7SL RNA, but not the 54-kd signal recognition particle protein, is an abundant component of both infectious HIV-1 and minimal virus-like particles

Onafuwa-Nuga, Adewunmi; Telesnitsky, Alice; King, Steven R.

doi:10.1261/rna.2306306

Cited by 87 publications

(155 citation statements)

References 30 publications

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“…1C). Consistent with reports that mRNAs are minor virion components (Onafuwa-Nuga et al 2006;Rulli et al 2007), only 3% of reads derived from mRNA exons (Fig. 1C).…”

Section: Characterizing the Hiv-1 Rna Packageomesupporting

confidence: 91%

“…Together with reports that 7SL RNA is recruited by both MLV and HIV-1 before assembling into mature SRP (Onafuwa-Nuga et al 2006;Wang et al 2007;Bach et al 2008;Apolonia et al 2015;Eckwahl et al 2015) and that many nascent ncRNAs are enriched in MLV virions (Garcia et al 2009;Eckwahl et al 2015), our data suggest that the encapsidation of newly made RNAs may be a general property of retroviruses. One theme that emerges from these studies is that forms of RNAs that are rare and difficult to detect in cells are strikingly enriched in virions.…”

Section: B Csupporting

confidence: 82%

“…For example, although 7SL is estimated to be present in 14 copies per HIV-1 virion, the SRP54 subunit is below the detection limit (Onafuwa-Nuga et al 2006). Similarly, although 7SL, Y RNAs, and vault RNAs are all highly enriched in MLV virions, their protein partners (SRP19, Ro60, and TEP1, respectively) were not detected (Garcia et al 2009;Eckwahl et al 2015).…”

Section: Introductionmentioning

confidence: 98%

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Analysis of the human immunodeficiency virus-1 RNA packageome

Eckwahl

Arnion

Kharytonchyk

et al. 2016

RNA

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All retroviruses package cellular RNAs into virions. Studies of murine leukemia virus (MLV) revealed that the major host cell RNAs encapsidated by this simple retrovirus were LTR retrotransposons and noncoding RNAs (ncRNAs). Several classes of ncRNAs appeared to be packaged by MLV shortly after synthesis, as precursors to tRNAs, small nuclear RNAs, and small nucleolar RNAs were all enriched in virions. To determine the extent to which the human immunodeficiency virus (HIV-1) packages similar RNAs, we used high-throughput sequencing to characterize the RNAs within infectious HIV-1 virions produced in CEM-SS T lymphoblastoid cells. We report that the most abundant cellular RNAs in HIV-1 virions are 7SL RNA and transcripts from numerous divergent and truncated members of the long interspersed element (LINE) and short interspersed element (SINE) families of retrotransposons. We also detected precursors to several tRNAs and small nuclear RNAs as well as transcripts derived from the ribosomal DNA (rDNA) intergenic spacers. We show that packaging of a pre-tRNA requires the nuclear export receptor Exportin 5, indicating that HIV-1 recruits at least some newly made ncRNAs in the cytoplasm. Together, our work identifies the set of RNAs packaged by HIV-1 and reveals that early steps in HIV-1 assembly intersect with host cell ncRNA biogenesis pathways.

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“…1C). Consistent with reports that mRNAs are minor virion components (Onafuwa-Nuga et al 2006;Rulli et al 2007), only 3% of reads derived from mRNA exons (Fig. 1C).…”

Section: Characterizing the Hiv-1 Rna Packageomesupporting

confidence: 91%

Section: B Csupporting

confidence: 82%

Section: Introductionmentioning

confidence: 98%

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Analysis of the human immunodeficiency virus-1 RNA packageome

Eckwahl

Arnion

Kharytonchyk

et al. 2016

RNA

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“…The perinuclear accumulation of Gag-GFP in the absence of SOCS1 expression coincides with observations made by Perlman and Resh, who described newly synthesised Gag-GFP transiently accumulating around the cell nucleus before trafficking to the plasma membrane [19]. Are these perinuclear aggregates a normal destination for Gag, for example to pick up viral and cellular RNA for virion incorporation [20,17]? Is SOCS1's role then to redirect Gag from these aggregates to sites of virion assembly before Gag gets degraded by lysosomes?…”

Section: Discussionsupporting

confidence: 87%

Socs1: A Host Factor Required for HIV-1 Gag Trafficking

Sivakumaran

Harrich²

2008

Future HIV Ther.

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Evaluation of: Ryo A, Tsurutani N, Ohba K et al.: SOCS1 is an inducible host factor during HIV-1 infection and regulates the intracellular trafficking and stability of HIV-1 Gag. Proc. Natl Acad. Sci. USA 105, 294–299 (2008). Gag is an essential HIV protein that is responsible for assembling infectious viral particles. The journey of Gag from synthesis to virion formation is an attractive target for anti-HIV therapy. While a lot is known about the cellular factors required for virion assembly and budding, relatively little is known about factors required for Gag trafficking. Ryo and colleagues provide the first evidence of such a factor, the suppressor of cytokine signaling (SOCS)1. They demonstrated that SOCS1 is important for Gag stability and plays a critical role in its trafficking within the cell. Without SOCS1 Gag accumulates in perinuclear bodies and is degraded by lysosomes. This article therefore highlights a new and novel target for stopping the production of HIV, a target that belongs to the relatively invariant host rather than the rapidly evolving virus.

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“…We also found many ncRNAs in the VLPs. Some of these elements have previously been demonstrated to be packaged by retroviruses, e.g., U6 snRNA in Rous-Sarcoma virus (29) and 7SL signal recognition particle RNA in HIV (30). The packaging of ncRNAs is interesting as some of these sequences (e.g., the Alu element widely found in the human genome that is derived from 7SL RNA) are known to be highly mobile elements that constitute members of the short interspersed element (SINE) class of nonautonomous retrotransposons that rely on reverse transcriptases encoded by other transposons for their genomic mobility.…”

Section: Resultsmentioning

confidence: 99%

Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus

Routh

Domitrovic

Johnson

2012

Proc. Natl. Acad. Sci. U.S.A.

106

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Next-generation sequencing is a valuable tool in our growing understanding of the genetic diversity of viral populations. Using this technology, we have investigated the RNA content of a purified nonenveloped single-stranded RNA virus, flock house virus (FHV). We have also investigated the RNA content of virus-like particles (VLPs) of FHV and the related Nudaurelia capensis omega virus. VLPs predominantly package ribosomal RNA and transcripts of their baculoviral expression vectors. In addition, we find that 5.3% of the packaged RNAs are transposable elements derived from the Sf21 genome. This observation may be important when considering the therapeutic use of VLPs. We find that authentic FHV virions also package a variety of host RNAs, accounting for 1% of the packaged nucleic acid. Significant quantities of host messenger RNAs, ribosomal RNA, noncoding RNAs, and transposable elements are readily detected. The packaging of these host RNAs elicits the possibility of horizontal gene transfer between eukaryotic hosts that share a viral pathogen. We conclude that the genetic content of nonenveloped RNA viruses is variable, not just by genome mutation, but also in the diversity of RNA transcripts that are packaged.deep-sequencing | virus evolution | virus assembly N ext-generation sequencing (NGS) is a powerful tool in the investigation of viral diversity from many different perspectives. NGS has been applied in directed approaches to investigate the prevalence of polymorphism or quasispecies present in a population of known viruses within a host, e.g., foot-and-mouth disease virus (1) or to follow the evolution of a viral genome and the frequency of known polymorphisms during the course of an infection, e.g., human rhinovirus (2) and HIV (3). The total genetic content of biological or clinical samples have been sequenced to uncover viruses present even at very low titers, for example, the presence of porcine circovirus-1 in Rotarix samples (4) and the identification of influenza virus subtypes and norovirus from nasopharyngeal and fecal samples collected during outbreaks (5).NGS has also been applied in unbiased approaches aimed at the discovery of new viral species without any advance genetic information. For example, the Merkel cell polyomavirus was discovered to be the causative agent of its eponymous carcinoma by deep sequencing the transcriptome of tumor cells and analyzing nonhost transcripts (6). Similarly, it has been possible to uncover the history of viral pathogens that have plagued an organism through the de novo assembly of the sequenced siRNAs that would have been generated to tackle viral infections. This approach has revealed the viral genomes of familiar miscreants as well as of new viruses, for example, in fruit flies, mosquitoes, and nematode worms (7).In this report, we employ NGS to investigate the total RNA encapsidated by authentic flock house virus (FHV) virions and by virus-like particles (VLPs) of FHV and of the related tetravirus, Nudaurelia capensis omega virus (NωV). Our analysis emplo...

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7SL RNA, but not the 54-kd signal recognition particle protein, is an abundant component of both infectious HIV-1 and minimal virus-like particles

Cited by 87 publications

References 30 publications

Analysis of the human immunodeficiency virus-1 RNA packageome

Analysis of the human immunodeficiency virus-1 RNA packageome

Socs1: A Host Factor Required for HIV-1 Gag Trafficking

Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus

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