Mammalian microRNAs: Post-transcriptional gene regulation in RNA virus infection and therapeutic applications

Frontiers in Microbiology

Volumn 1, Issue OCT, 2010, Pages

  Tsunetsugu Yokota, Yasuko ^a   Yamamoto, Takuya ^b  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Gene therapy; Host virus interaction; Mammalian microRNAs; RNA virus infection

Indexed keywords

EID: 84875359231     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2010.00108     Document Type: Review

References (71)

1. Baek, D., Villen, J., Shin, C., Camargo, F. D., Gygi, S. P., and Bartel, D. P. (2008). The impact of microRNAs on protein output. Nature 455, 64-71.
2. Baltimore, D., Boldin, M. P., O'Connell, R. M., Rao, D. S., and Taganov, K. D. (2008). MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 9, 839-845.
3. Barnes, D., Kunitomi, M., Vignuzzi, M., Saksela, K., and Andino, R. (2008). Harnessing endogenous miRNAs to control virus tissue tropism as a strategy for developing attenuated virus vaccines. Cell Host Microbe 4, 239-248.
4. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
5. Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
6. 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.
7. Berkhout, B., and Jeang, K. T. (2007). RISCy business: microRNAs, pathogenesis, and viruses. J. Biol. Chem. 282, 26641-26645.
8. Bernstein, E., Caudy, A. A., Hammond, S. M., and Hannon, G. J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366.
9. Bernstein, E., Kim, S. Y., Carmell, M. A., Murchison, E. P., Alcorn, H., Li, M. Z., Mills, A. A., Elledge, S. J., Anderson, K. V., and Hannon, G. J. (2003). Dicer is essential for mouse development. Nat. Genet. 35, 215-217.
10. Boland, A., Tritschler, F., Heimstadt, S., Izaurralde, E., and Weichenrieder, O. (2010). Crystal structure and ligand binding of the MID domain of a eukaryotic Argonaute protein. EMBO Rep. 11, 522-527.
11. Boss, I. W., Plaisance, K. B., and Renne, R. (2009). Role of virus-encoded microRNAs in herpesvirus biology. Trends Microbiol. 17, 544-553.
12. Britten, R. J., and Davidson, E. H. (1969). Gene regulation for higher cells: a theory. Science 165, 349-357.
13. Brown, B. D., Cantore, A., Annoni, A., Sergi, L. S., Lombardo, A., Della Valle, P. D'Angelo, A., and Naldini, L. (2007). A microRNA-regulated lentiviral vector mediates stable correction of hemophilia B mice. Blood 110, 4144-4152.
14. Brown, B. D., Gentner, B., Cantore, A., Colleoni, S., Amendola, M., Zingale, A. Baccarini, A., Lazzari, G. Galli, C., and Naldini, L. (2007). Endogenous microRNA can be broadly exploited to regulate transgene expression according to tissue, lineage and differentiation state. Nat. Biotechnol. 25, 1457-1467.
15. Cawood, R., Chen, H., Carroll, F., Bazan-Peregrino, M., van Rooijen, N., and Seymour, L. W. (2009). Use of tissue-specific microRNA to control pathology of wild-type adenovirus without attenuation of its ability to kill cancer cells. PLoS Pathog. 5, e1000440. doi:10.1371/journal.ppat.1000440.
16. Chendrimada, T. P., Gregory, R. I., Kumaraswamy, E., Norman, J., Cooch, N., Nishikura, K., and Shiekhattar, R. (2005). TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature 436, 740-744.
17. Choudhuri, S. (2009). Lesser known relatives of miRNA. Biochem. Biophys. Res. Commun. 388, 177-180.
18. Cobb, B. S., Nesterova, T. B., Thompson, E., Hertweck, A., O'Connor, E., Godwin, J., Wilson, C. B., Brockdorff, N., Fisher, A. G., Smale, S. T., and Merkenschlager, M. (2005). T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J. Exp. Med. 201, 1367-1373.
19. Croce, C. M. (2009). Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 10, 704-714.
20. Cullen, B. R. (2009). Viral and cellular messenger RNA targets of viral microRNAs. Nature 457, 421-425.
21. Cullen, B. R. (2010). Five questions about viruses and microRNAs. PLoS Pathog. 6, e1000787. doi:10.1371/journal.ppat.1000787.
22. Daniels, S. M., Melendez-Pena, C. E., Scarborough, R. J., Daher, A., Christensen, H. S., El Far, M., Purcell, D. F., Laine, S., and Gatignol, A. (2009). Characterization of the TRBP domain required for dicer interaction and function in RNA interference. BMC Mol. Biol. 10, 38.
23. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811.
24. Gottwein, E., and Cullen, B. R. (2008). Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 3, 375-387.
25. Haase, A. D., Jaskiewicz, L., Zhang, H., Laine, S., Sack, R., Gatignol, A., and Filipowicz, W. (2005). TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep. 6, 961-967.
26. Haasnoot, J., de Vries, W., Geutjes, E. J., Prins, M., de Haan, P., and Berkhout, B. (2007). The Ebola virus VP35 protein is a suppressor of RNA silencing. PLoS Pathog. 3, e86. doi:10.1371/journal. ppat.0030086.
27. Han, J., Lee, Y., Yeom, K. H., Nam, J. W., Heo, I., Rhee, J. K., Sohn, S. Y., Cho, Y., Zhang, B. T., and Kim, V. N. (2006). Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125, 887-901.
28. Hashimi, S. T., Fulcher, J. A., Chang, M. H., Gov, L., Wang, S., and Lee, B. (2009). MicroRNA profiling identifies miR-34a and miR-21 and their target genes JAG1 and WNT1 in the coordinate regulation of dendritic cell differentiation. Blood 114, 404-414.
29. 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.
30. Jinek, M., and Doudna, J. A. (2009). A three-dimensional view of the molecular machinery of RNA interference. Nature 457, 405-412.
31. Jopling, C. L., Schutz, S., and Sarnow, P. (2008). Position-dependent function for a tandem microRNA miR-122-binding site located in the hepatitis C virus RNA genome. Cell Host Microbe 4, 77-85.
32. 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.
33. Kash, J. C., Tumpey, T. M., Proll, S. C., Carter, V., Perwitasari, O., Thomas, M. J., Basler, C. F., Palese, P., Taubenberger, J. K., Garcia-Sastre, A., Swayne, D. E., and Katze, M. G. (2006). Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443, 578-581.
34. Kelly, E. J., Hadac, E. M., Greiner, S., and Russell, S. J. (2008). Engineering microRNA responsiveness to decrease virus pathogenicity. Nat. Med. 14, 1278-1283.
35. Kelly, E. J., Nace, R., Barber, G. N., and Russell, S. J. (2010). Attenuation of vesicular stomatitis virus encephalitis through microRNA targeting. J. Virol. 84, 1550-1562.
36. Kok, K. H., Ng, M. H. Ching, Y. P., and Jin, D. Y. (2007). Human TRBP and PACT directly interact with each other and associate with dicer to facilitate the production of small interfering RNA. J. Biol. Chem. 282, 17649-17657.
37. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A. O., Landthaler, M., Lin, C., Socci, N. D., Hermida, L., Fulci, V., Chiaretti, S., Foa, R., Schliwka, J., Fuchs, U., Novosel, A., Muller, R. U., Schermer, B., Bissels, U., Inman, J., Phan, Q., Chien, M., Weir, D. B., Choksi, R., De Vita, G., Frezzetti, D., Trompeter, H. I., Hornung, V., Teng, G., Hartmann, G., Palkovits, M., Di Lauro, R., Wernet, P., Macino, G., Rogler, C. E., Nagle, J. W., Ju, J., Papavasiliou, F. N., Benzing, T., Lichter, P., Tam, W. Brownstein, M. J. Bosio, A. Borkhardt, A. Russo, J. J. Sander, C. Zavolan, M., and Tuschl, T. (2007). A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129, 1401-1414.
38. Lanford, R. E., Hildebrandt-Eriksen, E. S., Petri, A., Persson, R., Lindow, M., Munk, M. E., Kauppinen, S., and Orum, H. (2010). Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science 327, 198-201.
39. 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.
40. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim S., and Kim, V. N. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419.
41. Lee, Y., Hur, I., Park, S. Y., Kim, Y. K., Suh, M. R., and Kim, V. N. (2006). The role of PACT in the RNA silencing pathway. EMBO J. 25, 522-532.
42. Lewin, B. (2004). Genes. Upper Saddle River, NJ: Pearson Education, Inc.
43. 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.
44. Li, Y., Chan, E. Y., Li, J., Ni, C., Peng, X., Rosenzweig, E., Tumpey, T. M., and Katze, M. G. (2010). MicroRNA expression and virulence in pandemic influenza virus-infected mice. J. Virol. 84, 3023-3032.
45. Liou, L. Y., Herrmann, C. H., and Rice, A. P. (2002). Transient induction of cyclin T1 during human macrophage differentiation regulates human immunodeficiency virus type 1 Tat transactivation function. J. Virol. 76, 10579-10587.
46. Lodish, H. F., Zhou, B. Liu, G., and Chen, C. Z. (2008). Micromanagement of the immune system by microRNAs. Nat. Rev. Immunol. 8, 120-130.
47. Lund, E., Guttinger, S., Calado, A., Dahlberg, J. E., and Kutay, U. (2004). Nuclear export of microRNA precursors. Science 303, 95-98.
48. Macrae, I. J., Zhou, K. Li, F., Repic, A., Brooks, A. N., Cande, W. Z., Adams, P. D., and Doudna, J. A. (2006). Structural basis for double-stranded RNA processing by Dicer. Science 311, 195-198.
49. Matskevich, A. A., and Moelling, K. (2007). Dicer is involved in protection against influenza A virus infection. J. Gen. Virol. 88, 2627-2635.
50. Morris, K. V., and Rossi, J. J. (2006). Lentiviral-mediated delivery of siRNAs for antiviral therapy. Gene Ther. 13, 553-558.
51. Muljo, S. A., Ansel, K. M., Kanellopoulou, C., Livingston, D. M., Rao, A., and Rajewsky, K. (2005). Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 202, 261-269.
52. O'Connell, R. M., Rao, D. S., Chaudhuri, A. A., and Baltimore, D. (2010). Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111-122.
53. Otsuka, M., Jing, Q. Georgel, P., New, L., Chen, J., Mols, J., Kang, Y. J., Jiang, Z., Du, X., Cook, R., Das, S. C. Pattnaik, A. K., Beutler, B., and Han, J. (2007). Hypersusceptibility to vesicular stomatitis virus infection in Dicer1-deficient mice is due to impaired miR24 and miR93 expression. Immunity 27, 123-134.
54. Pedersen, I. M., Cheng, G., Wieland, S., Volinia, S., Croce, C. M., Chisari, F. V., and David, M. (2007). Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449, 919-922.
55. Peng, G., Greenwell-Wild, T., Nares, S., Jin, W., Lei, K. J., Rangel, Z. G., Munson, P. J., and Wahl, S. M. (2007). Myeloid differentiation and susceptibility to HIV-1 are linked to APOBEC3 expression. Blood 110, 393-400.
56. Perez, J. T., Pham, A. M., Lorini, M. H., Chua, M. A., Steel, J., and tenOever, B. R. (2009). MicroRNA-mediated species-specific attenuation of influenza A virus. Nat. Biotechnol. 27, 572-576.
57. Peters, L., and Meister, G. (2007). Argonaute proteins: mediators of RNA silencing. Mol. Cell 26, 611-623.
58. Rossi, J. J., June, C. H., and Kohn, D. B. (2007). Genetic therapies against HIV. Nat. Biotechnol. 25, 1444-1454.
59. Sarasin-Filipowicz, M., Krol, J., Markiewicz, I., Heim, M. H., and Filipowicz, W. (2009). Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat. Med. 15, 31-33.
60. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R., and Rajewsky, N. (2008). Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63.
61. Sohn, S. Y., Bae, W. J., Kim, J. J., Yeom, K. H., Kim, V. N., and Cho, Y. (2007). Crystal structure of human DGCR8 core. Nat. Struct. Mol. Biol. 14, 847-853.
62. 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. doi:10.1371/journal. ppat.1000263.
63. Triboulet, R., Mari, B., Lin, Y. L., Chable-Bessia, C., Bennasser, Y., Lebrigand, K., Cardinaud, B., Maurin, T., Barbry, P., Baillat, V., Reynes, J., Corbeau, P., Jeang, K. T., and Benkirane, M. (2007). Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 315, 1579-1582.
64. Tsunetsugu-Yokota, Y. (2008). "Transmission of HIV from dendritic cells to CD4+ T cells: a promising target for vaccination and therapeutic intervention," in AIDS Vaccines, HIV Receptors and AIDS Research, ed. L. B. Kendow (New York: Nova Science Publishers, Inc.), 117-128.
65. Wang, X., Ye, L., Hou, W., Zhou, Y., Wang, Y. J., Metzger, D. S., and Ho, W. Z. (2009). Cellular microRNA expression correlates with susceptibility of monocytes/macrophages to HIV-1 infection. Blood 113, 671-674.
66. Wang, Y., Sheng, G., Juranek, S., Tuschl, T., and Patel, D. J. (2008). Structure of the guide-strand-containing argonaute silencing complex. Nature 456, 209-213.
67. Winter, J., Jung, S., Keller, S., Gregory, R. I., and Diederichs, S. (2009). Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat. Cell Biol. 11, 228-234.
68. Wu, H., Neilson, J. R., Kumar, P., Manocha, M., Shankar, P., Sharp, P. A., and Manjunath, N. (2007). miRNA profiling of naive, effector and memory CD8 T cells. PLoS One 2, e1020. doi:10.1371/journal.pone.0001020.
69. Xiao, C., and Rajewsky, K. (2009). MicroRNA control in the immune system: basic principles. Cell 136, 26-36.
70. Yamamoto, T., and Tsunetsugu-Yokota, Y. (2008). Prospects for the therapeutic application of lentivirus-based gene therapy to HIV-1 infection. Curr. Gene Ther. 8, 1-8.
71. Zamore, P. D., and Haley, B. (2005). Ribo-gnome: the big world of small RNAs. Science 309, 1519-1524.