БИОХИМИЯ, 2020, том 85, вып. 10, с. 1323–1330

УДК 577.24

Программируемая гибель клеток: исторические заметки из России

Мини-обзор

© 2020 Б. Животовский 1,2

Московский государственный университет имени М.В. Ломоносова, факультет фундаментальной медицины, 119991 Москва, Россия

Институт медицины окружающей среды, Каролинский институт, Стокгольм, Швеция; электронная почта: boris.zhivotovsky@ki.se

Поступила в редакцию 12.07.2020
После доработки 12.07.2020
Принята к публикации 16.07.2020

DOI: 10.31857/S0320972520100012

КЛЮЧЕВЫЕ СЛОВА: апоптоз, радиация, митохондрии, нуклеазы, протеазы.

Аннотация

Исследование механизмов гибели клеток – одна из наиболее быстро развивающихся областей современной биомедицины. Особый интерес к этой проблеме возник в 1972 г. после опубликования статьи Kerr, Wyllie и Currie, в которой апоптоз, один из типов гибели клеток, впервые был рассмотрен как базовый биологический феномен, регулирующий гомеостаз тканей. Несколько российских групп, занимавшихся изучением механизмов индуцируемой радиацией гибели клеток, обратили внимание на схожесть между этими двумя механизмами. По некоторым объективным причинам эти работы долгое время нe были доступны мировой общественности. В настоящем введении предпринята попытка восстановить цепь событий минувших дней.

Текст статьи

Пожалуйста, введите код, чтобы получить PDF файл с полным текстом статьи:

captcha

Финансирование

Работа выполнена при финансовой поддержке гранта РНФ (19-15-00125). Работа лабораторий также поддерживается грантами РФФИ (18-29-09005), Шведского (190345) и Стокгольмского (181301) противораковых фондов.

Конфликт интересов

Автор заявляет об отсутствии конфликта интересов.

Соблюдение этических норм

Настоящая работа не содержит описания выполненных авторами исследований с участием людей или использованием животных в качестве объектов.

Список литературы

1. Kerr, J. F., Wyllie, A. H., and Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics, Br. J. Cancer, 26, 239-257, doi: 10.1038/bjc.1972.33.

2. Wyllie, A. H. (1988) Apoptosis, ISI Atlas of Science: Immunology, 1, 192-196.

3. Schleiden, M. J. (1838) Beiträge zur phytogenesis, Arch. Anat. Physiol. Wiss Med., 137-176.

4. Schwann, T. (1839) Mikroskopische Untersuchungen über die Übereinstimmung in der Struktur und dem Wachsthum der Thiere und Pflanzen, Sander, Berlin.

5. Vogt, C. (1842) Untersuchungen uber die Entwicklungs-geschichte der Geburtshelferkröte (Alytes obstetricans), Solothurn: Jent und Gassmann.

6. Glücksmann, A. (1951) Cell deaths in normal vertebrate ontogeny, Biol. Rev. Camb. Philos. Soc., 26, 59-86, doi: 10.1111/j.1469-185x.1951.tb00774.x.

7. Saunders, J. W. (1966) Death in embryonic systems, Science, 154, 604-612, doi: 10.1126/science.154.3749.604.

8. Lockshin, R. A., and Williams, C. M. (1965) Programmed cell death: cytology of degeneration in the intersegmental muscles of the Pernyi silkmoth, J. Insect. Physiol., 11, 123-133, doi: 10.1016/0022-1910(65)90099-5.

9. Okada, S. (1970) Radiation biochemistry (Altman, K. L., Gerber, G. B., and Okada, Sh., eds.) Vol. 2, Tissue and Body Fluids, Academic Press, New York, London, pp. 247-307.

10. Hanson, K. P. (1979) Radiation-induced cell death, Radiobiology, 19, 814-820 (in Russian).

11. Umansky, S. R. (1982) Genetic program of cell death: hypothesis and some applications, Ach. Modern Biol., 93, 139-148 (in Russian).

12. Yamada, T., and Ohyama, H. (1988) Radiation-induced interphase death of rat thymocytes is internally programmed (apoptosis), Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 53, 65-75, doi: 10.1080/09553008814550431.

13. Wyllie, A. H. (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation, Nature, 284, 555-556, doi: 10.1038/284555a0.

14. Cole, L. J., and Ellis, M. E. (1957) Radiation-induced changes in tissue nucleic acids; release of soluble deoxypolynucleotides in the spleen, Radiat. Res., 7, 508-517, PMID: 13485392.

15. Ermolaeva, N. V., and Vodolazskaya, N. A. (1970) Separation on phosphate cellulose of deoxyribonucleoproteins formed after irradiation and in vitro treatment with enzymes, Biochemistry, 35, 641-647.

16. Skalka, M., Matyásová, J., and Cejková, M. (1975) DNA in chromatin of irradiated lymphoid tissues degrades in vivo into regular fragments, FEBS Lett., 72, 271-274, doi: 10.1016/0014-5793(76)80984-2.

17. Vodolazskaya, N. A., and Ermolaeva, N. V. (1974) Comparative analysis of the state of DNA and histone fraction in DNP and salt extracts of rat thymus after gamma radiation, as well as the introduction of degranol and hydrocortisone, Radiobiology, 14, 651-655.

18. Vodolazskaya, N. A., and Ermolaeva, N. V. (1971) Study of the decay products of deoxyribonucleoproteins induced by gamma irradiation, hydrocortisone and degranol in the thyroid gland of rats by the methods of separation into phosphate cellulose and viscometry, Radiobiology, 11, 335-358.

19. Zhivotovsky, B., Wade, D., Nicotera, P., and Orrenius, S. (1994) Role of nucleases in apoptosis, Int. Arch. Allergy Immunol., 105, 333-338, doi: 10.1159/000236778.

20. Yuan, J., Shaham, S., Ledoux, S., Ellis, H. M., and Horvitz, H. R. (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme, Cell, 75, 641-652, doi: 10.1016/0092-8674(93)90485-9.

21. Zhivotovsky, B., Burgess, D. H., Vanags, D. M., and Orrenius, S. (1997) Involvement of cellular proteolytic machinery in apoptosis, Biochem. Biophys. Res. Commun., 230, 481-488, doi: 10.1006/bbrc.1996.6016.

22. Soldatenko, V. A., Denisenko, M. F., Alferova, T. M., and Filippovich, I. V. (1991) Chromatin degradation during the death of thymic lymphocytes under the influence of radiation or dexamethasone: the need for a preliminary proteolysis stage, Radiobiology, 31, 180-187.

23. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A., and Nagata, S. (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD, Nature, 391, 43-50, doi: 10.1038/34112.

24. Sakahira, H., Enari, M., and Nagata, S. (1998) Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis, Nature, 391, 96-99, doi: 10.1038/34214.

25. Liu, X., Zou, H., Slaughter, C., and Wang, X. (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis, Cell, 89, 175-184, doi: 10.1016/s0092-8674(00)80197-x.

26. Liu, X., Li, P., Widlak, P., Zou, H., Luo, X., Garrard, W. T., and Wang, X. (1998) The 40-kDa subunit of DNA fragmentation factor induces DNA fragmentation and chromatin condensation during apoptosis, Proc. Natl. Acad. Sci. USA, 95, 8461-8466, doi: 10.1073/pnas.95.15.8461.

27. Wu, Y. C., Stanfield, G. M., and Horvitz, H. R. (2000) NUC-1, a Caenorhabditis elegans DNase II homolog, functions in an intermediate step of DNA degradation during apoptosis, Genes Dev., 14, 536-548, PMID: 10716942.

28. Kawane, K., Fukuyama, H., Kondoh, G., Takeda, J., Ohsawa, Y., Uchiyama, Y., and Nagata, S. (2001) Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver, Science, 292, 1546-1549, doi: 10.1126/science.292.5521.1546.

29. Lazebnik, Y. A., Kaufmann, S. H., Desnoyers, S., Poirier, G. G., and Earnshaw, W. C. (1994) Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE, Nature, 371, 346-347, doi: 10.1038/371346a0.

30. Zotova, R. N., Umansky, S. R., and Tokarskaya, V. I. (1983) Mechanism of chromatin degradation in thymocytes of irradiated rats. Part 6. Post-radiation changesin the activity of poly (ADP/ribose)-polymerase, Radiobiology, 23, 152-156.

31. Nelipovich, P. A., Nikonova, L. V., and Umansky, S. R. (1988) Inhibition of poly(ADP-ribose) polymerase as a possible reason for activation of Ca2+/Mg2+-dependent endonuclease in thymocytes of irradiated rats, Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 53, 749-765, doi: 10.1080/09553008814551111.

32. Denisenko, M. F., Belovskaya, L. N., Soldatenkov, V. A., Smirnova, T. N., and Filippovich, I. V. (1987) Poly(ADP-ribosylation) of proteins determines the pool of endogenous NAD and the radiosensitivity of thymic lymphocytes, Radiobiology, 27, 737-742.

33. Denisenko, M. F., Soldatenkov, V. A., Belovskaya, L. N., and Filippovich, I. V. (1989) Is the NAD-poly (ADP-ribose) polymerase system the trigger in radiation-induced death of mouse thymocytes? Int. J. Radiat. Biol., 56, 277-285, doi: 10.1080/09553008914551441.

34. Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c, Cell, 86, 147-157, doi: 10.1016/s0092-8674(00)80085-9.

35. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic proteasecascade, Cell, 91, 479-489, doi: 10.1016/s0092-8674(00)80434-1.

36. Zou, H., Henzel, W. J., Liu, X., Lutschg, A., and Wang, X. (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3, Cell, 90, 405-413, doi: 10.1016/s0092-8674(00)80501-2.

37. Ashwell, G., and Hickman, J., (1952) Effects of X-irradiation upon the enzyme systems of the mouse spleen, Proc. Soc. Exp. Biol. Med., 80, 407-413, doi: 10.3181/00379727-80-19639.

38. Van Bekkum, D. W. (1957) The effect of X-rays on phosphorylation in vivo, Biochim. Biophys. Acta, 25, 487-492, doi: 10.1016/0006-3002(57)90518-8.

39. Scaife, J. F. (1964) The nature of the radiation-induced lesion of the electron transport chain of thymus mitochondria, Can. J. Biochem., 42, 431-434, doi: 10.1139/o64-050.

40. Manoilov, S. E. (1968) Primary Mechanisms of the Biological Action of Ionizing Radiation, Medicine, Leningrad.

41. Hanson, K. P., and Mytareva, L. V. (1967) Mechanisms of the effect of ionizing radiation on oxidative phosphorylation in animals, Proc. Acad. Sci. (Estonia), 16, 80-87.

42. Van Bekkum, D. W., DeVries, M. J., and Klowen, H. M. (1964) Biochemical and morphological changes in lymphatic tissues following partial-body irradiation, Int. J. Radiat. Biol., 8, 395-401.

43. Scaife, J. F., and Hill, B. (1963) Uncoupling of oxidative phosphorylation by ionizing radiation. II. The stability of mitochondrial lipids and cytochrome c, Can. J. Biochem., 41, 1223-1227, PMID: 13976477.

44. Manoilov, S. E., and Hanson, K. P. (1964) The effect of exogenous cytochrome c on oxidative phosphorylation in mitochondria of tissues isolated from irradiated animals, Vopr. Med. Chem., 10, 410-416.

45. Scaife, J. F. (1966) The effect of lethal doses of X-irradiation on the enzymatic activity of mitochondrial cytochrome c, Can. J. Biochem., 44, 433-439, PMID: 4289628.

46. Kharbanda, S., Pandey, P., Schofield, L., Israels, S., Roncinske, R., Yoshida, K., Bharti, A., Yuan, Z. M., Saxena, S., Weichselbaum, R., Nalin, C., and Kufe, D. (1997) Role for Bcl-xL as an inhibitor of cytosolic cytochrome c accumulation in DNA damage-induced apoptosis, Proc. Natl. Acad. Sci. USA, 94, 6939-6942, doi: 10.1073/pnas.94.13.6939.

47. Hampton, M. B., Zhivotovsky, B., Slater, A. F. G., Burgess, D. H., and Orrenius, S. (1998) Importance of the redox state of cytochrome c during caspase activation in cytosolic extracts, Biochem. J., 329, 95-99, doi: 10.1042/bj3290095.

48. Ott, M., Robertson, J. D., Gogvadze, V., Zhivotovsky, B., and Orrenius, S. (2002) Cytochrome c release from mitochondria proceeds by a two-step process, Proc. Natl. Acad. Sci. USA, 99, 1259-1263, doi: 10.1073/pnas.241655498.

49. Kagan, V. E., Tyurin, V. A., Jiang, J., Tyurina, Y. Y., Ritov, V. B., Amoscato, A. A., Osipov, A. N., Belikova, N. A., Kapralov, A. A., Kini, V., Vlasova, I. I., Zhao, Q., Zou, M., Di, P., Svistunenko, D. A., Kurnikov, I. V., and Borisenko, G. G. (2005) Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors, Nat. Chem. Biol., 1, 223-232, doi: 10.1038/nchembio727.

50. Orrenius, S., and Zhivotovsky, B. (2005) Cardiolipin oxidation sets cytochrome c free, Nat. Chem. Biol., 1, 188-189, doi: 10.1038/nchembio0905-188.

51. Kuwana, T., Bouchier-Hayes, L., Chipuk, J. E., Bonzon, C., Sullivan, B. A., Green, D. R., and Newmeyer, D. D. (2005) BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly, Mol. Cell, 17, 525-535, doi: 10.1016/j.molcel.2005.02.003.

52. Zhivotovsky, B., Orrenius, S., Brustugun, O. T., and Doskeland, S. O. (1998) Injected cytochrome c induces apoptosis, Nature, 391, 449-450, doi: 10.1038/35060.

53. Eguchi, Y., Shimizu, S., and Tsujimoto, Y. (1997) Intra-cellular ATP levels determine cell death fate by apoptosis or necrosis, Cancer Res., 57, 1835-1840, PMID: 10232605.

54. Leist, M., Single, B., Castoldi, A. F., Kühnle, S., and Nicotera, P. (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis, J. Exp. Med., 185, 1481-1486, doi: 10.1084/jem.185.8.1481.

55. Reed, J. (1997) Cytochrome c: can’t live with it – can’t live without it, Cell, 91, 559-562, doi: 10.1016/s0092-8674(00)80442-0.

56. Schendel, S. L., Montal, M., and Reed, J. C. (1998) Bcl-2 family proteins as ion-channels, Cell Death Differ., 5, 372-380, doi: 10.1038/sj.cdd.4400365.

57. Skulachev, V. P. (1997) Aging is a specific biological function rather than the result of a disorder in complex living systems: biochemical evidence in support of Weismann’s hypothesis, Biochemistry (Moscow), 62, 1394-1399, PMID: 9467841.

58. Libertini, G. (2012) Classification of phenoptotic phenomena, Biochemistry (Moscow), 77, 707-715, doi: 10.1134/S0006297912070024.

59. Walker, R. F. (2017) On the causes and mechanisms of phenoptosis, Biochemistry (Moscow), 82, 1820-1841, doi: 10.1134/S0006297917120069.

60. Vyssokikh, M. Y., Holtze, S., Averina, O. A., Lyamzaev, K. G., Panteleeva, A. A., Marey, M. V., Zinovkin, R. A., Severin, F. F., Skulachev, M. V., Fasel, N., Hildebrandt, T. B., and Skulachev, V. P. (2020) Mild depolarization of the inner mitochondrial membrane is a crucial component of an anti-aging program. Proc. Natl. Acad. Sci. USA, 117, 6491-6501, doi: 10.1073/pnas.1916414117.