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Inspiration and application in the evolution of biomaterials

Abstract

Biomaterials, traditionally defined as materials used in medical devices, have been used since antiquity, but recently their degree of sophistication has increased significantly. Biomaterials made today are routinely information rich and incorporate biologically active components derived from nature. In the future, biomaterials will assume an even greater role in medicine and will find use in a wide variety of non-medical applications through biologically inspired design and incorporation of dynamic behaviour.

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Figure 1: History and growth of biomaterials as a field and industry.
Figure 2: Information-rich biomimetic materials.
Figure 3: Regulating biology at a distance: designing materials to target or mimic the niches of specific cell populations.
Figure 4: Using components of biological organisms and materials in novel applications.
Figure 5: The future: rethinking how inspiration is drawn from biology, and applying biological design principles to new areas.
Figure 6: The future: drawing inspiration from nature to rethink how materials and pharmaceuticals are manufactured.

References

  1. Ratner, B. D. & Bryant, S. J. Biomaterials: where we have been and where we are going. Annu. Rev. Biomed. Eng. 6, 41–75 (2004).This is an excellent, comprehensive review of the history of the biomaterials field.

    CAS  Article  Google Scholar 

  2. Anderson, J. M., Rodriguez, A. & Chang, D. T. Foreign body reaction to biomaterials. Semin. Immunol. 20, 86–100 (2008).

    CAS  Article  Google Scholar 

  3. Mroz, T., Yamashita, T. & Lieberman, I. The on- and off-label use of rhBMP-2 (INFUSE) in Medicare and non-Medicare patients. Spine J. 8, 41S–42S (2008).

    Article  Google Scholar 

  4. Shahani, S. Advanced Drug Delivery Systems: New Developments, New Technologies. Report No. PHM006F (Business Communications Company, 2006).

    Google Scholar 

  5. King, R. G. & Donohue, G. F. Estimates of medical device spending in the United States. AMSA <http://www.amsa.org/AMSA/libraries/committee_docs/king_paper_medical_device_spending.sflb.ashx> (2007).

  6. Shih, W. M., Quispe, J. D. & Joyce, G. F. A 1.7-kilobase single-stranded DNA that folds into a nanoscale octahedron. Nature 427, 618–621 (2004).

    ADS  CAS  Article  Google Scholar 

  7. Shin, H., Zygourakis, K., Farach-Carson, M. C., Yaszemski, M. J. & Mikos, A. G. Attachment, proliferation, and migration of marrow stromal osteoblasts cultured on biomimetic hydrogels modified with an osteopontin-derived peptide. Biomaterials 25, 895–906 (2004).

    Article  Google Scholar 

  8. Massia, S. P. & Hubbell, J. A. Covalently attached GRGD on polymer surfaces promotes biospecific adhesion of mammalian cells. Ann. NY Acad. Sci. 589, 261–270 (1990).

    ADS  CAS  Article  Google Scholar 

  9. Silva, G. A. et al. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 303, 1352–1355 (2004).

    ADS  CAS  Article  Google Scholar 

  10. Arnold, M. et al. Activation of integrin function by nanopatterned adhesive surfaces. ChemPhysChem 5, 383–388 (2004).

    CAS  Article  Google Scholar 

  11. Wosnick, J. H. & Shoichet, M. S. Three-dimensional chemical patterning of transparent hydrogels. Chem. Mater. 20, 55–60 (2008).

    CAS  Article  Google Scholar 

  12. Carrico, I. S. et al. Lithographic patterning of photoreactive cell-adhesive proteins. J. Am. Chem. Soc. 129, 4874–4875 (2007).

    CAS  Article  Google Scholar 

  13. Lutolf, M. P. et al. Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nature Biotechnol. 21, 513–518 (2003). This paper describes how materials can be designed to mimic key aspects of natural ECM (for example enzyme-mediated degradation) and function as templates for tissue regeneration.

    CAS  Article  Google Scholar 

  14. Shin, K., Jayasuriya, A. C. & Kohn, D. H. Effect of ionic activity products on the structure and composition of mineral self assembled on three-dimensional poly(lactide-co-glycolide) scaffolds. J. Biomed. Mater. Res. A 83, 1076–1086 (2007).

    Article  Google Scholar 

  15. Li, Y. J., Chung, E. H., Rodriguez, R. T., Firpo, M. T. & Healy, K. E. Hydrogels as artificial matrices for human embryonic stem cell self-renewal. J. Biomed. Mater. Res. A 79, 1–5 (2006).

    Article  Google Scholar 

  16. Benoit, D. S., Schwartz, M. P., Durney, A. R. & Anseth, K. S. Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nature Mater. 7, 816–823 (2008).

    ADS  CAS  Article  Google Scholar 

  17. Shin'oka, T. et al. Midterm clinical results of tissue-engineered vascular autografts seeded with autologous bone marrow cells. J. Thorac. Cardiovasc. Surg. 129, 1330–1338 (2005).

    Article  Google Scholar 

  18. Richardson, T. P., Peters, M. C., Ennett, A. B. & Mooney, D. J. Polymeric systems for dual growth factor delivery. Nature Biotechnol. 19, 1029–1034 (2001).

    CAS  Article  Google Scholar 

  19. Phillips, J. E., Burns, K. L., Le Doux, J. M., Guldberg, R. E. & Garcia, A. J. Engineering graded tissue interfaces. Proc. Natl Acad. Sci. USA 105, 12170–12175 (2008).

    ADS  CAS  Article  Google Scholar 

  20. Fan, V. H. et al. Tethered epidermal growth factor provides a survival advantage to mesenchymal stem cells. Stem Cells 25, 1241–1251 (2007).

    CAS  Article  Google Scholar 

  21. Tsapis, N., Bennett, D., Jackson, B., Weitz, D. A. & Edwards, D. A. Trojan particles: large porous carriers of nanoparticles for drug delivery. Proc. Natl Acad. Sci. USA 99, 12001–12005 (2002).

    ADS  CAS  Article  Google Scholar 

  22. Reddy, S. T. et al. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nature Biotechnol. 25, 1159–1164 (2007).

    CAS  Article  Google Scholar 

  23. Park, J. H. et al. Systematic surface engineering of magnetic nanoworms for in vivo tumor targeting. Small 5, 694–700 (2009).

    CAS  Article  Google Scholar 

  24. Silva, E. A., Kim, E. S., Kong, H. J. & Mooney, D. J. Material-based deployment enhances the efficacy of endothelial progenitor cells. Proc. Natl Acad. Sci. USA 105, 14347–14352 (2008).

    ADS  CAS  Article  Google Scholar 

  25. Ali, O. A., Huebsch, N., Cao, L., Dranoff, G. & Mooney, D. J. Infection-mimicking materials to program dendritic cells in situ . Nature Mater. 8, 151–158 (2009). This paper describes how biomaterials can be designed to regulate host biology at a distance by recruiting, locally programming and subsequently dispersing target cell populations to produce potent biological responses.

    ADS  CAS  Google Scholar 

  26. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677–689 (2006). This paper demonstrates the importance of physical properties of biomaterials in controlling cellular response.

    CAS  Article  Google Scholar 

  27. Tan, J. L. et al. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl Acad. Sci. USA 100, 1484–1489 (2003).

    ADS  CAS  Article  Google Scholar 

  28. Park, T. G. & Hoffman, A. S. Synthesis and characterization of pH- and or temperature-sensitive hydrogels. J. Appl. Polym. Sci. 46, 659–671 (1992).

    CAS  Article  Google Scholar 

  29. Podual, K., Doyle, F. J. & Peppas, N. A. Glucose-sensitivity of glucose oxidase-containing cationic copolymer hydrogels having poly(ethylene glycol) grafts. J. Control. Release 67, 9–17 (2000).

    CAS  Article  Google Scholar 

  30. Edelman, E. R., Brown, L., Taylor, J. & Langer, R. In vitro and in vivo kinetics of regulated drug release from polymer matrices by oscillating magnetic fields. J. Biomed. Mater. Res. 21, 339–353 (1987).

    CAS  Article  Google Scholar 

  31. Alsberg, E., Feinstein, E., Joy, M. P., Prentiss, M. & Ingber, D. E. Magnetically-guided self-assembly of fibrin matrices with ordered nano-scale structure for tissue engineering. Tissue Eng. 12, 3247–3256 (2006).

    CAS  Article  Google Scholar 

  32. Adams, D. S., Masi, A. & Levin, M. H+ pump-dependent changes in membrane voltage are an early mechanism necessary and sufficient to induce tail regeneration. Development 134, 1323–1335 (2007).

    CAS  Article  Google Scholar 

  33. Lahann, J. et al. A reversibly switching surface. Science 299, 371–374 (2003).

    ADS  CAS  Article  Google Scholar 

  34. Martinez, A. W., Phillips, S. T. & Whitesides, G. M. Three-dimensional microfluidic devices fabricated in layered paper and tape. Proc. Natl Acad. Sci. USA 105, 19606–19611 (2008).

    ADS  CAS  Article  Google Scholar 

  35. Khetani, S. R. & Bhatia, S. N. Microscale culture of human liver cells for drug development. Nature Biotechnol. 26, 120–126 (2008).

    CAS  Article  Google Scholar 

  36. Nagrath, S. et al. Isolation of rare circulating tumor cells in cancer patients by microchip technology. Nature 450, 1235–1239 (2007).

    ADS  CAS  Article  Google Scholar 

  37. Stern, E. et al. Label-free immunodetection with CMOS-compatible semiconducting nanowires. Nature 445, 519–522 (2007).

    ADS  CAS  Article  Google Scholar 

  38. Gupta, V. K., Dubrovsky, T. B. & Abbott, N. L. Optical amplification of ligand–receptor binding using liquid crystals. Science 279, 2077–2080 (1998).

    ADS  CAS  Article  Google Scholar 

  39. Madri, J. A., Pratt, B. M. & Tucker, A. M. Phenotypic modulation of endothelial cells by transforming growth factor-β depends upon the composition and organization of the extracellular matrix. J. Cell Biol. 106, 1375–1384 (1988).

    CAS  Article  Google Scholar 

  40. Fischbach, C. et al. Cancer cell angiogenic capability is regulated by 3D culture and integrin engagement. Proc. Natl Acad. Sci. USA 106, 399–404 (2009).

    ADS  CAS  Article  Google Scholar 

  41. Ghajar, C. M. et al. The effect of matrix density on the regulation of 3-D capillary morphogenesis. Biophys. J. 94, 1930–1941 (2008).

    ADS  CAS  Article  Google Scholar 

  42. Xu, M. et al. Encapsulated three-dimensional culture supports the development of nonhuman primate secondary follicles. Biol. Reprod. 81, 587–593 (2009).

    CAS  Article  Google Scholar 

  43. Khademhosseini, A., Langer, R., Borenstein, J. & Vacanti, J. P. Microscale technologies for tissue engineering and biology. Proc. Natl Acad. Sci. USA 103, 2480–2487 (2006).

    ADS  CAS  Article  Google Scholar 

  44. Lee, H., Scherer, N. F. & Messersmith, P. B. A reversible wet/dry adhesive inspired by mussels and geckos. Nature 448, 338–341 (2007).

    ADS  CAS  Article  Google Scholar 

  45. Jeong, K. H., Kim, J. & Lee, L. P. Biologically inspired artificial compound eyes. Science 312, 557–561 (2006).

    ADS  CAS  Article  Google Scholar 

  46. Nam, K. T. et al. Virus-enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science 312, 885–888 (2006). This paper discusses the engineering of non-medical materials through the templating of viruses. The precisely tuned patterns of spatial features of the natural organism promise distinct performance advantages.

    ADS  CAS  Article  Google Scholar 

  47. Needleman, D. J. et al. Higher-order assembly of microtubules by counterions: from hexagonal bundles to living necklaces. Proc. Natl Acad. Sci. USA 101, 16099–16103 (2004).

    ADS  CAS  Article  Google Scholar 

  48. Sidorenko, A., Krupenkin, T., Taylor, A., Fratzl, P. & Aizenberg, J. Reversible switching of hydrogel-actuated nanostructures into complex micropatterns. Science 315, 487–490 (2007).

    ADS  CAS  Article  Google Scholar 

  49. Omabegho, T., Sha, R. & Seeman, N. C. A bipedal DNA Brownian motor with coordinated legs. Science 324, 67–71 (2009).

    ADS  CAS  Article  Google Scholar 

  50. Kyriakides, T. R. et al. The CC chemokine ligand, CCL2/MCP1, participates in macrophage fusion and foreign body giant cell formation. Am. J. Pathol. 165, 2157–2166 (2004).

    CAS  Article  Google Scholar 

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Acknowledgements

We thank D. Ingber for discussions. We acknowledge funding from the US National Institutes of Health (National Institute of Dental and Craniofacial Research). N.H. is supported by a National Science Foundation Graduate Research Fellowship.

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Reprints and permissions information is available at http://www.nature.com/reprints. The authors declare no competing financial interests. Correspondence should be addressed to D.J.M. (mooneyd@seas.harvard.edu).

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Huebsch, N., Mooney, D. Inspiration and application in the evolution of biomaterials. Nature 462, 426–432 (2009). https://doi.org/10.1038/nature08601

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