Silk-elastin-like protein biomaterials for the controlled delivery of therapeutics

Expert Opinion on Drug Delivery

Volumn 12, Issue 5, 2015, Pages 779-791

  Huang, Wenwen ^a   Rollett, Alexandra ^a   Kaplan, David L ^a  

^a Tufts University   (United States)

Author keywords

Drug delivery; Gene delivery; Hydrogel; Nanoparticle; Protein; Self assembly; Silk elastin; Stimuli responsive

Indexed keywords

BIOMATERIAL; ELASTIN; NANOCARRIER; NANOPARTICLE; SILK; SILK ELASTIN LIKE PROTEIN; UNCLASSIFIED DRUG; HYDROGEL; POLYMER; RECOMBINANT PROTEIN;

BIOSYNTHESIS; CHEMICAL STRUCTURE; DRUG DELIVERY SYSTEM; DRUG RELEASE; HYDROGEL; IONIC STRENGTH; PH; PHYSICAL CHEMISTRY; REVIEW; SEQUENCE STRUCTURE FUNCTION RELATIONSHIP; ANIMAL; CHEMISTRY; GENETIC ENGINEERING; HUMAN;

ANIMALS; BIOCOMPATIBLE MATERIALS; DRUG DELIVERY SYSTEMS; ELASTIN; GENETIC ENGINEERING; HUMANS; HYDROGELS; POLYMERS; RECOMBINANT PROTEINS; SILK;

EID: 84928350060     PISSN: 17425247     EISSN: 17447593     Source Type: Journal    
DOI: 10.1517/17425247.2015.989830     Document Type: Review

References (129)

1. Nerini IF, Morosi L, Zucchetti M, et al. Intratumor heterogeneity and its impact on drug distribution and sensitivity. Clin Pharmacol Ther 2014;96:224-38
2. Yuan F. Transvascular drug delivery in solid tumors. Semin Radiat Oncol 1998;8:164-75
3. Meyer DE, Chilkoti A. Purification of recombinant proteins by fusion with thermally-responsive polypeptides. Nat Biotechnol 1999;17:1112-15
4. Qiu Y, Park K. Environment-sensitive hydrogels for drug delivery. Adv Drug Deliv Rev 2001;53:321-39
5. Moses MA, Brem H, Langer R. Advancing the field of drug delivery: taking aim at cancer. Cancer Cell 2003;4:337-41
6. Portney NG, Ozkan M. Nano-oncology: drug delivery, imaging, and sensing. Anal Bioanal Chem 2006;384:620-30
7. Zhang JL, Srivastava RS, Misra RDK. Core-shell magnetite nanoparticles surface encapsulated with smart stimuli-responsive polymer: synthesis, characterization, and LCST of viable drug-targeting delivery system. Langmuir 2007;23:6342-51
8. You Y-Z, Kalebaila KK, Brock SL, et al. Temperature-controlled uptake and release in PNIPAM-modified porous silica nanoparticles. Chem Mater 2008;20:3354-9
9. Bikram M, West JL. Thermo-responsive systems for controlled drug delivery. Expert Opin Drug Deliv 2008;5:1077-91
10. Ganta S, Devalapally H, Shahiwala A, et al. A review of stimuli-responsive nanocarriers for drug and gene delivery. J Control Release 2008;126:187-204
11. Raucher D, Massodi I, Bidwell GL. Thermally targeted delivery of chemotherapeutics and anti-cancer peptides by elastin-like polypeptide. Expert Opin Drug Deliv 2008;5:353-69
12. Wei H, Cheng S-X, Zhang X-Z, et al. Thermo-sensitive polymeric micelles based on poly(N-isopropylacrylamide) as drug carriers. Prog Polym Sci 2009;34:893-910
13. Stuart MAC, Huck WTS, Genzer J, et al. Emerging applications of stimuli-responsive polymer materials. Nat Mater 2010;9:101-13
14. Fleige E, Quadir MA, Haag R. Stimuli-responsive polymeric nanocarriers for the controlled transport of active compounds: concepts and applications. Adv Drug Deliv Rev 2012;64:866-84
15. Calejo MT, Sande SA, Nystrom B. Thermoresponsive polymers as gene and drug delivery vectors: architecture and mechanism of action. Expert Opin Drug Deliv 2013;10:1669-86
16. Mura S, Nicolas J, Couvreur P. Stimuli-responsive nanocarriers for drug delivery. Nat Mater 2013;12:991-1003
17. Ge Z, Liu S. Functional block copolymer assemblies responsive to tumor and intracellular microenvironments for site-specific drug delivery and enhanced imaging performance. Chem Soc Rev 2013;42:7289-325
18. Seib FP, Jones GT, Rnjak-Kovacina J, et al. pH-dependent anticancer drug release from silk nanoparticles. Adv Healthc Mater 2013;2:1606-11
19. Florczak A, Mackiewicz A, Dams-Kozlowska H. Functionalized spider silk spheres as drug carriers for targeted cancer therapy. Biomacromolecules 2014;15:2971-81
20. Ciofani G, Genchi GG, Guardia P, et al. Recombinant human elastin-like magnetic microparticles for drug delivery and targeting. Macromol Biosci 2014;14:632-42
21. Ryu JS, Raucher D. Elastin-like polypeptides: the influence of its molecular weight on local hyperthermia-induced tumor accumulation. Eur J Pharm Biopharm 2014;88:382-9
22. Shi P, Gustafson JA, MacKay JA. Genetically engineered nanocarriers for drug delivery. Int J Nanomedicine 2014;9:1617-26
23. Xia X-X, Wang M, Lin Y, et al. Hydrophobic drug-triggered self-assembly of nanoparticles from silk-elastin-like protein polymers for drug delivery. Biomacromolecules 2014;15:908-14
24. Nagarsekar A, Crissman J, Crissman M, et al. Genetic engineering of stimuli-sensitive silkelastin-like protein block copolymers. Biomacromolecules 2003;4:602-7
25. Xia XX, Xu QB, Hu X, et al. Tunable self-assembly of genetically engineered silk-elastin-like protein polymers. Biomacromolecules 2011;12:3844-50
26. Rauscher S, Baud S, Miao M, et al. Proline and glycine control protein self-organization into elastomeric or amyloid fibrils. Structure 2006;14:1667-76
27. Muiznieks LD, Keeley FW. Proline periodicity modulates the self-assembly properties of elastin-like polypeptides. J Biol Chem 2010;285:39779-89
28. Anderson JP, Cappello J, Martin DC. Morphology and primary crystal structure of a silk-like protein polymer synthesized by genetically engineered Escherichia coli bacteria. Biopolymers 1994;34:1049-58
29. Anderson JP. Morphology and crystal structure of a recombinant silk-like molecule, SLP4. Biopolymers 1998;45:307-21
30. Urry DW, Trapane TL, Prasad KU. Phase-structure transitions of the elastin polypentapeptide-water system within the framework of composition-temperature studies. Biopolymers 1985;24:2345-56
31. Urry DW. Entropic elastic processes in protein mechanisms. I. Elastic structure due to an inverse temperature transition and elasticity due to internal chain dynamic. J Protein Chem 1988;7:1-34
32. Urry DW, Luan CH, Parker TM, et al. Temperature of polypeptide inverse temperature transition depends on mean residue hydrophobicity. J Am Chem Soc 1991;113:4346-8
33. McPherson DT, Xu J, Urry DW. 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 1996;7:51-7
34. Urry DW, Hugel T, Seitz M, et al. Elastin: a representative ideal protein elastomer. Philos Trans R Soc Lond B Biol Sci 2002;357:169-84
35. Wang Q, Xia X, Huang W, et al. High throughput screening of dynamic silk-elastin-like protein biomaterials. Adv Funct Mater 2014;24:4303-10
36. Hwang W, Kim B-H, Dandu R, et al. Surface induced nanofiber growth by self-assembly of a silk-elastin-like protein polymer. Langmuir 2009;25:12682-6
37. Chang J, Peng X-F, Hijji K, et al. Nanomechanical stimulus accelerates and directs the self-assembly of silk-elastin-like nanofibers. J Am Chem Soc 2011;133:1745-7
38. Golinska MD, Pham TTH, Werten MWT, et al. Fibril formation by pH and temperature responsive silk-elastin block copolymers. Biomacromolecules 2013;14:48-55
39. Machado R, da Costa A, Sencadas V, et al. Electrospun silk-elastin-like fibre mats for tissue engineering applications. Biomed Mater 2013;8:1-13
40. Ozaki C, Somamoto S, Kawabata S, et al. Effect of an artificial silk elastin-like protein on the migration and collagen production of mouse fibroblasts. J Biomater Sci Polym Ed 2014;25:1266-77
41. Collins T, Azevedo-Silva J, da Costa A, et al. Batch production of a silk-elastin-like protein in E. coli BL21 (DE3): key parameters for optimisation. Microb Cell Fact 2013;12:1-16
42. Machado R, Azevedo-Silva J, Correia C, et al. High level expression and facile purification of recombinant silk-elastin-like polymers in auto induction shake flask cultures. AMB Express 2013;3:1-15
43. Collins T, Barroca M, Branca F, et al. High level biosynthesis of a silk-elastin-like protein in E. coli. Biomacromolecules 2014;15:2701-8
44. Rabotyagova OS, Cebe P, Kaplan DL. Self-assembly of genetically engineered spider silk block copolymers. Biomacromolecules 2009;10:229-36
45. Krishnaji ST, Huang WW, Rabotyagova O, et al. Thin film assembly of spider silk-like block copolymers. Langmuir 2011;27:1000-8
46. Huang WW, Krishnaji S, Hu X, et al. Heat capacity of spider silk-like block copolymers. Macromolecules 2011;44:5299-309
47. Hayashi CY, Shipley NH, Lewis RV. Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins. Int J Biol Macromol 1999;24:271-5
48. He D, Chung M, Chan E, et al. Comparative genomics of elastin: sequence analysis of a highly repetitive protein. Matrix Biol 2007;26:524-40
49. Kim W, Conticello VP. Protein engineering methods for investigation of structure-function relationships in protein-based elastomeric materials. Polym Rev 2007;47:93-119
50. Krishnaji ST, Bratzel G, Kinahan ME, et al. Sequence-structure-property relationships of recombinant spider silk proteins: integration of biopolymer design, processing, and modeling. Adv Funct Mater 2013;23:241-53
51. Huang WW, Krishnaji S, Tokareva OS, et al. Influence of water on protein transitions: thermal analysis. Macromolecules 2014;47:8098-106
52. Huang WW, Krishnaji S, Tokareva OS, et al. Influence of water on protein transitions: morphology and secondary structure. Macromolecules 2014;47:8107-14
53. Rodriguez-Cabello JC, Prieto S, Reguera J, et al. Biofunctional design of elastin-like polymers for advanced applications in nanobiotechnology. J Biomater Sci Polym Ed 2007;18:269-86
54. Floss DM, Schallau K, Rose-John S, et al. Elastin-like polypeptides revolutionize recombinant protein expression and their biomedical application. Trends Biotechnol 2010;28:37-45
55. Pritchard EM, Kaplan DL. Silk fibroin biomaterials for controlled release drug delivery. Expert Opin Drug Deliv 2011;8:797-811
56. Huang J, Valluzzi R, Mauney J, et al. Collagen supramolecular assembly and cellular responses. Am Chem Soc 2004;227:PMSE 188
57. Bracalello A, Santopietro V, Vassalli M, et al. Design and production of a chimeric resilin-, elastin-, and collagenlike engineered polypeptide. Biomacromolecules 2011;12:2957-65
58. An B, DesRochers TM, Qin GK, et al. The influence of specific binding of collagen-silk chimeras to silk biomaterials on hMSC behavior. Biomaterials 2013;34:402-12
59. Wlodarczyk-Biegun MK, Werten MWT, de Wolf FA, et al. Genetically engineered silk-collagen-like copolymer for biomedical applications: production, characterization and evaluation of cellular response. Acta Biomater 2014;10:3620-9
60. Pei Y, Chen J, Yang LM, et al. The effect of pH on the LCST of poly(N-isopropylacrylamide) and poly(N-isopropylacrylamide-co-acrylic acid). J Biomater Sci Polym Ed 2004;15:585-94
61. Nakayama M, Okano T, Miyazaki T, et al. Molecular design of biodegradable polymeric micelles for temperature-responsive drug release. J Control Release 2006;115:46-56
62. Dandu R, Von Cresce A, Briber R, et al. Silk-elastin-like protein polymer hydrogels: influence of monomer sequence on physicochemical properties. Polymer (Guildf) 2009;50:366-74
63. Ner Y, Stuart JA, Whited G, et al. Electrospinning nanoribbons of a bioengineered silk-elastin-like protein (SELP) from water. Polymer (Guildf) 2009;50:5828-36
64. Qiu WG, Teng WB, Cappello JY, et al. Wet-Spinning of recombinant silk-elastin-like protein polymer fibers with high tensile strength and high deformability. Biomacromolecules 2009;10:602-8
65. Qiu WG, Huang YD, Teng WB, et al. Complete Recombinant silk-elastinlike protein-based tissue scaffold. Biomacromolecules 2010;11:3219-27
66. Somamoto S, Tabata Y. An artificial silk-elastin-like protein suppresses cells adhesion without apoptosis. J Biotechnol Biomater 2012;2:139
67. Johnson S, Ko YK, Varongchayakul N, et al. Directed patterning of the self-assembled silk-elastin-like nanofibers using a nanomechanical stimulus. Chem Commun 2012;48:10654-6
68. Sun Z, Qin G, Xia X, et al. Photoresponsive retinal-modified silk-elastin copolymer. J Am Chem Soc 2013;135:3675-9
69. Lin Y, Xia X, Wang M, et al. Genetically programmable thermoresponsive plasmonic gold/silk-elastin protein core/shell nanoparticles. Langmuir 2014;30:4406-14
70. Zeng L, Jiang L, Teng W, et al. Engineering aqueous Fiber assembly into silk-elastin-like protein polymers. Macromol Rapid Commun 2014;35:1273-9
71. Daamen WF, Veerkamp JH, van Hest JCM, et al. Elastin as a biomaterial for tissue engineering. Biomaterials 2007;28:4378-98
72. Ghandehari H, Cappello J, Nagarsekar A, et al. Genetic engineering of silk-elastinlike protein polymers for drug delivery. Am Chem Soc 2002;224:POLY 308
73. Gustafson J, Greish K, Frandsen J, et al. Silk-elastinlike recombinant polymers for gene therapy of head and neck cancer: from molecular definition to controlled gene expression. J Control Release 2009;140:256-61
74. Gustafson JA, Ghandehari H. Silk-elastinlike protein polymers for matrix-mediated cancer gene therapy. Adv Drug Deliv Rev 2010;62:1509-23
75. Price R, Poursaid A, Ghandehari H. Controlled release from recombinant polymers. J Control Release 2014;190:304-13
76. Gosline J, Lillie M, Carrington E, et al. Elastic proteins: biological roles and mechanical properties. Philos Trans R Soc Lond B Biol Sci 2002;357:121-32
77. Haider M, Megeed Z, Ghandehari H. Genetically engineered polymers: status and prospects for controlled release. J Control Release 2004;95:1-26
78. Hart DS, Gehrke SH. Thermally associating polypeptides designed for drug delivery produced by genetically engineered cells. J Pharm Sci 2007;96:484-516
79. Dandu R, Ghandehari H. Delivery of bioactive agents from recombinant polymers. Prog Polym Sci 2007;32:1008-30
80. Mackay JA, Chilkoti A. Temperature sensitive peptides: engineering hyperthermia-directed therapeutics. Int J Hyperthermia 2008;24:483-95
81. Chow D, Nunalee ML, Lim DW, et al. Peptide-based biopolymers in biomedicine and biotechnology. Mater Sci Eng R Rep 2008;62:125-55
82. Li L, Charati MB, Kiick KL. Elastomeric polypeptide-based biomaterials. Polym Chem 2010;1:1160-70
83. Frandsen JL, Ghandehari H. Recombinant protein-based polymers for advanced drug delivery. Chem Soc Rev 2012;41:2696-706
84. Altunbas A, Pochan DJ. Peptide-based and polypeptide-based hydrogels for drug delivery and tissue engineering. Top Curr Chem 2012;310:135-67
85. Elzoghby AO, Samy WM, Elgindy NA. Protein-based nanocarriers as promising drug and gene delivery systems. J Control Release 2012;161:38-49
86. Tjin MS, Low PL, Fong E. Recombinant elastomeric protein biopolymers: progress and prospects. Polym J 2014;46:444-51
87. Meyer DE, Kong GA, Dewhirst MW, et al. Targeting a genetically engineered elastin-like polypeptide to solid tumors by local hyperthermia. Cancer Res 2001;61:1548-54
88. Megeed Z, Cappello J, Ghandehari H. Genetically engineered silk-elastinlike protein polymers for controlled drug delivery. Adv Drug Deliv Rev 2002;54:1075-91
89. Dandu R, Megeed Z, Haider M, et al. Silk-elastinlike hydrogels: thermal characterization and gene delivery. In: Polymeric drug delivery II: polymeric matrices and drug particle engineering. ACS Symposium Series 2006. p. 150-68
90. Foo CWP, Kaplan DL. Genetic engineering of fibrous proteins: spider dragline silk and collagen. Adv Drug Deliv Rev 2002;54:1131-43
91. Lammel A, Schwab M, Hofer M, et al. Recombinant spider silk particles as drug delivery vehicles. Biomaterials 2011;32:2233-40
92. Doel MT, Eaton M, Cook EA, et al. The expression in E. coli of synthetic repeating polymeric genes coding for poly(L-aspartyl-L-phenylalanine). Nucleic Acids Res 1980;8:4575-92
93. Cappello J, Crissman J, Dorman M, et al. Genetic engineering of structural protein polymers. Biotechnol Prog 1990;6:198-202
94. Ferrari FA, Cappello J, Crissman JW, et al. Construction of synthetic DNA and its use in large polypeptide synthesis 1986:EP0293443A1
95. Pray L. Recombinant DNA technology and transgenic animals. Nat Educ 2008;1:51
96. Numata K, Kaplan DL. Silk-based delivery systems of bioactive molecules. Adv Drug Deliv Rev 2010;62:1497-508
97. Urry DW, Urry KD, Szaflarski W, et al. Elastic-contractile model proteins: physical chemistry, protein function and drug design and delivery. Adv Drug Deliv Rev 2010;62:1404-55
98. Vrhovski B, Weiss AS. Biochemistry of tropoelastin. Eur J Biochem 1998;258:1-18
99. Yeo GC, Baldock C, Tuukkanen A, et al. Tropoelastin bridge region positions the cell-interactive C terminus and contributes to elastic fiber assembly. Proc Natl Acad Sci USA 2012;109:2878-83
100. Cox BA, Starcher BC, Urry DW. Coacervation of tropoelastin results in fiber formation. J Biol Chem 1974;249:997-8
101. Vrhovski B, Jensen S, Weiss AS. Coacervation characteristics of recombinant human tropoelastin. Eur J Biochem 1997;250:92-8
102. Chilkoti A, Dreher MR, Meyer DE, et al. Targeted drug delivery by thermally responsive polymers. Adv Drug Deliv Rev 2002;54:613-30
103. Davis ME, Chen Z, Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov 2008;7:771-82
104. Prabhakar U, Maeda H, Jain RK, et al. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res 2013;73:2412-17
105. Boddy AV, Plummer ER, Todd R, et al. A phase I and pharmacokinetic study of paclitaxel poliglumex (XYOTAX), investigating both 3-weekly and 2-weekly schedules. Clin Cancer Res 2005;11:7834-40
106. MacKay JA, Chen M, McDaniel JR, et al. Self-assembling chimeric polypeptide-doxorubicin conjugate nanoparticles that abolish tumours after a single injection. Nat Mater 2009;8:993-9
107. Daniels TR, Bernabeu E, Rodriguez JA, et al. The transferrin receptor and the targeted delivery of therapeutic agents against cancer. Biochim Biophys Acta 2012;1820:291-317
108. Gao H, Yang Z, Zhang S, et al. Ligand modified nanoparticles increases cell uptake, alters endocytosis and elevates glioma distribution and internalization. Sci Rep 2013;3:2534
109. Brigger I, Dubernet C, Couvreur P. Nanoparticles in cancer therapy and diagnosis. Adv Drug Deliv Rev 2002;54:631-51
110. Brigger I, Dubernet C, Couvreur P. Nanoparticles in cancer therapy and diagnosis. Adv Drug Deliv Rev 2012;64:24-36
111. Gaumet M, Vargas A, Gurny R, et al. Nanoparticles for drug delivery: the need for precision in reporting particle size parameters. Eur J Pharm Biopharm 2008;69:1-9
112. Megeed Z, Cappello J, Ghandehari H. Controlled release of plasmid DNA from a genetically engineered silk-elastinlike hydrogel. Pharm Res 2002;19:954-9
113. Megeed Z, Haider M, Li D, et al. In vitro and in vivo evaluation of recombinant silk-elastin-like hydrogels for cancer gene therapy. J Control Release 2004;94:433-45
114. Hatefi A, Cappello J, Ghandehari H. Adenoviral gene delivery to solid tumors by recombinant silk-elastinlike protein polymers. Pharm Res 2007;24:773-9
115. Dandu R, Ghandehari H, Cappello J. Characterization of structurally related adenovirus-laden silk-elastinlike hydrogels. J Bioact Compat Polym 2008;23:5-19
116. Hwang D, Moolchandani V, Dandu R, et al. Influence of polymer structure and biodegradation on DNA release from silk-elastinlike protein polymer hydrogels. Int J Pharm 2009;368:215-19
117. Greish K, Frandsen J, Scharff S, et al. Silk-elastinlike protein polymers improve the efficacy of adenovirus thymidine kinase enzyme prodrug therapy of head and neck tumors. J Gene Med 2010;12:572-9
118. Price R, Gustafson J, Greish K, et al. Comparison of silk-elastinlike protein polymer hydrogel and poloxamer in matrix-mediated gene delivery. Int J Pharm 2012;427:97-104
119. Gustafson JA, Price RA, Greish K, et al. Silk-elastin-like hydrogel improves the safety of adenovirus-mediated gene-directed enzyme-prodrug therapy. Mol Pharm 2010;7:1050-6
120. Numata K, Kaplan DL. Silk-based gene carriers with cell membrane destabilizing peptides. Biomacromolecules 2010;11:3189-95
121. Numata K, Reagan MR, Goldstein RH, et al. Spider silk-based gene carriers for tumor cell-specific delivery. Bioconjug Chem 2011;22:1605-10
122. Numata K, Mieszawska-Czajkowska AJ, Kvenvold LA, et al. Silk-based nanocomplexes with tumor-homing peptides for tumor-specific gene delivery. Macromol Biosci 2012;12:75-82
123. Simionescua DT, Lua QJ, Song Y, et al. Biocompatibility and remodeling potential of pure arterial elastin and collagen scaffolds. Biomaterials 2006;27:702-13
124. Rincon AC, Molina-Martinez IT, de las Heras B, et al. Biocompatibility of elastin-like polymer poly(VPAVG) microparticles: in vitro and in vivo studies. J Biomed Mater Res A 2006;78A:343-51
125. Hu X, Tang-Schomer MD, Huang W, et al. Charge-Tunable autoclaved silk-tropoelastin protein alloys that control neuron cell responses. Adv Funct Mater 2013;23:3875-84
126. Cappello J, Crissman JW, Crissman M, et al. In-situ self-assembling protein polymer gel systems for administration, delivery, and release of drugs. J Control Release 1998;53:105-17
127. Shen W. Engineered polypeptides for tissue engineering. In: Biomaterials for tissue engineering applications: a review of the past and future trends. Springer; New York: 2011. p. 243-75
128. Urry DW, Peng SQ, Parker TM. Hydrophobicity-induced pK shifts in elastin protein-based polymers. Biopolymers 1992;32:373-9
129. Liu Y, Cai H-L, Zelisko M, et al. Ferroelectric switching of elastin. Proc Natl Acad Sci USA 2014. 111:E2780-6