Uncoupling ribosome biogenesis regulation from RNA polymerase I activity during <i>herpes simplex</i> virus type 1 infection

Belin, Stéphane; Kindbeiter, Karine; Hacot, Sabine; Albaret, Marie Alexandra; Roca-Martinez, Jean-Xavier; Thérizols, Gabriel; Grosso, Olivier; Diaz, Jean‐Jacques

doi:10.1261/rna.1935610

Cited by 20 publications

(23 citation statements)

References 38 publications

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“…Ribosome biogenesis is one of the processes that is modulated during viral infection. For example, herpes simplex virus 1, induces posttranscriptional cleavage of precursor rRNA (78). Here, we report that infection with UD/72 induces host cell upregulation of snoRNAs ( Fig.…”

Section: Discussionmentioning

confidence: 60%

Strand-Specific Dual RNA Sequencing of Bronchial Epithelial Cells Infected with Influenza A/H3N2 Viruses Reveals Splicing of Gene Segment 6 and Novel Host-Virus Interactions

Fabozzi

Oler

Liu

et al. 2018

J Virol

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Host-influenza virus interplay at the transcript level has been extensively characterized in epithelial cells. Yet, there are no studies that simultaneously characterize human host and influenza A virus (IAV) genomes. We infected human bronchial epithelial BEAS-2B cells with two seasonal IAV/H3N2 strains, Brisbane/10/07 and Perth/16/09 (reference strains for past vaccine seasons) and the well-characterized laboratory strain Udorn/307/72. Strand-specific RNA sequencing (RNA-seq) of the infected BEAS-2B cells allowed for simultaneous analysis of host and viral transcriptomes, in addition to pathogen genomes, to reveal changes in mRNA expression and alternative splicing (AS). In general, patterns of global and immune gene expression induced by the three IAVs were mostly shared. However, AS of host transcripts and small nuclear RNAs differed between the seasonal and laboratory strains. Analysis of viral transcriptomes showed deletions of the polymerase components (defective interfering-like RNAs) within the genome. Surprisingly, we found that the neuraminidase gene undergoes AS and that the splicing event differs between seasonal and laboratory strains. Our findings reveal novel elements of the host-virus interaction and highlight the importance of RNA-seq in identifying molecular changes at the genome level that may contribute to shaping RNA-based innate immunity. The use of massively parallel RNA sequencing (RNA-seq) has revealed insights into human and pathogen genomes and their evolution. Dual RNA-seq allows simultaneous dissection of host and pathogen genomes and strand-specific RNA-seq provides information about the polarity of the RNA. This is important in the case of negative-strand RNA viruses like influenza virus, which generate positive (complementary and mRNA) and negative-strand RNAs (genome) that differ in their potential to trigger innate immunity. Here, we characterize interactions between human bronchial epithelial cells and three influenza A/H3N2 strains using strand-specific dual RNA-seq. We focused on this subtype because of its epidemiological importance in causing significant morbidity and mortality during influenza epidemics. We report novel elements that differ between seasonal and laboratory strains highlighting the complexity of the host-virus interplay at the RNA level.

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Section: Discussionmentioning

confidence: 60%

Strand-Specific Dual RNA Sequencing of Bronchial Epithelial Cells Infected with Influenza A/H3N2 Viruses Reveals Splicing of Gene Segment 6 and Novel Host-Virus Interactions

Fabozzi

Oler

Liu

et al. 2018

J Virol

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“…In addition to showing a strong nucleolar accumulation, US11 is also found associated with cytoplasmic ribosomes (12,31). We and others have shown that upon HSV-1 infection, rRNA synthesis is altered (1,41), whereas ribosomal protein synthesis is maintained until later in the infection (16,38). We have also shown that nucleolin interacts with certain ribosomal proteins and might be involved in their assembly within ribosomal subunits (4).…”

Section: Discussionmentioning

confidence: 67%

Nucleolin Interacts with US11 Protein of Herpes Simplex Virus 1 and Is Involved in Its Trafficking

Greco

Arata

Soler

et al. 2012

J Virol

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Herpes simplex virus type 1 (HSV-1) infection induces profound nucleolar modifications at the functional and organizational levels, including nucleolar invasion by several viral proteins. One of these proteins is US11, which exhibits several different functions and displays both cytoplasmic localization and clear nucleolar localization very similar to that of the major multifunctional nucleolar protein nucleolin. To determine whether US11 interacts with nucleolin, we purified US11 protein partners by coimmunoprecipitations using a tagged protein, Flag-US11. From extracts of cells expressing Flag-US11 protein, we copurified a protein of about 100 kDa that was further identified as nucleolin. In vitro studies have demonstrated that nucleolin interacts with US11 and that the C-terminal domain of US11, which is required for US11 nucleolar accumulation, is sufficient for interaction with nucleolin. This association was confirmed in HSV-1-infected cells. We found an increase in the nucleolar accumulation of US11 in nucleolin-depleted cells, thereby revealing that nucleolin could play a role in US11 nucleocytoplasmic trafficking through one-way directional transport out of the nucleolus. Since nucleolin is required for HSV-1 nuclear egress, the interaction of US11 with nucleolin may participate in the outcome of infection.

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“…Protein extraction and western blot were performed as described (Belin et al, 2010) using the following antibodies: anti-FBL (38F3, Abcam); anti-p53 (DO-1, Santa Cruz); anti-b-actin (AC-15, Sigma); anti-Mdm2 (4B2, Bethyl Laboratories); anti-p21 (F-5, Santa Cruz); and anti-IGF1Ra (N20, Santa Cruz). For ChIP assays, chromatin was prepared from 1% formaldehyde fixed cells by sonication.…”

Section: Western Blot and Chromatin Immunoprecipitationmentioning

confidence: 99%

p53 Acts as a Safeguard of Translational Control by Regulating Fibrillarin and rRNA Methylation in Cancer

et al. 2013

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Ribosomes are specialized entities that participate in regulation of gene expression through their rRNAs carrying ribozyme activity. Ribosome biogenesis is overactivated in p53-inactivated cancer cells, although involvement of p53 on ribosome quality is unknown. Here, we show that p53 represses expression of the rRNA methyl-transferase fibrillarin (FBL) by binding directly to FBL. High levels of FBL are accompanied by modifications of the rRNA methylation pattern, impairment of translational fidelity, and an increase of internal ribosome entry site (IRES)-dependent translation initiation of key cancer genes. FBL overexpression contributes to tumorigenesis and is associated with poor survival in patients with breast cancer. Thus, p53 acts as a safeguard of protein synthesis by regulating FBL and the subsequent quality and intrinsic activity of ribosomes.

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Uncoupling ribosome biogenesis regulation from RNA polymerase I activity during herpes simplex virus type 1 infection

Cited by 20 publications

References 38 publications

Strand-Specific Dual RNA Sequencing of Bronchial Epithelial Cells Infected with Influenza A/H3N2 Viruses Reveals Splicing of Gene Segment 6 and Novel Host-Virus Interactions

Strand-Specific Dual RNA Sequencing of Bronchial Epithelial Cells Infected with Influenza A/H3N2 Viruses Reveals Splicing of Gene Segment 6 and Novel Host-Virus Interactions

Nucleolin Interacts with US11 Protein of Herpes Simplex Virus 1 and Is Involved in Its Trafficking

p53 Acts as a Safeguard of Translational Control by Regulating Fibrillarin and rRNA Methylation in Cancer

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