Regulation of host gene expression by HIV-1 TAR microRNAs

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Ouellet, Dominique L ^a,b,c   Vigneault Edwards, Jimmy ^b,c   Létourneau, Kevin ^b,c   Gobeil, Lise Andrée ^b,c   Plante, Isabelle ^b,c   Burnett, John C ^a   Rossi, John J ^a   Provost, Patrick ^b,c  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b University Laval   (Canada)

^c UNIVERSITÉ LAVAL   (Canada)

Author keywords

Aiolos; Apoptosis; Caspase 8; HIV 1; Ikaros; Nucleophosmin (NPM) B23; TAR microRNAs

Indexed keywords

ARGONAUTE PROTEIN; CASPASE 8; IKAROS TRANSCRIPTION FACTOR; MESSENGER RNA; MICRORNA; NUCLEOPHOSMIN; PROTEIN AIOLOS; UNCLASSIFIED DRUG; VIRUS PROTEIN;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; BIOINFORMATICS; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN IMMUNODEFICIENCY VIRUS 1; LEUKEMIA CELL LINE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROVIRUS; REPORTER GENE; RNA STRUCTURE; T LYMPHOCYTE; TRANSACTIVATING RESPONSE ELEMENT; TRANSCRIPTION REGULATION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

APOPTOSIS; GENE EXPRESSION REGULATION; HIV LONG TERMINAL REPEAT; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MICRORNAS; RNA PROCESSING, POST-TRANSCRIPTIONAL; VIRUS REPLICATION;

EID: 84881285298     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-86     Document Type: Article

References (74)

1. Han J, et al. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 2004, 18(24):3016-27. 10.1101/gad.1262504, 535913, 15574589.
2. Bernstein E, et al. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409(6818):363-6. 10.1038/35053110, 11201747.
3. Provost P, et al. Ribonuclease activity and RNA binding of recombinant human Dicer. Embo J 2002, 21(21):5864-74. 10.1093/emboj/cdf578, 131075, 12411504.
4. Zhang H, et al. Human Dicer preferentially cleaves dsRNAs at their termini without a requirement for ATP. Embo J 2002, 21(21):5875-85. 10.1093/emboj/cdf582, 131079, 12411505.
5. Liu J, et al. Argonaute2 is the catalytic engine of mammalian RNAi. Science 2004, 305(5689):1437-41. 10.1126/science.1102513, 15284456.
6. Chendrimada TP, et al. TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 2005, 436(7051):740-4. 10.1038/nature03868, 2944926, 15973356.
7. Gregory RI, et al. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005, 123(4):631-40. 10.1016/j.cell.2005.10.022, 16271387.
8. Janowski BA, et al. Involvement of AGO1 and AGO2 in mammalian transcriptional silencing. Nat Struct Mol Biol 2006, 13(9):787-92. 10.1038/nsmb1140, 16936728.
9. Brennecke J, et al. Principles of microRNA-target recognition. PLoS Biol 2005, 3(3):e85. 10.1371/journal.pbio.0030085, 1043860, 15723116.
10. Dingwall C, et al. Human immunodeficiency virus 1 tat protein binds trans-activation-responsive region (TAR) RNA in vitro. Proc Natl Acad Sci U S A 1989, 86(18):6925-9. 10.1073/pnas.86.18.6925, 297963, 2476805.
11. Berkhout B, Silverman RH, Jeang KT. Tat trans-activates the human immunodeficiency virus through a nascent RNA target. Cell 1989, 59(2):273-82. 10.1016/0092-8674(89)90289-4, 2478293.
12. Laspia MF, Rice AP, Mathews MB. HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 1989, 59(2):283-92. 10.1016/0092-8674(89)90290-0, 2553266.
13. Kessler M, Mathews MB. Premature termination and processing of human immunodeficiency virus type 1-promoted transcripts. J Virol 1992, 66(7):4488-96. 241258, 1602555.
14. Williams SA, et al. NF-kappaB p50 promotes HIV latency through HDAC recruitment and repression of transcriptional initiation. EMBO J 2006, 25(1):139-49. 10.1038/sj.emboj.7600900, 1356344, 16319923.
15. Shapshak P. Molecule of the month: miRNA and HIV-1 TAR. Bioinformation 2013, 9(2):65-6. 10.6026/97320630009065, 3563399, 23390347.
16. Berkhout B. Structural features in TAR RNA of human and simian immunodeficiency viruses: a phylogenetic analysis. Nucleic Acids Res 1992, 20(1):27-31. 10.1093/nar/20.1.27, 310321, 1738599.
17. Berkhout B. Structure and function of the human immunodeficiency virus leader RNA. Prog Nucleic Acid Res Mol Biol 1996, 54:1-34.
18. Wilkinson KA, et al. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol 2008, 6(4):e96. 10.1371/journal.pbio.0060096, 2689691, 18447581.
19. Watts JM, et al. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 2009, 460(7256):711-6. 10.1038/nature08237, 2724670, 19661910.
20. Leonard JN, et al. HIV evades RNA interference directed at TAR by an indirect compensatory mechanism. Cell Host Microbe 2008, 4(5):484-94. 10.1016/j.chom.2008.09.008, 2742160, 18996348.
21. Klaver B, Berkhout B. Comparison of 5' and 3' long terminal repeat promoter function in human immunodeficiency virus. J Virol 1994, 68(6):3830-40. 236888, 8189520.
22. Das AT, Klaver B, Berkhout B. The 5' and 3' TAR elements of human immunodeficiency virus exert effects at several points in the virus life cycle. J Virol 1998, 72(11):9217-23. 110341, 9765469.
23. Ouellet DL, et al. Identification of functional microRNAs released through asymmetrical processing of HIV-1 TAR element. Nucleic Acids Res 2008, 36(7):2353-65. 10.1093/nar/gkn076, 2367715, 18299284.
24. Klase Z, et al. HIV-1 TAR element is processed by Dicer to yield a viral micro-RNA involved in chromatin remodeling of the viral LTR. BMC Mol Biol 2007, 8:63. 10.1186/1471-2199-8-63, 1955452, 17663774.
25. Wagschal A, et al. Microprocessor, Setx, Xrn2, and Rrp6 Co-operate to Induce Premature Termination of Transcription by RNAPII. Cell 2012, 150(6):1147-57. 10.1016/j.cell.2012.08.004, 3595997, 22980978.
26. Omoto S, et al. HIV-1 nef suppression by virally encoded microRNA. Retrovirology 2004, 1:44. 10.1186/1742-4690-1-44, 544868, 15601474.
27. Bennasser Y, et al. HIV-1 encoded candidate micro-RNAs and their cellular targets. Retrovirology 2004, 1:43. 10.1186/1742-4690-1-43, 544590, 15601472.
28. Narayanan A, et al. Analysis of the roles of HIV-derived microRNAs. Expert Opin Biol Ther 2011, 11(1):17-29. 10.1517/14712598.2011.540564, 21133815.
29. Klase Z, et al. HIV-1 TAR miRNA protects against apoptosis by altering cellular gene expression. Retrovirology 2009, 6:18. 10.1186/1742-4690-6-18, 2654423, 19220914.
30. Pfeffer S, et al. Identification of virus-encoded microRNAs. Science 2004, 304(5671):734-6. 10.1126/science.1096781, 15118162.
31. Choy EY, et al. An Epstein-Barr virus-encoded microRNA targets PUMA to promote host cell survival. J Exp Med 2008, 205(11):2551-60. 10.1084/jem.20072581, 2571930, 18838543.
32. Narayanan A, et al. Exosomes derived from HIV-1 infected cells contain TAR RNA. J Biol Chem 2013, 288(27):20014-33. 10.1074/jbc.M112.438895, 23661700.
33. Roshal M, Zhu Y, Planelles V. Apoptosis in AIDS. Apoptosis 2001, 6(1-2):103-16.
34. Varbanov M, Espert L, Biard-Piechaczyk M. Mechanisms of CD4 T-cell depletion triggered by HIV-1 viral proteins. AIDS Rev 2006, 8(4):221-36.
35. Genini D, et al. HIV induces lymphocyte apoptosis by a p53-initiated, mitochondrial-mediated mechanism. FASEB J 2001, 15(1):5-6.
36. Petit F, et al. Productive HIV-1 infection of primary CD4+ T cells induces mitochondrial membrane permeabilization leading to a caspase-independent cell death. J Biol Chem 2002, 277(2):1477-87. 10.1074/jbc.M102671200, 11689551.
37. Fevrier M, Dorgham K, Rebollo A. CD4+ T cell depletion in human immunodeficiency virus (HIV) infection: role of apoptosis. Viruses 2011, 3(5):586-612. 3185763, 21994747.
38. Maelfait J, Beyaert R. Non-apoptotic functions of caspase-8. Biochem Pharmacol 2008, 76(11):1365-73. 10.1016/j.bcp.2008.07.034, 18761323.
39. John LB, Ward AC. The Ikaros gene family: transcriptional regulators of hematopoiesis and immunity. Mol Immunol 2011, 48(9-10):1272-8.
40. Colombo E, Alcalay M, Pelicci PG. Nucleophosmin and its complex network: a possible therapeutic target in hematological diseases. Oncogene 2011, 30(23):2595-609. 10.1038/onc.2010.646, 21278791.
41. Plante I, et al. Dicer-derived microRNAs are utilized by the fragile X mental retardation protein for assembly on target RNAs. J Biomed Biotechnol 2006, 2006(4):64347. 1698263, 17057366.
42. Okuwaki M, Tsujimoto M, Nagata K. The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycle-dependent kinase and by association with its subtype. Mol Biol Cell 2002, 13(6):2016-30. 10.1091/mbc.02-03-0036, 117621, 12058066.
43. Brodersen P, Voinnet O. Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 2009, 10(2):141-8.
44. Ouellet DL, Provost P. Current knowledge of MicroRNAs and noncoding RNAs in virus-infected cells. Methods Mol Biol 2010, 623:35-65. 10.1007/978-1-60761-588-0_3, 2906133, 20217543.
45. Jordan A, Bisgrove D, Verdin E. HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. EMBO J 2003, 22(8):1868-77. 10.1093/emboj/cdg188, 154479, 12682019.
46. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136(2):215-33. 10.1016/j.cell.2009.01.002, 19167326.
47. Billot K, et al. Differential aiolos expression in human hematopoietic subpopulations. Leuk Res 2010, 34(3):289-93. 10.1016/j.leukres.2009.05.016, 19540588.
48. Lazebnik YA, et al. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 1994, 371(6495):346-7. 10.1038/371346a0, 8090205.
49. Li Q, et al. Microarray analysis of lymphatic tissue reveals stage-specific, gene expression signatures in HIV-1 infection. J Immunol 2009, 183(3):1975-82. 10.4049/jimmunol.0803222, 3552354, 19596987.
50. Triboulet R, et al. Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 2007, 315(5818):1579-82. 10.1126/science.1136319, 17322031.
51. Friedrich BM, et al. Host factors mediating HIV-1 replication. Virus Res 2011, 161(2):101-14. 10.1016/j.virusres.2011.08.001, 21871504.
52. Zhou H, et al. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 2008, 4(5):495-504. 10.1016/j.chom.2008.10.004, 18976975.
53. Konig R, et al. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 2008, 135(1):49-60. 10.1016/j.cell.2008.07.032, 2628946, 18854154.
54. Dueck A. microRNAs associated with the different human Argonaute proteins. Nucleic Acids Res 2012, 40(19):9850-62. 10.1093/nar/gks705, 3479175, 22844086.
55. Wee LM, et al. Argonaute divides its RNA guide into domains with distinct functions and RNA-binding properties. Cell 2012, 151(5):1055-67. 10.1016/j.cell.2012.10.036, 3595543, 23178124.
56. Chan EY, et al. Dynamic host energetics and cytoskeletal proteomes in human immunodeficiency virus type 1-infected human primary CD4 cells: analysis by multiplexed label-free mass spectrometry. J Virol 2009, 83(18):9283-95. 10.1128/JVI.00814-09, 2738255, 19587052.
57. Navare AT, et al. Quantitative proteomic analysis of HIV-1 infected CD4+ T cells reveals an early host response in important biological pathways: protein synthesis, cell proliferation, and T-cell activation. Virology 2012, 429(1):37-46. 10.1016/j.virol.2012.03.026, 3358407, 22542004.
58. Thorne N, Inglese J, Auld DS. Illuminating insights into firefly luciferase and other bioluminescent reporters used in chemical biology. Chem Biol 2010, 17(6):646-57. 10.1016/j.chembiol.2010.05.012, 2925662, 20609414.
59. Yamakuchi M, Ferlito M, Lowenstein CJ. miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A 2008, 105(36):13421-6. 10.1073/pnas.0801613105, 2533205, 18755897.
60. Guo H, et al. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466(7308):835-40. 10.1038/nature09267, 2990499, 20703300.
61. Huang V, et al. Upregulation of Cyclin B1 by miRNA and its implications in cancer. Nucleic Acids Res 2012, 40(4):1695-707. 10.1093/nar/gkr934, 3287204, 22053081.
62. Li LC, et al. Small dsRNAs induce transcriptional activation in human cells. Proc Natl Acad Sci U S A 2006, 103(46):17337-42. 10.1073/pnas.0607015103, 1859931, 17085592.
63. Bartz SR, Emerman M. Human immunodeficiency virus type 1 Tat induces apoptosis and increases sensitivity to apoptotic signals by up-regulating FLICE/caspase-8. J Virol 1999, 73(3):1956-63. 104437, 9971775.
64. Nie Z, et al. Human immunodeficiency virus type 1 protease cleaves procaspase 8 in vivo. J Virol 2007, 81(13):6947-56. 10.1128/JVI.02798-06, 1933285, 17442709.
65. Pulte D, et al. Ikaros increases normal apoptosis in adult erythroid cells. Am J Hematol 2006, 81(1):12-8. 10.1002/ajh.20507, 16369973.
66. He LC, et al. Ikaros is degraded by proteasome-dependent mechanism in the early phase of apoptosis induction. Biochem Biophys Res Commun 2011, 406(3):430-4. 10.1016/j.bbrc.2011.02.062, 21329675.
67. Rebollo A, et al. The association of Aiolos transcription factor and Bcl-xL is involved in the control of apoptosis. J Immunol 2001, 167(11):6366-73.
68. Romero F, et al. Aiolos transcription factor controls cell death in T cells by regulating Bcl-2 expression and its cellular localization. Embo J 1999, 18(12):3419-30. 10.1093/emboj/18.12.3419, 1171421, 10369681.
69. Li YP. Protein B23 is an important human factor for the nucleolar localization of the human immunodeficiency virus protein Tat. J Virol 1997, 71(5):4098-102. 191564, 9094689.
70. Fankhauser C, et al. Specific complex of human immunodeficiency virus type 1 rev and nucleolar B23 proteins: dissociation by the Rev response element. Mol Cell Biol 1991, 11(5):2567-75. 360026, 2017166.
71. Perkins A, et al. Structural and functional characterization of the human immunodeficiency virus rev protein. J Acquir Immune Defic Syndr 1989, 2(3):256-63.
72. Gadad SS, et al. HIV-1 infection induces acetylation of NPM1 that facilitates Tat localization and enhances viral transactivation. J Mol Biol 2011, 410(5):997-1007. 10.1016/j.jmb.2011.04.009, 21763502.
73. Meister G, et al. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 2004, 15(2):185-97. 10.1016/j.molcel.2004.07.007, 15260970.
74. Landry P, et al. Existence of a microRNA pathway in anucleate platelets. Nat Struct Mol Biol 2009, 16(9):961-6. 10.1038/nsmb.1651, 2911476, 19668211.