Роль мутаций генов piwi и aub в радиационно-индуцированном ответе у Drosophila melanogaster

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В данном исследовании впервые получены сведения о чувствительности животных с дисфункцией генов piwi и aub к хроническому облучению в малых дозах (20 сГр) и проявлении у анализируемых мутантов радиоадаптивного ответа. Реакция мутантных генотипов Drosophila melanogaster на облучение была проанализирована по показателям “продолжительность жизни”, “фертильность” и “повреждения ДНК”. Результаты экспериментов показали, что у самок с мутацией piwi обнаружено адаптивное действие хронического облучения в малых дозах (20 сГр) в ответ на последующую экспозицию в дозе 60 Гр. Хроническое низкоинтенсивное облучение не повлияло на репродуктивные функции и уровень повреждений ДНК в гонадах особей с дисфункцией генов piwi и aub, но привело к повышению их продолжительности жизни. Таким образом, функциональное снижение некоторых генов семейства Argonaute может модифицировать эффекты облучения с формированием у животных радиорезистентных признаков.

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Елена Александровна Юшкова

Коми научный центр Уральского отделения РАН

Автор, ответственный за переписку.
Email: ushkova@ib.komisc.ru
ORCID iD: 0000-0002-5580-2276

Институт биологии

Россия, Республика Коми, г. Сыктывкар, ул. Коммунистическая, 28

Список литературы

  1. Nikjoo H., O’Neill P, Wilson W.E. et al. Computational approach for determining the spectrum of DNA damage induced by ionizing radiation. Radiat. Res. 2001;156(5):577–583. https://doi.org/10.1667/0033-7587(2001)156[0577: cafdts]2.0.co;2
  2. Wei J., Wang B., Wang H. et al. Radiation-induced normal tissue damage: Oxidative stress and epigenetic mechanisms. Oxid. Med. Cell. Longev. 2019;2019: 3010342. https://doi.org/10.1155/2019/3010342
  3. Weigel C., Veldwijk M.R., Oakes C.C. et al. Epigenetic regulation of diacylglycerol kinase alpha promotes radiation-induced fibrosis. Nat. Commun. 2016;7:10893. https://doi.org/10.1038/ncomms10893
  4. Yushkova E. Genetic mechanisms of formation of radiation-induced instability of the genome and its transgenerational effects in the descendants of chronically irradiated individuals of Drosophila melanogaster. Radiat. Environ. Biophis. 2020;59(2): 221–236. https://doi.org/10.1007/s00411-020-00833-2
  5. Yushkova E. Contribution of transposable elements to transgenerational effects of chronic radioactive exposure of natural populations of Drosophila melanogaster living for a long time in the zone of the Chernobyl nuclear disaster. J. Environ. Radioact. 2022a;251–252:106945. https://doi.org/10.1016/j.jenvrad.2022.106945
  6. Seong K.M., Cenci G. Editorial: The genetic and epigenetic bases of cellular response to ionizing radiation. Front. Genet. 2022;13:857168. https://doi.org/10.3389/fgene.2022.857168
  7. Shesterikova E.M., Bondarenko V.S., Volkova P.Yu. Differential gene expression in chronically irradiated herbaceous species from the Chernobyl exclusion zone. Int. J. Radiat. Biol. 2023;99(2):229–237. https://doi.org/10.1080/09553002.2022.2087927
  8. Shin E., Lee S., Kang H. et al. Organ-specific effects of low dose radiation exposure: A comprehensive review. Front. Genet. 2020;11:566244. https://doi.org/10.3389/fgene.2020.566244
  9. Guéguen Y., Bontemps A., Ebrahimian T.G. Adaptive responses to low doses of radiation or chemicals their cellular and molecular mechanisms. Cell. Mol. Life Sci. 2019;76(7):1255‒1273. https://doi.org/10.1007/s00018-018-2987-5
  10. Yushkova E. Radiobiological features in offspring of natural populations of Drosophila melanogaster after Chernobyl accident. Environ. Mol. Mutagen. 2022b;63:84–97. https://doi.org/10.1002/em.22476
  11. Koval L., Proshkina E., Shaposhnikov M., Moskalev A. The role of DNA repair genes in radiation-induced adaptive response in Drosophila melanogaster is differential and conditional. Biogerontol. 2020;21:45–56. https://doi.org/10.1007/s10522-019-09842-1
  12. Dubrova Yu.E., Sarapultseva E.I. Radiation-induced transgenerational effects in animals. Int. J. Radiat. Biol. 2022;98(6):1047–1053. https://doi.org/10.1080/09553002.2020.1793027
  13. Sato K., Siomi M.C. The piRNA pathway in Drosophila ovarian germ and somatic cells. Proc. Jpn. Acad. Ser. B. Phys. Biol. Sci. 2020;96(1):32–42. https://doi.org/10.2183/pjab.96.003
  14. Toth K.F., Pezic D., Stuwe E. Webster A. The piRNA pathway guards the germline genome against transposable elements. Adv. Exp. Med Biol. 2016;886:51–77. https://doi.org/10.1007/978-94-017-7417-8_4
  15. Gonzalez L.E., Tang X., Lin H. Maternal Piwi regulates primordial germ cell development to ensure the fertility of female progeny in Drosophila. Genetics. 2021;219(1):iyab091. https://doi.org/10.1093/genetics/iyab091
  16. Sousa-Victor P., Ayyaz A., Hayashi R. et al. Piwi is required to limit exhaustion of aging somatic stem cells. Cell Reports. 2017;20:2527–2537. https://doi.org/10.1016/j.celrep.2017.08.059
  17. Proshkina E., Yushkova E., Koval L. et al. Tissue-specific knockdown of genes of the Argonaute family modulates lifespan and radioresistance in Drosophila melanogaster. Int. J. Mol. Sci. 2021;22(5):2396. https://doi.org/10.3390/ijms22052396
  18. Evangelou A., Ignatiou A., Antoniou C. et al. Unpredictable effects of the genetic background of transgenic lines in physiological quantitative traits. G3 (Bethesda). 2019;9(11):3877–3890. https://doi.org/10.1534/g3.119.400715
  19. Theron E., Maupetit-Mehouas S., Pouchin P. et al. The interplay between the Argonaute proteins Piwi and Aub within Drosophila germarium is critical for oogenesis, piRNA biogenesis and TE silencing. Nucl. Acids Res. 2018;46:10052–10065. https://doi.org/10.1093/nar/gky695
  20. Adashev V.E., Kotov A.A., Bazylev S.S. et al. Stellate genes and the piRNA pathway in speciation and reproductive isolation of Drosophila melanogaster. Front. Genet. 2021;11:610665. https://doi.org/10.3389/fgene.2020.610665
  21. Yushkova E.A. The effects of transpositions of functional I retrotransposons depend on the conditions and dose of parental exposure. Int. J. Radiat. Biol. 2023;99(5):737–749. https://doi.org/10.1080/09553002.2023.2142978
  22. Olive P.L., Wlodek D., Durand R.E., Banáth J.P. Factors influence DNA migration from individual cells subjected to gel electrophoresis. Exp. Cell Res. 1992;198(2):259–260. https://doi.org/10.1016/0014-4827(92)90378-l
  23. Han S.K., Lee D., Lee H. et al. OASIS 2: online application for survival analysis 2 with features for the analysis of maximal lifespan and healthspan in aging research. Oncotarget. 2016;7:56147–56152. https://doi.org/10.18632/oncotarget.11269
  24. Bonner W.M. Low-dose radiation: Thresholds, bystander effects, and adaptive responses. PNAS. 2003;100(9):4973–4975. https://doi.org/10.1073/pnas.1031538100
  25. Asaithamby A., Chen D.J. Cellular Responses to DNA double-strand breaks after low-dose gamma-irradiation. Nucl. Acid. Res. 2009;37(12):3912⎯3923. https://doi.org/10.1093/nar/gkp237
  26. Юшкова Е.А., Зайнуллин В.Г. Радиационно-индуцированная фрагментация ДНК в клетках соматических и генеративных тканей Drosophila melanogaster. Радиац. биология. Радиоэкология. 2015;55(1):97–103. [Yushkova E., Zainullin V. Radiation-induced DNA fragmentation in cells of somatic and generative tissues of Drosophila melanogaster. Radiats. Biol. Radioecol. 2015;55(1):97–103. (In Russ.)]. https://doi.org/10.7868/S0869803115010178
  27. Wayne M.L., Soundararajan U., Harshman L.G. Environmental stress and reproduction in Drosophila melanogaster: starvation resistance, ovariole numbers and early age egg production. BMC Evol. Biol. 2006;6:57. https://doi.org/10.1186/1471-2148-6-57
  28. Landis G., Shen J., Tower J. Gene expression changes in response to aging compared to heat stress, oxidative stress and ionizing radiation in Drosophila melanogaster. Aging. 2012;4(11):768–789. https://doi.org/10.18632/aging.100499
  29. Belyi A.A., Alekseev A.A., Fedintsev A.Y. et al. The resistance of Drosophila melanogaster to oxidative, genotoxic, proteotoxic, osmotic stress, infection, and starvation depends on age according to the stress factor. Antioxidants. 2020;9:1239. https://doi.org/10.3390/antiox9121239
  30. Pappalardo A.M., Ferrito V., Biscotti M.A. et al. Transposable elements and stress in vertebrates: An overview. Int. J. Mol. Sci. 2021;22(4):1970. https://doi.org/10.3390/ijms22041970
  31. Czech B., Preall J.B., McGinn J., Hannon G.J. A transcriptome-wide RNAi screen in the Drosophila ovary reveals factors of the germline piRNA pathway. Mol. Cell. 2013;50:749–761. https://doi.org/ 10.1016/j.molcel.2013.04.007
  32. Russell S.J., LaMarre J. Transposons and the PIWI pathway: genome defense in gametes and embryos. Reproduction. 2018;156(4):R111–R124. https://doi.org/10.1530/REP-18-0218
  33. Ross R.J., Weiner M.M., Lin H. PIWI proteins and PIWI-interacting RNAs in the soma. Nature. 2014;505:353–359. https://doi.org/10.1038/nature12987
  34. Jones B.C., Wood J.G., Chang C. et al. A somatic piRNA pathway in the Drosophila fat body ensures metabolic homeostasis and normal lifespan. Nat. Commun. 2016;7:13856. https://doi.org/10.1038/ncomms13856
  35. Zuo L., Wang Z., Tan Y. et al. piRNAs and their functions in the brain. Int. J. Hum. Genet. 2016;16:53–60. https://doi.org/10.1080/09723757.2016.11886278
  36. Perera B.P.U., Tsai Z. T.-Y., Colwell M. et al. Somatic expression of piRNA and associated machinery in the mouse identifies short, tissue-specific piRNA. Epigenetics. 2019;14(5):504–521. https://doi.org/10.1080/15592294.2019.1600389
  37. Lin K.Y., Wang W.D., Lin C.H. et al. Piwi reduction in the aged niche eliminates germline stem cells via Toll-GSK3 signaling. Nat. Commun. 2020;11:3147. https://doi.org/10.1038/s41467-020-16858-6
  38. Rajasethupathy P., Antonov I., Sheridan. R et al. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell. 2012;149:693–707. https://doi.org/10.1016/j.cell.2012.02.057
  39. Phay M., Kim H.H., Yoo S. Analysis of piRNA-like small non-coding RNAs present in axons of adult sensory neurons. Mol. Neurobiol. 2018;55:483–494. https://doi.org/10.1007/s12035-016-0340-2
  40. Praher D., Zimmermann B., Genikhovich G. et al. Characterization of the piRNA pathway during development of the sea anemone Nematostella vectensis. RNA Biol. 2017;14:1727–1741. https://doi.org/10.1080/15476286.2017.1349048
  41. Ma Z., Wang H., Cai Y. et al. Epigenetic drift of H3K27me3 in aging links glycolysis to healthy longevity in Drosophila. eLife. 2018;7:e35368. https://doi.org/10.7554/eLife.35368
  42. Heestand B., Simon M., Frenk S. et al. Transgenerational sterility of Piwi mutants represents a dynamic form of adult reproductive diapause. Cell Rep. 2018;23:156–171. https://doi.org/10.1016/j.celrep.2018.03.015
  43. Yushkova E. Interaction effect of mutations in the genes (piwi and aub) of the Argonaute family and hobo transposons on the integral survival parameters of Drosophila melanogaster. Biogerontology. 2024;5:131–146. https://doi.org/10.1007/s10522-023-10062-x
  44. Brennecke J., Aravin A.A., Stark A. et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell. 2007;128:1089–1103. https://doi.org/10.1016/j.cell.2007.01.043
  45. Gainetdinov I., Colpan C., Arif A, Cecchini K., Zamore P. A single mechanism of biogenesis, initiated and directed by PIWI proteins, explains piRNA production in most animals. Mol. Cell. 2018;71:775–790. https://doi.org/10.1016/j.molcel.2018.08.007
  46. van Lopik J., Alizada A., Trapotsi M.-A. et al. Unistrand piRNA clusters are an evolutionarily conserved mechanism to suppress endogenous retroviruses across the Drosophila genus. Nat. Commun. 2023;14:7337. https://doi.org/10.1038/s41467-023-42787-1
  47. Senti K.A., Jurczak D., Sachidanandam R., Brennecke J. piRNA-guided slicing of transposon transcripts enforces their transcriptional silencing via specifying the nuclear piRNA repertoire. Genes Dev. 2015;29(16):1747–1762. https://doi.org/10.1101/gad.267252.115

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2. Рис. 1. Фертильность самок D. melanogaster с мутациями в генах piwi и aub после хронического и острого облучения. *p < 0.05 – по сравнению с контролем.

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3. Рис. 2. Кривые выживания особей D. melanogaster с мутациями в генах piwi и aub после хронического и острого облучения. *p < 0.05, **p < 0.001, ***p < 0.0001 – по сравнению с контролем, ♂♂ – самцы, ♀♀ – самки.

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