Silk proteins for biomedical applications: Bioengineering perspectives

Progress in Polymer Science

Volumn 39, Issue 2, 2014, Pages 251-267

  Kundu, Banani ^a   Kurland, Nicholas E ^b   Bano, Subia ^a   Patra, Chinmoy ^c   Engel, Felix B ^c   Yadavalli, Vamsi K ^b   Kundu, Subhas C ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY   (India)

^b Virginia Commonwealth University   (United States)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Biomedical applications; Films; Hydrogels; Scaffolds; Silk

Indexed keywords

BIOACTIVE MOLECULES; BIOMEDICAL APPLICATIONS; FUNCTIONALIZATIONS; HIGH MECHANICAL STRENGTH; IMPLANTABLE DEVICES; MEDICAL DEVICES; PROTEIN POLYMERS; SILK PROTEINS;

BIOCOMPATIBILITY; BIODEGRADATION; BIOLOGICAL MATERIALS; BIOMEDICAL EQUIPMENT; BIOMIMETIC MATERIALS; BIOMIMETICS; FILMS; HYDROGELS; IMPLANTS (SURGICAL); MEDICAL APPLICATIONS; PROTEINS; SCAFFOLDS; SILK;

SCAFFOLDS (BIOLOGY);

EID: 84893663807     PISSN: 00796700     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.progpolymsci.2013.09.002     Document Type: Review

References (205)

1. R. Langer, and D.A. Tirrell Designing materials for biology and medicine Nature 428 2004 487 492 (Pubitemid 38480528)
2. M.P. Ho, H. Wang, and K.T. Lau Effect of degumming time on silkworm silk fibre for biodegradable polymer composites Appl Surf Sci 258 2012 3948 3955
3. Y. Cao, and B.C. Wang Biodegradation of silk biomaterials Int J Mol Sci 10 2009 1514 1524
4. B.D. Ratner, A.S. Hoffman, F.J. Schoen, and J.E. Lemons Biomaterials science: an introduction to materials in medicine 2nd ed. 2004 Elsevier Academic Press Amsterdam/Boston 864
5. F. Vollrath, D. Porter, and A. Appl Phys Spider silk as a model biomaterial vol. 82 2006 205 212
6. G.H. Altman, F. Diaz, C. Jakuba, T. Calabro, R.L. Horan, J.S. Chen, H. Lu, J. Richmond, and D.L. Kaplan Silk-based biomaterials Biomaterials 24 2003 401 416 (Pubitemid 35291198)
7. A.C. MacIntosh, V.R. Kearns, A. Crawford, and P.V. Hatton Skeletal tissue engineering using silk biomaterials J Tissue Eng Regen Med 2 2008 71 80
8. L. Meinel, R. Fajardo, S. Hofmann, R. Langer, J. Chen, B. Snyder, G. Vunjak-Novakovic, and D. Kaplan Silk implants for the healing of critical size bone defects Bone 37 2005 688 698 (Pubitemid 41476392)
9. C. Cassinelli, G. Cascardo, M. Morra, L. Draghi, A. Motta, and G. Catapano Physical-chemical and biological characterization of silk fibroin-coated porous membranes for medical applications Int J Artif Organs 29 2006 881 892 (Pubitemid 44698179)
10. X.H. Zhang, C.B. Baughman, and D.L. Kaplan In vitro evaluation of electrospun silk fibroin scaffolds for vascular cell growth Biomaterials 29 2008 2217 2227
11. X. Wang, X. Zhang, J. Castellot, I. Herman, M. Iafrati, and D.L. Kaplan Controlled release from multilayer silk biomaterial coatings to modulate vascular cell responses Biomaterials 29 2008 894 903 (Pubitemid 350278534)
12. J.G. Hardy, and T.R. Scheibel Silk-inspired polymers proteins Biochem Soc Trans 37 2009 677 681
13. K. Mita, S. Ichimura, and T.C. James Highly repetitive structure and its organization of the silk fibroin gene J Mol Evol 38 1994 583 592 (Pubitemid 24177291)
14. K. Yukuhiro, T. Kanda, and T. Tamura Preferential codon usage and two types of repetitive motifs in the fibroin gene of the Chinese oak silkworm, Antheraea pernyi Insect Mol Biol 6 1997 89 95 (Pubitemid 27102786)
15. H.J. Jin, and D.L. Kaplan Mechanism of silk processing in insects and spiders Nature 424 2003 1057 1061 (Pubitemid 37064306)
16. F. Vollrath, and D.P. Knight Liquid crystalline spinning of spider silk Nature 410 2001 541 548 (Pubitemid 32267190)
17. B. Kundu, and S.C. Kundu Osteogenesis of human stem cells in silk biomaterial for regenerative therapy Prog Polym Sci 35 2010 1116 1127
18. F.G. Omenetto, and D.L. Kaplan New opportunities for an ancient material Science 329 2010 528 531
19. C. Vepari, and D. Kaplan Silk as a biomaterial Prog Polym Sci 32 2007 991 1007 (Pubitemid 47198292)
20. H. Tao, D.L. Kaplan, and F.G. Omenetto Silk materials - aroad to sustainable high technology Adv Mater 24 2012 2824 2837
21. J.A. Kluge, U. Rabotyagova, G.G. Leisk, and D.L. Kaplan Spider silks and their applications Trends Biotechnol 26 2008 244 251
22. S.C. Kundu, B. Kundu, S. Talukdar, S. Bano, S. Nayak, J. Kundu, B.B. Mandal, N. Bhardwaj, M. Botlagunta, B.C. Dash, C. Acharya, and A.K. Ghosh Nonmulberry silk biopolymers Biopolymers 97 2012 455 467
23. H.K. Soong, and K.R. Kenyon Adverse reactions to virgin silk sutures in cataract-surgery Ophthalmology 91 1984 479 483 (Pubitemid 14149076)
24. Y.-H. Kim, C.-S. Cho, I.-K. Kang, S.Y. Kim, and O.H. Kwon The biocompatibility of silk scaffold for tissue engineered ligaments Key Eng Mater 342-343 2007 73 76
25. G.H. Altman, R.L. Horan, H.H. Lu, J. Moreau, I. Martin, J.C. Richmond, and D.L. Kaplan Silk matrix for tissue engineered anterior cruciate ligaments Biomaterials 23 2002 4131 4141 (Pubitemid 34765704)
26. M. Santin, A. Motta, G. Freddi, and M. Cannas In vitro evaluation of the inflammatory potential of the silk fibroin J Biomed Mater Res 46 1999 382 389 (Pubitemid 29293762)
27. B. Panilaitis, G.H. Altman, J. Chen, H.J. Jin, V. Karageorgiou, and D.L. Kaplan Macrophage responses to silk Biomaterials 24 2003 3079 3085 (Pubitemid 36944938)
28. I. Dal Pra, G. Freddi, J. Minic, A. Chiarini, and U. Armato De novo engineering of reticular connective tissue in vivo by silk fibroin nonwoven materials Biomaterials 26 2005 1987 1999 (Pubitemid 39575341)
29. B.B. Mandal, A.S. Priya, and S.C. Kundu Novel silk sericin/gelatin 3-D scaffolds and 2-D films: fabrication and characterization for potential tissue engineering applications Acta Biomater 5 2009 3007 3020
30. X. Hu, S.-H. Park, E.S. Gil, X.-X. Xia, A.S. Weiss, and D.L. Kaplan The influence of elasticity and surface roughness on myogenic and osteogenic-differentiation of cells on silk-elastin biomaterials Biomaterials 32 2011 8979 8989
31. E. Servoli, D. Maniglio, A. Motta, R. Predazzer, and C. Migliaresi Surface properties of silk fibroin films and their interaction with fibroblasts Macromol Biosci 5 2005 1175 1183 (Pubitemid 43015291)
32. J. Perez-Rigueiro, C. Viney, J. Llorca, and M. Elices Silkworm silk as an engineering material J Appl Polym Sci 70 1998 2439 2447 (Pubitemid 128568881)
33. N.E. Kurland, Z. Drira, and V.K. Yadavalli Measurement of nanomechanical properties of biomolecules using atomic force microscopy Micron 43 2012 116 128
34. Z. Shao, F. Vollrath, and Materials: surprising strength of silkworm silk Nature 418 2002 741 751
35. J. Perez-Rigueiro, M. Elices, J. Llorca, and C. Viney Effect of degumming on the tensile properties of silkworm (Bombyx mori) silk fiber J Appl Polym Sci 84 2002 1431 1437 (Pubitemid 34268518)
36. B.B. Mandal, A. Grinberg, E. Seok Gil, B. Panilaitis, and D.L. Kaplan High-strength silk protein scaffolds for bone repair Proc Nat Acad Sci U S A 109 2012 7699 7704
37. D.H. Kim, J. Viventi, J.J. Amsden, J.L. Xiao, L. Vigeland, Y.S. Kim, J.A. Blanco, B. Panilaitis, E.S. Frechette, D. Contreras, D.L. Kaplan, F.G. Omenetto, Y.G. Huang, K.C. Hwang, M.R. Zakin, B. Litt, and J.A. Rogers Dissolvable films of silk fibroin for ultrathin conformal bio-integrated electronics Nat Mater 9 2010 511 517
38. M. Tsukada, Y. Gotoh, M. Nagura, N. Minoura, N. Kasai, and G. Freddi Structural changes of silk fibroin membranes induced by immersion in methanol aqueous solutions J Polym Sci Part B Polym Phys 32 1994 961 968
39. N. Minoura, M. Tsukada, and M. Nagura Fine structure and oxygen permeability of silk fibroin membrane treated with methanol Polymer 31 1990 265 269 (Pubitemid 20638374)
40. K.A. Karve, E.S. Gil, S.P. McCarthy, and D.L. Kaplan Effect of beta-sheet crystalline content on mass transfer in silk films J Membr Sci 383 2011 44 49
41. S. Sofia, M.B. McCarthy, G. Gronowicz, and D.L. Kaplan Functionalized silk-based biomaterials for bone formation J Biomed Mater Res 54 2001 139 148
42. Y. Gotoh, M. Tsukada, S. Aiba, and N. Minoura Chemical modification of silk fibroin with N-acetyl-chito-oligosaccharides Int J Biol Macromol 19 1996 41 44
43. K.Y. Cai, K.D. Yao, S.B. Lin, Z.M. Yang, X.Q. Li, H.Q. Xie, T.W. Qing, and L.B. Gao Poly(d,l-lactic acid) surfaces modified by silk fibroin: effects on the culture of osteoblast in vitro Biomaterials 23 2002 1153 1160
44. T. Furuzono, K. Ishihara, N. Nakabayashi, and Y. Tamada Chemical modification of silk fibroin with 2-methacryloyloxyethyl phosphorylcholine. II. Graft-polymerization onto fabric through 2-methacryloyloxyethyl isocyanate and interaction between fabric and platelets Biomaterials 21 2000 327 333 (Pubitemid 30035461)
45. V. Karageorgiou, L. Meinel, S. Hofmann, A. Malhotra, V. Volloch, and D. Kaplan Bone morphogenetic protein-2 decorated silk fibroin films induce osteogenic differentiation of human bone marrow stromal cells J Biomed Mater Res A 71 2004 528 537 (Pubitemid 39489907)
46. A.R. Murphy, P.S. John, and D.L. Kaplan Modification of silk fibroin using diazonium coupling chemistry and the effects on hMSC proliferation and differentiation Biomaterials 29 2008 2829 2838
47. S. Sampaio, T.M.R. Miranda, J.G. Santos, and G.M.B. Soares Preparation of silk fibroin-poly(ethylene glycol) conjugate films through click chemistry Polym Int 60 2011 1737 1744
48. H. Teramoto, K. Nakajima, and C. Takabayashi Chemical modification of silk sericin in lithium chloride/dimethyl sulfoxide solvent with 4-cyanophenyl lsocyanate Biomacromolecules 5 2004 1392 1398 (Pubitemid 39089741)
49. C.P. Brown, F. Rosei, E. Traversa, and S. Licoccia Spider silk as a load bearing biomaterial: tailoring mechanical properties via structural modifications Nanoscale 3 2011 870 876
50. S.I. Roohani-Esfahani, Z.F. Lu, J.J. Li, R. Ellis-Behnke, D.L. Kaplan, and H. Zreiqat Effect of self-assembled nanofibrous silk/polycaprolactone layer on the osteoconductivity and mechanical properties of biphasic calcium phosphate scaffolds Acta Biomater 8 2012 302 312
51. Z.X. Cai, X.M. Mo, K.H. Zhang, L.P. Fan, A.L. Yin, C.L. He, and H.S. Wang Fabrication of chitosan/silk fibroin composite nanofibers for wound-dressing applications Int J Mol Sci 11 2010 3529 3539
52. Z.D. She, C.R. Jin, Z. Huang, B.F. Zhang, Q.L. Feng, and Y.X. Xu Silk fibroin/chitosan scaffold: preparation, characterization, and culture with HepG2 cell J Mater Sci Mater Med 19 2008 3545 3553
53. Y.Y. Xia, and Y. Lu Fabrication and properties of conductive conjugated polymers/silk fibroin composite fibers Compos Sci Technol 68 2008 1471 1479
54. S.-M. Lee, E. Pippel, U. GÃsele, C. Dresbach, Y. Qin, C.V. Chandran, T. BrÃuniger, G. Hause, and M. Knez Greatly increased toughness of infiltrated spider silk Science 324 2009 488 492
55. C. Acharya, S.K. Ghosh, and S.C. Kundu Silk fibroin protein from mulberry and non-mulberry silkworms: cytotoxicity, biocompatibility and kinetics of L929 murine fibroblast adhesion J Mater Sci Mater Med 19 2008 2827 2836
56. Y.Z. Wang, H.J. Kim, G. Vunjak-Novakovic, and D.L. Kaplan Stem cell-based tissue engineering with silk biomaterials Biomaterials 27 2006 6064 6082 (Pubitemid 44437574)
57. M. Fini, A. Motta, P. Torricelli, G. Glavaresi, N.N. Aldini, M. Tschon, R. Giardino, and C. Migliaresi The healing of confined critical size cancellous defects in the presence of silk fibroin hydrogel Biomaterials 26 2005 3527 3536 (Pubitemid 40038147)
58. R.E. Unger, K. Peters, M. Wolf, A. Motta, C. Migliaresi, and C.J. Kirkpatrick Endothelialization of a non-woven silk fibroin net for use in tissue engineering: growth and gene regulation of hunian endothelial cells Biomaterials 25 2004 5137 5146 (Pubitemid 38510399)
59. S. Sundar, J. Kundu, and S.C. Kundu Biopolymeric nanoparticles Sci Technol Adv Mater 11 2010 014104 1-13
60. Y. Patil, and J. Panyam Polymeric nanoparticles for siRNA delivery and gene silencing Int J Pharm 367 2009 195 203
61. T. Hino, M. Tanimoto, and S. Shimabayashi Change in secondary structure of silk fibroin during preparation of its microspheres by spray-drying and exposure to humid atmosphere J Colloid Interface Sci 266 2003 68 73 (Pubitemid 37083204)
62. X. Wang, E. Wenk, X. Hu, G.R. Castro, L. Meinel, X. Wang, C. Li, H. Merkle, and D.L. Kaplan Silk coatings on PLGA and alginate microspheres for protein delivery Biomaterials 28 2007 4161 4169 (Pubitemid 47048382)
63. O.S. Rabotyagova, P. Cebe, and D.L. Kaplan Self-assembly of genetically engineered spider silk block copolymers Biomacromolecules 10 2009 229 236
64. U.K. Slotta, S. Rammensee, S. Gorb, and T. Scheibel An engineered spider silk protein forms microspheres Angew Chem Int Ed 47 2008 4592 4594
65. K.D. Hermanson, D. Huemmerich, T. Scheibel, and A.R. Bausch Engineered microcapsules fabricated from reconstituted spider silk Adv Mater 19 2007 1810 1815 (Pubitemid 47167424)
66. M.P. Desai, V. Labhasetwar, E. Walter, R.J. Levy, and G.L. Amidon The mechanism of uptake of biodegradable microparticles in Caco-2 cells is size dependent Pharm Res 14 1997 1568 1573 (Pubitemid 28009208)
67. J. Kundu, Y.I. Chung, Y.H. Kim, G. Taeb, and S.C. Kundu Silk fibroin nanoparticles for cellular uptake and control release Int J Pharm 388 2010 242 250
68. N. Minoura, M. Tsukada, and M. Nagura Physicochemical properties of silk fibroin membrane as a biomaterial Biomaterials 11 1990 430 434 (Pubitemid 20300839)
69. D. Huemmerich, U. Slotta, and T. Scheibel Processing and modification of films made from recombinant spider silk proteins Appl Phys A 82 2006 219 222 (Pubitemid 41744318)
70. C.J. Fu, Z.Z. Shao, and V. Fritz Animal silks: their structures, properties and artificial production Chem Commun 2009 6515 6529
71. J.G. Hardy, L.M. Romer, and T.R. Scheibel Polymeric materials based on silk proteins Polymer 49 2008 4309 4327
72. H.J. Jin, J. Park, V. Karageorgiou, U.J. Kim, R. Valluzzi, and D.L. Kaplan Water-stable silk films with reduced beta-sheet content Adv Funct Mater 15 2005 1241 1247 (Pubitemid 41119966)
73. C.Y. Jiang, X.Y. Wang, R. Gunawidjaja, Y.H. Lin, M.K. Gupta, D.L. Kaplan, R.R. Naik, and V.V. Tsukruk Mechanical properties of robust ultrathin silk fibroin films Adv Funct Mater 17 2007 2229 2237 (Pubitemid 47396211)
74. F. Junghans, M. Morawietz, U. Conrad, T. Scheibel, A. Heilmann, and U. Spohn Preparation and mechanical properties of layers made of recombinant spider silk proteins and silk from silk worm Appl Phys A 82 2006 253 260 (Pubitemid 41744322)
75. K. Tsioris, W.K. Raja, E.M. Pritchard, B. Panilaitis, D.L. Kaplan, and F.G. Omenetto Fabrication of silk microneedles for controlled-release drug delivery Adv Funct Mater 22 2012 330 335
76. H.J. Jin, J.S. Chen, V. Karageorgiou, G.H. Altman, and D.L. Kaplan Human bone marrow stromal cell responses on electrospun silk fibroin mats Biomaterials 25 2004 1039 1047 (Pubitemid 37406657)
77. S. Arcidiacono, C.M. Mello, M. Butler, E. Welsh, J.W. Soares, A. Allen, D. Ziegler, T. Laue, and S. Chase Aqueous processing and fiber spinning of recombinant spider silks Macromolecules 35 2002 1262 1266 (Pubitemid 34176241)
78. A. Lazaris, S. Arcidiacono, Y. Huang, J.F. Zhou, F. Duguay, N. Chretien, E.A. Welsh, J.W. Soares, and C.N. Karatzas Spider silk fibers spun from soluble recombinant silk produced in mammalian cells Science 295 2002 472 476 (Pubitemid 34101631)
79. P.X. Ma, and R.Y. Zhang Synthetic nano-scale fibrous extracellular matrix J Biomed Mater Res 46 1999 60 72 (Pubitemid 29233181)
80. S.E. Paramonov, H.W. Jun, and J.D. Hartgerink Self-assembly of peptide-amphiphile nanofibers: the roles of hydrogen bonding and amphiphilic packing J Am Chem Soc 128 2006 7291 7298 (Pubitemid 43849130)
81. D.H. Reneker, A.L. Yarin, H. Fong, and S. Koombhongse Bending instability of electrically charged liquid jets of polymer solutions in electrospinning J Appl Phys 87 2000 4531 4547
82. M.M. Hohman, M. Shin, G. Rutledge, and M.P. Brenner Electrospinning and electrically forced jets. I. Stability theory Phys Fluids 13 2001 2201 2220 (Pubitemid 32731746)
83. J. Venugopal, S. Low, A.T. Choon, and S. Ramakrishna Interaction of cells and nanofiber scaffolds in tissue engineering J Biomed Mater Res Part B 84 2008 34 48
84. Q. Lu, X. Wang, S. Lu, M. Li, D.L. Kaplan, and H. Zhu Nanofibrous architecture of silk fibroin scaffolds prepared with a mild self-assembly process Biomaterials 32 2011 1059 1067
85. J. Ming, B. Zuo, and I. Silk structure formation through silk fibroin self-assembly J Appl Polym Sci 125 2012 2148 2154
86. V.L. Tsang, and S.N. Bhatia Three-dimensional tissue fabrication Adv Drug Deliv Rev 56 2004 1635 1647 (Pubitemid 39177693)
87. 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 J Phys Chem B 110 2006 2163 2168
88. A. Fournier Quantitative data on the Bombyx mori L. silkworm: a review Biochimie 61 1979 283 320
89. Y. Zhou, H. Yang, X. Liu, J. Mao, S. Gu, and W. Xu Electrospinning of carboxyethyl chitosan/poly(vinyl alcohol)/silk fibroin nanoparticles for wound dressings Int J Biol Macromol 53 2013 88 92
90. A. Hirabayashi, and Z. Ayub Gelation of silk fibroin Sen'i Gakkaishi 46 1990 521 524
91. A.E. Terry, D.P. Knight, D. Porter, and F. Vollrath pH induced changes in the rheology of silk fibroin solution from the middle division of Bombyx mori silkworm Biomacromolecules 5 2004 768 772 (Pubitemid 38702244)
92. U.J. Kim, J. Park, C. Li, H.J. Jin, R. Valluzzi, and D.L. Kaplan Structure and properties of silk hydrogels Biomacromolecules 5 2004 786 792 (Pubitemid 38702247)
93. K. Park, W.S.W. Shalaby, and H. Park Biodegradable hydrogels for drug delivery 1993 Technomic Pub. Lancaster, PA 262
94. R. Nazarov, H.J. Jin, and D.L. Kaplan Porous 3-D scaffolds from regenerated silk fibroin Biomacromolecules 5 2004 718 726 (Pubitemid 38702237)
95. M. Tsukada, G. Freddi, N. Minoura, and G. Allara Preparation and application of porous silk fibroin materials J Appl Polym Sci 54 1994 507 514
96. U.J. Kim, J. Park, H.J. Kim, M. Wada, and D.L. Kaplan Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin Biomaterials 26 2005 2285 2775
97. C.M. Li, C. Vepari, H.J. Jin, H.J. Kim, and D.L. Kaplan Electrospun silk-BMP-2 scaffolds for bone tissue engineering Biomaterials 27 2006 3115 3124 (Pubitemid 43247585)
98. N. Kukreja, Y. Onuma, J. Daemen, and P.W. Serruys The future of drug-eluting stents Pharmacol Res 57 2008 171 180
99. R. Kino, T. Ikorna, S. Yunoki, N. Nagai, J. Tanaka, T. Asakura, and M. Munekata Preparation and characterization of multilayered hydroxyapatite/silk fibroin film J Biosci Bioeng 103 2007 514 520 (Pubitemid 47043546)
100. T. Arai, D.L. Wilson, N. Kasai, G. Freddi, S. Hayasaka, and M. Tsukada Preparation of silk fibroin and polyallylamine composites J Appl Polym Sci 84 2002 1963 1970 (Pubitemid 34288271)
101. A. Sugihara, K. Sugiura, H. Morita, T. Ninagawa, K. Tubouchi, R. Tobe, M. Izumiya, T. Horio, N.G. Abraham, and S. Ikehara Promotive effects of a silk film on epidermal recovery from full-thickness skin wounds Proc Soc Exp Biol Med 225 2000 58 64
102. K.Y. Lee, and W.S. Ha DSC studies on bound water in silk fibroin/S-carboxymethyl kerateine blend films Polymer 40 1999 4131 4134 (Pubitemid 30122505)
103. Y. Tamada, M. Sano, K. Niwa, T. Imai, and G. Yoshino Sulfation of silk sericin and anticoagulant activity of sulfated sericin J Biomater Sci Polym E 15 2004 971 980 (Pubitemid 39220356)
104. O. Akturk, A. Tezcaner, H. Bilgili, M.S. Deveci, M.R. Gecit, and D. Keskin Evaluation of sericin/collagen membranes as prospective wound dressing biomaterial J Biosci Bioeng 112 2011 279 288
105. T. Furuzono, A. Kishida, and J. Tanaka Nano-scaled hydroxyapatite/polymer composite. I. Coating of sintered hydroxyapatite particles on poly(gamma-methacryloxypropyl trimethoxysilane)-grafted silk fibroin fibers through chemical bonding J Mater Sci Mater Med 15 2004 19 23 (Pubitemid 38175024)
106. N. Vachiraroj, J. Ratanavaraporn, S. Damrongsakkul, R. Pichyangkura, T. Banaprasert, and S. Kanokpanont A comparison of Thai silk fibroin-based and chitosan-based materials on in vitro biocompatibility for bone substitutes Int J Biol Macromol 45 2009 470 477
107. M. Kang, R. Jung, H.S. Kim, J.H. Youk, and H.J. Jin Silver nanoparticles incorporated electrospun silk fibers J Nanosci Nanotechnol 7 2007 3888 3891
108. Y.R. Zhu, Y.Y. Chen, G.H. Xu, X.J. Ye, D.N. He, and J. Zhong Micropattern of nano-hydroxyapatite/silk fibroin composite onto Ti alloy surface via template-assisted electrostatic spray deposition Mater Sci Eng C 32 2012 390 394
109. F.P. Seib, M.F. Maitz, X.A. Hu, C. Werner, and D.L. Kaplan Impact of processing parameters on the haemocompatibility of Bombyx mori silk films Biomaterials 33 2012 1017 1023
110. N. Minoura, S.I. Aiba, M. Higuchi, Y. Gotoh, M. Tsukada, and Y. Imai Attachment and growth of fibroblast cells on silk fibroin Biochem Biophys Res Commun 208 1995 511 516
111. J. Wu, Y.Q. Du, S.C. Watkins, J.L. Funderburgh, and W.R. Wagner The engineering of organized human corneal tissue through the spatial guidance of corneal stromal stem cells Biomaterials 33 2012 1343 1352
112. A.C. Jones, C.H. Arns, D.W. Hutmacher, B.K. Milthorpe, A.P. Sheppard, and M.A. Knackstedt The correlation of pore morphology, interconnectivity and physical properties of 3D ceramic scaffolds with bone ingrowth Biomaterials 30 2009 1440 1451
113. B.D. Lawrence, J.K. Marchant, M.A. Pindrus, F.G. Omenetto, and D.L. Kaplan Silk film biomaterials for cornea tissue engineering Biomaterials 30 2009 1299 1308
114. L.J. Bray, K.A. George, S.L. Ainscough, D.W. Hutmacher, T.V. Chirila, and D.G. Harkin Human corneal epithelial equivalents constructed on Bombyx mori silk fibroin membranes Biomaterials 32 2011 5086 5091
115. L.J. Bray, K.A. George, D.W. Hutmacher, T.V. Chirila, and D.G. Harkin A dual-layer silk fibroin scaffold for reconstructing the human corneal limbus Biomaterials 33 2012 3529 3538
116. D.G. Harkin, K.A. George, P.W. Madden, I.R. Schwab, D.W. Hutmacher, and T.V. Chirila Silk fibroin in ocular tissue reconstruction Biomaterials 32 2011 2445 2458
117. 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 32 2011 4076 4084
118. K. Hu, Q. Lv, F.Z. Cui, Q.L. Feng, X.D. Kong, H.L. Wang, L.Y. Huang, and T. Li Biocompatible fibroin blended films with recombinant human-like collagen for hepatic tissue engineering J Bioact Compat Polym 21 2006 23 37 (Pubitemid 43164995)
119. E.S. Gil, B.B. Mandal, S.H. Park, J.K. Marchant, F.G. Omenetto, and D.L. Kaplan Helicoidal multi-lamellar features of RGD-functionalized silk biomaterials for corneal tissue engineering Biomaterials 31 2010 8953 8963
120. B.C. Dash, B.B. Mandal, and S.C. Kundu Silk gland sericin protein membranes: fabrication and characterization for potential biotechnological applications J Biotechnol 144 2009 321 329
121. C.S. Chen, M. Mrksich, S. Huang, G.M. Whitesides, and D.E. Ingber Micropatterned surfaces for control of cell shape, position, and function Biotechnol Prog 14 1998 356 363 (Pubitemid 28278815)
122. H. Perry, A. Gopinath, D.L. Kaplan, L. Dal Negro, and F.G. Omenetto Nano- and micropatterning of optically transparent, mechanically robust, biocompatible silk fibroin films Adv Mater 20 2008 3070 3072
123. K. Tsioris, H. Tao, M.K. Liu, J.A. Hopwood, D.L. Kaplan, R.D. Averitt, and F.G. Omenetto Rapid transfer-based micropatterning and dry etching of silk microstructures Adv Mater 23 2011 2015 2019
124. M. Mao, J.K. He, Y.X. Liu, X. Li, and D.C. Li Ice-template-induced silk fibroin-chitosan scaffolds with predefined microfluidic channels and fully porous structures Acta Biomater 8 2012 2175 2184
125. C.J. Bettinger, K.M. Cyr, A. Matsumoto, R. Langer, J.T. Borenstein, and D.L. Kaplan Silk fibroin microfluidic devices Adv Mater 19 2007 2847 2850 (Pubitemid 47597874)
126. M.P. Lutolf, P.M. Gilbert, and H.M. Blau Designing materials to direct stem-cell fate Nature 462 2009 433 441
127. P. Fratzl, and F.G. Barth Biomaterial systems for mechanosensing and actuation Nature 462 2009 442 448
128. J.S. Chen, G.H. Altman, V. Karageorgiou, R. Horan, A. Collette, V. Volloch, T. Colabro, and D.L. Kaplan Human bone marrow stromal cell ligament fibroblast responses on RGD-modified silk fibers Biomed Mater Res J A 67 2003 559 570 (Pubitemid 37522463)
129. D.N. Rockwood, E.S. Gil, S.H. Park, J.A. Kluge, W. Grayson, S. Bhumiratana, R. Rajkhowa, X.G. Wang, S.J. Kim, G. Vunjak-Novakovic, and D.L. Kaplan Ingrowth of human mesenchymal stem cells into porous silk particle reinforced silk composite scaffolds: an in vitro study Acta Biomater 7 2011 144 151
130. D.E. Jaalouk, and J. Lammerding Mechanotransduction gone awry Nat Rev Mol Cell Biol 10 2009 63 73
131. S. Bhumiratana, W.L. Grayson, A. Castaneda, D.N. Rockwood, E.S. Gil, D.L. Kaplan, and G. Vunjak-Novakovic Nucleation and growth of mineralized bone matrix on silk-hydroxyapatite composite scaffolds Biomaterials 32 2011 2812 2820
132. A.J. Mieszawska, N. Fourligas, I. Georgakoudi, N.M. Ouhib, D.J. Belton, C.C. Perry, and D.L. Kaplan Osteoinductive silk-silica composite biomaterials for bone regeneration Biomaterials 31 2010 8902 8910
133. A.J. Mieszawska, J.G. Llamas, C.A. Vaiana, M.P. Kadakia, R.R. Naik, and D.L. Kaplan Clay enriched silk biomaterials for bone formation Acta Biomater 7 2011 3036 3041
134. H.S. Baek, Y.H. Park, C.S. Ki, J.C. Park, and D.K. Rah Enhanced chondrogenic responses of articular chondrocytes onto porous silk fibroin scaffolds treated with microwave-induced argon plasma Surf Coat Technol 202 2008 5794 5797
135. X.Z. Zhang, D. Bogdanowicz, C. Erisken, N.M. Lee, and H.H. Lu Biomimetic scaffold design for functional and integrative tendon repair J Shoulder Elb Surg 21 2012 266 277
136. K.E. Park, S.Y. Jung, S.J. Lee, B.M. Min, and W.H. Park Biomimetic nanofibrous scaffolds: preparation and characterization of chitin/silk fibroin blend nanofibers Int J Biol Macromol 38 2006 165 173 (Pubitemid 43732435)
137. B.M. Min, G. Lee, S.H. Kim, Y.S. Nam, T.S. Lee, and W.H. Park Electrospinning of silk fibroin nanofibers and its effect on the adhesion and spreading of normal human keratinocytes and fibroblasts in vitro Biomaterials 25 2004 1289 1297 (Pubitemid 37476206)
138. S. Martino, F. D'Angelo, I. Armentano, J.M. Kenny, and A. Orlacchio Stem cell-biomaterial interactions for regenerative medicine Biotechnol Adv 30 2012 338 351
139. X.D. Chen Extracellular matrix provides an optimal niche for the maintenance and propagation of mesenchymal stem cells Birth Defects Res C 90 2010 45 54
140. B.B. Mandal, S. Das, K. Choudhury, and S.C. Kundu Implication of silk film RGD availability and surface roughness on cytoskeletal organization and proliferation of primary rat bone marrow cells Tissue Eng Part A 16 2010 2391 2403
141. B.B. Mandal, and S.C. Kundu Non-bioengineered silk gland fibroin protein: characterization and evaluation of matrices for potential tissue engineering applications Biotechnol Bioeng 100 2008 1237 1250
142. C. Patra, S. Talukdar, T. Novoyatleva, S.R. Velagala, C. Muhlfeld, B. Kundu, S.C. Kundu, and F.B. Engel Silk protein fibroin from Antheraea mylitta for cardiac tissue engineering Biomaterials 33 2012 2673 2680
143. X.Y. Luan, Y. Wang, X. Duan, Q.Y. Duan, M.Z. Li, S.Z. Lu, H.X. Zhang, and X.G. Zhang Attachment and growth of human bone marrow derived mesenchymal stem cells on regenerated Antheraea pernyi silk fibroin films Biomed Mater 1 2006 181 187 (Pubitemid 46217607)
144. N. Kasoju, R.R. Bhonde, and U. Bora Preparation and characterization of Antheraea assama silk fibroin based novel non-woven scaffold for tissue engineering applications J Tissue Eng Regen Med 3 2009 539 552
145. H. Teramoto, K. Nakajima, and C. Takabayashi Preparation of elastic silk sericin hydrogel Biosci Biotechol Biochem 69 2005 845 847 (Pubitemid 40793795)
146. J.E. Moreau, J.S. Chen, R.L. Horan, D.L. Kaplan, and G.H. Altman Sequential growth factor application in bone marrow stromal cell ligament engineering Tissue Eng 11 2005 1887 1897 (Pubitemid 43120201)
147. H. Yoshimoto, Y.M. Shin, H. Terai, and J.P. Vacanti A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering Biomaterials 24 2003 2077 2082 (Pubitemid 36298779)
148. K. Yamamoto, N. Tomita, Y. Fukuda, S. Suzuki, N. Igarashi, T. Suguro, and Y. Tamada Time-dependent changes in adhesive force between chondrocytes and silk fibroin substrate Biomaterials 28 2007 1838 1846 (Pubitemid 46123540)
149. J.R. Mauney, T. Nguyen, K. Gillen, C. Kirker-Head, J.M. Gimble, and D.L. Kaplan Engineering adipose-like tissue in vitro and in vivo utilizing human bone marrow and adipose-derived mesenchymal stem cells with silk fibroin 3D scaffolds Biomaterials 28 2007 5280 5290 (Pubitemid 47532187)
150. X.H. Zou, Y.L. Zhi, X. Chen, H.M. Jin, L.L. Wang, Y.Z. Jiang, Z. Yin, and H.W. Ouyang Mesenchymal stem cell seeded knitted silk sling for the treatment of stress urinary incontinence Biomaterials 31 2010 4872 4879
151. L.P. Yan, J.M. Oliveira, A.L. Oliveira, S.G. Caridade, J.F. Mano, and R.L. Reis Macro/microporous silk fibroin scaffolds with potential for articular cartilage and meniscus tissue engineering applications Acta Biomater 8 2012 289 301
152. B.B. Mandal, and S.C. Kundu Osteogenic and adipogenic differentiation of rat bone marrow cells on non-mulberry and mulberry silk gland fibroin 3D scaffolds Biomaterials 30 2009 5019 5030
153. W. Huang, R. Begum, T. Barber, V. Ibba, N.C.H. Tee, M. Hussain, M. Arastoo, Q. Yang, L.G. Robson, S. Lesage, T. Gheysens, N.J.V. Skaer, D.P. Knight, and J.V. Priestley Regenerative potential of silk conduits in repair of peripheral nerve injury in adult rats Biomaterials 33 2012 59 71
154. S. Talukdar, M. Mandal, D.W. Hutmacher, P.J. Russell, C. Soekmadji, and S.C. Kundu Engineered silk fibroin protein 3D matrices for in vitro tumor model Biomaterials 32 2011 2149 2159
155. X.L. Wang, and D.L. Kaplan Hormone-responsive 3D multicellular culture model of human breast tissue Biomaterials 33 2012 3411 3420
156. Q. Fang, D.L. Chen, Z.M. Yang, and M. Li In vitro and in vivo research on using Antheraea pernyi silk fibroin as tissue engineering tendon scaffolds Mater Sci Eng C 29 2009 1527 1534
157. X.W. Wu, J.A. Ren, and J.S. Li Fibrin glue as the cell-delivery vehicle for mesenchymal stromal cells in regenerative medicine Cytotherapy 14 2012 555 562
158. S. Terada, T. Nishimura, M. Sasaki, H. Yamada, and M. Miki Sericin, a protein derived from silkworms, accelerates the proliferation of several mammalian cell lines including a hybridoma Cytotechnology 40 2002 3 12 (Pubitemid 36749588)
159. N. Nagai, T. Murao, Y. Ito, N. Okamoto, and M. Sasaki Enhancing effects of sericin on corneal wound healing in rat debrided corneal epithelium Biol Pharm Bull 32 2009 933 936
160. R.J. Xie, M.Z. Li, S.Z. Lu, W.H. Sheng, and Y.F. Xie Preparation of sericin film and its cytocompatibility Key Eng Mater 342-343 2007 241 244
161. K.H. Lee, D.H. Baek, C.S. Ki, and Y.H. Park Preparation and characterization of wet spun silk fibroin/poly(vinyl alcohol) blend filaments Int J Biol Macromol 41 2007 168 172 (Pubitemid 46635812)
162. M.L. Gulrajani, D. Gupta, S. Periyasamy, and S.G. Muthu Preparation and application of silver nanoparticles on silk for imparting antimicrobial properties J Appl Polym Sci 108 2008 614 623 (Pubitemid 351363335)
163. I.S. Yeo, J.E. Oh, L. Jeong, T.S. Lee, S.J. Lee, W.H. Park, and B.M. Min Collagen-based biomimetic nanofibrous scaffolds: preparation and characterization of collagen/silk fibroin bicomponent nanofibrous structures Biomacromolecules 9 2008 1106 1116 (Pubitemid 351639562)
164. B.B. Mandal, S.H. Park, E.S. Gil, and D.L. Kaplan Multilayered silk scaffolds for meniscus tissue engineering Biomaterials 32 2011 639 651
165. Z. Ge, Q. Yang, X. Xiang, and K.Z. Liu Assessment of silk fibroin for the repair of buccal mucosa in a rat model Int J Oral Maxillofacial Surg 41 2012 673 680
166. Y. Yang, F. Ding, J. Wu, W. Hu, W. Liu, J. Liu, and X. Gu Development and evaluation of silk fibroin-based nerve grafts used for peripheral nerve regeneration Biomaterials 28 2007 5526 5535 (Pubitemid 47610691)
167. M.L. Lovett, C.M. Cannizzaro, G. Vunjak-Novakovic, and D.L. Kaplan Gel spinning of silk tubes for tissue engineering Biomaterials 29 2008 4650 4657
168. B. Bondar, S. Fuchs, A. Motta, C. Migliaresi, and C.J. Kirkpatrick Functionality of endothelial cells on silk fibroin nets: comparative study of micro- and nanometric fibre size Biomaterials 29 2008 561 572 (Pubitemid 350100800)
169. L. Soffer, X.Y. Wang, X.H. Mang, J. Kluge, L. Dorfmann, D.L. Kaplan, and G. Leisk Silk-based electrospun tubular scaffolds for tissue-engineered vascular grafts J Biomat Sci Polym E 19 2008 653 664 (Pubitemid 351535787)
170. C. Szybala, E.M. Pritchard, T.A. Lusardi, T.F. Li, A. Wilz, D.L. Kaplan, and D. Boison Antiepileptic effects of silk-polymer based adenosine release in kindled rats Exp Neurol 219 2009 126 135
171. V. Benfenati, S. Toffanin, R. Capelli, L.M.A. Camassa, S. Ferroni, D.L. Kaplan, F.G. Omenetto, M. Muccini, and R. Zamboni A silk platform that enables electrophysiology and targeted drug delivery in brain astroglial cells Biomaterials 31 2010 7883 7891
172. S. Lu, X. Wang, Q. Lu, X. Hu, N. Uppal, F.G. Omenetto, and D.L. Kaplan Stabilization of enzymes in silk films Biomacromolecules 10 2009 1032 1042
173. J. Kundu, C. Patra, and S.C. Kundu Design, fabrication and characterization of silk fibroin-HPMC-PEG blended films as vehicle for transmucosal delivery Mater Sci Eng C 28 2008 1376 1380
174. R. Rujiravanit, S. Kruaykitanon, A.M. Jamieson, and S. Tokura Preparation of crosslinked chitosan/silk fibroin blend films for drug delivery system Macromol Biosci 3 2003 604 611 (Pubitemid 37309689)
175. S. Madduri, M. Papaloïzos, and B. Gander Trophically and topographically functionalized silk fibroin nerve conduits for guided peripheral nerve regeneration Biomaterials 31 2010 2323 2334
176. L. Uebersax, M. Mattotti, M. Papaloïzos, H.P. Merkle, B. Gander, and L. Meinel Silk fibroin matrices for the controlled release of nerve growth factor (NGF) Biomaterials 28 2007 4449 4460 (Pubitemid 47225114)
177. E. Wenk, A.J. Meinel, S. Wildy, H.P. Merkle, and L. Meinel Microporous silk fibroin scaffolds embedding PLGA microparticles for controlled growth factor delivery in tissue engineering Biomaterials 30 2009 2571 2581
178. E. Wenk, A.R. Murphy, D.L. Kaplan, L. Meinel, H.P. Merkle, and L. Uebersax The use of sulfonated silk fibroin derivatives to control binding, delivery and potency of FGF-2 in tissue regeneration Biomaterials 31 2010 1403 1413
179. P.J. Shi, and J.C.H. Goh Self-assembled silk fibroin particles: tunable size and appearance Powder Technol 215-216 2012 85 90
180. R.C. Mundargi, V.R. Babu, V. Rangaswamy, P. Patel, and T.M. Aminabhavi Nano/micro technologies for delivering macromolecular therapeutics using poly(D l-lactide-co-glycolide) and its derivatives J Control Release 125 2008 193 209
181. B.B. Mandal, and S.C. Kundu Calcium alginate beads embedded in silk fibroin as 3D dual drug releasing scaffolds Biomaterials 30 2009 5170 5177
182. A. Wilz, E.M. Pritchard, T. Li, J.Q. Lan, D.L. Kaplan, and D. Boison Silk polymer-based adenosine release: therapeutic potential for epilepsy Biomaterials 29 2008 3609 3616
183. J.F. Zhang, L.Y. Shi, and D.Z. Wei Chemical modification of l-asparaginase from Escherichia coli with a modified polyethyleneglycol under substrate protection conditions Biotechnol Lett 26 2004 753 756
184. J.S. Ahn, H.K. Choi, K.H. Lee, J.H. Nahm, and C.S. Cho Novel mucoadhesive polymer prepared by template polymerization of acrylic acid in the presence of silk sericin J Appl Polym Sci 80 2001 274 280
185. P. Aramwit, T. Siritientong, S. Kanokpanont, and T. Srichana Formulation and characterization of silk sericin-PVA scaffold crosslinked with genipin Int J Biol Macromol 47 2010 668 675
186. B.B. Mandal, S. Kapoor, and S.C. Kundu Silk fibroin/polyacrylamide semi-interpenetrating network hydrogels for controlled drug release Biomaterials 30 2009 2826 2836
187. J. Kundu, L.A. Poole-Warren, P. Martens, and S.C. Kundu Silk fibroin/poly(vinyl alcohol) photocrosslinked hydrogels for delivery of macromolecular drugs Acta Biomater 8 2012 1720 1729
188. K. Numata, and D.L. Kaplan Silk-based delivery systems of bioactive molecules Adv Drug Deliv Rev 62 2010 1497 1508
189. L. Uebersax, H.P. Merkle, and L. Meinel Insulin-like growth factor I releasing silk fibroin scaffolds induce chondrogenic differentiation of human mesenchymal stem cells J Control Release 127 2008 12 21
190. F. Zhang, C.L. He, L.J. Cao, W. Feng, H.S. Wang, X.M. Mo, and J.W. Wang Fabrication of gelatin-hyaluronic acid hybrid scaffolds with tunable porous structures for soft tissue engineering Int J Biol Macromol 48 2011 474 481
191. T.F. Li, G.Y. Ren, D.L. Kaplan, and D. Boison Human mesenchymal stem cell grafts engineered to release adenosine reduce chronic seizures in a mouse model of CA3-selective epileptogenesis Epilepsy Res 84 2009 238 241
192. 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 32 2011 2642 2650
193. B. Marelli, C.E. Ghezzi, A. Alessandrino, J.E. Barralet, G. Freddi, and S.N. Nazhat Silk fibroin derived polypeptide-induced biomineralization of collagen Biomaterials 33 2012 102 108
194. H. Tao, J.M. Kainerstorfer, S.M. Siebert, E.M. Pritchard, A. Sassaroli, B.J.B. Panilaitis, M.A. Brenckle, J.J. Amsden, J. Levitt, S. Fantini, D.L. Kaplan, and F.G. Omenetto Implantable multifunctional bioresorbable optics Proc Nat Acad Sci U S A 109 2012 19584 19589
195. S. Kim, A.N. Mitropoulos, J.D. Spitzberg, H. Tao, D.L. Kaplan, and F.G. Omenetto Silk inverse opals Nat Photonics 6 2012 817 822
196. J.E. Zhang, E. Pritchard, X. Hu, T. Valentin, B. Panilaitis, F.G. Omenetto, and D.L. Kaplan Stabilization of vaccines and antibiotics in silk and eliminating the cold chain Proc Natl Acad Sci U S A 109 2012 1198 1206
197. S.R. Fahnestock, and S.L. Irwin Synthetic spider dragline silk proteins and their production in Escherichia coli Appl Microbiol Biotechnol 47 1997 23 32 (Pubitemid 27077295)
198. J.T. Prince, K.P. Mcgrath, C.M. Digirolamo, and D.L. Kaplan Construction, cloning, and expression of synthetic genes encoding spider dragline silk Biochemistry 34 1995 1087 1985
199. J. Scheller, K.H. Guhrs, F. Grosse, and U. Conrad Production of spider silk proteins in tobacco and potato Nat Biotechnol 19 2001 573 577 (Pubitemid 32521191)
200. R. Menassa, Z. Hong, C.N. Karatzas, A. Lazaris, A. Richman, and J. Brandle Spider dragline silk proteins in transgenic tobacco leaves: accumulation and field production Plant Biotechnol J 2 2004 431 438 (Pubitemid 40199435)
201. Y.G. Miao, Y.S. Zhang, K. Nakagaki, T.F. Zhao, A.C. Zhao, Y. Meng, M. Nakagaki, E.Y. Park, and K. Maenaka Expression of spider flagelliform silk protein in Bombyx mori cell line by a novel Bac-to-Bac/BmNPV baculovirus expression system Appl Microbiol Biotechnol 71 2006 192 199 (Pubitemid 43873246)
202. T. Scheibel Spider silks: recombinant synthesis, assembly, spinning, and engineering of synthetic proteins Microb Cell Fact 3 14 2004 1 10
203. K. Gellynck, P.C.M. Verdonk, E. Van Nimmen, K.F. Almqvist, T. Gheysens, G. Schoukens, L. Van Langenhove, P. Kiekens, J. Mertens, and G. Verbruggen Silkworm and spider silk scaffolds for chondrocyte support J Mater Sci Mater Med 19 2008 3399 3409
204. J. Huang, C. Wong, A. George, and D.L. Kaplan The effect of genetically engineered spider silk-dentin matrix protein 1 chimeric protein on hydroxyapatite nucleation Biomaterials 28 2007 2358 2367 (Pubitemid 46282927)
205. A. Lammel, M. Schwab, M. Hofer, G. Winter, and T. Scheibel Recombinant spider silk particles as drug delivery vehicles Biomaterials 32 2011 2233 2240