Human cytomegalovirus microRNA miR-US4-1 inhibits CD8+ T cell responses by targeting the aminopeptidase ERAP1 (original) (raw)

• Hansen, T.H. & Bouvier, M. MHC class I antigen presentation: learning from viral evasion strategies. Nat. Rev. Immunol. 9, 503–513 (2009).
  Article CAS Google Scholar
• Vyas, J.M., Van der Veen, A.G. & Ploegh, H.L. The known unknowns of antigen processing and presentation. Nat. Rev. Immunol. 8, 607–618 (2008).
  Article CAS Google Scholar
• Nguyen, T.T. et al. Structural basis for antigenic peptide precursor processing by the endoplasmic reticulum aminopeptidase ERAP1. Nat. Struct. Mol. Biol. 18, 604–613 (2011).
  Article CAS Google Scholar
• Haroon, N. & Inman, R.D. Endoplasmic reticulum aminopeptidases: Biology and pathogenic potential. Nat. Rev. Rheumatol. 6, 461–467 (2010).
  Article CAS Google Scholar
• Saric, T. et al. An IFN-γ-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I–presented peptides. Nat. Immunol. 3, 1169–1176 (2002).
  Article CAS Google Scholar
• Saveanu, L. et al. Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat. Immunol. 6, 689–697 (2005).
  Article CAS Google Scholar
• Kanaseki, T. & Shastri, N. Endoplasmic reticulum aminopeptidase associated with antigen processing regulates quality of processed peptides presented by MHC class I molecules. J. Immunol. 181, 6275–6282 (2008).
  Article CAS Google Scholar
• Hammer, G.E., Gonzalez, F., James, E., Nolla, H. & Shastri, N. In the absence of aminopeptidase ERAAP, MHC class I molecules present many unstable and highly immunogenic peptides. Nat. Immunol. 8, 101–108 (2007).
  Article CAS Google Scholar
• Chang, S.C., Momburg, F., Bhutani, N. & Goldberg, A.L. The ER aminopeptidase, ERAP1, trims precursors to lengths of MHC class I peptides by a “molecular ruler” mechanism. Proc. Natl. Acad. Sci. USA 102, 17107–17112 (2005).
  Article CAS Google Scholar
• Fabian, M.R., Sonenberg, N. & Filipowicz, W. Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79, 351–379 (2010).
  Article CAS Google Scholar
• Pfeffer, S. et al. Identification of virus-encoded microRNAs. Science 304, 734–736 (2004).
  Article CAS Google Scholar
• Cullen, B.R. Viral and cellular messenger RNA targets of viral microRNAs. Nature 457, 421–425 (2009).
  Article CAS Google Scholar
• Pfeffer, S. et al. Identification of microRNAs of the herpesvirus family. Nat. Methods 2, 269–276 (2005).
  Article CAS Google Scholar
• Grey, F. et al. Identification and characterization of human cytomegalovirus-encoded microRNAs. J. Virol. 79, 12095–12099 (2005).
  Article CAS Google Scholar
• Grey, F., Meyers, H., White, E.A., Spector, D.H. & Nelson, J. A human cytomegalovirus-encoded microRNA regulates expression of multiple viral genes involved in replication. PLoS Pathog. 3, e163 (2007).
  Article Google Scholar
• Grey, F. et al. A viral microRNA down-regulates multiple cell cycle genes through mRNA 5′UTRs. PLoS Pathog. 6, e1000967 (2010).
  Article Google Scholar
• Stern-Ginossar, N. et al. Host immune system gene targeting by a viral miRNA. Science 317, 376–381 (2007).
  Article CAS Google Scholar
• Stern-Ginossar, N. et al. Analysis of human cytomegalovirus-encoded microRNA activity during infection. J. Virol. 83, 10684–10693 (2009).
  Article CAS Google Scholar
• Rehm, A. et al. Human cytomegalovirus gene products US2 and US11 differ in their ability to attack major histocompatibility class I heavy chains in dendritic cells. J. Virol. 76, 5043–5050 (2002).
  Article CAS Google Scholar
• Machold, R.P., Wiertz, E.J., Jones, T.R. & Ploegh, H.L. The HCMV gene products US11 and US2 differ in their ability to attack allelic forms of murine major histocompatibility complex (MHC) class I heavy chains. J. Exp. Med. 185, 363–366 (1997).
  Article CAS Google Scholar
• Gruhler, A., Peterson, P.A. & Fruh, K. Human cytomegalovirus immediate early glycoprotein US3 retains MHC class I molecules by transient association. Traffic 1, 318–325 (2000).
  Article CAS Google Scholar
• Lehner, P.J., Karttunen, J.T., Wilkinson, G.W. & Cresswell, P. The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc. Natl. Acad. Sci. USA 94, 6904–6909 (1997).
  Article CAS Google Scholar
• Park, B., Spooner, E., Houser, B.L., Strominger, J.L. & Ploegh, H.L. The HCMV membrane glycoprotein US10 selectively targets HLA-G for degradation. J. Exp. Med. 207, 2033–2041 (2010).
  Article CAS Google Scholar
• Gustems, M. et al. Regulation of the transcription and replication cycle of human cytomegalovirus is insensitive to genetic elimination of the cognate NF-kappa B binding sites in the enhancer. J. Virol. 80, 9899–9904 (2006).
  Article CAS Google Scholar
• Wu, J., O'Neill, J. & Barbosa, M.S. Transcription factor Sp1 mediates cell-specific trans-activation of the human cytomegalovirus DNA polymerase gene promoter by immediate-early protein IE86 in glioblastoma U373MG cells. J. Virol. 72, 236–244 (1998).
  CAS PubMed PubMed Central Google Scholar
• Chekulaeva, M. & Filipowicz, W. Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr. Opin. Cell Biol. 21, 452–460 (2009).
  Article CAS 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).
  Article CAS Google Scholar
• Rehmsmeier, M., Steffen, P., Hochsmann, M. & Giegerich, R. Fast and effective prediction of microRNA/target duplexes. RNA 10, 1507–1517 (2004).
  Article CAS Google Scholar
• Miranda, K.C. et al. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126, 1203–1217 (2006).
  Article CAS Google Scholar
• Wang, W.X., Wilfred, B.R., Hu, Y., Stromberg, A.J. & Nelson, P.T. Anti-Argonaute RIP-Chip shows that miRNA transfections alter global patterns of mRNA recruitment to microribonucleoprotein complexes. RNA 16, 394–404 (2010).
  Article CAS Google Scholar
• Nonne, N., Ameyar-Zazoua, M., Souidi, M. & Harel-Bellan, A. Tandem affinity purification of miRNA target mRNAs (TAP-Tar). Nucleic Acids Res. 38, e20 (2010).
  Article Google Scholar
• Moore, L.M. & Zhang, W. Targeting miR-21 in glioma: a small RNA with big potential. Expert Opin. Ther. Targets 14, 1247–1257 (2010).
  Article CAS Google Scholar
• Peters, L. & Meister, G. Argonaute proteins: mediators of RNA silencing. Mol. Cell 26, 611–623 (2007).
  Article CAS Google Scholar
• York, I.A., Brehm, M.A., Zendzian, S., Towne, C.F. & Rock, K.L. Endoplasmic reticulum aminopeptidase 1 (ERAP1) trims MHC class I-presented peptides in vivo and plays an important role in immunodominance. Proc. Natl. Acad. Sci. USA 103, 9202–9207 (2006).
  Article CAS Google Scholar
• Karttunen, J., Sanderson, S. & Shastri, N. Detection of rare antigen-presenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens. Proc. Natl. Acad. Sci. USA 89, 6020–6024 (1992).
  Article CAS Google Scholar
• Shastri, N. & Gonzalez, F. Endogenous generation and presentation of the ovalbumin peptide/Kb complex to T cells. J. Immunol. 150, 2724–2736 (1993).
  CAS PubMed Google Scholar
• Firat, E. et al. The role of endoplasmic reticulum-associated aminopeptidase 1 in immunity to infection and in cross-presentation. J. Immunol. 178, 2241–2248 (2007).
  Article CAS Google Scholar
• Yan, J. et al. In vivo role of ER-associated peptidase activity in tailoring peptides for presentation by MHC class Ia and class Ib molecules. J. Exp. Med. 203, 647–659 (2006).
  Article CAS Google Scholar
• Blanchard, N. et al. Endoplasmic reticulum aminopeptidase associated with antigen processing defines the composition and structure of MHC class I peptide repertoire in normal and virus-infected cells. J. Immunol. 184, 3033–3042 (2010).
  Article CAS Google Scholar
• Tanioka, T. et al. Human leukocyte-derived arginine aminopeptidase. The third member of the oxytocinase subfamily of aminopeptidases. J. Biol. Chem. 278, 32275–32283 (2003).
  Article CAS Google Scholar
• Fruci, D. et al. Altered expression of endoplasmic reticulum aminopeptidases ERAP1 and ERAP2 in transformed non-lymphoid human tissues. J. Cell. Physiol. 216, 742–749 (2008).
  Article CAS Google Scholar
• Georgiadou, D. et al. Placental leucine aminopeptidase efficiently generates mature antigenic peptides in vitro but in patterns distinct from endoplasmic reticulum aminopeptidase 1. J. Immunol. 185, 1584–1592 (2010).
  Article CAS Google Scholar
• Hansen, S.G. et al. Evasion of CD8+ T cells is critical for superinfection by cytomegalovirus. Science 328, 102–106 (2010).
  Article CAS Google Scholar
• Manley, T.J. et al. Immune evasion proteins of human cytomegalovirus do not prevent a diverse CD8+ cytotoxic T-cell response in natural infection. Blood 104, 1075–1082 (2004).
  Article CAS Google Scholar
• Evnouchidou, I. et al. The internal sequence of the peptide-substrate determines its N-terminus trimming by ERAP1. PLoS ONE 3, e3658 (2008).
  Article Google Scholar
• Niles, A.L., Moravec, R.A. & Riss, T.L. In vitro viability and cytotoxicity testing and same-well multi-parametric combinations for high throughput screening. Curr Chem Genomics 3, 33–41 (2009).
  Article CAS Google Scholar
• Lee, Y. et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415–419 (2003).
  Article CAS Google Scholar