Skip to main content
SpringerLink
Log in

Harnessing Cell–Biomaterial Interactions for Osteochondral Tissue Regeneration

  • Chapter
  • First Online:
Tissue Engineering III: Cell - Surface Interactions for Tissue Culture

Part of the book series: Advances in Biochemical Engineering Biotechnology ((ABE,volume 126))

Abstract

Articular cartilage that is damaged or diseased often requires surgical intervention to repair the tissue; therefore, tissue engineering strategies have been developed to aid in cartilage regeneration. Tissue engineering approaches often require the integration of cells, biomaterials, and growth factors to direct and support tissue formation. A variety of cell types have been isolated from adipose, bone marrow, muscle, and skin tissue to promote cartilage regeneration. The interaction of cells with each other and with their surrounding environment has been shown to play a key role in cartilage engineering. In tissue engineering approaches, biomaterials are commonly used to provide an initial framework for cell recruitment and proliferation and tissue formation. Modifications of the properties of biomaterials, such as creating sites for cell binding, altering their physicochemical characteristics, and regulating the delivery of growth factors, can have a significant influence on chondrogenesis. Overall, the goal is to completely restore healthy cartilage within an articular cartilage defect. This chapter aims to provide information about the importance of cell–biomaterial interactions for the chondrogenic differentiation of various cell populations that can eventually produce functional cartilage matrix that is indicative of healthy cartilage tissue.

Graphical Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ADSC:

Adipose-derived stem cell

BMP:

Bone morphogenetic protein

CS:

Chondroitin sulfate

EB:

Embryoid body

ECM:

Extracellular matrix

ESC:

Embryonic stem cell

FGF:

Fibroblast growth factor

HA:

Hyaluronic acid

hDF:

Human dermal fibroblast

GAG:

Glycosaminoglycan

GMP:

Gelatin microparticle

IGF:

Insulin-like growth factor

MDSC:

Muscle-derived stem cell

MMP:

Matrix metalloproteinase

MSC:

Mesenchymal stem cell

OPF:

Oligo(poly(ethylene glycol) fumarate)

PCL:

Poly(ε-caprolactone)

PDSC:

Periosteum-derived stem cell

PEG:

Poly(ethylene glycol)

PHA:

Poly(hydroxyalkanoate)

PLGA:

Poly(l,d-lactic-co-glycolic acid)

RGD:

Arg-Gly-Asp

mRNA:

Messenger RNA

TGF:

Transforming growth factor

References

  1. Freemont AJ, Hoyland J (2006) Lineage plasticity and cell biology of fibrocartilage and hyaline cartilage: its significance in cartilage repair and replacement. Eur J Radiol 57(1):32–36

    Article  Google Scholar 

  2. Yoon DM, Fisher JP (2006) Chondrocyte signaling and artificial matrices for articular cartilage engineering. Adv Exp Med Biol 585:67–86

    Article  CAS  Google Scholar 

  3. Temenoff JS, Mikos AG (2000) Review: tissue engineering for regeneration of articular cartilage. Biomaterials 21(5):431–440

    Article  CAS  Google Scholar 

  4. Archer CW, Francis-West P (2003) The chondrocyte. Int J Biochem Cell Biol 35(4):401–404

    Article  CAS  Google Scholar 

  5. Janners MY, Searls RL (1970) Changes in rate of cellular proliferation during the differentiation of cartilage and muscle in the mesenchyme of the embryonic chick wing. Dev Biol 23(1):136–165

    Article  CAS  Google Scholar 

  6. Fell HB (1925) The histogenesis of cartilage and bone in the long bones of the embryonic fowl. J Morphol Physiol 40(3):417–459

    Article  Google Scholar 

  7. Thorogood PV, Hinchliffe JR (1975) An analysis of the condensation process during chondrogenesis in the embryonic chick hind limb. J Embryol Exp Morphol 33(3):581–606

    CAS  Google Scholar 

  8. Summerbell D, Wolpert L (1972) Cell density and cell division in the early morphogenesis of the chick wing. Nat New Biol 239(88):24–26

    CAS  Google Scholar 

  9. Buckwalter JA, Mankin HJ (1998) Articular cartilage: tissue design and chondrocyte-matrix interactions. Instr Course Lect 47:477–486

    CAS  Google Scholar 

  10. Poole CA (1997) Articular cartilage chondrons: form, function and failure. J Anat 191(Pt 1):1–13

    Article  Google Scholar 

  11. Ulrich-Vinther M, Maloney MD, Schwarz EM, Rosier R, O’Keefe RJ (2003) Articular cartilage biology. J Am Acad Orthop Surg 11(6):421–430

    Google Scholar 

  12. Bobick BE, Chen FH, Le AM, Tuan RS (2009) Regulation of the chondrogenic phenotype in culture. Birth Defects Res C Embryo Today 87(4):351–371

    Article  CAS  Google Scholar 

  13. Buckwalter JA (1983) Articular cartilage. Instr Course Lect 32:349–370

    CAS  Google Scholar 

  14. Eyre DR, Wu JJ, Apone S (1987) A growing family of collagens in articular cartilage: identification of 5 genetically distinct types. J Rheumatol 14(Spec No):25–27

    Google Scholar 

  15. Rosso F, Giordano A, Barbarisi M, Barbarisi A (2004) From cell–ECM interactions to tissue engineering. J Cell Physiol 199(2):174–180

    Article  CAS  Google Scholar 

  16. Heinegard D, Hascall VC (1974) Aggregation of cartilage proteoglycans. 3. Characteristics of the proteins isolated from trypsin digests of aggregates. J Biol Chem 249(13):4250–4256

    CAS  Google Scholar 

  17. Franzen A, Bjornsson S, Heinegard D (1981) Cartilage proteoglycan aggregate formation. Role of link protein. Biochem J 197(3):669–674

    CAS  Google Scholar 

  18. Newman AP (1998) Articular cartilage repair. Am J Sports Med 26(2):309–324

    CAS  Google Scholar 

  19. Kao WJ (1999) Evaluation of protein-modulated macrophage behavior on biomaterials: designing biomimetic materials for cellular engineering. Biomaterials 20(23–24):2213–2221

    Article  CAS  Google Scholar 

  20. Khalafi A, Schmid TM, Neu C, Reddi AH (2007) Increased accumulation of superficial zone protein (SZP) in articular cartilage in response to bone morphogenetic protein-7 and growth factors. J Orthop Res 25(3):293–303

    Article  CAS  Google Scholar 

  21. Coates EE, Fisher JP (2010) Phenotypic variations in chondrocyte subpopulations and their response to in vitro culture and external stimuli. Ann Biomed Eng 38(11):3371–3388

    Article  Google Scholar 

  22. Buckwalter JA, Mow VC, Ratcliffe A (1994) Restoration of injured or degenerated articular cartilage. J Am Acad Orthop Surg 2(4):192–201

    Google Scholar 

  23. Wong M, Wuethrich P, Eggli P, Hunziker E (1996) Zone-specific cell biosynthetic activity in mature bovine articular cartilage: a new method using confocal microscopic stereology and quantitative autoradiography. J Orthop Res 14(3):424–432

    Article  CAS  Google Scholar 

  24. Toole BP, Jackson G, Gross J (1972) Hyaluronate in morphogenesis: inhibition of chondrogenesis in vitro. Proc Natl Acad Sci USA 69(6):1384–1386

    Article  CAS  Google Scholar 

  25. Kulyk WM, Upholt WB, Kosher RA (1989) Fibronectin gene expression during limb cartilage differentiation. Development 106(3):449–455

    CAS  Google Scholar 

  26. Oberlender SA, Tuan RS (1994) Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis. Development 120(1):177–187

    CAS  Google Scholar 

  27. Widelitz RB, Jiang TX, Murray BA, Chuong CM (1993) Adhesion molecules in skeletogenesis: II. Neural cell adhesion molecules mediate precartilaginous mesenchymal condensations and enhance chondrogenesis. J Cell Physiol 156(2):399–411

    Article  CAS  Google Scholar 

  28. Yoon YM, Oh CD, Kim DY, Lee YS, Park JW, Huh TL et al (2000) Epidermal growth factor negatively regulates chondrogenesis of mesenchymal cells by modulating the protein kinase C-alpha, Erk-1, and p38 MAPK signaling pathways. J Biol Chem 275(16):12353–12359

    Article  CAS  Google Scholar 

  29. Wright E, Hargrave MR, Christiansen J, Cooper L, Kun J, Evans T et al (1995) The Sry-related gene SOX9 is expressed during chondrogenesis in mouse embryos. Nat Genet 9(1):15–20

    Article  CAS  Google Scholar 

  30. Ng LJ, Wheatley S, Muscat GE, Conway-Campbell J, Bowles J, Wright E et al (1997) SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol 183(1):108–121

    Article  CAS  Google Scholar 

  31. Lefebvre V, Li P, de Crombrugghe B (1998) A new long form of SOX5 (L-SOX5), SOX6 and SOX9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J 17(19):5718–5733

    Article  CAS  Google Scholar 

  32. de Crombrugghe B, Lefebvre V, Behringer RR, Bi W, Murakami S, Huang W (2000) Transcriptional mechanisms of chondrocyte differentiation. Matrix Biol 19(5):389–394

    Article  Google Scholar 

  33. Mollenhauer J, Bee JA, Lizarbe MA, von der Mark K (1984) Role of anchorin CII, a 31,000-mol-wt membrane protein, in the interaction of chondrocytes with type II collagen. J Cell Biol 98(4):1572–1579

    Article  CAS  Google Scholar 

  34. Culty M, Miyake K, Kincade PW, Sikorski E, Butcher EC, Underhill C (1990) The hyaluronate receptor is a member of the CD44 (H-CAM) family of cell surface glycoproteins. J Cell Biol 111(6 Pt 1):2765–2774

    Article  CAS  Google Scholar 

  35. Loeser RF (2002) Integrins and cell signaling in chondrocytes. Biorheology 39(1–2):119–124

    CAS  Google Scholar 

  36. Midwood KS, Salter DM (2001) NG2/HMPG modulation of human articular chondrocyte adhesion to type VI collagen is lost in osteoarthritis. J Pathol 195(5):631–635

    Article  CAS  Google Scholar 

  37. Salter DM, Hughes DE, Simpson R, Gardner DL (1992) Integrin expression by human articular chondrocytes. Br J Rheumatol 31(4):231–234

    Article  CAS  Google Scholar 

  38. Wood JJ, Malek MA, Frassica FJ, Polder JA, Mohan AK, Bloom ET et al (2006) Autologous cultured chondrocytes: adverse events reported to the United States food and drug administration. J Bone Joint Surg 88(3):503–507

    Article  Google Scholar 

  39. Darling EM, Athanasiou KA (2005) Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J Orthop Res 23(2):425–432

    Article  CAS  Google Scholar 

  40. Hauselmann HJ, Fernandes RJ, Mok SS, Schmid TM, Block JA, Aydelotte MB et al (1994) Phenotypic stability of bovine articular chondrocytes after long-term culture in alginate beads. J Cell Sci 107(Pt 1):17–27

    Google Scholar 

  41. Benya PD, Shaffer JD (1982) Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30(1):215–224

    Article  CAS  Google Scholar 

  42. Becker AJ, Mc CE, Till JE (1963) Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 197:452–454

    Article  CAS  Google Scholar 

  43. Friedenstein AJ, Chailakhyan RK, Gerasimov UV (1987) Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 20(3):263–272

    CAS  Google Scholar 

  44. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315–317

    Article  CAS  Google Scholar 

  45. Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9(5):641–650

    Article  CAS  Google Scholar 

  46. Ashton BA, Allen TD, Howlett CR, Eaglesom CC, Hattori A, Owen M (1980) Formation of bone and cartilage by marrow stromal cells in diffusion chambers in vivo. Clin Orthop Relat Res 151:294–307

    Google Scholar 

  47. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411):143–147

    Article  CAS  Google Scholar 

  48. Yang IH, Kim SH, Kim YH, Sun HJ, Kim SJ, Lee JW (2004) Comparison of phenotypic characterization between “alginate bead” and “pellet” culture systems as chondrogenic differentiation models for human mesenchymal stem cells. Yonsei Med J 45(5):891–900

    CAS  Google Scholar 

  49. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU (1998) In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238(1):265–272

    Article  CAS  Google Scholar 

  50. Derfoul A, Perkins GL, Hall DJ, Tuan RS (2006) Glucocorticoids promote chondrogenic differentiation of adult human mesenchymal stem cells by enhancing expression of cartilage extracellular matrix genes. Stem Cells 24(6):1487–1495

    Article  CAS  Google Scholar 

  51. Fischer J, Dickhut A, Rickert M, Richter W (2010) Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum 62(9):2696–2706

    Article  CAS  Google Scholar 

  52. Winter A, Breit S, Parsch D, Benz K, Steck E, Hauner H et al (2003) Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthritis Rheum 48(2):418–429

    Article  CAS  Google Scholar 

  53. Tsuchiya K, Chen GP, Ushida T, Matsuno T, Tateishi T (2004) The effect of coculture of chondrocytes with mesenchymal stem cells on their cartilaginous phenotype in vitro. Mater Sci Eng C Biomim Supramol Syst 24(3):391–396

    Article  CAS  Google Scholar 

  54. Ma HL, Hung SC, Lin SY, Chen YL, Lo WH (2003) Chondrogenesis of human mesenchymal stem cells encapsulated in alginate beads. J Biomed Mater Res A 64(2):273–281

    Article  CAS  Google Scholar 

  55. Diekman BO, Rowland CR, Lennon DP, Caplan AI, Guilak F (2010) Chondrogenesis of adult stem cells from adipose tissue and bone marrow: induction by growth factors and cartilage-derived matrix. Tissue Eng Part A 16(2):523–533

    Article  CAS  Google Scholar 

  56. Chung C, Burdick JA (2009) Influence of three-dimensional hyaluronic acid microenvironments on mesenchymal stem cell chondrogenesis. Tissue Eng Part A 15(2):243–254

    Article  CAS  Google Scholar 

  57. Sharma B, Williams CG, Khan M, Manson P, Elisseeff JH (2007) In vivo chondrogenesis of mesenchymal stem cells in a photopolymerized hydrogel. Plast Reconstr Surg 119(1):112–120

    Article  CAS  Google Scholar 

  58. Park JS, Yang HN, Woo DG, Jeon SY, Park KH (2011) Chondrogenesis of human mesenchymal stem cells in fibrin constructs evaluated in vitro and in nude mouse and rabbit defects models. Biomaterials 32(6):1495–1507

    Article  CAS  Google Scholar 

  59. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13(12):4279–4295

    Article  CAS  Google Scholar 

  60. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ et al (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7(2):211–228

    Article  CAS  Google Scholar 

  61. Estes BT, Diekman BO, Gimble JM, Guilak F (2010) Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc 5(7):1294–1311

    Article  CAS  Google Scholar 

  62. Cheng NC, Estes BT, Awad HA, Guilak F (2009) Chondrogenic differentiation of adipose-derived adult stem cells by a porous scaffold derived from native articular cartilage extracellular matrix. Tissue Eng Part A 15(2):231–241

    Article  CAS  Google Scholar 

  63. Awad HA, Wickham MQ, Leddy HA, Gimble JM, Guilak F (2004) Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 25(16):3211–3222

    Article  CAS  Google Scholar 

  64. Betre H, Setton LA, Meyer DE, Chilkoti A (2002) Characterization of a genetically engineered elastin-like polypeptide for cartilaginous tissue repair. Biomacromolecules 3(5):910–916

    Article  CAS  Google Scholar 

  65. Merceron C, Portron S, Masson M, Fellah BH, Gauthier O, Lesoeur J et al (2010) Cartilage tissue engineering: From hydrogel to mesenchymal stem cells. Biomed Mater Eng 20(3):159–166

    CAS  Google Scholar 

  66. Lin Y, Luo E, Chen X, Liu L, Qiao J, Yan Z et al (2005) Molecular and cellular characterization during chondrogenic differentiation of adipose tissue-derived stromal cells in vitro and cartilage formation in vivo. J Cell Mol Med 9(4):929–939

    Article  CAS  Google Scholar 

  67. Masuoka K, Asazuma T, Hattori H, Yoshihara Y, Sato M, Matsumura K et al (2006) Tissue engineering of articular cartilage with autologous cultured adipose tissue-derived stromal cells using atelocollagen honeycomb-shaped scaffold with a membrane sealing in rabbits. J Biomed Mater Res B Appl Biomater 79(1):25–34

    Google Scholar 

  68. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145–1147

    Article  CAS  Google Scholar 

  69. Kawaguchi J (2006) Generation of osteoblasts and chondrocytes from embryonic stem cells. Methods Mol Biol 330:135–148

    CAS  Google Scholar 

  70. Koay EJ, Hoben GM, Athanasiou KA (2007) Tissue engineering with chondrogenically differentiated human embryonic stem cells. Stem Cells 25(9):2183–2190

    Article  CAS  Google Scholar 

  71. zur Nieden NI, Kempka G, Rancourt DE, Ahr HJ (2005) Induction of chondro-, osteo- and adipogenesis in embryonic stem cells by bone morphogenetic protein-2: effect of cofactors on differentiating lineages. BMC Dev Biol 5:1

    Article  CAS  Google Scholar 

  72. Kramer J, Hegert C, Guan K, Wobus AM, Muller PK, Rohwedel J (2000) Embryonic stem cell-derived chondrogenic differentiation in vitro: activation by BMP-2 and BMP-4. Mech Dev 92(2):193–205

    Article  CAS  Google Scholar 

  73. Nakagawa T, Lee SY, Reddi AH (2009) Induction of chondrogenesis from human embryonic stem cells without embryoid body formation by bone morphogenetic protein 7 and transforming growth factor beta1. Arthritis Rheum 60(12):3686–3692

    Article  CAS  Google Scholar 

  74. Yang Z, Sui L, Toh WS, Lee EH, Cao T (2009) Stage-dependent effect of TGF-beta1 on chondrogenic differentiation of human embryonic stem cells. Stem Cells Dev 18(6):929–940

    Article  CAS  Google Scholar 

  75. Oldershaw RA, Baxter MA, Lowe ET, Bates N, Grady LM, Soncin F et al (2010) Directed differentiation of human embryonic stem cells toward chondrocytes. Nat Biotechnol 28(11):1187–1194

    Article  CAS  Google Scholar 

  76. Toh WS, Yang Z, Liu H, Heng BC, Lee EH, Cao T (2007) Effects of culture conditions and bone morphogenetic protein 2 on extent of chondrogenesis from human embryonic stem cells. Stem Cells 25(4):950–960

    Article  CAS  Google Scholar 

  77. Vats A, Bielby RC, Tolley N, Dickinson SC, Boccaccini AR, Hollander AP et al (2006) Chondrogenic differentiation of human embryonic stem cells: the effect of the micro-environment. Tissue Eng 12(6):1687–1697

    Article  CAS  Google Scholar 

  78. Bigdeli N, Karlsson C, Strehl R, Concaro S, Hyllner J, Lindahl A (2009) Coculture of human embryonic stem cells and human articular chondrocytes results in significantly altered phenotype and improved chondrogenic differentiation. Stem Cells 27(8):1812–1821

    Article  Google Scholar 

  79. Hwang NS, Varghese S, Zhang Z, Elisseeff J (2006) Chondrogenic differentiation of human embryonic stem cell-derived cells in arginine-glycine-aspartate-modified hydrogels. Tissue Eng 12(9):2695–2706

    Article  CAS  Google Scholar 

  80. Adachi N, Sato K, Usas A, Fu FH, Ochi M, Han CW et al (2002) Muscle derived, cell based ex vivo gene therapy for treatment of full thickness articular cartilage defects. J Rheumatol 29(9):1920–1930

    CAS  Google Scholar 

  81. Nawata M, Wakitani S, Nakaya H, Tanigami A, Seki T, Nakamura Y et al (2005) Use of bone morphogenetic protein 2 and diffusion chambers to engineer cartilage tissue for the repair of defects in articular cartilage. Arthritis Rheum 52(1):155–163

    Article  CAS  Google Scholar 

  82. Kuroda R, Usas A, Kubo S, Corsi K, Peng H, Rose T et al (2006) Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells. Arthritis Rheum 54(2):433–442

    Article  CAS  Google Scholar 

  83. Ito Y, Fitzsimmons JS, Sanyal A, Mello MA, Mukherjee N, O’Driscoll SW (2001) Localization of chondrocyte precursors in periosteum. Osteoarthr Cartil 9(3):215–223

    Article  CAS  Google Scholar 

  84. Choi YS, Noh SE, Lim SM, Lee CW, Kim CS, Im MW et al (2008) Multipotency and growth characteristic of periosteum-derived progenitor cells for chondrogenic, osteogenic, and adipogenic differentiation. Biotechnol Lett 30(4):593–601

    Article  CAS  Google Scholar 

  85. Miura Y, Fitzsimmons JS, Commisso CN, Gallay SH, O’Driscoll SW (1994) Enhancement of periosteal chondrogenesis in vitro. Dose-response for transforming growth factor-beta 1 (TGF-beta 1). Clin Orthop Relat Res 301:271–280

    Google Scholar 

  86. Stevens MM, Marini RP, Martin I, Langer R, Prasad Shastri V (2004) FGF-2 enhances TGF-beta1-induced periosteal chondrogenesis. J Orthop Res 22(5):1114–1119

    Article  CAS  Google Scholar 

  87. Fukumoto T, Sperling JW, Sanyal A, Fitzsimmons JS, Reinholz GG, Conover CA et al (2003) Combined effects of insulin-like growth factor-1 and transforming growth factor-beta1 on periosteal mesenchymal cells during chondrogenesis in vitro. Osteoarthr Cartil 11(1):55–64

    Article  CAS  Google Scholar 

  88. Stevens MM, Qanadilo HF, Langer R, Shastri VP (2004) A rapid-curing alginate gel system: utility in periosteum-derived cartilage tissue engineering. Biomaterials 25(5):887–894

    Article  CAS  Google Scholar 

  89. Haniffa MA, Collin MP, Buckley CD, Dazzi F (2009) Mesenchymal stem cells: the fibroblasts’ new clothes? Haematologica 94(2):258–263

    Article  CAS  Google Scholar 

  90. Mizuno S, Glowacki J (1996) Chondroinduction of human dermal fibroblasts by demineralized bone in three-dimensional culture. Exp Cell Res 227(1):89–97

    Article  CAS  Google Scholar 

  91. French MM, Rose S, Canseco J, Athanasiou KA (2004) Chondrogenic differentiation of adult dermal fibroblasts. Ann Biomed Eng 32(1):50–56

    Article  CAS  Google Scholar 

  92. Singh M, Pierpoint M, Mikos AG, Kasper FK (2011) Chondrogenic differentiation of neonatal human dermal fibroblasts encapsulated in alginate beads with hydrostatic compression under hypoxic conditions in the presence of bone morphogenetic protein-2. J Biomed Mater Res A 98:412–424

    Google Scholar 

  93. Deng Y, Hu JC, Athanasiou KA (2007) Isolation and chondroinduction of a dermis-isolated, aggrecan-sensitive subpopulation with high chondrogenic potential. Arthritis Rheum 56(1):168–176

    Article  Google Scholar 

  94. Nicoll SB, Wedrychowska A, Smith NR, Bhatnagar RS (2001) Modulation of proteoglycan and collagen profiles in human dermal fibroblasts by high density micromass culture and treatment with lactic acid suggests change to a chondrogenic phenotype. Connect Tissue Res 42(1):59–69

    Article  CAS  Google Scholar 

  95. Liu X, Zhou G, Liu W, Zhang W, Cui L, Cao Y (2007) In vitro formation of lacuna structure by human dermal fibroblasts co-cultured with porcine chondrocytes on a 3D biodegradable scaffold. Biotechnol Lett 29(11):1685–1690

    Article  CAS  Google Scholar 

  96. Rutherford RB, Moalli M, Franceschi RT, Wang D, Gu K, Krebsbach PH (2002) Bone morphogenetic protein-transduced human fibroblasts convert to osteoblasts and form bone in vivo. Tissue Eng 8(3):441–452

    Article  CAS  Google Scholar 

  97. Yin S, Cen L, Wang C, Zhao G, Sun J, Liu W et al (2010) Chondrogenic transdifferentiation of human dermal fibroblasts stimulated with cartilage-derived morphogenetic protein 1. Tissue Eng Part A 16(5):1633–1643

    Article  CAS  Google Scholar 

  98. Hiramatsu K, Sasagawa S, Outani H, Nakagawa K, Yoshikawa H, Tsumaki N (2011) Generation of hyaline cartilaginous tissue from mouse adult dermal fibroblast culture by defined factors. J Clin Invest 121(2):640–657

    Article  CAS  Google Scholar 

  99. Lee CH, Cook JL, Mendelson A, Moioli EK, Yao H, Mao JJ (2010) Regeneration of the articular surface of the rabbit synovial joint by cell homing: a proof of concept study. Lancet 376(9739):440–448

    Article  CAS  Google Scholar 

  100. Karp JM, Leng Teo GS (2009) Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4(3):206–216

    Article  CAS  Google Scholar 

  101. Fong EL, Chan CK, Goodman SB (2011) Stem cell homing in musculoskeletal injury. Biomaterials 32(2):395–409

    Article  CAS  Google Scholar 

  102. Shapiro F, Koide S, Glimcher MJ (1993) Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg 75(4):532–553

    CAS  Google Scholar 

  103. Bryant SJ, Anseth KS (2002) Hydrogel properties influence ECM production by chondrocytes photoencapsulated in poly(ethylene glycol) hydrogels. J Biomed Mater Res 59(1):63–72

    Article  CAS  Google Scholar 

  104. Fedorovich NE, Alblas J, de Wijn JR, Hennink WE, Verbout AJ, Dhert WJ (2007) Hydrogels as extracellular matrices for skeletal tissue engineering: state-of-the-art and novel application in organ printing. Tissue Eng 13(8):1905–1925

    Article  CAS  Google Scholar 

  105. Nicodemus GD, Bryant SJ (2008) Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng Part B Rev 14(2):149–165

    Article  CAS  Google Scholar 

  106. Herlofsen SR, Kuchler AM, Melvik JE, Brinchmann JE (2011) Chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in self-gelling alginate discs reveals novel chondrogenic signature gene clusters. Tissue Eng Part A 17:1003–1013

    Article  CAS  Google Scholar 

  107. Wang W, Li B, Yang J, Xin L, Li Y, Yin H et al (2010) The restoration of full-thickness cartilage defects with BMSCs and TGF-beta 1 loaded PLGA/fibrin gel constructs. Biomaterials 31(34):8964–8973

    Article  CAS  Google Scholar 

  108. Tigli RS, Cannizaro C, Gumusderelioglu M, Kaplan DL (2011) Chondrogenesis in perfusion bioreactors using porous silk scaffolds and hESC-derived MSCs. J Biomed Mater Res A 96(1):21–28

    Google Scholar 

  109. Wang Y, Bella E, Lee CS, Migliaresi C, Pelcastre L, Schwartz Z et al (2010) The synergistic effects of 3-D porous silk fibroin matrix scaffold properties and hydrodynamic environment in cartilage tissue regeneration. Biomaterials 31(17):4672–4681

    Article  CAS  Google Scholar 

  110. Neves SC, Teixeira LSM, Moroni L, Reis RL, Van Blitterswijk CA, Alves NM et al (2011) Chitosan/poly(epsilon-caprolactone) blend scaffolds for cartilage repair. Biomaterials 32(4):1068–1079

    Article  CAS  Google Scholar 

  111. Suh JK, Matthew HW (2000) Application of chitosan-based polysaccharide biomaterials in cartilage tissue engineering: a review. Biomaterials 21(24):2589–2598

    Article  CAS  Google Scholar 

  112. Chang CH, Liu HC, Lin CC, Chou CH, Lin FH (2003) Gelatin-chondroitin-hyaluronan tri-copolymer scaffold for cartilage tissue engineering. Biomaterials 24(26):4853–4858

    Article  CAS  Google Scholar 

  113. Tan H, Chu CR, Payne KA, Marra KG (2009) Injectable in situ forming biodegradable chitosan-hyaluronic acid based hydrogels for cartilage tissue engineering. Biomaterials 30(13):2499–2506

    Article  CAS  Google Scholar 

  114. Baier Leach J, Bivens KA, Patrick CW Jr, Schmidt CE (2003) Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds. Biotechnol Bioeng 82(5):578–589

    Article  CAS  Google Scholar 

  115. Varghese S, Hwang NS, Canver AC, Theprungsirikul P, Lin DW, Elisseeff J (2008) Chondroitin sulfate based niches for chondrogenic differentiation of mesenchymal stem cells. Matrix Biol 27(1):12–21

    Article  CAS  Google Scholar 

  116. Varghese S, Elisseeff JH (2006) Hydrogels for musculoskeletal tissue engineering. Adv Polym Sci 203:95–144

    Google Scholar 

  117. Ma Z, Mao Z, Gao C (2007) Surface modification and property analysis of biomedical polymers used for tissue engineering. Colloids Surf B Biointerfaces 60(2):137–157

    Article  CAS  Google Scholar 

  118. Nguyen LH, Kudva AK, Guckert NL, Linse KD, Roy K (2011) Unique biomaterial compositions direct bone marrow stem cells into specific chondrocytic phenotypes corresponding to the various zones of articular cartilage. Biomaterials 32(5):1327–1338

    Article  CAS  Google Scholar 

  119. Wang C, Varshney RR, Wang DA (2010) Therapeutic cell delivery and fate control in hydrogels and hydrogel hybrids. Adv Drug Deliv Rev 62(7–8):699–710

    Article  CAS  Google Scholar 

  120. Shin H, Jo S, Mikos AG (2003) Biomimetic materials for tissue engineering. Biomaterials 24(24):4353–4364

    Article  CAS  Google Scholar 

  121. Kuo YC, Wang CC (2011) Surface modification with peptide for enhancing chondrocyte adhesion and cartilage regeneration in porous scaffolds. Colloids Surf B Biointerfaces 84(1):63–70

    Article  CAS  Google Scholar 

  122. Kaufmann D, Fiedler A, Junger A, Auernheimer J, Kessler H, Weberskirch R (2008) Chemical conjugation of linear and cyclic RGD moieties to a recombinant elastin-mimetic polypeptide—a versatile approach towards bioactive protein hydrogels. Macromol Biosci 8(6):577–588

    Article  CAS  Google Scholar 

  123. Sawyer AA, Hennessy KM, Bellis SL (2007) The effect of adsorbed serum proteins, RGD and proteoglycan-binding peptides on the adhesion of mesenchymal stem cells to hydroxyapatite. Biomaterials 28(3):383–392

    Article  CAS  Google Scholar 

  124. Shin H, Zygourakis K, Farach-Carson MC, Yaszemski MJ, Mikos AG (2004) Attachment, proliferation, and migration of marrow stromal osteoblasts cultured on biomimetic hydrogels modified with an osteopontin-derived peptide. Biomaterials 25(5):895–906

    Article  CAS  Google Scholar 

  125. Bahney CS, Hsu CW, Yoo JU, West JL, Johnstone B (2011) A bioresponsive hydrogel tuned to chondrogenesis of human mesenchymal stem cells. FASEB J 25:1486–1496

    Article  CAS  Google Scholar 

  126. Dong Y, Li P, Chen CB, Wang ZH, Ma P, Chen GQ (2010) The improvement of fibroblast growth on hydrophobic biopolyesters by coating with polyhydroxyalkanoate granule binding protein PhaP fused with cell adhesion motif RGD. Biomaterials 31(34):8921–8930

    Article  CAS  Google Scholar 

  127. You M, Peng G, Li J, Ma P, Wang Z, Shu W et al (2010) Chondrogenic differentiation of human bone marrow mesenchymal stem cells on polyhydroxyalkanoate (PHA) scaffolds coated with PHA granule binding protein PhaP fused with RGD peptide. Biomaterials 32(9):2305–2313

    Article  CAS  Google Scholar 

  128. Re’em T, Tsur-Gang O, Cohen S (2010) The effect of immobilized RGD peptide in macroporous alginate scaffolds on TGFbeta1-induced chondrogenesis of human mesenchymal stem cells. Biomaterials 31(26):6746–6755

    Article  CAS  Google Scholar 

  129. Vonwil D, Schuler M, Barbero A, Strobel S, Wendt D, Textor M et al (2010) An RGD-restricted substrate interface is sufficient for the adhesion, growth and cartilage forming capacity of human chondrocytes. Eur Cell Mater 20:316–328

    CAS  Google Scholar 

  130. Salinas CN, Anseth KS (2008) The enhancement of chondrogenic differentiation of human mesenchymal stem cells by enzymatically regulated RGD functionalities. Biomaterials 29(15):2370–2377

    Article  CAS  Google Scholar 

  131. Villanueva I, Weigel CA, Bryant SJ (2009) Cell–matrix interactions and dynamic mechanical loading influence chondrocyte gene expression and bioactivity in PEG-RGD hydrogels. Acta Biomater 5(8):2832–2846

    Article  CAS  Google Scholar 

  132. Chang JC, Hsu SH, Chen DC (2009) The promotion of chondrogenesis in adipose-derived adult stem cells by an RGD-chimeric protein in 3D alginate culture. Biomaterials 30(31):6265–6275

    Article  CAS  Google Scholar 

  133. Hwang NS, Varghese S, Lee HJ, Zhang Z, Ye Z, Bae J et al (2008) In vivo commitment and functional tissue regeneration using human embryonic stem cell-derived mesenchymal cells. Proc Natl Acad Sci USA 105(52):20641–20646

    Article  CAS  Google Scholar 

  134. Connelly JT, Garcia AJ, Levenston ME (2007) Inhibition of in vitro chondrogenesis in RGD-modified three-dimensional alginate gels. Biomaterials 28(6):1071–1083

    Article  CAS  Google Scholar 

  135. Matsuki K, Sasho T, Nakagawa K, Tahara M, Sugioka K, Ochiai N et al (2008) RGD peptide-induced cell death of chondrocytes and synovial cells. J Orthop Sci 13(6):524–532

    Article  CAS  Google Scholar 

  136. Davidson ENB, van der Kraan PM, van den Berg WB (2007) TGF-beta and osteoarthritis. Osteoarthr Cartil 15(6):597–604

    Article  Google Scholar 

  137. Park JS, Woo DG, Yang HN, Lim HJ, Park KM, Na K et al (2009) Chondrogenesis of human mesenchymal stem cells encapsulated in a hydrogel construct: neocartilage formation in animal models as both mice and rabbits. J Biomed Mater Res A 92(3):988–996

    Google Scholar 

  138. Park JS, Woo DG, Yang HN, Na K, Park KH (2009) Transforming growth factor beta-3 bound with sulfate polysaccharide in synthetic extracellular matrix enhanced the biological activities for neocartilage formation in vivo. J Biomed Mater Res A 91(2):408–415

    Google Scholar 

  139. van der Kraan PM, Blaney Davidson EN, Blom A, van den Berg WB (2009) TGF-beta signaling in chondrocyte terminal differentiation and osteoarthritis: modulation and integration of signaling pathways through receptor-Smads. Osteoarthr Cartil 17(12):1539–1545

    Article  Google Scholar 

  140. Zheng L, Fan HS, Sun J, Chen XN, Wang G, Zhang L et al (2010) Chondrogenic differentiation of mesenchymal stem cells induced by collagen-based hydrogel: an in vivo study. J Biomed Mater Res A 93(2):783–792

    CAS  Google Scholar 

  141. Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF (1998) Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4(4):415–428

    Article  CAS  Google Scholar 

  142. Elder BD, Athanasiou KA (2009) Systematic assessment of growth factor treatment on biochemical and biomechanical properties of engineered articular cartilage constructs. Osteoarthr Cartil 17(1):114–123

    Article  CAS  Google Scholar 

  143. Liu XW, Hu J, Man C, Zhang B, Ma YQ, Zhu SS (2011) Insulin-like growth factor-1 suspended in hyaluronan improves cartilage and subchondral cancellous bone repair in osteoarthritis of temporomandibular joint. Int J Oral Maxillofac Surg 40:184–190

    Article  Google Scholar 

  144. Longobardi L, O’Rear L, Aakula S, Johnstone B, Shimer K, Chytil A et al (2006) Effect of IGF-I in the chondrogenesis of bone marrow mesenchymal stem cells in the presence or absence of TGF-beta signaling. J Bone Miner Res 21(4):626–636

    Article  CAS  Google Scholar 

  145. Park H, Temenoff JS, Tabata Y, Caplan AI, Raphael RM, Jansen JA et al (2009) Effect of dual growth factor delivery on chondrogenic differentiation of rabbit marrow mesenchymal stem cells encapsulated in injectable hydrogel composites. J Biomed Mater Res A 88(4):889–897

    Google Scholar 

  146. Schmidt MB, Chen EH, Lynch SE (2006) A review of the effects of insulin-like growth factor and platelet derived growth factor on in vivo cartilage healing and repair. Osteoarthr Cartil 14(5):403–412

    Article  CAS  Google Scholar 

  147. Jiang Y, Chen LK, Zhu DC, Zhang GR, Guo C, Qi YY et al (2010) The inductive effect of bone morphogenetic protein-4 on chondral-lineage differentiation and in situ cartilage repair. Tissue Eng Part A 16(5):1621–1632

    Article  CAS  Google Scholar 

  148. Miljkovic ND, Cooper GM, Marra KG (2008) Chondrogenesis, bone morphogenetic protein-4 and mesenchymal stem cells. Osteoarthr Cartil 16(10):1121–1130

    Article  CAS  Google Scholar 

  149. Tamai N, Myoui A, Hirao M, Kaito T, Ochi T, Tanaka J et al (2005) A new biotechnology for articular cartilage repair: subchondral implantation of a composite of interconnected porous hydroxyapatite, synthetic polymer (PLA-PEG), and bone morphogenetic protein-2 (rhBMP-2). Osteoarthr Cartil 13(5):405–417

    Article  Google Scholar 

  150. Majumdar MK, Wang E, Morris EA (2001) BMP-2 and BMP-9 promotes chondrogenic differentiation of human multipotential mesenchymal cells and overcomes the inhibitory effect of IL-1. J Cell Physiol 189(3):275–284

    Article  CAS  Google Scholar 

  151. Sekiya I, Larson BL, Vuoristo JT, Reger RL, Prockop DJ (2005) Comparison of effect of BMP-2, -4, and -6 on in vitro cartilage formation of human adult stem cells from bone marrow stroma. Cell Tissue Res 320(2):269–276

    Article  CAS  Google Scholar 

  152. Fukuda A, Kato K, Hasegawa M, Hirata H, Sudo A, Okazaki K et al (2005) Enhanced repair of large osteochondral defects using a combination of artificial cartilage and basic fibroblast growth factor. Biomaterials 26(20):4301–4308

    Article  CAS  Google Scholar 

  153. Huang X, Yang D, Yan W, Shi Z, Feng J, Gao Y et al (2007) Osteochondral repair using the combination of fibroblast growth factor and amorphous calcium phosphate/poly(l-lactic acid) hybrid materials. Biomaterials 28(20):3091–3100

    Article  CAS  Google Scholar 

  154. Miyakoshi N, Kobayashi M, Nozaka K, Okada K, Shimada Y, Itoi E (2005) Effects of intraarticular administration of basic fibroblast growth factor with hyaluronic acid on osteochondral defects of the knee in rabbits. Arch Orthop Trauma Surg 125(10):683–692

    Article  Google Scholar 

  155. Nakayama J, Fujioka H, Nagura I, Kokubu T, Makino T, Kuroda R et al (2009) The effect of fibroblast growth factor-2 on autologous osteochondral transplantation. Int Orthop 33(1):275–280

    Article  Google Scholar 

  156. Siebert CH, Schneider U, Sopka S, Wahner T, Miltner O, Niedhart C (2006) Ingrowth of osteochondral grafts under the influence of growth factors: 6-month results of an animal study. Arch Orthop Trauma Surg 126(4):247–252

    Article  Google Scholar 

  157. Tanaka H, Mizokami H, Shiigi E, Murata H, Ogasa H, Mine T et al (2004) Effects of basic fibroblast growth factor on the repair of large osteochondral defects of articular cartilage in rabbits: dose-response effects and long-term outcomes. Tissue Eng 10(3–4):633–641

    Article  CAS  Google Scholar 

  158. Weiss S, Hennig T, Bock R, Steck E, Richter W (2010) Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. J Cell Physiol 223(1):84–93

    CAS  Google Scholar 

  159. Holland TA, Bodde EW, Cuijpers VM, Baggett LS, Tabata Y, Mikos AG et al (2007) Degradable hydrogel scaffolds for in vivo delivery of single and dual growth factors in cartilage repair. Osteoarthr Cartil 15(2):187–197

    Article  CAS  Google Scholar 

  160. Holland TA, Tabata Y, Mikos AG (2005) Dual growth factor delivery from degradable oligo(poly(ethylene glycol) fumarate) hydrogel scaffolds for cartilage tissue engineering. J Control Release 101(1–3):111–125

    Article  CAS  Google Scholar 

  161. Tabata Y, Nagano A, Ikada Y (1999) Biodegradation of hydrogel carrier incorporating fibroblast growth factor. Tissue Eng 5(2):127–138

    Article  CAS  Google Scholar 

  162. Fan H, Zhang C, Li J, Bi L, Qin L, Wu H et al (2008) Gelatin microspheres containing TGF-beta3 enhance the chondrogenesis of mesenchymal stem cells in modified pellet culture. Biomacromolecules 9(3):927–934

    Article  CAS  Google Scholar 

  163. Jo S, Shin H, Shung AK, Fisher JP, Mikos AG (2001) Synthesis and characterization of oligo(poly(ethylene glycol) fumarate) macromer. Macromolecules 34(9):2839–2844

    Article  CAS  Google Scholar 

  164. Tabata Y, Hijikata S, Muniruzzaman M, Ikada Y (1999) Neovascularization effect of biodegradable gelatin microspheres incorporating basic fibroblast growth factor. J Biomater Sci Polym Ed 10(1):79–94

    Article  CAS  Google Scholar 

  165. Holland TA, Tabata Y, Mikos AG (2003) In vitro release of transforming growth factor-beta 1 from gelatin microparticles encapsulated in biodegradable, injectable oligo(poly(ethylene glycol) fumarate) hydrogels. J Control Release 91(3):299–313

    Article  CAS  Google Scholar 

  166. Holland TA, Tessmar JK, Tabata Y, Mikos AG (2004) Transforming growth factor-beta 1 release from oligo(poly(ethylene glycol) fumarate) hydrogels in conditions that model the cartilage wound healing environment. J Control Release 94(1):101–114

    Article  CAS  Google Scholar 

  167. Park H, Temenoff JS, Holland TA, Tabata Y, Mikos AG (2005) Delivery of TGF-beta1 and chondrocytes via injectable, biodegradable hydrogels for cartilage tissue engineering applications. Biomaterials 26(34):7095–7103

    Article  CAS  Google Scholar 

  168. Park H, Temenoff JS, Tabata Y, Caplan AI, Mikos AG (2007) Injectable biodegradable hydrogel composites for rabbit marrow mesenchymal stem cell and growth factor delivery for cartilage tissue engineering. Biomaterials 28(21):3217–3227

    Article  CAS  Google Scholar 

  169. Park H, Guo X, Temenoff JS, Tabata Y, Caplan AI, Kasper FK et al (2009) Effect of swelling ratio of injectable hydrogel composites on chondrogenic differentiation of encapsulated rabbit marrow mesenchymal stem cells in vitro. Biomacromolecules 10(3):541–546

    Article  CAS  Google Scholar 

  170. Jaklenec A, Hinckfuss A, Bilgen B, Ciombor DM, Aaron R, Mathiowitz E (2008) Sequential release of bioactive IGF-I and TGF-beta 1 from PLGA microsphere-based scaffolds. Biomaterials 29(10):1518–1525

    Article  CAS  Google Scholar 

  171. Bouffi C, Thomas O, Bony C, Giteau A, Venier-Julienne MC, Jorgensen C et al (2010) The role of pharmacologically active microcarriers releasing TGF-beta3 in cartilage formation in vivo by mesenchymal stem cells. Biomaterials 31(25):6485–6493

    Article  CAS  Google Scholar 

  172. Bae SE, Choi DH, Han DK, Park K (2010) Effect of temporally controlled release of dexamethasone on in vivo chondrogenic differentiation of mesenchymal stromal cells. J Control Release 143(1):23–30

    Article  CAS  Google Scholar 

  173. Park JS, Na K, Woo DG, Yang HN, Park KH (2009) Determination of dual delivery for stem cell differentiation using dexamethasone and TGF-beta3 in/on polymeric microspheres. Biomaterials 30(27):4796–4805

    Article  CAS  Google Scholar 

  174. Park JS, Yang HN, Woo DG, Chung HM, Park KH (2009) In vitro and in vivo chondrogenesis of rabbit bone marrow-derived stromal cells in fibrin matrix mixed with growth factor loaded in nanoparticles. Tissue Eng Part A 15(8):2163–2175

    Article  CAS  Google Scholar 

  175. Ivkovic A, Pascher A, Hudetz D, Maticic D, Jelic M, Dickinson S et al (2010) Articular cartilage repair by genetically modified bone marrow aspirate in sheep. Gene Ther 17(6):779–789

    Article  CAS  Google Scholar 

  176. Madry H, Kaul G, Cucchiarini M, Stein U, Zurakowski D, Remberger K et al (2005) Enhanced repair of articular cartilage defects in vivo by transplanted chondrocytes overexpressing insulin-like growth factor I (IGF-I). Gene Ther 12(15):1171–1179

    Article  CAS  Google Scholar 

  177. Madry H, Orth P, Kaul G, Zurakowski D, Menger MD, Kohn D et al (2010) Acceleration of articular cartilage repair by combined gene transfer of human insulin-like growth factor I and fibroblast growth factor-2 in vivo. Arch Orthop Trauma Surg 130(10):1311–1322

    Article  Google Scholar 

  178. Pagnotto MR, Wang Z, Karpie JC, Ferretti M, Xiao X, Chu CR (2007) Adeno-associated viral gene transfer of transforming growth factor-beta1 to human mesenchymal stem cells improves cartilage repair. Gene Ther 14(10):804–813

    Article  CAS  Google Scholar 

  179. Cucchiarini M, Madry H, Ma C, Thurn T, Zurakowski D, Menger MD et al (2005) Improved tissue repair in articular cartilage defects in vivo by rAAV-mediated overexpression of human fibroblast growth factor 2. Mol Ther 12(2):229–238

    Article  CAS  Google Scholar 

  180. Cucchiarini M, Schetting S, Terwilliger EF, Kohn D, Madry H (2009) rAAV-mediated overexpression of FGF-2 promotes cell proliferation, survival, and alpha-SMA expression in human meniscal lesions. Gene Ther 16(11):1363–1372

    Article  CAS  Google Scholar 

  181. Ayala R, Zhang C, Yang D, Hwang Y, Aung A, Shroff SS et al (2011) Engineering the cell-material interface for controlling stem cell adhesion, migration, and differentiation. Biomaterials 32(15):3700–3711

    Article  CAS  Google Scholar 

  182. Park JS, Woo DG, Sun BK, Chung HM, Im SJ, Choi YM et al (2007) In vitro and in vivo test of PEG/PCL-based hydrogel scaffold for cell delivery application. J Control Release 124(1–2):51–59

    Article  CAS  Google Scholar 

  183. Chen JP, Su CH (2011) Surface modification of electrospun PLLA nanofibers by plasma treatment and cationized gelatin immobilization for cartilage tissue engineering. Acta Biomater 7(1):234–243

    Article  CAS  Google Scholar 

  184. Martins A, Pinho ED, Faria S, Pashkuleva I, Marques AP, Reis RL et al (2009) Surface modification of electrospun polycaprolactone nanofiber meshes by plasma treatment to enhance biological performance. Small 5(10):1195–1206

    CAS  Google Scholar 

  185. Kim K, Dean D, Lu A, Mikos AG, Fisher JP (2011) Early osteogenic signal expression of rat bone marrow stromal cells is influenced by both hydroxyapatite nanoparticle content and initial cell seeding density in biodegradable nanocomposite scaffolds. Acta Biomater 7(3):1249–1264

    Article  CAS  Google Scholar 

  186. Vlacic-Zischke J, Hamlet SM, Friis T, Tonetti MS, Ivanovski S (2011) The influence of surface microroughness and hydrophilicity of titanium on the up-regulation of TGFbeta/BMP signalling in osteoblasts. Biomaterials 32(3):665–671

    Article  CAS  Google Scholar 

  187. Lee JW, Kim YH, Park KD, Jee KS, Shin JW, Hahn SB (2004) Importance of integrin beta1-mediated cell adhesion on biodegradable polymers under serum depletion in mesenchymal stem cells and chondrocytes. Biomaterials 25(10):1901–1909

    Article  CAS  Google Scholar 

  188. Hamilton DW, Riehle MO, Monaghan W, Curtis AS (2006) Chondrocyte aggregation on micrometric surface topography: a time-lapse study. Tissue Eng 12(1):189–199

    Article  Google Scholar 

  189. Jeong CG, Hollister SJ (2010) A comparison of the influence of material on in vitro cartilage tissue engineering with PCL, PGS, and POC 3D scaffold architecture seeded with chondrocytes. Biomaterials 31(15):4304–4312

    Article  CAS  Google Scholar 

  190. Kim K, Dean D, Wallace J, Breithaupt R, Mikos AG, Fisher JP (2011) The influence of stereolithographic scaffold architecture and composition on osteogenic signal expression with rat bone marrow stromal cells. Biomaterials 32(15):3750–3763

    Article  CAS  Google Scholar 

  191. Kim K, Yeatts A, Dean D, Fisher JP (2010) Stereolithographic bone scaffold design parameters: osteogenic differentiation and signal expression. Tissue Eng Part B Rev 16(5):523–539

    Article  CAS  Google Scholar 

  192. Nuernberger S, Cyran N, Albrecht C, Redl H, Vecsei V, Marlovits S (2011) The influence of scaffold architecture on chondrocyte distribution and behavior in matrix-associated chondrocyte transplantation grafts. Biomaterials 32(4):1032–1040

    Article  CAS  Google Scholar 

  193. Li WJ, Mauck RL, Cooper JA, Yuan X, Tuan RS (2007) Engineering controllable anisotropy in electrospun biodegradable nanofibrous scaffolds for musculoskeletal tissue engineering. J Biomech 40(8):1686–1693

    Article  Google Scholar 

  194. Martins A, Araujo JV, Reis RL, Neves NM (2007) Electrospun nanostructured scaffolds for tissue engineering applications. Nanomedicine (Lond) 2(6):929–942

    Article  Google Scholar 

  195. Li WJ, Jiang YJ, Tuan RS (2006) Chondrocyte phenotype in engineered fibrous matrix is regulated by fiber size. Tissue Eng 12(7):1775–1785

    Article  CAS  Google Scholar 

  196. Li WJ, Tuli R, Okafor C, Derfoul A, Danielson KG, Hall DJ et al (2005) A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials 26(6):599–609

    Article  CAS  Google Scholar 

  197. Spadaccio C, Rainer A, Trombetta M, Vadala G, Chello M, Covino E et al (2009) Poly-L-lactic acid/hydroxyapatite electrospun nanocomposites induce chondrogenic differentiation of human MSC. Ann Biomed Eng 37(7):1376–1389

    Article  Google Scholar 

  198. Wise JK, Yarin AL, Megaridis CM, Cho M (2009) Chondrogenic differentiation of human mesenchymal stem cells on oriented nanofibrous scaffolds: engineering the superficial zone of articular cartilage. Tissue Eng Part A 15(4):913–921

    Article  CAS  Google Scholar 

  199. Binulal NS, Deepthy M, Selvamurugan N, Shalumon KT, Suja S, Mony U et al (2010) Role of nanofibrous poly(caprolactone) scaffolds in human mesenchymal stem cell attachment and spreading for in vitro bone tissue engineering–response to osteogenic regulators. Tissue Eng Part A 16(2):393–404

    Article  CAS  Google Scholar 

  200. Hu J, Feng K, Liu X, Ma PX (2009) Chondrogenic and osteogenic differentiations of human bone marrow-derived mesenchymal stem cells on a nanofibrous scaffold with designed pore network. Biomaterials 30(28):5061–5067

    Article  CAS  Google Scholar 

  201. Li WJ, Tuli R, Huang X, Laquerriere P, Tuan RS (2005) Multilineage differentiation of human mesenchymal stem cells in a three-dimensional nanofibrous scaffold. Biomaterials 26(25):5158–5166

    Article  CAS  Google Scholar 

  202. Casper ME, Fitzsimmons JS, Stone JJ, Meza AO, Huang Y, Ruesink TJ et al (2010) Tissue engineering of cartilage using poly-epsilon-caprolactone nanofiber scaffolds seeded in vivo with periosteal cells. Osteoarthr Cartil 18(7):981–991

    Article  CAS  Google Scholar 

  203. Li WJ, Chiang H, Kuo TF, Lee HS, Jiang CC, Tuan RS (2009) Evaluation of articular cartilage repair using biodegradable nanofibrous scaffolds in a swine model: a pilot study. J Tissue Eng Regen Med 3(1):1–10

    Article  CAS  Google Scholar 

  204. Sharma B, Williams CG, Kim TK, Sun D, Malik A, Khan M et al (2007) Designing zonal organization into tissue-engineered cartilage. Tissue Eng 13(2):405–414

    Article  CAS  Google Scholar 

  205. Ng KW, Ateshian GA, Hung CT (2009) Zonal chondrocytes seeded in a layered agarose hydrogel create engineered cartilage with depth-dependent cellular and mechanical inhomogeneity. Tissue Eng Part A 15(9):2315–2324

    Article  CAS  Google Scholar 

  206. Gao J, Dennis JE, Solchaga LA, Goldberg VM, Caplan AI (2002) Repair of osteochondral defect with tissue-engineered two-phase composite material of injectable calcium phosphate and hyaluronan sponge. Tissue Eng 8(5):827–837

    Article  CAS  Google Scholar 

  207. Schek RM, Taboas JM, Segvich SJ, Hollister SJ, Krebsbach PH (2004) Engineered osteochondral grafts using biphasic composite solid free-form fabricated scaffolds. Tissue Eng 10(9–10):1376–1385

    CAS  Google Scholar 

  208. Oliveira JM, Rodrigues MT, Silva SS, Malafaya PB, Gomes ME, Viegas CA et al (2006) Novel hydroxyapatite/chitosan bilayered scaffold for osteochondral tissue-engineering applications: Scaffold design and its performance when seeded with goat bone marrow stromal cells. Biomaterials 27(36):6123–6137

    Article  CAS  Google Scholar 

  209. Guo X, Liao J, Park H, Saraf A, Raphael RM, Tabata Y et al (2010) Effects of TGF-beta3 and preculture period of osteogenic cells on the chondrogenic differentiation of rabbit marrow mesenchymal stem cells encapsulated in a bilayered hydrogel composite. Acta Biomater 6(8):2920–2931

    Article  CAS  Google Scholar 

  210. Guo X, Park H, Liu G, Liu W, Cao Y, Tabata Y et al (2009) In vitro generation of an osteochondral construct using injectable hydrogel composites encapsulating rabbit marrow mesenchymal stem cells. Biomaterials 30(14):2741–2752

    Article  CAS  Google Scholar 

  211. Holland TA, Bodde EW, Baggett LS, Tabata Y, Mikos AG, Jansen JA (2005) Osteochondral repair in the rabbit model utilizing bilayered, degradable oligo(poly(ethylene glycol) fumarate) hydrogel scaffolds. J Biomed Mater Res A 75(1):156–167

    Google Scholar 

  212. Guo X, Park H, Young S, Kretlow JD, van den Beucken JJ, Baggett LS et al (2010) Repair of osteochondral defects with biodegradable hydrogel composites encapsulating marrow mesenchymal stem cells in a rabbit model. Acta Biomater 6(1):39–47

    Article  CAS  Google Scholar 

  213. Miller RE, Grodzinsky AJ, Vanderploeg EJ, Lee C, Ferris DJ, Barrett MF et al (2010) Effect of self-assembling peptide, chondrogenic factors, and bone marrow-derived stromal cells on osteochondral repair. Osteoarthr Cartil 18(12):1608–1619

    Article  CAS  Google Scholar 

  214. Fan H, Hu Y, Qin L, Li X, Wu H, Lv R (2006) Porous gelatin-chondroitin-hyaluronate tri-copolymer scaffold containing microspheres loaded with TGF-beta1 induces differentiation of mesenchymal stem cells in vivo for enhancing cartilage repair. J Biomed Mater Res A 77(4):785–794

    Google Scholar 

  215. Fan H, Hu Y, Zhang C, Li X, Lv R, Qin L et al (2006) Cartilage regeneration using mesenchymal stem cells and a PLGA-gelatin/chondroitin/hyaluronate hybrid scaffold. Biomaterials 27(26):4573–4580

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Work in the area of biomaterials science and cartilage tissue engineering is supported by the US National Institutes of Health (R01-AR048756, A.G.M. and F.K.K.; R01-AR057083, A.G.M.; and R21-AR056076, A.G.M.).

Author information

Authors and Affiliations

  1. Department of Bioengineering, Rice University, MS-142, P.O. Box 1892, Houston, TX, 77251-1892, USA

    Kyobum Kim, Diana M. Yoon, Antonios G. Mikos & F. Kurtis Kasper

Authors
  1. Kyobum Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diana M. Yoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antonios G. Mikos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Kurtis Kasper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. Kurtis Kasper .

Editor information

Editors and Affiliations

  1. Department für Biotechnologie, Universität für Bodenkultur, Muthgasse 18, Wien, 1190, Austria

    Cornelia Kasper

  2. , CrossBIT - Center for Biocompatibility, Hannover Medical School, Feodor-Lynen-Str. 31, Hannover, 30625, Germany

    Frank Witte

  3. , Bioprozess- und Biosystemtechnik, Technische Universität Hamburg-Harburg, Denickestrasse 15, Hamburg, 21073, Germany

    Ralf Pörtner

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Kim, K., Yoon, D.M., Mikos, A.G., Kasper, F.K. (2011). Harnessing Cell–Biomaterial Interactions for Osteochondral Tissue Regeneration. In: Kasper, C., Witte, F., Pörtner, R. (eds) Tissue Engineering III: Cell - Surface Interactions for Tissue Culture. Advances in Biochemical Engineering Biotechnology, vol 126. Springer, Berlin, Heidelberg. https://doi.org/10.1007/10_2011_107

Download citation

Publish with us

Policies and ethics

Search

Navigation