Advertisement

Application of Stem Cells and the Factors Influence Their Differentiation in Cartilage Tissue Engineering

  • Quanquan Ma
  • Taoran Tian
  • Nanxin Liu
  • Mi Zhou
  • Xiaoxiao CaiEmail author
Chapter
  • 686 Downloads
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)

Abstract

Articular cartilage is a unique tissue which contents only one cell type and lack the ability to heal spontaneously. Current treatment for cartilage defects include non-operative treatment, traditional operative treatment and the cartilage tissue engineering. Among these treatments cartilage tissue engineering have drawn attention to the scientists in recent years. Standard tissue engineering requires three factors: seed cells, scaffold and growth factors. Mature chondrocytes were first used as a seed cell in cartilage tissue engineering. While stem cells, however, have become a new candidate for cartilage tissue engineering. Main sources of stem cell in cartilage tissue engineering consist of embryonic stem cells (ESCs), mesenchymal stem cells (MSCs) and other kinds of stem cells.

In this chapter we will discuss the application of different kinds of stem cells and factors influence their differentiation in cartilage tissue engineering.

Keywords

Articular cartilage Tissue engineering Stem cell Chondrogenic differentiation Mesenchymal stem cells Embryonic stem cells 

References

  1. 1.
    Cucchiarini M, Madry H. Gene therapy for cartilage defects. J Gene Med. 2005;7(12):1495–509.PubMedCrossRefGoogle Scholar
  2. 2.
    Pearle AD, Warren RF, Rodeo SA. Basic science of articular cartilage and osteoarthritis. Clin Sports Med. 2005;24(1):1–12.PubMedCrossRefGoogle Scholar
  3. 3.
    Madry H, Grun UW, Knutsen G. Cartilage repair and joint preservation: medical and surgical treatment options. Dtsch Arztebl Int. 2011;108(40):669–77.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Hunter W. Of the structure and disease of articulating cartilages. 1743. Clin Orthop Relat Res. 1995(317):3–6.Google Scholar
  5. 5.
    Jiang Y, Tuan RS. Origin and function of cartilage stem/progenitor cells in osteoarthritis. Nat Rev Rheumatol. 2015;11(4):206–12.PubMedCrossRefGoogle Scholar
  6. 6.
    Alford JW, Cole BJ. Cartilage restoration, part 1: basic science, historical perspective, patient evaluation, and treatment options. Am J Sports Med. 2005;33(2):295–306.PubMedCrossRefGoogle Scholar
  7. 7.
    Langer R, Vacanti JP. Tissue engineering. Science. 1993;260(5110):920–6.Google Scholar
  8. 8.
    Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med. 1994;331(14):889–95.PubMedCrossRefGoogle Scholar
  9. 9.
    Musumeci G, Castrogiovanni P, Leonardi R, Trovato FM, Szychlinska MA, Di Giunta A, Loreto C, Castorina S. New perspectives for articular cartilage repair treatment through tissue engineering: a contemporary review. World J Orthod. 2014;5(2):80–8.CrossRefGoogle Scholar
  10. 10.
    Peterson L, Vasiliadis HS, Brittberg M, Lindahl A. Autologous chondrocyte implantation: a long-term follow-up. Am J Sports Med. 2010;38(6):1117–24.PubMedCrossRefGoogle Scholar
  11. 11.
    Bauge C, Duval E, Ollitrault D, Girard N, Leclercq S, Galera P, Boumediene K. Type II TGFbeta receptor modulates chondrocyte phenotype. Age (Dordr). 2013;35(4):1105–16.Google Scholar
  12. 12.
    Batty L, Dance S, Bajaj S, Cole BJ. Autologous chondrocyte implantation: an overview of technique and outcomes. ANZ J Surg. 2011;81(1–2):18–25.PubMedCrossRefGoogle Scholar
  13. 13.
    Fortier LA. Stem cells: classifications, controversies, and clinical applications. Vet Surg. 2005;34(5):415–23.PubMedCrossRefGoogle Scholar
  14. 14.
    Tuan RS, Chen AF, Klatt BA. Cartilage regeneration. J Am Acad Orthop Surg. 2013;21(5):303–11.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282(5391):1145–7.PubMedCrossRefGoogle Scholar
  16. 16.
    Odorico JS, Kaufman DS, Thomson JA. Multilineage differentiation from human embryonic stem cell lines. Stem cells. 2001;19(3):193–204.PubMedCrossRefGoogle Scholar
  17. 17.
    Reubinoff BE, Pera MF, Fong CY, Trounson A, Bongso A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol. 2000;18(4):399–404.PubMedCrossRefGoogle Scholar
  18. 18.
    Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292(5819):154–6.PubMedCrossRefGoogle Scholar
  19. 19.
    Mahla RS. Stem cells applications in regenerative medicine and disease therapeutics. Int J Cell Biol. 2016;2016:6940283.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Sa S, McCloskey KE. Stage-specific cardiomyocyte differentiation method for H7 and H9 human embryonic stem cells. Stem Cell Rev. 2012;8(4):1120–8.PubMedCrossRefGoogle Scholar
  21. 21.
    Koay EJ, Hoben GM, Athanasiou KA. Tissue engineering with chondrogenically differentiated human embryonic stem cells. Stem cells. 2007;25(9):2183–90.PubMedCrossRefGoogle Scholar
  22. 22.
    Toh WS, Lee EH, Guo XM, Chan JK, Yeow CH, Choo AB, Cao T. Cartilage repair using hyaluronan hydrogel-encapsulated human embryonic stem cell-derived chondrogenic cells. Biomaterials. 2010;31(27):6968–80.PubMedCrossRefGoogle Scholar
  23. 23.
    Heng BC, Cao T, Lee EH. Directing stem cell differentiation into the chondrogenic lineage in vitro. Stem cells. 2004;22(7):1152–67.PubMedCrossRefGoogle Scholar
  24. 24.
    Wakitani S, Takaoka K, Hattori T, Miyazawa N, Iwanaga T, Takeda S, Watanabe TK, Tanigami A. Embryonic stem cells injected into the mouse knee joint form teratomas and subsequently destroy the joint. Rheumatology (Oxford). 2003;42(1):162–5.Google Scholar
  25. 25.
    Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143–7.PubMedCrossRefGoogle Scholar
  26. 26.
    Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakowa SF, Luria EA, Ruadkow IA. Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol. 1974;2(2):83–92.PubMedGoogle Scholar
  27. 27.
    Cao B, Zheng B, Jankowski RJ, Kimura S, Ikezawa M, Deasy B, Cummins J, Epperly M, Qu-Petersen Z, Huard J. Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol. 2003;5(7):640–6.PubMedCrossRefGoogle Scholar
  28. 28.
    Tapp H, Hanley Jr EN, Patt JC, Gruber HE. Adipose-derived stem cells: characterization and current application in orthopaedic tissue repair. Exp Biol Med (Maywood). 2009;234(1):1–9.CrossRefGoogle Scholar
  29. 29.
    De Bari C, Dell’Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001;44(8):1928–42.PubMedCrossRefGoogle Scholar
  30. 30.
    Sakaguchi Y, Sekiya I, Yagishita K, Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum. 2005;52(8):2521–9.PubMedCrossRefGoogle Scholar
  31. 31.
    Khan WS, Hardingham TE. Mesenchymal stem cells, sources of cells and differentiation potential. J Stem Cells. 2012;7(2):75–85.PubMedGoogle Scholar
  32. 32.
    Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol. 2007;213(2):341–7.PubMedCrossRefGoogle Scholar
  33. 33.
    Noel D, Djouad F, Jorgense C. Regenerative medicine through mesenchymal stem cells for bone and cartilage repair. Curr Opin Investig Drugs. 2002;3(7):1000–4.PubMedGoogle Scholar
  34. 34.
    Richardson SM, Mobasheri A, Freemont AJ, Hoyland JA. Intervertebral disc biology, degeneration and novel tissue engineering and regenerative medicine therapies. Histol Histopathol. 2007;22(9):1033–41.PubMedGoogle Scholar
  35. 35.
    Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP. Bone marrow as a potential source of hepatic oval cells. Science. 1999;284(5417):1168–70.PubMedCrossRefGoogle Scholar
  36. 36.
    Kopen GC, Prockop DJ, Phinney DG. Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci U S A. 1999;96(19):10711–6.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–7.PubMedCrossRefGoogle Scholar
  38. 38.
    Uccelli A, Pistoia V, Moretta L. Mesenchymal stem cells: a new strategy for immunosuppression? Trends Immunol. 2007;28(5):219–26.PubMedCrossRefGoogle Scholar
  39. 39.
    Miura M, Miura Y, Padilla-Nash HM, Molinolo AA, Fu B, Patel V, Seo BM, Sonoyama W, Zheng JJ, Baker CC, Chen W, Ried T, Shi S. Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem cells. 2006;24(4):1095–103.PubMedCrossRefGoogle Scholar
  40. 40.
    Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng. 1998;4(4):415–28.PubMedCrossRefGoogle Scholar
  41. 41.
    Hubka KM, Dahlin RL, Meretoja VV, Kasper FK, Mikos AG. Enhancing chondrogenic phenotype for cartilage tissue engineering: monoculture and coculture of articular chondrocytes and mesenchymal stem cells. Tissue Eng Part B Rev. 2014;20(6):641–54.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Somoza RA, Welter JF, Correa D, Caplan AI. Chondrogenic differentiation of mesenchymal stem cells: challenges and unfulfilled expectations. Tissue Eng Part B Rev. 2014;20(6):596–608.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Tang YL, Zhao Q, Qin X, Shen L, Cheng L, Ge J, Phillips MI. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg 2005;80(1):229–36; discussion 36–7.Google Scholar
  44. 44.
    Baraniak PR, McDevitt TC. Stem cell paracrine actions and tissue regeneration. Regen Med. 2010;5(1):121–43.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Wakitani S, Imoto K, Yamamoto T, Saito M, Murata N, Yoneda M. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage. 2002;10(3):199–206.PubMedCrossRefGoogle Scholar
  46. 46.
    Kuroda R, Ishida K, Matsumoto T, Akisue T, Fujioka H, Mizuno K, Ohgushi H, Wakitani S, Kurosaka M. Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage. 2007;15(2):226–31.PubMedCrossRefGoogle Scholar
  47. 47.
    Nejadnik H, Hui JH, Feng Choong EP, Tai BC, Lee EH. Autologous bone marrow-derived mesenchymal stem cells versus autologous chondrocyte implantation: an observational cohort study. Am J Sports Med. 2010;38(6):1110–6.PubMedCrossRefGoogle Scholar
  48. 48.
    Hwang ES. Senescence suppressors: their practical importance in replicative lifespan extension in stem cells. Cell Mol Life Sci. 2014;71(21):4207–19.PubMedCrossRefGoogle Scholar
  49. 49.
    Rosland GV, Svendsen A, Torsvik A, Sobala E, McCormack E, Immervoll H, Mysliwietz J, Tonn JC, Goldbrunner R, Lonning PE, Bjerkvig R, Schichor C. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res. 2009;69(13):5331–9.PubMedCrossRefGoogle Scholar
  50. 50.
    Hillel AT, Taube JM, Cornish TC, Sharma B, Halushka M, McCarthy EF, Hutchins GM, Elisseeff JH. Characterization of human mesenchymal stem cell-engineered cartilage: analysis of its ultrastructure, cell density and chondrocyte phenotype compared to native adult and fetal cartilage. Cells Tissues Organs. 2010;191(1):12–20.PubMedCrossRefGoogle Scholar
  51. 51.
    Huey DJ, Hu JC, Athanasiou KA. Unlike bone, cartilage regeneration remains elusive. Science. 2012;338(6109):917–21.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Vonk LA, de Windt TS, Slaper-Cortenbach IC, Saris DB. Autologous, allogeneic, induced pluripotent stem cell or a combination stem cell therapy? Where are we headed in cartilage repair and why: a concise review. Stem Cell Res Ther. 2015;6:94.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Hunziker EB, Lippuner K, Keel MJ, Shintani N. An educational review of cartilage repair: precepts & practice—myths & misconceptions—progress & prospects. Osteoarthritis Cartilage. 2015;23(3):334–50.PubMedCrossRefGoogle Scholar
  54. 54.
    Friedenstein AJ, Piatetzky II S, Petrakova KV. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol. 1966;16(3):381–90.PubMedGoogle Scholar
  55. 55.
    Kristjansson B, Honsawek S. Current perspectives in mesenchymal stem cell therapies for osteoarthritis. Stem Cells Int. 2014;2014:194318.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Shintani N, Hunziker EB. Differential effects of dexamethasone on the chondrogenesis of mesenchymal stromal cells: influence of microenvironment, tissue origin and growth factor. Eur Cell Mater. 2011;22:302–19; discussion 19–20.Google Scholar
  57. 57.
    Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res. 1998;238(1):265–72.PubMedCrossRefGoogle Scholar
  58. 58.
    Wang WG, Lou SQ, Ju XD, Xia K, Xia JH. In vitro chondrogenesis of human bone marrow-derived mesenchymal progenitor cells in monolayer culture: activation by transfection with TGF-beta2. Tissue Cell. 2003;35(1):69–77.PubMedCrossRefGoogle Scholar
  59. 59.
    Wakitani S, Goto T, Pineda SJ, Young RG, Mansour JM, Caplan AI, Goldberg VM. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am. 1994;76(4):579–92.PubMedCrossRefGoogle Scholar
  60. 60.
    Gao J, Dennis JE, Solchaga LA, Awadallah AS, Goldberg VM, Caplan AI. Tissue-engineered fabrication of an osteochondral composite graft using rat bone marrow-derived mesenchymal stem cells. Tissue Eng. 2001;7(4):363–71.PubMedCrossRefGoogle Scholar
  61. 61.
    Yang Q, Peng J, Lu SB, Guo QY, Zhao B, Zhang L, Wang AY, Xu WJ, Xia Q, Ma XL, Hu YC, Xu BS. Evaluation of an extracellular matrix-derived acellular biphasic scaffold/cell construct in the repair of a large articular high-load-bearing osteochondral defect in a canine model. Chin Med J (Engl). 2011;124(23):3930–8.Google Scholar
  62. 62.
    Mrugala D, Bony C, Neves N, Caillot L, Fabre S, Moukoko D, Jorgensen C, Noel D. Phenotypic and functional characterisation of ovine mesenchymal stem cells: application to a cartilage defect model. Ann Rheum Dis. 2008;67(3):288–95.PubMedCrossRefGoogle Scholar
  63. 63.
    Haleem AM, Singergy AA, Sabry D, Atta HM, Rashed LA, Chu CR, El Shewy MT, Azzam A, Abdel Aziz MT. The clinical use of human culture-expanded autologous bone marrow mesenchymal stem cells transplanted on platelet-rich fibrin glue in the treatment of articular cartilage defects: a pilot study and preliminary results. Cartilage. 2010;1(4):253–61.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Gopal K, Amirhamed HA, Kamarul T. Advances of human bone marrow-derived mesenchymal stem cells in the treatment of cartilage defects: a systematic review. Exp Biol Med (Maywood). 2014;239(6):663–9.CrossRefGoogle Scholar
  65. 65.
    Deans RJ, Moseley AB. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol. 2000;28(8):875–84.PubMedCrossRefGoogle Scholar
  66. 66.
    Muschler GF, Nitto H, Boehm CA, Easley KA. Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res. 2001;19(1):117–25.PubMedCrossRefGoogle Scholar
  67. 67.
    Stenderup K, Justesen J, Clausen C, Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone. 2003;33(6):919–26.PubMedCrossRefGoogle Scholar
  68. 68.
    Mendes SC, Tibbe JM, Veenhof M, Bakker K, Both S, Platenburg PP, Oner FC, de Bruijn JD, van Blitterswijk CA. Bone tissue-engineered implants using human bone marrow stromal cells: effect of culture conditions and donor age. Tissue Eng. 2002;8(6):911–20.PubMedCrossRefGoogle Scholar
  69. 69.
    Makris EA, Gomoll AH, Malizos KN, Hu JC, Athanasiou KA. Repair and tissue engineering techniques for articular cartilage. Nat Rev Rheumatol. 2015;11(1):21–34.PubMedCrossRefGoogle Scholar
  70. 70.
    Strem BM, Hicok KC, Zhu M, Wulur I, Alfonso Z, Schreiber RE, Fraser JK, Hedrick MH. Multipotential differentiation of adipose tissue-derived stem cells. Keio J Med. 2005;54(3):132–41.PubMedCrossRefGoogle Scholar
  71. 71.
    Manferdini C, Maumus M, Gabusi E, Piacentini A, Filardo G, Peyrafitte JA, Jorgensen C, Bourin P, Fleury-Cappellesso S, Facchini A, Noel D, Lisignoli G. Adipose-derived mesenchymal stem cells exert antiinflammatory effects on chondrocytes and synoviocytes from osteoarthritis patients through prostaglandin E2. Arthritis Rheum. 2013;65(5):1271–81.PubMedCrossRefGoogle Scholar
  72. 72.
    Parker AM, Katz AJ. Adipose-derived stem cells for the regeneration of damaged tissues. Expert Opin Biol Ther. 2006;6(6):567–78.PubMedCrossRefGoogle Scholar
  73. 73.
    Boquest AC, Shahdadfar A, Fronsdal K, Sigurjonsson O, Tunheim SH, Collas P, Brinchmann JE. Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture. Mol Biol Cell. 2005;16(3):1131–41.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7(2):211–28.PubMedCrossRefGoogle Scholar
  75. 75.
    Bauge C, Boumediene K. Use of adult stem cells for cartilage tissue engineering: current status and future developments. Stem Cells Int. 2015;2015:438026.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun. 2002;290(2):763–9.PubMedCrossRefGoogle Scholar
  77. 77.
    Wu L, Cai X, Zhang S, Karperien M, Lin Y. Regeneration of articular cartilage by adipose tissue derived mesenchymal stem cells: perspectives from stem cell biology and molecular medicine. J Cell Physiol. 2013;228(5):938–44.PubMedCrossRefGoogle Scholar
  78. 78.
    Mizuno H, Itoi Y, Kawahara S, Ogawa R, Akaishi S, Hyakusoku H. In vivo adipose tissue regeneration by adipose-derived stromal cells isolated from GFP transgenic mice. Cells Tissues Organs. 2008;187(3):177–85.PubMedCrossRefGoogle Scholar
  79. 79.
    Fernandez FB, Shenoy S, Suresh Babu S, Varma HK, John A. Short-term studies using ceramic scaffolds in lapine model for osteochondral defect amelioration. Biomed Mater. 2012;7(3):035005.PubMedCrossRefGoogle Scholar
  80. 80.
    Pak J, Lee JH, Kartolo WA, Lee SH. Cartilage regeneration in human with adipose tissue-derived stem cells: current status in clinical implications. Biomed Res Int. 2016;2016:4702674.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Michalek J, Moster R, Lukac L, Proefrock K, Petrasovic M, Rybar J, Capkova M, Chaloupka A, Darinskas A, Michalek J Sr, Kristek J, Travnik J, Jabandziev P, Cibulka M, Holek M, Jurik M, Skopalik J, Kristkova Z, Dudasova Z. Autologous adipose tissue-derived stromal vascular fraction cells application in patients with osteoarthritis. Cell Transplant 2015.Google Scholar
  82. 82.
    Boeuf S, Richter W. Chondrogenesis of mesenchymal stem cells: role of tissue source and inducing factors. Stem Cell Res Ther. 2010;1(4):31.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Jones BA, Pei M. Synovium-derived stem cells: a tissue-specific stem cell for cartilage engineering and regeneration. Tissue Eng Part B Rev. 2012;18(4):301–11.PubMedCrossRefGoogle Scholar
  84. 84.
    Pei M, He F, Kish VL, Vunjak-Novakovic G. Engineering of functional cartilage tissue using stem cells from synovial lining: a preliminary study. Clin Orthop Relat Res. 2008;466(8):1880–9.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Futami I, Ishijima M, Kaneko H, Tsuji K, Ichikawa-Tomikawa N, Sadatsuki R, Muneta T, Arikawa-Hirasawa E, Sekiya I, Kaneko K. Isolation and characterization of multipotential mesenchymal cells from the mouse synovium. PLoS One. 2012;7(9):e45517.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Ito S, Sato M, Yamato M, Mitani G, Kutsuna T, Nagai T, Ukai T, Kobayashi M, Kokubo M, Okano T, Mochida J. Repair of articular cartilage defect with layered chondrocyte sheets and cultured synovial cells. Biomaterials. 2012;33(21):5278–86.PubMedCrossRefGoogle Scholar
  87. 87.
    Shintani N, Siebenrock KA, Hunziker EB. TGF-ss1 enhances the BMP-2-induced chondrogenesis of bovine synovial explants and arrests downstream differentiation at an early stage of hypertrophy. PLoS One. 2013;8(1):e53086.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Koga H, Muneta T, Ju YJ, Nagase T, Nimura A, Mochizuki T, Ichinose S, von der Mark K, Sekiya I. Synovial stem cells are regionally specified according to local microenvironments after implantation for cartilage regeneration. Stem Cells. 2007;25(3):689–96.PubMedCrossRefGoogle Scholar
  89. 89.
    Sekiya I, Muneta T, Koga H, Nimura A, Morito T, Shimaya M, Mochizuki T, Segawa Y, Sakaguchi Y, Tsuji K, Ichinose S. [Articular cartilage regeneration with synovial mesenchymal stem cells]. Clin Calcium. 2011;21(6):879–89.Google Scholar
  90. 90.
    Chong PP, Selvaratnam L, Abbas AA, Kamarul T. Human peripheral blood derived mesenchymal stem cells demonstrate similar characteristics and chondrogenic differentiation potential to bone marrow derived mesenchymal stem cells. J Orthop Res. 2012;30(4):634–42.PubMedCrossRefGoogle Scholar
  91. 91.
    Iwata H, Ono S, Sato K, Sato T, Kawamura M. Bone morphogenetic protein-induced muscle- and synovium-derived cartilage differentiation in vitro. Clin Orthop Relat Res. 1993;296:295–300.Google Scholar
  92. 92.
    Park J, Gelse K, Frank S, von der Mark K, Aigner T, Schneider H. Transgene-activated mesenchymal cells for articular cartilage repair: a comparison of primary bone marrow-, perichondrium/periosteum- and fat-derived cells. J Gene Med. 2006;8(1):112–25.PubMedCrossRefGoogle Scholar
  93. 93.
    Hilkens P, Gervois P, Fanton Y, Vanormelingen J, Martens W, Struys T, Politis C, Lambrichts I, Bronckaers A. Effect of isolation methodology on stem cell properties and multilineage differentiation potential of human dental pulp stem cells. Cell Tissue Res. 2013;353(1):65–78.PubMedCrossRefGoogle Scholar
  94. 94.
    Richardson SM, Kalamegam G, Pushparaj PN, Matta C, Memic A, Khademhosseini A, Mobasheri R, Poletti FL, Hoyland JA, Mobasheri A. Mesenchymal stem cells in regenerative medicine: focus on articular cartilage and intervertebral disc regeneration. Methods. 2016;99:69–80.PubMedCrossRefGoogle Scholar
  95. 95.
    Zvaifler NJ, Marinova-Mutafchieva L, Adams G, Edwards CJ, Moss J, Burger JA, Maini RN. Mesenchymal precursor cells in the blood of normal individuals. Arthritis Res. 2000;2(6):477–88.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Saw KY, Anz A, Siew-Yoke Jee C, Merican S, Ching-Soong Ng R, Roohi SA, Ragavanaidu K. Articular cartilage regeneration with autologous peripheral blood stem cells versus hyaluronic acid: a randomized controlled trial. Arthroscopy. 2013;29(4):684–94.PubMedCrossRefGoogle Scholar
  97. 97.
    Asakura A, Komaki M, Rudnicki M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation. 2001;68(4–5):245–53.PubMedCrossRefGoogle Scholar
  98. 98.
    Andriamanalijaona R, Duval E, Raoudi M, Lecourt S, Vilquin JT, Marolleau JP, Pujol JP, Galera P, Boumediene K. Differentiation potential of human muscle-derived cells towards chondrogenic phenotype in alginate beads culture. Osteoarthritis Cartilage. 2008;16(12):1509–18.PubMedCrossRefGoogle Scholar
  99. 99.
    Usas A, Maciulaitis J, Maciulaitis R, Jakuboniene N, Milasius A, Huard J. Skeletal muscle-derived stem cells: implications for cell-mediated therapies. Medicina (Kaunas). 2011;47(9):469–79.Google Scholar
  100. 100.
    Mara CS, Sartori AR, Duarte AS, Andrade AL, Pedro MA, Coimbra IB. Periosteum as a source of mesenchymal stem cells: the effects of TGF-beta3 on chondrogenesis. Clinics (Sao Paulo). 2011;66(3):487–92.CrossRefGoogle Scholar
  101. 101.
    De Bari C, Dell’Accio F, Luyten FP. Human periosteum-derived cells maintain phenotypic stability and chondrogenic potential throughout expansion regardless of donor age. Arthritis Rheum. 2001;44(1):85–95.PubMedCrossRefGoogle Scholar
  102. 102.
    Deng S, Huang R, Wang J, Zhang S, Chen Z, Wu S, Jiang Y, Peng Q, Cai X, Lin Y. Miscellaneous animal models accelerate the application of mesenchymal stem cells for cartilage regeneration. Curr Stem Cell Res Ther. 2014;9(3):223–33.PubMedCrossRefGoogle Scholar
  103. 103.
    Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol. 2000;109(1):235–42.PubMedCrossRefGoogle Scholar
  104. 104.
    McElreavey KD, Irvine AI, Ennis KT, McLean WH. Isolation, culture and characterisation of fibroblast-like cells derived from the Wharton’s jelly portion of human umbilical cord. Biochem Soc Trans. 1991;19(1):29s.PubMedCrossRefGoogle Scholar
  105. 105.
    Yoshimura H, Muneta T, Nimura A, Yokoyama A, Koga H, Sekiya I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res. 2007;327(3):449–62.PubMedCrossRefGoogle Scholar
  106. 106.
    Shirasawa S, Sekiya I, Sakaguchi Y, Yagishita K, Ichinose S, Muneta T. In vitro chondrogenesis of human synovium-derived mesenchymal stem cells: optimal condition and comparison with bone marrow-derived cells. J Cell Biochem. 2006;97(1):84–97.PubMedCrossRefGoogle Scholar
  107. 107.
    Nathan S, Das De S, Thambyah A, Fen C, Goh J, Lee EH. Cell-based therapy in the repair of osteochondral defects: a novel use for adipose tissue. Tissue Eng. 2003;9(4):733–44.PubMedCrossRefGoogle Scholar
  108. 108.
    Huang JI, Kazmi N, Durbhakula MM, Hering TM, Yoo JU, Johnstone B. Chondrogenic potential of progenitor cells derived from human bone marrow and adipose tissue: a patient-matched comparison. J Orthop Res. 2005;23(6):1383–9.PubMedCrossRefGoogle Scholar
  109. 109.
    Baksh D, Yao R, Tuan RS. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells. 2007;25(6):1384–92.PubMedCrossRefGoogle Scholar
  110. 110.
    Kern S, Eichler H, Stoeve J, Kluter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem cells. 2006;24(5):1294–301.PubMedCrossRefGoogle Scholar
  111. 111.
    Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663–76.PubMedCrossRefGoogle Scholar
  112. 112.
    Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131(5):861–72.PubMedCrossRefGoogle Scholar
  113. 113.
    Loh YH, Agarwal S, Park IH, Urbach A, Huo H, Heffner GC, Kim K, Miller JD, Ng K, Daley GQ. Generation of induced pluripotent stem cells from human blood. Blood. 2009;113(22):5476–9.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Wei Y, Zeng W, Wan R, Wang J, Zhou Q, Qiu S, Singh SR. Chondrogenic differentiation of induced pluripotent stem cells from osteoarthritic chondrocytes in alginate matrix. Eur Cell Mater. 2012;23:1–12.PubMedCrossRefGoogle Scholar
  115. 115.
    Guzzo RM, Gibson J, Xu RH, Lee FY, Drissi H. Efficient differentiation of human iPSC-derived mesenchymal stem cells to chondroprogenitor cells. J Cell Biochem. 2013;114(2):480–90.PubMedCrossRefGoogle Scholar
  116. 116.
    Kastenberg ZJ, Odorico JS. Alternative sources of pluripotency: science, ethics, and stem cells. Transplant Rev (Orlando). 2008;22(3):215–22.CrossRefGoogle Scholar
  117. 117.
    Zhao T, Zhang ZN, Rong Z, Xu Y. Immunogenicity of induced pluripotent stem cells. Nature. 2011;474(7350):212–5.PubMedCrossRefGoogle Scholar
  118. 118.
    Quarto N, Leonard B, Li S, Marchand M, Anderson E, Behr B, Francke U, Reijo-Pera R, Chiao E, Longaker MT. Skeletogenic phenotype of human Marfan embryonic stem cells faithfully phenocopied by patient-specific induced-pluripotent stem cells. Proc Natl Acad Sci U S A. 2012;109(1):215–20.PubMedCrossRefGoogle Scholar
  119. 119.
    O’Sullivan J, D'Arcy S, Barry FP, Murphy JM, Coleman CM. Mesenchymal chondroprogenitor cell origin and therapeutic potential. Stem Cell Res Ther. 2011;2(1):8.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Williams R, Khan IM, Richardson K, Nelson L, McCarthy HE, Analbelsi T, Singhrao SK, Dowthwaite GP, Jones RE, Baird DM, Lewis H, Roberts S, Shaw HM, Dudhia J, Fairclough J, Briggs T, Archer CW. Identification and clonal characterisation of a progenitor cell sub-population in normal human articular cartilage. PLoS One. 2010;5(10):e13246.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Khan IM, Bishop JC, Gilbert S, Archer CW. Clonal chondroprogenitors maintain telomerase activity and Sox9 expression during extended monolayer culture and retain chondrogenic potential. Osteoarthritis Cartilage. 2009;17(4):518–28.PubMedCrossRefGoogle Scholar
  122. 122.
    McCarthy HE, Bara JJ, Brakspear K, Singhrao SK, Archer CW. The comparison of equine articular cartilage progenitor cells and bone marrow-derived stromal cells as potential cell sources for cartilage repair in the horse. Vet J. 2012;192(3):345–51.PubMedCrossRefGoogle Scholar
  123. 123.
    van Osch GJ, Brittberg M, Dennis JE, Bastiaansen-Jenniskens YM, Erben RG, Konttinen YT, Luyten FP. Cartilage repair: past and future—lessons for regenerative medicine. J Cell Mol Med. 2009;13(5):792–810.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Vats A, Bielby RC, Tolley N, Dickinson SC, Boccaccini AR, Hollander AP, Bishop AE, Polak JM. Chondrogenic differentiation of human embryonic stem cells: the effect of the micro-environment. Tissue Eng. 2006;12(6):1687–97.PubMedCrossRefGoogle Scholar
  125. 125.
    Sui Y, Clarke T, Khillan JS. Limb bud progenitor cells induce differentiation of pluripotent embryonic stem cells into chondrogenic lineage. Differentiation. 2003;71(9–10):578–85.PubMedCrossRefGoogle Scholar
  126. 126.
    Yodmuang S, Marolt D, Marcos-Campos I, Gadjanski I, Vunjak-Novakovic G. Synergistic effects of hypoxia and morphogenetic factors on early chondrogenic commitment of human embryonic stem cells in embryoid body culture. Stem Cell Rev. 2015;11(2):228–41.PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Scarfi S. Use of bone morphogenetic proteins in mesenchymal stem cell stimulation of cartilage and bone repair. World J Stem Cells. 2016;8(1):1–12.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Marsano A, Medeiros da Cunha CM, Ghanaati S, Gueven S, Centola M, Tsaryk R, Barbeck M, Stuedle C, Barbero A, Helmrich U, Schaeren S, Kirkpatrick JC, Banfi A, Martin I. Spontaneous in vivo chondrogenesis of bone marrow-derived mesenchymal progenitor cells by blocking vascular endothelial growth factor signaling. Stem Cells Transl Med. 2016;5(12):1730–1738.Google Scholar
  129. 129.
    Miyanishi K, Trindade MC, Lindsey DP, Beaupre GS, Carter DR, Goodman SB, Schurman DJ, Smith RL. Effects of hydrostatic pressure and transforming growth factor-beta 3 on adult human mesenchymal stem cell chondrogenesis in vitro. Tissue Eng. 2006;12(6):1419–28.PubMedCrossRefGoogle Scholar
  130. 130.
    Toh WS, Lee EH, Cao T. Potential of human embryonic stem cells in cartilage tissue engineering and regenerative medicine. Stem Cell Rev. 2011;7(3):544–59.PubMedCrossRefGoogle Scholar
  131. 131.
    Singh Khillan J. Differentiation of embryonic stem cells into cartilage cells. Curr Protoc Stem Cell Biol. 2007;Chapter 1:Unit 1F.Google Scholar
  132. 132.
    Paschos NK, Brown WE, Eswaramoorthy R, Hu JC, Athanasiou KA. Advances in tissue engineering through stem cell-based co-culture. J Tissue Eng Regen Med. 2015;9(5):488–503.PubMedCrossRefGoogle Scholar
  133. 133.
    McIntosh Ambrose W, Schein O, Elisseeff J. A tale of two tissues: stem cells in cartilage and corneal tissue engineering. Curr Stem Cell Res Ther. 2010;5(1):37–48.PubMedCrossRefGoogle Scholar
  134. 134.
    Hwang NS, Varghese S, Elisseeff J. Derivation of chondrogenically-committed cells from human embryonic cells for cartilage tissue regeneration. PLoS One. 2008;3(6):e2498.PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Hwang NS, Varghese S, Lee HJ, Zhang Z, Ye Z, Bae J, Cheng L, Elisseeff J. In vivo commitment and functional tissue regeneration using human embryonic stem cell-derived mesenchymal cells. Proc Natl Acad Sci U S A. 2008;105(52):20641–6.PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Lettry V, Hosoya K, Takagi S, Okumura M. Coculture of equine mesenchymal stem cells and mature equine articular chondrocytes results in improved chondrogenic differentiation of the stem cells. Jpn J Vet Res. 2010;58(1):5–15.PubMedGoogle Scholar
  137. 137.
    Aung A, Gupta G, Majid G, Varghese S. Osteoarthritic chondrocyte-secreted morphogens induce chondrogenic differentiation of human mesenchymal stem cells. Arthritis Rheum. 2011;63(1):148–58.PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Amarilio R, Viukov SV, Sharir A, Eshkar-Oren I, Johnson RS, Zelzer E. HIF1alpha regulation of Sox9 is necessary to maintain differentiation of hypoxic prechondrogenic cells during early skeletogenesis. Development. 2007;134(21):3917–28.PubMedCrossRefGoogle Scholar
  139. 139.
    Ezashi T, Das P, Roberts RM. Low O2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci U S A. 2005;102(13):4783–8.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Koay EJ, Athanasiou KA. Hypoxic chondrogenic differentiation of human embryonic stem cells enhances cartilage protein synthesis and biomechanical functionality. Osteoarthritis Cartilage. 2008;16(12):1450–6.PubMedCrossRefGoogle Scholar
  141. 141.
    Teramura T, Onodera Y, Takehara T, Frampton J, Matsuoka T, Ito S, Nakagawa K, Miki Y, Hosoi Y, Hamanishi C, Fukuda K. Induction of functional mesenchymal stem cells from rabbit embryonic stem cells by exposure to severe hypoxic conditions. Cell Transplant. 2013;22(2):309–29.PubMedCrossRefGoogle Scholar
  142. 142.
    Markway BD, Cho H, Zilberman-Rudenko J, Holden P, McAlinden A, Johnstone B. Hypoxia-inducible factor 3-alpha expression is associated with the stable chondrocyte phenotype. J Orthop Res. 2015;33(11):1561–70.PubMedCrossRefGoogle Scholar
  143. 143.
    Zscharnack M, Poesel C, Galle J, Bader A. Low oxygen expansion improves subsequent chondrogenesis of ovine bone-marrow-derived mesenchymal stem cells in collagen type I hydrogel. Cells Tissues Organs. 2009;190(2):81–93.PubMedCrossRefGoogle Scholar
  144. 144.
    Khan WS, Adesida AB, Hardingham TE. Hypoxic conditions increase hypoxia-inducible transcription factor 2alpha and enhance chondrogenesis in stem cells from the infrapatellar fat pad of osteoarthritis patients. Arthritis Res Ther. 2007;9(3):R55.PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Cicione C, Muinos-Lopez E, Hermida-Gomez T, Fuentes-Boquete I, Diaz-Prado S, Blanco FJ. Effects of severe hypoxia on bone marrow mesenchymal stem cells differentiation potential. Stem Cells Int. 2013;2013:232896.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Gawlitta D, van Rijen MH, Schrijver EJ, Alblas J, Dhert WJ. Hypoxia impedes hypertrophic chondrogenesis of human multipotent stromal cells. Tissue Eng Part A. 2012;18(19–20):1957–66.PubMedCrossRefGoogle Scholar
  147. 147.
    Safran MR, Kim H, Zaffagnini S. The use of scaffolds in the management of articular cartilage injury. J Am Acad Orthop Surg. 2008;16(6):306–11.PubMedCrossRefGoogle Scholar
  148. 148.
    Crawford DC, Heveran CM, Cannon Jr WD, Foo LF, Potter HG. An autologous cartilage tissue implant NeoCart for treatment of grade III chondral injury to the distal femur: prospective clinical safety trial at 2 years. Am J Sports Med. 2009;37(7):1334–43.PubMedCrossRefGoogle Scholar
  149. 149.
    Williams CG, Kim TK, Taboas A, Malik A, Manson P, Elisseeff J. In vitro chondrogenesis of bone marrow-derived mesenchymal stem cells in a photopolymerizing hydrogel. Tissue Eng. 2003;9(4):679–88.PubMedCrossRefGoogle Scholar
  150. 150.
    Li WJ, Danielson KG, Alexander PG, Tuan RS. Biological response of chondrocytes cultured in three-dimensional nanofibrous poly(epsilon-caprolactone) scaffolds. J Biomed Mater Res A. 2003;67(4):1105–14.PubMedCrossRefGoogle Scholar
  151. 151.
    Coleman RM, Case ND, Guldberg RE. Hydrogel effects on bone marrow stromal cell response to chondrogenic growth factors. Biomaterials. 2007;28(12):2077–86.PubMedCrossRefGoogle Scholar
  152. 152.
    Xu J, Wang W, Ludeman M, Cheng K, Hayami T, Lotz JC, Kapila S. Chondrogenic differentiation of human mesenchymal stem cells in three-dimensional alginate gels. Tissue Eng Part A. 2008;14(5):667–80.PubMedCrossRefGoogle Scholar
  153. 153.
    Majumdar MK, Banks V, Peluso DP, Morris EA. Isolation, characterization, and chondrogenic potential of human bone marrow-derived multipotential stromal cells. J Cell Physiol. 2000;185(1):98–106.PubMedCrossRefGoogle Scholar
  154. 154.
    Shen Y, Fu Y, Wang J, Li G, Zhang X, Xu Y, Lin Y. Biomaterial and mesenchymal stem cell for articular cartilage reconstruction. Curr Stem Cell Res Ther. 2014;9(3):254–67.PubMedCrossRefGoogle Scholar
  155. 155.
    Kawaguchi J, Mee PJ, Smith AG. Osteogenic and chondrogenic differentiation of embryonic stem cells in response to specific growth factors. Bone. 2005;36(5):758–69.PubMedCrossRefGoogle Scholar
  156. 156.
    Fan H, Hu Y, Qin L, Li X, Wu H, Lv R. 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. 2006;77(4):785–94.PubMedCrossRefGoogle Scholar
  157. 157.
    Nixon AJ, Fortier LA, Williams J, Mohammed H. Enhanced repair of extensive articular defects by insulin-like growth factor-I-laden fibrin composites. J Orthop Res. 1999;17(4):475–87.PubMedCrossRefGoogle Scholar
  158. 158.
    Ikeda T, Kamekura S, Mabuchi A, Kou I, Seki S, Takato T, Nakamura K, Kawaguchi H, Ikegawa S, Chung UI. The combination of SOX5, SOX6, and SOX9 (the SOX trio) provides signals sufficient for induction of permanent cartilage. Arthritis Rheum. 2004;50(11):3561–73.PubMedCrossRefGoogle Scholar
  159. 159.
    Huang CY, Reuben PM, Cheung HS. Temporal expression patterns and corresponding protein inductions of early responsive genes in rabbit bone marrow-derived mesenchymal stem cells under cyclic compressive loading. Stem Cells. 2005;23(8):1113–21.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Quanquan Ma
    • 1
  • Taoran Tian
    • 1
  • Nanxin Liu
    • 1
  • Mi Zhou
    • 1
  • Xiaoxiao Cai
    • 1
    Email author
  1. 1.State Key Laboratory of Oral DiseasesWest China Hospital of Stomatology, Sichuan UniversityChengduChina

Personalised recommendations