Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity

Huang, Shengfeng; Yuan, Shaochun; Guo, Lei; Yu, Ye; Li, Jun; Wu, Tao Cheng; Tong, L.; Yang, Manyi; Wu, Kui; Liu, Huiling; Jin, Ge; Yu, Yaoguang; Huang, Huiqing; Dong, Meiling; Yu, Cuiling; Chen, Shangwu; Xu, Anlong

doi:10.1101/gr.069674.107

Cited by 351 publications

(301 citation statements)

References 57 publications

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“…NLR (CLR) proteins play an important role in immunity, cell death, and disease in vertebrates, and their close counterparts exert a similar action in plants (27); our results indicate that the negative regulatory functions shown in mammals by some members of this protein family are conserved across distant evolutionary lineages and associated with different proteins, which share the presence of a LRR domain. This is not surprising, as LRR domains are one of the most commonly occurring domains in proteins associated with innate immunity (35,36); moreover, the function of many LRR domains is to provide a structural framework for protein-protein interactions (37). The down-regulation of these inhibitory proteins upon immune challenge is required to trigger a defense response in mammals and likely plays a pivotal role in preventing an overzealous reaction that could be detrimental to the host (27).…”

Section: Resultsmentioning

confidence: 99%

Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees

Prisco

Cavaliere

Annoscia

et al. 2013

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

579

445

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Large-scale losses of honey bee colonies represent a poorly understood problem of global importance. Both biotic and abiotic factors are involved in this phenomenon that is often associated with high loads of parasites and pathogens. A stronger impact of pathogens in honey bees exposed to neonicotinoid insecticides has been reported, but the causal link between insecticide exposure and the possible immune alteration of honey bees remains elusive. Here, we demonstrate that the neonicotinoid insecticide clothianidin negatively modulates NF-κB immune signaling in insects and adversely affects honey bee antiviral defenses controlled by this transcription factor. We have identified in insects a negative modulator of NF-κB activation, which is a leucine-rich repeat protein. Exposure to clothianidin, by enhancing the transcription of the gene encoding this inhibitor, reduces immune defenses and promotes the replication of the deformed wing virus in honey bees bearing covert infections. This honey bee immunosuppression is similarly induced by a different neonicotinoid, imidacloprid, but not by the organophosphate chlorpyriphos, which does not affect NF-κB signaling. The occurrence at sublethal doses of this insecticide-induced viral proliferation suggests that the studied neonicotinoids might have a negative effect at the field level. Our experiments uncover a further level of regulation of the immune response in insects and set the stage for studies on neural modulation of immunity in animals. Furthermore, this study has implications for the conservation of bees, as it will contribute to the definition of more appropriate guidelines for testing chronic or sublethal effects of pesticides used in agriculture.Apis mellifera | DWV | NLR (CLR) | neuroimmunity | toxicology

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Section: Resultsmentioning

confidence: 99%

Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees

Prisco

Cavaliere

Annoscia

et al. 2013

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

579

445

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“…Analysis of immune-related genes in the amphioxus genome identified a TICAM2-like molecule [12]. However, the full-length sequence revealed that the protein architecture of bbtTICAM is more similar to vertebrate TICAM1, including its length, position of the TIR domain, the RHIM in the C terminus, and the potential TRAF2-binding motif in the N terminus.…”

Section: Discussion Bbtticam Is the Earliest Ortholog Of Vertebrate Tmentioning

confidence: 99%

“…MyD88, the first-identified TIR adaptor in mammals, is also present in poriferans [7], cnidarians [8], Drosophila [9], sea urchin [10,11], and amphioxus [12]. The direct interaction of MyD88 with TLRs in Drosophila and amphioxus suggests that this pathway is functionally conserved during evolution [13].…”

Section: Introductionmentioning

confidence: 96%

“…However, bbtTICAM specifically activates NF-κB, but does not induce the production of type I IFN. Moreover, genome annotation indicated that amphioxus lacks orthologs of IRF3, IRF7, or IFN [12]. Thus, it is inferred that the antiviral mechanism of bbtTICAM may not be fully established or may be completely different from vertebrates.…”

Section: Gradual Adaptation Of the Myd88-independent Pathway With Thementioning

confidence: 99%

“…Intestines from five individuals were collected at 2,4,8,12,24,36,48, and 72 h post-injection as a single sample. Intestines from five PBS-injected animals were collected concurrently as non-challenged controls.…”

Section: Acute Immune Challenges Of Adult Amphioxus and Real-time Pcrmentioning

confidence: 99%

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Characterization of bbtTICAM from amphioxus suggests the emergence of a MyD88-independent pathway in basal chordates

et al. 2011

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The MyD88-independent pathway, one of the two crucial TLR signaling routes, is thought to be a vertebrate innovation. However, a novel Toll/interleukin-1 receptor (TIR) adaptor, designated bbtTICAM, which was identified in the basal chordate amphioxus, links this pathway to invertebrates. The protein architecture of bbtTICAM is similar to that of vertebrate TICAM1 (TIR-containing adaptor molecule-1, also known as TRIF), while phylogenetic analysis based on the TIR domain indicated that bbtTICAM is the oldest ortholog of vertebrate TICAM1 and TICAM2 (TIR-containing adaptor molecule-2, also known as TRAM). Similar to human TICAM1, bbtTICAM activates NF-κB in a MyD88-independent manner by interacting with receptor interacting protein (RIP) via its RHIM motif. Such activation requires bbtTICAM to form homodimers in endosomes, and it may be negatively regulated by amphioxus SARM (sterile α and armadillo motif-containing protein) and TRAF2. However, bbtTICAM did not induce the production of type I interferon. Thus, our study not only presents the ancestral features of vertebrate TICAM1 and TI-CAM2, but also reveals the evolutionary origin of the MyD88-independent pathway from basal chordates, which will aid in understanding the development of the vertebrate TLR network.

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Analysis of the Amphioxus Genome

Satoh

2009

Encyclopedia of Life Sciences

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Amphioxus or cephalochordates are small fish‐like marine invertebrates. The sequenced genome of Branchiostoma floridae is approximately 520 Mb in size and estimated to contain approximately 21 900 protein‐coding loci. Comparison of the amphioxus genome with genomes of other animals made a great impact on the resolution of the long‐standing question of the origin of vertebrates. First, chordates are monophyletic group, in which cephalochordates represent the most basal extant chordate lineage, with urochordates sister to vertebrates. Second, there is highly conserved synteny between the cephalochordate and vertebrate genomes. This allows reconstruction of 17 ancestral chordate linkage groups that are conserved in the modern amphioxus and vertebrate genomes. Third, the two rounds of genome‐wide duplications occurred in the vertebrate lineage after their divergence from cephalochordates and urochordates. Fourth, whereas most duplicate genes have been lost, a disproportionate number of genes are retained and involved in developmental processes to produce novel features and complexity of vertebrate biology. Key concepts The phylum Chordata consists of the subphyla Cephalochordata (amphioxus), Urochordata (ascidians) and Vertebrata, and these three groups are characterized by possession of a notochord, a hollow dorsal neural tube, a perforated pharyngeal region and a post‐anal tail. Chordates are monophyletic group in which cephalochordates represent the most basal extant lineage, suggesting a free‐living ancestor of chordates. Seventeen ancestral chordate linkage groups that are conserved in the modern amphioxus and vertebrate genomes are revealed by highly conserved synteny between the two genomes. The two rounds of genome‐wide gene duplications occurred in the vertebrate lineage after their divergence from cephalochordates and urochordates. A disproportionate number of genes which were produced by the genome‐wide duplication are retained and involved in developmental processes to produce novel features and complexity of vertebrate biology.

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Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity

Cited by 351 publications

References 57 publications

Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees

Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees

Characterization of bbtTICAM from amphioxus suggests the emergence of a MyD88-independent pathway in basal chordates

Analysis of the Amphioxus Genome

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