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Molecular Properties and the Applications of Peptide Nucleic Acids

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A special issue of Molecules (ISSN 1420-3049). This special issue belongs to the section "Bioorganic Chemistry".

Deadline for manuscript submissions: closed (15 November 2017) | Viewed by 85810

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Prof. Dr. Roberto Corradini

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Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area delle Scienze 17/A, I-43124 Parma, Italy
Interests: bioorganic chemistry; nucleic acid recognition; peptide nucleic acids; chirality; stereochemistry; supramolecular chemistry; anti-miR; anti-gene; biosensing technologies

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Dear Colleagues,

After 25 years since their discovery, peptide nucleic acids (PNAs) are still a source of intense inspiration for scientists. Their properties and applications are actively being studied in different fields, from fundamental Chemistry to Biology, Medicine and Material Chemistry, with more than 100 papers published on this topic and more than 5000 citations every year.

As biomolecular tools, PNAs have intriguing properties, with exceptional affinities and sequence selectivities, high biological and chemical stability, and thus high persistence in biological fluids. Due to the relatively scarce structural data, the nature of PNA:DNA and PNA:RNA interactions, and the effect of chemical variation on PNA properties is still an open field of research. The quest for even better binding affinity and sequence selectivity is not over yet, and both modelling techniques and modern synthetic procedures can be fruitfully applied to the design and synthesis of new molecules based on the PNA scaffold. Using a ‘biomolecular engineering’ approach, new functions, in addition to DNA recognition, can be added to PNAs, e.g., cleaving activity, or signalling. In cellular systems, PNAs have proven to be very effective for the regulation of gene expression, especially for applications in which an appropriate cellular delivery system is used. In diagnostics, PNAs are the base of several new ultrasensitive and very specific techniques.

PNAs can also be useful in nanofabrication and in material chemistry as programmable objects that are able to self assemble with a rational scheme. Helical handedness can be controlled in these systems much more easily than in other DNA analogs.

We intend to capture a full picture of this field of research in the journal Molecules with a dedicated Special Issue to be published in 2017. We invite contributions from scientists in all of these areas of research.

Prof. Dr. Roberto Corradini
Guest Editor

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Keywords

PNA
modified PNA
DNA and RNA recognition
delivery systems
antisense
antigene
anti-miR
artificial nucleases
molecular modelling
molecular dynamics
solid-phase synthesis
genosensing
ultrasensitive techniques

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Peptide Nucleic Acids: Applications in Biomedical Sciences in Molecules (9 articles)

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Editorial

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3 pages, 156 KiB

Open AccessEditorial

Special Issue: Molecular Properties and the Applications of Peptide Nucleic Acids

by Roberto Corradini

Molecules 2018, 23(8), 1977; https://doi.org/10.3390/molecules23081977 - 8 Aug 2018

Cited by 3 | Viewed by 2550

Abstract

Polyamide analogs of DNA, or peptide nucleic acid (PNA), were first proposed in 1991 by a group of chemists and biochemists in a memorable Science paper [1].[…] Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

Research

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2531 KiB

Open AccessFeature PaperArticle

A Peptide Nucleic Acid against MicroRNA miR-145-5p Enhances the Expression of the Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) in Calu-3 Cells

by Enrica Fabbri, Anna Tamanini, Tiziana Jakova, Jessica Gasparello, Alex Manicardi, Roberto Corradini, Giuseppe Sabbioni, Alessia Finotti, Monica Borgatti, Ilaria Lampronti, Silvia Munari, Maria Cristina Dechecchi, Giulio Cabrini and Roberto Gambari

Molecules 2018, 23(1), 71; https://doi.org/10.3390/molecules23010071 - 29 Dec 2017

Cited by 42 | Viewed by 6408

Abstract

Peptide nucleic acids (PNAs) are very useful tools for gene regulation at different levels, but in particular in the last years their use for targeting microRNA (anti-miR PNAs) has provided impressive advancements. In this respect, microRNAs related to the repression of cystic fibrosis transmembrane conductance regulator (CFTR) gene, which is defective in cystic fibrosis, are of great importance in the development of new type of treatments. In this paper we propose the use of an anti-miR PNA for targeting miR-145, a microRNA reported to suppress CFTR expression. Octaarginine-anti-miR PNA conjugates were delivered to Calu-3 cells, exerting sequence dependent targeting of miR-145-5p. This allowed to enhance expression of the miR-145 regulated CFTR gene, analyzed at mRNA (RT-qPCR, Reverse Transcription quantitative Polymerase Chain Reaction) and CFTR protein (Western blotting) level. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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3517 KiB

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γPNA FRET Pair Miniprobes for Quantitative Fluorescent In Situ Hybridization to Telomeric DNA in Cells and Tissue

by Alexander Orenstein, April S. Berlyoung, Elizabeth E. Rastede, Ha H. Pham, Elise Fouquerel, Connor T. Murphy, Brian J. Leibowitz, Jian Yu, Tumul Srivastava, Bruce A. Armitage and Patricia L. Opresko

Molecules 2017, 22(12), 2117; https://doi.org/10.3390/molecules22122117 - 2 Dec 2017

Cited by 10 | Viewed by 5996

Abstract

Measurement of telomere length by fluorescent in situ hybridization is widely used for biomedical and epidemiological research, but there has been relatively little development of the technology in the 20 years since it was first reported. This report describes the use of dual gammaPNA (γPNA) probes that hybridize at alternating sites along a telomere and give rise to Förster resonance energy transfer (FRET) signals. Bright staining of telomeres is observed in nuclei, chromosome spreads and tissue samples. The use of FRET detection also allows for elimination of wash steps, normally required to remove unhybridized probes that would contribute to background signals. We found that these wash steps can diminish the signal intensity through the removal of bound, as well as unbound probes, so eliminating these steps not only accelerates the process but also enhances the quality of staining. Thus, γPNA FRET pairs allow for brighter and faster staining of telomeres in a wide range of research and clinical formats. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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2070 KiB

Open AccessArticle

Synthesis and Improved Cross-Linking Properties of C5-Modified Furan Bearing PNAs

by Joke Elskens, Alex Manicardi, Valentina Costi, Annemieke Madder and Roberto Corradini

Molecules 2017, 22(11), 2010; https://doi.org/10.3390/molecules22112010 - 20 Nov 2017

Cited by 17 | Viewed by 6850

Abstract

Over the past decades, peptide nucleic acid/DNA (PNA:DNA) duplex stability has been improved via backbone modification, often achieved via introducing an amino acid side chain at the α- or γ-position in the PNA sequence. It was previously shown that interstrand cross-linking can further enhance the binding event. In this work, we combined both strategies to fine-tune PNA crosslinking towards single stranded DNA sequences using a furan oxidation-based crosslinking method; for this purpose, γ-l-lysine and γ-l-arginine furan-PNA monomers were synthesized and incorporated in PNA sequences via solid phase synthesis. It was shown that the l-lysine γ-modification had a beneficial effect on crosslink efficiency due to pre-organization of the PNA helix and a favorable electrostatic interaction between the positively-charged lysine and the negatively-charged DNA backbone. Moreover, the crosslink yield could be optimized by carefully choosing the type of furan PNA monomer. This work is the first to describe a selective and biocompatible furan crosslinking strategy for crosslinking of γ-modified PNA sequences towards single-stranded DNA. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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11259 KiB

Open AccessArticle

DNA G-Wire Formation Using an Artificial Peptide is Controlled by Protease Activity

by Kenji Usui, Arisa Okada, Shungo Sakashita, Masayuki Shimooka, Takaaki Tsuruoka, Shu-ichi Nakano, Daisuke Miyoshi, Tsukasa Mashima, Masato Katahira and Yoshio Hamada

Molecules 2017, 22(11), 1991; https://doi.org/10.3390/molecules22111991 - 16 Nov 2017

Cited by 17 | Viewed by 6336

Abstract

The development of a switching system for guanine nanowire (G-wire) formation by external signals is important for nanobiotechnological applications. Here, we demonstrate a DNA nanostructural switch (G-wire <--> particles) using a designed peptide and a protease. The peptide consists of a PNA sequence for inducing DNA to form DNA–PNA hybrid G-quadruplex structures, and a protease substrate sequence acting as a switching module that is dependent on the activity of a particular protease. Micro-scale analyses via TEM and AFM showed that G-rich DNA alone forms G-wires in the presence of Ca²⁺, and that the peptide disrupted this formation, resulting in the formation of particles. The addition of the protease and digestion of the peptide regenerated the G-wires. Macro-scale analyses by DLS, zeta potential, CD, and gel filtration were in agreement with the microscopic observations. These results imply that the secondary structure change (DNA G-quadruplex <--> DNA/PNA hybrid structure) induces a change in the well-formed nanostructure (G-wire <--> particles). Our findings demonstrate a control system for forming DNA G-wire structures dependent on protease activity using designed peptides. Such systems hold promise for regulating the formation of nanowire for various applications, including electronic circuits for use in nanobiotechnologies. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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7648 KiB

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Peptide Nucleic Acid Based Molecular Authentication for Identification of Four Medicinal Paeonia Species Using Melting Array Analysis of the Internal Transcribed Spacer 2 Region

by Wook Jin Kim, Sungyu Yang, Goya Choi and Byeong Cheol Moon

Molecules 2017, 22(11), 1922; https://doi.org/10.3390/molecules22111922 - 7 Nov 2017

Cited by 8 | Viewed by 5475

Abstract

Accurate taxonomic identification of plant materials in herbal medicines is important for product quality control. The genus Paeonia (Saxifragales) is the source of the herbal preparations Paeoniae Radix (Paeoniae Radix Alba and Paeoniae Radix Rubra) and Moutan Radicis Cotex. However, confusion has arisen regarding their contents due to linguistic and taxonomic ambiguities, similar morphologies and different definitions of Paeoniae Radix in the Korean and Chinese national pharmacopoeias, leading to the distribution of adulterated products. To develop a method for identifying the four Paeonia species used in these medicines, three fluorescently-labeled peptide nucleic acid (PNA) probes were designed against ITS2 sequences containing single nucleotide polymorphisms (SNPs) and used in a real-time PCR melting curve assay. Each of the four Paeonia species was accurately identified using this analysis. The accuracy and analytical stability of the PNA melting curve assay was confirmed using commercially available samples of the four Paeonia species. This assay is a reliable genetic tool to distinguish between different Paeonia-derived herbal medicines and identify the botanical origins of Paeoniae Radix and Moutan Radicis Cortex. This technique may also contribute to quality control and standardization of herbal medicines by providing a reliable authentication tool and preventing the distribution of inauthentic adulterants. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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1264 KiB

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Detection of Rare Somatic GNAS Mutation in McCune-Albright Syndrome Using a Novel Peptide Nucleic Acid Probe in a Single Tube

by Fu-Sung Lo, Tai-Long Chen and Chiuan-Chian Chiou

Molecules 2017, 22(11), 1874; https://doi.org/10.3390/molecules22111874 - 1 Nov 2017

Cited by 5 | Viewed by 5630

Abstract

McCune-Albright syndrome (MAS) is characterized by the triad of precocious puberty, café au lait pigmentation, and polyostotic fibrous dysplasia (FD) of bone, and is caused by post-zygotic somatic mutations—R201H or R201C—in the guanine nucleotide binding protein, alpha stimulating (GNAS) gene. In the present study, a novel peptide nucleic acid (PNA) probe with fluorescent labeling was designed to detect trace amounts of somatic mutant GNAS in a single tube reaction. The method was applied to screen GNAS mutations in six patients with MAS/FD. The results showed that the PNA probe assay could detect low abundant mutants in 200-fold excess of wild-type alleles. The GNAS mutation was found in three patients with severe disease (MAS) by using the assay. The other three patients with mild disease (having only FD) showed a wild-type result. This study has provided a simple method to detect trace amounts of GNAS mutants with high sensitivity in large amounts of wild-type DNA. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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2008 KiB

Open AccessFeature PaperArticle

Zinc Ion-Dependent Peptide Nucleic Acid-Based Artificial Enzyme that Cleaves RNA—Bulge Size and Sequence Dependence

by Merita Murtola, Alice Ghidini, Pasi Virta and Roger Strömberg

Molecules 2017, 22(11), 1856; https://doi.org/10.3390/molecules22111856 - 29 Oct 2017

Cited by 16 | Viewed by 5366

Abstract

In this report, we investigate the efficiency and selectivity of a Zn²⁺-dependent peptide nucleic acid-based artificial ribonuclease (PNAzyme) that cleaves RNA target sequences. The target RNAs are varied to form different sizes (3 and 4 nucleotides, nt) and sequences in the bulge formed upon binding to the PNAzyme. PNAzyme-promoted cleavage of the target RNAs was observed and variation of the substrate showed a clear dependence on the sequence and size of the bulge. For targets that form 4-nt bulges, we identified systems with an improved efficacy (an estimated half-life of ca 7–8 h as compared to 11–12 h for sequences studied earlier) as well as systems with an improved site selectivity (up to over 70% cleavage at a single site as compared to 50–60% with previous targets sequences). For targets forming 3-nt bulges, the enhancement compared to previous systems was even more pronounced. Compared to a starting point of targets forming 3-nt AAA bulges (half-lives of ca 21–24 h), we could identify target sequences that were cleaved with half-lives three times lower (ca 7–8 h), i.e., at rates similar to those found for the fastest 4-nt bulge system. In addition, with the 3-nt bulge RNA target site selectivity was improved even further to reach well over 80% cleavage at a specific site. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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1668 KiB

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Design of Tail-Clamp Peptide Nucleic Acid Tethered with Azobenzene Linker for Sequence-Specific Detection of Homopurine DNA

by Shinjiro Sawada, Toshifumi Takao, Nobuo Kato and Kunihiro Kaihatsu

Molecules 2017, 22(11), 1840; https://doi.org/10.3390/molecules22111840 - 27 Oct 2017

Cited by 6 | Viewed by 5880

Abstract

DNA carries genetic information in its sequence of bases. Synthetic oligonucleotides that can sequence-specifically recognize a target gene sequence are a useful tool for regulating gene expression or detecting target genes. Among the many synthetic oligonucleotides, tail-clamp peptide nucleic acid (TC-PNA) offers advantages since it has two homopyrimidine PNA strands connected via a flexible ethylene glycol-type linker that can recognize complementary homopurine sequences via Watson-Crick and Hoogsteen base pairings and form thermally-stable PNA/PNA/DNA triplex structures. Here, we synthesized a series of TC-PNAs that can possess different lengths of azobenzene-containing linkers and studied their binding behaviours to homopurine single-stranded DNA. Introduction of azobenzene at the N-terminus amine of PNA increased the thermal stability of PNA-DNA duplexes. Further extension of the homopyrimidine PNA strand at the N-terminus of PNA-AZO further increased the binding stability of the PNA/DNA/PNA triplex to the target homopurine sequence; however, it induced TC-PNA/DNA/TC-PNA complex formation. Among these TC-PNAs, 9W5H-C4-AZO consisting of nine Watson-Crick bases and five Hoogsteen bases tethered with a beta-alanine conjugated azobenzene linker gave a stable 1:1 TC-PNA/ssDNA complex and exhibited good mismatch recognition. Our design for TC-PNA-AZO can be utilized for detecting homopurine sequences in various genes. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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2941 KiB

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Peptide Nucleic Acids as miRNA Target Protectors for the Treatment of Cystic Fibrosis

by Federica Zarrilli, Felice Amato, Carmine Marco Morgillo, Brunella Pinto, Giuliano Santarpia, Nicola Borbone, Stefano D’Errico, Bruno Catalanotti, Gennaro Piccialli, Giuseppe Castaldo and Giorgia Oliviero

Molecules 2017, 22(7), 1144; https://doi.org/10.3390/molecules22071144 - 8 Jul 2017

Cited by 31 | Viewed by 6363

Abstract

Cystic Fibrosis (CF) is one of the most common life shortening conditions in Caucasians. CF is caused by mutations in the CF Transmembrane Conductance Regulator (CFTR) gene which result in reduced or altered CFTR functionality. Several microRNAs (miRNAs) downregulate the expression of CFTR, thus causing or exacerbating the symptoms of CF. In this context, the design of anti-miRNA agents represents a valid functional tool, but its translation to the clinic might lead to unpredictable side effects because of the interference with the expression of other genes regulated by the same miRNAs. Herein, for the first time, is proposed the use of peptide nucleic acids (PNAs) to protect specific sequences in the 3’UTR (untranslated region) of the CFTR messenger RNA (mRNA) by action of miRNAs. Two PNAs (7 and 13 bases long) carrying the tetrapeptide Gly-SerP-SerP-Gly at their C-end, fully complementary to the 3’UTR sequence recognized by miR-509-3p, have been synthesized and the structural features of target PNA/RNA heteroduplexes have been investigated by spectroscopic and molecular dynamics studies. The co-transfection of the pLuc-CFTR-3´UTR vector with different combinations of PNAs, miR-509-3p, and controls in A549 cells demonstrated the ability of the longer PNA to rescue the luciferase activity by up to 70% of the control, thus supporting the use of suitable PNAs to counteract the reduction in the CFTR expression. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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Review

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15 pages, 1012 KiB

Open AccessFeature PaperReview

Peptide Nucleic Acids as a Tool for Site-Specific Gene Editing

by Adele S. Ricciardi, Elias Quijano, Rachael Putman, W. Mark Saltzman and Peter M. Glazer

Molecules 2018, 23(3), 632; https://doi.org/10.3390/molecules23030632 - 11 Mar 2018

Cited by 58 | Viewed by 10204

Abstract

Peptide nucleic acids (PNAs) can bind duplex DNA in a sequence-targeted manner, forming a triplex structure capable of inducing DNA repair and producing specific genome modifications. Since the first description of PNA-mediated gene editing in cell free extracts, PNAs have been used to successfully correct human disease-causing mutations in cell culture and in vivo in preclinical mouse models. Gene correction via PNAs has resulted in clinically-relevant functional protein restoration and disease improvement, with low off-target genome effects, indicating a strong therapeutic potential for PNAs in the treatment or cure of genetic disorders. This review discusses the progress that has been made in developing PNAs as an effective, targeted agent for gene editing, with an emphasis on recent in vivo, nanoparticle-based strategies. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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994 KiB

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Peptide Nucleic Acid-Based Biosensors for Cancer Diagnosis

by Roberta D’Agata, Maria Chiara Giuffrida and Giuseppe Spoto

Molecules 2017, 22(11), 1951; https://doi.org/10.3390/molecules22111951 - 11 Nov 2017

Cited by 83 | Viewed by 9984

Abstract

The monitoring of DNA and RNA biomarkers freely circulating in the blood constitutes the basis of innovative cancer detection methods based on liquid biopsy. Such methods are expected to provide new opportunities for a better understanding of cancer disease at the molecular level, thus contributing to improved patient outcomes. Advanced biosensors can advance possibilities for cancer-related nucleic acid biomarkers detection. In this context, peptide nucleic acids (PNAs) play an important role in the fabrication of highly sensitive biosensors. This review provides an overview of recently described PNA-based biosensors for cancer biomarker detection. One of the most striking features of the described detection approaches is represented by the possibility to detect target nucleic acids at the ultra-low concentration with the capability to identify single-base mutations. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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2482 KiB

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Applications of PNA-Based Artificial Restriction DNA Cutters

by Narumi Shigi, Jun Sumaoka and Makoto Komiyama

Molecules 2017, 22(10), 1586; https://doi.org/10.3390/molecules22101586 - 21 Sep 2017

Cited by 13 | Viewed by 7828

Abstract

More than ten years ago, artificial restriction DNA cutters were developed by combining two pseudo-complementary peptide nucleic acid (pcPNA) strands with either Ce(IV)/EDTA or S1 nuclease. They have remarkably high site-specificity and can cut only one predetermined site in the human genome. In this article, recent progress of these man-made tools have been reviewed. By cutting the human genome site-selectively, desired fragments can be clipped from either the termini of chromosomes (telomeres) or from the middle of genome. These fragments should provide important information on the biological functions of complicated genome system. DNA/RNA hybrid duplexes, which are formed in living cells, are also site-selectively hydrolyzed by these cutters. In order to further facilitate the applications of the artificial DNA cutters, various chemical modifications have been attempted. One of the most important successes is preparation of PNA derivatives which can form double-duplex invasion complex even under high salt conditions. This is important for in vivo applications, since the inside of living cells is abundant of metal ions. Furthermore, site-selective DNA cutters which require only one PNA strand, in place of a pair of pcPNA strands, are developed. This progress has opened a way to new fields of PNA-based biochemistry and biotechnology. Full article

(This article belongs to the Special Issue Molecular Properties and the Applications of Peptide Nucleic Acids)

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