Differences in the tissue tropism to chicken oviduct epithelial cells between avian coronavirus IBV strains QX and B1648 are not related to the sialic acid binding properties of their spike proteins

Abstract

The avian coronavirus (AvCoV) infectious bronchitis virus (IBV) is a major poultry pathogen. A characteristic feature of IBV is the occurrence of many different strains belonging to different serotypes, which makes a complete control of the disease by vaccinations a challenging task. Reasons for differences in the tissue tropism and pathogenicity between IBV strains, e.g. a predilection for the kidneys or the oviduct are still an open question. Strains of the QX genotype have been major pathogens in poultry flocks in Asia, Europe and other parts of the world. They are the cause of severe problems with kidney disease and reproductive tract disorders. We analysed infectivity and binding properties of the QX strain and compared them with those of the nephropathogenic strain B1648. As most IBV strains do not infect permanent cell lines and show infection only in primary chicken cells of the target organs, we developed a culture system for chicken oviduct explants. The epithelial cells of the oviduct showed a high susceptibility to infection by the QX strain and were almost resistant to infection by the nephropathogenic B1648 strain. Binding tests with isolated primary oviduct epithelial cells and soluble S1 proteins revealed that S1 proteins of two IBV strains bound with the same efficiency to oviduct epithelial cells. This attachment was sialic acid dependent, indicating that the sugar binding property of IBV spike proteins is not the limiting factor for differences in infection efficiency for the oviduct of the corresponding viruses.

The avian coronavirus spike protein

“…5). These results are in line with the previously observed binding patterns of dimeric S1 of B1648 and QX to oviduct explants (Mork et al, 2014) and other IBV permissive cells, including tracheal epithelial cells and primary chicken kidney cells (Shahwan et al, 2013). Similarly, dimeric Beaudette S1 bound to chicken cells (Hesse et al, 2012), while trimeric Beaudette S1 was not sufficient for binding to trachea ( Fig.…”

“…This suggests that either these proteins bind with much lower affinities to the same sialic acid, or that they recognize yet other unidentified host factor, including specific sialic acids which might be not present on this array. While the results of Mork et al (2014) suggest that binding of recombinant dimeric S1 proteins of IBV strains with different pathogenicity to sialic acids is comparable, our studies using trimeric S1 proteins indicate that there might not only be differences in binding characteristics of different spikes (Fig. 4), but also differences in the attachment profiles of the spike protein to tissues from different animals.…”

“…Binding of alpha2,3linked sialic acids to specific lectins corresponded with the susceptibility of these cells to IBV infection, and desialylation by neuraminidase hampered infection. Our lab (Wickramasinghe et al, 2011) and others (Mork et al, 2014;Shahwan et al, 2013) demonstrated that binding of recombinant S1 proteins to chicken tissues ex vivo (including trachea, lung, intestine and kidney) also depended on alpha2,3-linked sialic acids (Fig. 7A).…”

“…As read-out parameter for infection a scoring system for ciliostasis has been developed (Cook et al, 1999). Oviduct organ explants (Mork et al, 2014) have been developed to study IBV strains with tropism for reproductive tract. Finally, most IBV field strains grow on isolated primary chicken embryo kidney (CEK) (Gillette, 1973) cells ( Fig.…”

Identification and molecular characterization of a novel serotype infectious bronchitis virus (GI-28) in China

“…Similarly, the results of this study showed that obvious positive immunohistochemical reactions developed not only in the cytoplasm of the tubular epithelial cells and in the mucous membrane of the ureters and collecting ducts in the kidney, and in the epithelial cells of the tracheal mucosa of the secondary bronchi at 5 dpc, but the viral antigens were also detected in the cecal tonsils. This result suggests a broad tissue tropism of strain ck/CH/LGX/111119, similar as that of its deduced parental LX4 genotype viruses (Benyeda et al, 2009;de Wit et al, 2011;Mork et al, 2014).…”