Preview

Proceedings of the National Academy of Sciences of Belarus, Medical series

Advanced search

Biochemical features of parvovirus B19 genovariant 1a2 dominating during the incidence rise in Belarus

https://doi.org/10.29235/1814-6023-2020-17-2-211-220

Abstract

Two genovariants (1a1 and 1a2) are distinguished among Human parvovirus B19 (B19P) of subgenotype 1a, of which 1a2 was predominantly distributed during the incidence rise in Belarus. The aim of this study was a comparative analysis of the amino acid variability and of the mutational pressure directions in different parts of the genome between genovariants 1a1 and 1a2.

The analysis of the consensus amino acid sequences of two genovariants and the three-dimensional structure models of protein fragments was carried out. In total, two unique amino acid substitutions in the main non-structural protein NS1 of 1a2 were found (I181M and E114G), one of which E114G is close to the DNA-binding domain (OBD) responsible for attachment to the replication origin site and can affect the rate of virus replication and transcription. Three unique amino acid substitutions were found in the structural polypeptide VP of 1a2: V30L, S98N, and N533S. Two of them are located in the most immunogenic region VP1u and can contribute to the escape from immune response. The investigation of the mutational pressure direction revealed a decrease in the frequency of G to T transversions in the second reading frame of 1a2, which reflects a higher transcription rate as a result of amino acid substitution in the OBD protein.

The differences revealed between the genetic variants of subgenotype 1a B19P both in the antigenic sites and in the replication and transcription system can provide an increased “fitness” for the genetic variant 1a2 and explain its predominant distribution during the incidence rise.

About the Authors

M. A. Yermalovich
Republican Research and Practical Center for Epidemiology and Microbiology
Belarus

Marina A. Yermalovich – Ph. D. (Med.), Leading researcher

23, Filimonov Str., 220114, Minsk



V. V. Khrustalev
Belarusian State Medical University
Belarus

Vladislav V. Khrustalev – Ph. D. (Biol.), Associate Professor, Head of the Department

83, Dzerzhinski Ave., 220116, Minsk



T. A. Khrustaleva
Institute of Physiology of the National Academy of Sciences of Belarus
Belarus

Tatyana A. Khrustaleva – Ph. D. (Biol.), Senior researcher

28, Akademicheskaya Str., 220072, Minsk



V. V. Poboinev
Belarusian State Medical University
Belarus

Victor V. Poboinev – Master of Med. Sci., Postgraduate student

83, Dzerzhinski Ave., 220116, Minsk



E. O. Samoilovich
Republican Research and Practical Center for Epidemiology and Microbiology
Belarus

Elena O. Samoilovich – D. Sc. (Med.), Professor, Head of the Laboratory

23, Filimonov Str., 220114, Minsk



References

1. Cotmore S. F., Agbandje-McKenna M., Chiorini J. A., Gatherer D., Mukha D. V., Pintel D. J., Qiu J., SoderlundVenermo M., Tattersall P., Tijssen P. Rationalization and extension of the taxonomy of the family Parvoviridae. ICTV official taxonomy: Updates since the 8th Report, code 2013.001a-aaaV. International Committee on Taxonomy of Viruses (ICTV). Washington, 2013. 65 р.

2. Heegaard E. D., Brown K. E. Human parvovirus B19. Clinical Microbiology Reviews, 2002, vol. 15, no. 3, pp. 485–505. https://doi.org/10.1128/cmr.15.3.485-505.2002

3. Tu M., Liu F., Chen Sh., Wang M., Cheng A. Role of capsid proteins in parvoviruses infection. Virology Journal, 2015, vol. 12, art. 114. https://doi.org/10.1186/s12985-015-0344-y

4. Cotmore S. F., Agbandje-McKenna M., Canuti M., Chiorini J. A., Eis-Hubinger A. M., Hughes J. [et al.]. ICTV Virus Taxonomy Profile: Parvoviridae. ICTV Report Consortium. Journal of General Virology, 2019, vol. 100, no. 3, pp. 367–368. https://doi.org/10.1099/jgv.0.001212

5. Dong Y., Huang Y., Wang Y., Xu P., Yang Y., Liu K., Tijssen P., Peng J., Li Y. The effects of the 11 kDa protein and the putative X protein on the p6 promoter activity of parvovirus B19 in Hela cells. Virus Genes, 2013, vol. 46, no. 1, pp. 167–169. https://doi.org/10.1007/s11262-012-0839-1

6. Bonvicini F., Filippone C., Delbarba S., Manaresi E., Zerbini M., Musiani M., Gallinella G. Parvovirus B19 genome as a single, two-state replicative and transcriptional unit. Virology, 2006, vol. 347, no. 2, pp. 447–454. https://doi.org/10.1016/j. virol.2005.12.014

7. Bonvicini F., Filippone C., Manaresi E., Zerbini M., Musiani M., Gallinella G. Functional analysis and quantitative determination of the expression profile of human parvovirus B19. Virology, 2008, vol. 381, no. 2, pp. 168–177. https://doi.org/10.1016/j.virol.2008.09.002

8. Zhi N., Mills I. P., Lu J., Wong S., Filippone C., Brown K. E. Molecular and functional analyses of a human parvovirus B19 infectious clone demonstrates essential roles for NS1, VP1, and the 11-kilodalton protein in virus replication and infectivity. Journal of Virology, 2006, vol. 80, no. 12, pp. 5941–5950. https://doi.org/10.1128/JVI.02430-05

9. Morita E., Nakashima A., Asao H., Sato H., Sugamura K. Human parvovirus B19 nonstructural protein (NS1) induces cell cycle arrest at G(1) phase. Journal of Virology, 2003, vol. 77, no. 5, pp. 2915–2921. https://doi.org/10.1128/jvi.77.5.2915- 2921.2003

10. Wan Z., Zhi N., Wong S., Keyvanfar K., Liu D., Raghavachari N. [et al.]. Human parvovirus B19 causes cell cycle arrest of human erythroid progenitors via deregulation of the E2F family of transcription factors. Journal of Clinical Investigation, 2010, vol. 120, no. 10, pp. 3530–3544. https://doi.org/10.1172/JCI41805

11. Kaufmann B., Simpson A. A., Rossmann M. G. The structure of human parvovirus B19. Proceedings of the National Academy of Sciences of the United States of America, 2004, vol. 101, no. 32, pp. 11628–11633. https://doi.org/10.1073/pnas.0402992101

12. Dorsch S., Kaufmann B., Schaible U., Prohaska E., Wolf H., Modrow S. The VP1-unique region of parvovirus B19: amino acid variability and antigenic stability. Journal of General Virology, 2001, vol. 82, no. 1, pp. 191–199. https://doi.org/10.1099/0022-1317-82-1-191

13. Anderson S., Momoeda M., Kawase M., Kajigaya S., Young N. S. Peptides derived from the unique region of B19 parvovirus minor capsid protein elicit neutralizing antibodies in rabbits. Virology, 1995, vol. 206, no. 1, pp. 626–632. https://doi.org/10.1016/s0042-6822(95)80079-4

14. Zuffi E., Manaresi E., Gallinella G., Gentilomi G. A., Venturoli S., Zerbini M., Musiani M. Identification of immunodominant peptide in the parvovirus B19 VP1 unique region able to elicit a long-lasting immune response in humans. Viral Immunology, 2001, vol. 14, no. 2, pp. 151–158. https://doi.org/10.1089/088282401750234529

15. Zádori Z., Szelei J., Lacoste M. C., Li Y., Gariépy S., Raymond P., Allaire M., Nabi I. R., Tijssen P. A viral phospholipase A2 is required for parvovirus infectivity. Developmental Cell, 2001, vol. 1, pp. 291–302. https://doi.org/10.1016/s1534-5807(01)00031-4

16. Filippone C., Zhi N., Wong S., Lu J., Kajigaya S., Gallinella G., Kakkola L., Söderlund-Venermo M., Young N. S., Brown K. E. VP1u phospholipase activity is critical for infectivity of full-length parvovirus B19 genomic clones. Virology, 2008, vol. 374, no. 2, pp. 444–452. https://doi.org/10.1016/j.virol.2008.01.002

17. Deng X., Dong Y., Yi Q., Huang Y., Zhao D., Yang Y., Tijssen P., Qiu J., Liu K., Li Y. The determinants for the enzyme activity of human parvovirus B19 phospholipase A2 (PLA2) and its influence on cultured cells. PLoS ONE, 2013, vol. 8, no. 4, p. e61440. https://doi.org/10.1371/journal.pone.0061440

18. Kaufmann B., Chipman P. R., Kostyuchenko V. A., Modrow S., Rossmann M. G. Visualization of the externalized VP2 N termini of infectious human parvovirus B19. Journal of Virology, 2008, vol. 82, no. 15, pp. 7306–7312. https://doi.org/10.1128/JVI.00512-08

19. Servant A., Laperche S., Lallemand F., Marinho V., De Saint Maur G., Meritet J. F., Garbarg-Chenon A. Genetic diversity within human erythroviruses: identification of three genotypes. Journal of Virology, 2002, vol. 76, no. 18, pp. 9124– 9134. https://doi.org/10.1128/jvi.76.18.9124-9134.2002

20. Toan N. L., Duechting A., Kremsner P. G., Song L. H., Ebinger M., Aberle S. [et al.]. Phylogenetic analysis of human parvovirus B19, indicating two subgroups of genotype 1 in Vietnamese patients. Journal of General Virology, 2006, vol. 87, no. 10, pp. 2941–2949. https://doi.org/10.1099/vir.0.82037-0

21. Parsyan A., Szmaragd C., Allain J.-P., Candotti D. Identification and genetic diversity of two human parvovirus B19 genotype 3 subtypes. Journal of General Virology, 2007, vol. 88, no. 2, pp. 428–431. https://doi.org/10.1099/vir.0.82496-0

22. Ivanova S. K., Mihneva Z. G., Toshev A. K., Kovaleva V. P., Andonova L. G., Muller C. P., Hübschen J. M. Insights into epidemiology of human parvovirus B19 and detection of an unusual genotype 2 variant, Bulgaria, 2004 to 2013. Eurosurveillance, 2016, vol. 21, no. 4, pii 30116. https://doi.org/10.2807/1560-7917.ES.2016.21.4.30116

23. Molenaar-de Backer M. W. A., Lukashov V. V., van Binnendijk R. S., Boot H. J., Zaaijer H. L. Global co-existence of two evolutionary lineages of parvovirus B19 1a, different in genome-wide synonymous positions. PLoS ONE, 2012, vol. 7, no. 8, p. e43206. https://doi.org/10.1371/journal.pone.0043206

24. Slavov S. N., Haddad S. K., Silva-Pinto A. C., Amarilla A. A., Alfonso H. L., Aquino V. H., Covas D. T. Molecular and phylogenetic analyses of human parvovirus B19 isolated from Brazilian patients with sickle cell disease and β-thalassemia major and healthy blood donors. Journal of Medical Virology, 2012, vol. 84, no. 10, pp. 1652–1665. https://doi.org/10.1002/jmv.23358

25. Yermalovich M. A., Hübschen J. M., Semeiko G. V., Samoilovich E. O., Muller C. P. Human parvovirus B19 surveillance in patients with rash and fever from Belarus. Journal of Medical Virology, 2012, vol. 84, no. 6, pp. 973–978. https://doi.org/10.1002/jmv.23294

26. Ermolovich M. A., Semeiko G. V., Samoilovich E. O. Genetic variants of parvovirus B19 circulating in Belarus during the epidemic cycle of infection (2005–2016). Vestsi Natsyyanal’nai akademii navuk Belarusi. Seriya meditsinskikh navuk = Proceedings of the National Academy of Sciences of Belarus. Medical series, 2019, vol. 16, no. 1, pp. 35–45 (in Russian).

27. Waterhouse A., Bertoni M., Bienert S., Studer G., Tauriello G., Gumienny R. [et al.]. Swiss-model: homology modelling of protein structures and complexes. Nucleic Acids Research, 2018, vol. 46, no. W1, pp. W296–W303. https://doi.org/10.1093/nar/gky427

28. Hwang S., Gou Z., Kuznetsov I. B. DP-Bind: a web server for sequence-based prediction of DNA-binding residues in DNA-binding proteins. Bioinformatics, 2007, vol. 23, no. 5, pp. 634–636. https://doi.org/10.1093/bioinformatics/btl672

29. Khrustalev V. V., Ermalovich M. A., Hübschen J. M., Khrustaleva T. A. Transcription-associated mutational pressure in the parvovirus B19 genome: reactivated genomes contribute to the variability of viral populations. Journal of Theoretical Biology, 2017, vol. 435, pp. 199–207. https://doi.org/10.1016/j.jtbi.2017.09.019

30. Khrustalev V. V., Khrustaleva T. A., Poboinev V. V. Amino acid content of beta strands and alpha helices depends on their flanking secondary structure elements. Biosystems, 2018, vol. 168, pp. 45–54. https://doi.org/10.1016/j.biosystems.2018.04.002

31. Musayev F. N., Zarate-Perez F., Bardelli M., Bishop C., Saniev E. F., Linden R. M., Henckaerts E., Escalante C. R. Structural studies of AAV2 Rep68 reveal a partially structured linker and compact domain conformation. Biochemistry, 2015, vol. 54, no. 38, pp. 5907–5919. https://doi.org/10.1021/acs.biochem.5b00610

32. Gros L., Saparbaev M. K., Laval J. Enzymology of the repair of free radicals-induced DNA damage. Oncogene, 2002, vol. 21, no. 58, pp. 8905–8925. https://doi.org/10.1038/sj.onc.1206005

33. Weger S., Wistuba A., Grimm D., Kleinschmidt J. A. Control of adeno-associated virus type 2 cap gene expression: relative influence of helper virus, terminal repeats, and rep proteins. Journal of Virology, 1997, vol. 71, no. 11, pp. 8437–8447. https://doi.org/10.1128/jvi.71.11.8437-8447.1997

34. Weger S., Wendland M., Kleinschmidt J. A., Heilbronn R. The adeno-associated virus type 2 regulatory proteins rep78 and rep68 interact with the transcriptional coactivator PC4. Journal of Virology, 1999, vol. 73, no. 1, pp. 260–269. https://doi.org/10.1128/jvi.73.1.260-269.1999

35. Doerig C., Hirt B., Antonietti J. P., Beard P. Nonstructural protein of parvoviruses B19 and minute virus of mice controls transcription. Journal of Virology, 1990, vol. 64, no. 1, pp. 387–396. https://doi.org/10.1128/jvi.64.1.387-396.1990

36. Raab U., Beckenlehner K., Lowin T., Niller H. H., Doyle S., Modrow S. NS1 protein of parvovirus B19 interacts directly with DNA sequences of the P6 promoter and with the cellular transcription factors Sp1/Sp3. Virology, 2002, vol. 293, no. 1, pp. 86–93. https://doi.org/10.1006/viro.2001.1285


Review

For citations:


Yermalovich M.A., Khrustalev V.V., Khrustaleva T.A., Poboinev V.V., Samoilovich E.O. Biochemical features of parvovirus B19 genovariant 1a2 dominating during the incidence rise in Belarus. Proceedings of the National Academy of Sciences of Belarus, Medical series. 2020;17(2):211-220. (In Russ.) https://doi.org/10.29235/1814-6023-2020-17-2-211-220

Views: 601


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 1814-6023 (Print)
ISSN 2524-2350 (Online)