Amphibian Immune Defenses against Chytridiomycosis: Impacts of Changing Environments

Rollins‐Smith, Louise A.; Ramsey, Jeremy P.; Pask, James D.; Reinert, Laura K.; Woodhams, Douglas C.

doi:10.1093/icb/icr095

Cited by 202 publications

(184 citation statements)

References 88 publications

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“…Microbial invasion and infection due to disruptions of the surface cell layer occur frequently (25). To our knowledge, βγ-CAT is the first example of a naturally existing complex of bacterial PFT-like protein and TFF in vertebrates (10,11).…”

Section: Discussionmentioning

confidence: 99%

Host-derived, pore-forming toxin–like protein and trefoil factor complex protects the host against microbial infection

Xiang

Yan

Guo

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

112

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Aerolysins are virulence factors belonging to the bacterial β-poreforming toxin superfamily. Surprisingly, numerous aerolysin-like proteins exist in vertebrates, but their biological functions are unknown. βγ-CAT, a complex of an aerolysin-like protein subunit (two βγ-crystallin domains followed by an aerolysin pore-forming domain) and two trefoil factor subunits, has been identified in frogs (Bombina maxima) skin secretions. Here, we report the rich expression of this protein, in the frog blood and immune-related tissues, and the induction of its presence in peritoneal lavage by bacterial challenge. This phenomena raises the possibility of its involvement in antimicrobial infection. When βγ-CAT was administrated in a peritoneal infection model, it greatly accelerated bacterial clearance and increased the survival rate of both frogs and mice. Meanwhile, accelerated Interleukin-1β release and enhanced local leukocyte recruitments were determined, which may partially explain the robust and effective antimicrobial responses observed. The release of interleukin-1β was potently triggered by βγ-CAT from the frog peritoneal cells and murine macrophages in vitro. βγ-CAT was rapidly endocytosed and translocated to lysosomes, where it formed high molecular mass SDS-stable oligomers (>170 kDa). Lysosomal destabilization and cathepsin B release were detected, which may explain the activation of caspase-1 inflammasome and subsequent interleukin-1β maturation and release. To our knowledge, these results provide the first functional evidence of the ability of a host-derived aerolysin-like protein to counter microbial infection by eliciting rapid and effective host innate immune responses. The findings will also largely help to elucidate the possible involvement and action mechanisms of aerolysin-like proteins and/or trefoil factors widely existing in vertebrates in the host defense against pathogens.innate immunity | infectious disease | interleukin-1beta

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Section: Discussionmentioning

confidence: 99%

Host-derived, pore-forming toxin–like protein and trefoil factor complex protects the host against microbial infection

Xiang

Yan

Guo

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

112

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“…Innate immune responses, such as secretion of antimicrobial peptides, are one of several factors known to influence amphibian susceptibility (Rollins-Smith et al 2011); other factors include symbiotic skin bacteria that inhibit Bd (Harris et al 2006), microhabitat preferences (Brem andLips 2008), and thermoregulatory behavior (Richards-Zawacki 2010). The adaptive immune response of X. laevis appears to be inhibited by Bd (RollinsSmith et al 2011).…”

Section: Introductionmentioning

confidence: 99%

SUSCEPTIBILITY TO THE AMPHIBIAN CHYTRID FUNGUS VARIES WITH ONTOGENY IN THE DIRECT-DEVELOPING FROG,ELEUTHERODACTYLUS COQUI

Langhammer

Burrowes

Lips

et al. 2014

Journal of Wildlife Diseases

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ABSTRACT:Age-related differences in susceptibility to infectious disease are known from a wide variety of plant and animal taxonomic groups. For example, the immature immune systems of young vertebrates, along with limited prior exposure to pathogens and behavioral factors, can place juveniles at greater risk of acquiring and succumbing to a pathogen. We studied the ontogenetic susceptibility of terrestrial direct-developing frogs (Eleutherodactylus coqui) to the fungal pathogen, Batrachochytrium dendrobatidis (Bd), which is responsible for the decline of amphibian species worldwide. By exposing juvenile and adult frogs to the same dose and strain of Bd, we uncovered ontogenetic differences in susceptibility. Froglets exposed to the pathogen had significantly lower survival rates compared with control froglets, while adult frogs largely cleared infection and had survival rates indistinguishable from control frogs, even when exposed to a much higher dose of Bd. The high disease-induced mortality rate of juveniles may explain ongoing population declines in eastern Puerto Rico, where Bd is endemic and juveniles experience higher prevalence and infection intensity compared to adults. Our results have important implications for understanding and modeling the decline, possibly to extinction, of amphibian populations and species.

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“…The common laboratory species Xenopus laevis, which appears to be tolerant of Bd infection, does produce Bd-binding antibodies in response to repeated Bd exposure (Ramsey et al 2010), but the susceptible species Rana muscosa, R. sierrae, and Silurana tropicalis, do not demonstrate a robust immune response with Bd infection Rosenblum et al 2012). It has been demonstrated that Bd may produce factors that reduce or evade the normal cellmediated immune response Rollins-Smith et al 2011), and recently Bd zoospores and supernatant were found to inhibit splenic lymphocyte functioning and proliferation, and increase apoptosis in vitro (Fites et al 2013). However, certain amphibian species can acquire resistance in the form of reduced infection burden and mortality after repeated exposures to the pathogen (McMahon et al 2014).…”

Section: Facets Of the Amphibian Immune Systemmentioning

confidence: 99%

Interactions between amphibian skin sloughing and a cutaneous fungal disease: infection progression, immune defence, and phylogenetic patterns

Ohmer¹

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Worldwide, there has been an unprecedented rise in emerging infectious diseases of wildlife, and this has contributed to a widespread biodiversity crisis. Amphibian populations, in particular, are threatened by the fungal pathogen Batrachochytrium dendrobatidis (Bd), which in post-metamorphic animals only infects the skin, and causes the potentially lethal disease chytridiomycosis. Amphibians regularly slough their skin, and in doing so remove many skinassociated microbes. Thus, skin sloughing may play an important role in the pathogenesis of chytridiomycosis. To investigate this association, the influence of Bd infection on amphibian skin sloughing, and the role of sloughing in regulating infection, was examined. Furthermore, to better understand the variation in skin sloughing rates across species and ecological groups, and make inferences about the role of this process in susceptibility to this fungal disease, amphibian skin structure and function was investigated within a phylogenetic context. To determine the relationship between skin sloughing and disease progression (chapter 2), adult green tree frogs (Litoria caerulea) were exposed to an Australian Bd strain, and sloughing rates and infection load were monitored on a naturalistic cycling temperature regime (15 -23˚C).Sloughing rates were determined by filming frogs and infection intensity was monitored before and after sloughing with conventional swabbing and quantitative PCR. Sloughing rate was found to increase with Bd infection load in infected frogs, but sloughing itself did not affect Bd load on the ventral skin surface. Although a faster sloughing rate might be considered advantageous for Bdinfected animals, it does not appear to curb the progression of disease in susceptible species. In fact, sloughing may actually contribute to the loss of physiological homeostasis seen in terminally ill frogs by further inhibiting water and electrolyte transport across the skin.In some species less susceptible to chytridiomycosis, it has been demonstrated that Bd growth remains epibiotic, without penetrating the underlying epidermal layers. Therefore, sloughing may more effectively remove Bd zoospores in less susceptible species (chapter 3). To test this hypothesis, five Australian frog species, Lit. caerulea, Platyplectrum ornatum, Lechriodus fletcheri, Limnodynastes peronii, and Lim. tasmaniensis, were exposed to an Australian Bd strain, and their sloughing rates and infection loads monitored over time. Utilising an improved methodology to remove any artefacts from the swabbing itself, sloughing was found to reduce Bd load on the ventral skin surface, in all five species, despite wide ranging variation in susceptibility to Bd infection and subsequent disease. In less susceptible species, sloughing reduced Bd load up to 100%, leading to infection clearance. However, the drop in Bd load was only temporary in susceptible species, potentially due to the invasive growth of Bd in skin layers underlying the ii stratum corneum in these species. If less suscept...

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Amphibian Immune Defenses against Chytridiomycosis: Impacts of Changing Environments

Cited by 202 publications

References 88 publications

Host-derived, pore-forming toxin–like protein and trefoil factor complex protects the host against microbial infection

Host-derived, pore-forming toxin–like protein and trefoil factor complex protects the host against microbial infection

SUSCEPTIBILITY TO THE AMPHIBIAN CHYTRID FUNGUS VARIES WITH ONTOGENY IN THE DIRECT-DEVELOPING FROG,ELEUTHERODACTYLUS COQUI

Interactions between amphibian skin sloughing and a cutaneous fungal disease: infection progression, immune defence, and phylogenetic patterns

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