An amphioxus TLR with dynamic embryonic expression pattern responses to pathogens and activates NF-κB pathway via MyD88

Yuan, Shaochun; Huang, Shengfeng; Zhang, Wei; Wu, Tao Cheng; Dong, Meiling; Yu, Ye; Liu, Tong; Wu, Kui; Liu, Huiling; Yang, Manyi; Zhang, Hongwei; Xu, Anlong

doi:10.1016/j.molimm.2009.03.022

Cited by 68 publications

(57 citation statements)

References 25 publications

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“…bbtMyD88, identified in our previous study, is a conserved molecule that induces NF-κB activation, suggesting the existence of a MyD88-dependent pathway in amphioxus [13]. As mammalian TICAMs mediate a MyD88-independent pathway, it is important to assess whether activation of bbtTICAM is independent of MyD88.…”

Section: Analysis Of Bbtticam Expression Patternmentioning

confidence: 97%

“…The identification of both TLR and MyD88 in different evolutionary stages and the functional interaction of amphioxus TLR with MyD88 [13] suggest that the MyD88-dependent pathway is conserved and crucial for invertebrate TLR signaling in detecting invading pathogens. The characterization of bbtTICAM indicated that it is unrelated to amphioxus MyD88, although it showed a functional effect on NF-κB activation.…”

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

confidence: 99%

“…The direct interaction of MyD88 with TLRs in Drosophila and amphioxus suggests that this pathway is functionally conserved during evolution [13]. Unlike MyD88, no homolog of TICAM1 or TICAM2 has been identified in non-chordates such as Drosophila, Cnidaria [8], or sea urchin [10,11].…”

Section: Introductionmentioning

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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Section: Analysis Of Bbtticam Expression Patternmentioning

confidence: 97%

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

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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“…To study the transcriptional activity, the fulllength bbtIRFs were inserted into pCMV-BD (Promega). Vectors of bbtMyD88, bbtTRAF6, bbtRel, and bbtp105 have been described in our previous studies (31)(32)(33).…”

Section: Plasmid Constructionsmentioning

confidence: 99%

“…The same color box indicated amphioxus IRF genes with close sequence similarity. and immunofluorescence imaging were conducted according to the protocol described previously (31)(32)(33).…”

Section: Culture Of Amphioxus Intestinal Cells and Poly(i:c) Transfecmentioning

confidence: 99%

Characterization of Amphioxus IFN Regulatory Factor Family Reveals an Archaic Signaling Framework for Innate Immune Response

Yuan

Zheng

et al. 2015

The Journal of Immunology

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The IFN regulatory factor (IRF) family encodes transcription factors that play important roles in immune defense, stress response, reproduction, development, and carcinogenesis. Although the origin of the IRF family has been dated back to multicellular organisms, invertebrate IRFs differ from vertebrate IRFs in genomic structure and gene synteny, and little is known about their functions. Through comparison of multiple amphioxus genomes, in this study we suggested that amphioxus contains nine IRF members, whose orthologs are supposed to be shared among three amphioxus species. As the orthologs to the vertebrate IRF1 and IRF4 subgroups, Branchiostoma belcheri tsingtauense (bbt)IRF1 and bbtIRF8 bind the IFN-stimulated response element (ISRE) and were upregulated when amphioxus intestinal cells were stimulated with poly(I:C). As amphioxus-specific IRFs, both bbtIRF3 and bbtIRF7 bind ISRE. When activated, they can be phosphorylated by bbtTBK1 and then translocate into nucleus for target gene transcription. As transcriptional repressors, bbtIRF2 and bbtIRF4 can inhibit the transcriptional activities of bbtIRF1, 3, 7, and 8 by competing for the binding of ISRE. Interestingly, amphioxus IRF2, IRF8, and Rel were identified as target genes of bbtIRF1, bbtIRF7, and bbtIRF3, respectively, suggesting a dynamic feedback regulation among amphioxus IRF and NF-κB. Collectively, to our knowledge we present for the first time an archaic IRF signaling framework in a basal chordate, shedding new insights into the origin and evolution of vertebrate IFN-based antiviral networks.

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Gradual specialization of phagocytic ameboid cells may have impaired regenerative capacities in metazoan lineages

Lima

Abrahão

Pentagna

et al. 2022

Developmental Dynamics

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Animal regeneration is a fascinating field of research that has captured the attention of many generations of scientists. Among the cellular mechanisms underlying tissue and organ regeneration, we highlight the role of phagocytic ameboid cells (PACs). Beyond their ability to engulf nutritional particles, microbes, and apoptotic cells, their involvement in regeneration has been widely documented. It has been extensively described that, at least in part, animal regenerative mechanisms rely on PACs that serve as a hub for a range of critical physiological functions, both in health and disease. Considering the phylogenetics of PAC evolution, and the loss and gain of nutritional, immunological, and regenerative potential across Metazoa, we aim to discuss when and how phagocytic activity was first co‐opted to regenerative tissue repair. We propose that the gradual specialization of PACs during metazoan derivation may have contributed to the loss of regenerative potential in animals, with critical impacts on potential translational strategies for regenerative medicine.

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An amphioxus TLR with dynamic embryonic expression pattern responses to pathogens and activates NF-κB pathway via MyD88

Cited by 68 publications

References 25 publications

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

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

Characterization of Amphioxus IFN Regulatory Factor Family Reveals an Archaic Signaling Framework for Innate Immune Response

Gradual specialization of phagocytic ameboid cells may have impaired regenerative capacities in metazoan lineages

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