Стрессовые системы Escherichia coli и их роль в реакциях на воздействие терагерцового излучения
https://doi.org/10.18699/VJ16.206
Аннотация
Изложены результаты последних лет по изучению реакции стрессовых систем Escherichia coli в ответ на нетермическое воздействие терагерцового (ТГц) излучения. Наиболее простым и удобным объектом для изучения воздействия ТГц излучения на живые объекты является бактерия E. сoli. Это связано с ее высокой изученностью как на молекулярно-генетическом, так и на метаболическом уровне, а также c возможностью создания на основе промоторов ее стресс-активируемых генов и репортерного белка GFP геносенсорных конструкций. Введение этих конструкций в клетки E. coli позволяет исследовать реакцию конкретной стрессовой системы бактерии на ТГц излучение по интенсивности синтеза белка GFP, легко определяемого флуорометрически. В работе представлены данные литературных источников и собственные результаты по нетермическому воздействию ТГц излучения на конкретные стрессовые системы E. coli. Обсуждаются экспериментальные данные, полученные с использованием геносенсоров E. coli/pKatG-GFP, E. coli/pCopA-GFP и E. coli/pEmrR-GFP, которые являются маркерами генных сетей E. coli, активирующихся в условиях окислительного стресса, при нарушении гомеостаза ионов меди и в присутствии антисептиков соответственно. Обзор проведенных исследований показал, что нетермическое воздействие ТГц излучения индуцирует в клетках E. coli генные сети окислительного стресса и поддержания гомеостаза меди, но не влияет на активность стрессовых систем защиты от антибиотиков, протонофоров и супероксид-анионов. Наличие динамических особенностей в развитии стрессорного ответа у геносенсоров E. coli/ pKatG-GFP и E. coli/pCopA-GFP на ТГц излучение в сравнении с естественными индукторами позволяет предположить специфичность ответа систем окислительного стресса и поддержания гомеостаза меди в реакции адаптации клеток E. coli к ТГц излучению.
Об авторах
С. Е. ПельтекРоссия
Новосибирск, Россия
Е. В. Демидова
Россия
Новосибирск, Россия
В. М. Попик
Россия
Новосибирск, Россия
Т. Н. Горячковская
Россия
Новосибирск, Россия
Список литературы
1. Altuvia S., Weinstein-Fischer D., Zhang A., Postow L., Storz G. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell. 1997;90(1):43-53.
2. Altuvia S., Zhang A., Argamon L., Tiwari A., Storz G. The Escherichia coli OxyS regulatory RNA represses fhlA translation by blocking ribosome binding. EMBO J. 1998;17(20):6069-6075.
3. Andersen J., Sternberg C., Poulsen L.K., Bjorn S.P., Givskov M., Molin S. New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl. Environ. Microbiol. 1998;64(6):2240-2246.
4. Arsène F., Tomoyasu T., Bukau B. The heat shock response of Escherichia coli. Int. J. Food Microbiol. 2000;55(1-3):3-9.
5. Aslund F., Zheng M., Beckwith J., Storz G. Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl. Acad. Sci. USA. 1999;96(11):6161-6165.
6. Belkin S., Smulski D.R., Vollmer A.C., Van Dyk T.K., Larossa R.A. Oxidative stress detection with Escherichia coli harboring a katG’::lux fusion. Appl. Environ. Microbiol. 1996;62(7):2252-2256.
7. Bird L.J., Coleman M.L., Newman D.K. Iron and copper act synergistically to delay anaerobic growth of bacteria. Appl. Environ. Microbiol. 2013;79(12):3619-3627.
8. Bogomazova A.N., Vassina E.M., Goryachkovskaya T.N., Popik V.M., Sokolov A.S., Kolchanov N.A., Lagarkova M.A., Kiselev S.L., Peltek S.E. No DNA damage response and negligible genome-wide transcriptional changes in human embryonic stem cells exposed to terahertz radiation. Sci. Rep. 2015;5:7749. DOI 10.1038/srep07749.
9. Borges-Walmsley M.I., Beauchamp J., Kelly S.M., Jumel K., Candlish D., Harding S.E., Price N.C., Walmsley A.R. Identification of oligomerization and drug-binding domains of the membrane fusion protein EmrA. J. Biol. Chem. 2003;278(15):12903-12912.
10. Brown N.L., Stoyanov J.V., Kidd S.P., Hobman J.L. The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 2003;27(2-3): 145-163.
11. Cabiscol E., Tamarit J., Ros J. Oxidative stress in bacteria and protein damage by reactive oxygen species. Intern. Microbiol. 2000;3(1):3-8.
12. Chillappagari S., Seubert A., Trip H., Kuipers O.P., Marahiel M.A., Miethke M.J. Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis. J. Bacteriol. 2010; 192(10):2512-2524.
13. de Macario С.E., Macario A.J. Heat-shock response in Archaea. Trends Biotechnol. 1994;12(12):512-518.
14. Demidova E.V., Goryachkovskaya T.N., Malup T.K., Bannikova S.V., Semenov A.I., Vinokurov N.A., Kolchanov N.A., Popik V.M., Peltek S.E. Studying the non-thermal effects of terahertz radiation on E. coli/pkatG-GFP biosensor cells. Bioelectromagnetics. 2013; 34(1):15-21.
15. Demidova E.V., Goryachkovskaya T.N., Mescheryakova I.A., Malup T.K., Semenov A.I., Vinokurov N.A., Kolchanov N.A., Popik V.M., Peltek S.E. Impact of terahertz radiation on stress-sensitive genes of E. coli cell. IEEE Transactions Terahertz Sci. Technol. 2016;6(3):435-441. DOI 10.1109/TTHZ.2016.2532344.
16. Devyatkov N.D., Betskiy O.V. Features of the interaction of low-intensity millimetric radiation with biologic objects. Primenenie millimetrovogo izlucheniya nizkoy intensivnosti v biologii i meditsine [Applications of low-intensity millimetric radiation in biology and medicine]. Moscow, 1985;6-20. (in Russian).
17. Devyatkov N.D., Betskiy O.V., Ilyina S.A., Putvinskiy A.B. Influence of low-intensity millimetric radiation on the ionic permeability of erythrocyte membranes. Effekty neteplovogo vozdeystviya millimetrovogo izlucheniya na biologicheskie ob”ekty (pod red. N.D. Devyatkova) [Devyatkov N.D. (Ed.). Effects of the nonthermal action of millimetric radiation on biologic objects]. Moscow, IRE AN SSSR Publ. 1983a:78-96. (in Russian).
18. Devyatkov N.D., Betskiy O.V., Zavizion V.A., Kudryashova V.A., Hurgin Yu.I. Absorption of electromagnetic radiation of the MM range of wavelengths and negative hydration in aqueous urea solutions. Doklady AN SSSR = Proceedings of the Academy of Sciences of the USSR. 1982;264(6):1409-1411. (in Russian).
19. Devyatkov N.D., Golant M.B. On the informational essence of nonthermal and some energetic impacts of electromagnetic oscillations on a living organism. Pisma v ZhTF = Letters to the Journal of Technical Physics. 1982;8(1):39-41. (in Russian).
20. Devyatkov N.D., Golant M.B., Tager A.S. A synchronization role of the action of weak electromagnetic signals of the millimetric wavelength range on living organisms. Biofizika = Biophysics. 1983b;28(5): 895-896. (in Russian).
21. Finney L.A., O’Halloran T.V. Transition metal speciation in the cell: insights from the chemistry of metal ion receptors. Science. 2003; 300(5621):931-936.
22. Flint D.H., Tuminello J.F., Emptage M.H. The inactivation of Fe-S cluster containing hydro- lyases by superoxide. J. Biol. Chem. 1993; 268(30):22369-22376.
23. Franke S., Grass G., Rensing C., Nies D.H. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J. Bacteriol. 2003;185(13):3804-3812.
24. Fröhlich H. What are non-thermal electric biological effects? Bioelectromagnetics. 1982;3(1):45-46.
25. Fung D.K., Lau W.Y., Chan W.T., Yan A. Copper efflux is induced during anaerobic amino acid limitation in Escherichia coli to protect iron-sulfur cluster enzymes and biogenesis. J. Bacteriol. 2013; 195(20):4556-4568.
26. González-Flecha B., Demple B. Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J. Biol. Chem. 1995; 270:13681-13687.
27. González-Flecha B., Demple B. Genetic responses to free radicals. Homeostasis and gene control. Ann. N.Y. Acad. Sci. 2000;899:69-87.
28. Grass G., Rensinq C. Genes involved in copper homeostasis in Escherichia coli. J. Bacteriol. 2001;183(6):2145-2147.
29. Grass G., Thakali K., Klebba P.E., Thieme D., Müller A., Wildner G.F., Rensing C. Linkage between catecholate siderophores and the multicopper oxidase CueO in Escherichia coli. J. Bacteriol. 2004;186(17):5826-5833.
30. Grkovic S., Brown M.H., Skurray R.A. Regulation of bacterial drug export systems. Microbiol. Mol. Biol. Rev. 2002;66(4):671-701.
31. Gutteridge J.M., Halliwell B. Comments on review of free radicals in biology and medicine (2nd ed.). Free Radic. Biol. Med. 1992; 12(1):93-95.
32. Hakkila K., Maksimow M., Karp M., Virta M. Reporter genes lucFF, luxCDABE, gfp, and dsred have different characteristics in wholecell bacterial sensors. Anal. Biochem. 2002;301(2):235-242.
33. Helsel M.E., Franz K.J. Pharmacological activity of metal binding agents that alter copper bioavailability. Dalton Trans. 2015;44(19):8760-8770.
34. Hengge-Aronis R. Interplay of global regulators and cell physiology in the general stress response of Escherichia coli. Current Opinion Microbiol. 1999;2(2):148-152.
35. Hengge-Aronis R. Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 2002;66(3):373-395.
36. Henle E.S., Han Z., Nang N., Rai P., Luo Y. Sequence-specific DNA cleavage by Fe2+-mediated Fenton reactions has possible biological implications. J. Biol. Chem. 1999;274(2):962-971.
37. Hidalgo E., Bollinger J.M., Jr., Bradley T.M., Walsh C.T., Demple B. Binuclear [2Fe-2S] clusters in the Escherichia coli SoxR protein and role of the metal centers in transcription. J. Biol. Chem. 1995;270 (36):20908-20914.
38. Hidalgo E., Demple B. An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein. EMBO J. 1994; 13(1):138-146.
39. Imlay J.A., Linn S. DNA damage and oxygen radical toxicity. Science. 1988;240:1302-1309.
40. Imlay K.R., Imlay J.A. Cloning and analysis of sodC, encoding the copper-zinc superoxide dismutase of Escherichia coli. J. Bacteriol. 1996;178(9):2564-2571.
41. Jang S., Imlay J.A. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J. Biol. Chem. 2007;282(2):929-937.
42. Khlebodarova T.M. How cells protect themselves against stress? Genetika = Genetics (Moscow). 2002;38(4):437-452. (in Russian).
43. Khlebodarova T.M., Tikunova N.V., Kachko A.V., Stepanenko I.L., Podkolodny N.L., Kolchanov N.A. Application of bioinformatics resources for genosensor design. J. Bioinform. Comput. Biol. 2007; 5(2B):931-938.
44. Kullik I., Stevens J., Toledano M.B., Storz G. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for DNA binding and multimerization. J. Bacteriol. 1995;177(5):1285-1291.
45. Liochev S.I., Fridovich I. The role of O2 – in the production of HO: in vitro and in vivo. Free Radic. Biol. Med. 1994;16(1):29-33.
46. Loewen P.C., Hu B., Strutinsky J., Sparling R. Regulation in the rpoS regulon of Escherichia coli. Can. J. Microbiol. 1998;44(8):707-717.
47. Lomovskaya O., Lewis K., Matin A. EmrR is a negative regulator of the Escherichia coli multidrug resistance pump EmrAB. J. Bacteriol. 1995;177(9):2328-2334.
48. Lushchak V.I. Environmentally induced oxidative stress in aquatic animals. Aquat. Toxicol. 2011;101(1):13-30.
49. Macomber L., Imlay J.A. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl. Acad. Sci. USA. 2009;106(20):8344-8349.
50. Macomber L., Rensing C., Imlay J.A. Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J. Bacteriol. 2007;189(5):1616-1626.
51. Miller P. F., Sulavik M.C. Overlaps and parallels in the regulation of intrinsic multiple- antibiotic resistance in Escherichia coli. Mol. Microbiol. 1996;21(3):441-448.
52. Morona R., Manning P.A., Reeves P. Identification and characterization of the TolC protein, an outer membrane protein from Escherichia coli. J. Bacteriol. 1983;153(2):693-699.
53. Nies D.H. Microbial heavy-metal resistance. Appl. Microbiol. Biotechnol. 1999;51(6):730-750.
54. Nunoshiba T., DeRojas-Walker T., Tannenbaum S.R., Demple B. Roles of nitric oxide in inducible resistance of Escherichia coli to activated murine macrophages. Infect. Immun. 1995;63(3):794-798.
55. Outten F.W., Huffman D.L., Hale J.A., O’Halloran T.V. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J. Biol. Chem. 2001;276(33): 30670-30677.
56. Outten F.W., Outten C.E., Hale J., O’Halloran T.V. Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, cueR. J. Biol. Chem. 2000;275(40):31024-31029.
57. Park S., Imlay J.A. High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J. Bacteriol. 2003;185(6):1942-1950.
58. Park S., You X., Imlay J.A. Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx-mutants in Escherichia coli. Proc. Natl. Acad. Sci. USA. 2005;102(26):9317-9322.
59. Pena M.M., Lee J., Thiele D.J. A delicate balance: homeostatic control of copper uptake and distribution. J. Nutr. 1999;129(7):1251-1260.
60. Petersen C., Moller L.B. Control of copper homeostasis in Escherichia coli by a P-type ATPase, CopA, and a MerR-like transcriptional activator, CopR. Gene. 2000;261(2):289-298.
61. Pomposiello P.J., Demple B. Redox-operated genetic switches: the SoxR and OxyR transcription factors.TRENDS Biotechnol. 2001; 19(3):109-114.
62. Putman M., van Veen H.W., Konings W.N. Molecular properties of bacterial multidrug transporters. Microbiol. Mol. Biol. Rev. 2000;64(4): 672-693.
63. Rademacher C., Masepohl B. Copper-responsive gene regulation in bacteria. Microbiology. 2012;158(10):2451-2464. DOI 10.1099/mic.0.058487-0.
64. Ramseier T.M., Bledig S., Michotey V., Feghali R., Saier M.H. The global regulatory protein FruR modulates the direction of carbon flow in Escherichia coli. Mol. Microbiol. 1995;16(6):1157-1169.
65. Rensing C., Ghosh M., Rosen B. Families of soft-metal-ion-transporting ATPases. J. Bacteriol. 1999;181(9):5891-5897.
66. Rowley D.A., Halliwell B. Superoxide-dependent formation of hydroxyl radicals from NADH and NADPH in the presence of iron salts. FEBS Lett. 1982;142(1):39-41.
67. Saier M.H. Cyclic AMP-independent catabolite repression in bacteria. FEMS Microbiol. Lett. 1996;138(2-3):97-103.
68. Saier M.H., Ramseier T.M. The catabolite repressor/activator (Cra) protein of enteric bacteria. J. Bacteriol. 1996;178(12):3411-3417.
69. Sakamoto A., Terui Y., Yoshida T., Yamamoto T., Suzuki H., Yamamoto K., Ishihama A., Igarashi K., Kashiwagi K. Three members of polyamine modulon under oxidative stress conditions: two transcription factors (SoxR and EmrR) and a glutathione synthetic enzyme (GshA). PLoS One. 2015;10(4). DOI 10.1371/journal.pone.0124883.
70. Seoane A.S., Levy S.B. Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli. J. Bacteriol. 1995;177(12):3414-3419.
71. Storz G., Tartaglia L.A., Ames B.N. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science. 1990;248(4952):189-194.
72. Tao K., Fujita N., Ishihama A. Involvement of the RNA polymerase alpha subunit C-terminal region in co-operative interaction and transcriptional activation with OxyR protein. Mol. Microbiol. 1993; 7(6):859-864.
73. Thieme D., Neubauer P., Nies D.H., Grass G. Sandwich hybridization assay for sensitive detection of dynamic changes in mRNA transcript levels in crude Escherichia coli cell extracts in response to copperions. Appl. Environ. Microbiol. 2008;74(24):7463-7470.
74. Thomas C., Mackey M.M., Diaz A.A., Cox D.P. Hydroxyl radical is produced via the Fenton reaction in submitochondrial particles under oxidative stress: implications for diseases associated with iron accumulation. Redox Rep. 2009;14(3):102-108.
75. Tsaneva I.R., Weiss B. SoxR, a locus governing a superoxide response regulon in Escherichia coli K-12. J. Bacteriol. 1990;172(8):4197- 4205.
76. Woodmansee A.N., Imlay J.A. Reduced flavins promote oxidative DNA damage in nonrespiring Escherichia coli by delivering electrons to intracellular free iron. J. Biol. Chem. 2002;277(37):34055-34066.
77. Wu J., Dunham W.R., Weiss B. Overproduction and physical characterization of SoxR, a [2Fe- 2S] protein that governs an oxidative response regulon in Escherichia coli. J. Biol. Chem. 1995;270(17):10323-10327.
78. Xiong A., Gottman A., Park C., Baetens M., Pandza S., Matin A. The EmrR protein represses the Escherichia coli emrRAB multidrug resistance operon by directly binding to its promoter region. Antimicrob. Agents Chemother. 2000;44(10):2905-2907.
79. Yamamoto K., Ishihama A. Transcriptional response of Escherichia coli to external copper. Mol. Microbiol. 2005;56(1):215-227.
80. Yoshida M., Kashiwagi K., Shigemasa A., Taniguchi S., Yamamoto K., Makinoshima H., Ishihama A., Igarashi K. A unifying model for the role of polyamines in bacterial cell growth, the polyamine modulo. J. Biol. Chem. 2004;279(44):46008-46013.
81. Zhang A., Altuvia S., Tiwari A., Argaman L., Hengge-Aronis R., Storz G. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J. 1998;17(20):6061-6068.
82. Zhang Z., Aboulwafa M., Saier M.H. Regulation of crp gene expression by the catabolite repressor/activator, Cra, in Escherichia coli. J. Mol. Microbiol. Biotechnol. 2014;24(3):135-141.
83. Zheng M., Doan B., Schneider T.D., Storz G. OxyR and SoxRS regulation of fur. J. Bacteriol. 1999;181(15):4639-4643.
84. Zheng M., Wang X., Templeton L.J., Smulski D.R., LaRossa R.A., Storz G. DNA microarray- mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 2001;183:4562-4570.