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Chapter 27 : Effects of Viral Replication on Cellular Membrane Metabolism and Function

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Abstract:

As with the majority of cytolytic animal viruses, picornavirus infection leads to profound alterations in cellular membranes. Three types of changes are observed at late times of infection in cellular membranes: enhanced membrane permeability, proliferation of intracellular membranous vesicles, and inhibition of vesicular trafficking with the consequent blockage of protein glycosylation. This chapter focuses on both the structural and functional modifications that membranes of picornavirus (PV)-infected cells undergo during virus replication. Distinct portions of the vesicle membranes are very densely stained and thicker than typical intracellular membranes. PV 2B, 2BC, and 3A proteins are able to block glycoprotein transport when they are expressed individually in mammalian cells. Sedimentation of cytoplasmic extracts in sucrose gradients yielded viral RNA polymerase activity associated with the smooth membranes. Viral replication complexes from this fraction contain all types of PV RNA and several viral proteins involved in RNA replication. The sequence of protein 2B is one of the least conserved among picornaviruses. The permeabilizing activity of coxsackievirus B3 (CVB3) 2B has been implicated in virus release, since viruses carrying a mutant 2B protein exhibited a defect in virus yield. However, in the case of PV 2B, it has been reported that this protein is located mainly in the central portion of the cytoplasm, associated with the membranous vesicles that surround the viral replication complexes. PV protein 2C is a 329-amino-acid polypeptide that contains a typical nucleoside triphosphate (NTP)-binding domain. Its sequence is one of the most highly conserved among all picornaviruses.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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Image of FIGURE 1
FIGURE 1

Schematic depiction of membrane modifications induced by Picornavirus at early and late stages of infection. During viral entry, early membrane permeabilization is directed to locate the virus genome in the cytoplasm. Low-molecular-weight compounds, as well as macro-molecules such as α-sarcin, enter cells together with virus particles. At late times of infection three types of changes are observed in cellular membranes: ( ) proliferation of intracellular membranous vesicles, ( ) inhibition of vesicular trafficking with the consequent blockage of protein glycosylation, and ( ) enhanced membrane permeability.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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Image of FIGURE 2a
FIGURE 2a

(A) Membranes generated in PV-infected cells. Electron microscopic autoradiograph of a PV-infected, actinomycin D-treated and 3Ή-uridine-labeled HEp-2 cell at 4 hpi. Note the different types of vesicles filling the cytoplasm. Silver grains show different centers of viral RNA synthesis fused into a large area of vacuoles. The cell shows a typical PV CPE. The nucleus assumes the typical crescent shape and is pushed aside by the mass of vacuolated membranes. The outer part of the cytoplasm is devoid of ER and contains single ribosomes; it shows no silver grain indicative of viral RNA synthesis. Also free of silver grains are the “nuclear extrusions” that appear and tend to surround the central vacuolated region (×11,000). Reprinted from Virology ( ), with permission.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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Image of FIGURE 2b
FIGURE 2b

(B) Structure of the PV replication complex. Electron micrograph of a PV replication complex surrounded by and attached to a rosette of virus-induced membrane vesicles (V) and containing a second, compact membrane system (arrowheads). Immunocytochemical labeling with 2C-Mab and 5-nm colloidal gold. Bar: 100 nm. Reprinted from ( ), with permission.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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Image of FIGURE 3
FIGURE 3

Modifications of lipase activity by Picornavirus. Schematic representation of the action of phospholipases A2 and C on a phospholipid. All phospholipids have a common backbone of sn-glycerol. The wavy lines denote fatty acyl esters or fatty acids; phosphate oxygens have been omitted for simplicity. “X” represents a polar head. The structures shown do not reflect the actual stereoconfiguration of a phospholipid. PL, phospholipid; PC, phosphatidylcholine; PI, phosphati-dylinositol; 2-LPL, 2-lysophospholipid; FFA, free fatty acid; 1,2-DG, 1,2-diacylglycerol.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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Image of FIGURE 4
FIGURE 4

Schematic representation of protein transport in cerevisiae and the sites of action of PV 2BC. Synthesis and maturation of four yeast proteins, vacuolar carboxypeptidase Y (CPY), aminopeptidase I (API), KAR2, and α-mating factor in the presence of PV protein 2BC. Reprinted from The EMBO Journal ( ), with permission.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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Image of FIGURE 5
FIGURE 5

Structure of PV 2B. (A) Amino acid sequence of PV 2B protein. (B) Hydropathy plot according to Kyte and Doolittle ( ). (C) Helical wheel diagram of a putative amphipathic helix found according to the method of Schiffer and Edmundson ( ). The distribution of charged residues on the hydrophilic face is well conserved among all enteroviruses. Hydrophobic residues are boxed; charged amino acids are circled. (D) Model of 2B insertion into membranes. Cylinders represent helices, the amphipathic one (nearer the Ν terminus) and the hydrophobic one (nearer the C terminus). Hydrophilic α-helix face is darkly shaded. Reprinted from Virology ( ), with permission.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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Image of FIGURE 6
FIGURE 6

PV 2BC motifs. Linear map of PV protein 2BC. Functional domains for RNA and NTP binding are depicted for 2C. Reprinted from The ( ), with permission.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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Image of FIGURE 7
FIGURE 7

Intracellular vesicle proliferation induced by PV 2BC in yeast. Thin-section electron microscopy of yeast cells expressing 2BC. Cells were fixed at 20 hpi and were processed for electron microscopy. Bar = 1 μΜ. Reprinted from ( ), with permission.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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Image of FIGURE 8
FIGURE 8

Structure of PV 3AB. (A) Schematic representation of the 3AB protein showing the conserved hydrophobic region (amino acids 60 to 80) and the positions of the different amino acid changes. The length of the line showing each variant represents the degree of change as measured by the lack of permeabilization to hygromycin Β in . The largest line corresponds to the lowest permeabilizing capacity. (B) Two alternative models are represented to explain the mode of action of 3AB as a membrane permeabilizer in cells. Reprinted from ( ), with permission.

Citation: Carrasco L, Guinea R, Irurzun A, Barco Á. 2002. Effects of Viral Replication on Cellular Membrane Metabolism and Function, p 337-354. In Semler B, Wimmer E (ed), Molecular Biology of Picornavirus. ASM Press, Washington, DC. doi: 10.1128/9781555817916.ch27
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