Skip to main content

Advertisement

SpringerLink
Log in

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

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Albrecht FH (1983) Closure of joint cartilage defects using cartilage fragments and fibrin glue. Fortschr Med 101:1650–1652

    CAS  PubMed  Google Scholar 

  • 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 15:2979

    Article  CAS  Google Scholar 

  • 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 25:1384–1392

    Article  CAS  PubMed  Google Scholar 

  • 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 8

  • 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 40:389–397

    Article  CAS  PubMed  Google Scholar 

  • Cheng CW, Solorio LD, Alsberg E (2014) Decellularized tissue and cell-derived extracellular matrices as scaffolds for orthopaedic tissue engineering. Biotechnol Adv 32:462–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole BJ (2008) A randomized trial comparing autologous chondrocyte implantation with microfracture. J Bone Joint Surg Am 90:1165 author reply 1165-1166

    Article  PubMed  Google Scholar 

  • 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 68:149

    CAS  PubMed  Google Scholar 

  • Darling EM, Athanasiou KA (2005) Growth factor impact on articular cartilage subpopulations. Cell Tissue Res 322:463–473

    Article  CAS  PubMed  Google Scholar 

  • Elder BD, Eleswarapu SV, Athanasiou KA (2009) Extraction techniques for the decellularization of tissue engineered articular cartilage constructs. Biomaterials 30:3749–3756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 21:850–860

    Article  CAS  Google Scholar 

  • Foldager CB, Gomoll AH, Lind M, Spector M (2012) Cell seeding densities in Autologous Chondrocyte implantation techniques for cartilage repair. Cartilage 3:108–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 10:66

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilbert TW, Sellaro TL, Badylak SF (2006) Decellularization of tissues and organs. Biomaterials 27:3675–3683

    CAS  PubMed  Google Scholar 

  • 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 12:39

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 1:253–261

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 22:173–188

    Article  CAS  Google Scholar 

  • Juran CM, Dolwick MF, Mcfetridge PS (2015) Engineered microporosity: enhancing the early regenerative potential of Decellularized Temporomandibular joint discs. Tissue Eng A 21:829

    Article  CAS  Google Scholar 

  • 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:e98570

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 98:1332–1339

    Article  PubMed  Google Scholar 

  • Lakes EH, Matuska AM, McFetridge PS, Allen KD (2016) Mechanical integrity of a decellularized and laser drilled medial meniscus. J Biomech Eng 138(3):031006

  • 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 21:190

  • 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 9:929–939

    Article  CAS  PubMed  Google Scholar 

  • 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 2017:8760383

    PubMed  PubMed Central  Google Scholar 

  • 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 4:808–816

    Article  PubMed  Google Scholar 

  • 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 444–470

  • 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 225:291–295

    Article  CAS  PubMed  Google Scholar 

  • Mironov V, Visconti RP, Kasyanov V, Forgacs G, Drake CJ, Markwald RR (2009) Organ printing: tissue spheroids as building blocks. Biomaterials 30:2164–2174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 87:1911–1920

    Article  PubMed  Google Scholar 

  • 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 10:1695–1706

    Article  CAS  PubMed  Google Scholar 

  • 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 8:112–125

    Article  CAS  PubMed  Google Scholar 

  • 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 5:3935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peppas NA, Hilt JZ, Khademhosseini A, Langer R (2006) Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv Mater 18:1345–1360

    Article  CAS  Google Scholar 

  • 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 18:295–309

    Article  CAS  Google Scholar 

  • 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 6:260

    Article  PubMed  PubMed Central  Google Scholar 

  • Risbud MV, Sittinger M (2002) Tissue engineering: advances in in vitro cartilage generation. Trends Biotechnol 20:351–356

    Article  CAS  PubMed  Google Scholar 

  • Rowland CR, Colucci LA, Guilak F (2016) Fabrication of anatomically-shaped cartilage constructs using decellularized cartilage-derived matrix scaffolds. Biomaterials 91:57–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 352:495–507

    Article  PubMed  PubMed Central  Google Scholar 

  • Saldin LT, Cramer MC, Velankar SS, White LJ, Badylak SF (2017) Extracellular matrix hydrogels from decellularized tissues: structure and function. Acta Biomater 49:1–15

    Article  CAS  PubMed  Google Scholar 

  • 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 10:62

    Article  CAS  Google Scholar 

  • 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 18:2195–2209

    Article  CAS  Google Scholar 

  • 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–E251

    Article  CAS  PubMed  Google Scholar 

  • Smith BD, Grande DA (2015) The current state of scaffolds for musculoskeletal regenerative applications. Nat Rev Rheumatol 11:213–222

    Article  CAS  PubMed  Google Scholar 

  • Smith GD, Knutsen G, Richardson JB (2005) A clinical review of cartilage repair techniques. J Bone Joint Surg Br 87:445–449

    Article  CAS  PubMed  Google Scholar 

  • 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 B

  • 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 69:63–72

    Google Scholar 

  • Sutherland AJ, Converse GL, Hopkins RA, Detamore MS (2015) The bioactivity of cartilage extracellular matrix in Articular cartilage regeneration. Adv Healthc Mater 4:29–39

    Article  CAS  PubMed  Google Scholar 

  • Tuli R, Li WJ, Tuan RS (2003) Current state of cartilage tissue engineering. Arthritis Res Ther 5:235–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 2:515–520

    Article  CAS  PubMed  Google Scholar 

  • 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 3:173–180

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 18:1645–1655

    Article  Google Scholar 

  • 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 102:2448–2466

    Article  PubMed  Google Scholar 

  • Vinatier C, Guicheux J (2016) Cartilage tissue engineering: from biomaterials and stem cells to osteoarthritis treatments. Ann Phys Rehab Med 59:139–144

    Article  CAS  Google Scholar 

  • 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 5:146–150

    Article  PubMed  Google Scholar 

  • 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 35:69

    Article  PubMed  Google Scholar 

  • 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 22:2606–2618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:570

    Article  CAS  PubMed  Google Scholar 

  • 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 23:1

    Article  CAS  Google Scholar 

  • 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 1–14

  • Yamanaka S, Takahashi K (2006) induction of pluripotent stem cells from mouse fibroblast cultures. Cell 51:2346

  • 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 4:404

    Article  CAS  Google Scholar 

  • 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 29:2378–2387

    Article  CAS  PubMed  Google Scholar 

  • 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 33:96–109

    Article  CAS  PubMed  Google Scholar 

  • 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 22:193–207

    Article  Google Scholar 

  • 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 22:693–704

    Article  CAS  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Institute of Orthopedics, Chinese PLA General Hospital, Beijing, China

    Xuejian Liu, Haoye Meng, Quanyi Guo, Baichuan Sun, Kaihong Zhang, Wen Yu, Yu Wang, Xiaoguang Jing, Zengzeng Zhang & Jiang Peng

  2. First Affiliated Hospital of Jiamusi University, Jiamusi University, Jiamusi, China

    Xuejian Liu, Baichuan Sun, Shichen Liu, Xiaoguang Jing, Zengzeng Zhang & Jianhua Yang

  3. Beijing Key Lab of Regenerative Medicine in Orthopaedics, Beijing, China

    Haoye Meng, Quanyi Guo, Wen Yu, Yu Wang & Jiang Peng

  4. Longgang District People’s Hospital of Shenzhen, Shenzhen, China

    Jianhua Yang

Authors
  1. Xuejian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haoye Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Quanyi Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Baichuan Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kaihong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wen Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shichen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xiaoguang Jing
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zengzeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jiang Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jianhua Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jiang Peng or Jianhua Yang.

Ethics declarations

Disclosure Statement

No competing financial interests exist.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X., Meng, H., Guo, Q. et al. Tissue-derived scaffolds and cells for articular cartilage tissue engineering: characteristics, applications and progress. Cell Tissue Res 372, 13–22 (2018). https://doi.org/10.1007/s00441-017-2772-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-017-2772-z

Keywords

Search

Navigation