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Current Organic Synthesis

Editor-in-Chief

ISSN (Print): 1570-1794
ISSN (Online): 1875-6271

Mini-Review Article

Triazole-linked Nucleic Acids: Synthesis, Therapeutics and Synthetic Biology Applications

Author(s): Vivek K. Sharma*, Priyanka Mangla, Sunil K. Singh and Ashok K. Prasad

Volume 21, Issue 4, 2024

Published on: 12 July, 2023

Page: [436 - 455] Pages: 20

DOI: 10.2174/1570179420666230502123950

Price: $65

Abstract

This article covers the triazole-linked nucleic acids where the triazole linkage (TL) replaces the natural phosphate backbone. The replacement is done at either a few selected linkages or all the phosphate linkages. Two triazole linkages, the four-atom TL1 and the six-atom TL2, have been discussed in detail. These triazole-modified oligonucleotides have found a wide range of applications, from therapeutics to synthetic biology. For example, the triazole-linked oligonucleotides have been used in the antisense oligonucleotide (ASO), small interfering RNA (siRNA) and clustered regularly interspaced short palindromic repeats (CRISPR)-Cas9 technology as therapeutic agents. Due to the ease of the synthesis and a wide range of biocompatibility, the triazole linkage TL2 has been used to assemble a functional 300-mer DNA from alkyne- and azide-functionalized 100-mer oligonucleotides as well as an epigenetically modified variant of a 335 base-pair gene from ten short oligonucleotides. These outcomes highlight the potential of triazole-linked nucleic acids and open the doors for other TL designs and artificial backbones to fully exploit the vast potential of artificial nucleic acids in therapeutics, synthetic biology and biotechnology.

Keywords: Phosphate backbone modifications, triazole-linkage, triazole-modified oligonucleotides, locked nucleic acid (LNA), ASO, siRNA, CRISPR, synthetic genes.

Graphical Abstract
[1]
Minchin, S.; Lodge, J. Understanding biochemistry: Structure and function of nucleic acids. Essays Biochem., 2019, 63(4), 433-456.
[http://dx.doi.org/10.1042/EBC20180038] [PMID: 31652314]
[2]
Watson, J.D.; Crick, F.H.C. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature, 1953, 171(4356), 737-738.
[http://dx.doi.org/10.1038/171737a0] [PMID: 13054692]
[3]
Crick, F.H.C.; Barnett, L.; Brenner, S.; Watts-Tobin, R.J. General nature of the genetic code for proteins. Nature, 1961, 192(4809), 1227-1232.
[http://dx.doi.org/10.1038/1921227a0] [PMID: 13882203]
[4]
McCarty, M. Discovering genes are made of DNA. Nature, 2003, 421(6921), 406.
[http://dx.doi.org/10.1038/nature01398] [PMID: 12540908]
[5]
Polack, F.P. Thomas, S.J.; Kitchin, N.; Absalon, J.; Gurtman, A.; Lockhart, S.; Perez, J.L.; Pérez Marc, G.; Moreira, E.D.; Zerbini, C.; Bailey, R.; Swanson, K.A.; Roychoudhury, S.; Koury, K.; Li, P.; Kalina, W.V.; Cooper, D.; Frenck, R.W., Jr; Hammitt, L.L.; Türeci, Ö.; Nell, H.; Schaefer, A.; Ünal, S.; Tresnan, D.B.; Mather, S.; Dormitzer, P.R.; Şahin, U.; Jansen, K.U.; Gruber, W.C. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N. Engl. J. Med., 2020, 383(27), 2603-2615.
[http://dx.doi.org/10.1056/NEJMoa2034577] [PMID: 33301246]
[6]
Baden, L.R.; El Sahly, H.M.; Essink, B.; Kotloff, K.; Frey, S.; Novak, R.; Diemert, D.; Spector, S.A.; Rouphael, N.; Creech, C.B.; McGettigan, J.; Khetan, S.; Segall, N.; Solis, J.; Brosz, A.; Fierro, C.; Schwartz, H.; Neuzil, K.; Corey, L.; Gilbert, P.; Janes, H.; Follmann, D.; Marovich, M.; Mascola, J.; Polakowski, L.; Ledgerwood, J.; Graham, B.S.; Bennett, H.; Pajon, R.; Knightly, C.; Leav, B.; Deng, W.; Zhou, H.; Han, S.; Ivarsson, M.; Miller, J.; Zaks, T. Efficacy and Safety of the mRNA-1273 SARS-CoV-2 Vaccine. N. Engl. J. Med., 2021, 384(5), 403-416.
[http://dx.doi.org/10.1056/NEJMoa2035389] [PMID: 33378609]
[7]
Deoxyribonucleic Acid (DNA). Available from: https://www.genome.gov/genetics-glossary/Deoxyribonucleic-Acid
[8]
Freier, S.; Altmann, K-H. The ups and downs of nucleic acid duplex stability: Structure-stability studies on chemically-modified DNA:RNA duplexes. Nucleic Acids Res., 1997, 25(22), 4429-4443.
[http://dx.doi.org/10.1093/nar/25.22.4429] [PMID: 9358149]
[9]
Rostovtsev, V.V.; Green, L.G.; Fokin, V.V.; Sharpless, K.B. A stepwise huisgen cycloaddition process: Copper(I)-catalyzed regioselective “ligation” of azides and terminal alkynes. Angew. Chem. Int. Ed., 2002, 41(14), 2596-2599.
[http://dx.doi.org/10.1002/1521-3773(20020715)41:14<2596:AID-ANIE2596>3.0.CO;2-4] [PMID: 12203546]
[10]
Tornøe, C.W.; Christensen, C.; Meldal, M. Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(i)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem., 2002, 67(9), 3057-3064.
[http://dx.doi.org/10.1021/jo011148j] [PMID: 11975567]
[11]
El-Sagheer, A.H.; Brown, T. Click chemistry with DNA. Chem. Soc. Rev., 2010, 39(4), 1388-1405.
[http://dx.doi.org/10.1039/b901971p] [PMID: 20309492]
[12]
El-Sagheer, A.H.; Brown, T. Click nucleic acid ligation: Applications in biology and nanotechnology. Acc. Chem. Res., 2012, 45(8), 1258-1267.
[http://dx.doi.org/10.1021/ar200321n] [PMID: 22439702]
[13]
Isobe, H.; Fujino, T. Triazole-linked analogues of DNA and RNA ((TL)DNA and (TL)RNA): Synthesis and functions. Chem. Rec., 2014, 14(1), 41-51.
[http://dx.doi.org/10.1002/tcr.201300023] [PMID: 24734308]
[14]
Fantoni, N.Z.; El-Sagheer, A.H.; Brown, T. A Hitchhiker’s guide to click-chemistry with nucleic acids. Chem. Rev., 2021, 121(12), 7122-7154.
[http://dx.doi.org/10.1021/acs.chemrev.0c00928] [PMID: 33443411]
[15]
Qiu, J.; El-Sagheer, A.H.; Brown, T. Solid phase click ligation for the synthesis of very long oligonucleotides. Chem. Commun., 2013, 49(62), 6959-6961.
[http://dx.doi.org/10.1039/c3cc42451k] [PMID: 23814786]
[16]
Epple, S.; El-Sagheer, A.H.; Brown, T. Artificial nucleic acid backbones and their applications in therapeutics, synthetic biology and biotechnology. Emerg. Top. Life Sci., 2021, 5(5), 691-697.
[http://dx.doi.org/10.1042/ETLS20210169] [PMID: 34297063]
[17]
Kukwikila, M.; Gale, N.; El-Sagheer, A.H.; Brown, T.; Tavassoli, A. Assembly of a biocompatible triazole-linked gene by one-pot click-DNA ligation. Nat. Chem., 2017, 9(11), 1089-1098.
[http://dx.doi.org/10.1038/nchem.2850] [PMID: 29064492]
[18]
Sharma, V.K.; Singh, S.K.; Krishnamurthy, P.M.; Alterman, J.F.; Haraszti, R.A.; Khvorova, A.; Prasad, A.K.; Watts, J.K. Synthesis and biological properties of triazole-linked locked nucleic acid. Chem. Commun., 2017, 53(63), 8906-8909.
[http://dx.doi.org/10.1039/C7CC04092J] [PMID: 28736781]
[19]
Varizhuk, A.; Chizhov, A.; Smirnov, I.; Kaluzhny, D.; Florentiev, V. Triazole-linked oligonucleotides with mixed-base sequences: Synthesis and hybridization properties. Eur. J. Org. Chem., 2012, 2012(11), 2173-2179.
[http://dx.doi.org/10.1002/ejoc.201101700]
[20]
Watts, J.K.; Corey, D.R. Silencing disease genes in the laboratory and the clinic. J. Pathol., 2012, 226(2), 365-379.
[http://dx.doi.org/10.1002/path.2993] [PMID: 22069063]
[21]
Farzan, V.M.; Ulashchik, E.A.; Martynenko-Makaev, Y.V.; Kvach, M.V.; Aparin, I.O.; Brylev, V.A.; Prikazchikova, T.A.; Maklakova, S.Y.; Majouga, A.G.; Ustinov, A.V.; Shipulin, G.A.; Shmanai, V.V.; Korshun, V.A.; Zatsepin, T.S. Automated solid-phase click synthesis of oligonucleotide conjugates: From small molecules to diverse N -Acetylgalactosamine clusters. Bioconjug. Chem., 2017, 28(10), 2599-2607.
[http://dx.doi.org/10.1021/acs.bioconjchem.7b00462] [PMID: 28921968]
[22]
Sharma, V.K.; Osborn, M.F.; Hassler, M.R.; Echeverria, D.; Ly, S.; Ulashchik, E.A.; Martynenko-Makaev, Y.V.; Shmanai, V.V.; Zatsepin, T.S.; Khvorova, A.; Watts, J.K. Novel cluster and monomer-based GalNAc structures induce effective uptake of siRNAs in vitro and in vivo. Bioconjug. Chem., 2018, 29(7), 2478-2488.
[http://dx.doi.org/10.1021/acs.bioconjchem.8b00365] [PMID: 29898368]
[23]
El-Sagheer, A.H.; Sanzone, A.P.; Gao, R.; Tavassoli, A.; Brown, T. Biocompatible artificial DNA linker that is read through by DNA polymerases and is functional in Escherichia coli. Proc. Natl. Acad. Sci. USA, 2011, 108(28), 11338-11343.
[http://dx.doi.org/10.1073/pnas.1101519108] [PMID: 21709264]
[24]
Taemaitree, L.; Shivalingam, A.; El-Sagheer, A.H.; Brown, T. An artificial triazole backbone linkage provides a split-and-click strategy to bioactive chemically modified CRISPR sgRNA. Nat. Commun., 2019, 10(1), 1610.
[http://dx.doi.org/10.1038/s41467-019-09600-4] [PMID: 30962447]
[25]
Zamecnik, P.C.; Stephenson, M.L. Inhibition of Rous sarcoma virus replication and cell transformation by a specific oligodeoxynucleotide. Proc. Natl. Acad. Sci. USA, 1978, 75(1), 280-284.
[http://dx.doi.org/10.1073/pnas.75.1.280] [PMID: 75545]
[26]
Stephenson, M.L.; Zamecnik, P.C. Inhibition of Rous sarcoma viral RNA translation by a specific oligodeoxyribonucleotide. Proc. Natl. Acad. Sci. USA, 1978, 75(1), 285-288.
[http://dx.doi.org/10.1073/pnas.75.1.285] [PMID: 75546]
[27]
Bennett, C.F.; Swayze, E.E. RNA targeting therapeutics: Molecular mechanisms of antisense oligonucleotides as a therapeutic platform. Annu. Rev. Pharmacol. Toxicol., 2010, 50(1), 259-293.
[http://dx.doi.org/10.1146/annurev.pharmtox.010909.105654] [PMID: 20055705]
[28]
Sharma, V.K.; Rungta, P.; Prasad, A.K. Nucleic acid therapeutics: Basic concepts and recent developments. RSC Advances, 2014, 4(32), 16618-16631.
[http://dx.doi.org/10.1039/c3ra47841f]
[29]
Shen, X.; Corey, D.R. Chemistry, mechanism and clinical status of antisense oligonucleotides and duplex RNAs. Nucleic Acids Res., 2018, 46(4), 1584-1600.
[http://dx.doi.org/10.1093/nar/gkx1239] [PMID: 29240946]
[30]
Sharma, V.K.; Olety, B.; Prasad, A.K. Chapter Sixteen - N-acetylgalactosamine (GalNAc)-conjugates: Delivering oligonucleotide drugs to the liver. In: Carbohydrates in Drug Discovery and Development; Tiwari, V.K., Ed.; Elsevier, 2020; pp. 641-667.
[http://dx.doi.org/10.1016/B978-0-12-816675-8.00016-6]
[31]
Lima, W.F.; Prakash, T.P.; Murray, H.M.; Kinberger, G.A.; Li, W.; Chappell, A.E.; Li, C.S.; Murray, S.F.; Gaus, H.; Seth, P.P.; Swayze, E.E.; Crooke, S.T. Single-stranded siRNAs activate RNAi in animals. Cell, 2012, 150(5), 883-894.
[http://dx.doi.org/10.1016/j.cell.2012.08.014] [PMID: 22939618]
[32]
Khvorova, A.; Watts, J.K. The chemical evolution of oligonucleotide therapies of clinical utility. Nat. Biotechnol., 2017, 35(3), 238-248.
[http://dx.doi.org/10.1038/nbt.3765] [PMID: 28244990]
[33]
Watts, J.K. The medicinal chemistry of antisense oligonucleotides. In: Oligonucleotide‐Based Drugs and Therapeutics; , 2018; pp. 39-89.
[http://dx.doi.org/10.1002/9781119070153.ch2]
[34]
Sharma, V.K.; Sharma, R.K.; Singh, S.K. Antisense oligonucleotides: Modifications and clinical trials. MedChemComm, 2014, 5(10), 1454-1471.
[http://dx.doi.org/10.1039/C4MD00184B]
[35]
Sharma, V.K.; Watts, J.K. Oligonucleotide therapeutics: Chemistry, delivery and clinical progress. Future Med. Chem., 2015, 7(16), 2221-2242.
[http://dx.doi.org/10.4155/fmc.15.144] [PMID: 26510815]
[36]
Eckstein, F. Phosphorothioate oligodeoxynucleotides: What is their origin and what is unique about them? Antisense Nucleic Acid Drug Dev., 2000, 10(2), 117-121.
[http://dx.doi.org/10.1089/oli.1.2000.10.117] [PMID: 10805163]
[37]
Eckstein, F. Phosphorothioates, essential components of therapeutic oligonucleotides. Nucleic Acid Ther., 2014, 24(6), 374-387.
[http://dx.doi.org/10.1089/nat.2014.0506] [PMID: 25353652]
[38]
Liang, X.; Sun, H.; Shen, W.; Crooke, S.T. Identification and characterization of intracellular proteins that bind oligonucleotides with phosphorothioate linkages. Nucleic Acids Res., 2015, 43(5), 2927-2945.
[http://dx.doi.org/10.1093/nar/gkv143] [PMID: 25712094]
[39]
Vickers, T.A.; Rahdar, M.; Prakash, T.P.; Crooke, S.T. Kinetic and subcellular analysis of PS-ASO/protein interactions with P54nrb and RNase H1. Nucleic Acids Res., 2019, 47(20), 10865-10880.
[http://dx.doi.org/10.1093/nar/gkz771] [PMID: 31495875]
[40]
Micklefield, J. Backbone modification of nucleic acids: Synthesis, structure and therapeutic applications. Curr. Med. Chem., 2001, 8(10), 1157-1179.
[http://dx.doi.org/10.2174/0929867013372391] [PMID: 11472234]
[41]
Meade, B.R.; Gogoi, K.; Hamil, A.S.; Palm-Apergi, C.; Berg, A.; Hagopian, J.C.; Springer, A.D.; Eguchi, A.; Kacsinta, A.D.; Dowdy, C.F.; Presente, A.; Lönn, P.; Kaulich, M.; Yoshioka, N.; Gros, E.; Cui, X.S.; Dowdy, S.F. Efficient delivery of RNAi prodrugs containing reversible charge-neutralizing phosphotriester backbone modifications. Nat. Biotechnol., 2014, 32(12), 1256-1261.
[http://dx.doi.org/10.1038/nbt.3078] [PMID: 25402614]
[42]
Verma, S.; Eckstein, F. Modified oligonucleotides: Synthesis and strategy for users. Annu. Rev. Biochem., 1998, 67(1), 99-134.
[http://dx.doi.org/10.1146/annurev.biochem.67.1.99] [PMID: 9759484]
[43]
Fujino, T.; Suzuki, T.; Okada, K.; Kogashi, K.; Yasumoto, K.; Sogawa, K.; Isobe, H. Chimeric RNA oligonucleotides incorporating triazole-linked trinucleotides: Synthesis and function as mRNA in cell-free translation reactions. J. Org. Chem., 2016, 81(19), 8967-8976.
[http://dx.doi.org/10.1021/acs.joc.6b01618] [PMID: 27579606]
[44]
Dallmann, A.; El-Sagheer, A.H.; Dehmel, L.; Mügge, C.; Griesinger, C.; Ernsting, N.P.; Brown, T. Structure and dynamics of triazole-linked DNA: biocompatibility explained. Chemistry, 2011, 17(52), 14714-14717.
[http://dx.doi.org/10.1002/chem.201102979] [PMID: 22131102]
[45]
El-Sagheer, A.H.; Brown, T. A triazole linkage that mimics the DNA phosphodiester group in living systems. Q. Rev. Biophys., 2015, 48(4), 429-436.
[http://dx.doi.org/10.1017/S0033583515000141] [PMID: 26537402]
[46]
Perrone, D.; Marchesi, E.; Preti, L.; Navacchia, M.L. Modified nucleosides, nucleotides and nucleic acids via click azide-alkyne cycloaddition for pharmacological applications. Molecules, 2021, 26(11), 3100.
[http://dx.doi.org/10.3390/molecules26113100] [PMID: 34067312]
[47]
Baraniak, D.; Boryski, J. Triazole-modified nucleic acids for the application in bioorganic and medicinal chemistry. Biomedicines, 2021, 9(6), 628.
[http://dx.doi.org/10.3390/biomedicines9060628] [PMID: 34073038]
[48]
Isobe, H.; Fujino, T.; Yamazaki, N.; Guillot-Nieckowski, M.; Nakamura, E. Triazole-linked analogue of deoxyribonucleic acid ((TL) DNA): Design, synthesis, and double-strand formation with natural DNA. Org. Lett., 2008, 10(17), 3729-3732.
[http://dx.doi.org/10.1021/ol801230k] [PMID: 18656947]
[49]
Sanzone, A.P.; El-Sagheer, A.H.; Brown, T.; Tavassoli, A. Assessing the biocompatibility of click-linked DNA in Escherichia coli. Nucleic Acids Res., 2012, 40(20), 10567-10575.
[http://dx.doi.org/10.1093/nar/gks756] [PMID: 22904087]
[50]
Fujino, T.; Yamazaki, N.; Isobe, H. Convergent synthesis of oligomers of triazole-linked DNA analogue (TLDNA) in solution phase. Tetrahedron Lett., 2009, 50(28), 4101-4103.
[http://dx.doi.org/10.1016/j.tetlet.2009.04.101]
[51]
Fujino, T.; Yamazaki, N.; Hasome, A.; Endo, K.; Isobe, H. Efficient and improved synthesis of triazole-linked DNA (TLDNA) oligomers. Tetrahedron Lett., 2012, 53(7), 868-870.
[http://dx.doi.org/10.1016/j.tetlet.2011.12.026]
[52]
Fujino, T.; Tsunaka, N.; Guillot-Nieckowski, M.; Nakanishi, W.; Iwamoto, T.; Nakamura, E.; Isobe, H. Synthesis and structures of deoxyribonucleoside analogues for triazole-linked DNA (TLDNA). Tetrahedron Lett., 2010, 51(15), 2036-2038.
[http://dx.doi.org/10.1016/j.tetlet.2010.02.046]
[53]
Fujino, T.; Suzuki, T.; Ooi, T.; Ikemoto, K.; Isobe, H. Duplex-forming Oligonucleotide of Triazole-linked RNA. Chem. Asian J., 2019, 14(19), 3380-3385.
[http://dx.doi.org/10.1002/asia.201901112] [PMID: 31478313]
[54]
Fujino, T.; Yasumoto, K.; Yamazaki, N.; Hasome, A.; Sogawa, K.; Isobe, H. Triazole-linked DNA as a primer surrogate in the synthesis of first-strand cDNA. Chem. Asian J., 2011, 6(11), 2956-2960.
[http://dx.doi.org/10.1002/asia.201100712] [PMID: 21913333]
[55]
Fujino, T.; Miyauchi, Y.; Tsunaka, N.; Okada, K.; Isobe, H. Post-modification of triazole-linked analogues of dna for positively charged variants. Heterocycles, 2013, 87(5), 6.
[56]
Fujino, T.; Kogashi, K.; Okada, K.; Mattarella, M.; Suzuki, T.; Yasumoto, K.; Sogawa, K.; Isobe, H. Chimeric RNA oligonucleotides with triazole and phosphate linkages: Synthesis and RNA interference. Chem. Asian J., 2015, 10(12), 2683-2688.
[http://dx.doi.org/10.1002/asia.201500765] [PMID: 26248050]
[57]
El-Sagheer, A.H.; Brown, T. Combined nucleobase and backbone modifications enhance DNA duplex stability and preserve biocompatibility. Chem. Sci., 2014, 5(1), 253-259.
[http://dx.doi.org/10.1039/C3SC51753E]
[58]
Singh, S.; Sharma, V.; Bohra, K.; Olsen, C.; Prasad, A. Synthesis of Triazole-linked LNA-based non-ionic nucleoside dimers using Cu (I)- Catalyzed ‘Click’ reaction. Curr. Org. Synth., 2014, 11(5), 757-766.
[http://dx.doi.org/10.2174/1570179411666140204155505]
[59]
Obika, S.; Nanbu, D.; Hari, Y.; Andoh, J.; Morio, K.; Doi, T.; Imanishi, T. Stability and structural features of the duplexes containing nucleoside analogues with a fixed N-type conformation, 2′--O,4′--C-methyleneribonucleosides. Tetrahedron Lett., 1998, 39(30), 5401-5404.
[http://dx.doi.org/10.1016/S0040-4039(98)01084-3]
[60]
Obika, S.; Nanbu, D.; Hari, Y.; Morio, K. In, Y.; Ishida, T.; Imanishi, T. Synthesis of 2′-O, 4′-C-methyleneuridine and -cytidine. Novel bicyclic nucleosides having a fixed C3, -endo sugar puckering. Tetrahedron Lett., 1997, 38(50), 8735-8738.
[http://dx.doi.org/10.1016/S0040-4039(97)10322-7]
[61]
Singh, S.K.; Koshkin, A.A.; Wengel, J.; Nielsen, P. LNA (locked nucleic acids): Synthesis and high-affinity nucleic acid recognition. Chem. Commun., 1998, (4), 455-456.
[http://dx.doi.org/10.1039/a708608c]
[62]
Koshkin, A.A.; Singh, S.K.; Nielsen, P.; Rajwanshi, V.K.; Kumar, R.; Meldgaard, M.; Olsen, C.E.; Wengel, J. LNA (Locked Nucleic Acids): Synthesis of the adenine, cytosine, guanine, 5-methylcytosine, thymine and uracil bicyclonucleoside monomers, oligomerisation, and unprecedented nucleic acid recognition. Tetrahedron, 1998, 54(14), 3607-3630.
[http://dx.doi.org/10.1016/S0040-4020(98)00094-5]
[63]
Lundin, K.E.; Højland, T.; Hansen, B.R.; Persson, R.; Bramsen, J.B.; Kjems, J.; Koch, T.; Wengel, J.; Smith, C.I.E. Biological activity and biotechnological aspects of locked nucleic acids. Adv. Genet., 2013, 82, 47-107.
[http://dx.doi.org/10.1016/B978-0-12-407676-1.00002-0] [PMID: 23721720]
[64]
Wengel, J. Synthesis of 3‘- C - and 4‘- C -branched oligodeoxynucleotides and the development of Locked Nucleic Acid (LNA). Acc. Chem. Res., 1999, 32(4), 301-310.
[http://dx.doi.org/10.1021/ar980051p]
[65]
Sharma, V.K.; Kumar, M.; Olsen, C.E.; Prasad, A.K. Chemoenzymatic convergent synthesis of 2′-O, 4′-C-methyleneribonucleosides. J. Org. Chem., 2014, 79(13), 6336-6341.
[http://dx.doi.org/10.1021/jo5008338] [PMID: 24901539]
[66]
Sharma, V.K.; Rungta, P.; Maikhuri, V.K.; Prasad, A.K. An astute synthesis of locked nucleic acid monomers. Sustain. Chem. Process., 2015, 3(1), 2.
[http://dx.doi.org/10.1186/s40508-015-0028-3]
[67]
Li, L.; Shen, X.; Liu, Z.; Norrbom, M.; Prakash, T.P.; O’Reilly, D.; Sharma, V.K.; Damha, M.J.; Watts, J.K.; Rigo, F.; Corey, D.R. Activation of frataxin protein expression by antisense oligonucleotides targeting the mutant expanded repeat. Nucleic Acid Ther., 2018, 28(1), 23-33.
[http://dx.doi.org/10.1089/nat.2017.0703] [PMID: 29341839]
[68]
Kumar, P.; El-Sagheer, A.H.; Truong, L.; Brown, T. Locked nucleic acid (LNA) enhances binding affinity of triazole-linked DNA towards RNA. Chem. Commun., 2017, 53(63), 8910-8913.
[http://dx.doi.org/10.1039/C7CC05159J] [PMID: 28748236]
[69]
Kumar, P.; Truong, L.; Baker, Y.R.; El-Sagheer, A.H.; Brown, T. Synthesis, affinity for complementary RNA and DNA, and enzymatic stability of triazole-linked locked nucleic acids (t-LNAs). ACS Omega, 2018, 3(6), 6976-6987.
[http://dx.doi.org/10.1021/acsomega.8b01086] [PMID: 29978149]
[70]
Birts, C.N.; Sanzone, A.P.; El-Sagheer, A.H.; Blaydes, J.P.; Brown, T.; Tavassoli, A. Transcription of click-linked DNA in human cells. Angew. Chem. Int. Ed., 2014, 53(9), 2362-2365.
[http://dx.doi.org/10.1002/anie.201308691] [PMID: 24452865]
[71]
Shivalingam, A.; Tyburn, A.E.S.; El-Sagheer, A.H.; Brown, T. Molecular requirements of high-fidelity replication-competent DNA backbones for orthogonal chemical ligation. J. Am. Chem. Soc., 2017, 139(4), 1575-1583.
[http://dx.doi.org/10.1021/jacs.6b11530] [PMID: 28097865]
[72]
El-Sagheer, A.H.; Brown, T. Efficient RNA synthesis by in vitro transcription of a triazole-modified DNA template. Chem. Commun., 2011, 47(44), 12057-12058.
[http://dx.doi.org/10.1039/c1cc14316f] [PMID: 21961113]
[73]
El-Sagheer, A.H.; Brown, T. New strategy for the synthesis of chemically modified RNA constructs exemplified by hairpin and hammerhead ribozymes. Proc. Natl. Acad. Sci. USA, 2010, 107(35), 15329-15334.
[http://dx.doi.org/10.1073/pnas.1006447107] [PMID: 20713730]
[74]
Doudna, J.A.; Charpentier, E. The new frontier of genome engineering with CRISPR-Cas9. Science, 2014, 346(6213), 1258096.
[http://dx.doi.org/10.1126/science.1258096] [PMID: 25430774]
[75]
Jinek, M.; Chylinski, K.; Fonfara, I.; Hauer, M.; Doudna, J.A.; Charpentier, E. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science, 2012, 337(6096), 816-821.
[76]
Jiang, F.; Zhou, K.; Ma, L.; Gressel, S.; Doudna, J.A.A. Cas9–guide RNA complex preorganized for target DNA recognition. Science, 2015, 348(6242), 1477-1481.
[http://dx.doi.org/10.1126/science.aab1452] [PMID: 26113724]
[77]
Hsu, P.D.; Scott, D.A.; Weinstein, J.A.; Ran, F.A.; Konermann, S.; Agarwala, V.; Li, Y.; Fine, E.J.; Wu, X.; Shalem, O.; Cradick, T.J.; Marraffini, L.A.; Bao, G.; Zhang, F. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol., 2013, 31(9), 827-832.
[http://dx.doi.org/10.1038/nbt.2647] [PMID: 23873081]
[78]
Ledford, H.; Callaway, E. Pioneers of revolutionary CRISPR gene editing win chemistry Nobel. Nature, 2020, 586(7829), 346-347.
[http://dx.doi.org/10.1038/d41586-020-02765-9] [PMID: 33028993]
[79]
He, K.; Chou, E.T.; Begay, S.; Anderson, E.M.; van Brabant Smith, A. Conjugation and evaluation of triazole-linked single guide RNA for CRISPR-Cas9 gene editing. ChemBioChem, 2016, 17(19), 1809-1812.
[http://dx.doi.org/10.1002/cbic.201600320] [PMID: 27441384]

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