miRNA therapeutics: Delivery and biological activity of peptide nucleic acids targeting miRNAs

Epigenomics

Volumn 3, Issue 6, 2011, Pages 733-745

  Fabbri, Enrica ^a   Brognara, Eleonora ^a   Borgatti, Monica ^a   Lampronti, Ilaria ^a   Finotti, Alessia ^a   Bianchi, Nicoletta ^a   Sforza, Stefano ^b   Tedeschi, Tullia ^b   Manicardi, Alex ^b   Marchelli, Rosangela ^b   Corradini, Roberto ^b   Gambari, Roberto ^a  

^a UNIVERSITY OF FERRARA   (Italy)

^b UNIVERSITY OF PARMA   (Italy)

Author keywords

epigenetics; gene regulation; gene transcription; miRNAs; peptide nucleic acids

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; PEPTIDE NUCLEIC ACID;

3' UNTRANSLATED REGION; APOPTOSIS; BINDING AFFINITY; BIOAVAILABILITY; BIOLOGICAL ACTIVITY; CELL CYCLE; CELL DIFFERENTIATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW;

DRUG DELIVERY SYSTEMS; DRUG DISCOVERY; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; MODELS, BIOLOGICAL; PEPTIDE NUCLEIC ACIDS;

EID: 82455186405     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.11.90     Document Type: Review

References (123)

1. Nielsen PE, Egholm M, Berg RH, Buchardt O. Sequence-selective recognition of DNA by strand displacement with a thymine-substituted polyamide. Science 254, 1497-1500 (1991).
2. Demidov VV, Frank-Kamenetskii MD. Sequence-specific targeting of duplex DNA by peptide nucleic acids via triplex strand invasion. Methods 23, 108-122 (2001).
3. Gambari R. Peptide-nucleic acids (PNAs).A tool for the development of gene expression modifiers. Curr. Pharm. Des. 7, 1839-1862 (2001).
4. Paulasova P, Pellestor F. The peptide nucleic acids (PNAs).A new generation of probes for genetic and cytogenetic analyses. Ann. Genet. 47, 349-358 (2004).
5. Nielsen PE. Targeting double stranded DNA with peptide nucleic acid (PNA).Curr. Med. Chem. 8, 545-550 (2001).
6. Good L, Nielsen PE. Progress in developing PNA as a gene-targeted drug. Antisense Nucleic Acid Drug Dev. 7, 431-437 (1997).
7. Marin VL, Roy S, Armitage BA. Recent advances in the development of peptide nucleic acid as a gene-targeted drug. Expert Opin. Biol. Ther. 4, 337-348 (2004).
8. Nielsen PE. Antisense peptide nucleic acids. Curr. Opin. Mol. Ther. 2, 282-287 (2002).
9. Soomets U, Hällbrink M, Langel U. Antisense properties of peptide nucleic acids. Front. Biosci. 4, D782-D786 (1999).
10. Ray A, Nordén B. Peptide nucleic acid (PNA): its medical and biotechnical applications and promise for the future. FASEB J. 14, 1041-1060 (2000).
11. Fabani MM, Gait MJ. miR 122 targeting with LNA/2' O-methyl oligonucleotide mixmers, peptide nucleic acids (PNA), and PNA-peptide conjugates. RNA 14, 336-346 (2008).
12. Fabani MM, Abreu-Goodger C, Williams D et al. Efficient inhibition of miR 155 function in vivo by peptide nucleic acids. Nucleic Acids Res. 38, 4466-4475 (2010).
13. Ivanova GD, Fabani MM, Arzumanov AA et al. PNA-peptide conjugates as intracellular gene control agents. Nucleic Acids Symp. Ser. (Oxford) 52, 31-32 (2008).
14. Torres AG, Fabani MM, Vigorito E, Gait MJ. MicroRNA fate upon targeting with anti-miRNA oligonucleotides as revealed by an improved northern-blot-based method for miRNA detection. RNA 17(5), 933-943 (2011).
15. Oh SY, Ju Y, Kim S, Park H. PNA-based antisense oligonucleotides for microRNAs inhibition in the absence of a transfection reagent. Oligonucleotides 20(5), 225-230 (2010).
16. Oh SY, Ju Y, Park H. A highly effective and long-lasting inhibition of miRNAs with PNA-based antisense oligonucleotides. Mol. Cells 28(4), 341-345 (2009).
17. Marchelli R, Corradini R, Manicardi A et al. Gene modulation by peptide nucleic acids (PNAs) targeting microRNAs (miRs).In: Targets in Gene Therapy. You Y (Ed.).InTech (2011).
18. Costa FF. Epigenomics in cancer management. Cancer Manag. Res. 2, 255-265 (2010).
19. Filipowicz W, Jaskiewicz L, Kolb FA, Pillai RS. Post-transcriptional gene silencing by siRNAs and miRNAs. Curr. Opin. Struc. Biol. 15, 331-341 (2005).
20. He L, Hannon, GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5, 522-531 (2010).
21. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, D152-D157 (2010).
22. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597-610 (2010).
23. Calabretta A, Tedeschi T, Corradini R, Marchelli R, Sforza, S. DNA and RNA binding properties of an arginine-based 'extended chiral box' peptide nucleic acid. Tetrahedron Lett. 52, 300-304 (2011).
24. Borgatti M, Romanelli A, Saviano M et al. Resistance of decoy PNA-DNA chimeras to enzymatic degradation in cellular extracts and serum. Oncol. Res. 13(5), 279-287 (2003).
25. Borgatti M, Breda L, Cortesi R et al. Cationic liposomes as delivery systems for double-stranded PNA-DNA chimeras exhibiting decoy activity against NF-kB transcription factors. Biochem. Pharmacol. 64, 609-616 (2002).
26. Demidov VV, Potaman VN, Frank- Kamenetskii MD et al. Stability of peptide nucleic acids in human serum and cellular extracts. Biochem. Pharmacol. 48(6), 1310-1313 (1994).
27. Eriksson M, Nielsen PE. PNA-nucleic acid complexes. Structure, stability and dynamics. Q. Rev. Biophys. 29(4), 369-394 (1996).
28. Shiraishi T, Hamzavi R, Nielsen PE. Subnanomolar antisense activity of phosphonate-peptide nucleic acid (PNA) conjugates delivered by cationic lipids to HeLa cells. Nucleic Acids Res. 36(13), 4424-4432 (2008).
29. Gambari R, Borgatti M, Bezzerri V et al. Decoy oligodeoxyribonucleotides and peptide nucleic acids-DNA chimeras targeting nuclear factor kB: inhibition of IL 8 gene expression in cystic fibrosis cells infected with Pseudomonas aeruginosa. Biochem. Pharmacol. 80(12), 1887-1894 (2010).
30. Stein CA. Two problems in antisense biotechnology: in vitro delivery and the design of antisense experiments. Biochim. Biophys. Acta 1489, 45-52 (1999).
31. Hatamoto M, Ohashi A, Imachi H. Peptide nucleic acids (PNAs) antisense effect to bacterial growth and their application potentiality in biotechnology. Appl. Microbiol. Biotechnol. 86(2), 397-402 (2010).
32. Pandey VN, Upadhyay A, Chaubey B. Prospects for antisense peptide nucleic acid (PNA) therapies for HIV. Expert Opin. Biol. Ther. 9(8), 975-989 (2009).
33. Turner JJ, Jones S, Fabani MM, Ivanova G, Arzumanov AA, Gait MJ. RNA targeting with peptide conjugates of oligonucleotides, siRNA and PNA. Blood Cells Mol. Dis. 38(1), 1-7 (2007).
34. Lundin KE, Good L, Strömberg R, Gräslund A, Smith CI. Biological activity and biotechnological aspects of peptide nucleic acid. Adv. Genet. 56, 1-51 (2006).
35. Yin H, Betts C, Saleh AF et al. Optimization of peptide nucleic acid antisense oligonucleotides for local and systemic dystrophin splice correction in the mdx mouse. Mol. Ther. 18(4), 819-827 (2010).
36. Shiraishi T, Eysturskarth J, Nielsen PE. Modulation of mdm2 pre-mRNA splicing by 9 aminoacridine-PNA (peptide nucleic acid) conjugates targeting intron-exon junctions. BMC Cancer 10, 342 (2010).
37. Tonelli R, Purgato S, Camerin C et al. Anti-gene peptide nucleic acid specifically inhibits MYCN expression in human neuroblastoma cells leading to cell growth inhibition and apoptosis. Mol. Cancer Ther. 4(5), 779-786 (2005).
38. Møllegaard NE, Buchardt O, Egholm M, Nielsen PE. Peptide nucleic acid.DNA strand displacement loops as artificial transcription promoters. Proc. Natl Acad. Sci. USA 91(9), 3892-3895 (1994).
39. Mischiati C, Borgatti M, Bianchi N et al. Interaction of the human NF kB p52 transcription factor with DNA-PNA hybrids mimicking the NF kB binding sites of the human immunodeficiency virus type 1 promoter. J. Biol. Chem. 274(46), 33114-33122 (1999).
40. Saviano M, Romanelli A, Bucci E et al. Computational procedures to explain the different biological activity of DNA/DNA, DNA/PNA and PNA/PNA hybrid molecules mimicking NF kB binding sites. J. Biomol. Struct. Dyn. 18(3), 353-362 (2000).
41. Borgatti M, Lampronti I, Romanelli A et al. Transcription factor decoy molecules based on a peptide nucleic acid (PNA)-DNA chimera mimicking Sp1 binding sites. J. Biol. Chem. 278(9), 7500-7509 (2003).
42. Piva R, Gambari R. Transcription factor decoy (TFD) in breast cancer research and treatment. Technol. Cancer Res. Treat. 1(5), 405-416 (2002).
43. Penolazzi L, Borgatti M, Lambertini E et al. Peptide nucleic acid-DNA decoy chimeras targeting NF kB transcription factors: induction of apoptosis in human primary osteoclasts. Int. J. Mol. Med. 14(2), 145-152 (2004).
44. Gambari R. Biological activity and delivery of peptide nucleic acids (PNA)-DNA chimeras for transcription factor decoy (TFD) pharmacotherapy. Curr. Med. Chem. 11(10), 1253-1263 (2004).
45. Borgatti M, Finotti A, Romanelli A et al. Peptide nucleic acids (PNA)-DNA chimeras targeting transcription factors as a tool to modify gene expression. Curr. Drug. Targets 5(8), 735-744 (2004).
46. Borgatti M, Boyd DD, Lampronti I et al. Decoy molecules based on PNA-DNA chimeras and targeting Sp1 transcription factors inhibit the activity of urokinase-type plasminogen activator receptor (uPAR) promoter. Oncol. Res. 15(7-8), 373-383 (2005).
47. Romanelli A, Pedone C, Saviano M, Bianchi N, Borgatti M, Mischiati C et al. Molecular interactions with nuclear factor kB (NF-kB) transcription factors of a PNA-DNA chimera mimicking NF-kB binding sites. Eur. J. Biochem. 268, 6066-6075 (2001).
48. Cortesi R, Mischiati C, Borgatti M et al. Formulations for natural and peptide nucleic acids based on cationic polymeric submicron particles. AAPS J. 6(1), 10-21 (2004).
49. Mischiati C, Sereni A, Finotti A et al. Complexation to cationic microspheres of double-stranded peptide nucleic acid-DNA chimeras exhibiting decoy activity. J. Biomed. Sci. 11(5), 697-704 (2004).
50. Nastruzzi C, Cortesi R, Esposito E et al. Liposomes as carriers for DNA-PNA hybrids. J. Control. Release 68(2), 237-249 (2000).
51. Wojciechowski F, Hudson RH. Nucleobase modifications in peptide nucleic acids. Curr. Top Med. Chem. 7(7), 667-679 (2007).
52. Hansen ME, Bentin T, Nielsen PE. High-affinity triplex targeting of double stranded DNA using chemically modified peptide nucleic acid oligomers. Nucleic Acids Res. 37(13), 4498-4507 (2009).
53. Manicardi A, Calabretta A, Bencivenni M et al. Affinity and selectivity of C2 and C5 substituted 'chiral-box' PNA in solution and on microarrays. Chirality 22(Suppl. 1), E161-E172 (2010).
54. Berthold PR, Shiraishi T, Nielsen PE. Cellular delivery and antisense effects of peptide nucleic acid conjugated to polyethyleneimine via disulfide linkers. Bioconjug. Chem. 21(10), 1933-1938 (2010).
55. Pensato S, Saviano M, Bianchi N et al. g-hydroxymethyl PNAs: synthesis, interaction with DNA and inhibition of protein/DNA interactions. Bioorg. Chem. 38(5), 196-201 (2010).
56. Zhou P, Dragulescu-Andrasi A, Bhattacharya B et al. Synthesis of cell-permeable peptide nucleic acids and characterization of their hybridization and uptake properties. Bioorg. Med. Chem. Lett. 16, 4931-4935 (2006).
57. Zhou P, Wang MM, Du L, Fisher GW, Waggoner A, Ly DH. Novel binding and efficient cellular uptake of guanidine-based peptide nucleic acids (GPNA).J. Am. Chem. Soc. 125, 6878-6879 (2003).
58. Rasmussen FW, Bendifallah N, Zachar V et al. Evaluation of transfection protocols for unmodified and modified peptide nucleic acid (PNA) oligomers. Oligonucleotides 16, 43-57 (2006).
59. Joergensen M, Agerholm-Larsen B, Nielsen PE, Gehl J. Efficiency of cellular delivery of antisense peptide nucleic acid by electroporation depends on charge and electroporation geometry. Oligonucleotides 21, 29-37 (2011).
60. Shiraishi T, Nielsen PE. Enhanced cellular delivery of cell-penetrating peptide-peptide nucleic acid conjugates by photochemical internalization. Methods Mol. Biol. 683, 391-397 (2011).
61. Sontheimer EJ, Carthew RW. Silence from within: endogenous siRNAs and miRNAs. Cell 122, 9-12 (2005).
62. Subramanian S, Steer CJ. MicroRNAs as gatekeepers of apoptosis. J. Cell. Physiology 223, 89-98 (2010).
63. Wang YM, Blelloch R. Cell cycle regulation by MicroRNAs in embryonic stem cells. Cancer Res. 69, 4093-4096 (2010).
64. Alvarez-Garcia I, Miska EA. MicroRNA functions in animal development and human disease. Development 132, 4653-4662 (2005).
65. Taccioli C, Fabbri E, Visone R et al. UCbase & miRfunc: a database of ultraconserved sequences and microRNA function. Nucleic Acids Res. 37(Database issue), D41-D48 (2009).
66. Brown BD, Naldini L. Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications. Nat. Rev. Genet. 10, 578-585 (2009).
67. Czech MP. MicroRNAs as therapeutic targets. N. Engl. J. Med. 354, 1194-1195 (2006).
68. Kota SK, Balasubramanian S. Cancer therapy via modulation of microRNA levels: a promising future. Drug Discov. Today 15, 733-740 (2010).
69. Wang Z. MicroRNA interference: an update. J. Biol. Med. 1, 1-12 (2011).
70. Torres AG, Fabani MM, Vigorito E, Gait MJ. MicroRNA fate upon targeting with anti-miRNA oligonucleotides as revealed by an improved Northern-blot-based method for miRNA detection. RNA 17, 933-943 (2011).
71. Elmén J, Lindow M, Schütz S, Lawrence M, Petri A, Obad S, et al. LNA-mediated microRNA silencing in non-human primates. Nature 452, 896-900 (2008).
72. Elmén J, Lindow M, Silahtaroglu A, Bak M, Christensen M, Lind-Thomsen A. Antagonism of microRNA 122 in mice by systemically administered LNA-antimiR leads to upregulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Res. 36, 1153-1162 (2008).
73. Krutzfeldt J, Kuwajima S, Braich R, Rajeev K.G, Pena J et al. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res. 35, 2885-2892 (2007).
74. Krützfeldt J, Rajewsky N, Braich R et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 438, 685-689 (2005).
75. López-Fraga M, Wright N, Jiménez A. RNA interference-based therapeutics: new strategies to fight infectious disease. Infect. Disord. Drug Targets 8, 262-273 (2008).
76. Zhiguo W. MicroRNA interference: an update. J. Biol. Med. 1(1), 1-12 (2011).
77. Boutla A, Delidakis C, Tabler M. Developmental defects by antisense-mediated inactivation of micro-RNAs 2 and 13 in Drosophila and the identification of putative target genes. Nucleic Acids Res. 31(17), 4973-4980 (2003).
78. Meister G, Landthaler M, Dorsett Y, Tuschl T. Sequence-specific inhibition of microRNA-and siRNA-induced. RNA silencing RNA 10(3), 544-550 (2004).
79. Krtzfeldt J, Rajewsky N, Braich R et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 438(7068), 685-689 (2005).
80. Krtzfeldt J, Kuwajima S, Braich R et al. Specificity, duplex degradation and subcellular localization of antagomirs. Nucleic Acids Res. 35(9), 2885-2892 (2007).
81. Kauppinen S, Lund AH. LNA-modified oligonucleotides mediate specific inhibition of microRNA function. Gene 372, 137-141 (2006).
82. Davis S, Lollo B, Freier S, Esau C. Improved targeting of miRNA with antisense oligonucleotides. Nucleic Acids Res. 34(8), 2294-2304 (2006).
83. Fabani MM, Gait MJ. miR 122 targeting with LNA/2' O-methyl oligonucleotide mixmers, peptide nucleic acids (PNA), and PNA-peptide conjugates. RNA 14(2) 336-346 (2008).
84. Clancy JL, Wei GH, Echner N et al. mRNA isoform diversity can obscure detection of miRNA-mediated control of translation. RNA 17(6), 1025-1031 (2011).
85. Lee EK, Gorospe M. Coding region: the neglected post-transcriptional code. RNA Biol. 8(1), 44-48 (2011).
86. Wang Z. The concept of multiple-target anti-miRNA antisense oligonucleotide technology. Methods Mol. Biol. 676, 51-57 (2011).
87. Torres AG, Threlfall RN, Gait MJ. Potent and sustained cellular inhibition of miR-122 by lysine-derivatized peptide nucleic acids (PNA) and phosphorothioate locked nucleic acid (LNA)/2'-O-methyl (OMe) mixmer anti-miRs in the absence of transfection agents. Artif. DNA PNA XNA 2(3), 1-8 (2011).
88. Petersen L, de Koning MC, van Kuik- Romeijn P et al. Synthesis and in vitro evaluation of PNA-peptide-DETA conjugates as potential cell penetrating artificial ribonucleases. Bioconjug. Chem. 15(3), 576-582 (2004).
89. Tyagi P, Banerjee R, Basu S, Yoshimura N, Chancellor M, Huang L. Intravesical antisense therapy for cystitis using TAT-peptide nucleic acid conjugates. Mol. Pharm. 3(4), 398-406 (2006).
90. Frederickson R. PNA-NLS delivers. Nat. Biotechnol. 17(8), 739 (1999).
91. Albertshofer K, Siwkowski AM, Wancewicz EV et al. Structure-activity relationship study on a simple cationic peptide motif for cellular delivery of antisense peptide nucleic acid. J. Med. Chem. 48(21), 6741-6749 (2005).
92. Leifert JA, Whitton JL. 'Translocatory proteins' and 'protein transduction domains': a critical analysis of their biological effects and the underlying mechanisms. Mol. Ther. 8(1), 13-20 (2003).
93. Chaubey B, Tripathi S, Ganguly S, Harris D, Casale RA, Pandey VN. A PNA-transportan conjugate targeted to the TAR region of the HIV-1 genome exhibits both antiviral and virucidal properties. Virology 331(2), 418-428 (2005).
94. Braun K, Peschke P, Pipkorn R et al. A biological transporter for the delivery of peptide nucleic acids (PNAs) to the nuclear compartment of living cells. J. Mol. Biol. 318(2), 237-243 (2002).
95. Basu S, Wickstrom E. Synthesis and characterization of a peptide nucleic acid conjugated to a d-peptide analog of insulin-like growth factor 1 for increased cellular uptake. Bioconjug. Chem. 8(4), 481-488 (1997).
96. Abes S, Turner JJ, Ivanova GD et al. Efficient splicing correction by PNA conjugation to an R6-Penetratin delivery peptide. Nucleic Acids Res. 35(13), 4495-4502 (2007).
97. Mehiri M, Upert G, Tripathi S et al. An efficient biodelivery system for antisense polyamide nucleic acid (PNA).Oligonucleotides 18(3), 245-256 (2008).
98. Berg K, Folini M, Prasmickaite L et al. Photochemical internalization: a new tool for drug delivery. Curr. Pharm. Biotechnol. 8(6), 362-372 (2007).
99. Shiraishi T, Nielsen PE. Enhanced delivery of cell-penetrating peptide-peptide nucleic acid conjugates by endosomal disruption. Nat. Protoc. 1(2), 633-636 (2006).
100. Qavi AJ, Bailey RC. Multiplexed detection and label-free quantitation of microRNAs using arrays of silicon photonic microring resonators. Angew. Chem. Int. Ed. Engl. 49(27), 4608-4611 (2010).
101. Zhang GJ, Chua JH, Chee RE, Agarwal A, Wong SM. Label-free direct detection of miRNAs with silicon nanowire biosensors. Biosens. Bioelectron. 24(8), 2504-2508 (2009).
102. Pfeffer S, Baumert TF. Impact of microRNAs for pathogenesis and treatment of hepatitis C virus infection. Gastroenterol. Clin. Biol. 34(8-9), 431-435 (2010).
103. Young DD, Connelly CM, Grohmann C, Deiters A. Small molecule modifiers of microRNA miR 122 function for the treatment of hepatitis C virus infection and hepatocellular carcinoma. J. Am. Chem. Soc. 132(23), 7976-7981 (2010).
104. Morita K, Taketomi A, Shirabe K et al. Clinical significance and potential of hepatic microRNA-122 expression in hepatitis C. Liver Int. 31(4), 474-484 (2011).
105. Lanford RE, Hildebrandt-Eriksen ES, Petri A et al. Therapeutic silencing of microRNA 122 in primates with chronic hepatitis C virus infection. Science 327(5962), 198-201 (2010).
106. Tili E, Croce CM, Michaille JJ. miR 155: on the crosstalk between inflammation and cancer. Int. Rev. Immunol. 28(5), 264-284 (2009).
107. Kong W, He L, Coppola M et al. MicroRNA 155 regulates cell survival, growth, and chemosensitivity by targeting FOXO3a in breast cancer. J. Biol. Chem. 285(23), 17869-17879 (2010).
108. Jiang S, Zhang HW, Lu MH et al. MicroRNA 155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res. 70(8), 3119-3127 (2010).
109. Bianchi N, Zuccato C, Lampronti I, Borgatti M, Gambari R. Expression of miR-210 during erythroid differentiation and induction of gamma-globin gene expression. BMB Rep. 42(8), 493-499 (2009).
110. Yan LX, Wu QN, Zhang Y et al. Knockdown of miR 21 in human breast cancer cell lines inhibits proliferation, in vitro migration and in vivo tumor growth. Breast Cancer Res. 13(1), R2 (2011).
111. Chaubey B, Tripathi S, Pandey VN. Single acute-dose and repeat-doses toxicity of anti-HIV-1 PNA TAR-penetratin conjugate after intraperitoneal administration to mice. Oligonucleotides 18(1), 9-20 (2008).
112. Ganguly S, Chaubey B, Tripathi S et al. Pharmacokinetic analysis of polyamide nucleic-acid-cell penetrating peptide conjugates targeted against HIV 1 transactivation response element. Oligonucleotides 18(3), 277-286 (2008).
113. Corradini R, Sforza S, Tedeschi T, Totsingan F, Manicardi A, Marchelli R. Peptide nucleic acids with a structurally biased backbone. Updated review and emerging challenges Curr. Top Med. Chem. 11(12), 1535-1554 (2011).
114. Sahu B, Sacui I, Rapireddy S et al. Synthesis and characterization of conformationally preorganized, (R) diethylene glycol-containing g peptide nucleic acids with superior hybridization properties and water solubility. J. Org. Chem. 76(14), 5614-5627 (2011).
115. Wojciechowski F, Hudson RH. Peptide nucleic acid containing a meta-substituted phenylpyrrolocytosine exhibits a fluorescence response and increased binding affinity toward RNA. Org. Lett. 11(21), 4878-4881 (2009).
116. Govindaraju T, Madhuri V, Kumar VA, Ganesh KN. Cyclohexanyl peptide nucleic acids (chPNAs) for preferential RNA binding: effective tuning of dihedral angle beta in PNAs for DNA/RNA discrimination. J. Org. Chem. 71(1), 14-21 (2006).
117. Sforza S, Tedeschi T, Calabretta A et al. A peptide nucleic acid embedding a pseudo peptide nuclear localization sequence in the backbone bahaves as a peptide mimic. Eur. J. Org. Chem. 13, 2441-2444 (2010).
118. Ishizuka T, Tedeschi T, Corradini R, Komiyama M, Sforza S, Marchelli R. SSB-assisted duplex invasion of preorganized PNA into double-stranded DNA. Chem. Bio. Chem. 10(16), 2607-2612 (2009).
119. Ishizuka T, Yoshida J, Yamamoto Y et al. Chiral introduction of positive charges to PNA for double-duplex invasion to versatile sequences. Nucleic Acid Res. 36(5), 1464-1471 (2008).
120. Yuan X, Ma Z, Zhou W et al. Lipid-mediated delivery of peptide nucleic acids to pulmonary endothelium. Biochem. Biophys. Res. Commun. 302(1), 6-11 (2003).
121. Cutrona G, Boffa LC, Mariani MR et al. The peptide nucleic acid targeted to a regulatory sequence of the translocated c myc oncogene in Burkitt's lymphoma lacks immunogenicity: follow-up characterization of PNAEmu-NLS. Oligonucleotides 17(1), 146-150 (2007).
122. Ahn DG, Lee W, Choi JK et al. Interference of ribosomal frameshifting by antisense peptide nucleic acids suppresses SARS coronavirus replication. Antiviral Res. 91(1), 1-10 (2011).
123. Upadhyay A, Ponzio NM, Pandey VN. Immunological response to peptide nucleic acid and its peptide conjugate targeted to transactivation response (TAR) region of HIV 1 RNA genome. Oligonucleotides 18, 329-336 (2008).