Abstract
DNA-substrates containing fluorescent DNA base analogs are widely used to study protein–nucleic acid interactions. In the case of DNA-recognizing enzymes, this approach allows one to register conformational changes in DNA during the formation of enzyme–substrate complexes. An important part of such research is the design of model DNA substrates, which includes both the photophysical properties of the fluorescent groups and their location relative to a specific recognition site, namely, in the same chain on the 5′-, 3′-side or in the complementary chain opposite the specific site. In this work, we report a comparative study of the sensitivity of various fluorescent DNA base analogs, such as 2-aminopurine (aPu), pyrrolocytosine (CPy), 1,3-diaza-2-oxophenoxazine (tCO) and 3-hydroxychromone (3HC), to conformational transformations of DNA in the process of interaction with formamidopyrimidine-DNA glycosylase (Fpg) from Escherichia coli.
Similar content being viewed by others
REFERENCES
Lakowicz, J.R., Principles of Fluorescence Spectroscopy, 3rd ed., New York: Springer, 2006.
Carpenter, M.L., Oliver, A.W., and Kneale, G.G., Methods Mol. Biol., 2001, vol. 148, pp. 491–502.
Sinkeldam, R.W., Greco, N.J., and Tor, Y., Chem. Rev., 2010, vol. 110, pp. 2579–2619.
Wilhelmsson, L.M., Q. Rev. Biophys., 2010, vol. 43, pp. 159–183.
Kim, K.T., Kim, H.W., Moon, D., Rhee, Y.M., and Kim, B.H., Org. Biomol. Chem., 2013, vol. 11, pp. 5605–5614.
Suzuki, A., Takahashi, N., Okada, Y., Saito, I., Nemoto, N., and Saito, Y., Bioorg. Med. Chem. Lett., 2013, vol. 23, pp. 886–892.
Pawar, M.G., Nuthanakanti, A., and Srivatsan, S.G., Bioconjug. Chem., 2013, vol. 24, pp. 1367–77.
Pawar, M.G. and Srivatsan, S.G., J. Phys. Chem. B, 2013, vol. 117, pp. 14 273–14 282.
Segal, M., Yavin, E., Kafri, P., Shav-Tal, Y., and Fischer, B., J. Med. Chem., 2013, vol. 56, pp. 4860–4869.
Ward, D.C., Reich, E., and Stryer, L., J. Biol. Chem., 1969, vol. 244, pp. 1228–1237.
Kuznetsov, N.A., Koval, V.V., Nevinsky, G.A., Douglas, K.T., Zharkov, D.O., and Fedorova, O.S., J. Biol. Chem., 2007, vol. 282, pp. 1029–1038.
Wong, I., Lundquist, A.J., Bernards, A.S., and Mosbaugh, D.W., J. Biol. Chem., 2002, vol. 277, pp. 19 424–19 432.
Dunlap, C.A. and Tsai, M.D., Biochemistry, 2002, vol. 41, pp. 11 226–11 235.
Purohit, V., Grindley, N.D.F., and Joyce, C.M., Biochemistry, 2003, vol. 42, pp. 10 200–10 211.
Jia, Y., Kumar, A., and Patel, S.S., J. Biol. Chem., 1996, vol. 271, pp. 30 451–30 458.
Mandal, S.S., Fidalgo da Silva, E., and Reha-Krantz, L.J., Biochemistry, 2002, vol. 41, pp. 4399–4406.
Kuznetsov, N.A., Koval, V.V., Zharkov, D.O., Vorobjev, Y.N., Nevinsky, G.A., Douglas, K.T., and Fedorova, O.S., Biochemistry, 2007, vol. 46, pp. 424–435.
Watanabe, S.M. and Goodman, M.F., Proc. Natl. Acad. Sci. U. S. A., 1982, vol. 79, pp. 6429–6433.
Sowers, L.C., Fazakerley, G.V., Eritja, R., Karlan, B.E., and Goodman, M.F., Proc. Natl. Acad. Sci. U. S. A., 1986, vol. 83, pp. 5434–5438.
Sowers, L.C., Boulard, Y., and Fazakerley, G.V., Biochemistry, 2000, vol. 39, pp. 7613–7620.
Zang, H., Fang, Q., Pegg, A.E., and Guengerich, F.P., J. Biol. Chem., 2005, vol. 280, pp. 30 873–30 881.
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.
Kuznetsov, N.A., Vorobjev, Y.N., Krasnoperov, L.N., and Fedorova, O.S., Nucleic Acids Res., 2012, vol. 40, pp. 7384–7392.
Yang, K. and Stanley, R.J., Photochem. Photobiol., 2008, vol. 84, pp. 741–749.
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.
Borjesson, K., Sandin, P., and Wilhelmsson, L.M., Biophys. Chem., 2009, vol. 139, pp. 24–28.
Stengel, G., Purse, B.W., Wilhelmsson, L.M., Urban, M., and Kuchta, R.D., Biochemistry, 2009, vol. 48, pp. 7547–7555.
Stengel, G., Urban, M., Purse, B.W., and Kuchta, R.D., Anal. Chem., 2009, vol. 81, pp. 9079–9085.
Rodgers, B.J., Elsharif, N.A., Vashisht, N., Mingus, M.M., Mulvahill, M.A., Stengel, G., Kuchta, R.D., and Purse, B.W., Chemistry (Easton), 2014, vol. 20, pp. 2010–2015.
Sandin, P., Stengel, G., Ljungdahl, T., Borjesson, K., Macao, B., and Wilhelmsson, L.M., Nucleic Acids Res., 2009, vol. 37, pp. 3924–3933.
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.
Kladova, O.A., Krasnoperov, L.N., Kuznetsov, N.A., and Fedorova, O.S., Genes (Basel), 2018, vol. 9. E190.
Kladova, O.A., Kuznetsova, A.A., Fedorova, O.S., and Kuznetsov, N.A., Genes (Basel), 2017, vol. 8, pp. 1–13.
Spadafora, M., Postupalenko, V.Y., Shvadchak, V.V., Klymchenko, A.S., Mely, Y., Burger, A., and Benhida, R., Tetrahedron, 2009, vol. 65, pp. 7809–7816.
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.
Demchenko, A.P., FEBS Lett., 2006, vol. 580, pp. 2951–2957.
Shynkar, V.V., Klymchenko, A.S., Kunzelmann, C., Duportail, G., Muller, C.D., Demchenko, A.P., Freyssinet, J.M., and Mely, Y., J. Am. Chem. Soc., 2007, vol. 129, pp. 2187–2193.
Das, R., Klymchenko, A.S., Duportail, G., and Mely, Y., Photochem. Photobiol. Sci., 2009, vol. 8, pp. 1583–1589.
Zharkov, D.O., Shoham, G., and Grollman, A.P., DNA Repair, 2003, vol. 2, pp. 839–862.
Tchou, J., Kasai, H., Shibutani, S., Chung, M.H., Laval, J., Grollman, A.P., and Nishimura, S., Proc. Natl. Acad. Sci. U. S. A., 1991, vol. 88, pp. 4690–4694.
Boiteux, S., O’Connor, T.R., Lederer, F., Gouyette, A., and Laval, J., J. Biol. Chem., 1990, vol. 265, pp. 3916–3922.
Koval, V.V., Kuznetsov, N.A., Zharkov, D.O., Ishchenko, A.A., Douglas, K.T., Nevinsky, G.A., and Fedorova, O.S., Nucleic Acids Res., 2004, vol. 32, pp. 926–935.
Zaika, E.I., Perlow, R.A., Matz, E., Broyde, S., Gilboa, R., Grollman, A.P., and Zharkov, D.O., J. Biol. Chem., 2004, vol. 279, pp. 4849–4861.
Karakaya, A., Jaruga, P., Bohr, V.A., Grollman, A.P., and Dizdaroglu, M., Nucleic Acids Res., 1997, vol. 25, pp. 474–479.
Gilboa, R., Zharkov, D.O., Golan, G., Fernandes, A.S., Gerchman, S.E., Matz, E., Kycia, J.H., Grollman, A.P., and Shoham, G., J. Biol. Chem., 2002, vol. 277, pp. 19 811–19 816.
Tchou, J. and Grollman, A.P., J. Biol. Chem., 1995, vol. 270, pp. 11 671–11 677.
Zharkov, D.O., Rieger, R.A., Iden, C.R., and Grollman, A.P., J. Biol. Chem., 1997, vol. 272, pp. 5335–5341.
Bhagwat, M. and Gerlt, J.A., Biochemistry, 1996, vol. 35, pp. 659–665.
Tchou, J., Bodepudi, V., Shibutani, S., Antoshechkin, I., Miller, J., Grollman, A.P., and Johnson, F., J. Biol. Chem., 1994, vol. 269, pp. 15 318–15 324.
Fedorova, O.S., Nevinsky, G.A., Koval, V.V., Ishchenko, A.A., Vasilenko, N.L., and Douglas, K.T., Biochemistry, 2002, vol. 41, pp. 1520–1528.
Kuznetsov, N.A., Zharkov, D.O., Koval, V.V., Buckle, M., and Fedorova, O.S., Biochemistry, 2009, vol. 48, pp. 11 335–11 343.
Kuznetsov, N.A., Milov, A.D., Isaev, N.P., Vorobjev, Y.N., Koval, V.V., Dzuba, S.A., Fedorova, O.S., and Tsvetkov, Y.D., Mol. Biosyst., 2011, vol. 7, pp. 2670–2680.
Funding
The work was partially supported by the basic budgetary investment of PFNI GAN 2013-2020, project no. ААА-А17-117020210022-4.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
The work has no studies involving humans or animals as subjects of the study.
Conflict of Interest
Authors declare they have no conflicts of interest.
Additional information
Translated by N. Onishchenko
Abbreviation: aPu, 2-aminopurine; CPy, pyrrolocytosine; DHU, 5,6-dihydrouracyl; Fpg, formamifopyrimidine-DNA glycosylase; oxoG, 8-oxoguanine; tCO, 1,3-diaza-2-oxofenoxasine; 3HC, 3-hydroxychromone.
Corresponding authors: e-mails: O.S.F., fedorova@ niboch.nsc.ru; nikita.kuznetsov@niboch.nsc.ru.
Rights and permissions
About this article
Cite this article
Kuznetsova, A.A., Kladova, O.A., Barthes, N.P. et al. Comparative Analysis of Nucleotide Fluorescent Analogs for Registration of DNA Conformational Changes Induced by Interaction with Formamidopyrimidine-DNA Glycosylase Fpg. Russ J Bioorg Chem 45, 591–598 (2019). https://doi.org/10.1134/S1068162019060256
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1068162019060256