Cell and Tissue Research

, Volume 372, Issue 1, pp 13–22 | Cite as

Tissue-derived scaffolds and cells for articular cartilage tissue engineering: characteristics, applications and progress

  • Xuejian Liu
  • Haoye Meng
  • Quanyi Guo
  • Baichuan Sun
  • Kaihong Zhang
  • Wen Yu
  • Shichen Liu
  • Yu Wang
  • Xiaoguang Jing
  • Zengzeng Zhang
  • Jiang Peng
  • Jianhua Yang
Review
  • 181 Downloads

Abstract

There are many factors to consider in the field of tissue engineering. For articular cartilage repair, this includes seed cells, scaffolds and chondrotrophic hormones. This review primarily focuses on the seed cells and scaffolds. Extracellular matrix proteins provide a natural scaffold for cell attachment, proliferation and differentiation. The structure and composition of tissue-derived scaffolds and native tissue are almost identical. As such, tissue-derived scaffolds hold great promise for biomedical applications. However, autologous tissue-derived scaffolds also have many drawbacks for transplantation, as harvesting autografts is limited to available donor sites and requires secondary surgery, therefore imparting additional damage to the body. This review summarizes and analyzes various cell sources and tissue-derived scaffolds applied in orthopedic tissue engineering.

Keywords

Tissue engineering Tissue-derived scaffold Seed cells Extracellular matrix Articular cartilage 

Notes

Acknowledgements

This study was supported by the National Natural Science Foundation of China (81572148), National Key Research and Development Program of China (2016YFC1102104), the People’s Liberation Army 13th 5-year plan period (BWS13C029), Beijing Municipal Science and Technology Project (Z161100005016059) and Basic research project of Education Department of Heilongjiang (2016-KYYWF-0548).

Compliance with ethical standards

Disclosure Statement

No competing financial interests exist.

References

  1. Albrecht FH (1983) Closure of joint cartilage defects using cartilage fragments and fibrin glue. Fortschr Med 101:1650–1652PubMedGoogle Scholar
  2. Anraku K, Sato S, Jacob NT, Eubanks LM, Ellis BA, Janda KD (2017) The design and synthesis of an α-gal trisaccharide epitope that provides a highly specific anti-gal immune response. Organic Biomol Chem 15:2979CrossRefGoogle Scholar
  3. Baksh D, Yao R, Tuan RS (2007) Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells 25:1384–1392CrossRefPubMedGoogle Scholar
  4. Batsali AK, Pontikoglou C, Koutroulakis D, Pavlaki KI, Damianaki A, Mavroudi I, Alpantaki K, Kouvidi E, Kontakis G, Papadaki HA (2017) Differential expression of cell cycle and WNT pathway-related genes accounts for differences in the growth and differentiation potential of Wharton’s jelly and bone marrow-derived mesenchymal stem cells. Stem Cell Res Ther 8Google Scholar
  5. Chen CH, Lee MY, Shyu VB, Chen YC, Chen CT, Chen JP (2014) Surface modification of polycaprolactone scaffolds fabricated via selective laser sintering for cartilage tissue engineering. Mater Sci Eng C Mater Biol Appl 40:389–397CrossRefPubMedGoogle Scholar
  6. Cheng CW, Solorio LD, Alsberg E (2014) Decellularized tissue and cell-derived extracellular matrices as scaffolds for orthopaedic tissue engineering. Biotechnol Adv 32:462–484CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cole BJ (2008) A randomized trial comparing autologous chondrocyte implantation with microfracture. J Bone Joint Surg Am 90:1165 author reply 1165-1166CrossRefPubMedGoogle Scholar
  8. Danisovic L, Oravcova L, Krajciova L, Varchulova NZ, Bohac M, Varga I, Vojtassak J (2017) Effect of long-term culture on the biological and morphological characteristics of human adipose tissue-derived stem cells. J Physiol Pharmacol 68:149PubMedGoogle Scholar
  9. Darling EM, Athanasiou KA (2005) Growth factor impact on articular cartilage subpopulations. Cell Tissue Res 322:463–473CrossRefPubMedGoogle Scholar
  10. Elder BD, Eleswarapu SV, Athanasiou KA (2009) Extraction techniques for the decellularization of tissue engineered articular cartilage constructs. Biomaterials 30:3749–3756CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fisher MB, Belkin NS, Milby AH, Henning EA, Bostrom M, Kim M, Pfeifer C, Meloni G, Dodge GR, Burdick JA, Schaer TP, Steinberg DR, Mauck RL (2015) Cartilage repair and subchondral bone remodeling in response to focal lesions in a mini-pig model: implications for tissue engineering. Tissue Eng A 21:850–860CrossRefGoogle Scholar
  12. Foldager CB, Gomoll AH, Lind M, Spector M (2012) Cell seeding densities in Autologous Chondrocyte implantation techniques for cartilage repair. Cartilage 3:108–117CrossRefPubMedPubMedCentralGoogle Scholar
  13. Geraghty S, Kuang JQ, Yoo D, LeRoux-Williams M, Vangsness CT Jr, Danilkovitch A (2015) A novel, cryopreserved, viable osteochondral allograft designed to augment marrow stimulation for articular cartilage repair. J Orthop Surg Res 10:66CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gilbert TW, Sellaro TL, Badylak SF (2006) Decellularization of tissues and organs. Biomaterials 27:3675–3683PubMedGoogle Scholar
  15. Goldberg A, Mitchell K, Soans J, Kim L, Zaidi R (2017) The use of mesenchymal stem cells for cartilage repair and regeneration: a systematic review. J Orthop Surg Res 12:39CrossRefPubMedPubMedCentralGoogle Scholar
  16. Haleem AM, Singergy AA, Sabry D, Atta HM, Rashed LA, Chu CR, El Shewy MT, Azzam A, Abdel Aziz MT (2010) 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 1:253–261CrossRefPubMedPubMedCentralGoogle Scholar
  17. Izadifar Z, Chang T, Kulyk W, Chen X, Eames BF (2016) Analyzing biological performance of 3D-printed, cell-impregnated hybrid constructs for cartilage tissue engineering. Tissue Eng Part C 22:173–188CrossRefGoogle Scholar
  18. Juran CM, Dolwick MF, Mcfetridge PS (2015) Engineered microporosity: enhancing the early regenerative potential of Decellularized Temporomandibular joint discs. Tissue Eng A 21:829CrossRefGoogle Scholar
  19. Kalpakci KN, Brown WE, Hu JC, Athanasiou KA (2014) Cartilage tissue engineering using dermis isolated adult stem cells: the use of hypoxia during expansion versus Chondrogenic differentiation. PLoS ONE 9:e98570CrossRefPubMedPubMedCentralGoogle Scholar
  20. Knutsen G, Drogset JO, Engebretsen L, Grontvedt T, Ludvigsen TC, Loken S, Solheim E, Strand T, Johansen O (2016) A randomized multicenter trial comparing Autologous Chondrocyte implantation with microfracture: long-term follow-up at 14 to 15 years. J Bone Joint Surg Am 98:1332–1339CrossRefPubMedGoogle Scholar
  21. Lakes EH, Matuska AM, McFetridge PS, Allen KD (2016) Mechanical integrity of a decellularized and laser drilled medial meniscus. J Biomech Eng 138(3):031006Google Scholar
  22. Lee HS, Huang GT, Chiang H, Chiou LL, Chen MH, Hsieh CH, Ph.D C-CJMD (2003) Multipotential Mesenchymal stem cells from femoral bone marrow near the site of Osteonecrosis. Stem Cells 21:190Google Scholar
  23. Lin Y, Luo E, Chen X, Liu L, Qiao J, Yan Z, Li Z, Tang W, Zheng X, Tian W (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 9:929-939. J Cell Mol Med 9:929–939CrossRefPubMedGoogle Scholar
  24. Liu S, Jia Y, Yuan M, Guo W, Huang J, Zhao B, Peng J, Xu W, Lu S, Guo Q (2017) Repair of Osteochondral defects using human umbilical cord Wharton's jelly-derived Mesenchymal stem cells in a rabbit model. Biomed Res Int 2017:8760383PubMedPubMedCentralGoogle Scholar
  25. Lumpkins SB, Pierre N, McFetridge PS (2008) A mechanical evaluation of three decellularization methods in the design of a xenogeneic scaffold for tissue engineering the temporomandibular joint disc. Acta Biomater 4:808–816CrossRefPubMedGoogle Scholar
  26. Mankin HJ, Mow VC, Buckwalter JA, Iannotti JB, Ratcliffe A (1999) Articular cartilage structure, composition and function. In: Buckwalter JA, Einhorn TA, Simon SR (eds) Orthopaedic basic science: biology and biomechanics of the musculoskeletal system. American Academy of Orthopaedic Surgeons, Rosemont, IL, pp 444–470Google Scholar
  27. Matsumoto T, Okabe T, Ikawa T, Iida T, Yasuda H, Nakamura H, Wakitani S (2010) Articular cartilage repair with autologous bone marrow mesenchymal cells. J Cell Physiol 225:291–295CrossRefPubMedGoogle Scholar
  28. Mironov V, Visconti RP, Kasyanov V, Forgacs G, Drake CJ, Markwald RR (2009) Organ printing: tissue spheroids as building blocks. Biomaterials 30:2164–2174CrossRefPubMedPubMedCentralGoogle Scholar
  29. Mithoefer K, Williams RJ 3rd, Warren RF, Potter HG, Spock CR, Jones EC, Wickiewicz TL, Marx RG (2005) The microfracture technique for the treatment of articular cartilage lesions in the knee. A prospect cohort study. J Bone Joint Surg Am 87:1911–1920CrossRefPubMedGoogle Scholar
  30. Naumann A, Dennis JE, Aigner J, Coticchia J, Arnold J, Berghaus A, Kastenbauer ER, Caplan AI (2004) Tissue engineering of autologous cartilage grafts in three-dimensional in vitro macroaggregate culture system. Tissue Eng 10:1695–1706CrossRefPubMedGoogle Scholar
  31. Park J, Gelse K, Frank S, von der Mark K, Aigner T, Schneider H (2006) Transgene-activated mesenchymal cells for articular cartilage repair: a comparison of primary bone marrow-, perichondrium/periosteum- and fat-derived cells. J Gene Med 8:112–125CrossRefPubMedGoogle Scholar
  32. Pati F, Jang J, Ha DH, Won Kim S, Rhie JW, Shim JH, Kim DH, Cho DW (2014) Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun 5:3935CrossRefPubMedPubMedCentralGoogle Scholar
  33. Peppas NA, Hilt JZ, Khademhosseini A, Langer R (2006) Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv Mater 18:1345–1360CrossRefGoogle Scholar
  34. Ravindran S, Gao Q, Kotecha M, Magin RL, Karol S, Bedran-Russo A, George A (2012) Biomimetic extracellular matrix-incorporated scaffold induces osteogenic gene expression in human marrow stromal cells. Tissue Eng A 18:295–309CrossRefGoogle Scholar
  35. Reppel L, Schiavi J, Charif N, Leger L, Yu H, Pinzano A, Henrionnet C, Stoltz JF, Bensoussan D, Huselstein C (2015) Chondrogenic induction of mesenchymal stromal/stem cells from Wharton's jelly embedded in alginate hydrogel and without added growth factor: an alternative stem cell source for cartilage tissue engineering. Stem Cell Res Ther 6:260CrossRefPubMedPubMedCentralGoogle Scholar
  36. Risbud MV, Sittinger M (2002) Tissue engineering: advances in in vitro cartilage generation. Trends Biotechnol 20:351–356CrossRefPubMedGoogle Scholar
  37. Rowland CR, Colucci LA, Guilak F (2016) Fabrication of anatomically-shaped cartilage constructs using decellularized cartilage-derived matrix scaffolds. Biomaterials 91:57–72CrossRefPubMedPubMedCentralGoogle Scholar
  38. Saha S, Kirkham J, Wood D, Curran S, Yang XB (2013) Informing future cartilage repair strategies: a comparative study of three different human cell types for cartilage tissue engineering. Cell Tissue Res 352:495–507CrossRefPubMedPubMedCentralGoogle Scholar
  39. Saldin LT, Cramer MC, Velankar SS, White LJ, Badylak SF (2017) Extracellular matrix hydrogels from decellularized tissues: structure and function. Acta Biomater 49:1–15CrossRefPubMedGoogle Scholar
  40. Schnabel M, Marlovits S, Eckhoff G, Fichtel I, Gotzen L, Vécsei V, Schlegel J (2002) Dedifferentiation-associated changes in morphology and gene expression in primary human articular chondrocytes in cell culture. Osteoarthritis Cartil 10:62CrossRefGoogle Scholar
  41. Schwarz S, Koerber L, Elsaesser AF, Goldberg-Bockhorn E, Seitz AM, Durselen L, Ignatius A, Walther P, Breiter R, Rotter N (2012) Decellularized cartilage matrix as a novel biomatrix for cartilage tissue-engineering applications. Tissue Eng A 18:2195–2209CrossRefGoogle Scholar
  42. Schwarz S, Elsaesser AF, Koerber L, Goldberg-Bockhorn E, Seitz AM, Bermueller C, Durselen L, Ignatius A, Breiter R, Rotter N (2015) Processed xenogenic cartilage as innovative biomatrix for cartilage tissue engineering: effects on chondrocyte differentiation and function. J Tissue Eng Regen Med 9:E239–E251CrossRefPubMedGoogle Scholar
  43. Smith BD, Grande DA (2015) The current state of scaffolds for musculoskeletal regenerative applications. Nat Rev Rheumatol 11:213–222CrossRefPubMedGoogle Scholar
  44. Smith GD, Knutsen G, Richardson JB (2005) A clinical review of cartilage repair techniques. J Bone Joint Surg Br 87:445–449CrossRefPubMedGoogle Scholar
  45. Stone KR, Walgenbach A, Galili U (2017) Induced remodeling of porcine tendons to human anterior cruciate ligaments by α-gal epitope removal and partial crosslinking. Tissue Engineering Part BGoogle Scholar
  46. Strauss EJ, Fonseca LE, Shah MR, Yorum T (2011) Management of focal cartilage defects in the knee - is ACI the answer? Bull NYU Hosp Joint Dis 69:63–72Google Scholar
  47. Sutherland AJ, Converse GL, Hopkins RA, Detamore MS (2015) The bioactivity of cartilage extracellular matrix in Articular cartilage regeneration. Adv Healthc Mater 4:29–39CrossRefPubMedGoogle Scholar
  48. Tuli R, Li WJ, Tuan RS (2003) Current state of cartilage tissue engineering. Arthritis Res Ther 5:235–238CrossRefPubMedPubMedCentralGoogle Scholar
  49. Vadala G, Di Martino A, Tirindelli MC, Denaro L, Denaro V (2008) Use of autologous bone marrow cells concentrate enriched with platelet-rich fibrin on corticocancellous bone allograft for posterolateral multilevel cervical fusion. J Tissue Eng Regen Med 2:515–520CrossRefPubMedGoogle Scholar
  50. Vanlauwe J, Huylebroek J, Van Der Bauwhede J, Saris D, Veeckman G, Bobic V, Victor J, Almqvist KF, Verdonk P, Fortems Y, Van Lommel N, Haazen L (2012) Clinical outcomes of characterized Chondrocyte implantation. Cartilage 3:173–180CrossRefPubMedPubMedCentralGoogle Scholar
  51. Vasiliadis HS, Wasiak J, Salanti G (2010) Autologous chondrocyte implantation for the treatment of cartilage lesions of the knee: a systematic review of randomized studies. Knee Surg, Sports Traumatol, Arthroscopy 18:1645–1655CrossRefGoogle Scholar
  52. Veronesi F, Maglio M, Tschon M, Aldini NN, Fini M (2014) Adipose-derived mesenchymal stem cells for cartilage tissue engineering: state-of-the-art in in vivo studies. J Biomed Mater Res A 102:2448–2466CrossRefPubMedGoogle Scholar
  53. Vinatier C, Guicheux J (2016) Cartilage tissue engineering: from biomaterials and stem cells to osteoarthritis treatments. Ann Phys Rehab Med 59:139–144CrossRefGoogle Scholar
  54. Wakitani S, Okabe T, Horibe S, Mitsuoka T, Saito M, Koyama T, Nawata M, Tensho K, Kato H, Uematsu K, Kuroda R, Kurosaka M, Yoshiya S, Hattori K, Ohgushi H (2011) Safety of autologous bone marrow-derived mesenchymal stem cell transplantation for cartilage repair in 41 patients with 45 joints followed for up to 11 years and 5 months. J Tissue Eng Regen Med 5:146–150CrossRefPubMedGoogle Scholar
  55. Wang WG, Lou SQ, Ju XD, Xia K, Xia JH (2003) In vitro chondrogenesis of human bone marrow-derived mesenchymal progenitor cells in monolayer culture: activation by transfection with TGF-beta2. Tissue Cell 35:69CrossRefPubMedGoogle Scholar
  56. Wegmeyer H, Bröske AM, Leddin M, Kuentzer K, Nisslbeck AK, Hupfeld J, Wiechmann K, Kuhlen J, Schwerin CV, Stein C (2013) Mesenchymal Stromal cell characteristics vary depending on their origin. Stem Cells Dev 22:2606–2618CrossRefPubMedPubMedCentralGoogle Scholar
  57. Wei Y, Hu Y, Lv R, Li D (2006) Regulation of adipose-derived adult stem cells differentiating into chondrocytes with the use of rhBMP-2. Cytotherapy 8:570CrossRefPubMedGoogle Scholar
  58. Wei Y, Zeng W, Wan R, Wang J, Zhou Q, Qiu S, Singh SR (2012) Chondrogenic differentiation of induced pluripotent stem cells from osteoarthritic chondrocytes in alginate matrix. Eur Cells Mater 23:1CrossRefGoogle Scholar
  59. Wu LC, Kuo YJ, Sun FW, Chen CH, Chiang CJ, Weng PW, Tsuang YH, Huang YY (2017) Optimized decellularization protocol including α-Gal epitope reduction for fabrication of an acellular porcine annulus fibrosus scaffold. Cell & Tissue Banking 1–14Google Scholar
  60. Yamanaka S, Takahashi K (2006) induction of pluripotent stem cells from mouse fibroblast cultures. Cell 51:2346Google Scholar
  61. Yamashita A, Morioka M, Yahara Y, Okada M, Kobayashi T, Kuriyama S, Matsuda S, Tsumaki N (2015) Generation of scaffoldless hyaline cartilaginous tissue from human iPSCs. Stem Cell Rep 4:404CrossRefGoogle Scholar
  62. Yang Q, Peng J, Guo Q, Huang J, Zhang L, Yao J, Yang F, Wang S, Xu W, Wang A, Lu S (2008) A cartilage ECM-derived 3-D porous acellular matrix scaffold for in vivo cartilage tissue engineering with PKH26-labeled chondrogenic bone marrow-derived mesenchymal stem cells. Biomaterials 29:2378–2387CrossRefPubMedGoogle Scholar
  63. Yin H, Wang Y, Sun Z, Sun X, Xu Y, Li P, Meng H, Yu X, Xiao B, Fan T, Wang Y, Xu W, Wang A, Guo Q, Peng J, Lu S (2016) Induction of mesenchymal stem cell chondrogenic differentiation and functional cartilage microtissue formation for in vivo cartilage regeneration by cartilage extracellular matrix-derived particles. Acta Biomater 33:96–109CrossRefPubMedGoogle Scholar
  64. Zhang W, Zhu Y, Li J, Guo Q, Peng J, Liu S, Yang J, Wang Y (2016) Cell-derived extracellular matrix: basic characteristics and current applications in Orthopedic tissue engineering. Tissue Eng B 22:193–207CrossRefGoogle Scholar
  65. Zheng X, Yang F, Wang S, Lu S, Zhang W, Liu S, Huang J, Wang A, Yin B, Ma N, Zhang L, Xu W, Guo Q (2011) Fabrication and cell affinity of biomimetic structured PLGA/articular cartilage ECM composite scaffold. J Mater Sci Mater Med 22:693–704CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Xuejian Liu
    • 1
    • 2
  • Haoye Meng
    • 1
    • 3
  • Quanyi Guo
    • 1
    • 3
  • Baichuan Sun
    • 1
    • 2
  • Kaihong Zhang
    • 1
  • Wen Yu
    • 1
    • 3
  • Shichen Liu
    • 2
  • Yu Wang
    • 1
    • 3
  • Xiaoguang Jing
    • 1
    • 2
  • Zengzeng Zhang
    • 1
    • 2
  • Jiang Peng
    • 1
    • 3
  • Jianhua Yang
    • 2
    • 4
  1. 1.Institute of OrthopedicsChinese PLA General HospitalBeijingChina
  2. 2.First Affiliated Hospital of Jiamusi UniversityJiamusi UniversityJiamusiChina
  3. 3.Beijing Key Lab of Regenerative Medicine in OrthopaedicsBeijingChina
  4. 4.Longgang District People’s Hospital of ShenzhenShenzhenChina

Personalised recommendations