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Russian Journal of Bioorganic Chemistry

, Volume 45, Issue 6, pp 825–832 | Cite as

RNase P-Guiding Peptide Conjugates of Oligo(2'-O-methylribonucleotides) as Prospective Antibacterial Agents

  • N. A. Danilin
  • L. S. Koroleva
  • D. S. NovopashinaEmail author
  • A. G. Venyaminova
Article

Abstract

A novel variant of the synthesis of 3'- and 5'-peptide conjugates of oligo(2'-O-methylribonucleotides) has been developed using thiol-maleimide chemistry. The method is based on the introduction of the maleimide group into an oligonucleotide using a novel bifunctional reagent, pentafluorophenyl ester of 3‑maleimidopropionic acid (MPPf), and the subsequent interaction of the resulting compound with an SH‑bearing peptide, which facilitates cell penetration. A series of RNase P-guiding 3'- and 5'-peptide conjugates of oligo(2'-O-methylribonucleotides) targeted to mRNA of the ftsZ and gyrA genes of Acinetobacter baumannii have been synthesized. The ability of these conjugates to guide the hydrolysis of model RNA targets by RNase P has been demonstrated. It has been shown that the introduction of the peptide molecule at the 5'-end of EGS oligo(2'-O-methylribonucleotides) practically does not reduce the efficiency of RNA hydrolysis by RNAse P.

Keywords:

bacterial RNAse P EGS-oligonucleotides oligo(2'-O-methylribonucleotides) thiol-maleimide chemistry peptide conjugates 

Notes

ACKNOWLEDGMENTS

The authors would like to thank Prof. S. Altman for initiating the research in the field of EGS technologies at our Institute, Dr. D. Wesolowski for kindly provided plasmids to prepare components of RNase P holoenzyme, Dr. S.N. Khodyreva for the preparation of protein C5, and Dr. N.A. Moor for the preparation of M1 RNA.

FUNDING

The work was supported by the grant no. 17-04-01892 from the Russian Foundation for Basic Research. The synthesis and isolation of RNA were partially supported by Russian State funded budget project no. АААА-А17-117020210021-7.

COMPLIANCE WITH ETHICAL STANDARDS

This article does not contain any studies with the use of humans and animals as objects of research.

Conflict of Interests

The authors state that there is no conflict of interests.

REFERENCES

  1. 1.
    Llor, C. and Bjerrum, L., Ther. Adv. Drug Saf., 2014, vol. 5, pp. 229–241.CrossRefGoogle Scholar
  2. 2.
    Guidry, C.A., Mansfield, S.A., Cook, C.H., and Sawyer, R.G., Surg. Clin. North Am., 2014, vol. 94, pp. 1195–1218.CrossRefGoogle Scholar
  3. 3.
    Bai, H., Xue, X., Hou, Z., Zhou, Y., Meng, J., and Luo, X., Curr. Drug Discov. Technol., 2010, vol. 7, pp. 76–85.CrossRefGoogle Scholar
  4. 4.
    Forster, A.C. and Altman, S., Science, 1990, vol. 249, pp. 783–786.CrossRefGoogle Scholar
  5. 5.
    Davies-Sala, C., Soler-Bistué, A., Bonomo, R.A., Zorreguieta, A., and Tolmasky, M.E., Ann. N.Y. Acad. Sci., 2015, vol. 1354, pp. 98–110.CrossRefGoogle Scholar
  6. 6.
    Derksen, M., Mertens, V., and Pruijn, G.J., Biomolecules, 2015, vol. 5, pp. 3029–3050.CrossRefGoogle Scholar
  7. 7.
    Walker, S.C. and Engelke, D.R., Crit. Rev. Biochem. Mol. Biol., 2006, vol. 41, pp. 77–102.CrossRefGoogle Scholar
  8. 8.
    Lundblad, E.W. and Altman, S., Nat. Biotechnol., 2010, vol. 27, pp. 212–221.Google Scholar
  9. 9.
    Wesolowski, D., Tae, H.S., Gandotra, N., Llopis, P., Shen, N., and Altman, S., Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, p. 16582.CrossRefGoogle Scholar
  10. 10.
    Wesolowski, D., Alonso, D., and Altman, S., Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, pp. 8686–8689.CrossRefGoogle Scholar
  11. 11.
    Soler Bistué, A.J.C., Martín, F.A., Vozza, N., Ha, H., Joaquín, J.C., Zorreguieta, A., and Tolmasky, M.E., Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, pp. 13230–13235.CrossRefGoogle Scholar
  12. 12.
    Jackson, A., Jani, S., Sala, C.D., Soler-Bistué, A.J., Zorreguieta, A., and Tolmasky, M.E., Biol. Methods Protoc., 2016, vol. 1. bpw001.CrossRefGoogle Scholar
  13. 13.
    Shen, N., Ko, J., Xiao, G., Wesolowski, D., Shan, G., Geller, B., Izadjoo, M., and Altman, S., Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, pp. 8163–8168.CrossRefGoogle Scholar
  14. 14.
    Augagneur, Y., Wesolowski, D., Tae, H.S., Altman, S., and Ben Mamoun, C., Proc. Natl. Acad. Sci. U. S. A., 2012, vol. 109, pp. 6235–6240.CrossRefGoogle Scholar
  15. 15.
    Sala, C.D., Soler-Bistué, A.J.C., Korprapun, L., Zorreguieta, A., and Tolmasky, M.E., PLoS One, 2012, vol. 7, pp. 1–7.Google Scholar
  16. 16.
    Sawyer, A.J., Wesolowski, D., Gandotra, N., Stojadinovic, A., Izadjoo, M., Altman, S., and Kyriakides, T.R., Int. J. Pharm., 2013, vol. 453, pp. 651–655.CrossRefGoogle Scholar
  17. 17.
    Jani, S., Jackson, A., Davies-Sala, C., Chiem, K., Soler-Bistué, A., Zorreguieta, A., and Tolmasky, M.E., Methods Mol. Biol., 2018, vol. 1737, pp. 89–98.CrossRefGoogle Scholar
  18. 18.
    Wong, D., Nielsen, T.B., Bonomo, R.A., Pantapalangkoor, P., Luna, B., and Spellberg, B., Clin. Microbiol. Rev., 2017, vol. 30, pp. 409–447.PubMedGoogle Scholar
  19. 19.
    Harding, C.M., Hennon, S.W., and Feldman, M.F., Nat. Rev. Microbiol., 2018, vol. 16, pp. 91–102.CrossRefGoogle Scholar
  20. 20.
    Doi, Y., Bonomo, R.A., Hooper, D.C., Kaye, K.S., Johnson, J.R., Clancy, C.J., et al., Clin. Infect. Dis., 2017, vol. 64, suppl. 1, pp. S30–S35.CrossRefGoogle Scholar
  21. 21.
    Tacconelli, E., Carrara, E., Savoldi, A., Harbarth, S., Mendelson, M., Monnet, D.L., et al., Lancet. Infect. Dis., 2018, vol. 18, pp. 318–327.CrossRefGoogle Scholar
  22. 22.
    Tacconelli, E. and Magrini, N., Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics, Geneva: World Health Organization, 2018.Google Scholar
  23. 23.
    Vishnyakov, I.E. and Borchsenius, S.N., Cell Tissue Biol., 2007, vol. 1, pp. 206–214.CrossRefGoogle Scholar
  24. 24.
    Sidorenko, S.V. and Tishkov, V.I., Usp. Biol. Khim., 2004, vol. 44, pp. 263–306.Google Scholar
  25. 25.
    Cummins, L.L., Owens, S.R., Risen, L.M., Lesnik, E.A., Freier, S.M., McGee, D., Guinosso, C.J., and Cook, P.D., Nucleic Acids Res., 1995, vol. 23, pp. 2019–2024.CrossRefGoogle Scholar
  26. 26.
    Boutorine, A.S., Venyaminova, A.G., Repkova, M.N., Sergueyeva, Z.A., and Pyshnyi, D.V., Biochimie, 1994, vol. 76, pp. 23–32.CrossRefGoogle Scholar
  27. 27.
    Novopashina, D.S., Totskaya, O.S., Lomzov, A.A., and Venyaminova, A.G., Nucleosides Nucleotides Nucleic Acids, 2005, vol. 24, pp. 527–531.CrossRefGoogle Scholar
  28. 28.
    Werner, M., Rosa, E., Nordstrom, J.L., Goldberg, A.R., and George, S.T., RNA, 1998, vol. 4, pp. 847–855.CrossRefGoogle Scholar
  29. 29.
    Ma, M.Y., Jacob-Samuel, B., Dignam, J.C., Pace, U., Goldberg, A.R., and George, S.T., Antisense Nucl. Acid Drug Dev., 1998, vol. 8, pp. 415–426.CrossRefGoogle Scholar
  30. 30.
    Ma, M., Benimetskaya, L., Lebedeva, I., Dignam, J., Takle, G., and Stein, C.A., Nat. Biotechnol., 2000, vol. 18, pp. 58–61.CrossRefGoogle Scholar
  31. 31.
    Novopashina, D.S., Nazarov, A.S., Vorobjeva, M.A., Kuprushkin, M.S., Davydova, A.S., Lomzov, A.A., Pyshnyi, D.V., Altman, S., and Venyaminova, A.G., Mol. Biol. (Moscow), 2018, vol. 52, pp. 905–912.CrossRefGoogle Scholar
  32. 32.
    Kwon, E.J., Bergen, J.M., and Pun, S.H., Bioconjugate Chem., 2008, vol. 19, pp. 920–927.CrossRefGoogle Scholar
  33. 33.
    Kwon, E.J., Liong, S., and Pun, S.H., Mol. Pharm., 2010, vol. 7, pp. 1260–1265.CrossRefGoogle Scholar
  34. 34.
    Novopashina, D.S., Vorobyeva, M.A., Nazarov, A.S., Davydova, A.S., Danilin, N.A., Koroleva, L.S., Matveev, A.L., Bardasheva, A.V., Tikunova, N.V., Kupryushkin, M.S., Pyshnyi, D.V., Altman, S., and Venyaminova, A.G., Front. Pharmacol., 2019 (in press).Google Scholar
  35. 35.
    Hoyle, C.E. and Bowman, C.N., Angew. Chem., Int. Ed. Engl., 2010, vol. 49, pp. 1540–1573.CrossRefGoogle Scholar
  36. 36.
    Mather, B.D., Viswanathan, K., Miller, K.M., and Long, T.E., Prog. Polym. Sci., 2006, vol. 31, pp. 487–531.CrossRefGoogle Scholar
  37. 37.
    Guerrier-Takada, C., Lumelsky, N., and Altman, S., Science, 1989, vol. 246, pp. 1578–1584.CrossRefGoogle Scholar
  38. 38.
    Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N., and Altman, S., Cell, 1983, vol. 35, pp. 849–857.CrossRefGoogle Scholar
  39. 39.
    Sinclair, A.J., del Amo, V., and Philp, D., Org. Biomol. Chem., 2009, vol. 7, pp. 3308–3318.CrossRefGoogle Scholar
  40. 40.
    Kida, S., Maeda, M., Hojo, K., Eto, Y., Nakagawa, S., and Kawasakia, K., Chem. Pharm. Bull. (Tokyo), 2007, vol. 55, pp. 685–687.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • N. A. Danilin
    • 1
  • L. S. Koroleva
    • 1
    • 2
  • D. S. Novopashina
    • 1
    • 2
    Email author
  • A. G. Venyaminova
    • 2
  1. 1.Novosibirsk State UniversityNovosibirskRussia
  2. 2.Institute of Chemical Biology and Fundamental Medicine, Siberian Branch, Russian Academy of SciencesNovosibirskRussia

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