期刊论文详细信息
BMC Musculoskeletal Disorders
Effect of interleukin-1β treatment on co-cultures of human meniscus cells and bone marrow mesenchymal stromal cells
Adetola B Adesida1  Nadr M Jomha1  Aillette Mulet-Sierra1  Louis W Bezuidenhout1  Anika Chowdhury1 
[1] Department of Surgery, Division of Orthopaedic Surgery, Laboratory of Stem Cell Biology and Orthopaedic Tissue Engineering, University of Alberta, Edmonton, AB T6G 2E1, Canada
关键词: Tissue engineering;    Meniscus;    Meniscus cells;    Fibrochondrogenesis;    Co-cultures;    Chondrogenesis;    Bone marrow stromal cells;   
Others  :  1130272
DOI  :  10.1186/1471-2474-14-216
 received in 2012-12-17, accepted in 2013-07-05,  发布年份 2013
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【 摘 要 】

Background

Interleukin-1β (IL-1β) is a major mediator of local inflammation present in injured joints. In this study, we aimed at comparing the effect of IL-1β on engineered tissues from MCs, BMSCs and co-cultured MCs and BMSCs.

Methods

We compared the effect of IL-1β in 3 groups: (1) MCs, (2) BMSCs and, (3) co-cultures of MCs and BMSCs. We selected 1 to 3 ratio of MCs to BMSCs for the co-cultures. Passage two (P2) human BMSCs were obtained from two donors. Human MCs were isolated from menisci of 4 donors. Mono-cultures of MCs and BMSCs, and co-cultures of MCs and BMSCs were cultured in chondrogenic medium with TGFβ3, as cell pellets for 14 days. Thereafter, pellets were cultured for 3 more days in same medium as before with or without IL-1β (500 pg/ml). Pellets were assessed histologically, biochemically and by RT-PCR for gene expression of aggrecan, sox9, MMP-1, collagens I and II. Statistics was performed using one-way ANOVA with Tukey’s post-tests.

Results

Co-cultured pellets were the most intensely stained with safranin O and collagen II. Co-cultured pellets had the highest expression of sox9, collagen I and II. IL-1β treatment slightly reduced the GAG/DNA of co-cultured pellets but still exceeded the sum of the GAG/DNA from the proportion of MCs and BMSCs in the co-cultured pellets. After IL-1β treatment, the expression of sox9, collagen I and II in co-cultured pellets was higher compared to their expression in pure pellets. IL-1β induced MMP-1 expression in mono-cultures of MCs but not significantly in mono-cultures of BMSCs or in co-cultured pellets. IL-1β induced MMP-13 expression in mono-cultured pellets of BMSCs and in co-cultured pellets.

Conclusions

Co-cultures of MCs and BMSCs resulted in a synergistic production of cartilaginous matrix compared to mono-cultures of MCs and BMSCs. IL-1β did not abrogate the accumulated GAG matrix in co-cultures but mediated a decreased mRNA expression of aggrecan, collagen II and Sox9. These results strengthen the combinatorial use of primary MCs and BMSCs as a cell source for meniscus tissue engineering by demonstrating retention of fibrochondrogenic phenotype after exposure to IL-1β.

【 授权许可】

   
2013 Chowdhury et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Makris EA, Hadidi P, Athanasiou KA: The knee meniscus: Structure-function, pathophysiology, current repair techniques, and prospects for regeneration. Biomaterials 2011, 32(30):7411-7431.
  • [2]Messner K, Gao J: The menisci of the knee joint. Anatomical and functional characteristics, and a rationale for clinical treatment. J Anat 1998, 193(Pt 2):161-178.
  • [3]Levy IM, Torzilli PA, Fisch ID: The contribution of the menisci to the stabilty of the knee. In Knee Meniscus: Basic and Clinical Foundations. Edited by Mow VC, Arnoczky SP, Jackson DW. New York: Raven Press, Ltd; 1992:107-115.
  • [4]Ahmed AM: The load-bearing role of the knee meniscus. In Knee Meniscus: Basic and Clinical Foundations. Edited by Mow VC, Arnoczky SP, Jackson DW. New York: Raven Press, Ltd; 1992:59-73.
  • [5]Aagaard H, Verdonk R: Function of the normal meniscus and consequences of meniscal resection. Scand J Med Sci Sports 1999, 9(3):134-140.
  • [6]Aagaard H, Jorgensen U, Bojsen-Moller F: Reduced degenerative articular cartilage changes after meniscal allograft transplantation in sheep. Knee Surg Sports Traumatol Arthrosc 1999, 7(3):184-191.
  • [7]Adams ME, Hukins DWL: The extracellular matrix of the meniscus. In Knee Meniscus: Basic and Clinical Foundations. Edited by Mow VC, Arnoczky SP, Jackson DW. New York: Raven Press Ltd; 1992:15-28.
  • [8]McDevitt CA, Miller RR, Spindler KP: The cells and cell matrix interactions of the meniscus. In Knee Meniscus: Basic and Clinical Foundations. Edited by Mow VC, Arnoczky SP, Jackson DW. New York: Raven; 1992:29-36.
  • [9]McDevitt CA, Mukherjee S, Kambic H, Parker R: Emerging concepts of the cell biology of the meniscus. Curr Opin Orthop 2002, 13(5):345-350.
  • [10]McDermott ID, Amis AA: The consequences of meniscectomy. J Bone Joint Surg Br 2006, 88(12):1549-1556.
  • [11]Roos H, Lauren M, Adalberth T, Roos EM, Jonsson K, Lohmander LS: Knee osteoarthritis after meniscectomy: Prevalence of radiographic changes after twenty-one years, compared with matched controls. Arthritis Rheum 1998, 41(4):687-693.
  • [12]Fairbank T: Knee joint changes after menisectomy. J Bone Joint Surg 1948, 30B:664-670.
  • [13]Arnoczky SP: Building a meniscus. Biologic considerations. Clin Orthop 1999, (367 Suppl):S244-S253.
  • [14]Ibarra C, Jannetta C, Vacanti CA, Cao Y, Kim TH, Upton J, Vacanti JP: Tissue engineered meniscus: a potential new alternative to allogeneic meniscus transplantation. Transplant Proc 1997, 29(1–2):986-988.
  • [15]Ibarra C, Koski JA, Warren RF: Tissue engineering meniscus: cells and matrix. Orthop Clin North Am 2000, 31(3):411-418.
  • [16]Baker BM, Nathan AS, Huffman GR, Mauck RL: Tissue engineering with meniscus cells derived from surgical debris. Osteoarthritis Cartilage 2009, 17(3):336-345.
  • [17]Izuta Y, Ochi M, Adachi N, Deie M, Yamasaki T, Shinomiya R: Meniscal repair using bone marrow-derived mesenchymal stem cells: experimental study using green fluorescent protein transgenic rats. Knee 2005, 12(3):217-223.
  • [18]Kobayashi M: A study of polyvinyl alcohol-hydrogel (PVA-H) artificial meniscus in vivo. Biomed Mater Eng 2004, 14(4):505-515.
  • [19]Kon E, Filardo G, Tschon M, Fini M, Giavaresi G, Reggiani LM, Chiari C, Nehrer S, Martin I, Salter DM, et al.: Tissue engineering for total meniscal substitution: animal study in sheep model-results at 12 months. Tissue Eng Part A 2012, 18(15–16):1573-1582.
  • [20]Marsano A, Millward-Sadler SJ, Salter DM, Adesida A, Hardingham T, Tognana E, Kon E, Chiari-Grisar C, Nehrer S, Jakob M, et al.: Differential cartilaginous tissue formation by human synovial membrane, fat pad, meniscus cells and articular chondrocytes. Osteoarthritis Cartilage 2007, 15(1):48-58.
  • [21]Matthies NF, Mulet-Sierra A, Jomha NM, Adesida AB: Matrix formation is enhanced in co-cultures of human meniscus cells with bone marrow stromal cells. J Tissue Eng Regen Med 2012. In press
  • [22]Mauck RL, Martinez-Diaz GJ, Yuan X, Tuan RS: Regional multilineage differentiation potential of meniscal fibrochondrocytes: implications for meniscus repair. Anat Rec (Hoboken) 2007, 290(1):48-58.
  • [23]Mueller SM, Shortkroff S, Schneider TO, Breinan HA, Yannas IV, Spector M: Meniscus cells seeded in type I and type II collagen-GAG matrices in vitro. Biomaterials 1999, 20(8):701-709.
  • [24]Nakata K, Shino K, Hamada M, Mae T, Miyama T, Shinjo H, Horibe S, Tada K, Ochi T, Yoshikawa H: Human meniscus cell: characterization of the primary culture and use for tissue engineering. Clin Orthop Relat Res 2001, (391 Suppl):S208-218.
  • [25]Pabbruwe MB, Kafienah W, Tarlton JF, Mistry S, Fox DJ, Hollander AP: Repair of meniscal cartilage white zone tears using a stem cell/collagen-scaffold implant. Biomaterials 2010, 31(9):2583-2591.
  • [26]Pereira H, Frias AM, Oliveira JM, Espregueira-Mendes J, Reis RL: Tissue engineering and regenerative medicine strategies in meniscus lesions. Arthroscopy 2011, 27(12):1706-1719.
  • [27]Peretti GM, Gill TJ, Xu JW, Randolph MA, Morse KR, Zaleske DJ: Cell-based therapy for meniscal repair: a large animal study. Am J Sports Med 2004, 32(1):146-158.
  • [28]Buma P, Ramrattan NN, van Tienen TG, Veth RPH: Tissue engineering of the meniscus. Biomaterials 2004, 25(9):1523-1532.
  • [29]Chiari C, Koller U, Dorotka R, Eder C, Plasenzotti R, Lang S, Ambrosio L, Tognana E, Kon E, Salter D, et al.: A tissue engineering approach to meniscus regeneration in a sheep model. Osteoarthritis Cartilage 2006, 14(10):1056-1065.
  • [30]Angele P, Johnstone B, Kujat R, Zellner J, Nerlich M, Goldberg V, Yoo J: Stem cell based tissue engineering for meniscus repair. J Biomed Mater Res A 2008, 85(2):445-455.
  • [31]Murphy JM, Fink DJ, Hunziker EB, Barry FP: Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 2003, 48(12):3464-3474.
  • [32]Mueller MB, Tuan RS: Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 2008, 58(5):1377-1388.
  • [33]Saliken DJ, Mulet-Sierra A, Jomha NM, Adesida AB: Decreased hypertrophic differentiation accompanies enhanced matrix formation in co-cultures of outer meniscus cells with bone marrow mesenchymal stromal cells. Arthritis Res Ther 2012, 14(3):R153. BioMed Central Full Text
  • [34]Cui X, Hasegawa A, Lotz M, D’Lima D: Structured three-dimensional co-culture of mesenchymal stem cells with meniscus cells promotes meniscal phenotype without hypertrophy. Biotechnol Bioeng 2012, 109(9):2369-2380.
  • [35]Adesida AB, Mulet-Sierra A, Jomha NM: Hypoxia mediated isolation and expansion enhances the chondrogenic capacity of bone marrow mesenchymal stromal cells. Stem Cell Res Ther 2012, 3(2):9. BioMed Central Full Text
  • [36]Acharya C, Adesida A, Zajac P, Mumme M, Riesle J, Martin I, Barbero A: Enhanced chondrocyte proliferation and mesenchymal stromal cells chondrogenesis in coculture pellets mediate improved cartilage formation. J Cell Physiol 2012, 227:88-97.
  • [37]Farndale RW, Buttle DJ, Barrett AJ: Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 1986, 883(2):173-177.
  • [38]Murdoch AD, Grady LM, Ablett MP, Katopodi T, Meadows RS, Hardingham TE: Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: generation of scaffold-free cartilage. Stem Cells 2007, 25(11):2786-2796.
  • [39]Adesida AB, Grady LM, Khan WS, Hardingham TE: The matrix-forming phenotype of cultured human meniscus cells is enhanced after culture with fibroblast growth factor 2 and is further stimulated by hypoxia. Arthritis Res Ther 2006, 8(3):R61. BioMed Central Full Text
  • [40]Adesida AB, Grady LM, Khan WS, Millward-Sadler SJ, Salter DM, Hardingham TE: Human meniscus cells express hypoxia inducible factor-1alpha and increased SOX9 in response to low oxygen tension in cell aggregate culture. Arthritis Res Ther 2007, 9(4):R69. BioMed Central Full Text
  • [41]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2-[delta][delta]CT method. Methods 2001, 25(4):402-408.
  • [42]Scotti C, Osmokrovic A, Wolf F, Miot S, Peretti GM, Barbero A, Martin I: Response of human engineered cartilage based on articular or nasal chondrocytes to interleukin-1beta and low oxygen. Tissue Eng Part A 2012, 18(3–4):362-372.
  • [43]Le Maitre C, Hoyland J, Freemont A: Interleukin-1 receptor antagonist delivered directly and by gene therapy inhibits matrix degradation in the intact degenerate human intervertebral disc: an in situ zymographic and gene therapy study. Arthritis Res Ther 2007, 9(4):R83. BioMed Central Full Text
  • [44]Ortiz LA, Dutreil M, Fattman C, Pandey AC, Torres G, Go K, Phinney DG: Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci USA 2007, 104(26):11002-11007.
  • [45]Candrian C, Bonacina E, Frueh JA, Vonwil D, Dickinson S, Wirz D, Heberer M, Jakob M, Martin I, Barbero A: Intra-individual comparison of human ankle and knee chondrocytes in vitro: relevance for talar cartilage repair. Osteoarthritis Cartilage 2009, 17(4):489-496.
  • [46]Lemke AK, Sandy JD, Voigt H, Dreier R, Lee JH, Grodzinsky AJ, Mentlein R, Fay J, Schunke M, Kurz B: Interleukin-1alpha treatment of meniscal explants stimulates the production and release of aggrecanase-generated, GAG-substituted aggrecan products and also the release of pre-formed, aggrecanase-generated G1 and m-calpain-generated G1-G2. Cell Tissue Res 2010, 340(1):179-188.
  • [47]Chen CZ, Raghunath M: Focus on collagen: in vitro systems to study fibrogenesis and antifibrosis state of the art. Fibrogenesis Tissue Repair 2009, 2:7. BioMed Central Full Text
  • [48]Maier T, Güell M, Serrano L: Correlation of mRNA and protein in complex biological samples. FEBS Lett Syst Biol Nobel Symposium 146 2009, 583(24):3966-3973.
  • [49]Majumdar MK, Wang E, Morris EA: BMP-2 and BMP-9 promotes chondrogenic differentiation of human multipotential mesenchymal cells and overcomes the inhibitory effect of IL-1. J Cell Physiol 2001, 189(3):275-284.
  • [50]Kato Y, Nakashima K, Iwamoto M, Murakami H, Hiranuma H, Koike T, Suzuki F, Fuchihata H, Ikehara Y, Noshiro M: Effects of interleukin-1 on syntheses of alkaline phosphatase, type X collagen, and 1,25-dihydroxyvitamin D3 receptor, and matrix calcification in rabbit chondrocyte cultures. J Clin Invest 1993, 92(5):2323-2330.
  • [51]Sitcheran R, Cogswell PC, Baldwin AS Jr: NF-kappaB mediates inhibition of mesenchymal cell differentiation through a posttranscriptional gene silencing mechanism. Genes Dev 2003, 17(19):2368-2373.
  • [52]Wehling N, Palmer GD, Pilapil C, Liu F, Wells JW, Muller PE, Evans CH, Porter RM: Interleukin-1beta and tumor necrosis factor alpha inhibit chondrogenesis by human mesenchymal stem cells through NF-kappaB-dependent pathways. Arthritis Rheum 2009, 60(3):801-812.
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