MicroRNAs: expression, avoidance and subversion by vertebrate viruses (original) (raw)

• Chalfie, M., Horvitz, H. R. & Sulston, J. E. Mutations that lead to reiterations in the cell lineages of C. elegans. Cell 24, 59–69 (1981).
  CAS PubMed Google Scholar
• Horvitz, H. R. & Sulston, J. E. Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans. Genetics 96, 435–454 (1980).
  CAS PubMed PubMed Central Google Scholar
• Ambros, V. & Horvitz, H. R. Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226, 409–416 (1984).
  CAS PubMed Google Scholar
• Ambros, V. & Horvitz, H. R. The lin-14 locus of Caenorhabditis elegans controls the time of expression of specific postembryonic developmental events. Genes Dev. 1, 398–414 (1987).
  CAS PubMed Google Scholar
• Ambros, V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell 57, 49–57 (1989).
  CAS PubMed Google Scholar
• Lee, R. C., Feinbaum, R. L. & Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854 (1993).
  CAS PubMed Google Scholar
• Wightman, B., Ha, I. & Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855–862 (1993).
  CAS PubMed Google Scholar
• Olsen, P. H. & Ambros, V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671–680 (1999). This classic paper revealed that a small RNA regulator — which turned out to be the paradigmatic lin-4 miRNA — controls gene expression of target lin-14 mRNA at the post-transcriptional level.
  CAS PubMed Google Scholar
• Slack, F. J. et al. The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol. Cell 5, 659–669 (2000).
  CAS PubMed Google Scholar
• Reinhart, B. J. et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901–906 (2000).
  CAS PubMed Google Scholar
• Pasquinelli, A. E. et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86–89 (2000).
  CAS PubMed Google Scholar
• Lau, N. C., Lim, L. P., Weinstein, E. G. & Bartel, D. P. An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858–862 (2001).
  CAS PubMed Google Scholar
• Lee, R. C. & Ambros, V. An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862–864 (2001).
  CAS PubMed Google Scholar
• Lagos-Quintana, M., Rauhut, R., Lendeckel, W. & Tuschl, T. Identification of novel genes coding for small expressed RNAs. Science 294, 853–858 (2001). References 12–14 were the first reports of the identification of a large number of small (21-nucleotide) RNAs, leading to the realization that these molecules constitute a new class of RNA molecule.
  CAS PubMed Google Scholar
• Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281–297 (2004).
  CAS PubMed Google Scholar
• Griffiths-Jones, S. The microRNA Registry. Nucleic Acids Res. 32, D109–D111 (2004).
  CAS PubMed PubMed Central Google Scholar
• Pfeffer, S. et al. Identification of virus-encoded microRNAs. Science 304, 734–736 (2004). This was the first study to show that DNA viruses can encode miRNAs.
  CAS PubMed Google Scholar
• Pfeffer, S. et al. Identification of microRNAs of the herpesvirus family. Nature Methods 2, 269–276 (2005). This study identified virus-encoded miRNAs in the genomes of KSHV, MHV68 and HCMV. In addition, evidence was provided that MHV68 miRNAs are transcribed by RNA polymerase III.
  CAS PubMed Google Scholar
• Samols, M. A., Hu, J., Skalsky, R. L. & Renne, R. Cloning and identification of a microRNA cluster within the latency-associated region of Kaposi's sarcoma-associated herpesvirus. J. Virol. 79, 9301–9305 (2005).
  CAS PubMed PubMed Central Google Scholar
• Sullivan, C. S., Grundhoff, A. T., Tevethia, S., Pipas, J. M. & Ganem, D. SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells. Nature 435, 682–686 (2005). This was the first paper to report a biological function for a virus-encoded miRNA. Specifically, an SV40-encoded miRNA was found to downregulate virus-encoded mRNAs, reducing susceptibility to clearance by cytotoxic T lymphocytes.
  CAS PubMed Google Scholar
• Grey, F. et al. Identification and characterization of human cytomegalovirus-encoded microRNAs. J. Virol. 79, 12095–12099 (2005).
  CAS PubMed PubMed Central Google Scholar
• Cai, X. et al. Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. Proc. Natl Acad. Sci. USA 102, 5570–5575 (2005).
  CAS PubMed PubMed Central Google Scholar
• Andersson, M. G. et al. Suppression of RNA interference by adenovirus virus-associated RNA. J. Virol. 79, 9556–9565 (2005).
  CAS PubMed PubMed Central Google Scholar
• Sano, M., Kato, Y. & Taira, K. Sequence-specific interference by small RNAs derived from adenovirus VAI RNA. FEBS Lett. 580, 1553–1564 (2006).
  CAS PubMed Google Scholar
• Lee, Y., Jeon, K., Lee, J. T., Kim, S. & Kim, V. N. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 21, 4663–4670 (2002). This paper showed that miRNAs are processed by a series of cleavage events that occurs in the nucleus and the cytoplasm.
  CAS PubMed PubMed Central Google Scholar
• Rodriguez, A., Griffiths-Jones, S., Ashurst, J. L. & Bradley, A. Identification of mammalian microRNA host genes and transcription units. Genome Res. 14, 1902–1910 (2004).
  CAS PubMed PubMed Central Google Scholar
• Kim, V. N. MicroRNA biogenesis: coordinated cropping and dicing. Nature Rev. Mol. Cell Biol. 6, 376–385 (2005).
  CAS Google Scholar
• Cai, X., Hagedorn, C. H. & Cullen, B. R. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10, 1957–1966 (2004).
  CAS PubMed PubMed Central Google Scholar
• Lee, Y. et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051–4060 (2004).
  CAS PubMed PubMed Central Google Scholar
• Han, J. et al. Molecular basis for the recognition of primary microRNAs by the Drosha–DGCR8 complex. Cell 125, 887–901 (2006).
  CAS PubMed Google Scholar
• Yi, R., Qin, Y., Macara, I. G. & Cullen, B. R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17, 3011–3016 (2003).
  CAS PubMed PubMed Central Google Scholar
• Lund, E., Guttinger, S., Calado, A., Dahlberg, J. E. & Kutay, U. Nuclear export of microRNA precursors. Science 303, 95–98 (2004).
  CAS PubMed Google Scholar
• Bohnsack, M. T., Czaplinski, K. & Gorlich, D. Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 10, 185–191 (2004).
  CAS PubMed PubMed Central Google Scholar
• Chendrimada, T. P. et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740–744 (2005).
  CAS PubMed PubMed Central Google Scholar
• Forstemann, K. et al. Normal microRNA maturation and germ-line stem cell maintenance requires Loquacious, a double-stranded RNA-binding domain protein. PLoS Biol. 3, e236 (2005).
  PubMed PubMed Central Google Scholar
• Haase, A. D. et al. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 6, 961–967 (2005).
  CAS PubMed PubMed Central Google Scholar
• Patel, R. C. & Sen, G. C. PACT, a protein activator of the interferon-induced protein kinase, PKR. EMBO J. 17, 4379–4390 (1998).
  CAS PubMed PubMed Central Google Scholar
• Lee, Y. et al. The role of PACT in the RNA silencing pathway. EMBO J. 25, 522–532 (2006).
  CAS PubMed PubMed Central Google Scholar
• Basyuk, E., Suavet, F., Doglio, A., Bordonne, R. & Bertrand, E. Human let-7 stem–loop precursors harbor features of RNase III cleavage products. Nucleic Acids Res. 31, 6593–6597 (2003).
  CAS PubMed PubMed Central Google Scholar
• Lee, Y. et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419 (2003).
  CAS PubMed Google Scholar
• Zamore, P. D. Thirty-three years later, a glimpse at the ribonuclease III active site. Mol. Cell 8, 1158–1160 (2001).
  CAS PubMed Google Scholar
• Maniataki, E. & Mourelatos, Z. A human, ATP-independent, RISC assembly machine fueled by pre-miRNA. Genes Dev. 19, 2979–2990 (2005).
  CAS PubMed PubMed Central Google Scholar
• Hammond, S. M., Bernstein, E., Beach, D. & Hannon, G. J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404, 293–296 (2000).
  CAS PubMed Google Scholar
• Khvorova, A., Reynolds, A. & Jayasena, S. D. Functional siRNAs and miRNAs exhibit strand bias. Cell 115, 209–216 (2003).
  CAS PubMed Google Scholar
• Mourelatos, Z. et al. miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev. 16, 720–728 (2002).
  CAS PubMed PubMed Central Google Scholar
• Sasaki, T., Shiohama, A., Minoshima, S. & Shimizu, N. Identification of eight members of the Argonaute family in the human genome. Genomics 82, 323–330 (2003).
  CAS PubMed Google Scholar
• Meister, G. et al. Identification of novel Argonaute-associated proteins. Curr. Biol. 15, 2149–2155 (2005).
  CAS PubMed Google Scholar
• Meister, G. et al. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell 15, 185–197 (2004).
  CAS PubMed Google Scholar
• Liu, J. et al. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305, 1437–1441 (2004).
  CAS PubMed Google Scholar
• Nelson, P. T., Hatzigeorgiou, A. G. & Mourelatos, Z. miRNP:mRNA association in polyribosomes in a human neuronal cell line. RNA 10, 387–394 (2004).
  CAS PubMed PubMed Central Google Scholar
• Jin, P. et al. Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nature Neurosci. 7, 113–117 (2004).
  CAS PubMed Google Scholar
• Lewis, B. P., Burge, C. B. & Bartel, D. P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20 (2005).
  CAS PubMed Google Scholar
• Zeng, Y., Wagner, E. J. & Cullen, B. R. Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol. Cell 9, 1327–1333 (2002).
  CAS PubMed Google Scholar
• Pillai, R. S. et al. Inhibition of translational initiation by let-7 microRNA in human cells. Science 309, 1573–1576 (2005).
  CAS PubMed Google Scholar
• Humphreys, D. T., Westman, B. J., Martin, D. I. & Preiss, T. MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc. Natl Acad. Sci. USA 102, 16961–16966 (2005).
  CAS PubMed PubMed Central Google Scholar
• Petersen, C. P., Bordeleau, M. E., Pelletier, J. & Sharp, P. A. Short RNAs repress translation after initiation in mammalian cells. Mol. Cell 21, 533–542 (2006).
  CAS PubMed Google Scholar
• Yekta, S., Shih, I. H. & Bartel, D. P. MicroRNA-directed cleavage of HOXB8 mRNA. Science 304, 594–596 (2004).
  CAS PubMed Google Scholar
• Cai, X. et al. Epstein–Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog. 2, e23 (2006).
  PubMed PubMed Central Google Scholar
• Cai, X. & Cullen, B. R. Transcriptional origin of Kaposi's sarcoma-associated herpesvirus microRNAs. J. Virol. 80, 2234–2242 (2006).
  CAS PubMed PubMed Central Google Scholar
• Furnari, F. B., Adams, M. D. & Pagano, J. S. Unconventional processing of the 3′ termini of the Epstein–Barr virus DNA polymerase mRNA. Proc. Natl Acad. Sci. USA 90, 378–382 (1993).
  CAS PubMed PubMed Central Google Scholar
• Grundhoff, A., Sullivan, C. & Ganem, D. A combined computational and microarray-based approach identifies novel microRNAs encoded by human γ−herpesviruses. RNA 12, 733–750 (2006).
  CAS PubMed PubMed Central Google Scholar
• Gupta, A., Gartner, J. J., Sethupathy, P., Hatzigeorgiou, A. G. & Fraser, N. W. Anti-apoptotic function of a microRNA encoded by the HSV-1 latency-associated transcript. Nature 442, 82–85 (2006). This report shows that the non-protein-coding transcript LAT of HSV-1 encodes an miRNA that downregulates genes involved in the onset of apoptosis. This implies that an miRNA has a role in the protection of latently infected neurons.
  CAS PubMed Google Scholar
• Luciano, D. J., Mirsky, H., Vendetti, N. J. & Maas, S. RNA editing of a miRNA precursor. RNA 10, 1174–1177 (2004).
  CAS PubMed PubMed Central Google Scholar
• Bowden, R. J., Simas, J. P., Davis, A. J. & Efstathiou, S. Murine γherpesvirus 68 encodes tRNA-like sequences which are expressed during latency. J. Gen. Virol. 78, 1675–1687 (1997).
  CAS PubMed Google Scholar
• Dunn, W. et al. Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cell. Microbiol. 7, 1684–1695 (2005).
  CAS PubMed Google Scholar
• Mathews, M. B. & Shenk, T. Adenovirus virus-associated RNA and translation control. J. Virol. 65, 5657–5662 (1991).
  CAS PubMed PubMed Central Google Scholar
• Gwizdek, C. et al. Exportin-5 mediates nuclear export of minihelix-containing RNAs. J. Biol. Chem. 278, 5505–5508 (2003).
  CAS PubMed Google Scholar
• Lu, S. & Cullen, B. R. Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and microRNA biogenesis. J. Virol. 78, 12868–12876 (2004). This study provided the first evidence that a vertebrate-virus gene product inhibited RNA silencing by blocking different stages of the miRNA processing pathway.
  CAS PubMed PubMed Central Google Scholar
• Aparicio, O., Razquin, N., Zaratiegui, M., Narvaiza, I. & Fortes, P. Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J. Virol. 80, 1376–1384 (2006).
  CAS PubMed PubMed Central Google Scholar
• Omoto, S. & Fujii, Y. R. Regulation of human immunodeficiency virus 1 transcription by nef microRNA. J. Gen. Virol. 86, 751–755 (2005).
  CAS PubMed Google Scholar
• Bennasser, Y., Le, S. Y., Benkirane, M. & Jeang, K. T. Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity 22, 607–619 (2005).
  CAS PubMed Google Scholar
• Lecellier, C. H. & Saib, A. Foamy viruses: between retroviruses and pararetroviruses. Virology 271, 1–8 (2000).
  CAS PubMed Google Scholar
• Lecellier, C. H. et al. A cellular microRNA mediates antiviral defense in human cells. Science 308, 557–560 (2005). This is an interesting study in which an interaction between a cellular miRNA and a vertebrate virus (PFV-1) was shown. A suppressor protein encoded by the virus was shown to counteract the repressive effect of human miR-32 in a heterologous plant system.
  CAS PubMed Google Scholar
• Lakatos, L. et al. Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors. EMBO J. 25, 2768–2780 (2006).
  CAS PubMed PubMed Central Google Scholar
• Lakatos, L., Szittya, G., Silhavy, D. & Burgyan, J. Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses. EMBO J. 23, 876–884 (2004).
  CAS PubMed PubMed Central Google Scholar
• Dunoyer, P., Lecellier, C. H., Parizotto, E. A., Himber, C. & Voinnet, O. Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16, 1235–1250 (2004).
  CAS PubMed PubMed Central Google Scholar
• Baunach, G., Maurer, B., Hahn, H., Kranz, M. & Rethwilm, A. Functional analysis of human foamy virus accessory reading frames. J. Virol. 67, 5411–5418 (1993).
  CAS PubMed PubMed Central Google Scholar
• Meiering, C. D., Comstock, K. E. & Linial, M. L. Multiple integrations of human foamy virus in persistently infected human erythroleukemia cells. J. Virol. 74, 1718–1726 (2000).
  CAS PubMed PubMed Central Google Scholar
• Saib, A., Peries, J. & de The, H. A defective human foamy provirus generated by pregenome splicing. EMBO J. 12, 4439–4444 (1993).
  CAS PubMed PubMed Central Google Scholar
• Jopling, C. L., Yi, M., Lancaster, A. M., Lemon, S. M. & Sarnow, P. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309, 1577–1581 (2005). This paper provides an example of a cellular miRNA that binds and positively regulates a viral RNA. The liver-specific miRNA miR-122 was found to interact with the 5′-non-protein-coding region of HCV and increase viral RNA production, probably at the level of replication.
  CAS PubMed Google Scholar
• Moradpour, D. et al. Membrane association of the RNA-dependent RNA polymerase is essential for hepatitis C virus RNA replication. J. Virol. 78, 13278–13284 (2004).
  CAS PubMed PubMed Central Google Scholar
• Moradpour, D. et al. Membrane association of hepatitis C virus nonstructural proteins and identification of the membrane alteration that harbors the viral replication complex. Antiviral Res. 60, 103–109 (2003).
  CAS PubMed Google Scholar
• El-Hage, N. & Luo, G. Replication of hepatitis C virus RNA occurs in a membrane-bound replication complex containing nonstructural viral proteins and RNA. J. Gen. Virol. 84, 2761–2769 (2003).
  CAS PubMed Google Scholar
• Zhu, Q., Guo, J. T. & Seeger, C. Replication of hepatitis C virus subgenomes in nonhepatic epithelial and mouse hepatoma cells. J. Virol. 77, 9204–9210 (2003).
  CAS PubMed PubMed Central Google Scholar
• De Francesco, R. & Migliaccio, G. Challenges and successes in developing new therapies for hepatitis C. Nature 436, 953–960 (2005).
  CAS PubMed Google Scholar
• Chang, J. E. N. et al. miR-122, a mammalian liver-specific microRNA, is processed from hcr mRNA and may downregulate the high affinity cationic amino acid transporter CAT-1. RNA Biol. 1, 106–113 (2004).
  CAS PubMed Google Scholar
• Krützfeldt, J. et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 438, 685–689 (2005).
  PubMed Google Scholar
• Esau, C. et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 3, 87–98 (2006). References 87 and 88 examine the effect of miR-122 inhibition on the level of transcripts in mouse liver. They showed that miR-122 has an important role in upregulation of genes involved in cholesterol biosynthesis and fatty-acid metabolism.
  CAS PubMed Google Scholar
• Kapadia, S. B. & Chisari, F. V. Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc. Natl Acad. Sci. USA 102, 2561–2566 (2005).
  CAS PubMed PubMed Central Google Scholar
• Ye, J. et al. Disruption of hepatitis C virus RNA replication through inhibition of host protein geranylgeranylation. Proc. Natl Acad. Sci. USA 100, 15865–15870 (2003).
  CAS PubMed PubMed Central Google Scholar
• Clarke, P. A. & Mathews, M. B. Interactions between the double-stranded RNA binding motif and RNA: definition of the binding site for the interferon-induced protein kinase DAI (PKR) on adenovirus VA RNA. RNA 1, 7–20 (1995).
  CAS PubMed PubMed Central Google Scholar