The XNA world: Progress towards replication and evolution of synthetic genetic polymers

Current Opinion in Chemical Biology

Volumn 16, Issue 3-4, 2012, Pages 245-252

  Pinheiro, Vitor B ^a   Holliger, Philipp ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GENETIC POLYMER; NUCLEIC ACID; POLYMER; RNA; SUGAR; UNCLASSIFIED DRUG; XENO NUCLEIC ACID;

ENZYME SYNTHESIS; GENE REPLICATION; MOLECULAR EVOLUTION; NONHUMAN; REVIEW;

DNA; DNA REPLICATION; EVOLUTION, MOLECULAR; POLYMERS; RNA;

EID: 84865286097     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2012.05.198     Document Type: Review

References (99)

1. Benner S.A. Understanding nucleic acids using synthetic chemistry. Acc Chem Res 2004, 37:784-797.
2. Herdewijn P., Marliere P. Toward safe genetically modified organisms through the chemical diversification of nucleic acids. Chem Biodivers 2009, 6:791-808.
3. Hasegawa T., Shoji A., Kuwahara M., Ozaki H., Sawai H. Synthesis and property of DNA labeled with fluorescent acridone. Nucleic Acids Symp Ser (Oxf) 2006, 50:145-146.
4. Kuwahara M., Suto Y., Minezaki S., Kitagata R., Nagashima J., Sawai H. Substrate property and incorporation accuracy of various dATP analogs during enzymatic polymerization using thermostable DNA polymerases. Nucleic Acids Symp Ser (Oxf) 2006, 50:31-32.
5. Weisbrod S.H., Marx A. Novel strategies for the site-specific covalent labelling of nucleic acids. Chem Commun 2008, 44:5675-5685.
6. Brudno Y., Liu D.R. Recent progress toward the templated synthesis and directed evolution of sequence-defined synthetic polymers. Chem Biol 2009, 16:265-276.
7. Hocek M., Fojta M. Nucleobase modification as redox DNA labelling for electrochemical detection. Chem Soc Rev 2011, 40:5802-5814.
8. Ramsay N., Jemth A.S., Brown A., Crampton N., Dear P., Holliger P. CyDNA: synthesis and replication of highly Cy-dye substituted DNA by an evolved polymerase. J Am Chem Soc 2010, 132:5096-5104.
9. Jager S., Famulok M. Generation and enzymatic amplification of high-density functionalized DNA double strands. Angew Chem Int Ed Engl 2004, 43:3337-3340.
10. Jager S., Rasched G., Kornreich-Leshem H., Engeser M., Thum O., Famulok M. A versatile toolbox for variable DNA functionalization at high density. J Am Chem Soc 2005, 127:15071-15082.
11. Hollenstein M., Hipolito C.J., Lam C.H., Perrin D.M. A self-cleaving DNA enzyme modified with amines, guanidines and imidazoles operates independently of divalent metal cations (M2+). Nucleic Acids Res 2009, 37:1638-1649.
12. Vaught J.D., Bock C., Carter J., Fitzwater T., Otis M., Schneider D., Rolando J., Waugh S., Wilcox S.K., Eaton B.E. Expanding the chemistry of DNA for in vitro selection. J Am Chem Soc 2010, 132:4141-4151.
13. Gommers-Ampt J.H., Borst P. Hypermodified bases in DNA. FASEB J 1995, 9:1034-1042.
14. Ku C.S., Naidoo N., Wu M., Soong R. Studying the epigenome using next generation sequencing. J Med Genet 2011, 48:721-730.
15. Marliere P., Patrouix J., Doring V., Herdewijn P., Tricot S., Cruveiller S., Bouzon M., Mutzel R. Chemical evolution of a bacterium's genome. Angew Chem Int Ed Engl 2011, 50:7109-7114.
16. Lee A.H., Kool E.T. A new four-base genetic helix, yDNA, composed of widened benzopyrimidine-purine pairs. J Am Chem Soc 2005, 127:3332-3338.
17. Liu H., Gao J., Lynch S.R., Saito Y.D., Maynard L., Kool E.T. A four-base paired genetic helix with expanded size. Science 2003, 302:868-871.
18. Lee A.H., Kool E.T. Exploring the limits of DNA size: naphtho-homologated DNA bases and pairs. J Am Chem Soc 2006, 128:9219-9230.
19. Chelliserrykattil J., Lu H., Lee A.H., Kool E.T. Polymerase amplification, cloning, and gene expression of benzo-homologous "yDNA" base pairs. Chembiochem 2008, 9:2976-2980.
20. Lu H., Lynch S.R., Lee A.H., Kool E.T. Structure and replication of yDNA: a novel genetic set widened by benzo-homologation. Chembiochem 2009, 10:2530-2538.
21. Krueger A.T., Peterson L.W., Chelliserry J., Kleinbaum D.J., Kool E.T. Encoding phenotype in bacteria with an alternative genetic set. J Am Chem Soc 2011, 133:18447-18451.
22. Pochet S., Kaminski P.A., Van Aerschot A., Herdewijn P., Marliere P. Replication of hexitol oligonucleotides as a prelude to the propagation of a third type of nucleic acid in vivo. C R Biol 2003, 326:1175-1184.
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 U S A 2011, 108:11338-11343.
24. Hirao I., Kimoto M., Yamashige R. Natural versus artificial creation of base pairs in DNA: origin of nucleobases from the perspectives of unnatural base pair studies. Acc Chem Res 2012, Epub ahead of print. 10.1021/ar200257x.
25. Hoshika S., Chen F., Leal N.A., Benner S.A. Artificial genetic systems: self-avoiding DNA in PCR and multiplexed PCR. Angew Chem Int Ed Engl 2008, 49:5554-5557.
26. Yang Z., Hutter D., Sheng P., Sismour A.M., Benner S.A. Artificially expanded genetic information system: a new base pair with an alternative hydrogen bonding pattern. Nucleic Acids Res 2006, 34:6095-6101.
27. Ogata S., Takahashi M., Minakawa N., Matsuda A. Unnatural imidazopyridopyrimidine:naphthyridine base pairs: selective incorporation and extension reaction by Deep Vent (exo-) DNA polymerase. Nucleic Acids Res 2009, 37:5602-5609.
28. Kimoto M., Kawai R., Mitsui T., Yokoyama S., Hirao I. An unnatural base pair system for efficient PCR amplification and functionalization of DNA molecules. Nucleic Acids Res 2009, 37:e14.
29. Seo Y.J., Malyshev D.A., Lavergne T., Ordoukhanian P., Romesberg F.E. Site-specific labeling of DNA and RNA using an efficiently replicated and transcribed class of unnatural base pairs. J Am Chem Soc 2011, 133:19878-19888.
30. Kaul C., Muller M., Wagner M., Schneider S., Carell T. Reversible bond formation enables the replication and amplification of a crosslinking salen complex as an orthogonal base pair. Nat Chem 2011, 3:794-800.
31. Chiba J., Inouye M. Exotic DNAs made of nonnatural bases and natural phosphodiester bonds. Chem Biodivers 2010, 7:259-282.
32. Clever G.H., Shionoya M. Alternative DNA base pairing through metal coordination. Met Ions Life Sci 2012, 10:269-294.
33. Chelliserrykattil J., Ellington A.D. Evolution of a T7 RNA polymerase variant that transcribes 2'-O-methyl RNA. Nat Biotechnol 2004, 22:1155-1160.
34. Padilla R., Sousa R. Efficient synthesis of nucleic acids heavily modified with non-canonical ribose 2'-groups using a mutantT7 RNA polymerase (RNAP). Nucleic Acids Res 1999, 27:1561-1563.
35. Padilla R., Sousa R. A Y639F/H784A T7 RNA polymerase double mutant displays superior properties for synthesizing RNAs with non-canonical NTPs. Nucleic Acids Res 2002, 30:e138.
36. Burmeister P.E., Lewis S.D., Silva R.F., Preiss J.R., Horwitz L.R., Pendergrast P.S., McCauley T.G., Kurz J.C., Epstein D.M., Wilson C., et al. Direct in vitro selection of a 2'-O-methyl aptamer to VEGF. Chem Biol 2005, 12:25-33.
37. Mi J., Liu Y., Rabbani Z.N., Yang Z., Urban J.H., Sullenger B.A., Clary B.M. In vivo selection of tumor-targeting RNA motifs. Nat Chem Biol 2010, 6:22-24.
38. Cozens C., Pinheiro V.B., Vaisman A., Woodgate R., Holliger P. A short adaptive path from DNA to RNA polymerases. Proc Natl Acad Sci U S A 2012, 109:8067-8072. 10.1073/pnas.1120964109.
39. Siegmund V., Santner T., Micura R., Marx A. Enzymatic synthesis of 2'-methylseleno-modified RNA. Chem Sci 2011, 2:2224-2231.
40. Eschenmoser A. Chemical etiology of nucleic acid structure. Science 1999, 284:2118-2124.
41. Schoning K., Scholz P., Guntha S., Wu X., Krishnamurthy R., Eschenmoser A. Chemical etiology of nucleic acid structure: the alpha-threofuranosyl-(3'→2') oligonucleotide system. Science 2000, 290:1347-1351.
42. Ichida J.K., Horhota A., Zou K., McLaughlin L.W., Szostak J.W. High fidelity TNA synthesis by Therminator polymerase. Nucleic Acids Res 2005, 33:5219-5225.
43. Kataoka M., Kouda Y., Sato K., Minakawa N., Matsuda A. Highly efficient enzymatic synthesis of 3'-deoxyapionucleic acid (apioNA) having the four natural nucleobases. Chem Commun (Camb) 2011, 47:8700-8702.
44. Singh S.K., Koshkin A.A., Wengel J., Nielsen P. LNA (locked nucleic acids): synthesis and high-affinity nucleic acid recognition. Chem Commun 1998, 34:455-456.
45. Veedu R.N., Wengel J. Locked nucleic acids: promising nucleic acid analogs for therapeutic applications. Chem Biodivers 2010, 7:536-542.
46. Veedu R.N., Vester B., Wengel J. Enzymatic incorporation of LNA nucleotides into DNA strands. Chembiochem 2007, 8:490-492.
47. Herdewijn P. Nucleic acids with a six-membered 'carbohydrate' mimic in the backbone. Chem Biodivers 2010, 7:1-59.
48. Verheggen I., Van Aerschot A., Toppet S., Snoeck R., Janssen G., Balzarini J., De Clercq E., Herdewijn P. Synthesis and antiherpes virus activity of 1,5-anhydrohexitol nucleosides. J Med Chem 1993, 36:2033-2040.
49. Herdewijn P., De Clercq E. The cyclohexene ring as bioisostere of a furanose ring: synthesis and antiviral activity of cyclohexenyl nucleosides. Bioorg Med Chem Lett 2001, 11:1591-1597.
50. Wang J., Verbeure B., Luyten I., Froeyen M., Hendrix C., Rosemeyer H., Seela F., Van Aerschot A., Herdewijn P. Cyclohexene nucleic acids (CeNA) form stable duplexes with RNA and induce RNase H activity. Nucleosides Nucleotides Nucleic Acids 2001, 20:785-788.
51. Boudou V., Kerremans L., De Bouvere B., Lescrinier E., Schepers G., Busson R., Van Aerschot A., Herdewijn P. Base pairing of anhydrohexitol nucleosides with 2,6-diaminopurine, 5-methylcytosine and uracil as base moiety. Nucleic Acids Res 1999, 27:1450-1456.
52. Kempeneers V., Renders M., Froeyen M., Herdewijn P. Investigation of the DNA-dependent cyclohexenyl nucleic acid polymerization and the cyclohexenyl nucleic acid-dependent DNA polymerization. Nucleic Acids Res 2005, 33:3828-3836.
53. Vastmans K., Pochet S., Peys A., Kerremans L., Van Aerschot A., Hendrix C., Marliere P., Herdewijn P. Enzymatic incorporation in DNA of 1,5-anhydrohexitol nucleotides. Biochemistry 2000, 39:12757-12765.
54. Vastmans K., Froeyen M., Kerremans L., Pochet S., Herdewijn P. Reverse transcriptase incorporation of 1,5-anhydrohexitol nucleotides. Nucleic Acids Res 2001, 29:3154-3163.
55. Schlegel M.K., Peritz A.E., Kittigowittana K., Zhang L., Meggers E. Duplex formation of the simplified nucleic acid GNA. Chembiochem 2007, 8:927-932.
56. Joyce G.F., Schwartz A.W., Miller S.L., Orgel L.E. The case for an ancestral genetic system involving simple analogues of the nucleotides. Proc Natl Acad Sci U S A 1987, 84:4398-4402.
57. Heuberger B.D., Switzer C. A pre-RNA candidate revisited: both enantiomers of flexible nucleoside triphosphates are DNA polymerase substrates. J Am Chem Soc 2008, 130:412-413.
58. Chen J.J., Tsai C.H., Cai X., Horhota A.T., McLaughlin L.W., Szostak J.W. Enzymatic primer-extension with glycerol-nucleoside triphosphates on DNA templates. PLoS One 2009, 4:e4949.
59. Tsai C.H., Chen J., Szostak J.W. Enzymatic synthesis of DNA on glycerol nucleic acid templates without stable duplex formation between product and template. Proc Natl Acad Sci U S A 2007, 104:14598-14603.
60. Maiti M., Siegmund V., Abramov M., Lescrinier E., Rosemeyer H., Froeyen M., Ramaswamy A., Ceulemans A., Marx A., Herdewijn P. Solution structure and conformational dynamics of deoxyxylonucleic acids (dXNA): an orthogonal nucleic acid candidate. Chemistry 2012, 18:869-879.
61. Eckstein F. Nucleoside phosphorothioates. Annu Rev Biochem 1985, 54:367-402.
62. Porter K.W., Briley J.D., Shaw B.R. Direct PCR sequencing with boronated nucleotides. Nucleic Acids Res 1997, 25:1611-1617.
63. Shaw B.R., Dobrikov M., Wang X., Wan J., He K., Lin J.L., Li P., Rait V., Sergueeva Z.A., Sergueev D. Reading, writing, and modulating genetic information with boranophosphate mimics of nucleotides, DNA, and RNA. Ann N Y Acad Sci 2003, 1002:12-29.
64. Somasunderam A., Thiviyanathan V., Tanaka T., Li X., Neerathilingam M., Lokesh G.L., Mann A., Peng Y., Ferrari M., Klostergaard J., et al. Combinatorial selection of DNA thioaptamers targeted to the HA binding domain of human CD44. Biochemistry 2010, 49:9106-9112.
65. Ghadessy F.J., Ramsay N., Boudsocq F., Loakes D., Brown A., Iwai S., Vaisman A., Woodgate R., Holliger P. Generic expansion of the substrate spectrum of a DNA polymerase by directed evolution. Nat Biotechnol 2004, 22:755-759.
66. Nielsen P.E. Peptide nucleic acids (PNA) in chemical biology and drug discovery. Chem Biodivers 2010, 7:786-804.
67. Nielsen P.E., Haaima G., Lohse A., Buchardt O. Peptide nucleic acids (PNAs) containing thymine monomers derived from chiral amino acids: hybridization and solubility properties of d-lysine PNA. Angew Chem Int Ed Engl 1996, 35:1939-1942.
68. Zhou P., Dragulescu-Andrasi A., Bhattacharya B., O'Keefe H., Vatta P., Hyldig-Nielsen J.J., Ly D.H. Synthesis of cell-permeable peptide nucleic acids and characterization of their hybridization and uptake properties. Bioorg Med Chem Lett 2006, 16:4931-4935.
69. Ura Y., Beierle J.M., Leman L.J., Orgel L.E., Ghadiri M.R. Self-assembling sequence-adaptive peptide nucleic acids. Science 2009, 325:73-77.
70. Rosenbaum D.M., Liu D.R. Efficient and sequence-specific DNA-templated polymerization of peptide nucleic acid aldehydes. J Am Chem Soc 2003, 125:13924-13925.
71. 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, 10:3729-3732.
72. El-Sagheer A.H., Brown T. Synthesis and polymerase chain reaction amplification of DNA strands containing an unnatural triazole linkage. J Am Chem Soc 2009, 131:3958-3964.
73. Wu T., Orgel L.E. Nonenzymatic template-directed synthesis on hairpin oligonucleotides. 3. Incorporation of adenosine and uridine residues. J Am Chem Soc 1992, 114:7963-7969.
74. Wu T., Orgel L.E. Nonenzymatic template-directed synthesis on hairpin oligonucleotides. 2. Templates containing cytidine and guanosine residues. J Am Chem Soc 1992, 114:5496-5501.
75. Schrum J.P., Ricardo A., Krishnamurthy M., Blain J.C., Szostak J.W. Efficient and rapid template-directed nucleic acid copying using 2'-amino-2',3'-dideoxyribonucleoside-5'-phosphorimidazolide monomers. J Am Chem Soc 2009, 131:14560-14570.
76. Li X., Zhan Z.Y., Knipe R., Lynn D.G. DNA-catalyzed polymerization. J Am Chem Soc 2002, 124:746-747.
77. Brudno Y., Birnbaum M.E., Kleiner R.E., Liu D.R. An in vitro translation, selection and amplification system for peptide nucleic acids. Nat Chem Biol 2010, 6:148-155.
78. Kozlov I.A., De Bouvere B., Van Aerschot A., Herdewijn P., Orgel L.E. Efficient transfer of information from hexitol nucleic acids to RNA during nonenzymatic oligomerization. J Am Chem Soc 1999, 121:5856-5859.
79. Kozlov I.A., Zielinski M., Allart B., Kerremans L., Van Aerschot A., Busson R., Herdewijn P., Orgel L.E. Nonenzymatic template-directed reactions on altritol oligomers, preorganized analogues of oligonucleotides. Chemistry 2000, 6:151-155.
80. Zhang N., Zhang S., Szostak J.W. Activated ribonucleotides undergo a sugar pucker switch upon binding to a single-stranded RNA template. J Am Chem Soc 2012, 134:3691-3694.
81. Loakes D., Holliger P. Polymerase engineering: towards the encoded synthesis of unnatural biopolymers. Chem Commun (Camb) 2009, 45:4619-4631.
82. Pinheiro V.B., Ong J.L., Holliger P. Polymerase engineering: from PCR and sequencing to synthetic biology. Protein Engineering Handbook 2012, vol III. Wiley-VCH.
83. Yang G., Franklin M., Li J., Lin T.C., Konigsberg W. A conserved Tyr residue is required for sugar selectivity in a Pol alpha DNA polymerase. Biochemistry 2002, 41:10256-10261.
84. Patel P.H., Loeb L.A. Multiple amino acid substitutions allow DNA polymerases to synthesize RNA. J Biol Chem 2000, 275:40266-40272.
85. Staiger N., Marx A. A DNA polymerase with increased reactivity for ribonucleotides and C5-modified deoxyribonucleotides. Chembiochem 2010, 11:1963-1966.
86. Xia G., Chen L., Sera T., Fa M., Schultz P.G., Romesberg F.E. Directed evolution of novel polymerase activities: mutation of a DNA polymerase into an efficient RNA polymerase. Proc Natl Acad Sci U S A 2002, 99:6597-6602.
87. Ong J.L., Loakes D., Jaroslawski S., Too K., Holliger P. Directed evolution of DNA polymerase, RNA polymerase and reverse transcriptase activity in a single polypeptide. J Mol Biol 2006, 361:537-550.
88. McCullum E.O., Chaput J.C. Transcription of an RNA aptamer by a DNA polymerase. Chem Commun (Camb) 2009, 45:2938-2940.
89. Shinkai A., Patel P.H., Loeb L.A. The conserved active site motif A of Escherichia coli DNA polymerase I is highly mutable. J Biol Chem 2001, 276:18836-18842.
90. Pinheiro V.B., Taylor A.I., Cozens C., Abramov M., Renders M., Zhang S., Chaput J.C., Wengel J., Peak-Chew S.-Y., McLaughlin S.H., et al. Synthetic genetic polymers capable of heredity and evolution. Science 2012, 336:341-344.
91. Ichida J.K., Zou K., Horhota A., Yu B., McLaughlin L.W., Szostak J.W. An in vitro selection system for TNA. J Am Chem Soc 2005, 127:2802-2803.
92. Yu H., Zhang S., Chaput J.C. Darwinian evolution of an alternative genetic system provides support for TNA as an RNA progenitor. Nat Chem 2012, 4:183-187.
93. Jozwiakowski S.K., Connolly B.A. A modified family-B archaeal DNA polymerase with reverse transcriptase activity. Chembiochem 2011, 12:35-37.
94. Sano S., Yamada Y., Shinkawa T., Kato S., Okada T., Higashibata H., Fujiwara S. Mutations to create thermostable reverse transcriptase with bacterial family A DNA polymerase from Thermotoga petrophila K4. J Biosci Bioeng 2012, 113:315-321.
95. Sauter K.B., Marx A. Evolving thermostable reverse transcriptase activity in a DNA polymerase scaffold. Angew Chem Int Ed Engl 2006, 45:7633-7635.
96. Lockless S.W., Ranganathan R. Evolutionarily conserved pathways of energetic connectivity in protein families. Science 1999, 286:295-299.
97. Suel G.M., Lockless S.W., Wall M.A., Ranganathan R. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat Struct Biol 2003, 10:59-69.
98. Benner S.A. Redesigning genetics. Science 2004, 306:625-626.
99. Ebert M.O., Mang C., Krishnamurthy R., Eschenmoser A., Jaun B. The structure of a TNA-TNA complex in solution: NMR study of the octamer duplex derived from alpha-(l)-threofuranosyl-(3'-2')-CGAATTCG. J Am Chem Soc 2008, 130:15105-15115.