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Research articlesUse of adipose stem cells and polylactide discs for tissue engineering of the temporomandibular joint disc
Published:27 May 2009https://doi.org/10.1098/rsif.2009.0117
Abstract
There is currently no suitable replacement for damaged temporomandibular joint (TMJ) discs after discectomy. In the present study, we fabricated bilayer biodegradable polylactide (PLA) discs comprising a non-woven mat of poly(L/D)lactide (P(L/D)LA) 96/4 and a P(L/DL)LA 70/30 membrane plate. The PLA disc was examined in combination with adipose stem cells (ASCs) for tissue engineering of the fibrocartilaginous TMJ disc in vitro. ASCs were cultured in parallel in control and chondrogenic medium for a maximum of six weeks. Relative expression of the genes, aggrecan, type I collagen and type II collagen present in the TMJ disc extracellular matrix increased in the ASC-seeded PLA discs in the chondrogenic medium. The hypertrophic marker, type X collagen, was moderately induced. Alcian blue staining showed accumulation of sulphated glycosaminoglycans. ASC differentiation in the PLA discs was close to that observed in pellet cultures. Comparison of the mRNA levels revealed that the degree of ASC differentiation was lower than that in TMJ disc-derived cells and tissue. The pellet format supported the phenotype of the TMJ disc-derived cells under chondrogenic conditions and also enhanced their hyalinization potential, which is considered part of the TMJ disc degeneration process. Accordingly, the combination of ASCs and PLA discs has potential for the development of a tissue-engineered TMJ disc replacement.
References
Ali A. M.& Sharawy M. . 1996aHistochemical and immunohistochemical studies of the effects of experimental anterior disc displacement on sulfated glycosaminoglycans, hyaluronic acid, and link protein of the rabbit craniomandibular joint. J. Oral Maxillofac. Surg. 54, 992–1004. (doi:10.1016/S0278-2391(96)90399-7). Crossref, PubMed, ISI, Google ScholarAli A. M.& Sharawy M. M. . 1996bAn immunohistochemical study of collagen types III, VI and IX in rabbit craniomandibular joint tissues following surgical induction of anterior disk displacement. J. Oral Pathol. Med. 25, 78–85. (doi:10.1111/j.1600-0714.1996.tb00197.x). Crossref, PubMed, ISI, Google ScholarAllen K. D.& Athanasiou K. A. . 2006Growth factor effects on passaged TMJ disk cells in monolayer and pellet cultures. Orthod. Craniofac. Res. 9, 143–152. (doi:10.1111/j.1601-6343.2006.00370.x). Crossref, PubMed, Google ScholarAllen K. D.& Athanasiou K. A. . 2007Effect of passage and topography on gene expression of temporomandibular joint disc cells. Tissue Eng. 13, 101–110. (doi:10.1089/ten.2006.0094). Crossref, PubMed, Google ScholarAllen K. D.& Athanasiou K. A. . 2008Scaffold and growth factor selection in temporomandibular joint disc engineering. J. Dent. Res. 87, 180–185. (doi:10.1177/154405910808700205). Crossref, PubMed, ISI, Google ScholarAlmarza A. J.& Athanasiou K. A. . 2004aDesign characteristics for the tissue engineering of cartilaginous tissues. Ann. Biomed. Eng. 32, 2–17. (doi:10.1023/B:ABME.0000007786.37957.65). Crossref, PubMed, ISI, Google ScholarAlmarza A. J.& Athanasiou K. A. . 2004bSeeding techniques and scaffolding choice for tissue engineering of the temporomandibular joint disk. Tissue Eng. 10, 1787–1795. (doi:10.1089/ten.2004.10.1787). Crossref, PubMed, Google ScholarAlmarza A. J.& Athanasiou K. A. . 2005Effects of initial cell seeding density for the tissue engineering of the temporomandibular joint disc. Ann. Biomed. Eng. 33, 943–950. (doi:10.1007/s10439-005-3311-8). Crossref, PubMed, ISI, Google ScholarAwad H. A., Halvorsen Y. D., Gimble J. M.& Guilak F. . 2003Effects of transforming growth factor beta1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng. 9, 1301–1312. (doi:10.1089/10763270360728215). Crossref, PubMed, Google ScholarBallock R. T.& Reddi A. H. . 1994Thyroxine is the serum factor that regulates morphogenesis of columnar cartilage from isolated chondrocytes in chemically defined medium. J. Cell Biol. 126, 1311–1318. (doi:10.1083/jcb.126.5.1311). Crossref, PubMed, ISI, Google ScholarBerkovitz B. K. . 2000Crimping of collagen in the intra-articular disc of the temporomandibular joint: a comparative study. J. Oral Rehabil. 27, 608–613. (doi:10.1046/j.1365-2842.2000.00605.x). Crossref, PubMed, ISI, Google ScholarBerkovitz B. K.& Pacy J. . 2000Age changes in the cells of the intra-articular disc of the temporomandibular joints of rats and marmosets. Arch. Oral Biol. 45, 987–995. (doi:10.1016/S0003-9969(00)00067-4). Crossref, PubMed, ISI, Google ScholarDeLise A. M., Fischer L.& Tuan R. S. . 2000Cellular interactions and signaling in cartilage development. Osteoarthritis Cartilage 8, 309–334. (doi:10.1053/joca.1999.0306). Crossref, PubMed, ISI, Google ScholarDenker A. E., Nicoll S. B.& Tuan R. S. . 1995Formation of cartilage-like spheroids by micromass cultures of murine C3H10T1/2 cells upon treatment with transforming growth factor-beta 1. Differentiation 59, 25–34. (doi:10.1046/j.1432-0436.1995.5910025.x). Crossref, PubMed, ISI, Google ScholarDetamore M. S.& Athanasiou K. A. . 2003Motivation, characterization, and strategy for tissue engineering the temporomandibular joint disc. Tissue Eng. 9, 1065–1087. (doi:10.1089/10763270360727991). Crossref, PubMed, Google ScholarDetamore M. S.& Athanasiou K. A. . 2004Effects of growth factors on temporomandibular joint disc cells. Arch. Oral Biol. 49, 577–583. (doi:10.1016/j.archoralbio.2004.01.015). Crossref, PubMed, ISI, Google ScholarDetamore M. S., Orfanos J. G., Almarza A. J., French M. M., Wong M. E.& Athanasiou K. A. . 2005Quantitative analysis and comparative regional investigation of the extracellular matrix of the porcine temporomandibular joint disc. Matrix Biol. 24, 45–57. Crossref, PubMed, ISI, Google ScholarDetamore M. S., Hegde J. N., Wagle R. R., Almarza A. J., Montufar-Solis D., Duke P. J.& Athanasiou K. A. . 2006Cell type and distribution in the porcine temporomandibular joint disc. J. Oral Maxillofac. Surg. 64, 243–248. (doi:10.1016/j.joms.2005.10.009). Crossref, PubMed, ISI, Google ScholarDimitroulis G. . 2005The use of dermis grafts after discectomy for internal derangement of the temporomandibular joint. J. Oral Maxillofac. Surg. 63, 173–178. (doi:10.1016/j.joms.2004.06.051). Crossref, PubMed, ISI, Google ScholarDolwick M. F. . 1997The role of temporomandibular joint surgery in the treatment of patients with internal derangement. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 83, 150–155. (doi:10.1016/S1079-2104(97)90106-2). Crossref, PubMed, Google ScholarErickson G. R., Gimble J. M., Franklin D. M., Rice H. E., Awad H.& Guilak F. . 2002Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem. Biophys. Res. Commun. 290, 763–769. (doi:10.1006/bbrc.2001.6270). Crossref, PubMed, ISI, Google ScholarEriksson L.& Westesson P. L. . 1992Temporomandibular joint diskectomy. No positive effect of temporary silicone implant in a 5-year follow-up. Oral Surg. Oral Med. Oral Pathol. 74, 259–272. (doi:10.1016/0030-4220(92)90056-V). Crossref, PubMed, Google ScholarEriksson L.& Westesson P. L. . 2001Discectomy as an effective treatment for painful temporomandibular joint internal derangement: a 5-year clinical and radiographic follow-up. J. Oral Maxillofac. Surg. 59, 750–758. Discussion 758-9. (doi:10.1053/joms.2001.24288). Crossref, PubMed, ISI, Google ScholarEstabrooks L. N., Fairbanks C. E., Collett R. J.& Miller L. . 1990A retrospective evaluation of 301 TMJ Proplast-Teflon implants. Oral Surg. Oral Med. Oral Pathol. 70, 381–386. (doi:10.1016/0030-4220(90)90164-N). Crossref, PubMed, Google ScholarEstes B. T., Wu A. W.& Guilak F. . 2006Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthritis Rheum. 54, 1222–1232. (doi:10.1002/art.21779). Crossref, PubMed, Google ScholarFeinberg S. E.& McDonnell E. J. . 1995The use of a collagen sheet as a disc replacement in the rabbit temporomandibular joint. J. Oral Maxillofac. Surg. 53, 535–542. Discussion 543. (doi:10.1016/0278-2391(95)90066-7). Crossref, PubMed, ISI, Google ScholarFollmar K. E., Decroos F. C., Prichard H. L., Wang H. T., Erdmann D.& Olbrich K. C. . 2006Effects of glutamine, glucose, and oxygen concentration on the metabolism and proliferation of rabbit adipose-derived stem cells. Tissue Eng. 12, 3525–3533. (doi:10.1089/ten.2006.12.3525). Crossref, PubMed, Google ScholarFreed L. E., Marquis J. C., Nohria A., Emmanual J., Mikos A. G.& Langer R. . 1993Neocartilage formation in vitro and in vivo using cells cultured on synthetic biodegradable polymers. J. Biomed. Mater. Res. 27, 11–23. (doi:10.1002/jbm.820270104). Crossref, PubMed, ISI, Google ScholarGirdler N. M. . 1998In vitro synthesis and characterization of a cartilaginous meniscus grown from isolated temporomandibular chondroprogenitor cells. Scand. J. Rheumatol. 27, 446–453. (doi:10.1080/030097498442280). Crossref, PubMed, ISI, Google ScholarHennig T., Lorenz H., Thiel A., Goetzke K., Dickhut A., Geiger F.& Richter W. . 2007Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFbeta receptor and BMP profile and is overcome by BMP-6. J. Cell. Physiol. 211, 682–691. (doi:10.1002/jcp.20977). Crossref, PubMed, ISI, Google ScholarHuang J. I., Zuk P. A., Jones N. F., Zhu M., Lorenz H. P., Hedrick M. H.& Benhaim P. . 2004Chondrogenic potential of multipotential cells from human adipose tissue. Plast. Reconstr. Surg. 113, 585–594. (doi:10.1097/01.PRS.0000101063.27008.E1). Crossref, PubMed, ISI, Google ScholarJohns D. E.& Athanasiou K. A. . 2007Improving culture conditions for temporomandibular joint disc tissue engineering. Cells Tissues Organs 185, 246–257. (doi:10.1159/000102173). Crossref, PubMed, ISI, Google ScholarKurita K., Westesson P. L., Sternby N. H., Eriksson L., Carlsson L. E., Lundh H.& Toremalm N. G. . 1989Histologic features of the temporomandibular joint disk and posterior disk attachment: comparison of symptom-free persons with normally positioned disks and patients with internal derangement. Oral Surg. Oral Med. Oral Pathol. 67, 635–643. (doi:10.1016/0030-4220(89)90001-7). Crossref, PubMed, Google ScholarLandesberg R., Takeuchi E.& Puzas J. E. . 1996Cellular, biochemical and molecular characterization of the bovine temporomandibular joint disc. Arch. Oral Biol. 41, 761–767. (doi:10.1016/S0003-9969(96)00068-4). Crossref, PubMed, ISI, Google ScholarLi W. J., Tuli R., Okafor C., Derfoul A., Danielson K. G., Hall D. J.& Tuan R. S. . 2005A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials 26, 599–609. (doi:10.1016/j.biomaterials.2004.03.005). Crossref, PubMed, ISI, Google ScholarMercuri L. G.& Giobbie-Hurder A. . 2004Long-term outcomes after total alloplastic temporomandibular joint reconstruction following exposure to failed materials. J. Oral Maxillofac. Surg. 62, 1088–1096. (doi:10.1016/j.joms.2003.10.012). Crossref, PubMed, ISI, Google ScholarMercuri L. G., Edibam N. R.& Giobbie-Hurder A. . 2007Fourteen-year follow-up of a patient-fitted total temporomandibular joint reconstruction system. J. Oral Maxillofac. Surg. 65, 1140–1148. (doi:10.1016/j.joms.2006.10.006). Crossref, PubMed, ISI, Google ScholarMills D. K., Fiandaca D. J.& Scapino R. P. . 1994Morphologic, microscopic, and immunohistochemical investigations into the function of the primate TMJ disc. J. Orofac. Pain 8, 136–154. PubMed, Google ScholarMinarelli A. M.& Liberti E. A. . 1997A microscopic survey of the human temporomandibular joint disc. J. Oral Rehabil. 24, 835–840. (doi:10.1046/j.1365-2842.1997.00595.x). Crossref, PubMed, ISI, Google ScholarNakano T.& Scott P. G. . 1989A quantitative chemical study of glycosaminoglycans in the articular disc of the bovine temporomandibular joint. Arch. Oral Biol. 34, 749–757. (doi:10.1016/0003-9969(89)90082-4). Crossref, PubMed, ISI, Google ScholarNakano T.& Scott P. G. . 1996Changes in the chemical composition of the bovine temporomandibular joint disc with age. Arch. Oral Biol. 41, 845–853. (doi:10.1016/S0003-9969(96)00040-4). Crossref, PubMed, ISI, Google ScholarPfaffl M. W. . 2001A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45. (doi:10.1093/nar/29.9.e45). Crossref, PubMed, ISI, Google ScholarPuelacher W. C., Wisser J., Vacanti C. A., Ferraro N. F., Jaramillo D.& Vacanti J. P. . 1994Temporomandibular joint disc replacement made by tissue-engineered growth of cartilage. J. Oral Maxillofac. Surg. 52, 1172–1177. Discussion 1177–8. (doi:10.1016/0278-2391(94)90538-X). Crossref, PubMed, ISI, Google ScholarRichardson S. M., Curran J. M., Chen R., Vaughan-Thomas A., Hunt J. A., Freemont A. J.& Hoyland J. A. . 2006The differentiation of bone marrow mesenchymal stem cells into chondrocyte-like cells on poly-l-lactic acid (PLLA) scaffolds. Biomaterials 27, 4069–4078. (doi:10.1016/j.biomaterials.2006.03.017). Crossref, PubMed, ISI, Google ScholarRoelen B. A.& Dijke P. . 2003Controlling mesenchymal stem cell differentiation by TGFbeta family members. J. Orthop. Sci. 8, 740–748. (doi:10.1007/s00776-003-0702-2). Crossref, PubMed, Google ScholarRucklidge G. J., Milne G.& Robins S. P. . 1996Collagen type X: a component of the surface of normal human, pig, and rat articular cartilage. Biochem. Biophys. Res. Commun. 224, 297–302. (doi:10.1006/bbrc.1996.1024). Crossref, PubMed, ISI, Google ScholarScapino R. P., Obrez A.& Greising D. . 2006Organization and function of the collagen fiber system in the human temporomandibular joint disk and its attachments. Cells Tissues Organs 182, 201–225. (doi:10.1159/000093969). Crossref, PubMed, ISI, Google ScholarSpringer I. N., Fleiner B., Jepsen S.& Acil Y. . 2001Culture of cells gained from temporomandibular joint cartilage on non-absorbable scaffolds. Biomaterials 22, 2569–2577. (doi:10.1016/S0142-9612(01)00148-X). Crossref, PubMed, ISI, Google ScholarTacchetti C., Tavella S., Dozin B., Quarto R., Robino G.& Cancedda R. . 1992Cell condensation in chondrogenic differentiation. Exp. Cell Res. 200, 26–33. (doi:10.1016/S0014-4827(05)80067-9). Crossref, PubMed, ISI, Google ScholarTanaka E., Detamore M. S., Tanimoto K.& Kawai N. . 2008Lubrication of the temporomandibular joint. Ann. Biomed Eng. 36, 14–29. (doi:10.1007/s10439-007-9401-z). Crossref, PubMed, ISI, Google ScholarThomas M., Grande D.& Haug R. H. . 1991Development of an in vitro temporomandibular joint cartilage analog. J. Oral Maxillofac. Surg. 49, 854–856. Discussion 857. (doi:10.1016/0278-2391(91)90015-E). Crossref, PubMed, ISI, Google ScholarTucker M. R.& Spagnoli D. B. . 1996Autogenous dermal and auricular cartilage grafts for temporomandibular joint repair. Atlas Oral Maxillofac. Surg. Clin. North Am. 4, 75–92. Crossref, PubMed, Google ScholarWang Y., Kim U. J., Blasioli D. J., Kim H. J.& Kaplan D. L. . 2005In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells. Biomaterials 26, 7082–7094. (doi:10.1016/j.biomaterials.2005.05.022). Crossref, PubMed, ISI, Google ScholarZuk P. A., Zhu M., Mizuno H., Huang J., Futrell J. W., Katz A. J., Benhaim P., Lorenz H. P.& Hedrick M. H. . 2001Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7, 211–228. (doi:10.1089/107632701300062859). Crossref, PubMed, Google Scholar
