Nanoscale assemblies and their biomedical applications

Journal of the Royal Society Interface

Volumn 10, Issue 80, 2013, Pages

  Doll, Tais A P F ^a   Raman, Senthilkumar ^b   Dey, Raja ^a   Burkhard, Peter ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b Alpha O Peptides AG   (Switzerland)

Author keywords

Drug delivery; Nanoparticle; Nanoscale assemblies; Peptide nanoparticles; Vaccines; Virus like particles

Indexed keywords

DRUG DELIVERY; MEDICAL APPLICATIONS; NANOPARTICLES; NUCLEIC ACIDS; PEPTIDES; POLYMERS; VACCINES; VIRUSES;

BIO-IMAGING; BIOLOGICAL UNITS; BIOMEDICAL APPLICATIONS; BUILDING BLOCKES; CELL TARGETING; EUKARYOTIC CELLS; FERRITIN PROTEIN; MICRO-COMPARTMENTS; NANO-ASSEMBLIES; NANOSCALE ASSEMBLIES; PEPTIDE NANOTUBES; SELF-ASSEMBLING; VACCINE DELIVERY; VACCINE DEVELOPMENT; VIRUS-LIKE PARTICLES;

NANOTECHNOLOGY;

CHITOSAN; COPOLYMER; DOXORUBICIN; FERRITIN; GREEN FLUORESCENT PROTEIN; HEPATITIS B VACCINE; LIPID; LIPOSOME; MICROSPHERE; NANOCAPSULE; NANOFIBER; NANOMATERIAL; NANOPARTICLE; NANOTUBE; NUCLEIC ACID; OVALBUMIN; PEPTIDE NANOTUBE; POLYGLACTIN; POLYPEPTIDE; PROTEIN; SMALL INTERFERING RNA; VIRUS LIKE PARTICLE VACCINE; VIRUS VACCINE; WART VIRUS VACCINE; VACCINE;

ALPHA VIRUS; ANTINEOPLASTIC ACTIVITY; BIOCOMPATIBILITY; BIODEGRADABILITY; BIOMEDICINE; BREAST CANCER; CANCER IMMUNOTHERAPY; CANCER PREVENTION; CELL ORGANELLE; DRUG DELIVERY SYSTEM; EUKARYOTIC CELL; GENE TARGETING; HUMAN; HYDROPHOBICITY; LIPID BILAYER; LIVER CELL CARCINOMA; LUNG CANCER; MELANOMA; NANOBIOTECHNOLOGY; NANOEMULSION; NANOENCAPSULATION; NANOTECHNOLOGY; NONHUMAN; REVIEW; TARGET CELL; UTERINE CERVIX CARCINOMA; VACCINE PRODUCTION; VIRUS CAPSID; VIRUS LIKE AGENT; ANIMAL; METHODOLOGY;

ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; NANOFIBERS; NANOTECHNOLOGY; NANOTUBES, PEPTIDE; VACCINES;

MLCS; MLOWN;

EID: 84879137858     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2012.0740     Document Type: Review

References (126)

1. Gomez-Gualdron DA, Burgos JC, Yu J, Balbuena PB. 2011 Carbon nanotubes: engineering biomedical applications. Progr. Mol. Biol. Transl. Sci. 104, 175- 245. (doi:10.1016/B978-0-12-416020-0.00005-X).
2. Raman S. 2008 Design and analysis of peptide based nanoparticles. PhD thesis, University of Basel, Switzerland. (doi:10.5451/unibas-004642021).
3. Liu J, Jiang Z, Zhang S, Liu C, Gross RA, Kyriakides TR, Saltzman WM. 2011 Biodegradation, biocompatibility, and drug delivery in poly(omegapentadecalactone- co-p-dioxanone) copolyesters. Biomaterials 32, 6646-6654. (doi:10.1016/j. biomaterials.2011.05.046).
4. Danhier F, Ansorena E, Silva JM, Coco R, Le Breton A, Preat V. 2012 PLGA-based nanoparticles: an overview of biomedical applications. J. Control. Rel. 161, 505-522. (doi:10.1016/j.jconrel.2012.01.043).
5. Zhou J, Patel TR, Fu M, Bertram JP, Saltzman WM. 2012 Octa-functional PLGA nanoparticles for targeted and efficient siRNA delivery to tumors. Biomaterials 33, 583-591. (doi:10.1016/j. biomaterials.2011.09.061).
6. Gao H, Elsabahy M, Giger EV, Li D, Prud'homme RE, Leroux JC. 2010 Aminated linear and star-shape poly(glycerol methacrylate)s: synthesis and selfassembling properties. Biomacromolecules 11, 889-895. (doi:10.1021/ bm901241k).
7. Meier W. 2000 Polymer nanocapsules. Chem. Soc. Rev. 29, 295-303. (doi:10.1039/a809106d).
8. Foster EJ, Berda EB, Meijer EW. 2009 Metastable supramolecular polymer nanoparticles via intramolecular collapse of single polymer chains. J. Am. Chem. Soc. 131, 6964-6966. (doi:10.1021/ja901687d).
9. Kim D et al. 2007 Direct synthesis of polymer nanocapsules with a noncovalently tailorable surface. Angew. Chem. Int. Ed. Engl. 46, 3471-3474. (doi:10.1002/anie.200604526).
10. Sakai H, Sekita A, Tanaka K, Sakai K, Kondo T, Abe M. 2011 Preparation and properties of nanosized biodegradable polymer capsules. J. Oleo Sci. 60, 569-573. (doi:10.5650/jos.60.569).
11. Kuykendall DW, Zimmerman SC. 2007 Nanoparticles: a very versatile nanocapsule. Nat. Nanotechnol. 2, 201-202. (doi:10.1038/nnano. 2007.90).
12. Dash M, Chiellini F, Ottenbrite RM, Chiellini E. 2011 Chitosan-a versatile semi-synthetic polymer in biomedical applications. Progr. Polym. Sci. 36, 981- 1014. (doi:10.1016/j.progpolymsci.2011.02.001).
13. Xu Y, Du Y. 2003 Effect of molecular structure of chitosan on protein delivery properties of chitosan nanoparticles. Int. J. Pharm. 250, 215-226. (doi:10.1016/S0378-5173(02)00548-3).
14. Sy JC, Seshadri G, Yang SC, Brown M, Oh T, Dikalov S, Murthy N, Davis ME. 2008 Sustained release of a p38 inhibitor from non-inflammatory microspheres inhibits cardiac dysfunction. Nat. Mater. 7, 863- 868. (doi:10.1038/nmat2299).
15. Geng Y, Dalhaimer P, Cai S, Tsai R, Tewari M, Minko T, Discher DE. 2007 Shape effects of filaments versus spherical particles in flow and drug delivery. Nat. Nanotechnol. 2, 249-255. (doi:10.1038/nnano. 2007.70).
16. Lee LA, Wang Q. 2006 Adaptations of nanoscale viruses and other protein cages for medical applications. Nanomed. Nanotechnol. Biol. Med. 2, 137-149. (doi:10.1016/j.nano.2006.07.009).
17. Liu L, Xu K, Wang H, Tan PK, Fan W, Venkatraman SS, Li L, Yang YY. 2009 Self-assembled cationic peptide nanoparticles as an efficient antimicrobial agent. Nat. Nanotechnol. 4, 457-463. (doi:10.1038/nnano.2009.153).
18. Martin CR, Kohli P. 2003 The emerging field of nanotube biotechnology. Nat. Rev. Drug Disc. 2, 29-37. (doi:10.1038/nrd988).
19. Rudra JS, Tian YF, Jung JP, Collier JH. 2010 A selfassembling peptide acting as an immune adjuvant. Proc. Natl Acad. Sci. USA 107, 622-627. (doi:10. 1073/pnas.0912124107).
20. Yang H, McLaughlin CK, Aldaye FA, Hamblin GD, Rys AZ, Rouiller I, Sleiman HF. 2009 Metal-nucleic acid cages. Nat. Chem. 1, 390-396. (doi:10.1038/nchem. 290).
21. Bangham AD. 1995 Surrogate cells or Trojan horses. The discovery of liposomes. Bioessays 17, 1081- 1088. (doi:10.1002/bies.950171213).
22. Sun B, Lim DS, Kuo JS, Kuyper CL, Chiu DT. 2004 Fast initiation of chemical reactions with laserinduced breakdown of a nanoscale partition. Langmuir 20, 9437-9440. (doi:10.1021/la048444m).
23. Verma S, Dent S, Chow BJ, Rayson D, Safra T. 2008 Metastatic breast cancer: the role of pegylated liposomal doxorubicin after conventional anthracyclines. Cancer Treat. Rev. 34, 391-406. (doi:10.1016/j.ctrv.2008.01.008) .
24. Tian B, Al-Jamal WT, Al-Jamal KT, Kostarelos K. 2011 Doxorubicin-loaded lipid-quantum dot hybrids: surface topography and release properties. Int. J. Pharm. 416, 443-447. (doi:10.1016/j. ijpharm.2011.01.057).
25. Shih WM, Quispe JD, Joyce GF. 2004 A 1.7-kilobase single-stranded DNA that folds into a nanoscale octahedron. Nature 427, 618-621. (doi:10.1038/nature02307).
26. Rothemund PW. 2006 Folding DNA to create nanoscale shapes and patterns. Nature 440, 297-302. (doi:10.1038/nature04586).
27. Douglas SM, Dietz H, Liedl T, Hogberg B, Graf F, Shih WM. 2009 Self-assembly of DNA into nanoscale three-dimensional shapes. Nature 459, 414-418. (doi:10.1038/nature08016).
28. Andersen ES et al. 2009 Self-assembly of a nanoscale DNA box with a controllable lid. Nature 459, 73-76. (doi:10.1038/nature 07971).
29. Douglas SM, Bachelet I, Church GM. 2012 A logicgated nanorobot for targeted transport of molecular payloads. Science 335, 831-834. (doi:10.1126/science.1214081).
30. Torring T, Voigt NV, Nangreave J, Yan H, Gothelf KV. 2011 DNA origami: a quantum leap for selfassembly of complex structures. Chem. Soc. Rev. 40, 5636-5646. (doi:10.1039/c1cs15057j).
31. Mansouri S, Cuie Y, Winnik F, Shi Q, Lavigne P, Benderdour M, Beaumont E, Fernandes JC. 2006 Characterization of folate-chitosan-DNA nanoparticles for gene therapy. Biomaterials 27, 2060-2065. (doi:10.1016/j.biomaterials.2005.09. 020).
32. Noad R, Roy P. 2003 Virus-like particles as immunogens. Trends Microbiol. 11, 438-444. (doi:10.1016/S0966-842X(03)00208-7).
33. Brown WL et al. 2002 RNA bacteriophage capsidmediated drug delivery and epitope presentation. Intervirology 45, 371-380. (doi:10.1159/000067930).
34. Chatterji A, Ochoa W, Shamieh L, Salakian SP, Wong SM, Clinton G, Ghosh P, Lin T, Johnson JE. 2004 Chemical conjugation of heterologous proteins on the surface of cowpea mosaic virus. Bioconjug. Chem. 15, 807-813. (doi:10.1021/bc0402888).
35. Wang Q, Kaltgrad E, Lin T, Johnson JE, Finn MG. 2002 Natural supramolecular building blocks. Wildtype cowpea mosaic virus. Chem. Biol. 9, 805-811. (doi:10.1016/S1074-5521(02)00165-5).
36. Wang Q, Lin T, Johnson JE, Finn MG. 2002 Natural supramolecular building blocks. Cysteine-added mutants of cowpea mosaic virus. Chem. Biol. 9, 813-819. (doi:10.1016/S1074-5521(02)00166-7).
37. Patel KG, Swartz JR. 2011 Surface functionalization of virus-like particles by direct conjugation using azide-alkyne click chemistry. Bioconjug. Chem. 22, 376-387. (doi:10.1021/bc100367u).
38. 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, 17 093- 17 095. (doi:10.1021/ja902293w).
39. McKee SJ, Young VL, Clow F, Hayman CM, Baird MA, Hermans IF, Young SL, Ward VK. 2012 Viruslike particles and a-galactosylceramide form a selfadjuvanting composite particle that elicits antitumor responses. J. Control. Rel. 159, 338-345. (doi:10.1016/j.jconrel.2012.02.015).
40. Avogadri F, Merghoub T, Maughan MF, Hirschhorn-Cymerman D, Morris J, Ritter E, Olmsted R, Houghton AN, Wolchok JD. 2010 Alphavirus replicon particles expressing TRP-2 provide potent therapeutic effect on melanoma through activation of humoral and cellular immunity. PLoS ONE 5, e12670. (doi:10.1371/journal.pone.0012670).
41. Buonaguro L, Petrizzo A, Tornesello ML, Buonaguro FM. 2011 Translating tumor antigens into cancer vaccines. Clin. Vaccine Immunol. 18, 23-34. (doi:10. 1128/CVI.00286-10).
42. No JH, Kim MK, Jeon YT, Kim YB, Song YS. 2011 Human papillomavirus vaccine: widening the scope for cancer prevention. Mol. Carcinog. 50, 244-253. (doi:10.1002/mc.20657).
43. Goicochea NL, De M, Rotello VM, Mukhopadhyay S, Dragnea B. 2007 Core-like particles of an enveloped animal virus can self-assemble efficiently on artificial templates. Nano Lett. 7, 2281-2290. (doi:10.1021/nl070860e).
44. Janssens ME, Geysen D, Broos K, De Goeyse I, Robbens J, Van Petegem F, Timmermans JP, Guisez Y. 2010 Folding properties of the hepatitis B core as a carrier protein for vaccination research. Amino Acids 38, 1617-1626. (doi:10.1007/s00726-009- 0365-1).
45. Zhang Y, Orner BP. 2011 Self-assembly in the ferritin nano-cage protein superfamily. Int. J. Mol. Sci. 12, 5406-5421. (doi:10.3390/ijms12085406).
46. Lawson DM et al. 1991 Solving the structure of human H ferritin by genetically engineering intermolecular crystal contacts. Nature 349, 541- 544. (doi:10.1038/349541a0).
47. Douglas T, Dickson DP, Betteridge S, Charnock J, Garner CD, Mann S. 1995 Synthesis and structure of an iron(III) sulfide-ferritin bioinorganic nanocomposite. Science 269, 54-57. (doi:10.1126/science.269.5220.54).
48. Klem MT, Mosolf J, Young M, Douglas T. 2008 Photochemical mineralization of europium, titanium, and iron oxyhydroxide nanoparticles in the ferritin protein cage. Inorg. Chem. 47, 2237- 2239. (doi:10.1021/ic701740q).
49. Kramer RM, Li C, Carter DC, Stone MO, Naik RR. 2004 Engineered protein cages for nanomaterial synthesis. J. Am. Chem. Soc. 126, 13 282-13 286. (doi:10.1021/ja046735b).
50. 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, 1430-1437. (doi:10. 1016/j.biomaterials.2010.09.029).
51. Uchida M et al. 2006 Targeting of cancer cells with ferrimagnetic ferritin cage nanoparticles. J. Am. Chem. Soc. 128, 16 626-16 633. (doi:10.1021/ja0655690).
52. Beeby M, Bobik TA, Yeates TO. 2009 Exploiting genomic patterns to discover new supramolecular protein assemblies. Protein Sci. 18, 69-79. (doi:10. 1002/pro.1).
53. Tsai SJ, Yeates TO. 2011 Bacterial microcompartments: insights into the structure, mechanism, and engineering applications. Progr. Mol. Biol. Transl. Sci. 103, 1-20. (doi:10.1016/B978-0-12-415906-8.00008-X).
54. Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM. 2008 Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat. Rev. Microbiol. 6, 681-691. (doi:10.1038/nrmicro1913).
55. Cannon GC, Bradburne CE, Aldrich HC, Baker SH, Heinhorst S, Shively JM. 2001 Microcompartments in prokaryotes: carboxysomes and related polyhedra. Appl. Environ. Microbiol. 67, 5351-5361. (doi:10. 1128/AEM.67.12.5351-5361.2001).
56. Reinhold L, Zviman M, Kaplan A. 1989 A quantitative model for inorganic carbon fluxes and photosynthesis in cyanobacteria. Plant Physiol. Biochem. 27, 945-954.
57. Drews G, Niklowitz W. 1956 [Cytology of Cyanophycea. II. Centroplasm and granular inclusions of Phormidium uncinatum]. Archiv Mikrobiol. 24, 147-162. (doi:10.1007/BF00408629).
58. Shively JM, Ball F, Brown DH, Saunders RE. 1973 Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus. Science 182, 584-586. (doi:10.1126/science.182.4112.584).
59. Choudhary S, Quin MB, Sanders MA, Johnson ET, Schmidt-Dannert C. 2012 Engineered protein nanocompartments for targeted enzyme localization. PLoS ONE 7, e33342. (doi:10.1371/journal.pone. 0033342).
60. Renggli K, Baumann P, Langowska K, Onaca O, Bruns N, Meier W. 2011 Selective and responsive nanoreactors. Adv. Funct. Mater. 21, 1241-1259. (doi:10.1002/adfm.201001563).
61. Kedersha NL, Rome LH. 1986 Isolation and characterization of a novel ribonucleoprotein particle: large structures contain a single species of small RNA. J. Cell Biol. 103, 699-709. (doi:10. 1083/jcb.103.3.699).
62. Suprenant KA. 2002 Vault ribonucleoprotein particles: sarcophagi, gondolas, or safety deposit boxes? Biochemistry 41, 14 447-14 454. (doi:10. 1021/bi026747e).
63. Kong LB, Siva AC, Rome LH, Stewart PL. 1999 Structure of the vault, a ubiquitous cellular component. Structure 7, 371-379. (doi:10.1016/S0969-2126(99) 80050-1).
64. Stephen AG, Raval-Fernandes S, Huynh T, Torres M, Kickhoefer VA, Rome LH. 2001 Assembly of vaultlike particles in insect cells expressing only the major vault protein. J. Biol. Chem. 276, 23 217-23 220. (doi:10.1074/jbc.C100226200).
65. Kickhoefer VA et al. 2005 Engineering of vault nanocapsules with enzymatic and fluorescent properties. Proc. Natl Acad. Sci. USA 102, 4348-4352. (doi:10.1073/pnas.0500929102).
66. Champion CI et al. 2009 A vault nanoparticle vaccine induces protective mucosal immunity. PLoS ONE 4, e5409. (doi:10.1371/journal.pone.0005409).
67. Han M, Kickhoefer VA, Nemerow GR, Rome LH. 2011 Targeted vault nanoparticles engineered with an endosomolytic peptide deliver biomolecules to the cytoplasm. ACS Nano 5, 6128-6137. (doi:10.1021/nn2014613).
68. Shaw DE et al. 2010 Atomic-level characterization of the structural dynamics of proteins. Science 330, 341-346. (doi:10.1126/science.1187409).
69. Service RF. 2010 Computational biology. Custombuilt supercomputer brings protein folding into view. Science 330, 308-309. (doi:10.1126/science. 330.6002.308-a).
70. MacKay JA, Chen M, McDaniel JR, Liu W, Simnick AJ, Chilkoti A. 2009 Self-assembling chimeric polypeptide-doxorubicin conjugate nanoparticles that abolish tumours after a single injection. Nat. Mater. 8, 993-999. (doi:10.1038/nmat2569).
71. Zhang S. 2003 Fabrication of novel biomaterials through molecular self-assembly. Nat. Biotechnol. 21, 1171-1178. (doi:10.1038/nbt874).
72. Ryadnov MG. 2007 A self-assembling peptide polynanoreactor. Angew. Chem. Int. Ed. Engl. 46, 969-972. (doi:10.1002/anie.200604014).
73. Padilla JE, Colovos C, Yeates TO. 2001 Nanohedra: using symmetry to design self assembling protein cages, layers, crystals, and filaments. Proc. Natl Acad. Sci. USA 98, 2217-2221. (doi:10.1073/pnas. 041614998).
74. Haghpanah JS et al. 2009 Artificial protein block copolymers blocks comprising two distinct selfassembling domains. ChemBioChem 10, 2733- 2735. (doi:10.1002/cbic.200900539).
75. Matsuura K. 2012 Construction of spherical virusinspired peptide nanoassemblies. Polym. J. 44, 469-474. (doi:10.1038/pj.2012.16).
76. Hartgerink JD, Granja JR, Milligan RA, Ghadiri MR. 1996 Self-assembling peptide nanotubes. J. Am. Chem. Soc. 118, 43-50. (doi:10.1021/ja953070s).
77. Gobeaux F et al. 2012 Structural role of counterions adsorbed on self-assembled peptide nanotubes. J. Am. Chem. Soc. 134, 723-733. (doi:10.1021/ja210299g).
78. Fernandez-Lopez S et al. 2001 Antibacterial agents based on the cyclic D, L-a-peptide architecture. Nature 412, 452-455. (doi:10.1038/35086601).
79. Montero A, Gastaminza P, Law M, Cheng G, Chisari FV, Ghadiri MR. 2011 Self-assembling peptide nanotubes with antiviral activity against hepatitis C virus. Chem. Biol. 18, 1453-1462. (doi:10.1016/j. chembiol.2011.08.017).
80. Ghadiri MR, Granja JR, Buehler LK. 1994 Artificial transmembrane ion channels from self-assembling peptide nanotubes. Nature 369, 301-304. (doi:10. 1038/369301a0).
81. Hourani R, Zhang C, van der Weegen R, Ruiz L, Li C, Keten S, Helms BA, Xu T. 2011 Processable cyclic peptide nanotubes with tunable interiors. J. Am. Chem. Soc. 133, 15 296-15 299. (doi:10.1021/ja2063082).
82. Madine J, Davies HA, Shaw C, Hamley IW, Middleton DA. 2012 Fibrils and nanotubes assembled from a modified amyloid-b peptide fragment differ in the packing of the same b-sheet building blocks. Chem. Commun. 48, 2976-2978. (doi:10.1039/c2cc17118j).
83. Zhang S, Holmes T, Lockshin C, Rich A. 1993 Spontaneous assembly of a self-complementary oligopeptide to form a stable macroscopic membrane. Proc. Natl Acad. Sci. USA 90, 3334-3338. (doi:10.1073/pnas.90.8.3334).
84. Rudra JS, Sun T, Bird KC, Daniels MD, Gasiorowski JZ, Chong AS, Collier JH. 2012 Modulating adaptive immune responses to peptide self-assemblies. ACS Nano 6, 1557-1564. (doi:10.1021/nn204530r).
85. Pimentel TA, Yan Z, Jeffers SA, Holmes KV, Hodges RS, Burkhard P. 2009 Peptide nanoparticles as novel immunogens: design and analysis of a prototypic severe acute respiratory syndrome vaccine. Chem. Biol. Drug Des. 73, 53-61. (doi:10.1111/j.1747- 0285.2008.00746.x).
86. Kaba SA, Brando C, Guo Q, Mittelholzer C, Raman S, Tropel D, Aebi U, Burkhard P, Lanar DE. 2009 A nonadjuvanted polypeptide nanoparticle vaccine confers long-lasting protection against rodent malaria. J. Immunol. 183, 7268-7277. (doi:10. 4049/jimmunol.0901957).
87. Babapoor S, Neef T, Mittelholzer C, Girshick T, Garmendia A, Shang H, Khan MI, Burkhard P. 2011 A novel vaccine using nanoparticle platform to present immunogenic M2e against avian influenza infection. Influenza Res. Treat. 2011, 1-12. (doi:10. 1155/2011/126794).
88. Schroeder U et al. 2009 Peptide nanoparticles serve as a powerful platform for the immunogenic display of poorly antigenic actin determinants. J. Mol. Biol. 386, 1368-1381. (doi:10.1016/j.jmb. 2008.11.023).
89. Wahome N, Pfeiffer T, Ambiel I, Yang Y, Keppler OT, Bosch V, Burkhard P. 2012 Conformation-specific display of 4E10 and 2F5 epitopes on selfassembling protein nanoparticles as a potential HIV vaccine. Chem. Biol. Drug Des. 80, 349-357. (doi:10.1111/j.1747-0285.2012.01423.x).
90. Burkhard P, Stetefeld J, Strelkov SV. 2001 Coiled coils: a highly versatile protein folding motif. Trends Cell Biol. 11, 82-88. (doi:10.1016/S0962- 8924(00)01898-5).
91. Pandya MJ, Spooner GM, Sunde M, Thorpe JR, Rodger A, Woolfson DN. 2000 Sticky-end assembly of a designed peptide fiber provides insight into protein fibrillogenesis. Biochemistry 39, 8728-8734. (doi:10.1021/bi000246g).
92. Papapostolou D, Smith AM, Atkins ED, Oliver SJ, Ryadnov MG, Serpell LC, Woolfson DN. 2007 Engineering nanoscale order into a designed protein fiber. Proc. Natl Acad. Sci. USA 104, 10 853-10 858. (doi:10.1073/pnas.0700801104).
93. Banwell EF et al. 2009 Rational design and application of responsive a-helical peptide hydrogels. Nat. Mater. 8, 596-600. (doi:10.1038/nmat2479).
94. Ferstl M, Strasser A, Wittmann HJ, Drechsler M, Rischer M, Engel J, Goepferich A. 2011 Nanofibers resulting from cooperative electrostatic and hydrophobic interactions between peptides and polyelectrolytes of opposite charge. Langmuir 27, 14 450-14 459. (doi:10.1021/la202252m).
95. Luo J, Tong YW. 2011 Self-assembly of collagenmimetic peptide amphiphiles into biofunctional nanofiber. ACS Nano 5, 7739-7747. (doi:10.1021/nn202822f ).
96. Ghosh A, Haverick M, Stump K, Yang X, Tweedle MF, Goldberger JE. 2012 Fine-tuning the pH trigger of self-assembly. J. Am. Chem. Soc. 134, 3647-3650. (doi:10.1021/ja211113n).
97. Khadka DB, Haynie DT. 2012 Protein- and peptidebased electrospun nanofibers in medical biomaterials. Nanomed. Nanotechnol. Biol. Med. 8, 1242-1262. (doi:10.1016/j.nano.2012.02.013).
98. Boato F, Thomas RM, Ghasparian A, Freund-Renard A, Moehle K, Robinson JA. 2007 Synthetic virus-like particles from self-assembling coiled-coil lipopeptides and their use in antigen display to the immune system. Angew. Chem. Int. Ed. Engl. 46, 9015-9018. (doi:10.1002/anie.200702805).
99. Raman S, Machaidze G, Lustig A, Aebi U, Burkhard P. 2006 Structure-based design of peptides that self-assemble into regular polyhedral nanoparticles. Nanomed. Nanotechnol. Biol. Med. 2, 95-102. (doi:10.1016/j.nano.2006.04.007).
100. Raman S, Machaidze G, Lustig A, Olivieri V, Aebi U, Burkhard P. 2009 Design of peptide nanoparticles using simple protein oligomerization domains. Open Nanomed. J. 2, 15-26. (doi:10.2174/1875933500902010015).
101. Petros RA, DeSimone JM. 2010 Strategies in the design of nanoparticles for therapeutic applications. Nat. Rev. Drug Disc. 9, 615-627. (doi:10.1038/nrd2591).
102. Ashley CE et al. 2011 Cell-specific delivery of diverse cargos by bacteriophage MS2 virus-like particles. ACS Nano 5, 5729-5745. (doi:10.1021/nn201397z).
103. Smith AE, Lilie H, Helenius A. 2003 Gangliosidedependent cell attachment and endocytosis of murine polyomavirus-like particles. FEBS Lett. 555, 199-203. (doi:10.1016/S0014-5793(03)01220-1).
104. Caruso M, Belloni L, Sthandier O, Amati P, Garcia MI. 2003 a4b1 integrin acts as a cell receptor for murine polyomavirus at the postattachment level. J. Virol. 77, 3913-3921. (doi:10.1128/JVI.77.7. 3913-3921.2003).
105. Destito G, Yeh R, Rae CS, Finn MG, Manchester M. 2007 Folic acid-mediated targeting of cowpea mosaic virus particles to tumor cells. Chem. Biol. 14, 1152-1162. (doi:10.1016/j.chembiol.2007.08.015).
106. Kitai Y, Fukuda H, Enomoto T, Asakawa Y, Suzuki T, Inouye S, Handa H. 2011 Cell selective targeting of a simian virus 40 virus-like particle conjugated to epidermal growth factor. J. Biotechnol. 155, 251-256. (doi:10.1016/j.jbiotec.2011.06.030).
107. Xiao Z et al. 2012 Engineering of targeted nanoparticles for cancer therapy using internalizing aptamers isolated by cell-uptake selection. ACS Nano 6, 696-704. (doi:10.1021/nn204165v).
108. Kar UK, Srivastava MK, Andersson A, Baratelli F, Huang M, Kickhoefer VA, Dubinett SM, Rome LH, Sharma S. 2011 Novel CCL21-vault nanocapsule intratumoral delivery inhibits lung cancer growth. PLoS ONE 6, e18758. (doi:10.1371/journal. pone.0018758).
109. Lee S, Saito K, Lee HR, Lee MJ, Shibasaki Y, Oishi Y, Kim BS. 2012 Hyperbranched double hydrophilic block copolymer micelles of poly(ethylene oxide) and polyglycerol for pH-responsive drug delivery. Biomacromolecules 13, 1190-1196. (doi:10. 1021/bm300151m).
110. Song N, Liu W, Tu Q, Liu R, Zhang Y, Wang J. 2011 Preparation and in vitro properties of redoxresponsive polymeric nanoparticles for paclitaxel delivery. Colloids Surf. B 87, 454-463. (doi:10. 1016/j.colsurfb.2011.06.009).
111. Tong R, Hemmati HD, Langer R, Kohane DS. 2012 Photoswitchable nanoparticles for triggered tissue penetration and drug delivery. J. Am. Chem. Soc. 134, 8848-8855. (doi:10.1021/ja211888a).
112. Wong C et al. 2011 Multistage nanoparticle delivery system for deep penetration into tumor tissue. Proc. Natl Acad. Sci. USA 108, 2426-2431. (doi:10.1073/pnas.1018382108).
113. Jain RK, Stylianopoulos T. 2010 Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 7, 653-664. (doi:10.1038/nrclinonc.2010.139).
114. 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, 354-360. (doi:10.1038/nm1368).
115. Li K, Chen Y, Li S, Nguyen HG, Niu Z, You S, Mello CM, Lu X, Wang Q. 2010 Chemical modification of M13 bacteriophage and its application in cancer cell imaging. Bioconjug. Chem. 21, 1369-1377. (doi:10. 1021/bc900405q).
116. Gilbert L, Toivola J, Lehtomaki E, Donaldson L, Kapyla P, Vuento M, Oker-Blom C. 2004 Assembly of fluorescent chimeric virus-like particles of canine parvovirus in insect cells. Biochem. Biophys. Res. Commun. 313, 878-887. (doi:10.1016/j.bbrc.2003.11.176).
117. Dale BM, McNerney GP, Hubner W, Huser TR, Chen BK. 2011 Tracking and quantitation of fluorescent HIV during cell-to-cell transmission. Methods 53, 20-26. (doi:10.1016/j.ymeth.2010.06.018).
118. Medintz IL, Uyeda HT, Goldman ER, Mattoussi H. 2005 Quantum dot bioconjugates for imaging, labelling and sensing. Nat. Mater. 4, 435-446. (doi:10.1038/nmat1390).
119. Michalet X et al. 2005 Quantum dots for live cells, in vivo imaging, and diagnostics. Science 307, 538-544. (doi:10.1126/science.1104274).
120. Rieger J, Freichels H, Imberty A, Putaux JL, Delair T, Jerome C, Auzely-Velty R. 2009 Polyester nanoparticles presenting mannose residues: toward the development of new vaccine delivery systems combining biodegradability and targeting properties. Biomacromolecules 10, 651-657. (doi:10.1021/bm801492c).
121. Watson DS, Endsley AN, Huang L. 2012 Design considerations for liposomal vaccines: influence of formulation parameters on antibody and cellmediated immune responses to liposome associated antigens. Vaccine 30, 2256-2272. (doi:10.1016/j. vaccine.2012.01.070).
122. Laddy DJ, Weiner DB. 2006 From plasmids to protection: a review of DNA vaccines against infectious diseases. Int. Rev. Immunol. 25, 99-123. (doi:10.1080/08830180600785827).
123. Kar UK et al. 2012 Vault nanocapsules as adjuvants favor cell-mediated over antibody-mediated immune responses following immunization of mice. PLoS ONE 7, e38553. (doi:10.1371/journal. pone.0038553).
124. Jennings GT, Bachmann MF. 2009 Immunodrugs: therapeutic VLP-based vaccines for chronic diseases. Annu. Rev. Pharmacol. Toxicol. 49, 303- 326. (doi:10.1146/annurev-pharmtox-061008- 103129).
125. Ambuhl PM et al. 2007 A vaccine for hypertension based on virus-like particles: preclinical efficacy and phase I safety and immunogenicity. J. Hypertens. 25, 63-72. (doi:10.1097/HJH.0b013e32800ff5d6).
126. Yang Y, Ringler P, Muller SA, Burkhard P. 2012 Optimizing the refolding conditions of selfassembling polypeptide nanoparticles that serve as repetitive antigen display systems. J. Struct. Biol. 177, 168-176. (doi:10.1016/j.jsb.2011. 11.011).