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Staufen1 senses overall transcript secondary structure to regulate translation

Nature Structural & Molecular Biology volume 21, pages 26–35 (2014)Cite this article

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Abstract

Human Staufen1 (Stau1) is a double-stranded RNA (dsRNA)-binding protein implicated in multiple post-transcriptional gene-regulatory processes. Here we combined RNA immunoprecipitation in tandem (RIPiT) with RNase footprinting, formaldehyde cross-linking, sonication-mediated RNA fragmentation and deep sequencing to map Staufen1-binding sites transcriptome wide. We find that Stau1 binds complex secondary structures containing multiple short helices, many of which are formed by inverted Alu elements in annotated 3′ untranslated regions (UTRs) or in 'strongly distal' 3′ UTRs. Stau1 also interacts with actively translating ribosomes and with mRNA coding sequences (CDSs) and 3′ UTRs in proportion to their GC content and propensity to form internal secondary structure. On mRNAs with high CDS GC content, higher Stau1 levels lead to greater ribosome densities, thus suggesting a general role for Stau1 in modulating translation elongation through structured CDS regions. Our results also indicate that Stau1 regulates translation of transcription-regulatory proteins.

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Figure 1: Mapping of Stau1 RNA-binding sites reveals coding regions and 3′ UTRs as major occupancy sites.
Figure 2: Inverted Alu pairs are an important class of Stau1-binding sites.
Figure 3: Characterization of the structural features of Stau1 Alu-binding sites.
Figure 4: Examples of 3′-UTR non-Alu Staufen-binding sites.
Figure 5: Stau1 binding to 3′ UTRs correlates with GC content and predicted secondary-structure free energy.
Figure 6: Stau1 occupancy on the CDS strongly correlates with GC content and predicted secondary-structure free energy.
Figure 7: Consequences of Stau1 binding on RNA levels and ribosome density.
Figure 8: Model of Stau1 RNA binding and its functional role in translation.

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Acknowledgements

We would like to acknowledge M. Garber, A. Bicknell, A. Noma and J. Braun for comments on the manuscript and the University of Massachusetts Medical School Deep Sequencing Core for technical advice. We thank P.S. Chen for technical help in preparing plasmids and cell lines. We also thank H. Ozadam for technical advice in using RNA structure–prediction tools. Finally, we thank M. Janas, R. Lakshmi and D. Morrissey from Novartis for kindly sharing total RNA from Huh7 and HepG2 cells upon Stau1 and Stau2 knockdown. M.J.M. is supported as a Howard Hughes Medical Institute Investigator.

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  1. Can Cenik

    Present address: Present address: Department of Genetics, Stanford University School of Medicine, Stanford, California, USA.,

Authors and Affiliations

  1. Department of Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, Worcester, Massachusetts, USA

    Emiliano P Ricci, Alper Kucukural, Can Cenik, Blandine C Mercier, Guramrit Singh, Erin E Heyer, Ami Ashar-Patel, Lingtao Peng & Melissa J Moore

  2. RNA Therapeutics Institute, University of Massachusetts Medical School, Worcester, Massachusetts, USA

    Emiliano P Ricci, Alper Kucukural, Can Cenik, Blandine C Mercier, Guramrit Singh, Erin E Heyer, Ami Ashar-Patel, Lingtao Peng & Melissa J Moore

  3. Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, Massachusetts, USA

    Emiliano P Ricci, Alper Kucukural, Can Cenik, Blandine C Mercier, Guramrit Singh, Erin E Heyer, Ami Ashar-Patel, Lingtao Peng & Melissa J Moore

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Contributions

E.P.R. and M.J.M. conceived the study, designed the experiments and wrote the manuscript. E.P.R. performed the experiments. A.K. conducted most bioinformatics analyses. C.C. designed and implemented the ribo-seq analysis. E.P.R. and A.K. designed and performed GC-content and secondary structure–prediction analyses. B.C.M. and G.S. contributed with tandem-affinity purification of Stau1 complexes. E.E.H. contributed with cDNA library preparation for high-throughput sequencing. A.A.-P. prepared PAS-seq cDNA libraries. L.P. participated in quantitative PCR analysis.

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Correspondence to Melissa J Moore.

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Integrated supplementary information

Supplementary Figure 1 Tandem affinity purification of Stau1 complexes.

a, Western-blotting for endogenous hnrnp-A1 and Stau1 from total cell lysate and from proteins extracted from oligo(dT) pull-down of mRNA after cells were exposed to increasing doses of UV wave-lengths. b. Quantification of exogenous P32-labeled Arf1 mRNA eluted from Flag-Only, Flag-Stau1-Mut and Flag-Stau1-WT FLAG-immunoprecipitates. c, Western blotting for endogenous and Flag-Stau1 proteins during native tandem affinity purifications. d, Same as “c,” for Crosslinked tandem affinity purifications. e, Scatter plots of gene read counts between biological replicates of Stau1-WT and Mut CROSS libraries.

Supplementary Figure 2 Distribution of sequencing reads.

Distribution of sequencing reads to 28S rRNA or “Other rRNA” (18S + 5.8S + 5S rRNA) as well as Alu elements and non-Alu genomic or transcriptomic sequences for each library.

Supplementary Figure 3 Stau1 is associated with actively translating ribosomes.

a, Sucrose sedimentation analysis of Stau1 expressing cells. Cells were incubated with cycloheximide (100 μg.ml-1) for 10 minutes before cell lysis. Obtained lysates were treated with RNase A or not before loading them on top of a 10-50% linear sucrose gradient and subjected to ultracentrifugation. After fractionation, obtained samples are analyzed by western-blotting using anti-Stau1 antibodies. b, Ribosome run-off assay for Stau1 expressing cells. Cells were incubated with cycloheximide for 10 minutes (upper panel) or harringtonine (2 μg.ml-1) for 10 minutes (middle panel) or 40 minutes (lower panel) before adding cycloheximide and further incubating cells for 10 minutes before lysis. Cells lysates are then loaded on top of a 10-50% linear sucrose gradient and subjected to ultracentrifugation. After fractionation, obtained samples are analyzed by western-blotting using anti-Stau1 and anti-RPL26 antibodies.

Supplementary Figure 4 Full gene visualization of Stau1-binding sites in 3' UTRs, extended 3' UTRs and introns.

RNA-Seq (green) corresponds to sequencing of poly(A) selected total RNA. Stau1-WT CROSS (yellow) corresponds to FLAG-Stau1-WT tandem IPs from formaldehyde crosslinked cells, sonicated to shear Stau1 bound RNAs. Stau1-Mut CROSS (blue) corresponds to the same condition described above performed on cells expressing a mutant Stau1 lacking dsRNA binding activity. Stau1-WT FOOT (brown) corresponds to FLAG-Stau1-WT tandem IP under native conditions that are incubated with RNaseI in order to obtain a footprint of Stau1 bound RNAs. Stau1-Mut FOOT (violet) corresponds to the same condition described above performed on cells expressing a mutant Stau1 lacking dsRNA binding activity. PAS-Seq (black) corresponds to “polyadenylation site” sequencing reads from HEK293 cells.

Supplementary Figure 5 Stau1 binding to inverted Alu pairs in 3' UTRs, distal 3' UTRs and introns.

a, Composite plot of Stau1-WT CROSS, Stau1-Mut CROSS and RNA-Seq read counts around partial Tandem or Inverted Alu pairs where at least one of the Alu elements in the pair is shorter than 200 nt. Read counts normalized to RPKM of the host gene are calculated for a region encompassing each Alu element and 1 kb upstream the most 5' Alu and downstream the most 3' Alu element for both Tandem and Inverted Alu pairs. Results are presented for Tandem Alu elements separated by 0-200 nt (upper panel) or for Inverted Alu pairs separated by 0-200 nt, 200 to 500 nt, 500 to 1 kb, 1 kb to 2 kb or 2 kb and beyond (lower panels). b, Same composite plot for full-length Alu pairs located in distal 3'UTR regions. c, Same composite plot for full-length Alu pairs located in intronic regions.

Supplementary Figure 6 Gene visualization of Stau1-WT FOOT signal in Arf1 and Stau1-WT CROSS signal in a gene with labile Stau1-binding sites.

a, Top-panel, predicted secondary structure of the 3'UTR of Arf1 and position of the Stau1 binding site adapted from 20. Bottom panel, RNA-Seq (green), Stau1-WT FOOT (brown) and Stau1-Mut FOOT (blue) signal at the 3'UTR of Arf1 as well as position of the previously mapped Stau1 binding site from 20. b. RNA-Seq (green),Stau1-WT CROSS (yellow) and Stau1-WT FOOT (brown) on the HDAC11 gene.

Supplementary Figure 7 Correlation of RNA-seq and ribo-seq gene read counts between cells with reduced levels of Stau1 and cells overexpressing Stau1.

a, Uncropped western-blot against Stau1 and GPADH in HEK293 cells upon knock-down or overexpression of Stau1. b, Scatter plot of RNA-Seq read counts between cells with high or low Stau1 levels. c, Scatter plot of Ribo-Seq read counts between cells with high or low Stau1 levels. For both plots, Stau1 position is represented by a red colored dot.

Supplementary Figure 8 Quantitative RT-PCR of Stau1-target mRNAs in HEK293, Huh7 and SK-Hep1 cells.

a, Quantitative RT-PCR against Stau1 mRNA targets from HEK293 cells transfected with a control shRNA or with an shRNA targeting Stau1 or with a control shRNA and the addition of doxycycline to overexpress Flag-Stau1 WT. b and c, Quantitative RT-PCR against Stau1 and Stau2 as well as Stau1 targets from Huh7 and SK-Hep1 cells transfected with shRNAs against Stau1 or siRNA against Stau2 or both. Error bars correspond to the standard deviation calculated from 3 biological replicates.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–8 (PDF 2396 kb)

Supplementary Table 1

List of genes with Stau1 binding at extended 3' UTR (XLSX 71 kb)

Supplementary Table 2

List of genes with Alu and non-Alu Stau1-binding sites (XLSX 85 kb)

Supplementary Table 3

List of Gene Ontology terms enriched in Stau1 targets (XLSX 68 kb)

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Ricci, E., Kucukural, A., Cenik, C. et al. Staufen1 senses overall transcript secondary structure to regulate translation. Nat Struct Mol Biol 21, 26–35 (2014). https://doi.org/10.1038/nsmb.2739

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