Genome-wide investigation and expression analysis of MACPF gene family reveals its immune role in response to bacterial challenge of Manila clam

Jiang, Kunyin; Yin, Zhihui; Zhang, Yanming; Xu, Qiaoyue; Yu, Yongchao; Cong, Wanlin; Yan, Xiwu; Nie, Hongtao

doi:10.1016/j.ygeno.2021.02.013

Cited by 8 publications

(16 citation statements)

References 51 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…(8)(9)(10)(11)(12)(13)(33)(34)(35)(36). Current data suggest that some ACPs may have an important role in embryogenesis, development and immune responses (5,(7)(8)(9)(10)(11)(12)(13)(33)(34)(35)(36)(37)(38)(39)(40)(41), but in most cases, the underlying mechanisms have not been investigated. In fact, most ACPs have not been functionally investigated.…”

Section: Discussion and Conclusion Apec Is A Novel Protein Domain Widely Distributed In Invertebratesmentioning

confidence: 99%

Two Amphioxus ApeC-Containing Proteins Bind to Microbes and Inhibit the TRAF6 Pathway

Fan

et al. 2021

Front. Immunol.

View full text Add to dashboard Cite

The apextrin C-terminal (ApeC) domain is a class of newly discovered protein domains with an origin dating back to prokaryotes. ApeC-containing proteins (ACPs) have been found in various marine and aquatic invertebrates, but their functions and the underlying mechanisms are largely unknown. Early studies suggested that amphioxus ACP1 and ACP2 bind to bacterial cell walls and have a role in immunity. Here we identified another two amphioxus ACPs (ACP3 and ACP5), which belong to the same phylogenetic clade with ACP1/2, but show distinct expression patterns and sequence divergence (40-50% sequence identities). Both ACP3 and ACP5 were mainly expressed in the intestine and hepatic cecum, and could be up-regulated after bacterial challenge. Both prokaryotic-expressed recombinant ACP3 and ACP5 could bind with several species of bacteria and yeasts, showing agglutinating activity but no microbicidal activity. ELISA assays suggested that their ApeC domains could interact with peptidoglycan (PGN), but not with lipoteichoic acid (LTA), lipopolysaccharides (LPS) and zymosan A. Furthermore, they can only bind to Lys-type PGN from Staphylococcus aureus, but not to DAP-type PGN from Bacillus subtilis and not to moieties of PGN such as MDPs, NAMs and NAGs. This recognition spectrum is different from that of ACP1/2. We also found that when expressed in mammalian cells, ACP3 could interact with TRAF6 via a conserved non-ApeC region, which inhibited the ubiquitination of TRAF6 and hence suppressed downstream NF-κB activation. This work helped define a novel subfamily of ACPs, which have conserved structures, and have related yet diversified molecular functions. Its members have dual roles, with ApeC as a lectin and a conserved unknown region as a signal transduction regulator. These findings expand our understanding of the ACP functions and may guide future research on the role of ACPs in different animal clades.

show abstract

Section: Discussion and Conclusion Apec Is A Novel Protein Domain Widely Distributed In Invertebratesmentioning

confidence: 99%

Two Amphioxus ApeC-Containing Proteins Bind to Microbes and Inhibit the TRAF6 Pathway

Fan

et al. 2021

Front. Immunol.

View full text Add to dashboard Cite

show abstract

“…We conducted a One-Way analysis of variance (ANOVA) with the Tukey test to compare the significant differences Survival status groups. Differences were considered significant at P < 0.05 ( 31 ).…”

Section: Methodsmentioning

confidence: 99%

Molecular Mechanisms Underlying Vibrio Tolerance in Ruditapes philippinarum Revealed by Comparative Transcriptome Profiling

et al. 2022

Self Cite

View full text Add to dashboard Cite

The clam Ruditapes philippinarum is an important species in the marine aquaculture industry in China. However, in recent years, the aquaculture of R. philippinarum has been negatively impacted by various bacterial pathogens. In this study, the transcriptome libraries of R. philippinarum showing different levels of resistance to challenge with Vibrio anguillarum were constructed and RNA-seq was performed using the Illumina sequencing platform. Host immune factors were identified that responded to V. anguillarum infection, including C-type lectin domain, glutathione S-transferase 9, lysozyme, methyltransferase FkbM domain, heat shock 70 kDa protein, Ras-like GTP-binding protein RHO, C1q, F-box and BTB/POZ domain protein zf-C2H2. Ten genes were selected and verified by RT-qPCR, and nine of the gene expression results were consistent with those of RNA-seq. The lectin gene in the phagosome pathway was expressed at a significantly higher level after V. anguillarum infection, which might indicate the role of lectin in the immune response to V. anguillarum. Comparing the results from R. philippinarum resistant and nonresistant to V. anguillarum increases our understanding of the resistant genes and key pathways related to Vibrio challenge in this species. The results obtained here provide a reference for future immunological research focusing on the response of R. philippinarum to V. anguillarum infection.

show abstract

“…The role of short-form ACPs in the mucosal surface of the gill Mollusk ACPs have been suggested to play important roles in immunity, development and stress resistance (10)(11)(12)(15)(16)(17)(18). ACPs were even discovered in the pedal mucus of the limpets, suggesting a role in the glue-like adhesion (19).…”

Section: Molecular Functions Of the Mollusk Apec Domainsmentioning

confidence: 99%

“…In the oyster Crossostrea gigas, an ACP was found to be highly up-regulated under hypoxic conditions, suggesting a role in the anti-stress responses (12). In terms of immune roles, several ACP genes from sea urchins, oysters, mussels, clams, and brachiopods exhibited high expression in the immune cells and tissues and could be upregulated in response to bacterial challenge (11,(13)(14)(15)(16)(17)(18). Moreover, a recent study found that ACPs existed in the pedal mucus secreted by limpets, probably being involved in immunity and glue-like adhesion (19).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Two novel mollusk short-form ApeC-containing proteins act as pattern recognition proteins for peptidoglycan

Liu²,

Zhang³

et al. 2022

Front. Immunol.

View full text Add to dashboard Cite

The Apextrin C-terminal (ApeC) domain is a new protein domain largely specific to aquatic invertebrates. In amphioxus, a short-form ApeC-containing protein (ACP) family is capable of binding peptidoglycan (PGN) and agglutinating bacteria via its ApeC domain. However, the functions of ApeC in other phyla remain unknown. Here we examined 130 ACPs from gastropods and bivalves, the first and second biggest mollusk classes. They were classified into nine groups based on their phylogenetics and architectures, including three groups of short-form ACPs, one group of apextrins and two groups of ACPs of complex architectures. No groups have orthologs in other phyla and only four groups have members in both gastropods and bivalves, suggesting that mollusk ACPs are highly diversified. We selected one bivalve ACP (CgACP1; from the oyster Crossostrea gigas) and one gastropod ACP (BgACP1; from the snail Biomphalaria glabrata) for functional experiments. Both are highly-expressed, secreted short-form ACPs and hence comparable to the amphioxus ACPs previously reported. We found that recombinant CgACP1 and BgACP1 bound with yeasts and several bacteria with different affinities. They also agglutinated these microbes, but showed no inhibiting or killing effects. Further analyses show that both ACPs had high affinities to the Lys-type PGN from S. aureus but weak or no affinities to the DAP-type PGN from Bacillus subtilis. Both recombinant ACPs displayed weak or no affinities to other microbial cell wall components, including lipopolysaccharide (LPS), lipoteichoic acid (LTA), zymosan A, chitin, chitosan and cellulose, as well as to several PGN moieties, including muramyl dipeptide (MDP), N-acetylglucosamine (GlcNAc) and N-acetylmuramic acid (MurNAc). Besides, CgACP1 had the highest expression in the gill and could be greatly up-regulated quickly after bacterial challenge. This is reminiscent of the amphioxus ACP1/2 which serve as essential mucus lectins in the gill. Taken together, the current findings from mollusk and amphioxus ACPs suggest several basic common traits for the ApeC domains, including the high affinity to Lys-type PGN, the bacterial binding and agglutinating capacity, and the role as mucus proteins to protect the mucosal surface.

show abstract

Genome-wide investigation and expression analysis of MACPF gene family reveals its immune role in response to bacterial challenge of Manila clam

Cited by 8 publications

References 51 publications

Two Amphioxus ApeC-Containing Proteins Bind to Microbes and Inhibit the TRAF6 Pathway

Two Amphioxus ApeC-Containing Proteins Bind to Microbes and Inhibit the TRAF6 Pathway

Molecular Mechanisms Underlying Vibrio Tolerance in Ruditapes philippinarum Revealed by Comparative Transcriptome Profiling

Two novel mollusk short-form ApeC-containing proteins act as pattern recognition proteins for peptidoglycan

Contact Info

Product

Resources

About