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Chapter 23 : Cotranscriptional Paramyxovirus mRNA Editing: a Contradiction in Terms?

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Cotranscriptional Paramyxovirus mRNA Editing: a Contradiction in Terms?, Page 1 of 2

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Abstract:

The currently are organized in three genera: the paramyxovirus genus (including Sendai virus [SeV], human parainfluenza virus type 1 [hPIV1], and human and bovine PIV3); morbilliviruses [e.g., measles virus and the distemper viruses]; and rubulaviruses (e.g., mumps virus and simian virus 5 {SV5}]). The first rubulavirus P gene sequence determined correctly was that of SV5. This yielded the surprising result that there was no single open reading frame (ORF) large enough to code for the SV5 P protein. mRNA transcribed from cDNAs that were exact copies of the SV5 P gene could be translated into the shorter V protein encoded by the 5' proximal ORF, but not into the longer P protein. Paramyxovirus RNA synthesis is restricted to the cytoplasm, and these viruses fend for themselves in all aspects of mRNA synthesis. Given that they formed their poly (A) tails by the unusual mechanism of polymerase stuttering, this mechanism was immediately suggested as one that could also account for the unusual G insertions. Experimental evidence in favor of a stuttering mechanism came from work with SeV, a member of the remaining paramyxovirus genus. SeV mRNAs made in vitro with purified virions contained the same pattern of G insertions as those found intracellularly, indicating that the process was carried out by viral gene products.

Citation: Kolakofsky D, Hausmann S. 1998. Cotranscriptional Paramyxovirus mRNA Editing: a Contradiction in Terms?, p 413-420. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch23

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Figures

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Figure 1

(a) Schematic representation of the paramyxovirus Ρ gene mRNAs. The mRNAs are indicated as horizontal lines, and the ORFs are indicated as boxes. For each group, the upper line shows the mRNA that is an exact copy of the gene, and the beginning of the ORF box indicates the ribosomal start codon. When more than one ORF box is attached to the line, they are accessed by alternate initiation codons. The boxes below indicate alternate downstream ORFs that are accessed by G insertions in the mRNAs. The positions of the insertions are shown by the dotted vertical lines. The three possible ORFs are indicated by different shading, (b) Distribution of G insertions in various paramyxovirus Ρ gene mRNAs. The distribution of the number of Gs inserted in the indicated paramyxovirus Ρ gene mRNAs is shown as a bar graph. The mumps virus data is from and was determined by sequencing 54 mRNA clones. The Sendai and bPIV3 data is from and was determined by a primer extension method directly on the mRNA population. “No. Gs added” refers to the unedited mRNA.

Citation: Kolakofsky D, Hausmann S. 1998. Cotranscriptional Paramyxovirus mRNA Editing: a Contradiction in Terms?, p 413-420. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch23
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Image of Figure 2
Figure 2

(a) Comparison of the paramyxovirus editing sites. The sequences are written as (+) RNA, 5′ to 3′, and are grouped into the three genera of the subfamily . Spaces have been introduced to emphasize the different elements of the sequence. The short G run that is expanded on mRNA editing is shown on the right, together with the pattern of G insertions that occurs for each group (dotted brackets). Note that the A run that precedes the G run is the only part of this -acting sequence which is strictly conserved according to genera. Also note that the second A residue upstream of the rubulavirus G run is replaced by a G (highlighted with a rectangle), which presumably accounts for why rubulaviruses insert a minimum of two G residues ( ). The shaded boxes indicate sequence conservations. When the boxed lower case “ac” is changed to TT as in the other members of the genus , SeV now edits its mRNA like PIV3. (b) Realignment possibilities at the paramyxovirus mRNA editing sites. RNA synthesis complexes of the template (top strand, written 3′ to 5′) and nascent chain (5′ to 3′, bottom strand) containing four base pairs are shown, for the SeV group and morbilliviruses (left side) and rubulaviruses (right side). The polymerase (not shown) whose catalytic site contains the 3′ end of the nascent (bottom) chain, is proposed to pause after incorporation opposite the middle template С residue (second level, in dotted brackets) and the nascent chain to realign on the template, allowing for U:G pairs (highlighted with a shaded circle in between) but not A:C pairs (which are shown looping out). The frequencies of the realignments that occur during natural virus infections are indicated by the strengths of the arrows. The numbers indicate the realignment of the nascent chain: minus as upstream, and plus as downstream, that is, the opposite of the subsequent insertions. For rubulaviruses, the −1 realignment is prevented by the marked (arrowhead) template С residue (which is a U in the SeV/MeV group). Once bypassed by a −2 shift (bottom panel), this template С aligns only with G's in further shifts. MeV, measles virus; MuV, mumps virus.

Citation: Kolakofsky D, Hausmann S. 1998. Cotranscriptional Paramyxovirus mRNA Editing: a Contradiction in Terms?, p 413-420. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch23
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Image of Figure 3
Figure 3

A stuttering model for paramyxovirus mRNA editing. The putative RNA: RNA hybrid between the polypyrimidine tract of the (−) template (top strand, written 3′ to 5′) and the polypurine run of the nascent mRNA chain (bottom strand, written 5′ to 3′) is shown, when the active site of the transcription complex (indicated by the long vertical box) is successively at template positions 1053 and 1054, representing editing (stuttering) and nonediting (nonstuttering) sites, respectively. At an editing site, the transcription complex has the choice of realigning its nascent RNA chain upstream on the template before the next nucleotide is added. This is because the minimum requirement that the realigned hybrid be nearly as stable as its predecessor has been met, because permissible U:G pairs are the only non-Watson–Crick pairs whose formation is required for the helical stack to remain unbroken. We assume that the rate constant for pseudotemplated addition of the G residue is much greater than that for realignment, and thus that , is mostly determined by . Having stuttered once at template position 1053, the transcription complex is back to where it started from and has the same choice, but seems to be determined differently from (see text). Escape from this process requires the active site to move on to a site where realignment of the nascent chain upstream is no longer possible, because one or more critical base pairs will not be reformed.

Citation: Kolakofsky D, Hausmann S. 1998. Cotranscriptional Paramyxovirus mRNA Editing: a Contradiction in Terms?, p 413-420. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch23
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Image of Figure 4
Figure 4

Thermodynamic reaction pathway of the transcription elongation complex. A schematic diagram of the relative activation barriers heights for elongation and stuttering (realignment) at stuttering and nonstuttering sites is shown. The black dot represents the transcription elongation complex. Barriers heights are given as Δ*, the free energy of activation. Note that the thermodynamic free energy of extending the chain from to + 1 (Δ°) is shown as being the same for stuttering and nonstuttering sites.

Citation: Kolakofsky D, Hausmann S. 1998. Cotranscriptional Paramyxovirus mRNA Editing: a Contradiction in Terms?, p 413-420. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch23
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References

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