Skip to main content
SpringerLink
Log in

Extracellular Matrix-based Materials for Bone Regeneration

  • Chapter
  • First Online:
Racing for the Surface

  • 1407 Accesses

Abstract

Decellularized extracellular matrix (ECM)-based scaffolds are rapidly expanding in regenerative medicine. The ECM is an intricate microenvironment with excellent biochemical, biophysical, and biomechanical properties, which can regulate cell adhesion, proliferation, migration, and differentiation, as well as drive tissue homeostasis and regeneration. Decellularized tissue-derived ECMs have been reported to be successful in clinical application of cardiovascular, respiratory, and gastrointestinal surgery. In bone tissue engineering, decellularized ECMs derived either from tissues such as bone, cartilage, and small intestinal submucosa or from cells such as stem cells, osteoblasts, and chondrocytes have shown promising results. We begin this chapter with a brief description of the composition of the ECM and its changes during osteogenesis in vivo and in vitro. Next, the decellularization methods are summarized, followed by the latest development in matrices from native tissues, or cultured cells and their application in bone tissue engineering. Finally, we investigated the different engineering strategies for the design of ECM-based scaffolds in bone regenerative medicine. With this information, we hope to better understand the ECM-based materials and to develop biomaterials more close to the clinical needs in bone tissue engineering.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

References

  1. Friedlaender GE et al (2001) Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial nonunions. J Bone Joint Surg Am 83-A(Suppl 1):S151–S158

    Google Scholar 

  2. Bucholz RW (2002) Nonallograft osteoconductive bone graft substitutes. Clin Orthop Relat Res (395):44–52

    Google Scholar 

  3. Fernandez de Grado G et al (2018) Bone substitutes: a review of their characteristics, clinical use, and perspectives for large bone defects management. J Tissue Eng 9:2041731418776819. https://doi.org/10.1177/2041731418776819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Finkemeier CG (2002) Bone-grafting and bone-graft substitutes. J Bone Joint Surg Am 84-A:454–464

    Article  Google Scholar 

  5. Van Heest A, Swiontkowski M (1999) Bone-graft substitutes. Lancet 353(Suppl 1):SI28–SI29

    Article  PubMed  Google Scholar 

  6. Kane R, Ma PX (2013) Mimicking the nanostructure of bone matrix to regenerate bone. Mater Today 16:418–423. https://doi.org/10.1016/j.mattod.2013.11.001

    Article  CAS  Google Scholar 

  7. Pape HC, Evans A, Kobbe P (2010) Autologous bone graft: properties and techniques. J Orthop Trauma 24(Suppl 1):S36–S40. https://doi.org/10.1097/BOT.0b013e3181cec4a1

    Article  PubMed  Google Scholar 

  8. Zimmermann G, Moghaddam A (2011) Allograft bone matrix versus synthetic bone graft substitutes. Injury 42(Suppl 2):S16–S21. https://doi.org/10.1016/j.injury.2011.06.199

    Article  PubMed  Google Scholar 

  9. Habibovic P, de Groot K (2007) Osteoinductive biomaterials—properties and relevance in bone repair. J Tissue Eng Regen Med 1:25–32. https://doi.org/10.1002/term.5

    Article  CAS  PubMed  Google Scholar 

  10. Langer R, Vacanti JP (1993) Tissue engineering. Science 260:920–926

    Article  CAS  PubMed  Google Scholar 

  11. Griffith LG, Naughton G (2002) Tissue engineering—current challenges and expanding opportunities. Science 295:1009–1014. https://doi.org/10.1126/science.1069210

    Article  CAS  PubMed  Google Scholar 

  12. Yuan H et al (2010) Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci U S A 107:13614–13619. https://doi.org/10.1073/pnas.1003600107

    Article  PubMed  PubMed Central  Google Scholar 

  13. Parikh SN (2002) Bone graft substitutes in modern orthopedics. Orthopedics 25:1301–1309. ; quiz 1301–1310

    PubMed  Google Scholar 

  14. Chan G, Mooney DJ (2008) New materials for tissue engineering: towards greater control over the biological response. Trends Biotechnol 26:382–392. https://doi.org/10.1016/j.tibtech.2008.03.011

    Article  CAS  PubMed  Google Scholar 

  15. Shekaran A, Garcia AJ (2011) Extracellular matrix-mimetic adhesive biomaterials for bone repair. J Biomed Mater Res A 96A:261–272. https://doi.org/10.1002/jbm.a.32979

    Article  CAS  Google Scholar 

  16. Lind M et al (1996) Transforming growth factor-beta 1 stimulates bone ongrowth to weight-loaded tricalcium phosphate coated implants: an experimental study in dogs. J Bone Joint Surg Br 78:377–382

    Article  CAS  PubMed  Google Scholar 

  17. Inzana JA et al (2014) 3D printing of composite calcium phosphate and collagen scaffolds for bone regeneration. Biomaterials 35:4026–4034. https://doi.org/10.1016/j.biomaterials.2014.01.064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Hussey GS, Dziki JL, Badylak SF (2018) Extracellular matrix-based materials for regenerative medicine. Nat Rev Mater 3:159–173. https://doi.org/10.1038/s41578-018-0023-x

    Article  CAS  Google Scholar 

  19. Hynes RO (2009) The extracellular matrix: not just pretty fibrils. Science 326:1216–1219. https://doi.org/10.1126/science.1176009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. da Anunciacao A et al (2017) Extracellular matrix in epitheliochorial, endotheliochorial and haemochorial placentation and its potential application for regenerative medicine. Reprod Domest Anim 52:3–15. https://doi.org/10.1111/rda.12868

    Article  CAS  PubMed  Google Scholar 

  21. Ott HC et al (2010) Regeneration and orthotopic transplantation of a bioartificial lung. Nat Med 16:927–933. https://doi.org/10.1038/nm.2193

    Article  CAS  PubMed  Google Scholar 

  22. D’Onofrio A et al (2011) Clinical and hemodynamic outcomes after aortic valve replacement with stented and stentless pericardial xenografts: a propensity-matched analysis. J Heart Valve Dis 20:319–326

    PubMed  Google Scholar 

  23. Macchiarini P et al (2008) Clinical transplantation of a tissue-engineered airway. Lancet 372:2023–2030. https://doi.org/10.1016/S0140-6736(08)61598-6

    Article  PubMed  Google Scholar 

  24. 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. https://doi.org/10.1016/j.biotechadv.2013.12.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Clarke B (2008) Normal bone anatomy and physiology. Clin J Am Soc Nephrol 3(Suppl 3):S131–S139. https://doi.org/10.2215/CJN.04151206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Boskey AL (2013) Bone composition: relationship to bone fragility and antiosteoporotic drug effects. Bonekey Rep 2:447. https://doi.org/10.1038/bonekey.2013.181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wang Y et al (2012) The predominant role of collagen in the nucleation, growth, structure and orientation of bone apatite. Nat Mater 11:724–733. https://doi.org/10.1038/nmat3362

    Article  CAS  PubMed  Google Scholar 

  28. Nudelman F et al (2010) The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat Mater 9:1004–1009. https://doi.org/10.1038/nmat2875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Barradas AM, Yuan H, van Blitterswijk CA, Habibovic P (2011) Osteoinductive biomaterials: current knowledge of properties, experimental models and biological mechanisms. Eur Cell Mater 21:407–429. ; discussion 429

    Article  CAS  PubMed  Google Scholar 

  30. Legate KR, Wickstrom SA, Fassler R (2009) Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 23:397–418. https://doi.org/10.1101/gad.1758709

    Article  CAS  PubMed  Google Scholar 

  31. Sasano Y et al (2000) Immunohistochemical localization of type I collagen, fibronectin and tenascin C during embryonic osteogenesis in the dentary of mandibles and tibias in rats. Histochem J 32:591–598

    Article  CAS  PubMed  Google Scholar 

  32. Kamiya N, Shigemasa K, Takagi M (2001) Gene expression and immunohistochemical localization of decorin and biglycan in association with early bone formation in the developing mandible. J Oral Sci 43:179–188

    Article  CAS  PubMed  Google Scholar 

  33. Nakamura M et al (2005) Expression of versican and ADAMTS1, 4, and 5 during bone development in the rat mandible and hind limb. J Histochem Cytochem 53:1553–1562. https://doi.org/10.1369/jhc.5A6669.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hoshiba T, Kawazoe N, Tateishi T, Chen G (2009) Development of stepwise osteogenesis-mimicking matrices for the regulation of mesenchymal stem cell functions. J Biol Chem 284:31164–31173. https://doi.org/10.1074/jbc.M109.054676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Papadimitropoulos A, Scotti C, Bourgine P, Scherberich A, Martin I (2015) Engineered decellularized matrices to instruct bone regeneration processes. Bone 70:66–72. https://doi.org/10.1016/j.bone.2014.09.007

    Article  CAS  PubMed  Google Scholar 

  36. Al-Abedalla K et al (2015) Bone augmented with allograft onlays for implant placement could be comparable with native bone. J Oral Maxillofac Surg 73:2108–2122. https://doi.org/10.1016/j.joms.2015.06.151

    Article  PubMed  Google Scholar 

  37. Gilbert TW, Sellaro TL, Badylak SF (2006) Decellularization of tissues and organs. Biomaterials 27:3675–3683. https://doi.org/10.1016/j.biomaterials.2006.02.014

    Article  CAS  PubMed  Google Scholar 

  38. Hoshiba T, Lu H, Kawazoe N, Chen G (2010) Decellularized matrices for tissue engineering. Expert Opin Biol Ther 10:1717–1728. https://doi.org/10.1517/14712598.2010.534079

    Article  CAS  PubMed  Google Scholar 

  39. Keane TJ, Swinehart IT, Badylak SF (2015) Methods of tissue decellularization used for preparation of biologic scaffolds and in vivo relevance. Methods 84:25–34. https://doi.org/10.1016/j.ymeth.2015.03.005

    Article  CAS  PubMed  Google Scholar 

  40. Hashimoto Y et al (2011) The effect of decellularized bone/bone marrow produced by high-hydrostatic pressurization on the osteogenic differentiation of mesenchymal stem cells. Biomaterials 32:7060–7067. https://doi.org/10.1016/j.biomaterials.2011.06.008

    Article  CAS  PubMed  Google Scholar 

  41. Kabirian F, Mozafari M (2019) Decellularized ECM-derived bioinks: prospects for the future. Methods. https://doi.org/10.1016/j.ymeth.2019.04.019

  42. Seddon AM, Curnow P, Booth PJ (2004) Membrane proteins, lipids and detergents: not just a soap opera. Biochim Biophys Acta 1666:105–117. https://doi.org/10.1016/j.bbamem.2004.04.011

    Article  CAS  PubMed  Google Scholar 

  43. Hwang J et al (2017) Molecular assessment of collagen denaturation in decellularized tissues using a collagen hybridizing peptide. Acta Biomater 53:268–278. https://doi.org/10.1016/j.actbio.2017.01.079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Fitzpatrick JC, Clark PM, Capaldi FM (2010) Effect of decellularization protocol on the mechanical behavior of porcine descending aorta. Int J Biomater 2010:620503. https://doi.org/10.1155/2010/620503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. He M, Callanan A (2013) Comparison of methods for whole-organ decellularization in tissue engineering of bioartificial organs. Tissue Eng B Rev 19:194–208. https://doi.org/10.1089/ten.TEB.2012.0340

    Article  CAS  Google Scholar 

  46. Petersen TH et al (2010) Tissue-engineered lungs for in vivo implantation. Science 329:538–541. https://doi.org/10.1126/science.1189345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Woods T, Gratzer PF (2005) Effectiveness of three extraction techniques in the development of a decellularized bone-anterior cruciate ligament-bone graft. Biomaterials 26:7339–7349. https://doi.org/10.1016/j.biomaterials.2005.05.066

    Article  CAS  PubMed  Google Scholar 

  48. Boer U et al (2011) The effect of detergent-based decellularization procedures on cellular proteins and immunogenicity in equine carotid artery grafts. Biomaterials 32:9730–9737. https://doi.org/10.1016/j.biomaterials.2011.09.015

    Article  CAS  PubMed  Google Scholar 

  49. Bourgine PE, Pippenger BE, Todorov A Jr, Tchang L, Martin I (2013) Tissue decellularization by activation of programmed cell death. Biomaterials 34:6099–6108. https://doi.org/10.1016/j.biomaterials.2013.04.058

    Article  CAS  PubMed  Google Scholar 

  50. Bourgine PE et al (2014) Osteoinductivity of engineered cartilaginous templates devitalized by inducible apoptosis. Proc Natl Acad Sci U. S. A 111:17426–17431. https://doi.org/10.1073/pnas.1411975111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. van Engeland M, Kuijpers HJ, Ramaekers FC, Reutelingsperger CP, Schutte B (1997) Plasma membrane alterations and cytoskeletal changes in apoptosis. Exp Cell Res 235:421–430. https://doi.org/10.1006/excr.1997.3738

    Article  PubMed  Google Scholar 

  52. Raff M (1998) Cell suicide for beginners. Nature 396:119–122. https://doi.org/10.1038/24055

    Article  CAS  PubMed  Google Scholar 

  53. Bruyneel AAN, Carr CA (2017) Ambiguity in the presentation of decellularized tissue composition: the need for standardized approaches. Artif Organs 41:778–784. https://doi.org/10.1111/aor.12838

    Article  CAS  PubMed  Google Scholar 

  54. Chen XD, Dusevich V, Feng JQ, Manolagas SC, Jilka RL (2007) Extracellular matrix made by bone marrow cells facilitates expansion of marrow-derived mesenchymal progenitor cells and prevents their differentiation into osteoblasts. J Bone Miner Res Off 22:1943–1956. https://doi.org/10.1359/jbmr.070725

    Article  CAS  Google Scholar 

  55. Laurencin CT, Khan Y (2012) Regenerative engineering. Sci Transl Med 4:160–169. https://doi.org/10.1126/scitranslmed.3004467

    Article  Google Scholar 

  56. Esses SI, Halloran PF (1983) Donor marrow-derived cells as immunogens and targets for the immune response to bone and skin allografts. Transplantation 35:169–174

    Article  CAS  PubMed  Google Scholar 

  57. Campana V et al (2014) Bone substitutes in orthopaedic surgery: from basic science to clinical practice. J Mater Sci Mater Med 25:2445–2461. https://doi.org/10.1007/s10856-014-5240-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Rosenberg E, Rose LF (1998) Biologic and clinical considerations for autografts and allografts in periodontal regeneration therapy. Dent Clin N Am 42:467–490

    CAS  PubMed  Google Scholar 

  59. Freiberg RA, Ray RD (1964) Studies of devitalized bone implants. Arch Surg 89:417–427

    Article  CAS  PubMed  Google Scholar 

  60. Frohlich M et al (2010) Bone grafts engineered from human adipose-derived stem cells in perfusion bioreactor culture. Tissue Eng PartA 16:179–189. https://doi.org/10.1089/ten.TEA.2009.0164

    Article  Google Scholar 

  61. Marcos-Campos I et al (2012) Bone scaffold architecture modulates the development of mineralized bone matrix by human embryonic stem cells. Biomaterials 33:8329–8342. https://doi.org/10.1016/j.biomaterials.2012.08.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Hesse E et al (2010) Repair of a segmental long bone defect in human by implantation of a novel multiple disc graft. Bone 46:1457–1463. https://doi.org/10.1016/j.bone.2010.02.011

    Article  PubMed  Google Scholar 

  63. Drosos GI, Kazakos KI, Kouzoumpasis P, Verettas DA (2007) Safety and efficacy of commercially available demineralised bone matrix preparations: a critical review of clinical studies. Injury 38(Suppl 4):S13–S21

    Article  PubMed  Google Scholar 

  64. Schwartz Z et al (1998) Ability of commercial demineralized freeze-dried bone allograft to induce new bone formation is dependent on donor age but not gender. J Periodontol 69:470–478. https://doi.org/10.1902/jop.1998.69.4.470

    Article  CAS  PubMed  Google Scholar 

  65. Munting E, Wilmart JF, Wijne A, Hennebert P, Delloye C (1988) Effect of sterilization on osteoinduction. Comparison of five methods in demineralized rat bone. Acta Orthop Scand 59:34–38

    Article  CAS  PubMed  Google Scholar 

  66. Iwata H, Sakano S, Itoh T, Bauer TW (2002) Demineralized bone matrix and native bone morphogenetic protein in orthopaedic surgery. Clin Orthop Relat Res (395):99–109

    Google Scholar 

  67. Chen L et al (2010) Loading of VEGF to the heparin cross-linked demineralized bone matrix improves vascularization of the scaffold. J Mater Sci Mater Med 21:309–317. https://doi.org/10.1007/s10856-009-3827-9

    Article  CAS  PubMed  Google Scholar 

  68. Lee JH et al (2011) Combined effects of porous hydroxyapatite and demineralized bone matrix on bone induction: in vitro and in vivo study using a nude rat model. Biomed Mater 6:015008. https://doi.org/10.1088/1748-6041/6/1/015008

    Article  CAS  PubMed  Google Scholar 

  69. Jayasuriya AC, Ebraheim NA (2009) Evaluation of bone matrix and demineralized bone matrix incorporated PLGA matrices for bone repair. J Mater Sci Mater Med 20:1637–1644. https://doi.org/10.1007/s10856-009-3738-9

    Article  CAS  PubMed  Google Scholar 

  70. Park BW et al (2012) In vitro and in vivo osteogenesis of human mesenchymal stem cells derived from skin, bone marrow and dental follicle tissues. Differentiation 83:249–259. https://doi.org/10.1016/j.diff.2012.02.008

    Article  CAS  PubMed  Google Scholar 

  71. Liu G et al (2010) In vitro and in vivo evaluation of osteogenesis of human umbilical cord blood-derived mesenchymal stem cells on partially demineralized bone matrix. Tissue Eng Part A 16:971–982. https://doi.org/10.1089/ten.TEA.2009.0516

    Article  CAS  PubMed  Google Scholar 

  72. Kang EJ et al (2010) In vitro and in vivo osteogenesis of porcine skin-derived mesenchymal stem cell-like cells with a demineralized bone and fibrin glue scaffold. Tissue Eng Part A 16:815–827. https://doi.org/10.1089/ten.TEA.2009.0439

    Article  CAS  PubMed  Google Scholar 

  73. Sawkins MJ et al (2013) Hydrogels derived from demineralized and decellularized bone extracellular matrix. Acta Biomater 9:7865–7873. https://doi.org/10.1016/j.actbio.2013.04.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Supronowicz P et al (2011) Human adipose-derived side population stem cells cultured on demineralized bone matrix for bone tissue engineering. Tissue Eng Part A 17:789–798. https://doi.org/10.1089/ten.tea.2010.0357

    Article  CAS  PubMed  Google Scholar 

  75. Kurkalli BG, Gurevitch O, Sosnik A, Cohn D, Slavin S (2010) Repair of bone defect using bone marrow cells and demineralized bone matrix supplemented with polymeric materials. Curr Stem Cell Res Ther 5:49–56

    Article  CAS  PubMed  Google Scholar 

  76. Brighton CT, Sugioka Y, Hunt RM (1973) Cytoplasmic structures of epiphyseal plate chondrocytes. Quantitative evaluation using electron micrographs of rat costochondral junctions with special reference to the fate of hypertrophic cells. J Bone Joint Surg Am 55:771–784

    Article  CAS  PubMed  Google Scholar 

  77. Brighton CT, Hunt RM (1986) Histochemical localization of calcium in the fracture callus with potassium pyroantimonate. Possible role of chondrocyte mitochondrial calcium in callus calcification. J Bone Joint Surg Am 68:703–715

    Article  CAS  PubMed  Google Scholar 

  78. Gerber HP et al (1999) VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med 5:623–628. https://doi.org/10.1038/9467

    Article  CAS  PubMed  Google Scholar 

  79. Kronenberg HM (2003) Developmental regulation of the growth plate. Nature 423:332–336. https://doi.org/10.1038/nature01657

    Article  CAS  PubMed  Google Scholar 

  80. Krych AJ, Harnly HW, Rodeo SA, Williams RJ 3rd (2012) Activity levels are higher after osteochondral autograft transfer mosaicplasty than after microfracture for articular cartilage defects of the knee: a retrospective comparative study. J Bone Joint Surg Am 94:971–978. https://doi.org/10.2106/JBJS.K.00815

    Article  PubMed  Google Scholar 

  81. Pallante AL et al (2012) Treatment of articular cartilage defects in the goat with frozen versus fresh osteochondral allografts: effects on cartilage stiffness, zonal composition, and structure at six months. J Bone Joint Surg Am 94:1984–1995. https://doi.org/10.2106/JBJS.K.00439

    Article  PubMed  PubMed Central  Google Scholar 

  82. Pallante AL et al (2012) The in vivo performance of osteochondral allografts in the goat is diminished with extended storage and decreased cartilage cellularity. Am J Sports Med 40:1814–1823. https://doi.org/10.1177/0363546512449321

    Article  PubMed  PubMed Central  Google Scholar 

  83. Townsend JM et al (2017) Colloidal gels with extracellular matrix particles and growth factors for bone regeneration in critical size rat calvarial defects. AAPS J 19:703–711. https://doi.org/10.1208/s12248-017-0045-0

    Article  CAS  PubMed  Google Scholar 

  84. Gupta V et al (2017) Microsphere-based osteochondral scaffolds carrying opposing gradients of decellularized cartilage and demineralized bone matrix. ACS Biomater Sci Eng 3:1955–1963. https://doi.org/10.1021/acsbiomaterials.6b00071

    Article  CAS  PubMed  Google Scholar 

  85. Gawlitta D et al (2015) Decellularized cartilage-derived matrix as substrate for endochondral bone regeneration. Tissue Eng Part A 21:694–703. https://doi.org/10.1089/ten.TEA.2014.0117

    Article  CAS  PubMed  Google Scholar 

  86. Cunniffe GM et al (2017) Growth plate extracellular matrix-derived scaffolds for large bone defect healing. Eur Cell Mater 33:130–142. https://doi.org/10.22203/eCM.v033a10

    Article  CAS  PubMed  Google Scholar 

  87. Badylak SF, Freytes DO, Gilbert TW (2009) Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 5:1–13. https://doi.org/10.1016/j.actbio.2008.09.013

    Article  CAS  PubMed  Google Scholar 

  88. Kim KS et al (2010) Small intestine submucosa sponge for in vivo support of tissue-engineered bone formation in the presence of rat bone marrow stem cells. Biomaterials 31:1104–1113. https://doi.org/10.1016/j.biomaterials.2009.10.020

    Article  CAS  PubMed  Google Scholar 

  89. Li M, Zhang C, Cheng M, Gu Q, Zhao J (2017) Small intestinal submucosa: a potential osteoconductive and osteoinductive biomaterial for bone tissue engineering. Mater Sci Eng C Mater Biol Appl 75:149–156. https://doi.org/10.1016/j.msec.2017.02.042

    Article  CAS  PubMed  Google Scholar 

  90. Sun T et al (2018) Composite scaffolds of mineralized natural extracellular matrix on true bone ceramic induce bone regeneration through Smad1/5/8 and ERK1/2 pathways. Tissue Eng Part A 24:502–515. https://doi.org/10.1089/ten.TEA.2017.0179

    Article  CAS  PubMed  Google Scholar 

  91. Sun TF et al (2018) Guided osteoporotic bone regeneration with composite scaffolds of mineralized ECM/heparin membrane loaded with BMP2-related peptide. Int J Nanomed 13:791–804. https://doi.org/10.2147/Ijn.S152698

    Article  CAS  Google Scholar 

  92. Zhang C, Li M, Zhu J, Luo F, Zhao J (2017) Enhanced bone repair induced by human adipose-derived stem cells on osteogenic extracellular matrix ornamented small intestinal submucosa. Regen Med 12:541–552. https://doi.org/10.2217/rme-2017-0024

    Article  CAS  PubMed  Google Scholar 

  93. Li M, Zhang C, Mao YX, Zhong Y, Zhao JY (2018) A cell-engineered small intestinal submucosa-based bone mimetic construct for bone regeneration. Tissue Eng Part A 24:1099–1111. https://doi.org/10.1089/ten.tea.2017.0407

    Article  CAS  PubMed  Google Scholar 

  94. Moore DC, Pedrozo HA, Crisco JJ 3rd, Ehrlich MG (2004) Preformed grafts of porcine small intestine submucosa (SIS) for bridging segmental bone defects. J Biomed Mater Res A 69:259–266. https://doi.org/10.1002/jbm.a.20123

    Article  CAS  PubMed  Google Scholar 

  95. Zhao L, Zhao J, Wang S, Wang J, Liu J (2011) Comparative study between tissue-engineered periosteum and structural allograft in rabbit critical-sized radial defect model. J Biomed Mater Res B Appl Biomater 97:1–9. https://doi.org/10.1002/jbm.b.31768

    Article  CAS  PubMed  Google Scholar 

  96. Roberts SJ, van Gastel N, Carmeliet G, Luyten FP (2015) Uncovering the periosteum for skeletal regeneration: the stem cell that lies beneath. Bone 70:10–18. https://doi.org/10.1016/j.bone.2014.08.007

    Article  PubMed  Google Scholar 

  97. Zhang X et al (2005) Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. J Bone Miner Research 20:2124–2137. https://doi.org/10.1359/JBMR.050806

    Article  CAS  Google Scholar 

  98. Lin XF et al (2018) Periosteum extracellular-matrix-mediated acellular mineralization during bone formation. Adv Healthc Mater 7:1700660. https://doi.org/10.1002/Adhm.201700660

    Article  Google Scholar 

  99. Wang XY et al (2017) Preparation and characterization of a chitosan/gelatin/extracellular matrix scaffold and its application in tissue engineering. Tissue Eng Part C Methods 23:169–179. https://doi.org/10.1089/ten.tec.2016.0511

    Article  CAS  PubMed  Google Scholar 

  100. Schonmeyr B, Clavin N, Avraham T, Longo V, Mehrara BJ (2009) Synthesis of a tissue-engineered periosteum with acellular dermal matrix and cultured mesenchymal stem cells. Tissue Eng Part A 15:1833–1841. https://doi.org/10.1089/ten.tea.2008.0446

    Article  CAS  PubMed  Google Scholar 

  101. Kim HJ et al (2012) Effect of acellular dermal matrix as a delivery carrier of adipose-derived mesenchymal stem cells on bone regeneration. J Biomed Mater Res Part B Appl Biomater 100:1645–1653. https://doi.org/10.1002/jbm.b.32733

    Article  CAS  Google Scholar 

  102. Hwang JW, Kim S, Kim SW, Lee JH (2016) Effect of extracellular matrix membrane on bone formation in a rabbit tibial defect model. Biomed Res Int 2016:6715295. https://doi.org/10.1155/2016/6715295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Li W et al (2015) Investigating the potential of amnion-based scaffolds as a barrier membrane for guided bone regeneration. Langmuir 31:8642–8653. https://doi.org/10.1021/acs.langmuir.5b02362

    Article  CAS  PubMed  Google Scholar 

  104. Penolazzi L et al (2012) Human mesenchymal stem cells seeded on extracellular matrix-scaffold: viability and osteogenic potential. J Cell Physiol 227:857–866. https://doi.org/10.1002/jcp.22983

    Article  CAS  PubMed  Google Scholar 

  105. Beachley V et al (2018) Extracellular matrix particle-glycosaminoglycan composite hydrogels for regenerative medicine applications. J Biomed Mater Res A 106:147–159. https://doi.org/10.1002/jbm.a.36218

    Article  CAS  PubMed  Google Scholar 

  106. Wainwright D et al (1996) Clinical evaluation of an acellular allograft dermal matrix in full-thickness burns. J Burn Care Rehabil 17:124–136

    Article  CAS  PubMed  Google Scholar 

  107. Badylak SF (2007) The extracellular matrix as a biologic scaffold material. Biomaterials 28:3587–3593. https://doi.org/10.1016/j.biomaterials.2007.04.043

    Article  CAS  PubMed  Google Scholar 

  108. Trelford JD, Trelford-Sauder M (1979) The amnion in surgery, past and present. Am J Obstet Gynecol 134:833–845

    Article  CAS  PubMed  Google Scholar 

  109. Wei W et al (2017) In vitro osteogenic induction of bone marrow mesenchymal stem cells with a decellularized matrix derived from human adipose stem cells and in vivo implantation for bone regeneration. J Mater Chem B 5:2468–2482. https://doi.org/10.1039/c6tb03150a

    Article  CAS  PubMed  Google Scholar 

  110. Ravindran S et al (2012) Biomimetic extracellular matrix-incorporated scaffold induces osteogenic gene expression in human marrow stromal cells. Tissue Eng Part A 18:295–309. https://doi.org/10.1089/ten.TEA.2011.0136

    Article  CAS  PubMed  Google Scholar 

  111. Lai Y et al (2010) Reconstitution of marrow-derived extracellular matrix ex vivo: a robust culture system for expanding large-scale highly functional human mesenchymal stem cells. Stem Cells Dev 19:1095–1107. https://doi.org/10.1089/scd.2009.0217

    Article  CAS  PubMed  Google Scholar 

  112. Zhang Z et al (2015) Bone marrow stromal cell-derived extracellular matrix promotes osteogenesis of adipose-derived stem cells. Cell Biol Int 39:291–299. https://doi.org/10.1002/cbin.10385

    Article  CAS  PubMed  Google Scholar 

  113. Zeitouni S et al (2012) Human mesenchymal stem cell-derived matrices for enhanced osteoregeneration. Sci Transl Med 4:132–155. https://doi.org/10.1126/scitranslmed.3003396

    Article  Google Scholar 

  114. Antebi B et al (2015) Stromal-cell-derived extracellular matrix promotes the proliferation and retains the osteogenic differentiation capacity of mesenchymal stem cells on three-dimensional scaffolds. Tissue Eng Part C Methods 21:171–181. https://doi.org/10.1089/ten.TEC.2014.0092

    Article  CAS  PubMed  Google Scholar 

  115. Sadr N et al (2012) Enhancing the biological performance of synthetic polymeric materials by decoration with engineered, decellularized extracellular matrix. Biomaterials 33:5085–5093. https://doi.org/10.1016/j.biomaterials.2012.03.082

    Article  CAS  PubMed  Google Scholar 

  116. Baroncelli M et al (2018) Human osteoblast-derived extracellular matrix with high homology to bone proteome is osteopromotive. Tissue Eng Part A 24:1377–1389. https://doi.org/10.1089/ten.tea.2017.0448

    Article  CAS  PubMed  Google Scholar 

  117. Cunniffe GM et al (2015) Porous decellularized tissue engineered hypertrophic cartilage as a scaffold for large bone defect healing. Acta Biomater 23:82–90. https://doi.org/10.1016/j.actbio.2015.05.031

    Article  CAS  PubMed  Google Scholar 

  118. Takeshita K et al (2017) Xenotransplantation of interferon-gamma-pretreated clumps of a human mesenchymal stem cell/extracellular matrix complex induces mouse calvarial bone regeneration. Stem Cell Res Ther 8:101. https://doi.org/10.1186/S13287-017-0550-1

    Article  PubMed  PubMed Central  Google Scholar 

  119. Clough BH et al (2015) Bone regeneration with osteogenically enhanced mesenchymal stem cells and their extracellular matrix proteins. J Bone Miner Res 30:83–94. https://doi.org/10.1002/jbmr.2320

    Article  CAS  PubMed  Google Scholar 

  120. Deutsch ER, Guldberg RE (2010) Stem cell-synthesized extracellular matrix for bone repair. J Mater Chem 20:8942–8951

    Article  CAS  Google Scholar 

  121. Kang YQ, Kim S, Bishop J, Khademhosseini A, Yang YZ (2012) The osteogenic differentiation of human bone marrow MSCs on HUVEC-derived ECM and beta-TCP scaffold. Biomaterials 33:6998–7007. https://doi.org/10.1016/j.biomaterials.2012.06.061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Tour G, Wendel M, Tcacencu I (2013) Human fibroblast-derived extracellular matrix constructs for bone tissue engineering applications. J Biomed Mater Res A 101:2826–2837. https://doi.org/10.1002/jbm.a.34600

    Article  CAS  PubMed  Google Scholar 

  123. Xing Q, Qian Z, Kannan B, Tahtinen M, Zhao F (2015) Osteogenic differentiation evaluation of an engineered extracellular matrix based tissue sheet for potential periosteum replacement. ACS Appl Mater Interfaces 7:23239–23247. https://doi.org/10.1021/acsami.5b07386

    Article  CAS  PubMed  Google Scholar 

  124. Kim IG et al (2015) Bioactive cell-derived matrices combined with polymer mesh scaffold for osteogenesis and bone healing. Biomaterials 50:75–86. https://doi.org/10.1016/j.biomaterials.2015.01.054

    Article  CAS  PubMed  Google Scholar 

  125. Pati F et al (2015) Ornamenting 3D printed scaffolds with cell-laid extracellular matrix for bone tissue regeneration. Biomaterials 37:230–241. https://doi.org/10.1016/j.biomaterials.2014.10.012

    Article  CAS  PubMed  Google Scholar 

  126. Shtrichman R et al (2014) The generation of hybrid electrospun nanofiber layer with extracellular matrix derived from human pluripotent stem cells, for regenerative medicine applications. Tissue Eng Part A 20:2756–2767. https://doi.org/10.1089/ten.TEA.2013.0705

    Article  CAS  PubMed  Google Scholar 

  127. Narayanan K, Leck KJ, Gao S, Wan AC (2009) Three-dimensional reconstituted extracellular matrix scaffolds for tissue engineering. Biomaterials 30:4309–4317. https://doi.org/10.1016/j.biomaterials.2009.04.049

    Article  CAS  PubMed  Google Scholar 

  128. Lee HJ et al (2015) A new approach for fabricating collagen/ECM-based bioinks using preosteoblasts and human adipose stem cells. Adv Healthcare Mater 4:1359–1368. https://doi.org/10.1002/adhm.201500193

    Article  CAS  Google Scholar 

  129. Ma JX et al (2017) Biomimetic matrix fabricated by LMP-1 gene-transduced MC3T3-E1 cells for bone regeneration. Biofabrication 9:045010. https://doi.org/10.1088/1758-5090/Aa8dd1

    Article  PubMed  Google Scholar 

  130. Gao CY et al (2018) Directing osteogenic differentiation of BMSCs by cell-secreted decellularized extracellular matrixes from different cell types. J Mater Chem B 6:7471–7485. https://doi.org/10.1039/c8tb01785a

    Article  CAS  PubMed  Google Scholar 

  131. Fu Y, Liu LL, Cheng RY, Cui WG (2018) ECM decorated electrospun nanofiber for improving bone tissue regeneration. Polymers (Basel) 10:272. https://doi.org/10.3390/Polym10030272

    Article  Google Scholar 

  132. Kumar A, Nune KC, Misra RDK (2016) Biological functionality and mechanistic contribution of extracellular matrix-ornamented three dimensional Ti-6Al-4V mesh scaffolds. J Biomed Mater Res A 104:2751–2763. https://doi.org/10.1002/jbm.a.35809

    Article  CAS  PubMed  Google Scholar 

  133. Kumar A, Nune KC, Misra RDK (2016) Biological functionality of extracellular matrix-ornamented three-dimensional printed hydroxyapatite scaffolds. J Biomed Mater Res A 104:1343–1351. https://doi.org/10.1002/jbm.a.35664

    Article  CAS  PubMed  Google Scholar 

  134. Pham QP et al (2008) The influence of an in vitro generated bone-like extracellular matrix on osteoblastic gene expression of marrow stromal cells. Biomaterials 29:2729–2739. https://doi.org/10.1016/j.biomaterials.2008.02.025

    Article  CAS  PubMed  Google Scholar 

  135. Datta N et al (2006) In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc Natl Acad Sci U S A 103:2488–2493. https://doi.org/10.1073/pnas.0505661103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Datta N, Holtorf HL, Sikavitsas VI, Jansen JA, Mikos AG (2005) Effect of bone extracellular matrix synthesized in vitro on the osteoblastic differentiation of marrow stromal cells. Biomaterials 26:971–977. https://doi.org/10.1016/j.biomaterials.2004.04.001

    Article  CAS  PubMed  Google Scholar 

  137. Kwon SH et al (2013) Modulation of BMP-2-induced chondrogenic versus osteogenic differentiation of human mesenchymal stem cells by cell-specific extracellular matrices. Tissue Eng Part A 19:49–58. https://doi.org/10.1089/ten.TEA.2012.0245

    Article  CAS  PubMed  Google Scholar 

  138. Lau TT, Lee LQP, Vo BN, Su K, Wang DA (2012) Inducing ossification in an engineered 3D scaffold-free living cartilage template. Biomaterials 33:8406–8417. https://doi.org/10.1016/j.biomaterials.2012.08.025

    Article  CAS  PubMed  Google Scholar 

  139. Bourgine PE et al (2017) Engineered extracellular matrices as biomaterials of tunable composition and function. Adv Funct Mater 27:1605486

    Article  Google Scholar 

  140. Fu CC et al (2018) Embryonic-like mineralized extracellular matrix/stem cell microspheroids as a bone graft substitute. Adv Healthc Mater 7:1800705. https://doi.org/10.1002/Adhm.201800705

    Article  Google Scholar 

  141. Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT (2014) Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation. J Transl Med 12:8. https://doi.org/10.1186/1479-5876-12-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Carlson ME, Conboy IM (2007) Loss of stem cell regenerative capacity within aged niches. Aging Cell 6:371–382. https://doi.org/10.1111/j.1474-9726.2007.00286.x

    Article  CAS  PubMed  Google Scholar 

  143. Sun Y et al (2011) Rescuing replication and osteogenesis of aged mesenchymal stem cells by exposure to a young extracellular matrix. FASEB J 25:1474–1485. https://doi.org/10.1096/fj.10-161497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Ng CP et al (2014) Enhanced ex vivo expansion of adult mesenchymal stem cells by fetal mesenchymal stem cell ECM. Biomaterials 35:4046–4057. https://doi.org/10.1016/j.biomaterials.2014.01.081

    Article  CAS  PubMed  Google Scholar 

  145. Bilousova G et al (2011) Osteoblasts derived from induced pluripotent stem cells form calcified structures in scaffolds both in vitro and in vivo. Stem Cells 29:206–216. https://doi.org/10.1002/stem.566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Rohanizadeh R, Swain MV, Mason RS (2008) Gelatin sponges (Gelfoam) as a scaffold for osteoblasts. J Mater Sci Mater Med 19:1173–1182. https://doi.org/10.1007/s10856-007-3154-y

    Article  CAS  PubMed  Google Scholar 

  147. Pham QP et al (2009) Analysis of the osteoinductive capacity and angiogenicity of an in vitro generated extracellular matrix. J Biomed Mater Res A 88:295–303. https://doi.org/10.1002/jbm.a.31875

    Article  CAS  PubMed  Google Scholar 

  148. Garcia P et al (2012) Temporal and spatial vascularization patterns of unions and nonunions: role of vascular endothelial growth factor and bone morphogenetic proteins. J Bone Joint Surg Am 94A:49–58. https://doi.org/10.2106/Jbjs.J.00795

    Article  Google Scholar 

  149. Cricchio G, Lundgren S (2003) Donor site morbidity in two different approaches to anterior iliac crest bone harvesting. Clin Implant Dent Relat Res 5:161–169

    Article  PubMed  Google Scholar 

  150. Ventura RD, Padalhin AR, Min YK, Lee BT (2015) Bone regeneration using hydroxyapatite sponge scaffolds with in vivo deposited extracellular matrix. Tissue Eng Part A 21:2649–2661. https://doi.org/10.1089/ten.TEA.2015.0024

    Article  CAS  PubMed  Google Scholar 

  151. Kusuma GD et al (2018) Transferable matrixes produced from decellularized extracellular matrix promote proliferation and osteogenic differentiation of mesenchymal stem cells and facilitate scale-up. ACS Biomater Sci Eng 4:1760–1769. https://doi.org/10.1021/acsbiomaterials.7b00747

    Article  CAS  PubMed  Google Scholar 

  152. Lin H, Yang G, Tan J, Tuan RS (2012) Influence of decellularized matrix derived from human mesenchymal stem cells on their proliferation, migration and multi-lineage differentiation potential. Biomaterials 33:4480–4489. https://doi.org/10.1016/j.biomaterials.2012.03.012

    Article  CAS  PubMed  Google Scholar 

  153. Decaris ML, Mojadedi A, Bhat A, Leach JK (2012) Transferable cell-secreted extracellular matrices enhance osteogenic differentiation. Acta Biomater 8:744–752. https://doi.org/10.1016/j.actbio.2011.10.035

    Article  CAS  PubMed  Google Scholar 

  154. Decaris ML, Binder BY, Soicher MA, Bhat A, Leach JK (2012) Cell-derived matrix coatings for polymeric scaffolds. Tissue Eng Part A 18:2148–2157. https://doi.org/10.1089/ten.TEA.2011.0677

    Article  CAS  PubMed  Google Scholar 

  155. Keane TJ et al (2015) Tissue-specific effects of esophageal extracellular matrix. Tissue Eng Part A 21:2293–2300. https://doi.org/10.1089/ten.TEA.2015.0322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Shegarfi H, Reikeras O (2009) Review article: bone transplantation and immune response. J Orthop Surg 17:206–211. https://doi.org/10.1177/230949900901700218

    Article  Google Scholar 

  157. Bose S, Roy M, Bandyopadhyay A (2012) Recent advances in bone tissue engineering scaffolds. Trends Biotechnol 30:546–554. https://doi.org/10.1016/j.tibtech.2012.07.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Kittaka M et al (2015) Clumps of a mesenchymal stromal cell/extracellular matrix complex can be a novel tissue engineering therapy for bone regeneration. Cytotherapy 17:860–873. https://doi.org/10.1016/j.jcyt.2015.01.007

    Article  CAS  PubMed  Google Scholar 

  159. Motoike S et al (2018) Cryopreserved clumps of mesenchymal stem cell/extracellular matrix complexes retain osteogenic capacity and induce bone regeneration. Stem Cell Res Ther 9:73. https://doi.org/10.1186/s13287-018-0826-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Onishi T et al (2018) Osteogenic extracellular matrix sheet for bone tissue regeneration. Eur Cell Mater 36:68–80. https://doi.org/10.22203/eCM.v036a06

    Article  CAS  PubMed  Google Scholar 

  161. Akahane M et al (2010) Scaffold-free cell sheet injection results in bone formation. J Tissue Eng Regen Med 4:404–411. https://doi.org/10.1002/term.259

    Article  CAS  PubMed  Google Scholar 

  162. Nakamura A et al (2010) Cell sheet transplantation of cultured mesenchymal stem cells enhances bone formation in a rat nonunion model. Bone 46:418–424. https://doi.org/10.1016/j.bone.2009.08.048

    Article  CAS  PubMed  Google Scholar 

  163. Akahane M et al (2008) Osteogenic matrix sheet-cell transplantation using osteoblastic cell sheet resulted in bone formation without scaffold at an ectopic site. J Tissue Eng Regen Med 2:196–201. https://doi.org/10.1002/term.81

    Article  CAS  PubMed  Google Scholar 

  164. Gao Z et al (2009) Vitalisation of tubular coral scaffolds with cell sheets for regeneration of long bones: a preliminary study in nude mice. Br J Oral Maxillofac Surg 47:116–122. https://doi.org/10.1016/j.bjoms.2008.07.199

    Article  PubMed  Google Scholar 

  165. Kang Y, Ren L, Yang Y (2014) Engineering vascularized bone grafts by integrating a biomimetic periosteum and beta-TCP scaffold. ACS Appl Mater Interfaces 6:9622–9633. https://doi.org/10.1021/am502056q

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Liu SK et al (2018) Off-the-shelf biomimetic graphene oxide-collagen hybrid scaffolds wrapped with osteoinductive extracellular matrix for the repair of cranial defects in rats. ACS Appl Mater Inter 10:42948–42958. https://doi.org/10.1021/acsami.8b11071

    Article  CAS  Google Scholar 

  167. Matsuda N, Shimizu T, Yamato M, Okano T (2007) Tissue engineering based on cell sheet technology. Adv Mater 19:3089–3099. https://doi.org/10.1002/adma.200701978

    Article  CAS  Google Scholar 

  168. Long T et al (2014) The effect of mesenchymal stem cell sheets on structural allograft healing of critical sized femoral defects in mice. Biomaterials 35:2752–2759. https://doi.org/10.1016/j.biomaterials.2013.12.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Zou B et al (2012) Electrospun fibrous scaffolds with continuous gradations in mineral contents and biological cues for manipulating cellular behaviors. Acta Biomater 8:1576–1585. https://doi.org/10.1016/j.actbio.2012.01.003

    Article  CAS  PubMed  Google Scholar 

  170. Zhang SC et al (2019) Direct electronetting of high-performance membranes based on self-assembled 2D nanoarchitectured networks. Nat Commun 10:1458. https://doi.org/10.1038/S41467-019-09444-Y

    Article  PubMed  PubMed Central  Google Scholar 

  171. Khorshidi S et al (2016) A review of key challenges of electrospun scaffolds for tissue-engineering applications. J Tissue Eng Regen Med 10:715–738. https://doi.org/10.1002/term.1978

    Article  CAS  PubMed  Google Scholar 

  172. Reznikov N, Shahar R, Weiner S (2014) Bone hierarchical structure in three dimensions. Acta Biomater 10:3815–3826. https://doi.org/10.1016/j.actbio.2014.05.024

    Article  PubMed  Google Scholar 

  173. Carvalho MS et al (2019) Co-culture cell-derived extracellular matrix loaded electrospun microfibrous scaffolds for bone tissue engineering. Mater Sci Eng C Mater Biol Appl 99:479–490. https://doi.org/10.1016/j.msec.2019.01.127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Gibson M et al (2014) Tissue extracellular matrix nanoparticle presentation in electrospun nanofibers. Biomed Res Int 2014:469120. https://doi.org/10.1155/2014/469120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Thibault RA, Mikos AG, Kasper FK (2013) Winner of the 2013 young investigator award for the Society for Biomaterials annual meeting and exposition, April 10-13, 2013, Boston, Massachusetts Osteogenic differentiation of mesenchymal stem cells on demineralized and devitalized biodegradable polymer and extracellular matrix hybrid constructs. J Biomed Mater Res A 101:1225–1236. https://doi.org/10.1002/jbm.a.34610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Thibault RA, Scott Baggett L, Mikos AG, Kasper FK (2010) Osteogenic differentiation of mesenchymal stem cells on pregenerated extracellular matrix scaffolds in the absence of osteogenic cell culture supplements. Tissue Eng Part A 16:431–440. https://doi.org/10.1089/ten.TEA.2009.0583

    Article  CAS  PubMed  Google Scholar 

  177. Jeon H, Lee J, Lee H, Kim GH (2016) Nanostructured surface of electrospun PCL/dECM fibres treated with oxygen plasma for tissue engineering. RSC Adv 6:32887–32896. https://doi.org/10.1039/c6ra03840a

    Article  CAS  Google Scholar 

  178. Jang J, Park JY, Gao G, Cho DW (2018) Biomaterials-based 3D cell printing for next-generation therapeutics and diagnostics. Biomaterials 156:88–106. https://doi.org/10.1016/j.biomaterials.2017.11.030

    Article  CAS  PubMed  Google Scholar 

  179. Bose S, Vahabzadeh S, Bandyopadhyay A (2013) Bone tissue engineering using 3D printing. Mater Today 16:496–504. https://doi.org/10.1016/j.mattod.2013.11.017

    Article  CAS  Google Scholar 

  180. Hung BP et al (2016) Three-dimensional printing of bone extracellular matrix for craniofacial regeneration. ACS Biomater Sci Eng 2:1806–1816. https://doi.org/10.1021/acsbiomaterials.6b00101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Nyberg E, Rindone A, Dorafshar A, Grayson WL (2017) Comparison of 3D-printed poly-varepsilon-caprolactone scaffolds functionalized with tricalcium phosphate, hydroxyapatite, bio-oss, or decellularized bone matrix<sup/>. Tissue Eng Part A 23:503–514. https://doi.org/10.1089/ten.TEA.2016.0418

    Article  CAS  PubMed  Google Scholar 

  182. Chai YC et al (2017) Harnessing the osteogenicity of in vitro stem cell-derived mineralized extracellular matrix as 3D biotemplate to guide bone regeneration. Tissue Eng Part A 23:874–890. https://doi.org/10.1089/ten.tea.2016.0432

    Article  CAS  PubMed  Google Scholar 

  183. Kim JY et al (2018) Synergistic effects of beta tri-calcium phosphate and porcine-derived decellularized bone extracellular matrix in 3D-printed polycaprolactone scaffold on bone regeneration. Macromol Biosci 18:1800025. https://doi.org/10.1002/Mabi.201800025

    Article  Google Scholar 

  184. Davis HE, Leach JK (2011) Designing bioactive delivery systems for tissue regeneration. Ann Biomed Eng 39:1–13. https://doi.org/10.1007/s10439-010-0135-y

    Article  PubMed  Google Scholar 

  185. Wang XH et al (2016) 3D bioprinting technologies for hard tissue and organ engineering. Materials (Basel) 9:802. https://doi.org/10.3390/Ma9100802

    Article  Google Scholar 

  186. Mandrycky C, Wang ZJ, Kim K, Kim DH (2016) 3D bioprinting for engineering complex tissues. Biotechnol Adv 34:422–434. https://doi.org/10.1016/j.biotechadv.2015.12.011

    Article  CAS  PubMed  Google Scholar 

  187. Jang J et al (2016) Tailoring mechanical properties of decellularized extracellular matrix bioink by vitamin B2-induced photo-crosslinking. Acta Biomater 33:88–95. https://doi.org/10.1016/j.actbio.2016.01.013

    Article  CAS  PubMed  Google Scholar 

  188. Pati F et al (2014) Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun 5:3935. https://doi.org/10.1038/Ncomms4935

    Article  CAS  PubMed  Google Scholar 

  189. Hughes CS, Postovit LM, Lajoie GA (2010) Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics 10:1886–1890. https://doi.org/10.1002/pmic.200900758

    Article  CAS  PubMed  Google Scholar 

Download references

Conflicts of Interest

The authors declare that they have no competing financial interest.

Author information

Authors and Affiliations

  1. Department of Orthopaedics, School of Medicine, West Virginia University, Morgantown, WV, USA

    Sheng Zhou

  2. Department of Sports Medicine and Adult Reconstructive Surgery, School of Medicine, Nanjing Drum Tower Hospital, Nanjing University, Nanjing, Jiangsu, People’s Republic of China

    Sheng Zhou, Shichao Zhang & Qing Jiang

Authors
  1. Sheng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shichao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qing Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qing Jiang .

Editor information

Editors and Affiliations

  1. Department of Orthopaedics School of Medicine, West Virginia University, Morgantown, WV, USA

    Bingyun Li

  2. AO Research Institute Davos, Davos Platz, Graubünden, Switzerland

    Thomas Fintan Moriarty

  3. Department of Chemical Engineering, Northeastern University, Boston, MA, USA

    Thomas Webster

  4. Department of Mechanical Engineering, University of Manitoba, Winnipeg, MB, Canada

    Malcolm Xing

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Zhou, S., Zhang, S., Jiang, Q. (2020). Extracellular Matrix-based Materials for Bone Regeneration. In: Li, B., Moriarty, T., Webster, T., Xing, M. (eds) Racing for the Surface. Springer, Cham. https://doi.org/10.1007/978-3-030-34471-9_19

Download citation

Publish with us

Policies and ethics

Search

Navigation