Use of the interior cavity of the P22 capsid for site-specific initiation of atom-transfer radical polymerization with high-density cargo loading

Nature Chemistry

Volumn 4, Issue 10, 2012, Pages 781-788

  Lucon, Janice ^a   Qazi, Shefah ^a   Uchida, Masaki ^a   Bedwell, Gregory J ^b   Lafrance, Ben ^a   Prevelige, Peter E ^b   Douglas, Trevor ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CONTRAST MEDIUM; COORDINATION COMPOUND; FLUORESCEIN; GADOLINIUM; NANOMATERIAL; POLYMER;

ARTICLE; BACTERIOPHAGE P22; CHEMISTRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; POLYMERIZATION;

BACTERIOPHAGE P22; CAPSID PROTEINS; CONTRAST MEDIA; COORDINATION COMPLEXES; FLUORESCEIN; GADOLINIUM; MAGNETIC RESONANCE IMAGING; NANOSTRUCTURES; POLYMERIZATION; POLYMERS;

EID: 84866920418     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.1442     Document Type: Article

References (42)

1. Grover, G. N. & Maynard, H. D. Protein-polymer conjugates: synthetic approaches by controlled radical polymerizations and interesting applications. Curr. Opin. Chem. Biol. 14, 818-827 (2010).
2. Krishna, O. D. & Kiick, K. L. Protein- and peptide-modified synthetic polymeric biomaterials. Biopolymers 94, 32-48 (2010).
3. Thordarson, P., Le Droumaguet, B. & Velonia, K.Well-defined protein-polymer conjugates - synthesis and potential applications. Appl. Microbiol. Biotechnol. 73, 243-254 (2006).
4. Depp, V., Alikhani, A., Grammer, V. & Lele, B. S. Native protein-initiated ATRP: a viable and potentially superior alternative to PEGylation for stabilizing biologics. Acta Biomater. 5, 560-569 (2009).
5. Klok, H. A. Peptide/protein-synthetic polymer conjugates: quo vadis. Macromolecules 42, 7990-8000 (2009).
6. Pokorski, J. K., Breitenkamp, K., Liepold, L. O., Qazi, S. & Finn, M. G. Functional virus-based polymer-protein nanoparticles by atom transfer radical polymerization. J. Am. Chem. Soc. 133, 9242-9245 (2011).
7. Schlick, T. L., Ding, Z. B., Kovacs, E. W. & Francis, M. B. Dual-surface modification of the tobacco mosaic virus. J. Am. Chem. Soc. 127, 3718-3723 (2005).
8. de la Escosura, A., Nolte, R. J. M. & Cornelissen, J. Viruses and protein cages as nanocontainers and nanoreactors. J. Mater. Chem. 19, 2274-2278 (2009).
9. Aniagyei, S. E., DuFort, C., Kao, C. C. & Dragnea, B. Self-assembly approaches to nanomaterial encapsulation in viral protein cages. J. Mater. Chem. 18, 3763-3774 (2008).
10. Dixit, S. K. et al. Quantum dot encapsulation in viral capsids. Nano Lett. 6, 1993-1999 (2006).
11. Comellas-Aragones, M. et al. Controlled integration of polymers into viral capsids. Biomacromolecules 10, 3141-3147 (2009).
12. Douglas, T. & Young, M. Host-guest encapsulation of materials by assembled virus protein cages. Nature 393, 152-155 (1998).
13. Hu, Y. F., Zandi, R., Anavitarte, A., Knobler, C. M. & Gelbart, W. M. Packaging of a polymer by a viral capsid: the interplay between polymer length and capsid size. Biophys. J. 94, 1428-1436 (2008).
14. Abe, S. et al. Polymerization of phenylacetylene by rhodium complexes within a discrete space of apo-ferritin. J. Am. Chem. Soc. 131, 6958-6960 (2009).
15. Abedin, M. J., Liepold, L., Suci, P., Young, M. & Douglas, T. Synthesis of a cross-linked branched polymer network in the interior of a protein cage. J. Am. Chem. Soc. 131, 4346-4354 (2009).
16. Liepold, L. O. et al. Supramolecular protein cage composite MR contrast agents with extremely efficient relaxivity properties. Nano Lett. 9, 4520-4526 (2009).
17. Lucon, J. et al. A click chemistry based coordination polymer inside small heat shock protein. Chem. Commun. 46, 264-266 (2010).
18. Earnshaw W., Casjens, S. & Harrison, S. C. Assembly of head of bacteriophage P22: X-ray diffraction from heads, proheads and related structures. J. Mol. Biol. 104, 387-410 (1976).
19. Parent, K. N. et al. P22 coat protein structures reveal a novel mechanism for capsid maturation: stability without auxiliary proteins or chemical crosslinks. Structure 18, 390-401 (2010).
20. Teschke, C. M., McGough, A. & Thuman-Commike, P. A. Penton release from P22 heat-expanded capsids suggests importance of stabilizing penton-hexon interactions during capsid maturation. Biophys J 84, 2585-2592 (2003).
21. Chen, D. H. et al. Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proc. Natl Acad. Sci. USA 108, 1355-1360 (2011).
22. Kang, S. et al. Implementation of P22 viral capsids as nanoplatforms. Biomacromolecules 11, 2804-2809 (2010).
23. Tuma, R., Prevelige, P. E. & Thomas, G. J. Mechanism of capsid maturation in a double-stranded DNA virus. Proc. Natl Acad. Sci. USA 95, 9885-9890 (1998).
24. Mantovani, G. et al. Design and synthesis of N-maleimido-functionalized hydrophilic polymers via copper-mediated living radical polymerization: a suitable alternative to PEGylation chemistry. J. Am. Chem. Soc. 127, 2966-2973 (2005).
25. Heredia, K. L. et al. In situ preparation of protein: 'Smart' polymer conjugates with retention of bioactivity. J. Am. Chem. Soc. 127, 16955-16960 (2005).
26. Peeler, J. C. et al. Genetically encoded initiator for polymer growth from proteins. J. Am. Chem. Soc. 132, 13575-13577 (2010).
27. Alidedeoglu, A. H., York, A. W., Rosado, D. A., McCormick, C. L. & Morgan, S. E. Bioconjugation of D-glucuronic acid sodium salt to well-defined primary amine-containing homopolymers and block copolymers. J. Polym. Sci. A 48, 3052-3061 (2010).
28. Weinstein J. N., Yoshikami, S., Henkart, P., Blumenthal, R. & Hagins, W. A. Liposome-cell interaction: transfer and intracellular release of a trapped fluorescent marker. Science 195, 489-492 (1977).
29. Chen, R. F. & Knutson, J. R. Mechanism of fluorescence concentration quenching of carboxyfluorescein in liposomes: energy transfer to nonfluorescent dimers. Anal. Biochem. 172, 61-77 (1988).
30. Kang, S., Hawkridge, A. M., Johnson, K. L., Muddiman, D. C. & Prevelige, P. E. Identification of subunit-subunit interactions in bacteriophage P22 procapsids by chemical cross-linking and mass spectrometry. J. Proteome Res. 5, 370-377 (2006).
31. Allen, M. et al. Paramagnetic viral nanoparticles as potential highrelaxivity magnetic resonance contrast agents. Magn. Reson. Med. 54, 807-812 (2005).
32. Liepold, L. et al. Viral capsids as MRI contrast agents. Magn. Reson. Med. 58, 871-879 (2007).
33. Anderson, E. A. et al. Viral nanoparticles donning a paramagnetic coat: conjugation of MRI contrast agents to the MS2 capsid. Nano Lett. 6, 1160-1164 (2006).
34. Prasuhn, D. E., Yeh, R. M., Obenaus, A., Manchester, M. & Finn, M. G. Viral MRI contrast agents: coordination of Gd by native virions and attachment of Gd complexes by azide-alkyne cycloaddition. Chem. Commun. 1269-1271 (2007).
35. Datta, A. et al. High relaxivity gadolinium hydroxypyridonate-viral capsid conjugates: nanosized MRI contrast agents. J. Am. Chem. Soc. 130, 2546-2552 (2008).
36. Hooker, J. M., Datta, A., Botta, M., Raymond, K. N. & Francis, M. B. Magnetic resonance contrast agents from viral capsid shells: a comparison of exterior and interior cargo strategies. Nano Lett. 7, 2207-2210 (2007).
37. Dunand, F. A., Borel, A. & Helm, L. Gd(III) based MRI contrast agents: improved physical meaning in a combined analysis of EPR and NMR data? Inorg. Chem. Commun. 5, 811-815 (2002).
38. Mulder, W. J. M., Strijkers, G. J., van Tilborg, G. A. F., Griffioen, A. W. & Nicolay, K. Lipid-based nanoparticles for contrast-enhanced MRI and molecular imaging. NMR Biomed. 19, 142-164 (2006).
39. Ghaghada, K. B. et al. New dual mode gadolinium nanoparticle contrast agent for magnetic resonance imaging. PLoS One 4, 1-7 (2009).
40. Karfeld-Sulzer, L. S., Waters, E. A., Davis, N. E., Meade, T. J. & Barron, A. E. Multivalent protein polymer MRI contrast agents: controlling relaxivity via modulation of amino acid sequence. Biomacromolecules 11, 1429-1436 (2010).
41. Schuhmanngiampieri, G., Schmittwillich, H., Frenzel, T., Press, W. R. & Weinmann, H. J. In vivo and in vitro evaluation of Gd-DTPA-polylysine as a macromolecular contrast agent for magnetic resonance imaging. Invest. Radiol. 26, 969-974 (1991).
42. Ananta, J. S. et al. Geometrical confinement of gadolinium-based contrast agents in nanoporous particles enhances T(1) contrast. Nature Nanotech. 5, 815-821 (2010).