration: Implications for osteoarthritis treatment.. Semin Cell Dev Biol 2017 Jul;67:56-64.
- Zhang S, Chu WC, Lai RC, Lim SK, Hui JH, Toh WS. Exosomes derived from human embryonic mesenchymal stem cells promote osteochondral regeneration.. Osteoarthritis Cartilage 2016 Dec;24(12):2135-2140.
- Vonk LA, van Dooremalen SFJ, Liv N, Klumperman J, Coffer PJ, Saris DBF, Lorenowicz MJ. Mesenchymal Stromal/stem Cell-derived Extracellular Vesicles Promote Human Cartilage Regeneration In Vitro.. Theranostics 2018;8(4):906-920.
- Savkovic V, Li H, Seon JK, Hacker M, Franz S, Simon JC. Mesenchymal stem cells in cartilage regeneration.. Curr Stem Cell Res Ther 2014;9(6):469-88.
- Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H, Noiseux N, Zhang L, Pratt RE, Ingwall JS, Dzau VJ. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells.. Nat Med 2005 Apr;11(4):367-8.
- van Buul GM, Villafuertes E, Bos PK, Waarsing JH, Kops N, Narcisi R, Weinans H, Verhaar JA, Bernsen MR, van Osch GJ. Mesenchymal stem cells secrete factors that inhibit inflammatory processes in short-term osteoarthritic synovium and cartilage explant culture.. Osteoarthritis Cartilage 2012 Oct;20(10):1186-96.
- Lai RC, Arslan F, Lee MM, Sze NS, Choo A, Chen TS, Salto-Tellez M, Timmers L, Lee CN, El Oakley RM, Pasterkamp G, de Kleijn DP, Lim SK. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury.. Stem Cell Res 2010 May;4(3):214-22.
- Zhang S, Chuah SJ, Lai RC, Hui JHP, Lim SK, Toh WS. MSC exosomes mediate cartilage repair by enhancing proliferation, attenuating apoptosis and modulating immune reactivity.. Biomaterials 2018 Feb;156:16-27.
- Cosenza S, Ruiz M, Toupet K, Jorgensen C, Noël D. Mesenchymal stem cells derived exosomes and microparticles protect cartilage and bone from degradation in osteoarthritis.. Sci Rep 2017 Nov 24;7(1):16214.
- Gullo F, De Bari C. Prospective purification of a subpopulation of human synovial mesenchymal stem cells with enhanced chondro-osteogenic potency.. Rheumatology (Oxford) 2013 Oct;52(10):1758-68.
- Lee JC, Min HJ, Park HJ, Lee S, Seong SC, Lee MC. Synovial membrane-derived mesenchymal stem cells supported by platelet-rich plasma can repair osteochondral defects in a rabbit model.. Arthroscopy 2013 Jun;29(6):1034-46.
- Murata D, Miyakoshi D, Hatazoe T, Miura N, Tokunaga S, Fujiki M, Nakayama K, Misumi K. Multipotency of equine mesenchymal stem cells derived from synovial fluid.. Vet J 2014 Oct;202(1):53-61.
- Tao SC, Yuan T, Zhang YL, Yin WJ, Guo SC, Zhang CQ. Exosomes derived from miR-140-5p-overexpressing human synovial mesenchymal stem cells enhance cartilage tissue regeneration and prevent osteoarthritis of the knee in a rat model.. Theranostics 2017;7(1):180-195.
- Jiang Y, Tuan RS. Origin and function of cartilage stem/progenitor cells in osteoarthritis.. Nat Rev Rheumatol 2015 Apr;11(4):206-12.
- McCarthy HE, Bara JJ, Brakspear K, Singhrao SK, Archer CW. The comparison of equine articular cartilage progenitor cells and bone marrow-derived stromal cells as potential cell sources for cartilage repair in the horse.. Vet J 2012 Jun;192(3):345-51.
- Zhang B, Yin Y, Lai RC, Lim SK. Immunotherapeutic potential of extracellular vesicles.. Front Immunol 2014;5:518.
- Vyas N, Walvekar A, Tate D, Lakshmanan V, Bansal D, Lo Cicero A, Raposo G, Palakodeti D, Dhawan J. Vertebrate Hedgehog is secreted on two types of extracellular vesicles with different signaling properties.. Sci Rep 2014 Dec 8;4:7357.
- Neven KY, Nawrot TS, Bollati V. Extracellular Vesicles: How the External and Internal Environment Can Shape Cell-To-Cell Communication.. Curr Environ Health Rep 2017 Mar;4(1):30-37.
- Malda J, Benders KE, Klein TJ, de Grauw JC, Kik MJ, Hutmacher DW, Saris DB, van Weeren PR, Dhert WJ. Comparative study of depth-dependent characteristics of equine and human osteochondral tissue from the medial and lateral femoral condyles.. Osteoarthritis Cartilage 2012 Oct;20(10):1147-51.
- Boere J, van de Lest CH, Libregts SF, Arkesteijn GJ, Geerts WJ, Nolte-'t Hoen EN, Malda J, van Weeren PR, Wauben MH. Synovial fluid pretreatment with hyaluronidase facilitates isolation of CD44+ extracellular vesicles.. J Extracell Vesicles 2016;5:31751.
- de Grauw JC, van de Lest CH, Brama PA, Rambags BP, van Weeren PR. In vivo effects of meloxicam on inflammatory mediators, MMP activity and cartilage biomarkers in equine joints with acute synovitis.. Equine Vet J 2009 Sep;41(7):693-9.
- Ross TN, Kisiday JD, Hess T, McIlwraith CW. Evaluation of the inflammatory response in experimentally induced synovitis in the horse: a comparison of recombinant equine interleukin 1 beta and lipopolysaccharide.. Osteoarthritis Cartilage 2012 Dec;20(12):1583-90.
- Palmer JL, Bertone AL. Experimentally-induced synovitis as a model for acute synovitis in the horse.. Equine Vet J 1994 Nov;26(6):492-5.
- de Grauw JC, van de Lest CH, van Weeren PR. Inflammatory mediators and cartilage biomarkers in synovial fluid after a single inflammatory insult: a longitudinal experimental study.. Arthritis Res Ther 2009;11(2):R35.
- Cokelaere SM, Plomp SGM, de Boef E, de Leeuw M, Bool S, van de Lest CHA, van Weeren PR, Korthagen NM. Sustained intra-articular release of celecoxib in an equine repeated LPS synovitis model.. Eur J Pharm Biopharm 2018 Jul;128:327-336.
Citations
This article has been cited 22 times.- Li S, Zhang S, Chen Z, Zhang X, Ou R, Wei S, Liu Y, Xu Y, Chen K, Chen Z, Shu X. How to process synovial fluid samples of gouty arthritis and extract its exosomes for subsequent cytokine analysis.. Medicine (Baltimore) 2023 Aug 4;102(31):e34552.
- Yang B, Li X, Fu C, Cai W, Meng B, Qu Y, Kou X, Zhang Q. Extracellular vesicles in osteoarthritis of peripheral joint and temporomandibular joint.. Front Endocrinol (Lausanne) 2023;14:1158744.
- Wang S, Liu Z, Yang S, Huo N, Qiao B, Zhang T, Xu J, Shi Q. Extracellular vesicles secreted by human gingival mesenchymal stem cells promote bone regeneration in rat femoral bone defects.. Front Bioeng Biotechnol 2023;11:1098172.
- Moccia V, Sammarco A, Cavicchioli L, Castagnaro M, Bongiovanni L, Zappulli V. Extracellular Vesicles in Veterinary Medicine.. Animals (Basel) 2022 Oct 10;12(19).
- Wang H, Shu J, Zhang C, Wang Y, Shi R, Yang F, Tang X. Extracellular Vesicle-Mediated miR-150-3p Delivery in Joint Homeostasis: A Potential Treatment for Osteoarthritis?. Cells 2022 Sep 5;11(17).
- Clarke EJ, Lima C, Anderson JR, Castanheira C, Beckett A, James V, Hyett J, Goodacre R, Peffers MJ. Optical photothermal infrared spectroscopy can differentiate equine osteoarthritic plasma extracellular vesicles from healthy controls.. Anal Methods 2022 Sep 29;14(37):3661-3670.
- DiStefano TJ, Vaso K, Panebianco CJ, Danias G, Chionuma HN, Kunnath K, Karoulias SZ, Wang M, Xu P, Davé RN, Sahoo S, Weiser JR, Iatridis JC. Hydrogel-Embedded Poly(Lactic-co-Glycolic Acid) Microspheres for the Delivery of hMSC-Derived Exosomes to Promote Bioactive Annulus Fibrosus Repair.. Cartilage 2022 Jul-Sep;13(3):19476035221113959.
- Lai C, Liao B, Peng S, Fang P, Bao N, Zhang L. Synovial fibroblast-miR-214-3p-derived exosomes inhibit inflammation and degeneration of cartilage tissues of osteoarthritis rats.. Mol Cell Biochem 2023 Mar;478(3):637-649.
- Yin B, Ni J, Witherel CE, Yang M, Burdick JA, Wen C, Wong SHD. Harnessing Tissue-derived Extracellular Vesicles for Osteoarthritis Theranostics.. Theranostics 2022;12(1):207-231.
- Hotham WE, Thompson C, Szu-Ting L, Henson FMD. The anti-inflammatory effects of equine bone marrow stem cell-derived extracellular vesicles on autologous chondrocytes.. Vet Rec Open 2021 Dec;8(1):e22.
- DiStefano TJ, Vaso K, Danias G, Chionuma HN, Weiser JR, Iatridis JC. Extracellular Vesicles as an Emerging Treatment Option for Intervertebral Disc Degeneration: Therapeutic Potential, Translational Pathways, and Regulatory Considerations.. Adv Healthc Mater 2022 Mar;11(5):e2100596.
- Song H, Zhao J, Cheng J, Feng Z, Wang J, Momtazi-Borojeni AA, Liang Y. Extracellular Vesicles in chondrogenesis and Cartilage regeneration.. J Cell Mol Med 2021 Jun;25(11):4883-4892.
- Zhao P, Cao L, Wang X, Dong J, Zhang N, Li X, Li J, Zhang X, Gong P. Extracellular vesicles secreted by Giardia duodenalis regulate host cell innate immunity via TLR2 and NLRP3 inflammasome signaling pathways.. PLoS Negl Trop Dis 2021 Apr;15(4):e0009304.
- Kang T, Atukorala I, Mathivanan S. Biogenesis of Extracellular Vesicles.. Subcell Biochem 2021;97:19-43.
- She Z, Xie M, Hun M, Abdirahman AS, Li C, Wu F, Luo S, Wan W, Wen C, Tian J. Immunoregulatory Effects of Mitochondria Transferred by Extracellular Vesicles.. Front Immunol 2020;11:628576.
- Zhou Y, Ming J, Li Y, Li B, Deng M, Ma Y, Chen Z, Zhang Y, Li J, Liu S. Exosomes derived from miR-126-3p-overexpressing synovial fibroblasts suppress chondrocyte inflammation and cartilage degradation in a rat model of osteoarthritis.. Cell Death Discov 2021 Feb 24;7(1):37.
- Gantenbein B, Tang S, Guerrero J, Higuita-Castro N, Salazar-Puerta AI, Croft AS, Gazdhar A, Purmessur D. Non-viral Gene Delivery Methods for Bone and Joints.. Front Bioeng Biotechnol 2020;8:598466.
- Reinhold S, Blankesteijn WM, Foulquier S. The Interplay of WNT and PPARγ Signaling in Vascular Calcification.. Cells 2020 Dec 10;9(12).
- Mobasheri A, Choi H, Martín-Vasallo P. Over-Production of Therapeutic Growth Factors for Articular Cartilage Regeneration by Protein Production Platforms and Protein Packaging Cell Lines.. Biology (Basel) 2020 Oct 9;9(10).
- Mecocci S, Gevi F, Pietrucci D, Cavinato L, Luly FR, Pascucci L, Petrini S, Ascenzioni F, Zolla L, Chillemi G, Cappelli K. Anti-Inflammatory Potential of Cow, Donkey and Goat Milk Extracellular Vesicles as Revealed by Metabolomic Profile.. Nutrients 2020 Sep 23;12(10).
- Piazza N, Dehghani M, Gaborski TR, Wuertz-Kozak K. Therapeutic Potential of Extracellular Vesicles in Degenerative Diseases of the Intervertebral Disc.. Front Bioeng Biotechnol 2020;8:311.
- Ragni E, Perucca Orfei C, De Luca P, Lugano G, Viganò M, Colombini A, Valli F, Zacchetti D, Bollati V, de Girolamo L. Interaction with hyaluronan matrix and miRNA cargo as contributors for in vitro potential of mesenchymal stem cell-derived extracellular vesicles in a model of human osteoarthritic synoviocytes.. Stem Cell Res Ther 2019 Mar 29;10(1):109.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists