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Журнал микробиологии, эпидемиологии и иммунобиологии. 2020; 97: 216-226

Тетрануклеотидный профиль герпесвирусных ДНК

Филатов Феликс Петрович, Шаргунов Александр Валерьевич

https://doi.org/10.36233/0372-9311-2020-97-3-3

Аннотация

Введение. Герпесвирусные ДНК (около 90% всех полногеномных последовательностей семейства Herpesvirales, представленных в GenBank) содержат в минимальной концентрации один из двух тетрануклеотидов — CTAG или TCGA. «Недопредставленность» CTAG ранее наблюдалась только в ДНК некоторых бактерий и фагов. Ранее выявленная «недопредставленность» метилируемого димера CpG находит свое выражение в низкой концентрации TCAG в ДНК герпесвирусов.

Цель работы — продолжение анализа формальных характеристик герпесвирусных ДНК, а также сопоставление их с плотностью ДНК-микрогомологий вирус/хозяин и с геномной макроструктурой герпесвирусов.

Материалы и методы. Проанализированы по 20 штаммов и изолятов каждого из пяти типов вирусов герпеса человека (HHV1, HHV2, HHV3, HHV4, HHV5), 10 штаммов HHV8, 5 штаммов HHV6A, 4 штамма HHV6B и 3 штамма HHV7. Для определения частоты тетрануклеотидов использовали инструменты GenBank, а для сравнения — фрагменты ДНК человека размером с ДНК герпесвирусов.

Результаты. Минимальная концентрация CTAG в ДНК герпесвирусов в основном характерна для двух- и односегментных геномов с прямыми или инвертированными концевыми повторами (классов A, D и E), тогда как минимальная плотность TCGA — главным образом для значительно менее структурированной ДНК (классов B, C и F). По нарастанию плотности CTAG геномы герпесвирусов человека образуют последовательность, близкую к последовательности 20 нт-гомологий ДНК герпесвирус/человек, организованной по нарастанию плотности, что также коррелирует с макроструктурой ДНК. Параллель этой минимизации со структурой ДНК вирусов герпеса или с их принадлежностью к тому или иному подсемейству в литературе не отмечена. Хотя герпесвирусные ДНК довольно велики (125–295 Кб), некоторые из них (например, ДНК HHV4, HHV5 и HHV7) демонстрируют заметные отклонения от второго правила четности ДНК и, таким образом, могут служить компонентом вирусных молекулярных сигнатур.

В Обсуждении предлагаются возможные гипотезы происхождения некоторых из отмеченных явлений.

Список литературы

1. Whitley R., Kimberlin D., Prober C. Pathogenesis and disease. In: Arvin A., Campadelli-Fiume G., Mocarsky E., Moore P.S., Roizman B., Whitley R., eds. Human Herpesviruses: Biology, Therapy and Immunoprophylaxis. Chapter 32. Cambridge: Cambridge University Press; 2007.

2. Pellett P., Roizman B. Herpesviridae. In: Knipe D.M., Howley P.M., eds. Fields Virology. Philadelphia: Lippincott Williams & Wilkins; 2013: 1802-2.

3. Zabolotneva A., Tkachev V., Filatov F., Buzdin A. How many antiviral small interfering RNAs may be encoded by the mammalian genomes? Biol. Direct. 2010; 5: 62. DOI: http://doi.org/10.1186/1745-6150-5-62

4. Filatov F., Shargunov A. Short nucleotide sequences in herpesviral genomes identical to the human DNA. J. Theor. Biol. 2015; 372: 12-21. DOI: http://doi.org/10.1016/j.jtbi.2015.02.019

5. Filatov F., Shargunov A. Microhomology of Viral/Host DNAs and macrostructure of herpesviral genome. Int. J. Virol. AIDS. 2018; 5(1): 042. DOI: http://doi.org/10.23937/2469-567X/1510042

6. Rudner R., Karkas J.D., Chargaff E. Separation of B. subtilis DNA into complementary strands, 3. Direct Analysis. Proc. Natl. Acad. Sci. USA. 1968; 60(3): 921-2. DOI: http://doi.org/10.1073/pnas.60.3.921

7. Forsdyke D.R. Symmetry observations in long nucleotide sequences: a commentary on the discovery note of Qi and Cuticchia. Bioinformatics. 2002; 18(1): 215-7. DOI: http://doi.org/10.1093/bioinformatics/18.1.215

8. Albrecht-Buehler G. Asymptotically increasing compliance of genomes with Chargaff’s second parity rules through inversions and inverted transpositions. Version 2. Proc. Natl. Acad. Sci. USA. 2006; 103(47): 17828-33. DOI: http://doi.org/10.1073/pnas.0605553103

9. Baisnee P.F., Hampson S., Baldi P. Why are complementary strands symmetric? BioInformatics. 2002; 18(8): 1021‐33. DOI: http://doi.org/10.1093/bioinformatics/18.8.1021

10. Gori F., Mavroeidis D., Jetten M.S.M., Marchiori E. The importance of Chargaff’s second parity rule for genomic signatures in metagenomics. Available at: http://www.biorxiv.org/content/biorxiv/early/2017/06/04/146001.full.pdf

11. Pride D.T., Blaser M.J. Identification of horizontally acquired genetic elements in Helicobacter pylori and other prokaryotes using oligonucleotide difference analysis. Genome Lett. 2002; 1(1): 2-15. DOI: http://doi.org/doi.org/10.1166/gl.2002.003

12. Prabhu V.V. Symmetry observations in long nucleotide sequences. Nucleic Acids Res. 1993; 21(12): 2797‐800. DOI: http://doi.org/10.1093/nar/21.12.2797

13. Albrecht-Buehler G. The three classes of triplet profiles of natural genomes. Genomics. 2007; 89(5): 596‐601. DOI: http://doi.org/10.1016/j.ygeno.2006.12.009

14. Zhang S.H., Wang L. A novel common triplet profile for GCrich prokaryotic genomes. Genomics. 2011; 97(5): 330‐1. DOI: http://doi.org/10.1016/j.ygeno.2011.02.005

15. Burge C., Campbell A.M., Karlin S. Over- and under-representation of short oligonucleotides in DNA sequences. Proc. Natl. Acad. Sci. USA. 1992; 89(4): 1358-62. DOI: http://doi.org/10.1073/pnas.89.4.1358

16. Tang L., Zhu S., Mastriani E., Fang X., Zhou Y.J., Li Y.G., et al. Conserved intergenic sequences revealed by CTAG-profiling in Salmonella: thermodynamic modeling for function prediction. Sci. Rep. 2017; 7: 43565. DOI: http://doi.org/10.1038/srep43565

17. Bhende P.M., Seaman W.T., Delecluse H.J., Kenney S.C. The EBV lytic switch protein, Z, preferentially binds to and activates the methylated viral genome. Nat. Genet. 2004; 36(10): 1099-104. DOI: http://doi.org/10.1038/ng1424

18. Kaufer B.B., Flamand L. Chromosomally integrated HHV-6: impact on virus, cell and organismal biology. Curr. Opin. Virol. 2014; 9: 111‐8. DOI: http://doi.org/10.1016/j.coviro.2014.09.010

19. Woellmer A., Hammerschmidt W. Epstein-Barr virus and host cell methylation: regulation of latency, replication and virus reactivation. Curr. Opin. Virol. 2013; 3(3): 260‐5. DOI: http://doi.org/10.1016/j.coviro.2013.03.005

20. Lim C., Lee D., Seo T., Choi C., Choe J. Latency associated nuclear antigen of Kaposi’s sarcoma-associated herpesvirus functionally interacts with heterochromatin protein 1. J. Biol. Chem. 2003; 278(9): 7397-405. DOI: http://doi.org/10.1074/jbc.M211912200

21. Pantry S.N., Medveczky P.G. Epigenetic regulation of Kaposhi's sarcoma associated herpesvirus replication. Semin. Cancer Biol. 2009; 19(3): 153-7. DOI: http://doi.org/10.1016/j.semcancer.2009.02.010

22. Fatemi M., Pao M.M., Jeong S., Gal-Yam E.N., Egger G., Weisenberger D.J., et al. Footprinting of mammalian promoters: use of a CpG DNA methyltransferase revealing nucleosome positions at a single molecule level. Nucleic. Acids Res. 2005; 33(20): e176. DOI: http://doi.org/10.1093/nar/gni180

23. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., et al. Initial sequencing and analysis of the human genome. Nature. 2001; 409(6822): 860-921. DOI: http://doi.org/10.1038/35057062

24. Stevens M., Cheng J., Li D., Xi M., Hong C., Maire C., et al. Estimating absolute methylation levels at single-CpG resolution from methylation enrichment and restriction enzyme sequencing methods. Genome Res. 2013; 23(9): 1541‐53. DOI: http://doi.org/10.1101/gr.152231.112

25. Nicholas J. Evolutionary aspects of oncogenic herpesviruses. Mol. Pathol. 2000; 53(5): 222‐37. DOI: http://doi.org/10.1136/mp.53.5.222

Journal of microbiology, epidemiology and immunobiology. 2020; 97: 216-226

Tetranucleotide Profile of Herpesvirus DNA

Filatov Felix P., Shargunov Alexander V.

https://doi.org/10.36233/0372-9311-2020-97-3-3

Abstract

Introduction. Herpesvirus DNAs (about 90% of the total genomic sequences of the Herpesvirales family presented in GenBank) contain at a minimum concentration one of the two tetranucleotides, CTAG or TCGA. The “underrepresentation” of CTAG was previously observed only in the DNA of some bacteria and phages. The aim of the study was the further analysis of the formal characteristics of herpesvirus DNA, as well as their comparison with the density of the virus/host DNA microhomology and with the genomic macrostructure of herpes viruses.

Materials and methods. Twenty strains and isolates of each of the five types of human herpes viruses (HHV1, HHV2, HHV3, HHV4, HHV5), 10 strains of HHV8, 5 strains of HHV6A, 4 strains of HHV6B and 3 strains of HHV7 were analyzed. GenBank tools were used to determine the frequency of tetranucleotides, and human DNA fragments with size matched herpesvirus DNA were used for comparison.

Results. Minimum CTAG concentration in DNA of herpes viruses is mainly characteristic of two- and singlesegment genomes with direct or inverted terminal repeats (classes A,D,E), while the minimum TCGA density is characteristic mainly for DNA that is significantly less structured (classes B,C,F). By increasing CTAG density, human herpes viruses form a sequence close to the sequence of increasing the homology density of 20 nt with human DNA, which also correlates with the macrostructure of DNA. A parallel of this minimization with the DNA structure of herpes viruses or with their belonging to one or another subfamily — as well as the context of the “minimal” CpG (that is, TCGA) — is not noted in the literature. Although herpesvirus DNA is quite large (125– 295 Kb), some of them (for example, HHV4, HHV5 and HHV7 DNA) show noticeable deviations from the second DNA parity rule, and can thus serve as a component of the molecular signature.

The Discussion suggests possible hypotheses for the origin of some of the observed phenomena.

References

1. Whitley R., Kimberlin D., Prober C. Pathogenesis and disease. In: Arvin A., Campadelli-Fiume G., Mocarsky E., Moore P.S., Roizman B., Whitley R., eds. Human Herpesviruses: Biology, Therapy and Immunoprophylaxis. Chapter 32. Cambridge: Cambridge University Press; 2007.

2. Pellett P., Roizman B. Herpesviridae. In: Knipe D.M., Howley P.M., eds. Fields Virology. Philadelphia: Lippincott Williams & Wilkins; 2013: 1802-2.

3. Zabolotneva A., Tkachev V., Filatov F., Buzdin A. How many antiviral small interfering RNAs may be encoded by the mammalian genomes? Biol. Direct. 2010; 5: 62. DOI: http://doi.org/10.1186/1745-6150-5-62

4. Filatov F., Shargunov A. Short nucleotide sequences in herpesviral genomes identical to the human DNA. J. Theor. Biol. 2015; 372: 12-21. DOI: http://doi.org/10.1016/j.jtbi.2015.02.019

5. Filatov F., Shargunov A. Microhomology of Viral/Host DNAs and macrostructure of herpesviral genome. Int. J. Virol. AIDS. 2018; 5(1): 042. DOI: http://doi.org/10.23937/2469-567X/1510042

6. Rudner R., Karkas J.D., Chargaff E. Separation of B. subtilis DNA into complementary strands, 3. Direct Analysis. Proc. Natl. Acad. Sci. USA. 1968; 60(3): 921-2. DOI: http://doi.org/10.1073/pnas.60.3.921

7. Forsdyke D.R. Symmetry observations in long nucleotide sequences: a commentary on the discovery note of Qi and Cuticchia. Bioinformatics. 2002; 18(1): 215-7. DOI: http://doi.org/10.1093/bioinformatics/18.1.215

8. Albrecht-Buehler G. Asymptotically increasing compliance of genomes with Chargaff’s second parity rules through inversions and inverted transpositions. Version 2. Proc. Natl. Acad. Sci. USA. 2006; 103(47): 17828-33. DOI: http://doi.org/10.1073/pnas.0605553103

9. Baisnee P.F., Hampson S., Baldi P. Why are complementary strands symmetric? BioInformatics. 2002; 18(8): 1021‐33. DOI: http://doi.org/10.1093/bioinformatics/18.8.1021

10. Gori F., Mavroeidis D., Jetten M.S.M., Marchiori E. The importance of Chargaff’s second parity rule for genomic signatures in metagenomics. Available at: http://www.biorxiv.org/content/biorxiv/early/2017/06/04/146001.full.pdf

11. Pride D.T., Blaser M.J. Identification of horizontally acquired genetic elements in Helicobacter pylori and other prokaryotes using oligonucleotide difference analysis. Genome Lett. 2002; 1(1): 2-15. DOI: http://doi.org/doi.org/10.1166/gl.2002.003

12. Prabhu V.V. Symmetry observations in long nucleotide sequences. Nucleic Acids Res. 1993; 21(12): 2797‐800. DOI: http://doi.org/10.1093/nar/21.12.2797

13. Albrecht-Buehler G. The three classes of triplet profiles of natural genomes. Genomics. 2007; 89(5): 596‐601. DOI: http://doi.org/10.1016/j.ygeno.2006.12.009

14. Zhang S.H., Wang L. A novel common triplet profile for GCrich prokaryotic genomes. Genomics. 2011; 97(5): 330‐1. DOI: http://doi.org/10.1016/j.ygeno.2011.02.005

15. Burge C., Campbell A.M., Karlin S. Over- and under-representation of short oligonucleotides in DNA sequences. Proc. Natl. Acad. Sci. USA. 1992; 89(4): 1358-62. DOI: http://doi.org/10.1073/pnas.89.4.1358

16. Tang L., Zhu S., Mastriani E., Fang X., Zhou Y.J., Li Y.G., et al. Conserved intergenic sequences revealed by CTAG-profiling in Salmonella: thermodynamic modeling for function prediction. Sci. Rep. 2017; 7: 43565. DOI: http://doi.org/10.1038/srep43565

17. Bhende P.M., Seaman W.T., Delecluse H.J., Kenney S.C. The EBV lytic switch protein, Z, preferentially binds to and activates the methylated viral genome. Nat. Genet. 2004; 36(10): 1099-104. DOI: http://doi.org/10.1038/ng1424

18. Kaufer B.B., Flamand L. Chromosomally integrated HHV-6: impact on virus, cell and organismal biology. Curr. Opin. Virol. 2014; 9: 111‐8. DOI: http://doi.org/10.1016/j.coviro.2014.09.010

19. Woellmer A., Hammerschmidt W. Epstein-Barr virus and host cell methylation: regulation of latency, replication and virus reactivation. Curr. Opin. Virol. 2013; 3(3): 260‐5. DOI: http://doi.org/10.1016/j.coviro.2013.03.005

20. Lim C., Lee D., Seo T., Choi C., Choe J. Latency associated nuclear antigen of Kaposi’s sarcoma-associated herpesvirus functionally interacts with heterochromatin protein 1. J. Biol. Chem. 2003; 278(9): 7397-405. DOI: http://doi.org/10.1074/jbc.M211912200

21. Pantry S.N., Medveczky P.G. Epigenetic regulation of Kaposhi's sarcoma associated herpesvirus replication. Semin. Cancer Biol. 2009; 19(3): 153-7. DOI: http://doi.org/10.1016/j.semcancer.2009.02.010

22. Fatemi M., Pao M.M., Jeong S., Gal-Yam E.N., Egger G., Weisenberger D.J., et al. Footprinting of mammalian promoters: use of a CpG DNA methyltransferase revealing nucleosome positions at a single molecule level. Nucleic. Acids Res. 2005; 33(20): e176. DOI: http://doi.org/10.1093/nar/gni180

23. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., Baldwin J., et al. Initial sequencing and analysis of the human genome. Nature. 2001; 409(6822): 860-921. DOI: http://doi.org/10.1038/35057062

24. Stevens M., Cheng J., Li D., Xi M., Hong C., Maire C., et al. Estimating absolute methylation levels at single-CpG resolution from methylation enrichment and restriction enzyme sequencing methods. Genome Res. 2013; 23(9): 1541‐53. DOI: http://doi.org/10.1101/gr.152231.112

25. Nicholas J. Evolutionary aspects of oncogenic herpesviruses. Mol. Pathol. 2000; 53(5): 222‐37. DOI: http://doi.org/10.1136/mp.53.5.222