Two apextrin-like proteins mediate extracellular and intracellular bacterial recognition in amphioxus

Huang, Guangrui; Huang, Shengfeng; Yan, Xinyu; Yang, Ping-Shih; Li, Jun; Xu, Weiya; Zhang, Lingling; Wang, Ruihua; Yu, Yaoguang; Yuan, Shaochun; Chen, Shangwu; Luo, Guangbin; Xu, Anlong

doi:10.1073/pnas.1405414111

Cited by 31 publications

(33 citation statements)

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“…Using a de novo method, we identified 941 candidate novel domains that are conserved in the two lancelets but absent in vertebrates; the 375 most confident candidates were distributed in 1,884 proteins ( Supplementary Figs 30 and 31 ; Supplementary Note 11 ). We functionally verified one of the candidates, the ApeC domain (deposited in the Pfam database under accession PF16977), as a novel pattern recognition domain for bacterial peptidoglycan 31 . We also used a BLAST-clustering method to directly measure the sequence diversity of all protein domains (vertebrate-specific domains included) in humans, mice, zebrafish, tunicates and lancelets ( Supplementary Note 11 ).…”

Section: Resultsmentioning

confidence: 99%

Decelerated genome evolution in modern vertebrates revealed by analysis of multiple lancelet genomes

et al. 2014

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Vertebrates diverged from other chordates ~500 Myr ago and experienced successful innovations and adaptations, but the genomic basis underlying vertebrate origins are not fully understood. Here we suggest, through comparison with multiple lancelet (amphioxus) genomes, that ancient vertebrates experienced high rates of protein evolution, genome rearrangement and domain shuffling and that these rates greatly slowed down after the divergence of jawed and jawless vertebrates. Compared with lancelets, modern vertebrates retain, at least relatively, less protein diversity, fewer nucleotide polymorphisms, domain combinations and conserved non-coding elements (CNE). Modern vertebrates also lost substantial transposable element (TE) diversity, whereas lancelets preserve high TE diversity that includes even the long-sought RAG transposon. Lancelets also exhibit rapid gene turnover, pervasive transcription, fastest exon shuffling in metazoans and substantial TE methylation not observed in other invertebrates. These new lancelet genome sequences provide new insights into the chordate ancestral state and the vertebrate evolution.

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Section: Resultsmentioning

confidence: 99%

Decelerated genome evolution in modern vertebrates revealed by analysis of multiple lancelet genomes

et al. 2014

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“…The association of ApeC with MACPF, detected in 5 predicted mussel proteins, strongly indicates the combination of pathogen recognition and killing properties in the same protein sequence, as ApeC has been recently functionally linked to pathogen recognition in amphioxus [78] (see Section 3.1.1.8).…”

Section: Evidence Of An Ancient Bivalve Complement-like Systemmentioning

confidence: 92%

“…The apextrin C-terminal domain (ApeC) takes its name from a sea urchin protein involved in larval 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 development. This domain has been recently recognized as a novel PRR in amphioxus, since two ApeC domain containing proteins were demonstrated to act as intra-and extra-cellular sensors of PGN and its component muramyl dipeptide (MDP) [78]. Apextrinlike proteins have been involved in pathogen recognition and inactivation also in echinoderms [79] and the over-expression of two apextrin-related transcripts in response to bacterial challenges has been reported in M. galloprovincialis [80].…”

Section: Extracellular Prrsmentioning

confidence: 99%

An updated molecular basis for mussel immunity

Gerdol

Venier

2015

Fish & Shellfish Immunology

134

163

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Non-self recognition with the consequent tolerance or immune reaction is a crucial process to succeed as living organisms. At the same time the interactions between host species and their microbiome, including potential pathogens and parasites, significantly contribute to animal life diversity. Marine filter-feeding bivalves, mussels in particular, can survive also in heavily anthropized coastal waters despite being constantly surrounded by microorganisms. Based on the first outline of the Mytilus galloprovincialis immunome dated 2011, the continuously growing transcript data and the recent release of a draft mussel genome, we explored the available sequence data and scientific literature to reinforce our knowledge on the main gene-encoded elements of the mussel immune responses, from the pathogen recognition to its clearance. We carefully investigated molecules specialized in the sensing and targeting of potential aggressors, expected to show greater molecular diversification, and outlined, whenever relevant, the interconnected cascades of the intracellular signal transduction. Aiming to explore the diversity of extracellular, membrane-bound and intracellular pattern recognition receptors in mussel, we updated a highly complex immune system, comprising molecules which are described here in detail for the first time (e.g. NOD-like receptors) or which had only been partially characterized in bivalves (e.g. RIG-like receptors). Overall, our comparative sequence analysis supported the identification of over 70 novel full-length immunity-related transcripts in M. galloprovincialis. Nevertheless, the multiplicity of gene functions relevant to immunity, the involvement of part of them in other vital processes, and also the lack of a refined mussel genome make this work still not-exhaustive and support the development of more specific studies.

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“…We thus decided to 413 interrogate specifically the populations of small RNAs mapping on Branchiostoma 414 pathogen genomes. Several pathogenic bacteria (Staphylococcus aureus, Vibrio 415 alginolyticus and Vibrio anguillarum; [92,93]) have been described in various 416 Branchiostoma species. We asked whether RNAi could target those pathogens in vivo.…”

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confidence: 99%

Functional lability of RNA-dependent RNA polymerases in animals

Pinzón

Bertrand²,

Subirana³

et al. 2018

Preprint

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RNA interference (RNAi) requires RNA-dependent RNA polymerases (RdRPs) in many eukaryotes, and RNAi amplification constitutes the only known function for eukaryotic RdRPs. Yet in animals, classical model organisms can elicit RNAi without possessing RdRPs, and only nematode RNAi was shown to require RdRPs. Here we show that RdRP genes are much more common in animals than previously thought, even in insects, where they had been assumed not to exist. RdRP genes were present in the ancestors of numerous clades, and they were subsequently lost at a high frequency. In order to probe the function of RdRPs in a deuterostome (the cephalochordate Branchiostoma lanceolatum), we performed high-throughput analyses of small RNAs from various Branchiostoma developmental stages. Our results show that Branchiostoma RdRPs do not appear to participate in RNAi: we did not detect any candidate small RNA population exhibiting classical siRNA length or sequence features. Our results show that RdRPs have been independently lost in dozens of animal clades, and even in a clade where they have been conserved (cephalochordates) their function in RNAi amplification is not preserved. Such a dramatic functional variability reveals an unexpected plasticity in RNA silencing pathways. Author summaryRNA interference (RNAi) is a conserved gene regulation system in eukaryotes. In non-animal eukaryotes, it necessitates RNA-dependent RNA polymerases ("RdRPs"). Among animals, only nematodes appear to require RdRPs for RNAi. Yet additional animal clades have RdRPs and it is assumed that they participate in RNAi. Here, we find that RdRPs are much more common in animals than previously thought, but their genes were independently lost in many lineages. Focusing on a species with RdRP genes (a cephalochordate), we found that it does not use them for RNAi. While RNAi is the only known function for eukaryotic RdRPs, our results suggest additional roles. Eukaryotic RdRPs thus have a complex evolutionary history in animals, with frequent independent losses and apparent functional diversification. November 28, 2018 1/23 Phylogenetic tree reconstruction 100 Amino acid sequences of the eukaryotic RdRP domain (Pfam #PF05183) were retrieved 101 from PFAM [35], and supplemented with the RdRP domains of the proteins identified 102 in the 538 animal proteomes (cf above). Sequences were aligned using hmmalign [36] 103 using the HMM profile of the PF05183 RdRP domain. Sequences for which the domain 104 was incomplete were deteled from the alignment. Sites used to reconstruct the 105 phylogenetic tree were selected using trimAl [37] on the Phylemon 2.0 webserver [38]. 106 Bayesian inference (BI) tree was inferred using MrBayes 3.2.6 [39], with the model 107 recommended by ProtTest 1.4 [40] under the Akaike information criterion (LG+Γ), at 108 the CIPRES Science Gateway portal [41]. Two independent runs were performed, each 109 with 4 chains and one million generations. A burn-in of 25% was used and a fifty 110 majority-rule consensus tree was calculated for the remaining ...

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Two apextrin-like proteins mediate extracellular and intracellular bacterial recognition in amphioxus

Cited by 31 publications

References 44 publications

Decelerated genome evolution in modern vertebrates revealed by analysis of multiple lancelet genomes

Decelerated genome evolution in modern vertebrates revealed by analysis of multiple lancelet genomes

An updated molecular basis for mussel immunity

Functional lability of RNA-dependent RNA polymerases in animals

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