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DHX9 suppresses RNA processing defects originating from the Alu invasion of the human genome

Nature advance online publication 29 March 2017. doi:10.1038/nature21715

Authors: Tuğçe Aktaş, İbrahim Avşar Ilık, Daniel Maticzka, Vivek Bhardwaj, Cecilia Pessoa Rodrigues, Gerhard Mittler, Thomas Manke, Rolf Backofen & Asifa Akhtar

Transposable elements are viewed as ‘selfish genetic elements’, yet they contribute to gene regulation and genome evolution in diverse ways. More than half of the human genome consists of transposable elements. Alu elements belong to the short interspersed nuclear element (SINE) family of repetitive elements, and with over 1 million insertions they make up more than 10% of the human genome. Despite their abundance and the potential evolutionary advantages they confer, Alu elements can be mutagenic to the host as they can act as splice acceptors, inhibit translation of mRNAs and cause genomic instability. Alu elements are the main targets of the RNA-editing enzyme ADAR and the formation of Alu exons is suppressed by the nuclear ribonucleoprotein HNRNPC, but the broad effect of massive secondary structures formed by inverted-repeat Alu elements on RNA processing in the nucleus remains unknown. Here we show that DHX9, an abundant nuclear RNA helicase, binds specifically to inverted-repeat Alu elements that are transcribed as parts of genes. Loss of DHX9 leads to an increase in the number of circular-RNA-producing genes and amount of circular RNAs, translational repression of reporters containing inverted-repeat Alu elements, and transcriptional rewiring (the creation of mostly nonsensical novel connections between exons) of susceptible loci. Biochemical purifications of DHX9 identify the interferon-inducible isoform of ADAR (p150), but not the constitutively expressed ADAR isoform (p110), as an RNA-independent interaction partner. Co-depletion of ADAR and DHX9 augments the double-stranded RNA accumulation defects, leading to increased circular RNA production, revealing a functional link between these two enzymes. Our work uncovers an evolutionarily conserved function of DHX9. We propose that it acts as a nuclear RNA resolvase that neutralizes the immediate threat posed by transposon insertions and allows these elements to evolve as tools for the post-transcriptional regulation of gene expression.

Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP

Nature advance online publication 29 March 2017. doi:10.1038/nature21720

Authors: Dick Wu, Taulant Bacaj, Wade Morishita, Debanjan Goswami, Kristin L. Arendt, Wei Xu, Lu Chen, Robert C. Malenka & Thomas C. Südhof

Myeloid progenitor cluster formation drives emergency and leukaemic myelopoiesis

Nature advance online publication 29 March 2017. doi:10.1038/nature21693

Authors: Aurélie Hérault, Mikhail Binnewies, Stephanie Leong, Fernando J. Calero-Nieto, Si Yi Zhang, Yoon-A Kang, Xiaonan Wang, Eric M. Pietras, S. Haihua Chu, Keegan Barry-Holson, Scott Armstrong, Berthold Göttgens & Emmanuelle Passegué

Biomechanics: The aerodynamics buzz from mosquitoes

Nature advance online publication 29 March 2017. doi:10.1038/nature21904

Author: Laura A. Miller

Mosquitoes flap their long, thin wings four times faster than similarly sized insects. Imaging and computational analysis of mosquito flight illuminates some aerodynamic mechanisms not seen before in animal flight.

CRISPR–Cas systems exploit viral DNA injection to establish and maintain adaptive immunity

Nature advance online publication 29 March 2017. doi:10.1038/nature21719

Authors: Joshua W. Modell, Wenyan Jiang & Luciano A. Marraffini

Clustered regularly interspaced short palindromic repeats (CRISPR)–Cas systems provide protection against viral and plasmid infection by capturing short DNA sequences from these invaders and integrating them into the CRISPR locus of the prokaryotic host. These sequences, known as spacers, are transcribed into short CRISPR RNA guides that specify the cleavage site of Cas nucleases in the genome of the invader. It is not known when spacer sequences are acquired during viral infection. Here, to investigate this, we tracked spacer acquisition in Staphylococcus aureus cells harbouring a type II CRISPR–Cas9 system after infection with the staphylococcal bacteriophage ϕ12. We found that new spacers were acquired immediately after infection preferentially from the cos site, the viral free DNA end that is first injected into the cell. Analysis of spacer acquisition after infection with mutant phages demonstrated that most spacers are acquired during DNA injection, but not during other stages of the viral cycle that produce free DNA ends, such as DNA replication or packaging. Finally, we showed that spacers acquired from early-injected genomic regions, which direct Cas9 cleavage of the viral DNA immediately after infection, provide better immunity than spacers acquired from late-injected regions. Our results reveal that CRISPR–Cas systems exploit the phage life cycle to generate a pattern of spacer acquisition that ensures a successful CRISPR immune response.

Optically excited structural transition in atomic wires on surfaces at the quantum limit

Nature advance online publication 29 March 2017. doi:10.1038/nature21432

Authors: T. Frigge, B. Hafke, T. Witte, B. Krenzer, C. Streubühr, A. Samad Syed, V. Mikšić Trontl, I. Avigo, P. Zhou, M. Ligges, D. von der Linde, U. Bovensiepen, M. Horn-von Hoegen, S. Wippermann, A. Lücke, S. Sanna, U. Gerstmann & W. G. Schmidt

Transient control over the atomic potential-energy landscapes of solids could lead to new states of matter and to quantum control of nuclear motion on the timescale of lattice vibrations. Recently developed ultrafast time-resolved diffraction techniques combine ultrafast temporal manipulation with atomic-scale spatial resolution and femtosecond temporal resolution. These advances have enabled investigations of photo-induced structural changes in bulk solids that often occur on timescales as short as a few hundred femtoseconds. In contrast, experiments at surfaces and on single atomic layers such as graphene report timescales of structural changes that are orders of magnitude longer. This raises the question of whether the structural response of low-dimensional materials to femtosecond laser excitation is, in general, limited. Here we show that a photo-induced transition from the low- to high-symmetry state of a charge density wave in atomic indium (In) wires supported by a silicon (Si) surface takes place within 350 femtoseconds. The optical excitation breaks and creates In–In bonds, leading to the non-thermal excitation of soft phonon modes, and drives the structural transition in the limit of critically damped nuclear motion through coupling of these soft phonon modes to a manifold of surface and interface phonons that arise from the symmetry breaking at the silicon surface. This finding demonstrates that carefully tuned electronic excitations can create non-equilibrium potential energy surfaces that drive structural dynamics at interfaces in the quantum limit (that is, in a regime in which the nuclear motion is directed and deterministic). This technique could potentially be used to tune the dynamic response of a solid to optical excitation, and has widespread potential application, for example in ultrafast detectors.

Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition

Nature advance online publication 29 March 2017. doi:10.1038/nature21711

Authors: Ilya M. Flyamer, Johanna Gassler, Maxim Imakaev, Hugo B. Brandão, Sergey V. Ulianov, Nezar Abdennur, Sergey V. Razin, Leonid A. Mirny & Kikuë Tachibana-Konwalski

Chromatin is reprogrammed after fertilization to produce a totipotent zygote with the potential to generate a new organism. The maternal genome inherited from the oocyte and the paternal genome provided by sperm coexist as separate haploid nuclei in the zygote. How these two epigenetically distinct genomes are spatially organized is poorly understood. Existing chromosome conformation capture-based methods are not applicable to oocytes and zygotes owing to a paucity of material. To study three-dimensional chromatin organization in rare cell types, we developed a single-nucleus Hi-C (high-resolution chromosome conformation capture) protocol that provides greater than tenfold more contacts per cell than the previous method. Here we show that chromatin architecture is uniquely reorganized during the oocyte-to-zygote transition in mice and is distinct in paternal and maternal nuclei within single-cell zygotes. Features of genomic organization including compartments, topologically associating domains (TADs) and loops are present in individual oocytes when averaged over the genome, but the presence of each feature at a locus varies between cells. At the sub-megabase level, we observed stochastic clusters of contacts that can occur across TAD boundaries but average into TADs. Notably, we found that TADs and loops, but not compartments, are present in zygotic maternal chromatin, suggesting that these are generated by different mechanisms. Our results demonstrate that the global chromatin organization of zygote nuclei is fundamentally different from that of other interphase cells. An understanding of this zygotic chromatin ‘ground state’ could potentially provide insights into reprogramming cells to a state of totipotency.

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