Gelation of <i>Antheraea pernyi</i> Silk Fibroin Accelerated by Shearing — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Gelation of <i>Antheraea pernyi</i> Silk Fibroin Accelerated by Shearing
National Engineering Laboratory for Modern Silk, College of Textile and Clothing Engineering, Soochow University, Suzhou, China
,
National Engineering Laboratory for Modern Silk, College of Textile and Clothing Engineering, Soochow University, Suzhou, China; Suzhou Institute of Scientific & Technical Information, Suzhou, China
,
National Engineering Laboratory for Modern Silk, College of Textile and Clothing Engineering, Soochow University, Suzhou, China
,
National Engineering Laboratory for Modern Silk, College of Textile and Clothing Engineering, Soochow University, Suzhou, China
1 National Engineering Laboratory for Modern Silk, College of Textile and Clothing Engineering, Soochow University, Suzhou, China
2 National Engineering Laboratory for Modern Silk, College of Textile and Clothing Engineering, Soochow University, Suzhou, China; Suzhou Institute of Scientific & Technical Information, Suzhou, China
3 National Engineering Laboratory for Modern Silk, College of Textile and Clothing Engineering, Soochow University, Suzhou, China
4 National Engineering Laboratory for Modern Silk, College of Textile and Clothing Engineering, Soochow University, Suzhou, China
The rapid manufacture of silk fibroin gels in mild conditions is an important subject in the field of silk-based biomate rials. In this study, the gelation of Antheraea pernyi silk fibroin (ASF) aqueous solution was induced by shearing, without chemical cross-linking agents. Simple shearing controlled and accomplished the steady and rapid conforma tional transition to β -sheets with ease. The conformational transformation and rapid gelation mechanisms of ASF induced by shearing were tracked and analyzed by circular dichroism spectrometry, Fourier transform infrared spectroscopy and X-ray diffractometry, then compared with Bombyx mori silk fibroin (BSF). ASF quickly formed hydrogels within 24 - 48 h after shearing under different shearing rates for 30 - 90 min, resulting in sol-gel transformation when the β -sheet content reached nearly 50%, which is the minimum content needed to maintain a stable hydrogel system in ASF . The gel structures remained stable once formed. The rapid gelation of ASF through shearing compared with BSF was achieved because of ASF’s alternating polyalanine-containing units, which tend to form α -helix structures sponta neously. Further, the entropic cost during the conformational transition from the α -helix to the β -sheet structure is less than the cost of the transition from the random coil structure. This method is a simple, non-chemical cross-linking ap proach for the promotion of rapid gelation and the protection of the biological properties of ASF, and it may prove use ful for application in the field of biomedical materials.
G. R. Plaza, P. Corsini, E. Marsano, J. Perez-Rigueiro, M. Elices, C. Riekel, C. Vendrely and G. V. Guinea, “Correlation between Processing Conditions, Microstructure and Mechanical Behavior in Regenerated Silkworm Silk Fibers,” Journal of Polymer Science Part B: Polymer Physics, Vol. 50, No. 7, 2012, pp. 455-465. doi:10.1002/polb.23025
A. S. Lammel, X. Hu, S. H. Park, D. L. Kaplan and T. R. Scheibel, “Controlling Silk Fibroin Particle Features for Drug Delivery,” Biomaterials, Vol. 31, No. 16, 2010, pp. 4583-4591. doi:10.1016/j.biomaterials.2010.02.024
M. Z. Li, M. Ogiso and N. Minoura, “Enzymatic Degradation Behavior of Porous Silk Fibroin Sheets,” Biomaterials, Vol. 24, No. 2, 2003, pp. 357-365.
R. E. Unger, S. Ghanaati, C. Orth, A. Sartoris, M. Barbeck, S. Halstenberg, A. Motta, C. Migliaresi and C. J. Kirkpatrick, “The Rapid Anastomosis between Prevascularized Networks on Silk Fibroin Scaffolds Generated in Vitro with Cocultures of Human Microvascular Endothelial and Osteoblast Cells and the Host Vasculature,” Biomaterials, Vol. 31, No. 27, 2010, pp. 6959-6967. doi:10.1016/j.biomaterials.2010.05.057
R. Okabayashi, M. Nakamura, T. Okabayashi, Y. Tanaka, A. Nagai and K. Yamashita, “Efficacy of Polarized Hydroxyapatite and Silk Fibroin Composite Dressing Gel on Epidermal Recovery from Full-Thickness Skin Wounds,” Journal of Biomedical Materials Research Part B: Applied Biomaterials, Vol. 90B, No. 2, 2009, pp. 641-646.
B. B. Mandal and S. C. Kundu, “Cell Proliferation and Migration in Silk Fibroin 3D Scaffolds,” Biomaterials, Vol. 30, No. 15, 2009, pp. 2956-2965. doi:10.1016/j.biomaterials.2009.02.006
S. Sahoo, S. L. Tohb and J. C. H. Goha, “A bFGF-Releasing Silk/PLGA-Based Biohybrid Scaffold for Ligament/Tendon Tissue Engineering Using Mesenchymal Progenitor Cells,” Biomaterials, Vol. 31, No. 11, 2010, pp. 2990-2998. doi:10.1016/j.biomaterials.2010.01.004
S. Madduri, M. Papaloizos and B. Gander, “Trophically and Topographically Functionalized Silk Fibroin Nerve Conduits for Guided Peripheral Nerve Regeneration,” Biomaterials, Vol. 31, No. 8, 2010, pp. 2323-2334. doi:10.1016/j.biomaterials.2009.11.073
P. W. Madden, J. N. X. Lai, K. A. George, T. Giovenco, D. G. Harkin and T. V. Chirila, “Human Corneal Endothelial Cell Growth on a Silk Fibroin Membrane,” Biomaterials, Vol. 32, No. 17, 2011, pp. 4076-4084. doi:10.1016/j.biomaterials.2010.12.034
E. Wenk, H. P. Merkle, L. Meinel, “Silk Fibroin as a Vehicle for Drug Delivery Applications,” Journal of Controlled Release, Vol. 150, No. 2, 2011, pp. 128-141. doi:10.1016/j.jconrel.2010.11.007
E. Ruoslahti and M. D. Pierschbacher, “New Perspectives in Cell Adhesion: RGD and Integrins,” Science, Vol. 238, No. 4826, 1987, pp. 491-497. doi:10.1126/science.2821619
A. J. Meinel, K. E. Kubow, E. Klotzsch, M. GarciaFuentes, M. L. Smith, V. Vogel, H. P. Merkle and L. Meinel, “Optimization Strategies for Electrospun Silk Fibroin Tissue Engineering Scaffolds,” Biomaterials, Vol. 30, No. 17, 2009, pp. 3058-3067. doi:10.1016/j.biomaterials.2009.01.054
C. Acharya, S. K. Ghosh and S. C. Kundu, “Silk Fibroin Film from Non-Mulberry Tropical Tasar Silkworms: A Novel Substrate for in Vitro Fibroblast Culture,” Acta Biomaterialia, Vol. 5, No. 1, 2009, pp. 429-437. doi:10.1016/j.actbio.2008.07.003
Y. Z. Wang, 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, Vol. 29, No.24-25, 2008, pp. 3415-3428. doi:0.1016/j.biomaterials.2008.05.002
M. Z. Li, W. Tao, S. Z. Lu and C. X. Zhao, “Porous 3-D Scaffolds from Regenerated Antheraea pernyi Silk Fibroin,” Polymers for Advanced Technologies, Vol. 19, No. 3, 2008, pp. 207-212. doi:10.1002/pat.998
C. Patra, S. Talukdar, T. Novoyatleva, S. R. Velagala, C. Mühlfeld, B. Kundu, S. C. Kundu and F. B. Engel, “Silk Protein Fibroin from Antheraea mylitta for Cardiac Tissue Engineering,” Biomaterials, Vol. 33, No. 9, 2012, pp. 2673-2680. doi:10.1016/j.biomaterials.2011.12.036
E. S. Gil, R. J. Spontak and S. M. Hudson, “Effect of βSheet Crystals on the Thermal and Rheological Behavior of Protein-Based Hydrogels Derived from Gelatin and Silk Fibroin,” Macromolecular Bioscience, Vol.5, No. 8, 2005, pp. 702-709. doi:10.1002/mabi.200500076
M. N. Collins and C. Birkinshaw, “Morphology of Crosslinked Hyaluronic Acid Porous Hydrogels,” Journal of Applied Polymer Science, Vol. 120, No. 2, 2011, pp. 1040-1049. doi:10.1002/app.33241
M. L. Floren, S. Spilimbergo, A. Motta and C. Migliaresi, “Carbon Dioxide Induced Silk Protein Gelation for Biomedical Applications,” Biomacromolecules, Vol. 13, No. 7, 2012, pp. 2060-2072. doi:10.1021/bm300450a
N. Guziewicz, A. Best, B. Perez-Ramirez and D. L. Kaplan, “Lyophilized Silk Fibroin Hydrogels for the Sustained Local Delivery of Therapeutic Monoclonal Antibodies,” Biomaterials, Vol. 32, No. 10, 2011, pp. 2642-2650.
N. Bhattarai, J. Gunn and M. Zhang, “Chitosan-Based Hydrogels for Controlled, Localized Drug Delivery,” Advanced Drug Delivery Reviews, Vol. 62, No. 1, 2010, pp. 83-99. doi:10.1016/j.addr.2009.07.019
X. Hu, Q. Lu, L. Sun, P. Cebe, X. Q. Wang, X. H. Zhang and D. L. Kaplan, “Biomaterials from UltrasonicationInduced Silk Fibroin-Hyaluronic Acid Hydrogels,” Biomacromolecules, Vol. 11, No. 11, 2010, pp. 3178-3188. doi:10.1021/bm1010504
T. Yucel, P. Cebel and D. L. Kaplan, “Vortex-Induced Injectable Silk Fibroin Hydrogels,” Biophysical Journal, Vol. 97, No. 7, 2009, pp. 2044-2050. doi:10.1016/j.bpj.2009.07.028
A. Matsumoto, J. Chen, A. L. Collette, U. J. Kim, G. H. Altman, P. Cebe and D. L. Kaplan, “Mechanisms of Silk Fibroin Sol-Gel Transitions,” The Journal of Physical Chemistry B, Vol. 110, No. 43, 2006, pp. 21630-21638. doi:10.1021/jp056350v
U. J. Kim, J. Park, C. M. Li, H. J. Jin, R. Valluzzi and D. L. Kaplan, “Structure and Properties of Silk Hydrogels,” Biomacromolecules, Vol. 5, No. 3, 2004, pp. 786-792. doi:10.1021/bm0345460
X. Q. Wang, J. A. Kluge, G. G. Leisk and D. L. Kaplan, “Sonication-Induced Gelation of Silk fibroin for Cell Encapsulation,” Biomaterials, Vol. 29, No. 8, 2008, pp. 10541064. doi:10.1016/j.biomaterials.2007.11.003
K. Numata, T. Katashima and T. Sakai, “State of Water, Molecular Structure, and Cytotoxicity of Silk Hydrogels,” Biomacromolecules, Vol. 12, No. 6, 2011, pp. 2137-2144.
E. S. Gil, D. J. Frankowski, R. J. Spontak and S. M. Hudson, “Swelling Behavior and Morphological Evolution of Mixed Gelatin/Silk Fibroin Hydrogels,” Biomacromolecules, Vol. 6, No. 6, 2005, pp. 3079-3087. doi:10.1021/bm050396c
M. Fini, A. Mott, P. Torricelli, G. Giavaresi, A. N. Nicoli, M. Tschon, R. Giardino and C. Migliaresi, “The Healing of Confined Critical Size Cancellous Defects in the Presence of Silk Fibroin Hydrogel,” Biomaterials, Vol. 26, No. 17, 2005, pp. 3527-3536. doi:10.1016/j.biomaterials.2004.09.040
X. G. Li, L.Y. Wu, M. R. Huang, H. L. Shao and X. C. Hu, “Conformational Transition and Liquid Crystalline State of Regenerated Silk Fibroin in Water,” Biopolymers, Vol. 89, No. 6, 2008, pp. 497-505. doi:10.1002/bip.20905
S. Q. Yan, C. X. Zhao, X. F. Wu, Q. Zhang and M. Z. Li, “Gelation Behavior of Antheraea pernyi Silk Fibroin,” Science China Chemistry, Vol. 53, No. 3, 2010, pp. 535-541. doi:10.1007/s11426-010-0093-0
S. Brahms, “Determination of Protein Secondary Structure in Solution by Vacuum Ultraviolet Circular Dichroism,” Journal of Molecular Biology, Vol. 138, No. 2, 1980, pp. 149-178. doi:10.1016/0022-2836(80)90282-X
N. J. Greenfield, “Using Circular Dichroism Spectra to Estimate Protein Secondary Structure,” Nature Protocols, Vol. 1, 2007, pp. 2876-2890. doi:10.1038/nprot.2006.202
W. Tao, M. Z. Li and C. X. Zhao, “Structure and Properties of Regenerated Antheraea pernyi Silk Fibroin in Aqueous Solution,” International Journal of Biological Macromolecules, Vol. 40, No. 5, 2007, pp. 472-478. doi:10.1016/j.ijbiomac.2006.11.006
J. X. He, Y. M. Cheng and S. Z. Cui, “Preparation and Characterization of Electrospun Antheraea pernyi Silk Fibroin Nanofibers from Aqueous Solution,” Journal of Applied Polymer Science, Vol. 128, No. 2, 2013, pp. 1081-1088. doi:10.1002/app.38233
K. H. Zhang, Q. Z. Yu and X. M. Mo, “Fabrication and Intermolecular Interactions of Silk Fibroin/Hydroxybutyl Chitosan Blended Nanofibers,” International Journal of Molecular Sciences, Vol. 12, 2011, No. 4, pp. 2187-2199. doi:10.3390/ijms12042187
B. B. Mandal, S. Kapoor and S. C. Kundu, “Silk Fibroin/Polyacrylamide Semi-Interpenetrating Network Hydrogels for Controlled Drug Release,” Biomaterials, Vol. 30, No. 14, 2009, pp. 2826-2836. doi:10.1016/j.biomaterials.2009.01.040
S. W. Ha, A. E. Tonelli and S. M. Hudson, “Structural Studies of Bombyx mori Silk Fibroin during Regeneration from Solutions and Wet Fiber Spinning,” Biomacromolecules, Vol. 6, No. 3, 2005, pp. 1722-1731. doi:10.1021/bm050010y
F. U. Hart and M. Hayer-Hart, “Converging Concepts of Protein Folding in Vitro and in Vivo,” Nature Structural & Molecular Biology, Vol. 16, No. 6, 2009, pp. 574-581. doi:10.1038/nsmb.1591
J. R. Macdonald and J. R. Johnson, “Environmental Features are Important in Determining Protein Secondary Structure,” Protein Science, Vol. 10, No. 6, 2001, pp. 1172-1177. doi:10.1110/ps.420101
C. Vepari and D. L. Kaplan, “Silk as a Biomaterial,” Progress in Polymer Science, Vol. 32, No. 8-9, 2007, pp. 991-1007. doi:10.1016/j.progpolymsci.2007.05.013
J. G. Hardy and T. R. Scheibel, “Silk-Inspired Polymers and Proteins,” Biochemical Society Transactions, Vol. 37, No. 4, 2009, pp. 677-681. doi:10.1042/BST0370677
M. Blaber, X. J. Zhang and B. W. Matthews, “Structural Basis of amino Acid Alpha Helix Propensity,” Science, Vol. 260, No. 5114, 1993, pp. 1637-1640. doi:10.1126/science.8503008
S. M. LaPointe, S. Farrag, H. J. Bohorquez and R. J. Boyd, “QTAIM Study of an α-Helix Hydrogen Bond Network,” The Journal of Physical Chemistry B, Vol. 113, No. 31, 2009, pp. 10957-10964. doi:10.1021/jp903635h
Y. Nakazawa and T. Asakura, “Heterogeneous Exchange Behavior of Samia Cynthia Ricini Silk Fibroin during Helix-Coil Transition Studied with 13C NMR,” FEBS Letters, Vol. 529, No. 2-3, 2002, pp. 188-192. doi:10.1016/S0014-5793(02)03332-X
S. Nagarkar, A. Patil, A. Lele, S. Bhat, J. Bellare and R. A. Mashelkar, “Some Mechanistic Insights into the Gelation of Regenerated Silk Fibroin Sol,” Industrial & Engineering Chemistry Research, Vol. 48, No. 17, 2009, pp. 8014-8023. doi:10.1021/ie801723f
C. S. Ki, Y. H. Park and H. J. Jin, “Silk Protein as a Fascinating Biomedical Polymer: Structural Fundamentals and Applications,” Macromolecular Research, Vol. 17, No. 12, 2009, pp. 935-942. doi:10.1007/BF03218639
K. A. Scott, D. O. V. Alonso, S. Sato, A. R. Fersht and V. Daggett, “Conformational Entropy of Alanine versus Glycine in Protein Denatured States,” PNAS, Vol. 104, No. 8, 2007, pp. 2661-2666. doi:10.1073/pnas.0611182104
D. Chandler, “Interfaces and the Driving Force of Hydrophobic Assembly,” Nature, Vol. 437, No. 7059, 2005, pp. 640-647. doi:10.1038/nature04162
S. Mitsuhashi, M. Morimura, K. Kono and H. Oshima, “Elimination of Drug Resistance of Staphylococcus aureus By Treatment with Acriflavine,” Journal of Bacteriology, Vol. 86, No. 1, 1963, pp. 162-164.
A. J. Penning and A. M. Kiel, “Fractionation of Polymers by Crystallization from Solution, III. On the Morphology of Fibrillar Polyethylene Crystals Grown in Solution,” Colloid & Polymer Science, Vol. 205, No. 2, 1965, pp. 160-162. doi:10.1007/BF01507982
A. J. Pennings, Vander, J. M. A. A. Mark and A. M. Kiel, “Hydrodynamically Induced Crystallization of Polymers from Solution,” Colloid and Polymer Science, Vol. 237, No. 2, 1970, pp. 336-358.