Subscribe to RSS
DOI: 10.1055/a-2219-6680
Expansion of Genetic Alphabets: Designer Nucleobases and Their Applications
The authors thank the Department of Biotechnology (DBT), Ministry of Science and Technology, India [BT/PR5169/BMB/2015/39 and BT/PR5169/BRB/10/1065/2012] and the Department of Science and Technology (DST), [SR/SI/OC-69/2008] Govt. of India, for financial support.
Abstract
All living things use DNA and RNA to store, retrieve, and transmit their genetic information. The complementary Watson–Crick nucleobase-pairs (A/T and G/C base-pairs), have been documented for years as being essential for the integrity of the DNA double helix and also for replication and transcription. With only four poorly fluorescent naturally occurring nucleic acid bases (namely A, G, T/U, and C), the extraction of genetic information is difficult. Further, the chemical diversity of DNA and RNA is severely limited. Deoxyribose/ribose-phosphate backbones also constrain DNA and RNA characteristics and have poor chemical and physiological stability, which significantly restricts the practical applications of DNA and RNA. Over the years, extensively modified nucleobase pairs with novel base-pairing properties have been synthesized. Such designer nucleobases, serving as an expanded genetic alphabet, have been used for the design and synthesis of DNA and RNA analogues with tailored informational/functional properties. Recent developments in the production of synthetic unnatural base pairs pave the way for xenobiology research and genetic alphabet expansion technology. In this review, we present a brief history of the development of several hydrogen- and non-hydrogen-bonded unnatural base pairs and their applications. We also highlight our work in designing and synthesizing a new class of triazolyl unnatural nucleosides that offer a unique charge-transfer (CT) complexation force towards stabilizing DNA-duplexes when incorporated into short oligonucleotide sequences.
Key words
genetic alphabet expansion - unnatural nucleobase pairs - triazolyl nucleosides - tetrazolyl nucleosides - fluorescent nucleobases - nucleic acidsPublication History
Received: 16 August 2023
Accepted after revision: 29 November 2023
Accepted Manuscript online:
29 November 2023
Article published online:
22 January 2024
© 2023. Thieme. All rights reserved
Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany
-
References and Notes
- 1 Wojciechowski F, Leumann CJ. Chem. Soc. Rev. 2011; 40: 5669
- 2 Switzer C, Moroney SE, Benner SA. J. Am. Chem. Soc. 1989; 111: 8322
- 3 Bain JD, Switzer C, Chamberlin R, Benner SA. Nature 1992; 356: 537
- 4 Schweitzer BA, Kool ET. J. Org. Chem. 1994; 59: 7238
- 5 Hirao I, Kimoto M, Mitsui T, Fujiwara T, Kawai R, Sato A, Harada Y, Yokoyama S. Nat. Methods 2006; 3: 729
- 6 Malyshev DA, Seo YJ, Ordoukhanian P, Romesberg FE. J. Am. Chem. Soc. 2009; 131: 14620
- 7 Manandhar M, Chun E, Romesberg FE. J. Am. Chem. Soc. 2021; 143: 4859
- 8 Malyshev DA, Dhami K, Lavergne T, Chen T, Dai N, Foster JM, Corrêa IR, Romesberg FE. Nature 2014; 509: 385
- 9 Jurczyk SC, Kodra JT, Park J, Benner SA, Battersby TR. Helv. Chim. Acta 1999; 82: 1005
- 10 Kool ET. Curr. Opin. Chem. Biol. 2000; 4: 602
- 11 Hutter D, Benner SA. J. Org. Chem. 2003; 68: 9839
- 12 Yang Z, Hutter D, Sheng P, Sismour AM, Benner SA. Nucleic Acids Res. 2006; 34: 6095
- 13 Sheng P, Yang Z, Kim Y, Wu Y, Tan W, Benner SA. Chem. Commun. 2008; 5128
- 14 Yang Z, Sismour A, Sheng P, Puskar NL, Benner SA. Nucleic Acids Res. 2007; 35: 4238
- 15 Ohtsuki T, Kimoto M, Ishikawa M, Mitsui T, Hirao I, Yokoyama S. Proc. Natl. Acad. Sci. USA 2001; 98: 4922
- 16 Hirao I. Curr. Opin. Chem. Biol. 2006; 10: 622
- 17 Minakawa N, Ogata S, Takahashi M, Matsuda A. J. Am. Chem. Soc. 2009; 131: 1644
- 18 Hikishima S, Minakawa N, Kuramoto K, Fujisawa Y, Ogawa M, Matsuda A. Angew. Chem. Int. Ed. 2005; 44: 596
- 19 Liu H, Gao J, Lynch SR, Saito YD, Maynard L, Kool ET. Science 2003; 302: 868
- 20 Lu H, He K, Kool ET. Angew. Chem. Int. Ed. 2004; 43: 5834
- 21 Delaney JC, Gao J, Liu H, Shrivastav N, Essigmann JM, Kool ET. Angew. Chem. Int. Ed. 2009; 121: 4524
- 22 Kim TW, Kool ET. Org. Lett. 2004; 6: 3949
- 23 Morales JC, Kool ET. J. Am. Chem. Soc. 1999; 121: 2323
- 24 Kool ET. Annu. Rev. Biochem. 2002; 71: 191
- 25 Matray TJ, Kool ET. J. Am. Chem. Soc. 1998; 120: 6191
- 26 Smirnov S, Matray TJ, Kool ET, de los Santos C. Nucleic Acids Res. 2002; 30: 5561
- 27 Mitsui T, Kitamura A, Kimoto M, To T, Sato A, Hirao I, Yokoyama S. J. Am. Chem. Soc. 2003; 125: 5298
- 28 Kimoto M, Kawai R, Mitsui TS, Yokoyama I, Hirao I. Nucleic Acids Res. 2009; 37: e14
- 29 McMinn DL, Ogawa AK, Wu YQ, Liu JQ, Schultz PG, Romesberg FE. J. Am. Chem. Soc. 1999; 121: 11585
- 30 Ray SS, Kuruma M. Halogen-Free Flame-Retardant Polymers: Next-Generation Fillers for Polymer Nanocomposite Applications, Vol. 294. Springer Nature; Amsterdam: 2019
- 31 Matsuda S, Leconte AM, Romesberg FE. J. Am. Chem. Soc. 2007; 129: 5551
- 32 Leconte AM, Hwang GT, Matsuda S, Capek P, Hari Y, Romesberg FE. J. Am. Chem. Soc. 2008; 130: 2336
- 33 Seo YJ, Hwang GT, Ordoukhanian P, Romesberg FE. J. Am. Chem. Soc. 2009; 131: 3246
- 34 Bong D, Holliger P, Yang C. RSC Chem. Biol. 2022; 3: 1299
- 35 Hasegawa T, Shoji A, Kuwahara M, Ozaki H, Sawai H. In Nucleic Acids Symposium Series, Vol. 50. Oxford University Press; Oxford: 2006: 145
- 36 Kuwahara M, Suto Y, Minezaki S, Kitagata R, Nagashima J, Sawai H. In Nucleic Acids Symposium Series, Vol. 50. Oxford University Press; Oxford: 2006: 31
- 37 Hocek M, Fojta M. Chem. Soc. Rev. 2011; 40: 5802
- 38 Weisbrod SH, Marx A. Chem. Commun. 2008; 5675
- 39 Brudno Y, Liu DR. Chem. Biol. 2009; 16: 265
- 40 Ramsay N, Jemth A.-S, Brown A, Crampton N, Dear P, Holliger P. J. Am. Chem. Soc. 2010; 132: 5096
- 41 Hollenstein M, Hipolito CJ, Lam CH, Perrin DM. Nucleic Acids Res. 2009; 37: 1638
- 42 Vaught JD, Bock C, Carter J, Fitzwater T, Otis M, Schneider D, Rolando J, Waugh S, Wilcox SK, Eaton BE. J. Am. Chem. Soc. 2010; 132: 4141
- 43 Pinheiro VB, Holliger P. Curr. Opin. Chem. Biol. 2012; 16: 245
- 44 Herdewijn P. Chem. Biodivers. 2010; 7: 1
- 45 Pochet S, Kaminski PA, Van Aerschot A, Herdewijn P, Marlière P. C. R. Biol. 2003; 326: 1175
- 46 Wang J, Verbeure B, Luyten I, Froeyen M, Hendrix C, Rosemeyer H, Seela F, Van Aerschot A, Herdewijn P. Nucleosides, Nucleotides Nucleic Acids 2001; 20: 785
- 47 Boudou V, Kerremans L, De Bouvere B, Lescrinier E, Schepers G, Busson R, Van Aerschot A, Herdewijn P. Nucleic Acids Res. 1999; 27: 1450
- 48 Kempeneers V, Renders M, Froeyen M, Herdewijn P. Nucleic Acids Res. 2005; 33: 3828
- 49 Vastmans K, Pochet S, Peys A, Kerremans L, Van Aerschot A, Hendrix C, Marlière P, Herdewijn P. Biochemistry 2000; 39: 12757
- 50 Schoning K.-U, Scholz P, Guntha S, Wu X, Krishnamurthy R, Eschenmoser A. Science 2000; 290: 1347
- 51 Ichida JK, Horhota A, Zou K, McLaughlin LW, Szostak JW. Nucleic Acids Res. 2005; 33: 5219
- 52 Wilson JN, Teo YN, Kool ET. J. Am. Chem. Soc. 2007; 129: 15426
- 53 Kolpashchikov DM, Gerasimova YV, Khan MS. ChemBioChem 2011; 12: 2564
- 54 Liu L, Li Y, Liotta D, Lutz S. Nucleic Acids Res. 2009; 37: 4472
- 55 Drummond TG. Nat. Biotechnol. 2003; 21: 1192
- 56 Teo YN, Kool ET. Chem. Rev. 2012; 112: 4221
- 57 Hocek M. Chem. Rev. 2009; 109: 6729
- 58 Clever GH, Kaul C, Carell T. Angew. Chem. Int. Ed. 2007; 46: 6226
- 59 Tor Y, Dervan PB. J. Am. Chem. Soc. 1993; 115: 4461
- 60 Mulliken RS. J. Am. Chem. Soc. 1952; 74: 811
- 61 Amblard F, Cho JH, Schinazi RF. Chem. Rev. 2009; 109: 4207
- 62 Cahová H, Havran L, Brázdilová P, Pivoňková H, Pohl R, Fojta M, Hocek M. Angew. Chem. Int. Ed. 2008; 47: 2059
- 63 Bag SS, Kundu R. J. Org. Chem. 2011; 76: 3348
- 64 Ren RX.-F, Chaudhuri NC, Paris PL, Rumney S, Kool ET. J. Am. Chem. Soc. 1996; 118: 7671
- 65 Chen D.-W, Beuscher Beuscher, Stevens RC, Wirsching P, Lerner RA, Janda KD. J. Org. Chem. 2001; 66: 1725
- 66 Ostrovskii VA, Koren AO. Heterocycles 2000; 53: 1421
- 67 Malin AA, Ostrovskii VA, Yas’ko MV, Kraevskii AA. Russ. J. Org. Chem. 1995; 31: 581
- 68 Ostrovskii VA, Studentsov EP, Poplavskii VS, Ivanova NV, Gurskaya GV, Zavodnik VE, Jasko MV, Semizarov DG, Krayevsky AA. Nucleosides Nucleotides 1995; 14: 1289
- 69 Bag SS, Talukdar S, Anjali SJ. Bioorg. Med. Chem. Lett. 2016; 26: 2044
- 70 Müller J, Böhme D, Lax P, Cerdà M, Roitzsch M. Chem. Eur. J. 2005; 11: 6246
- 71 Hoffer M. Chem. Ber. 1960; 93: 2777
- 72 Rolland V, Kotera M, Lhomme J. Synth. Commun. 1997; 27: 3505
- 73 Walker JA, Liu W, Wise DS, Drach JC, Townsend LB. J. Med. Chem. 1998; 41: 1236
- 74 Cortese R, Kammen HO, Spengler SJ, Ames BN. J. Biol. Chem. 1974; 249: 1103
- 75 Michelson AM, Cohn WE. Biochemistry 1962; 1: 490
- 76 Temburnikar K, Seley-Radtke KL. Beilstein J. Org. Chem. 2018; 14: 772
- 77 Warren TK, Jordan R, Lo MK, Ray AS, Mackman RL, Soloveva V, Siegel D, Perron M, Bannister R, Hui HC. Nature 2016; 531: 381
- 78 Herdewijn P. Modified Nucleosides in Biochemistry, Biotechnology and Medicine. John Wiley & Sons; Weinheim: 2008
- 79 Pankiewicz KW, Chen L, Petrelli R, Felczak K, Gao G, Bonnac L, Yu JS, Bennett EM. Curr. Med. Chem. 2008; 15: 650
- 80 Robins RK, Srivastava PC, Narayanan VL, Plowman J, Paull KD. J. Med. Chem. 1982; 25: 107
- 81 Townsend LB, Devivar RV, Turk SR, Nassiri MR, Drach JC. J. Med. Chem. 1995; 38: 4098
- 82 Weber G, Prajda N, Abonyi M, Look KY, Tricot G. Anticancer Res. 1996; 16: 3313
- 83 Ho M.-C, Shi W, Rinaldo-Matthis A, Tyler PC, Evans GB, Clinch K, Almo SC, Schramm VL. Proc. Natl. Acad. Sci. U.S.A. 2010; 107: 4805
- 84 Cho A, Zhang L, Xu J, Lee R, Butler T, Metobo S, Aktoudianakis V, Lew W, Ye H, Clarke M. J. Med. Chem. 2014; 57: 1812
- 85 Gutowski GE, Sweeney MJ, DeLong DC, Hamill RL, Gerzon K, Dyke RW. Ann. N. Y. Acad. Sci. 1975; 255: 544
- 86 Bray N. Nat. Rev. Drug Discovery 2014; 13: 334
- 87 Bouton J, Van Calenbergh S, Hullaert J. Org. Lett. 2020; 22: 9287
- 88 Eastman RT, Roth JS, Brimacombe KR, Simeonov A, Shen M, Patnaik S, Hall MD. ACS Cent. Sci. 2020; 6: 672
- 89 Chu CK, Wempen I, Watanabe KA, Fox JJ. J. Org. Chem. 1976; 41: 2793
- 90 Lim M.-I, Klein RS. Tetrahedron Lett. 1981; 22: 25
- 91 Noyori R, Sato T, Hayakawa Y. J. Am. Chem. Soc. 1978; 100: 2561
- 92 Zhang M, Xue F, Ou J, Huang Y, Lu F, Zhou B, Zheng Z, Liu X.-Y, Zhong W, Qin Y. Org. Chem. Front. 2020; 7: 3675
- 93 Evans GB, Furneaux RH, Gainsford GJ, Schramm VL, Tyler PC. Tetrahedron 2000; 56: 3053
- 94 Warren TK, Wells J, Panchal RG, Stuthman KS, Garza NL, Van Tongeren SA, Dong L, Retterer CJ, Eaton BP, Pegoraro G. Nature 2014; 508: 402
- 95 Pfeiffer M, Nidetzky B. Curr. Opin. Biotechnol. 2023; 79: 102873
- 96 Bag SS, Das SK. Tetrahedron 2019; 75: 3024
- 97 Kool ET. Annu. Rev. Biophys. Biomol. Struct. 2001; 30: 1
- 98 Lu H, Lynch SR, Lee AH. F, Kool ET. ChemBioChem 2009; 10: 2530
- 99 Lee AH. F, Kool ET. J. Org. Chem. 2005; 70: 132
- 100 Krueger AT, Kool ET. J. Am. Chem. Soc. 2008; 130: 3989
- 101 Winnacker M, Kool ET. Angew. Chem. Int. Ed. 2013; 52: 12498
- 102 Migliore A, Corni S, Varsano D, Klein ML, Di Felice R. J. Phys. Chem. B 2009; 113: 9402
- 103 Fuentes-Cabrera M, Zhao X, Kent PR. C, Sumpter BG. J. Phys. Chem. B 2007; 111: 9057
- 104 Blas JR, Huertas O, Tabares C, Sumpter BG, Fuentes-Cabrera M, Orozco M, Ordejón P, Luque FJ. J. Phys. Chem. A 2011; 115: 11344
- 105 Jarchow-Choy SK, Krueger AT, Liu H, Gao J, Kool ET. Nucleic Acids Res. 2011; 39: 1586
- 106 Fuentes-Cabrera M, Sumpter BG, Lipkowski P, Wells JC. J. Phys. Chem. B 2006; 110: 6379
- 107 Fuentes-Cabrera M, Sumpter BG, Wells JC. J. Phys. Chem. B 2005; 109: 21135
- 108 Chelliserrykattil J, Lu H, Lee AH. F, Kool ET. ChemBioChem 2008; 9: 2976
- 109 Krueger AT, Peterson LW, Chelliserry J, Kleinbaum DJ, Kool ET. J. Am. Chem. Soc. 2011; 133: 18447
- 110 Wierzchowski J. Curr. Top. Biophys. 2010; 33: 9
- 111 Wierzchowski J, Antosiewicz JM, Shugar D. Mol. Biosyst. 2014; 10: 2756
- 112 Bag SS, Das SK, Gogoi H. Tetrahedron 2018; 74: 2218
- 113 Sherrill CB, Marshall DJ, Moser MJ, Larsen CA, Daudé-Snow L, Prudent JR. J. Am. Chem. Soc. 2005; 127: 15327
- 114 Svarovskaia ES, Moser MJ, Bae AS, Prudent JR, Miller MD, Borroto-Esoda K. J. Clin. Microbiol. 2006; 44: 4237
- 115 Moser MJ, Marshall DJ, Grenier JK, Kieffer CD, Killeen AA, Ptacin JL, Richmond CS, Roesch EB, Scherrer CW, Sherrill CB. Clin. Chem. 2003; 49: 407
- 116 Operario DJ, Moser MJ, St George K. J. Clin. Microbiol. 2010; 48: 3517
- 117 Yamashige R, Kimoto M, Mitsui T, Yokoyama S, Hirao I. Org. Biomol. Chem. 2011; 9: 7504
- 118 Glushakova LG, Alto BW, Kim MS, Hutter D, Bradley A, Bradley KM, Burkett-Cadena ND, Benner SA. BMC Infect. Dis. 2019; 19: 418
- 119 Sharma N, Hoshika S, Hutter D, Bradley KM, Benner SA. ChemBioChem 2014; 15: 2268
- 120 Glushakova LG, Bradley A, Bradley KM, Alto BW, Hoshika S, Hutter D, Sharma N, Yang Z, Kim M.-J, Benner SA. J. Virol. Methods 2015; 214: 60
- 121 Li Y, Abraham C, Suslov O, Yaren O, Shaw RW, Kim M.-J, Wan S, Marliere P, Benner SA. ACS Synth. Biol. 2023; 12: 1772
- 122 Zhang L, Yang Z, Sefah K, Bradley KM, Hoshika S, Kim M.-J, Kim H.-J, Zhu G, Jiménez E, Cansiz S. J. Am. Chem. Soc. 2015; 137: 6734
- 123 Leal NA, Kim HJ, Hoshika S, Kim MJ, Carrigan MA, Benner SA. ACS Synth. Biol. 2015; 4: 407
- 124 Hoshika S, Leal NA, Kim MJ, Kim MS, Karalkar NB, Kim HJ, Bates AM, Watkins NE, SantaLucia HA, Meyer AJ, DasGupta S, Piccirilli JA, Ellington AD, SantaLucia J, Georgiadis MM, Benner SA. Science 2019; 363: 884
- 125 Paige J, Wu K, Jaffrey SR. Science 2011; 333: 642
- 126 Kimoto M, Mitsui T, Harada Y, Sato A, Yokoyama S, Hirao I. Nucleic Acids Res. 2007; 35: 5360
- 127 Ellington AD, Szostak JW. Nature 1990; 346: 818
- 128 Morohashi N, Kimoto M, Sato A, Kawai R, Hirao I. Molecules 2012; 17: 2855
- 129 Ishizuka T, Kimoto M, Sato A, Hirao I. Chem. Commun. 2012; 48: 10835
- 130 Lavergne T, Lamichhane R, Malyshev DA, Li Z, Li L, Sperling E, Williamson JR, Millar DP, Romesberg FE. ACS Chem. Biol. 2016; 11: 1347
- 131 Lee KH, Kimoto M, Kawai G, Okamoto I, Fin A, Hirao I. Chem. Eur. J. 2022; 28: e202104396
- 132 Wang T, Chen C, Larcher LM, Barrero RA, Veedu RN. Biotechnol. Adv. 2019; 37: 28
- 133 McKeague M, McConnell EM, Cruz-Toledo J, Bernard ED, Pach A, Mastronardi E, Zhang X, Beking M, Francis T, Giamberardino A, Cabecinha A, Ruscito A, Aranda-Rodriguez R, Dumontier M, DeRosa MC. J. Mol. Evol. 2015; 81: 150
- 134 Kimoto M, Yamashige R, Matsunaga K, Yokoyama S, Hirao I. Nat. Biotechnol. 2013; 31: 453
- 135 Futami K, Kimoto M, Lim YW. S, Hirao I. Mol. Ther. Nucleic Acids 2019; 14: 158
- 136 Hirao I, Kimoto M, Lee KH. Biochimie 2018; 145: 15
- 137 Hirao I, Nishimura Y, Tagawa Y.-i, Watanabe K, Miura K.-i. Nucleic Acids Res. 1992; 20: 3891
- 138 Hirao I, Nishimura Y, Naraoka T, Watanabe K, Arata Y, Miura KI. Nucleic Acids Res. 1989; 17: 2223
- 139 Cataland SR, Peyvandi F, Manucci PM, Lämmle B, Hovinga JA. K, Machin SJ, Scully M, Rock G, Gilbert JC, Yang S, Wu H, Jilma B, Knoebl P. Am. J. Hematol. 2012; 87: 430
- 140 Sefah K, Yang Z, Bradley KM, Hoshika S, Jiménez E, Zhang L, Zhu G, Shanker S, Yu F, Turek D, Tan W, Benner SA. Proc. Natl. Acad. Sci. U.S.A. 2014; 111: 1449
- 141 Zumrut HE, Ara MN, Fraile M, Maio G, Mallikaratchy P. Nucleic Acid Ther. 2016; 26: 190
- 142 Zumrut H, Yang Z, Williams N, Arizala J, Batool S, Benner SA, Mallikaratchy P. Biochemistry 2019; 59: 552
- 143 Wu Y, Fa M, Tae EL, Schultz PG, Romesberg FE. J. Am. Chem. Soc. 2002; 124: 14626
- 144 Chen F, Zhang Y, Daugherty AB, Yang Z, Shaw R, Dong M, Lutz S, Benner SA. PLoS One 2017; 12: e0174163
- 145 Zhang Y, Lamb BM, Feldman AW, Zhou AX, Lavergne T, Li L, Romesberg FE. Proc. Natl. Acad. Sci. U.S.A. 2017; 114: 1317
- 146 Schlegel S, Genevaux P, de Gier J.-W. Cell Rep. 2015; 10: 1758
- 147 Hsu PD, Lander ES, Zhang F. Cell 2014; 157: 1262
- 148 Feldman AW, Dien VT, Karadeema RJ, Fischer EC, You Y, Anderson BA, Krishnamurthy R, Chen JS, Li L, Romesberg FE. J. Am. Chem. Soc. 2019; 141: 10644
- 149 Zhou AX.-Z, Sheng K, Feldman AW, Romesberg FE. J. Am. Chem. Soc. 2019; 141: 20166
- 150 Kiga D, Sakamoto K, Kodama K, Kigawa T, Matsuda T, Yabuki T, Shirouzu M, Harada Y, Nakayama H, Takio K. Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 9715
- 151 Ohno S, Yokogawa T, Nishikawa K. J. Biochem. 2001; 130: 417
- 152 Zhang Y, Ptacin JL, Fischer EC, Aerni HR, Caffaro CE, San Jose K, Feldman AW, Turner CR, Romesberg FE. Nature 2017; 551: 644
- 153 Lee KH, Hamashima K, Kimoto M, Hirao I. Curr. Opin. Biotechnol. 2018; 51: 8
- 154 Zhou AX.-Z, Dong X, Romesberg FE. J. Am. Chem. Soc. 2020; 142: 19029
- 155 Wilson DS, Szostak JW. Annu. Rev. Biochem. 1999; 68: 611
- 156 Houlihan G, Arangundy-Franklin S, Holliger P. Curr. Opin. Biotechnol. 2017; 48: 168
- 157 Gold L, Ayers D, Bertino J, Bock C, Bock A, Brody E, Carter J, Cunningham V, Dalby A, Eaton B, Fitzwater T, Flather D, Forbes A, Foreman T, Fowler C, Gawande B, Goss M, Gunn M, Gupta S, Halladay D, Heil J, Heilig J, Hicke B, Husar G, Janjic N, Jarvis T, Jennings S, Katilius E, Keeney T, Kim N, Kaske T, Koch T, Kraemer S, Kroiss L, Le N, Levine D, Lindsey W, Lollo B, Mayfield W, Mehan M, Mehler R, Nelson M, Nelson S, Nieuwlandt D, Nikrad M, Ochsner U, Ostroff R, Otis M, Parker T, Pietrasiewicz S, Resnicow D, Rohloff J, Sanders G, Sattin S, Schneider D, Singer B, Stanton M, Sterkel A, Stewart A, Stratford S, Vaught J, Vrkljan M, Walker J, Watrobka M, Waugh S, Weiss A, Wilcox S, Wolfson A, Wolk S, Zhang C, Zichi D. Nat. Prec. 2010; 1
- 158 Rangel AE, Chen Z, Ayele TM, Heemstra JM. Nucleic Acids Res. 2018; 46: 8057
- 159 Zhang L, Chaput JC. Molecules 2020; 25: 4194
- 160 Li X, Li Z, Yu H. Chem. Commun. 2020; 56: 14653
- 161 Dunn MR, McCloskey CM, Buckley P, Rhea K, Chaput JC. J. Am. Chem. Soc. 2020; 142: 7721
- 162 Ferreira-Bravo IA, DeStefano JJ. Viruses 2021; 13: 1983
- 163 Rose KM, Ferreira-Bravo IA, Li M, Craigie R, Ditzler MA, Holliger P, DeStefano JJ. ACS Chem. Biol. 2019; 14: 2166
- 164 Ferreira-Bravo IA, Cozens C, Holliger P, DeStefano JJ. Nucleic Acids Res. 2015; 43: 9587
- 165 Eremeeva E, Fikatas A, Margamuljana L, Abramov M, Schols D, Groaz E, Herdewijn P. Nucleic Acids Res. 2019; 47: 4927
- 166 Pinheiro VB, Taylor AI, Cozens C, Abramov M, Renders M, Zhang S, Chaput JC, Wengel J, Peak-Chew S.-Y, McLaughlin SH. Science 2012; 336: 341
- 167 Arangundy-Franklin S, Taylor AI, Porebski BT, Genna V, Peak-Chew S, Vaisman A, Woodgate R, Orozco M, Holliger P. Nat. Chem. 2019; 11: 533
- 168 Santoro SW, Joyce GF. Proc. Natl. Acad. Sci. U.S.A. 1997; 94: 4262
- 169 Wang Y, Nguyen K, Spitale RC, Chaput JC. Nat. Chem. 2021; 13: 319
- 170 Wang Y, Ngor AK, Nikoomanzar A, Chaput JC. Nat. Commun. 2018; 9: 5067
- 171 Taylor AI, Wan CJ. K, Donde MJ, Peak-Chew S.-Y, Holliger P. Nat. Chem. 2022; 14: 1295
- 172 Taylor AI, Holliger P. Nat. Chem. 2022; 14: 855
- 173 Takahashi M, Li H, Zhou J, Chomchan P, Aishwarya V, Damha MJ, Rossi JJ. Mol. Ther. Nucleic Acids 2019; 17: 615
- 174 Damha MJ, Wilds CJ, Noronha A, Brukner I, Borkow G, Arion D, Parniak MA. J. Am. Chem. Soc. 1998; 120: 12976
- 175 Gerecht K, Freund N, Liu W, Liu Y, Fürst MJ. L. J, Holliger P. Annu. Rev. Biophys. 2023; 52: 413
- 176 Bag SS, Talukdar S, Matsumoto K, Kundu R. J. Org. Chem. 2013; 78: 278
- 177 Bag SS, Kundu R, Talukdar S. RSC Adv. 2013; 3: 21352
- 178 Kool ET, Morales JC, Guckian KM. Angew. Chem. Int. Ed. 2000; 39: 990
- 179 Wojciechowski F, Lietard J, Leumann CJ. Org. Lett. 2012; 14: 5176
- 180 Nakano S, Uotani Y, Uenishi K, Fujii M, Sugimoto N. Nucleic Acids Res. 2005; 33: 7111
- 181 Verhagen C, Bryld T, Raunkjær M, Vogel S, Buchalová K, Wengel J. Eur. J. Org. Chem. 2006; 2538
- 182 Brotschi C, Mathis G, Leumann CJ. Chem. Eur. J. 2005; 11: 1911
- 183 Bag SS, Sinha S, Gogoi H, Datta S, Kundu R, Talukdar S. Biophys. Chem. 2020; 264: 106428
- 184 Bag SS, Pradhan MK, Talukdar S. J. Photochem. Photobiol., B 2017; 173: 165
- 185 Bag SS, Talukdar S, Kundu R, Saito I, Jana S. Chem. Commun. 2014; 50: 829
- 186 Bag SS, Das SK, Pradhan MK, Jana S. J. Photochem. Photobiol., B 2016; 162: 669
- 187 Bag SS, Pradhan MK, Talukdar S. Org. Biomol. Chem. 2017; 15: 10145
- 188 Bag SS, Talukdar S, Das SK, Pradhan MK, Mukherjee S. Org. Biomol. Chem. 2016; 14: 5088
- 189 Bag SS, Gogoi H. J. Org. Chem. 2018; 83: 7606