Whence flavins? Redox-active ribonucleotides link metabolism and genome repair to the RNA world

Accounts of Chemical Research

Volumn 45, Issue 12, 2012, Pages 2151-2159

  Nguyen, Khiem Van ^a   Burrows, Cynthia J ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYGUANINE; 8-HYDROXYGUANINE; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; DRUG DERIVATIVE; GUANINE; PYRIMIDINE DERIVATIVE; RIBOFLAVIN DERIVATIVE; RIBONUCLEOTIDE; RNA; URIC ACID;

ARTICLE; ASTRONOMY; CHEMISTRY; DNA DAMAGE; DNA REPAIR; METABOLISM; OXIDATION REDUCTION REACTION; RADIATION EXPOSURE; ULTRAVIOLET RADIATION;

DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DNA DAMAGE; DNA REPAIR; EVOLUTION, CHEMICAL; FLAVINS; GUANINE; OXIDATION-REDUCTION; PYRIMIDINES; RIBONUCLEOTIDES; RNA; ULTRAVIOLET RAYS; URIC ACID;

EID: 84871273149     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar300222j     Document Type: Article

References (53)

1. Benner, S. A.; Ellington, A. D.; Tauer, A. Modern metabolism as a palimpsest of the RNA world Proc. Natl. Acad. Sci. U.S.A. 1989, 86, 7054-7058
2. Morowitz, H. J. Beginnings of Cellular Life: Metabolism Recapitulates Biogenesis; Yale University Press: New Haven, 1992.
3. White, H. B. Coenzymes as fossils of an earlier metabolic state J. Mol. Evol. 1976, 7, 101-104
4. Yarus, M. Getting Past the RNA World: The Initial Darwinian Ancestor Cold Spring Harbor Perspect. Biol. 2011, 3, 003590
5. Burgstaller, P.; Famulok, M. Isolation of RNA Aptamers for Biological Cofactors by In Vitro Selection Angew. Chem., Int. Ed. Engl. 1994, 33, 1084-1087
6. Lauhon, C. T.; Szostak, J. W. RNA aptamers that bind flavin and nicotinamide redox cofactors J. Am. Chem. Soc. 1995, 117, 1246-1257
7. Tsukiji, S.; Pattnaik, S. B.; Suga, H. An alcohol dehydrogenase ribozyme Nat. Struct. Biol. 2003, 10, 713-717
8. 2+ dependent redox active ribozyme J. Am. Chem. Soc. 2004, 126, 5044-5045
9. Ferris, J. P.; Kuder, J. E.; Catalano, A. W. Photochemical reactions and the chemical evolution of purines and nicotinamide derivatives Science 1969, 166, 765-766
10. Powner, M.; Sutherland, J.; Szostak, J. Chemoselective multicomponent one-pot assembly of purine precursors in water J. Am. Chem. Soc. 2010, 132, 16677-16688
11. Powner, M. W.; Gerland, B.; Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions Nature 2009, 459, 239-242
12. Eschenmoser, A.; Loewenthal, E. Chemistry of potentially prebiological natural products Chem. Soc. Rev. 1992, 21, 1-16
13. Heinz, B.; Ried, W. The formation of chromophores through amino acid thermolysis and their possible role as prebiotic photoreceptors Biosystems 1981, 14, 33-40
14. Heinz, B.; Ried, W.; Dose, K. Thermal Generation of Pteridines and Flavines from Amino Acid Mixtures Angew. Chem., Int. Ed. Engl. 1979, 18, 478-483
15. Kritsky, M. S.; Telegina, T. A.; Vechtomova, Y. L.; Kolesnikov, M. P.; Lyudnikova, T. A.; Golub, O. A. Excited flavin and pterin coenzyme molecules in evolution Biochemistry (Moscow) 2010, 75, 1200-1216
16. Callahan, M. P.; Smith, K. E.; Cleaves, H. J.; Ruzicka, J.; Stern, J. C.; Glavin, D. P.; House, C. H.; Dworkin, J. P. Carbonaceous meteorites contain a wide range of extraterrestrial nucleobases Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 13995-13998
17. Botta, O.; Bada, J. L. Extraterrestrial Organic Compounds in Meteorites Surveys Geophys. 2002, 23, 411-467
18. Martin, W.; Russell, M. J. On the origin of biochemistry at an alkaline hydrothermal vent Philos. Trans. R. Soc., B 2007, 362, 1887-1926
19. Kritsky, M. S.; Telegina, T. A. Role of Nucleotide-Like Coenzymes in Primitive Evolution. In Cellular Origin and Life in Extreme Habitats; Seckbach, J., Ed.; Kluwer Academic: Dordrecht, 2005; Vol. 4, pp 215-231.
20. Sutherland, J. D.; Whitfield, J. N. Prebiotic Chemistry: A Bioorganic Perspective Tetrahedron 1997, 53, 11493-11527
21. Steenken, S.; Jovanovic, S. V. How Easily Oxidizable Is DNA? One-Electron Reduction Potentials of Adenosine and Guanosine Radicals in Aqueous Solution J. Am. Chem. Soc. 1997, 119, 617-618
22. Sugiyama, H.; Saito, I. Theoretical studies of GG-specific photocleavage of DNA via electron transfer: Signficant lowering of ionization potential and 5′-localization of HOMO of GG bases in B-form DNA J. Am. Chem. Soc. 1996, 118, 7063-7068
23. Chinnapen, D. J. F.; Sen, D. Towards Elucidation of the Mechanism of UV1C, a Deoxyribozyme with Photolyase Activity J. Mol. Biol. 2007, 365, 1326-1336
24. Chinnapen, D. J.-F.; Sen, D. A deoxyribozyme that harnesses light to repair thymine dimers in DNA Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 65-69
25. Steenken, S.; Jovanovic, S. V.; Bietti, M.; Bernhard, K. The Trap Depth (in DNA) of 8-Oxo-7,8-dihydro-2′-deoxyguanosine as Derived from Electron-Transfer Equilibria in Aqueous Solution J. Am. Chem. Soc. 2000, 122, 2373-2374
26. Luo, W.; Muller, J. G.; Burrows, C. J. The pH-dependent role of superoxide in riboflavin-catalyzed photooxidation of 8-oxo-7,8-dihydroguanosine Org. Lett. 2001, 3, 2801-2804
27. 18O-labeled guanidinohydantoin from guanosine oxidation with singlet oxygen. Implications for structure and mechanism J. Am. Chem. Soc. 2003, 125, 13926-13927
28. Ye, Y.; Munk, B. H.; Muller, J. G.; Cogbill, A.; Burrows, C. J.; Schlegel, H. B. Mechanistic aspects of the formation of guanidinohydantoin from spiroiminodihydantoin under acidic conditions Chem. Res. Toxicol. 2009, 22, 526-535
29. Bruice, T. C. Mechanisms of flavin catalysis Acc. Chem. Res. 1980, 13, 256-262
30. Smith, S. S.; Bruice, T. C. Mechanisms of isoalloxazine (flavin) hydrolysis J. Am. Chem. Soc. 1975, 97, 2875-2881
31. Nguyen, K. V.; Muller, J. G.; Burrows, C. J. Oxidation of 9-beta-D-ribofuranosyl uric acid by one-electron oxidants vs. singlet oxygen and its implications for the oxidation of 8-oxo-7,8-dihydroguanosine Tetrahedron Lett. 2011, 52, 2176-2180
32. Lazcano, A.; Guerrero, R.; Margulis, L.; Oro, J. The evolutionary transition from RNA to DNA in early cells J. Mol. Evol. 1988, 27, 283-290
33. Orgel, L. Prebiotic chemistry and the origin of the RNA world Crit. Rev. Biochem. Mol. Biol. 2004, 39, 99-123
34. Liang, M.-C.; Hartman, H.; Kopp, R. E.; Kirschvink, J. L.; Yung, Y. L. Production of hydrogen peroxide in the atmosphere of a Snowball Earth and the origin of oxygenic photosynthesis Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 18896-18899
35. Middleton, C. T.; de, L. H. K.; Su, C.; Law, Y. K.; Crespo-Hernandez, C. E.; Kohler, B. DNA excited-state dynamics: from single bases to the double helix Annu. Rev. Phys. Chem. 2009, 60, 217-239
36. Chen, J.; Kohler, B. Ultrafast nonradiative decay by hypoxanthine and several methylxanthines in aqueous and acetonitrile solution Phys. Chem. Chem. Phys. 2012, 14, 10677-10682
37. Sancar, A. Structure and Function of DNA Photolyase and Cryptochrome Blue-Light Photoreceptors Chem. Rev. 2003, 103, 2203-2238
38. Rokita, S. E.; Walsh, C. T. Flavin and 5-deazaflavin photosensitized cleavage of thymine dimer: a model of in vivo light-requiring DNA repair J. Am. Chem. Soc. 1984, 106, 4589-4595
39. Heil, K.; Pearson, D.; Carell, T. Chemical investigation of light induced DNA bipyrimidine damage and repair Chem. Soc. Rev. 2011, 40, 4271-4278
40. Nguyen, K. V.; Burrows, C. J. A Prebiotic Role for 8-Oxoguanosine as a Flavin Mimic in Pyrimidine Dimer Photorepair J. Am. Chem. Soc. 2011, 133, 14586-14589
41. Park, H.; Zhang, K.; Ren, Y.; Nadji, S.; Sinha, N.; Taylor, J.-S.; Kang, C. Crystal structure of a DNA decamer containing a cis-syn thymine dimer Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 15965-15970
42. Holman, M. R.; Ito, T.; Rokita, S. E. Self-Repair of Thymine Dimer in Duplex DNA J. Am. Chem. Soc. 2006, 129, 6-7
43. Pan, Z.; Hariharan, M.; Arkin, J. D.; Jalilov, A. S.; McCullagh, M.; Schatz, G. C.; Lewis, F. D. Electron Donor-Acceptor Interactions with Flanking Purines Influence the Efficiency of Thymine Photodimerization J. Am. Chem. Soc. 2012, 134, 3611-3611
44. Kumar, A.; Sevilla, M. D. Proton-Coupled Electron Transfer in DNA on Formation of Radiation-Produced Ion Radicals Chem. Rev. 2010, 110, 7002-7023
45. Liu, Z.; Tan, C.; Guo, X.; Kao, Y.-T.; Li, J.; Wang, L.; Sancar, A.; Zhong, D. Dynamics and mechanism of cyclobutane pyrimidine dimer repair by DNA photolyase Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 14831-14836
46. Ito, T.; Rokita, S. E. Criteria for Efficient Transport of Excess Electrons in DNA Angew. Chem., Int. Ed 2004, 43, 1839-1842
47. O'Neill, M. A.; Barton, J. K. Effects of strand and directional asymmetry on base-base coupling and charge transfer in double-helical DNA Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 16543-16550
48. Tanaka, M.; Elias, B.; Barton, J. K. DNA-Mediated Electron Transfer in Naphthalene-Modified Oligonucleotides J. Org. Chem. 2010, 75, 2423-2428
49. Nguyen, K. V.; Burrows, C. J. Photorepair of cyclobutane pyrimidine dimers by 8-oxopurine nucleosides J. Phys. Org. Chem. 2012, 25, 574-577
50. Yanagawa, H.; Ogawa, Y.; Ueno, M.; Sasaki, K.; Sato, T. A novel minimum ribozyme with oxidoreduction activity Biochemistry 1990, 29, 10585-10589
51. Yanagawa, H.; Ogawa, Y.; Ueno, M. Redox ribonucleosides. Isolation and characterization of 5-hydroxyuridine, 8-hydroxyguanosine, and 8-hydroxyadenosine from Torula yeast RNA J. Biol. Chem. 1992, 267, 13320-13326
52. Ren, J.; Kotaka, M.; Lockyer, M.; Lamb, H. K.; Hawkins, A. R.; Stammers, D. K. GTP Cyclohydrolase II Structure and Mechanism J. Biol. Chem. 2005, 280, 36912-36919
53. Steele, A.; McCubbin, F. M.; Fries, M.; Kater, L.; Boctor, N. Z.; Fogel, M. L.; Conrad, P. G.; Glamoclija, M.; Spencer, M.; Morrow, A. L.; Hammond, M. R.; Zare, R. N.; Vicenzi, E. P.; Siljeström, S.; Bowden, R.; Herd, C. D. K.; Mysen, B. O.; Shirey, S. B.; Amundsen, H. E. F.; Treiman, A. H.; Bullock, E. S.; Jull, A. J. T. A Reduced Organic Carbon Component in Martian Basalts Science 2012, 337, 212-215