Incorporation of Naked Peptide Nucleic Acids into Liposomes Leads to Fast and Efficient Delivery

Bioconjugate Chemistry

Volumn 26, Issue 8, 2015, Pages 1533-1541

  Avitabile, Concetta ^a   Accardo, Antonella ^b,c   Ringhieri, Paola ^b   Morelli, Giancarlo ^b,c   Saviano, Michele ^c,d   Montagner, Giulia ^e   Fabbri, Enrica ^e   Gallerani, Eleonora ^e   Gambari, Roberto ^e   Romanelli, Alessandra ^b,c  

^a CNR   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c Interuniversity Research Centre on Bioactive Peptides   (Italy)

^d CNR   (Italy)

^e UNIVERSITY OF FERRARA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDES; RNA;

CELL-BE; CELL/B.E; CELL/BE; DELIVERY SYSTEMS; DOWN-REGULATION; FLUORESCENT PEPTIDES; K562 CELLS; LIPOSOMAL FORMULATION; NUCLEIC ACID OLIGOMERS; PEPTIDE NUCLEIC ACID;

LIPOSOMES;

CHOLESTEROL; LIPOSOME; MACROGOL 2000; MICRORNA 210; OLIGOMER; PEPTIDE NUCLEIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; 1,2-DISTEAROYL-SN-GLYCERO-3-PHOSPHOETHANOLAMINE-N-METHOXY-POLY(ETHYLENE GLYCOL 2000); ANTISENSE OLIGONUCLEOTIDE; MACROGOL DERIVATIVE; MICRORNA; MIRN210 MICRORNA, HUMAN;

ARTICLE; CELL GROWTH; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG FORMULATION; FLUORESCENCE; HUMAN; HUMAN CELL; K562 CELL LINE; NANOENCAPSULATION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS;

DOWN-REGULATION; DRUG DELIVERY SYSTEMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; K562 CELLS; LIPOSOMES; MICRORNAS; OLIGONUCLEOTIDES, ANTISENSE; PEPTIDE NUCLEIC ACIDS; PHOSPHATIDYLETHANOLAMINES; POLYETHYLENE GLYCOLS;

EID: 84939805602     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/acs.bioconjchem.5b00156     Document Type: Article

References (45)

1. Avitabile, C., Cimmino, A., and Romanelli, A. (2014) Oligonucleotide Analogues as Modulators of the Expression and Function of Noncoding RNAs (ncRNAs): Emerging Therapeutics Applications J. Med. Chem. 57, 10220-40 10.1021/jm5006594
2. Nielsen, P. E., Egholm, M., Berg, R. H., and Buchardt, O. (1991) Sequence-selective recognition of DNA by strand displacement with a thymine-substituted polyamide Science 254, 1497-500 10.1126/science.1962210
3. Egholm, M., Buchardt, O., Christensen, L., Behrens, C., Freier, S. M., Driver, D. A., Berg, R. H., Kim, S. K., Norden, B., and Nielsen, P. E. (1993) PNA hybridizes to complementary oligonucleotides obeying the Watson-Crick hydrogen-bonding rules Nature 365, 566-8 10.1038/365566a0
4. Nielsen, P. E. (2010) Gene targeting and expression modulation by peptide nucleic acids (PNA) Curr. Pharm. Des. 16, 3118-23 10.2174/138161210793292546
5. Borgatti, M., Lampronti, I., Romanelli, A., Pedone, C., Saviano, M., Bianchi, N., Mischiati, C., and Gambari, R. (2003) Transcription factor decoy molecules based on a peptide nucleic acid (PNA)-DNA chimera mimicking Sp1 binding sites J. Biol. Chem. 278, 7500-9 10.1074/jbc.M206780200
6. Gambari, R., Fabbri, E., Borgatti, M., Lampronti, I., Finotti, A., Brognara, E., Bianchi, N., Manicardi, A., Marchelli, R., and Corradini, R. (2011) Targeting microRNAs involved in human diseases: a novel approach for modification of gene expression and drug development Biochem. Pharmacol. 82, 1416-29 10.1016/j.bcp.2011.08.007
7. Gambari, R. (2014) Peptide nucleic acids: a review on recent patents and technology transfer Expert Opin. Ther. Pat. 24, 267-94 10.1517/13543776.2014.863874
8. Piva, R., Spandidos, D. A., and Gambari, R. (2013) From microRNA functions to microRNA therapeutics: novel targets and novel drugs in breast cancer research and treatment (Review) Int. J. Oncol. 43, 985-94
9. Pensato, S., Saviano, M., and Romanelli, A. (2007) New peptide nucleic acid analogues: synthesis and applications Expert Opin. Biol. Ther. 7, 1219-32 10.1517/14712598.7.8.1219
10. Roviello, G. N., Musumeci, D., Bucci, E. M., and Pedone, C. (2012) Synthesis of a diaminopropanoic acid-based nucleoamino acid and assembly of cationic nucleopeptides for biomedical applications Amino Acids 43, 2537-43 10.1007/s00726-012-1335-6
11. Roviello, G. N., Musumeci, D., D'Alessandro, C., and Pedone, C. (2013) Synthesis of a thymine-functionalized nucleoamino acid for the solid phase assembly of cationic nucleopeptides Amino Acids 45, 779-84 10.1007/s00726-013-1520-2
12. Dragulescu-Andrasi, A., Zhou, P., He, G., and Ly, D. H. (2005) Cell-permeable GPNA with appropriate backbone stereochemistry and spacing binds sequence-specifically to RNA Chem. Commun. (Cambridge, U. K.) 244-6 10.1039/b412522c
13. Dragulescu-Andrasi, A., Rapireddy, S., He, G., Bhattacharya, B., Hyldig-Nielsen, J. J., Zon, G., and Ly, D. H. (2006) Cell-permeable peptide nucleic acid designed to bind to the 5′-untranslated region of E-cadherin transcript induces potent and sequence-specific antisense effects J. Am. Chem. Soc. 128, 16104-12 10.1021/ja063383v
14. Shiraishi, T., Hamzavi, R., and Nielsen, P. E. (2008) Subnanomolar antisense activity of phosphonate-peptide nucleic acid (PNA) conjugates delivered by cationic lipids to HeLa cells Nucleic Acids Res. 36, 4424-32 10.1093/nar/gkn401
15. Capparelli, R., De Chiara, F., Nocerino, N., Montella, R. C., Iannaccone, M., Fulgione, A., Romanelli, A., Avitabile, C., Blaiotta, G., and Capuano, F. (2012) New perspectives for natural antimicrobial peptides: application as antinflammatory drugs in a murine model BMC Immunol. 13, 61 10.1186/1471-2172-13-61
16. de Koning, M. C., van der Marel, G. A., and Overhand, M. (2003) Synthetic developments towards PNA-peptide conjugates Curr. Opin. Chem. Biol. 7, 734-40 10.1016/j.cbpa.2003.10.006
17. Cheng, C. J., Bahal, R., Babar, I. A., Pincus, Z., Barrera, F., Liu, C., Svoronos, A., Braddock, D. T., Glazer, P. M., and Engelman et al. 2014, MicroRNA silencing for cancer therapy targeted to the tumour microenvironment Nature 518, 107-10 10.1038/nature13905
18. Ma, X., Devi, G., Qu, Q., Toh, D. F., Chen, G., and Zhao, Y. (2014) Intracellular delivery of antisense peptide nucleic acid by fluorescent mesoporous silica nanoparticles Bioconjugate Chem. 25, 1412-20 10.1021/bc5002714
19. McNeer, N. A., Schleifman, E. B., Cuthbert, A., Brehm, M., Jackson, A., Cheng, C., Anandalingam, K., Kumar, P., Shultz, L. D., and Greiner, D. L. et al. 2013, Systemic delivery of triplex-forming PNA and donor DNA by nanoparticles mediates site-specific genome editing of human hematopoietic cells in vivo Gene Ther. 20, 658-69 10.1038/gt.2012.82
20. Immordino, M. L., Dosio, F., and Cattel, L. (2006) Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential Int. J. Nanomedicine 1, 297-315
21. Janowski, B. A., Kaihatsu, K., Huffman, K. E., Schwartz, J. C., Ram, R., Hardy, D., Mendelson, C. R., and Corey, D. R. (2005) Inhibiting transcription of chromosomal DNA with antigene peptide nucleic acids Nat. Chem. Biol. 1, 210-5 10.1038/nchembio724
22. Borgatti, M., Breda, L., Cortesi, R., Nastruzzi, C., Romanelli, A., Saviano, M., Bianchi, N., Mischiati, C., Pedone, C., and Gambari, R. (2002) Cationic liposomes as delivery systems for double-stranded PNA-DNA chimeras exhibiting decoy activity against NF-kappaB transcription factors Biochem. Pharmacol. 64, 609-16 10.1016/S0006-2952(02)01188-7
23. Nastruzzi, C., Cortesi, R., Esposito, E., Gambari, R., Borgatti, M., Bianchi, N., Feriotto, G., and Mischiati, C. (2000) Liposomes as carriers for DNA-PNA hybrids J. Controlled Release 68, 237-49 10.1016/S0168-3659(00)00273-X
24. Manicardi, A., Fabbri, E., Tedeschi, T., Sforza, S., Bianchi, N., Brognara, E., Gambari, R., Marchelli, R., and Corradini, R. (2012) Cellular uptakes, biostabilities and anti-miR-210 activities of chiral arginine-PNAs in leukaemic K562 cells ChemBioChem 13, 1327-37 10.1002/cbic.201100745
25. Brognara, E., Fabbri, E., Bazzoli, E., Montagner, G., Ghimenton, C., Eccher, A., Cantu, C., Manicardi, A., Bianchi, N., and Finotti, A. et al. 2014, Uptake by human glioma cell lines and biological effects of a peptide-nucleic acids targeting miR-221 J. Neuro-Oncol. 118, 19-28 10.1007/s11060-014-1405-6
26. Fabbri, E., Manicardi, A., Tedeschi, T., Sforza, S., Bianchi, N., Brognara, E., Finotti, A., Breveglieri, G., Borgatti, M., and Corradini, R. et al. 2011, Modulation of the biological activity of microRNA-210 with peptide nucleic acids (PNAs) ChemMedChem 6, 2192-202 10.1002/cmdc.201100270
27. Bianchi, N., Finotti, A., Ferracin, M., Lampronti, I., Zuccato, C., Breveglieri, G., Brognara, E., Fabbri, E., Borgatti, M., Negrini, M., and Gambari, R. (2015) Increase of microRNA-210, decrease of raptor gene expression and alteration of mammalian target of rapamycin regulated proteins following mithramycin treatment of human erythroid cells PLoS One 10, e0121567 10.1371/journal.pone.0121567
28. Riche, E. L., Erickson, B. W., and Cho, M. J. (2004) Novel long-circulating liposomes containing peptide library-lipid conjugates: synthesis and in vivo behavior J. Drug Target 12, 355-61 10.1080/10611860412331285279
29. Ducat, E., Brion, M., Lecomte, F., Evrard, B., and Piel, G. (2010) The experimental design as practical approach to develop and optimize a formulation of peptide-loaded liposomes AAPS PharmSciTech 11, 966-75 10.1208/s12249-010-9463-3
30. Lao, J., Madani, J., Puertolas, T., Alvarez, M., Hernandez, A., Pazo-Cid, R., Artal, A., and Anton Torres, A. (2013) Liposomal Doxorubicin in the treatment of breast cancer patients: a review J. Drug Delivery 2013, 1 10.1155/2013/456409
31. Martin, C., Low, W. L., Gupta, A., Amin, M. C. I. M., Radecka, I., Raj, P., Britland, S., and Kenward, K. (2014) Liposomal delivery of antimicrobial agents in advances in liposome research, Nova Science Publisher.
32. Bakandritsos, A., Fatourou, A. G., and Fatouros, D. G. (2012) Magnetoliposomes and their potential in the intelligent drug-delivery field Ther. Delivery 3, 1469-82 10.4155/tde.12.129
33. Accardo, A., Tesauro, D., Aloj, L., Pedone, C., and Morelli, G. (2009) Supramolecular aggregates containing lipophilic Gd(III) complexes as contrast agents in MRI Coord. Chem. Rev. 253, 2193-2213 10.1016/j.ccr.2009.01.015
34. Zhang, Y., Chan, H. F., and Leong, K. W. (2013) Advanced materials and processing for drug delivery: the past and the future Adv. Drug Delivery Rev. 65, 104-20 10.1016/j.addr.2012.10.003
35. Coderch, L., Fonollosa, J., De Pera, M., Estelrich, J., De La Maza, A., and Parra, J. L. (2000) Influence of cholesterol on liposome fluidity by EPR. Relationship with percutaneous absorption J. Controlled Release 68, 85-95 10.1016/S0168-3659(00)00240-6
36. Bianchi, N., Zuccato, C., Lampronti, I., Borgatti, M., and Gambari, R. (2009) Expression of miR-210 during erythroid differentiation and induction of gamma-globin gene expression BMB Rep 42, 493-9 10.5483/BMBRep.2009.42.8.493
37. Morrissey, D. V., Lockridge, J. A., Shaw, L., Blanchard, K., Jensen, K., Breen, W., Hartsough, K., Machemer, L., Radka, S., and Jadhav, V. et al. 2005, Potent and persistent in vivo anti-HBV activity of chemically modified siRNAs Nat. Biotechnol. 23, 1002-7 10.1038/nbt1122
38. Heyes, J., Palmer, L., Bremner, K., and MacLachlan, I. (2005) Cationic lipid saturation influences intracellular delivery of encapsulated nucleic acids J. Controlled Release 107, 276-87 10.1016/j.jconrel.2005.06.014
39. Avitabile, C., Fabbri, E., Bianchi, N., Gambari, R., and Romanelli, A. (2012) Inhibition of miRNA maturation by Peptide Nucleic Acids, in MiRNA maturation, Methods and Protocols (Arenz, C., Ed.) pp 157-164, Humana Press.
40. Avitabile, C., Saviano, M., D'Andrea, L., Bianchi, N., Fabbri, E., Brognara, E., Gambari, R., and Romanelli, A. (2012) Targeting pre-miRNA by peptide nucleic acids: a new strategy to interfere in the miRNA maturation Artif DNA PNA XNA 3, 88-96 10.4161/adna.20911
41. Uster, P. S., Allen, T. M., Daniel, B. E., Mendez, C. J., Newman, M. S., and Zhu, G. Z. (1996) Insertion of poly(ethylene glycol) derivatized phospholipid into pre-formed liposomes results in prolonged in vivo circulation time FEBS Lett. 386, 243-6 10.1016/0014-5793(96)00452-8
42. Brognara, E., Fabbri, E., Bianchi, N., Finotti, A., Corradini, R., and Gambari, R. (2014) Molecular methods for validation of the biological activity of peptide nucleic acids targeting microRNAs Methods Mol. Biol. 1095, 165-76 10.1007/978-1-62703-703-7-14
43. Franceschini, A., Capece, M., Chiozzi, P., Falzoni, S., Sanz, J. M., Sarti, A. C., Bonora, M., Pinton, P., and Di Virgilio, F. (2015) The P2 × 7 receptor directly interacts with the NLRP3 inflammasome scaffold protein FASEB J. 29, 2450-61 10.1096/fj.14-268714
44. Venco, P., Bonora, M., Giorgi, C., Papaleo, E., Iuso, A., Prokisch, H., Pinton, P., and Tiranti, V. (2015) Mutations of C19orf12, coding for a transmembrane glycine zipper containing mitochondrial protein, cause mis-localization of the protein, inability to respond to oxidative stress and increased mitochondrial Ca (2.) Front. Genet. 6, 185 10.3389/fgene.2015.00185
45. Brognara, E., Fabbri, E., Aimi, F., Manicardi, A., Bianchi, N., Finotti, A., Breveglieri, G., Borgatti, M., Corradini, R., and Marchelli, R. et al. 2012, Peptide nucleic acids targeting miR-221 modulate p27Kip1 expression in breast cancer MDA-MB-231 cells Int. J. Oncol. 41, 2119-27