Skip to main content
SpringerLink
Log in

M13 Bacteriophage-Based Bio-nano Systems for Bioapplication

  • Review Article
  • Published:
BioChip Journal Aims and scope Submit manuscript

Abstract

M13 bacteriophage is a promising biomolecule with unique biochemical and structural traits (e.g., high aspect ratio, 2700 copies of identical coat proteins covering the phage surface) that can also be programmable, making it a versatile material for bio-nano and biomimetic applications. Although M13 bacteriophage is mostly known as a carrier in the phage display screening process, pioneers have used the phage’s properties to develop the virus into a bionanomaterial that can be used for various applications. This study reviews M13 bacteriophage-based bio-nano systems derived from the structural and biochemical properties of M13 bacteriophage for both bio-nano and material science applications. Two major approaches regarding the fabrication of the bio-nano systems are introduced: surface engineering of individual M13 bacteriophage into single bio-nano templates and self-assembly of M13 bacteriophages into bio-nano matrices. Various genetic engineering and chemical engineering methods are reported for the surface engineering of M13 bacteriophage, which enables the bionanomaterial to have a wide range of functionalities. The bio-nano and material science applications of the self-assembled bio-nano matrices are also examined in this study. These complex engineered M13 bacteriophage-based matrices are capable of guiding a new generation of bionanomaterials for bio-nano and material science applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Barderas, R., Benito-Peña, E.: The 2018 Nobel Prize in chemistry: phage display of peptides and antibodies. Anal. Bioanal. Chem. 411, 2475–2479 (2019)

    Article  CAS  PubMed  Google Scholar 

  2. Smith, G.P., Petrenko, V.A.: Phage display. Chem. Rev. 97, 391–410 (1997)

    Article  CAS  PubMed  Google Scholar 

  3. Nam, K.T., et al.: Virus-enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science 312, 885–888 (2006)

    Article  CAS  PubMed  Google Scholar 

  4. Li, K., et al.: Chemical modification of M13 bacteriophage and its application in cancer cell imaging. Bioconjug. Chem. 21, 1369–1377 (2010)

    Article  CAS  PubMed  Google Scholar 

  5. Chung, W.J., Lee, D.Y., Yoo, S.Y.: Chemical modulation of M13 bacteriophage and its functional opportunities for nanomedicine. Int. J. Nanomed. 9, 5825–5836 (2014)

    Google Scholar 

  6. Morag, O., Sgourakis, N.G., Baker, D., Goldbourt, A.: The NMR-Rosetta capsid model of M13 bacteriophage reveals a quadrupled hydrophobic packing epitope. Proc. Natl. Acad. Sci. USA 112, 971–976 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Xu, J., Dayan, N., Goldbourt, A., Xiang, Y.: Cryo-electron microscopy structure of the filamentous bacteriophage IKe. Proc. Natl. Acad. Sci. USA 116, 5493–5498 (2019)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Morag, O., Abramov, G., Goldbourt, A.: Similarities and differences within members of the Ff family of filamentous bacteriophage viruses. J. Phys. Chem. B 115, 15370–15379 (2011)

    Article  CAS  PubMed  Google Scholar 

  9. Beck, E., Zink, B.: Nucleotide sequence and genome organisation of filamentous bacteriophages f1 and fd. Gene 16, 35–58 (1981)

    Article  CAS  PubMed  Google Scholar 

  10. Hill, D.F., Petersen, G.B.: Nucleotide sequence of bacteriophage f1 DNA. J. Virol. 44, 32–46 (1982)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. van Wezenbeek, P.M.G.F., Hulsebos, T.J.M., Schoenmakers, J.G.G.: Nucleotide sequence of the filamentous bacteriophage M13 DNA genome: comparison with phage fd. Gene 11, 129–148 (1980)

    Article  PubMed  Google Scholar 

  12. Haigh, N.G., Webster, R.E.: The pI and pXI assembly proteins serve separate and essential roles in filamentous phage assembly. J. Mol. Biol. 293, 1017–1027 (1999)

    Article  CAS  PubMed  Google Scholar 

  13. Sidhu, S.S.: Engineering M13 for phage display. Biomol. Eng. 18, 57–63 (2001)

    Article  CAS  PubMed  Google Scholar 

  14. Rasched, I., Oberer, E.: Ff coliphages: structural and functional relationships. Microbiol. Rev. 50, 401–427 (1986)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  16. Papavoine, C.H., Christiaans, B.E., Folmer, R.H., Konings, R.N., Hilbers, C.W.: Solution structure of the M13 major coat protein in detergent micelles: a basis for a model of phage assembly involving specific residues. J. Mol. Biol. 282, 401–419 (1998)

    Article  CAS  PubMed  Google Scholar 

  17. Williams, K.A., et al.: Packing of coat protein amphipathic and transmembrane helices in filamentous bacteriophage M13: role of small residues in protein oligomerization. J. Mol. Biol. 252, 6–14 (1995)

    Article  CAS  PubMed  Google Scholar 

  18. Wickner, W.: Mechanisms of membrane assembly: general lessons from the study of M13 coat protein and Escherichia coli leader peptidase. Biochemistry 27, 1081–1086 (1988)

    Article  CAS  PubMed  Google Scholar 

  19. Day, L.A., Marzee, C.J., Reisberg, S.A., Casadevall, A.: DNA packing in filamentous bacteriophages. Annu. Rev. Biophys. Biophys. Chem. 17, 509–539 (1988)

    Article  CAS  PubMed  Google Scholar 

  20. Lubkowski, J., Hennecke, F., Pluckthun, A., Wlodawer, A.: The structural basis of phage display elucidated by the crystal structure of the N-terminal domains of g3p. Nat. Struct. Biol. 5, 140–147 (1998)

    Article  CAS  PubMed  Google Scholar 

  21. Rakonjac, J., Russel, M., Khanum, S., Brooke, S.J., Rajič, M.: Filamentous phage: structure and biology. Recombin. Antibod. Infect. Dis. 1053, 1–20 (2017)

    Article  CAS  Google Scholar 

  22. Yang, S.H., Chung, W.J., McFarland, S., Lee, S.W.: Assembly of bacteriophage into functional materials. Chem. Rec. 13, 43–59 (2013)

    Article  CAS  PubMed  Google Scholar 

  23. Glucksman, M.J., Bhattacharjee, S., Makowski, L.: Three-dimensional structure of a cloning vector: X-ray diffraction studies of filamentous bacteriophage M13 at 7 Å resolution. J. Mol. Biol. 226, 455–470 (1992)

    Article  CAS  PubMed  Google Scholar 

  24. Goldbourt, A.: Structural characterization of bacteriophage viruses by NMR. Prog. Nucl. Magn. Reson. Spectrosc. 114, 192–210 (2019)

    Article  PubMed  CAS  Google Scholar 

  25. Branston, S.D., Stanley, E.C., Ward, J.M., Keshavarz-Moore, E.: Determination of the survival of bacteriophage M13 from chemical and physical challenges to assist in its sustainable bioprocessing. Biotechnol. Bioprocess Eng. 18, 560–566 (2013)

    Article  CAS  Google Scholar 

  26. Stopar, D., Spruijt, R.B., Wolfs, C.J., Hemminga, M.A.: Mimicking initial interactions of bacteriophage M13 coat protein disassembly in model membrane systems. Biochemistry 37, 10181–10187 (1998)

    Article  CAS  PubMed  Google Scholar 

  27. Muzard, J., Platt, M., Lee, G.U.: M13 Bacteriophage-activated superparamagnetic beads for affinity separation. Small 8, 2403–2411 (2012)

    Article  CAS  PubMed  Google Scholar 

  28. Lee, B.Y., et al.: Virus-based piezoelectric energy generation. Nat. Nanotechnol. 7, 351–356 (2012)

    Article  CAS  PubMed  Google Scholar 

  29. Lee, J.H., Domaille, D.W., Cha, J.N.: Amplified protein detection and identification through DNA-conjugated M13 bacteriophage. ACS Nano 6, 5621–5626 (2012)

    Article  CAS  PubMed  Google Scholar 

  30. Domaille, D.W., Lee, J.H., Cha, J.N.: High density DNA loading on the m13 bacteriophage provides access to colorimetric and fluorescent protein microarray biosensors. Chem. Commun. 49, 1759–1761 (2013)

    Article  CAS  Google Scholar 

  31. Flynn, C.E., Lee, S.W., Peelle, B.R., Belcher, A.M.: Viruses as vehicles for growth, organization and assembly of materials. Acta Mater. 51, 5867–5880 (2003)

    Article  CAS  Google Scholar 

  32. Jaworski, J.W., Raorane, D., Huh, J.H., Majumdar, A., Lee, S.W.: Evolutionary screening of biomimetic coatings for selective detection of explosives. Langmuir 24, 4938–4943 (2008)

    Article  CAS  PubMed  Google Scholar 

  33. Sarikaya, M., Tamerler, C., Jen, A.K., Schulten, K., Baneyx, F.: Molecular biomimetics: nanotechnology through biology. Nat. Mater. 2, 577–585 (2003)

    Article  CAS  PubMed  Google Scholar 

  34. Mao, C., et al.: Viral assembly of oriented quantum dot nanowires. Proc. Natl. Acad. Sci. USA 100, 6946–6951 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Belcher, A.M., et al.: Virus-based genetic toolkit for the directed synthesis of magnetic and semiconducting nanowires. Science 303, 213–217 (2004)

    Article  PubMed  CAS  Google Scholar 

  36. Mao, C., et al.: Virus-based toolkit for the directed synthesis of magnetic and semiconducting nanowires. Science 303, 213–217 (2004)

    Article  CAS  PubMed  Google Scholar 

  37. Ki, T.N., et al.: Stamped microbattery electrodes based on self-assembled M13 viruses. Proc. Natl. Acad. Sci. USA 105, 17227–17231 (2008)

    Article  Google Scholar 

  38. Lee, Y.J., et al.: Fabricating genetically engineered high-power lithium-ion batteries using multiple virus genes. Science 324, 1051–1055 (2009)

    Article  CAS  PubMed  Google Scholar 

  39. Allen, M.A., Kolesnikov-Lindsey, R. & Belcher, A.M. Virus templated lithium ion battery materials: New cathodes for higher energy and capacity. (2010).

  40. Lee, Y.J., et al.: Biologically activated noble metal alloys at the nanoscale: for lithium ion battery anodes. Nano Lett. 10, 2433–2440 (2010)

    Article  CAS  PubMed  Google Scholar 

  41. Lee, Y.J., Belcher, A.M.: Nanostructure design of amorphous FePO4 facilitated by a virus for 3 v lithium ion battery cathodes. J. Mater. Chem. 21, 1033–1039 (2011)

    Article  CAS  Google Scholar 

  42. Xu, K., et al.: Genetically programming interfaces between active materials, conductive pathway and current collector in Li ion batteries. ESC Trans. 41, 55–64 (2012)

    CAS  Google Scholar 

  43. Oh, D., et al.: Biologically enhanced cathode design for improved capacity and cycle life for lithium-oxygen batteries. Nat. Commun. 4, 1–8 (2013)

    Article  CAS  Google Scholar 

  44. Oh, D., et al.: M13 virus-directed synthesis of nanostructured metal oxides for lithium-oxygen batteries. Nano Lett. 14, 4837–4845 (2014)

    Article  CAS  PubMed  Google Scholar 

  45. Moradi, M., et al.: Improving the capacity of sodium ion battery using a virus-templated nanostructured composite cathode. Nano Lett. 15, 2917–2921 (2015)

    Article  CAS  PubMed  Google Scholar 

  46. Zhang, G., Wei, S., Belcher, A.M.: Biotemplated zinc sulfide nanofibers as anode materials for sodium-ion batteries. ACS Appl. Nano Mater. 1, 5631–5639 (2018)

    Article  CAS  Google Scholar 

  47. Records, W.C., Wei, S., Belcher, A.M.: Virus-templated nickel phosphide nanofoams as additive-free, thin-film li-ion microbattery anodes. Small 15, 1903166 (2019)

    Article  CAS  Google Scholar 

  48. Niyogi, S., et al.: Chemistry of single-walled carbon nanotubes. Acc. Chem. Res. 35, 1105–1113 (2002)

    Article  CAS  PubMed  Google Scholar 

  49. Dang, X., et al.: Virus-templated self-assembled single-walled carbon nanotubes for highly efficient electron collection in photovoltaic devices. Nat. Nanotechnol. 6, 377–384 (2011)

    Article  CAS  PubMed  Google Scholar 

  50. Chen, P.Y., et al.: Versatile three-dimensional virus-based template for dye-sensitized solar cells with improved electron transport and light harvesting. ACS Nano 7, 6563–6574 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Dorval Courchesne, N.M., et al.: Constructing multifunctional virus-templated nanoporous composites for thin film solar cells: contributions of morphology and optics to photocurrent generation. J. Phys. Chem. C 119, 13987–14000 (2015)

    Article  CAS  Google Scholar 

  52. Nuraje, N., Lei, Y., Belcher, A.: Virus-templated visible spectrum active perovskite photocatalyst. Catal. Commun. 44, 68–72 (2014)

    Article  CAS  Google Scholar 

  53. Nam, Y.S., et al.: Biologically templated photocatalytic nanostructures for sustained light-driven water oxidation. Nat. Nanotechnol. 5, 340–344 (2010)

    Article  CAS  PubMed  Google Scholar 

  54. Records, W.C., Yoon, Y., Ohmura, J.F., Chanut, N., Belcher, A.M.: Virus-templated Pt–Ni(OH) 2 nanonetworks for enhanced electrocatalytic reduction of water. Nano Energy 58, 167–174 (2019)

    Article  CAS  Google Scholar 

  55. Tao, Z., et al.: Early tumor detection afforded by in vivo imaging of near-infrared II fluorescence. Biomaterials 134, 202–215 (2017)

    Article  CAS  PubMed  Google Scholar 

  56. Bardhan, N.M., Ghosh, D., Belcher, A.M.: M13 Virus based detection of bacterial infections in living hosts. J. Biophoton. 7, 617–623 (2014)

    Article  CAS  Google Scholar 

  57. Yi, H., et al.: M13 phage-functionalized single-walled carbon nanotubes as nanoprobes for second near-infrared window fluorescence imaging of targeted tumors. Nano Lett. 12, 1176–1183 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Ghosh, D., et al.: Deep, noninvasive imaging and surgical guidance of submillimeter tumors using targeted M13-stabilized single-walled carbon nanotubes. Proc. Natl. Acad. Sci. USA 111, 13948–13953 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Ghosh, D., Kohli, A.G., Moser, F., Endy, D., Belcher, A.M.: Refactored M13 bacteriophage as a platform for tumor cell imaging and drug delivery. ACS Synth. Biol. 1, 576–582 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Bardhan, N.M., Ghosh, D., Belcher, A.M.: Carbon nanotubes as in vivo bacterial probes. Nat. Commun. 5, 1–1 (2014)

    Article  CAS  Google Scholar 

  61. Khan, A.R., Williams, K.A., Boggs, J.M., Deber, C.M.: Accessibility and dynamics of Cys residues in Bacteriophage IKe and M13 major coat protein mutants. Biochemistry 34, 12388–12397 (1995)

    Article  CAS  PubMed  Google Scholar 

  62. Spruijt, R.B., Wolfs, C.J.A.M., Verver, J.W.G., Hemminga, M.A.: Accessibility and environment probing using cysteine residues introduced along the putative transmembrane domain of the major coat protein of bacteriophage M13. Biochemistry 35, 10383–10391 (1996)

    Article  CAS  PubMed  Google Scholar 

  63. Heinis, C., Rutherford, T., Freund, S., Winter, G.: Phage-encoded combinatorial chemical libraries based on bicyclic peptides. Nat. Chem. Biol. 5, 502–507 (2009)

    Article  CAS  PubMed  Google Scholar 

  64. Ng, S., Jafari, M.R., Matochko, W.L., Derda, R.: Quantitative synthesis of genetically encoded glycopeptide libraries displayed on M13 phage. ACS Chem. Biol. 7, 1482–1487 (2012)

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Yacoby, I., Shamis, M., Bar, H., Shabat, D., Benhar, I.: Targeting antibacterial agents by using drug-carrying filamentous bacteriophages. Antimicrob. Agents Chemother. 50, 2087–2097 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Carrico, Z.M., et al.: N-Terminal labeling of filamentous phage to create cancer marker imaging agents. ACS Nano 6, 6675–6680 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Adhikari, M., et al.: Functionalized viral nanoparticles as ultrasensitive reporters in lateral-flow assays. Analyst 138, 5584–5587 (2013)

    Article  CAS  PubMed  Google Scholar 

  69. Suthiwangcharoen, N., et al.: M13 bacteriophage-polymer nanoassemblies as drug delivery vehicles. Nano Res. 4, 483–493 (2011)

    Article  CAS  Google Scholar 

  70. Lee, J.H., et al.: M13 bacteriophage as materials for amplified surface enhanced raman scattering protein sensing. Adv. Func. Mater. 24, 2079–2084 (2014)

    Article  CAS  Google Scholar 

  71. Onsager, L.: The effects of shape on the interaction of colloidal particles. Ann. N. Y. Acad. Sci. 51, 627–659 (1949)

    Article  CAS  Google Scholar 

  72. Tjipto-Margo, B., Evans, G.T.: The Onsager theory of the isotropic–nematic liquid–crystal transition: biaxial particles in uniaxial phases. J. Chem. Phys. 94, 4546–4556 (1991)

    Article  Google Scholar 

  73. Tang, J., Fraden, S.: Nonmonotonic temperature dependence of the flexibility of bacteriophage fd. Biopolymers 39, 13–22 (1996)

    Article  CAS  Google Scholar 

  74. Kramer, E.M., Herzfeld, J.: Distribution functions for reversibly self-assembling spherocylinders. Phys. Rev. E 58, 5934 (1998)

    Article  CAS  Google Scholar 

  75. Asakura, S., Oosawa, F.: On Interaction between two bodies immersed in a solution of macromolecules. J. Chem. Phys. 22, 1255–1256 (1954)

    Article  CAS  Google Scholar 

  76. Biben, T., Bladon, P., Frenkel, D.: Depletion effects in binary hard-sphere fluids. J. Phys. 8, 10799–10821 (1996)

    CAS  Google Scholar 

  77. Bechinger, C., Rudhardt, D., Leiderer, P., Roth, R., Dietrich, S.: Understanding depletion forces beyond entropy. Phys. Rev. Lett. 83, 3960–3963 (1999)

    Article  CAS  Google Scholar 

  78. Bhattacharjee, S., Glucksman, M.J., Makowski, L.: Structural polymorphism correlated to surface charge in filamentous bacteriophages. Biophys. J. 61, 725–735 (1992)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Xu, Q., et al.: Construction of bio-piezoelectric platforms: from structures and synthesis to applications. Adv. Mater. 33, 2008452 (2021)

    Article  CAS  Google Scholar 

  80. Chung, W.J., et al.: Biomimetic self-templating supramolecular structures. Nature 478, 364–368 (2011)

    Article  CAS  PubMed  Google Scholar 

  81. Neville, A.C.: Biology of fibrous composites: development beyond the cell membrane. Cambridge University Press, Cambridge (1993)

    Book  Google Scholar 

  82. Place, E.S., Evans, N.D., Stevens, M.M.: Complexity in biomaterials for tissue engineering. Nat. Mater. 8, 457–470 (2009)

    Article  CAS  PubMed  Google Scholar 

  83. Wu, L., et al.: Electrospinning fabrication, structural and mechanical characterization of rod-like virus-based composite nanofibers. J. Mater. Chem. 21, 8550–8557 (2011)

    Article  CAS  Google Scholar 

  84. Yoo, S.Y., Kobayashi, M., Lee, P.P., Lee, S.W.: Early osteogenic differentiation of mouse preosteoblasts induced by collagen-derived DGEA-peptide on nanofibrous phage tissue matrices. Biomacromol. 12, 987–996 (2011)

    Article  CAS  Google Scholar 

  85. Oh, J.-W., et al.: Biomimetic virus-based colourimetric sensors. Nat. Commun. 5, 3043 (2014)

    Article  PubMed  CAS  Google Scholar 

  86. Lee, J.H., et al.: Phage-based structural color sensors and their pattern recognition sensing system. ACS Nano 11, 3632–3641 (2017)

    Article  CAS  PubMed  Google Scholar 

  87. Thomson, P.G., et al.: Acoustic telemetry around Western Australia’s oil and gas infrastructure helps detect the presence of an elusive and endangered migratory giant. Front. Mar. Sci. 8, 1–9 (2021)

    Article  Google Scholar 

  88. Moon, J.-S., et al.: Bioinspired M-13 bacteriophage-based photonic nose for differential cell recognition. Chem. Sci. 8, 921–927 (2017)

    Article  CAS  PubMed  Google Scholar 

  89. Seol, D., Jang, D., Cha, K., Oh, J.-W., Chung, H.: Use of multiple bacteriophage-based structural color sensors to improve accuracy for discrimination of geographical origins of agricultural products. Sensors 21, 986 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Lee, J.-M., et al.: Investigation of colorimetric biosensor array based on programable surface chemistry of M13 bacteriophage towards artificial nose for volatile organic compound detection: From basic properties of the biosensor to practical application. Biosens. Bioelectron. 188, 113339 (2021)

    Article  CAS  PubMed  Google Scholar 

  91. Yoo, Y.J., et al.: Large-area virus coated ultrathin colorimetric sensors with a highly lossy resonant promoter for enhanced chromaticity. Adv. Sci. 7, 2000978 (2020)

    Article  CAS  Google Scholar 

  92. Moon, J.-S., et al.: M-13 bacteriophage based structural color sensor for detecting antibiotics. Sens. Actuat. B 240, 757–762 (2017)

    Article  CAS  Google Scholar 

  93. Lee, J.-M., et al.: A DNA-derived phage nose using machine learning and artificial neural processing for diagnosing lung cancer. Biosens. Bioelectron. 194, 113567 (2021)

    Article  CAS  PubMed  Google Scholar 

  94. Lee, J.-M., et al.: Neural mechanism mimetic selective electronic nose based on programmed M13 bacteriophage. Biosens. Bioelectron. 196, 113693 (2022)

    Article  CAS  PubMed  Google Scholar 

  95. Siavashpouri, M., Sharma, P., Fung, J., Hagan, M.F., Dogic, Z.: Structure, dynamics and phase behavior of short rod inclusions dissolved in a colloidal membrane. Soft Matter 15, 7033–7042 (2019)

    Article  CAS  PubMed  Google Scholar 

  96. Yang, Y., Barry, E., Dogic, Z., Hagan, M.F.: Self-assembly of 2D membranes from mixtures of hard rods and depleting polymers. Soft Matter 8, 707–714 (2012)

    Article  CAS  PubMed  Google Scholar 

  97. Israelachvili, J.: Intermolecular and surface forces revised, 3rd edn. Academic Press, New York (2011)

    Google Scholar 

  98. Barry, E. & Dogic, Z. Entropy driven self-assembly of nonamphiphilic colloidal membranes. (National Acad Sciences, 2010).

  99. Dogic, Z.: Filamentous phages as a model system in soft matter physics. Front. Microbiol. 7, 1013 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  100. Dogic, Z., Fraden, S.: Phase behavior of rod-like viruses and virus-sphere mixtures. Soft Matter 2, 1–86 (2007)

    Google Scholar 

  101. Lee, J.H., et al.: Production of tunable nanomaterials using hierarchically assembled bacteriophages. Nat. Protoc. 12, 1999–2013 (2017)

    Article  CAS  PubMed  Google Scholar 

  102. Kehoe, J.W., Kay, B.K.: Filamentous phage display in the new millennium. Chem. Rev. 105, 4056–4072 (2005)

    Article  CAS  PubMed  Google Scholar 

  103. Krag, D.N., et al.: Selection of tumor-binding ligands in cancer patients with phage display libraries. Can. Res. 66, 7724–7733 (2006)

    Article  CAS  Google Scholar 

  104. Di Lullo, G.A., Sweeney, S.M., Körkkö, J., Ala-Kokko, L., San Antonio, J.D.: Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, Type I collagen. J. Biol. Chem. 277, 4223–4231 (2002)

    Article  PubMed  CAS  Google Scholar 

  105. Jacob, J., More, N., Kalia, K., Kapusetti, G.: Piezoelectric smart biomaterials for bone and cartilage tissue engineering. Inflamm. Regener. 38, 2 (2018)

    Article  CAS  Google Scholar 

  106. Miara, B., Rohan, E., Zidi, M., Labat, B.: Piezomaterials for bone regeneration design—homogenization approach. J. Mech. Phys. Solids 53, 2529–2556 (2005)

    Article  CAS  Google Scholar 

  107. Lee, J.H., et al.: Vertical self-assembly of polarized phage nanostructure for energy harvesting. Nano Lett. 19, 2661–2667 (2019)

    Article  CAS  PubMed  Google Scholar 

  108. Nam, K.T., Reelle, B.R., Lee, S.W., Belcher, A.M.: Genetically driven assembly of nanorings based on the M13 virus. Nano Lett. 4, 23–27 (2004)

    Article  CAS  Google Scholar 

  109. Lee, S.W., Mao, C., Flynn, C.E., Belcher, A.M.: Ordering of quantum dots, using genetically engineered viruses. Science 296, 892–895 (2002)

    Article  CAS  PubMed  Google Scholar 

  110. Flynn, C.E., et al.: Synthesis and organization of nanoscale II-VI semiconductor materials using evolved peptide specificity and viral capsid assembly. J. Mater. Chem. 13, 2414–2421 (2003)

    Article  CAS  Google Scholar 

  111. Huang, Y., et al.: Programmable assembly of nanoarchitectures using genetically engineered viruses. Nano Lett. 5, 1429–1434 (2005)

    Article  CAS  PubMed  Google Scholar 

  112. Whaley, S.R., English, D.S., Hu, E.L., Barbara, P.F., Belcher, A.M.: Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly. Nature 405, 665–668 (2000)

    Article  CAS  PubMed  Google Scholar 

  113. Reiss, B.D., et al.: Biological routes to metal alloy ferromagnetic nanostructures. Nano Lett. 4, 1127–1132 (2004)

    Article  CAS  Google Scholar 

  114. Lee, S.K., Yun, D.S., Belcher, A.M.: Cobalt ion mediated self-assembly of genetically engineered bacteriophage for biomimetic Co - Pt hybrid material. Biomacromol. 7, 14–17 (2006)

    Article  CAS  Google Scholar 

  115. Oh, D., et al.: Graphene sheets stabilized on genetically engineered M13 viral templates as conducting frameworks for hybrid energy-storage materials. Small 8, 1006–1011 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Wang, E.E. UC Berkeley (2012).

  117. Borg, S., Rothenstein, D., Bill, J., Schüler, D.: Generation of multishell magnetic hybrid nanoparticles by encapsulation of genetically engineered and fluorescent bacterial magnetosomes with ZnO and SiO2. Small 11, 4209–4217 (2015)

    Article  CAS  PubMed  Google Scholar 

  118. Naik, R.R., Brott, L.L., Clarson, S.J., Stone, M.O.: Silica-precipitating peptides isolated from a combinatorial phage display peptide library. J. Nanosci. Nanotechnol. 2, 95–100 (2002)

    Article  CAS  PubMed  Google Scholar 

  119. Liu, Y., Mao, J., Zhou, B., Wei, W., Gong, S.: Peptide aptamers against titanium-based implants identified through phage display. J. Mater. Sci. Mater. Med. 21, 1103–1107 (2010)

    Article  CAS  PubMed  Google Scholar 

  120. Clauder, F., et al.: Endothelialization of titanium surfaces by bioinspired cell adhesion peptide coatings. Bioconjug. Chem. 30, 2664–2674 (2019)

    Article  CAS  PubMed  Google Scholar 

  121. Vreuls, C., et al.: Inorganic-binding peptides as tools for surface quality control. J. Inorg. Biochem. 104, 1013–1021 (2010)

    Article  CAS  PubMed  Google Scholar 

  122. Lower, B.H., et al.: In vitro evolution of a peptide with a hematite binding motif that may constitute a natural metal-oxide binding archetype. Environ. Sci. Technol. 42, 3821–3827 (2008)

    Article  CAS  PubMed  Google Scholar 

  123. Zuo, R., Ornek, D., Wood, T.K.: Aluminum- and mild steel-binding peptides from phage display. Appl. Microbiol. Biotechnol. 68, 505–509 (2005)

    Article  CAS  PubMed  Google Scholar 

  124. Naik, R.R., et al.: Peptide templates for nanoparticle synthesis derived from polymerase chain reaction-driven phage display. Adv. Func. Mater. 14, 25–30 (2004)

    Article  CAS  Google Scholar 

  125. Roy, M.D., Stanley, S.K., Amis, E.J., Becker, M.L.: Identification of a highly specific hydroxyapatite-binding peptide using phage display. Adv. Mater. 20, 1830–1836 (2008)

    Article  CAS  Google Scholar 

  126. Romanov, V.I., Durand, D.B., Petrenko, V.A.: Phage display selection of peptides that affect prostate carcinoma cells attachment and invasion. Prostate 47, 239–251 (2001)

    Article  CAS  PubMed  Google Scholar 

  127. Zhang, L., et al.: In vitro screening of ovarian tumor specific peptides from a phage display peptide library. Biotech. Lett. 33, 1729–1735 (2011)

    Article  CAS  Google Scholar 

  128. Bolhuis, P., Frenkel, D.: Tracing the phase boundaries of hard spherocylinders. J. Chem. Phys. 106, 666–687 (1997)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Research Foundation of Korea (NRF), funded by the Ministry of Science and ICT (Grant Number 2020R1C1C1012122). This work was also supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Science and ICT (Grant Number 2020R1A4A1016840).

Author information

Author notes

  1. Sang Min Han, Yu Jin Lee, Mun Hwan Lee, and Cheong Woo Park have contributed equally to this work.

Authors and Affiliations

  1. Department of Bionano Engineering, Center for Bionano Intelligence Education and Research, Hanyang University, 55 Hanyangdaehak-ro, Sangnok-gu, Ansan, 15588, Republic of Korea

    Sang Min Han, Yu Jin Lee, Mun Hwan Lee, Cheong Woo Park, Sang Min Lee, Jeong Ook Soh & Ju Hun Lee

Authors
  1. Sang Min Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu Jin Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mun Hwan Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cheong Woo Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sang Min Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jeong Ook Soh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ju Hun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ju Hun Lee.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, S.M., Lee, Y.J., Lee, M.H. et al. M13 Bacteriophage-Based Bio-nano Systems for Bioapplication. BioChip J 16, 227–245 (2022). https://doi.org/10.1007/s13206-022-00069-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13206-022-00069-w

Keywords

Search

Navigation