Systematic MicroRNA Analysis Identifies ATP6V0C as an Essential Host Factor for Human Cytomegalovirus Replication

PLoS Pathogens

Volumn 9, Issue 12, 2013, Pages 1-13

  Pavelin, Jon ^a   Reynolds, Natalie ^a   Chiweshe, Stephen ^a   Wu, Guanming ^b   Tiribassi, Rebecca ^b   Grey, Finn ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GREEN FLUORESCENT PROTEIN; HOST FACTOR; LIPOFECTAMINE; MICRORNA; RNA INDUCED SILENCING COMPLEX; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; US25 1; VIRUS RNA; ATP6V0C PROTEIN, HUMAN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; VIRUS PROTEIN;

ACIDIFICATION; ARTICLE; ATP6V0C; BCKDHA; CCNE2; CONTROLLED STUDY; ENDOSOME; FIBROBLAST; GENE SILENCING; GENETIC ALGORITHM; GROWTH CURVE; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; HUMAN HERPESVIRUS 5 (STRAIN AD169); IMMUNOPRECIPITATION; LGALS3; LIN28B; LUCIFERASE ASSAY; NONHUMAN; NUCB2; RANK SUM TEST; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCREENING; SEQUENCE ANALYSIS; SGSH; TARGET CELL; VIRAL GENE DELIVERY SYSTEM; VIRUS GENE; VIRUS MUTATION; VIRUS REPLICATION; WESTERN BLOTTING; CELL CULTURE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION PROFILING; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; MICROARRAY ANALYSIS; PATHOGENICITY; PHYSIOLOGY; TRANSGENIC ORGANISM;

CELLS, CULTURED; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; GENE EXPRESSION PROFILING; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICROARRAY ANALYSIS; MICRORNAS; ORGANISMS, GENETICALLY MODIFIED; RNA, SMALL INTERFERING; VACUOLAR PROTON-TRANSLOCATING ATPASES; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84892887731     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003820     Document Type: Article

References (50)

1. Nelson JA, Gnann JW Jr, Ghazal P, (1990) Regulation and tissue-specific expression of human cytomegalovirus. Curr Top Microbiol Immunol 154: 75-100.
2. Boehler A, Schaffner A, Salomon F, Keusch G, (1994) Cytomegalovirus disease of late onset following renal transplantation: a potentially fatal entity. Scand J Infect Dis 26: 369-373.
3. Ballard RA, Drew WL, Hufnagle KG, Riedel PA, (1979) Acquired cytomegalovirus infection in preterm infants. Am J Dis Child 133: 482-485.
4. Adler SP, (1983) Transfusion-associated cytomegalovirus infections. Rev Infect Dis 5: 977-993.
5. Einhorn L, Ost A, (1984) Cytomegalovirus infection of human blood cells. J Infect Dis 149: 207-214.
6. Macher AM, Reichert CM, Straus SE, Longo DL, Parrillo J, et al. (1983) Death in the AIDS patient: role of cytomegalovirus. N Engl J Med 309: 1454.
7. Neiman P, Wasserman PB, Wentworth BB, Kao GF, Lerner KG, et al. (1973) Interstitial pneumonia and cytomegalovirus infection as complications of human marrow transplantation. Transplantation 15: 478-485.
8. Tegtmeier GE, (1988) The use of cytomegalovirus-screened blood in neonates. Transfusion 28: 201-203.
9. Larsson S, Soderberg-Naucler C, Wang FZ, Moller E, (1998) Cytomegalovirus DNA can be detected in peripheral blood mononuclear cells from all seropositive and most seronegative healthy blood donors over time. Transfusion 38: 271-278.
10. Soderberg-Naucler C, Fish KN, Nelson JA, (1997) Reactivation of latent human cytomegalovirus by allogeneic stimulation of blood cells from healthy donors. Cell 91: 119-126.
11. Stanier P, Kitchen AD, Taylor DL, Tyms AS, (1992) Detection of human cytomegalovirus in peripheral mononuclear cells and urine samples using PCR. Mol Cell Probes 6: 51-58.
12. Taylor-Wiedeman J, Sissons JG, Borysiewicz LK, Sinclair JH, (1991) Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J Gen Virol 72 (Pt 9) (): 2059-2064.
13. Myerson D, Hackman RC, Nelson JA, Ward DC, McDougall JK, (1984) Widespread presence of histologically occult cytomegalovirus. Hum Pathol 15: 430-439.
14. Goodrum F, Caviness K, Zagallo P, (2012) Human cytomegalovirus persistence. Cell Microbiol 14: 644-655.
15. Grundhoff A, Sullivan CS, (2011) Virus-encoded microRNAs. Virology 411: 325-343.
16. Dunn W, Trang P, Zhong Q, Yang E, van Belle C, et al. (2005) Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cell Microbiol 7: 1684-1695.
17. Grey F, Antoniewicz A, Allen E, Saugstad J, McShea A, et al. (2005) Identification and characterization of human cytomegalovirus-encoded microRNAs. J Virol 79: 12095-12099.
18. Meshesha MK, Veksler-Lublinsky I, Isakov O, Reichenstein I, Shomron N, et al. (2012) The microRNA Transcriptome of Human Cytomegalovirus (HCMV). Open Virol J 6: 38-48.
19. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, et al. (2005) Identification of microRNAs of the herpesvirus family. Nat Methods 2: 269-276.
20. Stark TJ, Arnold JD, Spector DH, Yeo GW, (2012) High-resolution profiling and analysis of viral and host small RNAs during human cytomegalovirus infection. J Virol 86: 226-235.
21. Tuddenham L, Pfeffer S, (2011) Roles and regulation of microRNAs in cytomegalovirus infection. Biochim Biophys Acta 1809: 613-622.
22. Grey F, Meyers H, White EA, Spector DH, Nelson J, (2007) A Human Cytomegalovirus-Encoded microRNA Regulates Expression of Multiple Viral Genes Involved in Replication. PLoS Pathog 3: e163.
23. Bellare P, Ganem D, (2009) Regulation of KSHV lytic switch protein expression by a virus-encoded microRNA: an evolutionary adaptation that fine-tunes lytic reactivation. Cell Host Microbe 6: 570-575.
24. Lei X, Bai Z, Ye F, Xie J, Kim CG, et al. (2010) Regulation of NF-kappaB inhibitor IkappaBalpha and viral replication by a KSHV microRNA. Nat Cell Biol 12: 193-199.
25. Lu F, Stedman W, Yousef M, Renne R, Lieberman PM, (2010) Epigenetic regulation of Kaposi's sarcoma-associated herpesvirus latency by virus-encoded microRNAs that target Rta and the cellular Rbl2-DNMT pathway. J Virol 84: 2697-2706.
26. Murphy E, Vanicek J, Robins H, Shenk T, Levine AJ, (2008) Suppression of immediate-early viral gene expression by herpesvirus-coded microRNAs: implications for latency. Proc Natl Acad Sci U S A 105: 5453-5458.
27. Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N, et al. (2007) Host immune system gene targeting by a viral miRNA. Science 317: 376-381.
28. Karginov FV, Conaco C, Xuan Z, Schmidt BH, Parker JS, et al. (2007) A biochemical approach to identifying microRNA targets. Proc Natl Acad Sci U S A 104: 19291-19296.
29. Grey F, Tirabassi R, Meyers H, Wu G, McWeeney S, et al. (2010) A viral microRNA down-regulates multiple cell cycle genes through mRNA 5′UTRs. PLoS Pathog 6: e1000967.
30. Dolken L, Malterer G, Erhard F, Kothe S, Friedel CC, et al. (2010) Systematic analysis of viral and cellular microRNA targets in cells latently infected with human gamma-herpesviruses by RISC immunoprecipitation assay. Cell Host Microbe 7: 324-334.
31. Farh KK, Grimson A, Jan C, Lewis BP, Johnston WK, et al. (2005) The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 310: 1817-1821.
32. Lewis BP, Burge CB, Bartel DP, (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
33. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, et al. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773.
34. Lim JH, Park JW, Kim SJ, Kim MS, Park SK, et al. (2007) ATP6V0C competes with von Hippel-Lindau protein in hypoxia-inducible factor 1alpha (HIF-1alpha) binding and mediates HIF-1alpha expression by bafilomycin A1. Mol Pharmacol 71: 942-948.
35. Gottwein E, Corcoran DL, Mukherjee N, Skalsky RL, Hafner M, et al. (2011) Viral microRNA targetome of KSHV-infected primary effusion lymphoma cell lines. Cell Host Microbe 10: 515-526.
36. Haecker I, Gay LA, Yang Y, Hu J, Morse AM, et al. (2012) Ago HITS-CLIP expands understanding of Kaposi's sarcoma-associated herpesvirus miRNA function in primary effusion lymphomas. PLoS Pathog 8: e1002884.
37. Riley KJ, Rabinowitz GS, Yario TA, Luna JM, Darnell RB, et al. (2012) EBV and human microRNAs co-target oncogenic and apoptotic viral and human genes during latency. EMBO J 31: 2207-2221.
38. Skalsky RL, Corcoran DL, Gottwein E, Frank CL, Kang D, et al. (2012) The viral and cellular microRNA targetome in lymphoblastoid cell lines. PLoS Pathog 8: e1002484.
39. Kim Y, Lee S, Kim S, Kim D, Ahn JH, et al. (2012) Human cytomegalovirus clinical strain-specific microRNA miR-UL148D targets the human chemokine RANTES during infection. PLoS Pathog 8: e1002577.
40. Lee SH, Kalejta RF, Kerry J, Semmes OJ, O'Connor CM, et al. (2012) BclAF1 restriction factor is neutralized by proteasomal degradation and microRNA repression during human cytomegalovirus infection. Proc Natl Acad Sci U S A 109: 9575-9580.
41. Forgac M, (2007) Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 8: 917-929.
42. Ryckman BJ, Jarvis MA, Drummond DD, Nelson JA, Johnson DC, (2006) Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J Virol 80: 710-722.
43. Sanchez V, Greis KD, Sztul E, Britt WJ, (2000) Accumulation of virion tegument and envelope proteins in a stable cytoplasmic compartment during human cytomegalovirus replication: characterization of a potential site of virus assembly. J Virol 74: 975-986.
44. Stern-Ginossar N, Saleh N, Goldberg MD, Prichard M, Wolf DG, et al. (2009) Analysis of human cytomegalovirus-encoded microRNA activity during infection. J Virol 83: 10684-10693.
45. Benaroch P, Yilla M, Raposo G, Ito K, Miwa K, et al. (1995) How MHC class II molecules reach the endocytic pathway. EMBO J 14: 37-49.
46. Macfarlane DE, Manzel L, (1998) Antagonism of immunostimulatory CpG-oligodeoxynucleotides by quinacrine, chloroquine, and structurally related compounds. J Immunol 160: 1122-1131.
47. Umashankar M, Petrucelli A, Cicchini L, Caposio P, Kreklywich CN, et al. (2011) A novel human cytomegalovirus locus modulates cell type-specific outcomes of infection. PLoS Pathog 7: e1002444.
48. Easow G, Teleman AA, Cohen SM, (2007) Isolation of microRNA targets by miRNP immunopurification. Rna 13: 1198-1204.
49. Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R, (2004) Fast and effective prediction of microRNA/target duplexes. Rna 10: 1507-1517.
50. Rue CA, Jarvis MA, Knoche AJ, Meyers HL, DeFilippis VR, et al. (2004) A cyclooxygenase-2 homologue encoded by rhesus cytomegalovirus is a determinant for endothelial cell tropism. J Virol 78: 12529-12536.