An Ancient BCR-like Signaling Promotes ICP Production and Hemocyte Phagocytosis in Oyster

Overview

Journal iScience

Publisher Cell Press

Date 2020 Jan 27

PMID 31982779

Citations 6

Authors

Jiejie Sun

Lingling Wang

Chuanyan Yang

Linsheng Song

Affiliations

Soon will be listed here.

Abstract

BCR/TCR-based adaptive immune systems arise in the jawed vertebrates, and B cell receptors (BCRs) play an important role in the clonal selection of B cells and their differentiation into antibody-secreting plasma cells. The existence of BCR-like molecule and the activation mechanism of the downstream response are still not clear in invertebrates. In this study, an ancient BCR-like molecule (designated as CgIgR) with an immunoreceptor tyrosine-based activation motif (ITAM) in its cytoplasmic tail was identified from the Pacific oyster Crassostrea gigas to investigate its involvement in immune response. CgIgR could bind different bacteria through five extracellular Ig domains and formed dimers. The activated CgIgR recruited CgSyk to promote CgERK phosphorylation. The CgIgR-mediated signaling promoted the production of immunoglobulin domain-containing proteins (CgICP-2 and CgLRRIG-1) through inducing CgH3K4me2. The produced CgICPs eventually facilitated hemocytes to phagocytize and eliminate V. splendidus. This study proposed that there was an ancient BCR-like molecule and BCR-like signaling in molluscs.

Citing Articles

LRSAM1 mediated the degradation of intracellular Vibrio through the ubiquitination-autophagy-lysosome pathway in oyster.

Yang W, Sun J, Guo Q, Wang W, Leng J, Wang L Cell Commun Signal. 2025; 23(1):110.

PMID: 40001133 PMC: 11863841. DOI: 10.1186/s12964-025-02111-4.

NCAM1-SHIP2 axis upon recognizing microbes inhibits the expressions of inflammatory factors through P38-H3K4me and P38-NF-κB pathways in oyster.

Sun J, Shi X, Wang M, He M, Yang W, Song L Cell Commun Signal. 2025; 23(1):102.

PMID: 39979940 PMC: 11841013. DOI: 10.1186/s12964-025-02087-1.

KDM4 Regulates the Glycolysis of Hemocytes in the Immune Priming of .

Zhao X, Qiao X, Yu S, Jin Y, Niu J, Li J Int J Mol Sci. 2024; 25(23).

PMID: 39684884 PMC: 11642315. DOI: 10.3390/ijms252313174.

Syk regulates the haemocyte autophagy through inducing the mRNA expressions of autophagy-related genes and the cleavage of LC3 in oyster antibacterial immunity.

Yao H, Sun J, Zhang T, Wang L, Song L Fish Shellfish Immunol Rep. 2023; 4:100085.

PMID: 37065179 PMC: 10102855. DOI: 10.1016/j.fsirep.2023.100085.

CgDM9CP-5-Integrin-MAPK Pathway Regulates the Production of CgIL-17s and Cgdefensins in the Pacific Oyster, Crassostrea gigas.

Liu Y, Wang W, Sun J, Li Y, Wu S, Li Q J Immunol. 2022; 210(3):245-258.

PMID: 36548464 PMC: 9842941. DOI: 10.4049/jimmunol.2200016.

References

Yang J, Reth M . The dissociation activation model of B cell antigen receptor triggering. FEBS Lett. 2010; 584(24):4872-7. DOI: 10.1016/j.febslet.2010.09.045. View

Ivashkiv L . Cross-regulation of signaling by ITAM-associated receptors. Nat Immunol. 2009; 10(4):340-7. PMC: 2753670. DOI: 10.1038/ni.1706. View

Jirapongpairoj W, Hirono I, Kondo H . Development and evaluation of polyclonal antisera for detection of the IgM heavy chain of multiple fish species. J Immunol Methods. 2017; 449:71-75. DOI: 10.1016/j.jim.2017.06.011. View

De S, Zhang B, Shih T, Singh S, Winkler A, Donnelly R . B Cell-Intrinsic Role for IRF5 in TLR9/BCR-Induced Human B Cell Activation, Proliferation, and Plasmablast Differentiation. Front Immunol. 2018; 8:1938. PMC: 5768180. DOI: 10.3389/fimmu.2017.01938. View

Liu C, Wang M, Jiang S, Wang L, Chen H, Liu Z . A novel junctional adhesion molecule A (CgJAM-A-L) from oyster (Crassostrea gigas) functions as pattern recognition receptor and opsonin. Dev Comp Immunol. 2015; 55:211-20. DOI: 10.1016/j.dci.2015.09.011. View

Wang W, Song X, Wang L, Song L . Pathogen-Derived Carbohydrate Recognition in Molluscs Immune Defense. Int J Mol Sci. 2018; 19(3). PMC: 5877582. DOI: 10.3390/ijms19030721. View

Netea M, Joosten L, Latz E, Mills K, Natoli G, Stunnenberg H . Trained immunity: A program of innate immune memory in health and disease. Science. 2016; 352(6284):aaf1098. PMC: 5087274. DOI: 10.1126/science.aaf1098. View

Teh Y, Neuberger M . The immunoglobulin (Ig)alpha and Igbeta cytoplasmic domains are independently sufficient to signal B cell maturation and activation in transgenic mice. J Exp Med. 1997; 185(10):1753-8. PMC: 2196318. DOI: 10.1084/jem.185.10.1753. View

Yu Y, Kong W, Yin Y, Dong F, Huang Z, Yin G . Mucosal immunoglobulins protect the olfactory organ of teleost fish against parasitic infection. PLoS Pathog. 2018; 14(11):e1007251. PMC: 6237424. DOI: 10.1371/journal.ppat.1007251. View

10.

Zhang T, Qiu L, Sun Z, Wang L, Zhou Z, Liu R . The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendidus. Dev Comp Immunol. 2014; 45(1):141-50. DOI: 10.1016/j.dci.2014.02.015. View

11.

Chang Y, Kumar R, Ng T, Wang H . What vaccination studies tell us about immunological memory within the innate immune system of cultured shrimp and crayfish. Dev Comp Immunol. 2017; 80:53-66. DOI: 10.1016/j.dci.2017.03.003. View

12.

Teichmann S, Chothia C . Immunoglobulin superfamily proteins in Caenorhabditis elegans. J Mol Biol. 2000; 296(5):1367-83. DOI: 10.1006/jmbi.1999.3497. View

13.

Simon R, Diaz-Rosales P, Morel E, Martin D, Granja A, Tafalla C . CpG Oligodeoxynucleotides Modulate Innate and Adaptive Functions of IgM B Cells in Rainbow Trout. Front Immunol. 2019; 10:584. PMC: 6443966. DOI: 10.3389/fimmu.2019.00584. View

14.

Bengten E, Wilson M . Antibody Repertoires in Fish. Results Probl Cell Differ. 2015; 57:193-234. DOI: 10.1007/978-3-319-20819-0_9. View

15.

Quintin J, Saeed S, Martens J, Giamarellos-Bourboulis E, Ifrim D, Logie C . Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe. 2012; 12(2):223-32. PMC: 3864037. DOI: 10.1016/j.chom.2012.06.006. View

16.

Pluddemann A, Mukhopadhyay S, Gordon S . Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry. Immunol Rev. 2011; 240(1):11-24. DOI: 10.1111/j.1600-065X.2010.00989.x. View

17.

Zhang G, Fang X, Guo X, Li L, Luo R, Xu F . The oyster genome reveals stress adaptation and complexity of shell formation. Nature. 2012; 490(7418):49-54. DOI: 10.1038/nature11413. View

18.

Yang S, Zhuang T, Si Y, Qi K, Zhao J . Coriolus versicolor mushroom polysaccharides exert immunoregulatory effects on mouse B cells via membrane Ig and TLR-4 to activate the MAPK and NF-κB signaling pathways. Mol Immunol. 2014; 64(1):144-51. DOI: 10.1016/j.molimm.2014.11.007. View

19.

Koiwai K, Kondo H, Hirono I . The immune functions of sessile hemocytes in three organs of kuruma shrimp Marsupenaeus japonicus differ from those of circulating hemocytes. Fish Shellfish Immunol. 2018; 78:109-113. DOI: 10.1016/j.fsi.2018.04.036. View

20.

Wang J, Wang L, Yang C, Jiang Q, Zhang H, Yue F . The response of mRNA expression upon secondary challenge with Vibrio anguillarum suggests the involvement of C-lectins in the immune priming of scallop Chlamys farreri. Dev Comp Immunol. 2013; 40(2):142-7. DOI: 10.1016/j.dci.2013.02.003. View