Peptide Nucleic Acids and Gene Editing: Perspectives on Structure and Repair
Identifieur interne : 000F22 ( Ncbi/Merge ); précédent : 000F21; suivant : 000F23Peptide Nucleic Acids and Gene Editing: Perspectives on Structure and Repair
Auteurs : Nicholas G. Economos ; Stanley Oyaghire ; Elias Quijano ; Adele S. Ricciardi ; W. Mark Saltzman ; Peter M. GlazerSource :
- Molecules [ 1420-3049 ] ; 2020.
Abstract
Unusual nucleic acid structures are salient triggers of endogenous repair and can occur in sequence-specific contexts. Peptide nucleic acids (PNAs) rely on these principles to achieve non-enzymatic gene editing. By forming high-affinity heterotriplex structures within the genome, PNAs have been used to correct multiple human disease-relevant mutations with low off-target effects. Advances in molecular design, chemical modification, and delivery have enabled systemic in vivo application of PNAs resulting in detectable editing in preclinical mouse models. In a model of β-thalassemia, treated animals demonstrated clinically relevant protein restoration and disease phenotype amelioration, suggesting a potential for curative therapeutic application of PNAs to monogenic disorders. This review discusses the rationale and advances of PNA technologies and their application to gene editing with an emphasis on structural biochemistry and repair.
Url:
DOI: 10.3390/molecules25030735
PubMed: 32046275
PubMed Central: 7037966
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PMC:7037966Le document en format XML
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<author><name sortKey="Economos, Nicholas G" sort="Economos, Nicholas G" uniqKey="Economos N" first="Nicholas G." last="Economos">Nicholas G. Economos</name>
<affiliation><nlm:aff id="af1-molecules-25-00735">Department of Genetics, Yale University School of Medicine, New Haven, CT 06520, USA;<email>nicholas.economos@yale.edu</email>
(N.G.E.);<email>elias.quijano@yale.edu</email>
(E.Q.)</nlm:aff>
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<author><name sortKey="Oyaghire, Stanley" sort="Oyaghire, Stanley" uniqKey="Oyaghire S" first="Stanley" last="Oyaghire">Stanley Oyaghire</name>
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<author><name sortKey="Quijano, Elias" sort="Quijano, Elias" uniqKey="Quijano E" first="Elias" last="Quijano">Elias Quijano</name>
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<author><name sortKey="Saltzman, W Mark" sort="Saltzman, W Mark" uniqKey="Saltzman W" first="W. Mark" last="Saltzman">W. Mark Saltzman</name>
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<affiliation><nlm:aff id="af2-molecules-25-00735">Department of Therapeutic Radiology, Yale University School of Medicine, New Haven, CT 06520, USA;<email>stanley.oyaghire@yale.edu</email>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Peptide Nucleic Acids and Gene Editing: Perspectives on Structure and Repair</title>
<author><name sortKey="Economos, Nicholas G" sort="Economos, Nicholas G" uniqKey="Economos N" first="Nicholas G." last="Economos">Nicholas G. Economos</name>
<affiliation><nlm:aff id="af1-molecules-25-00735">Department of Genetics, Yale University School of Medicine, New Haven, CT 06520, USA;<email>nicholas.economos@yale.edu</email>
(N.G.E.);<email>elias.quijano@yale.edu</email>
(E.Q.)</nlm:aff>
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<author><name sortKey="Oyaghire, Stanley" sort="Oyaghire, Stanley" uniqKey="Oyaghire S" first="Stanley" last="Oyaghire">Stanley Oyaghire</name>
<affiliation><nlm:aff id="af2-molecules-25-00735">Department of Therapeutic Radiology, Yale University School of Medicine, New Haven, CT 06520, USA;<email>stanley.oyaghire@yale.edu</email>
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<author><name sortKey="Quijano, Elias" sort="Quijano, Elias" uniqKey="Quijano E" first="Elias" last="Quijano">Elias Quijano</name>
<affiliation><nlm:aff id="af1-molecules-25-00735">Department of Genetics, Yale University School of Medicine, New Haven, CT 06520, USA;<email>nicholas.economos@yale.edu</email>
(N.G.E.);<email>elias.quijano@yale.edu</email>
(E.Q.)</nlm:aff>
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<author><name sortKey="Ricciardi, Adele S" sort="Ricciardi, Adele S" uniqKey="Ricciardi A" first="Adele S." last="Ricciardi">Adele S. Ricciardi</name>
<affiliation><nlm:aff id="af3-molecules-25-00735">Department of Biomedical Engineering, Yale University, New Haven, CT 06511, USA;<email>adele.ricciardi@yale.edu</email>
(A.S.R.);<email>Mark.saltzman@yale.edu</email>
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<author><name sortKey="Saltzman, W Mark" sort="Saltzman, W Mark" uniqKey="Saltzman W" first="W. Mark" last="Saltzman">W. Mark Saltzman</name>
<affiliation><nlm:aff id="af3-molecules-25-00735">Department of Biomedical Engineering, Yale University, New Haven, CT 06511, USA;<email>adele.ricciardi@yale.edu</email>
(A.S.R.);<email>Mark.saltzman@yale.edu</email>
(W.M.S.)</nlm:aff>
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<author><name sortKey="Glazer, Peter M" sort="Glazer, Peter M" uniqKey="Glazer P" first="Peter M." last="Glazer">Peter M. Glazer</name>
<affiliation><nlm:aff id="af1-molecules-25-00735">Department of Genetics, Yale University School of Medicine, New Haven, CT 06520, USA;<email>nicholas.economos@yale.edu</email>
(N.G.E.);<email>elias.quijano@yale.edu</email>
(E.Q.)</nlm:aff>
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<affiliation><nlm:aff id="af2-molecules-25-00735">Department of Therapeutic Radiology, Yale University School of Medicine, New Haven, CT 06520, USA;<email>stanley.oyaghire@yale.edu</email>
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<front><div type="abstract" xml:lang="en"><p>Unusual nucleic acid structures are salient triggers of endogenous repair and can occur in sequence-specific contexts. Peptide nucleic acids (PNAs) rely on these principles to achieve non-enzymatic gene editing. By forming high-affinity heterotriplex structures within the genome, PNAs have been used to correct multiple human disease-relevant mutations with low off-target effects. Advances in molecular design, chemical modification, and delivery have enabled systemic in vivo application of PNAs resulting in detectable editing in preclinical mouse models. In a model of β-thalassemia, treated animals demonstrated clinically relevant protein restoration and disease phenotype amelioration, suggesting a potential for curative therapeutic application of PNAs to monogenic disorders. This review discusses the rationale and advances of PNA technologies and their application to gene editing with an emphasis on structural biochemistry and repair.</p>
</div>
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</TEI>
<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Molecules</journal-id>
<journal-id journal-id-type="iso-abbrev">Molecules</journal-id>
<journal-id journal-id-type="publisher-id">molecules</journal-id>
<journal-title-group><journal-title>Molecules</journal-title>
</journal-title-group>
<issn pub-type="epub">1420-3049</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">32046275</article-id>
<article-id pub-id-type="pmc">7037966</article-id>
<article-id pub-id-type="doi">10.3390/molecules25030735</article-id>
<article-id pub-id-type="publisher-id">molecules-25-00735</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Peptide Nucleic Acids and Gene Editing: Perspectives on Structure and Repair</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-4691-808X</contrib-id>
<name><surname>Economos</surname>
<given-names>Nicholas G.</given-names>
</name>
<xref ref-type="aff" rid="af1-molecules-25-00735">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Oyaghire</surname>
<given-names>Stanley</given-names>
</name>
<xref ref-type="aff" rid="af2-molecules-25-00735">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Quijano</surname>
<given-names>Elias</given-names>
</name>
<xref ref-type="aff" rid="af1-molecules-25-00735">1</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-2637-8522</contrib-id>
<name><surname>Ricciardi</surname>
<given-names>Adele S.</given-names>
</name>
<xref ref-type="aff" rid="af3-molecules-25-00735">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Saltzman</surname>
<given-names>W. Mark</given-names>
</name>
<xref ref-type="aff" rid="af3-molecules-25-00735">3</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-4525-5560</contrib-id>
<name><surname>Glazer</surname>
<given-names>Peter M.</given-names>
</name>
<xref ref-type="aff" rid="af1-molecules-25-00735">1</xref>
<xref ref-type="aff" rid="af2-molecules-25-00735">2</xref>
<xref rid="c1-molecules-25-00735" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Yavin</surname>
<given-names>Eylon</given-names>
</name>
<role>Academic Editor</role>
</contrib>
</contrib-group>
<aff id="af1-molecules-25-00735"><label>1</label>
Department of Genetics, Yale University School of Medicine, New Haven, CT 06520, USA;<email>nicholas.economos@yale.edu</email>
(N.G.E.);<email>elias.quijano@yale.edu</email>
(E.Q.)</aff>
<aff id="af2-molecules-25-00735"><label>2</label>
Department of Therapeutic Radiology, Yale University School of Medicine, New Haven, CT 06520, USA;<email>stanley.oyaghire@yale.edu</email>
</aff>
<aff id="af3-molecules-25-00735"><label>3</label>
Department of Biomedical Engineering, Yale University, New Haven, CT 06511, USA;<email>adele.ricciardi@yale.edu</email>
(A.S.R.);<email>Mark.saltzman@yale.edu</email>
(W.M.S.)</aff>
<author-notes><corresp id="c1-molecules-25-00735"><label>*</label>
Correspondence: <email>peter.glazer@yale.edu</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>08</day>
<month>2</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="collection"><month>2</month>
<year>2020</year>
</pub-date>
<volume>25</volume>
<issue>3</issue>
<elocation-id>735</elocation-id>
<history><date date-type="received"><day>16</day>
<month>1</month>
<year>2020</year>
</date>
<date date-type="accepted"><day>06</day>
<month>2</month>
<year>2020</year>
</date>
</history>
<permissions><copyright-statement>© 2020 by the authors.</copyright-statement>
<copyright-year>2020</copyright-year>
<license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract><p>Unusual nucleic acid structures are salient triggers of endogenous repair and can occur in sequence-specific contexts. Peptide nucleic acids (PNAs) rely on these principles to achieve non-enzymatic gene editing. By forming high-affinity heterotriplex structures within the genome, PNAs have been used to correct multiple human disease-relevant mutations with low off-target effects. Advances in molecular design, chemical modification, and delivery have enabled systemic in vivo application of PNAs resulting in detectable editing in preclinical mouse models. In a model of β-thalassemia, treated animals demonstrated clinically relevant protein restoration and disease phenotype amelioration, suggesting a potential for curative therapeutic application of PNAs to monogenic disorders. This review discusses the rationale and advances of PNA technologies and their application to gene editing with an emphasis on structural biochemistry and repair.</p>
</abstract>
<kwd-group><kwd>peptide nucleic acids</kwd>
<kwd>PNA</kwd>
<kwd>triplex</kwd>
<kwd>gene editing</kwd>
<kwd>structure</kwd>
<kwd>recombination</kwd>
<kwd>repair</kwd>
<kwd>nanoparticles</kwd>
<kwd>β-thalassemia</kwd>
<kwd>cystic fibrosis</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="molecules-25-00735-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>(<bold>A</bold>
) Phosphodiester and polyamide backbone structures of DNA and PNA polymers, (<bold>B</bold>
) Simplified schematic of triplex-forming PNA-mediated gene editing.</p>
</caption>
<graphic xlink:href="molecules-25-00735-g001"></graphic>
</fig>
<fig id="molecules-25-00735-f002" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>PNA structural variations to drive exergonic strand invasion. (<bold>A</bold>
) single-stranded (monomeric) PNA; (<bold>B</bold>
) bis (dimeric) PNA; (<bold>C</bold>
) tcPNA; (<bold>D</bold>
) γtcPNA; (<bold>E</bold>
) γssPNA; (<bold>F</bold>
) pcPNA.</p>
</caption>
<graphic xlink:href="molecules-25-00735-g002"></graphic>
</fig>
<fig id="molecules-25-00735-f003" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Structural modifications in PNA backbone and nucleobases to enhance strand invasion. (<bold>A</bold>
) Hydrogen bonding of C<sup>+</sup>
GC and JGC triplets (<bold>B</bold>
) PNA and gamma(γ) modified PNA monomers (<bold>C</bold>
) A:T, Dap:T, and A:sU hydrogen binding pairs</p>
</caption>
<graphic xlink:href="molecules-25-00735-g003"></graphic>
</fig>
<table-wrap id="molecules-25-00735-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">molecules-25-00735-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>Guidelines for Triplex PNA Design for Gene Editing</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Guidelines for Triplex PNA Design for Gene Editing</th>
</tr>
</thead>
<tbody><tr><td align="left" valign="middle" rowspan="1" colspan="1"><list list-type="bullet"><list-item><p>Target polypurine (A or G) sequence stretches in proximity to modification of interest, ideally ≥ 7 consecutive bases and within 500 bp of intended edit</p>
</list-item>
</list>
</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1"><list list-type="bullet"><list-item><p>PNA design: ≥20 Watson–Crick base stretch followed by flexible linker sequence and antiparallel triplex-forming Hoogsteen base stretch corresponding to polypurine target, three lysine residue cap at each N and C-terminus</p>
</list-item>
</list>
</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1"><list list-type="bullet"><list-item><p>PNA modification: consider introduction of gamma (γ) modified PNA monomers distributed throughout sequence</p>
</list-item>
</list>
</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1"><list list-type="bullet"><list-item><p>ssDNA donor: 60 mer single-stranded DNA oligonucleotide with centered modification sequence and three terminal phosphorothioate backbone modifications on 3′ and 5′ ends</p>
</list-item>
</list>
</td>
</tr>
<tr><td align="left" valign="middle" rowspan="1" colspan="1"><list list-type="bullet"><list-item><p>Nanoparticle encapsulation at 2:1 PNA:DNA ratio</p>
</list-item>
</list>
</td>
</tr>
<tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><list list-type="bullet"><list-item><p>If possible, screen multiple candidate PNA target sequences and modification approaches for optimal editing activity</p>
</list-item>
</list>
</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list></list>
<tree><noCountry><name sortKey="Economos, Nicholas G" sort="Economos, Nicholas G" uniqKey="Economos N" first="Nicholas G." last="Economos">Nicholas G. Economos</name>
<name sortKey="Glazer, Peter M" sort="Glazer, Peter M" uniqKey="Glazer P" first="Peter M." last="Glazer">Peter M. Glazer</name>
<name sortKey="Oyaghire, Stanley" sort="Oyaghire, Stanley" uniqKey="Oyaghire S" first="Stanley" last="Oyaghire">Stanley Oyaghire</name>
<name sortKey="Quijano, Elias" sort="Quijano, Elias" uniqKey="Quijano E" first="Elias" last="Quijano">Elias Quijano</name>
<name sortKey="Ricciardi, Adele S" sort="Ricciardi, Adele S" uniqKey="Ricciardi A" first="Adele S." last="Ricciardi">Adele S. Ricciardi</name>
<name sortKey="Saltzman, W Mark" sort="Saltzman, W Mark" uniqKey="Saltzman W" first="W. Mark" last="Saltzman">W. Mark Saltzman</name>
</noCountry>
</tree>
</affiliations>
</record>
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