horse; synoviocytes; joint; osteoarthritis; free oxygen radicals; equine; articulation; osteoarthrite; formes activées de l’oxygène
Abstract :
[fr] L’ostéo-arthropathie dégénérative est une cause importante de morbidité chez le cheval. Elle provoque de la douleur et mène à la destruction du cartilage des articulations diarthrodiales. Dans cette pathologie, la membrane synoviale est un élément articulaire constitutif dont il n’est pas toujours tenu compte parce que ses modifications sont peu visibles ; pourtant son rôle dans l’articulation est crucial. Cette synthèse de la littérature reprend l’embryogenèse et l’aspect histologique des synoviocytes in vivo et in vitro, les données existantes sur leur production de médiateurs inflammatoires, d’enzymes protéolytiques, et de formes activées de l’oxygène, sur les composants du liquide synovial et sur leurs interactions avec les chondrocytes. Le nombre des études ne traitant que de l’espèce équine et de l’ostéo-arthropathie étant très limité, nous avons tenu compte des travaux faits sur d’autres espèces et d’autres formes d’atteinte articulaire pour donner une vue aussi complète que possible des mécanismes complexes, interdépendants et réciproques. [en] The degenerative osteoarthritis is a common source of disease in the horse, causing pain and leading finally to the destruction of the cartilage in the diarthrodial joints. The synovial membrane is a constitutive element of the joint, but often neglected due to its less obvious alterations, despite its crucial role. This review of literature considers the embryology, the histology of synoviocytes in vivo and in vitro, gives information about the production of inflammatory mediators, degrading enzymes, free oxygen radicals, about the composition of the synovial fluid and the interaction with chondrocytes. The number of studies on equine synoviocytes in osteoarthritis is very restricted, therefore we included studies in other species and other types of joint diseases to achieve a more complete image of the complex, interdependent and mutual acting mechanisms.
Research center :
CORD - Centre de l'Oxygène, Recherche et Développement - ULiège Centre européen du Cheval de Mont-le-Soie
Disciplines :
Veterinary medicine & animal health Human health sciences: Multidisciplinary, general & others
Author, co-author :
Schneider, Nicole ; Université de Liège - ULiège > CARE "Le Réseau des bibliothèques" > Bibliothèque des Sciences de la vie
Lejeune, Jean-Philippe ; Université de Liège - ULiège > Département clinique des animaux de compagnie et des équidés > Anesthésiologie gén. et pathologie chirurg. des grds animaux
Deby-Dupont, Ginette
Serteyn, Didier ; Université de Liège - ULiège > Département clinique des animaux de compagnie et des équidés > Anesthésiologie gén. et pathologie chirurg. des grds animaux
Language :
French
Title :
Le rôle des synoviocytes dans l’articulation diarthrodiale enflammée
Alternative titles :
[en] The role of synoviocytes in the inflamed diarthrodial joint.
AHLQVIST J. A hypothesis on the pathogenesis of rheumatoid and other non-specific synovitides: IV A. the possible intermediate role of local hypoxia and metabolic alterations. Med. Hypotheses, 1984, 13, 257-302.
ALLEN R.E., BLAKE D.R., NAZHAT N.B., JONEX P. Superoxide radical generation by inflamed human synovium after hypoxia. Lancet, 1989, 29, 282-283.
ALWAN W.H., CARTER S.D., DIXON J.B., BENNETT D., MAY S.A., EDWARDS G.B. Interleukin-1-like activity in synovial fluids and sera of horses with arthritis. Res. Vet. Sci., 1991, 51, 72-77.
ARMSTRONG S., LEES P. Effects of carprofen (R and S enantiomers and racemate) on the production of IL-1, IL-6 and TNF-alpha by equine chondrocytes and synoviocytes. J. Vet. Pharmacol. Ther., 2002, 25, 145-153.
AUER D.E. An hypothesis on the etio-pathogenesis of equine inflammatory joint disease. Vet. Clin. Pathol., 1989,18, 21-26.
AUER D.E., NG J.C., SEAWRIGHT A.A. Effect of palosein (superoxide dismutase) and catalase upon oxygen derived free radical induced degradation of equine synovial fluid. Equine Vet. J., 1990, 22, 13-17.
AUER D.E., NG J.C., REILLY J.S., SEAWRIGHT A.A. Anti-inflammatory drugs inhibit degradation of equine synovial fluid induced by free radicals. Aust. Vet. J., 1991, 68, 403-405.
AUER D.E., NG J.C., SEAWRIGHT A.A. Free radical oxidation products in plasma and synovial fluid of horses with synovial inflammation. Aust. Vet. J., 1993, 70, 49-52.
BAKER M.S., FEIGAN J., LOWTHER D.A. Chondrocytes antioxidant defences: the roles of catalase and glutathione peroxidase in protection against H 2O2 dependent inhibition of proteoglycan biosynthesis. J. Rheumatol., 1988, 15, 670-677.
BARRATT M.E., FELL H.B., COOMBS R.R., GLAUERT A.M. The pig synovium, II. some properties of isolated intimal cells. J. Anat., 1977, 123, 47-66.
BASSLEER A., LHOEST-GAUTHIER M.P., RENARD A.M., HEINEN E., GOESSENS G. Histological structure and function of synovium. Department of histology, notes de cours. University of Liège: Liège, 1981, 15-22.
BERNARDI P., PETRONELLI V., DI LISA F., FORTE M. Mitochondrial perspective on cell death. Trends Biochem. Sci., 2001, 26, 112-117.
BERTONE A.L., PALMER J.L., JONES J. Synovial fluid cytokines and eicosanoids as markers of joint disease in horses. Vet. Surg., 2001, 30, 528-538.
BONNET C., BERTIN P., COOK-MOREAU J., CHABLE-RABINOVITCH H., TREVES R., RIGAUD M. Lipoxygenase products and expression of 5-lipoxygenase and 5-lipoxygenase-activating protein in human cultured synovial cells. Prostaglandins, 1995, 50,127-135.
BORDERIE D., HILLIQUIN P., HERNVANN A., LEMARECHAL H., MENKES C.J., EKINDJIAN O.G. Apoptosis induced by nitric oxide is associated with nuclear p53 protein expression in cultured osteoarthritic synoviocytes. Osteoarthr. Cartil., 1999, 7, 203-213.
BORDERIE D., LEMARECHAL H., EKINDJIAN O.G., HERNVANN A. Nitric oxide modifies glycolytic pathways in cultured human synoviocytes. Cell. Biol. Int., 2000, 24, 285-289.
BOWKER R.M., ABHOLD H.A., CARON J.P., SONEA I.M., VEX B, KOTYK R. Neuropeptidergic innervation of equine synovial joints. Am. J. Vet. Res., 1993, 54, 1831-1839.
BREIT S., KÖNIG H.E. Rasterelektronenmikroskopische Untersuchungenzur Synovialmembran an Hufgelenk und Bursa podotrochlearis beim Pferde. Tierärztl. Prax., 1995, 23, 273-279.
BROWN M.P., WEST L.A., MERRITT K.A., PLAAS A.H.K. Changes in sulfation patterns of chondroitin sulfate in equine articular cartilage and synovial fluid in response to aging and osteoarthritis. Am. J. Vet. Res., 1998, 59, 786-790.
CADORE J.L., DONABEDIAN M. Implications des cytokines dans la pathogénie des phénomènes articulaires chez le cheval. Prat. Vet. Equine, 1997, 29, 31-39.
CHOCKALINGAM P.S., ZENG W., MORRIS E.A., FLANNERY C.R. Release of hyaluronan and hyaladherins (aggrecan G1 domain and link proteins) from articular cartilage exposed to ADAMTS-4 (aggrecanase 1) or ADAMTS-5 (aggrecanase 2). Arthritis Rheum., 2004, 50, 2839-2848.
CHU S.C., YANG S.F., LUE K.H., HSIEH Y.S., WU C.L., LU K.H. Regulation of gelatinases expression by cytokines, endotoxin, and pharmacological agents in the human osteoarthritic knee. Connect. Tissue Res., 2004, 45, 142-150.
CLEGG P.D., CARTER S.D. Matrix metalloproteinase-2 and-9 are activated in joint diseases. Equine Vet. J., 1999, 31, 324-330.
DE BARI C., DELL'ACCIO F., TYLZANOWSKI P., LUYTEN F.P. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum., 2001, 44, 1928-1942.
DEMASI M., CLELAND L.G., COOK-JOHNSON R.J., JAMES M.J. Effects of hypoxia on the expression and activity of cyclooxygenase 2 in fibroblast-like synoviocytes: interactions with monocyte-derived soluble mediators. Arthritis Rheum., 2004, 50, 2441-2449.
DIMOCK A.N., SICILIANO P.D., MCILWRAITH C.W. Evidence supporting an increased presence of reactive oxygen species in the diseased equine joint. Equine Vet. J., 2000, 32, 439-443.
DOBBIE J.W., HIND C., MEIJERS P., BODART C., TASIAUX N., PERRET J., ANDERSON J.D. Lamellar body secretion: ultrastructural analysis of an unexplored function of synoviocytes. Br. J. Rheumatol., 1995, 34, 13-23.
EDWARDS J.C.W. The nature and origins of synovium: exper imental approaches to the study of synoviocyte differentiation. J. Anat., 1994, 184 (Pt 3), 493-501.
EDWARDS J.C.W. Fibroblast biology. Development and differentiation of synovial fibroblasts in arthritis. Arthritis Res., 2000, 2, 344-347.
FABRY G. Ultrastructural changes in synovium and cartilage in experimental hemarthrosis in dogs. Arch. Orthop. Trauma Surg., 1990, 109, 21-29.
FELL H.B., GLAUERT A.M., BARRATT M.E., GREEN R. The pig synovium. I. The intact synovium in vivo and in organ culture. J. Anat., 1976, 122, 663-680.
FERNANDES J.C., MARTEL-PELLETIER J., PELLETIER J.P. The role of cytokines in osteoarthritis pathophysiology. Biorheology, 2002, 39, 237-246.
FREAN S.P., BRYANT C.E., FRÖLING I.L., ELLIOTT J., LEES P. Nitric oxide production by equine articular cells in vitro. Equine Vet. J., 1997, 29, 98-102.
FREAN S.P., LEES P. Effects of polysulfated glycosaminoglycan and hyaluronan on prostaglandin E2 production by cultured equine synoviocytes. Am. J. Vet. Res., 2000, 61, 499-505.
FULLER C.J., BARR A.R., SHARIF M., DIEPPE P.A. Cross-sectional comparison of synovial fluid biochemical markers in equine osteoarthritis and the correlation of these markers with articular cartilage damage. Osteoarthr. Cartil., 2001, 1, 49-55.
GALLERON S., BORDERIE D., PONTEZIERE C., LEMARECHAL H., JAMBOU M., ROCH-ARVEILLER M., EKINDJIAN O.G., CALS M.J. Reactive oxygen species induce apoptosis of synoviocytes in vitro. alpha-tocopherol provides no protection. Cell Biol. Int., 1999, 23, 637-642.
GÄNGEL H., RAHN A. Zur Frage der diagnostischen Verwertbarkeit der Enzymaktivitäten in der Synovia bei Gelenkerkrankungen des Pferdes. Mh. Vet.-Med., 1992, 47, 17-24.
GEORGESCU H.I., MENDELOW D., EVANS C.H. HIG-82: an established cell line from rabbit periarticular soft tissue, which retains the « activatable» phenotype. In Vitro Cell. Dev. Biol., 1988, 24, 1015-1022.
GIATROMANOLAKI A., SIVRIDIS E., ATHANASSOU N., ZOIS E., THORPE P.E., BREKKEN R.A., GATTER K.C., HARRIS A.L., KOUKOURAKIS I.M., KOUKOURAKIS M.I. The angiogenic pathway "vascular endothelial growth factor/flk-1(KDR)- receptor" in rheumatoid arthritis and osteoarthritis. J. Pathol., 2001, 194, 101-108.
GRIGOLO B., ROSETI L., FIORINI M., FACCHINI A. Enhanced lipid peroxidation in synoviocytes from patients with osteoarthritis. J. Rheumatol., 2003, 30, 345-347.
GROOTVELD M., HENDERSON E.B., FARRELL A., BLAKE D.R., PARKES H.G., HAYCOCK P. Oxidative damage to hyaluronate and glucose in synovial fluid during exercise of the inflamed rheumatoid joint. Detection of abnormal low-molecular-mass metabolites by proton-n.m.r. spectroscopy. Biochem. J., 1991, 273 (Pt 2), 459-467.
GUICHEUX J., PALMER G., RELIC B., MEZIN F., CAVERZASIO J., APOSTOLIDES P., GAUCHAT J.F., GABAY C., GUERNE P.A. Primary human articular chondrocytes, dedifferentiated chondrocytes, and synoviocytes exhibit differential responsiveness to interleukin-4: correlation with the expression pattern of the common receptor gamma chain. J. Cell Physiol., 2002, 192, 93-101.
HENROTIN Y.E. Les enzymes et leur inhibiteurs : pathogénie de l'arthrose. In: Henrotin Y.E., Approche expérimentale de la pathogénie et du traitement de l'arthrose. Mémoire présenté en vue de l'obtention du grade d'Agrégé de l'Enseignement Supérieur. Faculté de Médecine : Université de Liège, 2003, 13-14.
HERNVANN A., AUSSEL C., CYNOBER L., MOATTI N., EKINDJIAN O.G. IL-1 beta, a strong mediator for glucose uptake by rheumatoid and non-rheumatoid cultured human synoviocytes. FEBS Lett., 1992, 303, 77-80.
HILLS B.A., CRAWFORD R.W. Normal and prosthetic synovial joints are lubricated by surface-active phospholipid: a hypothesis. J. Arthroplasty, 2003, 18, 499-505.
INOUE K., MASUKO-HONGO K., OKAMOTO M., NISHIOKA K. Induction of vascular endothelial growth factor and matrix metalloproteinase-3 (stromelysin) by interleukin-1 in human articular chondrocytes and synoviocytes. Rheumatol. Int., 2005, 26, 93-98.
ISHIGURO N., ITO T., ITO H., IWATA H., JUGESSUR H., IONESCU M., POOLE A.R. Relationship of matrix metalloproteinases and their inhibitors to cartilage proteoglycan and collagen turnover: analyses of synovial fluid from patients with osteoarthritis. Arthritis Rheum., 1999, 42, 129-136.
IWANAGA T., SHIKICHI M., KITAMURA H., YANASE H., NOZAWA-INOUE K. Morphology and functional roles of synoviocytes in the joint. Arch. Histol. Cytol., 2000, 63, 17-31.
JACKSON J.R., MINTON J.A., HO M.L., WEI N., WINKLER J.D. Expression of vascular endothelial growth factor in synovial fibroblasts is induced by hypoxia and interleukin 1beta. J. Rheumatol., 1997, 24, 1253-1259.
JAMES M.J., CLELAND L.G., ROFE A.M., LESLIE A.L. Intraarticular pressure and the relationship between synovial perfusion and metabolic demand. J. Rheumatol., 1990, 17, 521-527.
JOUGLIN M., ROBERT C., VALETTE J.P., GAVARD F., QUINTIN-COLONN F., DENOIX J.M. Metalloproteinases and tumor necrosis factor-alpha activities in synovial fluids of horses: correlation with articular cartilage alterations. Vet. Res., 2000, 31, 507-515.
JOVANOVIC D., PELLETIER J.P., ALAAEDDINE N., MINEAU F., GENG C., RANGER P., MARTEL-PELLETIER J. Effect of IL-13 on cytokines, cytokine receptors and inhibitors on human osteoarthritis synovium and synovial fibroblasts. Osteoarthr. Cart., 1998, 6, 40-49.
JOVANOVIC D.V., MINEAU F., NOTOYA K., REBOUL P., MARTEL-PELLETIER J., PELLETIER J.P. Nitric oxide induced cell death in human osteoarthritic synoviocytes is mediated by tyrosine kinase activation and hydrogen peroxide and/or superoxide formation. J. Rheumatol., 2002, 29, 2165-2175.
KARATAY S., KIZILTUNC A., YILDIRIM K., KARANFIL R.C., SENEL K. Effects of different hyaluronic acid products on synovial fluid levels of intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in knee osteoarthritis. Ann. Clin. Lab. Sci., 2004, 34, 330-335.
KITAMURA H.P., YANASE H., KITAMURA H., IWANAGA T. Unique localization of protein gene product 9.5 in type B synoviocytes in the joints of horses. J. Histochem. Cytochem., 1999, 47, 343-351.
KITAMURA H., OKUMURA M., SATO F., KIMOTO K., KOHAMA M., HASHIMOTO Y., TAGAMI M., IWANAGA T. Increased concentrations of protein gene product 9.5 in the synovial fluid from horses with osteoarthritis. Jpn. J. Vet. Res., 2001, 49, 115-123.
KNORTH H., DORFMULLER P., LEBERT R., SCHMIDT W.E., WITTENBERG R.H., HEUKAMP M., WIESE M., WILLBURGER R.E. Participation of cyclooxygenase-1 in prostaglandin E2 release from synovitis tissue in primary osteoarthritis in vitro. Osteoarthr. Cart., 2004, 12, 658-666.
KOBAYASHI K., MATSUZAKA S., YOSHIDA Y., MIYAUCHI S., WADA Y., MORIYA H. The effects of intraarticularly injected sodium hyaluronate on levels of intact aggrecan and nitric oxide in the joint fluid of patients with knee osteoarthritis. Osteoarthr. Cart., 2004, 12, 536-542.
KOLOMYTKIN O.V., MARINO A.A., WADDELL D.D., MATHIS J.M., WOLF R.E., SADASIVAN K.K., ALBRIGHT J.A. IL-1 beta-induced production of metalloproteinases by synovial cells depends on gap junction conductance. Am. J. Physiol. Cell. Physiol., 2002, 282, C1254-1260.
KOPPENOL W.H. The Haber-Weiss cycle : 70 years later. Redox Rep., 2001, 6, 229-234.
KRAUS V.B., HUEBNER J.L., FINK C., KING J.B., BROWN S., VAIL T.P., GUILAK F. Urea as a passive transport marker for arthritis biomarker studies. Arthritis Rheum., 2002, 46, 420-427.
KURZ B., STEINHAGEN J., SCHÜNKE M. Articular chondrocytes and synoviocytes in a co-culture system : influence on reactive oxygen species-induced cytotoxicity and lipid peroxidation. Cell Tissue Res., 1999, 296, 555-563.
LANDONI M.F., FOOT R., FREAN S., LEES P. Effects of flunixin, tolfenamic acid, R(-) and S(+) ketoprofen on the response of equine synoviocytes to lipopolysaccharide stimulation. Equine Vet. J., 1996, 28, 468-475.
LAPADULA G., NICO B., CANTATORE F.P., LA CANNA R., RONCALI L., PIPITONE V. Early ultrastructural changes of articular cartilage and synovial membrane in experimental vitamin A-induced osteoarthritis. J. Rheumatol., 1995, 22, 1913-1921.
LAUFER S. Role of eicosanoids in structural degradation in osteoarthritis. Curr. Opin. Rheumatol., 2003, 15, 623-627.
LEMBURG A.K. Histologische und immunohistologische Untersuchungen an der Synovialmembran von Hunden mit spontanem vorderen Kreuzbandabriss oder Polyarthritis. Dissertation, TiHo, Hannover 2001.[en ligne] (sans date) Adresse URL:http://elib.tiho-hannover.de/dissertations/lemburga_2001.pdf. consulté le 24 août 04.
LIBERG P., MAGNUSSON L.-E., SCHOUGAARD H. Studies on the synovia in healthy horse with particular reference to the protein composition. Equine Vet. J., 1977, 9, 87-89.
LIN C.W., PHILLIPS S.L., BRINCKERHOFF C.E., GEORGESCU H.I., BANDARA G., EVANS C.H. Induction of collagenase mRNA in lapine articular chondrocytes by synovial factors and interleukin-1. Arch. Biochem. Biophys., 1988, 264, 351-354.
LISIGNOLI G., GRASSI F., PIACENTINI A., COCCHINI B., REMIDDI G., BEVILACQUA C., FACCHINI A. Hyaluronan does not affect cytokine and chemokine expression in osteoarthritic chondrocytes and synoviocytes. Osteoarthr. Cart., 2001, 9, 161-168.
LYNCH T.M., CARON J.P., ARNOCZKY S.P., LLOYD J.W., STICK J.A., RENDER J.A. Influence of exogenous hyaluronan on synthesis of hyaluronan and collagenase by equine synoviocytes. Am. J. Vet. Res., 1998, 59, 888-92.
MARCOUILLER P., PELLETIER J.P., GUEVREMONT M., MARTEL-PELLETIER J., RANGER P., LAUFER S., REBOUL P. Leukotriene and prostaglandin synthesis pathways in osteoarthritic synovial membranes: regulating factors for interleukin 1beta synthesis. J. Rheumatol., 2005, 32, 704-712.
MARINO A.A., WADDELL D.D., KOLOMYTKIN O.V., MEEK W.D., WOLF R., SADASIVAN K.K., ALBRIGHT J.A. Increased intercellular communication through gap junctions may contribute to progression of osteoarthritis. Clin. Orthop., 2004, 422, 224-232.
MARTEL-PELLETIER J., MINEAU F., FAHMI H., LAUFER S., REBOUL P., BOILEAU C., LAVIGNE M., PELLETIER J.P. Regulation of the expression of 5-lipoxygenase-activating protein/5-lipoxygenase and the synthesis of leukotriene B(4) in osteoarthritic chondrocytes: role of transforming growth factor beta and eicosanoids. Arthritis Rheum., 2004, 50, 3925-3933.
MAY S.A., HOOKE R.E., LEES P. Species restrictions demonstrated by the stimulation of equine cells with recombinant human interleukin-1. Vet. Immunol. Immunopathol., 1992a, 30, 373-384.
MAY S.A., HOOKE R.E., LEES P. Interleukin-1 stimulation of equine articular cells. Res. Vet. Sci., 1992b, 52, 342-348.
MAY S.A., HOOKE R.E., LEES P. Inhibition of interleukin-1 activity by equine synovial fluid. Equine Vet. J., 1992c, 24, 99-102.
MAY S.A., HOOKE R.E., LEES P. Equine chondrocyte activation by a variety of stimuli. Br. Vet. J., 1992d, 148, 389-397.
MCILWRAITH C.W. Intra articular and systemic medication used in the treatment of equine traumatic joint disease. In: Geneva Congress of Equine Medicine and Surgery, Founex, 12th to 14th December 1999. Editions de Médecine et Hygiène: Chêne-Bourg 1999, 76-82.
MOE S.M., BAILEY A.M. A coculture model of synoviocytes and bone for the evaluation of potential arthritis therapies. J. Pharmacol. Toxicol. Methods, 1999, 41, 127-134.
NAGAO M., ISHII S., KITAMURA K., AKINO T. Arachidonic acid metabolism in articular chondrocytes. Clin. Orthop., 1991, 271, 288-295.
NAGASE H., KASHIWAGI M. Aggrecanases and cartilage matrix degradation. Arthritis Res. Ther., 2003, 5, 94-103.
NEVO Z., SILVER J., CHOREV Y., RIKLIS I., ROBINSON D., YOSIPOVITCH Z. Adhesion characteristics of chondrocytes cultured separately and in cocultures with synovial fibroblasts. Cell Biol. Int., 1993, 17, 255-273.
NIO J., YOKOYAMA A., OKUMURA M., IWANAGA T. Three-dimensional ultrastructure of synoviocytes in the knee joint of rabbits and morphological changes in osteoarthritis model. Arch. Histol. Cytol., 2002, 65, 189-200.
O'CONNOR T.M., O'CONNELL J., O'BRIEN D.I., GOODE T., BREDIN C.P., SHANAHAN F.J. The role of substance P in inflammatory disease. Cell. Physiol., 2004, 201, 167-180.
PANASYUK A., COLANTUONI G., KHATIB A.M., LOMRI A., MITROVIC D.R. Human synovium produces substances that inhibit DNA and stimulate proteoglycan and collagen synthesis by cultured human articular chondrocytes and synovial fibroblasts. Scand. J. Rheumatol., 2003, 32, 240-246.
POLI A., COLEMAN P.J., MASON R.M., LEVICK J.R. Contribution of F-actin to barrier properties of the blood-joint pathway. Microcirculation, 2002, 9, 419-430.
PUNZI L., TODESCO S., TOFFANO G., CATENA R., BIGON E., BRUNI A. Phospholipids in inflammatory synovial effusions. Rheumatol. Int., 1986, 6, 7-11.
REBOUL P., PELLETIER J.P., TARDIF G., CLOUTIER J.M., MARTEL-PELLETIER J. The new collagenase, collagenase-3, is expressed and synthesized by human chondrocytes but not by synoviocytes. a role in osteoarthritis. J. Clin. Invest., 1996, 97, 2011-2019.
RICHMAN A.I., SU E.Y., HO G. Jr. Reciprocal relationship of synovial fluid volume and oxygen tension. Arthritis Rheum., 1981, 24, 701-705.
RITCHLIN C. Fibroblast biology. Effector signals released by the synovial fibroblast in arthritis. Arthritis Res., 2000, 2, 356-360.
RONCHETTI P.I., GUERRA D., TAPARELLI F., BORALDI F., BERGAMIN G., MORI G., ZIZZI F., FRIZZIERO L. Morphological analysis of knee synovial membrane biopsies from a randomized controlled clinical study comparing the effects of sodium hyaluronate (Hyalgan) and methylprednisolone acetate (Depomedrol) in osteoarthritis. Rheumatology, 2001, 40, 158-169.
SAKURAI H., KOHSAKA H., LIU M.F., HIGASHIYAMA H., HIRATA Y., KANNO K., SAITO I., MIYASAKA N. Nitric oxide production and inducible nitric oxide synthase expression in inflammatory arthritides. J. Clin. Invest., 1995, 96, 2357-2363.
SANDHU J.K., ROBERTSON S., BIRNBOIM H.C., GOLDSTEIN R. Distribution of protein nitrotyrosine in synovial tissues of patients with rheumatoid arthritis and osteoarthritis. J. Rheumatol., 2003, 30, 1173-1181.
SAXNE T., PALLADINO M.A. Jr, HEINEGARD D., TALAL N., WOLLHEIM F.A. Detection of tumor necrosis factor alpha but not tumor necrosis factor beta in rheumatoid arthritis synovial fluid and serum. Arthritis Rheum., 1988, 31, 1041-1045.
SCHÄFER D.B., WENDT D., MORETTI M., JAKOB M., JAY G.D., HEBERER M., MARTIN I. Lubricin reduces cartilage-cartilage integration. Biorheology, 2004, 41, 503-508.
SCHÄFFLER A., EHLING A., NEUMANN E., HERFARTH H., TARNER I., SCHOLMERICH J., GAY S., MÜLLER-LADNER U. Adipocytokines in synovial fluid. JAMA, 2003, 290, 1709-1710.
SCHNEIDER N., MOUITHYS-MICKALAD A.L., LEJEUNE J.P., DEBY-DUPONT G.P., HOEBELE M., SERTEYN D.A. Synoviocytes, not chondrocytes, release free radicals after cycles of anoxia/re-oxygenation. Biochem. Biophys. Res. Commun., 2005, 334, 669-673.
SCHWARZ I.M., HILLS B.A. Surface-active phospholipid as the lubricating component of lubricin. Br. J. Rheumatol., 1998, 37, 21-26.
SHIKICHI M., KITAMURA H.P., YANASE H., KONNO A., TAKAHASHI-IWANAGA H., IWANAGA T. Three-dimensional ultrastructure of synoviocytes in the horse joint as revealed by the scanning electron microscope. Arch. Histol. Cytol., 1999, 62, 219-229.
SKIOLDEBRAND E., LORENZO P., ZUNINO L., RUCKLIDGE G.J., SANDGREN B., CARLSTEN J., EKMAN S. Concentration of collagen, aggrecan and cartilage oligomeric matrix protein (COMP) in synovial fluid from equine middle carpal joints. Equine Vet. J., 2001, 33, 394-402.
SMITH M.D., BARG E., WEEDON H., PAPENGELIS V., SMEETS T., TAK P.P., KRAAN M., COLEMAN M., AHERN M.J. Microarchitecture and protective mechanisms in synovial tissue from clinically and arthroscopically normal knee joints. Ann. Rheum. Dis., 2003, 62, 303-307.
STARK D.D., BRADLEY W.G. Chapter 38 Knee Bony injuries. In: Corra E. Magnetic Resonance Imaging. Mosby by Greenwood G. St. Louis, Missouri.1999, 837-840.
STEFANOVIC-RACIC M., STADLER J., GEORGESCU H.I., EVANS C.H. Nitric oxide synthesis and its regulation by rabbit synoviocytes. J. Rheumatol., 1994, 21, 1892-1898.
SUNG K., MENDELOW D., GEORGESCU H.I., EVANS C.H. Characterisation of chondrocyte activation in response to cytokines synthesised by a synovial cell line. Biochim. Biophys. Acta, 1988, 971, 148-156.
TAGUCHI K., HIRANO T., IWASAKI K., SUGIHARA H. Reconstruction culture system simulating human synovium: a three-dimensional collagen gel culture of synoviocytes. Cell Struct. Funct., 1997, 22, 443-453.
TANIMOTO K., OHNO S., FUJIMOTO K., HONDA K., IJUIN C., TANAKA N., DOI T., NAKAHARA M., TANNE K. Proinflammatory cytokines regulate the gene expression of hyaluronic acid synthetase in cultured rabbit synovial membrane cells. Connect. Tissue Res., 2001, 42, 187-195.
TODHUNTER R.J., FUBINI S.L., FREEMAN K.P., LUST G. Concentrations of keratan sulfate in plasma and synovial fluid from clinically normal horses and horses with joint disease. J. Am. Vet. Med. Assoc., 1997, 210, 369-374.
TOLBOOM T.C., PIETREMAN E., VAN DER LAAN W.H., TOES R.E., HUIDEKOPER A.L., NELISSEN R.G., BREEDVELD F.C., HUIZINGA T.W. Invasive properties of fibroblast-like synoviocytes: correlation with growth characteristics and expression of MMP-1, MMP-3, and MMP-10. Ann. Rheum. Dis., 2002, 61, 975-980.
TOPPETS V., PASTORET V., DE BEHR V., ANTOINE N., DESSY C., GABRIEL A. Morphologie, croissance et remaniement du tissu osseux. Ann. Méd. Vét., 2004, 148, 1-13.
TRUMBLE T.N., TROTTER G.W., OXFORD J.R., McILWRAITH C. W., CAMMARATA S., GOODNIGHT J.L., BILLINGHURST R.C., FRISBIE D.D. Synovial fluid gelatinase concentrations and matrix metalloproteinase and cytokine expression in naturally occurring joint disease in the horses. Am. J. Vet. Res., 2001, 9, 1467-1476.
TUCCI M.A., TSAO A., HUGHES J., BAKER R., BENGHUZZI H. Release of inflammatory cytokines by macrophages and synovial cells challenged with tumor necrosis factor. Biomed. Sci. Instrum., 2002, 38, 89-94.
TULAMO R.M., BRAMLAGE L.R., GABEL A.A. The influence of corticosteroids on sequential clinical and synovial fluid parameters in joints with acute infectious arthritis in the horse. Equine Vet. J., 1989a, 21, 332-337.
TULAMO R.M., BRAMLAGE L.R., GABEL A.A. Sequential clinical and synovial fluid changes associated with acute infectious arthritis in the horse. Equine Vet. J., 1989b, 21, 325-331.
VANDENABEELE F., DE BARI C., MOREELS M., LAMBRICHTS I., DELL'ACCIO F., LIPPENS P.L., LUYTEN F.P. Morphological and immunocytochemical characterization of cultured fibroblast-like cells derived from adult human synovial membrane. Arch. Histol. Cytol., 66, 2003, 145-153.
VAN DEN BOOM R., BRAMA P.A., KIERS G.H., DE GROOT J., VAN WEEREN P.R. Assessment of the effects of age and joint disease on hydroxyproline and glycosaminoglycan concentrations in synovial fluid from the metacarpophalangeal joint of horses. Am. J. Vet. Res., 2004, 65, 296-302.
VANKEMMELBEKE M.N., ILIC M.Z., HANDLEY C.J., KNIGHT C.G., BUTTLE D. Coincubation of bovine synovial or capsular tissue with cartilage generates a soluble «Aggrecanase» activity. Biochem. Biophys. Res. Commun., 1999, 255, 686-691.
VERGNE B., BERTIN P., BANNET C., PAIRET M., UEU L.P., RIGAUD M. Differential inhibition of COX-1 and COX-2 by NSAIDS in cultured synovial cells. [en ligne] (sans date) adresse url: www.cpm.es/rheumaclub/cox2/pos7.htm. Consulté le 30 mai 2002.
VIITANEN M., BIRD J., MAISI P., SMITH R., TULAMO R.M., MAY S. Differences in the concentration of various synovial fluid constituents between the distal interphalangeal joint, the metacarpophalangeal joint and the navicular bursa in normal horses. Res. Vet. Sci., 2000, 69, 63-67.
VON RECHENBERG B., McILWRAITH C.W., AKENS M.K., FRISBIE D.D., LEUTENEGGER C., AUER J.A. Spontaneous production of nitric oxide (NO), prostaglandin (PGE2) and neutral metalloproteases (NMPs) in media of explant cultures of equine synovial membrane and articular cartilage from normal and osteoarthritic joints. Equine Vet. J., 2000, 32, 140-150.
WITTENBERG R.H., WILLBURGER R.E., KLEEMEYER K.S., PESKAR B.A. In vitro release of prostaglandins and leukotrienes from synovial tissue, cartilage, and bone in degenerative joint diseases. Arthritis Rheum., 1993, 36, 1444-1450.
YAO Q., WANG S., GLORIOSO J.C., EVANS C.H., ROBBINS P.D., GHIVIZZANI S.C., OLIGINO T.J. Gene transfer of p53 to arthritic joints stimulates synovial apoptosis and inhibits inflammation. Mol. Ther., 2001, 3, 901-910.
ZHANG X., MAO Z., YU C.J. Suppression of early experimental osteoarthritis by gene transfer of interleukin-1 receptor antagonist and interleukin-10. Orthop. Res. 2004, 22, 742-750.
ZIMMERING T. Radiological and arthroscopic examination in comparison with light microscopical diagnosis of synovia of clinical sound fetlock joints of horses. Dissertation, TiHo Hannover 2000. [en ligne] (sans date) Adresse URL: http://elib.tiho-hannover.de/dissertations/zimmert_2000.pdf.
