Influenza a virus expresses high levels of an unusual class of small viral leader RNAs in infected cells

mBio

Volumn 1, Issue 4, 2010, Pages

  Umbach, Jennifer L ^a   Yen, Hui Ling ^b,c   Poon, Leo L M ^c   Cullen, Bryan R ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; NUCLEOTIDE; PHOSPHORUS DERIVATIVE; VIRUS RNA;

5' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLUENZA; INFLUENZA VIRUS A; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA PROCESSING; RNA SEQUENCE; RNA SYNTHESIS; RNA TRANSCRIPTION; RNA VIRUS; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS GENOME; VIRUS REPLICATION;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE; RNA VIRUSES;

EID: 79952068189     PISSN: None     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00204-10     Document Type: Article

References (42)

1. Bartel, D. P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297.
2. Cullen, B. R. 2004. Transcription and processing of human microRNA precursors. Mol. Cell 16:861-865.
3. Ma, J. B., K. Ye, and D. J. Patel. 2004. Structural basis for overhangspecific small interfering RNA recognition by the PAZ domain. Nature 429:318-322.
4. Wang, Y., G. Sheng, S. Juranek, T. Tuschl, and D. J. Patel. 2008. Structure of the guide-strand-containing argonaute silencing complex. Nature 456:209-213.
5. Umbach, J. L., and B. R. Cullen. 2009. The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev. 23:1151-1164.
6. Cai, X., S. Lu, Z. Zhang, C. M. Gonzalez, B. Damania, and B. R. Cullen. 2005. Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc. Natl. Acad. Sci. U. S. A. 102:5570-5575.
7. Cai, X., A. Schäfer, S. Lu, J. P. Bilello, R. C. Desrosiers, R. Edwards, N. Raab-Traub, and B. R. Cullen. 2006. Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. 2:e23.
8. Grey, F., A. Antoniewicz, E. Allen, J. Saugstad, A. McShea, J. C. Carrington, and J. Nelson. 2005. Identification and characterization of human cytomegalovirus-encoded microRNAs. J. Virol. 79:12095-12099.
9. Pfeffer, S., A. Sewer, M. Lagos-Quintana, R. Sheridan, C. Sander, F. A. Grasser, L. F. van Dyk, C. K. Ho, S. Shuman, M. Chien, J. J. Russo, J. Ju, G. Randall, B. D. Lindenbach, C. M. Rice, V. Simon, D. D. Ho, M. Zavolan, and T. Tuschl. 2005. Identification of microRNAs of the herpesvirus family. Nat. Methods 2:269-276.
10. Pfeffer, S., M. Zavolan, F. A. Grasser, M. Chien, J. J. Russo, J. Ju, B. John, A. J. Enright, D. Marks, C. Sander, and T. Tuschl. 2004. Identification of virus-encoded microRNAs. Science 304:734-736.
11. Samols, M. A., J. Hu, R. L. Skalsky, and R. Renne. 2005. Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi's sarcoma-associated herpesvirus. J. Virol. 79:9301-9305.
12. Sullivan, C. S., A. T. Grundhoff, S. Tevethia, J. M. Pipas, and D. Ganem. 2005. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 435:682-686.
13. Umbach, J. L., M. F. Kramer, I. Jurak, H. W. Karnowski, D. M. Coen, and B. R. Cullen. 2008. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454:780-783.
14. Lin, J., and B. R. Cullen. 2007. Analysis of the interaction of primate retroviruses with the human RNA interference machinery. J. Virol. 81:12218-12226.
15. Omoto, S., M. Ito, Y. Tsutsumi, Y. Ichikawa, H. Okuyama, E. A. Brisibe, N. K. Saksena, and Y. R. Fujii. 2004. HIV-1 nef suppression by virally encoded microRNA. Retrovirology 1:44.
16. Ouellet, D. L., I. Plante, P. Landry, C. Barat, M. E. Janelle, L. Flamand, M. J. Tremblay, and P. Provost. 2008. Identification of functional micro- RNAs released through asymmetrical processing of HIV-1 TAR element. Nucleic Acids Res. 36:2353-2365.
17. Palese, P., and M. L. Shaw. 2007. Orthomyxoviridae: the viruses and their replication, p. 1647-1689. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 5th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
18. Yen, H. L., L. M. Herlocher, E. Hoffmann, M. N. Matrosovich, A. S. Monto, R. G. Webster, and E. A. Govorkova. 2005. Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrob. Agents Chemother. 49:4075-4084.
19. Bitko, V., A. Musiyenko, M. A. Bayfield, R. J. Maraia, and S. Barik. 2008. Cellular La protein shields nonsegmented negative-strand RNA viral leader RNA from RIG-I and enhances virus growth by diverse mechanisms. J. Virol. 82:7977-7987.
20. Blumberg, B. M., M. Leppert, and D. Kolakofsky. 1981. Interaction of VSV leader RNA and nucleocapsid protein may control VSV genome replication. Cell 23:837-845.
21. Colonno, R. J., and A. K. Banerjee. 1978. Complete nucleotide sequence of the leader RNA synthesized in vitro by vesicular stomatitis virus. Cell 15:93-101.
22. Kurilla, M. G., C. D. Cabradilla, B. P. Holloway, and J. D. Keene. 1984. Nucleotide sequence and host La protein interactions of rabies virus leader RNA. J. Virol. 50:773-778.
23. Leppert, M., L. Rittenhouse, J. Perrault, D. F. Summers, and D. Kolakofsky. 1979. Plus and minus strand leader RNAs in negative strand virusinfected cells. Cell 18:735-747.
24. Beaton, A. R., and R. M. Krug. 1986. Transcription antitermination during influenza viral template RNA synthesis requires the nucleocapsid protein and the absence of a 5= capped end. Proc. Natl. Acad. Sci. U. S. A. 83:6282-6286.
25. Hatada, E., M. Hasegawa, J. Mukaigawa, K. Shimizu, and R. Fukuda. 1989. Control of influenza virus gene expression: quantitative analysis of each viral RNA species in infected cells. J. Biochem. 105:537-546.
26. Medcalf, L., E. Poole, D. Elton, and P. Digard. 1999. Temperaturesensitive lesions in two influenza A viruses defective for replicative transcription disrupt RNA binding by the nucleoprotein. J. Virol. 73:7349-7356.
27. Hay, A. J., B. Lomniczi, A. R. Bellamy, and J. J. Skehel. 1977. Transcription of the influenza virus genome. Virology 83:337-355.
28. Shapiro, G. I., T. Gurney, Jr., and R. M. Krug. 1987. Influenza virus gene expression: control mechanisms at early and late times of infection and nuclear-cytoplasmic transport of virus-specific RNAs. J. Virol. 61:764-773.
29. Cheung, C. Y., L. L. Poon, A. S. Lau, W. Luk, Y. L. Lau, K. F. Shortridge, S. Gordon, Y. Guan, and J. S. Peiris. 2002. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360:1831-1837.
30. Murphy, B. R., E. L. Tierney, S. B. Spring, and R. M. Chanock. 1976. Temperature-sensitive mutants of influenza A virus. XI. Transfer of ts lesions in the Hong Kong/68-ts-1 [a] virus to the influenza A/Udorn/72 wild type. J. Infect. Dis. 134:577-584.
31. Kawaguchi, A., and K. Nagata. 2007. De novo replication of the influenza virusRNAgenome is regulated byDNAreplicative helicase, MCM. EMBO J. 26:4566-4575.
32. Kurilla, M. G., H. Piwnica-Worms, and J. D. Keene. 1982. Rapid and transient localization of the leader RNA of vesicular stomatitis virus in the nuclei of infected cells. Proc. Natl. Acad. Sci. U. S. A. 79:5240-5244.
33. Wilusz, J., M. G. Kurilla, and J. D. Keene. 1983. A host protein (La) binds to a unique species of minus-sense leader RNA during replication of vesicular stomatitis virus. Proc. Natl. Acad. Sci. U. S. A. 80:5827-5831.
34. Kurilla, M. G., and J. D. Keene. 1983. The leader RNA of vesicular stomatitis virus is bound by a cellular protein reactive with anti-La lupus antibodies. Cell 34:837-845.
35. Perez, J. T., A. Varble, R. Sachidanandam, I. Zlatev, M. Manoharan, A. Garcia-Sastre, and B. R. tenOever. 2010. Influenza A virus-generated small RNAs regulate the switch from transcription to replication. Proc. Natl. Acad. Sci. U. S. A. 107:11525-11530.
36. Elmen, J., M. Lindow, S. Schutz, M. Lawrence, A. Petri, S. Obad, M. Lindholm, M. Hedtjarn, H. F. Hansen, U. Berger, S. Gullans, P. Kearney, P. Sarnow, E. M. Straarup, and S. Kauppinen. 2008. LNA-mediated microRNA silencing in non-human primates. Nature 452:896-899.
37. Fodor, E., P. Palese, G. G. Brownlee, and A. Garcia-Sastre. 1998. Attenuation of influenza A virus mRNA levels by promoter mutations. J. Virol. 72:6283-6290.
38. Patton, J. T., N. L. Davis, and G. W. Wertz. 1984. N protein alone satisfies the requirement for protein synthesis during RNA replication of vesicular stomatitis virus. J. Virol. 49:303-309.
39. Friedlander, M. R., W. Chen, C. Adamidi, J. Maaskola, R. Einspanier, S. Knespel, and N. Rajewsky. 2008. Discovering microRNAs from deep sequencing data using miRDeep. Nat. Biotechnol. 26:407-415.
40. Umbach, J. L., M. A. Nagel, R. J. Cohrs, D. H. Gilden, and B. R. Cullen. 2009. Analysis of human alphaherpesvirus microRNA expression in latently infected human trigeminal ganglia. J. Virol. 83:10677-10683.
41. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
42. Parameswaran, P., E. Sklan, C. Wilkins, T. Burgon, M. A. Samuel, R. Lu, K. M. Ansel, V. Heissmeyer, S. Einav, W. Jackson, T. Doukas, S. Paranjape, C. Polacek, F. B. dos Santos, R. Jalili, F. Babrzadeh, B. Gharizadeh, D. Grimm, M. Kay, S. Koike, P. Sarnow, M. Ronaghi, S. W. Ding, E. Harris, M. Chow, M. S. Diamond, K. Kirkegaard, J. S. Glenn, and A. Z. Fire. 2010. Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS Pathog. 6:e1000764.