Co-Assembly Tags Based on Charge Complementarity (CATCH) for Installing Functional Protein Ligands into Supramolecular Biomaterials

Springer Science and Business Media LLC - Tập 9 - Trang 335-350 - 2016
Dillon T. Seroski1, Antonietta Restuccia1, Anthony D. Sorrentino1, Kevin R. Knox1, Stephen J. Hagen2, Gregory A. Hudalla1
1J. Crayton Pruitt Family Department of Biomedical Engineering, University of Florida, Gainesville, USA
2Department of Physics, University of Florida, Gainesville, USA

Tóm tắt

Installing folded proteins into biomaterials is gaining interest for imparting functional properties that often cannot be provided by unfolded peptides or small molecules, such as catalysis, antigen conformation, or molecular recognition. Although covalent grafting provides a simple means to immobilize proteins onto pre-formed biomaterials, amenable chemistries can alter protein bioactivity, are relatively non-specific, and can be difficult to reproduce. Covalent fusions of bioactive molecules and synthetic peptides that can self-assemble into nano-scale architectures are a promising alternative for creating functional supramolecular biomaterials with precise and reproducible composition. Here we created a pair of oppositely charged synthetic peptides, referred to as “CATCH” (Co-Assembly Tags based on CHarge complementarity), to install folded proteins into supramolecular biomaterials. CATCH peptides co-assemble into β-sheet nanofibers when combined, yet cannot assemble independently due to electrostatic repulsion. Electrostatically controlled assembly enabled high yield production of soluble CATCH-green fluorescent protein (CATCH(−)GFP) by E. coli. Binary mixtures of CATCH-GFP and its charge-complementary peptide self-assembled into fluorescent microparticles, whereas ternary mixtures of CATCH(−)GFP and both CATCH peptides self-assembled into fluorescent nanofibers and macroscopic hydrogels. The CATCH system is therefore likely to be broadly useful for creating functional supramolecular biomaterials with integrated folded protein components for various biomedical and biotechnological applications.

Tài liệu tham khảo

Baldwin, A. J., R. Bader, J. Christodoulou, C. E. MacPhee, C. M. Dobson, and P. D. Barker. Cytochrome display on amyloid fibrils. J. Am. Chem. Soc. 128(7):2162–2163, 2006.

Baxa, U., V. Speransky, A. C. Steven, and R. B. Wickner. Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein. Proc Natl Acad Sci USA. 99(8):5253–5260, 2002.

Black, M., A. Trent, Y. Kostenko, J. S. Lee, C. Olive, and M. Tirrell. Self-assembled peptide amphiphile micelles containing a cytotoxic T-cell epitope promote a protective immune response in vivo. Adv. Mater. 24(28):3845–3849, 2012.

Bowerman, C. J., and B. L. Nilsson. Self-assembly of amphipathic beta-sheet peptides: insights and applications. Biopolymers. 98(3):169–184, 2012.

Chen, J., R. R. Pompano, F. W. Santiago, L. Maillat, R. Sciammas, T. Sun, H. Han, D. J. Topham, A. S. Chong, and J. H. Collier. The use of self-adjuvanting nanofiber vaccines to elicit high-affinity B cell responses to peptide antigens without inflammation. Biomaterials. 34(34):8776–8785, 2013.

Chow, L. W., L. J. Wang, Kaufman DB, and Stupp SI. Self-assembling nanostructures to deliver angiogenic factors to pancreatic islets. Biomaterials. 31(24):6154–6161, 2010.

Collier, J. H., and Messersmith PB. Enzymatic modification of self-assembled peptide structures with tissue transglutaminase. Bioconjugate Chem. 14(4):748–755, 2003.

Collier, J. H., J. S. Rudra, Gasiorowski JZ, and J. P. Jung. Multi-component extracellular matrices based on peptide self-assembly. Chem. Soc. Rev. 39(9):3413–3424, 2010.

Davis, M. E., P. C. Hsieh, T. Takahashi, Q. Song, S. Zhang, R. D. Kamm, A. J. Grodzinsky, P. Anversa, and R. T. Lee. Local myocardial insulin-like growth factor 1 (IGF-1) delivery with biotinylated peptide nanofibers improves cell therapy for myocardial infarction. Proc. Natl Acad. Sci. U S A. 103(21):8155–8160, 2006.

Davis, M. E., J. P. Motion, D. A. Narmoneva, T. Takahashi, D. Hakuno, R. D. Kamm, S. Zhang, and R. T. Lee. Injectable self-assembling peptide nanofibers create intramyocardial microenvironments for endothelial cells. Circulation. 111(4):442–450, 2005.

Du, X., J. Zhou, J. Shi, and B. Xu. Supramolecular hydrogelators and hydrogels: from soft matter to molecular biomaterials. Chem. Rev. 115(24):13165–13307, 2015.

Fettis, M. M., Y. Wei, A. Restuccia, J. Kurian, S. M. Wallet, and G. A. Hudalla. Microgels with tunable affinity-controlled protein release via desolvation of self-assembled peptide nanofibers. J. Mater. Chem. B 4:3054–3064, 2016.

Guler, M. O., S. Soukasene, J. F. Hulvat, and S. I. Stupp. Presentation and recognition of biotin on nanofibers formed by branched peptide amphiphiles. Nano Lett. 5(2):249–252, 2005.

Haines-Butterick, L. A., D. A. Salick, D. J. Pochan, and J. P. Schneider. In vitro assessment of the pro-inflammatory potential of beta-hairpin peptide hydrogels. Biomaterials. 29(31):4164–4169, 2008.

Holmes, T. C., S. de Lacalle, X. Su, G. Liu, A. Rich, and S. Zhang. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc. Natl Acad. Sci. U S A. 97(12):6728–6733, 2000.

Hortschansky, P., V. Schroeckh, T. Christopeit, G. Zandomeneghi, and M. Fandrich. The aggregation kinetics of Alzheimer’s beta-amyloid peptide is controlled by stochastic nucleation. Protein Sci. 14(7):1753–1759, 2005.

Hsieh, P. C., M. E. Davis, J. Gannon, C. MacGillivray, and R. T. Lee. Controlled delivery of PDGF-BB for myocardial protection using injectable self-assembling peptide nanofibers. J. Clin. Invest. 116(1):237–248, 2006.

Hudalla, G. A., and J. H. Collier. Supramolecular artificial extracellular matrices. In: Mimicking the extracellular matrix: the intersection of matrix biology and biomaterials, edited by G. A. Hudalla, and W. L. Murphy. London: Royal Society of Chemistry, 2015.

Hudalla, G. A., T. Sun, J. Z. Gasiorowski, H. Han, Y. F. Tian, A. S. Chong, and J. H. Collier. Gradated assembly of multiple proteins into supramolecular nanomaterials. Nat Mater. 13(8):829–836, 2014.

Jung, J. P., J. Z. Gasiorowski, and J. H. Collier. Fibrillar peptide gels in biotechnology and biomedicine. Biopolymers. 94(1):49–59, 2010.

Jung, J. P., J. V. Moyano, and J. H. Collier. Multifactorial optimization of endothelial cell growth using modular synthetic extracellular matrices. Integr. Biol. (Camb). 3(3):185–196, 2011.

Jung, J. P., A. K. Nagaraj, E. K. Fox, J. S. Rudra, J. M. Devgun, and J. H. Collier. Co-assembling peptides as defined matrices for endothelial cells. Biomaterials. 30(12):2400–2410, 2009.

Khan, S., S. Sur, P. Y. Dankers, R. M. da Silva, J. Boekhoven, T. A. Poor, and S. I. Stupp. Post-assembly functionalization of supramolecular nanostructures with bioactive peptides and fluorescent proteins by native chemical ligation. Bioconjug Chem. 25(4):707–717, 2014.

Kim, W., Y. Kim, J. Min, D. J. Kim, Y. T. Chang, and M. H. Hecht. A high-throughput screen for compounds that inhibit aggregation of the Alzheimer’s peptide. ACS Chem. Biol. 1(7):461–469, 2006.

Kyle, S., S. H. Felton, M. J. McPherson, A. Aggeli, and E. Ingham. Rational molecular design of complementary self-assembling peptide hydrogels. Adv. Healthc. Mater. 1(5):640–645, 2012.

Lee, S. S., E. L. Hsu, M. Mendoza, J. Ghodasra, M. S. Nickoli, A. Ashtekar, M. Polavarapu, J. Babu, R. M. Riaz, J. D. Nicolas, D. Nelson, S. Z. Hashmi, S. R. Kaltz, J. S. Earhart, B. R. Merk, J. S. McKee, S. F. Bairstow, R. N. Shah, W. K. Hsu, and S. I. Stupp. Gel scaffolds of BMP-2-binding peptide amphiphile nanofibers for spinal arthrodesis. Adv. Healthc. Mater. 4(1):131–141, 2015.

Lee, S. S., B. J. Huang, S. R. Kaltz, S. Sur, C. J. Newcomb, S. R. Stock, R. N. Shah, and S. I. Stupp. Bone regeneration with low dose BMP-2 amplified by biomimetic supramolecular nanofibers within collagen scaffolds. Biomaterials. 34(2):452–459, 2013.

Leng, Y., H. P. Wei, Z. P. Zhang, Y. F. Zhou, J. Y. Deng, Z. Q. Cui, D. Men, X. Y. You, Z. N. Yu, M. Luo, and X. E. Zhang. Integration of a fluorescent molecular biosensor into self-assembled protein nanowires: a large sensitivity enhancement. Angew. Chem. Int. Edit. 49(40):7243–7246, 2010.

Mahmoud, Z. N., S. B. Gunnoo, A. R. Thomson, J. M. Fletcher, and D. N. Woolfson. Bioorthogonal dual functionalization of self-assembling peptide fibers. Biomaterials. 32(15):3712–3720, 2011.

Matson, J. B., R. H. Zha, and S. I. Stupp. Peptide self-assembly for crafting functional biological materials. Curr. Opin. Solid State Mater. Sci. 15(6):225–235, 2011.

Matsumura, S., S. Uemura, and H. Mihara. Construction of biotinylated peptide nanotubes for arranging proteins. Mol. Biosyst. 1(2):146–148, 2005.

Mehrban, N., E. Abelardo, A. Wasmuth, K. L. Hudson, L. M. Mullen, A. R. Thomson, M. A. Birchall, and D. N. Woolfson. Assessing cellular response to functionalized alpha-helical peptide hydrogels. Adv. Healthc. Mater. 3(9):1387–1391, 2014.

Men, D., Y. C. Guo, Z. P. Zhang, H. P. Wei, Y. F. Zhou, Z. Q. Cui, X. S. Liang, K. Li, Y. Leng, X. Y. You, and X. E. Zhang. Seeding-induced self-assembling protein nanowires dramatically increase the sensitivity of immunoassays. Nano Lett. 9(6):2246–2250, 2009.

Mendes, A. C., E. T. Baran, R. L. Reis, and H. S. Azevedo. Self-assembly in nature: using the principles of nature to create complex nanobiomaterials. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 5(6):582–612, 2013.

Miyachi, A., T. Takahashi, S. Matsumura, and H. Mihara. Peptide nanofibers modified with a protein by using designed anchor molecules bearing hydrophobic and functional moieties. Chemistry. 16(22):6644–6650, 2010.

Pedelacq, J. D., S. Cabantous, T. Tran, T. C. Terwilliger, and G. S. Waldo. Engineering and characterization of a superfolder green fluorescent protein. Nat. Biotechnol. 24(1):79–88, 2006.

Pompano, R. R., J. Chen, E. A. Verbus, H. Han, A. Fridman, T. McNeely, J. H. Collier, and A. S. Chong. Titrating T-cell epitopes within self-assembled vaccines optimizes CD4 + helper T cell and antibody outputs. Adv. Healthc. Mater. 3(11):1898–1908, 2014.

Reches, M., and E. Gazit. Biological and chemical decoration of peptide nanostructures via biotin-avidin interactions. J. Nanosci. Nanotechnol. 7(7):2239–2245, 2007.

Restuccia, A., Y. F. Tian, J. H. Collier, and G. A. Hudalla. Self-assembled glycopeptide nanofibers as modulators of galectin-1 bioactivity. Cell Mol. Bioeng. 8(3):471–487, 2015.

Rudra, J. S., T. Sun, K. C. Bird, M. D. Daniels, J. Z. Gasiorowski, A. S. Chong, and J. H. Collier. Modulating adaptive immune responses to peptide self-assemblies. ACS Nano. 6(2):1557–1564, 2012.

Rudra, J. S., Y. F. Tian, J. P. Jung, and J. H. Collier. A self-assembling peptide acting as an immune adjuvant. Proc. Natl Acad. Sci. U S A. 107(2):622–627, 2010.

Sangiambut, S., K. Channon, N. M. Thomson, S. Sato, T. Tsuge, Y. Doi, and E. Sivaniah. A robust route to enzymatically functional, hierarchically self-assembled peptide frameworks. Adv. Mater. 25(19):2661–2665, 2013.

Sawada, T., and H. Mihara. Dense surface functionalization using peptides that recognize differences in organized structures of self-assembling nanomaterials. Mol. Biosyst. 8(4):1264–1274, 2012.

Sawada, T., T. Takahashi, and H. Mihara. Affinity-based screening of peptides recognizing assembly states of self-assembling peptide nanomaterials. J. Am. Chem. Soc. 131(40):14434–14441, 2009.

Stendahl, J. C., L. J. Wang, L. W. Chow, D. B. Kaufman, and S. I. Stupp. Growth factor delivery from self-assembling nanofibers to facilitate islet transplantation. Transplantation. 86(3):478–481, 2008.

Tian, Y. F., J. M. Devgun, and J. H. Collier. Fibrillized peptide microgels for cell encapsulation and 3D cell culture. Soft Matter 7(13):6005–6011, 2011.

Vassar, P. S., and C. F. Culling. Fluorescent stains, with special reference to amyloid and connective tissues. Arch. Pathol. 68:487–498, 1959.

Webber, M. J., E. A. Appel, E. W. Meijer, and R. Langer. Supramolecular biomaterials. Nat. Mater. 15(1):13–26, 2016.

Whitesides, G. M., and M. Boncheva. Beyond molecules: self-assembly of mesoscopic and macroscopic components. Proc. Natl Acad. Sci. U S A. 99(8):4769–4774, 2002.

Wu, W., L. Xing, B. Zhou, and Z. Lin. Active protein aggregates induced by terminally attached self-assembling peptide ELK16 in Escherichia coli. Microb. Cell Fact. 10:9, 2011.

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Springer Science and Business Media LLC

Tập 9

335-350

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