БИОХИМИЯ, 2019, том 84, вып. 11, с. 1718–1732

УДК 577.151.63

Особенности устройства и механизма катализа двух семейств терминальных оксидаз: гем-медных и bd-типа

Обзор

© 2019 В.Б. Борисов *,**, С.А. Силецкий

НИИ физико-химической биологии им. А.Н. Белозерского, Московский государственный университет им. М.В. Ломоносова, 119991 Москва, Россия; электронная почта: bor@belozersky.msu.ru, siletsky@belozersky.msu.ru

Поступила в редакцию 03.06.2019
После доработки 09.07.2019
Принята к публикации 10.07.2019

DOI: 10.1134/S0320972519110137

КЛЮЧЕВЫЕ СЛОВА: дыхательная цепь, терминальная оксидаза, цитохромоксидаза, цитохром bd, гем, каталитический цикл, кислородные интермедиаты, мембранный потенциал, протонный насос.

Аннотация

Терминальные оксидазы аэробных дыхательных цепей организмов катализируют перенос электронов с дыхательного субстрата, цитохрома с или хинола, на О2 с образованием 2Н2О. Известно два семейства этих оксидоредуктаз, интегрированных в мембрану: семейство гем-медных оксидаз и семейство оксидаз типа bd (цитохромов bd), найденных только у прокариот. Катализируемая этими ферментами окислительно-восстановительная реакция сопряжена с генерацией протон-движущей силы, которая используется клеткой для синтеза АТФ и совершения иной полезной работы. Благодаря наличию протонного насоса гем-медные оксидазы создают мембранный потенциал с большей энергетической эффективностью, чем цитохромы bd. Последние, однако, играют важную физиологическую роль, позволяя бактериям, в том числе патогенным, выживать и размножаться в неблагоприятных условиях окружающей среды. В обзоре рассматриваются особенности устройства и молекулярных механизмов функционирования терминальных окидаз из этих двух семейств в свете полученных за последнее время экспериментальных данных.

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Сноски

* Адресат для корреспонденции.

** Автор является выпускником кафедры биохимии биологического факультета МГУ им. М.В. Ломоносова.

Финансирование

Работа выполнена при финансовой поддержке Российского научного фонда (проект № 19-14-00063).

Благодарности

Авторы признательны В.П. Скулачеву, А.А. Константинову и А.Д. Виноградову за интерес к работе, полезное обсуждение и критические замечания.

Конфликт интересов

Авторы заявляют, что у них нет конфликта интересов.

Соблюдение этических норм

Настоящая статья не содержит каких-либо исследований с участием людей или использованием животных в качестве объектов исследований.

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76. Borisov, V.B., Forte, E., Davletshin, A., Mastronicola, D., Sarti, P., and Giuffre, A. (2013) Cytochrome bd oxidase from Escherichia coli displays high catalase activity: an additional defense against oxidative stress, FEBS Lett., 587, 2214–2218, doi: 10.1016/j.febslet.2013.05.047.

77. Borisov, V.B., Forte, E., Siletsky, S.A., Sarti, P., and Giuffre, A. (2015) Cytochrome bd from Escherichia coli catalyzes peroxynitrite decomposition, Biochim. Biophys. Acta, 1847, 182–188, doi: 10.1016/j.bbabio.2014.10.006.

78. Hoeser, J., Hong, S., Gehmann, G., Gennis, R.B., and Friedrich, T. (2014) Subunit CydX of Escherichia coli cytochrome bd ubiquinol oxidase is essential for assembly and stability of the di-heme active site, FEBS Lett., 588, 1537–1541, doi: 10.1016/j.febslet.2014.03.036.

79. Borisov, V., Arutyunyan, A.M., Osborne, J.P., Gennis, R.B., and Konstantinov, A.A. (1999) Magnetic circular dichroism used to examine the interaction of Escherichia coli cytochrome bd with ligands, Biochemistry, 38, 740–750, doi: 10.1021/bi981908t.

80. Arutyunyan, A.M., Sakamoto, J., Inadome, M., Kabashima, Y., and Borisov, V.B. (2012) Optical and magneto-optical activity of cytochrome bd from Geobacillus thermodenitrificans, Biochim. Biophys. Acta, 1817, 2087–2094, doi: 10.1016/j.bbabio.2012.06.009.

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82. Murali, R., and Gennis, R.B. (2018) Functional importance of Glutamate-445 and Glutamate-99 in proton-coupled electron transfer during oxygen reduction by cytochrome bd from Escherichia coli, Biochim. Biophys. Acta, 1859, 577–590, doi: 10.1016/j.bbabio.2018.04.012.

83. Borisov, V.B., and Verkhovsky, M.I. (2015) Oxygen as acceptor, EcoSal Plus, 6, doi: 10.1128/ecosalplus.ESP-0012-2015.

84. Forte, E., Borisov, V.B., Davletshin, A., Mastronicola, D., Sarti, P., and Giuffre, A. (2013) Cytochrome bd oxidase and hydrogen peroxide resistance in Mycobacterium tuberculosis, MBio, 4, e01006–e01013, doi: 10.1128/mBio.01006-13.

85. Borisov, V.B., Sedelnikova, S.E., Poole, R.K., and Konstantinov, A.A. (2001) Interaction of cytochrome bd with carbon monoxide at low and room temperatures: evidence that only a small fraction of heme b595 reacts with CO, J. Biol. Chem., 276, 22095–22099, doi: 10.1074/jbc.M011542200.

86. Borisov, V.B., and Verkhovsky, M.I. (2013) Accommodation of CO in the di-heme active site of cytochrome bd terminal oxidase from Escherichia coli, J. Inorg. Biochem., 118, 65–67, doi: 10.1016/j.jinorgbio.2012.09.016.

87. Siletsky, S.A., Dyuba, A.V., Elkina, D.A., Monakhova, M.V., and Borisov, V.B. (2017) Spectral-kinetic analysis of recombination reaction of heme centers of bd-type quinol oxidase from Escherichia coli with carbon monoxide, Biochemistry (Moscow), 82, 1354–1366, doi: 10.1134/S000629791711013X.

88. Arutyunyan, A.M., Borisov, V.B., Novoderezhkin, V.I., Ghaim, J., Zhang, J., Gennis, R. B., and Konstantinov, A.A. (2008) Strong excitonic interactions in the oxygen-reducing site of bd-type oxidase: the Fe-to-Fe distance between hemes d and b595 is 10 Å, Biochemistry, 47, 1752–1759, doi: 10.1021/bi701884g.

89. Siletsky, S.A., Rappaport, F., Poole, R.K., and Borisov, V.B. (2016) Evidence for fast electron transfer between the high-spin haems in cytochrome bd-I from Escherichia coli, PLoS One, 11, e0155186, doi: 10.1371/journal.pone.0155186.

90. Siletsky, S.A., Zaspa, A.A., Poole, R.K., and Borisov, V.B. (2014) Microsecond time-resolved absorption spectroscopy used to study CO compounds of cytochrome bd from Escherichia coli, PLoS One, 9, e95617, doi: 10.1371/journal.pone.0095617.

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92. Borisov, V.B., Gennis, R.B., and Konstantinov, A.A. (1995) Interaction of cytochrome bd from Escherichia coli with hydrogen peroxide, Biochemistry (Moscow), 60, 231–239.

93. Vos, M.H., Borisov, V.B., Liebl, U., Martin, J.L., and Konstantinov, A.A. (2000) Femtosecond resolution of ligand-heme interactions in the high-affinity quinol oxidase bd: a di-heme active site? Proc. Natl. Acad. Sci. USA, 97, 1554–1559, doi: 10.1073/pnas.030528197.

94. Borisov, V.B., Liebl, U., Rappaport, F., Martin, J.L., Zhang, J., Gennis, R.B., Konstantinov, A.A., and Vos, M.H. (2002) Interactions between heme d and heme b595 in quinol oxidase bd from Escherichia coli: a photoselection study using femtosecond spectroscopy, Biochemistry, 41, 1654–1662, doi: 10.1021/bi0158019.

95. Borisov, V.B. (2008) Interaction of bd-type quinol oxidase from Escherichia coli and carbon monoxide: heme d binds CO with high affinity, Biochemistry (Moscow), 73, 14–22, doi: 10.1134/S0006297908010021.

96. Rappaport, F., Zhang, J., Vos, M.H., Gennis, R.B., and Borisov, V.B. (2010) Heme-heme and heme-ligand interactions in the di-heme oxygen-reducing site of cytochrome bd from Escherichia coli revealed by nanosecond absorption spectroscopy, Biochim. Biophys. Acta, 1797, 1657–1664, doi: 10.1016/j.bbabio.2010.05.010.

97. Paulus, A., Rossius, S.G., Dijk, M., and de Vries, S. (2012) Oxoferryl-porphyrin radical catalytic intermediate in cytochrome bd oxidases protects cells from formation of reactive oxygen species, J. Biol. Chem., 287, 8830–8838, doi: 10.1074/jbc.M111.333542.

98. Borisov, V.B., Forte, E., Sarti, P., and Giuffre, A. (2011) Catalytic intermediates of cytochrome bd terminal oxidase at steady-state: ferryl and oxy-ferrous species dominate, Biochim. Biophys. Acta, 1807, 503–509, doi: 10.1016/j.bbabio.2011.02.007.

99. Yang, K., Borisov, V.B., Konstantinov, A.A., and Gennis, R.B. (2008) The fully oxidized form of the cytochrome bd quinol oxidase from E. coli does not participate in the catalytic cycle: direct evidence from rapid kinetics studies, FEBS Lett., 582, 3705–3709, doi: 10.1016/j.febslet.2008.09.038.

100. Azarkina, N., Siletsky, S., Borisov, V., von Wachenfeldt, C., Hederstedt, L., and Konstantinov, A.A. (1999) A cytochrome bb’-type quinol oxidase in Bacillus subtilis strain 168, J. Biol. Chem., 274, 32810–32817, doi: 10.1074/jbc.274.46.32810.