Advertisement

Applied Microbiology and Biotechnology

, Volume 99, Issue 22, pp 9361–9380 | Cite as

To spin or not to spin: spider silk fibers and more

  • Elena Doblhofer
  • Aniela Heidebrecht
  • Thomas ScheibelEmail author
Mini-Review

Abstract

Spider silk fibers have a sophisticated hierarchical structure composed of proteins with highly repetitive sequences. Their extraordinary mechanical properties, defined by a unique combination of strength and extensibility, are superior to most man-made fibers. Therefore, spider silk has fascinated mankind for thousands of years. However, due to their aggressive territorial behavior, farming of spiders is not feasible on a large scale. For this reason, biotechnological approaches were recently developed for the production of recombinant spider silk proteins. These recombinant proteins can be assembled into a variety of morphologies with a great range of properties for technical and medical applications. Here, the different approaches of biotechnological production and the advances in material processing toward various applications will be reviewed.

Keywords

Spider silk Recombinant protein production Protein morphologies 

Notes

Acknowledgments

We kindly thank Elise DeSimone for proofreading the manuscript. A.H. kindly appreciates the financial support by the “Universität Bayern, e.V., Graduiertenförderung nach dem bayerischen Eliteförderungsgesetz.” This work was financially supported by DFG grant SFB 840 TP A8 (to T.S.), DFG SCHE 603/4, and the Technologie Allianz Oberfranken (TAO).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethics approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 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 14:1751–1760. doi: 10.1021/bm400125w PubMedPubMedCentralCrossRefGoogle Scholar
  2. 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 29:225–234. doi: 10.1016/j.jmbbm.2013.09.002 PubMedCrossRefGoogle Scholar
  3. Allmeling C, Jokuszies A, Reimers K, Kall S, Vogt PM (2006) Use of spider silk fibres as an innovative material in a biocompatible artificial nerve conduit. J Cell Mol Med 10:770–777. doi: 10.2755/jcmm010.003.18 PubMedCrossRefGoogle Scholar
  4. Allmeling C, Jokuszies A, Reimers K, Kall S, Choi CY, Brandes G, Kasper C, Scheper T, Guggenheim M, Vogt PM (2008) Spider silk fibres in artificial nerve constructs promote peripheral nerve regeneration. Cell Prolif 41:408–420. doi: 10.1111/j.1365-2184.2008.00534.x PubMedCrossRefGoogle Scholar
  5. Altman GH, Diaz F, Jakuba C, Calabro T, Horan RL, Chen J, Lu H, Richmond J, Kaplan DL (2003) Silk-based biomaterials. Biomaterials 24:401–416. doi: 10.1016/S0142-9612(02)00353-8 PubMedCrossRefGoogle Scholar
  6. 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 12:2375–2381. doi: 10.1021/bm200463e PubMedPubMedCentralCrossRefGoogle Scholar
  7. Andersen SO (1970) Amino acid composition of spider silks. Comp Biochem Physiol 35:705–711. doi: 10.1016/0010-406X(70)90988-6 CrossRefGoogle Scholar
  8. Andersson M, Chen G, Otikovs M, Landreh M, Nordling K, Kronqvist N, Westermark P, Jornvall H, Knight S, Ridderstrale Y, Holm L, Meng Q, Jaudzems K, Chesler M, Johansson J, Rising A (2014) Carbonic anhydrase generates CO2 and H+ that drive spider silk formation via opposite effects on the terminal domains. PLoS Biol 12:e1001921. doi: 10.1371/journal.pbio.1001921 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Arcidiacono S, Mello CM, Butler M, Welsh E, Soares JW, Allen A, Ziegler D, Laue T, Chase S (2002) Aqueous processing and fiber spinning of recombinant spider silks. Macromolecules 35:1262–1266. doi: 10.1021/Ma011471o CrossRefGoogle Scholar
  10. 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:e514. doi: 10.1371/journal.pone.0000514 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Baoyong L, Jian Z, Denglong C, Min L (2010) Evaluation of a new type of wound dressing made from recombinant spider silk protein using rat models. Burns 36:891–896. doi: 10.1016/j.burns.2009.12.001 PubMedCrossRefGoogle Scholar
  12. Barr LA, Fahnestock SR, Yang JJ (2004) Production and purification of recombinant DP1B silk-like protein in plants. Mol Breed 13:345–356. doi: 10.1016/j.burns.2009.12.001 CrossRefGoogle Scholar
  13. Bauer F, Wohlrab S, Scheibel T (2013) Controllable cell adhesion, growth and orientation on layered silk protein films. Biomater Sci 1:1244–1249. doi: 10.1039/C3bm60114e CrossRefGoogle Scholar
  14. Belton DJ, Mieszawska AJ, Currie HA, Kaplan DL, Perry CC (2012) Silk-silica composites from genetically engineered chimeric proteins: materials properties correlate with silica condensation rate and colloidal stability of the proteins in aqueous solution. Langmuir 28:4373–4381. doi: 10.1021/La205084z PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bettinger CJ, Bao Z (2010) Biomaterials-based organic electronic devices. Polym Int 59:563–567. doi: 10.1002/pi.2827 PubMedPubMedCentralGoogle Scholar
  16. Bini E, Foo CW, Huang J, Karageorgiou V, Kitchel B, Kaplan DL (2006) RGD-functionalized bioengineered spider dragline silk biomaterial. Biomacromolecules 7:3139–3145. doi: 10.1021/bm0607877 PubMedCrossRefGoogle Scholar
  17. Blackledge TA, Hayashi CY (2006) Silken toolkits: biomechanics of silk fibers spun by the orb web spider Argiope argentata (Fabricius 1775). J Exp Biol 209:2452–2461. doi: 10.1242/jeb.02275 PubMedCrossRefGoogle Scholar
  18. Blond D, McCarthy DN, Blau WJ, Coleman JN (2007) Toughening of artificial silk by incorporation of carbon nanotubes. Biomacromolecules 8:3973–3976. doi: 10.1021/Bm700971g PubMedCrossRefGoogle Scholar
  19. Blüm C, Scheibel T (2012) Control of drug loading and release properties of spider silk sub-microparticles. J Bionanosci 2:67–74. doi: 10.1007/s12668-012-0036-7 CrossRefGoogle Scholar
  20. Bogush VG, Sokolova OS, Davydova LI, Klinov DV, Sidoruk KV, Esipova NG, Neretina TV, Orchanskyi IA, Makeev VY, Tumanyan VG, Shaitan KV, Debabov VG, Kirpichnikov MP (2009) A novel model system for design of biomaterials based on recombinant analogs of spider silk proteins. J Neuroimmune Pharmacol 4:17–27. doi: 10.1007/s11481-008-9129-z PubMedCrossRefGoogle Scholar
  21. Bon M (1710) A discourse upon the usefulness of the silk of spiders. By Monsieur Bon, President of the Court of Accounts, Aydes and Finances, and President of the Royal Society of Sciences at Montpellier. Communicated by the author. Philos Trans R Soc London 27:2–16. doi:10.1098/rstl.1710.0001Google Scholar
  22. Borkner CB, Elsner MB, Scheibel T (2014) Coatings and films made of silk proteins. ACS Appl Mater Interfaces 6:15611–15625. doi: 10.1021/Am5008479 PubMedCrossRefGoogle Scholar
  23. Brooks AE, Stricker SM, Joshi SB, Kamerzell TJ, Middaugh CR, Lewis RV (2008) Properties of synthetic spider silk fibers based on Argiope aurantia MaSp2. Biomacromolecules 9:1506–1510. doi: 10.1021/bm701124p PubMedCrossRefGoogle Scholar
  24. Brown CP, Harnagea C, Gill HS, Price AJ, Traversa E, Licoccia S, Rosei F (2012) Rough fibrils provide a toughening mechanism in biological fibers. ACS Nano 6:1961–1969. doi: 10.1021/nn300130q PubMedCrossRefGoogle Scholar
  25. Cao B, Mao C (2007) Oriented nucleation of hydroxylapatite crystals on spider dragline silks. Langmuir 23:10701–10705. doi: 10.1021/la7014435 PubMedCrossRefGoogle Scholar
  26. Cary LC, Goebel M, Corsaro BG, Wang HG, Rosen E, Fraser MJ (1989) Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology 172:156–169. doi: 10.1016/0042-6822(89)90117-7 PubMedCrossRefGoogle Scholar
  27. Challis RJ, Goodacre SL, Hewitt GM (2006) Evolution of spider silks: conservation and diversification of the C-terminus. Insect Mol Biol 15:45–56. doi: 10.1111/j.1365-2583.2005.00606.x PubMedCrossRefGoogle Scholar
  28. Chen X, Knight DP, Shao ZZ, Vollrath F (2002) Conformation transition in silk protein films monitored by time-resolved Fourier transform infrared spectroscopy: effect of potassium ions on Nephila spidroin films. Biochemistry 41:14944–14950. doi: 10.1021/Bi026550m PubMedCrossRefGoogle Scholar
  29. Craig CL, Riekel C, Herberstein ME, Weber RS, Kaplan D, Pierce NE (2000) Evidence for diet effects on the composition of silk proteins produced by spiders. Mol Biol Evol 17:1904–1913PubMedCrossRefGoogle Scholar
  30. Denny M (1976) Physical properties of spiders silk and their role in design of orb-webs. J Exp Biol 65:483–506Google Scholar
  31. Doblhofer E, Scheibel T (2015) Engineering of recombinant spider silk proteins allows defined uptake and release of substances. J Pharm Sci 104:988–994. doi: 10.1002/jps.24300 PubMedCrossRefGoogle Scholar
  32. Eisoldt L, Hardy JG, Heim M, Scheibel TR (2010) The role of salt and shear on the storage and assembly of spider silk proteins. J Struct Biol 170:413–419. doi: 10.1016/j.jsb.2009.12.027 PubMedCrossRefGoogle Scholar
  33. Eisoldt L, Smith A, Scheibel T (2011) Decoding the secrets of spider silk. Mater Today 14:80–86. doi: 10.1016/S1369-7021(11)70057-8 CrossRefGoogle Scholar
  34. Eisoldt L, Thamm C, Scheibel T (2012) The role of terminal domains during storage and assembly of spider silk proteins. Biopolymers 97:355–361. doi: 10.1002/bip.22006 PubMedCrossRefGoogle Scholar
  35. Elsner MB, Herold HM, Muller-Herrmann S, Bargel H, Scheibel T (2015) Enhanced cellular uptake of engineered spider silk particles. Biomater Sci 3:543–551. doi: 10.1039/C4bm00401a PubMedCrossRefGoogle Scholar
  36. Exler JH, Hummerich D, Scheibel T (2007) The amphiphilic properties of spider silks are important for spinning. Angew Chem Int Ed 46:3559–3562. doi: 10.1002/anie.200604718 CrossRefGoogle Scholar
  37. Fahnestock SR, Bedzyk LA (1997) Production of synthetic spider dragline silk protein in Pichia pastoris. Appl Microbiol Biotechnol 47:33–39PubMedCrossRefGoogle Scholar
  38. Fahnestock SR, Irwin SL (1997) Synthetic spider dragline silk proteins and their production in Escherichia coli. Appl Microbiol Biotechnol 47:23–32PubMedCrossRefGoogle Scholar
  39. Fahnestock SR, Yao Z, Bedzyk LA (2000) Microbial production of spider silk proteins. Rev Mol Biotechnol 74:105–119. doi: 10.1016/S1389-0352(00)00008-8 CrossRefGoogle Scholar
  40. Foo CWP, Patwardhan SV, Belton DJ, Kitchel B, Anastasiades D, Huang J, Naik RR, Perry CC, Kaplan DL (2006) Novel nanocomposites from spider silk-silica fusion (chimeric) proteins. Proc Natl Acad Sci U S A 103:9428–9433. doi: 10.1073/pnas.0601096103 CrossRefGoogle Scholar
  41. Fox LR (1975) Cannibalism in natural populations. Annu Rev Ecol Syst 6:87–106CrossRefGoogle Scholar
  42. Fredriksson C, Hedhammar M, Feinstein R, Nordling K, Kratz G, Johansson J, Huss F, Rising A (2009) Tissue response to subcutaneously implanted recombinant spider silk: an in vivo study. Materials 2:1908–1922. doi: 10.3390/Ma2041908 CrossRefGoogle Scholar
  43. Gellynck K, Verdonk P, Forsyth R, Almqvist KF, Van Nimmen E, Gheysens T, Mertens J, Van Langenhove L, Kiekens P, Verbruggen G (2008a) Biocompatibility and biodegradability of spider egg sac silk. J Mater Sci Mater Med 19:2963–2970. doi: 10.1007/s10856-007-3330-0 PubMedCrossRefGoogle Scholar
  44. Gellynck K, Verdonk PCM, Van Nimmen E, Almqvist KF, Gheysens T, Schoukens G, Van Langenhove L, Kiekens P, Mertens J, Verbruggen G (2008b) Silkworm and spider silk scaffolds for chondrocyte support. J Mater Sci Mater Med 19:3399–3409. doi: 10.1007/s10856-008-3474-6 PubMedCrossRefGoogle Scholar
  45. George M, Abraham TE (2006) Polyionic hydrocolloids for the intestinal delivery of protein drugs: alginate and chitosan—a review. J Control Release 114:1–14. doi: 10.1016/j.jconrel.2006.04.017 PubMedCrossRefGoogle Scholar
  46. Gerritsen VB (2002) The tiptoe of an airbus. Protein Spotlight Swiss Prot 24:1–2Google Scholar
  47. 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
  48. Greiner A, Wendorff JH (2007) Electrospinning: a fascinating method for the preparation of ultrathin fibres. Angew Chem Int Ed 46:5670–5703. doi: 10.1002/anie.200604646 CrossRefGoogle Scholar
  49. Greiner A, Wendorff JH, Yarin AL, Zussman E (2006) Biohybrid nanosystems with polymer nanofibers and nanotubes. Appl Microbiol Biotechnol 71:387–393. doi: 10.1007/s00253-006-0356-z PubMedCrossRefGoogle Scholar
  50. Grip S, Johansson J, Hedhammar M (2009) Engineered disulfides improve mechanical properties of recombinant spider silk. Protein Sci 18:1012–1022. doi: 10.1002/Pro.111 PubMedPubMedCentralCrossRefGoogle Scholar
  51. 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 465:239–242. doi: 10.1038/Nature08936 PubMedCrossRefGoogle Scholar
  52. 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 Int Ed 50:310–313. doi: 10.1002/anie.201003795 CrossRefGoogle Scholar
  53. Hakimi O, Gheysens T, Vollrath F, Grahn MF, Knight DP, Vadgama P (2010) Modulation of cell growth on exposure to silkworm and spider silk fibers. J Biomed Mater Res A 92:1366–1372. doi: 10.1002/jbm.a.32462 PubMedGoogle Scholar
  54. Hardy JG, Scheibel TR (2010) Composite materials based on silk proteins. Prog Polym Sci 35:1093–1115. doi: 10.1016/j.progpolymsci.2010.04.005 CrossRefGoogle Scholar
  55. Hardy JG, Romer LM, Scheibel TR (2008) Polymeric materials based on silk proteins. Polymer 49:4309–4327. doi: 10.1016/j.polymer.2008.08.006 CrossRefGoogle Scholar
  56. Hardy JG, Leal-Eganã A, Scheibel T (2013) Engineered spider silk protein-based composites for drug delivery. Macromol Biosci 13:1431–1437. doi: 10.1002/mabi.201300233 PubMedCrossRefGoogle Scholar
  57. Hauptmann V, Weichert N, Rakhimova M, Conrad U (2013) Spider silks from plants—a challenge to create native-sized spidroins. Biotechnol J 8:1183–1192. doi: 10.1002/biot.201300204 PubMedCrossRefGoogle Scholar
  58. Hayashi CY, Shipley NH, Lewis RV (1999) Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins. Int J Biol Macromol 24:271–275. doi: 10.1016/S0141-8130(98)00089-0 PubMedCrossRefGoogle Scholar
  59. Hedhammar M, Rising A, Grip S, Martinez AS, Nordling K, Casals C, Stark M, Johansson J (2008) Structural properties of recombinant nonrepetitive and repetitive parts of major ampullate spidroin 1 from Euprosthenops australis: implications for fiber formation. Biochemistry 47:3407–3417. doi: 10.1021/bi702432y PubMedCrossRefGoogle Scholar
  60. Heidebrecht A, Scheibel T (2013) Recombinant production of spider silk proteins. Adv Appl Microbiol 82:115–153PubMedCrossRefGoogle Scholar
  61. 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 27:2189–2194. doi: 10.1002/adma.201404234 PubMedCrossRefGoogle Scholar
  62. Heim M, Keerl D, Scheibel T (2009) Spider silk: from soluble protein to extraordinary fiber. Angew Chem Int Ed 48:3584–3596. doi: 10.1002/anie.200803341 CrossRefGoogle Scholar
  63. Helfricht N, Klug M, Mark A, Kuznetsov V, Blum C, Scheibel T, Papastavrou G (2013) Surface properties of spider silk particles in solution. Biomater Sci 1:1166–1171. doi: 10.1039/c3bm60109a CrossRefGoogle Scholar
  64. Hermanson KD, Huemmerich D, Scheibel T, Bausch AR (2007) Engineered microcapsules fabricated from reconstituted spider silk. Adv Mater 19:1810–1815. doi: 10.1002/adma.200602709 CrossRefGoogle Scholar
  65. Hinman MB, Lewis RV (1992) Isolation of a clone encoding a second dragline silk fibroin. Nephila clavipes dragline silk is a two-protein fiber. J Biol Chem 267:19320–19324PubMedGoogle Scholar
  66. Hinman MB, Jones JA, Lewis RV (2000) Synthetic spider silk: a modular fiber. Trends Biotechnol 18:374–379. doi: 10.1016/S0167-7799(00)01481-5 PubMedCrossRefGoogle Scholar
  67. Hofer M, Winter G, Myschik J (2012) Recombinant spider silk particles for controlled delivery of protein drugs. Biomaterials 33:1554–1562. doi: 10.1016/j.biomaterials.2011.10.053 PubMedCrossRefGoogle Scholar
  68. Hu X, Lu Q, Sun L, Cebe P, Wang X, Zhang X, Kaplan DL (2010) Biomaterials from ultrasonication-induced silk fibroin-hyaluronic acid hydrogels. Biomacromolecules 11:3178–3188. doi: 10.1021/bm1010504 PubMedCrossRefGoogle Scholar
  69. Huang J, Wong C, George A, Kaplan DL (2007) The effect of genetically engineered spider silk-dentin matrix protein 1 chimeric protein on hydroxyapatite nucleation. Biomaterials 28:2358–2367. doi: 10.1016/j.biomaterials.2006.11.021 PubMedCrossRefGoogle Scholar
  70. 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 43:13604–13612. doi: 10.1021/Bi048983q PubMedCrossRefGoogle Scholar
  71. Huemmerich D, Scheibel T, Vollrath F, Cohen S, Gat U, Ittah S (2004b) Novel assembly properties of recombinant spider dragline silk proteins. Curr Biol 14:2070–2074. doi: 10.1016/j.cub.2004.11.005 PubMedCrossRefGoogle Scholar
  72. Huemmerich D, Slotta U, Scheibel T (2006) Processing and modification of films made from recombinant spider silk proteins. Appl Phys A Mater Sci Process 82:219–222. doi: 10.1007/s00339-005-3428-5 CrossRefGoogle Scholar
  73. Jestin S, Poulin P (2014) Chapter 6—wet spinning of CNT-based fibers. In: Yin Z, Schulz MJ, Shanov VN (eds) Nanotube superfiber materials. William Andrew Publishing, Boston, pp 167–209. doi: 10.1016/B978-1-4557-7863-8.00006-2 CrossRefGoogle Scholar
  74. Jiang C, Wang X, Gunawidjaja R, Lin YH, Gupta MK, Kaplan DL, Naik RR, Tsukruk VV (2007) Mechanical properties of robust ultrathin silk fibroin films. Adv Funct Mater 17:2229–2237. doi: 10.1002/adfm.200601136 CrossRefGoogle Scholar
  75. 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 16:1418–1425. doi: 10.1021/acs.biomac.5b00226 PubMedCrossRefGoogle Scholar
  76. Karageorgiou V, Meinel L, Hofmann S, Malhotra A, Volloch V, Kaplan D (2004) Bone morphogenetic protein-2 decorated silk fibroin films induce osteogenic differentiation of human bone marrow stromal cells. J Biomed Mater Res A 71A:528–537. doi: 10.1002/jbm.a.30186 CrossRefGoogle Scholar
  77. Karatzas CN, Turner JD, Karatzas A-L (1999) Production of biofilaments in transgenic animals. Canada PatentGoogle Scholar
  78. Keten S, Buehler MJ (2008) Geometric confinement governs the rupture strength of H-bond assemblies at a critical length scale. Nano Lett 8:743–748. doi: 10.1021/nl0731670 PubMedCrossRefGoogle Scholar
  79. Kiliani OG (1901) II. On traumatic keloid of the median nerve, with observations upon the absorption of silk sutures. Ann Surg 33:13PubMedPubMedCentralCrossRefGoogle Scholar
  80. Kim U-J, Park J, Joo Kim H, Wada M, Kaplan DL (2005) Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin. Biomaterials 26:2775–2785. doi: 10.1016/j.biomaterials.2004.07.044 PubMedCrossRefGoogle Scholar
  81. Kim D-H, Viventi J, Amsden JJ, Xiao J, Vigeland L, Kim Y-S, Blanco JA, Panilaitis B, Frechette ES, Contreras D, Kaplan DL, Omenetto FG, Huang Y, Hwang K-C, Zakin MR, Litt B, Rogers JA (2010) Dissolvable films of silk fibroin for ultrathin conformal bio-integrated electronics. Nat Mater 9:511–517. doi: 10.1038/nmat2745 PubMedPubMedCentralCrossRefGoogle Scholar
  82. Kluge JA, Rabotyagova O, Leisk GG, Kaplan DL (2008) Spider silks and their applications. Trends Biotechnol 26:244–251. doi: 10.1016/j.tibtech.2008.02.006 PubMedCrossRefGoogle Scholar
  83. Knight DP, Vollrath F (1999) Liquid crystals and flow elongation in a spider’s silk production line. Proc R Soc London, Ser B 266:519–523. doi: 10.1098/rspb.1999.0667 CrossRefGoogle Scholar
  84. Knight DP, Vollrath F (2001) Changes in element composition along the spinning duct in a Nephila spider. Naturwissenschaften 88:179–182PubMedCrossRefGoogle Scholar
  85. Knight DP, Nash L, Hu XW, Haffegee J, Ho MW (1998) In vitro formation by reverse dialysis of collagen gels containing highly oriented arrays of fibrils. J Biomed Mater Res 41:185–191. doi: 10.1002/(sici)1097-4636(199808)41:2<185::aid-jbm2>3.0.co;2-e PubMedCrossRefGoogle Scholar
  86. Kojima K, Kuwana Y, Sezutsu H, Kobayashi I, Uchino K, Tamura T, Tamada Y (2007) A new method for the modification of fibroin heavy chain protein in the transgenic silkworm. Biosci Biotechnol Biochem 71:2943–2951. doi: 10.1271/bbb.70353 PubMedCrossRefGoogle Scholar
  87. Kronqvist N, Otikovs M, Chmyrov V, Chen G, Andersson M, Nordling K, Landreh M, Sarr M, Jornvall H, Wennmalm S, Widengren J, Meng Q, Rising A, Otzen D, Knight SD, Jaudzems K, Johansson J (2014) Sequential pH-driven dimerization and stabilization of the N-terminal domain enables rapid spider silk formation. Nat Commun 5:3254. doi: 10.1038/ncomms4254 PubMedCrossRefGoogle Scholar
  88. Kummerlen J, vanBeek JD, Vollrath F, Meier BH (1996) Local structure in spider dragline silk investigated by two-dimensional spin-diffusion nuclear magnetic resonance. Macromolecules 29:2920–2928CrossRefGoogle Scholar
  89. Kuwana Y, Sezutsu H, Nakajima K, Tamada Y, Kojima K (2014) High-toughness silk produced by a transgenic silkworm expressing spider (Araneus ventricosus) dragline silk protein. PLoS ONE 9:e105325. doi: 10.1371/journal.pone.0105325 PubMedPubMedCentralCrossRefGoogle Scholar
  90. Lammel A, Schwab M, Slotta U, Winter G, Scheibel T (2008) Processing conditions for the formation of spider silk microspheres. ChemSusChem 1:413–416. doi: 10.1002/cssc.200800030 PubMedCrossRefGoogle Scholar
  91. Lammel A, Schwab M, Hofer M, Winter G, Scheibel T (2011) Recombinant spider silk particles as drug delivery vehicles. Biomaterials 32:2233–2240. doi: 10.1016/j.biomaterials.2010.11.060 PubMedCrossRefGoogle Scholar
  92. Lang G, Jokisch S, Scheibel T (2013) Air filter devices including nonwoven meshes of electrospun recombinant spider silk proteins. J Vis Exp e50492 doi: 10.3791/50492
  93. Lawrence BD, Cronin-Golomb M, Georgakoudi I, Kaplan DL, Omenetto FG (2008) Bioactive silk protein biomaterial systems for optical devices. Biomacromolecules 9:1214–1220. doi: 10.1021/Bm701235f PubMedCrossRefGoogle Scholar
  94. Lawrence BD, Wharram S, Kluge JA, Leisk GG, Omenetto FG, Rosenblatt MI, Kaplan DL (2010) Effect of hydration on silk film material properties. Macromol Biosci 10:393–403. doi: 10.1002/mabi.200900294 PubMedPubMedCentralCrossRefGoogle Scholar
  95. 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 295:472–476. doi: 10.1126/science.1065780 PubMedCrossRefGoogle Scholar
  96. 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–B75. doi: 10.1002/adem.201180072 CrossRefGoogle Scholar
  97. Lee KY, Mooney DJ (2001) Hydrogels for tissue engineering. Chem Rev 101:1869–1879. doi: 10.1021/cr000108x PubMedCrossRefGoogle Scholar
  98. Lee S-M, Pippel E, Gösele U, Dresbach C, Qin Y, Chandran CV, Bräuniger T, Hause G, Knez M (2009) Greatly increased toughness of infiltrated spider silk. Science 324:488–492. doi: 10.1126/science.1168162 PubMedCrossRefGoogle Scholar
  99. Lepore E, Bonaccorso F, Bruna M, Bosia F, Taioli S, Garberoglio G, Ferrari A, Pugno NM (2015) Silk reinforced with graphene or carbon nanotubes spun by spiders. arXiv preprint arXiv:150406751Google Scholar
  100. Lewis RV (1992) Spider silk: the unraveling of a mystery. Acc Chem Res 25:392–398. doi: 10.1021/ar00021a002 CrossRefGoogle Scholar
  101. Lewis R (1996) Unraveling the weave of spider silk. Bioscience 46:636–638CrossRefGoogle Scholar
  102. Lin Z, Deng Q, Liu XY, Yang D (2013) Engineered large spider eggcase silk protein for strong artificial fibers. Adv Mater 25:1216–1220. doi: 10.1002/adma.201204357 PubMedCrossRefGoogle Scholar
  103. Liu X, Sun Q, Wang H, Zhang L, Wang JY (2005) Microspheres of corn protein, zein, for an ivermectin drug delivery system. Biomaterials 26:109–115. doi: 10.1016/j.biomaterials.2004.02.013 PubMedCrossRefGoogle Scholar
  104. Lucke M, Winter G, Engert J (2015) The effect of steam sterilization on recombinant spider silk particles. Int J Pharm 481:125–131. doi: 10.1016/j.ijpharm.2015.01.024 PubMedCrossRefGoogle Scholar
  105. Mackintosh FC, Kas J, Janmey PA (1995) Elasticity of semiflexible biopolymer networks. Phys Rev Lett 75:4425–4428PubMedCrossRefGoogle Scholar
  106. 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
  107. Mehta N, Hede S (2005) Spider silk calcite composite. Hypothesis 3:21. doi: 10.1021/nn204506d Google Scholar
  108. Menassa R, Hong Z, Karatzas CN, Lazaris A, Richman A, Brandle J (2004) Spider dragline silk proteins in transgenic tobacco leaves: accumulation and field production. Plant Biotechnol J 2:431–438. doi: 10.1111/j.1467-7652.2004.00087.x PubMedCrossRefGoogle Scholar
  109. Metwalli E, Slotta U, Darko C, Roth SV, Scheibel T, Papadakis CM (2007) Structural changes of thin films from recombinant spider silk proteins upon post-treatment. Appl Phys A Mater Sci Process 89:655–661. doi: 10.1007/s00339-007-4265-5 CrossRefGoogle Scholar
  110. Mieszawska AJ, Fourligas N, Georgakoudi I, Ouhib NM, Belton DJ, Perry CC, Kaplan DL (2010) Osteoinductive silk-silica composite biomaterials for bone regeneration. Biomaterials 31:8902–8910. doi: 10.1016/j.biomaterials.2010.07.109 PubMedPubMedCentralCrossRefGoogle Scholar
  111. Minoura N, Aiba S, Gotoh Y, Tsukada M, Imai Y (1995) Attachment and growth of cultured fibroblast cells on silk protein matrices. J Biomed Mater Res 29:1215–1221PubMedCrossRefGoogle Scholar
  112. Motriuk-Smith D, Smith A, Hayashi CY, Lewis RV (2005) Analysis of the conserved N-terminal domains in major ampullate spider silk proteins. Biomacromolecules 6:3152–3159. doi: 10.1021/bm050472b PubMedCrossRefGoogle Scholar
  113. Müller-Herrmann S, Scheibel T (2015) Enzymatic degradation of films, particles, and nonwoven meshes made of a recombinant spider silk protein. ACS Biomater Sci Eng 1:247–259. doi: 10.1021/ab500147u CrossRefGoogle Scholar
  114. Munch E, Launey ME, Alsem DH, Saiz E, Tomsia AP, Ritchie RO (2008) Tough, bio-inspired hybrid materials. Science 322:1516–1520. doi: 10.1126/science.1164865 PubMedCrossRefGoogle Scholar
  115. Nazarov R, Jin H-J, Kaplan DL (2004) Porous 3-D scaffolds from regenerated silk fibroin. Biomacromolecules 5:718–726. doi: 10.1021/bm034327e PubMedCrossRefGoogle Scholar
  116. Neubauer MP, Blum C, Agostini E, Engert J, Scheibel T, Fery A (2013) Micromechanical characterization of spider silk particles. Biomater Sci 1:1160–1165. doi: 10.1039/c3bm60108k CrossRefGoogle Scholar
  117. Numata K, Hamasaki J, Subramanian B, Kaplan DL (2010) Gene delivery mediated by recombinant silk proteins containing cationic and cell binding motifs. J Control Release 146:136–143. doi: 10.1016/j.jconrel.2010.05.006 PubMedPubMedCentralCrossRefGoogle Scholar
  118. Papadopoulos P, Solter J, Kremer F (2007) Structure-property relationships in major ampullate spider silk as deduced from polarized FTIR spectroscopy. Eur Phys J E: Soft Matter Biol Phys 24:193–199. doi: 10.1140/epje/i2007-10229-9 CrossRefGoogle Scholar
  119. Peng H, Zhou S, Jiang J, Guo T, Zheng X, Yu X (2009) Pressure-induced crystal memory effect of spider silk proteins. J Phys Chem B 113:4636–4641. doi: 10.1021/jp811461b PubMedCrossRefGoogle Scholar
  120. Perez-Rigueiro J, Elices M, Guinea GV, Plaza GR, Karatzas C, Riekel C, Agullo-Rueda F, Daza R (2011) Bioinspired fibers follow the track of natural spider silk. Macromolecules 44:1166–1176. doi: 10.1021/ma102291m CrossRefGoogle Scholar
  121. Rabotyagova OS, Cebe P, Kaplan DL (2009) Self-assembly of genetically engineered spider silk block copolymers. Biomacromolecules 10:229–236. doi: 10.1021/bm800930x PubMedCrossRefGoogle Scholar
  122. Rabotyagova OS, Cebe P, Kaplan DL (2010) Role of polyalanine domains in beta-sheet formation in spider silk block copolymers. Macromol Biosci 10:49–59. doi: 10.1002/mabi.200900203 PubMedCrossRefGoogle Scholar
  123. Radtke C, Allmeling C, Waldmann K-H, Reimers K, Thies K, Schenk HC, Hillmer A, Guggenheim M, Brandes G, Vogt PM (2011) Spider silk constructs enhance axonal regeneration and remyelination in long nerve defects in sheep. PLoS ONE 6:e16990. doi: 10.1371/journal.pone.0016990 PubMedPubMedCentralCrossRefGoogle Scholar
  124. Rammensee S, Huemmerich D, Hermanson KD, Scheibel T, Bausch AR (2006) Rheological characterization of hydrogels formed by recombinantly produced spider silk. Appl Phys A Mater Sci Process 82:261–264. doi: 10.1007/s00339-005-3431-x CrossRefGoogle Scholar
  125. Rammensee S, Slotta U, Scheibel T, Bausch AR (2008) Assembly mechanism of recombinant spider silk proteins. Proc Natl Acad Sci U S A 105:6590–6595. doi: 10.1073/pnas.0709246105 PubMedPubMedCentralCrossRefGoogle Scholar
  126. Rising A (2014) Controlled assembly: a prerequisite for the use of recombinant spider silk in regenerative medicine? Acta Biomater 10:1627–1631. doi: 10.1016/j.actbio.2013.09.030 PubMedCrossRefGoogle Scholar
  127. Rising A, Johansson J (2015) Toward spinning artificial spider silk. Nat Chem Biol 11:309–315. doi: 10.1038/nchembio.1789 PubMedCrossRefGoogle Scholar
  128. Rising A, Hjalm G, Engstrom W, Johansson J (2006) N-terminal nonrepetitive domain common to dragline, flagelliform, and cylindriform spider silk proteins. Biomacromolecules 7:3120–3124. doi: 10.1021/bm060693x PubMedCrossRefGoogle Scholar
  129. Roemer L, Scheibel T (2007) Basis for new material—spider silk protein. Chem Unserer Zeit 41:306–314CrossRefGoogle Scholar
  130. Schacht K, Scheibel T (2011) Controlled hydrogel formation of a recombinant spider silk protein. Biomacromolecules 12:2488–2495. doi: 10.1021/bm200154k PubMedCrossRefGoogle Scholar
  131. Schacht K, Jüngst T, Schweinlin M, Ewald A, Groll J, Scheibel T (2015) Biofabrication of cell-loaded 3D spider silk constructs. Angew Chem Int Ed 54:2816–2820. doi: 10.1002/anie.201409846 CrossRefGoogle Scholar
  132. Scheibel T (2004) Spider silks: recombinant synthesis, assembly, spinning, and engineering of synthetic proteins. Microb Cell Factories 3:14. doi: 10.1186/1475-2859-3-14 CrossRefGoogle Scholar
  133. Seidel A, Liivak O, Jelinski LW (1998) Artificial spinning of spider silk. Macromolecules 31:6733–6736. doi: 10.1021/Ma9808880 CrossRefGoogle Scholar
  134. 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 33:775–780. doi: 10.1021/Ma990893j CrossRefGoogle Scholar
  135. Shao ZZ, Vollrath F, Yang Y, Thogersen HC (2003) Structure and behavior of regenerated spider silk. Macromolecules 36:1157–1161. doi: 10.1021/Ma0214660 CrossRefGoogle Scholar
  136. Shin H, Jo S, Mikos AG (2003) Biomimetic materials for tissue engineering. Biomaterials 24:4353–4364PubMedCrossRefGoogle Scholar
  137. Simmons AH, Michal CA, Jelinski LW (1996) Molecular orientation and two-component nature of the crystalline fraction of spider dragline silk. Science 271:84–87PubMedCrossRefGoogle Scholar
  138. Singh A, Hede S, Sastry M (2007) Spider silk as an active scaffold in the assembly of gold nanoparticles and application of the gold–silk bioconjugate in vapor sensing. Small 3:466–473. doi: 10.1002/smll.200600413 PubMedCrossRefGoogle Scholar
  139. Slotta U, Tammer M, Kremer F, Koelsch P, Scheibel T (2006) Structural analysis of spider silk films. Supramol Chem 18:465–471. doi: 10.1080/10610270600832042 CrossRefGoogle Scholar
  140. Slotta U, Hess S, Spiess K, Stromer T, Serpell L, Scheibel T (2007) Spider silk and amyloid fibrils: a structural comparison. Macromol Biosci 7:183–188. doi: 10.1002/mabi.200600201 PubMedCrossRefGoogle Scholar
  141. Slotta UK, Rammensee S, Gorb S, Scheibel T (2008) An engineered spider silk protein forms microspheres. Angew Chem Int Ed 47:4592–4594. doi: 10.1002/anie.200800683 CrossRefGoogle Scholar
  142. Smit E, Buttner U, Sanderson RD (2005) Continuous yarns from electrospun fibers. Polymer 46:2419–2423. doi: 10.1016/j.polymer.2005.02.002 CrossRefGoogle Scholar
  143. Smith A, Scheibel T (2013) Basis for new material—spider silk protein. In: Fratzl P, Dunlop J, Weinkamer R (eds) Materials design inspired by nature: function through inner architecture. RSC smart materials, vol 4. RSC Publishing, Cambridge, pp 256–281. doi: 10.1039/9781849737555-00256 CrossRefGoogle Scholar
  144. Sofia S, McCarthy MB, Gronowicz G, Kaplan DL (2001) Functionalized silk-based biomaterials for bone formation. J Biomed Mater Res 54:139–148. doi: 10.1002/1097-4636(200101)54:1<139 PubMedCrossRefGoogle Scholar
  145. Sørensen HP, Mortensen KK (2005) Advanced genetic strategies for recombinant protein expression in Escherichia coli. J Biotechnol 115:113–128. doi: 10.1016/j.jbiotec.2004.08.004 PubMedCrossRefGoogle Scholar
  146. Spiess K, Lammel A, Scheibel T (2010a) Recombinant spider silk proteins for applications in biomaterials. Macromol Biosci 10:998–1007. doi: 10.1002/mabi.201000071 PubMedCrossRefGoogle Scholar
  147. Spiess K, Wohlrab S, Scheibel T (2010b) Structural characterization and functionalization of engineered spider silk films. Soft Matter 6:4168–4174. doi: 10.1039/b927267d CrossRefGoogle Scholar
  148. Sponner A, Vater W, Monajembashi S, Unger E, Grosse F, Weisshart K (2007) Composition and hierarchical organisation of a spider silk. PLoS ONE 2:e998. doi: 10.1371/journal.pone.0000998 PubMedPubMedCentralCrossRefGoogle Scholar
  149. Sridharan I, Kim T, Strakova Z, Wang R (2013) Matrix-specified differentiation of human decidua parietalis placental stem cells. Biochem Biophys Res Commun 437:489–495. doi: 10.1016/j.bbrc.2013.07.002 PubMedPubMedCentralCrossRefGoogle Scholar
  150. Stark M, Grip S, Rising A, Hedhammar M, Engstrom W, Hjalm G, Johansson J (2007) Macroscopic fibers self-assembled from recombinant miniature spider silk proteins. Biomacromolecules 8:1695–1701. doi: 10.1021/Bm070049y PubMedCrossRefGoogle Scholar
  151. Steinkraus HB, Rothfuss H, Jones JA, Dissen E, Shefferly E, Lewis RV (2012) The absence of detectable fetal microchimerism in nontransgenic goats (Capra aegagrus hircus) bearing transgenic offspring. J Anim Sci 90:481–488. doi: 10.2527/jas.2011-4034 PubMedCrossRefGoogle Scholar
  152. 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 6:1405–1413. doi: 10.1021/Bm049296h PubMedCrossRefGoogle Scholar
  153. Steven E, Saleh WR, Lebedev V, Acquah SFA, Laukhin V, Alamo RG, Brooks JS (2013) Carbon nanotubes on a spider silk scaffold. Nat Commun 4:2435. doi: 10.1038/ncomms3435 PubMedPubMedCentralCrossRefGoogle Scholar
  154. 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 18:81–84. doi: 10.1038/71978 PubMedCrossRefGoogle Scholar
  155. Teo WE, Ramakrishna S (2006) A review on electrospinning design and nanofibre assemblies. Nanotechnology 17:R89–R106. doi: 10.1088/0957-4484/17/14/R01 PubMedCrossRefGoogle Scholar
  156. Teule F, Furin WA, Cooper AR, Duncan JR, Lewis RV (2007) Modifications of spider silk sequences in an attempt to control the mechanical properties of the synthetic fibers. J Mater Sci 42:8974–8985. doi: 10.1007/s10853-007-1642-6 CrossRefGoogle Scholar
  157. Teule F, Cooper AR, Furin WA, Bittencourt D, Rech EL, Brooks A, Lewis RV (2009) A protocol for the production of recombinant spider silk-like proteins for artificial fiber spinning. Nat Protoc 4:341–355. doi: 10.1038/nprot.2008.250 PubMedPubMedCentralCrossRefGoogle Scholar
  158. Teule F, Miao YG, Sohn BH, Kim YS, Hull JJ, Fraser MJ, Lewis RV, Jarvis DL (2012) Silkworms transformed with chimeric silkworm/spider silk genes spin composite silk fibers with improved mechanical properties. Proc Natl Acad Sci U S A 109:923–928. doi: 10.1073/pnas.1109420109 PubMedPubMedCentralCrossRefGoogle Scholar
  159. Um IC, Ki CS, Kweon H, Lee KG, Ihm DW, Park YH (2004) Wet spinning of silk polymer. II. Effect of drawing on the structural characteristics and properties of filament. Int J Biol Macromol 34:107–119. doi: 10.1016/j.ijbiomac.2004.03.011 PubMedCrossRefGoogle Scholar
  160. 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 99:10266–10271. doi: 10.1073/pnas.152162299 PubMedPubMedCentralCrossRefGoogle Scholar
  161. Vendrely C, Scheibel T (2007) Biotechnological production of spider-silk proteins enables new applications. Macromol Biosci 7:401–409. doi: 10.1002/mabi.200600255 PubMedCrossRefGoogle Scholar
  162. Vepari C, Kaplan DL (2007) Silk as a biomaterial. Prog Polym Sci 32:991–1007. doi: 10.1016/j.progpolymsci.2007.05.013 PubMedPubMedCentralCrossRefGoogle Scholar
  163. Viney C (1997) Natural silks: archetypal supramolecular assembly of polymer fibres. Supramol Sci 4:75–81CrossRefGoogle Scholar
  164. Vollrath F (2000) Strength and structure of spiders’ silks. J Biotechnol 74:67–83. doi: 10.1016/S1389-0352(00)00006-4 PubMedGoogle Scholar
  165. Vollrath F, Knight DP (1999) Structure and function of the silk production pathway in the spider Nephila edulis. Int J Biol Macromol 24:243–249. doi: 10.1016/S0141-8130(98)00095-6 PubMedCrossRefGoogle Scholar
  166. Vollrath F, Knight DP (2001) Liquid crystalline spinning of spider silk. Nature 410:541–548. doi: 10.1038/35069000 PubMedCrossRefGoogle Scholar
  167. Vollrath F, Barth P, Basedow A, Engstrom W, List H (2002) Local tolerance to spider silks and protein polymers in vivo. In vivo 16:229–234PubMedGoogle Scholar
  168. Wang X, Wenk E, Matsumoto A, Meinel L, Li C, Kaplan DL (2007) Silk microspheres for encapsulation and controlled release. J Control Release 117:360–370. doi: 10.1016/j.jconrel.2006.11.021 PubMedCrossRefGoogle Scholar
  169. Wang X, Yucel T, Lu Q, Hu X, Kaplan DL (2010) Silk nanospheres and microspheres from silk/PVA blend films for drug delivery. Biomaterials 31:1025–1035. doi: 10.1016/j.biomaterials.2009.11.002 PubMedCrossRefGoogle Scholar
  170. Wen HX, Lan XQ, Zhang YS, Zhao TF, Wang YJ, Kajiura Z, Nakagaki M (2010) Transgenic silkworms (Bombyx mori) produce recombinant spider dragline silk in cocoons. Mol Biol Rep 37:1815–1821. doi: 10.1007/s11033-009-9615-2 PubMedCrossRefGoogle Scholar
  171. Wendt H, Hillmer A, Reimers K, Kuhbier JW, Schafer-Nolte F, Allmeling C, Kasper C, Vogt PM (2011) Artificial skin—culturing of different skin cell lines for generating an artificial skin substitute on cross-weaved spider silk fibres. PLoS ONE 6:e21833. doi: 10.1371/journal.pone.0021833 PubMedPubMedCentralCrossRefGoogle Scholar
  172. Widhe M, Bysell H, Nystedt S, Schenning I, Malmsten M, Johansson J, Rising A, Hedhammar M (2010) Recombinant spider silk as matrices for cell culture. Biomaterials 31:9575–9585. doi: 10.1016/j.biomaterials.2010.08.061 PubMedCrossRefGoogle Scholar
  173. Wohlrab S, Müller S, Schmidt A, Neubauer S, Kessler H, Leal-Egaña A, Scheibel T (2012a) Cell adhesion and proliferation on RGD-modified recombinant spider silk proteins. Biomaterials 33:6650–6659. doi: 10.1016/j.biomaterials.2012.05.069 PubMedCrossRefGoogle Scholar
  174. Wohlrab S, Spieß K, Scheibel T (2012b) Varying surface hydrophobicities of coatings made of recombinant spider silk proteins. J Mater Chem 22:22050–22054. doi: 10.1039/C2JM35075K CrossRefGoogle Scholar
  175. Wong Po Foo C, Patwardhan SV, Belton DJ, Kitchel B, Anastasiades D, Huang J, Naik RR, Perry CC, Kaplan DL (2006) Novel nanocomposites from spider silk-silica fusion (chimeric) proteins. Proc Natl Acad Sci U S A 103:9428–9433. doi: 10.1073/pnas.0601096103 PubMedPubMedCentralCrossRefGoogle Scholar
  176. Xia X-X, Qian Z-G, 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 U S A 107:14059–14063. doi: 10.1073/pnas.1003366107 PubMedPubMedCentralCrossRefGoogle Scholar
  177. Xu M, Lewis RV (1990) Structure of a protein superfiber: spider dragline silk. Proc Natl Acad Sci 87:7120–7124PubMedPubMedCentralCrossRefGoogle Scholar
  178. 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 18:1–12. doi: 10.1080/10495390601091024 PubMedCrossRefGoogle Scholar
  179. Yu Q, Xu S, Zhang H, Gu L, Xu Y, Ko F (2014) Structure-property relationship of regenerated spider silk protein nano/microfibrous scaffold fabricated by electrospinning. J Biomed Mater Res Part A 102:3828–3837. doi: 10.1002/jbm.a.35051 CrossRefGoogle Scholar
  180. Zarkoob S, Eby RK, Reneker DH, Hudson SD, Ertley D, Adams WW (2004) Structure and morphology of electrospun silk nanofibers. Polymer 45:3973–3977. doi: 10.1016/j.polymer.2003.10.102 CrossRefGoogle Scholar
  181. Zeplin PH, Berninger AK, Maksimovikj NC, van Gelder P, Scheibel T, Walles H (2014a) Verbesserung der Biokompatibilität von Silikonimplantaten durch Spinnenseidenbeschichtung: Immunhistochemische Untersuchungen zum Einfluss auf die Kapselbildung. Handchir Mikrochir Plast Chir 46:336–341. doi: 10.1055/s-0034-1395558 PubMedCrossRefGoogle Scholar
  182. Zeplin PH, Maksimovikj NC, Jordan MC, Nickel J, Lang G, Leimer AH, Römer L, Scheibel T (2014b) Spider silk coatings as a bioshield to reduce periprosthetic fibrous capsule formation. Adv Funct Mater 24:2658–2666. doi: 10.1002/adfm.201302813 CrossRefGoogle Scholar
  183. 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 35:329–335. doi: 10.1007/s11033-007-9090-6 PubMedCrossRefGoogle Scholar
  184. Zhang C-Y, Zhang D-C, Chen D, M L (2014) A bilayered scaffold based on RGD recombinant spider silk proteins for small diameter tissue engineering. Polym Compos. doi: 10.1002/pc.23208 Google Scholar
  185. Zhou S, Peng H, Yu X, Zheng X, Cui W, Zhang Z, Li X, Wang J, Weng J, Jia W, Li F (2008) Preparation and characterization of a novel electrospun spider silk fibroin/poly(D, L-lactide) composite fiber. J Phys Chem B 112:11209–11216. doi: 10.1021/jp800913k PubMedCrossRefGoogle Scholar
  186. Zhu ZH, Kikuchi Y, Kojima K, Tamura T, Kuwabara N, Nakamura T, Asakura T (2010) Mechanical properties of regenerated Bombyx mori silk fibers and recombinant silk fibers produced by transgenic silkworms. J Biomater Sci Polym Ed 21:395–412. doi: 10.1163/156856209x423126 PubMedCrossRefGoogle Scholar
  187. Zhu B, Li W, Lewis RV, Segre CU, Wang R (2015) E-spun composite fibers of collagen and dragline silk protein: fiber mechanics, biocompatibility, and application in stem cell differentiation. Biomacromolecules 16:202–213. doi: 10.1021/bm501403f PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Elena Doblhofer
    • 1
  • Aniela Heidebrecht
    • 1
  • Thomas Scheibel
    • 1
    • 2
    • 3
    • 4
    • 5
    Email author
  1. 1.Lehrstuhl Biomaterialien, Fakultät für IngenieurswissenschaftenUniversität BayreuthBayreuthGermany
  2. 2.Institut für Bio-Makromoleküle (bio-mac)Universität BayreuthBayreuthGermany
  3. 3.Bayreuther Zentrum für Kolloide und Grenzflächen (BZKG)Universität BayreuthBayreuthGermany
  4. 4.Bayreuther Zentrum für Molekulare Biowissenschaften (BZMB)Universität BayreuthBayreuthGermany
  5. 5.Bayreuther Materialzentrum (BayMAT)Universität BayreuthBayreuthGermany

Personalised recommendations