Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-24T14:22:51.308Z Has data issue: false hasContentIssue false
  • English
  • Français

Silk apatite composites from electrospun fibers

Published online by Cambridge University Press:  01 December 2005

Chunmei Li ,
Hyoung-Joon Jin ,
Gregory D. Botsaris  and
David L. Kaplan
Chunmei Li
Affiliation:
Tufts University, Departments of Biomedical Engineering, Chemical and Biological Engineering, and Bioengineering Center, Medford, Massachusetts 02155
Hyoung-Joon Jin
Affiliation:
Tufts University, Departments of Biomedical Engineering, Chemical and Biological Engineering, and Bioengineering Center, Medford, Massachusetts 02155; and Inha University, Department of Polymer Science and Engineering, Incheon 402-751, South Korea
Gregory D. Botsaris
Affiliation:
Tufts University, Departments of Biomedical Engineering, Chemical and Biological Engineering, and Bioengineering Center, Medford, Massachusetts 02155
David L. Kaplan*
Affiliation:
Tufts University, Departments of Biomedical Engineering, Chemical and Biological Engineering, and Bioengineering Center, Medford, Massachusetts 02155
*
a)Address all correspondence to this author.e-mail: [email protected]
Get access

Abstract

Human bone is a three-dimensional composite structure consisting of inorganic apatite crystals and organic collagen fibers. An attractive strategy for fabricating mimics of these types of composite biomaterials is to selectively grow apatite on polymers with control of structure, mechanical properties, and function. In the present study, silk/apatite composites were prepared by growing apatite on functionalized nanodiameter silk fibroin fibers prepared by electrospinning. The functionalized fibers were spun from an aqueous solution of silk/polyethylene oxide (PEO) (78/22 wt/wt) containing poly(L-aspartate) (poly-Asp), which was introduced as an analogue of noncollageous proteins normally found in bone. Silk fibroin associated with the acidic poly-Asp and acted as template for mineralization. Apatite mineral growth occurred preferentially along the longitudinal direction of the fibers, a feature that was not present in the absence of the combination of components at appropriate concentrations. Energy dispersive spectroscopy and x-ray diffraction confirmed that the mineral deposits were apatite. The results suggest that this approach can be used to form structures with potential utility for bone-related biomaterials based on the ability to control the interface wherein nucleation and crystal growth occur on the silk fibroin. With this level of inorganic–organic control, coupled with the unique mechanical properties, slow rates of biodegradation, and polymorphic features of this type of proteins, new opportunities emerge for utility of biomaterials.

Keywords

BiomimeticCompositeNanofiber
Type
Articles
Information
Journal of Materials Research , Volume 20 , Issue 12 , December 2005 , pp. 3374 - 3384
Copyright
Copyright © Materials Research Society 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1.Li, C. and Kaplan, D.L.: Biomimetic composites via molecular scale self-assembly and biomineralization. Curr. Opin. Solid State Mater. Sci. 7, 265 (2003).CrossRefGoogle Scholar
2.Sato, K., Kumagai, Y. and Tanaka, J.: Apatite formation on organic monolayers in simulated body environment. J. Biomed. Mater. Res. 50, 16 (2000).3.0.CO;2-G>CrossRefGoogle ScholarPubMed
3.Tanahashi, M. and Matsuda, T.: Surface functional group dependence on apatite formation on self-assembled monolayers in a simulated body fluid. J. Biomed. Mater. Res. 34, 305 (1997).3.0.CO;2-O>CrossRefGoogle Scholar
4.Kamei, S., Tomita, N., Tamai, S., Kato, K. and Ikada, Y.: Histologic and mechanical evaluation for bone bonding of polymer surfaces grafted with a phosphate-containing polymer. J. Biomed. Mater. Res. 37, 384 (1997).3.0.CO;2-H>CrossRefGoogle ScholarPubMed
5.Kato, K., Eika, Y. and Ikada, Y.: Deposition of a hydroxyapatite thin layer onto a polymer surface carrying grafted phosphate polymer chains. J. Biomed. Mater. Res. 32, 687 (1996).3.0.CO;2-9>CrossRefGoogle ScholarPubMed
6.Tretinnikov, O., Kato, K. and Ikada, Y.: In vitro hydroxyapatite deposition onto a film surface-grafted with organophosphate polymer. J. Biomed. Mater. Res. 28, 1365 (1994).CrossRefGoogle Scholar
7.Taguchi, T., Muraoka, Y., Matsuyama, H., Kishida, A. and Akashi, M.: Apatite coating on hydrophilic polymer-grafted poly(ethylene) films using an alternate soaking process. Biomaterials 22, 53 (2001).CrossRefGoogle ScholarPubMed
8.Tanahashi, M., Yao, T., Kokubo, T., Minoda, M., Miyamoto, T., Nakamura, T. and Yamamuro, T.: Apatite coated on organic polymers by biomimetic process: Improvement in its adhesion to substrate by glow-discharge treatment. J. Biomed. Mater. Res. 29, 349 (1995).CrossRefGoogle ScholarPubMed
9.Tanahashi, M., Yao, T., Kokubo, T., Minoda, M., Miyamoto, T., Nakamura, T. and Yamamuro, T.: Apatite coated on organic polymers by biomimetic process: Improvement in its adhesion to substrated by naoh treatment. J. Appl. Biomater. 5, 339 (1994).CrossRefGoogle ScholarPubMed
10.Kawai, T., Ohtsuki, C., Kamitakahara, M., Miyazaki, T., Tanihara, M., Sakaguchi, Y. and Konagaya, S.: Coating of an apatite layer on polyamide films containing sulfonic groups by a biomimetic process. Biomaterials 25, 4529 (2004).CrossRefGoogle ScholarPubMed
11.Wan, A.C.A., Khor, E. and Hastings, G.W.: Preparation of a chitin– apatite composite by in situ precipitation onto porous chitin scaffolds. J. Biomed. Mater. Res. 41, 541 (1998).3.0.CO;2-C>CrossRefGoogle ScholarPubMed
12.Kawashita, M., Nakao, M., Minoda, M., Kim, H-M., Beppu, T., Miyamoto, T., Kokubo, T. and Nakamura, T.: Apatite-forming ability of carboxyl group-containing polymer gels in a simulated body fluid. Biomaterials 24, 2477 (2003).CrossRefGoogle Scholar
13.Bigi, A., Boanini, E., Panzavolta, S., Roveri, N. and Rubini, K.: Bonelike apatite growth on hydroxyapatite-gelatin sponges from simulated body fluid. J. Biomed. Mater. Res. 59, 709 (2002).CrossRefGoogle ScholarPubMed
14.Zhang, R. and Ma, P.X.: Porous poly(l-lactic acid)/apatite composites created by biomimetic process. J. Biomed. Mater. Res. 45, 285 (1999).3.0.CO;2-2>CrossRefGoogle ScholarPubMed
15.Murphy, W.L., Kohn, D.H. and Mooney, D.J.: Growth of continuous bonelike mineral within porous poly(lactide-co-glycolide) scaffolds in vitro. J. Biomed. Mater. Res. 50, 50 (2000).3.0.CO;2-F>CrossRefGoogle ScholarPubMed
16.Oyane, A., Kawashita, M., Nakanishi, K., Kokubo, T., Minoda, M., Miyamoto, T. and Nakamura, T.: Bonelike apatite formation on ethylene-vinyl alcohol copolymer modified with silane coupling agent and calcium silicate solutions. Biomaterials 24, 1729 (2003).CrossRefGoogle ScholarPubMed
17.Altman, G.H., Diaz, F., Jakuba, C., Calabro, T., Horan, R.L., Chen, J., Lu, H., Richmond, J. and Kaplan, D.L.: Silk-based biomaterials. Biomaterials 24, 401 (2003).CrossRefGoogle ScholarPubMed
18.Panilaitis, B., Altman, G.H., Chen, J., Jin, H-J., Karageorgiou, V. and Kaplan, D.L.: Macrophage responses to silk. Biomaterials 24, 3079 (2003).CrossRefGoogle ScholarPubMed
19.Altman, G.H., Horan, R.L., Lu, H.H., Moreau, J., Martin, I., Richmond, J.C. and Kaplan, D.L.: Silk matrix for tissue engineered anterior cruciate ligaments. Biomaterials 23, 4131 (2002).CrossRefGoogle ScholarPubMed
20.Chen, J., Altman, G.H., Karageorgiou, V., Horan, R.L., Collette, A., Volloch, V., Calabro, T. and Kaplan, D.L.: Human bone marrow stromal cell and ligment fibroblast responses on rgd-modified silk fibers. J. Biomed. Mater. Res. 67A, 559 (2003).CrossRefGoogle Scholar
21.Yoshimoto, H., Shin, Y.M., Terai, H. and Vacanti, J.P.: A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering. Biomaterials 24, 2077 (2003).CrossRefGoogle ScholarPubMed
22.Matthews, J.A., Wnek, G.E., Simpson, D.G. and Bowlin, G.L.: Electrospinning of collagen nanofibers. Biomacromolecules 3, 232 (2002).CrossRefGoogle ScholarPubMed
23.Jin, H-J., Chen, J., Karageorgiou, V., Altman, G.H. and Kaplan, D.L.: Human bone marrow stromal cell responses on electrospun silk fibroin mats. Biomaterials 25, 1039 (2004).CrossRefGoogle ScholarPubMed
24.Kenawy, E-R., Bowlin, G.L., Mansfield, K., Layman, J., Simpson, D.G., Sanders, E.H. and Wnek, G.E.: Release of tetracycline hydrochloride from electrospun poly(ethylene-co-vinylacetate), poly(lactic acid), and a blend. J. Controlled Release 81, 57 (2002).CrossRefGoogle Scholar
25.Stitzel, J.D., Pawlowski, K., Wnek, G.E., Simpson, D.G. and Bowlin, G.L.: Arterial smooth muscle cell proliferation on a novel biomimicking vascular graft scaffolds. J. Biomater. Appl. 16, 22 (2001).CrossRefGoogle Scholar
26.Huang, L., Mcmillan, A., Apkarian, R.P., Pourdeyhimi, B., Conticello, V.P. and Chaikof, E.L.: Generation of synthetic elastin-mimetic small diameter fibers and fiber networks. Macromolecules 33, 2989 (2000).CrossRefGoogle Scholar
27.Anderson, J.P., Nilsson, S.C., Rajachar, R.M., Logan, R., Weissman, N.A. and Martin, D.C.: Bioactive genetically engineered protein polymer films on silicon devices, in Biomolecular Materials by Design, edited by Alper, M., Bayley, M., Kaplan, D., and Navis, M. (Mater. Res. Soc. Symp. Proc. 330, Pittsburgh, PA, 1994), p. 171.Google Scholar
28.Buchko, C.J., Chen, L.C., Shen, Y. and Martin, D.C.: Processing and microstructural characterization of porous biocompatible protein polymer thin films. Polymer 40, 7397 (1999).CrossRefGoogle Scholar
29.Buchko, C.J., Kozloff, K.M. and Martin, D.C.: Surface characterization of porous, biocompatible protein polymer thin films. Biomaterials 22, 1289 (2001).CrossRefGoogle ScholarPubMed
30.Jin, H-J., Fridrikh, S.V., Rutledge, G.C. and Kaplan, D.L.: Electrospinning bombyx mori silk with poly(ethylene oxide). Biomacromolecules 3, 1233 (2002).CrossRefGoogle ScholarPubMed
31.Huang, L., Apkarian, R.P. and Chaikof, E.L.: High-resolution analysis of engineered type i collagen nanofibers by electron microscopy. Scanning 23, 372 (2001).CrossRefGoogle ScholarPubMed
32.Huang, L., Nagapudi, K., Apkarian, R.P. and Chaikof, E.L.: Engineered collagen-PEO nanofibers and fabrics. J. Biomater. Sci. Polym. Ed. 12, 979 (2001).CrossRefGoogle ScholarPubMed
33.Zarkoob, S., Reneker, D.H., Eby, R.K., Hudson, S.D., Ertley, D. and Adams, W.W.: Structure and morphology of nano electrospun silk fibers. Polymer Preprints (Am. Chem. Soc., Division of Polymer Chemistry). 39, 244, (1998).Google Scholar
34.Bini, E., Knight, D.P. and Kaplan, D.L.: Mapping domain structures in silks from insects and spiders related to protein assembly. J. Mol. Biol. 335, 27 (2004).CrossRefGoogle ScholarPubMed
35.Jin, H-J. and Kaplan, D.L.: Mechanism of silk processing in insects and spiders. Nature 424, 1057 (2003).CrossRefGoogle ScholarPubMed
36.Furuzono, T., Taguchi, T., Kishida, A., Akashi, M. and Tamada, Y.: Preparation and characterization of apatite deposited on silk fabric using an alternate soaking process. J. Biomed. Mater. Res. 50, 344 (2000).3.0.CO;2-D>CrossRefGoogle ScholarPubMed
37.Chen, X., Knight, D.P., Shao, Z. and Vollrath, F.: Regenerated bombyx silk solutions studied with rheometry and FTIR. Polymer 42, 09969 (2001).CrossRefGoogle Scholar
38.Tretinnikov, O.N. and Tamada, Y.: Influence of casting temperature on the near-surface structure and wettability of cast silk fibroin films. Langmuir 17, 7406 (2001).CrossRefGoogle Scholar
39.Um, I.C., Kweon, H., Park, Y.H. and Hudson, S.: Structural characteristics and properties of the regenerated silk fibroin prepared from formic acid. Int. J. Biol. Macromol. 29, 91 (2001).CrossRefGoogle ScholarPubMed
40.Dersch, R., Liu, T., Schaper, A.K., Greiner, A. and Wendorff, J.H.: Electrospun nanofibers: Internal structure and intrinsic orientation. J. Polym. Sci., Part A: Polym. Chem. 41, 545 (2003).CrossRefGoogle Scholar
41.Chen, X., Shao, Z., Marinkovic, N.S., Miller, L.M., Zhou, P. and Chance, M.R.: Conformation transition kinetics of regenerated bombyx mori silk fibroin membrane monitored by time-resolved FTIR spectroscopy. Biophys. Chem. 89, 25 (2001).CrossRefGoogle ScholarPubMed
42.Li, M., Tao, W., Kuga, S. and Nishiyama, Y.: Controlling molecular conformation of regenerated wild silk fibroin by aqueous ethanol treatment. Polym. Adv. Technol. 14, 694 (2003).CrossRefGoogle Scholar
43.Chen, Z., Foster, M.D., Zhou, W., Fong, H. and Reneker, D.H.: Structure of poly(ferrocenyldimethylsilane) in electrospun nanofibers. Macromolecules 34, 6156 (2001).CrossRefGoogle Scholar
44.Jaeger, R., Schönherr, H. and Vancso, G.J.: Chain packing in electrospun poly(ethylene oxide) visualized by atomic force microscopy. Macromolecules 29, 7634 (1996).CrossRefGoogle Scholar
45.Sasaki, N. and Sudoh, Y.: X-ray pole figure analysis of apatite crystals and collagen molecules in bone. Calcif. Tissue Int. 60, 361 (1997).CrossRefGoogle ScholarPubMed
46.Weiner, S. and Traub, W.: Organization of hydroxyapatite crystals within collagen fibrils. FEBS Lett. 206, 262 (1986).CrossRefGoogle ScholarPubMed
47.Kikuchi, M., Itoh, S., Ichinose, S., Shinomiya, K. and Tanaka, J.: Self-organization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vitro and its biological reaction in vivo. Biomaterials 22, 1705 (2001).CrossRefGoogle Scholar
48.Rhee, S-H., Suetsugu, Y. and Tanaka, J.: Biomimetic configurational arrays of hydroxyapatite nanocrystals on bio-organics. Biomaterials 22, 2843 (2001).CrossRefGoogle ScholarPubMed
49.Roveri, N., Falini, G., Sidoti, M.C., Tampieri, A., Landi, E., Sandri, M. and Parma, B.: Biologically inspired growth of hydroxyapatite nanocrystals inside self-assembled collagen fibers. Mater. Sci. Eng. C 23, 441 (2003).CrossRefGoogle Scholar
50.Takeuchi, A., Ohtsuki, C., Miyazaki, T., Tanaka, H., Yamazaki, M. and Tanihara, M.: Deposition of bone-like apatite on silk fiber in a solution that mimics extracellular fluid. J. Biomed. Mater. Res. 65A, 283 (2003).CrossRefGoogle Scholar
51.Gao, H., Ji, B., Jager, I.L., Arzt, E. and Fratzl, P.: Materials become insensitive to flaws at nanoscale: Lessons from nature. Proc. Natl. Acad. Sci. USA 100, 5597 (2003).CrossRefGoogle ScholarPubMed
52.Jager, I. and Fratzl, P.: Mineralized collagen fibrils: A mechanical model with a staggered arrangement of mineral particles. Biophys. J. 79, 1737 (2000).CrossRefGoogle ScholarPubMed
53.Li, C.: Silk polymer templates in biomineralization. Ph.D. Thesis, Tufts University, Medford, MA (2005), p. 259.Google Scholar
54.Li, D., Wang, Y. and Xia, Y.: Electrospinning nanofibers as uniaxially aligned arrays and layer-by-layer stacked films. Adv. Mater. 16, 361 (2004).CrossRefGoogle Scholar
55.Kim, H-M., Kim, Y., Park, S-J., Rey, C., Lee, H., Glimcher, M.J. and Ko, J. Seung: Thin film of low-crystalline calcium phosphate apatite formed at low temperature. Biomaterials 21, 1129 (2000).CrossRefGoogle ScholarPubMed
56.Frayssinet, P., Trouillet, J.L., Rouquet, N., Azimus, E. and Autefage, A.: Osseointegration of macroporous calcium phosphate ceramics having a different chemical composition. Biomaterials 14, 423 (1993).CrossRefGoogle ScholarPubMed
57.Jin, H-J., Park, J., Valluzzi, R., Cebe, P. and Kaplan, D.L.: Biomaterial films of bombyx mori silk fibroin with poly(ethylene oxide). Biomacromolecules 5, 711 (2004).CrossRefGoogle ScholarPubMed
58.Nazarov, R., Jin, H-J. and Kaplan, D.L.: Porous 3-D scaffolds from regenerated silk fibroin. Biomacromolecules 5, 718 (2004).CrossRefGoogle ScholarPubMed
59.Kim, U-J., Park, J., Kim, H. Joo, Wada, M. and Kaplan, D.L.: Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin. Biomaterials 26, 2775 (2005).CrossRefGoogle ScholarPubMed