Influence of cartilage interstitial fluid on the mRNA levels of matrix proteins, cytokines, metalloproteases and their inhibitors in synovial membrane

Hyc,Anna; Moskalewski,Stanislaw; Osiecka-Iwan,Anna

doi:10.3892/ijmm.2016.2684

Influence of cartilage interstitial fluid on the mRNA levels of matrix proteins, cytokines, metalloproteases and their inhibitors in synovial membrane

Authors:
- Anna Hyc
- Stanislaw Moskalewski
- Anna Osiecka-Iwan
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Affiliations: Department of Histology and Embryology, Medical University of Warsaw, PL-02004 Warsaw, Poland
Published online on: July 19, 2016 https://doi.org/10.3892/ijmm.2016.2684
Pages: 937-942

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Abstract

Articular cartilage and the synovial membrane both ensure the smooth action of synovial joints; however, the influence of chondrocytes on synovial metabolism remains unclear. The secretory activity of chondrocytes is usually studied in cell cultures and may differ from that in intact cartilage. According to McCutchen's theory of ‘weeping’ joint lubrication, loading of the articular cartilage during motion squeezes the fluid with lubricating properties from the cartilage. The purpose of the study was to obtain cartilage interstitial fluid (CIF) from intact cartilage and to evaluate its influence on gene expression in the synovial membrane cells. CIF was rinsed out from the cartilage of newborn rats at a pressure of three bar. The chondrocytes survived rinsing and grew in culture. Cytokines in CIF were detected using the enzyme-linked immunosorbent assay (ELISA). The influence of CIF and CIF-like cocktail (all cytokines found in CIF) on gene expression in the synovial membrane cells was studied after a 4 h-incubation, by real-time PCR. Data were analyzed using the Wilcoxon matched-pair test or by the Mann‑Whitney U test. CIF contained basic fibroblast growth factor (bFGF), insulin-like growth factor (IGF)‑1, transforming growth factor β1 (TGFβ1), bone morphogenetic protein 7 (BMP7), macrophage (M)-colony-stimulating factor (CSF), granulocyte (G)-CSF and leukemia inhibitory factor (LIF). CIF stimulated the expression of hyaluronan synthase (HAS)1 and 2, lubricin, collagen I, versican, aggrecan, matrix metalloproteinases (MMPs)2 and 3, tissue inhibitors of metalloproteinases (TIMPs) 1-3, interleukin (IL)-6 and TGFβ1, and decreased the expression of tumor necrosis factor (TNF) and IL-1β. Incubation of the synovial membrane with CIF-like cocktail partially imitated the effects of CIF. Analysis of CIF composition may help to characterize the secretory activity of chondrocytes in their natural environment under various physiological and pathological conditions and to understand the interactions between articular cartilage and the synovial membrane.

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1	Swann DA: Structure and function of lubricin, the glycoprotein responsible for the boundary lubrication of articular cartilage. Articular Synovium. Franchimont P and Karger S: Basel: pp. 45–58. 1982
2	Hui AY, McCarty WJ, Masuda K, Firestein GS and Sah RL: A systems biology approach to synovial joint lubrication in health, injury, and disease. Wiley Interdiscip Rev Syst Biol Med. 4:15–37. 2012. View Article : Google Scholar
3	Bandara G, Georgescu HI, Lin CW and Evans CH: Synovial activation of chondrocytes: evidence for complex cytokine interactions. Agents Actions. 34:285–288. 1991. View Article : Google Scholar : PubMed/NCBI
4	Lee DA, Salih V, Stockton EF, Stanton JS and Bentley G: Effect of normal synovial fluid on the metabolism of articular chondrocytes in vitro. Clin Orthop Relat Res. 342:228–238. 1997. View Article : Google Scholar : PubMed/NCBI
5	Hirsch MS, Lunsford LE, Trinkaus-Randall V and Svoboda KK: Chondrocyte survival and differentiation in situ are integrin mediated. Dev Dyn. 210:249–263. 1997. View Article : Google Scholar : PubMed/NCBI
6	Jakob M, Démarteau O, Schäfer D, Stumm M, Heberer M and Martin I: Enzymatic digestion of adult human articular cartilage yields a small fraction of the total available cells. Connect Tissue Res. 44:173–180. 2003. View Article : Google Scholar : PubMed/NCBI
7	Hayman DM, Blumberg TJ, Scott CC and Athanasiou KA: The effects of isolation on chondrocyte gene expression. Tissue Eng. 12:2573–2581. 2006. View Article : Google Scholar : PubMed/NCBI
8	Schulze-Tanzil G, de Souza P, Villegas Castrejon H, John T, Merker HJ, Scheid A and Shakibaei M: Redifferentiation of dedifferentiated human chondrocytes in high-density cultures. Cell Tissue Res. 308:371–379. 2002. View Article : Google Scholar : PubMed/NCBI
9	Marlovits S, Hombauer M, Tamandl D, Vècsei V and Schlegel W: Quantitative analysis of gene expression in human articular chondrocytes in monolayer culture. Int J Mol Med. 13:281–287. 2004.PubMed/NCBI
10	Osiecka-Iwan A, Hyc A, Niderla-Bielińska J and Moskalewski S: Chondrocyte-associated antigen and matrix components in a 2-and 3-dimensional culture of rat chondrocytes. Mol Med Rep. 1:881–887. 2008.PubMed/NCBI
11	Polacek M, Bruun J-A, Elvenes J, Figenschau Y and Martinez I: The secretory profiles of cultured human articular chondrocytes and mesenchymal stem cells: implications for autologous cell transplantation strategies. Cell Transplant. 20:1381–1393. 2011. View Article : Google Scholar
12	Melas IN, Chairakaki AD, Chatzopoulou EI, Messinis DE, Katopodi T, Pliaka V, Samara S, Mitsos A, Dailiana Z, Kollia P and Alexopoulos LG: Modeling of signaling pathways in chondrocytes based on phosphoproteomic and cytokine release data. Osteoarthritis Cartilage. 22:509–518. 2014. View Article : Google Scholar : PubMed/NCBI
13	McCutchen CW: Sponge-hydrostatic and weeping bearings. Nature. 184:1284–1285. 1959. View Article : Google Scholar : PubMed/NCBI
14	Morrell KC, Hodge WA, Krebs DE and Mann RW: Corroboration of in vivo cartilage pressures with implications for synovial joint tribology and osteoarthritis causation. Proc Natl Acad Sci USA. 102:14819–14824. 2005. View Article : Google Scholar : PubMed/NCBI
15	Caligaris M and Ateshian GA: Effects of sustained interstitial fluid pressurization under migrating contact area, and boundary lubrication by synovial fluid, on cartilage friction. Osteoarthritis Cartilage. 16:1220–1227. 2008. View Article : Google Scholar : PubMed/NCBI
16	Hyc A, Osiecka-Iwan A, Niderla-Bielińska J, Jankowska-Steifer E and Moskalewski S: Pro- and anti-inflammatory cytokines increase hyaluronan production by rat synovial membrane in vitro. Int J Mol Med. 24:579–585. 2009.PubMed/NCBI
17	Hyc A, Osiecka-Iwan A, Niderla-Bielińska J and Moskalewski S: Influence of LPS, TNF, TGF-β1 and IL-4 on the expression of MMPs, TIMPs and selected cytokines in rat synovial membranes incubated in vitro. Int J Mol Med. 27:127–137. 2011.
18	Hyc A, Osiecka-Iwan A, Dziunycz P and Moskalewski S: Preparation of rat synovial membrane for studies of cytokine secretion. Folia Histochem Cytobiol. 45:57–60. 2007.PubMed/NCBI
19	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25:402–408. 2001. View Article : Google Scholar
20	Darling EM and Athanasiou KA: Growth factor impact on articular cartilage subpopulations. Cell Tissue Res. 322:463–473. 2005. View Article : Google Scholar : PubMed/NCBI
21	Sah RL, Chen AC, Grodzinsky AJ and Trippel SB: Differential effects of bFGF and IGF-I on matrix metabolism in calf and adult bovine cartilage explants. Arch Biochem Biophys. 308:137–147. 1994. View Article : Google Scholar : PubMed/NCBI
22	Trippel SB: Growth factor actions on articular cartilage. J Rheumatol Suppl. 43:129–132. 1995.PubMed/NCBI
23	Blackstock CD, Higashi Y, Sukhanov S, Shai SY, Stefanovic B, Tabony AM, Yoshida T and Delafontaine P: Insulin-like growth factor-1 increases synthesis of collagen type I via induction of the mRNA-binding protein LARP6 expression and binding to the 5′ stem-loop of COL1a1 and COL1a2 mRNA. J Biol Chem. 289:7264–7274. 2014. View Article : Google Scholar : PubMed/NCBI
24	Schalkwijk J, Joosten LA, van den Berg WB, van Wyk JJ and van de Putte LB: Insulin-like growth factor stimulation of chondrocyte proteoglycan synthesis by human synovial fluid. Arthritis Rheum. 32:66–71. 1989. View Article : Google Scholar : PubMed/NCBI
25	Patil AS, Sable RB and Kothari RM: An update on transforming growth factor-β (TGF-β): sources, types, functions and clinical applicability for cartilage/bone healing. J Cell Physiol. 226:3094–3103. 2011. View Article : Google Scholar : PubMed/NCBI
26	Verrecchia F and Mauviel A: TGF-β and TNF-α: Antagonistic cytokines controlling type I collagen gene expression. Cell Signal. 16:873–880. 2004. View Article : Google Scholar : PubMed/NCBI
27	Yaeger PC, Masi TL, de Ortiz JL, Binette F, Tubo R and McPherson JM: Synergistic action of transforming growth factor-β and insulin-like growth factor-I induces expression of type II collagen and aggrecan genes in adult human articular chondrocytes. Exp Cell Res. 237:318–325. 1997. View Article : Google Scholar
28	Seifarth C, Csaki C and Shakibaei M: Anabolic actions of IGF-I and TGF-β1 on interleukin-1β-treated human articular chondrocytes: Evaluation in two and three dimensional cultures. Histol Histopathol. 24:1245–1262. 2009.PubMed/NCBI
29	Campo GM, Avenoso A, Campo S, D'Ascola A, Traina P and Calatroni A: Effects of cytokines on hyaluronan synthase activity and response to oxidative stress by fibroblasts. Br J Biomed Sci. 66:28–36. 2009. View Article : Google Scholar
30	Barrientos S, Stojadinovic O, Golinko MS, Brem H and Tomic-Canic M: Growth factors and cytokines in wound healing. Wound Repair Regen. 16:585–601. 2008. View Article : Google Scholar
31	Piek E, Ju WJ, Heyer J, Escalante-Alcalde D, Stewart CL, Weinstein M, Deng C, Kucherlapati R, Bottinger EP and Roberts AB: Functional characterization of transforming growth factor beta signaling in Smad2- and Smad3-deficient fibroblasts. J Biol Chem. 276:19945–19953. 2001. View Article : Google Scholar : PubMed/NCBI
32	Luan Y, Praul CA, Gay CV and Leach RM Jr: Basic fibroblast growth factor: an autocrine growth factor for epiphyseal growth plate chondrocytes. J Cell Biochem. 62:372–382. 1996. View Article : Google Scholar : PubMed/NCBI
33	Loeser RF, Chubinskaya S, Pacione C and Im HJ: Basic fibroblast growth factor inhibits the anabolic activity of insulin-like growth factor 1 and osteogenic protein 1 in adult human articular chondrocytes. Arthritis Rheum. 52:3910–3917. 2005. View Article : Google Scholar : PubMed/NCBI
34	Alsalameh S, Firestein GS, Oez S, Kurrle R, Kalden JR and Burmester GR: Regulation of granulocyte macrophage colony stimulating factor production by human articular chondrocytes. Induction by both tumor necrosis factor-alpha and interleukin 1, downregulation by transforming growth factor β and upregulation by fibroblast growth factor. J Rheumatol. 21:993–1002. 1994.PubMed/NCBI
35	Campbell IK, Ianches G and Hamilton JA: Production of macrophage colony-stimulating factor (M-CSF) by human articular cartilage and chondrocytes. Modulation by interleukin-1 and tumor necrosis factor alpha. Biochim Biophys Acta. 1182:57–63. 1993. View Article : Google Scholar : PubMed/NCBI
36	Mathieu ME, Saucourt C, Mournetas V, Gauthereau X, Thézé N, Praloran V, Thiébaud P and Bœuf H: LIF-dependent signaling: new pieces in the Lego. Stem Cell Rev. 8:1–15. 2012. View Article : Google Scholar :
37	Henrotin YE, De Groote DD, Labasse AH, Gaspar SE, Zheng SX, Geenen VG and Reginster JY: Effects of exogenous IL-1β, TNF alpha, IL-6, IL-8 and LIF on cytokine production by human articular chondrocytes. Osteoarthritis Cartilage. 4:163–173. 1996. View Article : Google Scholar : PubMed/NCBI
38	Wolf J, Rose-John S and Garbers C: Interleukin-6 and its receptors: a highly regulated and dynamic system. Cytokine. 70:11–20. 2014. View Article : Google Scholar : PubMed/NCBI
39	Guerne PA, Carson DA and Lotz M: IL-6 production by human articular chondrocytes. Modulation of its synthesis by cytokines, growth factors, and hormones in vitro. J Immunol. 144:499–505. 1990.PubMed/NCBI
40	Seong GJ, Hong S, Jung SA, Lee JJ, Lim E, Kim SJ and Lee JH: TGF-β-induced interleukin-6 participates in transdifferentiation of human Tenon's fibroblasts to myofibroblasts. Mol Vis. 15:2123–2128. 2009.
41	Wajant H, Pfizenmaier K and Scheurich P: Tumor necrosis factor signaling. Cell Death Differ. 10:45–65. 2003. View Article : Google Scholar : PubMed/NCBI
42	Nathan CF: Secretory products of macrophages. J Clin Invest. 79:319–326. 1987. View Article : Google Scholar : PubMed/NCBI
43	Renier G, Clément I, Desfaits AC and Lambert A: Direct stimulatory effect of insulin-like growth factor-I on monocyte and macrophage tumor necrosis factor-alpha production. Endocrinology. 137:4611–4618. 1996.PubMed/NCBI