1932

Abstract

Modern polymer science increasingly requires precise control over macromolecular structure and properties for engineering advanced materials and biomedical systems. The application of biological processes to design and synthesize artificial protein polymers offers a means for furthering macromolecular tunability, enabling polymers with dispersities of ∼1.0 and monomer-level sequence control. Taking inspiration from materials evolved in nature, scientists have created modular building blocks with simplified monomer sequences that replicate the function of natural systems. The corresponding protein engineering toolbox has enabled the systematic development of complex functional polymeric materials across areas as diverse as adhesives, responsive polymers, and medical materials. This review discusses the natural proteins that have inspired the development of key building blocks for protein polymer engineering and the function of these elements in material design. The prospects and progress for scalable commercialization of protein polymers are reviewed, discussing both technology needs and opportunities.

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2017-06-07
2024-06-17
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Literature Cited

  1. DiMarco RL, Heilshorn SC. 1.  2012. Multifunctional materials through modular protein engineering. Adv. Mater. 24:3923–40 [Google Scholar]
  2. Sarikaya M. 2.  1994. An introduction to biomimetics: a structural viewpoint. Microsc. Res. Tech. 27:360–75 [Google Scholar]
  3. Geim AK, Dubonos S, Grigorieva I, Novoselov K, Zhukov A, Shapoval SY. 3.  2003. Microfabricated adhesive mimicking gecko foot-hair. Nat. Mater. 2:461–63 [Google Scholar]
  4. Xu M, Lewis RV. 4.  1990. Structure of a protein superfiber: spider dragline silk. PNAS 87:7120–24 [Google Scholar]
  5. Lawrence BD, Cronin-Golomb M, Georgakoudi I, Kaplan DL, Omenetto FG. 5.  2008. Bioactive silk protein biomaterial systems for optical devices. Biomacromolecules 9:1214–20 [Google Scholar]
  6. Hu X, Cebe P, Weiss AS, Omenetto F, Kaplan DL. 6.  2012. Protein-based composite materials. Mater. Today 15:208–15 [Google Scholar]
  7. Bechtle S, Ang SF, Schneider GA. 7.  2010. On the mechanical properties of hierarchically structured biological materials. Biomaterials 31:6378–85 [Google Scholar]
  8. Reddy N, Yang Y. 8.  2005. Biofibers from agricultural byproducts for industrial applications. Trends Biotechnol 23:22–27 [Google Scholar]
  9. Andersen DC, Krummen L. 9.  2002. Recombinant protein expression for therapeutic applications. Curr. Opin. Biotechnol. 13:117–23 [Google Scholar]
  10. Langer R, Tirrell DA. 10.  2004. Designing materials for biology and medicine. Nature 428:487–92 [Google Scholar]
  11. van Hest JC, Tirrell DA. 11.  2001. Protein-based materials, toward a new level of structural control. Chem. Commun. 2001:1897–904 [Google Scholar]
  12. Hyun J, Lee WK, Nath N, Chilkoti A, Zauscher S. 12.  2004. Capture and release of proteins on the nanoscale by stimuli-responsive elastin-like polypeptide “switches”. J. Am. Chem. Soc. 126:7330–35 [Google Scholar]
  13. Johnson JA, Lu YY, Van Deventer JA, Tirrell DA. 13.  2010. Residue-specific incorporation of non-canonical amino acids into proteins: recent developments and applications. Curr. Opin. Chem. Biol. 14:774–80 [Google Scholar]
  14. Baneyx F, Mujacic M. 14.  2004. Recombinant protein folding and misfolding in Escherichia coli. . Nat. Biotechnol. 22:1399–408 [Google Scholar]
  15. Palomo JM. 15.  2014. Solid-phase peptide synthesis: an overview focused on the preparation of biologically relevant peptides. RSC Adv 4:32658–72 [Google Scholar]
  16. Jenkins N, Murphy L, Tyther R. 16.  2008. Post-translational modifications of recombinant proteins: significance for biopharmaceuticals. Mol. Biotechnol. 39:113–18 [Google Scholar]
  17. Main ER, Jackson SE, Regan L. 17.  2003. The folding and design of repeat proteins: reaching a consensus. Curr. Opin. Struct. Biol. 13:482–89 [Google Scholar]
  18. Xia X-X, Xu Q, Hu X, Qin G, Kaplan DL. 18.  2011. Tunable self-assembly of genetically engineered silk–elastin-like protein polymers. Biomacromolecules 12:3844–50 [Google Scholar]
  19. Wlodarczyk-Biegun MK, Werten MW, de Wolf FA, van den Beucken JJ, Leeuwenburgh SC. 19.  et al. 2014. Genetically engineered silk-collagen-like copolymer for biomedical applications: production, characterization and evaluation of cellular response. Acta Biomater 10:3620–29 [Google Scholar]
  20. Bracalello A, Santopietro V, Vassalli M, Marletta G, Del Gaudio R. 20.  et al. 2011. Design and production of a chimeric resilin-, elastin-, and collagen-like engineered polypeptide. Biomacromolecules 12:2957–65 [Google Scholar]
  21. Qiu W, Teng W, Cappello J, Wu X. 21.  2009. Wet-spinning of recombinant silk-elastin-like protein polymer fibers with high tensile strength and high deformability. Biomacromolecules 10:602–8 [Google Scholar]
  22. Brodsky B, Ramshaw JA. 22.  1997. The collagen triple-helix structure. Matrix Biol 15:545–54 [Google Scholar]
  23. Wang B, Yang W, McKittrick J, Meyers MA. 23.  2016. Keratin: structure, mechanical properties, occurrence in biological organisms, and efforts at bioinspiration. Prog. Mater. Sci. 76:229–318 [Google Scholar]
  24. Fu CJ, Shao ZZ, Fritz V. 24.  2009. Animal silks: their structures, properties and artificial production. Chem. Commun.6515–29 [Google Scholar]
  25. Evans ML, Chapman MR. 25.  2014. Curli biogenesis: order out of disorder. Biochim. Biophys. Acta 1843:1551–58 [Google Scholar]
  26. Debelle L, Tamburro AM. 26.  1999. Elastin: molecular description and function. Int. J. Biochem. Cell Biol. 31:261–72 [Google Scholar]
  27. Hayashi CY, Lewis RV. 27.  2001. Spider flagelliform silk: lessons in protein design, gene structure, and molecular evolution. Bioessays 23:750–56 [Google Scholar]
  28. Ardell DH, Andersen SO. 28.  2001. Tentative identification of a resilin gene in Drosophila melanogaster. . Insect Biochem. Mol. Biol. 31:965–70 [Google Scholar]
  29. Gorski JP. 29.  1992. Acidic phosphoproteins from bone matrix: a structural rationalization of their role in biomineralization. Calcif. Tissue Int. 50:391–96 [Google Scholar]
  30. He G, Ramachandran A, Dahl T, George S, Schultz D. 30.  et al. 2005. Phosphorylation of phosphophoryn is crucial for its function as a mediator of biomineralization. J. Biol. Chem. 280:33109–14 [Google Scholar]
  31. Politi Y, Priewasser M, Pippel E, Zaslansky P, Hartmann J. 31.  et al. 2012. A spider's fang: how to design an injection needle using chitin-based composite material. Adv. Funct. Mater. 22:2519–28 [Google Scholar]
  32. Broomell CC, Mattoni MA, Zok FW, Waite JH. 32.  2006. Critical role of zinc in hardening of Nereis jaws. J. Exp. Biol. 209:3219–25 [Google Scholar]
  33. Holten-Andersen N, Mates TE, Toprak MS, Stucky GD, Zok FW, Waite JH. 33.  2009. Metals and the integrity of a biological coating: the cuticle of mussel byssus. Langmuir 25:3323–26 [Google Scholar]
  34. Zhao H, Waite JH. 34.  2006. Proteins in load-bearing junctions: the histidine-rich metal-binding protein of mussel byssus. Biochemistry 45:14223–31 [Google Scholar]
  35. Hirata K, Tsuji N, Miyamoto K. 35.  2005. Biosynthetic regulation of phytochelatins, heavy metal-binding peptides. J. Biosci. Bioeng. 100:593–99 [Google Scholar]
  36. Cobbett C, Goldsbrough P. 36.  2002. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 53:159–82 [Google Scholar]
  37. Nicklisch SCT, Waite JH. 37.  2012. Mini-review: the role of redox in Dopa-mediated marine adhesion. Biofouling 28:865–77 [Google Scholar]
  38. Frey S, Görlich D. 38.  2009. FG/FxFG as well as GLFG repeats form a selective permeability barrier with self-healing properties. EMBO J 28:2554–67 [Google Scholar]
  39. Crookes WJ, Ding L-L, Huang QL, Kimbell JR, Horwitz J, McFall-Ngai MJ. 39.  2004. Reflectins: the unusual proteins of squid reflective tissues. Science 303:235–38 [Google Scholar]
  40. Zhu JM, Marchant RE. 40.  2011. Design properties of hydrogel tissue-engineering scaffolds. Expert Rev. Med. Devices 8607–26 [Google Scholar]
  41. Duchstein P, Clark T, Zahn D. 41.  2015. Atomistic modeling of a KRT35/KRT85 keratin dimer: folding in aqueous solution and unfolding under tensile load. Phys. Chem. Chem. Phys. 17:21880–84 [Google Scholar]
  42. Miserez A, Wasko SS, Carpenter CF, Waite JH. 42.  2009. Non-entropic and reversible long-range deformation of an encapsulating bioelastomer. Nat. Mater. 8:910–16 [Google Scholar]
  43. Olsen BD, Kornfield JA, Tirrell DA. 43.  2010. Yielding behavior in injectable hydrogels from telechelic proteins. Macromolecules 43:9094–99 [Google Scholar]
  44. Seidel A, Liivak O, Jelinski LW. 44.  1998. Artificial spinning of spider silk. Macromolecules 31:6733–36 [Google Scholar]
  45. McDaniel JR, MacEwan SR, Dewhirst M, Chilkoti A. 45.  2012. Doxorubicin-conjugated chimeric polypeptide nanoparticles that respond to mild hyperthermia. J. Control. Release 159:362–67 [Google Scholar]
  46. Qin GK, Hu X, Cebe P, Kaplan DL. 46.  2012. Mechanism of resilin elasticity. Nat. Commun. 3:1003 [Google Scholar]
  47. Lupas A. 47.  1996. Coiled coils: new structures and new functions. Trends Biochem. Sci. 21:375–82 [Google Scholar]
  48. Kohn WD, Mant CT, Hodges RS. 48.  1997. α-Helical protein assembly motifs. J. Biol. Chem. 272:2583–86 [Google Scholar]
  49. MacPhee CE, Woolfson DN. 49.  2004. Engineered and designed peptide-based fibrous biomaterials. Curr. Opin. Solid State Mater. Sci. 8:141–49 [Google Scholar]
  50. Kadler KE, Baldock C, Bella J, Boot-Handford RP. 50.  2007. Collagens at a glance. J. Cell Sci. 120:1955–58 [Google Scholar]
  51. Shoulders MD, Raines RT. 51.  2009. Collagen structure and stability. Annu. Rev. Biochem. 78:929–58 [Google Scholar]
  52. Luo JN, Tong YW. 52.  2011. Self-assembly of collagen-mimetic peptide amphiphiles into biofunctional nanofiber. ACS Nano 5:7739–47 [Google Scholar]
  53. Toman PD, Chisholm G, McMullin H, Giere LM, Olsen DR. 53.  et al. 2000. Production of recombinant human type I procollagen trimers using a four-gene expression system in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 275:23303–9 [Google Scholar]
  54. Teles H, Skrzeszewska PJ, Werten MW, van der Gucht J, Eggink G, de Wolf FA. 54.  2010. Influence of molecular size on gel-forming properties of telechelic collagen-inspired polymers. Soft Matter 6:4681–87 [Google Scholar]
  55. San BH, Li Y, Tarbet EB, Yu SM. 55.  2016. Nanoparticle assembly and gelatin binding mediated by triple helical collagen mimetic peptide. ACS Appl. Mater. Interfaces 8:19907–15 [Google Scholar]
  56. Dickerson MB, Sierra AA, Bedford NM, Lyon WJ, Gruner WE. 56.  et al. 2013. Keratin-based antimicrobial textiles, films, and nanofibers. J. Mater. Chem. B 1:5505–14 [Google Scholar]
  57. Fraser RDB, MacRae TP, Suzuki E. 57.  1976. Structure of the α-keratin microfibril. J. Mol. Biol. 108:435–52 [Google Scholar]
  58. Landschulz W, Johnson P, McKnight S. 58.  1988. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240:1759–64 [Google Scholar]
  59. Xu C, Breedveld V, Kopecek J. 59.  2005. Reversible hydrogels from self-assembling genetically engineered protein block copolymers. Biomacromolecules 6:1739–49 [Google Scholar]
  60. Shen W, Zhang KC, Kornfield JA, Tirrell DA. 60.  2006. Tuning the erosion rate of artificial protein hydrogels through control of network topology. Nat. Mater. 5:153–58 [Google Scholar]
  61. Glassman MJ, Chan J, Olsen BD. 61.  2013. Reinforcement of shear thinning protein hydrogels by responsive block copolymer self-assembly. Adv. Funct. Mater. 23:1182–93 [Google Scholar]
  62. Petka WA, Harden JL, McGrath KP, Wirtz D, Tirrell DA. 62.  1998. Reversible hydrogels from self-assembling artificial proteins. Science 281:389–92 [Google Scholar]
  63. Dooley K, Kim YH, Lu HD, Tu R, Banta S. 63.  2012. Engineering of an environmentally responsive beta roll peptide for use as a calcium-dependent cross-linking domain for peptide hydrogel formation. Biomacromolecules 13:1758–64 [Google Scholar]
  64. Ifkovits JL, Burdick JA. 64.  2007. Review: photopolymerizable and degradable biomaterials for tissue engineering applications. Tissue Eng 13:2369–85 [Google Scholar]
  65. Foo C, Lee JS, Mulyasasmita W, Parisi-Amon A, Heilshorn SC. 65.  2009. Two-component protein-engineered physical hydrogels for cell encapsulation. PNAS 106:22067–72 [Google Scholar]
  66. Danmark S, Aronsson C, Aili D. 66.  2016. Tailoring supramolecular peptide-poly(ethylene glycol) hydrogels by coiled coil self-assembly and self-sorting. Biomacromolecules 17:2260–67 [Google Scholar]
  67. Yamaguchi N, Kiick KL. 67.  2005. Polysaccharide-poly(ethylene glycol) star copolymer as a scaffold for the production of bioactive hydrogels. Biomacromolecules 6:1921–30 [Google Scholar]
  68. Lu HD, Charati MB, Kim IL, Burdick JA. 68.  2012. Injectable shear-thinning hydrogels engineered with a self-assembling Dock-and-Lock mechanism. Biomaterials 33:2145–53 [Google Scholar]
  69. Tang SC, Glassman MJ, Li SL, Socrate S, Olsen BD. 69.  2014. Oxidatively responsive chain extension to entangle engineered protein hydrogels. Macromolecules 47:791–99 [Google Scholar]
  70. Tang S, Wang M, Olsen BD. 70.  2015. Anomalous self-diffusion and sticky Rouse dynamics in associative protein hydrogels. J. Am. Chem. Soc. 137:3946–57 [Google Scholar]
  71. Valluzzi R, Winkler S, Wilson D, Kaplan DL. 71.  2002. Silk: molecular organization and control of assembly. Philos. Trans. R. Soc. B 357:165–67 [Google Scholar]
  72. Altman GH, Diaz F, Jakuba C, Calabro T, Horan RL. 72.  et al. 2003. Silk-based biomaterials. Biomaterials 24:401–16 [Google Scholar]
  73. Hardy JG, Romer LM, Scheibel TR. 73.  2008. Polymeric materials based on silk proteins. Polymer 49:4309–27 [Google Scholar]
  74. Kundu B, Rajkhowa R, Kundu SC, Wang XG. 74.  2013. Silk fibroin biomaterials for tissue regenerations. Adv. Drug Deliv. Rev. 65:457–70 [Google Scholar]
  75. Pritchard EM, Kaplan DL. 75.  2011. Silk fibroin biomaterials for controlled release drug delivery. Expert Opin. Drug Deliv. 8:797–811 [Google Scholar]
  76. Omenetto FG, Kaplan DL. 76.  2008. A new route for silk. Nat. Photonics 2:641–43 [Google Scholar]
  77. Yanagisawa S, Zhu ZH, Kobayashi I, Uchino K, Tamada Y. 77.  et al. 2007. Improving cell-adhesive properties of recombinant Bombyx mori silk by incorporation of collagen or fibronectin derived peptides produced by transgenic silkworms. Biomacromolecules 8:3487–92 [Google Scholar]
  78. Vendrely C, Scheibel T. 78.  2007. Biotechnological production of spider-silk proteins enables new applications. Macromol. Biosci. 7:401–9 [Google Scholar]
  79. Hardy JG, Scheibel TR. 79.  2010. Composite materials based on silk proteins. Prog. Polymer Sci. 35:1093–115 [Google Scholar]
  80. Hayashi CY, Shipley NH, Lewis RV. 80.  1999. Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins. Int. J. Biol. Macromol. 24:271–75 [Google Scholar]
  81. Xia XX, Qian ZG, Ki CS, Park YH, Kaplan DL, Lee SY. 81.  2010. Native-sized recombinant spider silk protein produced in metabolically engineered Escherichia coli results in a strong fiber. PNAS 107:14059–63 [Google Scholar]
  82. Spiess K, Lammel A, Scheibel T. 82.  2010. Recombinant spider silk proteins for applications in biomaterials. Macromol. Biosci. 10:998–1007 [Google Scholar]
  83. Nguyen PQ, Botyanszki Z, Tay PKR, Joshi NS. 83.  2014. Programmable biofilm-based materials from engineered curli nanofibres. Nat. Commun. 5:4945 [Google Scholar]
  84. Botyanszki Z, Tay PKR, Nguyen PQ, Nussbaumer MG, Joshi NS. 84.  2015. Engineered catalytic biofilms: site-specific enzyme immobilization onto E. coli curli nanofibers. Biotechnol. Bioeng. 112:2016–24 [Google Scholar]
  85. Prusiner SB, Hsiao KK. 85.  1994. Human prion diseases. Ann. Neurol. 35:385–95 [Google Scholar]
  86. Krejchi MT, Cooper SJ, Deguchi Y, Atkins ED, Fournier MJ. 86.  et al. 1997. Crystal structures of chain-folded antiparallel β-sheet assemblies from sequence-designed periodic polypeptides. Macromolecules 30:5012–24 [Google Scholar]
  87. Cantor EJ, Atkins EDT, Cooper SJ, Fournier MJ, Mason TL, Tirrell DA. 87.  1997. Effects of amino acid side-chain volume on chain packing in genetically engineered periodic polypeptides. J. Biochem. 122:217–25 [Google Scholar]
  88. Lednev IK, Ermolenkov VV, Higashiya S, Popova LA, Topilina NI, Welch JT. 88.  2006. Reversible thermal denaturation of a 60-kDa genetically engineered β-sheet polypeptide. Biophys. J. 91:3805–18 [Google Scholar]
  89. Yeo GC, Keeley FW, Weiss AS. 89.  2011. Coacervation of tropoelastin. Adv. Colloid Interface Sci. 167:94–103 [Google Scholar]
  90. Urry DW, Parker TM. 90.  2003. Mechanics of elastin: molecular mechanism of biological elasticity and its relationship to contraction. Mechanics of Elastic Biomolecules WA Linke, H Granzier, MSZ Kellermayer 543–59 Dordrecht, Neth.: Springer [Google Scholar]
  91. Martín L, Arias FJ, Alonso M, García-Arévalo C, Rodríguez-Cabello JC. 91.  2010. Rapid micropatterning by temperature-triggered reversible gelation of a recombinant smart elastin-like tetrablock-copolymer. Soft Matter 6:1121–24 [Google Scholar]
  92. MacEwan SR, Chilkoti A. 92.  2014. Applications of elastin-like polypeptides in drug delivery. J. Control. Release 190:314–30 [Google Scholar]
  93. Urry DW, Luan CH, Parker TM, Gowda DC, Prasad KU. 93.  et al. 1991. Temperature of polypeptide inverse temperature transition depends on mean residue hydrophobicity. J. Am. Chem. Soc. 113:4346–48 [Google Scholar]
  94. Ribeiro A, Arias FJ, Reguera J, Alonso M, Rodríguez-Cabello JC. 94.  2009. Influence of the amino-acid sequence on the inverse temperature transition of elastin-like polymers. Biophys. J. 97:312–20 [Google Scholar]
  95. Meyer DE, Chilkoti A. 95.  1999. Purification of recombinant proteins by fusion with thermally-responsive polypeptides. Nat. Biotechnol. 17:1112–15 [Google Scholar]
  96. Kim W, Chaikof EL. 96.  2010. Recombinant elastin-mimetic biomaterials: emerging applications in medicine. Adv. Drug Deliv. Rev. 62:1468–78 [Google Scholar]
  97. McDaniel JR, Radford DC, Chilkoti A. 97.  2013. A unified model for de novo design of elastin-like polypeptides with tunable inverse transition temperatures. Biomacromolecules 14:2866–72 [Google Scholar]
  98. Quiroz FG, Chilkoti A. 98.  2015. Sequence heuristics to encode phase behaviour in intrinsically disordered protein polymers. Nat. Mater. 14:1164–71 [Google Scholar]
  99. Rodríguez-Cabello JC, Reguera J, Alonso M, Parker TM, McPherson DT, Urry DW. 99.  2004. Endothermic and exothermic components of an inverse temperature transition for hydrophobic association by TMDSC. Chem. Phys. Lett. 388:127–31 [Google Scholar]
  100. Reguera J, Lagarón JM, Alonso M, Reboto V, Calvo B, Rodríguez-Cabello JC. 100.  2003. Thermal behavior and kinetic analysis of the chain unfolding and refolding and of the concomitant nonpolar solvation and desolvation of two elastin-like polymers. Macromolecules 36:8470–76 [Google Scholar]
  101. Hayashi CY, Lewis RV. 101.  1998. Evidence from flagelliform silk cDNA for the structural basis of elasticity and modular nature of spider silks. J. Mol. Biol. 275:773–84 [Google Scholar]
  102. Heim M, Ackerschott CB, Scheibel T. 102.  2010. Characterization of recombinantly produced spider flagelliform silk domains. J. Struct. Biol. 170:420–25 [Google Scholar]
  103. Kim M, Elvin C, Brownlee A, Lyons R. 103.  2007. High yield expression of recombinant pro-resilin: lactose-induced fermentation in E. coli and facile purification. Protein Expr. Purif. 52:230–36 [Google Scholar]
  104. Tamburro AM, Panariello S, Santopietro V, Bracalello A, Bochicchio B, Pepe A. 104.  2010. Molecular and supramolecular structural studies on significant repetitive sequences of resilin. ChemBioChem 11:83–93 [Google Scholar]
  105. Elvin CM, Carr AG, Huson MG, Maxwell JM, Pearson RD. 105.  et al. 2005. Synthesis and properties of crosslinked recombinant pro-resilin. Nature 437:999–1002 [Google Scholar]
  106. Li L, Teller S, Clifton RJ, Jia X, Kiick KL. 106.  2011. Tunable mechanical stability and deformation response of a resilin-based elastomer. Biomacromolecules 12:2302–10 [Google Scholar]
  107. Li L, Tong Z, Jia X, Kiick KL. 107.  2013. Resilin-like polypeptide hydrogels engineered for versatile biological function. Soft Matter 9:665–73 [Google Scholar]
  108. Tatham AS, Shewry PR. 108.  2000. Elastomeric proteins: biological roles, structures and mechanisms. Trends Biochem. Sci. 25:567–71 [Google Scholar]
  109. Roberts S, Dzuricky M, Chilkoti A. 109.  2015. Elastin-like polypeptides as models of intrinsically disordered proteins. FEBS Lett 589:2477–86 [Google Scholar]
  110. Muiznieks LD, Keeley FW. 110.  2010. Proline periodicity modulates the self-assembly properties of elastin-like polypeptides. J. Biol. Chem. 285:39779–89 [Google Scholar]
  111. Truong MY, Dutta NK, Choudhury NR, Kim M, Elvin CM. 111.  et al. 2011. The effect of hydration on molecular chain mobility and the viscoelastic behavior of resilin-mimetic protein-based hydrogels. Biomaterials 32:8462–73 [Google Scholar]
  112. Uversky VN, Gillespie JR, Fink AL. 112.  2000. Why are “natively unfolded” proteins unstructured under physiologic conditions?. Proteins: Struct. Funct. Bioinform. 41:415–27 [Google Scholar]
  113. Wasko SS, Tay G, Schwaighofer A, Nowak C, Waite JH, Miserez A. 113.  2014. Structural proteins from whelk egg capsule with long range elasticity associated with a solid-state phase transition. Biomacromolecules 15:30–42 [Google Scholar]
  114. Tatham AS, Shewry PR. 114.  2002. Comparative structures and properties of elastic proteins. Philos. Trans. R. Soc. B 357:229–34 [Google Scholar]
  115. Fujisawa R, Tamura M. 115.  2011. Acidic bone matrix proteins and their roles in calcification. Front. Biosci. 17:1891–903 [Google Scholar]
  116. Ping H, Xie H, Su B-L, Cheng Y-B, Wang W. 116.  et al. 2015. Organized intrafibrillar mineralization, directed by a rationally designed multi-functional protein. J. Mater. Chem. B 3:4496–502 [Google Scholar]
  117. Holten-Andersen N, Harrington MJ, Birkedal H, Lee BP, Messersmith PB. 117.  et al. 2011. pH-induced metal-ligand cross-links inspired by mussel yield self-healing polymer networks with near-covalent elastic moduli. PNAS 108:2651–55 [Google Scholar]
  118. McKee MD, Hoac B, Addison WN, Barros NM, Millán JL, Chaussain C. 118.  2013. Extracellular matrix mineralization in periodontal tissues: noncollagenous matrix proteins, enzymes, and relationship to hypophosphatasia and X-linked hypophosphatemia. Periodontol. 2000 63:102–22 [Google Scholar]
  119. Chen Y, Bal BS, Gorski JP. 119.  1992. Calcium and collagen binding properties of osteopontin, bone sialoprotein, and bone acidic glycoprotein-75 from bone. J. Biol. Chem. 267:24871–78 [Google Scholar]
  120. Christensen B, Nielsen MS, Haselmann KF, Petersen TE, Sørensen ES. 120.  2005. Post-translationally modified residues of native human osteopontin are located in clusters: identification of 36 phosphorylation and five O-glycosylation sites and their biological implications. Biochem. J. 390:285–92 [Google Scholar]
  121. Dahl T, Sabsay B, Veis A. 121.  1998. Type I collagen-phosphophoryn interactions: specificity of the monomer-monomer binding. J. Struct. Biol. 123:162–68 [Google Scholar]
  122. Chirila TV, Minamisawa T, Keen I, Shiba K. 122.  2009. Effect of motif-programmed artificial proteins on the calcium uptake in a synthetic hydrogel. Macromol. Biosci. 9:959–67 [Google Scholar]
  123. Song X, Wang X, Li L, Zhang G. 123.  2014. Identification two novel nacrein-like proteins involved in the shell formation of the Pacific oyster Crassostrea gigas. Mol. Biol. Rep. 41:4273–78 [Google Scholar]
  124. Cui W, Beniash E, Gawalt E, Xu Z, Sfeir C. 124.  2013. Biomimetic coating of magnesium alloy for enhanced corrosion resistance and calcium phosphate deposition. Acta Biomater 9:8650–59 [Google Scholar]
  125. Sarikaya M, Tamerler C, Jen AK-Y, Schulten K, Baneyx F. 125.  2003. Molecular biomimetics: nanotechnology through biology. Nat. Mater. 2:577–85 [Google Scholar]
  126. Zeng HB, Hwang DS, Israelachvili JN, Waite JH. 126.  2010. Strong reversible Fe3+-mediated bridging between Dopa-containing protein films in water. PNAS 107:12850–53 [Google Scholar]
  127. Degtyar E, Mlynarczyk B, Fratzl P, Harrington MJ. 127.  2015. Recombinant engineering of reversible cross-links into a resilient biopolymer. Polymer 69:255–63 [Google Scholar]
  128. Vestergaard M, Matsumoto S, Nishikori S, Shiraki K, Hirata K, Takagi M. 128.  2008. Chelation of cadmium ions by phytochelatin synthase: role of the cysteine-rich C-terminal. Anal. Sci. 24:277–81 [Google Scholar]
  129. Park TJ, Lee SY, Heo NS, Seo TS. 129.  2010. In vivo synthesis of diverse metal nanoparticles by recombinant Escherichia coli. . Angew. Chem. Int. Ed. 49:7019–24 [Google Scholar]
  130. Bontidean I, Ahlqvist J, Mulchandani A, Chen W, Bae W. 130.  et al. 2003. Novel synthetic phytochelatin-based capacitive biosensor for heavy metal ion detection. Biosens. Bioelectron. 18:547–53 [Google Scholar]
  131. Brubaker CE, Kissler H, Wang L-J, Kaufman DB, Messersmith PB. 131.  2010. Biological performance of mussel-inspired adhesive in extrahepatic islet transplantation. Biomaterials 31:420–27 [Google Scholar]
  132. Li QC, Barret DG, Messersmith PB, Holten-Andersen N. 132.  2016. Controlling hydrogel mechanics via bio-inspired polymer-nanoparticle bond dynamics. ACS Nano 10:1317–24 [Google Scholar]
  133. Kersey FR, Loveless DM, Craig SL. 133.  2007. A hybrid polymer gel with controlled rates of cross-link rupture and self-repair. J. R. Soc. Interface 4:373–80 [Google Scholar]
  134. Yount WC, Loveless DM, Craig SL. 134.  2005. Strong means slow: dynamic contributions to the bulk mechanical properties of supramolecular networks. Angew. Chem. Int. Ed. 44:2746–48 [Google Scholar]
  135. Wilker JJ. 135.  2011. Biomaterials: redox and adhesion on the rocks. Nat. Chem. Biol. 7:579–80 [Google Scholar]
  136. Wei W, Yu J, Broomell C, Israelachvili JN, Waite JH. 136.  2013. Hydrophobic enhancement of Dopa-mediated adhesion in a mussel foot protein. J. Am. Chem. Soc. 135:377–83 [Google Scholar]
  137. Choi YS, Yang YJ, Yang B, Cha HJ. 137.  2012. In vivo modification of tyrosine residues in recombinant mussel adhesive protein by tyrosinase co-expression in Escherichia coli.. Microb. Cell Factories 11:139 [Google Scholar]
  138. Ayyadurai N, Deepankumar K, Prabhu NS, Lee S, Yun H. 138.  2011. A facile and efficient method for the incorporation of multiple unnatural amino acids into a single protein. Chem. Commun. 47:3430–32 [Google Scholar]
  139. Priftis D, Tirrell M. 139.  2012. Phase behaviour and complex coacervation of aqueous polypeptide solutions. Soft Matter 8:9396–405 [Google Scholar]
  140. Waite JH, Andersen NH, Jewhurst S, Sun C. 140.  2005. Mussel adhesion: finding the tricks worth mimicking. J. Adhes. 81:297–317 [Google Scholar]
  141. Stewart RJ, Wang CS, Song IT, Jones JP. 141.  2017. The role of coacervation and phase transitions in the sandcastle worm adhesive system. Adv. Colloid Interface Sci. 239:88–96 [Google Scholar]
  142. Jensen RA, Morse DE. 142.  1988. The bioadhesive of Phragmatopoma californica tubes: a silk-like cement containing L-DOPA. J. Comp. Physiol. B 158:317–24 [Google Scholar]
  143. Zhao H, Sun CJ, Stewart RJ, Waite JH. 143.  2005. Cement proteins of the tube-building polychaete Phragmatopoma californica. . J. Biol. Chem. 280:42938–44 [Google Scholar]
  144. Choi YS, Kang DG, Lim S, Yang YJ, Kim CS, Cha HJ. 144.  2011. Recombinant mussel adhesive protein fp-5 (MAP fp-5) as a bulk bioadhesive and surface coating material. Biofouling 27:729–37 [Google Scholar]
  145. Voets IK, de Keizer A, Stuart MAC. 145.  2009. Complex coacervate core micelles. Adv. Colloid Interface Sci.147–48300–18 [Google Scholar]
  146. Veis A. 146.  2011. A review of the early development of the thermodynamics of the complex coacervation phase separation. Adv. Colloid Interface Sci. 167:2–11 [Google Scholar]
  147. Cooper CL, Dubin PL, Kayitmazer AB, Turksen S. 147.  2005. Polyelectrolyte-protein complexes. Curr. Opin. Colloid Interface Sci. 10:52–78 [Google Scholar]
  148. Perry SL, Leon L, Hoffmann KQ, Kade MJ, Priftis D. 148.  et al. 2015. Chirality-selected phase behaviour in ionic polypeptide complexes. Nat. Commun. 6:6052 [Google Scholar]
  149. Priftis D, Laugel N, Tirrell M. 149.  2012. Thermodynamic characterization of polypeptide complex coacervation. Langmuir 28:15947–57 [Google Scholar]
  150. Kim M, Chen WG, Kang JW, Glassman MJ, Ribbeck K, Olsen BD. 150.  2015. Artificially engineered protein hydrogels adapted from the nucleoporin Nsp1 for selective biomolecular transport. Adv. Mater. 27:4207–12 [Google Scholar]
  151. DeMartini DG, Izumi M, Weaver AT, Pandolfi E, Morse DE. 151.  2015. Structures, organization, and function of reflectin proteins in dynamically tunable reflective cells. J. Biol. Chem. 290:15238–49 [Google Scholar]
  152. Chiang Y-W, Chou C-Y, Wu C-S, Lin E-L, Yoon J, Thomas EL. 152.  2015. Large-area block copolymer photonic gel films with solvent-evaporation-induced red- and blue-shift reflective bands. Macromolecules 48:4004–11 [Google Scholar]
  153. Yang YJ, Kwon Y, Choi B-H, Jung D, Seo JH. 153.  et al. 2014. Multifunctional adhesive silk fibroin with blending of RGD-bioconjugated mussel adhesive protein. Biomacromolecules 15:1390–98 [Google Scholar]
  154. Liu JC, Tirrell DA. 154.  2008. Cell response to RGD density in cross-linked artificial extracellular matrix protein films. Biomacromolecules 9:2984–88 [Google Scholar]
  155. Walde S, Kehlenbach RH. 155.  2010. The part and the whole: functions of nucleoporins in nucleocytoplasmic transport. Trends Cell Biol 20:461–69 [Google Scholar]
  156. Ribbeck K, Görlich D. 156.  2001. Kinetic analysis of translocation through nuclear pore complexes. EMBO J 20:1320–30 [Google Scholar]
  157. Wente SR, Rout MP. 157.  2010. The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2:a000562 [Google Scholar]
  158. Frey S, Görlich D. 158.  2007. A saturated FG-repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell 130:512–23 [Google Scholar]
  159. Jovanovic-Talisman T, Tetenbaum-Novatt J, McKenney AS, Zilman A, Peters R. 159.  et al. 2009. Artificial nanopores that mimic the transport selectivity of the nuclear pore complex. Nature 457:1023–27 [Google Scholar]
  160. Tao AR, DeMartini DG, Izumi M, Sweeney AM, Holt AL, Morse DE. 160.  2010. The role of protein assembly in dynamically tunable bio-optical tissues. Biomaterials 31:793–801 [Google Scholar]
  161. Izumi M, Sweeney AM, DeMartini D, Weaver JC, Powers ML. 161.  et al. 2009. Changes in reflectin protein phosphorylation are associated with dynamic iridescence in squid. J. R. Soc. Interface 7:549–60 [Google Scholar]
  162. Arnau J, Lauritzen C, Petersen GE, Pedersen J. 162.  2006. Current strategies for the use of affinity tags and tag removal for the purification of recombinant proteins. Protein Expr. Purif. 48:1–13 [Google Scholar]
  163. Sakiyama-Elbert SE, Hubbell JA. 163.  2000. Development of fibrin derivatives for controlled release of heparin-binding growth factors. J. Control. Release 65:389–402 [Google Scholar]
  164. Yeboah A, Cohen RI, Rabolli C, Yarmush ML, Berthiaume F. 164.  2016. Elastin-like polypeptides: a strategic fusion partner for biologics. Biotechnol. Bioeng. 113:1617–27 [Google Scholar]
  165. Gupta SK, Shukla P. 165.  2016. Advanced technologies for improved expression of recombinant proteins in bacteria: perspectives and applications. Crit. Rev. Biotechnol. 36:1089–98 [Google Scholar]
  166. 166. International Sericultural Commission. 2013. Silk industry: statistics International Sericultural Commission, accessed on October 19, 2016. http://inserco.org/en/statistics [Google Scholar]
  167. 167. EmergingTextiles.com. 2016. Silk yarn and cocoon prices in China. EmergingTextiles.com March 9. Accessed Oct. 19. http://www.emergingtextiles.com/?q=art&s=160309-silk-market-price [Google Scholar]
  168. Carmichael A. 168.  2015. Man-made fibers continue to grow. Textile World Feb. 3. http://www.textileworld.com/textile-world/fiber-world/2015/02/man-made-fibers-continue-to-grow/ [Google Scholar]
  169. Scott A. 169.  2014. Spider silk poised for commercial entry. Chem. Eng. News 92:22–27 [Google Scholar]
  170. 170. Tech. Univ. Munich. 2013. High-strength fibers from spider silk Press Release, Nov. 3. https://www.tum.de/en/about-tum/news/press-releases/detail/article/30514/ [Google Scholar]
  171. 171. Bolt Threads. 2016. Frequently asked questions Bolt Threads, accessed Aug. 8, 2016. https://boltthreads.com/technology/#faq [Google Scholar]
  172. 172. AMSilk GmbH. 2016. Industries. AMSilk GmbH, accessed Aug. 16, 2016. https://www.amsilk.com/industries/
  173. 173. Spiber Technol. 2016. Targeting life science Spiber Technol., accessed Aug. 16, 2016. http://www.spiber.se/targeting-life-science [Google Scholar]
  174. 174. Kraig Biocraft Laboratories. 2017. Spider Silk Kraig Biocraft Lab., accessed Feb. 16, 2017. http://www.kraiglabs.com/spider-silk/ [Google Scholar]
  175. 175. Protein Polymer Technologies. Aug. 21, 2006. Form 10QSB on 21-Aug-2006 for Protein Polymer Technologies Inc Yahoo Finance, accessed Aug. 23, 2016. https://biz.yahoo.com/e/060821/ppti.ob10qsb.html [Google Scholar]
  176. Kumar M. 176.  2003. Use of repeat sequence protein polymers in personal care compositions US Patent No. 12/062,305 [Google Scholar]
  177. Kumar M. 177.  2005. Composites of repeat sequence proteins and their preparation US Patent No. 11/990,658 [Google Scholar]
  178. 178. PhaseBio Pharmaceuticals. 2015. Development pipeline PhaseBio Pharmaceuticals, Inc., accessed Oct. 19, 2016. http://phasebio.com/pipeline/ [Google Scholar]
  179. Brubaker CE, Messersmith PB. 179.  2012. The present and future of biologically inspired adhesive interfaces and materials. Langmuir 28:2200–5 [Google Scholar]
  180. 180. Kollodis BioSciences. 2012. An ECM mimetic library for engineering surfaces to direct cell surface receptor binding specificity and signaling http://www.kollodis.com/down/MAPTrixECMLibrary.pdf [Google Scholar]
  181. Chang L-C, Xue Y, Hsieh F-H. 181.  2001. Dynamic-mechanical study of water-blown rigid polyurethane foams with and without soy flour. J. Appl. Polymer Sci. 81:2027–35 [Google Scholar]
  182. 182. United Soybean Board. 2016. 2016 Soy Products Guide Chesterfield, MO: United Soybean Board56 http://reader.mediawiremobile.com/USB/issues/106902/viewer [Google Scholar]
  183. Basak S, Punetha VD, Bisht G, Bisht SS, Sahoo NG, Cho JW. 183.  2015. Recent trends of polymer-protein conjugate application in biocatalysis: a review. Polymer Rev 55:163–98 [Google Scholar]
  184. Yin XL, Loh XJ. 184.  2016. Polymers for personal care—natural protein-based polymers. Polymers Pers. Care Prod. Cosmet. 20:18–36 [Google Scholar]
  185. McCloskey RV. 185.  2004. Creating therapeutic proteins from bioengineered systems. Biotechnol. Healthc. 1:57–61 [Google Scholar]
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