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Functional Augmentation of Naturally-Derived Materials for Tissue Regeneration

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Abstract

Tissue engineering strategies have utilized a wide spectrum of synthetic and naturally-derived scaffold materials. Synthetic scaffolds are better defined and offer the ability to precisely and reproducibly control their properties, while naturally-derived scaffolds typically have inherent biological and structural properties that may facilitate tissue growth and remodeling. More recently, efforts to design optimized biomaterial scaffolds have blurred the line between these two approaches. Naturally-derived scaffolds can be engineered through the manipulation of intrinsic properties of the pre-existing backbone (e.g., structural properties), as well as the addition of controllable functional components (e.g., biological properties). Chemical and physical processing techniques used to modify structural properties of synthetic scaffolds have been tailored and applied to naturally-derived materials. Such strategies include manipulation of mechanical properties, degradation, and porosity. Furthermore, biofunctional augmentation of natural scaffolds via incorporation of exogenous cells, proteins, peptides, or genes has been shown to enhance functional regeneration over endogenous response to the material itself. Moving forward, the regenerative mode of action of naturally-derived materials requires additional investigation. Elucidating such mechanisms will allow for the determination of critical design parameters to further enhance efficacy and capitalize on the full potential of naturally-derived scaffolds.

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References

  1. Adair-Kirk, T. L., J. J. Atkinson, T. J. Broekelmann, M. Doi, K. Tryggvason, J. H. Miner, R. P. Mecham, and R. M. Senior. A site on laminin alpha 5, AQARSAASKVKVSMKF, induces inflammatory cell production of matrix metalloproteinase-9 and chemotaxis. J. Immunol. 171:398–406, 2003.

    CAS  PubMed  Google Scholar 

  2. Allen, A. B., Z. Gazit, S. Su, H. Y. Stevens, and R. E. Guldberg. In vivo bioluminescent tracking of mesenchymal stem cells within large hydrogel constructs. Tissue Eng. Part C Methods 20:806–816, 2014.

  3. Alsberg, E., H. J. Kong, Y. Hirano, M. K. Smith, A. Albeiruti, and D. J. Mooney. Regulating bone formation via controlled scaffold degradation. J. Dent. Res. 82:903–908, 2003.

    CAS  PubMed  Google Scholar 

  4. Andree, B., A. Bar, A. Haverich, and A. Hilfiker. Small intestinal submucosa segments as matrix for tissue engineering: review. Tissue Eng. Part B Rev. 19:279–291, 2013.

    CAS  PubMed  Google Scholar 

  5. Anitua, E., I. Andia, B. Ardanza, P. Nurden, and A. T. Nurden. Autologous platelets as a source of proteins for healing and tissue regeneration. Thromb. Haemost. 91:4–15, 2004.

    CAS  PubMed  Google Scholar 

  6. Annabi, N., S. M. Mithieux, A. S. Weiss, and F. Dehghani. Cross-linked open-pore elastic hydrogels based on tropoelastin, elastin and high pressure CO2. Biomaterials 31:1655–1665, 2010.

    CAS  PubMed  Google Scholar 

  7. Annabi, N., S. M. Mithieux, A. S. Weiss, and F. Dehghani. The fabrication of elastin-based hydrogels using high pressure CO2. Biomaterials 30:1–7, 2009.

    CAS  PubMed  Google Scholar 

  8. Bajaj, P., R. M. Schweller, A. Khademhosseini, J. L. West, and R. Bashir. 3D biofabrication strategies for tissue engineering and regenerative medicine. Ann. Rev. Biomed. Eng. 16:247–276, 2014.

  9. Boontheekul, T., H. J. Kong, and D. J. Mooney. Controlling alginate gel degradation utilizing partial oxidation and bimodal molecular weight distribution. Biomaterials 26:2455–2465, 2005.

    CAS  PubMed  Google Scholar 

  10. Bouhadir, K. H., K. Y. Lee, E. Alsberg, K. L. Damm, K. W. Anderson, and D. J. Mooney. Degradation of partially oxidized alginate and its potential application for tissue engineering. Biotechnol. Prog. 17:945–950, 2001.

    CAS  PubMed  Google Scholar 

  11. Breitbart, E. A., S. Meade, V. Azad, S. Yeh, L. Al-Zube, Y. S. Lee, J. Benevenia, T. L. Arinzeh, and S. S. Lin. Mesenchymal stem cells accelerate bone allograft incorporation in the presence of diabetes mellitus. J. Orthop. Res. 28:942–949, 2010.

    PubMed  Google Scholar 

  12. Brown, B. N., and S. F. Badylak. Extracellular matrix as an inductive scaffold for functional tissue reconstruction. Transl. Res. 163:268–285, 2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  13. Burdick, J. A., and G. D. Prestwich. Hyaluronic acid hydrogels for biomedical applications. Adv. Mater. 23:H41–H56, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  14. Cai, S., Y. Liu, X. Zheng Shu, and G. D. Prestwich. Injectable glycosaminoglycan hydrogels for controlled release of human basic fibroblast growth factor. Biomaterials 26:6054–6067, 2005.

    CAS  PubMed  Google Scholar 

  15. Caliari, S. R., M. A. Ramirez, and B. A. Harley. The development of collagen-GAG scaffold-membrane composites for tendon tissue engineering. Biomaterials 32:8990–8998, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  16. Caplan, A. I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell. Physiol. 213:341–347, 2007.

    CAS  PubMed  Google Scholar 

  17. Casettari, L., D. Vllasaliu, J. K. Lam, M. Soliman, and L. Illum. Biomedical applications of amino acid-modified chitosans: a review. Biomaterials 33:7565–7583, 2012.

    CAS  PubMed  Google Scholar 

  18. Cavazzana-Calvo, M., A. Thrasher, and F. Mavilio. The future of gene therapy. Nature 427:779–781, 2004.

    CAS  PubMed  Google Scholar 

  19. Caves, J. M., W. Cui, J. Wen, V. A. Kumar, C. A. Haller, and E. L. Chaikof. Elastin-like protein matrix reinforced with collagen microfibers for soft tissue repair. Biomaterials 32:5371–5379, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  20. Chan, B. K., C. C. Wippich, C. J. Wu, P. M. Sivasankar, and G. Schmidt. Robust and semi-interpenetrating hydrogels from poly(ethylene glycol) and collagen for elastomeric tissue scaffolds. Macromol. Biosci. 12:1490–1501, 2012.

    CAS  PubMed  Google Scholar 

  21. Chen, B. S., H. Xie, S. L. Zhang, H. Q. Geng, J. M. Zhou, J. Pan, and F. Chen. Tissue engineering of bladder using vascular endothelial growth factor gene-modified endothelial progenitor cells. Int. J. Artif. Organs 34:1137–1146, 2011.

    CAS  PubMed  Google Scholar 

  22. Chen, L., X. Lu, S. Li, Q. Sun, W. Li, and D. Song. Sustained delivery of BMP-2 and platelet-rich plasma-released growth factors contributes to osteogenesis of human adipose-derived stem cells. Orthopedics. 35:e1402–e1409, 2012.

    PubMed  Google Scholar 

  23. Choi, Y. J., J. Y. Lee, J. H. Park, J. B. Park, J. S. Suh, Y. S. Choi, S. J. Lee, C. P. Chung, and Y. J. Park. The identification of a heparin binding domain peptide from bone morphogenetic protein-4 and its role on osteogenesis. Biomaterials 31:7226–7238, 2010.

    CAS  PubMed  Google Scholar 

  24. Chow, L. W., R. Bitton, M. J. Webber, D. Carvajal, K. R. Shull, A. K. Sharma, and S. I. Stupp. A bioactive self-assembled membrane to promote angiogenesis. Biomaterials 32:1574–1582, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Collins, C., L. D. Osborne, C. Guilluy, Z. Chen, E. T. O’Brien, 3rd, J. S. Reader, K. Burridge, R. Superfine, and E. Tzima. Haemodynamic and extracellular matrix cues regulate the mechanical phenotype and stiffness of aortic endothelial cells. Nat Commun. 5:3984, 2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  26. Dang, J. M., and K. W. Leong. Natural polymers for gene delivery and tissue engineering. Adv Drug Deliver Rev. 58:487–499, 2006.

    CAS  Google Scholar 

  27. De Paoli Lacerda, S. H., B. Ingber, and N. Rosenzweig. Structure-release rate correlation in collagen gels containing fluorescent drug analog. Biomaterials 26:7164–7172, 2005.

    CAS  PubMed  Google Scholar 

  28. Dewavrin, J.-Y., N. Hamzavi, V. P. W. Shim, and M. Raghunath. Tuning the architecture of 3D collagen hydrogels by physiological macromolecular crowding. Acta Biomater. 2014. doi:10.1016/j.actbio.2014.06.006.

    PubMed  Google Scholar 

  29. El-Sharkawy, H., A. Kantarci, J. Deady, H. Hasturk, H. Liu, M. Alshahat, and T. E. Van Dyke. Platelet-rich plasma: growth factors and pro- and anti-inflammatory properties. J. Periodontol. 78:661–669, 2007.

    CAS  PubMed  Google Scholar 

  30. Elangovan, S., S. R. D’Mello, L. Hong, R. D. Ross, C. Allamargot, D. V. Dawson, C. M. Stanford, G. K. Johnson, D. R. Sumner, and A. K. Salem. The enhancement of bone regeneration by gene activated matrix encoding for platelet derived growth factor. Biomaterials 35:737–747, 2014.

    CAS  PubMed  Google Scholar 

  31. Engelhardt, E. M., L. A. Micol, S. Houis, F. M. Wurm, J. Hilborn, J. A. Hubbell, and P. Frey. A collagen-poly(lactic acid-co-varepsilon-caprolactone) hybrid scaffold for bladder tissue regeneration. Biomaterials 32:3969–3976, 2011.

    CAS  PubMed  Google Scholar 

  32. Engler, A. J., S. Sen, H. L. Sweeney, and D. E. Discher. Matrix elasticity directs stem cell lineage specification. Cell 126:677–689, 2006.

    CAS  PubMed  Google Scholar 

  33. Erdbrugger, W., W. Konertz, P. M. Dohmen, S. Posner, H. Ellerbrok, O. E. Brodde, H. Robenek, D. Modersohn, A. Pruss, S. Holinski, M. Stein-Konertz, and G. Pauli. Decellularized xenogenic heart valves reveal remodeling and growth potential in vivo. Tissue Eng. 12:2059–2068, 2006.

    PubMed  Google Scholar 

  34. Evans, C. H. Advances in regenerative orthopedics. Mayo Clin. Proc. 88:1323–1339, 2013.

    PubMed Central  PubMed  Google Scholar 

  35. Falanga, V., S. Iwamoto, M. Chartier, T. Yufit, J. Butmarc, N. Kouttab, D. Shrayer, and P. Carson. Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng. 13:1299–1312, 2007.

    CAS  PubMed  Google Scholar 

  36. Fu, J., Y. K. Wang, M. T. Yang, R. A. Desai, X. Yu, Z. Liu, and C. S. Chen. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat. Methods 7:733–736, 2010.

    PubMed Central  CAS  PubMed  Google Scholar 

  37. Gao, M., P. Lu, B. Bednark, D. Lynam, J. M. Conner, J. Sakamoto, and M. H. Tuszynski. Templated agarose scaffolds for the support of motor axon regeneration into sites of complete spinal cord transection. Biomaterials 34:1529–1536, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  38. Gelse, K., E. Poschl, and T. Aigner. Collagens–structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 55:1531–1546, 2003.

    CAS  PubMed  Google Scholar 

  39. Glover, D. J., H. J. Lipps, and D. A. Jans. Towards safe, non-viral therapeutic gene expression in humans. Nat. Rev. Genet. 6:299–310, 2005.

    CAS  PubMed  Google Scholar 

  40. Gu, H., Z. Xiong, X. Yin, B. Li, N. Mei, G. Li, and C. Wang. Bone regeneration in a rabbit ulna defect model: use of allogeneic adipose-derived stem cells with low immunogenicity. Cell Tissue Res. 358:453–464, 2014.

  41. Guo, H. D., G. H. Cui, J. J. Yang, C. Wang, J. Zhu, L. S. Zhang, J. Jiang, and S. J. Shao. Sustained delivery of VEGF from designer self-assembling peptides improves cardiac function after myocardial infarction. Biochem. Biophys. Res. Commun. 424:105–111, 2012.

    CAS  PubMed  Google Scholar 

  42. Haghi, A. K., and M. Akbari. Trends in electrospinning of natural nanofibers. Phys. Status Solidi A 204:1830–1834, 2007.

    CAS  Google Scholar 

  43. Hahn, S. K., J. S. Kim, and T. Shimobouji. Injectable hyaluronic acid microhydrogels for controlled release formulation of erythropoietin. J. Biomed. Mater. Res. A 80:916–924, 2007.

    PubMed  Google Scholar 

  44. Harley, B. A., M. H. Spilker, J. W. Wu, K. Asano, H. P. Hsu, M. Spector, and I. V. Yannas. Optimal degradation rate for collagen chambers used for regeneration of peripheral nerves over long gaps. Cells Tissues Organs 176:153–165, 2004.

    CAS  PubMed  Google Scholar 

  45. Harvey, A. L. Natural products in drug discovery. Drug Discov. Today. 13:894–901, 2008.

    CAS  PubMed  Google Scholar 

  46. Hersel, U., C. Dahmen, and H. Kessler. RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24:4385–4415, 2003.

    CAS  PubMed  Google Scholar 

  47. Hettiaratchi, M. H., T. Miller, J. S. Temenoff, R. E. Guldberg, and T. C. McDevitt. Heparin microparticle effects on presentation and bioactivity of bone morphogenetic protein-2. Biomaterials 35:7228–7238, 2014.

    CAS  PubMed  Google Scholar 

  48. Hodde, J. P., R. D. Record, H. A. Liang, and S. F. Badylak. Vascular endothelial growth factor in porcine-derived extracellular matrix. Endothelium 8:11–24, 2001.

    CAS  PubMed  Google Scholar 

  49. Hoffmann, A., G. Pelled, G. Turgeman, P. Eberle, Y. Zilberman, H. Shinar, K. Keinan-Adamsky, A. Winkel, S. Shahab, G. Navon, G. Gross, and D. Gazit. Neotendon formation induced by manipulation of the Smad8 signalling pathway in mesenchymal stem cells. J. Clin. Invest. 116:940–952, 2006.

    PubMed Central  CAS  PubMed  Google Scholar 

  50. Houghton, A. M., P. A. Quintero, D. L. Perkins, D. K. Kobayashi, D. G. Kelley, L. A. Marconcini, R. P. Mecham, R. M. Senior, and S. D. Shapiro. Elastin fragments drive disease progression in a murine model of emphysema. J. Clin. Invest. 116:753–759, 2006.

    PubMed Central  CAS  PubMed  Google Scholar 

  51. Howes, E. L., and S. C. Harvey. The strength of the healing wound in relation to the holding strength of the catgut suture. New Engl J. Med. 200:1285–1291, 1929.

    Google Scholar 

  52. Huang, N. F., A. Lam, Q. Fang, R. E. Sievers, S. Li, and R. J. Lee. Bone marrow-derived mesenchymal stem cells in fibrin augment angiogenesis in the chronically infarcted myocardium. Regen. Med. 4:527–538, 2009.

    PubMed Central  CAS  PubMed  Google Scholar 

  53. Inzana, J. A., D. Olvera, S. M. Fuller, J. P. Kelly, O. A. Graeve, E. M. Schwarz, S. L. Kates, and H. A. Awad. 3D printing of composite calcium phosphate and collagen scaffolds for bone regeneration. Biomaterials 35:4026–4034, 2014.

    CAS  PubMed  Google Scholar 

  54. Ito, H., M. Koefoed, P. Tiyapatanaputi, K. Gromov, J. J. Goater, J. Carmouche, X. Zhang, P. T. Rubery, J. Rabinowitz, R. J. Samulski, T. Nakamura, K. Soballe, R. J. O’Keefe, B. F. Boyce, and E. M. Schwarz. Remodeling of cortical bone allografts mediated by adherent rAAV-RANKL and VEGF gene therapy. Nat. Med. 11:291–297, 2005.

    PubMed Central  CAS  PubMed  Google Scholar 

  55. Jang, Y. S., C. H. Choi, Y. B. Cho, M. K. Kang, and C. H. Jang. Recombinant human BMP-2 enhances osteogenesis of demineralized bone matrix in experimental mastoid obliteration. Acta Otolaryngol. 134:785–790, 2014.

    CAS  PubMed  Google Scholar 

  56. Jayasuriya, A. C., and N. A. Ebraheim. Evaluation of bone matrix and demineralized bone matrix incorporated PLGA matrices for bone repair. J. Mater. Sci.-Mater. M. 20:1637–1644, 2009.

    Google Scholar 

  57. Jeon, O., C. Powell, L. D. Solorio, M. D. Krebs, and E. Alsberg. Affinity-based growth factor delivery using biodegradable, photocrosslinked heparin-alginate hydrogels. J. Control Release. 154:258–266, 2011.

    PubMed Central  CAS  PubMed  Google Scholar 

  58. Jeon, O., J. E. Samorezov, and E. Alsberg. Single and dual crosslinked oxidized methacrylated alginate/PEG hydrogels for bioadhesive applications. Acta Biomater. 10:47–55, 2014.

    CAS  PubMed  Google Scholar 

  59. Ji, J., B. Bar-On, and H. D. Wagner. Mechanics of electrospun collagen and hydroxyapatite/collagen nanofibers. J. Mech. Behav. Biomed. Mater. 13:185–193, 2012.

    CAS  PubMed  Google Scholar 

  60. Jia, H., G. Zhu, B. Vugrinovich, W. Kataphinan, D. H. Reneker, and P. Wang. Enzyme-carrying polymeric nanofibers prepared via electrospinning for use as unique biocatalysts. Biotechnol. Prog. 18:1027–1032, 2002.

    CAS  PubMed  Google Scholar 

  61. Jiang, T., G. Wang, J. Qiu, L. Luo, and G. Zhang. Heparinized poly(vinyl alcohol)—small intestinal submucosa composite membrane for coronary covered stents. Biomed. Mater. 4:025012, 2009.

    PubMed  Google Scholar 

  62. Johnson, T. D., J. A. Dequach, R. Gaetani, J. Ungerleider, D. Elhag, V. Nigam, A. Behfar, and K. L. Christman. Human versus porcine tissue sourcing for an injectable myocardial matrix hydrogel. Biomater. Sci. 2014:60283D, 2014.

    PubMed Central  PubMed  Google Scholar 

  63. Kim, U. J., J. Park, H. J. Kim, M. Wada, and D. L. Kaplan. Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin. Biomaterials 26:2775–2785, 2005.

    CAS  PubMed  Google Scholar 

  64. Kode, J. A., S. Mukherjee, M. V. Joglekar, and A. A. Hardikar. Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy. 11:377–391, 2009.

    CAS  PubMed  Google Scholar 

  65. Kong, H. J., J. D. Liu, K. Riddle, T. Matsumoto, K. Leach, and D. J. Mooney. Non-viral gene delivery regulated by stiffness of cell adhesion substrates. Nat. Mater. 4:460–464, 2005.

    CAS  PubMed  Google Scholar 

  66. Koob, T. J., R. Rennert, N. Zabek, M. Massee, J. J. Lim, J. S. Temenoff, W. W. Li, and G. Gurtner. Biological properties of dehydrated human amnion/chorion composite graft: implications for chronic wound healing. Int. Wound J. 10:493–500, 2013.

    PubMed Central  PubMed  Google Scholar 

  67. Krishna, O. D., and K. L. Kiick. Protein- and peptide-modified synthetic polymeric biomaterials. Biopolymers 94:32–48, 2010.

    CAS  PubMed  Google Scholar 

  68. Kumar, G., H. Hara, C. Long, H. Shaikh, D. Ayares, D. K. Cooper, and M. Ezzelarab. Adipose-derived mesenchymal stromal cells from genetically modified pigs: immunogenicity and immune modulatory properties. Cytotherapy. 14:494–504, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  69. Kurkalli, B. G. S., O. Gurevitch, A. Sosnik, D. Cohn, and S. Slavin. Repair of bone defect using bone marrow cells and demineralized bone matrix supplemented with polymeric materials. Curr. Stem Cell Res. T. 5:49–56, 2010.

    CAS  Google Scholar 

  70. Leach, J. B., J. B. Wolinsky, P. J. Stone, and J. Y. Wong. Crosslinked alpha-elastin biomaterials: towards a processable elastin mimetic scaffold. Acta Biomater. 1:155–164, 2005.

    PubMed  Google Scholar 

  71. Lee, F., J. E. Chung, and M. Kurisawa. An injectable hyaluronic acid-tyramine hydrogel system for protein delivery. J. Control Release. 134:186–193, 2009.

    CAS  PubMed  Google Scholar 

  72. Lee, H. J., and W. G. Koh. Hydrogel micropattern-incorporated fibrous scaffolds capable of sequential growth factor delivery for enhanced osteogenesis of hMSCs. ACS Appl. Mater. Interfaces. 6:9338–9348, 2014.

    CAS  PubMed  Google Scholar 

  73. Li, J., M. B. Ezzelarab, D. Ayares, and D. K. Cooper. The potential role of genetically-modified pig mesenchymal stromal cells in xenotransplantation. Stem Cell Rev. 10:79–85, 2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  74. Lin, K. L., L. Chen, H. Y. Qu, J. X. Lu, and J. Chang. Improvement of mechanical properties of macroporous beta-tricalcium phosphate bioceramic scaffolds with uniform and interconnected pore structures. Ceram. Int. 37:2397–2403, 2011.

    CAS  Google Scholar 

  75. Liu, Z., X. Feng, H. Wang, J. Ma, W. Liu, D. Cui, Y. Gu, and R. Tang. Carbon nanotubes as VEGF carriers to improve the early vascularization of porcine small intestinal submucosa in abdominal wall defect repair. Int. J. Nanomed. 9:1275–1286, 2014.

    Google Scholar 

  76. Lu, C. H., Y. H. Chang, S. Y. Lin, K. C. Li, and Y. C. Hu. Recent progresses in gene delivery-based bone tissue engineering. Biotechnol. Adv. 31:1695–1706, 2013.

    CAS  PubMed  Google Scholar 

  77. Lutolf, M. P., and J. A. Hubbell. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat. Biotechnol. 23:47–55, 2005.

    CAS  PubMed  Google Scholar 

  78. Ma, F., Z. Xiao, B. Chen, X. Hou, J. Dai, and R. Xu. Linear ordered collagen scaffolds loaded with collagen-binding basic fibroblast growth factor facilitate recovery of sciatic nerve injury in rats. Tissue Eng. Part A 20:1253–1262, 2014.

    CAS  PubMed  Google Scholar 

  79. Maheshwari, G., G. Brown, D. A. Lauffenburger, A. Wells, and L. G. Griffith. Cell adhesion and motility depend on nanoscale RGD clustering. J. Cell Sci. 113(Pt 10):1677–1686, 2000.

    CAS  PubMed  Google Scholar 

  80. Malafaya, P. B., G. A. Silva, and R. L. Reis. Natural-origin polymers as carriers and scaffolds for biomolecules and cell delivery in tissue engineering applications. Adv. Drug Deliv. Rev. 59:207–233, 2007.

    CAS  PubMed  Google Scholar 

  81. Marelli, B., C. E. Ghezzi, D. Mohn, W. J. Stark, J. E. Barralet, A. R. Boccaccini, and S. N. Nazhat. Accelerated mineralization of dense collagen-nano bioactive glass hybrid gels increases scaffold stiffness and regulates osteoblastic function. Biomaterials 32:8915–8926, 2011.

    CAS  PubMed  Google Scholar 

  82. Marshall, A. J., and B. D. Ratner. Quantitative characterization of sphere-templated porous biomaterials. AIChE J. 51:1221–1232, 2005.

    CAS  Google Scholar 

  83. Martinez, E. C., D. T. Vu, J. Wang, S. Lilyanna, L. H. Ling, S. U. Gan, A. L. Tan, T. T. Phan, C. N. Lee, and T. Kofidis. Grafts enriched with subamnion-cord-lining mesenchymal stem cell angiogenic spheroids induce post-ischemic myocardial revascularization and preserve cardiac function in failing rat hearts. Stem Cells Dev. 22:3087–3099, 2013.

    PubMed Central  CAS  PubMed  Google Scholar 

  84. Martino, M. M., P. S. Briquez, E. Guc, F. Tortelli, W. W. Kilarski, S. Metzger, J. J. Rice, G. A. Kuhn, R. Muller, M. A. Swartz, and J. A. Hubbell. Growth factors engineered for super-affinity to the extracellular matrix enhance tissue healing. Science 343:885–888, 2014.

    CAS  PubMed  Google Scholar 

  85. Mueller-Rath, R., K. Gavenis, S. Andereya, T. Mumme, M. Albrand, M. Stoffel, D. Weichert, and U. Schneider. Condensed cellular seeded collagen gel as an improved biomaterial for tissue engineering of articular cartilage. Bio-Med. Mater. Eng. 20:317–328, 2010.

    CAS  Google Scholar 

  86. Murphy, W. L., T. C. McDevitt, and A. J. Engler. Materials as stem cell regulators. Nat. Mater. 13:547–557, 2014.

    PubMed Central  CAS  PubMed  Google Scholar 

  87. Nauta, A. J., and W. E. Fibbe. Immunomodulatory properties of mesenchymal stromal cells. Blood 110:3499–3506, 2007.

    CAS  PubMed  Google Scholar 

  88. Neff, J. A., P. A. Tresco, and K. D. Caldwell. Surface modification for controlled studies of cell–ligand interactions. Biomaterials 20:2377–2393, 1999.

    CAS  PubMed  Google Scholar 

  89. Park, H., J. S. Temenoff, Y. Tabata, A. I. Caplan, R. M. Raphael, J. A. Jansen, and A. G. Mikos. Effect of dual growth factor delivery on chondrogenic differentiation of rabbit marrow mesenchymal stem cells encapsulated in injectable hydrogel composites. J. Biomed. Mater. Res. A. 88:889–897, 2009.

    PubMed  Google Scholar 

  90. Park, Y. D., N. Tirelli, and J. A. Hubbell. Photopolymerized hyaluronic acid-based hydrogels and interpenetrating networks. Biomaterials 24:893–900, 2003.

    CAS  PubMed  Google Scholar 

  91. Pellegrini, L., D. F. Burke, F. von Delft, B. Mulloy, and T. L. Blundell. Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature 407:1029–1034, 2000.

    CAS  PubMed  Google Scholar 

  92. Pierschbacher, M. D., and E. Ruoslahti. Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. J. Biol. Chem. 262:17294–17298, 1987.

    CAS  PubMed  Google Scholar 

  93. Pietrzak, W. S., J. Woodell-May, and N. McDonald. Assay of bone morphogenetic protein-2, -4, and -7 in human demineralized bone matrix. J. Craniofac. Surg. 17:84–90, 2006.

    PubMed  Google Scholar 

  94. Priddy, L. B., O. Chaudhuri, H. Y. Stevens, L. Krishnan, B. A. Uhrig, N. J. Willett, and R. E. Guldberg, Oxidized alginate hydrogels for bone morphogenetic protein-2 delivery in long bone defects. Acta Biomater. 10:4390–4399, 2014.

  95. Puppi, D., F. Chiellini, A. M. Piras, and E. Chiellini. Polymeric materials for bone and cartilage repair. Prog. Polym. Sci. 35:403–440, 2010.

    CAS  Google Scholar 

  96. Rabenstein, D. L. Heparin and heparan sulfate: structure and function. Nat. Prod. Rep. 19:312–331, 2002.

    CAS  PubMed  Google Scholar 

  97. Renth, A. N., and M. S. Detamore. Leveraging, “raw materials” as building blocks and bioactive signals in regenerative medicine. Tissue Eng. Part B Rev. 18:341–362, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  98. Rezwan, K., Q. Z. Chen, J. J. Blaker, and A. R. Boccaccini. Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 27:3413–3431, 2006.

    CAS  PubMed  Google Scholar 

  99. Rnjak-Kovacina, J., S. G. Wise, Z. Li, P. K. Maitz, C. J. Young, Y. Wang, and A. S. Weiss. Electrospun synthetic human elastin:collagen composite scaffolds for dermal tissue engineering. Acta Biomater. 8:3714–3722, 2012.

    CAS  PubMed  Google Scholar 

  100. Rosso, F., G. Marino, A. Giordano, M. Barbarisi, D. Parmeggiani, and A. Barbarisi. Smart materials as scaffolds for tissue engineering. J. Cell. Physiol. 203:465–470, 2005.

    CAS  PubMed  Google Scholar 

  101. Rowley, J. A., and D. J. Mooney. Alginate type and RGD density control myoblast phenotype. J. Biomed. Mater. Res. 60:217–223, 2002.

    CAS  PubMed  Google Scholar 

  102. Ruoslahti, E. The RGD story: a personal account. Matrix Biol. 22:459–465, 2003.

    CAS  PubMed  Google Scholar 

  103. Schantz, J. T., D. W. Hutmacher, C. X. Lam, M. Brinkmann, K. M. Wong, T. C. Lim, N. Chou, R. E. Guldberg, and S. H. Teoh. Repair of calvarial defects with customised tissue-engineered bone grafts II. Evaluation of cellular efficiency and efficacy in vivo. Tissue Eng. 9(Suppl 1):S127–S139, 2003.

    CAS  PubMed  Google Scholar 

  104. Schmidt, C., D. Bezuidenhout, P. Zilla, and N. H. Davies. A slow-release fibrin matrix increases adeno-associated virus transduction of wound repair cells in vivo. J. Biomater. Appl. 28:1408–1418, 2014.

    CAS  PubMed  Google Scholar 

  105. Schmoekel, H. G., F. E. Weber, J. C. Schense, K. W. Gratz, P. Schawalder, and J. A. Hubbell. Bone repair with a form of BMP-2 engineered for incorporation into fibrin cell ingrowth matrices. Biotechnol. Bioeng. 89:253–262, 2005.

    CAS  PubMed  Google Scholar 

  106. Schubert, T., H. Poilvache, C. Galli, P. Gianello, and D. Dufrane. Galactosyl-knock-out engineered pig as a xenogenic donor source of adipose MSCs for bone regeneration. Biomaterials 34:3279–3289, 2013.

    CAS  PubMed  Google Scholar 

  107. Senior, R. M., A. Hinek, G. L. Griffin, D. J. Pipoly, E. C. Crouch, and R. P. Mecham. Neutrophils show chemotaxis to type-Iv collagen and Its 7s domain and contain a 67-Kd type-Iv collagen binding-protein with lectin properties. Am. J. Resp. Cell Mol. 1:479–487, 1989.

    CAS  Google Scholar 

  108. Sheyn, D., M. Ruthemann, O. Mizrahi, I. Kallai, Y. Zilberman, W. Tawackoli, L. E. A. Kanim, L. Zhao, H. Bae, G. Pelled, J. G. Snedeker, and D. Gazit. Genetically modified mesenchymal stem cells induce mechanically stable posterior spine fusion. Tissue Eng. Pt. A. 16:3679–3686, 2010.

    CAS  Google Scholar 

  109. Shoichet, M. S., R. H. Li, M. L. White, and S. R. Winn. Stability of hydrogels used in cell encapsulation: an in vitro comparison of alginate and agarose. Biotechnol. Bioeng. 50:374–381, 1996.

    CAS  PubMed  Google Scholar 

  110. Silva, E. A., and D. J. Mooney. Spatiotemporal control of vascular endothelial growth factor delivery from injectable hydrogels enhances angiogenesis. J. Thromb. Haemost. 5:590–598, 2007.

    CAS  PubMed  Google Scholar 

  111. Silva, R., B. Fabry, and A. R. Boccaccini. Fibrous protein-based hydrogels for cell encapsulation. Biomaterials 35:6727–6738, 2014.

    CAS  PubMed  Google Scholar 

  112. Simmons, C. A., E. Alsberg, S. Hsiong, W. J. Kim, and D. J. Mooney. Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells. Bone 35:562–569, 2004.

    CAS  PubMed  Google Scholar 

  113. Stabenfeldt, S. E., M. Gourley, L. Krishnan, J. B. Hoying, and T. H. Barker. Engineering fibrin polymers through engagement of alternative polymerization mechanisms. Biomaterials 33:535–544, 2012.

    PubMed Central  CAS  PubMed  Google Scholar 

  114. Storm, C., J. J. Pastore, F. C. MacKintosh, T. C. Lubensky, and P. A. Janmey. Nonlinear elasticity in biological gels. Nature 435:191–194, 2005.

    CAS  PubMed  Google Scholar 

  115. Syedain, Z. H., J. S. Weinberg, and R. T. Tranquillo. Cyclic distension of fibrin-based tissue constructs: evidence of adaptation during growth of engineered connective tissue. Proc. Natl. Acad. Sci. USA 105:6537–6542, 2008.

    PubMed Central  CAS  PubMed  Google Scholar 

  116. Tejeda-Montes, E., K. H. Smith, M. Poch, M. J. Lopez-Bosque, L. Martin, M. Alonso, E. Engel, and A. Mata. Engineering membrane scaffolds with both physical and biomolecular signaling. Acta Biomater. 8:998–1009, 2012.

    CAS  PubMed  Google Scholar 

  117. Tejeda-Montes, E., K. H. Smith, E. Rebollo, R. Gomez, M. Alonso, J. C. Rodriguez-Cabello, E. Engel, and A. Mata. Bioactive membranes for bone regeneration applications: effect of physical and biomolecular signals on mesenchymal stem cell behavior. Acta Biomater. 10:134–141, 2014.

    CAS  PubMed  Google Scholar 

  118. Thomas, C. B., S. Maxson, and K. J. Burg. Preparation and characterization of a composite of demineralized bone matrix fragments and polylactide beads for bone tissue engineering. J. Biomater. Sci. Polym. Ed. 22:589–610, 2011.

    CAS  PubMed  Google Scholar 

  119. Thomas, V., D. R. Dean, M. V. Jose, B. Mathew, S. Chowdhury, and Y. K. Vohra. Nanostructured biocomposite scaffolds based on collagen coelectrospun with nanohydroxyapatite. Biomacromolecules 8:631–637, 2007.

    CAS  PubMed  Google Scholar 

  120. Valentin, J. E., A. M. Stewart-Akers, T. W. Gilbert, and S. F. Badylak. Macrophage participation in the degradation and remodeling of extracellular matrix scaffolds. Tissue Eng. Part A 15:1687–1694, 2009.

    PubMed Central  CAS  PubMed  Google Scholar 

  121. van Amerongen, M. J., M. C. Harmsen, A. H. Petersen, G. Kors, and M. J. van Luyn. The enzymatic degradation of scaffolds and their replacement by vascularized extracellular matrix in the murine myocardium. Biomaterials 27:2247–2257, 2006.

    PubMed  Google Scholar 

  122. Wallace, D. G., and J. Rosenblatt. Collagen gel systems for sustained delivery and tissue engineering. Adv. Drug Deliv. Rev. 55:1631–1649, 2003.

    CAS  PubMed  Google Scholar 

  123. Wang, L., D. M. Lai, B. Yang, Z. P. Jiang, Y. C. Zhang, J. Zhou, W. Lai, and S. Chen. Reconstruction of abdominal wall defects using small intestinal submucosa coated with gelatin hydrogel incorporating basic fibroblast growth factor. Acta Cir. Bras. 29:252–260, 2014.

    CAS  PubMed  Google Scholar 

  124. Wang, Y., M. J. Cooke, N. Sachewsky, C. M. Morshead, and M. S. Shoichet. Bioengineered sequential growth factor delivery stimulates brain tissue regeneration after stroke. J. Control Release. 172:1–11, 2013.

    CAS  PubMed  Google Scholar 

  125. Wang, Y., D. D. Rudym, A. Walsh, L. Abrahamsen, H. J. Kim, H. S. Kim, C. Kirker-Head, and D. L. Kaplan. In vivo degradation of three-dimensional silk fibroin scaffolds. Biomaterials 29:3415–3428, 2008.

    PubMed Central  CAS  PubMed  Google Scholar 

  126. Wegman, F., F. C. Oner, W. J. Dhert, and J. Alblas. Non-viral gene therapy for bone tissue engineering. Biotechnol. Genet. Eng. Rev. 29:206–220, 2013.

    CAS  PubMed  Google Scholar 

  127. West, J. L., and J. A. Hubbell. Polymeric biomaterials with degradation sites for proteases involved in cell migration. Macromolecules 32:241–244, 1999.

    CAS  Google Scholar 

  128. Wipff, P. J., and B. Hinz. Integrins and the activation of latent transforming growth factor beta1—an intimate relationship. Eur. J. Cell Biol. 87:601–615, 2008.

    CAS  PubMed  Google Scholar 

  129. Wolf, M. T., K. A. Daly, J. E. Reing, and S. F. Badylak. Biologic scaffold composed of skeletal muscle extracellular matrix. Biomaterials 33:2916–2925, 2012.

    CAS  PubMed  Google Scholar 

  130. Wust, S., R. Muller, and S. Hofmann. Controlled positioning of cells in biomaterials-approaches towards 3D tissue printing. J. Funct. Biomater. 2:119–154, 2011.

    PubMed Central  PubMed  Google Scholar 

  131. Yang, H. S., W. G. La, S. H. Bhang, J. Y. Jeon, J. H. Lee, and B. S. Kim. Heparin-conjugated fibrin as an injectable system for sustained delivery of bone morphogenetic protein-2. Tissue Eng. Pt. A. 16:1225–1233, 2010.

    CAS  Google Scholar 

  132. Yang, Y. M., W. Hu, X. D. Wang, and X. S. Gu. The controlling biodegradation of chitosan fibers by N-acetylation in vitro and in vivo. J. Mater. Sci. Mater. Med. 18:2117–2121, 2007.

    CAS  PubMed  Google Scholar 

  133. Yue, T. W., W. C. Chien, S. J. Tseng, and S. C. Tang. EDC/NHS-mediated heparinization of small intestinal submucosa for recombinant adeno-associated virus serotype 2 binding and transduction. Biomaterials 28:2350–2357, 2007.

    CAS  PubMed  Google Scholar 

  134. Yun, Y. H., D. J. Goetz, P. Yellen, and W. Chen. Hyaluronan microspheres for sustained gene delivery and site-specific targeting. Biomaterials 25:147–157, 2004.

    CAS  PubMed  Google Scholar 

  135. Zhang, F., C. He, L. Cao, W. Feng, H. Wang, X. Mo, and J. Wang. Fabrication of gelatin-hyaluronic acid hybrid scaffolds with tunable porous structures for soft tissue engineering. Int. J. Biol. Macromol. 48:474–481, 2011.

    CAS  PubMed  Google Scholar 

  136. Zhong, S., W. E. Teo, X. Zhu, R. Beuerman, S. Ramakrishna, and L. Y. Yung. Formation of collagen-glycosaminoglycan blended nanofibrous scaffolds and their biological properties. Biomacromolecules 6:2998–3004, 2005.

    CAS  PubMed  Google Scholar 

  137. Zhu, J. Bioactive modification of poly(ethylene glycol) hydrogels for tissue engineering. Biomaterials 31:4639–4656, 2010.

    PubMed Central  CAS  PubMed  Google Scholar 

  138. Zurita, M., L. Otero, C. Aguayo, C. Bonilla, E. Ferreira, A. Parajon, and J. Vaquero. Cell therapy for spinal cord repair: optimization of biologic scaffolds for survival and neural differentiation of human bone marrow stromal cells. Cytotherapy 12:522–537, 2010.

    CAS  PubMed  Google Scholar 

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  1. Wallace H. Coulter Department of Biomedical Engineering, Parker H. Petit Institute for Bioengineering & Bioscience, Georgia Institute of Technology, 315 Ferst Drive NW, Atlanta, GA, 30332, USA

    Ashley B. Allen, Lauren B. Priddy & Mon-Tzu A. Li

  2. George W. Woodruff School of Mechanical Engineering, Parker H. Petit Institute for Bioengineering & Bioscience, Georgia Institute of Technology, 315 Ferst Drive NW, Atlanta, GA, 30332, USA

    Robert E. Guldberg

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  1. Ashley B. Allen
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Allen, A.B., Priddy, L.B., Li, MT.A. et al. Functional Augmentation of Naturally-Derived Materials for Tissue Regeneration. Ann Biomed Eng 43, 555–567 (2015). https://doi.org/10.1007/s10439-014-1192-4

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