Expansion of Genetic Alphabets: Designer Nucleobases and Their Applications

S. S. Bag; A. Banerjee; S. Sinha

doi:10.1055/a-2219-6680

Synlett, Inhaltsverzeichnis

Synlett 2024; 35(11): 1195-1227
DOI: 10.1055/a-2219-6680

account

Special Issue Chemical Synthesis and Catalysis in India

Expansion of Genetic Alphabets: Designer Nucleobases and Their Applications

Authors

S. S. Bag ∗

^aChemical Biology Laboratory, Department of Chemistry, Indian Institute of Technology Guwahati, 781039, Assam, India

^bCentre for the Environment, Indian Institute of Technology Guwahati, 781039, Assam, India

^cBhupet Mehta School of Health Science and Technology, Indian Institute of Technology Guwahati, 781039, Assam, India
A. Banerjee

^bCentre for the Environment, Indian Institute of Technology Guwahati, 781039, Assam, India
S. Sinha

^bCentre for the Environment, Indian Institute of Technology Guwahati, 781039, Assam, India

Abstract

Alle Artikel dieser Rubrik

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 acids

Volltext

Referenzen

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