Filamentous influenza viruses

Abstract

Clinical isolates of influenza virus produce pleomorphic virus particles, including extremely long filamentous virions. In contrast, strains of influenza that have adapted to laboratory growth typically produce only spherical virions. As a result, the filamentous phenotype has been overlooked in most influenza virus research. Recent advances in imaging and improved animal models have highlighted the distinct structure and functional relevance of filamentous virions. In this review we summarize what is currently known about these strikingly elongated virus particles and discuss their possible roles in clinical infections.

Figure 1. Filamentous influenza virions are lost on laboratory passage.

Filamentous influenza virions are clearly visible after two passages of the clinical isolate influenza A/Rockefeller Institute/1/1957 (H2N2) virus in embryonated chicken eggs (a) but are lost following twelve passages (b). Electron micrographs © Choppin et al., 1960. Originally published in THE JOURNAL OF EXPERIMENTAL MEDICINE. 112:945-52.

Figure 2. Bacilliform and filamentous influenza virions at high resolution.

Electron tomograms of influenza virions, showing slices (left panels) and segmented images (right panels) of (a) a transverse section of a bacilliform virion, (b) a longitudinal section of the tip of a filamentous virion and (c) a longitudinal section of an Archetti body at the end of a filamentous virion. Images were manually segmented and coloured to show viral glycoproteins (green), membrane and associated matrix (purple), genome (brown) and putative free M1 sheets (yellow). Tomograms were obtained as part of a previous study (Vijayakrishnan et al., 2013) and manually segmented using Amira (TGS).

Figure 3. Dimensions of influenza virions.

The dimensions of influenza virions, shown (a) as a schematic of budding and released virions, with typical sizes indicated, and (b) as measurements of purified influenza A/Udorn/72 virions. For (a) it should be noted that the incorporation of NS1 and NEP has so far only been examined in spherical virions, and their general incorporation is inferred from this. For (b) measurements of 96 virions were taken by cryoelectron microscopy (data replotted from Vijayakrishnan et al., 2013). Open circles indicate filaments which extended beyond the field of view and so are longer than measured. Spherical virions (s) are distinguished from bacilliform virions (b) by having an axial ratio less than 1.2 (dashed line); filaments (f) are distinguished from bacilliform virions by having a length greater than 250 nm (solid line).