Abstract
While amphibians around the globe are facing catastrophic declines, in part because of infections with pathogens such as the Frog Virus 3 (FV3) ranavirus; the mechanisms governing amphibian susceptibility and resistance to such pathogens remain poorly understood. The type I and type III interferon (IFN) cytokines represent a cornerstone of vertebrate antiviral immunity, while our recent work indicates that tadpoles and adult frogs of the amphibian Xenopus laevis may differ in their IFN responses to FV3. In this respect, it is notable that anuran (frogs and toads) tadpoles are significantly more susceptible to FV3 than adult frogs, and thus, gaining greater insight into the differences in the tadpole and adult frog antiviral immunity would be invaluable. Accordingly, we examined the FV3-elicited expression of a panel of type I and type III IFN genes in the skin (site of FV3 infection) and kidney (principal FV3 target) tissues and isolated cells of X. laevis tadpoles and adult frogs. We also examined the consequence of tadpole and adult frog skin and kidney cell stimulation with hallmark pathogen-associated molecular patterns (PAMPs) on the IFN responses of these cells. Together, our findings indicate that tadpoles and adult frogs mount drastically distinct IFN responses to FV3 as well as to viral and non-viral PAMPs, while these expression differences do not appear to be the result of a distinct pattern recognition receptor expression by tadpoles and adults.
Highlights
Escalating infections of amphibians by ranaviruses such as Frog Virus 3 (FV3; ranavirus genus and family Iridoviridae) are significantly contributing to the worldwide amphibian declines [1,2,3].It is notable that the tadpoles of anurans are generally much more susceptible to ranaviruses than the adult frogs of the respective species [4,5,6,7,8]
III IFN responses at their skin following water exposure to FV3 [19]
Considering the differences in the tadpole and adult frog skin, but not their kidney cell expression of the pattern recognition receptors (PRRs) (Figure 1A,B), we examined the expression of representative X. laevis type I and III IFN genes from distinct phylogenetic clades (Figure S1) in the isolated tadpole and adult frog skin and kidney cells that were stimulated with viral and non-viral pathogen-associated molecular patterns (PAMPs; Figures 2 and 3)
Summary
Escalating infections of amphibians by ranaviruses such as Frog Virus 3 (FV3; ranavirus genus and family Iridoviridae) are significantly contributing to the worldwide amphibian declines [1,2,3]. IFN cytokine families in tadpoles and adult anurans will undoubtedly lend to greater insight into tadpole susceptibility and adult frog resistance to amphibian pathogens like FV3. In this respect, it is notable that our recent work indicates that while tadpoles of the anuran X. laevis respond to FV3 infections by upregulating a type III IFN X. laevis, adults instead respond by upregulating a type I. We expand on our previous work by examining the roles of a panel of intronless and intron containing type I and type III IFNs in the X. laevis tadpole and adult frog responses to FV3 challenge, as well as to a range of pathogen pattern recognition receptor agonists such as lipoprotein, lipopolysaccharide, polyinosinic:polycytidylic acid, CpG DNA, imiquimod, single stranded RNA and several viral DNAs
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