Probing murine methyltransfease Dnmt3a interactions with benzo[a]pyrene-modified DNA by fluorescence methods

FEBS Journal

Volumn 279, Issue 20, 2012, Pages 3965-3980

  Minero, Antonio S ^a   Lukashevich, Olga V ^a   Cherepanova, Natalia A ^a   Kolbanovskiy, Alexander ^b   Geacintov, Nicholas E ^b   Gromova, Elizaveta S ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

benzo a pyrene DNA; fluorescence; intercalation; methylation; minor groove

Indexed keywords

ADENINE; BENZO[A]PYRENE; CYTOSINE; DIHYDROXYBENZO[A]PYRENE OXIDE; DNA; DNA METHYLTRANSFERASE 3A; GUANINE; OLIGODEOXYRIBONUCLEOTIDE;

ARTICLE; CARCINOGEN DNA INTERACTION; CATALYSIS; CONFORMATION; CONTROLLED STUDY; COVALENT BOND; CPG ISLAND; DNA MODIFICATION; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; FLUORESCENCE; INTERCALATION COMPLEX; METHYLATION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; STEREOISOMERISM;

ADENINE; ANIMALS; BASE SEQUENCE; BENZO(A)PYRENE; BINDING SITES; BIOCATALYSIS; CATALYTIC DOMAIN; CYTOSINE; DNA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA ADDUCTS; DNA METHYLATION; GUANINE; KINETICS; MICE; NUCLEIC ACID CONFORMATION; OLIGODEOXYRIBONUCLEOTIDES; PROTEIN BINDING; SPECTROMETRY, FLUORESCENCE; STEREOISOMERISM; SUBSTRATE SPECIFICITY;

EUKARYOTA; MURINAE;

EID: 84867096917     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08756.x     Document Type: Article

References (57)

1. Harvey RG, (1991) Polycyclic Aromatic Hydrocarbons: Chemistry and Carcinogenicity. Cambridge University Press, Cambridge.
2. Xue W, &, Warshawsky D, (2005) Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol Appl Pharmacol 206, 73-93.
3. Gillet LC, &, Scharer OD, (2006) Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev 106, 253-276.
4. Jeltsch A, (2002) Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. ChemBioChem 3, 274-293.
5. Weisenberger DJ, &, Romano LJ, (1999) Cytosine methylation in a CpG sequence leads to enhanced reactivity with benzo[a]pyrene diol epoxide that correlates with a conformational change. J Biol Chem 274, 23948-23955.
6. Baskunov VB, Subach FV, Kolbanovskiy A, Kolbanovskiy M, Eremin SA, Johnson F, Bonala R, Geacintov NE, &, Gromova ES, (2005) Effects of benzo[a]pyrene-deoxyguanosine lesions on DNA methylation catalyzed by EcoRII DNA methyltransferase and on DNA cleavage effected by EcoRII restriction endonuclease. Biochemistry 44, 1054-1066.
7. Subach OM, Baskunov VB, Darii MV, Maltseva DV, Alexandrov DA, Kirsanova OV, Kolbanovskiy A, Kolbanovskiy M, Johnson F, Bonala R, et al,. (2006) Impact of benzo[a]pyrene-2'-deoxyguanosine lesions on methylation of DNA by SssI and HhaI DNA methyltransferases. Biochemistry 45, 6142-6159.
8. Subach OM, Maltseva DV, Shastry A, Kolbanovskiy A, Klimasauskas S, Geacintov NE, &, Gromova ES, (2007) The stereochemistry of benzo[a]pyrene-2'-deoxyguanosine adducts affects DNA methylation by SssI and HhaI DNA methyltransferases. FEBS J 274, 2121-2134.
9. Geacintov NE, Cosman M, Hingerty BE, Amin S, Broyde S, &, Patel DJ, (1997) NMR solution structures of stereoisometric covalent polycyclic aromatic carcinogen-DNA adduct: principles, patterns, and diversity. Chem Res Toxicol 10, 111-146.
10. Okano M, Bell DW, Haber DA, &, Li E, (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257.
11. Gowher H, Liebert K, Hermann A, Xu G, &, Jeltsch A, (2005) Mechanism of stimulation of catalytic activity of Dnmt3A and Dnmt3B DNA-(cytosine-C5)- methyltransferases by Dnmt3L. J Biol Chem 280, 13341-13348.
12. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, &, Cheng X, (2007) Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449, 248-251.
13. Jurkowska RZ, Anspach N, Urbanke C, Jia D, Reinhardt R, Nellen W, Cheng X, &, Jeltsch A, (2008) Formation of nucleoprotein filaments by mammalian DNA methyltransferase Dnmt3a in complex with regulator Dnmt3L. Nucleic Acids Res 36, 6656-6663.
14. Lukashevich OV, Baskunov VB, Darii MV, Kolbanovskiy A, Baykov AA, &, Gromova ES, (2011) Dnmt3a-CD is less susceptible to bulky benzo[a]pyrene diol epoxide-derived DNA lesions than prokaryotic DNA methyltransferases. Biochemistry 50, 875-881.
15. Cosman M, de los Santos C, Fiala R, Hingerty BE, Singh SB, Ibanez V, Margulis LA, Live D, Geacintov NE, Broyde S, et al,. (1992) Solution conformation of the major adduct between the carcinogen (+)-anti-benzo[a]pyrene diol epoxide and DNA. Proc Natl Acad Sci USA 89, 1914-1918.
16. de los Santos C, Cosman M, Hingerty BE, Ibanez V, Margulis LA, Geacintov NE, Broyde S, &, Patel DJ, (1992) Influence of benzo[a]pyrene diol epoxide chirality on solution conformations of DNA covalent adducts: the (-)-trans-anti-[BP]G.C adduct structure and comparison with the (+)-trans-anti-[BP]G.C enantiomer. Biochemistry 31, 5245-5252.
17. Cosman M, de los Santos C, Fiala R, Hingerty BE, Ibanez V, Luna E, Harvey R, Geacintov NE, Broyde S, &, Patel DJ, (1993) Solution conformation of the (+)-cis-anti-[BP]dG adduct in a DNA duplex: intercalation of the covalently attached benzo[a]pyrenyl ring into the helix and displacement of the modified deoxyguanosine. Biochemistry 32, 4145-4155.
18. Cosman M, Hingerty BE, Luneva N, Amin S, Geacintov NE, Broyde S, &, Patel DJ, (1996) Solution conformation of the (-)-cis-anti-benzo[a]pyrenyl-dG adduct opposite dC in a DNA duplex: intercalation of the covalently attached BP ring into the helix with base displacement of the modified deoxyguanosine into the major groove. Biochemistry 35, 9850-9863.
19. Schurter EJ, Yeh HJ, Sayer JM, Lakshman MK, Yagi H, Jerina DM, &, Gorenstein DG, (1995) NMR solution structure of a nonanucleotide duplex with a dG mismatch opposite a 10R adduct derived from trans addition of a deoxyadenosine N6-amino group to (-)-(7S,8R,9R,10S)-7,8-dihydroxy-9,10-epoxy-7, 8,9,10-tetrahydrobenzo[a]pyrene. Biochemistry 34, 1364-1375.
20. Yeh HJ, Sayer JM, Liu X, Altieri AS, Byrd RA, Lakshman MK, Yagi H, Schurter EJ, Gorenstein DG, &, Jerina DM, (1995) NMR solution structure of a nonanucleotide duplex with a dG mismatch opposite a 10S adduct derived from trans addition of a deoxyadenosine N6-amino group to (+)-(7R,8S,9S,10R)-7,8- dihydroxy-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene: an unusual syn glycosidic torsion angle at the modified dA. Biochemistry 34, 13570-13581.
21. Wittung P, Funk M, Jernstrom B, Norden B, &, Takahashi M, (1995) Fluorescence-detected interactions of oligonucleotides in RecA complexes. FEBS Lett 368, 64-68.
22. Zou Y, Bassett H, Walker R, Bishop A, Amin S, Geacintov NE, &, Van Houten B, (1998) Hydrophobic forces dominate the thermodynamic characteristics of UvrA-DNA damage interactions. J Mol Biol 281, 107-119.
23. Liu Y, Yang Z, Utzat CD, Geacintov NE, Basu AK, &, Zou Y, (2005) Interactions of human replication protein A with single-stranded DNA adducts. Biochem J 385, 519-526.
24. Christian TD, &, Romano LJ, (2009) Monitoring the conformation of benzo[a]pyrene adducts in the polymerase active site using fluorescence resonance energy transfer. Biochemistry 48, 5382-5388.
25. Cai Y, Kropachev K, Kolbanovskiy M, Kolbanovskiy A, Broyde S, Patel DJ, &, Geacintov NE, (2010) Recognition and removal of bulky DNA lesions by the Nucleotide Excision Repair system. In The Chemical Biology of DNA Damage (Geacintov NE & Broyde S, eds) Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany.
26. Fountain MA, &, Krugh TR, (1995) Structural characterization of a (+)-trans-anti-benzo[a]pyrene-DNA adduct using NMR, restrained energy minimization, and molecular dynamics. Biochemistry 34, 3152-3161.
27. Yakovleva L, Tian L, Sayer JM, Kalena GP, Kroth H, Jerina DM, &, Shuman S, (2003) Site-specific DNA transesterification by vaccinia topoisomerase: effects of benzo[alpha]pyrene-dA, 8-oxoguanine, 8-oxoadenine and 2-aminopurine modifications. J Biol Chem 278, 42170-42177.
28. Pradhan P, Tirumala S, Liu X, Sayer JM, Jerina DM, &, Yeh HJ, (2001) Solution structure of a trans-opened (10S)-dA adduct of (+)-(7S,8R,9S,10R)-7,8- dihydroxy-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a]pyrene in a fully complementary DNA duplex: evidence for a major syn conformation. Biochemistry 40, 5870-5881.
29. Handa V, &, Jeltsch A, (2005) Profound flanking sequence preference of Dnmt3a and Dnmt3b mammalian DNA methyltransferases shape the human epigenome. J Mol Biol 348, 1103-1112.
30. Wyszynski MW, Gabbara S, Kubareva EA, Romanova EA, Oretskaya TS, Gromova ES, Shabarova ZA, &, Bhagwat AS, (1993) The cysteine conserved among DNA cytosine methylases is required for methyl transfer, but not for specific DNA binding. Nucleic Acids Res 21, 295-301.
31. Klimasauskas S, &, Roberts RJ, (1995) M.HhaI binds tightly to substrates containing mismatches at the target base. Nucleic Acids Res 23, 1388-1395.
32. Nur I, Szyf M, Razin A, Glaser G, Rottem S, &, Razin S, (1985) Procaryotic and eucaryotic traits of DNA methylation in spiroplasmas (mycoplasmas). J Bacteriol 164, 19-24.
33. Wilson JN, &, Kool ET, (2006) Fluorescent DNA base replacements: reporters and sensors for biological systems. Org Biomol Chem 4, 4265-4274.
34. Geacintov NE, Mao B, France LL, Zhao R, Chen J, Liu TM, Ya N, Margulis LA, &, Sutherland JC, (1992) Photoinduced electron transfer and fluorescence mechanisms in covalently linked polynuclear aromatic-nucleotide complexes. Proc SPIE Time-Resolved Laser Spectrosc Biochem III 1640, 774-783.
35. Huang W, Amin S, &, Geacintov NE, (2002) Fluorescence characteristics of site-specific and stereochemically distinct benzo[a]pyrene diol epoxide-DNA adducts as probes of adduct conformation. Chem Res Toxicol 15, 118-126.
36. Wittung P, Norden B, &, Takahashi M, (1994) Spectroscopic observation of renaturation between polynucleotides with RecA in the presence of ATP hydrolysis. Eur J Biochem 224, 39-45.
37. Margulis L, Pluzhnikov PF, Mao B, Kuzmin VA, Chang YJ, Scott TW, &, Geacintov NE, (1991) Photoinduced electron transfer in a covalent benzo[a]pyrene diol epoxide-2'-deoxyguanosine complex. Chem Phys Lett 187, 597-603.
38. Geacintov NE, Zhao R, Kuzmin VA, Kim SK, &, Pecora LJ, (1993) Mechanisms of quenching of the fluorescence of a benzo[a]pyrene tetraol metabolite model compound by 2'-deoxynucleosides. Photochem Photobiol 58, 185-194.
39. Shafirovich VY, Levin PP, Kuzmin VA, Thorgeiersson TE, Kliger DS, &, Geacintov NE, (1994) Photoinduced electron transfer and enhanced triplet yields in benzo[a]pyrene derivative-nucleic acid complexes and covalent adducts. J Am Chem Soc 116, 63-72.
40. Shafirovich VY, Courtney SH, Ya N, &, Geacintov NE, (1995) Proton-coupled photoinduced electron transfer, deuterium isotope effects, and fluorescence quenching in noncovalent benzo[a]pyrenetetraol-nucleoside complexes in aqueous solutions. J Am Chem Soc 117, 4920-4929.
41. Geacintov NE, Cosman M, Mao B, Alfano A, Ibanez V, &, Harvey RG, (1991) Spectroscopic characteristics and site I/site II classification of cis and trans benzo[a]pyrene diolepoxide enantiomer-guanosine adducts in oligonucleotides and polynucleotides. Carcinogenesis 12, 2099-2108.
42. Geacintov NE, Zinger D, Ibanez V, Santella R, Grunberger D, &, Harvey RG, (1987) Properties of covalent benzo[a]pyrene diol epoxide-DNA adducts investigated by fluorescence techniques. Carcinogenesis 8, 925-935.
43. LeBreton PR, Huang CR, Fernando H, Zajc B, Lakshman MK, Sayer JM, &, Jerina DM, (1995) Multiple fluorescence lifetimes for oligonucleotides containing single, site-specific modifications at guanine and adenine corresponding to trans addition of exocyclic amino groups to (+)-(7R,8S,9S,10R)- and (+)-(7S,8R,9R,10S)-7,8-dihydroxy-9,10-epoxy-7,8,9,10-tetrahydrobenzo[a] pyrene. Chem Res Toxicol 8, 338-348.
44. Geacintov NE, Solntsev K, Johnson LW, Chen J, Kolbanovskiy AD, Liu T, &, Shafirovich VY, (1998) Photoinduced electron transfer and strand cleavage in pyrenyl-DNA complexes and adducts. J Phys Org Chem 11, 561-565.
45. Huang X, Colgate KC, Kolbanovskiy A, Amin S, &, Geacintov NE, (2002) Conformational changes of a benzo[a]pyrene diol epoxide-N(2)-dG adduct induced by a 5'-flanking 5-methyl-substituted cytosine in a (Me)CG double-stranded oligonucleotide sequence context. Chem Res Toxicol 15, 438-444.
46. Klimasauskas S, Kumar S, Roberts RJ, &, Cheng X, (1994) HhaI methyltransferase flips its target base out of the DNA helix. Cell 76, 357-369.
47. Gerasimaite R, Merkiene E, &, Klimasauskas S, (2011) Direct observation of cytosine flipping and covalent catalysis in a DNA methyltransferase. Nucleic Acids Res 39, 3771-3780.
48. Svedruzic ZM, &, Reich NO, (2004) The mechanism of target base attack in DNA cytosine carbon 5 methylation. Biochemistry 43, 11460-11473.
49. Kim SK, Brenner HC, Soh BJ, &, Geacintov NE, (1989) Fluorescence spectroscopy of benzo[a]pyrene diol epoxide-DNA adducts. Conformation-specific emission spectra. Photochem Photobiol 50, 327-337.
50. Maltseva DV, Baykov AA, Jeltsch A, &, Gromova ES, (2009) Impact of 7,8-dihydro-8-oxoguanine on methylation of the CpG site by Dnmt3a. Biochemistry 48, 1361-1368.
51. Yan S, Wu M, Patel DJ, Geacintov NE, &, Broyde S, (2003) Simulating structural and thermodynamic properties of carcinogen-damaged DNA. Biophys J 84, 2137-2148.
52. Cheng X, &, Blumenthal RM, (2008) Mammalian DNA methyltransferases: a structural perspective. Structure 16, 341-350.
53. Ruchirawat M, Becker FF, &, Lapeyre JN, (1984) Mechanism of rat liver DNA methyltransferase interaction with anti-benzo[a]pyrenediol epoxide modified DNA templates. Biochemistry 23, 5426-5432.
54. Sadikovic B, &, Rodenhiser DI, (2006) Benzopyrene exposure disrupts DNA methylation and growth dynamics in breast cancer cells. Toxicol Appl Pharmacol 216, 458-468.
55. Damiani LA, Yingling CM, Leng S, Romo PE, Nakamura J, &, Belinsky SA, (2008) Carcinogen-induced gene promoter hypermethylation is mediated by DNMT1 and causal for transformation of immortalized bronchial epithelial cells. Cancer Res 68, 9005-9014.
56. Cosman M, Ibanez V, Geacintov NE, &, Harvey RG, (1990) Preparation and isolation of adducts in high yield derived from the binding of two benzo[a]pyrene-7,8-dihydroxy-9,10-oxide stereoisomers to the oligonucleotide d(ATATGTATA). Carcinogenesis 11, 1667-1672.
57. Darii MV, Cherepanova NA, Subach OM, Kirsanova OV, Rasko T, Slaska-Kiss K, Kiss A, Deville-Bonne D, Reboud-Ravaux M, &, Gromova ES, (2009) Mutational analysis of the CG recognizing DNA methyltransferase SssI: insight into enzyme-DNA interactions. Biochim Biophys Acta 1794, 1654-1662.