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Chapter 19 : Possible Unifying Mechanism of Picornavirus Genome Replication

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Abstract:

This chapter summarizes all the pertinent experimental evidence that is currently available and proposes a unified model for picornavirus RNA replication. These data are derived from three types of experiments. In the simplest type, purified enzymes are used to study biochemical reactions in vitro. The second in complexity are those studies that use crude replication complexes isolated either from infected cells or from coupled translation/replication reactions of viral RNA. Finally, the most difficult method involves studying reactions in the infected cell itself. The proteins of the P3 domain are those that are most directly involved in the process of RNA synthesis. During translation of poliovirus RNA the P3 precursor is generated from the polyprotein by a fast cleavage event at the amino terminus of the 3A-coding region. The RNA polymerases of poliovirus and human rhinoviruses (HRV)2 are dependent in vitro on an RNA template and on a primer, either RNA, DNA, or VPg. Properties and functions of proteins encoded by the P3 domain of the poliovirus polyprotein are discussed. Mutational analysis of the heteropolymeric sequences in the 3 ' nontranslated region (NTR) of entero- and rhinoviruses indicated that this region is important for RNA replication. Prior to the initiation of minus-strand RNA synthesis, the RNA polymerase has to recognize its own viral RNA in a pool of cellular mRNAs and then select it as the only template for transcription.

Citation: Paul A. 2002. Possible Unifying Mechanism of Picornavirus Genome Replication, p 227-246. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch19

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Figures

Image of FIGURE 1
FIGURE 1

Structure of poliovirus genomic RNA and processing of the polyprotein. The single-stranded RNA of poliovirus is shown with the terminal protein VPg at its 5′ end and the 3′ NTR with the poly(A) tail at its 3′ end. The 5′ NTR consists of the cloverleaf and the large IRES element. The location of the cre(2C) hairpin in the coding region of 2C is indicated. The attachment site of the 5′-terminal UMP to the tyrosine of VPg is shown enlarged. The polyprotein contains structural (P1) and nonstructural (P2, P3) domains. Processing of the P2 and P3 precursors of the polyprotein by 3C/3CD is shown enlarged, with vertical lines indicating the proteinase cleavage sites.

Citation: Paul A. 2002. Possible Unifying Mechanism of Picornavirus Genome Replication, p 227-246. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch19
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Image of FIGURE 2
FIGURE 2

Predicted secondary structures of picornaviral -replicating elements. (A) The PV1(M) 5′ cloverleaf. (B) The PV1(M) 3′ NTR-poly(A). (C) The PV1(M) (2C), HRV14 (VP1), and HRV2 (2A) RNAs. The conserved sequences in the loops are shown with bold letters. Also shown (boxed in) is the conserved sequence in all the known internal -replicating elements of picornaviral RNAs. See Note Added in Proof.

Citation: Paul A. 2002. Possible Unifying Mechanism of Picornavirus Genome Replication, p 227-246. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch19
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Image of FIGURE 3
FIGURE 3

Proposed model of picornaviral minus-strand RNA synthesis. An RNP complex formed around the 5′ cloverleaf interacts with the PABP bound to the 3′ NTR-poly(A) resulting in a circularized genome ( ). Proteinase 3CD cleaves membrane-bound 3AB to yield VPg and 3A. 3D, 3CD, and VPg form a complex with the cre RNA hairpin. The polymerase synthesizes VPgpU and VPgpUpU using the AAACA sequence in the loop as template, and the complex is transferred to the 3′ end of the poly(A) tail. The VPg-linked precursors then serve as primer for 3Dduring the elongation step, a reaction possibly stimulated by membrane-bound 3AB.

Citation: Paul A. 2002. Possible Unifying Mechanism of Picornavirus Genome Replication, p 227-246. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch19
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Image of FIGURE 4
FIGURE 4

Slide-back model of VPgpUpU synthesis by PV1(M) 3D. Proteins 3D, 3CD, and VPg form a complex with the PV1(M) (2C) RNA hairpin. Using A, in the A1A2CA sequence of the loop as template, the complementary nucleotide is selected and 3Dpol catalyzes the formation of a phosphodiester bond between UMP and the hydroxyl group of tyrosine in VPg. VPgpU then slides back and hydrogen bonds with A and the second UMP is added on the A template nucleotide.

Citation: Paul A. 2002. Possible Unifying Mechanism of Picornavirus Genome Replication, p 227-246. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch19
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Image of FIGURE 6
FIGURE 6

Comparison of protein-primed RNA and DNA synthesis. (A) Initiation of picornaviral minus-strand RNA synthesis and phage Φ29 DNA synthesis. The slide-back mechanism is used by the picornaviral RNA polymerase and by phage Φ29 DNA polymerase ( ) for the synthesis of the dinucleotidylylated protein precursors. Details of the mechanism are described in the text. (B) Picornaviral minus-strand RNA synthesis and HBV cDNA synthesis. Both viral polymerases use an internal RNA hairpin as the template for the protein-priming reaction and the nucleotidylylated proteins are translocated to the 3′ end of the plus strand where they are elongated into the complementary strands ( ). (C) Picornaviral plus-strand RNA synthesis and phage Φ29 DNA synthesis ( ). The end of the double-stranded template is first unwound by the binding of proteins to the plus and minus strands. The viral polymerases use the 3′ end of their RNA/DNA strand as template for the nucleotidylylation teaction. The precursors are elongated into complementary RNA/DNA strands. RT, reverse transcriptase; DP, DNA polymerase; TP, terminal protein.

Citation: Paul A. 2002. Possible Unifying Mechanism of Picornavirus Genome Replication, p 227-246. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch19
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Image of FIGURE 5
FIGURE 5

Proposed model of picornaviral plus-strand RNA synthesis. The end of the RF is unwound by the binding of PCBP2/3CD and 3AB/3CD to the plus strand and of 2C to the minus strand of the 5′ cloverleaf. 3CD catalyzes the cleavage of membrane-bound 3AB to 3A and VPg, and 3CD undergoes autoprocessing. The polymerase synthesizes VPgpUpU using the 3′-terminal two As of the minus strand as template. The precursors are elongated into plus strands by the polymerase, possibly using the stimulatory activity of membrane-bound 3AB.

Citation: Paul A. 2002. Possible Unifying Mechanism of Picornavirus Genome Replication, p 227-246. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch19
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Tables

Generic image for table
TABLE 1

Properties and functions of proteins encoded by the P3 domain of the poliovirus polyprotein

Citation: Paul A. 2002. Possible Unifying Mechanism of Picornavirus Genome Replication, p 227-246. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch19
Generic image for table
TABLE 2

Viral and cellular proteins binding to picornaviral -replicating RNA elements

Brackets indicate references.

Citation: Paul A. 2002. Possible Unifying Mechanism of Picornavirus Genome Replication, p 227-246. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch19

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