Bioconjugation of Bacteriophage Pf1 and Extension to Pf1-Based Bionanomaterials

Taylor       Urquhart; Bradley       Howie; Lei       Zhang; Kam    Tong    Leung; John    F.    Honek

doi:10.2174/1573413716999200614142202

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

10

1

Journal Information

For Authors

For Editors

For Reviewers

Explore Articles

Open Access

Open Access Articles

For Visitors

DOI https://dx.doi.org/10.2174/1573413716999200614142202	Print ISSN 1573-4137
Publisher Name Bentham Science Publisher	Online ISSN 1875-6786

Current Nanoscience

Bioconjugation of Bacteriophage Pf1 and Extension to Pf1-Based Bionanomaterials

Abstract Play Pause

Graphical Abstract

Related Journals

Related Books

Abstract