Designing protein-based biomaterials for medical applications

Acta Biomaterialia

Volumn 10, Issue 4, 2014, Pages 1542-1557

  Gagner, Jennifer E ^a   Kim, Wookhyun ^a   Chaikof, Elliot L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Biomimetic materials; Elastin like peptides; Molecular imaging; Nanotherapeutics; Recombinant polypeptides

Indexed keywords

BIOMATERIALS; BIOMIMETIC MATERIALS; BIOMIMETICS; DIAGNOSIS; FUNCTIONAL POLYMERS; GENETIC ENGINEERING; GLYCOPROTEINS; MEDICAL APPLICATIONS; MOLECULAR IMAGING; PEPTIDES; RECOMBINANT PROTEINS;

BIOLOGICAL PROPERTIES; ELASTIN-LIKE PEPTIDE; ELASTIN-LIKE POLYPEPTIDES; NANOTHERAPEUTIC; NATURALLY OCCURRING; PROTEIN SEQUENCES; PROTEIN-BASED MATERIALS; RECOMBINANT POLYPEPTIDES; STRUCTURE-FUNCTION RELATIONSHIP; THERMAL MECHANICAL PROPERTIES;

ELASTIN;

BIOMATERIAL; CELL PENETRATING PEPTIDE; ELASTIN; HYBRID PROTEIN; INORGANIC COMPOUND; ORGANIC COMPOUND; POLYPEPTIDE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BIOMEDICINE; DRUG DELIVERY SYSTEM; ENCAPSULATION; GENETIC ENGINEERING; IMAGING; PERMEABILITY; PRIORITY JOURNAL; PROTEIN STRUCTURE; SYNTHESIS;

BIOMIMETIC MATERIALS; ELASTIN-LIKE PEPTIDES; MOLECULAR IMAGING; NANOTHERAPEUTICS; RECOMBINANT POLYPEPTIDES;

ANIMALS; BIOCOMPATIBLE MATERIALS; BIOMEDICAL TECHNOLOGY; ELASTIN; HUMANS; PEPTIDES; PROTEINS; RECOMBINANT PROTEINS;

EID: 84896391062     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.10.001     Document Type: Review

References (199)

1. D.W. Urry, K.D. Urry, W. Szaflarski, and M. Nowicki Elastic-contractile model proteins: Physical chemistry, protein function and drug design and delivery Adv Drug Deliv Rev 62 2010 1404 1455
2. W. Kim, and E.L. Chaikof Recombinant elastin-mimetic biomaterials: Emerging applications in medicine Adv Drug Deliv Rev 62 2010 1468 1478
3. N. Kamaly, Z. Xiao, P.M. Valencia, A.F. Radovic-Moreno, and O.C. Farokhzad Targeted polymeric therapeutic nanoparticles: Design, development and clinical translation Chem Soc Rev 41 2012 2971
4. C.-Y. Chen, T.H. Kim, W.-C. Wu, C.-M. Huang, H. Wei, and C.W. Mount et al. pH-dependent, thermosensitive polymeric nanocarriers for drug delivery to solid tumors Biomaterials 34 2013 4501 4509
5. A.S. Tatham, and P.R. Shewry Elastomeric proteins: Biological roles, structures and mechanisms Trends Biochem Sci 25 2000 567 571
6. D.W. Urry, R.G. Shaw, and K.U. Prasad Polypentapeptide of elastin: Temperature dependence of ellipticity and correlation with elastomeric force Biochem Biophys Res Commun 130 1985 50 57
7. D.W. Urry, and T.M. Parker Mechanics of elastin: Molecular mechanism of biological elasticity and its relationship to contraction J Muscle Res Cell Motil 23 2002 543 591
8. D.W. Urry, C.H. Luan, T.M. Parker, D.C. Gowda, K.U. Prasad, and M.C. Reid et al. Temperature of polypeptide inverse temperature transition depends on mean residue hydrophobicity J Am Chem Soc 113 1991 4346 4348
9. A. D'Souza, D.S. Hart, C.R. Middaugh, and S.H. Gehrke Characterization of the changes in secondary structure and architecture of elastin-mimetic triblock polypeptides during thermal gelation Macromolecules 39 2006 7084 7091
10. R.E. Sallach, W. Cui, J. Wen, A. Martinez, V.P. Conticello, and E.L. Chaikof Elastin-mimetic protein polymers capable of physical and chemical crosslinking Biomaterials 30 2009 409 422
11. J. van Hest, and D.A. Tirrell Protein-based materials, toward a new level of structural control Chem Commun (Camb) 2001 1897 1904
12. D. Sengupta, and S.C. Heilshorn Protein-engineered biomaterials: Highly tunable tissue engineering scaffolds Tissue Eng Part B Rev 16 2010 285 293
13. J. Lee, C.W. Macosko, and D.W. Urry Elastomeric polypentapeptides cross-linked into matrixes and fibers Biomacromolecules 2 2001 170 179
14. S.R. Kakivaya, and C.A. Hoeve The glass point of elastin Proc Natl Acad Sci U S A 72 1975 3505 3507
15. M.A. Lillie, and J.M. Gosline The effects of hydration on the dynamic mechanical properties of elastin Biopolymers 29 1990 1147 1160
16. D.W. Urry Entropic elastic processes in protein mechanisms. I. Elastic structure due to an inverse temperature transition and elasticity due to internal chain dynamics J Protein Chem 7 1988 1 34
17. D.W. Urry, T. Hugel, M. Seitz, H.E. Gaub, L. Sheiba, and J. Dea et al. Elastin: A representative ideal protein elastomer Philos Trans R Soc Lond B Biol Sci 357 2002 169 184
18. T. Yamaoka, T. Tamura, Y. Seto, T. Tada, S. Kunugi, and D.A. Tirrell Mechanism for the phase transition of a genetically engineered elastin model peptide (VPGIG)40 in aqueous solution Biomacromolecules 4 2003 1680 1685
19. D.W. Urry Molecular machines: How motion and other functions of living organisms can result from reversible chemical changes Angew Chem Int Ed Engl 32 1993 819 841
20. B. Li, and V. Daggett The molecular basis of the temperature- and pH-induced conformational transitions in elastin-based peptides Biopolymers 68 2002 121 129
21. C.H. Luan, T.M. Parker, D.C. Gowda, and D.W. Urry Hydrophobicity of amino acid residues: Differential scanning calorimetry and synthesis of the aromatic analogues of the polypentapeptide of elastin Biopolymers 32 1992 1251 1261
22. D.E. Meyer, and A. Chilkoti Genetically encoded synthesis of protein-based polymers with precisely specified molecular weight and sequence by recursive directional ligation: Examples from the elastin-like polypeptide system Biomacromolecules 3 2002 357 367
23. K.P. McGrath, D.A. Tirrell, M. Kawai, T.L. Mason, and M.J. Fournier Chemical and biosynthetic approaches to the production of novel polypeptide materials Biotechnol Prog 6 1990 188 192
24. M. Shah, P.-Y. Hsueh, G. Sun, H.Y. Chang, S.M. Janib, and J.A. MacKay Biodegradation of elastin-like polypeptide nanoparticles Protein Sci 21 2012 743 750
25. J. Cappello, J. Crissman, M. Dorman, M. Mikolajczak, G. Textor, and M. Marquet et al. Genetic engineering of structural protein polymers Biotechnol Prog 6 1990 198 202
26. D.A. Tirrell, M.J. Fournier, and T.L. Mason Protein engineering for materials applications Curr Opin Struct Biol 1 1991 638 641
27. R.A. McMillan, and V.P. Conticello Synthesis and characterization of elastin-mimetic protein gels derived from a well-defined polypeptide precursor Macromolecules 33 2000 4809 4821
28. J.R. McDaniel, J.A. MacKay, F.G. Quiroz, and A. Chilkoti Recursive directional ligation by plasmid reconstruction allows rapid and seamless cloning of oligomeric genes Biomacromolecules 11 2010 944 952
29. M. Amiram, F.G. Quiroz, D.J. Callahan, and A. Chilkoti A highly parallel method for synthesizing DNA repeats enables the discovery of "smart" protein polymers Nat Mater 10 2011 141 148
30. F. Baneyx Recombinant protein expression in Escherichia coli Curr Opin Biotechnol 10 1999 411 421
31. D.C. Chow, M.R. Dreher, K. Trabbic-Carlson, and A. Chilkoti Ultra-high expression of a thermally responsive recombinant fusion protein in E. coli Biotechnol Prog 22 2006 638 646
32. A.J. Conley, J.J. Joensuu, A.M. Jevnikar, R. Menassa, and J.E. Brandle Optimization of elastin-like polypeptide fusions for expression and purification of recombinant proteins in plants Biotechnol Bioeng 103 2009 562 573
33. R.E. Sallach, V.P. Conticello, and E.L. Chaikof Expression of a recombinant elastin-like protein in Pichia pastoris Biotechnol Prog 25 2009 1810 1818
34. D.T. McPherson, J. Xu, and D.W. Urry Product purification by reversible phase transition following Escherichia coli expression of genes encoding up to 251 repeats of the elastomeric pentapeptide GVGVP Protein Expr Purif 7 1996 51 57
35. J. Lee, C.W. Macosko, and D.W. Urry Phase transition and elasticity of protein-based hydrogels J Biomater Sci Polym Ed 12 2001 229 242
36. C. Wang, N.T. Flynn, and R. Langer Controlled structure and properties of thermoresponsive nanoparticle-hydrogel composites Adv Mater 16 2004 1074 1079
37. S. Dublin, Y. Zimenkov, and V.P. Conticello Engineering responsive mechanisms to control the assembly of peptide-based nanostructures Biochem Soc Trans 37 2009 653
38. W. Kim, A. McMillan, J.P. Snyder, and V.P. Conticello A stereoelectronic effect on turn formation due to proline substitution in elastin-mimetic polypeptides J Am Chem Soc 127 2005 18121 18132
39. W. Kim, and V.P. Conticello Protein engineering methods for investigation of structure-function relationships in protein-based elastomeric materials Polym Rev (Phila Pa) 47 2007 93 119
40. L. Walker, E. Perkins, F. Kratz, and D. Raucher Cell penetrating peptides fused to a thermally targeted biopolymer drug carrier improve the delivery and antitumor efficacy of an acid-sensitive doxorubicin derivative Int J Pharm 436 2012 825 832
41. S.R. MacEwan, and A. Chilkoti Harnessing the power of cell-penetrating peptides: Activatable carriers for targeting systemic delivery of cancer therapeutics and imaging agents Wiley Interdiscip Rev Nanomed Nanobiotechnol 5 2012 31 48
42. W. Hassouneh, K. Fischer, S.R. MacEwan, R. Branscheid, C.L. Fu, and R. Liu et al. Unexpected multivalent display of proteins by temperature triggered self-assembly of elastin-like polypeptide block copolymers Biomacromolecules 13 2012 1598 1605
43. D.W. Urry, D.K. Chang, N.R. Krishna, D.H. Huang, T.L. Trapane, and K.U. Prasad Two-dimensional proton NMR studies on poly(VPGVG) and its cyclic conformational correlate, cyclo(VPGVG)3 Biopolymers 28 1989 819 833
44. F. Sciortino, D.W. Urry, M.U. Palma, and K.U. Prasad Self-assembly of a bioelastomeric structure: Solution dynamics and the spinodal and coacervation lines Biopolymers 29 1990 1401 1407
45. K. Nagapudi, W.T. Brinkman, J. Leisen, B.S. Thomas, E.R. Wright, and C. Haller et al. Protein-based thermoplastic elastomers Macromolecules 38 2005 345 354
46. D.W. Urry Physical chemistry of biological free energy transduction as demonstrated by elastic protein-based polymers J Phys Chem B 101 1997 11007 11028
47. J.A. Johnson, Y.Y. Lu, J.A. Van Deventer, and D.A. Tirrell Residue-specific incorporation of non-canonical amino acids into proteins: Recent developments and applications Curr Opin Chem Biol 14 2010 774 780
48. M.G. Hoesl, and N. Budisa In vivo incorporation of multiple noncanonical amino acids into proteins Angew Chem Int Ed Engl 50 2011 2896 2902
49. J. Tcherkezian, P.A. Brittis, F. Thomas, P.P. Roux, and J.G. Flanagan Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation Cell 141 2010 632 644
50. M.M. Zhang, L.K. Tsou, G. Charron, A.S. Raghavan, and H.C. Hang Tandem fluorescence imaging of dynamic S-acylation and protein turnover Proc Natl Acad Sci U S A 107 2010 8627 8632
51. M.D. Shoulders, K.A. Satyshur, K.T. Forest, and R.T. Raines Stereoelectronic and steric effects in side chains preorganize a protein main chain Proc Natl Acad Sci U S A 107 2010 559 564
52. T. Steiner, P. Hess, J.H. Bae, B. Wiltschi, L. Moroder, and N. Budisa Synthetic biology of proteins: Tuning GFPs folding and stability with fluoroproline PLoS One 3 2008 e1680
53. C. Wolschner, A. Giese, H.A. Kretzschmar, R. Huber, L. Moroder, and N. Budisa Design of anti- and pro-aggregation variants to assess the effects of methionine oxidation in human prion protein Proc Natl Acad Sci U S A 106 2009 7756 7761
54. A. Goulding, S. Shrestha, K. Dria, E. Hunt, and S.K. Deo Red fluorescent protein variants with incorporated non-natural amino acid analogues Protein Eng Des Sel 21 2008 101 106
55. L. Merkel, M.G. Hoesl, M. Albrecht, A. Schmidt, and N. Budisa Blue fluorescent amino acids as in vivo building blocks for proteins ChemBioChem 11 2010 305 314
56. R.J. Mart, R.D. Osborne, M.M. Stevens, and R.V. Ulijn Peptide-based stimuli-responsive biomaterials Soft Matter 2 2006 822
57. D.K. Chang, and D.W. Urry The molecular dynamics of the β-spiral of the polypentapeptide of elastin in "state III" with 2.9 pentamers per turn Theochemistry 199 1989 303 312
58. J.T. Cirulis, and F.W. Keeley Kinetics and morphology of self-assembly of an elastin-like polypeptide based on the alternating domain arrangement of human tropoelastin Biochemistry 49 2010 5726 5733
59. M.T. Krejchi, E.D. Atkins, A.J. Waddon, M.J. Fournier, T.L. Mason, and D.A. Tirrell Chemical sequence control of beta-sheet assembly in macromolecular crystals of periodic polypeptides Science 265 1994 1427 1432
60. D.A. Tirrell, S.M. Yu, V.P. Conticello, G. Zhang, C. Kayser, and M.J. Fournier et al. Smectic ordering in solutions and films of a rod-like polymer owing to monodispersity of chain length Nature 389 1997 167 170
61. W.A. Petka, J.L. Harden, K.P. McGrath, D. Wirtz, and D.A. Tirrell Reversible hydrogels from self-assembling artificial proteins Science 281 1998 389 392
62. N. Annabi, A. Fathi, S.M. Mithieux, P. Martens, and A.S. Weiss The effect of elastin on chondrocyte adhesion and proliferation on poly (É-caprolactone)/elastin composites Biomaterials 2011 1517 1525
63. L. Martín, M. Alonso, A. Girotti, F.J. Arias, and J.C. Rodríguez-Cabello Synthesis and characterization of macroporous thermosensitive hydrogels from recombinant elastin-like polymers Biomacromolecules 10 2009 3015 3022
64. X. Wu, M.E. Levenston, and E.L. Chaikof A constitutive model for protein-based materials Biomaterials 27 2006 5315 5325
65. X. Wu, R. Sallach, C.A. Haller, J.A. Caves, K. Nagapudi, and V.P. Conticello et al. Alterations in physical cross-linking modulate mechanical properties of two-phase protein polymer networks Biomacromolecules 6 2005 3037 3044
66. X. Wu, R.E. Sallach, J.M. Caves, V.P. Conticello, and E.L. Chaikof Deformation responses of a physically cross-linked high molecular weight elastin-like protein polymer Biomacromolecules 9 2008 1787 1794
67. T. Lee, A. Cooper, R.P. Apkarian, and V.P. Conticello Thermo-reversible self-assembly of nanoparticles derived from elastin-mimetic polypeptides Adv Mater 12 2000 1105 1110
68. M.R. Dreher, A.J. Simnick, K. Fischer, R.J. Smith, A. Patel, and M. Schmidt et al. Temperature triggered self-assembly of polypeptides into multivalent spherical micelles J Am Chem Soc 130 2008 687 694
69. R.E. Sallach, J. Leisen, J.M. Caves, E. Fotovich, R.P. Apkarian, and V.P. Conticello et al. A permanent change in protein mechanical responses can be produced by thermally-induced microdomain mixing J Biomater Sci Polym Ed 20 2009 1629 1644
70. W. Kim, J. Thévenot, E. Ibarboure, S. Lecommandoux, and E.L. Chaikof Self-assembly of thermally responsive amphiphilic diblock copolypeptides into spherical micellar nanoparticles Angew Chem Int Ed Engl 49 2010 4257 4260
71. L. Martín, E. Castro, A. Ribeiro, M. Alonso, and J.C. Rodríguez-Cabello Temperature-triggered self-assembly of elastin-like block co-recombinamers: The controlled formation of micelles and vesicles in an aqueous medium Biomacromolecules 13 2012 293 298
72. O.S. Rabotyagova, P. Cebe, and D.L. Kaplan Self-assembly of genetically engineered spider silk block copolymers Biomacromolecules 10 2009 229 236
73. P.L. Benitez, J.A. Sweet, H. Fink, K.P. Chennazhi, S.V. Nair, and A. Enejder et al. Sequence-specific crosslinking of electrospun, elastin-like protein preserves bioactivity and native-like mechanics Adv Healthc Mater 2 2012 114 118
74. J.D. Hartgerink, E. Beniash, and S.I. Stupp Self-assembly and mineralization of peptide-amphiphile nanofibers Science 294 2001 1684 1687
75. S. Aluri, M.K. Pastuszka, A.S. Moses, and J.A. MacKay Elastin-like peptide amphiphiles form nanofibers with tunable length Biomacromolecules 13 2012 2645 2654
76. X. Hu, P. Cebe, A.S. Weiss, F. Omenetto, and D.L. Kaplan Protein-based composite materials Mater Today 15 2012 208 215
77. W.F. Daamen, J.H. Veerkamp, J.C.M. van Hest, and T.H. van Kuppevelt Elastin as a biomaterial for tissue engineering Biomaterials 28 2007 4378 4398
78. J.A. Jansen, W.F. Daamen, and T.H. van Kuppevelt Controlled fabrication of triple layered and molecularly defined collagen/elastin vascular grafts resembling the native blood vessel Acta Biomater 6 2010 4666 4674
79. R. Anumolu, J.A. Gustafson, J.J. Magda, J. Cappello, H. Ghandehari, and L.F. Pease III Fabrication of highly uniform nanoparticles from recombinant silk-elastin-like protein polymers for therapeutic agent delivery ACS Nano 5 2011 5374 5382
80. R. Machado, J. Azevedo-Silva, C. Correia, and T. Collins High level expression and facile purification of recombinant silk-elastin-like polymers in auto induction shake flask cultures AMB Express 3 2013 1 15
81. Z. Megeed, J. Cappello, and H. Ghandehari Genetically engineered silk-elastinlike protein polymers for controlled drug delivery Adv Drug Deliv Rev 54 2002 1075 1091
82. K. Numata, and D.L. Kaplan Silk-based delivery systems of bioactive molecules Adv Drug Deliv Rev 62 2010 1497 1508
83. J.A. Gustafson, and H. Ghandehari Silk-elastin-like protein polymers for matrix-mediated cancer gene therapy Adv Drug Deliv Rev 62 2010 1509 1523
84. W. Qiu, W. Teng, J. Cappello, and X. Wu Wet-spinning of recombinant silk-elastin-like protein polymer fibers with high tensile strength and high deformability Biomacromolecules 10 2009 602 608
85. X. Wang, T. Yucel, Q. Lu, X. Hu, and D.L. Kaplan Silk nanospheres and microspheres from silk/pva blend films for drug delivery Biomaterials 31 2010 1025 1035
86. A. Chen, Y. Li, J. Hu, X. Liu, J. Li, and Y. Zhang et al. Fabrication of silk fibroin nanoparticles for controlled drug delivery J Nanopart Res 14 2012 736 746
87. G.H. Altman, F. Diaz, C. Jakuba, T. Calabro, R.L. Horan, and J. Chen et al. Silk-based biomaterials Biomaterials 24 2003 401 416
88. S. Winkler, D. Wilson, and D.L. Kaplan Controlling β-sheet assembly in genetically engineered silk by enzymatic phosphorylation/dephosphorylation Biochemistry 39 2000 12739 12746
89. S.K. Holmgren, L.E. Bretscher, K.M. Taylor, and R.T. Raines A hyperstable collagen mimic Chem Biol 6 1999 63 64
90. P. Hobza, J. Hurych, and R. Zahradník Quantum chemical study of the mechanism of collagen proline hydroxylation Biochim Biophys Acta 304 1973 466 472
91. K.A. Faraj, T.H. van Kuppevelt, and W.F. Daamen Construction of collagen scaffolds that mimic the three-dimensional architecture of specific tissues Tissue Eng 13 2007 2387 2394
92. A. Shamloo, H. Xu, and S. Heilshorn Mechanisms of vascular endothelial growth factor-induced pathfinding by endothelial sprouts in biomaterials Tissue Eng Part A 18 2012 320 330
93. L. Cen, W. Liu, L. Cui, W. Zhang, and Y. Cao Collagen tissue engineering: Development of novel biomaterials and applications Pediatr Res 63 2008 492 496
94. C.M. Curtin, G.M. Cunniffe, F.G. Lyons, K. Bessho, G.R. Dickson, and G.P. Duffy et al. Innovative collagen nano-hydroxyapatite scaffolds offer a highly efficient non-viral gene delivery platform for stem cell-mediated bone formation Adv Mater 24 2012 749 754
95. A. Bracalello, V. Santopietro, M. Vassalli, G. Marletta, R. Del Gaudio, and B. Bochicchio et al. Design and production of a chimeric resilin-, elastin-, and collagen-like engineered polypeptide Biomacromolecules 12 2011 2957 2965
96. L. Li, Z. Tong, X. Jia, and K.L. Kiick Resilin-like polypeptide hydrogels engineered for versatile biological function Soft Matter 9 2012 665
97. L. Ayres, M.R.J. Vos, P.J.H.M. Adams, I.O. Shklyarevskiy, and J.C.M. van Hest Elastin-based side-chain polymers synthesized by ATRP Macromolecules 36 2003 5967 5973
98. M. Pechar, J. Brus, L. Kostka, Č. Koňák, M. Urbanová, and M. Šlouf Thermoresponsive self-assembly of short elastin-like polypentapeptides and their poly(ethylene glycol) derivatives Macromol Biosci 7 2007 56 69
99. O. Rathore, and D.Y. Sogah Nanostructure formation through β-sheet self-assembly in silk-based materials Macromolecules 34 2001 1477 1486
100. Y. Huang, C.-Y. Chiang, S.K. Lee, Y. Gao, E.L. Hu, and J. De Yoreo et al. Programmable assembly of nanoarchitectures using genetically engineered viruses Nano Lett 5 2005 1429 1434
101. Y. Lee, J. Kim, D.S. Yun, Y.S. Nam, Y. Shao-Horn, and A.M. Belcher Virus-templated Au and Au-Pt core-shell nanowires and their electrocatalytic activities for fuel cell applications Energy Environ Sci 5 2012 8328
102. R. Djalali, Y.-F. Chen, and H. Matsui Au nanowire fabrication from sequenced histidine-rich peptide J Am Chem Soc 124 2002 13660 13661
103. Y.N. Tan, J.Y. Lee, and D.I.C. Wang Uncovering the design rules for peptide synthesis of metal nanoparticles J Am Chem Soc 132 2010 5677 5686
104. C.-L. Chen, P. Zhang, and N.L. Rosi A new peptide-based method for the design and synthesis of nanoparticle superstructures: Construction of highly ordered gold nanoparticle double helices J Am Chem Soc 130 2008 13555 13557
105. J.M. Slocik, M.O. Stone, and R.R. Naik Synthesis of gold nanoparticles using multifunctional peptides Small 1 2005 1048 1052
106. D.L. Minor Jr, and P.S. Kim Measurement of the β-sheet-forming propensities of amino acids Nature 367 1994 660 663
107. C. Song, G. Zhao, P. Zhang, and N.L. Rosi Expeditious synthesis and assembly of sub-100 nm hollow spherical gold nanoparticle superstructures J Am Chem Soc 132 2010 14033 14035
108. L. Hwang, G. Zhao, P. Zhang, and N.L. Rosi Size-controlled peptide-directed synthesis of hollow spherical gold nanoparticle superstructures Small 7 2011 1939 1942
109. N. Nath, and A. Chilkoti Interfacial phase transition of an environmentally responsive elastin biopolymer adsorbed on functionalized gold nanoparticles studied by colloidal surface plasmon resonance J Am Chem Soc 123 2001 8197 8202
110. H.-C. Huang, P. Koria, S.M. Parker, L. Selby, Z. Megeed, and K. Rege Optically responsive gold nanorod-polypeptide assemblies Langmuir 24 2008 14139 14144
111. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori Tumor vascular permeability and the EPR effect in macromolecular therapeutics: A review J Control Release 65 2000 271 284
112. A.N. Lukyanov, W.C. Hartner, and V.P. Torchilin Increased accumulation of PEG-PE micelles in the area of experimental myocardial infarction in rabbits J Control Release 94 2004 187 193
113. W. Kim, C. Brady, and E.L. Chaikof Amphiphilic protein micelles for targeted in vivo imaging Acta Biomater 8 2012 2476 2482
114. M.R. Dreher, W. Liu, C.R. Michelich, M.W. Dewhirst, F. Yuan, and A. Chilkoti Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers J Natl Cancer Inst 98 2006 335 344
115. F. Heitz, M.C. Morris, and G. Divita Twenty years of cell-penetrating peptides: From molecular mechanisms to therapeutics Br J Pharmacol 157 2009 195 206
116. E. Koren, and V.P. Torchilin Cell-penetrating peptides: Breaking through to the other side Trends Mol Med 18 2012 385 393
117. A.D. Frankel, and C.O. Pabo Cellular uptake of the Tat protein from human immunodeficiency virus Cell 55 1988 1189 1193
118. D. Derossi, S. Calvet, A. Trembleau, A. Brunissen, G. Chassaing, and A. Prochiantz Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent J Biol Chem 271 1996 18188 18193
119. K. Sadler, K.D. Eom, J.-L. Yang, Y. Dimitrova, and J.P. Tam Translocating proline-rich peptides from the antimicrobial peptide bactenecin 7 Biochemistry 41 2002 14150 14157
120. I. Massodi, G.L. Bidwell, and D. Raucher Evaluation of cell penetrating peptides fused to elastin-like polypeptide for drug delivery J Control Release 108 2005 396 408
121. J.B. Rothbard, T.C. Jessop, R.S. Lewis, B.A. Murray, and P.A. Wender Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells J Am Chem Soc 126 2004 9506 9507
122. I. Nakase, A. Tadokoro, N. Kawabata, T. Takeuchi, H. Katoh, and K. Hiramoto et al. Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis Biochemistry 46 2007 492 501
123. S.R. MacEwan, and A. Chilkoti Digital switching of local arginine density in a genetically encoded self-assembled polypeptide nanoparticle controls cellular uptake Nano Lett 12 2012 3322 3328
124. A.J. Simnick, C.A. Valencia, R. Liu, and A. Chilkoti Morphing low-affinity ligands into high-avidity nanoparticles by thermally triggered self-assembly of a genetically encoded polymer ACS Nano 4 2010 2217 2227
125. A.J. Simnick, M. Amiram, W. Liu, G. Hanna, M.W. Dewhirst, and C.D. Kontos et al. In vivo tumor targeting by a NGR-decorated micelle of a recombinant diblock copolypeptide J Control Release 155 2011 144 151
126. D. Topcic, W. Kim, J.K. Holien, F. Jia, P.C. Armstrong, and J.D. Hohmann et al. An activation-specific platelet inhibitor that can be turned on/fff by medically used hypothermia Arterioscler Thromb Vasc Biol 31 2011 2015 2023
127. G. Sun, P.-Y. Hsueh, S.M. Janib, S. Hamm-Alvarez, and J. Andrew MacKay Design and cellular internalization of genetically engineered polypeptide nanoparticles displaying adenovirus knob domain J Control Release 155 2011 218 226
128. E.G. Soltesz, R.G. Laurence, A.M. De Grand, L.H. Cohn, T. Mihaljevic, and J.V. Frangioni Image-guided quantification of cardioplegia delivery during cardiac surgery Health Sociol Rev 10 2007 E381 E386
129. M.A. Funovics, H. Alencar, H.S. Su, K. Khazaie, R. Weissleder, and U.U. Mahmood Miniaturized multichannel near infrared endoscope for mouse imaging Mol Imaging 2 2003 350 357
130. K.E. Adams, S. Ke, S. Kwon, F. Liang, Z. Fan, and Y. Lu et al. Comparison of visible and near-infrared wavelength-excitable fluorescent dyes for molecular imaging of cancer J Biomed Opt 12 2007 024017
131. K. Chang, and F. Jaffer Advances in fluorescence imaging of the cardiovascular system J Nucl Cardiol 15 2008 417 428
132. H.S. Choi, S.L. Gibbs, J.H. Lee, S.H. Kim, Y. Ashitate, and F. Liu et al. Targeted zwitterionic near-infrared fluorophores for improved optical imaging Nat Biotechnol 31 2013 148 153
133. C.-L. Chen, and N.L. Rosi Peptide-based methods for the preparation of nanostructured inorganic materials Angew Chem Int Ed Engl 49 2010 1924 1942
134. T.S. Troutman, J.K. Barton, and M. Romanowski Biodegradable plasmon resonant nanoshells Adv Mater 20 2008 2604 2608
135. Lin C-AJ, Lee C-H, Hsieh J-T, Yu W-C, Yang H-Z, Li JK, et al. Synthesis and surface modification of highly fluorescent gold nanoclusters and their exploitation for cellular labeling. In: Proc SPIE, vol. 7575. International Society for Optics and Photonics; 2010, p. 757506-8.
136. A.M. Smith, H. Duan, A.M. Mohs, and S. Nie Bioconjugated quantum dots for in vivo molecular and cellular imaging Adv Drug Deliv Rev 60 2008 1226 1240
137. P. Zrazhevskiy, and X. Gao Quantum dot imaging platform for single-cell molecular profiling Nat Commun 4 2013 1619
138. T. Pons, E. Pic, N. Lequeux, E. Cassette, L. Bezdetnaya, and F. Guillemin et al. Cadmium-free CuInS2/ZnS quantum dots for sentinel lymph node imaging with reduced toxicity ACS Nano 4 2010 2531 2538
139. J. Park, C. Dvoracek, K.H. Lee, J.F. Galloway, H.-E.C. Bhang, and M.G. Pomper et al. Imaging: CuInSe/ZnS core/shell NIR quantum dots for biomedical imaging Small 7 2011 3106
140. H. Mattoussi, J.M. Mauro, E.R. Goldman, G.P. Anderson, V.C. Sundar, and F.V. Mikulec et al. Self-assembly of CdSe-ZnS quantum dot bioconjugates using an engineered recombinant orotein J Am Chem Soc 122 2000 12142 12150
141. S.M. Janib, A.S. Moses, and J.A. MacKay Imaging and drug delivery using theranostic nanoparticles Adv Drug Deliv Rev 62 2010 1052 1063
142. E.M. Sevick-Muraca, J.P. Houston, and M. Gurfinkel Fluorescence-enhanced, near infrared diagnostic imaging with contrast agents Curr Opin Chem Biol 6 2002 642 650
143. S. Mallidi, G.P. Luke, and S. Emelianov Photoacoustic imaging in cancer detection, diagnosis, and treatment guidance Trends Biotechnol 29 2011 213 221
144. C.L. Bayer, Y.-S. Chen, S. Kim, S. Mallidi, K.V. Sokolov, and S. Emelianov Multiplex photoacoustic molecular imaging using targeted silica-coated gold nanorods Biomedical Optics Express 2 2011 1828 1835
145. S.M. Janib, S. Liu, R. Park, M.K. Pastuszka, P. Shi, and A.S. Moses et al. Kinetic quantification of protein polymer nanoparticles using non-invasive imaging Integr Biol 5 2012 183
146. H. Cai, J. Fissekis, and P.S. Conti Synthesis of a novel bifunctional chelator AmBaSar based on sarcophagine for peptide conjugation and (64)Cu radiolabelling Dalton Trans 5 2009 395 400
147. D.Y. Furgeson, M.R. Dreher, and A. Chilkoti Structural optimization of a "smart" doxorubicin-polypeptide conjugate for thermally targeted delivery to solid tumors J Control Release 110 2006 362 369
148. M.R. Dreher, D. Raucher, N. Balu, O.M. Colvin, S.M. Ludeman, and A.A. Chilkoti Evaluation of an elastin-like polypeptide-doxorubicin conjugate for cancer therapy J Control Release 91 2003 31 43
149. D.E. Meyer, B.C. Shin, G.A. Kong, M.W. Dewhirst, and A. Chilkoti Drug targeting using thermally responsive polymers and local hyperthermia J Control Release 74 2001 213 224
150. J. Andrew MacKay, M. Chen, J.R. McDaniel, W. Liu, A.J. Simnick, and A. Chilkoti Self-assembling chimeric polypeptide-doxorubicin conjugate nanoparticles that abolish tumours after a single injection Nat Mater 8 2009 993 999
151. P.C. Bessa, R. Machado, S. Nürnberger, D. Dopler, A. Banerjee, and A.M. Cunha et al. Thermoresponsive self-assembled elastin-based nanoparticles for delivery of BMPs J Control Release 142 2010 312 318
152. R. Herrero-Vanrell, A.C. Rincón, M. Alonso, V. Reboto, I.T. Molina-Martinez, and J.C. Rodríguez-Cabello Self-assembled particles of an elastin-like polymer as vehicles for controlled drug release J Control Release 102 2005 113 122
153. P. Schmidt, J. Dybal, J.C. Rodríguez-Cabello, and V. Reboto Role of water in structural changes of poly(AVGVP) and poly(GVGVP) studied by FTIR and Raman spectroscopy and ab initio calculations Biomacromolecules 6 2005 697 706
154. S. Moktan, E. Perkins, F. Kratz, and D. Raucher Thermal targeting of an acid-sensitive doxorubicin conjugate of elastin-like polypeptide enhances the therapeutic efficacy compared with the parent compound in vivo Mol Cancer Ther 11 2012 1547 1556
155. R.B. Weiss, R.C. Donehower, P.H. Wiernik, T. Ohnuma, R.J. Gralla, and D.L. Trump et al. Hypersensitivity reactions from taxol J Clin Oncol 8 1990 1263 1268
156. S. Moktan, C. Ryppa, F. Kratz, and D. Raucher A thermally responsive biopolymer conjugated to an acid-sensitive derivative of paclitaxel stabilizes microtubules, arrests cell cycle, and induces apoptosis Invest New Drugs 30 2010 236 248
157. T.H. Wang, H.S. Wang, and Y.K. Soong Paclitaxel-induced cell death: Where the cell cycle and apoptosis come together Cancer 88 2000 2619 2628
158. W. Kim, J. Xiao, and E.L. Chaikof Recombinant amphiphilic protein micelles for drug delivery Langmuir 27 2011 14329 14334
159. W. Liu, J.A. MacKay, M.R. Dreher, M. Chen, J.R. McDaniel, and A.J. Simnick et al. Injectable intratumoral depot of thermally responsive polypeptide-radionuclide conjugates delays tumor progression in a mouse model J Control Release 144 2010 2 9
160. A.A. Manzoor, L.H. Lindner, C.D. Landon, J.Y. Park, A.J. Simnick, and M.R. Dreher et al. Overcoming limitations in nanoparticle drug delivery: Triggered, intravascular release to improve drug penetration into tumors Cancer Res 72 2012 5566 5575
161. D.R. Gius, S.A. Ezhevsky, M. Becker-Hapak, H. Nagahara, M.C. Wei, and S.F. Dowdy Transduced p16INK4a peptides inhibit hypophosphorylation of the retinoblastoma protein and cell cycle progression prior to activation of Cdk2 complexes in late G1 Cancer Res 59 1999 2577 2580
162. Y. Miyamoto, K.K. Fujimoto, R. Doi, A. Otaka, N. Fujii, and M. Imamura Trojan p16 peptide suppresses pancreatic cancer growth and prolongs survival in mice Clin Cancer Res 8 2002 1271 1276
163. H.M. Ellerby, W. Arap, L.M. Ellerby, R. Kain, R. Andrusiak, and G.D. Rio et al. Anti-cancer activity of targeted pro-apoptotic peptides Nat Med 5 1999 1032 1038
164. X.-X. Zhang, H.S. Eden, and X.X. Chen Peptides in cancer nanomedicine: Drug carriers, targeting ligands and protease substrates J Control Release 159 2012 2 13
165. K.L. Ball, S. Lain, R. Fâhraeus, C. Smythe, and D.P. Lane Cell-cycle arrest and inhibition of Cdk4 activity by small peptides based on the carboxy-terminal domain of p21WAF1 Curr Biol 7 1997 10
166. G.L. Bidwell, A.A. Whittom, E. Thomas, D. Lyons, M.D. Hebert, and D. Raucher A thermally targeted peptide inhibitor of symmetrical dimethylation inhibits cancer-cell proliferation Peptides 31 2010 8
167. G.L. Bidwell, and D. Raucher Application of thermally responsive polypeptides directed against c-Myc transcriptional function for cancer therapy Mol Cancer Ther 4 2005 1076 1085
168. G.L. Bidwell, A.N. Davis, and D. Raucher Targeting a c-Myc inhibitory polypeptide to specific intracellular compartments using cell penetrating peptides J Control Release 135 2009 2 10
169. G.L. Bidwell, E. Perkins, and D. Raucher A thermally targeted c-Myc inhibitory polypeptide inhibits breast tumor growth Cancer Lett 319 2012 136 143
170. G.L. Bidwell, E. Perkins, J. Hughes, M. Khan, J.R. James, and D. Raucher Thermally targeted delivery of a c-Myc inhibitory polypeptide inhibits tumor progression and extends survival in a rat glioma model PLoS One 8 2013 e55104
171. S.M. Hearst, L.R. Walker, Q. Shao, M. Lopez, D. Raucher, and P.J.S. Vig The design and delivery of a thermally responsive peptide to inhibit S100B-mediated neurodegeneration Neuroscience 197 2011 369 380
172. S. Moktan, and D. Raucher Anticancer activity of proapoptotic peptides is highly improved by thermal targeting using elastin-like polypeptides Int J Pept Res Ther 18 2012 227 237
173. W.F. McKay, S.M. Peckham, and J.M. Badura A comprehensive clinical review of recombinant human bone morphogenetic protein-2 (INFUSE Bone Graft) Int Orthop 31 2007 729 734
174. O.C. Thamm, P. Koenen, N. Bader, A. Schneider, S. Wutzler, and E.A. Neugebauer et al. Acute and chronic wound fluids influence keratinocyte function differently Int Wound J 2013 10.1111/iwj.12069
175. S. Kobsa, N.J. Kristofik, A.J. Sawyer, A.L.M. Bothwell, T.R. Kyriakides, and W.M.W. Saltzman An electrospun scaffold integrating nucleic acid delivery
176. Y.-P. Xia, Y. Zhao, J. Marcus, P.A. Jimenez, S.M. Ruben, and P.A. Moore et al. Effects of keratinocyte growth factor-2 (KGF-2) on wound healing in an ischaemia-impaired rabbit ear model and on scar formation J Pathol 188 1999 431 438
177. P. Koria, H. Yagi, Y. Kitagawa, Z. Megeed, Y. Nahmias, and R. Sheridan et al. Self-assembling elastin-like peptides growth factor chimeric nanoparticles for the treatment of chronic wounds Proc Natl Acad Sci U S A 108 2011 1034 1039
178. J.-H. Jang, D.V. Schaffer, and L.D. Shea Engineering biomaterial systems to enhance viral vector gene delivery Mol Ther 19 2011 1407 1415
179. M. Haider, Z. Megeed, and H. Ghandehari Genetically engineered polymers: Status and prospects for controlled release J Control Release 95 2004 1 26
180. von A. Wald Cresce, R. Dandu, A. Burger, J. Cappello, and H. Ghandehari Characterization and real-time imaging of gene expression of adenovirus embedded silk-elastinlike protein polymer hydrogels Mol Pharm 5 2008 891 897
181. A. Hatefi, J. Cappello, and H.H. Ghandehari Adenoviral gene delivery to solid tumors by recombinant silk-elastinlike protein polymers Pharm Res 24 2007 773 779
182. R. Price, J. Gustafson, K. Greish, J. Cappello, L. McGill, and H. Ghandehari Comparison of silk-elastinlike protein polymer hydrogel and poloxamer in matrix-mediated gene delivery Int J Pharm 427 2012 97 104
183. T.-H.H. Chen, Y. Bae, and D.Y. Furgeson Intelligent biosynthetic nanobiomaterials (IBNs) for hyperthermic gene delivery Pharm Res 25 2007 683 691
184. T.-H.H. Chen, Y. Bae, D.Y. Furgeson, and G.S. Kwon Biodegradable hybrid recombinant block copolymers for non-viral gene transfection Int J Pharm 427 2012 105 112
185. K. Itaka, T. Ishii, Y. Hasegawa, and K. Kataoka Biodegradable polyamino acid-based polycations as safe and effective gene carrier minimizing cumulative toxicity Biomaterials 31 2010 8
186. M. Mehdizadeh, and J. Yang Design strategies and applications of tissue bioadhesives Macromol Biosci 13 2012 271 288
187. M. Larregola, S. Moore, and N. Budisa Congeneric bio-adhesive mussel foot proteins designed by modified prolines revealed a chiral bias in unnatural translation Biochem Biophys Res Commun 421 2012 646 650
188. F.A. Jaffer, M.A. Calfon, A. Rosenthal, G. Mallas, R.N. Razansky, and A. Mauskapf et al. Two-dimensional intravascular near-infrared fluorescence molecular maging of inflammation in atherosclerosis and stent-induced vascular injury J Am Coll Cardiol 57 2011 2516 2526
189. M. Dreher, and A. Chilkoti Intravital laser scanning confocal microscopy for drug carrier imaging in solid tumors Mam 13 2007
190. J.R. McDaniel, D.J. Callahan, and A. Chilkoti Drug delivery to solid tumors by elastin-like polypeptides Adv Drug Deliv Rev 62 2010 1456 1467
191. J.R. McDaniel, J. Bhattacharyya, K.B. Vargo, W. Hassouneh, D.A. Hammer, and A. Chilkoti Self-Assembly of thermally responsive nanoparticles of a genetically encoded peptide polymer by drug conjugation Angew Chemie Int Ed 52 2012 1683 1687
192. M.R. Dreher, W. Liu, C.R. Michelich, M.W. Dewhirst, and A. Chilkoti Thermal cycling enhances the accumulation of a temperature-sensitive biopolymer in solid tumors Cancer Res 67 2007 4418 4424
193. M.H. Falk, and R.D. Issels Hyperthermia in oncology Int J Hyperthermia 17 2001 1 18
194. P.I. Soares, I.M. Ferreira, R.A. Igreja, C.M. Novo, and J.P. Borges Application of hyperthermia for cancer treatment: Recent patents review Recent Pat Anticancer Drug Discov 7 2012 64 73
195. S.R. Gameiro, J.P. Higgins, M.R. Dreher, D.L. Woods, G. Reddy, and B.J. Wood et al. Combination therapy with local radiofrequency ablation and systemic vaccine enhances antitumor immunity and mediates local and distal tumor regression PLoS One 8 2013 e70417
196. R.B. Cameron, and D. Hou Intraoperative hyperthermic chemotherapy perfusion for malignant pleural mesothelioma: An in vitro evaluation J Thorac Cardiovasc Surg 145 2013 496 504
197. T.J. Vogl, P. Farshid, N.N.N. Naguib, and S. Zangos Thermal ablation therapies in patients with breast cancer liver metastases: A review Eur Radiol 23 2013 797 804
198. P. Wust, U. Gneveckow, P. Wust, U. Gneveckow, M. Johannsen, and D. Böhmer et al. Magnetic nanoparticles for interstitial thermotherapy - feasibility, tolerance and achieved temperatures Int J Hyperthermia 22 2006 673 685
199. W.J. Cook, H. Einspahr, T.L. Trapane, D.W. Urry, and C.E. Bugg Crystal structure and conformation of the cyclic trimer of a repeat pentapeptide of elastin, cyclo-(l-valyl-l-prolylglycyl-l-valylglycyl)3 J Am Chem Soc 102 1980 5502 5505