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Ultrastructural Analysis of Healthy Synovial Fluids in Three Mammalian Species

Published online by Cambridge University Press:  18 March 2014

Constantin I. Matei ,
Caroline Boulocher ,
Christelle Boulé ,
Michael Schramme ,
Eric Viguier ,
Thierry Roger ,
Yves Berthier ,
Ana-Maria Trunfio-Sfarghiu  and
Marie-Geneviève Blanchin
Constantin I. Matei
Affiliation:
LaMCoS UMR5259, INSA-Lyon, CNRS, University of Lyon, 69621 Villeurbanne, France ILM, UMR5306-CNRS, University Claude Bernard Lyon 1,University of Lyon, 69622 Villeurbanne, France CTmu, University Claude Bernard Lyon 1, University of Lyon, 69622 Villeurbanne, France
Caroline Boulocher*
Affiliation:
UPSP ICE 2011-03-101, VetAgro Sup, Veterinary Campus, University Claude Bernard Lyon 1, University of Lyon, 69280 Marcy lʼEtoile, France
Christelle Boulé
Affiliation:
CTmu, University Claude Bernard Lyon 1, University of Lyon, 69622 Villeurbanne, France
Michael Schramme
Affiliation:
UPSP ICE 2011-03-101, VetAgro Sup, Veterinary Campus, University Claude Bernard Lyon 1, University of Lyon, 69280 Marcy lʼEtoile, France
Eric Viguier
Affiliation:
UPSP ICE 2011-03-101, VetAgro Sup, Veterinary Campus, University Claude Bernard Lyon 1, University of Lyon, 69280 Marcy lʼEtoile, France
Thierry Roger
Affiliation:
UPSP ICE 2011-03-101, VetAgro Sup, Veterinary Campus, University Claude Bernard Lyon 1, University of Lyon, 69280 Marcy lʼEtoile, France
Yves Berthier
Affiliation:
LaMCoS UMR5259, INSA-Lyon, CNRS, University of Lyon, 69621 Villeurbanne, France
Ana-Maria Trunfio-Sfarghiu
Affiliation:
LaMCoS UMR5259, INSA-Lyon, CNRS, University of Lyon, 69621 Villeurbanne, France
Marie-Geneviève Blanchin
Affiliation:
ILM, UMR5306-CNRS, University Claude Bernard Lyon 1,University of Lyon, 69622 Villeurbanne, France
*
*Corresponding author. [email protected]
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Abstract

A better knowledge of synovial fluid (SF) ultrastructure is required to further understand normal joint lubrication and metabolism. The aim of the present study was to elucidate SF structural features in healthy joints from three mammalian species of different size compared with features in biomimetic SF. High-resolution structural analysis was performed using transmission electron microscopy (TEM) and scanning electron microscopy (SEM) and environmental SEM/wet scanning transmission electron microscopy mode complemented by TEM and SEM cryogenic methods. Laser-scanning confocal microscopy (LCM) was used to locate the main components of SF with respect to its ultrastructural organization. The present study showed that the ultrastructure of healthy SF is built from a network of vesicles with a size range from 100 to a few hundred nanometers. A multilayered organization of the vesicle membranes was observed with a thickness of about 5 nm. LCM study of biological SF compared with synthetic SF showed that the microvesicles consist of a lipid-based membrane enveloping a glycoprotein gel. Thus, healthy SF has a discontinuous ultrastructure based on a complex network of microvesicles. This finding offers novel perspectives for the diagnosis and treatment of synovial joint diseases.

Keywords

synovial fluidultrastructuremicrovesicleslipid membraneslubrication
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 20 , Issue 3 , June 2014 , pp. 903 - 911
Copyright
© Microscopy Society of America 2014 

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References

Al-Nedaw, K., Meehan, B. & Rak, J. (2009). Microvesicles messengers and mediators of tumor progression. Cell Cycle 8, 2014–2018.Google Scholar
Bali, R. & Shukla, A.K. (2001). Rheological effects of synovial fluid on nutritional transport. Tribol Lett 9, 233–239.CrossRefGoogle Scholar
Barton, N.J., Stevens, D.A., Hughes, J.P., Rossi, A.G., Chessell, I.P., Reeve, A.J. & Mcqueen, D.S. (2007). Demonstration of a novel technique to quantitatively assess inflammatory mediators and cells in rat knee joints. J Inflamm (Lond) 4, 13. doi:10.1186/1476-9255-4-13.CrossRefGoogle ScholarPubMed
Blewis, M.E., Nugent-Derfus, G.E., Schmidt, T.A., Schumacher, B.L. & Sah, R.L. (2007). A model of synovial fluid lubricant composition in normal and injured joints. Eur Cell Mater 13, 26–39.Google Scholar
Bogner, A., Jouneau, P.H., Thollet, G., Basset, D. & Gauthier, C. (2007). A history of scanning electron microscopy developments: Towards ‘Wet-STEM’ imaging. Micron 38, 390–401.Google Scholar
Bogner, A., Thollet, G., Basset, D., Jouneau, P.H. & Gauthier, C. (2005). Wet STEM: A new development in environmental SEM for imaging nano-objects included in a liquid phase. Ultramicroscopy 104, 290–301.Google Scholar
Burger, C., Hao, J., Ying, Q., Isobe, H., Sawamura, M., Nakamura, E. & Chu, B. (2004). Multilayer vesicles and vesicle clusters formed by the fullerene-based surfactant C60(CH3)5K. J Colloid Interface Sci 275, 632–641.Google Scholar
Conde-Vancells, J., Rodriguez-Suarez, E., Embade, N., Gil, D., Matthiesen, R., Valle, M., Elortza, F., Lu, S.C., Mato, J.M. & Falcon-Perez, J.M. (2008). Characterization and comprehensive proteome profiling of exosomes secreted by hepatocytes. J Proteome Res 7, 5157–5166.CrossRefGoogle ScholarPubMed
Crescenzi, V., Taglienti, A. & Pasquali-Ronchetti, I. (2004). Supramolecular structures in aqueous hyaluronic acid and phospholipid vesicles mixtures: An electron microscopy and rheometric study. Colloids Surf 245, 133–135.Google Scholar
Dobbie, J.W. (1996). Surfactant protein A and lamellar bodies: A homologous secretory function of peritoneum, synovium, and lung. Perit Dial Int 16, 574–581.Google Scholar
Dowson, D. & Jin, Z.M. (1986). Micro-elastohydrodynamic lubrication of synovial joints. Eng Med 15, 63–65.Google Scholar
Goldberg, R. & Klein, J. (2012). Liposomes as lubricants: Beyond drug delivery. Chem Phys Lipids 165, 374–381.Google Scholar
Goldberg, R., Schroeder, A., Barenholz, Y. & Klein, J. (2011). Interactions between adsorbed hydrogenated soy phosphatidylcholine (hspc) vesicles at physiologically high pressures and salt concentrations. Biophys J 100, 2403–2411.Google Scholar
Gonzalez, G., Vituret, C., Di Pietro, A., Chanson, M., Boulanger, P. & Hong, S.S. (2012). Microparticle-mediated transfer of the viral receptors CAR and CD46, and the CFTR channel in a CHO cell model confers new functions to target cells. PLoS One 7(12), e52326.Google Scholar
György, B., Szabó, T.G., Pásztói, M., Pál, Z., Misják, P., Aradi, B., László, V., Pállinger, E., Pap, E., Kittel, A., Nagy, G., Falus, A. & Buzás, E.I. (2011). Membrane vesicles, current state-of-the-art: Emerging role of extracellular vesicles. Cell Mol Life Sci 68, 2667–2688.Google Scholar
György, B., Szabó, T.G., 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, E.I. (2012). Improved flow cytometric assessment reveals distinct microvesicle (cell-derived microparticle) signatures in joint diseases. PLoS One 7(11), e49726.Google Scholar
Hills, B.A. (1989). Oligolamellar lubrication of joints by surface active phospholipids. J Rheumatol 16, 82–91.Google Scholar
Mause, F. & Weber, C. (2010). Microparticles: Protagonists of a novel communication network for intercellular information exchange. Circ Res 107, 1047–1057.CrossRefGoogle Scholar
Mavraki, A., Cann, P.M., Mischler, S., Boedo, S., Booker, J.F., Bayada, G., van Leeuwen, H., van Ostayen, R.A.J., Bayada, G., Meurisse, M.H., Renondeau, H., Papke, B.L., Pozebanchuk, M., Parthasarathy, P.P., Davies, L., Nilsson, D., Isaksson, P., Prakash, B. & Bansal, D. (2009). Friction and lubricant film thickness measurements on simulated synovial fluid. P I Mech Ing J-J Eng 223, 606–607.Google Scholar
Medley, J.B., Dowson, D. & Wright, V. (1984). Transient elastohydrodynamic lubrication models for the human ankle joint. Eng Med 13, 137–151.Google Scholar
Meziani, F., Tesse, A. & Andriantsitohaina, R. (2008). Microparticles are vectors of paradoxical information in vascular cells including the endothelium: Role in health and diseases. Pharmacol Rep 60, 75–84.Google Scholar
Mirea, D., Trunfio-Sfarghiu, A.M., Matei, C.I., Munteanu, B., Piednoir, A., Rieu, J.P., Blanchin, M.G. & Berthier, Y. (2013). Role of the biomolecular interactions in the structure and tribological properties of synovial fluid. Tribol Int 59, 302–311.Google Scholar
Pasquali-Ronchetti, I., Quaglino, D., Mori, G., Bacchelli, B. & Ghosh, P. (1997). Hyaluronan-phospholipid interactions. J Struct Biol 120, 1–10.Google Scholar
Pawlak, Z. & Oloyede, A. (2008). Conceptualisation of articular cartilage as a giant reverse micelle: A hypothetical mechanism for joint biocushioning and lubrication. Biosystems 94, 193–201.Google Scholar
Pozo-Navas, B., Raghunathan, V.A., Katsaras, J., Rappolt, M., Lohner, K. & Pabst, G. (2003). Discontinuous unbinding of lipid multibilayers. Phys Rev Lett 91(2), 028101.Google Scholar
Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A. & Ratajczak, M.Z. (2006). Membrane-derived microvesicles: Important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487–1495.Google Scholar
Sawyer, D.C. (1963). Synovial fluid analysis of canine joints. J Am Vet Med Assoc 43, 609–612.Google Scholar
Schmitz, G. & Muller, G. (1991). Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids. J Lip Res 32, 1539–1570.Google Scholar
Schwarz, I.M. & Hills, B.A. (1996). Synovial surfactant: Lamellar bodies in type B synoviocytes and proteolipid in synovials fluid and the articular lining. J Rheumatol 35, 821–827.Google Scholar
Trunfio-Sfarghiu, A.M., Berthier, Y., Meurisse, M.H. & Rieu, J.P. (2007). Multiscale analysis of the tribological role of the molecular assembly of synovial fluid. Case of a healthy joint and implants. Tribol Int 40, 1500–1515.Google Scholar
Trunfio-Sfarghiu, A.M., Berthier, Y., Meurisse, M.H. & Rieu, J.P. (2008). Role of nanomechanical properties in the tribological performance of phospholipid biomimetic surfaces. Langmuir 24, 8765–8771.Google Scholar
Unsworth, A., Dowson, D. & Wright, V. (1975). The frictional behavior of human synovial joints—Part I: Natural joints. J Lubrication Tech 97(3), 369–376.Google Scholar
van Der Pol, E., Böing, A.N., Harrison, P., Sturk, A. & Nieuwland, R. (2012). Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev 64, 676–705.Google Scholar
van Pelt, R.W. (1967). Characteristics of normal equine tarsal synovial fluid. Can J Comp Med Vet Sci 31, 342–347.Google Scholar
Walker, P.S., Dowson, D., Longfield, M.D. & Wright, V. (1968). Boosted lubrication of human joints by fluid enrichement and entrapment. Ann Rheum Dis 27, 512–520.Google Scholar
Watanabe, M., Leng, C., Toriumi, H., Hamada, Y., Akamatsu, N. & Ohno, S. (2003). Ultrastructural study of upper surface layer in rat articular cartilage by ‘‘in vivo cryotechnique’’ combined with various treatments. Med Electron Microsc 33, 16–24.Google Scholar