Advertisement

Protein Cage Nanoparticles as Delivery Nanoplatforms

  • Bongseo Choi
  • Hansol Kim
  • Hyukjun Choi
  • Sebyung KangEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1064)

Abstract

Protein cage nanoparticles are made of biomaterials, proteins, and have well-defined cage-like architectures designed and built by nature. They are composed of multiple copies of one or a small number of chemically identical subunits having a highly uniform nano-size and symmetric structure. Protein cage nanoparticles have genetic and chemical plasticity amenable to simultaneously introducing multiple cell-specific targeting ligands, diagnostic agents, and their corresponding therapeutic agents at desired sites depending on its purpose. A wide range of protein cage nanoparticles, such as ferritin, lumazine synthase, encapsulin, and virus-like particles, has been extensively explored and utilized in biomedical fields as effective delivery nanoplatforms of diagnostics and/or therapeutics. Highly biocompatible and plastic protein cage nanoparticles may provide a new paradigm for developing simple, but versatile in vivo delivery systems.

Keywords

Protein cage nanoparticle Delivery nanoplatform Cargo delivery Vaccine delivery MRI contrast agent 

References

  1. Aljabali AAA, Shukla S, Lomonossoff GP, Steinmetz NF, Evans DJ (2013) CPMV-DOX delivers. Mol Pharm 10(1):3–10.  https://doi.org/10.1021/mp3002057 CrossRefGoogle Scholar
  2. Allen TM, Cullis PR (2013) Liposomal drug delivery systems: from concept to clinical applications. Adv Drug Deliv Rev 65(1):36–48.  https://doi.org/10.1016/j.addr.2012.09.037 CrossRefPubMedGoogle Scholar
  3. Anand P, O’Neil A, Lin E, Douglas T, Holford M (2015) Tailored delivery of analgesic ziconotide across a blood brain barrier model using viral nanocontainers. Sci Rep 5:12497.  https://doi.org/10.1038/srep12497 CrossRefPubMedCentralPubMedGoogle Scholar
  4. Anderson EA, Isaacman S, Peabody DS, Wang EY, Canary JW, Kirshenbaum K (2006) Viral nanoparticles Donning a paramagnetic coat: conjugation of MRI contrast agents to the MS2 capsid. Nano Lett 6(6):1160–1164.  https://doi.org/10.1021/nl060378g CrossRefGoogle Scholar
  5. Ashley CE, Carnes EC, Phillips GK, Durfee PN, Buley MD, Lino CA, Padilla DP, Phillips B, Carter MB, Willman CL, Brinker CJ, Caldeira JC, Chackerian B, Wharton W, Peabody DS (2011) Cell-specific delivery of diverse cargos by bacteriophage MS2 virus-like particles. ACS Nano 5(7):5729–5745.  https://doi.org/10.1021/nn201397z CrossRefPubMedCentralPubMedGoogle Scholar
  6. Azuma Y, Zschoche R, Hilvert D (2017) The C-terminal peptide of Aquifex aeolicus riboflavin synthase directs encapsulation of native and foreign guests by a cage-forming lumazine synthase. J Biol Chem 292(25):10321–10327.  https://doi.org/10.1074/jbc.C117.790311 CrossRefPubMedCentralPubMedGoogle Scholar
  7. Bachmann MF, Jennings GT (2010) Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 10(11):787–796.  https://doi.org/10.1038/nri2868 CrossRefGoogle Scholar
  8. Beck T, Tetter S, Künzle M, Hilvert D (2015) Construction of Matryoshka-type structures from supercharged protein nanocages. Angew Chem Int Ed 54(3):937–940.  https://doi.org/10.1002/anie.201408677 CrossRefGoogle Scholar
  9. Berzofsky JA, Ahlers JD, Belyakov IM (2001) Strategies for designing and optimizing new generation vaccines. Nat Rev Immunol 1(3):209–219.  https://doi.org/10.1038/35105075 CrossRefGoogle Scholar
  10. Bode SA, Minten IJ, Nolte RJM, Cornelissen JJLM (2011) Reactions inside nanoscale protein cages. Nanoscale 3(6):2376–2389.  https://doi.org/10.1039/C0NR01013H CrossRefPubMedGoogle Scholar
  11. Brasch M, de la Escosura A, Ma Y, Uetrecht C, Heck AJR, Torres T, Cornelissen JJLM (2011) Encapsulation of Phthalocyanine supramolecular stacks into virus-like particles. J Am Chem Soc 133(18):6878–6881.  https://doi.org/10.1021/ja110752u CrossRefGoogle Scholar
  12. Brigger I, Dubernet C, Couvreur P (2002) Nanoparticles in cancer therapy and diagnosis. Adv Drug Deliv Rev 54(5):631–651.  https://doi.org/10.1016/S0169-409X(02)00044-3 CrossRefGoogle Scholar
  13. Brown SD, Fiedler JD, Finn MG (2009) Assembly of hybrid bacteriophage Qβ virus-like particles. Biochemistry 48(47):11155–11157.  https://doi.org/10.1021/bi901306p CrossRefPubMedCentralPubMedGoogle Scholar
  14. Brumfield S, Willits D, Tang L, Johnson JE, Douglas T, Young M (2004) Heterologous expression of the modified coat protein of Cowpea chlorotic mottle bromovirus results in the assembly of protein cages with altered architectures and function. J Gen Virol 85(4):1049–1053.  https://doi.org/10.1099/vir.0.19688-0 CrossRefGoogle Scholar
  15. Brune KD, Leneghan DB, Brian IJ, Ishizuka AS, Bachmann MF, Draper SJ, Biswas S, Howarth M (2016) Plug-and-display: decoration of virus-like particles via isopeptide bonds for modular immunization. Sci Rep 6:19234.  https://doi.org/10.1038/srep19234 CrossRefPubMedCentralPubMedGoogle Scholar
  16. Cao C, Wang X, Cai Y, Sun L, Tian L, Wu H, He X, Lei H, Liu W, Chen G, Zhu R, Pan Y (2014) Targeted in vivo imaging of microscopic tumors with Ferritin-based nanoprobes across biological barriers. Adv Mater 26(16):2566–2571.  https://doi.org/10.1002/adma.201304544 CrossRefGoogle Scholar
  17. Caravan P (2006) Strategies for increasing the sensitivity of gadolinium based MRI contrast agents. Chem Soc Rev 35(6):512–523.  https://doi.org/10.1039/B510982P CrossRefGoogle Scholar
  18. Chackerian B (2007) Virus-like particles: flexible platforms for vaccine development. Expert Review of Vaccines 6(3):381–390.  https://doi.org/10.1586/14760584.6.3.381 CrossRefGoogle Scholar
  19. Chen Y, Xiong X, Liu X, Li J, Wen Y, Chen Y, Dai Q, Cao Z, Yu W (2006) Immunoreactivity of HCV/HBV epitopes displayed in an epitope-presenting system. Mol Immunol 43(5):436–442.  https://doi.org/10.1016/j.molimm.2005.03.002 CrossRefGoogle Scholar
  20. Chen W, Cao Y, Liu M, Zhao Q, Huang J, Zhang H, Deng Z, Dai J, Williams DF, Zhang Z (2012) Rotavirus capsid surface protein VP4-coated Fe3O4 nanoparticles as a theranostic platform for cellular imaging and drug delivery. Biomaterials 33(31):7895–7902.  https://doi.org/10.1016/j.biomaterials.2012.07.016 CrossRefGoogle Scholar
  21. Choi B, Moon H, Hong SJ, Shin C, Do Y, Ryu S, Kang S (2016) Effective delivery of antigen–encapsulin nanoparticle fusions to dendritic cells leads to antigen-specific cytotoxic T cell activation and tumor rejection. ACS Nano 10(8):7339–7350.  https://doi.org/10.1021/acsnano.5b08084 CrossRefGoogle Scholar
  22. 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(8):2546–2552.  https://doi.org/10.1021/Ja0765363 CrossRefGoogle Scholar
  23. Douglas T, Young M (2006) Viruses: making friends with Old Foes. Science 312(5775):873.  https://doi.org/10.1126/science.1123223 CrossRefGoogle Scholar
  24. Enomoto T, Kawano M, Fukuda H, Sawada W, Inoue T, Haw KC, Kita Y, Sakamoto S, Yamaguchi Y, Imai T, Hatakeyama M, Saito S, Sandhu A, Matsui M, Aoki I, Handa H (2013) Viral protein-coating of magnetic nanoparticles using simian virus 40 VP1. J Biotechnol 167(1):8–15.  https://doi.org/10.1016/j.jbiotec.2013.06.005 CrossRefGoogle Scholar
  25. Fan K, Cao C, Pan Y, Lu D, Yang D, Feng J, Song L, Liang M, Yan X (2012) Magnetoferritin nanoparticles for targeting and visualizing tumour tissues. Nat Nano 7(7):459–464.  https://doi.org/10.1038/nnano.2012.90 CrossRefGoogle Scholar
  26. Ferreira MF, Mousavi B, Ferreira PM, Martins CIO, Helm L, Martins JA, Geraldes CFGC (2012) Gold nanoparticles functionalised with stable, fast water exchanging Gd3+ chelates as high relaxivity contrast agents for MRI. Dalton Trans 41(18):5472–5475.  https://doi.org/10.1039/c2dt30388d CrossRefGoogle Scholar
  27. Flenniken ML, Uchida M, Liepold LO, Kang S, Young MJ, Douglas T (2009) A library of protein cage architectures as nanomaterials. Curr Top Microbiol Immunol 327:71–93Google Scholar
  28. Frey R, Hayashi T, Hilvert D (2016) Enzyme-mediated polymerization inside engineered protein cages. Chem Commun 52(68):10423–10426.  https://doi.org/10.1039/C6CC05301G CrossRefGoogle Scholar
  29. Galaway FA, Stockley PG (2013) MS2 viruslike particles: a robust, semisynthetic targeted drug delivery platform. Mol Pharm 10(1):59–68.  https://doi.org/10.1021/mp3003368 CrossRefGoogle Scholar
  30. 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(37):14704–14709.  https://doi.org/10.1021/ja204516p CrossRefPubMedCentralPubMedGoogle Scholar
  31. Giessen TW (2016) Encapsulins: microbial nanocompartments with applications in biomedicine, nanobiotechnology and materials science. Curr Opin Chem Biol 34:1–10.  https://doi.org/10.1016/j.cbpa.2016.05.013 CrossRefPubMedGoogle Scholar
  32. Grgacic EVL, Anderson DA (2006) Virus-like particles: passport to immune recognition. Methods 40(1):60–65.  https://doi.org/10.1016/j.ymeth.2006.07.018 CrossRefGoogle Scholar
  33. Han J-A, Kang YJ, Shin C, Ra J-S, Shin H-H, Hong SY, Do Y, Kang S (2014) Ferritin protein cage nanoparticles as versatile antigen delivery nanoplatforms for dendritic cell (DC)-based vaccine development. Nanomedicine 10(3):561–569.  https://doi.org/10.1016/j.nano.2013.11.003 CrossRefPubMedGoogle Scholar
  34. Hooker JM, Datta A, Botta M, Raymond KN, Francis MB (2007) Magnetic resonance contrast agents from viral capsid shells: a comparison of exterior and Interior Cargo strategies. Nano Lett 7(8):2207–2210.  https://doi.org/10.1021/nl070512c CrossRefPubMedGoogle Scholar
  35. Huang X, Stein BD, Cheng H, Malyutin A, Tsvetkova IB, Baxter DV, Remmes NB, Verchot J, Kao C, Bronstein LM, Dragnea B (2011) Magnetic virus-like nanoparticles in N. benthamiana Plants: a new paradigm for environmental and agronomic biotechnological research. ACS Nano 5(5):4037–4045.  https://doi.org/10.1021/nn200629g CrossRefPubMedCentralPubMedGoogle Scholar
  36. Janitzek CM, Matondo S, Thrane S, Nielsen MA, Kavishe R, Mwakalinga SB, Theander TG, Salanti A, Sander AF (2016) Bacterial superglue generates a full-length circumsporozoite protein virus-like particle vaccine capable of inducing high and durable antibody responses. Malar J 15:545.  https://doi.org/10.1186/s12936-016-1574-1 CrossRefPubMedCentralPubMedGoogle Scholar
  37. Jardine J, Julien J-P, Menis S, Ota T, Kalyuzhniy O, McGuire A, Sok D, Huang P-S, MacPherson S, Jones M, Nieusma T, Mathison J, Baker D, Ward AB, Burton DR, Stamatatos L, Nemazee D, Wilson IA, Schief WR (2013) Rational HIV immunogen design to target specific germline B cell receptors. Science (New York, NY) 340(6133):711–716.  https://doi.org/10.1126/science.1234150 CrossRefGoogle Scholar
  38. Jennings GT, Bachmann MF (2009) Immunodrugs: therapeutic VLP-based vaccines for chronic diseases. Annu Rev Pharmacol Toxicol 49(1):303–326.  https://doi.org/10.1146/annurev-pharmtox-061008-103129 CrossRefPubMedGoogle Scholar
  39. Jordan PC, Patterson DP, Saboda KN, Edwards EJ, Miettinen HM, Basu G, Thielges MC, Douglas T (2016) Self-assembling biomolecular catalysts for hydrogen production. Nat Chem 8(2):179–185.  https://doi.org/10.1038/nchem.2416 CrossRefPubMedGoogle Scholar
  40. Kanekiyo M, Wei C-J, Yassine HM, McTamney PM, Boyington JC, Whittle JRR, Rao SS, Kong W-P, Wang L, Nabel GJ (2013) Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature 499(7456):102–106.  https://doi.org/10.1038/nature12202 CrossRefPubMedCentralPubMedGoogle Scholar
  41. Kanekiyo M, Bu W, Joyce MG, Meng G, Whittle JRR, Baxa U, Yamamoto T, Narpala S, Todd J-P, Rao SS, McDermott AB, Koup RA, Rossmann MG, Mascola JR, Graham BS, Cohen JI, Nabel GJ (2015) Rational design of an Epstein-Barr Virus vaccine targeting the receptor-binding site. Cell 162(5):1090–1100.  https://doi.org/10.1016/j.cell.2015.07.043 CrossRefPubMedCentralPubMedGoogle Scholar
  42. Kang S, Douglas T (2010) Some enzymes just need a space of their own. Science 327(5961):42–43.  https://doi.org/10.1126/science.1184318 CrossRefGoogle Scholar
  43. Kang S, Lander GC, Johnson JE, Prevelige PE (2008a) Development of bacteriophage P22 as a platform for molecular display: genetic and chemical modifications of the procapsid exterior surface. Chembiochem 9(4):514–518.  https://doi.org/10.1002/cbic.200700555 CrossRefGoogle Scholar
  44. Kang S, Oltrogge LM, Broomell CC, Liepold LO, Prevelige PE, Young M, Douglas T (2008b) Controlled assembly of bifunctional chimeric protein cages and composition analysis using noncovalent Mass spectrometry. J Am Chem Soc 130(49):16527–16529.  https://doi.org/10.1021/ja807655t CrossRefPubMedGoogle Scholar
  45. Kang S, Suci PA, Broomell CC, Iwahori K, Kobayashi M, Yamashita I, Young M, Douglas T (2009) janus-like protein cages. Spatially controlled dual-functional surface modifications of protein cages. Nano Lett 9(6):2360–2366.  https://doi.org/10.1021/nl9009028 CrossRefGoogle Scholar
  46. Kang HJ, Kang YJ, Lee Y-M, Shin H-H, Chung SJ, Kang S (2012) Developing an antibody-binding protein cage as a molecular recognition drug modular nanoplatform. Biomaterials 33:5423–5430.  https://doi.org/10.1016/j.biomaterials.2012.03.055 CrossRefPubMedGoogle Scholar
  47. Kang YJ, Yang HJ, Jeon S, Kang Y-S, Do Y, Hong SY, Kang S (2014) Polyvalent display of monosaccharides on Ferritin protein cage nanoparticles for the recognition and binding of cell-surface lectins. Macromol Biosci 14(5):619–625.  https://doi.org/10.1002/mabi.201300528 CrossRefGoogle Scholar
  48. Kim H, Kang YJ, Min J, Choi H, Kang S (2016) Development of an antibody-binding modular nanoplatform for antibody-guided targeted cell imaging and delivery. RSC Adv 6(23):19208–19213.  https://doi.org/10.1039/C6RA00233A CrossRefGoogle Scholar
  49. Kitagawa T, Kosuge H, Uchida M, Iida Y, Dalman RL, Douglas T, McConnell MV (2017) RGD targeting of human ferritin iron oxide nanoparticles enhances in vivo MRI of vascular inflammation and angiogenesis in experimental carotid disease and abdominal aortic aneurysm. J Magn Reson Imaging 45(4):1144–1153.  https://doi.org/10.1002/jmri.25459 CrossRefPubMedGoogle Scholar
  50. Kushnir N, Streatfield SJ, Yusibov V (2012) Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine 31(1):58–83.  https://doi.org/10.1016/j.vaccine.2012.10.083 CrossRefGoogle Scholar
  51. Kwon C, Kang YJ, Jeon S, Jung S, Hong SY, Kang S (2012) Development of protein-cage-based delivery Nanoplatforms by Polyvalently displaying β-Cyclodextrins on the surface of Ferritins through Copper(I)-catalyzed Azide/Alkyne cycloaddition. Macromol Biosci 12(11):1452–1458.  https://doi.org/10.1002/mabi.201200178 CrossRefGoogle Scholar
  52. Lauffer RB (1987) Paramagnetic metal complexes as water proton relaxation agents for NMR imaging: theory and design. Chem Rev 87(5):901–927.  https://doi.org/10.1021/cr00081a003 CrossRefGoogle Scholar
  53. Lee EJ, Lee NK, Kim I-S (2016) Bioengineered protein-based nanocage for drug delivery. Adv Drug Deliv Rev 106:157–171.  https://doi.org/10.1016/j.addr.2016.03.002 CrossRefGoogle Scholar
  54. Leneghan DB, Miura K, Taylor IJ, Li Y, Jin J, Brune KD, Bachmann MF, Howarth M, Long CA, Biswas S (2017) Nanoassembly routes stimulate conflicting antibody quantity and quality for transmission-blocking malaria vaccines. Sci Rep 7:3811.  https://doi.org/10.1038/s41598-017-03798-3 CrossRefPubMedCentralPubMedGoogle Scholar
  55. Leong HS, Steinmetz NF, Ablack A, Destito G, Zijlstra A, Stuhlmann H, Manchester M, Lewis JD (2010) Intravital imaging of embryonic and tumor neovasculature using viral nanoparticles. Nat Protoc 5(8):1406–1417.  https://doi.org/10.1038/nprot.2010.103 CrossRefPubMedCentralPubMedGoogle Scholar
  56. Lewis JD, Destito G, Zijlstra A, Gonzalez MJ, Quigley JP, Manchester M, Stuhlmann H (2006) Viral nanoparticles as tools for intravital vascular imaging. Nat Med 12(3):354–360.  https://doi.org/10.1038/nm1368 CrossRefPubMedCentralPubMedGoogle Scholar
  57. Liepold L, Anderson S, Willits D, Oltrogge L, Frank JA, Douglas T, Young M (2007) Viral capsids as MRI contrast agents. Magn Reson Med 58(5):871–879.  https://doi.org/10.1002/mrm.21307 CrossRefGoogle Scholar
  58. Liepold LO, Abedin MJ, Buckhouse ED, Frank JA, Young MJ, Douglas T (2009) supramolecular protein cage composite MR contrast agents with extremely efficient relaxivity properties. Nano Lett 9(12):4520–4526.  https://doi.org/10.1021/Nl902884p CrossRefPubMedCentralPubMedGoogle Scholar
  59. Ma Y, Nolte RJM, Cornelissen JJLM (2012) Virus-based nanocarriers for drug delivery. Adv Drug Deliv Rev 64(9):811–825.  https://doi.org/10.1016/j.addr.2012.01.005 CrossRefGoogle Scholar
  60. Maham A, Tang Z, Wu H, Wang J, Lin Y (2009) Protein-based nanomedicine platforms for drug delivery. Small 5(15):1706–1721.  https://doi.org/10.1002/smll.200801602 CrossRefGoogle Scholar
  61. Manayani DJ, Thomas D, Dryden KA, Reddy V, Siladi ME, Marlett JM, Rainey GJA, Pique ME, Scobie HM, Yeager M, Young JAT, Manchester M, Schneemann A (2007) A viral nanoparticle with dual function as an Anthrax Antitoxin and vaccine. PLoS Pathog 3(10):e142.  https://doi.org/10.1371/journal.ppat.0030142 CrossRefPubMedCentralPubMedGoogle Scholar
  62. Maurer P, Jennings GT, Willers J, Rohner F, Lindman Y, Roubicek K, Renner WA, Müller P, Bachmann MF (2005) A therapeutic vaccine for nicotine dependence: preclinical efficacy, and phase I safety and immunogenicity. Eur J Immunol 35(7):2031–2040.  https://doi.org/10.1002/eji.200526285 CrossRefGoogle Scholar
  63. Min J, Jung H, Shin H-H, Cho G, Cho H, Kang S (2013) Implementation of P22 viral capsids as intravascular magnetic resonance T1 contrast Conjugates via site-selective attachment of Gd(III)-chelating agents. Biomacromolecules 14(7):2332–2339.  https://doi.org/10.1021/bm400461j CrossRefGoogle Scholar
  64. Min J, Kim S, Lee J, Kang S (2014a) Lumazine synthase protein cage nanoparticles as modular delivery platforms for targeted drug delivery. RSC Adv 4(89):48596–48600.  https://doi.org/10.1039/C4RA10187A CrossRefGoogle Scholar
  65. Min J, Moon H, Yang HJ, Shin H-H, Hong SY, Kang S (2014b) Development of P22 viral capsid nanocomposites as anti-cancer drug, Bortezomib (BTZ), delivery nanoplatforms. Macromol Biosci 14(4):557–564.  https://doi.org/10.1002/mabi.201300401 CrossRefGoogle Scholar
  66. Molino NM, Anderson AKL, Nelson EL, Wang S-W (2013) biomimetic protein nanoparticles facilitate enhanced dendritic cell activation and cross-presentation. ACS Nano 7(11):9743–9752.  https://doi.org/10.1021/nn403085w CrossRefPubMedCentralPubMedGoogle Scholar
  67. Moon H, Kim WG, Lim S, Kang YJ, Shin H-H, Ko H, Hong SY, Kang S (2013) Fabrication of uniform layer-by-layer assemblies with complementary protein cage nanobuilding blocks via simple His-tag/metal recognition. J Mater Chem B 1(35):4504–4510.  https://doi.org/10.1039/C3TB20554A CrossRefGoogle Scholar
  68. Moon H, Lee J, Kim H, Heo S, Min J, Kang S (2014a) Genetically engineering encapsulin protein cage nanoparticle as a SCC-7 Cell targeting optical nanoprobe. Biomaterials research 18:21.  https://doi.org/10.1186/2055-7124-18-21 CrossRefPubMedCentralPubMedGoogle Scholar
  69. Moon H, Lee J, Min J, Kang S (2014b) Developing genetically engineered encapsulin protein cage nanoparticles as a targeted delivery nanoplatform. Biomacromolecules 15:3794–3801.  https://doi.org/10.1021/bm501066m CrossRefGoogle Scholar
  70. Moon H, Bae Y, Kim H, Kang S (2016) Plug-and-playable fluorescent cell imaging modular toolkits using the bacterial superglue, SpyTag/SpyCatcher. Chem Commun 52(97):14051–14054.  https://doi.org/10.1039/C6CC07363H CrossRefGoogle Scholar
  71. O’Neil A, Prevelige PE, Basu G, Douglas T (2012) coconfinement of fluorescent proteins: spatially enforced communication of GFP and mCherry encapsulated within the P22 capsid. Biomacromolecules 13(12):3902–3907.  https://doi.org/10.1021/bm301347x CrossRefGoogle Scholar
  72. Ochoa WF, Chatterji A, Lin T, Johnson JE (2006) Generation and structural analysis of reactive empty particles derived from an icosahedral virus. Chem Biol 13(7):771–778.  https://doi.org/10.1016/j.chembiol.2006.05.014 CrossRefGoogle Scholar
  73. Pan Y, Jia T, Zhang Y, Zhang K, Zhang R, Li J, Wang L (2012a) MS2 VLP-based delivery of microRNA-146a inhibits autoantibody production in lupus-prone mice. Int J Nanomedicine 7:5957–5967.  https://doi.org/10.2147/IJN.S37990 CrossRefPubMedCentralPubMedGoogle Scholar
  74. Pan Y, Zhang Y, Jia T, Zhang K, Li J, Wang L (2012b) Development of a microRNA delivery system based on bacteriophage MS2 virus-like particles. FEBS J 279(7):1198–1208.  https://doi.org/10.1111/j.1742-4658.2012.08512.x CrossRefGoogle Scholar
  75. Patterson DP, Prevelige PE, Douglas T (2012) Nanoreactors by programmed enzyme encapsulation inside the capsid of the bacteriophage P22. ACS Nano 6(6):5000–5009.  https://doi.org/10.1021/nn300545z CrossRefGoogle Scholar
  76. Patterson DP, Rynda-Apple A, Harmsen AL, Harmsen AG, Douglas T (2013) Biomimetic antigenic nanoparticles elicit controlled protective immune response to influenza. ACS Nano 7(4):3036–3044.  https://doi.org/10.1021/nn4006544 CrossRefPubMedCentralPubMedGoogle Scholar
  77. Patterson DP, Schwarz B, Waters RS, Gedeon T, Douglas T (2014) Encapsulation of an enzyme cascade within the bacteriophage P22 virus-like particle. ACS Chem Biol 9(2):359–365.  https://doi.org/10.1021/cb4006529 CrossRefGoogle Scholar
  78. Peabody DS (2003) A viral platform for chemical modification and multivalent display. Journal of Nanobiotechnology 1(1):5.  https://doi.org/10.1186/1477-3155-1-5 CrossRefPubMedCentralPubMedGoogle Scholar
  79. Peabody DS, Manifold-Wheeler B, Medford A, Jordan SK, Caldeira JC, Chackerian B (2008) Immunogenic display of diverse peptides on virus-like particles of RNA phage MS2. J Mol Biol 380(1):252–263.  https://doi.org/10.1016/j.jmb.2008.04.049 CrossRefPubMedCentralPubMedGoogle Scholar
  80. Plummer EM, Manchester M (2011) Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. Wiley Interdiscip Rev Nanomed Nanobiotechnol 3(2):174–196.  https://doi.org/10.1002/wnan.119 CrossRefGoogle Scholar
  81. Pokorski JK, Breitenkamp K, Finn MG (2011) Functional virus-based polymer-protein nanoparticles by atom transfer radical polymerization. J Am Chem Soc 133(24):9242–9245.  https://doi.org/10.1021/ja203286n CrossRefPubMedCentralPubMedGoogle Scholar
  82. Prasuhn JDE, Yeh RM, Obenaus A, Manchester M, Finn MG (2007) Viral MRI contrast agents: coordination of Gd by native virions and attachment of Gd complexes by azide-alkyne cycloaddition. Chem Commun 12:1269–1271.  https://doi.org/10.1039/B615084E CrossRefGoogle Scholar
  83. Prevelige PE, Thomas D, King J (1988) Scaffolding protein regulates the polymerization of P22 coat subunits into icosahedral shells in vitro. J Mol Biol 202(4):743–757.  https://doi.org/10.1016/0022-2836(88)90555-4 CrossRefGoogle Scholar
  84. Qazi S, Liepold LO, Abedin MJ, Johnson B, Prevelige P, Frank JA, Douglas T (2013) P22 viral capsids as nanocomposite high-relaxivity MRI contrast agents. Mol Pharm 10(1):11–17.  https://doi.org/10.1021/mp300208g CrossRefGoogle Scholar
  85. Qazi S, Miettinen HM, Wilkinson RA, McCoy K, Douglas T, Wiedenheft B (2016) Programmed self-assembly of an active P22-Cas9 nanocarrier system. Mol Pharm 13(3):1191–1196.  https://doi.org/10.1021/acs.molpharmaceut.5b00822 CrossRefGoogle Scholar
  86. Ra J-S, Shin H-H, Kang S, Do Y (2014) Lumazine synthase protein cage nanoparticles as antigen delivery nanoplatforms for dendritic cell-based vaccine development. Clin Exp Vaccine Res 3(2):227–234.  https://doi.org/10.7774/cevr.2014.3.2.227 CrossRefPubMedCentralPubMedGoogle Scholar
  87. Rhee J-K, Baksh M, Nycholat C, Paulson JC, Kitagishi H, Finn MG (2012) Glycan-targeted virus-like nanoparticles for photodynamic therapy. Biomacromolecules 13(8):2333–2338.  https://doi.org/10.1021/bm300578p CrossRefPubMedCentralPubMedGoogle Scholar
  88. Richert LE, Servid AE, Harmsen AL, Rynda-Apple A, Han S, Wiley JA, Douglas T, Harmsen AG (2012) A virus-like particle vaccine platform elicits heightened and hastened local lung mucosal antibody production after a single dose. Vaccine 30(24):3653–3665.  https://doi.org/10.1016/j.vaccine.2012.03.035 CrossRefPubMedCentralPubMedGoogle Scholar
  89. Rösler A, Vandermeulen GWM, Klok H-A (2001) Advanced drug delivery devices via self-assembly of amphiphilic block copolymers. Adv Drug Deliv Rev 53(1):95–108.  https://doi.org/10.1016/S0169-409X(01)00222-8 CrossRefGoogle Scholar
  90. Schwarz B, Douglas T (2015) Development of virus-like particles for diagnostic and prophylactic biomedical applications. Wiley Interdiscip Rev Nanomed Nanobiotechnol 7(5):722–735.  https://doi.org/10.1002/wnan.1336 CrossRefPubMedCentralPubMedGoogle Scholar
  91. Scodeller EA, Tisminetzky SG, Porro F, Schiappacassi M, De Rossi A, Chiecco-Bianchi L, Baralle FE (1995) A new epitope presenting system displays a HIV-1 V3 loop sequence and induces neutralizing antibodies. Vaccine 13(13):1233–1239.  https://doi.org/10.1016/0264-410X(95)00058-9 CrossRefGoogle Scholar
  92. Seebeck FP, Woycechowsky KJ, Zhuang W, Rabe JP, Hilvert D (2006) A simple tagging system for protein encapsulation. J Am Chem Soc 128(14):4516–4517.  https://doi.org/10.1021/ja058363s CrossRefGoogle Scholar
  93. Sharma J, Uchida M, Miettinen HM, Douglas T (2017) Modular interior loading and exterior decoration of a virus-like particle. Nano 9(29):10420–10430.  https://doi.org/10.1039/C7NR03018E CrossRefGoogle Scholar
  94. Shukla S, Steinmetz NF (2015) Virus-based nanomaterials as PET and MR contrast agents: from technology development to translational medicine. Wiley Interdiscip Rev Nanomed Nanobiotechnol 7(5):708–721.  https://doi.org/10.1002/wnan.1335 CrossRefPubMedCentralPubMedGoogle Scholar
  95. Song Y, Kang YJ, Jung H, Kim H, Kang S, Cho H (2015) Lumazine synthase protein nanoparticle-Gd(III)-DOTA conjugate as a T1 contrast agent for high-field MRI. Sci Rep 5:15656.  https://doi.org/10.1038/srep15656 CrossRefPubMedCentralPubMedGoogle Scholar
  96. Steinmetz NF, Hong V, Spoerke ED, Lu P, Breitenkamp K, Finn MG, Manchester M (2009) Buckyballs meet viral nanoparticles: candidates for biomedicine. J Am Chem Soc 131(47):17093–17095.  https://doi.org/10.1021/ja902293w CrossRefPubMedCentralPubMedGoogle Scholar
  97. 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(10):6014–6020.  https://doi.org/10.1021/nn1014769 CrossRefGoogle Scholar
  98. Suci P, Kang S, Gmur R, Douglas T, Young M (2010) Targeted delivery of a photosensitizer to aggregatibacter actinomycetemcomitans biofilm. Antimicrob Agents Chemother 54(6):2489–2496.  https://doi.org/10.1128/aac.00059-10 CrossRefPubMedCentralPubMedGoogle Scholar
  99. Sutter M, Boehringer D, Gutmann S, Gunther S, Prangishvili D, Loessner MJ, Stetter KO, Weber-Ban E, Ban N (2008) Structural basis of enzyme encapsulation into a bacterial nanocompartment. Nat Struct Mol Biol 15(9):939–947.  https://doi.org/10.1038/nsmb.1473 CrossRefGoogle Scholar
  100. Terashima M, Uchida M, Kosuge H, Tsao PS, Young MJ, Conolly SM, Douglas T, McConnell MV (2011) Human Ferritin cages for imaging vascular macrophages. Biomaterials 32(5):1430–1437.  https://doi.org/10.1016/j.biomaterials.2010.09.029 CrossRefGoogle Scholar
  101. Theil EC, Behera RK, Tosha T (2013) Ferritins for Chemistry and for life. Coord Chem Rev 257(2):579–586.  https://doi.org/10.1016/j.ccr.2012.05.013 CrossRefGoogle Scholar
  102. Thrane S, Janitzek CM, Matondo S, Resende M, Gustavsson T, de Jongh WA, Clemmensen S, Roeffen W, van de Vegte-Bolmer M, van Gemert GJ, Sauerwein R, Schiller JT, Nielsen MA, Theander TG, Salanti A, Sander AF (2016) Bacterial superglue enables easy development of efficient virus-like particle based vaccines. J Nanobiotechnol 14:30.  https://doi.org/10.1186/s12951-016-0181-1 CrossRefGoogle Scholar
  103. Tissot AC, Maurer P, Nussberger J, Sabat R, Pfister T, Ignatenko S, Volk H-D, Stocker H, Müller P, Jennings GT, Wagner F, Bachmann MF (2008) Effect of immunisation against angiotensin II with CYT006-AngQb on ambulatory blood pressure: a double-blind, randomised, placebo-controlled phase IIa study. Lancet 371(9615):821–827.  https://doi.org/10.1016/S0140-6736(08)60381-5 CrossRefGoogle Scholar
  104. Tissot AC, Renhofa R, Schmitz N, Cielens I, Meijerink E, Ose V, Jennings GT, Saudan P, Pumpens P, Bachmann MF (2010) Versatile virus-like particle carrier for epitope based vaccines. PLoS One 5(3):e9809.  https://doi.org/10.1371/journal.pone.0009809 CrossRefPubMedCentralPubMedGoogle Scholar
  105. Uchida M, Flenniken ML, Allen M, Willits DA, Crowley BE, Brumfield S, Willis AF, Jackiw L, Jutila M, Young MJ, Douglas T (2006) Targeting of cancer cells with ferrimagnetic ferritin cage nanoparticles. J Am Chem Soc 128(51):16626–16633.  https://doi.org/10.1021/ja0655690 CrossRefGoogle Scholar
  106. Uchida M, Terashima M, Cunningham CH, Suzuki Y, Willits DA, Willis AF, Yang PC, Tsao PS, McConnell MV, Young MJ, Douglas T (2008) A human ferritin iron oxide nano-composite magnetic resonance contrast agent. Magn Reson Med 60(5):1073–1081.  https://doi.org/10.1002/mrm.21761 CrossRefGoogle Scholar
  107. Uchida M, Kang S, Reichhardt C, Harlen K, Douglas T (2010) The ferritin superfamily: supramolecular templates for materials synthesis. Biochim Biophys Acta Gen Subj 1800:834–845.  https://doi.org/10.1016/j.bbagen.2009.12.005 CrossRefGoogle Scholar
  108. Wang AZ, Langer R, Farokhzad OC (2012) Nanoparticle delivery of cancer drugs. Annu Rev Med 63(1):185–198.  https://doi.org/10.1146/annurev-med-040210-162544 CrossRefGoogle Scholar
  109. Wörsdörfer B, Woycechowsky KJ, Hilvert D (2011) Directed evolution of a protein container. Science 331(6017):589–592.  https://doi.org/10.1126/science.1199081 CrossRefGoogle Scholar
  110. Wörsdörfer B, Pianowski Z, Hilvert D (2012) Efficient in vitro encapsulation of protein cargo by an engineered protein container. J Am Chem Soc 134(2):909–911.  https://doi.org/10.1021/ja211011k CrossRefGoogle Scholar
  111. Wu M, Sherwin T, Brown WL, Stockley PG (2005) Delivery of antisense oligonucleotides to leukemia cells by RNA bacteriophage capsids. Nanomedicine 1(1):67–76.  https://doi.org/10.1016/j.nano.2004.11.011 CrossRefGoogle Scholar
  112. Zakeri B, Fierer JO, Celik E, Chittock EC, Schwarz-Linek U, Moy VT, Howarth M (2012) Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc Natl Acad Sci U S A 109(12):E690–E697.  https://doi.org/10.1073/pnas.1115485109 CrossRefPubMedCentralPubMedGoogle Scholar
  113. Zhang X, Meining W, Fischer M, Bacher A, Ladenstein R (2001) X-ray structure analysis and crystallographic refinement of lumazine synthase from the hyperthermophile Aquifex aeolicus at 1.6 Å resolution: determinants of thermostability revealed from structural comparisons. J Mol Biol 306(5):1099–1114.  https://doi.org/10.1006/jmbi.2000.4435 CrossRefGoogle Scholar
  114. Zhang X, Meining W, Cushman M, Haase I, Fischer M, Bacher A, Ladenstein R (2003) A structure-based model of the reaction catalyzed by Lumazine synthase from Aquifex aeolicus. J Mol Biol 328(1):167–182.  https://doi.org/10.1016/S0022-2836(03)00186-4 CrossRefGoogle Scholar
  115. Zhen Z, Tang W, Chen H, Lin X, Todd T, Wang G, Cowger T, Chen X, Xie J (2013) RGD-modified Apoferritin nanoparticles for efficient drug delivery to tumors. ACS Nano 7(6):4830–4837.  https://doi.org/10.1021/nn305791q CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Bongseo Choi
    • 1
  • Hansol Kim
    • 1
  • Hyukjun Choi
    • 1
  • Sebyung Kang
    • 1
    Email author
  1. 1.Department of Biological Sciences, School of Life SciencesUlsan National Institute of Science and Technology (UNIST)UlsanSouth Korea

Personalised recommendations