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New Fluorescent Analogs of Nucleotides Based on 3-Hydroxychromone for Recording Conformational Changes of DNA

Abstract

It has recently been found that derivatives of nucleotides containing а 3-hydroxychromone fluorescent dye can be used as sensitive markers of conformational changes of DNA. In this work, a comparative analysis of two fluorescent nucleotide derivatives—3-hydroxychromone a (3HC) and 3HC-modified uridine (FCU)—was performed during the study of protein–nucleic acid interactions for several human DNA repair enzymes, removing damaged nucleotides: DNA glycosylases AAG, OGG1, UNG2, and MBD4 and AP endonuclease APE1. The changes of fluorescence intensity significantly depended on the nature of neighbor nucleotides and may be opposite in direction for different cases. The FCU residue located in the complementary strand opposite to damaged nucleotide or in the same strand moved by few nucleotides, is very sensitive to processes induced by DNA glycosylases in the course of formation of enzyme–substrate complexes, which include local melting and bending of the DNA chain, as well as eversion of the damaged nucleotide from DNA double helix and insertion of amino acids of the active site into the void.

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REFERENCES

  1. 1

    Carpenter, M.L., Oliver, A.W., and Kneale, G.G., Methods Mol. Biol., 2001, vol. 148, pp. 491–502. https://doi.org/10.1385/1-59259-208-2:491

  2. 2

    Lakowicz, J.R., Principles of Fluorescence Spectroscopy, 3rd ed., New York: Springer, 2006.

  3. 3

    Sinkeldam, R.W., Greco, N.J., and Tor, Y., Chem. Rev., 2010, vol. 110, pp. 2579–2619. https://doi.org/10.1021/cr900301e

  4. 4

    Wilhelmsson, L.M., Q. Rev. Biophysics, 2010, vol. 43, pp. 159–183. https://doi.org/10.1017/S0033583510000090

  5. 5

    Dunlap, C.A. and Tsai, M.D., Biochemistry, 2002, vol. 41, pp. 11 226–11 235. https://doi.org/10.1021/bi025837g

  6. 6

    Wong, I., Lundquist, A.J., Bernards, A.S., and Mosbaugh, D.W., J. Biol. Chem., 2002, vol. 277, pp. 19 424–19 432. https://doi.org/10.1074/jbc.M201198200

  7. 7

    Kuznetsov, N.A., Bergonzo, C., Campbell, A.J., Li, H., Mechetin, G.V., Santos, C., Grollman, A.P., Fedorova, O.S., Zharkov, D.O., and Simmerling, C., Nucleic Acids Res., 2015, vol. 43, pp. 272–281. https://doi.org/10.1093/nar/gku1300

  8. 8

    Kuznetsova, A.A., Fedorova, O.S., and Kuznetsov, N.A., Molecules, 2018, vol. 23, p. 2101. https://doi.org/10.3390/molecules23092101

  9. 9

    Alekseeva, I.V., Davletgildeeva, A.T., Arkova, O.V., Kuznetsov, N.A., and Fedorova, O.S., Biochimie, 2019, vol. 163, pp. 73–83. https://doi.org/10.1016/j.biochi.2019.05.015

  10. 10

    Kuznetsova, A.A., Iakovlev, D.A., Misovets, I.V., Ishchenko, A.A., Saparbaev, M.K., Kuznetsov, N.A., and Fedorova, O.S., Mol. Biosyst., 2017, vol. 13, pp. 2638–2649. https://doi.org/10.1039/c7mb00457e

  11. 11

    Jean, J.M. and Hall, K.B., Proc. Natl. Acad. Sci. U. S. A., 2001, vol. 98, pp. 37–41. https://doi.org/ 10.1073ypnas.011442198

  12. 12

    Rachofsky, E.L., Osman, R., and Ross, J.B.A., Biochemistry, 2001, vol. 40, pp. 946–956. https://doi.org/10.1021/bi001664o

  13. 13

    Zang, H., Fang, Q., Pegg, A.E., and Guengerich, F.P., J. Biol. Chem., 2005, vol. 280, pp. 30 873–30 881. https://doi.org/10.1074/jbc.M505283200

  14. 14

    Kuznetsov, N.A., Vorobjev, Y.N., Krasnoperov, L.N., and Fedorova, O.S., Nucleic Acids Res., 2012, vol. 40, pp. 7384–7392. https://doi.org/10.1093/nar/gks423

  15. 15

    Rist, M.J. and Marino, J.P., Curr. Org. Chem., 2002, vol. 6, pp. 775–793. https://doi.org/10.2174/1385272023373914

  16. 16

    Berry, D.A., Jung, K.Y., Wise, D.S., Sercel, A.D., Pearson, W.H., Mackie, H., Randolph, J.B., and Somers, R.L., Tetrahedron Lett., 2004, vol. 45, pp. 2457–2461. https://doi.org/10.1016/j.tetlet.2004.01.108

  17. 17

    Sandin, P., Borjesson, K., Li, H., Martensson, J., Brown, T., Wilhelmsson, L.M., and Albinsson, B., Nucleic Acids Res., 2008, vol. 36, pp. 157–167. https://doi.org/10.1093/nar/gkm1006

  18. 18

    Borjesson, K., Sandin, P., and Wilhelmsson, L.M., Biophys. Chem., 2009, vol. 139, pp. 24–28. https://doi.org/10.1016/j.bpc.2008.09.021

  19. 19

    Kuznetsov, N.A., Kladova, O.A., Kuznetsova, A.A., Ishchenko, A.A., Saparbaev, M.K., Zharkov, D.O., and Fedorova, O.S., J. Biol. Chem., 2015, vol. 290, pp. 14 338–14 349. https://doi.org/10.1074/jbc.M114.621128

  20. 20

    Kladova, O.A., Kuznetsov, N.A., and Fedorova, O.S., Acta Naturae, 2019, vol. 11, pp. 29–37.

  21. 21

    Kladova, O.A., Krasnoperov, L.N., Kuznetsov, N.A., and Fedorova, O.S., Genes (Basel), 2018, vol. 9, p. 190. https://doi.org/10.3390/genes9040190

  22. 22

    Dziuba, D., Postupalenko, V.Y., Spadafora, M., Klymchenko, A.S., Guerineau, V., Mely, Y., Benhida, R., and Burger, A., J. Am. Chem. Soc., 2012, vol. 134, pp. 10 209–10 213. https://doi.org/10.1021/ja3030388

  23. 23

    Gavvala, K., Barthes, N.P.F., Bonhomme, D., Dabert-Gay, A.S., Debayle, D., Michel, B.Y., Burger, A., and Mely, Y., RSC Adv., 2016, vol. 81, pp. 10 733–10 741. https://doi.org/10.1021/acs.joc.6b01807

  24. 24

    Kuznetsova, A.A., Kuznetsov, N.A., Vorobjev, Y.N., Barthes, N.P.F., Michel, B.Y., Burger, A., and Fedorova, O.S., PLoS One, 2014, vol. 9. e100007. https://doi.org/10.1371/journal.pone.0100007

  25. 25

    Brooks, S.C., Adhikary, S., Rubinson, E.H., and Eichman, B.F., Biochim. Biophys. Acta, 2013, vol. 1834, pp. 247–271. https://doi.org/10.1016/j.bbapap.2012.10.005

  26. 26

    Lau, A.Y., Scharer, O.D., Samson, L., Verdine, G.L., and Ellenberger, T., Cell, 1998, vol. 95, pp. 249–258.

  27. 27

    Lau, A.Y., Wyatt, M.D., Glassner, B.J., Samson, L.D., and Ellenberger, T., Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, pp. 13 573–13 578. https://doi.org/10.1073/pnas.97.25.13573

  28. 28

    Setser, J.W., Lingaraju, G.M., Davis, C.A., Samson, L.D., and Drennan, C.L., Biochemistry, 2012, vol. 51, pp. 382–390. https://doi.org/10.1021/bi201484k

  29. 29

    Parikh, S.S., Mol., C.D., Slupphaug, G., Bharati, S., Krokan, H.E., and Tainer, J.A., EMBO J., 1998, vol. 17, pp. 5214–5226. https://doi.org/10.1093/emboj/17.17.5214

  30. 30

    Manvilla, B.A., Maiti, A., Begley, M.C., Toth, E.A., and Drohat, A.C., J. Mol. Biol., 2012, vol. 420, pp. 164–175. https://doi.org/10.1016/j.jmb.2012.04.028

  31. 31

    Mol., C.D., Izumi, T., Mitra, S., Talner, J.A., and Tainer, J.A., Nature, 2000, vol. 403, pp. 451–456. https://doi.org/10.1038/35000249

  32. 32

    Bruner, S.D., Norman, D.P., and Verdine, G.L., Nature, 2000, vol. 403, pp. 859–866. https://doi.org/10.1038/35002510

  33. 33

    Bjoras, M., Seeberg, E., Luna, L., Pearl, L.H., and Barrett, T.E., J. Mol. Biol., 2002, vol. 317, pp. 171–177. https://doi.org/10.1006/jmbi.2001.5400

  34. 34

    Norman, D.P., Chung, S.J., and Verdine, G.L., Biochemistry, 2003, vol. 42, pp. 1564–1572. https://doi.org/10.1021/bi026823d

  35. 35

    Banerjee, A., Yang, W., Karplus, M., and Verdine, G.L., Nature, 2005, vol. 434, pp. 612–618. https://doi.org/10.1038/nature03458

  36. 36

    Miroshnikova, A.D., Kuznetsova, A.A., Kuznetsov, N.A., and Fedorova, O.S., Acta Naturae, 2016, vol. 8, pp. 103–110.

  37. 37

    Miroshnikova, A.D., Kuznetsova, A.A., Vorobjev, Y.N., Kuznetsov, N.A., and Fedorova, O.S., Mol. BioSyst., 2016, vol. 12, pp. 1527–1539. https://doi.org/10.1039/c6mb00128a

  38. 38

    Kanazhevskaya, L.Y., Koval, V.V., Vorobjev, Y.N., and Fedorova, O.S., Biochemistry, 2012, vol. 51, pp. 1306–1321. https://doi.org/10.1021/bi201444m

  39. 39

    Kuznetsov, N.A., Koval, V.V., Zharkov, D.O., Nevinsky, G.A., Douglas, K.T., and Fedorova, O.S., Nucleic Acids Res., 2005, vol. 33, pp. 3919–3931. https://doi.org/10.1093/nar/gki694

  40. 40

    Kuznetsova, A.A., Kuznetsov, N.A., Ishchenko, A.A., Saparbaev, M.K., and Fedorova, O.S., Biochim. Biophys. Acta, 2014, vol. 1840, pp. 387–395. https://doi.org/10.1016/j.bbagen.2013.09.035

  41. 41

    Slupphaug, G., Eftedal, I., Kavli, B., Bharati, S., Helle, N.M., Haug, T., Levine, D.W., and Krokan, H.E., Biochemistry, 1995, vol. 34, pp. 128–138. https://doi.org/10.1021/Bi00001a016

  42. 42

    Saparbaev, M., Langouet, S., Privezentzev, C.V., Guengerich, F.P., Cai, H., Elder, R.H., and Laval, J., J. Biol. Chem., 2002, vol. 277, pp. 26 987–26 993. https://doi.org/10.1074/jbc.M111100200

  43. 43

    Kuznetsov, N.A., Kiryutin, A.S., Kuznetsova, A.A., Panov, M.S., Barsukova, M.O., Yurkovskaya, A.V., and Fedorova, O.S., J. Biomol. Struct. Dyn., 2017, vol. 35, pp. 950–967. https://doi.org/10.1080/07391102.2016.1171800

  44. 44

    Morera, S., Grin, I., Vigouroux, A., Couve, S., Henriot, V., Saparbaev, M., and Ishchenko, A.A., Nucleic Acids Res., 2012, vol. 40, pp. 9917–9926. https://doi.org/10.1093/nar/gks714

  45. 45

    Yakovlev, D.A., Kuznetsova, A.A., Fedorova, O.S., and Kuznetsov, N.A., Acta Naturae, 2017, vol. 9, pp. 88–98.

  46. 46

    Daviet, S., Couve-Privat, S., Gros, L., Shinozuka, K., Ide, H., Saparbaev, M., and Ishchenko, A.A., DNA Repair, 2007, vol. 6, pp. 8–18. https://doi.org/10.1016/j.dnarep.2006.08.001

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Author information

Correspondence to O. S. Fedorova or N. A. Kuznetsov.

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The work has no studies involving humans or animals as subjects of the study.

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Authors declare they have no conflicts of interest.

Additional information

Translated by N. Onishchenko

Abbreviations: aPu, 2-aminopurine; CPy, pyrollocytosine; tCO, 1,3-diaza-2-oxophenoxazine; 3-HC, 3-hydroxychromone; FCU, 2-furyl-3-HC-uracyl moiety; F site, 2-hydroxymethyl-3-hydroxytetrahydrofurane; AP site, apurine–apyrimidine site; AAG, alkyladenine-DNA glycosylase; APE1, human AP endonuclease; Hx, hypoxanthine; MBD4, human methylcytosine-binding domain 4; OGG1, human 8-oxoguanine-DNA glycosylase; UNG2, uracyl-DNA glycosylase.

The authors contributed equally to the work.

Corresponding authors: e-mails: fedorova@niboch.nsc.ru; nikita.kuznetsov@niboch.nsc.ru.

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Kladova, O.A., Kuznetsova, A.A., Barthes, N.P. et al. New Fluorescent Analogs of Nucleotides Based on 3-Hydroxychromone for Recording Conformational Changes of DNA. Russ J Bioorg Chem 45, 599–607 (2019). https://doi.org/10.1134/S1068162019060220

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Keywords:

  • DNA
  • conformational changes
  • damage repair
  • DNA glycosylase
  • AP endonuclease
  • fluorescence
  • enzyme kinetics