MicroRNAs: expression, avoidance and subversion by vertebrate viruses

MicroRNAs (miRNAs), which can be expressed in a cell-type and tissue-specific manner, can influence the activities of genes that control cell growth and differentiation. Viruses often have clear tissue tropisms, raising the possibility that cellular miRNAs might modulate their pathogenesis. In this Review, we discuss recent findings that some vertebrate viruses either encode miRNAs or subvert cellular miRNAs, and that these miRNAs participate in both the infectious and the latent phase of the viral life cycle.

[1]  T. Tuschl,et al.  Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. , 2004, Molecular cell.

[2]  Olivier Voinnet,et al.  RETRACTED: Probing the MicroRNA and Small Interfering RNA Pathways with Virus-Encoded Suppressors of RNA Silencing[W] , 2004, Plant Cell.

[3]  F. Penin,et al.  Membrane association of hepatitis C virus nonstructural proteins and identification of the membrane alteration that harbors the viral replication complex. , 2003, Antiviral research.

[4]  Henry Mirsky,et al.  RNA editing of a miRNA precursor. , 2004, RNA.

[5]  E. Bertrand,et al.  Human let-7 stem-loop precursors harbor features of RNase III cleavage products. , 2003, Nucleic acids research.

[6]  Anton J. Enright,et al.  Identification of Virus-Encoded MicroRNAs , 2004, Science.

[7]  S. Le,et al.  Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. , 2005, Immunity.

[8]  B. Cullen,et al.  Transcriptional Origin of Kaposi's Sarcoma-Associated Herpesvirus MicroRNAs , 2006, Journal of Virology.

[9]  A. Hatzigeorgiou,et al.  Anti-apoptotic function of a microRNA encoded by the HSV-1 latency-associated transcript , 2006, Nature.

[10]  V. Kim,et al.  MicroRNA maturation: stepwise processing and subcellular localization , 2002, The EMBO journal.

[11]  F. Chisari,et al.  Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[12]  C. Sander,et al.  miR-122, a Mammalian Liver-Specific microRNA, is Processed from hcr mRNA and MayDownregulate the High Affinity Cationic Amino Acid Transporter CAT-1 , 2004, RNA biology.

[13]  B. Reinhart,et al.  The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans , 2000, Nature.

[14]  Artemis G Hatzigeorgiou,et al.  miRNP:mRNA association in polyribosomes in a human neuronal cell line. , 2004, RNA.

[15]  M. Samols,et al.  Cloning and Identification of a MicroRNA Cluster within the Latency-Associated Region of Kaposi's Sarcoma-Associated Herpesvirus , 2005, Journal of Virology.

[16]  T. Tuschl,et al.  Identification of Novel Argonaute-Associated Proteins , 2005, Current Biology.

[17]  H. Horvitz,et al.  Heterochronic mutants of the nematode Caenorhabditis elegans. , 1984, Science.

[18]  Alexandra Schäfer,et al.  Epstein–Barr Virus MicroRNAs Are Evolutionarily Conserved and Differentially Expressed , 2006, PLoS pathogens.

[19]  L. Lim,et al.  An Abundant Class of Tiny RNAs with Probable Regulatory Roles in Caenorhabditis elegans , 2001, Science.

[20]  B. Reinhart,et al.  Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA , 2000, Nature.

[21]  Blossom Damania,et al.  Kaposi's sarcoma-associated herpesvirus expresses an array of viral microRNAs in latently infected cells. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  V. Ambros,et al.  The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 , 1993, Cell.

[23]  J. Sulston,et al.  Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans. , 1980, Genetics.

[24]  C. Burge,et al.  Conserved Seed Pairing, Often Flanked by Adenosines, Indicates that Thousands of Human Genes are MicroRNA Targets , 2005, Cell.

[25]  Jay Nelson,et al.  Identification and Characterization of Human Cytomegalovirus-Encoded MicroRNAs , 2005, Journal of Virology.

[26]  D. Görlich,et al.  mediates nuclear export of pre-miRNAs Exportin 5 is a RanGTP-dependent dsRNA-binding protein that , 2004 .

[27]  M. Gale,et al.  Disruption of hepatitis C virus RNA replication through inhibition of host protein geranylgeranylation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Eric J Wagner,et al.  Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. , 2002, Molecular cell.

[29]  G Baunach,et al.  Functional analysis of human foamy virus accessory reading frames , 1993, Journal of virology.

[30]  Anne Gatignol,et al.  TRBP, a regulator of cellular PKR and HIV‐1 virus expression, interacts with Dicer and functions in RNA silencing , 2005, EMBO reports.

[31]  Sam Griffiths-Jones,et al.  The microRNA Registry , 2004, Nucleic Acids Res..

[32]  G. Sen,et al.  PACT, a protein activator of the interferon‐induced protein kinase, PKR , 1998, The EMBO journal.

[33]  U. Kutay,et al.  Nuclear Export of MicroRNA Precursors , 2004, Science.

[34]  David I. K. Martin,et al.  MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[35]  K. Comstock,et al.  Multiple Integrations of Human Foamy Virus in Persistently Infected Human Erythroleukemia Cells , 2000, Journal of Virology.

[36]  V. Ambros.  A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans , 1989, Cell.

[37]  J. M. Thomson,et al.  Argonaute2 Is the Catalytic Engine of Mammalian RNAi , 2004, Science.

[38]  M. Mathews,et al.  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. , 1995, RNA.

[39]  H. Horvitz,et al.  The lin-14 locus of Caenorhabditis elegans controls the time of expression of specific postembryonic developmental events. , 1987, Genes & development.

[40]  Edward Yang,et al.  Human cytomegalovirus expresses novel microRNAs during productive viral infection , 2005, Cellular microbiology.

[41]  P. Zamore,et al.  Thirty-three years later, a glimpse at the ribonuclease III active site. , 2001, Molecular cell.

[42]  Martin Chalfie,et al.  Mutations that lead to reiterations in the cell lineages of C. elegans , 1981, Cell.

[43]  B. Cullen,et al.  Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. , 2003, Genes & development.

[44]  James M. Pipas,et al.  SV40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells , 2005, Nature.

[45]  O. Aparicio,et al.  Adenovirus Virus-Associated RNA Is Processed to Functional Interfering RNAs Involved in Virus Production , 2006, Journal of Virology.

[46]  F. Penin,et al.  Membrane Association of the RNA-Dependent RNA Polymerase Is Essential for Hepatitis C Virus RNA Replication , 2004, Journal of Virology.

[47]  B. Cullen,et al.  Adenovirus VA1 Noncoding RNA Can Inhibit Small Interfering RNA and MicroRNA Biogenesis , 2004, Journal of Virology.

[48]  J. Pipas,et al.  SV 40-encoded microRNAs regulate viral gene expression and reduce susceptibility to cytotoxic T cells , 2005 .

[49]  G. Ruvkun,et al.  Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans , 1993, Cell.

[50]  D. Bartel,et al.  MicroRNA-Directed Cleavage of HOXB8 mRNA , 2004, Science.

[51]  V. Ambros,et al.  The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. , 1999, Developmental biology.

[52]  P. Sarnow,et al.  Modulation of Hepatitis C Virus RNA Abundance by a Liver-Specific MicroRNA , 2005, Science.

[53]  Sanghyuk Lee,et al.  MicroRNA genes are transcribed by RNA polymerase II , 2004, The EMBO journal.

[54]  R. Bowden,et al.  Murine gammaherpesvirus 68 encodes tRNA-like sequences which are expressed during latency. , 1997, The Journal of general virology.

[55]  Y. Fujii,et al.  Regulation of human immunodeficiency virus 1 transcription by nef microRNA. , 2005, The Journal of general virology.

[56]  C. Sander,et al.  Identification of microRNAs of the herpesvirus family , 2005, Nature Methods.

[57]  Adam Grundhoff,et al.  A combined computational and microarray-based approach identifies novel microRNAs encoded by human gamma-herpesviruses. , 2006, RNA.

[58]  V. Kim,et al.  The nuclear RNase III Drosha initiates microRNA processing , 2003, Nature.

[59]  C. Seeger,et al.  Replication of Hepatitis C Virus Subgenomes in Nonhepatic Epithelial and Mouse Hepatoma Cells , 2003, Journal of Virology.

[60]  A. Denli,et al.  Normal microRNA Maturation and Germ-Line Stem Cell Maintenance Requires Loquacious, a Double-Stranded RNA-Binding Domain Protein , 2005, PLoS biology.

[61]  K. Taira,et al.  Sequence‐specific interference by small RNAs derived from adenovirus VAI RNA , 2006, FEBS letters.

[62]  V. Ambros,et al.  An Extensive Class of Small RNAs in Caenorhabditis elegans , 2001, Science.

[63]  Z. Mourelatos,et al.  A human, ATP-independent, RISC assembly machine fueled by pre-miRNA. , 2005, Genes & development.

[64]  R. Shiekhattar,et al.  TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing , 2005, Nature.

[65]  Daniela C. Zarnescu,et al.  Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway , 2004, Nature Neuroscience.

[66]  A. Bradley,et al.  Identification of mammalian microRNA host genes and transcription units. , 2004, Genome research.

[67]  Edouard Bertrand,et al.  Exportin-5 Mediates Nuclear Export of Minihelix-containing RNAs* , 2003, The Journal of Biological Chemistry.

[68]  B. Cullen,et al.  Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. , 2004, RNA.

[69]  Mark Graham,et al.  miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. , 2006, Cell metabolism.

[70]  M. Mathews,et al.  Adenovirus virus-associated RNA and translation control , 1991, Journal of virology.

[71]  G. Szittya,et al.  Molecular mechanism of RNA silencing suppression mediated by p19 protein of tombusviruses , 2004, The EMBO journal.

[72]  M. Adams,et al.  Unconventional processing of the 3' termini of the Epstein-Barr virus DNA polymerase mRNA. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[73]  A. Saïb,et al.  Foamy viruses: between retroviruses and pararetroviruses. , 2000, Virology.

[74]  V. Kim.  MicroRNA biogenesis: coordinated cropping and dicing , 2005, Nature Reviews Molecular Cell Biology.

[75]  A. Saïb,et al.  A Cellular MicroRNA Mediates Antiviral Defense in Human Cells , 2005, Science.

[76]  Shinsei Minoshima,et al.  Identification of eight members of the Argonaute family in the human genome. , 2003, Genomics.

[77]  R. Francesco,et al.  Challenges and successes in developing new therapies for hepatitis C , 2005, Nature.

[78]  Byoung-Tak Zhang,et al.  Molecular Basis for the Recognition of Primary microRNAs by the Drosha-DGCR8 Complex , 2006, Cell.

[79]  G. Luo,et al.  Replication of hepatitis C virus RNA occurs in a membrane-bound replication complex containing nonstructural viral proteins and RNA. , 2003, The Journal of general virology.

[80]  N. Rajewsky,et al.  Silencing of microRNAs in vivo with ‘antagomirs’ , 2005, Nature.

[81]  T. Tuschl,et al.  Identification of Novel Genes Coding for Small Expressed RNAs , 2001, Science.

[82]  D. Bartel.  MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[83]  F. Slack,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. , 2000, Molecular cell.

[84]  M. Mann,et al.  miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. , 2002, Genes & development.

[85]  Ben Berkhout,et al.  Suppression of RNA Interference by Adenovirus Virus-Associated RNA , 2005, Journal of Virology.

[86]  A. Saïb,et al.  A defective human foamy provirus generated by pregenome splicing. , 1993, The EMBO journal.

[87]  V. Kim,et al.  The role of PACT in the RNA silencing pathway , 2006, The EMBO journal.

[88]  Anastasia Khvorova,et al.  Functional siRNAs and miRNAs Exhibit Strand Bias , 2003, Cell.

[89]  W. Filipowicz,et al.  Inhibition of Translational Initiation by Let-7 MicroRNA in Human Cells , 2005, Science.

[90]  Jerry Pelletier,et al.  Short RNAs repress translation after initiation in mammalian cells. , 2006, Molecular cell.

[91]  S. Hammond,et al.  An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells , 2000, Nature.

[92]  K. Czaplinski,et al.  Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. , 2004, RNA.

[93]  V. Dolja,et al.  Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors , 2006, The EMBO journal.