Fibrous Proteins: Structures and Mechanisms pp 527-573

Part of the Subcellular Biochemistry book series (SCBI, volume 82)

Properties of Engineered and Fabricated Silks

Chapter

Abstract

Silk is a protein-based material which is predominantly produced by insects and spiders. Hundreds of millions of years of evolution have enabled these animals to utilize different, highly adapted silk types in a broad variety of applications. Silk occurs in several morphologies, such as sticky glue or in the shape of fibers and can, depending on the application by the respective animal, dissipate a high mechanical energy, resist heat and radiation, maintain functionality when submerged in water and withstand microbial settling. Hence, it’s unsurprising that silk piqued human interest a long time ago, which catalyzed the domestication of silkworms for the production of silk to be used in textiles. Recently, scientific progress has enabled the development of analytic tools to gain profound insights into the characteristics of silk proteins. Based on these investigations, the biotechnological production of artificial and engineered silk has been accomplished, which allows the production of a sufficient amount of silk materials for several industrial applications. This chapter provides a review on the biotechnological production of various silk proteins from different species, as well as on the processing techniques to fabricate application-oriented material morphologies.

Keywords

Silk fibers Artificial silk Recombinant silk Engineered silk Silk processing 

References

  1. Addison JB, Ashton NN, Weber WS, Stewart RJ, Holland GP, Yarger JL (2013) beta-Sheet nanocrystalline domains formed from phosphorylated serine-rich motifs in caddisfly larval silk: a solid state NMR and XRD study. Biomacromolecules 14:1140–1148PubMedPubMedCentralCrossRefGoogle Scholar
  2. Addison JB, Weber WS, Mou Q, Ashton NN, Stewart RJ, Holland GP, Yarger JL (2014) Reversible assembly of beta-sheet nanocrystals within caddisfly silk. Biomacromolecules 15:1269–1275PubMedPubMedCentralCrossRefGoogle Scholar
  3. Adrianos SL, Teule F, Hinman MB, Jones JA, Weber WS, Yarger JL, Lewis RV (2013) Nephila clavipes Flagelliform silk-like GGX motifs contribute to extensibility and spacer motifs contribute to strength in synthetic spider silk fibers. Biomacromolecules 14:1751–1760PubMedPubMedCentralCrossRefGoogle Scholar
  4. Agapov II, Pustovalova OL, Moisenovich MM, Bogush VG, Sokolova OS, Sevastyanov VI, Debabov VG, Kirpichnikov MP (2009) Three-dimensional scaffold made from recombinant spider Silk protein for tissue engineering. Dokl Biochem Biophys 426:127–130PubMedCrossRefGoogle Scholar
  5. Albertson AE, Teule F, Weber W, Yarger JL, Lewis RV (2014) Effects of different post-spin stretching conditions on the mechanical properties of synthetic spider silk fibers. J Mech Behav Biomed Mater 29:225–234PubMedCrossRefGoogle Scholar
  6. Altman GH, Diaz F, JAKUBA C, Calabro T, Horan RL, Chen J, Lu H, Richmond J, Kaplan DL (2003) Silk-based biomaterials. Biomaterials 24:401–416PubMedCrossRefGoogle Scholar
  7. An B, Hinman MB, Holland GP, Yarger JL, Lewis RV (2011) Inducing beta-sheets formation in synthetic spider silk fibers by aqueous post-spin stretching. Biomacromolecules 12:2375–2381PubMedPubMedCentralCrossRefGoogle Scholar
  8. Anderson JP, Cappello J, Martin DC (1994) Morphology and primary crystal structure of a silk-like protein polymer synthesized by genetically engineered Escherichia coli bacteria. Biopolymers 34:1049–1058PubMedCrossRefGoogle Scholar
  9. Arcidiacono S, Mello C, Kaplan D, Cheley S, Bayley H (1998) Purification and characterization of recombinant spider silk expressed in Escherichia coli. Appl Microbiol Biotechnol 49:31–38PubMedCrossRefGoogle Scholar
  10. Ashton NN, Stewart RJ (2015) Self-recovering caddisfly silk: energy dissipating, Ca(2+)-dependent, double dynamic network fibers. Soft Matter 11:1667–1676PubMedCrossRefGoogle Scholar
  11. Ashton NN, Roe DR, Weiss RB, Cheatham TE, Stewart RJ (2013) Self-tensioning aquatic caddisfly silk: Ca2+−dependent structure, strength, and load cycle hysteresis. Biomacromolecules 14:3668–3681PubMedCrossRefGoogle Scholar
  12. Askarieh G, Hedhammar M, Nordling K, Saenz A, Casals C, Rising A, Johansson J, Knight SD (2010) Self-assembly of spider silk proteins is controlled by a pH-sensitive relay. Nature 465:236–238PubMedCrossRefGoogle Scholar
  13. Atkins EDT (1967) A four-strand coiled coil model for some insect fibrous proteins. J Mol Biol 24:139–141CrossRefGoogle Scholar
  14. Ayoub NA, Garb JE, Tinghitella RM, Collin MA, Hayashi CY (2007) Blueprint for a high-performance biomaterial: full-length spider dragline silk genes. PLoS One 2:e514PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bai X, Sakaguchi M, Yamaguchi Y, Ishihara S, Tsukada M, Hirabayashi K, Ohkawa K, Nomura T, Arai R (2015) Molecular cloning, gene expression analysis, and recombinant protein expression of novel silk proteins from larvae of a retreat-maker caddisfly, Stenopsyche marmorata. Biochem Biophys Res Commun 464:814–819PubMedCrossRefGoogle Scholar
  16. Barr LA, Fahnestock SR, Yang J (2004) Production and purification of recombinant DP1B silk-like protein in plants. Mol Breed 13:345–356CrossRefGoogle Scholar
  17. Bauer F, Bertinetti L, Masic A, Scheibel T (2012) Dependence of mechanical properties of lacewing egg stalks on relative humidity. Biomacromolecules 13:3730–3735PubMedCrossRefGoogle Scholar
  18. Bauer F, Scheibel T (2012) Artificial egg stalks made of a recombinantly produced lacewing silk protein. Angew Chem 51:6521–6524CrossRefGoogle Scholar
  19. Bauer F, Wohlrab S, Scheibel T (2013) Controllable cell adhesion, growth and orientation on layered silk protein films. Biomed Sci 1:1244–1249Google Scholar
  20. Becker N, Oroudjev E, Mutz S, Cleveland JP, Hansma PK, Hayashi CY, Makarov DE, Hansma HG (2003) Molecular nanosprings in spider capture-silk threads. Nat Mater 2:278–283PubMedCrossRefGoogle Scholar
  21. Bhardwaj G, Webster T (2015) Coating polyurethane surfaces by electrostatic charging followed by dip coating/electrophoretic deposition. FASEB J:29Google Scholar
  22. Bhardwaj N, Nguyen QT, Chen AC, Kaplan DL, Sah RL, Kundu SC (2011) Potential of 3-D tissue constructs engineered from bovine chondrocytes/silk fibroin-chitosan for in vitro cartilage tissue engineering. Biomaterials 32:5773–5781PubMedPubMedCentralCrossRefGoogle Scholar
  23. Bini E, Knight DP, Kaplan DL (2004) Mapping domain structures in silks from insects and spiders related to protein assembly. J Mol Biol 335:27–40PubMedCrossRefGoogle Scholar
  24. Bini E, Foo CWP, Huang J, Karageorgiou V, Kitchel B, Kaplan DL (2006) RGD-functionalized bioengineered spider dragline silk biomaterial. Biomacromolecules 7:3139–3145PubMedCrossRefGoogle Scholar
  25. Blackledge TA, Summers AP, Hayashi CY (2005) Gumfooted lines in black widow cobwebs and the mechanical properties of spider capture silk. Zoology 108:41–46PubMedCrossRefGoogle Scholar
  26. Blüm C, Scheibel T (2012) Control of drug loading and release properties of spider silk sub-microparticles. Bio Nano Science 2:67–74Google Scholar
  27. Blum C, Nichtl A, Scheibel T (2014) Spider silk capsules as protective reaction containers for enzymes. Adv Funct Mater 24:763–768CrossRefGoogle Scholar
  28. Borkner CB, Elsner MB, Scheibel T (2014) Coatings and films made of silk proteins. ACS Appl Mater Interfaces 6:15611–15625PubMedCrossRefGoogle Scholar
  29. Brubaker CE, Messersmith PB (2012) The present and future of biologically inspired adhesive interfaces and materials. Langmuir : the ACS journal of surfaces and colloids 28:2200–2205CrossRefGoogle Scholar
  30. Buchko CJ, Chen LC, Shen Y, Martin DC (1999) Processing and microstructural characterization of porous biocompatible protein polymer thin films. Polymer 40:7397–7407CrossRefGoogle Scholar
  31. Cebe P, Hu X, Kaplan DL, Zhuravlev E, Wurm A, Arbeiter D, Schick C (2013) Beating the heat - fast scanning melts silk beta sheet crystals. Sci Rep 3Google Scholar
  32. Cereghino GP, Cereghino JL, Ilgen C, Cregg JM (2002) Production of recombinant proteins in fermenter cultures of the yeast Pichia pastoris. Curr Opin Biotechnol 13:329–332PubMedCrossRefGoogle Scholar
  33. Challis RJ, Goodacre SL, Hewitt GM (2006) Evolution of spider silks: conservation and diversification of the C-terminus. Insect Mol Biol 15:45–56PubMedCrossRefGoogle Scholar
  34. Chao PHG, Yodmuang S, Wang XQ, Sun L, Kaplan DL, Vunjak-Novakovic G (2010) Silk hydrogel for cartilage tissue engineering. J Biomed Mater Res B Appl Biomater 95B:84–90CrossRefGoogle Scholar
  35. Chen GP, Ushida T, Tateishi T (2002) Scaffold design for tissue engineering. Macromol Biosci 2:67–77CrossRefGoogle Scholar
  36. Chen X, Cai H, Ling S, Shao Z, Huang Y (2012) Conformation transition of Bombyx mori silk protein monitored by time-dependent fourier transform infrared (FT-IR) spectroscopy: effect of organic solvent. Appl Spectrosc 66:696–699PubMedCrossRefGoogle Scholar
  37. Craig CL (1997) Evolution of arthropod silks. Annu Rev Entomol 42:231–267PubMedCrossRefGoogle Scholar
  38. Cregg JM, Vedvick TS, Raschke WC (1993) Recent advances in the expression of foreign genes in Pichia pastoris. Bio/Technology 11:905–910PubMedCrossRefGoogle Scholar
  39. Das S, Pati F, Choi YJ, Rijal G, Shim JH, Kim SW, Ray AR, Cho DW, Ghosh S (2015) Bioprintable, cell-laden silk fibroin-gelatin hydrogel supporting multilineage differentiation of stem cells for fabrication of three-dimensional tissue constructs. Acta Biomater 11:233–246PubMedCrossRefGoogle Scholar
  40. Dhandayuthapani B, Yoshida Y, Maekawa T, Kumar DS (2011). Polymeric scaffolds in tissue engineering application: a review. Int J Polym Sci 2011:1–9Google Scholar
  41. Dicko C, Knight D, Kenney JM, Vollrath F (2004) Secondary structures and conformational changes in flagelliform, cylindrical, major, and minor ampullate silk proteins. Temperature and concentration effects. Biomacromolecules 5:2105–2115PubMedCrossRefGoogle Scholar
  42. Dinerman AA, Cappello J, El-Sayed M, Hoag SW, Ghandehari H (2010) Influence of solute charge and hydrophobicity on partitioning and diffusion in a genetically engineered silk-elastin-like protein polymer hydrogel. Macromol Biosci 10:1235–1247PubMedCrossRefGoogle Scholar
  43. Dinerman AA, Cappello J, Ghandehari H, Hoag SW (2002) Swelling behavior of a genetically engineered silk-elastinlike protein polymer hydrogel. Biomaterials 23:4203–4210PubMedCrossRefGoogle Scholar
  44. Doblhofer E, Scheibel T (2015) Engineering of recombinant spider silk proteins allows defined uptake and release of substances. J Pharm Sci 104:988–994PubMedCrossRefGoogle Scholar
  45. Drury JL, Mooney DJ (2003) Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24:4337–4351PubMedCrossRefGoogle Scholar
  46. Du B, Wang JJ, Zhou ZM, Tang HB, LI XM, Liu YJ, Zhang QQ (2014) Synthesis of silk-based microcapsules by desolvation and hybridization. Chem Commun 50:4423–4426CrossRefGoogle Scholar
  47. Elia R, Michelson CD, Perera AL, Brunner TF, Harsono M, Leisk GG, Kugel G, Kaplan DL (2015) Electrodeposited silk coatings for bone implants. J Biomed Mater Res B Appl Biomater 103:1602–1609PubMedCrossRefGoogle Scholar
  48. Engster MS (1976) Studies on silk secretion in the trichoptera (F. Limnephilidae). Cell Tissue Res 169:77–92PubMedCrossRefGoogle Scholar
  49. Etienne O, Schneider A, Kluge JA, Bellemin-Laponnaz C, Polidori C, Leisk GG, Kaplan DL, Garlick JA, Egles C (2009) Soft tissue augmentation using silk gels: an in vitro and in vivo study. J Periodontol 80:1852–1858PubMedPubMedCentralCrossRefGoogle Scholar
  50. Fahnestock SR, Bedzyk LA (1997) Production of synthetic spider dragline silk protein in Pichia pastoris. Appl Microbiol Biotechnol 47:33–39PubMedCrossRefGoogle Scholar
  51. Garb JE, Ayoub NA, Hayashi CY (2010) Untangling spider silk evolution with spidroin terminal domains. BMC Evol Biol 10:243PubMedPubMedCentralCrossRefGoogle Scholar
  52. Garb JE, Hayashi CY (2005) Modular evolution of egg case silk genes across orb-weaving spider superfamilies. Proc Natl Acad Sci U S A 102:11379–11384PubMedPubMedCentralCrossRefGoogle Scholar
  53. Garg K, Bowlin GL (2011) Electrospinning jets and nanofibrous structures. Biomicrofluidics 5Google Scholar
  54. Geisler M, Pirzer T, Ackerschott C, Lud S, Garrido J, Scheibel T, Hugel T (2008) Hydrophobic and Hofmeister effects on the adhesion of spider silk proteins onto solid substrates: an AFM-based single-molecule study. Langmuir 24:1350–1355PubMedCrossRefGoogle Scholar
  55. Genov S, Riester D, Hirth T, Tovar G, Borchers K, Weber A (2011) Preparation and characterisation of dry thin native protein trehalose films on titanium-coated cyclo-olefin polymer (COP) foil generated by spin-coating/drying process and applied for protein transfer by Laser-Induced-Forward Transfer (LIFT). Chem Eng Process 50:558–564CrossRefGoogle Scholar
  56. Gill HS, Prausnitz MR (2007) Coating formulations for microneedles. Pharm Res 24:1369–1380PubMedCrossRefGoogle Scholar
  57. Gosline JM, Denny MW, Demont ME (1984) Spider silk as rubber. Nature 309:551–552CrossRefGoogle Scholar
  58. Gosline JM, Guerette PA, Ortlepp CS, Savage KN (1999) The mechanical design of spider silks: from fibroin sequence to mechanical function. J Exp Biol 202:3295–3303PubMedGoogle Scholar
  59. Gotoh Y, Tsukada M, Baba T, Minoura N (1997) Physical properties and structure of poly(ethylene glycol)-silk fibroin conjugate films. Polymer 38:487–490CrossRefGoogle Scholar
  60. Greiner A, Wendorff JH (2007) Electrospinning: a fascinating method for the preparation of ultrathin fibres. Angew Chem Int Ed 46:5670–5703CrossRefGoogle Scholar
  61. Greish K, Frandsen J, Scharff S, Gustafson J, Cappello J, Li DQ, O’malley BW, Ghandehari H (2010) Silk-elastinlike protein polymers improve the efficacy of adenovirus thymidine kinase enzyme prodrug therapy of head and neck tumors. J Gene Med 12:572–579PubMedPubMedCentralCrossRefGoogle Scholar
  62. Greving I, Cai MZ, Vollrath F, Schniepp HC (2012) Shear-induced self-assembly of native silk proteins into fibrils studied by atomic force microscopy. Biomacromolecules 13:676–682PubMedCrossRefGoogle Scholar
  63. Grip S, Rising A, Nimmervoll H, Storckenfeldt E, Mcqueen-Mason SJ, Pouchkina-Stantcheva N, Vollrath F, Engsträm W, Fernandez-Arias A (2006) Transient expression of a major ampullate spidroin 1 gene fragment from Euprosthenops sp. in mammalian cells. Cancer Genomics Proteomics 3:83–87Google Scholar
  64. Guerette PA, Ginzinger DG, Weber BH, Gosline JM (1996) Silk properties determined by gland-specific expression of a spider fibroin gene family. Science 272:112–115PubMedCrossRefGoogle Scholar
  65. Gustafson JA, Price RA, Greish K, Cappello J, Ghandehari H (2010) Silk-elastin-like hydrogel improves the safety of adenovirus-mediated gene-directed enzyme-prodrug therapy. Mol Pharm 7:1050–1056PubMedPubMedCentralCrossRefGoogle Scholar
  66. Hagn F, Eisoldt L, Hardy JG, Vendrely C, Coles M, Scheibel T, Kessler H (2010) A conserved spider silk domain acts as a molecular switch that controls fibre assembly. Nature 465:239–242PubMedCrossRefGoogle Scholar
  67. Hagn F, Thamm C, Scheibel T, Kessler H (2011) pH-dependent dimerization and salt-dependent stabilization of the N-terminal domain of spider dragline silk–implications for fiber formation. Angew Chem 50:310–313CrossRefGoogle Scholar
  68. Hajer J, Rehakova D (2003) Spinning activity of the spider Trogloneta granulum (Araneae, Mysmenidae): web, cocoon, cocoon handling behaviour, draglines and attachment discs. Zoology 106:223–231PubMedCrossRefGoogle Scholar
  69. Hauptmann V, Weichert N, Menzel M, Knoch D, Paege N, Scheller J, Spohn U, Conrad U, Gils M (2013) Native-sized spider silk proteins synthesized in planta via intein-based multimerization. Transgenic Res 22:369–377PubMedCrossRefGoogle Scholar
  70. Hauptmann V, Menzel M, Weichert N, Reimers K, Spohn U, Conrad U (2015) In planta production of ELPylated spidroin-based proteins results in non-cytotoxic biopolymers. BMC Biotechnol 15:9PubMedPubMedCentralCrossRefGoogle Scholar
  71. Hayashi CY, Blackledge TA, Lewis RV (2004) Molecular and mechanical characterization of aciniform silk: uniformity of iterated sequence modules in a novel member of the spider silk fibroin gene family. Mol Biol Evol 21:1950–1959PubMedCrossRefGoogle Scholar
  72. Heidebrecht A, Scheibel T (2013) Recombinant production of spider silk proteins. Adv Appl Microbiol 82:115–153PubMedCrossRefGoogle Scholar
  73. Heidebrecht A, Eisoldt L, Diehl J, Schmidt A, Geffers M, Lang G, Scheibel T (2015) Biomimetic fibers made of recombinant spidroins with the same toughness as natural spider silk. Adv Mater 27:2189–2194PubMedCrossRefGoogle Scholar
  74. Heim M, Keerl D, Scheibel T (2009) Spider silk: from soluble protein to extraordinary fiber. Angew Chem 48:3584–3596CrossRefGoogle Scholar
  75. Heim M, Romer L, Scheibel T (2010) Hierarchical structures made of proteins. The complex architecture of spider webs and their constituent silk proteins. Chem Soc Rev 39:156–164PubMedCrossRefGoogle Scholar
  76. Hepburn HR, Chandler HD, Davidoff MR (1979) Extensometric properties of insect fibroins – green lacewing cross-beta, honeybee alpha-helical and greater waxmoth parallel-beta conformations. Insect Biochem 9:69–77CrossRefGoogle Scholar
  77. Hepburn HR, Kurstjens SP (1988) The combs of honeybees as composite materials. Apidologie 19:25–36CrossRefGoogle Scholar
  78. Hermanson KD, Harasim MB, Scheibel T, Bausch AR (2007a) Permeability of silk microcapsules made by the interfacial adsorption of protein. Phys Chem Chem Phys 9:6442–6446PubMedCrossRefGoogle Scholar
  79. Hermanson KD, Huemmerich D, Scheibel T, Bausch AR (2007b) Engineered microcapsules fabricated from reconstituted spider silk. Adv Mater 19:1810CrossRefGoogle Scholar
  80. Hijirida DH, Do KG, Michal C, Wong S, Zax D, Jelinski LW (1996) 13C NMR of Nephila clavipes major ampullate silk gland. Biophys J 71:3442–3447PubMedPubMedCentralCrossRefGoogle Scholar
  81. Hofer M, Winter G, Myschik J (2012) Recombinant spider silk particles for controlled delivery of protein drugs. Biomaterials 33:1554–1562PubMedCrossRefGoogle Scholar
  82. Holland GP, Jenkins JE, Creager MS, Lewis RV, Yarger JL (2008) Quantifying the fraction of glycine and alanine in beta-sheet and helical conformations in spider dragline silk using solid-state NMR. Chem Commun 43:5568–5570CrossRefGoogle Scholar
  83. Horinek D, Serr A, Geisler M, Pirzer T, Slotta U, Lud SQ, Garrido JA, Scheibel T, Hugel T, Netz RR (2008) Peptide adsorption on a hydrophobic surface results from an interplay of solvation, surface, and intrapeptide forces. Proc Natl Acad Sci U S A 105:2842–2847PubMedPubMedCentralCrossRefGoogle Scholar
  84. Hu X, Yuan J, Wang X, Vasanthavada K, Falick AM, Jones PR, La Mattina C, Vierra CA (2007) Analysis of aqueous glue coating proteins on the silk fibers of the cob weaver, Latrodectus hesperus. Biochemistry 46:3294–3303PubMedCrossRefGoogle Scholar
  85. Huemmerich D, Helsen CW, Quedzuweit S, Oschmann J, Rudolph R, Scheibel T (2004a) Primary structure elements of spider dragline silks and their contribution to protein solubility. Biochemistry 43:13604–13612PubMedCrossRefGoogle Scholar
  86. Huemmerich D, Scheibel T, Vollrath F, Cohen S, Gat U, Ittah S (2004b) Novel assembly properties of recombinant spider dragline silk proteins. Curr Biol 14:2070–2074PubMedCrossRefGoogle Scholar
  87. Inoue S, Tanaka K, Arisaka F, Kimura S, Ohtomo K, Mizuno S (2000) Silk fibroin of Bombyx mori is secreted, assembling a high molecular mass elementary unit consisting of H-chain, L-chain, and P25, with a 6:6:1 molar ratio. J Biol Chem 275:40517–40528PubMedCrossRefGoogle Scholar
  88. Jenkins JE, Creager MS, Butler EB, Lewis RV, Yarger JL, Holland GP (2010) Solid-state NMR evidence for elastin-like beta-turn structure in spider dragline silk. Chem Commun 46:6714–6716CrossRefGoogle Scholar
  89. Johansson J, Nerelius C, Willander H, Presto J (2010) Conformational preferences of non-polar amino acid residues: an additional factor in amyloid formation. Biochem Biophys Res Commun 402:515–518PubMedCrossRefGoogle Scholar
  90. Jones JA, Harris TI, Tucker CL, Berg KR, Christy SY, Day BA, Gaztambide DA, Needham NJ, Ruben AL, Oliveira PF, Decker RE, Lewis RV (2015) More than just fibers: an aqueous method for the production of innovative recombinant spider silk protein materials. Biomacromolecules 16:1418–1425PubMedCrossRefGoogle Scholar
  91. Jonker AM, Lowik DWPM, Van Hest JCM (2012) Peptide- and protein-based hydrogels. Chem Mater 24:759–773CrossRefGoogle Scholar
  92. Junghans F, Morawietz M, Conrad U, Scheibel T, Heilmann A, Spohn U (2006) Preparation and mechanical properties of layers made of recombinant spider silk proteins and silk from silk worm. Appl Phys Mater Sci Process 82:253–260CrossRefGoogle Scholar
  93. Kameda T, Walker AA, Sutherland TD (2014) Evolution and application of coiled coil silks from insects. In: Asakura T, Miller T (eds) Biotechnology of silk. Springer, DordrechtGoogle Scholar
  94. Kamenskiy AV, Dzenis YA, Kazmi SAJ, Pemberton MA, Pipinos II, Phillips NY, Herber K, Woodford T, Bowen RE, Lomneth CS, Mactaggart JN (2014) Biaxial mechanical properties of the human thoracic and abdominal aorta, common carotid, subclavian, renal and common iliac arteries. Biomech Model Mechanobiol 13:1341–1359PubMedCrossRefGoogle Scholar
  95. Khalid A, Lodin R, Domachuk P, Tao H, Moreau JE, Kaplan DL, Omenetto FG, Gibson BC, Tomljenovic-HANIC S (2014) Synthesis and characterization of biocompatible nanodiamond-silk hybrid material. Biomed Opt Express 5:596–608PubMedPubMedCentralCrossRefGoogle Scholar
  96. Kinahan ME, Filippidi E, Koster S, Hu X, Evans HM, Pfohl T, Kaplan DL, Wong J (2011) Tunable silk: using microfluidics to fabricate silk fibers with controllable properties. Biomacromolecules 12:1504–1511PubMedPubMedCentralCrossRefGoogle Scholar
  97. Lammel A, Schwab M, Slotta U, Winter G, Scheibel T (2008) Processing conditions for the formation of spider silk microspheres. ChemSusChem 1:413–416PubMedCrossRefGoogle Scholar
  98. Lammel AS, Hu X, Park SH, Kaplan DL, Scheibel TR (2010) Controlling silk fibroin particle features for drug delivery. Biomaterials 31:4583–4591PubMedPubMedCentralCrossRefGoogle Scholar
  99. Lammel A, Schwab M, Hofer M, Winter G, Scheibel T (2011) Recombinant spider silk particles as drug delivery vehicles. Biomaterials 32:2233–2240PubMedCrossRefGoogle Scholar
  100. Lane DD, Kaur S, Weerasakare GM, Stewart RJ (2015) Toughened hydrogels inspired by aquatic caddisworm silk. Soft Matter 11:6981–6990PubMedCrossRefGoogle Scholar
  101. Lang G, Jokisch S, Scheibel T (2013) Air filter devices including nonwoven meshes of electrospun recombinant spider silk proteins. J Vis Exp 75:e50492Google Scholar
  102. Lazaris A, Arcidiacono S, Huang Y, Zhou JF, Duguay F, Chretien N, Welsh EA, Soares JW, Karatzas CN (2002) Spider silk fibers spun from soluble recombinant silk produced in mammalian cells. Science 295:472–476PubMedCrossRefGoogle Scholar
  103. Leal-Egana A, Lang G, Mauerer C, Wickinghoff J, Weber M, Geimer S, Scheibel T (2012) Interactions of fibroblasts with different morphologies made of an engineered spider silk protein. Adv Eng Mater 14:B67–B75CrossRefGoogle Scholar
  104. Lee PA, Tullman-Ercek D, Georgiou G (2006) The bacterial twin-arginine translocation pathway. Annu Rev Microbiol 60:373–395PubMedPubMedCentralCrossRefGoogle Scholar
  105. Lee H, Rho J, Messersmith PB (2009) Facile conjugation of biomolecules onto surfaces via mussel adhesive protein inspired coatings. Adv Mater 21:431PubMedPubMedCentralCrossRefGoogle Scholar
  106. Lewis RV, Hinman M, Kothakota S, Fournier MJ (1996) Expression and purification of a spider silk protein: a new strategy for producing repetitive proteins. Protein Expr Purif 7:400–406PubMedCrossRefGoogle Scholar
  107. Li JB, Mohwald H, An ZH, Lu G (2005) Molecular assembly of biomimetic microcapsules. Soft Matter 1:259–264CrossRefGoogle Scholar
  108. Li LH, Puhl S, Meinel L, Germershaus O (2014) Silk fibroin layer-by-layer microcapsules for localized gene delivery. Biomaterials 35:7929–7939PubMedCrossRefGoogle Scholar
  109. Liebmann B, Huemmerich D, Scheibel T, Fehr M (2008) Formulation of poorly water-soluble substances using self-assembling spider silk protein. Colloids and Surfaces a-Physicochemical and Engineering Aspects 331:126–132Google Scholar
  110. Lintz ES, Scheibel TR (2013) Dragline, egg stalk and byssus: a comparison of outstanding protein fibers and their potential for developing new materials. Adv Funct Mater 23:4467–4482CrossRefGoogle Scholar
  111. Liu Y, Shao Z, Vollrath F (2005) Relationships between supercontraction and mechanical properties of spider silk. Nat Mater 4:901–905PubMedCrossRefGoogle Scholar
  112. Lucas F, Rudall KM (1968) Extracellular fibrous proteins: the silks. In: Florkin M, Stotz EH (eds) Comprehensive biochemistry. Elsevier, NewYorkGoogle Scholar
  113. Luo J, Zhang LL, Peng QF, Sun MJ, Zhang YP, Shao HL, Hu XC (2014) Tough silk fibers prepared in air using a biomimetic microfluidic chip. Int J Biol Macromol 66:319–324PubMedCrossRefGoogle Scholar
  114. Maa YF, Hsu CC (1997) Feasibility of protein spray coating using a fluid-bed Wurster processor. Biotechnol Bioeng 53:560–566PubMedCrossRefGoogle Scholar
  115. Machado R, Da Costa A, Sencadas V, Garcia-Arevalo C, Costa CM, Padrao J, Gomes A, Lanceros-Mendez S, Rodriguez-Cabello JC, Casal M (2013) Electrospun silk-elastin-like fibre mats for tissue engineering applications. Biomed Mater 8Google Scholar
  116. Madsen B, Shao ZZ, Vollrath F (1999) Variability in the mechanical properties of spider silks on three levels: interspecific, intraspecific and intraindividual. Int J Biol Macromol 24:301–306PubMedCrossRefGoogle Scholar
  117. Maeda S, Kawai T, Obinata M, Fujiwara H, Horiuchi T, Saeki Y, Sato Y, Furusawa M (1985) Production of human alpha-interferon in silkworm using a baculovirus vector. Nature 315:592–594PubMedCrossRefGoogle Scholar
  118. Maitip J, Trueman HE, Kaehler BD, Huttley GA, Chantawannakul P, Sutherland TD (2015) Folding behavior of four silks of giant honey bee reflects the evolutionary conservation of aculeate silk proteins. Insect Biochem Mol Biol 59:72–79PubMedCrossRefGoogle Scholar
  119. Malda J, Visser J, Melchels FP, Jungst T, Hennink WE, Dhert WJA, Groll J, Hutmacher DW (2013) 25th anniversary article: engineering hydrogels for biofabrication. Adv Mater 25:5011–5028PubMedCrossRefGoogle Scholar
  120. Marolt D, Augst A, Freed LE, Vepari C, Fajardo R, Patel N, Gray M, Farley M, Kaplan D, Vunjak-Novakovic G (2006) Bone and cartilage tissue constructs grown using human bone marrow stromal cells, silk scaffolds and rotating bioreactors. Biomaterials 27:6138–6149PubMedCrossRefGoogle Scholar
  121. Marsh RE, Corey RB, Pauling L (1955) An investigation of the structure of silk fibroin. Biochim Biophys Acta 16:1–34PubMedCrossRefGoogle Scholar
  122. Megeed Z, Cappello J, Ghandehari H (2002) Genetically engineered silk-elastinlike protein polymers for controlled drug delivery. Adv Drug Deliv Rev 54:1075–1091PubMedCrossRefGoogle Scholar
  123. Megeed Z, Haider M, Li DQ, O’malley BW, Cappello J, Ghandehari H (2004) In vitro and in vivo evaluation of recombinant silk-elastinlike hydrogels for cancer gene therapy. J Control Release 94:433–445PubMedCrossRefGoogle Scholar
  124. Miao Y, Zhang Y, Nakagaki K, Zhao T, Zhao A, Meng Y, Nakagaki M, Park EY, Maenaka K (2005) Expression of spider flagelliform silk protein in Bombyx mori cell line by a novel Bac-to-Bac/BmNPV baculovirus expression system. Appl Microbiol Biotechnol 71:192–199PubMedCrossRefGoogle Scholar
  125. Mikos AG, Thorsen AJ, Czerwonka LA, Bao Y, Langer R, Winslow DN, Vacanti JP (1994) Preparation and characterization of poly(L-Lactic Acid) foams. Polymer 35:1068–1077CrossRefGoogle Scholar
  126. Moraes ML, Lima LR, Silva RR, Cavicchioli M, Ribeiro SJL (2013) Immunosensor based on immobilization of antigenic peptide NS5A-1 from HCV and silk fibroin in nanostructured films. Langmuir 29:3829–3834PubMedCrossRefGoogle Scholar
  127. Morse JC (1997) Phylogeny of trichoptera. Annu Rev Entomol 42:427–450PubMedCrossRefGoogle Scholar
  128. Nagarajan R, Drew C, Mello CM (2007) Polymer-micelle complex as an aid to electrospinning nanofibers from aqueous solutions. J Phys Chem C 111:16105–16108CrossRefGoogle Scholar
  129. Neuenfeldt M, Scheibel T (2014) Silks from insects: from natural diversity to applications. Insect molecular biology and ecology. CRC Press, Boca RatonGoogle Scholar
  130. Ohshima Y, Suzuki Y (1977) Cloning of the silk fibroin gene and its flanking sequences. Proc Natl Acad Sci U S A 74:5363–5367PubMedPubMedCentralCrossRefGoogle Scholar
  131. Omenetto FG, Kaplan DL (2010) New opportunities for an ancient material. Science 329:528–531PubMedPubMedCentralCrossRefGoogle Scholar
  132. Osaki S (2012) Spider silk violin strings with a unique packing structure generate a soft and profound timbre. Phys Rev Lett 108:154301PubMedCrossRefGoogle Scholar
  133. Papov VV, Diamond TV, Biemann K, Waite JH (1995) Hydroxyarginine-containing polyphenolic proteins in the adhesive plaques of the marine mussel Mytilus edulis. J Biol Chem 270:20183–20192PubMedCrossRefGoogle Scholar
  134. Park WM, Champion JA (2014) Thermally triggered self-assembly of folded proteins into vesicles. J Am Chem Soc 136:17906–17909PubMedCrossRefGoogle Scholar
  135. Parker KD, Rudall KM (1957) The Silk of the egg-stalk of the green lace-wing fly: structure of the silk of chrysopa egg-stalks. Nature 179:905–906CrossRefGoogle Scholar
  136. Parkhe AD, Seeley SK, Gardner K, Thompson L, Lewis RV (1997) Structural studies of spider silk proteins in the fiber. J Mol Recognit : JMR 10:1–6PubMedCrossRefGoogle Scholar
  137. Pilotto F, Filosi M (1977) Relationship between collagen fibril diameters and body size – study of fish derma. Cell Tissue Res 182:119–131PubMedCrossRefGoogle Scholar
  138. Porter D, Guan J, Vollrath F (2013) Spider silk: super material or thin fibre? Adv Mater 25:1275–1279PubMedCrossRefGoogle Scholar
  139. Prince JT, Mcgrath KP, Digirolamo CM, Kaplan DL (1995) Construction, cloning, and expression of synthetic genes encoding spider dragline silk. Biochemistry 34:10879–10885PubMedCrossRefGoogle Scholar
  140. Qiu W, Huang Y, Teng W, Cohn CM, Cappello J, WU X (2010) Complete recombinant silk-elastinlike protein-based tissue scaffold. Biomacromolecules 11:3219–3227PubMedPubMedCentralCrossRefGoogle Scholar
  141. Rabotyagova OS, Cebe P, Kaplan DL (2009) Self-assembly of genetically engineered spider silk block copolymers. Biomacromolecules 10:229–236PubMedCrossRefGoogle Scholar
  142. Rajkhowa R, Hu X, Tsuzuki T, Kaplan DL, Wang X (2012) Structure and biodegradation mechanism of milled Bombyx mori silk particles. Biomacromolecules 13:2503–2512PubMedPubMedCentralCrossRefGoogle Scholar
  143. Rammensee S, Slotta U, Scheibel T, Bausch AR (2008) Assembly mechanism of recombinant spider silk proteins. Proc Natl Acad Sci U S A 105:6590–6595PubMedPubMedCentralCrossRefGoogle Scholar
  144. Raphel J, Parisi-Amon A, Heilshorn SC (2012) Photoreactive elastin-like proteins for use as versatile bioactive materials and surface coatings. J Mater Chem 22:19429–19437PubMedPubMedCentralCrossRefGoogle Scholar
  145. Reneker DH, Yarin AL (2008) Electrospinning jets and polymer nanofibers. Polymer 49:2387–2425CrossRefGoogle Scholar
  146. Riekel C, Vollrath F (2001) Spider silk fibre extrusion: combined wide- and small-angle X-ray microdiffraction experiments. Int J Biol Macromol 29:203–210PubMedCrossRefGoogle Scholar
  147. Rising A, Hjalm G, Engstrom W, Johansson J (2006) N-terminal nonrepetitive domain common to dragline, flagelliform, and cylindriform spider silk proteins. Biomacromolecules 7:3120–3124PubMedCrossRefGoogle Scholar
  148. Römer L, Scheibel T (2008) The elaborate structure of spider silk: structure and function of a natural high performance fiber. Prion 2:154–161PubMedPubMedCentralCrossRefGoogle Scholar
  149. Rosano GL, Ceccarelli EA (2014) Recombinant protein expression in Escherichia coli: advances and challenges. Front Microbiol 5:172PubMedPubMedCentralGoogle Scholar
  150. Rudall KM, Kenchington W (1971) Arthropod silks: the problem of fibrous proteins in animal tissues. Annu Rev Entomol 16:73–96CrossRefGoogle Scholar
  151. Santoso S, Hwang W, Hartman H, Zhang SG (2002) Self-assembly of surfactant-like peptides with variable glycine tails to form nanotubes and nanovesicles. Nano Lett 2:687–691CrossRefGoogle Scholar
  152. Schacht K, Scheibel T (2011) Controlled hydrogel formation of a recombinant spider silk protein. Biomacromolecules 12:2488–2495PubMedCrossRefGoogle Scholar
  153. Schacht K, Jungst T, Schweinlin M, Ewald A, Groll J, Scheibel T (2015) Biofabrication of cell-loaded 3D spider silk constructs. Angewandte Chemie-International Edition 54:2816–2820PubMedCrossRefGoogle Scholar
  154. Schacht K, Vogt J, Scheibel T (2016). Foams made of engineered recombinant spider silk proteins as 3D scaffolds for cell growth. ACS Biomater Sci Eng, dx.doi.org/10.1021/acsbiomaterials.5b00483Google Scholar
  155. Scheibel T (2004) Spider silks: recombinant synthesis, assembly, spinning, and engineering of synthetic proteins. Microb Cell Factories 3:14CrossRefGoogle Scholar
  156. Scheller J, Conrad U (2005) Plant-based material, protein and biodegradable plastic. Curr Opin Plant Biol 8:188–196PubMedCrossRefGoogle Scholar
  157. Scheller J, Guhrs KH, Grosse F, Conrad U (2001) Production of spider silk proteins in tobacco and potato. Nat Biotechnol 19:573–577PubMedCrossRefGoogle Scholar
  158. Scheller J, Henggeler D, Viviani A, Conrad U (2004) Purification of spider silk-elastin from transgenic plants and application for human chondrocyte proliferation. Transgenic Res 13:51–57PubMedCrossRefGoogle Scholar
  159. Sehnal F, Akai H (1990) Insect silk glands: their types, development and function, and effects of environmental factors and morphogenetic hormones on them. Int J Insect Morphol Embryol 19:79–132CrossRefGoogle Scholar
  160. Seidel A, Liivak O, Calve S, Adaska J, Ji GD, Yang ZT, Grubb D, Zax DB, Jelinski LW (2000) Regenerated spider silk: processing, properties, and structure. Macromolecules 33:775–780CrossRefGoogle Scholar
  161. Shchepelina O, Drachuk I, Gupta MK, Lin J, Tsukruk VV (2011) Silk-on-silk layer-by-layer microcapsules. Adv Mater 23:4655PubMedCrossRefGoogle Scholar
  162. Shi J, Lua S, Du N, Liu X, Song J (2008) Identification, recombinant production and structural characterization of four silk proteins from the Asiatic honeybee Apis cerana. Biomaterials 29:2820–2828PubMedCrossRefGoogle Scholar
  163. Silva-Zacarin EC, De Moraes R L S, Taboga SR (2003) Silk formation mechanisms in the larval salivary glands of Apis mellifera (Hymenoptera: Apidae). J Biosci 28:753–764PubMedCrossRefGoogle Scholar
  164. Slotta U, Hess S, Spiess K, Stromer T, Serpell L, Scheibel T (2007) Spider silk and amyloid fibrils: a structural comparison. Macromol Biosci 7:183–188PubMedCrossRefGoogle Scholar
  165. Slotta UK, Rammensee S, Gorb S, Scheibel T (2008) An engineered spider silk protein forms microspheres. Angew Chem Int Ed 47:4592–4594CrossRefGoogle Scholar
  166. Spiess K, Lammel A, Scheibel T (2010) Recombinant spider silk proteins for applications in biomaterials. Macromol Biosci 10:998–1007PubMedCrossRefGoogle Scholar
  167. Spiess K, Ene R, Keenan CD, Senker J, Kremer F, Scheibel T (2011) Impact of initial solvent on thermal stability and mechanical properties of recombinant spider silk films. J Mater Chem 21:13594–13604CrossRefGoogle Scholar
  168. Sponner A, Schlott B, Vollrath F, Unger E, Grosse F, Weisshart K (2005) Characterization of the protein components of Nephila clavipes dragline silk. Biochemistry 44:4727–4736PubMedCrossRefGoogle Scholar
  169. Stephens JS, Fahnestock SR, Farmer RS, Kiick KL, Chase DB, Rabolt JF (2005) Effects of electrospinning and solution casting protocols on the secondary structure of a genetically engineered dragline spider silk analogue investigated via fourier transform Raman spectroscopy. Biomacromolecules 6:1405–1413PubMedCrossRefGoogle Scholar
  170. Stewart RJ (2011) Protein-based underwater adhesives and the prospects for their biotechnological production. Appl Microbiol Biotechnol 89:27–33PubMedCrossRefGoogle Scholar
  171. Stewart RJ, Wang CS (2010) Adaptation of caddisfly larval silks to aquatic habitats by phosphorylation of h-fibroin serines. Biomacromolecules 11:969–974PubMedCrossRefGoogle Scholar
  172. Sun W, Yu H, Shen Y, Banno Y, Xiang Z, Zhang Z (2012) Phylogeny and evolutionary history of the silkworm. Sci China Life Sci 55:483–496PubMedCrossRefGoogle Scholar
  173. Sundaray B, Subramanian V, Natarajan TS, Xiang RZ, Chang CC, Fann WS (2004) Electrospinning of continuous aligned polymer fibers. Appl Phys Lett 84:1222–1224CrossRefGoogle Scholar
  174. Sutherland TD, Campbell PM, Weisman S, Trueman HE, Sriskantha A, Wanjura WJ, Haritos VS (2006) A highly divergent gene cluster in honey bees encodes a novel silk family. Genome Res 16:1414–1421PubMedPubMedCentralCrossRefGoogle Scholar
  175. Sutherland TD, Weisman S, Trueman HE, Sriskantha A, Trueman JW, Haritos VS (2007) Conservation of essential design features in coiled coil silks. Mol Biol Evol 24:2424–2432PubMedCrossRefGoogle Scholar
  176. Sutherland TD, Young JH, Weisman S, Hayashi CY, Merritt DJ (2010) Insect silk: one name, many materials. Annu Rev Entomol 55:171–188PubMedCrossRefGoogle Scholar
  177. Sutherland TD, Weisman S, Walker AA, Mudie ST (2012) The coiled coil silk of bees, ants, and hornets. Biopolymers 97:446–454PubMedCrossRefGoogle Scholar
  178. Sutherland TD, Trueman HE, Walker AA, Weisman S, Campbell PM, Dong Z, Huson MG, Woodhead AL, Church JS (2014) Convergently-evolved structural anomalies in the coiled coil domains of insect silk proteins. J Struct Biol 186:402–411PubMedCrossRefGoogle Scholar
  179. Tamada Y (2005) New process to form a silk fibroin porous 3-D structure. Biomacromolecules 6:3100–3106PubMedCrossRefGoogle Scholar
  180. Tamura T, Thibert C, Royer C, Kanda T, Abraham E, Kamba M, Komoto N, Thomas JL, Mauchamp B, Chavancy G, Shirk P, Fraser M, Prudhomme JC, Couble P (2000) Germline transformation of the silkworm Bombyx mori L. using a piggyBac transposon-derived vector. Nat Biotechnol 18:81–84PubMedCrossRefGoogle Scholar
  181. Tanaka K, Mori K, Mizuno S (1993) Immunological identification of the major disulfide-linked light component of silk fibroin. J Biochem 114:1–4PubMedGoogle Scholar
  182. Tanaka K, Inoue S, Mizuno S (1999a) Hydrophobic interaction of P25, containing Asn-linked oligosaccharide chains, with the H-L complex of silk fibroin produced by Bombyx mori. Insect Biochem Mol Biol 29:269–276PubMedCrossRefGoogle Scholar
  183. Tanaka K, Kajiyama N, Ishikura K, Waga S, Kikuchi A, Ohtomo K, Takagi T, Mizuno S (1999b) Determination of the site of disulfide linkage between heavy and light chains of silk fibroin produced by Bombyx mori. Biochim Biophys Acta 1432:92–103PubMedCrossRefGoogle Scholar
  184. Teng W, Huang Y, Cappello J, Wu X (2011) Optically transparent recombinant silk-elastinlike protein polymer films. J Phys Chem B 115:1608–1615PubMedPubMedCentralCrossRefGoogle Scholar
  185. Tokareva O, Michalczechen-Lacerda VA, Rech EL, Kaplan DL (2013) Recombinant DNA production of spider silk proteins. Microb Biotechnol 6:651–663PubMedPubMedCentralCrossRefGoogle Scholar
  186. Tomita M (2011) Transgenic silkworms that weave recombinant proteins into silk cocoons. Biotechnol Lett 33:645–654PubMedCrossRefGoogle Scholar
  187. Tsukada M, Khan MM, Inoue E, Kimura G, Hun JY, Mishima M, Hirabayashi K (2010) Physical properties and structure of aquatic silk fiber from Stenopsyche marmorata. Int J Biol Macromol 46:54–58PubMedCrossRefGoogle Scholar
  188. Tucker CL, Jones JA, Bringhurst HN, Copeland CG, Addison JB, Weber WS, Mou Q, Yarger JL, Lewis RV (2014) Mechanical and physical properties of recombinant spider silk films using organic and aqueous solvents. Biomacromolecules 15:3158–3170PubMedPubMedCentralCrossRefGoogle Scholar
  189. Van Beek JD, Hess S, Vollrath F, Meier BH (2002) The molecular structure of spider dragline silk: Folding and orientation of the protein backbone. Proc Natl Acad Sci U S A 99:10266–10271PubMedPubMedCentralCrossRefGoogle Scholar
  190. Vasconcelos A, Freddi G, Cavaco-Paulo A (2008) Biodegradable materials based on silk fibroin and keratin. Biomacromolecules 9:1299–1305PubMedCrossRefGoogle Scholar
  191. Vauthey S, Santoso S, Gong HY, Watson N, Zhang SG (2002) Molecular self-assembly of surfactant-like peptides to form nanotubes and nanovesicles. Proc Natl Acad Sci U S A 99:5355–5360PubMedPubMedCentralCrossRefGoogle Scholar
  192. Vendrely C, Scheibel T (2007) Biotechnological production of spider-silk proteins enables new applications. Macromol Biosci 7:401–409PubMedCrossRefGoogle Scholar
  193. Vepari C, Kaplan DL (2007) Silk as a biomaterial. Prog Polym Sci 32:991–1007PubMedPubMedCentralCrossRefGoogle Scholar
  194. Vollrath F (2000) Strength and structure of spiders silks. J Biotechnol 74:67–83PubMedGoogle Scholar
  195. Vollrath F (2006) Spider silk: thousands of nano-filaments and dollops of sticky glue. Curr Biol : CB 16:R925–R927PubMedCrossRefGoogle Scholar
  196. Vollrath F, Knight DP (2001) Liquid crystalline spinning of spider silk. Nature 410:541–548PubMedCrossRefGoogle Scholar
  197. Vollrath F, Porter D (2006) Spider silk as archetypal protein elastomer. Soft Matter 2:377–385CrossRefGoogle Scholar
  198. Wang YZ, Kim UJ, Blasioli DJ, Kim HJ, Kaplan DL (2005) In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells. Biomaterials 26:7082–7094PubMedCrossRefGoogle Scholar
  199. Wang Y, Sanai K, Wen H, Zhao T, Nakagaki M (2010) Characterization of unique heavy chain fibroin filaments spun underwater by the caddisfly Stenopsyche marmorata (Trichoptera; Stenopsychidae). Mol Biol Rep 37:2885–2892PubMedCrossRefGoogle Scholar
  200. Wang CS, Ashton NN, Weiss RB, Stewart RJ (2014) Peroxinectin catalyzed dityrosine crosslinking in the adhesive underwater silk of a casemaker caddisfly larvae, Hysperophylax occidentalis. Insect Biochem Mol Biol 54:69–79PubMedCrossRefGoogle Scholar
  201. Weichert N, Hauptmann V, Helmold C, Conrad U (2016) Seed-specific expression of spider silk protein multimers causes long-term stability. Front Plant Sci 7:6PubMedPubMedCentralCrossRefGoogle Scholar
  202. Weisman S, Trueman HE, Mudie ST, Church JS, Sutherland TD, Haritos VS (2008) An unlikely silk: the composite material of green lacewing cocoons. Biomacromolecules 9:3065–3069PubMedCrossRefGoogle Scholar
  203. Weisman S, Okada S, Mudie ST, Huson MG, Trueman HE, Sriskantha A, Haritos VS, Sutherland TD (2009) Fifty years later: the sequence, structure and function of lacewing cross-beta silk. J Struct Biol 168:467–475PubMedCrossRefGoogle Scholar
  204. Weisman S, Haritos VS, Church JS, Huson MG, Mudie ST, Rodgers AJ, Dumsday GJ, Sutherland TD (2010) Honeybee silk: recombinant protein production, assembly and fiber spinning. Biomaterials 31:2695–2700PubMedCrossRefGoogle Scholar
  205. Wen H, Lan X, Zhang Y, Zhao T, Wang Y, Kajiura Z, Nakagaki M (2010) Transgenic silkworms (Bombyx mori) produce recombinant spider dragline silk in cocoons. Mol Biol Rep 37:1815–1821PubMedCrossRefGoogle Scholar
  206. Widmaier DM, Tullman-Ercek D, Mirsky EA, Hill R, Govindarajan S, Minshull J, Voigt CA (2009) Engineering the Salmonella type III secretion system to export spider silk monomers. Mol Syst Biol 5:309PubMedPubMedCentralCrossRefGoogle Scholar
  207. Wiggins GB (2004) Caddisflies: the underwater architects. University of Toronto Press, TorontoGoogle Scholar
  208. Wittmer CR, Hu X, Gauthier PC, Weisman S, Kaplan DL, Sutherland TD (2011) Production, structure and in vitro degradation of electrospun honeybee silk nanofibers. Acta Biomater 7:3789–3795PubMedPubMedCentralCrossRefGoogle Scholar
  209. Wohlrab S, Spieß K, Scheibel T (2012) Varying surface hydrophobicities of coatings made of recombinant spider silk proteins. J Mater Chem 22:22050–22054CrossRefGoogle Scholar
  210. Woolfson DN (2005) The design of coiled-coil structures and assemblies. Adv Protein Chem 70:79–112PubMedCrossRefGoogle Scholar
  211. Xia XX, Qian ZG, Ki CS, Park YH, Kaplan DL, Lee SY (2010) Native-sized recombinant spider silk protein produced in metabolically engineered Escherichia coli results in a strong fiber. Proc Natl Acad Sci USA 107:14059–14063PubMedPubMedCentralCrossRefGoogle Scholar
  212. Xu H (2014) The advances and perspectives of recombinant protein production in the silk gland of silkworm Bombyx mori. Transgenic Res 23:697–706PubMedCrossRefGoogle Scholar
  213. Xu HT, Fan BL, Yu SY, Huang YH, Zhao ZH, Lian ZX, DAI YP, Wang LL, Liu ZL, Fei J, Li N (2007) Construct synthetic gene encoding artificial spider dragline silk protein and its expression in milk of transgenic mice. Anim Biotechnol 18:1–12PubMedCrossRefGoogle Scholar
  214. Xu L, Tremblay ML, Orrell KE, Leclerc J, Meng Q, Liu XQ, Rainey JK (2013) Nanoparticle self-assembly by a highly stable recombinant spider wrapping silk protein subunit. FEBS Lett 587:3273–3280PubMedCrossRefGoogle Scholar
  215. Yamaguchi K, Kikuchi Y, Takagi T, Kikuchi A, Oyama F, Shimura K, Mizuno S (1989) Primary structure of the silk fibroin light chain determined by cDNA sequencing and peptide analysis. J Mol Biol 210:127–139PubMedCrossRefGoogle Scholar
  216. Yanagisawa S, Zhu Z, Kobayashi I, Uchino K, Tamada Y, Tamura T, Asakura T (2007) Improving cell-adhesive properties of recombinant Bombyx mori silk by incorporation of collagen or fibronectin derived peptides produced by transgenic silkworms. Biomacromolecules 8:3487–3492PubMedCrossRefGoogle Scholar
  217. Yang M, Tanaka C, Yamauchi K, Ohgo K, Kurokawa M, Asakura T (2008) Silklike materials constructed from sequences of Bombyx mori silk fibroin, fibronectin, and elastin. J Biomed Mater Res A 84:353–363PubMedCrossRefGoogle Scholar
  218. Yao J, Yanagisawa S, asakura T (2004) Design, expression and characterization of collagen-like proteins based on the cell adhesive and crosslinking sequences derived from native collagens. J Biochem 136:643–649PubMedCrossRefGoogle Scholar
  219. Yonemura N, Sehnal F, Mita K, Tamura T (2006) Protein composition of silk filaments spun under water by caddisfly larvae. Biomacromolecules 7:3370–3378PubMedCrossRefGoogle Scholar
  220. Young SL, Gupta M, Hanske C, Fery A, Scheibel T, Tsukruk VV (2012) Utilizing conformational changes for patterning thin films of recombinant spider silk proteins. Biomacromolecules 13:3189–3199PubMedCrossRefGoogle Scholar
  221. Yucel T, Cebe P, Kaplan DL (2009) Vortex-induced injectable silk fibroin hydrogels. Biophys J 97:2044–2050PubMedPubMedCentralCrossRefGoogle Scholar
  222. Zeplin PH, Berninger AK, Maksimovikj NC, Van Gelder P, Scheibel T, Walles H (2014a) Improving the biocompatibility of silicone implants using spider silk coatings: immunohistochemical analysis of capsule formation. Handchir Mikrochir Plast Chir 46:336–341PubMedCrossRefGoogle Scholar
  223. Zeplin PH, Maksimovikj NC, Jordan MC, Nickel J, Lang G, Leimer AH, Roemer L, Scheibel T (2014b) Spider silk coatings as a bioshield to reduce periprosthetic fibrous capsule formation. Adv Funct Mater 24:2658–2666CrossRefGoogle Scholar
  224. Zhang Y, Hu J, Miao Y, Zhao A, Zhao T, Wu D, Liang L, Miikura A, Shiomi K, Kajiura Z, Nakagaki M (2008) Expression of EGFP-spider dragline silk fusion protein in BmN cells and larvae of silkworm showed the solubility is primary limit for dragline proteins yield. Mol Biol Rep 35:329–335PubMedCrossRefGoogle Scholar
  225. Zhang K, Duan H, Karihaloo BL, Wang J (2010) Hierarchical, multilayered cell walls reinforced by recycled silk cocoons enhance the structural integrity of honeybee combs. Proc Natl Acad Sci U S A 107:9502–9506PubMedPubMedCentralCrossRefGoogle Scholar
  226. Zhao QH, Li BY (2008) pH-controlled drug loading and release from biodegradable microcapsules. Nanomed Nanotechnol Biol Med 4:302–310CrossRefGoogle Scholar
  227. Zhou CZ, Confalonieri F, Jacquet M, Perasso R, LI ZG, Janin J (2001) Silk fibroin: structural implications of a remarkable amino acid sequence. Proteins 44:119–122PubMedCrossRefGoogle Scholar
  228. Zhu JM, Marchant RE (2011) Design properties of hydrogel tissue-engineering scaffolds. Expert Rev Med Devices 8:607–626PubMedPubMedCentralCrossRefGoogle Scholar
  229. Zhu B, Wang H, Leow WR, Cai Y, Loh XJ, Han MY, Chen X (2015) Silk fibroin for flexible electronic devices. Adv Mater 28(22):4250–4265PubMedCrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Research Group Biopolymer ProcessingUniversity of BayreuthBayreuthGermany
  2. 2.Department of BiomaterialsUniversity of BayreuthBayreuthGermany

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