Highly efficient incorporation of the fluorescent nucleotide analogs tC and tCO by Klenow fragment

Nucleic Acids Research

Volumn 37, Issue 12, 2009, Pages 3924-3933

  Sandin, Peter ^a   Stengel, Gudrun ^b   Ljungdahl, Thomas ^a   Börjesson, Karl ^a   Macao, Bertil ^c   Wilhelmsson, L Marcus ^a  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

1,3 DIAZA 2 OXO PHENOTHIAZINE; 1,3 DIAZA 2 OXO PHENOXAZINE; CYTIDINE TRIPHOSPHATE; CYTOSINE DERIVATIVE; DNA POLYMERASE; GUANINE; KLENOW FRAGMENT PROTEIN; PHENOTHIAZINE 5 TRIPHOSPHATE; PHENOTHIAZINE DERIVATIVE; PHENOXAZINE 5 TRIPHOSPHATE; PHENOXAZINE DERIVATIVE; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BASE PAIRING; BINDING COMPETITION; CONTROLLED STUDY; DNA BINDING; ENZYME ACTIVE SITE; ENZYME BINDING; ESCHERICHIA COLI; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION;

BINDING, COMPETITIVE; DEOXYRIBONUCLEOSIDES; DNA; DNA POLYMERASE I; DNA PRIMERS; FLUORESCENCE POLARIZATION; FLUORESCENT DYES; KINETICS; OXAZINES; PHENOTHIAZINES;

EID: 67651163670     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp266     Document Type: Article

References (58)

1. Asseline,U. (2006) Development and applications of fluorescent oligonucleotides. Curr. Org. Chem., 10, 491-518.
2. Cekan,P. and Sigurdsson,S.T. (2008) Single base interrogation by a fluorescent nucleotide: Each of the four DNA bases identified by fluorescence spectroscopy. Chem. Commun., 29, 3393-3395.
3. Tanaka,K. and Okamoto,A. (2008) Design of a pyrene-containing fluorescence probe for labeling of RNA poly(A) tracts. Bioorg. Med. Chem., 16, 400-404.
4. Srivatsan,S.G., Weizman,H. and Tor,Y. (2008) A highly fluorescent nucleoside analog based on thieno[3,4-d] pyrimidine senses mismatched pairing. Org. Biomol. Chem., 6, 1334-1338.
5. Srivatsan,S.G. and Tor,Y. (2007) Fluorescent pyrimidine ribonucleotide: Synthesis, enzymatic incorporation, and utilization. J. Am. Chem. Soc., 129, 2044-2053.
6. Socher,E., Jarikote,D.V., Knoll,A., Roglin,L., Burmeister,J. and Seitz,O. (2008) FIT probes: Peptide nucleic acid probes with a fluorescent base surrogate enable real-time DNA quantification and single nucleotide polymorphism discovery. Anal. Biochem., 375 318-330.
7. Saito,Y., Hanawa,K., Kawasaki,N., Bag,S.S. and Saito,I. (2006) Acridone-labeled base-discriminating fluorescence (BDF) nucleoside: Synthesis and their photophysical properties. Chem. Lett., 35 1182-1183.
8. Okamoto,A., Tainaka,K. and Saito,I. (2003) Clear distinction of purine bases on the complementary strand by a fluorescence change of a novel fluorescent nucleoside. J. Am. Chem. Soc., 125, 4972-4973.
9. Mizuta,M., Seio,K., Miyata,K. and Sekine,M. (2007) Fluorescent pyrimidopyrimidoindole nucleosides: Control of photophysical characterizations by substituent effects. J. Org. Chem., 72, 5046-5055.
10. Krueger,A.T. and Kool,E.T. (2008) Fluorescence of size-expanded DNA bases: Reporting on DNA sequence and structure with an unnatural genetic set. J. Am. Chem. Soc., 130, 3989-3999.
11. Ikeda,S., Kubota,T., Kino,K. and Okamoto,A. (2008) Sequence dependence of fluorescence emission and quenching of doubly thiazole orange labeled DNA: Effective design of a hybridization-sensitive probe. Bioconjugate Chem., 19, 1719-1725.
12. Moser,A.M., Patel,M., Yoo,H., Balis,F.M. and Hawkins,M.E. (2000) Real-time fluorescence assay for O-6-alkylguanine-DNA alkyltransferase. Anal. Biochem., 281, 216-222.
13. Stivers,J.T., Pankiewicz,K.W. and Watanabe,K.A. (1999) Kinetic mechanism of damage site recognition and uracil flipping by Escherichia coli uracil DNA glycosylase. Biochemistry., 38, 952-963.
14. Otto,M.R., Bloom,L.B., Goodman,M.F. and Beechem,J.M. (1998) Stopped-flow fluorescence study of precatalytic primer strand base-unstacking transitions in the exonuclease cleft of bacteriophage T4 DNA polymerase. Biochemistry., 37, 10156-10163.
15. Hawkins,M.E., Pfeiderer,W., Mazumder,A., Pommier,Y.G. and Falls,F.M. (1995) Incorporation of a fluorescent guanosine analog into oligonucleotides and its application to a real-time assay for the HIV-1 integrase 3′-processing reaction. Nucleic Acids Res., 23, 2872-2880.
16. Raney,K.D., Sowers,L.C., Millar,D.P. and Benkovic,S.J. (1994) A fluorescence-based assay for monitoring helicase activity. Proc. Natl Acad. Sci. USA, 91, 6644-6648.
17. Giller,G., Tasara,T., Angerer,B., Muhlegger,K., Amacker,M. and Winter,H. (2003) Incorporation of reporter molecule-labeled nucleotides by DNA polymerases. I. Chemical synthesis of various reporter group-labeled 2′-deoxyribonucleoside-5′-triphosphates. Nucleic Acids Res., 31, 2630-2635.
18. Tasara,T., Angerer,B., Damond,M., Winter,H., Dorhofer,S., Hubscher,U. and Amacker,M. (2003) Incorporation of reporter molecule-labeled nucleotides by DNA polymerases. II. High-density labeling of natural DNA. Nucleic Acids Res., 31, 2636-2646.
19. Rist,M.J. and Marino,J.P. (2002) Fluorescent nucleotide base analogs as probes of nucleic acid structure, dynamics and interactions. Curr. Org. Chem., 6, 775-793.
20. Yang,K.S., Matsika,S. and Stanley,R.J. (2007) 6MAP, a fluorescent adenine analogue, is a probe of base flipping by DNA photolyase. J. Phys. Chem. B., 111, 10615-10625.
21. Chandrashekaran,S., Manjunatha,U.H. and Nagaraja,V. (2004) KpnI restriction endonuclease and methyltransferase exhibit contrasting mode of sequence recognition. Nucleic Acids Res., 32, 3148-3155.
22. Gowher,H. and Jeltsch,A. (2000) Molecular enzymology of the EcoRV DNA-(adenine-N(6))-methyltransferase: Kinetics of DNA binding and bending, kinetic mechanism and linear diffusion of the enzyme on DNA. J. Mol. Biol., 303, 93-110.
23. Pues,H., Bleimling,N., Holz,B., Wolcke,J. and Weinhold,E. (1999) Functional roles of the conserved aromatic amino acid residues at position 108 (motif IV) and position 196 (motif VIII) in base flipping and catalysis by the N6-adenine DNA methyltransferase from Thermus aquaticus. Biochemistry, 38, 1426-1434.
24. Mernagh,D.R., Taylor,I.A. and Kneale,G.G. (1998) Interaction of the type I methyltransferase M.EcoR1241 with modified DNA substrates: Sequence discrimination and base flipping. Biochem. J., 336, 719-725.
25. Holz,B., Klimasauskas,S., Serva,S. and Weinhold,E. (1998) 2-Aminopurine as a fluorescent probe for DNA base flipping by methyltransferases. Nucleic Acids Res., 26, 1076-1083.
26. Allan,B.W., Beechem,J.M., Lindstrom,W.M. and Reich,N.O. (1998) Direct real time observation of base flipping by the EcoRI DNA methyltransferase. J. Biol. Chem., 273, 2368-2373.
27. Kenfack,C.A., Piemont,E., Ben Gaied,N., Burger,A. and Mely,Y. (2008) Time-resolved fluorescent properties of 8-vinyl-deoxyadenosine and 2-amino-deoxyribosylpurine exhibit different sensitivity to their opposite base in duplexes. J. Phys. Chem. B., 112, 9736-9745.
28. Lee,B.J., Barch,M., Castner,E.W., Volker,J. and Breslauer,K.J. (2007) Structure and dynamics in DNA looped domains: CAG triplet repeat sequence dynamics probed by 2-aminopurine fluorescence. Biochemistry 46, 10756-10766.
29. Raghavan,S.C., Houston,S., Hegde,B.G., Langen,R., Haworth,I.S. and Lieber,M.R. (2004) Stability and strand asymmetry in the non-B DNA structure at the bcl-2 major breakpoint region. J. Biol. Chem., 279, 46213-46225.
30. Huizenga,D.E. and Szostak,J.W. (1995) A DNA aptamer that binds adenosine and ATP. Biochemistry, 34, 656-665.
31. Guest,C.R., Hochstrasser,R.A., Sowers,L.C. and Millar,D.P. (1991) Dynamics of mismatched base-pairs in DNA. Biochemistry, 30, 3271-3279.
32. Nordlund,T.M., Andersson,S., Nilsson,L., Rigler,R., Gräslund,A. and McLaughlin,L.W. (1989) Structure and dynamics of a fluorescent DNA oligomer containing the EcorI recognition sequence - fluorescence, molecular-dynamics, and NMR-studies. Biochemistry, 28, 9095-9103.
33. Zhang,H., Cao,W., Zakharova,E., Konigsberg,W. and De la Cruz,E.M. (2007) Fluorescence of 2-aminopurine reveals rapid conformational changes in the RB69 DNA polymerase-primer/template complexes upon binding and incorporation of matched deoxynucleoside triphosphates. Nucleic Acids Res., 35, 6052-6062.
34. Stengel,G., Gill,J.P., Sandin,P., Wilhelmsson,L.M., Albinsson,B., Nordén,B. and Millar,D. (2007) Conformational dynamics of DNA polymerase probed with a novel fluorescent DNA base analogue. Biochemistry, 46, 12289-12297.
35. DeLucia,A.M., Grindley,N.D.F. and Joyce,C.M. (2007) Conformational changes during normal and error-prone incorporation of nucleotides by a y-family DNA polymerase detected by 2-aminopurine fluorescence. Biochemistry, 46, 10790-10803.
36. Purohit,V., Grindley,N.D.F. and Joyce,C.M. (2003) Use of 2-aminopurine fluorescence to examine conformational changes during nucleotide incorporation by DNA polymerase I (Klenow fragment). Biochemistry, 42, 10200-10211.
37. Hawkins,M.E., Pfleiderer,W., Balis,F.M., Porter,D. and Knutson,J.R. (1997) Fluorescence properties of pteridine nucleoside analogs as monomers and incorporated into oligonucleotides. Anal. Biochem, 244, 86-95.
38. Godde,F., Toulmé,J.-J. and Moreau,S. (1998) Benzoquinazoline derivatives as substitutes for thymine in nucleic acid complexes. Use of fluorescence emission of benzo[g]quinazoline-2,4-(1H,3H)-dione in probing duplex and triplex formation. Biochemistry, 37, 13765-13775.
39. Lin,K.Y., Jones,R.J. and Matteucci,M. (1995) Tricyclic 2′-deoxycytidine analogs - syntheses and incorporation into oligodeoxynucleotides which have enhanced binding to complementary RNA. J. Am. Chem. Soc., 117, 3873-3874.
40. Sandin,P., Börjesson,K., Li,H., Mårtensson,J., Brown,T., Wilhelmsson,L.M. and Albinsson,B. (2008) Characterization and use of an unprecedentedly bright and structurally nonperturbing fluorescent DNA base analogue. Nucleic Acids Res., 36, 157-167.
41. Sandin,P., Wilhelmsson,L.M., Lincoln,P., Powers,V.E.C., Brown,T. and Albinsson,B. (2005) Fluorescent properties of DNA base analogue tC upon incorporation into DNA - negligible influence of neighbouring bases on fluorescence quantum yield. Nucleic Acids Res., 33, 5019-5025.
42. Engman,K.C., Sandin,P., Osborne,S., Brown,T., Billeter,M., Lincoln,P., Nordén,B., Albinsson,B. and Wilhelmsson,L.M. (2004) DNA adopts normal B-form upon incorporation of highly fluorescent DNA base analogue tC: NMR structure and UV-Vis spectroscopy characterization. Nucleic Acids Res., 32, 5087-5095.
43. Wilhelmsson,L.M., Sandin,P., Holmén,A., Albinsson,B., Lincoln,P. and Nordén,B. (2003) Photophysical characterization of fluorescent DNA base analogue, tC. J. Phys. Chem. B., 107, 9094-9101.
44. Chelliserrykattil,J., Lu,H., Lee,A.H.F. and Kool,E.T. (2008) Polymerase ampli.cation, cloning, and gene expression of benzohomologues 'yDNA' base pairs. Chem. Bio. Chem., 9, 2976-2980.
45. Bloom,L.B., Otto,M.R., Beechem,J.M. and Goodman,M.F. (1993) Influence of 5′-nearest neighbors on the insertion kinetics of the fluorescent nucleotide analog 2-aminopurine by Klenow fragment. Biochemistry, 32, 11247-11258.
46. Matray,T.J. and Kool,E.T. (1999) A specific partner for abasic damage in DNA. Nature, 399, 704-708.
47. Kool,E.T. (2002) Active site tightness and substrate fit in DNA replication. Annu. Rev. Biochem., 71, 191-219.
48. Sandin,P., Lincoln,P., Brown,T. and Wilhelmsson,L.M. (2007) Synthesis and oligonucleotide incorporation of fluorescent cytosine analogue tC: A promising nucleic acid probe. Nature Protocols, 2, 615-623.
49. Ludwig,J. (1981) A new route to nucleoside 5′-triphosphates. Acta Biochim. Biophys. Acad. Sci. Hung., 16, 131-133.
50. Goodman,M.F., Creighton,S., Bloom,L.B. and Petruska,J. (1993) Biochemical basis of DNA-replication fidelity. Crit. Rev. Biochem. Mol. Biol., 28, 83-126.
51. O. Biophys. Chem., 139, 24-28.
52. Beckman,J., Kincaid,K., Hocek,M., Spratt,T., Engels,J., Cosstick,R. and Kuchta,R.D. (2007) Human DNA polymerase alpha uses a combination of positive and negative selectivity to polymerize purine dNTPs with high fidelity. Biochemistry, 46, 448-460.
53. Dahlberg,M.E. and Benkovic,S.J. (1991) Kinetic mechanism of DNA polymerase I (Klenow fragment): Identification of a second conformational change and evaluation of the internal equilibrium constant. Biochemistry, 30, 4835-4843.
54. Li,Y., Korolev,S. and Waksman,G. (1998) Crystal structures of open and closed forms of binary and tertnary complexes of the large fragment of Thermus aquaticus DNA polymerase I: Structural basis for nucleotide incorporation. EMBO J., 17, 7514-7525.
55. Bailey,M.F., van der Schans,E.J.C. and Millar,D.P. (2004) Thermodynamic dissection of the polymerizing and editing modes of a DNA polymerase. J. Mol. Biol., 336, 673-693.
56. Eger,B.T., Kuchta,R.D., Carroll,S.S., Benkovic,P.A., Dahlberg,M.E., Joyce,C.M. and Benkovic,S.J. (1991) Mechanism of DNA-replication fidelity for 3 mutants of DNA-polymerase I: Klenow fragment KF(Exo+), KF(Pola5), and KF(Exo-). Biochemistry, 30, 1441-1448.
57. Cheng,Y. and Prusoff,W.H. (1973) Relationship between inhibition constant (K1) and concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic-reaction. Biochem. Pharmacol., 22, 3099-3108.
58. Moran,S., Ren,R.X.F., Rumney,S. and Kool,E.T. (1997) Difluorotoluene, a nonpolar isostere for thymine, codes specifically and efficiently for adenine in DNA replication. J. Am. Chem. Soc., 119, 2056-2057.