Abstract
As they assemble, retroviruses encapsidate both their genomic RNAs and several types of host RNA. Whereas limited amounts of messenger RNA (mRNA) are detectable within virion populations, the predominant classes of encapsidated host RNAs do not encode proteins, but instead include endogenous retroelements and several classes of non-coding RNA (ncRNA), some of which are packaged in significant molar excess to the viral genome. Surprisingly, although the most abundant host RNAs in retroviruses are also abundant in cells, unusual forms of these RNAs are packaged preferentially, suggesting that these RNAs are recruited early in their biogenesis: before associating with their cognate protein partners, and/or from transient or rare RNA populations. These RNAs’ packaging determinants differ from the viral genome’s, and several of the abundantly packaged host ncRNAs serve cells as the scaffolds of ribonucleoprotein particles. Because virion assembly is equally efficient whether or not genomic RNA is available, yet RNA appears critical to the structural integrity of retroviral particles, it seems possible that the selectively encapsidated host ncRNAs might play roles in assembly. Indeed, some host ncRNAs appear to act during replication, as some transfer RNA (tRNA) species may contribute to nuclear import of human immunodeficiency virus 1 (HIV-1) reverse transcription complexes, and other tRNA interactions with the viral Gag protein aid correct trafficking to plasma membrane assembly sites. However, despite high conservation of packaging for certain host RNAs, replication roles for most of these selectively encapsidated RNAs—if any—have remained elusive.
Highlights
As they assemble, retroviruses encapsidate both their genomic RNAs and several types of host RNA
Besides 7SL and transfer RNA (tRNA), packaged host RNAs that are present in at least one copy per virion for one retrovirus or another include the 60 kDa Ro autoantigen-associated RNAs Y1 and Y3, which are each present at about four copies per MLV virion [20], the spliceosomal RNA U6, which is present at about one copy per MLV or Rous sarcoma virus (RSV) virion [8,19], 5S rRNA in MLV [8] and vault RNA, which is present at about one copy per MLV [9]
Because 7SL RNA is packaged by minimal assembly-competent human immunodeficiency virus 1 (HIV-1) virus-like particles (VLPs), the viral determinants of its incorporation into HIV-1 particles map to the carboxy-terminal domain of capsid protein (CA) plus spacer peptide SP1 [10]
Summary
In the late 1960s, before RNA tumor viruses were known to reverse-transcribe and at a time when experiments characterizing RNA required radioactive cell labeling and cumbersome sedimentation gradients, it was already clear that RNA tumor viruses contained multiple RNA species: a high molecular weight class that was presumed to be the viral genome, and a heterogeneous pool of smaller. One study that quantified relative levels of certain RNA species in virions and cells found that the host non-coding 7SL RNA is 250-fold more highly enriched in virions than actin mRNA [10]. Based on their total mass (about 1/3 or more of total virion RNA) and average length (very roughly 100 nucleotides (nt)), the host non-coding RNAs in retroviruses likely outnumber viral gRNAs by a factor of at least 50.
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