Osteoarthritis and Cartilage
Volume 18, Issue 11 , Pages 1477-1486 , November 2010

Adult bone marrow stromal cell-based tissue-engineered aggrecan exhibits ultrastructure and nanomechanical properties superior to native cartilage

  • H.-Y. Lee

      Affiliations

    • Department of Electrical Engineering and Computer Science, Massachusetts Institute of Technology, Cambridge, MA, United States
  • ,
  • P.W. Kopesky

      Affiliations

    • Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, United States
  • ,
  • A. Plaas

      Affiliations

    • Department of Biochemistry, Rush University Medical Center, Chicago, IL, United States
  • ,
  • J. Sandy

      Affiliations

    • Department of Biochemistry, Rush University Medical Center, Chicago, IL, United States
  • ,
  • J. Kisiday

      Affiliations

    • Equine Orthopaedic Research Center, Colorado State University, Fort Collins, CO, United States
  • ,
  • D. Frisbie

      Affiliations

    • Equine Orthopaedic Research Center, Colorado State University, Fort Collins, CO, United States
  • ,
  • A.J. Grodzinsky

      Affiliations

    • Department of Electrical Engineering and Computer Science, Massachusetts Institute of Technology, Cambridge, MA, United States
    • Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, United States
    • Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA, United States
  • ,
  • C. Ortiz

      Affiliations

    • Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, MA, United States
    • Corresponding Author InformationAddress correspondence and reprint requests to: C. Ortiz, Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, MA, United States. Tel: 1-617-452-3084.

Received 21 January 2010 ,Accepted 30 July 2010.

References 

  1. Langer RS, Vacanti JP. Tissue engineering: the challenges ahead. Sci Am. 1999;280(4):86
  2. Chung C, Burdick JA. Engineering cartilage tissue. Adv Drug Deliv Rev. 2008;60(2):243–262
  3. Hunziker EB. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage. 2002;10(6):432–463
  4. Farndale RW, Buttle DJ, Barrett AJ. Improved quantitation and discrimination of sulfated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta. 1986;883173–883177
  5. Hollander AP, Heathfield TF, Webber C, Iwata Y, Bourne R, Rorabeck C, et al. Increased damage to type ii collagen in osteoarthritic articular cartilage detected by a new immunoassay. J Clin Invest. 1994;93(4):1722
  6. Freed LE, Vunjak-Novakovic G. Cultivation of cell-polymer tissue constructs in simulated microgravity. Biotechnol Bioeng. 1995;46(4):306–313
  7. Brown MP, Trumble TN, Sandy JD, Merritt KA. A simplified method of determining synovial fluid chondroitin sulfate chain length. Osteoarthritis Cartilage. 2007;15(12):1443–1445
  8. Calabro A, Midura R, Wang A, West L, Plaas A, Hascall VC. Fluorophore-assisted carbohydrate electrophoresis (FACE) of glycosaminoglycans. Osteoarthritis Cartilage. 2001;916–922
  9. Riesle J, Hollander AP, Langer R, Freed LE, Vunjak-Novakovic G. Collagen in tissue-engineered cartilage: types, structure, and crosslinks. J Cell Biochem. 1998;71(3):313–327
  10. Athanasiou KA, Agarwal A, Dzida FJ. Comparative study of the intrinsic mechanical properties of the human acetabular and femoral head cartilage. J Orthop Res. 1994;12(3):340–349
  11. Frank EH, Jin M, Loening AM, Levenston ME, Grodzinsky AJ. A versatile shear and compression apparatus for mechanical stimulation of tissue culture explants. J Biomech. 2000;33(11):1523–1527
  12. Williamson AK, Chen AC, Sah RL. Compressive properties and function-composition relationships of developing bovine articular cartilage. J Orthop Res. 2001;19(6):1113–1121
  13. Eggli PS, Hunzinker EB, Schenk RK. Quantitation of structural features characterizing weight- and less-weight-bearing regions in articular cartilage: a stereological analysis of medial femoral condyles in young adult rabbits. Anat Rec. 1988;222(3):217–227
  14. Ng L, Grodzinsky AJ, Patwari P, Sandy J, Plaas A, Ortiz C. Individual cartilage aggrecan macromolecules and their constituent glycosaminoglycans visualized via atomic force microscopy. J Struct Biol. 2003;143(3):242–257
  15. Dean D, Han L, Grodzinsky AJ, Ortiz C. Compressive nanomechanics of opposing aggrecan macromolecules. J Biomech. 2006;39(14):2555–2565
  16. Bos KJ, Holmes DF, Kadler KE, McLeod D, Morris NP, Bishop PN. Axial structure of the heterotypic collagen fibrils of vitreous humour and cartilage. J Mol Biol. 2001;306(5):1011–1022
  17. Wenger MPE, Bozec L, Horton MA, Mesquida P. Mechanical properties of collagen fibrils. Biophys J. 2007;93(4):1255–1263
  18. Cowman MK, Li M, Balazs EA. Tapping mode atomic force microscopy of hyaluronan: extended and intramolecularly interacting chains. Biophys J. 1998;75(4):2030–2037
  19. Dudhia J. Aggrecan, aging and assembly in articular cartilage. Cell Mol Life Sci. 2005;62(19):2241–2256
  20. Mauck RL, Yuan X, Tuan RS. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthritis Cartilage. 2006;14(2):179–189
  21. Im GI, Jung NH, Tae SK. Chondrogenic differentiation of mesenchymal stem cells isolated from patients in late adulthood: the optimal conditions of growth factors. Tissue Eng. 2006;12(3):527–536
  22. Connelly JT, Wilson CG, Levenston ME. Characterization of proteoglycan production and processing by chondrocytes and BMSCs in tissue engineered constructs. Osteoarthritis Cartilage. 2008;16(9):1092–1100
  23. Kopesky PW, Lee H-Y, Vanderploeg EJ, Kisiday JD, Frisbie DD, Ortiz C, et al. Adult equine bone-marrow stromal cells produce a cartilage-like ECM mechanically superior to animal-matched adult chondrocytes. Matrix Biol. 2010;29(5):427–438
  24. Erickson IE, Huang AH, Chung C, Li RT, Burdick JA, Mauck RL. Differential maturation and structure-function relationships in mesenchymal stem cell- and chondrocyte-seeded hydrogels. Tissue Eng Part A. 2009;15(5):1041–1052
  25. Scharstuhl A, Schewe B, Benz K, Gaissmaier C, Bühring H-J, Stoop R. Chondrogenic potential of human adult mesenchymal stem cells is independent of age or osteoarthritis etiology. Stem Cells. 2007;25(12):3244–3251
  26. Nöth U, Steinert AF, Tuan RS. Technology insight: adult mesenchymal stem cells for osteoarthritis therapy. Nat Clin Pract Rheumatol. 2008;4(7):371–380
  27. Roughley PJ, White RJ. Age-related changes in the structure of the proteoglycan subunits from human articular cartilage. J Biol Chem. 1980;255(1):217–224
  28. Sheiko SS, Moller M. Visualization of macromolecules: a first step to manipulation and controlled response. Chem Rev. 2001;101(12):4099–4124
  29. Wilbur JL, Kumar A, Biebuyck HA, Kim E, Whitesides GM. Microcontact printing of self-assembled monolayers: applications in microfabrication. Nanotechnology. 1996;7(4):452–457
  30. Bhattacharjee S, Elimelech M. Surface element integration: a novel technique for evaluation of DLVO interaction between a particle and a flat plate. J Colloid Interface Sci. 1997;193(2):273–285
  31. Patwari P, Kurz B, Sandy JD, Grodzinsky AJ. Mannosamine inhibits aggrecanase-mediated changes in the physical properties and biochemical composition of articular cartilage. Arch Biochem Biophys. 2000;374(1):79–85
  32. Nagase H, Kashiwagi M. Aggrecanases and cartilage matrix degradation. Arthritis Res Ther. 2003;5(2):94–103
  33. Oshita H, Sandy JD, Suzuki Kiichi, Akaike A, Bai Y, Sasaki T, et al. Mature bovine articular cartilage contains abundant aggrecan that is c-terminally truncated at Ala719–Ala720, a site which is readily cleaved by m-calpain. Biochem J. 2004;382253–382259
  34. Deutsch AJ, Midura RJ, Plaas AHK. Structure of chondroitin sulfate on aggrecan isolated from bovine tibial and costochondral growth plates. J Orthop Res. 1995;13(2):230–239
  35. Brown MP, West LA, Merritt KA, Plaas AHK. 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;59786–59791
  36. Sandy JD, Verscharen C. Analysis of aggrecan in human knee cartilage and synovial fluid indicates that aggrecanase (adamts) activity is responsible for the catabolic turnover and loss of whole aggrecan whereas other protease activity is required for c-terminal processing in vivo. Biochem J. 2001;358(Pt 3):615
  37. Qureshi HY, Ahmad R, Sylvester J, Zafarullah M. Requirement of phosphatidylinositol 3-kinase/akt signaling pathway for regulation of tissue inhibitor of metalloproteinases-3 gene expression by TGF-β in human chondrocytes. Cell Signal. 2007;19(8):1643–1651
  38. Moulharat N, Lesur C, Thomas M, Rolland-Valognes G, Pastoureau P, Anract P, et al. Effects of transforming growth factor-[beta] on aggrecanase production and proteoglycan degradation by human chondrocytes in vitro. Osteoarthritis Cartilage. 2004;12(4):296–305
  39. Inerot S, Heinegård D, Audell L, Olsson SE. Articular-cartilage proteoglycans in aging and osteoarthritis. Biochem J. 1978;169(1):143
  40. Thonar EJ, Buckwalter JA, Kuettner KE. Maturation-related differences in the structure and composition of proteoglycans synthesized by chondrocytes from bovine articular cartilage. J Biol Chem. 1986;261(5):2467–2474
  41. Plaas AHK, Wong-Palms S, Roughley PJ, Midura RJ, Hascall VC. Chemical and immunological assay of the nonreducing terminal residues of chondroitin sulfate from human aggrecan. J Biol Chem. 1997;272(33):20603–20610
  42. Brown MP, Trumble TN, Plaas AHK, Sandy JD, Romano M, Hernandez J, et al. Exercise and injury increase chondroitin sulfate chain length and decrease hyaluronan chain length in synovial fluid. Osteoarthritis Cartilage. 2007;15(11):1318–1325
  43. Carney SL, Billingham MEJ, Muir H, Sandy JD. Structure of newly synthesised (35s)-proteoglycans and (35s)-proteoglycan turnover products of cartilage explant cultures from dogs with experimental osteoarthritis. J Orthop Res. 1985;3(2):140–147
  44. Midura RJ, Calabro A, Yanagishita M, Hascall VC. Nonreducing end structures of chondroitin sulfate chains on aggrecan isolated from swarm rat chondrosarcoma cultures. J Biol Chem. 1995;270(14):8009
  45. Hascall VC, Midura RJ, Sorrell JM, Plaas AH. Immunology of chondroitin/dermatan sulfate. Adv Exp Med Biol. 1995;376205
  46. Maroudas A, Muir H, Wingham J. The correlation of fixed negative charge with glycosaminoglycan content of human articular cartilage. Biochim Biophys Acta. 1969;177(3):492
  47. Buschmann MD, Grodzinsky AJ. A molecular model of proteoglycan-associated electrostatic forces in cartilage mechanics. J Biomech Eng. 1995;117(2):179–192
  48. Lee H-Y, Han L, Daher L, Bonaparte R, Roughley PJ, Ortiz C, et al. Age-related Changes in Human Aggrecan Molecular Structure and its Nanomechanical Properties. In: Trans. 54th Orthop Res Soc, San Francisco, 2008.

PII: S1063-4584(10)00253-0

doi: 10.1016/j.joca.2010.07.015

Osteoarthritis and Cartilage
Volume 18, Issue 11 , Pages 1477-1486 , November 2010