Nanoparticulate architecture of protein-based artificial viruses is supported by protein-DNA interactions

Nanomedicine

Volumn 6, Issue 6, 2011, Pages 1047-1061

  Domingo Espín, Joan ^a,b   Vazquez, Esther ^a,b   Ganz, Javier ^c,d   Conchillo, Oscar ^a   García Fruitós, Elena ^a,b   Cedano, Juan ^a   Unzueta, Ugutz ^a,b   Petegnief, Valérie ^e   Gonzalez Montalbán, Nuria ^a,b   Planas, Anna M ^e   Daura, Xavier ^a,f   Peluffo, Hugo ^c,d   Ferrer Miralles, Neus ^a,b   Villaverde, Antonio ^a,b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^c INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^d DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^e INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^f INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

DNA protein interaction; gene therapy; innovative medicine; nanomedicine; protein engineering; protein nanoparticl

Indexed keywords

ARGININE; ASPARTIC ACID; CHIMERIC PROTEIN; CORE PROTEIN; DNA; GLYCINE; NANOPARTICLE; PEPTIDE; VIRUS VECTOR;

ALPHA HELIX; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE THERAPY; MAMMAL CELL; NANOANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN STRUCTURE; RAT; TRANSGENE;

ANIMALS; CELLS, CULTURED; CIRCULAR DICHROISM; DNA; GENE THERAPY; MASS SPECTROMETRY; MICROSCOPY, ELECTRON, TRANSMISSION; PEPTIDES; PROTEIN BINDING; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80052281139     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.11.28     Document Type: Article

References (64)

1. Smaglik P. Clinical trials end at gene-therapy institute. Nature 405(6786), 497 (2000).
2. Edelstein ML, Abedi MR, Wixon J. Gene therapy clinical trials worldwide to 2007 an update. J. Gene Med. 9(10), 833-842 (2007).
3. Marshall E. Gene therapy. Second child in French trial is found to have leukemia. Science 299(5605), 320 (2003).
4. Marshall E. Gene therapy. What to do when clear success comes with an unclear risk? Science 298(5593), 510-511 (2002).
5. Smaglik P. Tighter watch urged on adenoviral vectors with proposal to report all 'adverse events'. Nature 402(6763), 707 (1999).
6. Douglas KL. Toward development of artificial viruses for gene therapy: A comparative evaluation of viral and non-viral transfection. Biotechnol. Prog. 24(4), 871-883 (2008).
7. Mastrobattista E, van der Aa MA, Hennink WE, Crommelin DJ. Artificial viruses: A nanotechnological approach to gene delivery. Nat. Rev. Drug Discov. 5(2), 115-121 (2006). nn The basic principles of artificial virus design and construction are reviewed, describing the diversity of structural approaches and chemical composition of the building blocks.
8. Wagner E. Strategies to improve DNA polyplexes for in vivo gene transfer: Will "artificial viruses" be the answer? Pharm. Res. 21(1), 8-14 (2004).
9. Maham A, Tang Z, Wu H, Wang J, Lin Y. Protein-based nanomedicine platforms for drug delivery. Small 5(15), 1706-1721 (2009). n The spectrum of self-assembling protein materials with potential as platforms for drug delivery is extensively reviewed.
10. Petry H, Goldmann C, Ast O, Luke W. The use of virus-like particles for gene transfer. Curr. Opin. Mol. Ther. 5(5), 524-528 (2003).
11. Wu M, Sherwin T, Brown WL, Stockley PG. Delivery of antisense oligonucleotides to leukemia cells by RNA bacteriophage capsids. Nanomedicine (Lond.) 1(1), 67-76 (2005).
12. Aris A, Villaverde A. Modular protein engineering for non-viral gene therapy. Trends Biotechnol. 22(7), 371-377 (2004).
13. Vazquez E, Ferrer-Miralles N, Villaverde A. Peptide-assisted traffic engineering for nonviral gene therapy. Drug Discov. Today 13(23-24), 1067-1074 (2008).
14. Ferrer-Miralles N, Vazquez E, Villaverde A. Membrane-active peptides for non-viral gene therapy: Making the safest easier. Trends Biotechnol. 26(5), 267-275 (2008).
15. Vazquez E, Roldán M, Diez-Gil C et al. Protein nanodisk assembling and intracellular trafficking powered by an arginine-rich (R9) peptide. Nanomedicine (Lond.) 5, 259-268 (2010).
16. Vazquez E, Cubarsi R, Unzueta U et al. Internalization and kinetics of nuclear migration of protein-only, arginine-rich nanoparticles. Biomaterials 31(35), 9333-9339 (2010). nn The internalization pattern and nuclear migration routes of a self-assembling, protein-only nanoparticle based on arginine-rich peptides are finely dissected.
17. Xavier J, Singh S, Dean DA, Rao NM, Gopal V. Designed multi-domain protein as a carrier of nucleic acids into cells. J. Control Release 133(2), 154-160 (2009). n The potential of a protein-only, Tat-derived modular construct for gene therapy is clearly shown through elegant experiments.
18. Peluffo H, Acarin L, Aris A et al. Neuroprotection from NMDA excitotoxic lesion by Cu/Zn superoxide dismutase gene delivery to the postnatal rat brain by a modular protein vector. BMC Neurosci. 7, 35 (2006).
19. Peluffo H, Aris A, Acarin L, Gonzalez B, Villaverde A, Castellano B. Nonviral gene delivery to the central nervous system based on a novel integrin-targeting multifunctional protein. Hum. Gene Ther. 14(13), 1215-1223 (2003).
20. Benito A, Mateu MG, Villaverde A. Improved mimicry of a foot-and-mouth disease virus antigenic site by a viral peptide displayed on b-galactosidase surface. Biotechnol. NY 13(8), 801-804 (1995).
21. Feliu JX, Benito A, Oliva B, Aviles FX, Villaverde A. Conformational flexibility in a highly mobile protein loop of foot-and-mouth disease virus: Distinct structural requirements for integrin and antibody binding. J. Mol. Biol. 283(2), 331-338 (1998).
22. Villaverde A, Feliu JX, Harbottle RP, Benito A, Coutelle C. A recombinant, arginine-glycine-aspartic acid (RGD)
23. Feliu JX, Benito A, Oliva B, Aviles FX, Villaverde A. Conformational flexibility in a highly mobile protein loop of foot-and-mouth disease virus: Distinct structural requirements for integrin and antibody binding. J. Mol. Biol. 283(2), 331-338 (1998).
24. Villaverde A, Feliu JX, Harbottle RP, Benito A, Coutelle C. A recombinant, arginine-glycine-aspartic acid (RGD) binding and condensing properties of adenoviral core peptide μ. Biochemistry 41(2), 652-659 (2002).
25. Yoneda Y. How proteins are transported from cytoplasm to the nucleus. J. Biochem. 121(5), 811-817 (1997).
26. Collins E, Birchall JC, Williams JL, Gumbleton M. Nuclear localisation and pDNA condensation in non-viral gene delivery. J. Gene Med. 9(4), 265-274 (2007).
27. Saccardo P, Villaverde A, Gonzalez-Montalban N. Peptide-mediated DNA condensation for non-viral gene therapy. Biotechnol. Adv. 27(4), 432-438 (2009).
28. Block H, Maertens B, Spriestersbach A et al. Immobilized-metal affinity chromatography (IMAC): A review. Methods Enzymol. 463, 439-473 (2009).
29. Garcia-Fruitos E, Seras-Franzoso J, Vazquez E, Villaverde A. Tunable geometry of bacterial inclusion bodies as substrate materials for tissue engineering. Nanotechnology 21(20), 205101 (2010).
30. Eswar N, Marti-Renom MA, Webb B et al. Comparative protein structure modeling with MODELLER. John Wiley & Sons, Inc., NJ, USA (Suppl. 15), 5.6.1-5.6.30 (2009).
31. Fontes MR, Teh T, Toth G et al. Role of flanking sequences and phosphorylation in the recognition of the simian-virus-40 large T-antigen nuclear localization sequences by importin-a. Biochem. J. 375(Pt 2), 339-349 (2003).
32. Hewat EA, Verdaguer N, Fita I et al. Structure of the complex of an Fab fragment of a neutralizing antibody with foot-and-mouth disease virus: Positioning of a highly mobile antigenic loop. EMBO J. 16(7), 1492-1500 (1997).
33. Davidson B, Fasman GD. The conformational transitions of uncharged poly-l-lysine. a helix-random coil-b structure. Biochemistry 6(6), 1616-1629 (1967).
34. Pakhomova ON, Deep S, Huang Q, Zwieb C, Hinck AP: Solution structure of protein SRP19 of Archaeoglobus fulgidus signal recognition particle. J. Mol. Biol. 317(1), 145-158 (2002).
35. Chen J, Lee KH, Steinhauer DA, Stevens DJ, Skehel JJ, Wiley DC. Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 95(3), 409-417 (1998).
36. Petegnief V, Friguls B, Sanfeliu C, Sunol C, Planas AM. Transforming growth factor-a attenuates N-methyl-d-aspartic acid toxicity in cortical cultures by preventing protein synthesis inhibition through an Erk1/2-dependent mechanism. J. Biol. Chem. 278(32), 29552-29559 (2003).
37. Garcia-Fruitos E, Rodriguez-Carmona E, Diez-Gil C et al. Surface cell growth engineering assisted by a novel bacterial nanomaterial. Adv. Mater. 21(42), 4249-4253 (2009).
38. de Marco A , Schroedel A. Characterization of the aggregates formed during recombinant protein expression in bacteria. BMC Biochem. 6(1), 10 (2005).
39. Martinez-Alonso M, Gonzalez-Montalban N, Garcia-Fruitos E, Villaverde A. The functional quality of soluble recombinant polypeptides produced in Escherichia coli is defined by a wide conformational spectrum. Appl. Environ. Microbiol. 101(6), 1353-1358 (2008).
40. Doglia SM, Ami D, Natalello A, Gatti-Lafranconi P, Lotti M. Fourier transform infrared spectroscopy analysis of the conformational quality of recombinant proteins within inclusion bodies. Biotechnol. J. 3(2), 193-201 (2008).
41. Gonzalez-Montalban N, Natalello A, Garcia-Fruitos E, Villaverde A, Doglia SM. In situ protein folding and activation in bacterial inclusion bodies. Biotechnol. Bioeng. 100(4), 797-802 (2008).
42. Ami D, Natalello A, Taylor G, Tonon G, Maria DS. Structural analysis of protein inclusion bodies by Fourier transform infrared microspectroscopy. Biochim. Biophys. Acta 1764(4), 793-799 (2006).
43. Wang L, Maji SK, Sawaya MR, Eisenberg D, Riek R. Bacterial inclusion bodies contain amyloid-like structure. PLoS Biol. 6(8), e195 (2008).
44. Carrio M, Gonzalez-Montalban N, Vera A, Villaverde A, Ventura S. Amyloid-like properties of bacterial inclusion bodies. J. Mol. Biol. 347(5), 1025-1037 (2005).
45. Natalello A, Ami D, Brocca S, Lotti M, Doglia SM. Secondary structure, conformational stability and glycosylation of a recombinant Candida rugosa lipase studied by Fourier-transform infrared spectroscopy. Biochem. J. 385(Pt 2), 511-517 (2005).
46. Greenfield NJ. Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nat. Protoc. 1(6), 2527-2535 (2006).
47. Jiang W, Kim BY, Rutka JT, Chan WC. Nanoparticle-mediated cellular response is size-dependent. Nat. Nanotechnol. 3(3), 145-150 (2008). nn The size effect of nanoparticles on the mammalian cell biology is demonstrated in biological interfaces.
48. Chithrani BD, Ghazani AA, Chan WC. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 6(4), 662-668 (2006).
49. Jiang W, Kim BY, Rutka JT, Chan WC. Advances and challenges of nanotechnology-based drug delivery systems. Expert. Opin. Drug Deliv. 4(6), 621-633 (2007).
50. Corchero JL , Villaverde A. Biomedical applications of distally controlled magnetic nanoparticles. Trends Biotechnol. 27(8), 468-476 (2009).
51. Vazquez E, Ferrer-Miralles N, Mangues R, Corchero JL, Schwartz S Jr, Villaverde A. Modular protein engineering in emerging cancer therapies. Curr. Pharm. Des 15(8), 893-916 (2009).
52. Ferrer-Miralles N, Domingo-Espin J, Corchero JL, Vazquez E, Villaverde A. Microbial factories for recombinant pharmaceuticals. Microb. Cell Fact. 8(1), 17 (2009).
53. Rodriguez-Carmona E, Villaverde A. Nanostructured bacterial materials for innovative medicines. Trends Microbiol. 18(9), 423-430 (2010).
54. Uchida M, Klem MT, Allen M et al. Biological containers: Protein cages as multifunctional nanoplatforms. Adv. Mater. 19, 1025-1042 (2007).
55. Aris A, Feliu JX, Knight A, Coutelle C, Villaverde A. Exploiting viral cell-targeting abilities in a single polypeptide, non-infectious, recombinant vehicle for integrin-mediated DNA delivery and gene expression. Biotechnol Bioeng 68(6), 689-696 (2000).
56. Aris A , Villaverde A. Engineering nuclear localization signals in modular protein vehicles for gene therapy. Biochem. Biophys. Res. Commun. 304(4), 625-631 (2003).
57. Jacobson RH, Zhang XJ, DuBose RF, Matthews BW. Three-dimensional structure of b-galactosidase from E. coli. Nature 369(6483), 761-766 (1994).
58. Aris A, Villaverde A. Molecular organization of protein-DNA complexes for cell-targeted DNA delivery. Biochem. Biophys. Res. Commun. 278(2), 455-461 (2000).
59. Peluffo H, Gonzalez P, Aris A et al. RGD domains neuroprotect the immature brain by a glial-dependent mechanism. Ann. Neurol. 62(3), 251-261 (2007).
60. Tagawa T, Manvell M, Brown N et al. Characterisation of LMD virus-like nanoparticles self-assembled from cationic liposomes, adenovirus core peptide mu and plasmid DNA. Gene Ther. 9(9), 564-576 (2002).
61. Keller M, Tagawa T, Preuss M, Miller AD. Biophysical characterization of the DNA
62. Midoux P, LeCam E, Coulaud D, Delain E, Pichon C. Histidine containing peptides and polypeptides as nucleic acid vectors. Somat. Cell Mol. Genet. 27(1-6), 27-47 (2002).
63. Ramsay E, Hadgraft J, Birchall J, Gumbleton M. Examination of the biophysical interaction between plasmid DNA and the polycations, polylysine and polyornithine, as a basis for their differential gene transfection in-vitro. Int. J. Pharm. 210(1-2), 97-107 (2000).
64. Tecle M, Preuss M, Miller AD. Kinetic study of DNA condensation by cationic peptides used in nonviral gene therapy: Analogy of DNA condensation to protein folding. Biochemistry 42(35), 10343-10347 (2003). n The states of DNA condensation during interaction with cationic peptides have been analyzed, revealing the obstacles posed to DNA transcription at high peptide-DNA ratios.