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Bacteriophages in Nanotechnology: History and Future

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Abstract

Bacteriophage (phage) proteins and whole phage particles are being used in the development of new functional materials with nanoscale features. Bacteriophage capsids and accessory structures (tails, tail fibers, etc.), based on size scale, can be considered evolved protein-based nanotechnological structures. Because of the ease of genetic manipulation, bacteriophages are a useful system for developing proteins with applicability to functional material development. Most of these materials fall into two categories – biological sensors and biologically/chemically active peptides. Biological sensors may take advantage of a bacteriophage’s natural tropism for its host bacteria, although this tropism can be modified. Peptides that can be used to create new materials are typically isolated using phage display, a process for identifying peptides with specific binding capacities from a random peptide library. In this review, we describe some of the methods used to create these materials and their potential applications. This has mostly been done in laboratory studies as very few of these materials have been developed into commercialized products. We conclude with a discussion of the challenges to commercialization of the phage-based materials.

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References

  • Ackermann HW (1998) Tailed bacteriophages: the order caudovirales. Adv Virus Res 51:135–201

    PubMed  CrossRef  PubMed Central  CAS  Google Scholar 

  • Ackermann HW (2001) Frequency of morphological phage descriptions in the year 2000. Brief review. Arch Virol 146:843–857

    PubMed  CrossRef  CAS  Google Scholar 

  • Ackermann H, Dubow M (1987) Description and identification of new phages. In: Ackermann H, Dubow M (eds) Viruses of prokaryotes. CRC Press, Boca Raton, pp 103–142

    Google Scholar 

  • Adams MH (1959) Bacteriophages. InterScience, New York

    Google Scholar 

  • Anany H, Chen W, Pelton R, Griffiths MW (2011) Biocontrol of Listeria monocytogenes and Escherichia coli O157:H7 in meat by using phages immobilized on modified cellulose membranes. Appl Environ Microbiol 77:6379–6387

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Ardekani LS, Gargari SL, Rasooli I, Bazl MR, Mohammadi M, Ebrahimizadeh W, Bakherad H, Zare H (2013) A novel nanobody against urease activity of Helicobacter pylori. Int J Infect Dis 17:e723–e728

    PubMed  CrossRef  CAS  Google Scholar 

  • Arya SK, Singh A, Naidoo R, Wu P, McDermott MT, Evoy S (2011) Chemically immobilized T4-bacteriophage for specific Escherichia coli detection using surface plasmon resonance. Analyst 136:486–492

    PubMed  CrossRef  CAS  Google Scholar 

  • Balasubramanian S, Sorokulova IB, Vodyanoy VJ, Simonian AL (2007) Lytic phage as a specific and selective probe for detection of Staphylococcus aureus – a surface plasmon resonance spectroscopic study. Biosens Bioelectron 22:948–955

    PubMed  CrossRef  CAS  Google Scholar 

  • Bardhan NM, Ghosh D, Belcher AM (2014) Carbon nanotubes as in vivo bacterial probes. Nat Commun 5:4918

    PubMed  CrossRef  CAS  Google Scholar 

  • Bassett CA, Becker RO (1962) Generation of electric potentials by bone in response to mechanical stress. Science 137:1063–1064

    PubMed  CrossRef  CAS  Google Scholar 

  • Bell MR, Engleka MJ, Malik A, Strickler JE (2013) To fuse or not to fuse: what is your purpose? Protein Sci 22:1466–1477

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Benhar I, Eshkenazi I, Neufeld T, Opatowsky J, Shaky S, Rishpon J (2001) Recombinant single chain antibodies in bioelectrochemical sensors. Talanta 55:899–907

    PubMed  CrossRef  CAS  Google Scholar 

  • Bonnycastle L, Shen J, Menendez A, Scott J (2001) Production of peptide libraries. In: Barbas CF III, Burton DR, Scott J, Silverman GJ (eds) Phage display: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 16.1–16.28

    Google Scholar 

  • Brzozowska E, Smietana M, Koba M, Gorska S, Pawlik K, Gamian A, Bock WJ (2015) Recognition of bacterial lipopolysaccharide using bacteriophage-adhesin-coated long-period gratings. Biosens Bioelectron 67:93–99

    PubMed  CrossRef  CAS  Google Scholar 

  • Cao B, Yang M, Mao C (2016) Phage as a genetically modifiable supramacromolecule in chemistry, materials and medicine. Acc Chem Res 49:1111–1120

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Chen L, Wang Y, Liu X, Dou S, Liu G, Hnatowich DJ, Rusckowski M (2008) A new TAG-72 cancer marker peptide identified by phage display. Cancer Lett 272:122–132

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Chen PY, Dang X, Klug MT, Qi J, Dorval Courchesne NM, Burpo FJ, Fang N, Hammond PT, Belcher AM (2013) Versatile three-dimensional virus-based template for dye-sensitized solar cells with improved electron transport and light harvesting. ACS Nano 7:6563–6574

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Chiang CY, Mello C, Gu J, Silva E, Van Vliet K, Belcher A (2007) Weaving genetically engineered functionaliry into mechanically robust virus fibers. Adv Mater 19:826–832

    CrossRef  CAS  Google Scholar 

  • Chung WJ, Merzlyak A, Lee SW (2010a) Fabrication of engineered M13 bacteriophages into liquid crystalline films and fibers for directional growth and encapsulation of fibroblasts. Soft Matter 6:4454–4459

    CrossRef  CAS  Google Scholar 

  • Chung WJ, Merzlyak A, Yoo SY, Lee SW (2010b) Genetically engineered liquid-crystalline viral films for directing neural cell growth. Langmuir 26:9885–9890

    PubMed  CrossRef  CAS  Google Scholar 

  • Clark J, Abedon ST, Hyman P (2012) Phages as therapeutic delivery vehicles. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 86–100

    CrossRef  Google Scholar 

  • Comor L, Dolinska S, Bhide K, Pulzova L, Jimenez-Munguia I, Bencurova E, Flachbartova Z, Potocnakova L, Kanova E, Bhide M (2017) Joining the in vitro immunization of alpaca lymphocytes and phage display: rapid and cost effective pipeline for sdAb synthesis. Microb Cell Factories 16:13

    CrossRef  CAS  Google Scholar 

  • Cooper IR, Illsley M, Korobeinyk AV, Whitby RL (2015) Bacteriophage-nanocomposites: an easy and reproducible method for the construction, handling, storage and transport of conjugates for deployment of bacteriophages active against Pseudomonas aeruginosa. J Microbiol Methods 111:111–118

    PubMed  CrossRef  CAS  Google Scholar 

  • Costa LE, Goulart LR, Pereira NC, Lima MI, Duarte MC, Martins VT, Lage PS, Menezes-Souza D, Ribeiro TG, Melo MN, Fernandes AP, Soto M, Tavares CA, Chavez-Fumagalli MA, Coelho EA (2014) Mimotope-based vaccines of Leishmania infantum antigens and their protective efficacy against visceral leishmaniasis. PLoS One 9:e110014

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Dadarwal R, Namvar A, Thomas DF, Hall JC, Warriner K (2009) Organic conducting polymer electrode based sensors for detection of Salmonella infecting bacteriophages. Mater Sci Eng C 29:761–765

    CrossRef  CAS  Google Scholar 

  • Dang X, Yi H, Ham MH, Qi J, Yun DS, Ladewski R, Strano MS, Hammond PT, Belcher AM (2011) Virus-templated self-assembled single-walled carbon nanotubes for highly efficient electron collection in photovoltaic devices. Nat Nanotechnol 6:377–384

    PubMed  CrossRef  CAS  Google Scholar 

  • Denyes JM, Dunne M, Steiner S, Mittelviefhaus M, Weiss A, Schmidt H, Klumpp J, Loessner MJ (2017) Modified bacteriophage S16 long tail fiber proteins for rapid and specific immobilization and detection of Salmonella cells. Appl Environ Microbiol 83:e00277–17

    Google Scholar 

  • Douglas T, Young M (1999) Virus particles as templates for materials synthesis. Adv Mater 11:679–681

    CrossRef  CAS  Google Scholar 

  • Drexler KE (1986) The engines of creation. Anchor Press/Doubleday, New York

    Google Scholar 

  • Dultsev FN, Speight RE, Fiorini MT, Blackburn JM, Abell C, Ostanin VP, Klenerman D (2001) Direct and quantitative detection of bacteriophage by “hearing” surface detachment using a quartz crystal microbalance. Anal Chem 73:3935–3939

    PubMed  CrossRef  CAS  Google Scholar 

  • Fischetti VA (2010) Bacteriophage endolysins: a novel anti-infective to control gram-positive pathogens. Int J Med Microbiol 300:357–362

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Fu Y, Li J (2016) A novel delivery platform based on bacteriophage MS2 virus-like particles. Virus Res 211:9–16

    PubMed  CrossRef  CAS  Google Scholar 

  • Fu L, Li S, Zhang K, Chen I-H, Petrenko VA, Cheng A (2007) Magnetostrictive microcantilever as an advanced transducer for biosensors. Sensors 2007:2929–2941

    CrossRef  Google Scholar 

  • Fu L, Li S, Zhang K, Chen I-H, Barbaree J, Zhang A, Cheng Z (2011) Detection of Bacillus anthracis spores using phage-immobilized magnetostrictive milli/micro cantilevers. IEEE Sensors J 11:1684–1691

    CrossRef  Google Scholar 

  • Green MA, Emery K, Hishikawa Y, Warta W, Dunlop ED (2015) Solar cell efficiency tables (version 45). Prog Photovolt Res Appl 23:1–9

    CrossRef  Google Scholar 

  • Handa H, Gurczynski S, Jackson MP, Auner G, Mao G (2008) Recognition of Salmonella typhimurium by immobilized phage P22 monolayers. Surf Sci 602:1392–1400

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Henry M, Debarbieux L (2012) Tools from viruses: bacteriophage successes and beyond. Virology 434:151–161

    PubMed  CrossRef  CAS  Google Scholar 

  • Hoogenboom HR, de Bruine AP, Hufton SE, Hoet RM, Arends JW, Roovers RC (1998) Antibody phage display technology and its applications. Immunotechnology 4:1–20

    PubMed  CrossRef  CAS  Google Scholar 

  • Hosseinidoust Z, Olsson AL, Tufenkji N (2014) Going viral: designing bioactive surfaces with bacteriophage. Colloids Surf B Biointerfaces 124:2–16

    PubMed  CrossRef  CAS  Google Scholar 

  • Houshmand H, Froman G, Magnusson G (1999) Use of bacteriophage T7 displayed peptides for determination of monoclonal antibody specificity and biosensor analysis of the binding reaction. Anal Biochem 268:363–370

    PubMed  CrossRef  CAS  Google Scholar 

  • Huang S, Yang H, Lakshmanan RS, Johnson ML, Wan J, Chen I-H, Wikle HC III, Petrenko VA, Barbaree JM, Chin BA (2009) Sequential detection of Salmonella typhimurium and Bacillus anthracis spores using magnetoelastic biosensors. Biosens Bioelectron 24:1730–1736

    PubMed  CrossRef  CAS  Google Scholar 

  • Huang R, Ma H, Guo Y, Liu S, Kuang Y, Shao K, Li J, Liu Y, Han L, Huang S, An S, Ye L, Lou J, Jiang C (2013) Angiopep-conjugated nanoparticles for targeted long-term gene therapy of Parkinson’s disease. Pharm Res 30:2549–2559

    PubMed  CrossRef  CAS  Google Scholar 

  • Hyman P (2012) Bacteriophages and nanostructured materials. Adv Appl Microbiol 78:55–73

    PubMed  CrossRef  CAS  Google Scholar 

  • Hyman P (2017) Phage receptor. In: Reference module in life sciences. Elsevier

    Google Scholar 

  • Hyman P, Valluzzi R, Goldberg E (2002) Design of protein struts for self-assembling nanoconstructs. Proc Natl Acad Sci U S A 99:8488–8493

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Jahns AC, Rehm BH (2012) Relevant uses of surface proteins – display on self-organized biological structures. Microb Biotechnol 5:188–202

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • James SW, Tatam RP (2003) Optical fibre long-period grating sensors: characteristics and application. Meas Sci Technol 14:R49–R61

    CrossRef  CAS  Google Scholar 

  • Jarvinen TA, May U, Prince S (2015) Systemically administered, target organ-specific therapies for regenerative medicine. Int J Mol Sci 16:23556–23571

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Jeong CK, Kim I, Park KI, Oh MH, Paik H, Hwang GT, No K, Nam YS, Lee KJ (2013) Virus-directed design of a flexible BaTiO3 nanogenerator. ACS Nano 7:11016–11025

    PubMed  CrossRef  CAS  Google Scholar 

  • Johnson ML, Wan J, Huang S, Cheng Z, Petrenko VA, Kim DJ, Chen IH, Barbaree JM, Hong JW, Chin BA (2008) A wireless biosensor using microfabricated phage-interfaced magnetoelastic particles. Sensors Actuators A 144:38–47

    CrossRef  CAS  Google Scholar 

  • Jordan PC, Patterson DP, Saboda KN, Edwards EJ, Miettinen HM, Basu G, Thielges MC, Douglas T (2016) Self-assembling biomolecular catalysts for hydrogen production. Nat Chem 8:179–185

    PubMed  CrossRef  CAS  Google Scholar 

  • Karimi M, Mirshekari H, Moosavi Basri SM, Bahrami S, Moghoofei M, Hamblin MR (2016) Bacteriophages and phage-inspired nanocarriers for targeted delivery of therapeutic cargos. Adv Drug Deliv Rev 106:45–62

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Kretzer JW, Lehmann R, Schmelcher M, Banz M, Kim KP, Korn C, Loessner MJ (2007) Use of high-affinity cell wall-binding domains of bacteriophage endolysins for immobilization and separation of bacterial cells. Appl Environ Microbiol 73:1992–2000

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Kudva IT, Jelacic S, Tarr PI, Youderian P, Hovde CJ (1999) Biocontrol of Escherichia coli O157 with O157-specific bacteriophages. Appl Environ Microbiol 65:3767–3773

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ladner RC, Sato AK, Gorzelany J, de Souza M (2004) Phage display-derived peptides as therapeutic alternatives to antibodies. Drug Discov Today 9:525–529

    PubMed  CrossRef  CAS  Google Scholar 

  • Lakshmanan RS, Guntupalli R, Hu J, Kim DJ, Petrenko VA, Barbaree JM, Chin BA (2007) Phage immobilized magnetoelastic sensor for the detection of Salmonella typhimurium. J Microbiol Methods 71:55–60

    PubMed  CrossRef  CAS  Google Scholar 

  • Lee SW, Mao C, Flynn CE, Belcher AM (2002) Ordering of quantum dots using genetically engineered viruses. Science 296:892–895

    PubMed  CrossRef  CAS  Google Scholar 

  • Lee YJ, Yi H, Kim WJ, Kang K, Yun DS, Strano MS, Ceder G, Belcher AM (2009) Fabricating genetically engineered high-power lithium-ion batteries using multiple virus genes. Science 324:1051–1055

    PubMed  CAS  Google Scholar 

  • Lee YJ, Lee Y, Oh D, Chen T, Ceder G, Belcher AM (2010) Biologically activated noble metal alloys at the nanoscale: for lithium ion battery anodes. Nano Lett 10:2433–2440

    PubMed  CrossRef  CAS  Google Scholar 

  • Lee BY, Zhang J, Zueger C, Chung WJ, Yoo SY, Wang E, Meyer J, Ramesh R, Lee SW (2012) Virus-based piezoelectric energy generation. Nat Nanotechnol 7:351–356

    PubMed  CrossRef  CAS  Google Scholar 

  • Liedberg B, Nylander C, Lundstrom I (1983) Surface plasmon resonance for gas detection and biosensing. Sensors Actuators 4:299–304

    CrossRef  CAS  Google Scholar 

  • Liu JK (2014) The history of monoclonal antibody development – progress, remaining challenges and future innovations. Ann Med Surg (Lond) 3:113–116

    CrossRef  Google Scholar 

  • Liu A, Abbineni G, Mao C (2009) Nanocomposite films assembled from genetically engineered filamentous viruses and gold nanoparticles. Adv Mater 21:1001–1005

    CrossRef  CAS  Google Scholar 

  • Lone A, Anany H, Hakeem M, Aguis L, Avdjian A-C, Bouget M, Atashi A, Brovko L, Rochefort D, Griffiths MW (2016) Development of prototypes of bioactive packaging materials based on immobilized bacteriophages for control of growth of bacterial pathogens in foods. Int J Food Microbiol 217:49–58

    PubMed  CrossRef  CAS  Google Scholar 

  • Mao C, Flynn CE, Hayhurst A, Sweeney R, Qi J, Georgiou G, Iverson B, Belcher AM (2003) Viral assembly of oriented quantum dot nanowires. Proc Natl Acad Sci U S A 100:6946–6951

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Mao C, Solis DJ, Reiss BD, Kottmann ST, Sweeney RY, Hayhurst A, Georgiou G, Iverson B, Belcher AM (2004) Virus-based toolkit for the directed synthesis of magnetic and semiconducting nanowires. Science 303:213–217

    PubMed  CrossRef  CAS  Google Scholar 

  • Marti R, Zurfluh K, Hagens S, Pianezzi J, Klumpp J, Loessner MJ (2013) Long tail fibres of the novel broad-host-range T-even bacteriophage S16 specifically recognize Salmonella OmpC. Mol Microbiol 87:818–834

    PubMed  CrossRef  CAS  Google Scholar 

  • Mejri MB, Baccar H, Baldrich E, Del Campo FJ, Helali S, Ktari T, Simonian A, Aouni M, Abdelghani A (2010) Impedance biosensing using phages for bacteria detection: generation of dual signals as the clue for in-chip assay confirmation. Biosens Bioelectron 26:1261–1267

    PubMed  CrossRef  CAS  Google Scholar 

  • Merlin M, Gecchele E, Capaldi S, Pezzotti M, Avesani L (2014) Comparative evaluation of recombinant protein production in different biofactories: the green perspective. Biomed Res Int 2014:136419

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Merzlyak A, Indrakanti S, Lee SW (2009) Genetically engineered nanofiber-like viruses for tissue regenerating materials. Nano Lett 9:846–852

    PubMed  CrossRef  CAS  Google Scholar 

  • Minary-Jolandan M, Yu MF (2009) Nanomechanical heterogeneity in the gap and overlap regions of type I collagen fibrils with implications for bone heterogeneity. Biomacromolecules 10:2565–2570

    PubMed  CrossRef  CAS  Google Scholar 

  • Murugesan M, Abbineni G, Nimmo SL, Cao B, Mao C (2013) Virus-based photo-responsive nanowires formed by linking site-directed mutagenesis and chemical reaction. Sci Rep 3:1820

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Myerson JW, Brenner JS, Greineder CF, Muzykantov VR (2015) Systems approaches to design of targeted therapeutic delivery. Wiley Interdiscip Rev Syst Biol Med 7:253–265

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Nam KT, Kim DW, Yoo PJ, Chiang CY, Meethong N, Hammond PT, Chiang YM, Belcher AM (2006) Virus-enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science 312:885–888

    PubMed  CrossRef  CAS  Google Scholar 

  • Nam KT, Wartena R, Yoo PJ, Liau FW, Lee YJ, Chiang YM, Hammond PT, Belcher AM (2008) Stamped microbattery electrodes based on self-assembled M13 viruses. Proc Natl Acad Sci U S A 105:17227–17231

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Nam YS, Magyar AP, Lee D, Kim JW, Yun DS, Park H, Pollom TS Jr, Weitz DA, Belcher AM (2010a) Biologically templated photocatalytic nanostructures for sustained light-driven water oxidation. Nat Nanotechnol 5:340–344

    PubMed  CrossRef  CAS  Google Scholar 

  • Nam YS, Shin T, Park H, Magyar AP, Choi K, Fantner G, Nelson KA, Belcher AM (2010b) Virus-templated assembly of porphyrins into light-harvesting nanoantennae. J Am Chem Soc 132:1462–1463

    PubMed  CrossRef  CAS  Google Scholar 

  • Nanduri V, Balasubramanian S, Sista S, Vodyanoy VJ, Simonian AL (2007a) Highly sensitive phage-based biosensor for the detection of beta-galactosidase. Anal Chim Acta 589:166–172

    PubMed  CrossRef  CAS  Google Scholar 

  • Nanduri V, Sorokulova IB, Samoylov AM, Simonian AL, Petrenko VA, Vodyanoy V (2007b) Phage as a molecular recognition element in biosensors immobilized by physical adsorption. Biosens Bioelectron 22:986–992

    PubMed  CrossRef  CAS  Google Scholar 

  • Neltner B, Peddie B, Xu A, Doenlen W, Durand K, Yun DS, Speakman S, Peterson A, Belcher A (2010) Production of hydrogen using nanocrystalline protein-templated catalysts on m13 phage. ACS Nano 4:3227–3235

    PubMed  CrossRef  CAS  Google Scholar 

  • Niu Z, Bruckman MA, Harp B, Mello CM, Wang Q (2008) Bacteriophage M13 as a scaffold for preparing conductive polymeric composite fibers. Nano Res 1:235–241

    CrossRef  CAS  Google Scholar 

  • Noren KA, Noren CJ (2001) Construction of high-complexity combinatorial phage display peptide libraries. Methods 23:169–178

    PubMed  CrossRef  CAS  Google Scholar 

  • Oh JW, Chung WJ, Heo K, Jin HE, Lee BY, Wang E, Zueger C, Wong W, Meyer J, Kim C, Lee SY, Kim WG, Zemla M, Auer M, Hexemer A, Lee SW (2014) Biomimetic virus-based colourimetric sensors. Nat Commun 5:3043

    PubMed  CrossRef  CAS  Google Scholar 

  • Olichon A, de Marco A (2012) Preparation of a naive library of camelid single domain antibodies. Methods Mol Biol 911:65–78

    PubMed  CrossRef  CAS  Google Scholar 

  • Olsen EV, Sorokulova IB, Petrenko VA, Chen IH, Barbaree JM, Vodyanoy VJ (2006) Affinity-selected filamentous bacteriophage as a probe for acoustic wave biodetectors of Salmonella typhimurium. Biosens Bioelectron 21:1434–1442

    PubMed  CrossRef  CAS  Google Scholar 

  • Omidfar K, Daneshpour M (2015) Advances in phage display technology for drug discovery. Expert Opin Drug Discov 10:651–669

    PubMed  CrossRef  CAS  Google Scholar 

  • Park JP, Do M, Jin HE, Lee SW, Lee H (2014) M13 bacteriophage displaying DOPA on surfaces: fabrication of various nanostructured inorganic materials without time-consuming screening processes. ACS Appl Mater Interfaces 6:18653–18660

    PubMed  CrossRef  CAS  Google Scholar 

  • Pasqualini R, Ruoslahti E (1996) Organ targeting in vivo using phage display peptide libraries. Nature 380:364–366

    PubMed  CrossRef  CAS  Google Scholar 

  • Petrenko VA, Gillespie JW (2017) Paradigm shift in bacteriophage-mediated delivery of anticancer drugs: from targeted ‘magic bullets’ to self-navigated ‘magic missiles’. Expert Opin Drug Deliv 14:373–384

    PubMed  CrossRef  CAS  Google Scholar 

  • Rakhuba DV, Kolomiets EI, Dey ES, Novik GI (2010) Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol 59:145–155

    PubMed  CAS  Google Scholar 

  • Rakonjac J, Bennett NJ, Spagnuolo J, Gagic D, Russel M (2011) Filamentous bacteriophage: biology, phage display and nanotechnology applications. Curr Issues Mol Biol 13:51–76

    PubMed  CAS  Google Scholar 

  • Ramakrishnan SK, Jebors S, Martin M, Cloitre T, Agarwal V, Mehdi A, Martinez J, Subra G, Gergely C (2015) Engineered adhesion peptides for improved silicon adsorption. Langmuir 31:11868–11874

    PubMed  CrossRef  CAS  Google Scholar 

  • Reiss BD, Mao CB, Solis DJ, Ryan KS, Thomson T, Belcher AM (2004) Biological routes to metal alloy ferromagnetic nanostructures. Nano Lett 4:1127–1132

    CrossRef  CAS  Google Scholar 

  • Ren Z, Black LW (1998) Phage T4 SOC and HOC display of biologically active, full-length proteins on the viral capsid. Gene 215:439–444

    PubMed  CrossRef  CAS  Google Scholar 

  • Roach DR, Donovan DM (2015) Antimicrobial bacteriophage-derived proteins and therapeutic applications. Bacteriophage 5:e1062590

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Rozand C, Feng PC (2009) Specificity analysis of a novel phage-derived ligand in an enzyme-linked fluorescent assay for the detection of Escherichia coli O157:H7. J Food Prot 72:1078–1081

    PubMed  CrossRef  Google Scholar 

  • Samuelson P, Hansson M, Ahlborg N, Andreoni C, Gotz F, Bachi T, Nguyen TN, Binz H, Uhlen M, Stahl S (1995) Cell surface display of recombinant proteins on Staphylococcus carnosus. J Bacteriol 177:1470–1476

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Savoye F, Feng P, Rozand C, Bouvier M, Gleizal A, Thevenot D (2011) Comparative evaluation of a phage protein ligand assay with real-time PCR and a reference method for the detection of Escherichia coli O157:H7 in raw ground beef and trimmings. J Food Prot 74:6–12

    PubMed  CrossRef  CAS  Google Scholar 

  • Schmelcher M, Loessner MJ (2014) Application of bacteriophages for detection of foodborne pathogens. Bacteriophage. 4:e28137

    PubMed  PubMed Central  CrossRef  Google Scholar 

  • Seker UO, Demir HV (2011) Material binding peptides for nanotechnology. Molecules 16:1426–1451

    PubMed  CrossRef  PubMed Central  CAS  Google Scholar 

  • Shabani A, Zourob M, Allain B, Marquette CA, Lawrence MF, Mandeville R (2008) Bacteriophage-modified microarrays for the direct impedimetric detection of bacteria. Anal Chem 80:9475–9482

    PubMed  CrossRef  CAS  Google Scholar 

  • Shin D-M, Han HJ, Kim W-G, Kim E, Kim C, Hong SW, Kim HK, Oh J-W, Hwang Y-H (2015) Bioinspired piezoelectric nanogenerators based on vertically aligned phage nanopillars. Energy Environ Sci 8:3198–3203

    CrossRef  CAS  Google Scholar 

  • Siegel DL (2012) Clinical applications of phage display peptides. In: Hyman P, Abedon ST (eds) Bacteriophages in health and disease. CABI Press, Wallingford, pp 101–118

    CrossRef  Google Scholar 

  • Singh A, Glass N, Tolba M, Brovko L, Griffiths M, Evoy S (2009) Immobilization of bacteriophages on gold surfaces for the specific capture of pathogens. Biosens Bioelectron 24:3645–3651

    PubMed  CrossRef  CAS  Google Scholar 

  • Singh A, Arya SK, Glass N, Hanifi-Moghaddam P, Naidoo R, Szymanski CM, Tanha J, Evoy S (2010) Bacteriophage tailspike proteins as molecular probes for sensitive and selective bacterial detection. Biosens Bioelectron 26:131–138

    PubMed  CrossRef  CAS  Google Scholar 

  • Singh A, Arutyunov D, McDermott MT, Szymanski CM, Evoy S (2011) Specific detection of Campylobacter jejuni using the bacteriophage NCTC 12673 receptor binding protein as a probe. Analyst 136:4780–4786

    PubMed  CrossRef  CAS  Google Scholar 

  • Singh A, Arutyunov D, Szymanski CM, Evoy S (2012) Bacteriophage based probes for pathogen detection. Analyst 137:3405–3421

    PubMed  CrossRef  CAS  Google Scholar 

  • Smartt AE, Ripp S (2011) Bacteriophage reporter technology for sensing and detecting microbial targets. Anal Bioanal Chem 400:991–1007

    PubMed  CrossRef  CAS  Google Scholar 

  • Smietana M, Bock WJ, Mikulic P, Ng A, Chinnappan R, Zourob M (2011) Detection of bacteria using bacteriophages as recognition elements immobilized on long-period fiber gratings. Opt Express 19:7971–7978

    PubMed  CrossRef  CAS  Google Scholar 

  • Smith GP (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science 228:1315–1317

    PubMed  CrossRef  CAS  Google Scholar 

  • Smith GP, Petrenko VA (1997) Phage display. Chem Rev 97:391–410

    PubMed  CrossRef  CAS  Google Scholar 

  • Sohrab SS, Karim S, Kamal MA, Abuzenadah AM, Chaudhary AG, Al-Qahtani MH, Mirza Z (2014) Bacteriophage – a common divergent therapeutic approach for Alzheimer’s disease and type II diabetes mellitus. CNS Neurol Disord Drug Targets 13:491–500

    PubMed  CrossRef  CAS  Google Scholar 

  • Taniguchi N (1974) On the basic concept of ‘Nano-Technology’. In: Proceedings of the international conference on production engineering, Tokyo, Part II. Japan Society of Precision Engineering, Tokyo

    Google Scholar 

  • Tay LL, Huang PJ, Tanha J, Ryan S, Wu X, Hulse J, Chau LK (2012) Silica encapsulated SERS nanoprobe conjugated to the bacteriophage tailspike protein for targeted detection of Salmonella. Chem Commun (Camb) 48:1024–1026

    CrossRef  CAS  Google Scholar 

  • Tlili C, Sokullu E, Safavieh M, Tolba M, Ahmed MU, Zourob M (2013) Bacteria screening, viability, and confirmation assays using bacteriophage-impedimetric/loop-mediated isothermal amplification dual-response biosensors. Anal Chem 85:4893–4901

    PubMed  CrossRef  CAS  Google Scholar 

  • Tolba M, Minikh O, Brovko LY, Evoy S, Griffiths MW (2010) Oriented immobilization of bacteriophages for biosensor applications. Appl Environ Microbiol 76:528–535

    PubMed  CrossRef  CAS  Google Scholar 

  • Tolba M, Ahmed MU, Tlili C, Eichenseher F, Loessner MJ, Zourob M (2012) A bacteriophage endolysin-based electrochemical impedance biosensor for the rapid detection of Listeria cells. Analyst 137:5749–5756

    PubMed  CrossRef  CAS  Google Scholar 

  • Tripathi SM, Bock WJ, Mikulic P, Chinnappan R, Ng A, Tolba M, Zourob M (2012) Long period grating based biosensor for the detection of Escherichia coli bacteria. Biosens Bioelectron 35:308–312

    PubMed  CrossRef  CAS  Google Scholar 

  • Tseng RJ, Tsai C, Ma L, Ouyang J, Ozkan CS, Yang Y (2006) Digital memory device based on tobacco mosaic virus conjugated with nanoparticles. Nat Nanotechnol 1:72–77

    PubMed  CrossRef  CAS  Google Scholar 

  • Urquhart T, Daub E, Honek JF (2016) Bioorthogonal modification of the major sheath protein of bacteriophage M13: extending the versatility of bionanomaterial scaffolds. Bioconjug Chem 27:2276–2280

    PubMed  CrossRef  CAS  Google Scholar 

  • Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D, Hull MS (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769–1780

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Walcher G, Stessl B, Wagner M, Eichenseher F, Loessner MJ, Hein I (2010) Evaluation of paramagnetic beads coated with recombinant Listeria phage endolysin-derived cell-wall-binding domain proteins for separation of Listeria monocytogenes from raw milk in combination with culture-based and real-time polymerase chain reaction-based quantification. Foodborne Pathog Dis 7:1019–1024

    PubMed  CrossRef  CAS  Google Scholar 

  • Wan J, Johnson ML, Guntupalli R, Petrenko VA, Chin BA (2007) Detection of Bacillus anthracis spores in liquid using phage-based magnetoelastic micro-resonators. Sensors Actuators B 127:559–566

    CrossRef  CAS  Google Scholar 

  • Wang C, Sauvageau D, Elias A (2016) Immobilization of active bacteriophages on polyhydroxyalkanoate surfaces. ACS Appl Mater Interfaces 8:1128–1138

    PubMed  CrossRef  CAS  Google Scholar 

  • Whaley SR, English DS, Hu EL, Barbara PF, Belcher AM (2000) Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly. Nature 405:665–668

    PubMed  CrossRef  CAS  Google Scholar 

  • Whitney MA, Crisp JL, Nguyen LT, Friedman B, Gross LA, Steinbach P, Tsien RY, Nguyen QT (2011) Fluorescent peptides highlight peripheral nerves during surgery in mice. Nat Biotechnol 29:352–356

    PubMed  PubMed Central  CrossRef  CAS  Google Scholar 

  • Yang LM, Tam PY, Murray BJ, McIntire TM, Overstreet CM, Weiss GA, Penner RM (2006) Virus electrodes for universal biodetection. Anal Chem 78:3265–3270

    PubMed  CrossRef  CAS  Google Scholar 

  • Ye X, Hemida M, Zhang HM, Hanson P, Ye Q, Yang D (2012) Current advances in Phi29 pRNA biology and its application in drug delivery. Wiley Interdiscip Rev RNA 3:469–481

    PubMed  CrossRef  CAS  Google Scholar 

  • Yoo SY, Chung WJ, Kim TH, Le M, Lee SW (2011a) Facile patterning of genetically engineered M13 bacteriophage for directional growth of human fibroblast cells. Soft Matter 7:363–368

    CrossRef  CAS  Google Scholar 

  • Yoo SY, Kobayashi M, Lee PP, Lee SW (2011b) Early osteogenic differentiation of mouse preosteoblasts induced by collagen-derived DGEA-peptide on nanofibrous phage tissue matrices. Biomacromolecules 12:987–996

    PubMed  CrossRef  CAS  Google Scholar 

  • Yoo SY, Merzlyak A, Lee SW (2011c) Facile growth factor immobilization platform based on engineered phage matrices. Soft Matter 7:1660–1666

    CrossRef  CAS  Google Scholar 

  • Zhu H, White IM, Suter JD, Fan X (2008) Phage-based label-free biomolecule detection in an opto-fluidic ring resonator. Biosens Bioelectron 24:461–466

    PubMed  CrossRef  CAS  Google Scholar 

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Glossary

Adhesin

Most generically, any protein or other structures a microbe uses for attachment, but in this chapter a bacteriophage adhesin is essentially the same as the receptor binding protein.

Antigen binding region

In an antibody or related molecule, the region that actually contacts and has affinity for the antigen; elsewhere this is also called the epitope binding region.

Binding affinity

The strength of interaction between two molecules, one of which binds the other.

Binding peptides

In general, a peptide with binding affinity for some target molecule; more specifically a peptide in a phage or other display library with affinity for a target molecule or material.

Bionanotechnology or nanobiotechnology

The field of science or technology concerned with using biological molecules such as proteins or nucleic acids to create a material with nanoscale functional features.

Biosensor

A sensor that detects the presence of some microorganism or other biological molecule.

Biotin/biotinylation

Biotin is a small organic molecule that can be attached to proteins (biotinylation) to act as an attachment site for streptavidin or avidin, which is usually attached to some detection molecule. Thus, the biotin-streptavidin acts as an attachment linkage between two molecules that otherwise have no affinity for each other. Biotin is attached to biotinylation sites within a protein (naturally or by genetic engineering) by enzymes normally found in E. coli or other protein expression systems.

Carbon nanotube

Cylindrical nanostructures composed of carbon with an extended fullerene structure. Carbon nanotubes can be chemically modified using a variety of organic chemistry reactions to attach other molecules as linkers for attachment. Carbon nanotubes have useful optical, thermal, electrical, and other properties for materials applications.

Cell wall binding domain (CBD)

The domain in endolysins with affinity for a bacterial cell wall component.

Conjugation

In the context of this chapter, conjugation refers to the joining of two entities via a chemical linkage.

Liquid crystal

A phase of matter in which molecules form ordered crystalline regions under certain conditions but can become disordered when conditions change. Properties such as ability to flow, optical properties, and others may be quite different between the two conditions making liquid crystals useful as sensors or transducers.

Nanocrystal/nanoparticle

A particle of uniform composition with at least one dimension measuring less than 100 nm. Quantum dots are a subset of nanocrystals. Nanocrystals may be coated with other materials increasing their size above the nanoscale without loss of some useful nanocrystal properties.

Nanomaterials

A general term for any material with a functionality due to some nanoscale feature or molecule.

Nanoscale (nanoscopic scale)

A size scale between 1 and 100 nm.

Paramagnetic bead

Beads usually made of iron oxide that are magnetic and attracted to an external magnetic field but not magnetic in the absence of the external field. Paramagnetic beads are typically too large to be nanoparticles.

Piezoelectric

The property of a material that gains an electrical charge in response to mechanical stress. Piezoelectric materials may be inorganic or organic.

Quantum dot

A nanocrystal of a semiconductor material whose size and composition result in it acting as a single atom with electron energy state transitions being quantized. Physical properties such as absorption and emission of light will be different in quantum dots of the same composition, but different sizes although chemical properties will be identical.

Self-assembly

A process in which subunits assemble into an ordered structure based in internal properties without external, nonstructural components. Bacteriophage capsids and appendages are often described as self-assembling although they may require a few nonstructural proteins (chaperones) for complete assembly.

Semiconductor

A material typically composed of one or more of the metalloid elements whose conductivity is less than a metal conductor but more than a nonmetal insulator. Semiconductors’ electrical properties can change in response to external stimuli such as electrical fields or temperature. They are used in construction of transistors and integrated circuits.

Single-chain antibody (ScFv)

An antibody-like protein in which the heavy and light subunits are joined into a single polypeptide. These proteins may be derived from naturally made camelid single-chain antibodies or by genetic engineering of mammalian four-chain antibodies to fuse the light and heavy chain binding domains into a single polypeptide. ScFvs have just a single antigen binding domain per molecule; hence they are also described as single-domain antibodies.

Tag

Any peptide sequence added to a protein to allow for binding of a marker entity for detection or other purposes. In some embodiments, the tag is a large marker such as GFP.

Transduction or signal transduction (non-biological, not phage transduction of genetic material)

In the context of this chapter, transduction methods are ways of converting the binding of a molecule to a biosensor into a detectable signal. The output signal may be mechanical, optical, or electrical. Details of methods discussed in this chapter are found in the section “Signal Transduction Methods.”

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Hyman, P., Denyes, J. (2018). Bacteriophages in Nanotechnology: History and Future. In: Harper, D., Abedon, S., Burrowes, B., McConville, M. (eds) Bacteriophages. Springer, Cham. https://doi.org/10.1007/978-3-319-40598-8_22-1

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