Proteins that contain a functional Z-DNA-binding domain localize to cytoplasmic stress granules

Nucleic Acids Research

Volumn 41, Issue 21, 2013, Pages 9786-9799

  Ng, Siew Kit ^a   Weissbach, Rebekka ^a   Ronson, George E ^a   Scadden, A D J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; ADENOSINE DEAMINASE THAT ACT ON RNA 1; BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; POLYINOSINIC POLYCYTIDYLIC ACID; POLYPYRIMIDINE TRACT BINDING PROTEIN; POLYPYRIMIDINE TRACT BINDING PROTEIN 4; UNCLASSIFIED DRUG; VIRULENCE FACTOR E3L; Z DNA BINDING PROTEIN 1;

ARTICLE; CELL GRANULE; CONTROLLED STUDY; CYTOPLASMIC STRESS GRANULE; DNA BINDING; HELA CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; RNA BINDING; Z DNA BINDING DOMAIN;

ADENOSINE DEAMINASE; AMINO ACIDS; CYTOPLASMIC GRANULES; DNA, Z-FORM; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; ISOENZYMES; OXIDATIVE STRESS; POLY I-C; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA; VIRAL PROTEINS;

EID: 84890045060     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt750     Document Type: Article

References (50)

1. Nishikura, K. (2010) Functions and regulation of RNA editing by ADAR deaminases. Annu. Rev. Biochem., 79, 321-349.
2. Bass, B.L. (2002) RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem., 71, 817-846.
3. Patterson, J.B. and Samuel, C.E. (1995) Expression and regulation by interferon of a double-stranded-RNA-specific adenosine deaminase from human cells: evidence for two forms of the deaminase. Mol. Cell. Biol., 15, 5376-5388.
4. George, C.X. and Samuel, C.E. (1999) 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. USA, 96, 4621-4626.
5. Poulsen, H., Nilsson, J., Damgaard, C.K., Egebjerg, J. and Kjems, J. (2001) CRM1 mediates the export of ADAR1 through a nuclear export signal within the Z-DNA binding domain. Mol. Cell. Biol., 21, 7862-7871.
6. Desterro, J.M.P., Keegan, L.P., Lafarga, M., Berciano, M.T., O'Connell, M. and Carmo-Fonseca, M. (2003) Dynamic association of RNA-editing enzymes with the nucleolus. J. Cell Sci., 116, 1805-1818.
7. Eckmann, C.R., Neunteufl, A., Pfaffstetter, L. and Jantsch, M.F. (2001) The human but not the Xenopus RNA-editing enzyme ADAR1 has an atypical nuclear localization signal and displays the characteristics of a shuttling protein. Mol. Biol. Cell, 12, 1911-1924.
8. Kim, U., Wang, Y., Sanford, T., Zeng, Y. and Nishikura, K. (1994) Molecular cloning of cDNA for double-stranded RNA adenosine deaminase, a candidate enzyme for nuclear RNA editing. Proc. Natl Acad. Sci. USA, 91, 11457-11461.
9. Herbert, A., Alfken, J., Kim, Y.G., Mian, I.S., Nishikura, K. and Rich, A. (1997) A Z-DNA binding domain present in the human editing enzyme, double-stranded RNA adenosine deaminase. Proc. Natl Acad. Sci. USA, 94, 8421-8426.
10. Athanasiadis, A., Placido, D., Maas, S., Brown Ii, B.A., Lowenhaupt, K. and Rich, A. (2005) The crystal structure of the Zb domain of the RNA-editing enzyme ADAR1 reveals distinct conserved surfaces among Z-domains. J. Mol. Biol., 351, 496-507.
11. Koeris, M., Funke, L., Shrestha, J., Rich, A. and Maas, S. (2005) Modulation of ADAR1 editing activity by Z-RNA in vitro. Nucleic Acids Res., 33, 5362-5370.
12. Rich, A. (2003) Z-DNA: the long road to biological function. Nat. Rev. Genet., 4, 566-572.
13. Schwartz, T., Rould, M.A., Lowenhaupt, K., Herbert, A. and Rich, A. (1999) Crystal structure of the Za domain of the human editing enzyme ADAR1 bound to left-handed Z-DNA. Science, 284, 1841-1845.
14. Schwartz, T., Behlke, J., Lowenhaupt, K., Heinemann, U. and Rich, A. (2001) Structure of the DLM-1-Z-DNA complex reveals a conserved family of Z-DNA-binding proteins. Nat. Struct. Mol. Biol., 8, 761-765.
15. Brown, B.A., Lowenhaupt, K., Wilbert, C.M., Hanlon, E.B. and Rich, A. (2000) The Zalpha domain of the editing enzyme dsRNA adenosine deaminase binds left-handed Z-RNA as well as Z-DNA. Proc. Natl Acad. Sci. USA, 97, 13532-13536.
16. Takaoka, A., Wang, Z., Choi, M.K., Yanai, H., Negishi, H., Ban, T., Lu, Y., Miyagishhi, M., Kodama, T., Honda, K. et al. (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature, 448, 501-505.
17. Ha, S.C., Lokanath, N.K., Van Quyen, D., Wu, C.A., Lowenhaupt, K., Rich, A., Kim, Y.-G. and Kim, K.K. (2004) A poxvirus protein forms a complex with left-handed Z-DNA: crystal structure of a Yatapoxvirus Za bound to DNA. Proc. Natl Acad. Sci. USA, 101, 14367-14372.
18. Kim, Y.G., Lowenhaupt, K., Oh, D.B., Kim, K.K. and Rich, A. (2004) Evidence that vaccinia virulence factor E3L binds to ZDNA in vivo: implications for development of a therapy for poxvirus infection. Proc. Natl Acad. Sci. USA, 101, 1514-1518.
19. Li, H., Xiao, J., Li, J., Lu, L., Feng, S. and Dröge, P. (2009) Human genomic Z-DNA segments probed by the Za domain of ADAR1. Nucleic Acids Res., 37, 2737-2746.
20. Tomé, A.R., Kus, K., Correia, S., Paulo, L.M., Zacarias, S., de Rosa, M., Figueiredo, D., Parkhouse, R.M.E. and Athanasiadis, A. (2013) Crystal structure of a poxvirus-Like zalpha domain from cyprinid Herpesvirus 3. J. Virol., 87, 3998-4004.
21. Barraud, P. and Allain, F. (2012) ADAR proteins: double-stranded RNA and Z-DNA binding domains. Curr. Top. Microbiol. Immunol., 353, 35-60.
22. Kim, Y.-G., Muralinath, M., Brandt, T., Pearcy, M., Hauns, K., Lowenhaupt, K., Jacobs, B.L. and Rich, A. (2003) A role for ZDNA binding in vaccinia virus pathogenesis. Proc. Natl Acad. Sci. USA, 100, 6974-6979.
23. Deigendesch, N., Koch-Nolte, F. and Rothenburg, S. (2006) ZBP1 subcellular localization and association with stress granules is controlled by its Z-DNA binding domains. Nucleic Acids Res., 34, 5007-5020.
24. Weissbach, R. and Scadden, A.D.J. (2012) Tudor-SN and ADAR1 are components of cytoplasmic stress granules. RNA, 18, 462-471.
25. Anderson, P. and Kedersha, N. (2008) Stress granules: the Tao of RNA triage. Trends Biochem. Sci., 33, 141-150.
26. Anderson, P. and Kedersha, N. (2009) RNA granules: posttranscriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol., 10, 430-436.
27. Buchan, J.R. and Parker, R. (2009) Eukaryotic stress granules: the ins and outs of translation. Mol. Cell, 36, 932-941.
28. Kedersha, N., Chen, S., Gilks, N., Li, W., Miller, I.J., Stahl, J. and Anderson, P. (2002) Evidence that ternary complex (eIF2-GTPtRNAiMet)-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell, 13, 195-210.
29. Kedersha, N., Stoecklin, G., Ayodele, M., Yacono, P., Lykke-Andersen, J., Fritzler, M.J., Scheuner, D., Kaufman, R.J., Golan, D.E. and Anderson, P. (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol., 169, 871-884.
30. Sambrook, J. and Russell, D.W. (2000) Molecular Cloning: A Laboratory Manual, 3rd Revised edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.
31. Gromak, N., Rideau, A., Southby, J., Scadden, A.D.J., Gooding, C., Huttelmaier, S., Singer, R.H. and Smith, C.W.J. (2003) The PTB interacting protein raver1 regulates a-tropomyosin alternative splicing. EMBO J., 22, 6356-6364.
32. Robinson, F. and Smith, C.W.J. (2006) A splicing repressor domain in polypyrimidine tract-binding protein. J. Biol. Chem., 281, 800-806.
33. Scadden, A.D.J. (2007) Inosine-containing dsRNA binds a stressgranule-like complex and downregulates gene expression in trans. Mol. Cell, 28, 491-500.
34. Lai, F., Drakas, R. and Nishikura, K. (1995) Mutagenic analysis of double-stranded RNA adenosine deaminase, a candidate enzyme for RNA editing of glutamate-gated ion channel transcripts. J. Biol. Chem., 270, 17098-17105.
35. Maas, S., Kawahara, Y., Tamburro, K.M. and Nishikura, K. (2006) A-to-I RNA editing and human disease. RNA Biol., 3, 1-9.
36. Schade, M., Turner, C.J., Kühne, R., Schmieder, P., Lowenhaupt, K., Herbert, A., Rich, A. and Oschkinat, H. (1999) The solution structure of the Za domain of the human RNA editing enzyme ADAR1 reveals a prepositioned binding surface for Z-DNA. Proc. Natl Acad. Sci. USA, 96, 12465-12470.
37. Anderson, P. and Kedersha, N. (2002) Visibly stressed: the role of eIF2, TIA-1, and stress granules in protein translation. Cell Stress Chaperones, 7, 213-221.
38. Placido, D., Brown Ii, B.A., Lowenhaupt, K., Rich, A. and Athanasiadis, A. (2007) A left-handed RNA double helix bound by the Za domain of the RNA-editing enzyme ADAR1. Structure, 15, 395-404.
39. Schade, M., Turner, C.J., Lowenhaupt, K., Rich, A. and Herbert, A. (1999) Structure-function analysis of the Z-DNA-binding domain Za of dsRNA adenosine deaminase type I reveals similarity to the (a+b) family of helix-turn-helix proteins. EMBO J., 18, 470-479.
40. Zarling, D.A., Calhoun, C.J., Feuerstein, B.G. and Sena, E.P. (1990) Cytoplasmic microinjection of immunoglobulin Gs recognizing RNA helices inhibits human cell growth. J. Mol. Biol., 211, 147-160.
41. Liu, Y., Wolff, K.C., Jacobs, B.L. and Samuel, C.E. (2001) Vaccinia virus E3L interferon resistance protein inhibits the interferoninduced adenosine deaminase A-to-I editing activity. Virology, 289, 378-387.
42. Khuu, P., Sandor, M., DeYoung, J. and Ho, P.S. (2007) Phylogenomic analysis of the emergence of GC-rich transcription elements. Proc. Natl Acad. Sci. USA, 104, 16528-16533.
43. Schroth, G.P., Chou, P.J. and Ho, P.S. (1992) Mapping Z-DNA in the human genome. Computer-aided mapping reveals a nonrandom distribution of potential Z-DNA-forming sequences in human genes. J. Biol. Chem., 267, 11846-11855.
44. Fitzpatrick, T. and Huang, S. (2012) 30-UTR-located inverted Alu repeats facilitate mRNA translational repression and stress granule accumulation. Nucleus, 3, 359-369.
45. Morse, D.P., Aruscavage, P.J. and Bass, B.L. (2002) RNA hairpins in noncoding regions of human brain and Caenorhabditis elegans mRNA are edited by adenosine deaminases that act on RNA. Proc. Natl Acad. Sci. USA, 99, 7906-7911.
46. Blow, M., Futreal, P.A., Wooster, R. and Stratton, M.R. (2004) A survey of RNA editing in human brain. Genome Res., 14, 2379-2387.
47. Barak, M., Levanon, E.Y., Eisenberg, E., Paz, N., Rechavi, G., Church, G.M. and Mehr, R. (2009) Evidence for large diversity in the human transcriptome created by Alu RNA editing. Nucleic Acids Res., 37, 6905-6915.
48. Levanon, E.Y., Eisenberg, E., Yelin, R., Nemzer, S., Hallegger, M., Shemesh, R., Fligelman, Z.Y., Shoshan, A., Pollock, S.R., Sztybel, D. et al. (2004) Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat. Biotechnol., 22, 1001-1005.
49. Vitali, P. and Scadden, A.D.J. (2010) Double-stranded RNAs containing multiple IU pairs are sufficient to suppress interferon induction and apoptosis. Nat. Struct. Mol. Biol., 17, 1043-1050.
50. Samuel, C.E. (2011) Adenosine deaminases acting on RNA (ADARs) are both antiviral and proviral. Virology, 411, 180-193.