Adenovirus and miRNAs

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1809, Issue 11-12, 2011, Pages 660-667

  Carnero, Elena ^a   Sutherland, James D ^b   Fortes, Puri ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b CIC BIOGUNE   (Spain)

Author keywords

Adenovirus; miRNAs; RNAi; TIA 1; VA RNA

Indexed keywords

ADENOVIRUS VECTOR; ARGONAUTE PROTEIN; DICER; EXPORTIN 5; MICRORNA; VIRUS RNA;

ADENOVIRUS; ADENOVIRUS INFECTION; CELL PROLIFERATION; DNA REPAIR; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE SILENCING; HUMAN; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; RNA CLEAVAGE; RNA INTERFERENCE; VIRAL GENE THERAPY; VIRUS GENOME; VIRUS RECOMBINANT;

ADENOVIRIDAE; ANIMALS; DNA REPAIR; GENE SILENCING; GENOME, VIRAL; HUMANS; MICRORNAS; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA, VIRAL;

ADENOVIRIDAE;

EID: 80655144440     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2011.05.004     Document Type: Review

References (109)

1. Fabian M.R., Sonenberg N., Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 2010, 79:351-379.
2. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
3. Tomari Y., Zamore P.D. Perspective: machines for RNAi. Genes Dev. 2005, 19:517-529.
4. Kim V.N. MicroRNA biogenesis: coordinated cropping and dicing. Nat. Rev. Mol. Cell Biol. 2005, 6:376-385.
5. Kim V.N., Han J., Siomi M.C. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 2009, 10:126-139.
6. Medina P.P., Slack F.J. microRNAs and cancer: an overview. Cell Cycle 2008, 7:2485-2492.
7. Dykxhoorn D.M., Lieberman J. The silent revolution: RNA interference as basic biology, research tool, and therapeutic. Annu. Rev. Med. 2005, 56:401-423.
8. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
9. Zhang C. Novel functions for small RNA molecules. Curr. Opin. Mol. Ther. 2009, 11:641-651.
10. Leung A.K., Sharp P.A. MicroRNA functions in stress responses. Mol. Cell 2010, 40:205-215.
11. Newman M.A., Hammond S.M. Emerging paradigms of regulated microRNA processing. Genes Dev. 2010, 24:1086-1092.
12. Cullen B.R. Five questions about viruses and microRNAs. PLoS Pathog. 2010, 6:e1000787.
13. Skalsky R.L., Cullen B.R. Viruses, microRNAs, and host interactions. Annu. Rev. Microbiol. 2010, 64:123-141.
14. Umbach J.L., Cullen B.R. The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev. 2009, 23:1151-1164.
15. Cullen B.R. Viral and cellular messenger RNA targets of viral microRNAs. Nature 2009, 457:421-425.
16. Gottwein E., Cullen B.R. Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe 2008, 3:375-387.
17. Randall G., Panis M., Cooper J.D., Tellinghuisen T.L., Sukhodolets K.E., et al. Cellular cofactors affecting hepatitis C virus infection and replication. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:12884-12889.
18. Li L.M., Hu Z.B., Zhou Z.X., Chen X., Liu F.Y., et al. Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res. 2010, 70:9798-9807.
19. Cameron J.E., Fewell C., Yin Q., McBride J., Wang X., et al. Epstein-Barr virus growth/latency III program alters cellular microRNA expression. Virology 2008, 382:257-266.
20. Yeung M.L., Bennasser Y., Myers T.G., Jiang G., Benkirane M., et al. Changes in microRNA expression profiles in HIV-1-transfected human cells. Retrovirology 2005, 2:81.
21. Li Y., Wang F., Xu J., Ye F., Shen Y., et al. Progressive miRNA expression profiles in cervical carcinogenesis and identification of HPV-related target genes for miR-29. J. Pathol. 2011.
22. Bouzar A.B., Willems L. How HTLV-1 may subvert miRNAs for persistence and transformation. Retrovirology 2008, 5:101.
23. Ginsberg H.S. The life and times of adenoviruses. Adv. Virus Res. 1999, 54:1-13.
24. Shenk T. Raven publishers editor 1996, Adenoviridae: The viruses and their replication, Philadelphia.
25. Chinnadurai G. Opposing oncogenic activities of small DNA tumor virus transforming proteins. Trends Microbiol. 2011, 19:174-183.
26. Estmer Nilsson C., Petersen-Mahrt S., Durot C., Shtrichman R., Krainer A.R., et al. The adenovirus E4-ORF4 splicing enhancer protein interacts with a subset of phosphorylated SR proteins. EMBO J. 2001, 20:864-871.
27. Stracker T.H., Carson C.T., Weitzman M.D. Adenovirus oncoproteins inactivate the Mre11-Rad50-NBS1 DNA repair complex. Nature 2002, 418:348-352.
28. Ghadge G.D., Swaminathan S., Katze M.G., Thimmapaya B. Binding of the adenovirus VAI RNA to the interferon-induced 68-kDa protein kinase correlates with function. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:7140-7144.
29. Pilder S., Moore M., Logan J., Shenk T. The adenovirus E1B-55K transforming polypeptide modulates transport or cytoplasmic stabilization of viral and host cell mRNAs. Mol. Cell. Biol. 1986, 6:470-476.
30. Xi Q., Cuesta R., Schneider R.J. Tethering of eIF4G to adenoviral mRNAs by viral 100k protein drives ribosome shunting. Genes Dev. 2004, 18:1997-2009.
31. Lecellier C.H., Dunoyer P., Arar K., Lehmann-Che J., Eyquem S., et al. A cellular microRNA mediates antiviral defense in human cells. Science 2005, 308:557-560.
32. Bennasser Y., Le S.Y., Benkirane M., Jeang K.T. Evidence that HIV-1 encodes an siRNA and a suppressor of RNA silencing. Immunity 2005, 22:607-619.
33. Bucher E., Hemmes H., de Haan P., Goldbach R., Prins M. The influenza A virus NS1 protein binds small interfering RNAs and suppresses RNA silencing in plants. J. Gen. Virol. 2004, 85:983-991.
34. Li W.X., Li H., Lu R., Li F., Dus M., et al. Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:1350-1355.
35. Wang Y., Kato N., Jazag A., Dharel N., Otsuka M., et al. Hepatitis C virus core protein is a potent inhibitor of RNA silencing-based antiviral response. Gastroenterology 2006, 130:883-892.
36. Haasnoot J., de Vries W., Geutjes E.J., Prins M., de Haan P., et al. The Ebola virus VP35 protein is a suppressor of RNA silencing. PLoS Pathog. 2007, 3:e86.
37. Fabozzi G., Nabel C.S., Dolan M.A., Sullivan N.J. Ebolavirus proteins suppress the effects of small interfering RNA by direct interaction with the mammalian RNA interference pathway. J. Virol. 2011, 85:2512-2523.
38. Abe M., Suzuki H., Nishitsuji H., Shida H., Takaku H. Interaction of human T-cell lymphotropic virus type I Rex protein with Dicer suppresses RNAi silencing. FEBS Lett. 2010, 584:4313-4318.
39. Karjee S., Minhas A., Sood V., Ponia S.S., Banerjea A.C., et al. The 7a accessory protein of severe acute respiratory syndrome coronavirus acts as an RNA silencing suppressor. J. Virol. 2010, 84:10395-10401.
40. Bennasser Y., Yeung M.L., Jeang K.T. HIV-1 TAR RNA subverts RNA interference in transfected cells through sequestration of TAR RNA-binding protein, TRBP. J. Biol. Chem. 2006, 281:27674-27678.
41. Andersson M.G., Haasnoot P.C., Xu N., Berenjian S., Berkhout B., et al. Suppression of RNA interference by adenovirus virus-associated RNA. J. Virol. 2005, 79:9556-9565.
42. Lu S., Cullen B.R. Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and MicroRNA biogenesis. J. Virol. 2004, 78:12868-12876.
43. Akusjarvi G., Mathews M.B., Andersson P., Vennstrom B., Pettersson U. Structure of genes for virus-associated RNAI and RNAII of adenovirus type 2. Proc. Natl. Acad. Sci. U.S.A. 1980, 77:2424-2428.
44. Ma Y., Mathews M.B. Comparative analysis of the structure and function of adenovirus virus-associated RNAs. J. Virol. 1993, 67:6605-6617.
45. Ma Y., Mathews M.B. Structure, function, and evolution of adenovirus-associated RNA: a phylogenetic approach. J. Virol. 1996, 70:5083-5099.
46. Mellits K.H., Mathews M.B. Effects of mutations in stem and loop regions on the structure and function of adenovirus VA RNAI. EMBO J. 1988, 7:2849-2859.
47. Mellits K.H., Pe'ery T., Mathews M.B. Role of the apical stem in maintaining the structure and function of adenovirus virus-associated RNA. J. Virol. 1992, 66:2369-2377.
48. Clarke P.A., Pe'ery T., Ma Y., Mathews M.B. Structural features of adenovirus 2 virus-associated RNA required for binding to the protein kinase DAI. Nucleic Acids Res. 1994, 22:4364-4374.
49. Furtado M.R., Subramanian S., Bhat R.A., Fowlkes D.M., Safer B., et al. Functional dissection of adenovirus VAI RNA. J. Virol. 1989, 63:3423-3434.
50. Pe'ery T., Mellits K.H., Mathews M.B. Mutational analysis of the central domain of adenovirus virus-associated RNA mandates a revision of the proposed secondary structure. J. Virol. 1993, 67:3534-3543.
51. Bhat R.A., Domer P.H., Thimmappaya B. Structural requirements of adenovirus VAI RNA for its translation enhancement function. Mol. Cell. Biol. 1985, 5:187-196.
52. Rahman A., Malhotra P., Dhar R., Kewalramani T., Thimmapaya B. Effect of single-base substitutions in the central domain of virus-associated RNA I on its function. J. Virol. 1995, 69:4299-4307.
53. Wahid A.M., Coventry V.K., Conn G.L. The PKR-binding domain of adenovirus VA RNAI exists as a mixture of two functionally non-equivalent structures. Nucleic Acids Res. 2009, 37:5830-5837.
54. Thimmappaya B., Weinberger C., Schneider R.J., Shenk T. Adenovirus VAI RNA is required for efficient translation of viral mRNAs at late times after infection. Cell 1982, 31:543-551.
55. Bhat R.A., Thimmappaya B. Adenovirus mutants with DNA sequence perturbations in the intragenic promoter of VAI RNA gene allow the enhanced transcription of VAII RNA gene in HeLa cells. Nucleic Acids Res. 1984, 12:7377-7388.
56. Kitajewski J., Schneider R.J., Safer B., Munemitsu S.M., Samuel C.E., et al. Adenovirus VAI RNA antagonizes the antiviral action of interferon by preventing activation of the interferon-induced eIF-2 alpha kinase. Cell 1986, 45:195-200.
57. Bhat R.A., Thimmappaya B. Construction and analysis of additional adenovirus substitution mutants confirm the complementation of VAI RNA function by two small RNAs encoded by Epstein-Barr virus. J. Virol. 1985, 56:750-756.
58. Levin D.H., Petryshyn R., London I.M. Characterization of double-stranded-RNA-activated kinase that phosphorylates alpha subunit of eukaryotic initiation factor 2 (eIF-2 alpha) in reticulocyte lysates. Proc. Natl. Acad. Sci. U.S.A. 1980, 77:832-836.
59. Petryshyn R., Levin D.H., London I.M. Double-stranded RNA-dependent eIF-2alpha protein kinase. Methods Enzymol. 1983, 99:346-362.
60. O'Malley R.P., Mariano T.M., Siekierka J., Mathews M.B. A mechanism for the control of protein synthesis by adenovirus VA RNAI. Cell 1986, 44:391-400.
61. McKenna S.A., Kim I., Liu C.W., Puglisi J.D. Uncoupling of RNA binding and PKR kinase activation by viral inhibitor RNAs. J. Mol. Biol. 2006, 358:1270-1285.
62. Gwizdek C., Ossareh-Nazari B., Brownawell A.M., Doglio A., Bertrand E., et al. Exportin-5 mediates nuclear export of minihelix-containing RNAs. J. Biol. Chem. 2003, 278:5505-5508.
63. Reich P.R., Forget B.G., Weissman S.M. RNA of low molecular weight in KB cells infected with adenovirus type 2. J. Mol. Biol. 1966, 17:428-439.
64. Soderlund H., Pettersson U., Vennstrom B., Philipson L., Mathews M.B. A new species of virus-coded low molecular weight RNA from cells infected with adenovirus type 2. Cell 1976, 7:585-593.
65. Fowlkes D.M., Shenk T. Transcriptional control regions of the adenovirus VAI RNA gene. Cell 1980, 22:405-413.
66. Zhang H., Kolb F.A., Jaskiewicz L., Westhof E., Filipowicz W. Single processing center models for human Dicer and bacterial RNase III. Cell 2004, 118:57-68.
67. Aparicio O., Razquin N., Zaratiegui M., Narvaiza I., Fortes P. Adenovirus virus-associated RNA is processed to functional interfering RNAs involved in virus production. J. Virol. 2006, 80:1376-1384.
68. Sano M., Kato Y., Taira K. Sequence-specific interference by small RNAs derived from adenovirus VAI RNA. FEBS Lett. 2006, 580:1553-1564.
69. Xu N., Segerman B., Zhou X., Akusjarvi G. Adenovirus virus-associated RNAII-derived small RNAs are efficiently incorporated into the rna-induced silencing complex and associate with polyribosomes. J. Virol. 2007, 81:10540-10549.
70. Ouellet D.L., Plante I., Landry P., Barat C., Janelle M.E., et al. Identification of functional microRNAs released through asymmetrical processing of HIV-1 TAR element. Nucleic Acids Res. 2008, 36:2353-2365.
71. Yeung M.L., Bennasser Y., Watashi K., Le S.Y., Houzet L., et al. Pyrosequencing of small non-coding RNAs in HIV-1 infected cells: evidence for the processing of a viral-cellular double-stranded RNA hybrid. Nucleic Acids Res. 2009, 37:6575-6586.
72. Klase Z., Kale P., Winograd R., Gupta M.V., Heydarian M., 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.
73. Klase Z., Winograd R., Davis J., Carpio L., Hildreth R., et al. HIV-1 TAR miRNA protects against apoptosis by altering cellular gene expression. Retrovirology 2009, 6:18.
74. Xu N., Gkountela S., Saeed K., Akusjarvi G. The 5'-end heterogeneity of adenovirus virus-associated RNAI contributes to the asymmetric guide strand incorporation into the RNA-induced silencing complex. Nucleic Acids Res. 2009, 37:6950-6959.
75. Aparicio O., Carnero E., Abad X., Razquin N., Guruceaga E., et al. Adenovirus VA RNA-derived miRNAs target cellular genes involved in cell growth, gene expression and DNA repair. Nucleic Acids Res. 2010, 38:750-763.
76. Minamitani T., Iwakiri D., Takada K. Adenovirus virus-associated RNAs induce type I interferon expression through a RIG-I-mediated pathway. J. Virol. 2011, 85:4035-4040.
77. Yamaguchi T., Kawabata K., Kouyama E., Ishii K.J., Katayama K., et al. Induction of type I interferon by adenovirus-encoded small RNAs. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17286-17291.
78. Forch P., Puig O., Kedersha N., Martinez C., Granneman S., et al. The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing. Mol. Cell 2000, 6:1089-1098.
79. Forch P., Puig O., Martinez C., Seraphin B., Valcarcel J. The splicing regulator TIA-1 interacts with U1-C to promote U1 snRNP recruitment to 5' splice sites. EMBO J. 2002, 21:6882-6892.
80. Forch P., Valcarcel J. Molecular mechanisms of gene expression regulation by the apoptosis-promoting protein TIA-1. Apoptosis 2001, 6:463-468.
81. Gilks N., Kedersha N., Ayodele M., Shen L., Stoecklin G., et al. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 2004, 15:5383-5398.
82. McInerney G.M., Kedersha N.L., Kaufman R.J., Anderson P., Liljestrom P. Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol. Biol. Cell 2005, 16:3753-3763.
83. Emara M.M., Brinton M.A. Interaction of TIA-1/TIAR with West Nile and dengue virus products in infected cells interferes with stress granule formation and processing body assembly. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:9041-9046.
84. White J.P., Cardenas A.M., Marissen W.E., Lloyd R.E. Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2007, 2:295-305.
85. Le Guiner C., Lejeune F., Galiana D., Kister L., Breathnach R., et al. TIA-1 and TIAR activate splicing of alternative exons with weak 5' splice sites followed by a U-rich stretch on their own pre-mRNAs. J. Biol. Chem. 2001, 276:40638-40646.
86. Qi Y., Tu J., Cui L., Guo X., Shi Z., et al. High-throughput sequencing of microRNAs in adenovirus type 3 infected human laryngeal epithelial cells. J. Biomed. Biotechnol. 2010, 2010:915980.
87. Cazalla D., Yario T., Steitz J.A. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 2010, 328:1563-1566.
88. Buck A.H., Perot J., Chisholm M.A., Kumar D.S., Tuddenham L., et al. Post-transcriptional regulation of miR-27 in murine cytomegalovirus infection. RNA 2010, 16:307-315.
89. Nuovo G.J., Wu X., Volinia S., Yan F., di Leva G., et al. Strong inverse correlation between microRNA-125b and human papillomavirus DNA in productive infection. Diagn. Mol. Pathol. 2010, 19:135-143.
90. Su J.L., Chen P.B., Chen Y.H., Chen S.C., Chang Y.W., et al. Downregulation of microRNA miR-520h by E1A contributes to anticancer activity. Cancer Res. 2010, 70:5096-5108.
91. Campos S.K., Barry M.A. Current advances and future challenges in Adenoviral vector biology and targeting. Curr. Gene Ther. 2007, 7:189-204.
92. Cascallo M., Gros A., Bayo N., Serrano T., Capella G., et al. Deletion of VAI and VAII RNA genes in the design of oncolytic adenoviruses. Hum. Gene Ther. 2006, 17:929-940.
93. Cascallo M., Capella G., Mazo A., Alemany R. Ras-dependent oncolysis with an adenovirus VAI mutant. Cancer Res. 2003, 63:5544-5550.
94. Wang Y., Xue S.A., Hallden G., Francis J., Yuan M., et al. Virus-associated RNA I-deleted adenovirus, a potential oncolytic agent targeting EBV-associated tumors. Cancer Res. 2005, 65:1523-1531.
95. Lasaro M.O., Ertl H.C. New insights on adenovirus as vaccine vectors. Mol. Ther. 2009, 17:1333-1339.
96. Grimm D., Streetz K.L., Jopling C.L., Storm T.A., Pandey K., et al. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 2006, 441:537-541.
97. Narvaiza I., Aparicio O., Vera M., Razquin N., Bortolanza S., et al. Effect of adenovirus-mediated RNA interference on endogenous microRNAs in a mouse model of multidrug resistance protein 2 gene silencing. J. Virol. 2006, 80:12236-12247.
98. Witting S.R., Brown M., Saxena R., Nabinger S., Morral N. Helper-dependent adenovirus-mediated short hairpin RNA expression in the liver activates the interferon response. J. Biol. Chem. 2008, 283:2120-2128.
99. Zhang F., Yao Y., Hao J., Zhou R., Liu C., et al. A dual-functioning adenoviral vector encoding both transforming growth factor-beta3 and shRNA silencing type I collagen: construction and controlled release for chondrogenesis. J. Control. Release 2010, 142:70-77.
100. Ruiz R., Witting S.R., Saxena R., Morral N. Robust hepatic gene silencing for functional studies using helper-dependent adenoviral vectors. Hum. Gene Ther. 2009, 20:87-94.
101. Rauschhuber C., Xu H., Salazar F.H., Marion P.L., Ehrhardt A. Exploring gene-deleted adenoviral vectors for delivery of short hairpin RNAs and reduction of hepatitis B virus infection in mice. J. Gene Med. 2008, 10:878-889.
102. Huang B., Schiefer J., Sass C., Landwehrmeyer G.B., Kosinski C.M., et al. High-capacity adenoviral vector-mediated reduction of huntingtin aggregate load in vitro and in vivo. Hum. Gene Ther. 2007, 18:303-311.
103. Pei D.S., Di J.H., Chen F.F., Zheng J.N. Oncolytic-adenovirus-expressed RNA interference for cancer therapy. Expert Opin. Biol. Ther. 2010, 10:1331-1341.
104. Gurlevik E., Woller N., Schache P., Malek N.P., Wirth T.C., et al. p53-dependent antiviral RNA-interference facilitates tumor-selective viral replication. Nucleic Acids Res. 2009, 37:e84.
105. Ylosmaki E., Hakkarainen T., Hemminki A., Visakorpi T., Andino R., et al. Generation of a conditionally replicating adenovirus based on targeted destruction of E1A mRNA by a cell type-specific MicroRNA. J. Virol. 2008, 82:11009-11015.
106. Cawood R., Chen H.H., Carroll F., Bazan-Peregrino M., van Rooijen N., et al. Use of tissue-specific microRNA to control pathology of wild-type adenovirus without attenuation of its ability to kill cancer cells. PLoS Pathog. 2009, 5:e1000440.
107. de Vries W., Haasnoot J., van der Velden J., van Montfort T., Zorgdrager F., et al. Increased virus replication in mammalian cells by blocking intracellular innate defense responses. Gene Ther. 2008, 15:545-552.
108. Thomas M.A., Spencer J.F., La Regina M.C., Dhar D., Tollefson A.E., et al. Syrian hamster as a permissive immunocompetent animal model for the study of oncolytic adenovirus vectors. Cancer Res. 2006, 66:1270-1276.
109. Bortolanza S., Alzuguren P., Bunuales M., Qian C., Prieto J., et al. Human adenovirus replicates in immunocompetent models of pancreatic cancer in Syrian hamsters. Hum. Gene Ther. 2007, 18:681-690.