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Natural antisense transcripts of UL123 packaged in human cytomegalovirus virions

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Abstract

In this study, we demonstrated that antisense transcripts of human cytomegalovirus (HCMV) UL123, UL21.5 and cellular GAPDH genes were present in highly purified virions. These virion RNAs were delivered into the host cells upon infection, and de novo synthesized ones appeared in the infected cell at the immediate early stage. Although the sequence of UL123 antisense transcripts in virions is uncertain, we found that these transcripts in Towne-infected human fibroblasts had novel transcriptional start sites (TSSs) with various 5’-terminal deletions of open reading frame (ORF) 59. These findings not only provide new insight into the composition of HCMV virions but also reveal a possible viral strategy for initiating latent infection and switching between latent and productive infections.

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References

  1. Bresnahan WA, Shenk T (2000) A subset of viral transcripts packaged within human cytomegalovirus particles. Science 288(5475):2373–2376

    Article  CAS  PubMed  Google Scholar 

  2. Greijer AE, Dekkers CA, Middeldorp JM (2000) Human cytomegalovirus virions differentially incorporate viral and host cell RNA during the assembly process. J Virol 74(19):9078–9082

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Terhune SS, Schroer J, Shenk T (2004) RNAs are packaged into human cytomegalovirus virions in proportion to their intracellular concentration. J Virol 78(19):10390–10398. doi:10.1128/JVI.78.19.10390-10398.2004

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Sarcinella E, Brown M, Tellier R, Petric M, Mazzulli T (2004) Detection of RNA in purified cytomegalovirus virions. Virus Res 104(2):129–137. doi:10.1016/j.virusres.2004.03.008

    Article  CAS  PubMed  Google Scholar 

  5. Sciortino MT, Suzuki M, Taddeo B, Roizman B (2001) RNAs extracted from herpes simplex virus 1 virions: apparent selectivity of viral but not cellular RNAs packaged in virions. J Virol 75(17):8105–8116

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Bechtel J, Grundhoff A, Ganem D (2005) RNAs in the virion of Kaposi’s sarcoma-associated herpesvirus. J Virol 79(16):10138–10146. doi:10.1128/JVI.79.16.10138-10146.2005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Lin X, Li X, Liang D, Lan K (2012) MicroRNAs and unusual small RNAs discovered in Kaposi’s sarcoma-associated herpesvirus virions. J Virol 86(23):12717–12730. doi:10.1128/JVI.01473-12

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Cliffe AR, Nash AA, Dutia BM (2009) Selective uptake of small RNA molecules in the virion of murine gammaherpesvirus 68. J Virol 83(5):2321–2326. doi:10.1128/JVI.02303-08

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Jochum S, Ruiss R, Moosmann A, Hammerschmidt W, Zeidler R (2012) RNAs in Epstein-Barr virions control early steps of infection. Proc Nat Acad Sci USA 109(21):E1396–E1404. doi:10.1073/pnas.1115906109

    Article  CAS  PubMed  Google Scholar 

  10. Zhang Y, Liu XS, Liu QR, Wei L (2006) Genome-wide in silico identification and analysis of cis natural antisense transcripts (cis-NATs) in ten species. Nucleic Acids Res 34(12):3465–3475. doi:10.1093/nar/gkl473

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Arnold J, Yamamoto B, Li M, Phipps AJ, Younis I, Lairmore MD, Green PL (2006) Enhancement of infectivity and persistence in vivo by HBZ, a natural antisense coded protein of HTLV-1. Blood 107(10):3976–3982. doi:10.1182/blood-2005-11-4551

    Article  CAS  PubMed  Google Scholar 

  12. Gaudray G, Gachon F, Basbous J, Biard-Piechaczyk M, Devaux C, Mesnard JM (2002) The complementary strand of the human T-cell leukemia virus type 1 RNA genome encodes a bZIP transcription factor that down-regulates viral transcription. J Virol 76(24):12813–12822

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Vanhee-Brossollet C, Thoreau H, Serpente N, D’Auriol L, Levy JP, Vaquero C (1995) A natural antisense RNA derived from the HIV-1 env gene encodes a protein which is recognized by circulating antibodies of HIV+ individuals. Virology 206(1):196–202

    Article  CAS  PubMed  Google Scholar 

  14. Higgins GD, Uzelin DM, Phillips GE, Burrell CJ (1991) Presence and distribution of human papillomavirus sense and antisense RNA transcripts in genital cancers. J Gen Virol 72(Pt 4):885–895

    Article  CAS  PubMed  Google Scholar 

  15. Xu Y, Ganem D (2010) Making sense of antisense: seemingly noncoding RNAs antisense to the master regulator of Kaposi’s sarcoma-associated herpesvirus lytic replication do not regulate that transcript but serve as mRNAs encoding small peptides. J Virol 84(11):5465–5475. doi:10.1128/JVI.02705-09

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Kondo K, Kaneshima H, Mocarski ES (1994) Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proc Nat Acad Sci USA 91(25):11879–11883

    Article  CAS  PubMed  Google Scholar 

  17. Kondo K, Xu J, Mocarski ES (1996) Human cytomegalovirus latent gene expression in granulocyte-macrophage progenitors in culture and in seropositive individuals. Proc Nat Acad Sci USA 93(20):11137–11142

    Article  CAS  PubMed  Google Scholar 

  18. Zhang G, Raghavan B, Kotur M, Cheatham J, Sedmak D, Cook C, Waldman J, Trgovcich J (2007) Antisense transcription in the human cytomegalovirus transcriptome. J Virol 81(20):11267–11281. doi:10.1128/JVI.00007-07

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Baldick CJ Jr, Shenk T (1996) Proteins associated with purified human cytomegalovirus particles. J Virol 70(9):6097–6105

    CAS  PubMed Central  PubMed  Google Scholar 

  20. Patrone M, Secchi M, Fiorina L, Ierardi M, Milanesi G, Gallina A (2005) Human cytomegalovirus UL130 protein promotes endothelial cell infection through a producer cell modification of the virion. J Virol 79(13):8361–8373. doi:10.1128/JVI.79.13.8361-8373.2005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Luo MH, Schwartz PH, Fortunato EA (2008) Neonatal neural progenitor cells and their neuronal and glial cell derivatives are fully permissive for human cytomegalovirus infection. J Virol 82(20):9994–10007. doi:10.1128/JVI.00943-08

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Lunetta JM, Wiedeman JA (2000) Latency-associated sense transcripts are expressed during in vitro human cytomegalovirus productive infection. Virology 278(2):467–476. doi:10.1006/viro.2000.0666

    Article  CAS  PubMed  Google Scholar 

  23. Ma Y, Wang N, Li M, Gao S, Wang L, Ji Y, Qi Y, He R, Sun Z, Ruan Q (2011) An antisense transcript in the human cytomegalovirus UL87 gene region. Virol J 8:515. doi:10.1186/1743-422X-8-515

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Snaar SP, Verdijk P, Tanke HJ, Dirks RW (2002) Kinetics of HCMV immediate early mRNA expression in stably transfected fibroblasts. J Cell Sci 115(Pt 2):321–328

    CAS  PubMed  Google Scholar 

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Acknowledgments

This project was supported by the National Natural Science Foundation of China (31000090 and 81071350), National Program on Key Basic Research Project (973 Program, 2011CB504800), “Hundred Talents Program” of the Chinese Academy of Sciences (2010-88), and RO1 AI20211 (to ESM).

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Authors and Affiliations

  1. State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, 430071, China

    Cui-Qing Yang, Ling-Feng Miao, Xing Pan, Cong-Cong Wu, Simon Rayner, Han-Qing Ye & Min-Hua Luo

  2. Department of Microbiology and Immunology, Emory Vaccine Center, Emory University School of Medicine, Atlanta, GA, 30322, USA

    Edward S. Mocarski

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  1. Cui-Qing Yang
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  2. Ling-Feng Miao
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  3. Xing Pan
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  4. Cong-Cong Wu
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  5. Simon Rayner
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  6. Edward S. Mocarski
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  7. Han-Qing Ye
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  8. Min-Hua Luo
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Correspondence to Han-Qing Ye or Min-Hua Luo.

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Yang, CQ., Miao, LF., Pan, X. et al. Natural antisense transcripts of UL123 packaged in human cytomegalovirus virions. Arch Virol 159, 147–151 (2014). https://doi.org/10.1007/s00705-013-1793-5

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  • DOI: https://doi.org/10.1007/s00705-013-1793-5

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