An impact of 1H-indol-4-, -5-, -6-, -7-ylamines-substituted compounds on the microbial cell genetic apparatus

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Abstract

The study of new antimicrobial compounds includes determining the mechanism of their effect on the microbial cell. As a rule, an effect for the majority of current synthetic antimicrobials is associated either with suppressed DNA synthesis, or with inhibiting bacterial protein production at translational or transcriptional level. A number of sensitive and easy-todo methods are available for screening and monitoring potential genotoxic activity of a wide range of natural and synthetic compounds. To date, the Ames test has been widely used, which is based on the sensitivity of Salmonella strains to carcinogenic chemicals, although some compounds resulting in Ames negative reactions could actually be carcinogenic to animals. Likewise, the SOS chromotest represents a SOS transcriptional analysis able to assess DNA damage caused by chemical and physical mutagens by measuring the expression of a reporter gene (β-galactosidase) encoding the β-galactosidase enzyme that metabolizes ortho-nitrophenyl galactopyranoside resulting in emerging a yellow-colored compound detected at wavelength 420 nm. Next, the induction of β-galactosidase is normalized by the activity of alkaline phosphatase, an enzyme expressed constitutively by Escherichia coli. SOS chromotest is also widely used for genotoxicological studies providing a quick answer (several hours) and requiring no survival of the test strain. Dose-response curves for various chemicals consist of a linear region, which slope corresponds to the SOS induction. Therefore, the SOS chromotest was selected for the study allowing to identify DNA-mediated effects of the analyzed compounds. The aim of the study was to evaluate the SOSinducing activity for 1H-indol-4-, -5-, -6-, -7-ylamines-substituted antimicrobial compounds. The Escherichia coli PQ 37 with the genotype F-thr leu his-4 pyrD thi galE lacΔU169 srl300::Th10 rpoB rpsL uvrA rfa trp::Mis+ sfiA:: Mud (Ar, lac) cts was used as a test strain. Due to the link of the sfi A::lac Z genes, lacZ β-galactosidase gene expression in the strain PQ 37 is controlled by the sfiA gene promoter, one of the components in the E. coli SOS regulon. Activity of β-galactosidase assessed relative to constitutive microbial alkaline phosphatase reflects SOS-inducing activity triggered by examined compounds in the SOS chromotest that also allows to control their toxic effects on bacterial cells. The data showed that 4,4,4-trifluoroN-(6-methoxy-1,2,3-trimethyl-1H-indol-5-yl)-3-oxobutanamide (1), 4,4,4-trifluoro-N-(6-methyl-2-phenyl-1H-indol-5-yl)- 3-oxobutanamide (2) and N-(1,5-dimethyl-2-phenyl-1H-indol-6-yl)-4,4,4-trifluoro-3-oxobutanamide (3) exerted no SOSinducing activity at the examined concentrations. In contrast, 4-Hydroxy-8-phenyl-4-(trifluoromethyl)-1,3,4,7-tetrahydro- 2H-pyrrolo [2,3-h]-quinoliN-2-one (4), 9-hydroxy-5-methyl-2-phenyl-9-(trifluoromethyl)-1,6,8,9-tetrahydro-7Н-pyrrolo- [2,3-f]-quinoliN-7-one (5), 6-hydroxy-2,3-dimethyl-6-(trifluoromethyl)-1,6,7,9-tetrahydro-8H-pyrrolo[3,2-h]quinoliN-8- one (6) and 1,2,3,9-tetramethyl-6-(trifluoromethyl)-1,9-dihydro-8H-pyrrolo [3,2-h]-quinoliN-8-one (7) displayed a dosedependent SOS-inducing activity at bactericidal concentrations. The data obtained allowed us to identify compounds 4, 5, 6, 7, which mechanism of action relies on affecting microbial cell DNA.

About the authors

A. A. Maseykina

National Research Ogarev Mordovia State University

Author for correspondence.
Email: minibat@mail.ru
ORCID iD: 0000-0001-7604-0680

Alena A. Maseykina,  PhD Student, Department of Immunology, Microbiology and Virology 

430005, Saransk, Bolshevistskaya str., 68

Phone: +7 (951) 343-54-08 

Россия

I. S. Stepanenko

National Research Ogarev Mordovia State University

Email: ymahkina@mail.ru
ORCID iD: 0000-0001-5793-438X

PhD, MD (Medicine), Associate Professor, Department of Immunology, Microbiology and Virology 

Saransk 

S. A. Yamashkin

Mordovia State Pedagogical Institute named after M.E. Evseviev

Email: chem-teh@mail.ru
ORCID iD: 0000-0001-8601-2640

PhD, MD (Chemistry), Professor, Department of Chemistry, Technology and Methods of Training 

Saransk 

E. D. Slastnikov

National Research Ogarev Mordovia State University

Email: slast08@yandex.ru
ORCID iD: 0000-0003-2843-8672

Student 

Saransk 

References

  1. Бояршинов В.Д., Михалев А.И., Ухов С.В., Новикова В.В., Данилов Ю.Л. Синтез и противомикробная активность эфиров и амидов пиридин-2-карбоновой кислоты // Фундаментальные исследования. 2014. Ч. 1, № 11. С. 105–109. [Boyarshinov V.D., Mihalev A.I., Ukhov S.V., Novikova V.V., Danilov Yu.L. Synthesis and antimicrobial activity of pyridine- 2-carboxylic acid esters and amides. Fundamental’nye issledovaniya = Fundamental Researches, 2014, pt. 1, no. 11, pp. 105–109. (In Russ.)]
  2. Кадималиев Д.А., Степаненко И.С., Надежина О.С., Ямашкин С.А. Влияние различно замещенных пирролохинолонов на физиолого-биохимические характеристики лигнолитического гриба Lentinus tigrinus // Микология и фитопато логия. 2014. Т. 48, № 5. С. 309–314. [Kadimaliev D.A., Stepanenko I.S., Nadezhina O.S., Yamashkin S.A. Influence of variously substituted pyrroloquinolones on physiological and biochemical characteristics of the lignolytic fungus Lentinus tigrinus. Mikologiya i fitopatalogiya = Mycology and Phytopathology, 2014, vol. 48, no. 5, pp. 309–314. (In Russ.)]
  3. Миллер Д. Эксперименты в молекулярной генетике / Под ред. С.И. Алиханяна. М.: Мир, 1976. 436 с. [Miller D. Experiments in molecular genetics. Ed. by S.I. Alikhanyan. Moscow: Mir, 1976. 436 p. (In Russ.)]
  4. Патент № 2227140 Российская Федерация, МПК 7C07D 209/16. Способ получения серотонина и его фармакологических солей: № 2002128129; заявлено 2002.10.22: опубликовано 2004.04.27 / Алферов А.В., Северин Е.С., Крюков Л.Н. Патентообладатель: ЗАО «Лорр». [Patent No. 2227140 Russian Federation, Int. Cl. C07D 209/16. Method of production of serotonin and serotonin salts. No. 2002128129; application: 2002.10.22: date of publication 2004.04.27 / Alferov A.V., Severin E.S., Krjukov L.N., Panov A.E., Vorontsov E.A., Kuznetsov S.L., Mikerin I.E. Proprietors: Lorr Ltd.]
  5. Патент № 2404982 Российская Федерация, МПК C07D 471/04 (2006.01), A61K 31/4439 (2006.01), A61P 31/04 (2006.01), A61P 31/06 (2006.01). Применение пирролохинолиновых соединений для уничтожения клинически латентных микроорганизмов: № 2008122912/04; заявлено 2006.08.11: опубликовано 2010.11.27 / Бек П.Х., Браун М.Б., Кларк Д.Е., Коутес Э., Дайк Х.Д., Ху Я., Лондесбро Д.Д., Миллс К., Паллин Т.Д., Рейд Г.П., Стоддарт Г. Патентообладатель: Хелперби терапьютикс лимитед. 122 с. [Patent No. 2404982 Russian Federation, Int. Cl. C07D 471/04 (2006.01), A61K 31/4439 (2006.01), A61P 31/04 (2006.01), A61P 31/06 (2006.01). Application of pyrroloquinoline compounds for killing clinically latent microorganisms. No. 2008122912/04; application: 2006.08.11: date of publication 2010.11.27 / Bek P.H., Braun M.B., Klark D.E., Coates A., Dyke H.J., Hu Y., Londesbrough D.J., Mills K., Pallin Th.D., Reid G.P., Stoddart G. Proprietors: Helperby therapeutics limited. 122 p.]
  6. Рогачева А.В., Празднова Е.В., Мазанко М.С., Чистяков В.А. Ингибирование SOS-репарации у бактерий // Актуальная биотехнология. 2017. № 2. С. 77–79. [Rogacheva A.V., Prazdnova E.V., Mazanko M.S., Chistyakov V.A. Inhibition of SOS repair in bacteria. Aktual’naya biotekhnologiya = Current Biotechnology, 2017, no. 2, pp. 77–79. (In Russ.)]
  7. Руководство по проведению доклинических исследований лекарственных средств. Часть первая / Под ред. А.Н. Миронова. М.: Гриф и К, 2012. 944 с. [Guidelines for Conducting Preclinical Trials of Medicines. Part one / Ed. by A.N. Miro nov. Moscow: Grif and K, 2012. 944 p. (In Russ.)]
  8. Садовникова М.С., Беликов В.М. Пути применения аминокислот в промышленности // Успехи химии. 1978. Т. 47, № 2. С. 357–383. [Sadovnikova M.S., Belikov V.M. Ways of using amino acids in industry. Uspekhi khimii = Advances in Chemistry, 1978, vol. 47, no. 2, pp. 357–383. doi: 10.1070/RC1978v047n02ABEH002212 (In Russ.)]
  9. Сафарова А.Я., Гицу Г.А., Михайлицын Ф.С., Севбо Д.П., Трусов С.Н. Получение салициламида МСТ-28 и изучение противогименолепидозной активности // Медицинская паразитология и паразитарные болезни. 2015. № 2. С. 41–42. [Safarova A.Ya., Gicu G.A., Mihajlicyn F.S., Sevbo D.P., Trusov S.N. Preparation of salicylamide MST-28 and study of antihymenolepidosis activity. Medicinskaya parazitologiya i parazitarnye bolezni = Medical Parasitology and Parasitic Diseases, 2015, no. 2, pp. 41–42. (In Russ.)]
  10. Ушаков В.Ю. SOS-система репараций ДНК у бактерий (обзор) // Вестник Пермского университета. 2010. № 2. С. 19–30. [Ushakov V.Yu. SOS-system repair system in bacteria (review). Vestnik Permskogo universiteta = Perm University Bulletin, 2010, no. 2, pp. 19–30. (In Russ.)]
  11. Alyamkina E.A., Yamashkin S.A., Stepanenko I.S., Yurovskaya M.A. 4-Amino-2-phenylindole-based compounds with potential antibacterial activity. Moscow University Chemistry Bulletin, 2017, vol. 72, no. 1, pp. 24–28. doi: 10.3103/S0027131417010023
  12. Barrett T.C., Mok W.W., Murawski A.M., Brynildsen M.P. Enhanced antibiotic resistance development from fluoroquinolone persisters after a single exposure to antibiotic. Nat. Commun., 2019, vol. 10, no. 1: 1177. doi: 10.1038/s41467-019-09058-4
  13. Cox M.M., Goodman M.F., Kreuzer K.N., Sherratt D.J., Sandler S.J., Marians K.J. The importance of repairing stalled replication forks. Nature, 2000, vol. 404, no. 6773, pp. 37–41. doi: 10.1038/35003501
  14. Hooper D.C. Мechanisms of аction of аntimicrobials: focus on fluoroquinolones. Clin. Infect. Dis., 2001, vol. 32, no. 1, pp. S9– S15. doi: 10.1086/319370
  15. Kohanski M.A., Dwyer D.J., Collins J.J. How antibiotics kill bacteria: from targets to networks. Nat. Rev. Microbiol., 2010, vol. 8, pp. 423–435. doi: 10.1038/nrmicro2333
  16. Koonin E.V., Makarova K.S., Wolf Y.I. Evolutionary genomics of defense systems in archaea and bacteria. Annu. Rev. Microbiol., 2017, vol. 71, pp. 233–261. doi: 10.1146/annurev-micro-090816-093830
  17. Kreuzer K.N. DNA damage responses in prokaryotes: regulating gene expression, modulating growth patterns, and manipulating replication forks. CSH Perspectives in Biology, 2013, vol. 5, no. 11: a012674. doi: 10.1101/cshperspect.a012674
  18. Maeda T., Horinouchi T., Sakata N., Sakai A., Furusawa C. High-throughput identification of the sensitivities of an Escherichia coli Δ recA mutant strain to various chemical compounds. J. Antibiot. (Tokyo), 2019, vol. 72, no. 7, pp. 566–573. doi: 10.1038/s41429-019-0160-5
  19. Mersch-Sundermann V., Kern S., Wintermann F. Gеnоtoxicity of nitrated polycyclic аromatic hydrocarbons and related structures on Escherichia coli PQ37 (SOS-Сhromotest). Environ. Mol. Mutagen., 1991, no. 18, pp. 41–50. doi: 10.1002/em.2850180108
  20. Quillardet P., Hofnung M. The SOS Chromotest, a colorimetric bacterial assay for genotoxins: procedures. Mut. Res., 1985, vol. 147, no. 3, pp. 65–78. doi: 10.1016/0165-1161(85)90020-2
  21. Quillardet P., Нuisman О., Аri R.D., Нofnung М. SOS-сhromotest, a direct аssay of a SOS-function in Еscherichia сoli K12 to measure genotoxity. Proc. Natl. Acad. Sci. USA, 1982, vol. 79, no. 19, pp. 5971–5975. doi: 10.1073/pnas.79.19.5971
  22. Russell А.D., Hugo W.В., Аyliffe’s G.А.J., Fraise А.Р., Lambert Р.А. Рrinciples and рractice of disinfection, рreservation and sterilization. 4th ed. Massachussetts: Blackwell Publishing, 2004. 689 p. doi: 10.1002/9781118425831
  23. Sanyal G., Doig P. Bacterial DNA replication enzymes as targets for antibacterial drug discovery. Expert Opin. Drug Discov., 2012, vol. 7, no. 4, pp. 327–339. doi: 10.1517/17460441.2012.660478
  24. Stepanenko I.S., Yamashkin S.A., Kostina Y.A., Batarsheva A.A., Mironov M.A. A new group of compounds derived from 4-, 5-, 6- and 7-aminoindoles with antimicrobial activity. Res. Results Pharmacol., 2018, vol. 4, no. 3, pp. 17–26. doi: 10.3897/rrpharmacology.4.29905
  25. Stepanenko I.S., Yamashkin S.A., Kostina Y.A., Slastnikov E.D., Batarsheva A.A. A study of the type of antimicrobial action of novel compounds synthesized from substituted benzaminoindoles. Bulletin of RSMU, 2019, no. 2, pp. 57–64. doi: 10.24075/brsmu.2019.030
  26. Sutton M.D., Smith B.T., Godoy V.G., Walker G.C. The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu. Rev. Genet., 2000, vol. 34, pp. 479–497. doi: 10.1146/annurev.genet.34.1.479
  27. Yamashkin S.A., Oreshkina E.A., Romanova I.S., Yurovskaya M.A. The potential use 6-amino-5-methoxy(methyl)-2,3-dimethyl- and 6-amino-5-methoxy(methyl)-1,2,3-trimethylindoles in synthesis pyrrolo[2,3-f]quinolines. Chem. Heterocycl. Comd., 2006, vol. 42, no. 1, pp. 86–91. doi: 10.1002/chin.200641152
  28. Yamashkin S.A., Oreshkina E.A., Yurovskaya M.A. Reaction of 2,3-dimethyl- and 1,2,3-trimethyl-6-amino-indoles with ethyl 4,4,4-trifluoroacetoacetate. Moscow University Chemistry Bulletin, 2007, vol. 62, no. 2, pp. 105–108. doi: 10.3103/S0027131407020113

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