Journal Home > Volume 10 , Issue 10

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.


menu
Abstract
Full text
Outline
Electronic supplementary material
About this article

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

Show Author's information Wenjing Zhang1,2Zhi-Ping Zhang1Xian-En Zhang3( )Feng Li1( )
State Key Laboratory of VirologyWuhan Institute of VirologyChinese Academy of SciencesWuhan430071China
University of Chinese Academy of SciencesBeijing100049China
National Laboratory of BiomacromoleculesCAS Center for Excellence in BiomacromoleculesInstitute of BiophysicsChinese Academy of SciencesBeijing100101China

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

References(49)

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.

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.

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.

4

Jutz, G.; van Rijn, P.; Miranda, B. S.; Boker, A. Ferritin: A versatile building block for bionanotechnology. Chem. Rev. 2015, 115, 1653–1701.

5

Li, F.; Wang, Q. B. Fabrication of nanoarchitectures templated by virus-based nanoparticles: Strategies and applications. Small 2014, 10, 230–245.

6

Dickerson, M. B.; Sandhage, K. H.; Naik, R. R. Proteinand peptide-directed syntheses of inorganic materials. Chem. Rev. 2008, 108, 4935–4978.

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.

8

Douglas, T.; Young, M. Host–guest encapsulation of materials by assembled virus protein cages. Nature 1998, 393, 152–155.

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.

10

Chen, W.; Wang, G. C.; Tang, R. K. Nanomodification of living organisms by biomimetic mineralization. Nano Res. 2014, 7, 1404–1428.

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.

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.

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.

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.

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.

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.

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.

18

Molino, N. M.; Wang, S. -W. Caged protein nanoparticles for drug delivery. Curr. Opin. Biotechnol. 2014, 28, 75–82.

19

Klem, M. T.; Young, M.; Douglas, T. Biomimetic synthesis of β-TiO2 inside a viral capsid. J. Mater. Chem. 2008, 18, 3821–3823.

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.

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.

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.

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.

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.

DOI
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.

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.

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.

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.

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.

30

Taton, T. A.; Mirkin, C. A.; Letsinger, R. L. Scanometric DNA array detection with nanoparticle probes. Science 2000, 289, 1757–1760.

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.

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.

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.

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.

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.

36

Khlebtsov, B.; Khanadeev, V.; Khlebtsov, N. Surfaceenhanced Raman scattering inside Au@Ag core/shell nanorods. Nano Res. 2016, 9, 2303–2318.

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.

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.

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.

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.

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.

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.

43

Nair, L. S.; Laurencin, C. T. Silver nanoparticles: Synthesis and therapeutic applications. J. Biomed. Nanotechnol. 2007, 3, 301–316.

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.

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.

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.

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.

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.https://doi.org/10.1016/B978-0-12-333927-0.50007-6
DOI
49

Graf, C.; van Blaaderen, A. Metallodielectric colloidal core–shell particles for photonic applications. Langmuir 2002, 18, 524–534.

File
nr-10-10-3285_ESM.pdf (2.2 MB)
Publication history
Copyright
Acknowledgements

Publication history

Received: 17 November 2016
Revised: 14 February 2017
Accepted: 15 February 2017
Published: 23 May 2017
Issue date: October 2017

Copyright

© Tsinghua University Press and Springer-Verlag Berlin Heidelberg 2017

Acknowledgements

Acknowledgements

We greatly appreciate the financial support from the the National Natural Science Foundation of China (Nos. 31271076, 31470931 and 91527302) and the Key Research Program of the Chinese Academy of Sciences (No. KGZD-EW-T02-3). We are grateful to Dr. D. Gao, B. C. Xu, P. Zhang and A. N. Du at the Center for Instrumental Analysis and Metrology, Wuhan Institute of Virology, CAS for assistance with TEM imaging and Dr. Kun Zhou at Suzhou Institute of Nano-Tech and Nano-Bionics, CAS for help with EDS analysis.

Return