Generation of aptamers with an expanded chemical repertoire

Molecules

Volumn 20, Issue 9, 2015, Pages 16643-16671

  Diafa, Stella ^a   Hollenstein, Marcel ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Aptamers; Chemically modified nucleic acids; Modified nucleoside triphosphates; Polymerases; Selex; Synthetic genetic polymers; Therapeutic oligonucleotides

Indexed keywords

APTAMER;

ANIMAL; CHEMISTRY; COMBINATORIAL CHEMISTRY; HUMAN; PROCEDURES; SYSTEMATIC EVOLUTION OF LIGANDS BY EXPONENTIAL ENRICHMENT APTAMER TECHNIQUE;

ANIMALS; APTAMERS, NUCLEOTIDE; COMBINATORIAL CHEMISTRY TECHNIQUES; HUMANS; SELEX APTAMER TECHNIQUE;

EID: 84942746901     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules200916643     Document Type: Review

References (173)

1. Mayer, G. The Chemical Biology of Aptamers. Angew. Chem. Int. Ed. 2009, 48, 2672-2689.
2. Tolle, F.; Mayer, G. Dressed for success-Applying chemistry to modulate aptamer functionality. Chem. Sci. 2013, 4, 60-67.
3. Ellington, A.D.; Szostak, J.W. In vitro selection of RNA molecules that bind specific ligands. Nature 1990, 346, 818-822.
4. Tuerk, C.; Gold, L. Systematic Evolution of Ligands by Exponential Enrichment: RNA Ligands to Bacteriophage T4 DNA Polymerase. Science 1990, 249, 505-510.
5. Robertson, D.L.; Joyce, G.F. Selection in vitro of an RNA enzyme that specifically cleaves single-stranded DNA. Nature 1990, 344, 467-468.
6. Joyce, G.F. Forty Years of in Vitro Evolution. Angew. Chem. Int. Ed. 2007, 46, 6420-6436.
7. Silverman, S.K. Catalytic DNA (deoxyribozymes) for synthetic applications-Current abilities and future prospects. Chem. Commun. 2008, 30, 3467-3485.
8. Sun, H.; Zu, Y. A Highlight of Recent Advances in Aptamer Technology and Its Application. Molecules 2015, 20, 11959-11980.
9. Ozer, A.; Pagano, J.M.; Lis, J.T. New Technologies Provide Quantum Changes in the Scale, Speed, and Success of SELEX Methods and Aptamer Characterization. Mol. Ther. Nucleic Acids 2014, 3, e183.
10. Darmostuk, M.; Rimpelová, S.; Gbelcová, H.; Ruml, T. Current approaches in SELEX: An update to aptamer selection technology. Biotechnol. Adv. 2015, 33, doi:10.1016/j.biotechadv.2015.02.008.
11. Keefe, A.D.; Cload, S.T. SELEX with modified nucleotides. Curr. Opin. Chem. Biol. 2008, 12, 448-456.
12. Li, Y.; Breaker, R.R. Kinetics of RNA Degradation by Specific Base Catalysis of Transesterification Involving the 2'-Hydroxyl Group. J. Am. Chem. Soc. 1999, 121, 5364-5372.
13. Lindahl, T. Instability and decay of the primary structure of DNA. Nature 1993, 362, 709-715.
14. Hollenstein, M. Nucleoside Triphosphates-Building Blocks for the Modification of Nucleic Acids. Molecules 2012, 17, 13569-13591.
15. Jellinek, D.; Green, L.S.; Bell, C.; Lynott, C.K.; Gill, N.; Vargeese, C.; Kirschenheuter, G.; McGee, D.P.C.; Abesinghe, P.; Picken, W.A.; et al. Potent 2'-Amino-2'-deoxypyrimidine RNA Inhibitors of Basic Fibroblast Growth Factor. Biochemistry 1995, 34, 11363-11372.
16. Pagratis, N.C.; Bell, C.; Chang, Y.F.; Jennings, S.; Fitzwater, T.; Jellinek, D.; Dang, C. Potent 2'-amino-, and 2'-fluoro-2'-deoxyribonucleotide RNA inhibitors of keratinocyte growth factor. Nat. Biotechnol. 1997, 15, 68-73.
17. Kuwahara, M.; Sugimoto, N. Molecular Evolution of Functional Nucleic Acids with Chemical Modifications. Molecules 2010, 15, 5423-5444.
18. Herdewijn, P.; Marlière, P. Toward Safe Genetically Modified Organisms through the Chemical Diversification of Nucleic Acids. Chem. Biodivers. 2009, 6, 791-808.
19. Pinheiro, V.B.; Holliger, P. The XNA world: Progress towards replication and evolution of synthetic genetic polymers. Curr. Opin. Chem. Biol. 2012, 16, 245-252.
20. Pinheiro, V.B.; Holliger, P. Towards XNA nanotechnology: New materials from synthetic genetic polymers. Trends Biotechnol. 2014, 32, 321-328.
21. Liu, Q.; Jin, C.; Wang, Y.; Fang, X.; Zhang, X.; Chen, Z.; Tan, W. Aptamer-conjugated nanomaterials for specific cancer cell recognition and targeted cancer therapy. NPG Asia Mater. 2014, 6, e95.
22. Ray, P.; Viles, K.D.; Soule, E.E.; Woodruff, R.S. Application of Aptamers for Targeted Therapeutics. Arch. Immunol. Ther. Exp. 2013, 61, 255-271.
23. Bruno, J.G. Predicting the Uncertain Future of Aptamer-Based Diagnostics and Therapeutics. Molecules 2015, 20, 6866-6887.
24. Keefe, A.D.; Pai, S.; Ellington, A. Aptamers as therapeutics. Nat. Rev. Drug Discov. 2010, 9, 537-550.
25. Bruno, J.G. A Review of Therapeutic Aptamer Conjugates with Emphasis on New Approaches. Pharmaceuticals 2013, 6, 340-357.
26. Nimjee, S.M.; Rusconi, C.P.; Sullenger, B.A. Aptamers: An Emerging Class of Therapeutics. Annu. Rev. Med. 2005, 56, 555-583.
27. Lao, Y.-H.; Phua, K.K.L.; Leong, K.W. Aptamer Nanomedicine for Cancer Therapeutics: Barriers and Potential for Translation. ACS Nano 2015, 9, 2235-2254.
28. Rusconi, C.P.; Scardino, E.; Layzer, J.; Pitoc, G.A.; Ortel, T.L.; Monroe, D.; Sullenger, B.A. RNA aptamers as reversible antagonists of coagulation factor IXa. Nature 2002, 419, 90-94.
29. Rusconi, C.P.; Roberts, J.D.; Pitoc, G.A.; Nimjec, S.M.; White, R.R.; Quick, G. Jr.; Scardino, E.; Fay, W.P.; Sullenger, B.A. Antidote-mediated control of an anticoagulant aptamer in vivo. Nat. Biotechnol. 2004, 22, 1423-1428.
30. Li, L.; Tong, R.; Chu, H.; Wang, W.; Langer, R.; Kohane, D.S. Aptamer photoregulation in vivo. Proc. Natl. Acad. Sci. USA 2014, 111, 17099-17103.
31. Martin, J.A.; Parekh, P.; Kim, Y.; Morey, T.E.; Sefah, K.; Gravenstein, N.; Dennis, D.M.; Tan, W. Selection of an Aptamer Antidote to the Anticoagulant Drug Bivalirudin. PLoS ONE 2013, 8, e57341.
32. Ng, E.W.; Shima, D.T.; Calias, P.; Cunningham, E.T.; Guyer, D.R.; Adamis, A.P. Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease. Nat. Rev. Drug Discov. 2006, 5, 123-132.
33. McNamara, J.O.I.; Andrechek, E.R.; Wang, Y.; Viles, K.D.; Rempel, R.E.; Gilboa, E.; Sullenger, B.A.; Giangrande, P.H. Cell type-specific delivery of siRNAs with aptamersiRNA chimeras. Nat. Biotechnol. 2006, 24, 1005-1015.
34. Li, L.; Hou, J.; Liu, X.; Guo, Y.; Wu, Y.; Zhang, L.; Yang, Z. Nucleolin-targeting liposomes guided by aptamer AS1411 for the delivery of siRNA for the treatment of malignant melanomas. Biomaterials 2014, 35, 3840-3850.
35. Lai, W.Y.; Wang, W.Y.; Chang, Y.C.; Chang, C.J.; Yang, P.C.; Peck, K. Synergistic inhibition of lung cancer cell invasion, tumor growth and angiogenesis using aptamer-siRNA chimeras. Biomaterials 2014, 35, 2905-2914.
36. Santulli-Marotto, S.; Nair, S.K.; Rusconi, C.; Sullenger, B.; Gilboa, E. Multivalent RNA Aptamers That Inhibit CTLA-4 and Enhance Tumor Immunity. Cancer Res. 2003, 63, 7483-7489.
37. Herrmann, A.; Priceman, S.J.; Kujawski, M.; Xin, H.; Cherryholmes, G.A.; Zhang, W.; Zhang, C.; Lahtz, C.; Kowolik, C.; Forman, S.J.; et al. CTLA4 aptamer delivers STAT3 siRNA to tumor-associated and malignant T cells. J. Clin. Investig. 2014, 124, 2977-2987.
38. Ma, H.; Liu, J.; Ali, M.M.; Mahmood, M.A.I.; Labanieh, L.; Lu, M.; Iqbal, S.M.; Zhang, Q.; Zhao, W.; Wan, Y. Nucleic acid aptamers in cancer research, diagnosis and therapy. Chem. Soc. Rev. 2015, 44, 1240-1256.
39. Shi, H.; Tang, Z.; Kim, Y.; Nie, H.; Huang, Y.F.; He, X.; Deng, K.; Wang, K.; Tan, W. In vivo Fluorescence Imaging of Tumors using Molecular Aptamers Generated by Cell-SELEX. Chem. Asian J. 2010, 5, 2209-2213.
40. Ding, F.; Guo, S.; Xie, M.; Luo, W.; Yuan, C.; Huang, W.; Zhou, Y.; Zhang, X.L.; Zhou, X. Diagnostic applications of gastric carcinoma cell aptamers in vitro and in vivo. Talanta 2015, 134, 30-36.
41. Hipolito, C.J.; Hollenstein, M.; Lam, C.H.; Perrin, D.M. Protein-inspired modified DNAzymes: Dramatic effects of shortening side-chain length of 8-imidazolyl modified deoxyadenosines in selecting RNaseA mimicking DNAzymes. Org. Biomol. Chem. 2011, 9, 2266-2273.
42. Ghadessy, F.J.; Ong, J.L.; Holliger, P. Directed evolution of polymerase function by compartmentalized self-replication. Proc. Natl. Acad. Sci. USA 2001, 98, 4552-4557.
43. Packer, M.S.; Liu, D.R. Methods for the directed evolution of proteins Nat. Rev. Genet. 2015, 16, 379-394.
44. Kranaster, R.; Marx, A. Engineered DNA Polymerases in Biotechnology. ChemBioChem 2010, 11, 2077-2084.
45. Laos, R.; Thomson, J.M.; Benner, S.A. DNA polymerases engineered by directed evolution to incorporate non-standard nucleotides. Front. Microbiol. 2014, 5, 565, doi:10.3389/fmicb.2014.00565.
46. Lauridsen, L.H.; Rothnagel, J.A.; Veedu, R.N. Enzymatic Recognition of 2'-Modified Ribonucleoside 5'-Triphosphates: Towards the Evolution of Versatile Aptamers. ChemBioChem 2012, 13, 19-25.
47. Lin, Y.; Qiu, Q.; Gill, S.C.; Jayasena, S.D. Modified RNA sequence pools for in vitro selection. Nucleic Acids Res. 1994, 22, 5229-5234.
48. Green, L.S.; Jellinek, D.; Bell, C.; Beebe, L.A.; Feistner, B.D.; Gill, S.C.; Jucker, F.M.; Janjić, N. Nuclease-resistant nucleic acid ligands to vascular permeability factor/vascular endothelial growth factor. Chem. Biol. 1995, 2, 683-695.
49. Lin, Y.; Nieuwlandt, D.; Magallanez, A.; Feistner, B.; Jayasena, S.D. High-affinity and specific recognition of human thyroid stimulating hormone (hTSH) by in vitro selected 2'-amino-modified RNA. Nucleic Acids Res. 1996, 24, 3407-3414.
50. Kubik, M.F.; Bell, C.; Fitzwater, T.; Watson, S.R.; Tasset, D.M. Isolation and characterization of 2'-fluoro-, 2'-amino-, and 2'-fluoro-/amino-modified RNA ligands to human IFN-gamma that inhibit receptor binding. J. Immunol. 1997, 159, 259-267.
51. Proske, D.; Gilch, S.; Wopfner, F.; Schätzl, H.M.; Winnacker, E.L.; Famulok, M. Prion-Protein- Specific Aptamer Reduces PrPSc Formation. ChemBioChem 2002, 3, 717-725.
52. Proske, D.; Höfliger, M.; Söll, R.M.; Beck-Sickinger, A.G.; Famulok, M. A Y2 Receptor Mimetic Aptamer Directed against Neuropeptide Y. J. Biol. Chem. 2002, 277, 11416-11422.
53. Pan, W.; Craven, R.C.; Qiu, Q.; Wilson, C.B.; Wills, J.W.; Golovine, S.; Wang, J.F. Isolation of virus-neutralizing RNAs from a large pool of random sequences. Proc. Natl. Acad. Sci. USA 1995, 92, 11509-11513.
54. Ruckman, J.; Green, L.S.; Beeson, J.; Waugh, S.; Gillette, W.L.; Henninger, D.D.; Claesson-Welsh, L.; Janjic, N. 2'-Fluoropyrimidine RNA-based Aptamers to the 165-Amino Acid Form of Vascular Endothelial Growth Factor (VEGF165). J. Biol. Chem. 1998, 273, 20556-20567.
55. Khati, M.; Schüman, M.; Ibrahim, J.; Sattentau, Q.; Gordon, S.; James, W. Neutralization of Infectivity of Diverse R5 Clinical Isolates of Human Immunodeficiency Virus Type 1 by gp120-Binding 2'F-RNA Aptamers. J. Virol. 2003, 77, 12692-12698.
56. 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.
57. Burmeister, P.E.; Wang, C.; Killough, J.R.; Lewis, S.D.; Horwitz, L.R.; Ferguson, A.; Thompson, K.M.; Pendergrast, P.S.; McCauley, T.G.; Kurz, M.; et al. 2'-Deoxy Purine, 2'-O-Methyl Pyrimidine (dRmY) Aptamers as Candidate Therapeutics. Oligonucleotides 2006, 16, 337-351.
58. Rohloff, J.C.; Gelinas, A.D.; Jarvis, T.C.; Ochsner, U.A.; Schneider, D.J.; Gold, L.; Janjic, N. Nucleic Acid Ligands With Protein-like Side Chains: Modified Aptamers and Their Use as Diagnostic and Therapeutic Agents. Mol. Ther. Nucleic Acids 2014, 3, e201.
59. Bugaut, A.; Toulmé, J.J.; Rayner, B. SELEX and dynamic combinatorial chemistry interplay for the selection of conjugated RNA aptamers. Org. Biomol. Chem. 2006, 4, 4082-4088.
60. Li, N.; Nguyen, H.H.; Byrom, M.; Ellington, A.D. Inhibition of Cell Proliferation by an Anti-EGFR Aptamer. PLoS ONE 2011, 6, e20299.
61. Esposito, C.L.; Passaro, D.; Longobardo, I.; Condorelli, G.; Marotta, P.; Affuso, A.; de Franciscis, V.; Cerchia, L. A Neutralizing RNA Aptamer against EGFR Causes Selective Apoptotic Cell Death. PLoS ONE 2011, 6, e24071.
62. Layzer, J.M.; McCaffrey, A.P.; Tanner, A.K.; Huang, Z.; Kay, M.A.; Sullenger, B.A. In vivo activity of nuclease-resistant siRNAs. RNA 2004, 10, 766-771.
63. Svobodova, M.; Bunka, D.H.J.; Nadal, P.; Stockley, P.G.; O'Sullivan, C.K. Selection of 2'F-modified RNA aptamers against prostate-specific antigen and their evaluation for diagnostic and therapeutic applications. Anal. Bioanal. Chem. 2013, 405, 9149-9157.
64. Lupold, S.E.; Hicke, B.J.; Lin, Y.; Coffey, D.S. Identification and Characterization of Nuclease-stabilized RNA Molecules That Bind Human Prostate Cancer Cells via the Prostate-specific Membrane Antigen. Cancer Res. 2002, 62, 4029-4033.
65. 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.
66. Cheng, C.; Chen, Y.H.; Lennox, K.A.; Behlke, M.A.; Davidson, B.L. In vivo SELEX for Identification of Brain-penetrating Aptamers. Mol. Ther. Nucleic Acids 2013, 2, e67, doi:10.1038/mtna.2012.59.
67. Lee, C.H.; Lee, Y.J.; Kim, J.H.; Lim, J.H.; Kim, J.H.; Han, W.; Lee, S.H.; Noh, G.J.; Lee, S.W. Inhibition of Hepatitis C Virus (HCV) Replication by Specific RNA Aptamers against HCV NS5B RNA Replicase. J. Virol. 2013, 87, 7064-7074.
68. Camorani, S.; Esposito, C.L.; Rienzo, A.; Catuogno, S.; Iaboni, M.; Condorelli, G.; De Franciscis, V.; Cerchia, L. Inhibition of Receptor Signaling and of Glioblastoma-derived Tumor Growth by a Novel PDGFR beta Aptamer. Mol. Ther. 2014, 22, 828-841.
69. Cerchia, L.; Esposito, C.L.; Camorani, S.; Rienzo, A.; Stasio, L.; Insabato, L.; Affuso, A.; de Franciscis, V. Targeting Axl With an High-affinity Inhibitory Aptamer. Mol. Ther. Nucleic Acids 2012, 20, 2291-2303.
70. Zhou, J.; Satheesan, S.; Li, H.; Weinberg, M.S.; Morris, K.V.; Burnett, J.C.; Rossi, J.J. Cell-Specific RNA Aptamer against Human CCR5 Specifically Targets HIV-1 Susceptible Cells and Inhibits HIV-1 Infectivity. Chem. Biol. 2015, 22, 379-390.
71. Lee, G.; MacLean, D.M.; Ulrich, H.; Zhao, X.; Aronowski, J.; Jayaraman, V. RNA Based Antagonist of NMDA Receptors. ACS Chem. Neurosci. 2014, 5, 559-567.
72. Ababneh, N.; Alshaer, W.; Allozi, O.; Mahafzah, A.; El-Khateeb, M.; Hillaireau, H.; Noiray, M.; Fattal, E.; Ismail, S. In Vitro Selection of Modified RNA Aptamers against CD44 Cancer Stem Cell Marker. Nucleic Acid Ther. 2013, 23, 401-407.
73. Zhou, J.; Swiderski, P.; Li, H.; Zhang, J.; Neff, C.P.; Akkina, R.; Rossi, J.J. Selection, characterization and application of new RNA HIV gp 120 aptamers for facile delivery of dicer substrate siRNAs into HIV infected cells. Nucleic Acids Res. 2009, 37, 3094-3109.
74. Cerchia, L.; Esposito, C.L.; Jacobs, A.H.; Tavitian, B.; De Franciscis, V. Differential SELEX in Human Glioma Cell Lines. PLoS ONE 2009, 4, e7971.
75. Meyer, C.; Berg, K.; Eydeler-Haeder, K.; Lorenzen, I.; Groetziger, J.; Rose-John, S.; Hahn, U. Stabilized Interleukin-6 receptor binding RNA aptamers. RNA Biol. 2014, 11, 57-65.
76. Pastor, F.; Soldevilla, M.M.; Villanueva, H.; Kolonias, D.; Inoges, S.; de Cerio, A.L.; Kandzia, R.; Klimyuk, V.; Gleba, Y.; Gilboa, E.; et al. CD28 Aptamers as Powerful Immune Response Modulators. Mol. Ther. Nucleic. Acids 2013, 2, e98, doi:10.1038/mtna.2013.26.
77. Pratico, E.D.; Sullenger, B.A.; Nair, S.K. Identification and Characterization of an Agonistic Aptamer against the T Cell Costimulatory Receptor, OX40. Nucleic Acid Ther. 2013, 23, 35-43.
78. Gong, Q.; Wang, J.F.; Ahmad, K.M.; Csordas, A.T.; Zhou, J.; Nie, J.; Stewart, R.; Thomson, J.A.; Rossi, J.J.; Soh, H.T. Selection Strategy to Generate Aptamer Pairs that Bind to Distinct Sites on Protein Targets. Anal. Chem. 2012, 84, 5365-5371.
79. 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.
80. Fa, M.; Radeghieri, A.; Henry, A.A.; Romesberg, F.E. Expanding the Substrate Repertoire of a DNA Polymerase by Directed Evolution. J. Am. Chem. Soc. 2004, 126, 1748-1754.
81. Chelliserrykattil, J.; Ellington, A.D. Evolution of a T7 RNA polymerase variant that transcribes 2'-O-methyl RNA. Nat. Biotechnol. 2004, 22, 1155-1160.
82. Siegmund, V.; Santner, T.; Micura, R.; Marx, A. Screening mutant libraries of T7 RNA polymerase for candidates with increased acceptance of 2'-modified nucleotides. Chem. Commun. 2012, 48, 9870-9872.
83. Waters, E.K.; Genga, R.M.; Schwartz, M.C.; Nelson, J.A.; Schaub, R.G.; Olson, K.A.; Kurz, J.C.; McGinness, K.E. Aptamer ARC19499 mediates a procoagulant hemostatic effect by inhibiting tissue factor pathway inhibitor. Blood 2011, 117, 5514-5522.
84. Xiao, Z.; Levy-Nissenbaum, E.; Alexis, F.; Lupták, A.; Teply, B.A.; Chan, J.M.; Shi, J.; Digga, E.; Cheng, J.; Langer, R.; Farokhzad, O.C. Engineering of Targeted Nanoparticles for Cancer Therapy Using InteRNAlizing Aptamers Isolated by Cell-Uptake Selection. ACS Nano 2012, 6, 696-704.
85. Wu, Y.; Sefah, K.; Liu, H.; Wang, R.; Tan, W. DNA aptamer-micelle as an efficient detection/delivery vehicle toward cancer cells. Proc. Natl. Acad. Sci. USA 2010, 107, 5-10.
86. Kato, Y.; Minakawa, N.; Komatsu, Y.; Kamiya, H.; Ogawa, N.; Harashima, H.; Matsuda, A. New NTP analogs: The synthesis of 4'-thioUTP and 4'-thioCTP and their utility for SELEX. Nucleic Acids Res. 2005, 33, 2942-2951.
87. Minakawa, N.; Sanji, M.; Kato, Y.; Matsuda, A. Investigations toward the selection of fully-modified 4'-thioRNA aptamers: Optimization of in vitro transcription steps in the presence of 4'-thioNTPs. Bioorg. Med. Chem. 2008, 16, 9450-9456.
88. Inoue, N.; Shionoya, A.; Minakawa, N.; Kawakami, A.; Ogawa, N.; Matsuda, A. Amplification of 4'-ThioDNA in the Presence of 4'-Thio-dTTP and 4'-Thio-dCTP, and 4'-ThioDNA-Directed Transcription in Vitro and in Mammalian Cells. J. Am. Chem. Soc. 2007, 129, 15424-15425.
89. Kojima, T.; Furukawa, K.; Maruyama, H.; Inoue, N.; Tarashima, N.; Matsuda, A.; Minakawa, N. PCR Amplification of 4'-ThioDNA Using 2'-Deoxy-4'-thionucleoside 5'-triphosphates. ACS Synth. Biol. 2013, 2, 529-536.
90. Siegmund, V.; Santner, T.; Micura, R.; Marx, A. Enzymatic synthesis of 2'-methylseleno-modified RNA. Chem. Sci. 2011, 2, 2224-2231.
91. Santner, T.; Siegmund, V.; Marx, A.; Micura, R. The synthesis of 2'-methylseleno adenosine and guanosine 5'-triphosphates. Bioorg. Med. Chem. 2012, 20, 2416-2418.
92. Tarashima, N.; Sumitomo, T.; Ando, H.; Furukawa, K.; Ishida, T.; Minakawa, N. Synthesis of DNA fragments containing 2'-deoxy-4'-selenonucleoside units using DNA polymerases: Comparison of dNTPs with O, S and Se at the 4'-position in replication. Org. Biomol. Chem. 2015, 13, 6949-6952.
93. Eckstein, F. Phosphorothioate Oligodeoxynucleotides: What Is Their Origin and What Is Unique about Them? Antisense Nucleic Acid Drug Dev. 2000, 10, 117-121.
94. Mann, A.P.; Somasunderam, A.; Nieves-Alicea, R.; Li, X.; Hu, A.; Sood, A.K.; Ferrari, M.; Gorenstein, D.G.; Tanaka, T. Identification of Thioaptamer Ligand against E-Selectin: Potential Application for Vasculature Targeting. PLoS ONE 2010, 5, e13050.
95. King, D.J.; Bassett, S.E.; Li, X.; Fennewald, S.A.; Herzog, N.K.; Luxon, B.A.; Shope, R.; Gorenstein, D.G. Combinatorial Selection and Binding of Phosphorothioate Aptamers Targeting Human NF-κB RelA(p65) and p50. Biochemistry 2002, 41, 9696-9706.
96. Somasunderam, A.; Ferguson, M.R.; Rojo, D.R.; Thiviyanathan, V.; Li, X.; O'Brien, W.A.; Gorenstein, D.G. Combinatorial Selection, Inhibition, and Antiviral Activity of DNA Thioaptamers Targeting the RNase H Domain of HIV-1 Reverse Transcriptase. Biochemistry 2005, 44, 10388-10395.
97. Somasunderam, A.; Thiviyanathan, V.; Tanaka, T.; Li, X.; Neerathilingam, M.; Lokesh, G.L.R.; 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.
98. Gandham, S.H.A.; Volk, D.E.; Lokesh, G.L.R.; Neerathilingam, M.; Gorenstein, D.G. Thioaptamers targeting dengue virus type-2 envelope protein domain III. Biochem. Biophys. Res. Commun. 2014, 453, 309-315.
99. He, W.; Elizondo-Riojas, M.A.; Li, X.; Lokesh, G.L.R.; Somasunderam, A.; Thiviyanathan, V.; Volk, D.E.; Durland, R.H.; Englehardt, J.; Cavasotto, C.N.; et al. X-Aptamers: A Bead-Based Selection Method for Random Incorporation of Druglike Moieties onto Next-Generation Aptamers for Enhanced Binding. Biochemistry 2012, 51, 8321-8323.
100. Carrasco, N.; Huang, Z. Enzymatic Synthesis of Phosphoroselenoate DNA Using Thymidine 5'-(α-P-seleno)triphosphate and DNA Polymerase for X-ray Crystallography via MAD. J. Am. Chem. Soc. 2004, 126, 448-449.
101. Victorova, L.S.; Dyatkina, N.B.; Mozzherin, D.J.; Atrazhev, A.M.; Krayevsky, A.A.; Kukhanova, M.K. Formation of phosphonester bonds catalyzed by DNA polymerase. Nucleic Acids Res. 1992, 20, 783-789.
102. Dineva, M.A.; Ivanov, I.G.; Petkov, D.D. P-alpha-methyl deoxynucleoside triphosphates as substrates for E. coli DNA polymerase I in a template-directed synthesis of DNA. Nucleosides Nucleotides 1997, 16, 1875-1882.
103. Lin, J.; Shaw, B.R. Synthesis of a novel triphosphate analogue: Nucleoside α-P-borano, α-Pthiotriphosphate. Chem. Commun. 2000, 2115-2116.
104. Lato, S.M.; Ozerova, N.D.S.; He, K.; Sergueeva, Z.; Shaw, B.R.; Burke, D.H. Boron-containing aptamers to ATP. Nucleic Acids Res. 2002, 30, 1401-1407.
105. Jäger, 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.
106. Hollenstein, M. Synthesis of deoxynucleoside triphosphates that include proline, urea, or sulfamide groups and their polymerase incorporation into DNA. Chem. Eur. J. 2012, 18, 13320-13330.
107. Hollenstein, M. Deoxynucleoside triphosphates bearing histamine, carboxylic acid, and hydroxyl residues-Synthesis and biochemical characterization. Org. Biomol. Chem. 2013, 11, 5162- 5172.
108. Hocek, M. Synthesis of Base-Modified 2'-Deoxyribonucleoside Triphosphates and Their Use in Enzymatic Synthesis of Modified DNA for Applications in Bioanalysis and Chemical Biology. J. Org. Chem. 2014, 79, 9914-9921.
109. Latham, J.A.; Johnson, R.; Toole, J.J. The application of a modified nucleotide in aptamer selection: Novel thrombin aptamers containing-(1-pentynyl)-2'-deoxyuridine. Nucleic Acids Res. 1994, 22, 2817-2822.
110. Jensen, K.B.; Atkinson, B.L.; Willis, M.C.; Koch, T.H.; Gold, L. Using in vitro selection to direct the covalent attachment of human immunodeficiency virus type 1 Rev protein to high-affinity RNA ligands. Proc. Natl. Acad. Sci. USA 1995, 92, 12220-12224.
111. Battersby, T.R.; Ang, D.N.; Burgstaller, P.; Jurczyk, S.C.; Bowser, M.T.; Buchanan, D.D.; Kennedy, R.T.; Benner, S.A. Quantitative Analysis of Receptors for Adenosine Nucleotides Obtained via In Vitro Selection from a Library Incorporating a Cationic Nucleotide Analog. J. Am. Chem. Soc. 1999, 121, 9781-9789.
112. Vaish, N.K.; Larralde, R.; Fraley, A.W.; Szostak, J.W.; McLaughlin, L.W. A Novel, Modification-Dependent ATP-Binding Aptamer Selected from an RNA Library Incorporating a Cationic Functionality. Biochemistry 2003, 42, 8842-8851.
113. Li, M.; Lin, N.; Huang, Z.; Lupei, D.; Altier, C.; Fang, H.; Wang, B. Selecting Aptamers for a Glycoprotein through the Incorporation of the Boronic Acid Moiety. J. Am. Chem. Soc. 2008, 130, 12636-12638.
114. Imaizumi, Y.; Kasahara, Y.; Fujita, H.; Kitadume, S.; Ozaki, H.; Endoh, T.; Kuwahara, M.; Sugimoto, N. Efficacy of Base-Modification on Target Binding of Small Molecule DNA Aptamers. J. Am. Chem. Soc. 2013, 135, 9412-9419.
115. Shoji, A.; Kuwahara, M.; Ozaki, H.; Sawai, H. Modified DNA aptamer that binds the (R)-Isomer of a thalidomide derivative with high enantioselectivity. J. Am. Chem. Soc. 2007, 129, 1456-1464.
116. Horiya, S.; MacPherson, I.S.; Krauss, I.J. Recent strategies targeting HIV glycans in vaccine design. Nat. Chem. Biol. 2014, 10, 990-999.
117. MacPherson, I.S.; Temme, J.S.; Habeshian, S.; Felczak, K.; Pankiewicz, K.; Hedstrom, L.; Krauss, I.J. Multivalent Glycocluster Design through Directed Evolution. Angew. Chem. Int. Ed. 2011, 50, 11238-11242.
118. Temme, J.S.; Drzyzga, M.G.; MacPherson, I.S.; Krauss, I.J. Directed Evolution of 2G12-Targeted Nonamannose Glycoclusters by SELMA. Chem. Eur. J. 2013, 19, 17291-17295.
119. Temme, J.S.; MacPherson, I.S.; DeCourcey, J.F.; Krauss, I.J. High Temperature SELMA: Evolution of DNA-Supported Oligomannose Clusters Which Are Tightly Recognized by HIV bnAb 2G12. J. Am. Chem. Soc. 2014, 136, 1726-1729.
120. Masud, M.M.; Kuwahara, M.; Ozaki, H.; Sawai, H. Sialyllactose-binding modified DNA aptamer bearing additional functionality by SELEX. Bioorg. Med. Chem. 2004, 12, 1111-1120.
121. Ohsawa, K.; Kasamatsu, T.; Nagashima, J.-I.; Hanawa, K.; Kuwahara, M.; Ozaki, H.; Sawai, H. Arginine-modified DNA Aptamers That Show Enantioselective Recognition of the Dicarboxylic Acid Moiety of Glutamic Acid. Anal. Sci. 2008, 24, 167-172.
122. 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.
123. Morihiro, K.; Hoshino, H.; Hasegawa, O.; Kasahara, Y.; Nakajima, K.; Kuwahara, M.; Tsunoda, S.I.; Obika, S. Polymerase incorporation of a 2'-deoxynucleoside-5'-triphosphate bearing a 4-hydroxy-2-mercaptobenzimidazole nucleobase analogue. Bioorg. Med. Chem. Lett. 2015, 25, 2888-2891.
124. Smith, C.C.; Hollenstein, M.; Leumann, C.J. The synthesis and application of a diazirine-modified uridine analogue for investigating RNA-protein interactions. RSC Adv. 2014, 4, 48228-48235.
125. Brody, E.; Gold, L.; Mehan, M.; Ostroff, R.; Rohloff, J.; Walker, J.; Zichi, D. Life's Simple Measures: Unlocking the Proteome. J. Mol. Biol. 2012, 422, 595-606.
126. Davies, D.R.; Gelinas, A.D.; Zhang, C.; Rohloff, J.C.; Carter, J.D.; O'Connell, D.; Gold, L.; Janjic, N.; Jarvis, T.C. Unique motifs and hydrophobic interactions shape the binding of modified DNA ligands to protein targets. Proc. Natl. Acad. Sci. USA 2012, 109, 19971-19976.
127. Cox, J.; Mann, J. Quantitative, High-Resolution Proteomics for Data-Driven Systems Biology. Annu. Rev. Biochem. 2011, 80, 273-299.
128. Gold, L.; Ayers, D.; Bertino, J.; Bock, C.; Bock, A.; Brody, E.N.; Carter, J.; Dalby, A.B.; Eaton, B.E.; Fitzwater, T.; et al. Aptamer-Based Multiplexed Proteomic Technology for Biomarker Discovery. PLoS ONE 2010, 5, e15004.
129. Gelinas, A.D.; Davies, D.R.; Edwards, T.E.; Rohloff, J.C.; Carter, J.D.; Zhang, C.; Gupta, S.; Ishikawa, Y.; Hirota, M.; Nakaishi, Y.; et al. Crystal Structure of Interleukin-6 in Complex with a Modified Nucleic Acid Ligand. J. Biol. Chem. 2014, 289, 8720-8734.
130. Gupta, S.; Hirota, M.; Waugh, S.M.; Murakami, I.; Suzuki, T.; Muraguchi, M.; Shibamori, M.; Ishikawa, Y.; Jarvis, T.C.; Carter, J.D.; et al. Chemically-Modified DNA Aptamers Bind Interleukin-6 with High Affinity and Inhibit Signaling by Blocking its Interaction with Interleukin-6 Receptor. J. Biol. Chem. 2014, 289, 8706-8719.
131. Hopfield, J.J. Kinetic Proofreading: A New Mechanism for Reducing Errors in Biosynthetic Processes Requiring High Specificity. Proc. Natl. Acad. Sci. USA 1974, 71, 4135-4139.
132. Hathout, Y.; Brody, E.; Clemens, P.R.; Cripe, L.; DeLisle, R.K.; Furlong, P.; Gordish-Dressman, H.; Hache, L.; Henricson, E.; Hoffman, E.P.; et al. Large-scale serum protein biomarker discovery in Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. USA 2015, 112, 7153-7158.
133. Nolte, A.; Klussmann, S.; Bald, R.; Erdmann, V.A.; Fuerste, J.P. Mirror-design of L-oligonucleotide ligands binding to L-arginine. Nat. Biotechnol. 1996, 14, 1116-1119.
134. Klussmann, S.; Nolte, A.; Bald, R.; Erdmann, V.A.; Fuerste, J.P. Mirror-image RNA that binds D-adenosine. Nat. Biotechnol. 1996, 14, 1112-1115.
135. Sooter, L.J.; Ellington, A.D. Reflections on a Novel Therapeutic Candidate. Chem. Biol. 2002, 9, 857-858.
136. Semizarov, D.G.; Arzumanov, A.A.; Dyatkina, N.B.; Meyer, A.; Vichier-Guerre, S.; Gosselin, G.; Rayner, B.; Imbach, J.L.; Krayevsky, A.A. Stereoisomers of Deoxynucleoside 5'-Triphosphates as Substrates for Template-dependent and -independent DNA Polymerases. J. Biol. Chem. 1997, 272, 9556-9560.
137. Forsman, J.J.; Leino, R. L-Pentoses in Biological and Medicinal Applications. Chem. Rev. 2011, 111, 3334-3357.
138. Loakes, D.; Holliger, P. Polymerase engineering: Towards the encoded synthesis of unnatural biopolymers. Chem. Commun. 2009, 4619-4631.
139. Sczepanski, J.T.; Joyce, G.F. A cross-chiral RNA polymerase ribozyme. Nature 2014, 515, 440-442.
140. Vater, A.; Klussmann, S. Turning mirror-image oligonucleotides into drugs: The evolution of Spiegelmer therapeutics. Drug Discov Today 2015, 20, 147-155.
141. Vater, A.; Sell, S.; Kaczmarek, P.; Maasch, C.; Buchner, K.; Pruszynska-Oszmalek, E.; Kolodziejski, P.; Purschke, W.G.; Nowak, K.W.; Strowski, M.Z.; et al. A Mixed Mirror-image DNA/RNA Aptamer Inhibits Glucagon and Acutely Improves Glucose Tolerance in Models of Type 1 and Type 2 Diabetes. J. Biol. Chem. 2013, 288, 21136-21147.
142. Purschke, W.G.; Hoehlig, K.; Buchner, K.; Zboralski, D.; Schwoebel, F.; Vater, A.; Klussmann, S. Identification and characterization of a mirror-image oligonucleotide that binds and neutralizes sphingosine 1-phosphate, a central mediator of angiogenesis. Biochem. J. 2014, 462, 153-162.
143. Sczepanski, J.T.; Joyce, G.F. Binding of a Structured D-RNA Molecule by an L-RNA Aptamer. J. Am. Chem. Soc. 2013, 135, 13290-13293.
144. Eschenmoser, A. Chemical Etiology of Nucleic Acid Structure. Science 1999, 284, 2118-2124.
145. Pinheiro, V.B.; Taylor, A.I.; Cozens, C.; Abramov, M.; Renders, M.; Zhang, S.; Chaput, J.C.; Wengel, J.; Peak-Chew, S.; McLaughlin, S.H.; et al. Synthetic Genetic Polymers Capable of Heredity and Evolution. Science 2012, 336, 341-344.
146. Kimoto, M.; Yamashige, R.; Matsunaga, K.; Yokoyama, S.; Hirao, I. Generation of high-affinity DNA aptamers using an expanded genetic alphabet. Nat. Biotechnol. 2013, 31, 453-457.
147. Taylor, A.I.; Pinheiro, V.B.; Smola, M.J.; Morgunov, A.S.; Peak-Chew, S.; Cozens, C.; Weeks, K.M.; Herdewijn, P.; Holliger, P. Catalysts from synthetic genetic polymers. Nature 2015, 518, 427-430.
148. Xiao, H.; Nasertorabi, F.; Choi, S.-H.; Han, G.W.; Reed, S.A.; Stevens, R.C.; Schultz, P.G. Exploring the potential impact of an expanded genetic code on protein function. Proc. Natl. Acad. Sci. USA 2015, 112, 6961-6966.
149. Attwater, J.; Holliger, P. A synthetic approach to abiogenesis. Nat. Methods 2014, 11, 495-498.
150. Malyshev, D.A.; Dhami, K.; Lavergne, T.; Chen, T.; Dai, N.; Foster, J.M.; Corrêa, I.R. Jr.; Romesberg, F.E. A semi-synthetic organism with an expanded genetic alphabet. Nature 2014, 509, 385-388.
151. Georgiadis, M.M.; Singh, I.; Kellett, W.F.; Hoshika, S.; Benner, S.A.; Richards, N.G.J. Structural Basis for a Six Nucleotide Genetic Alphabet. J. Am. Chem. Soc. 2015, 137, 6947-6955.
152. Zhang, L.Q.; Yang, Z.Y.; Sefah, K.; Bradley, K.M.; Hoshika, S.; Kim, M.J.; Kim, H.J.; Zhu, G.Z.; Jimenez, E.; Cansiz, S.; et al. Evolution of Functional Six-Nucleotide DNA. J. Am. Chem. Soc. 2015, 137, 6734-6737.
153. Herdewijn, P. Nucleic Acids with a Six-Membered "Carbohydrate" Mimic in the Backbone. Chem. Biodivers. 2010, 7, 1-59.
154. Horhota, A.; Zou, K.; Ichida, J.K.; Yu, B.; McLaughlin, L.W.; Szostak, J.W.; Chaput, J.C. Kinetic Analysis of an Efficient DNA-Dependent TNA Polymerase. J. Am. Chem. Soc. 2005, 127, 7427- 7434.
155. Dunn, M.R.; Larsen, A.C.; Zahurancik, W.J.; Fahmi, N.E.; Meyers, M.; Suo, Z.; Chaput, J.C. DNA Polymerase-Mediated Synthesis of Unbiased Threose Nucleic Acid (TNA) Polymers Requires 7-Deazaguanine To Suppress G:G Mispairing during TNA Transcription. J. Am. Chem. Soc. 2015, 137, 4014-4017.
156. 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.
157. Yu, H.; Zhang, S.; Chaput, J.C. Darwinian evolution of an alteRNAtive genetic system provides support for TNA as an RNA progenitor. Nat. Chem. Biol. 2012, 4, 183-187.
158. 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, 5401-5404.
159. Singh, S.K.; Koshkin, A.A.; Wengel, J.; Nielsen, P. LNA (locked nucleic acids): Synthesis and high-affinity nucleic acid recognition. Chem. Commun. 1998, 455-456.
160. Jespen, J.S.; Sørensen, M.D.; Wengel, J. Locked Nucleic Acid: A Potent Nucleic Acid Analog in Therapeutics and Biotechnology. Oligonucleotides 2004, 14, 130-146.
161. Lundin, K.E.; Hojland, T.; Hansen, B.R.; Persson, R.; Bramsen, J.B.; Kjems, J.; Koch, T.; Wengel, J.;Smith, C. Biological activity and biotechnological aspects of locked nucleic acids. Adv. Genet. 2013, 82, 47-107.
162. Astakhova, I.K.; Wengel, J. Scaffolding along Nucleic Acid Duplexes Using 2'-Amino-Locked Nucleic Acids. Acc. Chem. Res. 2014, 47, 1768-1777.
163. Veedu, R.N.; Vester, B.; Wengel, J. Polymerase Chain Reaction and Transcription Using Locked Nucleic Acid Nucleotide Triphosphates. J. Am. Chem. Soc. 2008, 130, 8124-8125.
164. Crouzier, L.; Dubois, C.; Edwards, S.L.; Lauridsen, L.H.; Wengel, J.; Veedu, R.N. Efficient Reverse Transcription Using Locked Nucleic Acid Nucleotides towards the Evolution of Nuclease Resistant RNA Aptamers. PLoS ONE 2012, 7, e35990.
165. Doessing, H.; Hansen, L.H.; Veedu, R.N.; Wengel, J.; Vester, B. Amplification and Re-Generation of LNA-Modified Libraries. Molecules 2012, 17, 13087-13097.
166. Kasahara, Y.; Irisawa, Y.; Ozaki, H.; Obika, S.; Kuwahara, M. 2', 4'-BNA/LNA aptamers: CE-SELEX using a DNA-based library of fulllength 2'-O, 4'-C-methylene-bridged/linked bicyclic ribonucleotides. Bioorg. Med. Chem. Lett. 2013, 23, 1288-1292.
167. Edwards, S.L.; Poongavanam, V.; Kanwar, J.R.; Roy, K.; Hillman, K.M.; Prasad, N.; Leth-Larsen, R.; Petersen, M.; Marusic, M.; Plavec, J.; et al. Targeting VEGF with LNA-stabilized G-rich oligonucleotide for efficient breast cancer inhibition. Chem. Commun. 2015, 51, 9499-9502.
168. Elle, I.C.; Karlsen, K.K.; Terp, M.G.; Larsen, N.; Nielsen, R.; Derbyshire, N.; Mandrup, S.; Ditzel, H.J.; Wengel, J. Selection of LNA-containing DNA aptamers against recombinant human CD73. Mol. BioSyst. 2015, 11, 1260-1270.
169. Hagiwara, K.; Fujita, H.; Kasahara, Y.; Irisawa, Y.; Obika, S.; Kuwahara, M. In vitro selection of DNA-based aptamers that exhibit RNA-like conformations using a chimeric oligonucleotide library that contains two different xeno-nucleic acids. Mol. BioSyst. 2015, 11, 71-76.
170. Bande, O.; El Asrar, R.A.; Braddick, D.; Dumbre, S.; Pezo, V.; Schepers, G.; Pinheiro, V.B.; Lescrinier, E.; Holliger, P.; Marlière, P.; et al. Isoguanine and 5-Methyl-Isocytosine Bases, in vitro and in vivo. Chem. Eur. J. 2015, 21, 5009-5022.
171. Veedu, R.N.; Burri, H.V.; Kumar, P.; Sharma, P.K.; Hrdlicka, P.J.; Vester, B.; Wengel, J. Polymerase-directed synthesis of C5-ethynyl locked nucleic acids. Bioorg. Med. Chem. Lett. 2010, 20, 6565-6568.
172. Sefah, K.; Yang, Z.Y.; Bradley, K.M.; Hoshika, S.; Jimenez, E.; Zhang, L.Q.; Zhu, G.Z.; Shanker, S.; Yu, F.H.; Turek, D.; et al. In vitro selection with artificial expanded genetic information systems. Proc. Natl. Acad. Sci. USA 2014, 111, 1449-1454.
173. Renders, M.; Miller, E.; Hollenstein, M.; Perrin, D.M. A Method for Selecting Modified DNAzymes without the Use of Modified DNA as a Template in PCR. Chem. Commun. 2015, 51, 1360-1362.