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Possible mechanisms of acquisition of herpesvirus virokines

  • Molecular and Cellular Mechanisms of Inflammation (Special Issue) Guest Editors S. A. Nedospasov and D. V. Kuprash
  • Published:
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Abstract

The genomes of certain types of human and primate herpesviruses contain functional homologs of important host cytokines (IL-6, IL-17, and IL-10), or so-called virokines. Virokines can interact with immune cell receptors, transmit a signal to them, and thus switch the type of immune response that facilitates viral infection development. In this work, we have summarized possible ways of virokine origin and proposed an evolutionary scenario of virokine acquisition with involvement of retroviral coinfection of the host. This scenario is probably valid for vIL-6 of HHV-8 and MRV-5 viruses, vIL-17 of HVS virus, and vIL-10 of HHV-4, Bonobo-HV, RhLCV, and BaLCV viruses. The ability to acquire cytokine genes allows herpesviruses to implement unique strategies of avoiding the immune response and provides them an evolutionary advantage: more than 90% of the host population can be chronically infected with different herpesviruses. It is possible that the biological success of herpesviruses can be partially due to their cooperation with another group of viruses. This hypothesis emphasizes the importance of studies on the reciprocal influence of pathogens on their coinfection, as well as their impact on the host organism.

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Abbreviations

BaLCV:

baboon lymphocryptovirus

BonoboHV:

bonobo herpesvirus

EBV:

Epstein–Barr virus

HHV:

human herpesvirus

HVS:

herpesvirus saimiri

IFN:

interferon

IL:

interleukin

MRV:

rhesus macaque rhadinovirus

RhCMV:

rhesus macaque cytomegalovirus

RhLCV:

rhesus macaque lymphocryptovirus

SaHV-2:

Saimiriine herpesvirus 2

vIL:

virokine, interleukin homolog

References

  1. Kunin, E. V. (2014) Logic of Case. On the Nature and Origin of Biological Evolution [in Russian], Tsentrolitograf, Moscow.

  2. Kotwal, G. J. (1999) Virokines: mediators of virus-host interaction and future immunomodulators in medicine, Arch. Immunol. Ther. Exp. (Warsz.), 47, 135–138.

    CAS  Google Scholar 

  3. Alcami, A. (2003) Viral mimicry of cytokines, chemokines and their receptors, Nat. Rev. Immunol., 3, 36–50.

    Article  CAS  PubMed  Google Scholar 

  4. Brown, J. C. (2014) The role of DNA repair in herpesvirus pathogenesis, Genomics, 104, 287–294.

    Article  CAS  PubMed  Google Scholar 

  5. Zheng, Z.-M. (2003) Split genes and their expression in Kaposi’s sarcoma-associated herpesvirus, Rev. Med. Virol., 13, 173–184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Farlow, A., Meduri, E., and Schlotterer, C. (2011) DNA double-strand break repair and the evolution of intron density, Trends Genet., 27, 1–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Rice, P., Longden, I., and Bleasby, A. (2000) EMBOSS: the European molecular biology open software suite, Trends Genet., 16, 276–277.

    Article  CAS  PubMed  Google Scholar 

  8. Katoh, K., Misawa, K., Kuma, K. I., and Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Res., 30, 3059–3066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Katoh, K., Kuma, K., Toh, H., and Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment, Nucleic Acids Res., 33, 511–518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0, Mol. Biol. Evol., 30, 27252729.

    Article  CAS  Google Scholar 

  11. Drummond, A. J., and Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees, BMC Evol. Biol., 7, 1.

    Article  CAS  Google Scholar 

  12. Kent, W. J. (2002) BLAT–the BLAST-like alignment tool, Genome Res., 12, 656–664.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hedges, S. B., Dudley, J., and Kumar, S. (2006) TimeTree: a public knowledge base of divergence times among organisms, Bioinformatics, 22, 2971–2972.

    Article  CAS  PubMed  Google Scholar 

  14. Maul, D. H., Zaiss, C. P., MacKenzie, M. R., Shiigi, S. M., Marx, P. A., and Gardner, M. B. (1988) Simian retrovirus D serogroup 1 has a broad cellular tropism for lymphoid and nonlymphoid cells, J. Virol., 62, 1768–1773.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Rogers, D. L., McClure, G. B., Ruiz, J. C., Abee, C. R., and Vanchiere, J. A. (2015) Endemic viruses of squirrel monkeys (Saimiri spp.), Comp. Med., 65, 232–240.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Ouyang, P., Rakus, K., Van Beurden, S. J., Westphal, A. H., Davison, A. J., Gatherer, D., and Vanderplasschen, A. F. (2014) IL-10 encoded by viruses: a remarkable example of independent acquisition of a cellular gene by viruses and its subsequent evolution in the viral genome, J. Gen. Virol., 95, 245–262.

    Article  CAS  PubMed  Google Scholar 

  17. Bruce, A. G., Thouless, M. E., Haines, A. S., Pallen, M. J., Grundhoff, A., and Rose, T. M. (2015) Complete genome sequence of pig-tailed macaque rhadinovirus 2 and its evolutionary relationship with rhesus macaque rhadinovirus and human herpesvirus 8/Kaposi’s sarcoma-associated herpesvirus, J. Virol., 89, 3888–3909.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sin, S. H., and Dittmer, D. P. (2012) Cytokine homologs of human gammaherpesviruses, J. Interferon Cytokine Res., 32, 53–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Chatterjee, M., Osborne, J., Bestetti, G., Chang, Y., and Moore, P. S. (2002) Viral IL-6-induced cell proliferation and immune evasion of interferon activity, Science, 298, 1432–1435.

    Article  CAS  PubMed  Google Scholar 

  20. Polizzotto, M. N., Uldrick, T. S., Wyvill, K. M., Aleman, K., Marshall, V., Wang, V., Whitby, D., Pittaluga, S., Jaffe, E. S., Millo, C., Tosato, G., Little, R. F., Steinberg, S. M., Sereti, I., and Yarchoan, R. (2016) Clinical features and outcomes of patients with symptomatic Kaposi sarcoma herpesvirus (KSHV)-associated inflammation: prospective characterization of KSHV inflammatory cytokine syndrome (KICS), Clin. Infect. Dis., 62, 730–738.

    Article  PubMed  Google Scholar 

  21. Damania, B., and Desrosiers, R. C. (2001) Simian homologs of human herpesvirus 8, Philos. Trans. R Soc. Lond. B: Biol. Sci., 356, 535–543.

    Article  CAS  Google Scholar 

  22. Estep, R. D., and Wong, S. W. (2013). Rhesus macaque rhadinovirus-associated disease, Curr. Opin. Virol., 3, 245–250.

  23. Gorshkova, E. A., Nedospasov, S. A., and Shilov, E. S. (2016) Evolutionary plasticity of the IL-6 family cytokines, Mol. Biol., 50, in press.

  24. Boulanger, M. J., Chow, D. C., Brevnova, E. E., and Garcia, K. C. (2003) Hexameric structure and assembly of the interleukin-6/IL-6 a-receptor/gp130 complex, Science, 300, 2101–2104.

    Article  CAS  PubMed  Google Scholar 

  25. Chow, D. C., Brevnova, L., He, X. L., Martick, M. M., Bankovich, A., and Garcia, K. C. (2002) A structural template for gp130-cytokine signaling assemblies, Biochim. Biophys. Acta, 1592, 225–235.

    Article  CAS  PubMed  Google Scholar 

  26. Sakakibara, S., and Tosato, G. (2011) Viral interleukin-6: role in Kaposi’s sarcoma-associated herpesvirus-associated malignancies, J. Interferon Cytokine Res., 31, 791–801.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. McGeoch, D. J., Gatherer, D., and Dolan, A. (2005) On phylogenetic relationships among major lineages of the Gammaherpesvirinae, J. Gen. Virol., 86, 307–316.

    Article  CAS  PubMed  Google Scholar 

  28. Ensser, A., Thurau, M., Wittmann, S., and Fickenscher, H. (2003) The genome of herpesvirus saimiri C488 which is capable of transforming human T-cells, Virology, 314, 471487.

    Article  CAS  Google Scholar 

  29. Folcik, V. A., Garofalo, M., Coleman, J., Donegan, J. J., Rabbani, E., Suster, S., Nuovo, A., Magro, C. M., Di Leva, G., and Nuovo, G. J. (2014) Idiopathic pulmonary fibrosis is strongly associated with productive infection by herpesvirus saimiri, Modern Pathol., 27, 851–862.

    Article  CAS  Google Scholar 

  30. Yao, Z., Fanslow, W. C., Seldin, M. F., Rousseau, A. M., Painter, S. L., Comeau, M. R., and Spriggs, M. K. (1995) Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor, Immunity, 3, 811–821.

    CAS  PubMed  Google Scholar 

  31. Gasse, P., Riteau, N., Vacher, R., Michel, M. L., Fautrel, A., Di Padova, F., Fick, L., Charron, S., Lagente, V., Eberl, G., and Le Bert, M. (2011) IL-1 and IL-23 mediate early IL-17A production in pulmonary inflammation leading to late fibrosis, PLoS One, 6, e23185.

    Article  CAS  Google Scholar 

  32. Ouyang, P., Rakus, K., Van Beurden, S. J., Westphal, A. H., Davison, A. J., Gatherer, D., and Vanderplasschen, A. F. (2014) IL-10 encoded by viruses: a remarkable example of independent acquisition of a cellular gene by viruses and its subsequent evolution in the viral genome, J. Gen. Virol., 95, 245–262.

    Article  CAS  PubMed  Google Scholar 

  33. Nicholas, J., Zong, J. C., Alcendor, D. J., Ciufo, D. M., Poole, L. J., Sarisky, R. T., Chiou, C. J., Zhang, X., Wan, X., Guo, H. G., Reitz, M.S., and Hayward, G. S. (1998) Novel organizational features, captured cellular genes, and strain variability within the genome of KSHV/HHV8, J. Natl. Cancer Inst. Monogr., 23, 79–88.

    CAS  Google Scholar 

  34. Brinzevich, D., Young, G. R., Sebra, R., Ayllon, J., Maio, S. M., Deikus, G., Chen, B. K., Fernandez-Sesma, A., Simon, V., and Mulder, L. C. (2014) HIV-1 interacts with HERV-K (HML-2) envelopes derived from human primary lymphocytes, J. Virol., 88, 6213–6223.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Aswad, A., and Katzourakis, A. (2015) Convergent capture of retroviral superantigens by mammalian herpesviruses, Nat. Commun., 6, 8299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kimura, A., and Kishimoto, T. (2010) IL-6: regulator of Treg/Th17 balance, Eur. J. Immunol., 40, 1830–1835.

    Article  CAS  PubMed  Google Scholar 

  37. Rossi, J. F., Lu, Z. Y., Jourdan, M., and Klein, B. (2015) Interleukin-6 as a therapeutic target, Clin. Cancer Res., 6, 1248–1257.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Faculty of Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    E. A. Gorshkova & E. S. Shilov

  2. Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991, Moscow, Russia

    E. A. Gorshkova & E. S. Shilov

Authors
  1. E. A. Gorshkova
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  2. E. S. Shilov
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Correspondence to E. S. Shilov.

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Original Russian Text © E. A. Gorshkova, E. S. Shilov, 2016, published in Biokhimiya, 2016, Vol. 81, No. 11, pp. 1604–1613.

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Gorshkova, E.A., Shilov, E.S. Possible mechanisms of acquisition of herpesvirus virokines. Biochemistry Moscow 81, 1350–1357 (2016). https://doi.org/10.1134/S0006297916110122

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  • DOI: https://doi.org/10.1134/S0006297916110122

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