Login Register Cart 0
Generic placeholder image

Current Nanoscience

Editor-in-Chief

ISSN (Print): 1573-4137
ISSN (Online): 1875-6786

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Bioconjugation of Bacteriophage Pf1 and Extension to Pf1-Based Bionanomaterials

Author(s): Taylor Urquhart, Bradley Howie, Lei Zhang, Kam Tong Leung and John F. Honek*

Volume 17, Issue 1, 2021

Published on: 14 June, 2020

Page: [139 - 150] Pages: 12

DOI: 10.2174/1573413716999200614142202

open access plus

Abstract

Background: Filamentous bacteriophages such as M13 are an important class of macromolecular assembly, rich in chemical moieties that can be used to impart modifiable positions at the nanoscale.

Objective: To explore the structurally more complex Pf1 bacteriophage with respect to a diverse set of bioconjugation reactions and to prepare novel fluorescently-labelled Pf1-based composite biomembranes for future applications in areas such as nanoporous filtration biofilms and photoconducting nanocomposite materials.

Methods: Pf1 was characterized with respect to amine (N-terminal, Gly1 and Lys20), carboxylate (aspartate, glutamate), and aromatic (tyrosine) modification and its extension to the creation of functional biomaterials. Modification with an amine reactive fluorophore was carried out with Pf1.

Results: The reaction profiles between M13 and Pf1 differ, with M13 capable of modification at two primary amines on its major coat protein, while Pf1 is capable of a single reaction per coat protein. Subsequent to the production of dye-functionalized Pf1, a biocomposite of wild type and functionalized Pf1 could be fabricated into a bulk material by glutaraldehyde (amine-reactive) crosslinking. These biomaterials were characterized by scanning electron and confocal microscopy, showing a distribution of patches of functionalized Pf1 within the main Pf1 construct.

Conclusion: The current study provides a framework for future fabrication of advanced bionanomaterials based on the Pf1 bacteriophage.

Keywords: Bacteriophage, Pf1, TAMRA, crosslinking, bioconjugation, electron microscopy.

« Previous Next »
Graphical Abstract

[1]
Molek, P.; Bratkovič, T. Bacteriophages as scaffolds for bipartite display: designing swiss army knives on a nanoscale. Bioconjug. Chem., 2015, 26(3), 367-378.
[http://dx.doi.org/10.1021/acs.bioconjchem.5b00034] [PMID: 25654261]
[2]
Petrescu, D.S.; Blum, A.S. Viral-based nanomaterials for plasmonic and photonic materials and devices. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 2018, 10(4)e1508
[http://dx.doi.org/10.1002/wnan.1508] [PMID: 29418076]
[3]
He, D.; Marles-Wright, J. Ferritin family proteins and their use in bionanotechnology. N. Biotechnol., 2015, 32(6), 651-657.
[http://dx.doi.org/10.1016/j.nbt.2014.12.006] [PMID: 25573765]
[4]
Lee, E.J. Recent advances in protein-based nanoparticles. Korean J. Chem. Eng., 2018, 35, 1765-1778.
[http://dx.doi.org/10.1007/s11814-018-0102-0]
[5]
Malam, Y.; Loizidou, M.; Seifalian, A.M. Liposomes and nanoparticles: nanosized vehicles for drug delivery in cancer. Trends Pharmacol. Sci., 2009, 30(11), 592-599.
[http://dx.doi.org/10.1016/j.tips.2009.08.004] [PMID: 19837467]
[6]
Barile, L.; Vassalli, G. Exosomes: Therapy delivery tools and biomarkers of diseases. Pharmacol. Ther., 2017, 174, 63-78.
[http://dx.doi.org/10.1016/j.pharmthera.2017.02.020] [PMID: 28202367]
[7]
Chidchob, P.; Sleiman, H.F. Recent advances in DNA nanotechnology. Curr. Opin. Chem. Biol., 2018, 46, 63-70.
[http://dx.doi.org/10.1016/j.cbpa.2018.04.012] [PMID: 29751162]
[8]
Chen, W.; Yu, H.; Lee, S-Y.; Wei, T.; Li, J.; Fan, Z. Nanocellulose: a promising nanomaterial for advanced electrochemical energy storage. Chem. Soc. Rev., 2018, 47(8), 2837-2872.
[http://dx.doi.org/10.1039/C7CS00790F] [PMID: 29561005]
[9]
Chen, Z.; Li, N.; Li, S.; Dharmarwardana, M.; Schlimme, A.; Gassensmith, J.J. Viral chemistry: the chemical functionalization of viral architectures to create new technology. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol., 2016, 8(4), 512-534.
[http://dx.doi.org/10.1002/wnan.1379] [PMID: 26663821]
[10]
Pokorski, J.K.; Steinmetz, N.F. The art of engineering viral nanoparticles. Mol. Pharm., 2011, 8(1), 29-43.
[http://dx.doi.org/10.1021/mp100225y] [PMID: 21047140]
[11]
Wang, Q.; Lin, T.; Tang, L.; Johnson, J.E.; Finn, M.G. Icosahedral virus particles as addressable nanoscale building blocks. Angew. Chem. Int. Ed. Engl., 2002, 41(3), 459-462.
[http://dx.doi.org/10.1002/1521-3773(20020201)41:3<459:AID-ANIE459>3.0.CO;2-O] [PMID: 12491378]
[12]
Pokorski, J.K.; Breitenkamp, K.; Liepold, L.O.; Qazi, S.; Finn, M.G. Functional virus-based polymer-protein nanoparticles by atom transfer radical polymerization. J. Am. Chem. Soc., 2011, 133(24), 9242-9245.
[http://dx.doi.org/10.1021/ja203286n] [PMID: 21627118]
[13]
Sen Gupta, S.; Kuzelka, J.; Singh, P.; Lewis, W.G.; Manchester, M.; Finn, M.G. Accelerated bioorthogonal conjugation: a practical method for the ligation of diverse functional molecules to a polyvalent virus scaffold. Bioconjug. Chem., 2005, 16(6), 1572-1579.
[http://dx.doi.org/10.1021/bc050147l] [PMID: 16287257]
[14]
Li, S.; Dharmarwardana, M.; Welch, R.P.; Ren, Y.; Thompson, C.M.; Smaldone, R.A.; Gassensmith, J.J. Template-directed synthesis of porous and protective core–shell bionanoparticles. Angew. Chem. Int. Ed. Engl., 2016, 55(36), 10691-10696.
[http://dx.doi.org/10.1002/anie.201604879] [PMID: 27485579]
[15]
Choi, D.S.; Jin, H-E.; Yoo, S.Y.; Lee, S-W. Cyclic RGD peptide incorporation on phage major coat proteins for improved internalization by HeLa cells. Bioconjug. Chem., 2014, 25(2), 216-223.
[http://dx.doi.org/10.1021/bc4003234] [PMID: 24328047]
[16]
DePorter, S.M.; McNaughton, B.R. Engineered M13 bacteriophage nanocarriers for intracellular delivery of exogenous proteins to human prostate cancer cells. Bioconjug. Chem., 2014, 25(9), 1620-1625.
[http://dx.doi.org/10.1021/bc500339k] [PMID: 25134017]
[17]
Lee, J.Y.; Chung, W-J.; Kim, G. A mechanically improved virus-based hybrid scaffold for bone tissue regeneration. RSC Advances, 2016, 6, 55022-55032.
[http://dx.doi.org/10.1039/C6RA07054J]
[18]
Wang, J.; Yang, M.; Zhu, Y.; Wang, L.; Tomsia, A.P.; Mao, C. Phage nanofibers induce vascularized osteogenesis in 3D printed bone scaffolds. Adv. Mater., 2014, 26(29), 4961-4966.
[http://dx.doi.org/10.1002/adma.201400154] [PMID: 24711251]
[19]
Lee, H-S.; Kang, J-I.; Chung, W-J.; Lee, D.H.; Lee, B.Y.; Lee, S-W.; Yoo, S.Y. Engineered phage matrix stiffness-modulating osteogenic differentiation. ACS Appl. Mater. Interfaces, 2018, 10(5), 4349-4358.
[http://dx.doi.org/10.1021/acsami.7b17871] [PMID: 29345898]
[20]
Mao, C.; Solis, D.J.; Reiss, B.D.; Kottmann, S.T.; Sweeney, R.Y.; Hayhurst, A.; Georgiou, G.; Iverson, B.; Belcher, A.M. Virus-based toolkit for the directed synthesis of magnetic and semiconducting nanowires. Science, 2004, 303(5655), 213-217.
[http://dx.doi.org/10.1126/science.1092740] [PMID: 14716009]
[21]
Park, J.P.; Do, M.; Jin, H-E.; Lee, S-W.; Lee, H. M13 bacteriophage displaying DOPA on surfaces: fabrication of various nanostructured inorganic materials without time-consuming screening processes. ACS Appl. Mater. Interfaces, 2014, 6(21), 18653-18660.
[http://dx.doi.org/10.1021/am506873g] [PMID: 25317741]
[22]
Zaman, M.S.; Haberer, E.D. Mineralization and optical characterization of copper oxide nanoparticles using a high aspect ratio bio-template. J. Appl. Phys., 2014, 116154308
[http://dx.doi.org/10.1063/1.4898809]
[23]
Moradi, M.; Kim, J.C.; Qi, J.; Xu, K.; Li, X.; Ceder, G.; Belcher, A.M. A bio-facilitated synthetic route for nano-structured complex electrode materials. Green Chem., 2016, 18, 2619-2624.
[http://dx.doi.org/10.1039/C6GC00273K]
[24]
De Plano, L.M.; Scibilia, S.; Rizzo, M.G.; Crea, S.; Franco, D.; Mezzasalma, A.M.; Guglielmino, S.P.P. One-step production of phage-silicon nanoparticles by PLAL as fluorescent nanoprobes for cell identification. Appl. Phys., A Mater. Sci. Process., 2018, 124, 222.
[http://dx.doi.org/10.1007/s00339-018-1637-y]
[25]
Nam, K.T.; Kim, D.W.; Yoo, P.J.; Chiang, C.Y.; Meethong, N.; Hammond, P.T.; Chiang, Y.M.; Belcher, A.M. Virus-enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science, 2006, 312(5775), 885-888.
[http://dx.doi.org/10.1126/science.1122716] [PMID: 16601154]
[26]
Lee, B.Y.; Zhang, J.; Zueger, C.; Chung, W-J.; Yoo, S.Y.; Wang, E.; Meyer, J.; Ramesh, R.; Lee, S-W. Virus-based piezoelectric energy generation. Nat. Nanotechnol., 2012, 7(6), 351-356.
[http://dx.doi.org/10.1038/nnano.2012.69] [PMID: 22581406]
[27]
Chen, P-Y.; Dang, X.; Klug, M.T.; Qi, J.; Dorval Courchesne, N-M.; Burpo, F.J.; Fang, N.; Hammond, P.T.; Belcher, A.M. Versatile three-dimensional virus-based template for dye-sensitized solar cells with improved electron transport and light harvesting. ACS Nano, 2013, 7(8), 6563-6574.
[http://dx.doi.org/10.1021/nn4014164] [PMID: 23808626]
[28]
Jeong, C.K.; Kim, I.; Park, K-I.; Oh, M.H.; Paik, H.; Hwang, G-T.; No, K.; Nam, Y.S.; Lee, K.J. Virus-directed design of a flexible BaTiO3 nanogenerator. ACS Nano, 2013, 7(12), 11016-11025.
[http://dx.doi.org/10.1021/nn404659d] [PMID: 24229091]
[29]
Shin, D-M.; Han, H.J.; Kim, W-G.; Kim, E.; Kim, C.; Hong, S.W.; Kim, H.K.; Oh, J-W.; Hwang, Y-H. Bioinspired piezoelectric nanogenerators based on vertically aligned phage nanopillars. Energy Environ. Sci., 2015, 8, 3198-3203.
[http://dx.doi.org/10.1039/C5EE02611C]
[30]
Lee, H-E.; Lee, H.K.; Chang, H.; Ahn, H-Y.; Erdene, N.; Lee, H-Y.; Lee, Y-S.; Jeong, D.H.; Chung, J.; Nam, K.T. Virus templated gold nanocube chain for SERS nanoprobe. Small, 2014, 10(15), 3007-3011.
[http://dx.doi.org/10.1002/smll.201400527] [PMID: 24700483]
[31]
Oh, J-W.; Chung, W-J.; Heo, K.; Jin, H-E.; Lee, B.Y.; Wang, E.; Zueger, C.; Wong, W.; Meyer, J.; Kim, C.; Lee, S-Y.; Kim, W-G.; Zemla, M.; Auer, M.; Hexemer, A.; Lee, S-W. Biomimetic virus-based colourimetric sensors. Nat. Commun., 2014, 5, 3043.
[http://dx.doi.org/10.1038/ncomms4043] [PMID: 24448217]
[32]
Adhikari, M.; Strych, U.; Kim, J.; Goux, H.; Dhamane, S.; Poongavanam, M-V.; Hagström, A.E.V.; Kourentzi, K.; Conrad, J.C.; Willson, R.C. Aptamer-phage reporters for ultrasensitive lateral flow assays. Anal. Chem., 2015, 87(23), 11660-11665.
[http://dx.doi.org/10.1021/acs.analchem.5b00702] [PMID: 26456715]
[33]
Brasino, M.; Lee, J.H.; Cha, J.N. Creating highly amplified enzyme-linked immunosorbent assay signals from genetically engineered bacteriophage. Anal. Biochem., 2015, 470, 7-13.
[http://dx.doi.org/10.1016/j.ab.2014.10.006] [PMID: 25447463]
[34]
Yan, Y.; Zhang, M.; Moon, C.H.; Su, H-C.; Myung, N.V.; Haberer, E.D. Viral-templated gold/polypyrrole nanopeapods for an ammonia gas sensor. Nanotechnology, 2016, 27(32)325502
[http://dx.doi.org/10.1088/0957-4484/27/32/325502] [PMID: 27354441]
[35]
Lee, J.H.; Fan, B.; Samdin, T.D.; Monteiro, D.A.; Desai, M.S.; Scheideler, O.; Jin, H-E.; Kim, S.; Lee, S-W. Phage-based structural color sensors and their pattern recognition sensing system. ACS Nano, 2017, 11(4), 3632-3641.
[http://dx.doi.org/10.1021/acsnano.6b07942] [PMID: 28355060]
[36]
Koh, E.H.; Mun, C.; Kim, C.; Park, S-G.; Choi, E.J.; Kim, S.H.; Dang, J.; Choo, J.; Oh, J-W.; Kim, D-H.; Jung, H.S. M13 bacteriophage/silver nanowire surface-enhanced raman scattering sensor for sensitive and selective pesticide detection. ACS Appl. Mater. Interfaces, 2018, 10(12), 10388-10397.
[http://dx.doi.org/10.1021/acsami.8b01470] [PMID: 29505228]
[37]
Niu, Z.; Bruckman, M.A.; Harp, B.; Mello, C.M.; Wang, Q. Bacteriophage M13 as a scaffold for preparing conductive polymeric composite fibers. Nano Res., 2008, 1, 235-241.
[http://dx.doi.org/10.1007/s12274-008-8027-2]
[38]
Courchesne, N-M.D.; Klug, M.T.; Chen, P-Y.; Kooi, S.E.; Yun, D.S.; Hong, N.; Fang, N.X.; Belcher, A.M.; Hammond, P.T. Assembly of a bacteriophage-based template for the organization of materials into nanoporous networks. Adv. Mater., 2014, 26(21), 3398-3404.
[http://dx.doi.org/10.1002/adma.201305928] [PMID: 24648015]
[39]
Jung, S.M.; Qi, J.; Oh, D.; Belcher, A.; Kong, J. M13 virus aerogels as a scaffold for functional inorganic materials. Adv. Funct. Mater., 2017, 271603203
[http://dx.doi.org/10.1002/adfm.201603203]
[40]
Devaraj, V.; Han, J.; Kim, C.; Kang, Y-C.; Oh, J-W. Self-assembled nanoporous biofilms from functionalized nanofibrous M13 bacteriophage. Viruses, 2018, 10(6), 322.
[http://dx.doi.org/10.3390/v10060322] [PMID: 29895757]
[41]
Hansen, M.R.; Mueller, L.; Pardi, A. Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions. Nat. Struct. Biol., 1998, 5(12), 1065-1074.
[http://dx.doi.org/10.1038/4176] [PMID: 9846877]
[42]
Hennig, J.; Militti, C.; Popowicz, G.M.; Wang, I.; Sonntag, M.; Geerlof, A.; Gabel, F.; Gebauer, F.; Sattler, M. Structural basis for the assembly of the Sxl-Unr translation regulatory complex. Nature, 2014, 515(7526), 287-290.
[http://dx.doi.org/10.1038/nature13693] [PMID: 25209665]
[43]
Marvin, D.A.; Symmons, M.F.; Straus, S.K. Structure and assembly of filamentous bacteriophages. Prog. Biophys. Mol. Biol., 2014, 114(2), 80-122.
[http://dx.doi.org/10.1016/j.pbiomolbio.2014.02.003] [PMID: 24582831]
[44]
Day, L.A.; Marzec, C.J.; Reisberg, S.A.; Casadevall, A. DNA packing in filamentous bacteriophages. Annu. Rev. Biophys. Biophys. Chem., 1988, 17, 509-539.
[http://dx.doi.org/10.1146/annurev.bb.17.060188.002453] [PMID: 3293598]
[45]
Mohan, K.; Weiss, G.A. Chemically modifying viruses for diverse applications. ACS Chem. Biol., 2016, 11(5), 1167-1179.
[http://dx.doi.org/10.1021/acschembio.6b00060] [PMID: 26930417]
[46]
Pires, D.P.; Cleto, S.; Sillankorva, S.; Azeredo, J.; Lu, T.K. Genetically engineered phages: A review of advances over the last decade. Microbiol. Mol. Biol. Rev., 2016, 80(3), 523-543.
[http://dx.doi.org/10.1128/MMBR.00069-15] [PMID: 27250768]
[47]
Urquhart, T.; Daub, E.; Honek, J.F. Bioorthogonal modification of the major sheath protein of bacteriophage M13: extending the versatility of bionanomaterial scaffolds. Bioconjug. Chem., 2016, 27(10), 2276-2280.
[http://dx.doi.org/10.1021/acs.bioconjchem.6b00460] [PMID: 27626459]
[48]
Nakashima, Y.; Konigsberg, W.H. Chemical modification and molecular orientation of the B protein in the filamentous bacterial virus Pf1. J. Mol. Biol., 1980, 138(3), 493-501.
[http://dx.doi.org/10.1016/S0022-2836(80)80014-3] [PMID: 6774098]
[49]
Li, K.; Chen, Y.; Li, S.; Nguyen, H.G.; Niu, Z.; You, S.; Mello, C.M.; Lu, X.; Wang, Q. Chemical modification of M13 bacteriophage and its application in cancer cell imaging. Bioconjug. Chem., 2010, 21(7), 1369-1377.
[http://dx.doi.org/10.1021/bc900405q] [PMID: 20499838]
[50]
Zhang, Z.; Grelet, E. Tuning chirality in the self-assembly of rod-like viruses by chemical surface modifications. Soft Matter, 2013, 9, 1015-1024.
[http://dx.doi.org/10.1039/C2SM27264D]
[51]
Berkowitz, S.A.; Day, L.A. Mass, length, composition and structure of the filamentous bacterial virus fd. J. Mol. Biol., 1976, 102(3), 531-547.
[http://dx.doi.org/10.1016/0022-2836(76)90332-6] [PMID: 775110]
[52]
Fleming, K.; Matthews, S. Media for Studies of Partially Aligned States.In: Protein NMR Techniques;; Downing, A.K., Ed.; Methods in Molecular BiologyTM; Humana Press:; Downing, A.K., Ed.; Totowa, NJ, 2004.
[http://dx.doi.org/10.1385/1-59259-809-9:079]
[53]
Meadows, D.L.; Shafer, J.S.; Schultz, J.S. Determining the extent of labeling for tetramethylrhodamine protein conjugates. J. Immunol. Methods, 1991, 143(2), 263-272.
[http://dx.doi.org/10.1016/0022-1759(91)90051-G] [PMID: 1719100]
[54]
Hooker, J.M.; Kovacs, E.W.; Francis, M.B. Interior surface modification of bacteriophage MS2. J. Am. Chem. Soc., 2004, 126(12), 3718-3719.
[http://dx.doi.org/10.1021/ja031790q] [PMID: 15038717]
[55]
Strohalm, M.; Kavan, D.; Novák, P.; Volný, M.; Havlícek, V. mMass 3: a cross-platform software environment for precise analysis of mass spectrometric data. Anal. Chem., 2010, 82(11), 4648-4651.
[http://dx.doi.org/10.1021/ac100818g] [PMID: 20465224]
[56]
Welsh, L.C.; Symmons, M.F.; Marvin, D.A. The molecular structure and structural transition of the α-helical capsid in filamentous bacteriophage Pf1. Acta Crystallogr. D Biol. Crystallogr., 2000, 56(Pt 2), 137-150.
[http://dx.doi.org/10.1107/S0907444999015334] [PMID: 10666593]
[57]
Berman, H.M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T.N.; Weissig, H.; Shindyalov, I.N.; Bourne, P.E. The protein data bank. Nucleic Acids Res., 2000, 28(1), 235-242.
[http://dx.doi.org/10.1093/nar/28.1.235] [PMID: 10592235]
[58]
Sastry, G.M.; Adzhigirey, M.; Day, T.; Annabhimoju, R.; Sherman, W. Protein and ligand preparation: parameters, protocols, and influence on virtual screening enrichments. J. Comput. Aided Mol. Des., 2013, 27(3), 221-234.
[http://dx.doi.org/10.1007/s10822-013-9644-8] [PMID: 23579614]
[59]
Jacobson, M.P.; Pincus, D.L.; Rapp, C.S.; Day, T.J.F.; Honig, B.; Shaw, D.E.; Friesner, R.A. A hierarchical approach to all-atom protein loop prediction. Proteins, 2004, 55(2), 351-367.
[http://dx.doi.org/10.1002/prot.10613] [PMID: 15048827]
[60]
Shelley, J.C.; Cholleti, A.; Frye, L.L.; Greenwood, J.R.; Timlin, M.R.; Uchimaya, M. Epik: a software program for pK(a) prediction and protonation state generation for drug-like molecules. J. Comput. Aided Mol. Des., 2007, 21(12), 681-691.
[http://dx.doi.org/10.1007/s10822-007-9133-z] [PMID: 17899391]
[61]
Harder, E.; Damm, W.; Maple, J.; Wu, C.; Reboul, M.; Xiang, J.Y.; Wang, L.; Lupyan, D.; Dahlgren, M.K.; Knight, J.L.; Kaus, J.W.; Cerutti, D.S.; Krilov, G.; Jorgensen, W.L.; Abel, R.; Friesner, R.A. OPLS3: A force field providing broad coverage of drug-like small molecules and proteins. J. Chem. Theory Comput., 2016, 12(1), 281-296.
[http://dx.doi.org/10.1021/acs.jctc.5b00864] [PMID: 26584231]
[62]
Christie, R.J.; Tadiello, C.J.; Chamberlain, L.M.; Grainger, D.W. Optical properties and application of a reactive and bioreducible thiol-containing tetramethylrhodamine dimer. Bioconjug. Chem., 2009, 20(3), 476-480.
[http://dx.doi.org/10.1021/bc800367e] [PMID: 19249862]
[63]
Hernando, J.; van der Schaaf, M.; van Dijk, E.M.H.P.; Sauer, M.; García-Parajó, M.F.; van Hulst, N.F. Excitonic behavior of rhodamine dimers: A single-molecule study. J. Phys. Chem. A, 2003, 107, 43-52.
[http://dx.doi.org/10.1021/jp0218995]
[64]
Valdes-Aguilera, O.; Neckers, D.C. Aggregation phenomena in xanthene dyes. Acc. Chem. Res., 1989, 22, 171-177.
[http://dx.doi.org/10.1021/ar00161a002]
[65]
Hermanson, G.T. 1 - Functional Targets. Bioconjugate Techniques; Hermanson, G.T., Ed.; Academic Press: San Diego, 1996, pp. 3-136.
[http://dx.doi.org/10.1016/B978-012342335-1/50002-6]
[66]
Schlick, T.L.; Ding, Z.; Kovacs, E.W.; Francis, M.B. Dual-surface modification of the tobacco mosaic virus. J. Am. Chem. Soc., 2005, 127(11), 3718-3723.
[http://dx.doi.org/10.1021/ja046239n] [PMID: 15771505]
[67]
Pogorelov, A.G.; Selezneva, I.I. Evaluation of collagen gel microstructure by scanning electron microscopy. Bull. Exp. Biol. Med., 2010, 150(1), 153-156.
[http://dx.doi.org/10.1007/s10517-010-1091-0] [PMID: 21161075]
[68]
Chen, P-Y.; Hyder, M.N.; Mackanic, D.; Courchesne, N-M.D.; Qi, J.; Klug, M.T.; Belcher, A.M.; Hammond, P.T. Assembly of viral hydrogels for three-dimensional conducting nanocomposites. Adv. Mater., 2014, 26(30), 5101-5107.
[http://dx.doi.org/10.1002/adma.201400828] [PMID: 24782428]
[69]
Yu, T.; Li, Y.; Yang, T.; Gong, Y.; Sudibya, H.G.; Chen, P.; Luo, K.Q.; Liao, K. Fabrication of all-in-one multifunctional phage liquid crystalline fibers. RSC Advances, 2013, 3, 20437-20445.
[http://dx.doi.org/10.1039/c3ra43034k]
[70]
Mao, J.Y.; Belcher, A.M.; Vliet, K.J.V. Genetically engineered phage fibers and coatings for antibacterial applications. Adv. Funct. Mater., 2010, 20, 209-214.
[http://dx.doi.org/10.1002/adfm.200900782]
[71]
Chiang, C-Y.; Mello, C.M.; Gu, J.; Silva, E.C.C.M.; Van Vliet, K.J.; Belcher, A.M. Weaving genetically engineered functionality into mechanically robust virus fibers. Adv. Mater., 2007, 19, 826-832.
[http://dx.doi.org/10.1002/adma.200602262]
[72]
Niyomdecha, S.; Limbut, W.; Numnuam, A.; Kanatharana, P.; Charlermroj, R.; Karoonuthaisiri, N.; Thavarungkul, P. Phage-based capacitive biosensor for Salmonella detection. Talanta, 2018, 188, 658-664.
[http://dx.doi.org/10.1016/j.talanta.2018.06.033] [PMID: 30029427]
[73]
Wu, L.; Lee, L.A.; Niu, Z.; Ghoshroy, S.; Wang, Q. Visualizing cell extracellular matrix (ECM) deposited by cells cultured on aligned bacteriophage M13 thin films. Langmuir, 2011, 27(15), 9490-9496.
[http://dx.doi.org/10.1021/la201580v] [PMID: 21678980]
[74]
Kuhn, J.H.; Wolf, Y.I.; Krupovic, M.; Zhang, Y-Z.; Maes, P.; Dolja, V.V.; Koonin, E.V. Classify viruses - the gain is worth the pain. Nature, 2019, 566(7744), 318-320.
[http://dx.doi.org/10.1038/d41586-019-00599-8] [PMID: 30787460]
[75]
Willis, B.; Eubanks, L.M.; Wood, M.R.; Janda, K.D.; Dickerson, T.J.; Lerner, R.A. Biologically templated organic polymers with nanoscale order. Proc. Natl. Acad. Sci. USA, 2008, 105(5), 1416-1419.
[http://dx.doi.org/10.1073/pnas.0711308105] [PMID: 18216240]

Rights & Permissions Print Cite
Article Metrics
21
1
© 2024 Bentham Science Publishers | Privacy Policy