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Encapsulation of Negatively Charged Cargo in MS2 Viral Capsids

  • Ioana L. Aanei
  • Jeff E. Glasgow
  • Stacy L. Capehart
  • Matthew B. FrancisEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1776)

Abstract

Encapsulation into virus-like particles is an efficient way of loading cargo of interest for delivery applications. Here, we describe the encapsulation of proteins with tags comprising anionic amino acids or DNA and gold nanoparticles with negative surface charges inside MS2 bacteriophage capsids to obtain homogeneous nanoparticles with a diameter of 27 nm.

Key words

MS2 bacteriophage Encapsulation Virus-like particles Delivery vehicles Nanoparticles Self-assembly 

Notes

Acknowledgments

This work was generously supported by the Office of Science, Materials Sciences and Engineering Division, of the US Department of Energy under Contract No. DEAC02-05CH11231. SLC was supported by an NSF graduate research fellowship (NSF GRFP). JEG was supported by the Hellman Family Faculty Fund and the UC Berkeley Chemical Biology Graduate Program (NIH Training Grant 1 T32 GMO66698).

References

  1. 1.
    Maeda H, Wu J, Sawa T, Matsumura Y, Hori K (2000) Vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release 65:271–284CrossRefPubMedGoogle Scholar
  2. 2.
    Wang Q, Lin T, Tang L, Johnson JE, Finn MG (2002) Icosahedral virus particles as addressable nanoscale building blocks. Angew Chem Int Ed 41:459–462CrossRefGoogle Scholar
  3. 3.
    Hooker JM, Kovacs EW, Francis MB (2004) Interior surface modification of bacteriophage MS2. J Am Chem Soc 126:3718–3719CrossRefPubMedGoogle Scholar
  4. 4.
    Datta A, Hooker JM, Botta M, Francis MB, Aime S, Raymond KN (2008) High relaxivity gadolinium hydroxypyridonate-viral capsid conjugates: nanosized MRI contrast agents. J Am Chem Soc 130:2546–2552CrossRefPubMedGoogle Scholar
  5. 5.
    Garimella PD, Datta A, Romanini DW, Raymond KN, Francis MB (2011) Multivalent, high-relaxivity MRI contrast agents using rigid cysteine-reactive gadolinium complexes. J Am Chem Soc 133:14704–14709CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Farkas ME, Aanei IL, Behrens CR, Tong GJ, Murphy ST, O’Neil JP, Francis MB (2013) PET imaging and biodistribution of chemically modified bacteriophage MS2. Mol Pharm 10:69–76CrossRefPubMedGoogle Scholar
  7. 7.
    Wu W, Hsiao SC, Carrico ZM, Francis MB (2009) Genome-free viral capsids as multivalent carriers for taxol delivery. Angew Chem Int Ed 48:9493–9497CrossRefGoogle Scholar
  8. 8.
    Stephanopoulos N, Tong GJ, Hsiao SC, Francis MB (2010) Dual-surface modified virus capsids for targeted delivery of photodynamic agents to cancer cells. ACS Nano 4:6014–6020CrossRefPubMedGoogle Scholar
  9. 9.
    Li F, Wang Q (2014) Fabrication of nanoarchitectures templated by virus-based nanoparticles: strategies and applications. Small 10:230–245CrossRefPubMedGoogle Scholar
  10. 10.
    Minten IJ, Claessen VI, Blank K, Rowan AE, Nolte RJM, Cornelissen JJLM (2011) Catalytic capsids: the art of confinement. Chem Sci 2:358–362CrossRefGoogle Scholar
  11. 11.
    Fiedler JD, Brown SD, Lau JL, Finn MG (2010) RNA-directed packaging of enzymes within virus-like particles. Angew Chem Int Ed 49:9648–9651CrossRefGoogle Scholar
  12. 12.
    O’Neil A, Reichhardt C, Johnson B, Prevelige PE, Douglas T (2011) Genetically programmed in vivo packaging of protein cargo and its controlled release from bacteriophage P22. Angew Chem Int Ed 50:7425–7428CrossRefGoogle Scholar
  13. 13.
    Patterson DP, Prevelige PE, Douglas T (2012) Nanoreactors by programmed enzyme encapsulation inside the capsid of the bacteriophage P22. ACS Nano 6:5000–5009CrossRefPubMedGoogle Scholar
  14. 14.
    Patterson DP, Schwarz B, El-Boubbou K, van der Oost J, Prevelige PE, Douglas T (2012) Virus-like particle nanoreactors: programmed encapsulation of the thermostable CelB glycosidase inside the P22 capsid. Soft Matter 8:10158–10166CrossRefGoogle Scholar
  15. 15.
    Wu M, Brown W, Stockley P (1995) Cell-specific delivery of bacteriophage-encapsidated Ricin A chain. Bioconjug Chem 6:587–595CrossRefPubMedGoogle Scholar
  16. 16.
    Ashley CE, Carnes EC, Phillips GK, Durfee PN, Buley MD, Lino CA, Padilla DP, Phillips B, Carter MB, Willman CL, Brinker CJ, Caldeira Jdo C, Chackerian B, Wharton W, Peabody DS (2011) Cell-specific delivery of diverse cargos by bacteriophage MS2 virus-like particles. ACS Nano 5:5729–5745CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Loo L, Guenther RH, Lommel SA, Franzen S (2007) Encapsidation of nanoparticles by red clover necrotic mosaic virus. J Am Chem Soc 129:11111–11117CrossRefPubMedGoogle Scholar
  18. 18.
    Dragnea B, Chen C, Kwak ES, Stein B, Kao CC (2003) Gold nanoparticles as spectroscopic enhancers for in vitro studies on single viruses. J Am Chem Soc 125:6374–6377CrossRefPubMedGoogle Scholar
  19. 19.
    Chen C, Kwak ES, Stein B, Kao CC, Dragnea B (2005) Packaging of gold particles in viral capsids. J Nanosci Nanotechnol 5:2029–2033CrossRefPubMedGoogle Scholar
  20. 20.
    Loo L, Guenther RH, Basnayake VR, Lommel SA, Franzen S (2006) Controlled encapsidation of gold nanoparticles by a viral protein shell. J Am Chem Soc 128:4502–4503CrossRefPubMedGoogle Scholar
  21. 21.
    Chen C, Daniel MC, Quinkert ZT, De M, Stein B, Bowman VD, Chipman PR, Rotello VM, Kao CC, Dragnea B (2006) Nanoparticle-templated assembly of viral protein cages. Nano Lett 6:611–615CrossRefPubMedGoogle Scholar
  22. 22.
    Aniagyei SE, Kennedy CJ, Stein B, Willits DA, Douglas T, Young MJ, De M, Rotello VM, Srisathiyanarayanan D, Kao CC, Dragnea B (2009) Synergistic effects of mutations and nanoparticle templating in the self-assembly of cowpea chlorotic mottle virus capsids. Nano Lett 9:393–398CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Daniel MC, Tsvetkova IB, Quinkert ZT, Murali A, De M, Rotello VM, Kao CC, Dragnea B (2010) Role of surface charge density in nanoparticle-templated assembly of bromovirus protein cages. ACS Nano 4:3853–3860CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Young M, Debbie W, Uchida M, Douglas T (2008) Plant viruses as biotemplates for materials and their use in nanotechnology. Annu Rev Phytopathol 46:361–384CrossRefPubMedGoogle Scholar
  25. 25.
    Glasgow JE (2014) Encapsulation of biomolecules in bacteriophage MS2 viral capsids. Dissertation, University of California, BerkeleyGoogle Scholar
  26. 26.
    Capehart S L (2014) New synthetic methods for integrating metal nanoparticles with biomolecules. Dissertation, University of California, BerkeleyGoogle Scholar
  27. 27.
    Glasgow JE, Capehart SL, Francis MB, Tullman-Ercek D (2012) Osmolyte-mediated encapsulation of proteins inside MS2 viral capsid. ACS Nano 6:8658–8664CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Glasgow JE, Asensio MA, Jakobson CM, Francis MB, Tullman-Ercek D (2015) The influence of electrostatics on small molecule flux through a protein nanoreactor. ACS Synth Biol 4:1011–1019CrossRefPubMedGoogle Scholar
  29. 29.
    Capehart SL, Coyle MP, Glasgow JE, Francis MB (2013) Controlled integration of gold nanoparticles and organic fluorophores using synthetically modified MS2 viral capsids. J Am Chem Soc 135:3011–3016CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Hooker JM, Esser-Kahn AP, Francis MB (2006) Modification of aniline containing proteins using an oxidative coupling strategy. J Am Chem Soc 128:15558–15559CrossRefPubMedGoogle Scholar
  31. 31.
    Carrico ZM, Romanini DW, Mehl RA, Francis MB (2008) Oxidative coupling of peptides to a virus capsid containing unnatural amino acids. Chem Commun 10:1205–1207.  https://doi.org/10.1039/b717826cCrossRefGoogle Scholar
  32. 32.
    Mehl RA, Anderson JC, Santoro SW, Wan L, Martin AB, King DS, Horn DM, Schultz PG (2003) Generation of a bacterium with a 21 amino acid genetic code. J Am Chem Soc 125:935–939CrossRefPubMedGoogle Scholar
  33. 33.
    Loweth CJ, Caldwell WB, Peng X, Alivisatos AP, Schultz PG (1999) DNA-based assembly of gold nanocrystals. Angew Chem Int Ed 38:1808–1812CrossRefGoogle Scholar
  34. 34.
    Hurst SJ, Lytton-Jean AKR, Mirkin CA (2006) Maximizing DNA loading on a range of gold nanoparticle sizes. Anal Chem 78:8313–8318CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Street TO, Bolen DW, Rose GD (2006) A molecular mechanism for osmolyte-induced protein stability. Proc Nat Acad Sci USA 103:13997–14002CrossRefPubMedGoogle Scholar
  36. 36.
    Zhang Y, Cremer PS (2010) Chemistry of Hofmeister anions and osmolytes. Ann Rev Phys Chem 61:63–83CrossRefGoogle Scholar
  37. 37.
    Zacharias DA, Violin JD, Newton AC, Tsien RY (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296:913–916CrossRefPubMedGoogle Scholar
  38. 38.
    ElSawy K, Caves L, Twarock R (2010) The impact of viral RNA on the association rates of capsid protein assembly: bacteriophage MS2 as a case study. J Mol Biol 400:935–947CrossRefPubMedGoogle Scholar
  39. 39.
    Rolfsson O, Toropova K, Ranson NA, Stockley PG (2010) Mutually-induced conformational switching of RNA and coat protein underpins efficient assembly of a viral capsid. J Mol Biol 401:309–322CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
  41. 41.
    Claridge SA, Goh SL, Fréchet JMJ, Williams SC, Micheel CM, Alivisatos AP (2005) Directed assembly of discrete gold nanoparticle groupings using branched DNA scaffolds. Chem Mater 17:1628–1635CrossRefGoogle Scholar
  42. 42.
    Claridge SA, Liang HW, Basu SR, Fréchet JMJ, Alivisatos AP (2008) Isolation of discrete nanoparticle-DNA conjugates for plasmonic applications. Nano Lett 8:1202–1206CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Ioana L. Aanei
    • 1
    • 2
  • Jeff E. Glasgow
    • 1
  • Stacy L. Capehart
    • 1
  • Matthew B. Francis
    • 1
    • 2
    Email author
  1. 1.Department of ChemistryUniversity of CaliforniaBerkeleyUSA
  2. 2.Materials Sciences DivisionLawrence Berkeley National LaboratoriesBerkeleyUSA

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