Z-DNA and Z-RNA in human disease

Bioinformatics
  • 1.

    Herbert, A. et al. A Z-DNA binding domain present in the human editing enzyme, double-stranded RNA adenosine deaminase. Proc. Natl Acad. Sci. USA 94, 8421–8426 (1997).

  • 2.

    Herbert, A. G., Spitzner, J. R., Lowenhaupt, K. & Rich, A. Z-DNA binding protein from chicken blood nuclei. Proc. Natl Acad. Sci. USA 90, 3339–3342 (1993).

  • 3.

    Kim, U., Wang, Y., Sanford, T., Zeng, Y. & Nishikura, K. 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 (1994).

  • 4.

    Patterson, J. B., Thomis, D. C., Hans, S. L. & Samuel, C. E. Mechanism of interferon action: double-stranded RNA-specific adenosine deaminase from human cells is inducible by alpha and gamma interferons. Virology 210, 508–511 (1995).

  • 5.

    Schade, M. et al. A 6 bp Z-DNA hairpin binds two Z alpha domains from the human RNA editing enzyme ADAR1. FEBS Lett. 458, 27–31 (1999).

  • 6.

    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 284, 1841–1845 (1999).

  • 7.

    Pohl, F. M. & Jovin, T. M. Salt-induced co-operative conformational change of a synthetic DNA: equilibrium and kinetic studies with poly (dG-dC). J. Mol. Biol. 67, 375–396 (1972).

  • 8.

    Wang, A. H. et al. Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature 282, 680–686 (1979).

  • 9.

    Peck, L. J. & Wang, J. C. Energetics of B-to-Z transition in DNA. Proc. Natl Acad. Sci. USA 80, 6206–6210 (1983).

  • 10.

    Ho, P. S., Ellison, M. J., Quigley, G. J. & Rich, A. A computer aided thermodynamic approach for predicting the formation of Z-DNA in naturally occurring sequences. EMBO J. 5, 2737–2744 (1986).

  • 11.

    Schade, M. et al. The solution structure of the Zalpha domain of the human RNA editing enzyme ADAR1 reveals a prepositioned binding surface for Z-DNA. Proc. Natl Acad. Sci. USA 96, 12465–12470 (1999).

  • 12.

    Kus, K. et al. The structure of the cyprinid herpesvirus 3 ORF112-Zalpha.Z-DNA complex reveals a mechanism of nucleic acids recognition conserved with E3L, a Poxvirus inhibitor of interferon response. J. Biol. Chem. 290, 30713–30725 (2015).

  • 13.

    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 437, 1183–1186 (2005).

  • 14.

    Vasquez, K. M. & Wang, G. The yin and yang of repair mechanisms in DNA structure-induced genetic instability. Mutat. Res. 743–744, 118–131 (2013).

  • 15.

    de Rosa, M. et al. Crystal structure of a junction between two Z-DNA helices. Proc. Natl Acad. Sci. USA 107, 9088–9092 (2010).

  • 16.

    Bae, S., Kim, D., Kim, K. K., Kim, Y. G. & Hohng, S. Intrinsic Z-DNA is stabilized by the conformational selection mechanism of Z-DNA-binding proteins. J. Am. Chem. Soc. 133, 668–671 (2011).

  • 17.

    Kolimi, N., Ajjugal, Y. & Rathinavelan, T. A B-Z junction induced by an A… A mismatch in GAC repeats in the gene for cartilage oligomeric matrix protein promotes binding with the hZalphaADAR1 protein. J. Biol. Chem. 292, 18732–18746 (2017).

  • 18.

    Bothe, J. R., Lowenhaupt, K. & Al-Hashimi, H. M. Incorporation of CC steps into Z-DNA: interplay between B-Z junction and Z-DNA helical formation. Biochemistry 51, 6871–6879 (2012).

  • 19.

    Placido, D. et al. A left-handed RNA double helix bound by the Z alpha domain of the RNA-editing enzyme ADAR1. Structure 15, 395–404 (2007).

  • 20.

    Bae, S. et al. Energetics of Z-DNA binding protein-mediated helicity reversals in DNA, RNA, and DNA-RNA duplexes. J. Phys. Chem. B 117, 13866–13871 (2013).

  • 21.

    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. 8, 761–765 (2001).

  • 22.

    Ha, S. C. et al. 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. USA 105, 20671–20676 (2008).

  • 23.

    de Rosa, M., Zacarias, S. & Athanasiadis, A. Structural basis for Z-DNA binding and stabilization by the zebrafish Z-DNA dependent protein kinase PKZ. Nucleic Acids Res. 41, 9924–9933 (2013).

  • 24.

    Subramani, V. K., Kim, D., Yun, K. & Kim, K. K. Structural and functional studies of a large winged Z-DNA-binding domain of Danio rerio protein kinase PKZ. FEBS Lett. 590, 2275–2285 (2016).

  • 25.

    Ha, S. C. 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. USA 101, 14367–14372 (2004).

  • 26.

    Hartner, J. C. et al. Liver disintegration in the mouse embryo caused by deficiency in the RNA-editing enzyme ADAR1. J. Biol. Chem. 279, 4894–4902 (2004).

  • 27.

    Kang, H. J. et al. Novel interaction of the Z-DNA binding domain of human ADAR1 with the oncogenic c-Myc promoter G-quadruplex. J. Mol. Biol. 426, 2594–2604 (2014).

  • 28.

    Chung, W. J. et al. Structure of a left-handed DNA G-quadruplex. Proc. Natl Acad. Sci. USA 112, 2729–2733 (2015).

  • 29.

    D’Ascenzo, L., Vicens, Q. & Auffinger, P. Identification of receptors for UNCG and GNRA Z-turns and their occurrence in rRNA. Nucleic Acids Res. 46, 7989–7997 (2018).

  • 30.

    Teplova, M., Song, J., Gaw, H. Y., Teplov, A. & Patel, D. J. Structural insights into RNA recognition by the alternate-splicing regulator CUG-binding protein 1. Structure 18, 1364–1377 (2010).

  • 31.

    Abbas, Y. M., Pichlmair, A., Gorna, M. W., Superti-Furga, G. & Nagar, B. Structural basis for viral 5’-PPP-RNA recognition by human IFIT proteins. Nature 494, 60–64 (2013).

  • 32.

    Bass, B. L. RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem. 71, 817–846 (2002).

  • 33.

    Nishikura, K. A-to-I editing of coding and non-coding RNAs by ADARs. Nat. Rev. Mol. Cell Biol. 17, 83–96 (2016).

  • 34.

    Solomon, O. et al. RNA editing by ADAR1 leads to context-dependent transcriptome-wide changes in RNA secondary structure. Nat. Commun. 8, 1440 (2017).

  • 35.

    Athanasiadis, A. et al. The crystal structure of the Zbeta domain of the RNA-editing enzyme ADAR1 reveals distinct conserved surfaces among Z-domains. J. Mol. Biol. 351, 496–507 (2005).

  • 36.

    Strehblow, A., Hallegger, M. & Jantsch, M. F. Nucleocytoplasmic distribution of human RNA-editing enzyme ADAR1 is modulated by double-stranded RNA-binding domains, a leucine-rich export signal, and a putative dimerization domain. Mol. Biol. Cell 13, 3822–3835 (2002).

  • 37.

    George, C. X., Gan, Z., Liu, Y. & Samuel, C. E. Adenosine deaminases acting on RNA, RNA editing, and interferon action. J. Interferon Cytokine Res. 31, 99–117 (2011).

  • 38.

    Sakurai, M. et al. ADAR1 controls apoptosis of stressed cells by inhibiting Staufen1-mediated mRNA decay. Nat. Struct. Mol. Biol. 24, 534–543 (2017).

  • 39.

    Herbert, A. & Rich, A. The role of binding domains for dsRNA and Z-DNA in the in vivo editing of minimal substrates by ADAR1. Proc. Natl Acad. Sci. USA 98, 12132–12137 (2001).

  • 40.

    Zheng, Y., Lorenzo, C. & Beal, P. A. DNA editing in DNA/RNA hybrids by adenosine deaminases that act on RNA. Nucleic Acids Res. 45, 3369–3377 (2017).

  • 41.

    Honda, K., Takaoka, A. & Taniguchi, T. Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25, 349–360 (2006).

  • 42.

    Vitali, P. & Scadden, A. D. Double-stranded RNAs containing multiple IU pairs are sufficient to suppress interferon induction and apoptosis. Nat. Struct. Mol. Biol. 17, 1043–1050 (2010).

  • 43.

    Pestal, K. et al. Isoforms of RNA-editing enzyme ADAR1 independently control nucleic acid sensor MDA5-driven autoimmunity and multi-organ development. Immunity 43, 933–944 (2015).

  • 44.

    George, C. X., Ramaswami, G., Li, J. B. & Samuel, C. E. Editing of cellular self-RNAs by adenosine deaminase ADAR1 suppresses innate immune stress responses. J. Biol. Chem. 291, 6158–6168 (2016).

  • 45.

    Cao, H. et al. Innate immune response of human plasmacytoid dendritic cells to poxvirus infection is subverted by vaccinia E3 via its Z-DNA/RNA binding domain. PLoS ONE 7, e36823 (2012).

  • 46.

    de Koning, A. P., Gu, W., Castoe, T. A., Batzer, M. A. & Pollock, D. D. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet. 7, e1002384 (2011).

  • 47.

    Batzer, M. A. & Deininger, P. L. Alu repeats and human genomic diversity. Nat. Rev. Genet. 3, 370–379 (2002).

  • 48.

    Grover, D., Mukerji, M., Bhatnagar, P., Kannan, K. & Brahmachari, S. K. Alu repeat analysis in the complete human genome: trends and variations with respect to genomic composition. Bioinformatics 20, 813–817 (2004).

  • 49.

    Kim, D. D. et al. Widespread RNA editing of embedded alu elements in the human transcriptome. Genome Res. 14, 1719–1725 (2004).

  • 50.

    Athanasiadis, A., Rich, A. & Maas, S. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol. 2, e391 (2004).

  • 51.

    Levanon, E. Y. et al. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat. Biotechnol. 22, 1001–1005 (2004).

  • 52.

    Kawahara, Y. & Nishikura, K. Extensive adenosine-to-inosine editing detected in Alu repeats of antisense RNAs reveals scarcity of sense-antisense duplex formation. FEBS Lett. 580, 2301–2305 (2006).

  • 53.

    Ramaswami, G. & Li, J. B. RADAR: a rigorously annotated database of A-to-I RNA editing. Nucleic Acids Res. 42, D109–D113 (2014).

  • 54.

    Ahmad, S. et al. Breaching self-tolerance to Alu duplex RNA underlies MDA5-mediated inflammation. Cell 172, 797–810 (2018).

  • 55.

    Mannion, N. M. et al. The RNA-editing enzyme ADAR1 controls innate immune responses to RNA. Cell Rep. 9, 1482–1494 (2014).

  • 56.

    Wu, H. et al. Cathepsin S activity controls injury-related vascular repair in mice via the TLR2-mediated p38MAPK and PI3K-Akt/p-HDAC6 signaling pathway. Arterioscler., Thromb., Vasc. Biol. 36, 1549–1557 (2016).

  • 57.

    Stellos, K. et al. Adenosine-to-inosine RNA editing controls cathepsin S expression in atherosclerosis by enabling HuR-mediated post-transcriptional regulation. Nat. Med. 22, 1140–1150 (2016).

  • 58.

    Champ, P. C., Maurice, S., Vargason, J. M., Camp, T. & Ho, P. S. Distributions of Z-DNA and nuclear factor I in human chromosome 22: a model for coupled transcriptional regulation. Nucleic Acids Res. 32, 6501–6510 (2004).

  • 59.

    Bahn, J. H. et al. Genomic analysis of ADAR1 binding and its involvement in multiple RNA processing pathways. Nat. Commun. 6, 6355 (2015).

  • 60.

    Ditlevson, J. V. et al. Inhibitory effect of a short Z-DNA forming sequence on transcription elongation by T7 RNA polymerase. Nucleic Acids Res. 36, 3163–3170 (2008).

  • 61.

    Voorhees, R. M. & Hegde, R. S. Structures of the scanning and engaged states of the mammalian SRP-ribosome complex. eLife 4, e07975 (2015).

  • 62.

    Ahl, V., Keller, H., Schmidt, S. & Weichenrieder, O. Retrotransposition and crystal structure of an Alu RNP in the ribosome-stalling conformation. Mol. Cell 60, 715–727 (2015).

  • 63.

    Halic, M. et al. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427, 808–814 (2004).

  • 64.

    Bennett, E. A. et al. Active Alu retrotransposons in the human genome. Genome Res. 18, 1875–1883 (2008).

  • 65.

    Lehnert, S. et al. Evidence for co-evolution between human microRNAs and Alu-repeats. PLoS ONE 4, e4456 (2009).

  • 66.

    Price, A. L., Eskin, E. & Pevzner, P. A. Whole-genome analysis of Alu repeat elements reveals complex evolutionary history. Genome Res. 14, 2245–2252 (2004).

  • 67.

    Rubin, C. M., Kimura, R. H. & Schmid, C. W. Selective stimulation of translational expression by Alu RNA. Nucleic Acids Res. 30, 3253–3261 (2002).

  • 68.

    Berger, A. et al. Direct binding of the Alu binding protein dimer SRP9/14 to 40S ribosomal subunits promotes stress granule formation and is regulated by Alu RNA. Nucleic Acids Res. 42, 11203–11217 (2014).

  • 69.

    Ivanova, E., Berger, A., Scherrer, A., Alkalaeva, E. & Strub, K. Alu RNA regulates the cellular pool of active ribosomes by targeted delivery of SRP9/14 to 40S subunits. Nucleic Acids Res. 43, 2874–2887 (2015).

  • 70.

    Lomakin, I. B. & Steitz, T. A. The initiation of mammalian protein synthesis and mRNA scanning mechanism. Nature 500, 307–311 (2013).

  • 71.

    Leroy, M. et al. Rae1/YacP, a new endoribonuclease involved in ribosome-dependent mRNA decay in Bacillus subtilis. EMBO J. 36, 1167–1181 (2017).

  • 72.

    Nielsen, M. H., Flygaard, R. K. & Jenner, L. B. Structural analysis of ribosomal RACK1 and its role in translational control. Cell Signal. 35, 272–281 (2017).

  • 73.

    Cate, J. H. Human eIF3: from ‘blobology’ to biological insight. Philos. Trans. Roy. Soc. London, Ser. B Biol. Sci. 372, 20160176 (2017).

  • 74.

    Feng, S. et al. Alternate rRNA secondary structures as regulators of translation. Nat. Struct. Mol. Biol. 18, 169–176 (2011).

  • 75.

    Chen, L. L. & Yang, L. ALUternative regulation for gene expression. Trends Cell Biol. 27, 480–490 (2017).

  • 76.

    Shin, S. I. et al. Z-DNA-forming sites identified by ChIP-Seq are associated with actively transcribed regions in the human genome. DNA Res. 23, 477–486 (2016).

  • 77.

    Liu, R. et al. Regulation of CSF1 promoter by the SWI/SNF-like BAF complex. Cell 106, 309–318 (2001).

  • 78.

    Maruyama, A., Mimura, J., Harada, N. & Itoh, K. Nrf2 activation is associated with Z-DNA formation in the human HO-1 promoter. Nucleic Acids Res. 41, 5223–5234 (2013).

  • 79.

    Ebert, M. S. & Sharp, P. A. Roles for microRNAs in conferring robustness to biological processes. Cell 149, 515–524 (2012).

  • 80.

    Lukic, S., Nicolas, J. C. & Levine, A. J. The diversity of zinc-finger genes on human chromosome 19 provides an evolutionary mechanism for defense against inherited endogenous retroviruses. Cell Death Differ. 21, 381–387 (2014).

  • 81.

    Karpova, A. Y., Ronco, L. V. & Howley, P. M. Functional characterization of interferon regulatory factor 3a (IRF-3a), an alternative splice isoform of IRF-3. Mol. Cell Biol. 21, 4169–4176 (2001).

  • 82.

    Galipon, J., Ishii, R., Suzuki, Y., Tomita, M. & Ui-Tei, K. Differential binding of three major human ADAR isoforms to coding and long non-coding transcripts. Genes 8, 68 (2017).

  • 83.

    Rutkowski, A. J. et al. Widespread disruption of host transcription termination in HSV-1 infection. Nat. Commun. 6, 7126 (2015).

  • 84.

    McKenna, S. D. et al. Formation of human IFN-beta complex with the soluble type I interferon receptor IFNAR-2 leads to enhanced IFN stability, pharmacokinetics, and antitumor activity in xenografted SCID mice. J. Interferon Cytokine Res. 24, 119–129 (2004).

  • 85.

    Samarajiwa, S. A. et al. Soluble IFN receptor potentiates in vivo type I IFN signaling and exacerbates TLR4-mediated septic shock. J. Immunol. 192, 4425–4435 (2014).

  • 86.

    Ota, H. et al. ADAR1 forms a complex with Dicer to promote microRNA processing and RNA-induced gene silencing. Cell 153, 575–589 (2013).

  • 87.

    Maillard, P. V. et al. Antiviral RNA interference in mammalian cells. Science 342, 235–238 (2013).

  • 88.

    Tarallo, V. et al. DICER1 loss and Alu RNA induce age-related macular degeneration via the NLRP3 inflammasome and MyD88. Cell 149, 847–859 (2012).

  • 89.

    Kerur, N. et al. cGAS drives noncanonical-inflammasome activation in age-related macular degeneration. Nat. Med. 24, 50–61 (2018).

  • 90.

    Costa, E. A., Subramanian, K., Nunnari, J. & Weissman, J. S. Defining the physiological role of SRP in protein-targeting efficiency and specificity. Science 359, 689–692 (2018).

  • 91.

    Szczesny, B. et al. Mitochondrial DNA damage and subsequent activation of Z-DNA binding protein 1 links oxidative stress to inflammation in epithelial cells. Sci. Rep. 8, 914 (2018).

  • 92.

    DeFilippis, V. R., Alvarado, D., Sali, T., Rothenburg, S. & Fruh, K. Human cytomegalovirus induces the interferon response via the DNA sensor ZBP1. J. Virol. 84, 585–598 (2010).

  • 93.

    Ma, Z. & Damania, B. The cGAS-STING defense pathway and its counteraction by viruses. Cell Host Microbe 19, 150–158 (2016).

  • 94.

    Krol, J. et al. Ribonuclease dicer cleaves triplet repeat hairpins into shorter repeats that silence specific targets. Mol. Cell 25, 575–586 (2007).

  • 95.

    McCormick, C. & Khaperskyy, D. A. Translation inhibition and stress granules in the antiviral immune response. Nat. Rev. Immunol. 17, 647–660 (2017).

  • 96.

    Van Treeck, B. et al. RNA self-assembly contributes to stress granule formation and defining the stress granule transcriptome. Proc. Natl Acad. Sci. USA 115, 2734–2739 (2018).

  • 97.

    Mao, C., Sun, W. & Seeman, N. C. Assembly of Borromean rings from DNA. Nature 386, 137–138 (1997).

  • 98.

    Ng, S. K., Weissbach, R., Ronson, G. E. & Scadden, A. D. Proteins that contain a functional Z-DNA-binding domain localize to cytoplasmic stress granules. Nucleic Acids Res. 41, 9786–9799 (2013).

  • 99.

    Kelly, S. A., Panhuis, T. M. & Stoehr, A. M. Phenotypic plasticity: molecular mechanisms and adaptive significance. Compr. Physiol. 2, 1417–1439 (2012).

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