The c-Jun N-terminal kinase prevents oxidative stress induced by UV and thermal stresses in corals and human cells

Courtial, Lucile; Picco, Vincent; Grover, Renaud; Cormerais, Yann; Rottier, Cécile; Labbé, Antoine; Pagès, Gilles; Ferrier‐Pagés, Christine

doi:10.1038/srep45713

Cited by 28 publications

(27 citation statements)

References 78 publications

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“…Due to its multiple functions, it is therefore not surprising that this pathway is conserved in most tardigrades (eutardigrades) and other ecdysozoans (Figure 5b). In fact, some functionality of the JNK pathway has been shown to be conserved from Cnidaria to Chordata, since it was shown to prevent oxidative stress caused by UV and thermal stresses in cells of both corals and humans (Courtial et al 2017). It is therefore possible that this pathway is involved in tardigrade UV and thermal stress responsesstresses to which tardigrades are well known to be extremely resilient against (Jönsson et al 2008).…”

Section: Tardigrades Have a Conserved D Melanogaster Jnk Pathwaymentioning

confidence: 99%

The Unique Antimicrobial Recognition and Signaling Pathways in Tardigrades with a Comparison Across Ecdysozoa

Mapalo

Arakawa

Baker

et al. 2020

G3 Genes|Genomes|Genetics

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Tardigrades are microscopic animals known to withstand unfavorable abiotic conditions. These animals are also constantly exposed to biotic stresses, including parasites and internal microbiomes. However, the tardigrade immune mechanisms against these biotic stresses are largely uncharacterized. Due to the contentious phylogenetic position of tardigrades, it is not intuitive whether they possess an immune system more similar to that of arthropods (e.g., Toll, Imd, and JNK pathways of the Drosophila melanogaster antimicrobial response) or to that of nematodes (e.g., the Tir-1/Nsy-1/Sek-1/Pmk-1/Atf-7 signaling cassette [called Tir-1 pathway here]) in Caenorhabditis elegans). In this study, comparative genomic analyses were conducted to mine homologs of canonical D. melanogaster and C. elegans immune pathway genes from eight tardigrades (Echiniscoides cf. sigismundi, Echiniscus testudo, Hypsibius exemplaris, Mesobiotus philippinicus, Milnesium tardigradum, Paramacrobiotus richtersi, Richtersius cf. coronifer, and Ramazzottius varieornatus) and four non-arthropod ecdysozoans (two onychophorans: Epiperipatus sp. and Opisthopatus kwazululandi; one nematomorph: Paragordius varius; and one priapulan: Priapulus caudatus) in order to provide insights into the tardigrade antimicrobial system. No homologs of the intracellular components of the Toll pathway were detected in any of the tardigrades examined. Likewise, no homologs of most of the Imd pathway genes were detected in any of the tardigrades or any of the other non-arthropod ecdysozoans. Both the JNK and Tir-1 pathways, on the other hand, were found to be conserved across ecdysozoans. Interestingly, tardigrades had no detectable homologs of NF-κB, the major activator of antimicrobial response gene expression. Instead, tardigrades appear to possess NF-κB distantly related NFAT homologs. Overall, our results show that tardigrades have a unique gene pathway repertoire that differs from that of other ecdysozoans. Our study also provides a framework for future studies on tardigrade immune responses.

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Section: Tardigrades Have a Conserved D Melanogaster Jnk Pathwaymentioning

confidence: 99%

The Unique Antimicrobial Recognition and Signaling Pathways in Tardigrades with a Comparison Across Ecdysozoa

Mapalo

Arakawa

Baker

et al. 2020

G3 Genes|Genomes|Genetics

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“…The mitogen-activated protein kinase JNK plays a role in responses to stress stimuli, inflammation, and apoptosis 71 . JNK prevents the accumulation of reactive oxygen species (ROS) in corals in response to thermal and UV stress, and inhibition of JNK leads to coral bleaching and cell death 72 . The NF-κB transcription factor may also link oxidative stress and apoptosis involved in coral bleaching 73 , in addition to its central role in innate immunity 39 .…”

Section: Resultsmentioning

confidence: 99%

Comparative analysis of the Pocillopora damicornis genome highlights role of immune system in coral evolution

Cunning

Bay

Gillette

et al. 2018

Sci Rep

113

119

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Comparative analysis of the expanding genomic resources for scleractinian corals may provide insights into the evolution of these organisms, with implications for their continued persistence under global climate change. Here, we sequenced and annotated the genome of Pocillopora damicornis, one of the most abundant and widespread corals in the world. We compared this genome, based on protein-coding gene orthology, with other publicly available coral genomes (Cnidaria, Anthozoa, Scleractinia), as well as genomes from other anthozoan groups (Actiniaria, Corallimorpharia), and two basal metazoan outgroup phlya (Porifera, Ctenophora). We found that 46.6% of P. damicornis genes had orthologs in all other scleractinians, defining a coral ‘core’ genome enriched in basic housekeeping functions. Of these core genes, 3.7% were unique to scleractinians and were enriched in immune functionality, suggesting an important role of the immune system in coral evolution. Genes occurring only in P. damicornis were enriched in cellular signaling and stress response pathways, and we found similar immune-related gene family expansions in each coral species, indicating that immune system diversification may be a prominent feature of scleractinian coral evolution at multiple taxonomic levels. Diversification of the immune gene repertoire may underlie scleractinian adaptations to symbiosis, pathogen interactions, and environmental stress.

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“…Furthermore, such studies are inherently compromised by a lack of proven gene homologues among the datasets analyzed, as has been suggested by others (Djordevic et al, 2016). Therefore, we propose that studies, such as ours and a recent study of the c-Jun N-terminal kinase JNK (Courtial et al, 2017), that are investigating induced or inherent differences in transcription factor activity will ultimately be required to identify cell networks and pathways that contribute to biological processes related to symbiosis and thermal sensitivity. Values are averages of three biological replicates from each of two experimental trials (thus n=6, except for colony 1, which had one NF-κB band below the detection limit) and are expressed relative to that for colony 2 (set at 1.0).…”

Section: Discussionmentioning

confidence: 99%

Varied effects of algal symbionts on transcription factor NF-κB in a sea anemone and a coral: possible roles in symbiosis and thermotolerance

Mansfield¹,

Cleves

Vlack³

et al. 2019

Preprint

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Many cnidarians, including the reef-building corals, undergo symbiotic mutualisms with photosynthetic dinoflagellate algae of the family Symbiodiniaceae. These partnerships are sensitive to temperature extremes, which cause symbiont loss and increased coral mortality.Previous studies have implicated host immunity and specifically immunity transcription factor NF-κB as having a role in the maintenance of the cnidarian-algal symbiosis. Here we have further investigated a possible role for NF-κB in establishment and loss of symbiosis in various strains of the anemone Exaiptasia (Aiptasia) and in the coral Pocillopora damicornis. Our results show that NF-κB expression is reduced in Aiptasia larvae and adults that host certain algae strains. Treatment of Aiptasia larvae with a known symbiosis-promoting cytokine, transforming growth factor β , also led to decreased NF-κB expression. We also show that aposymbiotic Aiptasia (with high NF-κB expression) have increased survival following infection with the pathogenic bacterium Serratia marcescens as compared to symbiotic Aiptasia (low NF-κB expression). Furthermore, a P. damicornis coral colony hosting Durusdinium spp. (formerly clade D) symbionts had higher basal NF-κB expression and decreased heat-induced bleaching as compared to two individuals hosting Cladocopium spp. (formerly clade C) symbionts. Lastly, genome-wide gene expression profiling and genomic promoter analysis identified putative NFκ B target genes that may be involved in thermal bleaching, symbiont maintenance, and/or immune protection in P. damicornis. Our results provide further support for the hypothesis that modulation of NF-κB and immunity plays a role in some, but perhaps not all, cnidarian-Symbiodiniaceae partnerships as well as in resistance to pathogens and bleaching. 2017; Mansfield et al., 2017; Williams et al., 2018). We and others have shown that the expression and activity of NF-κB are modulated during the onset of symbiosis and after loss of symbiosis in both Aiptasia (Wolfowicz et al., 2016; Mansfield et al., 2017) and the coral Acropora palmata (DeSalvo et al., 2010). For example, Mansfield et al. (2017) demonstrated that the establishment of algal symbiosis in naïve Aiptasia larvae is associated with a reduction in NF-κB expression and that heat-induced loss of symbiosis in adult Aiptasia is associated with increased NF-κB expression and DNA-binding activity. Furthermore, genomic analyses have shown that symbiotic cnidarians, such as the coral Pocillopora damicornis (Cunning et al., 2018), have extensive repertoires of immune signaling genes. Based on these data, we hypothesized that algal symbionts can modulate host NF-κB expression to effect a decrease in host immunity to allow for the establishment of symbiosis (Mansfield et al., 2017; Mansfield and Gilmore, 2019).Herein, we have used Aiptasia and P. damicornis to further investigate Symbiodiniaceaeinduced downregulation of NF-κB, as well as the implications of decreased NF-κB levels and symbiont type for cnidarian immunity and suscept...

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The c-Jun N-terminal kinase prevents oxidative stress induced by UV and thermal stresses in corals and human cells

Cited by 28 publications

References 78 publications

The Unique Antimicrobial Recognition and Signaling Pathways in Tardigrades with a Comparison Across Ecdysozoa

The Unique Antimicrobial Recognition and Signaling Pathways in Tardigrades with a Comparison Across Ecdysozoa

Comparative analysis of the Pocillopora damicornis genome highlights role of immune system in coral evolution

Varied effects of algal symbionts on transcription factor NF-κB in a sea anemone and a coral: possible roles in symbiosis and thermotolerance

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