Zalpha-domains: At the intersection between RNA editing and innate immunity

Seminars in Cell and Developmental Biology

Volumn 23, Issue 3, 2012, Pages 275-280

  Athanasiadis, Alekos ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

A to I RNA editing; ADAR1; DNA structure; Interferon response; Z DNA; Zalpha

Indexed keywords

ADENOSINE; ADENOSINE DEAMINASE ACTING ON RNA; ADENOSINE DEAMINASE ACTING ON RNA 1; DNA Z; INOSINE; INTERFERON; NUCLEIC ACID; PROTEIN KINASE RNA DEPENDED; RNA; UNCLASSIFIED DRUG;

CPG ISLAND; DNA STRUCTURE; INNATE IMMUNITY; REVIEW; RNA EDITING; RNA VIRUS;

RNA VIRUSES; VERTEBRATA;

EID: 84860357612     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2011.11.001     Document Type: Review

References (74)

1. Bass B.L., Weintraub H. An unwinding activity that covalently modifies its double-stranded RNA substrate. Cell 1988, 55:1089-1098.
2. O'Connell M.A. R.N.A. editing: rewriting receptors. Curr Biol 1997, 7:R437-R439.
3. Laurencikiene J., Kallman A.M., Fong N., Bentley D.L., Ohman M. R.N.A. editing and alternative splicing: the importance of co-transcriptional coordination. EMBO Rep 2006, 7:303-307.
4. O'Connell M.A., Keegan L.P. Drosha versus ADAR: wrangling over pri-miRNA. Nat Struct Mol Biol 2006, 13:3-4.
5. Polson A.G., Bass B.L. Preferential selection of adenosines for modification by double-stranded RNA adenosine deaminase. EMBO J 1994, 13:5701-5711.
6. Eggington J.M., Greene T., Bass B.L. Predicting sites of ADAR editing in double-stranded RNA. Nat Commun 2011, 2:319.
7. Schmauss C., Howe J.R. R.N.A. editing of neurotransmitter receptors in the mammalian brain. Sci STKE 2002, 2002:PE26.
8. Ohlson J., Pedersen J.S., Haussler D., Ohman M. Editing modifies the GABA(A) receptor subunit alpha3. RNA 2007, 13:698-703.
9. Semenov E.P., Pak W.L. Diversification of Drosophila chloride channel gene by multiple posttranscriptional mRNA modifications. J Neurochem 1999, 72:66-72.
10. Grauso M., Reenan R.A., Culetto E., Sattelle D.B. Novel putative nicotinic acetylcholine receptor subunit genes, Dalpha5, Dalpha6 and Dalpha7, in Drosophila melanogaster identify a new and highly conserved target of adenosine deaminase acting on RNA-mediated A-to-I pre-mRNA editing. Genetics 2002, 160:1519-1533.
11. Hoopengardner B., Bhalla T., Staber C., Reenan R. Nervous system targets of RNA editing identified by comparative genomics. Science 2003, 301:832-836.
12. Athanasiadis A., Rich A., Maas S. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol 2004, 2:e391.
13. Blow M., Futreal P.A., Wooster R., Stratton M.R. A survey of RNA editing in human brain. Genome Res 2004, 14:2379-2387.
14. Kim D.D., Kim T.T., Walsh T., Kobayashi Y., Matise T.C., Buyske S., et al. Widespread RNA editing of embedded alu elements in the human transcriptome. Genome Res 2004, 14:1719-1725.
15. Levanon E.Y., Eisenberg E., Yelin R., Nemzer S., Hallegger M., Shemesh R., et al. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat Biotechnol 2004, 22:1001-1005.
16. Ding S.W., Voinnet O. Antiviral immunity directed by small RNAs. Cell 2007, 130:413-426.
17. Gantier M.P., Williams B.R. The response of mammalian cells to double-stranded RNA. Cytokine Growth Factor Rev 2007, 18:363-371.
18. Cattaneo R., Schmid A., Eschle D., Baczko K., ter Meulen V., Billeter M.A. Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell 1988, 55:255-265.
19. Cattaneo R. Biased (A→I) hypermutation of animal RNA virus genomes. Curr Opin Genet Dev 1994, 4:895-900.
20. Bass B.L. R.N.A. editing and hypermutation by adenosine deamination. Trends Biochem Sci 1997, 22:157-162.
21. Samuel C.E. Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral. Virology 2011, 411:180-193.
22. Carpenter J.A., Keegan L.P., Wilfert L., O'Connell M.A., Jiggins F.M. Evidence for ADAR-induced hypermutation of the Drosophila sigma virus (Rhabdoviridae). BMC Genet 2009, 10:75.
23. George C.X., Samuel C.E. Host response to polyomavirus infection is modulated by RNA adenosine deaminase ADAR1 but not by ADAR2. J Virol 2011, 85:8338-8347.
24. Casey J.L., Gerin J.L. Hepatitis D virus RNA editing: specific modification of adenosine in the antigenomic RNA. J Virol 1995, 69:7593-7600.
25. Sharmeen L., Bass B., Sonenberg N., Weintraub H., Groudine M. Tat-dependent adenosine-to-inosine modification of wild-type transactivation response RNA. Proc Natl Acad Sci U S A 1991, 88:8096-8100.
26. Doria M., Neri F., Gallo A., Farace M.G., Michienzi A. Editing of HIV-1 RNA by the double-stranded RNA deaminase ADAR1 stimulates viral infection. Nucleic Acids Res 2009, 37:5848-5858.
27. Phuphuakrat A., Kraiwong R., Boonarkart C., Lauhakirti D., Lee T.H., Auewarakul P. Double-stranded RNA adenosine deaminases enhance expression of human immunodeficiency virus type 1 proteins. J Virol 2008, 82:10864-10872.
28. Pfeffer S., Sewer A., Lagos-Quintana M., Sheridan R., Sander C., Grasser F.A., et al. Identification of microRNAs of the herpesvirus family. Nat Methods 2005, 2:269-276.
29. Gandy S.Z., Linnstaedt S.D., Muralidhar S., Cashman K.A., Rosenthal L.J., Casey J.L. R.N.A. editing of the human herpesvirus 8 kaposin transcript eliminates its transforming activity and is induced during lytic replication. J Virol 2007, 81:13544-13551.
30. George C.X., Samuel C.E. Human RNA-specific adenosine deaminase ADAR1 transcripts possess alternative exon 1 structures that initiate from different promoters, one constitutively active and the other interferon inducible. Proc Natl Acad Sci U S A 1999, 96:4621-4626.
31. Hartner J.C., Schmittwolf C., Kispert A., Muller A.M., Higuchi M., Seeburg P.H. Liver disintegration in the mouse embryo caused by deficiency in the RNA-editing enzyme ADAR1. J Biol Chem 2004, 279:4894-4902.
32. Wang Q., Miyakoda M., Yang W., Khillan J., Stachura D.L., Weiss M.J., et al. Stress-induced apoptosis associated with null mutation of ADAR1 RNA editing deaminase gene. J Biol Chem 2004, 279:4952-4961.
33. Hartner J.C., Walkley C.R., Lu J., Orkin S.H. ADAR1 is essential for the maintenance of hematopoiesis and suppression of interferon signaling. Nat Immunol 2009, 10:109-115.
34. Ward S.V., George C.X., Welch M.J., Liou L.Y., Hahm B., Lewicki H., et al. RNA editing enzyme adenosine deaminase is a restriction factor for controlling measles virus replication that also is required for embryogenesis. Proc Natl Acad Sci U S A 2011, 108:331-336.
35. Toth A.M., Li Z., Cattaneo R., Samuel C.E. RNA-specific adenosine deaminase ADAR1 suppresses measles virus-induced apoptosis and activation of protein kinase PKR. J Biol Chem 2009, 284:29350-29356.
36. Gelinas J.F., Clerzius G., Shaw E., Gatignol A. Enhancement of replication of RNA viruses by ADAR1 via RNA editing and inhibition of RNA-activated protein kinase. J Virol 2011, 85:8460-8466.
37. Wang Y., Samuel C.E. Adenosine deaminase ADAR1 increases gene expression at the translational level by decreasing protein kinase PKR dependent eIF-2alpha phosphorylation. J Mol Biol 2009, 393:777-787.
38. Li Z., Wolff K.C., Samuel C.E. RNA adenosine deaminase ADAR1 deficiency leads to increased activation of protein kinase PKR and reduced vesicular stomatitis virus growth following interferon treatment. Virology 2010, 396:316-322.
39. Nejepinska J., Malik R., Filkowski J., Flemr M., Filipowicz W., Svoboda P. dsRNA expression in the mouse elicits RNAi in oocytes and low adenosine deamination in somatic cells. Nucleic Acids Res 2011, 10.1093/nar/gkr702.
40. Tonkin L.A., Bass B.L. Mutations in RNAi rescue aberrant chemotaxis of ADAR mutants. Science 2003, 302:1725.
41. Wu D., Lamm A.T., Fire A.Z. Competition between ADAR and RNAi pathways for an extensive class of RNA targets. Nat Struct Mol Biol 2011, 18:1094-1101.
42. Yang W., Wang Q., Howell K.L., Lee J.T., Cho D.S., Murray J.M., et al. ADAR1 RNA deaminase limits short interfering RNA efficacy in mammalian cells. J Biol Chem 2005, 280:3946-3953.
43. Schoggins J.W., Wilson S.J., Panis M., Murphy M.Y., Jones C.T., Bieniasz P., et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472:481-485.
44. Herbert A.G., Spitzner J.R., Lowenhaupt K., Rich A. Z-DNA binding protein from chicken blood nuclei. Proc Natl Acad Sci U S A 1993, 90:3339-3342.
45. Herbert A., Alfken J., Kim Y.G., Mian I.S., Nishikura K., Rich A. A Z-DNA binding domain present in the human editing enzyme, double-stranded RNA adenosine deaminase. Proc Natl Acad Sci U S A 1997, 94:8421-8426.
46. Wang A.H., Quigley G.J., Kolpak F.J., Crawford J.L., van Boom J.H., van der Marel G., et al. Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature 1979, 282:680-686.
47. Schwartz T., Rould M.A., Lowenhaupt K., Herbert A., Rich A. Crystal structure of the Zalpha domain of the human editing enzyme ADAR1 bound to left-handed Z-DNA. Science 1999, 284:1841-1845.
48. Schade M., Turner C.J., Lowenhaupt K., Rich A., Herbert A. Structure-function analysis of the Z-DNA-binding domain Zalpha of dsRNA adenosine deaminase type I reveals similarity to the (alpha+beta) family of helix-turn-helix proteins. EMBO J 1999, 18:470-479.
49. Ha S.C., Choi J., Hwang H.Y., Rich A., Kim Y.G., Kim K.K. The structures of non-CG-repeat Z-DNAs co-crystallized with the Z-DNA-binding domain, hZalpha (ADAR1). Nucleic Acids Res 2009, 37:629-637.
50. Ha S.C., Lowenhaupt K., Rich A., Kim Y.G., Kim K.K. Crystal structure of a junction between B-DNA and Z-DNA reveals two extruded bases. Nature 2005, 437:1183-1186.
51. de Rosa M., de Sanctis D., Rosario A.L., Archer M., Rich A., Athanasiadis A., et al. Crystal structure of a junction between two Z-DNA helices. Proc Natl Acad Sci U S A 2010, 107:9088-9092.
52. Hall K., Cruz P., Tinoco I., Jovin T.M., van de Sande J.H. 'Z-RNA'-a left-handed RNA double helix. Nature 1984, 311:584-586.
53. Brown B.A., Lowenhaupt K., Wilbert C.M., Hanlon E.B., Rich A. The zalpha domain of the editing enzyme dsRNA adenosine deaminase binds left-handed Z-RNA as well as Z-DNA. Proc Natl Acad Sci U S A 2000, 97:13532-13536.
54. Placido D., Brown B.A., Lowenhaupt K., Rich A., Athanasiadis A. A left-handed RNA double helix bound by the Z alpha domain of the RNA-editing enzyme ADAR1. Structure 2007, 15:395-404.
55. Schwartz T., Behlke J., Lowenhaupt K., Heinemann U., Rich A. Structure of the DLM-1-Z-DNA complex reveals a conserved family of Z-DNA-binding proteins. Nat Struct Biol 2001, 8:761-765.
56. Ha S.C., Kim D., Hwang H.Y., Rich A., Kim Y.G., Kim K.K. The crystal structure of the second Z-DNA binding domain of human DAI (ZBP1) in complex with Z-DNA reveals an unusual binding mode to Z-DNA. Proc Natl Acad Sci U S A 2008, 105:20671-20676.
57. Kim K., Khayrutdinov B.I., Lee C.K., Cheong H.K., Kang S.W., Park H., et al. Solution structure of the Z{beta} domain of human DNA-dependent activator of IFN-regulatory factors and its binding modes to B- and Z-DNAs. Proc Natl Acad Sci U S A 2011, 108:6921-6926.
58. Ha S.C., Lokanath N.K., Van Quyen D., Wu C.A., Lowenhaupt K., Rich A., et al. A poxvirus protein forms a complex with left-handed Z-DNA: crystal structure of a Yatapoxvirus Zalpha bound to DNA. Proc Natl Acad Sci U S A 2004, 101:14367-14372.
59. Rothenburg S., Deigendesch N., Dittmar K., Koch-Nolte F., Haag F., Lowenhaupt K., et al. A PKR-like eukaryotic initiation factor 2alpha kinase from zebrafish contains Z-DNA binding domains instead of dsRNA binding domains. Proc Natl Acad Sci U S A 2005, 102:1602-1607.
60. Takaoka A., Wang Z., Choi M.K., Yanai H., Negishi H., Ban T., et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448:501-505.
61. Wang Z., Choi M.K., Ban T., Yanai H., Negishi H., Lu Y., et al. Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc Natl Acad Sci U S A 2008, 105:5477-5482.
62. DeFilippis V.R., Alvarado D., Sali T., Rothenburg S., Fruh K. Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J Virol 2010, 84:585-598.
63. Furr S.R., Chauhan V.S., Moerdyk-Schauwecker M.J., Marriott I. A role for DNA-dependent activator of interferon regulatory factor in the recognition of herpes simplex virus type 1 by glial cells. J Neuroinflammation 2011, 8:99.
64. Lippmann J., Rothenburg S., Deigendesch N., Eitel J., Meixenberger K., van Laak V., et al. IFNbeta responses induced by intracellular bacteria or cytosolic DNA in different human cells do not require ZBP1 (DLM-1/DAI). Cell Microbiol 2008, 10:2579-2588.
65. Bergan V., Jagus R., Lauksund S., Kileng O., Robertsen B. The Atlantic salmon Z-DNA binding protein kinase phosphorylates translation initiation factor 2 alpha and constitutes a unique orthologue to the mammalian dsRNA-activated protein kinase R. FEBS J 2008, 275:184-197.
66. Kim Y.G., Muralinath M., Brandt T., Pearcy M., Hauns K., Lowenhaupt K., et al. A role for Z-DNA binding in vaccinia virus pathogenesis. Proc Natl Acad Sci U S A 2003, 100:6974-6979.
67. Langland J.O., Kash J.C., Carter V., Thomas M.J., Katze M.G., Jacobs B.L. Suppression of proinflammatory signal transduction and gene expression by the dual nucleic acid binding domains of the vaccinia virus E3L proteins. J Virol 2006, 80:10083-10095.
68. Athanasiadis A., Placido D., Maas S., Brown B.A., Lowenhaupt K., Rich A. The crystal structure of the Zbeta domain of the RNA-editing enzyme ADAR1 reveals distinct conserved surfaces among Z-domains. J Mol Biol 2005, 351:496-507.
69. Li H., Xiao J., Li J., Lu L., Feng S., Droge P. Human genomic Z-DNA segments probed by the Z alpha domain of ADAR1. Nucleic Acids Res 2009, 37:2737-2746.
70. Feng S., Li H., Zhao J., Pervushin K., Lowenhaupt K., Schwartz T.U., et al. Alternate rRNA secondary structures as regulators of translation. Nat Struct Mol Biol 2011, 18:169-176.
71. Deigendesch N., Koch-Nolte F., Rothenburg S. ZBP1 subcellular localization and association with stress granules is controlled by its Z-DNA binding domains. Nucleic Acids Res 2006, 34:5007-5020.
72. Nordheim A., Rich A. Negatively supercoiled simian virus 40 DNA contains Z-DNA segments within transcriptional enhancer sequences. Nature 1983, 303:674-679.
73. Ablasser A., Bauernfeind F., Hartmann G., Latz E., Fitzgerald K.A., Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol 2009, 10:1065-1072.
74. Valentine R., Smith G.L. Inhibition of the RNA polymerase III-mediated dsDNA sensing pathway of innate immunity by vaccinia virus protein E3. J Gen Virol 2010, 91:2221-2229.