Nano Research

pp 1–10

Reaction inside a viral protein nanocage: Mineralization on a nanoparticle seed after encapsulation via self-assembly

Research Article

Abstract

Protein nanocages are ideal templates for the bio-inspired fabrication of nanomaterials due to several advantageous properties. During the mineralization of nanoparticles (NPs) inside protein nanocages, most studies have employed a common strategy: seed formation inside protein nanocages followed by seeded NP growth. However, the seed formation step is restricted to gentle reaction conditions to avoid damage to the protein nanocages, which may greatly limit the spectrum of seed materials used for NP growth. We put forward a simple route to circumvent such a limitation: encapsulation of a preformed NP as the seed via self-assembly, followed by the growth of an outer metal layer. Using such a method, we succeeded in mineralizing size-tunable Au NPs and Au@Ag core–shell NPs (<10 nm in diameter) with narrow size distributions inside the virus-based NPs of simian virus 40. The present route enables the utilization of NPs synthesized under any conditions as the starting seeds for nanomaterial growth inside protein nanocages. Therefore, it potentially leads to novel bioinorganic chimeric nanomaterials with tailorable components and structures.

Keywords

protein nanocages mineralization gold nanoparticles gold–silver core–shell nanoparticles self-assembly 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

12274_2017_1541_MOESM1_ESM.pdf (2.2 mb)
Reaction inside a viral protein nanocage: Mineralization on a nanoparticle seed after encapsulation via self-assembly

References

  1. [1]
    Huang, J. L.; Lin, L. Q.; Sun, D. H.; Chen, H. M.; Yang, D. P.; Li, Q. B. Bio-inspired synthesis of metal nanomaterials and applications. Chem. Soc. Rev. 2015, 44, 6330–6374.CrossRefGoogle Scholar
  2. [2]
    Zhou, K.; Eiben, S.; Wang, Q. B. Coassembly of tobacco mosaic virus coat proteins into nanotubes with uniform length and improved physical stability. ACS Appl. Mater. Interfaces 2016, 8, 13192–13196.CrossRefGoogle Scholar
  3. [3]
    Luo, Q.; Hou, C. X.; Bai, Y. S.; Wang, R. B.; Liu, J. Q. Protein assembly: Versatile approaches to construct highly ordered nanostructures. Chem. Rev. 2016, 116, 13571–13632.CrossRefGoogle Scholar
  4. [4]
    Jutz, G.; van Rijn, P.; Miranda, B. S.; Boker, A. Ferritin: A versatile building block for bionanotechnology. Chem. Rev. 2015, 115, 1653–1701.CrossRefGoogle Scholar
  5. [5]
    Li, F.; Wang, Q. B. Fabrication of nanoarchitectures templated by virus-based nanoparticles: Strategies and applications. Small 2014, 10, 230–245.CrossRefGoogle Scholar
  6. [6]
    Dickerson, M. B.; Sandhage, K. H.; Naik, R. R. Proteinand peptide-directed syntheses of inorganic materials. Chem. Rev. 2008, 108, 4935–4978.CrossRefGoogle Scholar
  7. [7]
    Yang, D. P.; Chen, S. H.; Huang, P.; Wang, X. S.; Jiang, W. Q.; Pandoli, O.; Cui, D. X. Bacteria-template synthesized silver microspheres with hollow and porous structures as excellent SERS substrate. Green Chem. 2010, 12, 2038–2042.CrossRefGoogle Scholar
  8. [8]
    Douglas, T.; Young, M. Host–guest encapsulation of materials by assembled virus protein cages. Nature 1998, 393, 152–155.CrossRefGoogle Scholar
  9. [9]
    Zhou, K.; Zhang, J. T.; Wang, Q. B. Site-selective nucleation and controlled growth of gold nanostructures in tobacco mosaic virus nanotubulars. Small 2015, 11, 2505–2509.CrossRefGoogle Scholar
  10. [10]
    Chen, W.; Wang, G. C.; Tang, R. K. Nanomodification of living organisms by biomimetic mineralization. Nano Res. 2014, 7, 1404–1428.CrossRefGoogle Scholar
  11. [11]
    Ghosh, D.; Lee, Y.; Thomas, S.; Kohli, A. G.; Yun, D. S.; Belcher, A. M.; Kelly, K. A. M13-templated magnetic nanoparticles for targeted in vivo imaging of prostate cancer. Nat. Nanotechnol. 2012, 7, 677–682.CrossRefGoogle Scholar
  12. [12]
    Górzny, M. Ł.; Walton, A. S.; Evans, S. D. Synthesis of high-surface-area platinum nanotubes using a viral template. Adv. Funct. Mater. 2010, 20, 1295–1300.CrossRefGoogle Scholar
  13. [13]
    Yang, C. X.; Manocchi, A. K.; Lee, B.; Yi, H. M. Viraltemplated palladium nanocatalysts for Suzuki coupling reaction. J. Mater. Chem. 2011, 21, 187–194.CrossRefGoogle Scholar
  14. [14]
    Lee, L. A.; Niu, Z. W.; Wang, Q. Viruses and virus-like protein assemblies-chemically programmable nanoscale building blocks. Nano Res. 2009, 2, 349–364.CrossRefGoogle Scholar
  15. [15]
    Dang, X. N.; Yi, H. J.; Ham, M. H.; Qi, J. F.; Yun, D. S.; Ladewski, R.; Strano, M. S.; Hammond, P. T.; Belcher, A. M. Virus-templated self-assembled single-walled carbon nanotubes for highly efficient electron collection in photovoltaic devices. Nat. Nanotechnol. 2011, 6, 377–384.CrossRefGoogle Scholar
  16. [16]
    Liu, Y. H.; Xu, Y. H.; Zhu, Y. J.; Culver, J. N.; Lundgren, C. A.; Xu, K.; Wang, C. S. Tin-coated viral nanoforests as sodium-ion battery anodes. ACS Nano 2013, 7, 3627–3634.CrossRefGoogle Scholar
  17. [17]
    Wang, Z. T.; Huang, P.; Jacobson, O.; Wang, Z.; Liu, Y. J.; Lin, L. S.; Lin, J.; Lu, N.; Zhang, H. M.; Tian, R. et al. Biomineralization-inspired synthesis of copper sulfide-ferritin nanocages as cancer theranostics. ACS Nano 2016, 10, 3453–3460.CrossRefGoogle Scholar
  18. [18]
    Molino, N. M.; Wang, S.-W. Caged protein nanoparticles for drug delivery. Curr. Opin. Biotechnol. 2014, 28, 75–82.CrossRefGoogle Scholar
  19. [19]
    Klem, M. T.; Young, M.; Douglas, T. Biomimetic synthesis of β-TiO2 inside a viral capsid. J. Mater. Chem. 2008, 18, 3821–3823.CrossRefGoogle Scholar
  20. [20]
    Reichhardt, C.; Uchida, M.; O'Neil, A.; Li, R.; Prevelige, P. E.; Douglas, T. Templated assembly of organic-inorganic materials using the core shell structure of the P22 bacteriophage. Chem. Commun. 2011, 47, 6326–6328.CrossRefGoogle Scholar
  21. [21]
    Okuda, M.; Suzumoto, Y.; Iwahori, K.; Kang, S.; Uchida, M.; Douglas, T.; Yamashita, I. Bio-templated CdSe nanoparticle synthesis in a cage shaped protein, Listeria-Dps, and their two dimensional ordered array self-assembly. Chem. Commun. 2010, 46, 8797–8799.CrossRefGoogle Scholar
  22. [22]
    Kasyutich, O.; Ilari, A.; Fiorillo, A.; Tatchev, D.; Hoell, A.; Ceci, P. Silver ion incorporation and nanoparticle formation inside the cavity of Pyrococcus furiosus ferritin: Structural and size-distribution analyses. J. Am. Chem. Soc. 2010, 132, 3621–3627.CrossRefGoogle Scholar
  23. [23]
    Zhou, Z. Y.; Bedwell, G. J.; Li, R.; Prevelige, P. E.; Gupta, A. Formation mechanism of chalcogenide nanocrystals confined inside genetically engineered virus-like particles. Sci. Rep. 2014, 4, 3832.CrossRefGoogle Scholar
  24. [24]
    Douglas, T.; Strable, E.; Willits, D.; Aitouchen, A.; Libera, M.; Young, M. Protein engineering of a viral cage for constrained nanomaterials synthesis. Adv. Mater. 2002, 14, 415–418.CrossRefGoogle Scholar
  25. [25]
    Fan, R. L.; Chew, S. W.; Cheong, V. V.; Orner, B. P. Fabrication of gold nanoparticles inside unmodified horse spleen apoferritin. Small 2010, 6, 1483–1487.CrossRefGoogle Scholar
  26. [26]
    Li, T.; Chattopadhyay, S.; Shibata, T.; Cook, R. E.; Miller, J. T.; Suthiwangcharoen, N.; Lee, S.; Winans, R. E.; Lee, B. Synthesis and characterization of Au-core Ag-shell nanoparticles from unmodified apoferritin. J. Mater. Chem. 2012, 22, 14458–14464.CrossRefGoogle Scholar
  27. [27]
    Li, F.; Gao, D.; Zhai, X. M.; Chen, Y. H.; Fu, T.; Wu, D. M.; Zhang, Z. P.; Zhang, X. E.; Wang, Q. B. Tunable, discrete, three-dimensional hybrid nanoarchitectures. Angew. Chem., Int. Ed. 2011, 50, 4202–4205.CrossRefGoogle Scholar
  28. [28]
    Li, F.; Chen, H. L.; Zhang, Y. J.; Chen, Z.; Zhang, Z. P.; Zhang, X. E.; Wang, Q. B. Three-dimensional gold nanoparticle clusters with tunable cores templated by a viral protein scaffold. Small 2012, 8, 3832–3838.CrossRefGoogle Scholar
  29. [29]
    Li, F.; Chen, Y. H.; Chen, H. L.; He, W.; Zhang, Z. P.; Zhang, X. E.; Wang, Q. B. Monofunctionalization of protein nanocages. J. Am. Chem. Soc. 2011, 133, 20040–20043.CrossRefGoogle Scholar
  30. [30]
    Taton, T. A.; Mirkin, C. A.; Letsinger, R. L. Scanometric DNA array detection with nanoparticle probes. Science 2000, 289, 1757–1760.CrossRefGoogle Scholar
  31. [31]
    Wang, T. J.; Zhang, Z. P.; Gao, D.; Li, F.; Wei, H. P.; Liang, X. S.; Cui, Z. Q.; Zhang, X. E. Encapsulation of gold nanoparticles by simian virus 40 capsids. Nanoscale 2011, 3, 4275–4282.CrossRefGoogle Scholar
  32. [32]
    Gilroy, K. D.; Ruditskiy, A.; Peng, H. C.; Qin, D.; Xia, Y. N. Bimetallic nanocrystals: Syntheses, properties, and applications. Chem. Rev. 2016, 116, 10414–10472.CrossRefGoogle Scholar
  33. [33]
    Zeng, J. B.; Cao, Y. Y.; Chen, J. J.; Wang, X. D.; Yu, J. F.; Yu, B. B.; Yan, Z. F.; Chen, X. Au@Ag core/shell nanoparticles as colorimetric probes for cyanide sensing. Nanoscale 2014, 6, 9939–9943.CrossRefGoogle Scholar
  34. [34]
    Lee, I. H.; Lee, J. M.; Jung, Y. Controlled protein embedment onto Au/Ag core–shell nanoparticles for immunolabeling of nanosilver surface. ACS Appl. Mater. Interfaces 2014, 6, 7659–7664.CrossRefGoogle Scholar
  35. [35]
    Li, Y. J.; Shi, Q. R.; Zhang, P. N.; Xiahou, Y. J.; Li, S. Z.; Wang, D. Y.; Xia, H. B. Empirical structural design of core@shell Au@Ag nanoparticles for SERS applications. J. Mater. Chem. C 2016, 4, 6649–6656.CrossRefGoogle Scholar
  36. [36]
    Khlebtsov, B.; Khanadeev, V.; Khlebtsov, N. Surfaceenhanced Raman scattering inside Au@Ag core/shell nanorods. Nano Res. 2016, 9, 2303–2318.CrossRefGoogle Scholar
  37. [37]
    Banerjee, M.; Sharma, S.; Chattopadhyay, A.; Ghosh, S. S. Enhanced antibacterial activity of bimetallic gold–silver core–shell nanoparticles at low silver concentration. Nanoscale 2011, 3, 5120–5125.CrossRefGoogle Scholar
  38. [38]
    Haldar, K. K.; Kundu, S.; Patra, A. Core-size-dependent catalytic properties of bimetallic Au/Ag core–shell nanoparticles. ACS Appl. Mater. Interfaces 2014, 6, 21946–21953.CrossRefGoogle Scholar
  39. [39]
    Chuntonov, L.; Bar-Sadan, M.; Houben, L.; Harant, G. Correlating electron tomography and plasmon spectroscopy of single noble metal core–shell nanoparticles. Nano Lett. 2012, 12, 145–150.CrossRefGoogle Scholar
  40. [40]
    Ma, Y. Y.; Li, W. Y.; Cho, E. C.; Li, Z. Y.; Yu, T.; Zeng, J.; Xie, Z. X.; Xia, Y. N. Au@Ag core–shell nanocubes with finely tuned and well-controlled sizes, shell thicknesses, and optical properties. ACS Nano 2010, 4, 6725–6734.CrossRefGoogle Scholar
  41. [41]
    Chiang, C.; Huang, M. H. Synthesis of small Au–Ag core–shell cubes, cuboctahedra, and octahedra with size tunability and their optical and photothermal properties. Small 2015, 11, 6018–6025.CrossRefGoogle Scholar
  42. [42]
    Lu, L.; Burkey, G.; Halaciuga, I.; Goia, D. V. Core–shell gold/silver nanoparticles: Synthesis and optical properties. J. Colloid Interface Sci. 2013, 392, 90–95.CrossRefGoogle Scholar
  43. [43]
    Nair, L. S.; Laurencin, C. T. Silver nanoparticles: Synthesis and therapeutic applications. J. Biomed. Nanotechnol. 2007, 3, 301–316.CrossRefGoogle Scholar
  44. [44]
    Bykov, Y. S.; Cortese, M.; Briggs, J. A. G.; Bartenschlager, R. Correlative light and electron microscopy methods for the study of virus–cell interactions. FEBS Lett. 2016, 590, 1877–1895.CrossRefGoogle Scholar
  45. [45]
    Samal, A. K.; Polavarapu, L.; Rodal-Cedeira, S.; Liz-Marzán, L. M.; Pérez-Juste, J.; Pastoriza-Santos, I. Size tunable Au@Ag core–shell nanoparticles: Synthesis and surfaceenhanced Raman scattering properties. Langmuir 2013, 29, 15076–15082.CrossRefGoogle Scholar
  46. [46]
    Padmos, J. D.; Boudreau, R. T. M.; Weaver, D. F.; Zhang, P. Impact of protecting ligands on surface structure and antibacterial activity of silver nanoparticles. Langmuir 2015, 31, 3745–3752.CrossRefGoogle Scholar
  47. [47]
    Li, F.; Li, K.; Cui, Z. Q.; Zhang, Z. P.; Wei, H. P.; Gao, D.; Deng, J. Y.; Zhang, X. E. Viral coat proteins as flexible nano-building-blocks for nanoparticle encapsulation. Small 2010, 6, 2301–2308.CrossRefGoogle Scholar
  48. [48]
    Handley, D. A. Methods for synthesis of colloidal gold. In Colloidal Gold: Principles, Methods, and Applications; Hayat, M. A., Ed.; Academic Press: New York, 1989; Vol. 1, pp 13–32.CrossRefGoogle Scholar
  49. [49]
    Graf, C.; van Blaaderen, A. Metallodielectric colloidal core–shell particles for photonic applications. Langmuir 2002, 18, 524–534.CrossRefGoogle Scholar

Copyright information

© Tsinghua University Press and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.State Key Laboratory of Virology, Wuhan Institute of VirologyChinese Academy of SciencesWuhanChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of BiophysicsChinese Academy of SciencesBeijingChina

Personalised recommendations