RESEARCH ARTICLE
A comparison study of different decellularization treatments on bovine articular cartilage
Toktam Ghassemi,
Nasser Saghatoleslami,
Nasser Mahdavi-Shahri,
Maryam M. Matin,
Reza Gheshlaghi,
Ali Moradi,
Toktam Ghassemi
Department of Chemical Engineering, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorNasser Saghatoleslami
Department of Chemical Engineering, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorNasser Mahdavi-Shahri
Department of Biology, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorMaryam M. Matin
Department of Biology, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorReza Gheshlaghi
Department of Chemical Engineering, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorCorresponding Author
Ali Moradi
Orthopedic Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
Correspondence
Ali Moradi, Bone and Joint Research Lab, Library Building, Ghaem Hospital, Shariati Square, Mashhad, Iran.
Email: [email protected]
Search for more papers by this authorToktam Ghassemi,
Nasser Saghatoleslami,
Nasser Mahdavi-Shahri,
Maryam M. Matin,
Reza Gheshlaghi,
Ali Moradi,
Toktam Ghassemi
Department of Chemical Engineering, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorNasser Saghatoleslami
Department of Chemical Engineering, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorNasser Mahdavi-Shahri
Department of Biology, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorMaryam M. Matin
Department of Biology, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorReza Gheshlaghi
Department of Chemical Engineering, Ferdowsi University of Mashhad (FUM), Mashhad, Iran
Search for more papers by this authorCorresponding Author
Ali Moradi
Orthopedic Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
Correspondence
Ali Moradi, Bone and Joint Research Lab, Library Building, Ghaem Hospital, Shariati Square, Mashhad, Iran.
Email: [email protected]
Search for more papers by this authorAbstract
Previous researches have emphasized on suitability of decellularized tissues for regenerative applications. The decellularization of cartilage tissue has always been a challenge as the final product must be balanced in both immunogenic residue and mechanical properties. This study was designed to compare and optimize the efficacy of the most common chemical decellularization treatments on articular cartilage. Freeze/thaw cycles, trypsin, ethylenediaminetetraacetic acid (EDTA), sodium dodecyl sulfate (SDS), and Triton-X 100 were used at various concentrations and time durations for decellularization of bovine distal femoral joint cartilage samples. Histological staining, scanning electron microscopy, DNA quantification, compressive strength test, and Fourier-transform infrared spectroscopy were performed for evaluation of the decellularized cartilage samples. Treatment with 0.05% trypsin/EDTA for 1 day followed by 3% SDS for 2 days and 3% Triton X-100 for another 2 days resulted in significant reduction in DNA content and simultaneous maintenance of mechanical properties. Seeding the human adipose-derived stem cells onto the decellularized cartilage confirmed its biocompatibility. According to our findings, an optimized physiochemical decellularization method can yield in a nonimmunogenic biomechanically compatible decellularized tissue for cartilage regeneration application.
CONFLICT OF INTEREST
The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.
REFERENCES
- Arai, S., & Orton, E. C. (2009). Immunoblot detection of soluble protein antigens from sodium dodecyl sulfate-and sodium deoxycholate-treated candidate bioscaffold tissues. The Journal of Heart Valve Disease, 18, 439–443.
- Badylak, S. F. (2007). The extracellular matrix as a biologic scaffold material. Biomaterials, 28, 3587–3593.
- Badylak, S. F., Freytes, D. O., & Gilbert, T. W. (2009). Extracellular matrix as a biological scaffold material: Structure and function. Acta Biomaterialia, 5, 1–13. https://doi.org/10.1016/j.actbio.2008.09.013
- Bahrami, A. R., Ebrahimi, M., Matin, M. M., Neshati, Z., Almohaddesin, M. R., Aghdami, N., & Bidkhori, H. R. (2011). Comparative analysis of chemokine receptor's expression in mesenchymal stem cells derived from human bone marrow and adipose tissue. Journal of Molecular Neuroscience, 44, 178–185.
- Benders, K., Boot, W., Cokelaere, S., Van Weeren, P., Gawlitta, D., Bergman, H., … Malda, J. (2014). Multipotent stromal cells outperform chondrocytes on cartilage-derived matrix scaffolds. Cartilage, 5, 221–230. https://doi.org/10.1177/1947603514535245
- Benders, K. E. M., Boot, W., Cokelaere, S. M., Weeren, P. R. V., Gawlitta, D., Bergman, H. J., … Malda, J. (2014). Multipotent stromal cells outperform chondrocytes on cartilage-derived matrix scaffolds. Cartilage, 5(4), 1–10.
- Bijlsma, J. W., Berenbaum, F., & Lafeber, F. P. (2011). Osteoarthritis: An update with relevance for clinical practice. The Lancet, 377, 2115–2126. https://doi.org/10.1016/S0140-6736(11)60243-2
- Blanco, F. J., & Ruiz-Romero, C. (2012). Osteoarthritis: Metabolomic characterization of metabolic phenotypes in OA. Nature Reviews Rheumatology, 8, 130–132. https://doi.org/10.1038/nrrheum.2012.11
- Chang, C.-H., Chen, C.-C., Liao, C.-H., Lin, F.-H., Hsu, Y.-M., & Fang, H.-W. (2014). Human acellular cartilage matrix powders as a biological scaffold for cartilage tissue engineering with synovium-derived mesenchymal stem cells. Biomedical Materials Research, 102A, 2248–2257.
- Conaghan, P. G. (2013). Osteoarthritis in 2012: Parallel evolution of OA phenotypes and therapies. Nature Reviews Rheumatology, 9, 68–70. https://doi.org/10.1038/nrrheum.2012.225
- Crapo, P. M., Gilbert, T. W., & Badylak, S. F. (2011). An overview of tissue and whole organ decellularization processes. Biomaterials, 32, 3233–3243.
- Elder, B. D., Eleswarapu, S. V., & Athanasiou, K. A. (2009). Extraction techniques for the decellularization of tissue engineered articular cartilage constructs. Biomaterials, 30, 3749–3756.
- Gilbert, T. W. (2012). Strategies for tissue and organ decellularization. Cell Biochemistry, 113, 2217–2222.
- Gilbert, T. W., Sellaro, T. L., & Badylak, S. F. (2006). Decellularization of tissues and organs. Biomaterials, 27, 3675–3683.
- Gong, Y. Y., Xue, J. X., Zhang, W. J., Zhou, G. D., Liu, W., & Cao, Y. (2011). A sandwich model for engineering cartilage with acellular cartilage sheets and chondrocytes. Biomaterials, 32, 2265–2273.
- Graham, M. E., Gratzer, P. F., Bezuhly, M., & Hong, P. (2016). Development and characterization of decellularized human nasoseptal cartilage matrix for use in tissue engineering. The Laryngoscope, 126, 2226–2231. https://doi.org/10.1002/lary.25884
- Grefrath, S. P., & Reynolds, J. A. (1974). The molecular weight of the major glycoprotein from the human erythrocyte membrane. Proceedings of the National Academy of Sciences, 71, 3913–3916.
- Henrotin, Y. (2014). Does signaling pathway inhibition hold therapeutic promise for osteoarthritis? Joint, Bone, Spine, 81, 281–283. https://doi.org/10.1016/j.jbspin.2014.03.002
- Im, O., Li, J., Wang, M., Zhang, L. G., & Keidar, M. (2012). Biomimetic three-dimensional nanocrystalline hydroxyapatite and magnetically synthesized single-walled carbon nanotube chitosan nanocomposite for bone regeneration. International Journal of Nanomedicine, 7, 2087–2099.
- Izadifar, Z., Chen, X., & Kulyk, W. (2012). Strategic design and fabrication of engineered scaffolds for articular cartilage repair. Journal of Functional Biomaterials, 3, 799–838. https://doi.org/10.3390/jfb3040799
- Jia, S., Liu, L., Pan, W., Meng, G., Duan, C., Zhang, L., … Liu, J. (2012). Oriented cartilage extracellular matrix-derived scaffold for cartilage tissue engineering. Bioscience and Bioengineering, 113, 647–653. https://doi.org/10.1016/j.jbiosc.2011.12.009
- Jorge-Herrero, E., Fernandez, P., De la Tone, N., Escudero, C., Garcia-Paez, J., Bujan, J., & Castillo-Olivares, J. (1994). Inhibition of the calcification of porcine valve tissue by selective lipid removal. Biomaterials, 15, 815–820. https://doi.org/10.1016/0142-9612(94)90036-1
- Kang, H., Peng, J., Lu, S., Liu, S., Zhang, L., Huang, J., … Guo, Q. (2014). In vivo cartilage repair using adipose-derived stem cell-loaded decellularized cartilage ECM scaffolds. Tissue Engineering and Regenerative Medicine, 8, 442–453. https://doi.org/10.1002/term.1538
- Kawazoye, S., Tian, S.-F., Toda, S., Takashima, T., Sunaga, T., Fujitani, N., … Matsumura, S. (1995). The mechanism of interaction of sodium dodecyl sulfate with elastic fibers. Journal of Biochemistry, 117, 1254–1260. https://doi.org/10.1093/oxfordjournals.jbchem.a124852
- Kheir, E., Stapleton, T., Shaw, D., Jin, Z., Fisher, J., & Ingham, E. (2011). Development and characterization of an acellular porcine cartilage bone matrix for use in tissue engineering. Biomedical Materials Research, 99A, 283–294. https://doi.org/10.1002/jbm.a.33171
- Knight, R., Wilcox, H., Korossis, S., Fisher, J., & INgham, E. (2008). The use of acellular matrices for the tissue engineering of cardiac valves. Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine, 222, 129–143.
- Luo, L., Eswaramoorthy, R., Mulhall, K. J., & Kelly, D. J. (2016). Decellularization of porcine articular cartilage explants and their subsequent repopulation with human chondroprogenitor cells. The Mechanical Behavior of Biomedical Materials, 55, 21–31.
- Manek, N. J., & Lane, N. E. (2000). Osteoarthritis: Current concepts in diagnosis and management. American Family Physician, 61, 1795–1804.
- Marcacci, M., Filardo, G., & Kon, E. (2013). Treatment of cartilage lesions: What works and why? Injury, 44, S11–S15. https://doi.org/10.1016/S0020-1383(13)70004-4
- Mendoza-Novelo, B., & Cauich-Rodríguez, J. V. (2011). Decellularization, stabilization and functionalization of collagenous tissues used as cardiovascular biomaterials. London, UK: INTECH Open Access Publisher. https://doi.org/10.5772/25184
10.5772/25184 Google Scholar
- Moore, M., Sarntinoranont, M., & Mcfetridge, P. (2012). Mass transfer trends occurring in engineered ex vivo tissue scaffolds. NIH, 100A, 2194–2203. https://doi.org/10.1002/jbm.a.34092
- Moradi, A. 2015. Development of bovine cartilage extracellular matrix as a potential scaffold for chondrogenic induction of human dermal fibroblasts.pdf>. PhD, University of Malaya.
- Moradi, A., Ataollahi, F., Sayar, K., Pramanik, S., Chong, P. P., Khalil, A. A., … Pingguan-Murphy, B. (2016). Chondrogenic potential of physically treated bovine cartilage matrix derived porous scaffolds on human dermal fibroblast cells. Journal of Biomedical Materials Research Part A, 104, 243–254.
- Moradi, A., Pramanik, S., Ataollahi, F., Abdul-Khalil, A., Kamarul, T., & Pingguan-Murphy, B. (2014). A comparison study of different physical treatments on cartilage matrix derived porous scaffolds for tissue engineering applications. Science and Technology of Advanced Materials, 15, 065001. https://doi.org/10.1088/1468-6996/15/6/065001
- Moradi, A., Pramanik, S., Ataollahi, F., Khalil, A. A., Kamarul, T., & Pingguan-Murphy, B. (2014). A comparison study of different physical treatments on cartilage matrix derived porous scaffolds for tissue engineering applications. Science and Technology of Advanced Materials, 15, 1–12.
- Muir, H. (1980). The chemistry of the ground substance of joint cartilage. The joints and synovial fluid, 2, 27–94.
10.1016/B978-0-12-655102-0.50008-4 Google Scholar
- Peretti, G. M., Randolph, M. A., Villa, M. T., Buragas, M. S., & Yaremchuk, M. J. (2000). Cell-based tissue-engineered allogeneic implant for cartilage repair. Tissue Engineering, 6, 567–576. https://doi.org/10.1089/107632700750022206
- Platt, J. L., Fischel, R. J., Matas, A. J., Reif, S. A., Bolman, R. M., & Bach, F. H. (1991). Immunopathology of hyperacute xenograft rejection in a swine-to-primate model. Transplantation, 52, 214–220. https://doi.org/10.1097/00007890-199108000-00006
- Redman, S. N., Oldfield, S. F., & Archer, C. W. (2005). Current strategies for articular cartilage repair. European Cells & Materials, 9, 23–32. https://doi.org/10.22203/eCM.v009a04
- Reing, J. E., Brown, B. N., Daly, K. A., Freund, J. M., Gilbert, T. W., Hsiong, S. X., … Wolf, M. T. (2010). The effects of processing methods upon mechanical and biologic properties of porcine dermal extracellular matrix scaffolds. Biomaterials, 31, 8626–8633.
- Rémi, E., Meddahi-Pelle, A., Roques, C., Letourneur, D., Lansac, E., Medjahed-Hamidi, F., … Khelil, N. (2011). Pericardial processing: Challenges, outcomes and future prospects. London, UK: INTECH Open Access Publisher.
- Rowland, C. R., Colucci, L. A., & Guilak, F. (2016). Fabrication of anatomically-shaped cartilage constructs using decellularized cartilage-derived matrix scaffolds. Biomaterials, 91, 57–72.
- Saarakkala, S., Rieppo, L., Rieppo, J., & Jurvelin, J. S. (2010). Fourier transform infrared (FTIR) microspectroscopy of immature, mature and degenerated articular cartilage. Microscopy: Science, Technology, Applications and Education, 1, 403–414.
- Schmitz, N., Laverty, S., Kraus, V., & Aigner, T. (2010). Basic methods in histopathology of joint tissues. Osteoarthritis and Cartilage, 18, S113–S116. https://doi.org/10.1016/j.joca.2010.05.026
- Schwarz, S., Koerber, L., Elsaesser, A. F., Goldberg-Bockhorn, E., Seitz, A. M., Dürselen, L., … Rotter, N. (2012). Decellularized cartilage matrix as a novel biomatrix for cartilage tissue-engineering applications. Tissue Engineering Part A, 18, 2195–2209.
- Sutherland, A. J., Beck, E. C., Dennis, S. C., Converse, G. L., Hopkins, R. A., Berkland, C. J., & Detamore, M. S. (2015). Decellularized cartilage may be a chondroinductive material for osteochondral tissue engineering. PLoS ONE, 10(5), e0121966.
- Sutherland, A. J., Converse, G. L., Hopkins, R. A., & Detamore, M. S. (2015). The bioactivity of cartilage extracellular matrix in articular cartilage regeneration. Advanced Healthcare Materials, 4, 29–39. https://doi.org/10.1002/adhm.201400165
- Toolan, B. C., Frenkel, S. R., Pereira, D. S., & Alexander, H. (1998). Development of a novel osteochondral graft for cartilage repair. Biomedical Materials Research, 41, 244–250.
10.1002/(SICI)1097-4636(199808)41:2<244::AID-JBM9>3.0.CO;2-I CAS PubMed Web of Science® Google Scholar
- Valiani, A., Hashemibeni, B., Esfandiary, E., Ansar, M. M., Kazemi, M., & Esmaeili, N. (2014). Study of carbon nano-tubes effects on the chondrogenesis of human adipose derived stem cells in alginate scaffold. International Journal of Preventive Medicine, 5(7), 825–834.
- Yang, Q., Peng, J., Guo, Q., Huang, J., Zhang, L., Yao, J., … Lu, S. (2008). A Cartilage ECM-derived 3-D porous acellular matrix scaffold for in vivo cartilage tissue engineering with PKH26-labeled chondrogenic bone marrow-derived mesenchymal stem cells. Biomaterials, 29, 2378–2387. https://doi.org/10.1016/j.biomaterials.2008.01.037
- Yang, Z., Shi, Y., Wei, X., He, J., Yang, S., Dickson, G., … Li, G. (2010). Fabrication and repair of cartilage defects with a novel acellular cartilage matrix scaffold. Tissue Engineering, 16, 865–876. https://doi.org/10.1089/ten.tec.2009.0444
- Zheng, X., Lu, S., Zhang, W., Liu, S., Huang, J., & Guo, Q. (2011). Mesenchymal stem cells on a decellularized cartilage matrix for cartilage tissue engineering. Biotechnology and Bioprocess Engineering, 16, 593–602. https://doi.org/10.1007/s12257-010-0348-9
