БИОХИМИЯ, 2021, том 86, вып. 3, с. 297–307

УДК 577.216.35

Структура и механизмы экспрессии больших (+)РНК-геномов вирусов высших эукариот

Мини-обзор

© 2021 А.А. Аграновскийetdonas2@gmail.com

Московский государственный университет имени М.В. Ломоносова, биологический факультет, кафедра вирусологии, 119234 Москва, Россия

Поступила в редакцию 17.08.2020
После доработки 21.09.2020
Принята к публикации 29.09.2020

DOI: 10.31857/S0320972521030027

КЛЮЧЕВЫЕ СЛОВА: вирусные РНК-геномы, нидовирусы, SARS-CoV, клостеровирусы, эволюция, экспрессия генов.

Статья на английском языке опубликована в режиме Open Access (открытого доступа) на сайте издательства Springer. DOI: 10.1134/S0006297921030020.

Аннотация

Быстрые темпы эволюции РНК-геномов, которые обусловлены высоким уровнем мутаций и рекомбинацией при копировании цепей РНК, позволяют вирусу изменять и приобретать последовательности для оптимальной адаптации. Размеры РНК-генома ограничены факторами, связанными с точностью РНК-полимераз и упаковкой. В ходе эволюции (+)РНК-геномы нидовирусов животных (артеривирусов, ронивирусов, коронавирусов) и клостеровирусов растений преодолели барьер в 12 тыс. нуклеотидов. Коронавирусы и клостеровирусы имеют общие свойства. Их РНК-геномы содержат 5′-концевые гены, экспрессируемые с помощью рибосомального сдвига рамки считывания и кодирующие домены папаин-подобной протеиназы, метилтрансферазы, мембраносвязывающих белков, хеликазы и РНК-полимеразы. Коронавирусы, в дополнение к этому, содержат домены экзонуклеазы с редактирующей активностью, гипотетической праймазы, нуклеотидилтрансферазы и эндонуклеазы. РНК-геном коронавирусов и клостеровирусов содержит на 3′-конце гены структурных и вспомогательных белков, для экспрессии которых используется набор котерминальных субгеномных РНК. В ходе эволюции вирионов представители обеих вирусных групп приобрели гибкие спирально-симметричные нуклеокапсиды, что позволило снять ограничения на размер инкапсидируемых молекул РНК. Филогенетические реконструкции домена РНК-полимеразы указывают лишь на отдаленное родство коронавирусов и клостеровирусов, и их общие свойства скорее всего возникли независимо при эволюции больших РНК-геномов.

Текст статьи

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

captcha

Благодарности

Автор выражает признательность проф. А.Г. Соловьеву и проф. С.Ю. Морозову за обсуждение и критические замечания по тексту настоящего обзора.

Конфликт интересов

Автор заявляет об отсутствии конфликта интересов.

Соблюдение этических норм

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

Список литературы

1. Koonin, E. V., and Dolja, V. V. (1993) Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences, Crit. Rev. Biochem. Mol. Biol., 28, 375-430, doi: 10.3109/10409239309078440.

2. Steinhauer, D. A., and Holland, J. (1987) Rapid evolution of RNA viruses, Annu. Rev. Microbiol., 41, 409-431, doi: 10.1146/annurev.mi.41.100187.002205.

3. Drake, J. W. (1993) Rates of spontaneous mutation among RNA viruses, Proc. Natl. Acad. Sci. USA, 90, 4171-4175.

4. Holmes, E. C. (2003) Error thresholds and the constraints to RNA virus evolution, Trends Microbiol., 11, 543-546.

5. Dolja, V. V., Karasev, A. V., and Koonin, E. V. (1994) Molecular biology and evolution of closteroviruses: sophisticated build-up of large RNA genomes, Annu. Rev. Phytopathol., 32, 261-285.

6. Saberi, A., Gulyaeva, A. A., Brubacher, J. L., Newmark, P. A., and Gorbalenya, A. E. (2018) A planarian nidovirus expands the limits of RNA genome size, PLoS Pathog., 14, e1007314, doi: 10.1371/journal.ppat.1007314.

7. Agranovsky, A. A., Koonin, E. V., Boyko, V. P., Maiss, E., Froetschl, R., Lunina, N. A., and Atabekov, J. G. (1994) Beet yellows closterovirus: complete genome structure and identification of a leader papain-like thiol protease, Virology, 198, 311-324, doi: 10.1006/viro.1994.1034.

8. Karasev, A. V., Boyko, V. P., Gowda, S., Nikolaeva, O. V., Hilf, M. E., et al. (1995) Complete sequence of the citrus tristeza virus RNA genome, Virology, 208, 511-520, doi: 10.1006/viro.1995.1182.

9. Enjuanes, L., Gorbalenya, A. E., de Groot, R. J., Cowley, J. A., Ziebuhr, J., and Snijder, E. J. (2008) Nidovirales, in Encyclopedia of Virology (Mahy, B. W. J., and Van Regenmortel, M. H. V., eds) Oxford, Elsevier, pp. 419-430.

10. Koonin, E. V., Dolja, V. V., Krupovic, M., Varsani, A., Wolf, Y. I., et al. (2020) Global organization and proposed megataxonomy of the virus world, Microbiol. Mol. Biol. Rev., 84, e00061-19, doi: 10.1128/MMBR.00061-19.

11. Sawicki, S. G., and Sawicki, D. L. (2005) Coronavirus transcription: a perspective, Curr. Top. Microbiol. Immunol., 287, 31-55, doi: 10.1007/3-540-26765-4_2.

12. Sola, I., Almazán, F., Zúńiga, S., and Enjuanes, L. (2015) Continuous and discontinuous RNA synthesis in coronaviruses, Annu. Rev. Virol., 2, 265-288, doi: 10.1146/annurev-virology-100114-055218.

13. Zuńiga, S., Cruz, J. L., Sola, I., Mateos-Gomez, P. A., Palacio, L., and Enjuanes, L. (2010) Coronavirus nucleocapsid protein facilitates template switching and is required for efficient transcription, J. Virol., 84, 2169-2175.

14. Wu, C. H., Chen, P. J., and Yeh, S. H. (2014) Nucleocapsid phosphorylation and RNA helicase DDX1 recruitment enables coronavirus transition from discontinuous to continuous transcription, Cell Host Microbe, 16, 462-72.

15. Terada, Y., Kawachi, K., Matsuura, Y., and Kamitani, W. (2017) MERS coronavirus nsp1 participates in an efficient propagation through a specific interaction with viral RNA, Virology, 511, 95-105, doi: 10.1016/j.virol.2017.08.026.

16. Lokugamage, K. G., Narayanan, K., Huang, C., and Makino, S. (2012) Severe acute respiratory syndrome coronavirus protein nsp1 is a novel eukaryotic translation inhibitor that represses multiple steps of translation initiation, J. Virol., 86, 13598-13608, doi: 10.1128/JVI.01958-12.

17. Nakagawa, K., Narayanan, K., Wada, M., Popov, V. L., Cajimat, M., Baric, R. S., and Makino, S. (2018) The endonucleolytic RNA cleavage function of nsp1 of middle east respiratory syndrome coronavirus promotes the production of infectious virus particles in specific human cell lines, J. Virol., 92, e01157-18, doi: 10.1128/JVI.01157-18.

18. Graham, R. L., Sims, A. C., Brockway, S. M., Baric, R. S., and Denison, M. R. (2005) The nsp2 replicase proteins of murine hepatitis virus and severe acute respiratory syndrome coronavirus are dispensable for viral replication, J. Virol., 79, 13399-13411, doi: 10.1128/JVI.79.21.13399-13411.2005.

19. Sawicki, S. G., Sawicki, D. L., Younker, D., Meyer, Y., Thiel, V., Stokes, H., and Siddell, S. G. (2005) Functional and genetic analysis of coronavirus replicase-transcriptase proteins, PLoS Pathog., 1, e39, doi: 10.1371/journal.ppat.0010039.

20. Angelini, M. M., Akhlaghpour, M., Neuman, B. W., and Buchmeier, M. J. (2013) Severe acute respiratory syndrome coronavirus nonstructural proteins 3, 4, and 6 induce double-membrane vesicles, MBio, 4, e00524-e00513.

21. de Wilde, A. H., Snijder, E. J., Kikkert, M., and van Hemert, M. J. (2018) Host factors in coronavirus replication, Curr. Top. Microbiol. Immunol., 419, 1-42, doi: 10.1007/82_2017_25.

22. Knoops, K., Kikkert, M., Worm, S. H., Zevenhoven-Dobbe, J. C., van der Meer, Y., et al. (2008) SARS-corona-virus replication is supported by a reticulovesicular network of modified endoplasmic reticulum, PLoS Biol., 6, e226, doi: 10.1371/journal.pbio.0060226.

23. Te Velthuis, A. J., van den Worm, S. H., and Snijder, E. J. (2012) The SARS-coronavirus nsp7+nsp8 complex is a unique multimeric RNA polymerase capable of both de novo initiation and primer extension, Nucleic Acids Res, 40, 1737-1747, doi: 10.1093/nar/gkr893.

24. Kirchdoerfer, R. N., and Ward, A. B. (2019) Structure of the SARS-CoV nsp12 polymerase bound to nsp7 and nsp8 co-factors, Nat. Commun., 10, 2342. doi: 10.1038/s41467-019-10280-3.

25. Bouvet, M., Imbert, I., Subissi, L., Gluais, L., Canard, B., and Decroly, E. (2012) RNA 3′-end mismatch excision by the severe acute respiratory syndrome coronavirus nonstructural protein nsp10/nsp14 exoribonuclease complex, Proc. Natl. Acad. Sci. USA, 109, 9372-9377, doi: 10.1073/pnas.1201130109.

26. Subissi, L., Posthuma, C. C., Collet, A., Zevenhoven-Dobbe, J. C., Gorbalenya, A. E., et al. (2014) One severe acute respiratory syndrome coronavirus protein complex integrates processive RNA polymerase and exonuclease activities, Proc. Natl. Acad. Sci. USA, 111, E3900-9, doi: 10.1073/pnas.1323705111.

27. Jin, X., Chen, Y., Sun, Y., Zeng, C., Wang, Y., et al. (2013) Characterization of the guanine-N7 methyltransferase activity of coronavirus nsp14 on nucleotide GTP, Virus Res., 176, 45-52, doi: 10.1016/j.virusres.2013.05.001.

28. Ivanov, K. A., Hertzig, T., Rozanov, M., Bayer, S., Thiel, V., Gorbalenya, A. E., and Ziebuhr, J. (2004) Major genetic marker of nidoviruses encodes a replicative endoribonuclease, Proc. Natl. Acad. Sci. USA, 101, 12694-12699, doi: 10.1073/pnas.0403127101.

29. Chen, Y., Cai, H., Pan, J., Xiang, N., Tien, P., Ahola, T., and Guo, D. (2009) Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase, Proc. Natl. Acad. Sci. USA, 106, 3484-3489.

30. Daffis, S., Szretter, K. J., Schriewer, J., Li, J., Youn, S., et al. (2010) 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members, Nature, 468, 452-456, doi: 10.1038/nature09489.

31. Kalicharran, K., Mohandas, D., Wilson, G., and Dales, S. (1996) Regulation of the initiation of coronavirus JHM infection in primary oligodendrocytes and L-2 fibroblasts, Virology, 225, 33-43, doi: 10.1006/viro.1996.0572.

32. Wolff, G., Ronald, W., Limpens R., Zevenhoven-Dobbe, J. C., Laugks, U., et al. (2020) A molecular pore spans the double membrane of the coronavirus replication organelle, Science, 369, 1395-1398, doi: 10.1126/science.abd3629.

33. Agranovsky, A. A. (1996) Principles of molecular organization, expression and evolution of closteroviruses: over the barriers, Adv. Virus Res., 47, 119-158.

34. Agranovsky A. A. (2016) Closteroviruses: molecular biology, evolution and interactions with cells, in Plant Viruses: Evolution and Management (Gaur, R. K., Petrova, N., and Stoyanova, M. I., eds) Springer Science+Business Media, Singapore, Chapt. 14, pp. 231-252, doi: 10.1007/978-981-10-1406-2_14.

35. Agranovsky, A. A., Boyko, V. P., Karasev, A. V., Lunina, N. A., Koonin, E. V., and Dolja, V. V. (1991) Nucleotide sequence of the 3′-terminal half of beet yellows closterovirus RNA genome: unique arrangement of eight virus genes, J. Gen. Virol., 72, 15-23.

36. Firth, A. E., Brierley, I. (2012) Non-canonical translation in RNA viruses, J. Gen. Virol., 93, 1385-1409, doi: 10.1099/vir.0.042499-0.

37. Giedroc, D. P., and Cornish, P. V. (2009) Frameshifting RNA pseudoknots: structure and mechanism, Virus Res., 139, 193-208.

38. Peremyslov, V. V., Hagiwara, Y., and Dolja, V. V. (1998) Genes required for replication of the 15.5-kilobase RNA genome of a plant closterovirus, J. Virol., 72, 5870-5876.

39. Peng, C. W., Napuli, A. J., and Dolja, V.V. (2003) Leader proteinases of beet yellows virus functions in long-distance transport, J. Virol., 77, 2843-2849.

40. Erokhina, T. N., Zinovkin, R. A., Vitushkina, M. V., Jelkmann, W., and Agranovsky, A. A. (2000) Detection of beet yellows closterovirus methyltransferase-like and helicase-like proteins in vivo using monoclonal antibodies, J. Gen. Virol., 81, 597-603.

41. Agranovsky, A. A., Lesemann, D. E., Maiss, E., Hull, R. and Atabekov, J. G. (1995) “Rattlesnake” structure of a filamentous plant RNA virus built of two capsid proteins, Proc. Natl. Acad. Sci. USA, 92, 2470-2473.

42. Zinovkin, R. A., Jelkmann, W., and Agranovsky, A. A. (1999) The minor coat protein of beet yellows closterovirus encapsidates the 5′-terminus of RNA in virions, J. Gen. Virol., 80, 269-272.

43. Napuli, A. J., Alzhanova, D. V., Doneanu, C. E., Barofsky, D. F., Koonin, E. V., and Dolja, V. V. (2003) The 64-kDa capsid protein homolog of beet yellows virus is required for assembly of virion tails, J. Virol., 77, 2377-2384.

44. Napuli, A. J., Falk, B. W., and Dolja, V. V. (2000). Interaction between HSP70 homolog and filamentous virions of the beet yellows virus, Virology, 274, 232-239.

45. Alzhanova, D. V., Napuli, A., Creamer, R., and Dolja, V. V. (2001) Cell-to-cell movement and assembly of a plant closterovirus: roles for the capsid proteins and Hsp70 homolog, EMBO J., 20, 6997-7007.

46. Agranovsky, A. A., Boyko, V. P., Karasev, A. V., Koonin, E. V., and Dolja, V. V. (1991) The putative 65K protein of beet yellows closterovirus is a homologue of HSP70 heat shock proteins, J. Mol. Biol., 217, 603-610.

47. Agranovsky, A. A., Folimonova, S. Y., Folimonov, A. S., Denisenko, O. N., and Zinovkin, R. A. (1997) The beet yellows closterovirus p65 homologue of HSP70 chaperones has ATPase activity associated with its conserved N-terminal domain but does not interact with unfolded protein chains, J. Gen. Virol., 78, 535-542.

48. Medina, V., Peremyslov, V. V., Hagiwara, Y., and Dolja, V. V. (1999) Subcellular localization of the HSP70-homolog encoded by beet yellows closterovirus, Virology, 260, 173-181.

49. Agranovsky, A. A., Folimonov, A. S., Folimonova, S. Y., Morozov, S. Y., Schiemann, J., Lesemann, D. E., and Atabekov, J. G. (1998) Beet yellows closterovirus HSP70-like protein mediates the cell-to-cell movement of a potexvirus transport-deficient mutant and a hordeivirus-based chimeric virus, J. Gen. Virol., 79, 889-895.

50. Alzhanova, D. V., Hagiwara, Y., Peremyslov, V. V., and Dolja, V. V. (2000) Genetic analysis of the cell-to-cell movement of beet yellows closterovirus, Virology, 268, 192-200.

51. Dolja, V. V., Kreuze, J. F., and Valkonen, J. P. (2006) Comparative and functional genomics of closteroviruses, Virus Res., 117, 38-51.

52. Goldbach, R., Le Gall, O., and Wellink, J. (1991) Alpha-like viruses of plants, Semin. Virol., 2,19-25.

53. Buck, K. W. (1996) Comparison of the replication of positive-stranded RNA viruses of plants and animals, Adv. Virus Res., 47, 159-251, doi: 10.1016/s0065-3527(08)60736-8.

54. Miller, W. A., and Koev, G. (2000) Synthesis of subgenomic RNAs by positive strand RNA viruses, Virology, 273, 1-8.

55. Agranovsky, A. A., Koenig, R., Maiss, E., Boyko, V. P., Casper, R., and Atabekov, J. G. (1994) Expression of the beet yellows closterovirus capsid protein and p24, a capsid protein homologue, in vitro and in vivo, J. Gen. Virol., 75, 1431-1439.

56. Karasev, A. V., Hilf, M. E., Garnsey, S. M., and Dawson, W. O. (1997) Transcriptional strategy of closteroviruses: mapping the 5′ termini of the citrus tristeza virus subgenomic RNAs, J. Virol., 71, 6233-6236.

57. Peremyslov, V. V., and Dolja, V. V. (2002) Identification of the subgenomic mRNAs that encode 6-kDa movement protein and Hsp70 homolog of beet yellows virus, Virology, 295, 299-306.

58. Vitushkina, M. V., Rogozin, I. B., Jelkmann, W., Koonin, E. V., and Agranovsky, A. A. (2007) Completion of the mapping of transcription start sites for the five-gene block subgenomic RNAs of beet yellows closterovirus and identification of putative subgenomic promoters, Virus Res., 128, 153-158.

59. Cronshaw, J., Hoefert, L., and Esau, K. (1966) Ultrastructural features of beta leaves infected with beet yellows virus, J. Cell. Biol., 31, 429-443.

60. Gushchin, V. A., Solovyev, A. G., Erokhina, T. N., Morozov, S. Y., and Agranovsky, A. A. (2013) Beet yellows virus replicase and replicative compartments: parallels with other RNA viruses, Front. Microbiol., 4, 38, doi: 10.3389/fmicb.2013.00038.

61. Erokhina, T. N., Vitushkina, M. V., Zinovkin, R. A., Lesemann, D. E., Jelkmann, W., Koonin, E. V., and Agranovsky, A. A. (2001) Ultrastructural localisation and epitope mapping of beet yellows closterovirus methyltransferase-like and helicase-like proteins, J. Gen. Virol., 82, 1983-1994.

62. Zinovkin, R. A., Erokhina, T. N., Lesemann, D. E., Jelkmann, W., and Agranovsky, A. A. (2003) Processing and subcellular localization of the leader papain-like proteinase of beet yellows closterovirus, J. Gen. Virol., 84, 2265-2270.

63. Gushchin V. A., Karlin, D. G., Makhotenko, A. V., Khromov, A. V., Erokhina T. N., et al. (2017) A conserved region in the Closterovirus 1a polyprotein drives extensive remodeling of endoplasmic reticulum membranes and induces motile globules in Nicotiana benthamiana cells, Virology, 506, 106-113, doi: 10.1016/j.virol.2016.12.006.

64. Godeny, E. K., Chen, L., Kumar, S., Methven, S. L., Koonin, E. V., and Brinton, M. A. (1993) Complete genome sequence and phylogenie analysis of the lactate dehydrogenase-elevating virus (LDV), Virology, 194,585-96.

65. Simmonds, P. (2020) Rampant C/U hypermutation in the genomes of SARS-CoV-2 and other coronaviruses: causes and consequences for their short- and long-term evolutionary trajectories, mSphere, 5, e00408-20, doi: 10.1128/mSphere.00408-20.

66. Bentley, K., and Evans, D. J. (2018) Mechanisms and consequences of positive-strand RNA virus recombination, J. Gen. Virol., 99, 1345-1356, doi: 10.1099/jgv.0.001142.

67. Zeng, Q., Langereis, M. A., van Vliet A. L., Huizinga, E. G., and de Groot, R. J. (2008) Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution, Proc. Natl. Acad. Sci. USA, 105, 9065-9069, doi: 10.1073/pnas.0800502105.

68. Harper, S. J. (2013) Citrus tristeza virus: evolution of complex and varied genotypic groups, Front. Microbiol., 4, 9310, doi: 10.3389/fmicb.2013.00093.