Interplay between HIV-1 infection and host microRNAs

Nucleic Acids Research

Volumn 40, Issue 5, 2012, Pages 2181-2196

  Sun, Guihua ^a   Li, Haitang ^a   Wu, Xiwei ^a   Covarrubias, Maricela ^a   Scherer, Lisa ^a   Meinking, Keith ^a   Luk, Brian ^a   Chomchan, Pritsana ^a   Alluin, Jessica ^a   Gombart, Adrian F ^b   Rossi, John J ^a  

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

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; MICRORNA; MICRORNA 155; MICRORNA 21; MICRORNA 223; MICRORNA 29; MICRORNA 29A; MICRORNA 29B; NEF PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; APOPTOSIS; ARTICLE; BINDING SITE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; LONG TERMINAL REPEAT; MICROARRAY ANALYSIS; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA BINDING; RNA STRUCTURE; UPREGULATION; VIRUS CELL INTERACTION; VIRUS GENE;

BINDING SITES; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; MICRORNAS; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; RNA INTERFERENCE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84863346515     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr961     Document Type: Article

References (85)

1. Dennis, C. (2002) Small RNAs: the genome's guiding hand? Nature, 420, 732.
2. Lecellier, C. H., Dunoyer, P., Arar, K., Lehmann-Che, J., Eyquem, S., Himber, C., Saib, A. and Voinnet, O. (2005) A cellular microRNA mediates antiviral defense in human cells. Science, 308, 557-560.
3. Jopling, C. L., Yi, M., Lancaster, A. M., Lemon, S. M. and Sarnow, P. (2005) Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science, 309, 1577-1581.
4. Hariharan, M., Scaria, V., Pillai, B. and Brahmachari, S. K. (2005) Targets for human encoded microRNAs in HIV genes. Biochem. Biophys. Res. Commun., 337, 1214-1218.
5. Bennasser, Y., Le, S. Y., Benkirane, M. and Jeang, K. T. (2005) Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity, 22, 607-619.
6. Bennasser, Y. and Jeang, K. T. (2006) HIV-1 Tat interaction with Dicer: requirement for RNA. Retrovirology, 3, 95.
7. Triboulet, R., Mari, B., Lin, Y. L., Chable-Bessia, C., Bennasser, Y., Lebrigand, K., Cardinaud, B., Maurin, T., Barbry, P., Baillat, V. et al. (2007) Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science, 315, 1579-1582.
8. Huang, J., Wang, F., Argyris, E., Chen, K., Liang, Z., Tian, H., Huang, W., Squires, K., Verlinghieri, G. and Zhang, H. (2007) Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+T lymphocytes. Nat. Med., 13, 1241-1247.
9. Houzet, L., Yeung, M. L., de Lame, V., Desai, D., Smith, S. M. and Jeang, K. T. (2008) MicroRNA profile changes in human immunodeficiency virus type 1 (HIV-1) seropositive individuals. Retrovirology, 5, 118.
10. Pichler, K., Schneider, G. and Grassmann, R. (2008) MicroRNA miR-146a and further oncogenesis-related cellular microRNAs are dysregulated in HTLV-1-transformed T lymphocytes. Retrovirology, 5, 100.
11. Bellon, M., Lepelletier, Y., Hermine, O. and Nicot, C. (2009) Deregulation of micro-RNA involved in hematopoiesis and the immune response in HTLV-I adult T-cell leukemia. Blood., 113, 4914-4917.
12. Nathans, R., Chu, C. Y., Serquina, A. K., Lu, C. C., Cao, H. and Rana, T. M. (2009) Cellular microRNA and P bodies modulate host-HIV-1 interactions. Mol. Cell, 34, 696-709.
13. Mattapallil, J. J., Douek, D. C., Hill, B., Nishimura, Y., Martin, M. and Roederer, M. (2005) Massive infection and loss of memory CD4+T cells in multiple tissues during acute SIV infection. Nature, 434, 1093-1097.
14. Li, Q., Duan, L., Estes, J. D., Ma, Z. M., Rourke, T., Wang, Y., Reilly, C., Carlis, J., Miller, C. J. and Haase, A. T. (2005) Peak SIV replication in resting memory CD4+T cells depletes gut lamina propria CD4+T cells. Nature, 434, 1148-1152.
15. Sun, G., Yan, J., Noltner, K., Feng, J., Li, H., Sarkis, D. A., Sommer, S. S. and Rossi, J. J. (2009) SNPs in human miRNA genes affect biogenesis and function. RNA., 15, 1640-1651.
16. Whitfield, M. L., Sherlock, G., Saldanha, A. J., Murray, J. I., Ball, C. A., Alexander, K. E., Matese, J. C., Perou, C. M., Hurt, M. M., Brown, P. O. et al. (2002) Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol. Biol. Cell, 13, 1977-2000.
17. Dunn, W., Trang, P., Zhong, Q., Yang, E., van Belle, C. and Liu, F. (2005) Human cytomegalovirus expresses novel microRNAs during productive viral infection. Cell. Microbiol., 7, 1684-1695.
18. Sun, G., Li, H. and Rossi, J. J. (2009) Sequence context outside the target region influences the effectiveness of miR-223 target sites in the RhoB 3'UTR. Nucleic Acids Res., 38, 239-252.
19. Ritchie, M. E., Silver, J., Oshlack, A., Holmes, M., Diyagama, D., Holloway, A. and Smyth, G. K. (2007) A comparison of background correction methods for two-colour microarrays. Bioinformatics, 23, 2700-2707.
20. Eisen, M. B., Spellman, P. T., Brown, P. O. and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl Acad. Sci. USA, 95, 14863-14868.
21. Saldanha, A. J. (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics, 20, 3246-3248.
22. Schmittgen, T. D. and Livak, K. J. (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc., 3, 1101-1108.
23. Lewis, B. P., Burge, C. B. and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell, 120, 15-20.
24. Grimson, A., Farh, K. K., Johnston, W. K., Garrett-Engele, P., Lim, L. P. and Bartel, D. P. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell, 27, 91-105.
25. Kertesz, M., Iovino, N., Unnerstall, U., Gaul, U. and Segal, E. (2007) The role of site accessibility in microRNA target recognition. Nat. Genet., 39, 1278-1284.
26. Betel, D., Wilson, M., Gabow, A., Marks, D. S. and Sander, C. (2008) The microRNA. org resource: targets and expression. Nucleic Acids Res., 36, D149-D153.
27. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A. O., Landthaler, M. et al. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell, 129, 1401-1414.
28. Omoto, S. and Fujii, Y. R. (2005) Regulation of human immunodeficiency virus 1 transcription by nef microRNA. J. Gen. Virol., 86, 751-755.
29. Omoto, S., Ito, M., Tsutsumi, Y., Ichikawa, Y., Okuyama, H., Brisibe, E. A., Saksena, N. K. and Fujii, Y. R. (2004) HIV-1 nef suppression by virally encoded microRNA. Retrovirology, 1, 44.
30. Connor, R. I., Chen, B. K., Choe, S. and Landau, N. R. (1995) Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology, 206, 935-944.
31. He, J., Choe, S., Walker, R., Di Marzio, P., Morgan, D. O. and Landau, N. R. (1995) Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol., 69, 6705-6711.
32. Sung, T. L. and Rice, A. P. (2009) miR-198 inhibits HIV-1 gene expression and replication in monocytes and its mechanism of action appears to involve repression of cyclin T1. PLoS Pathog., 5, e1000263.
33. John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C. and Marks, D. S. (2004) Human MicroRNA targets. PLoS Biol., 2, e363.
34. Lewis, B. P., Shih, I. H., Jones-Rhoades, M. W., Bartel, D. P. and Burge, C. B. (2003) Prediction of mammalian microRNA targets. Cell, 115, 787-798.
35. Krek, A., Grun, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., MacMenamin, P., da Piedade, I., Gunsalus, K. C., Stoffel, M. et al. (2005) Combinatorial microRNA target predictions. Nat. Genet., 37, 495-500.
36. Fazi, F., Rosa, A., Fatica, A., Gelmetti, V., De Marchis, M. L., Nervi, C. and Bozzoni, I. (2005) A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell, 123, 819-831.
37. Rodriguez, P. L., Sahay, S., Olabisi, O. O. and Whitehead, I. P. (2007) ROCK I-mediated activation of NF-kappaB by RhoB. Cell Signal., 19, 2361-2369.
38. Chen, Y. X., Li, Z. B., Diao, F., Cao, D. M., Fu, C. C. and Lu, J. (2006) Up-regulation of RhoB by glucocorticoids and its effects on the cell proliferation and NF-kappaB transcriptional activity. J. Steroid. Biochem. Mol. Biol., 101, 179-187.
39. Zhang, J., Zhu, J., Bu, X., Cushion, M., Kinane, T. B., Avraham, H. and Koziel, H. (2005) Cdc42 and RhoB activation are required for mannose receptor-mediated phagocytosis by human alveolar macrophages. Mol. Biol. Cell, 16, 824-834.
40. Sheehy, A. M., Gaddis, N. C., Choi, J. D. and Malim, M. H. (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature, 418, 646-650.
41. Muckenfuss, H., Kaiser, J. K., Krebil, E., Battenberg, M., Schwer, C., Cichutek, K., Munk, C. and Flory, E. (2007) Sp1 and Sp3 regulate basal transcription of the human APOBEC3G gene. Nucleic Acids Res., 35, 3784-3796.
42. Tjernlund, A., Barqasho, B., Nowak, P., Kinloch, S., Thorborn, D., Perrin, L., Sonnerborg, A., Walther-Jallow, L. and Andersson, J. (2006) Early induction of leukemia inhibitor factor (LIF) in acute HIV-1 infection. Aids, 20, 11-19.
43. Tjernlund, A., Walther-Jallow, L., Behbahani, H., Screpanti, V., Nowak, P., Grandien, A., Andersson, J. and Patterson, B. K. (2007) Leukemia inhibitor factor (LIF) inhibits HIV-1 replication via restriction of stat 3 activation. AIDS Res. Hum. Retroviruses, 23, 398-406.
44. Patterson, B. K., Behbahani, H., Kabat, W. J., Sullivan, Y., O'Gorman, M. R., Landay, A., Flener, Z., Khan, N., Yogev, R. and Andersson, J. (2001) Leukemia inhibitory factor inhibits HIV-1 replication and is upregulated in placentae from nontransmitting women. J. Clin. Invest., 107, 287-294.
45. Fabbri, M., Garzon, R., Cimmino, A., Liu, Z., Zanesi, N., Callegari, E., Liu, S., Alder, H., Costinean, S., Fernandez-Cymering, C. et al. (2007) MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc. Natl Acad. Sci. USA, 104, 15805-15810.
46. Mott, J. L., Kobayashi, S., Bronk, S. F. and Gores, G. J. (2007) mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene, 26, 6133-6140.
47. Pekarsky, Y., Santanam, U., Cimmino, A., Palamarchuk, A., Efanov, A., Maximov, V., Volinia, S., Alder, H., Liu, C. G., Rassenti, L. et al. (2006) Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res., 66, 11590-11593.
48. Park, S. Y., Lee, J. H., Ha, M., Nam, J. W. and Kim, V. N. (2009) miR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat. Struct. Mol. Biol., 16, 23-29.
49. Johnston, J. B., Paul, J. T., Neufeld, N. J., Haney, N., Kropp, D. M., Hu, X., Cheang, M. and Gibson, S. B. (2004) Role of myeloid cell factor-1 (Mcl-1) in chronic lymphocytic leukemia. Leuk. Lymphoma, 45, 2017-2027.
50. Lu, X., Wu, X., Plemenitas, A., Yu, H., Sawai, E. T., Abo, A. and Peterlin, B. M. (1996) CDC42 and Rac1 are implicated in the activation of the Nef-associated kinase and replication of HIV-1. Curr. Biol., 6, 1677-1684.
51. Manninen, A., Hiipakka, M., Vihinen, M., Lu, W., Mayer, B. J. and Saksela, K. (1998) SH3-Domain binding function of HIV-1 Nef is required for association with a PAK-related kinase. Virology, 250, 273-282.
52. Fackler, O. T., Lu, X., Frost, J. A., Geyer, M., Jiang, B., Luo, W., Abo, A., Alberts, A. S. and Peterlin, B. M. (2000) p21-activated kinase 1 plays a critical role in cellular activation by Nef. Mol. Cell. Biol., 20, 2619-2627.
53. Renkema, G. H., Manninen, A. and Saksela, K. (2001) Human immunodeficiency virus type 1 Nef selectively associates with a catalytically active subpopulation of p21-activated kinase 2 (PAK2) independently of PAK2 binding to Nck or beta-PIX. J. Virol., 75, 2154-2160.
54. Sawalha, A. H. (2008) Epigenetics and T-cell immunity. Autoimmunity, 41, 245-252.
55. Pekarsky, Y., Koval, A., Hallas, C., Bichi, R., Tresini, M., Malstrom, S., Russo, G., Tsichlis, P. and Croce, C. M. (2000) Tcl1 enhances Akt kinase activity and mediates its nuclear translocation. Proc. Natl Acad. Sci. USA, 97, 3028-3033.
56. Laine, J., Kunstle, G., Obata, T., Sha, M. and Noguchi, M. (2000) The protooncogene TCL1 is an Akt kinase coactivator. Mol. Cell, 6, 395-407.
57. Noguchi, M., Ropars, V., Roumestand, C. and Suizu, F. (2007) Proto-oncogene TCL1: more than just a coactivator for Akt. FASEB J., 21, 2273-2284.
58. Boden, D., Pusch, O., Lee, F., Tucker, L. and Ramratnam, B. (2003) Human immunodeficiency virus type 1 escape from RNA interference. J. Virol., 77, 11531-11535.
59. Westerhout, E. M., Ooms, M., Vink, M., Das, A. T. and Berkhout, B. (2005) HIV-1 can escape from RNA interference by evolving an alternative structure in its RNA genome. Nucleic Acids Res., 33, 796-804.
60. Berkhout, B. and Sanders, R. W. (2011) Molecular strategies to design an escape-proof antiviral therapy. Antiviral Res., 92, 7-14.
61. Reynolds, A., Leake, D., Boese, Q., Scaringe, S., Marshall, W. S. and Khvorova, A. (2004) Rational siRNA design for RNA interference. Nat. Biotechnol., 22, 326-330.
62. Tafer, H., Ameres, S. L., Obernosterer, G., Gebeshuber, C. A., Schroeder, R., Martinez, J. and Hofacker, I. L. (2008) The impact of target site accessibility on the design of effective siRNAs. Nat. Biotechnol., 26, 578-583.
63. Watts, J. M., Dang, K. K., Gorelick, R. J., Leonard, C. W., Bess, J. W. Jr, Swanstrom, R., Burch, C. L. and Weeks, K. M. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature, 460, 711-716.
64. Chen, C. Z., Li, L., Lodish, H. F. and Bartel, D. P. (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science, 303, 83-86.
65. Fukao, T., Fukuda, Y., Kiga, K., Sharif, J., Hino, K., Enomoto, Y., Kawamura, A., Nakamura, K., Takeuchi, T. and Tanabe, M. (2007) An evolutionarily conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell, 129, 617-631.
66. Ambrosino, C., Ruocco, M. R., Chen, X., Mallardo, M., Baudi, F., Trematerra, S., Quinto, I., Venuta, S. and Scala, G. (1997) HIV-1 Tat induces the expression of the interleukin-6 (IL6) gene by binding to the IL6 leader RNA and by interacting with CAAT enhancer-binding protein beta (NF-IL6) transcription factors. J. Biol. Chem., 272, 14883-14892.
67. Roux, P., Alfieri, C., Hrimech, M., Cohen, E. A. and Tanner, J. E. (2000) Activation of transcription factors NF-kappaB and NF-IL-6 by human immunodeficiency virus type 1 protein R (Vpr) induces interleukin-8 expression. J. Virol., 74, 4658-4665.
68. Cossarizza, A. (2008) Apoptosis and HIV infection: about molecules and genes. Curr. Pharm. Des., 14, 237-244.
69. Geleziunas, R., Xu, W., Takeda, K., Ichijo, H. and Greene, W. C. (2001) HIV-1 Nef inhibits ASK1-dependent death signalling providing a potential mechanism for protecting the infected host cell. Nature, 410, 834-838.
70. Wang, H., Garzon, R., Sun, H., Ladner, K. J., Singh, R., Dahlman, J., Cheng, A., Hall, B. M., Qualman, S. J., Chandler, D. S. et al. (2008) NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell, 14, 369-381.
71. Kwon, H. S., Brent, M. M., Getachew, R., Jayakumar, P., Chen, L. F., Schnolzer, M., McBurney, M. W., Marmorstein, R., Greene, W. C. and Ott, M. (2008) Human immunodeficiency virus type 1 Tat protein inhibits the SIRT1 deacetylase and induces T cell hyperactivation. Cell Host Microbe, 3, 158-167.
72. Hwang, H. W., Wentzel, E. A. and Mendell, J. T. (2007) A hexanucleotide element directs microRNA nuclear import. Science, 315, 97-100.
73. Richardson, R. T., Batova, I. N., Widgren, E. E., Zheng, L. X., Whitfield, M., Marzluff, W. F. and O'Rand, M. G. (2000) Characterization of the histone H1-binding protein, NASP, as a cell cycle-regulated somatic protein. J. Biol. Chem., 275, 30378-30386.
74. Finn, R. M., Browne, K., Hodgson, K. C. and Ausio, J. (2008) sNASP, a histone H1-specific eukaryotic chaperone dimer that facilitates chromatin assembly. Biophys. J., 95, 1314-1325.
75. Richardson, R. T., Alekseev, O. M., Grossman, G., Widgren, E. E., Thresher, R., Wagner, E. J., Sullivan, K. D., Marzluff, W. F. and O'Rand, M. G. (2006) Nuclear autoantigenic sperm protein (NASP), a linker histone chaperone that is required for cell proliferation. J. Biol. Chem., 281, 21526-21534.
76. Re, F., Braaten, D., Franke, E. K. and Luban, J. (1995) Human immunodeficiency virus type 1 Vpr arrests the cell cycle in G2 by inhibiting the activation of p34cdc2-cyclin B. J. Virol., 69, 6859-6864.
77. Jowett, J. B., Planelles, V., Poon, B., Shah, N. P., Chen, M. L. and Chen, I. S. (1995) The human immunodeficiency virus type 1 vpr gene arrests infected T cells in the G2+M phase of the cell cycle. J. Virol., 69, 6304-6313.
78. Andersen, J. L., Le Rouzic, E. and Planelles, V. (2008) HIV-1 Vpr: mechanisms of G2 arrest and apoptosis. Exp. Mol. Pathol., 85, 2-10.
79. Poon, B., Chang, M. A. and Chen, I. S. (2007) Vpr is required for efficient Nef expression from unintegrated human immunodeficiency virus type 1 DNA. J. Virol., 81, 10515-10523.
80. Foster, J. L. and Garcia, J. V. (2008) HIV-1 Nef: at the crossroads. Retrovirology, 5, 84.
81. Yeung, M. L., Bennasser, Y., Myers, T. G., Jiang, G., Benkirane, M. and Jeang, K. T. (2005) Changes in microRNA expression profiles in HIV-1-transfected human cells. Retrovirology, 2, 81.
82. Ach, R. A., Wang, H. and Curry, B. (2008) Measuring microRNAs: comparisons of microarray and quantitative PCR measurements, and of different total RNA prep methods. BMC Biotechnol., 8, 69.
83. Ahluwalia, J. K., Khan, S. Z., Soni, K., Rawat, P., Gupta, A., Hariharan, M., Scaria, V., Lalwani, M., Pillai, B., Mitra, D. et al. (2008) Human cellular microRNA hsa-miR-29a interferes with viral nef protein expression and HIV-1 replication. Retrovirology, 5, 117.
84. Didiano, D. and Hobert, O. (2008) Molecular architecture of a miRNA-regulated 30 UTR. RNA, 14, 1297-1317.
85. Sun, G. and Rossi, J. J. (2009) Problems associated with reporter assays in RNAi studies. RNA Biol., 6, 406-411.