RGD-Labeled Hemocytes With High Migration Activity Display a Potential Immunomodulatory Role in the Pacific Oyster

Overview

Journal Front Immunol

Specialty Allergy & Immunology

Date 2022 Jul 22

PMID 35865522

Authors

Zhao Lv

Limei Qiu

Weilin Wang

Zhaoqun Liu

Qing Liu

Lingling Wang

Linsheng Song

Affiliations

Soon will be listed here.

Abstract

Immunocyte migration to infection sites is important for host cellular defense, but the main types of migrating hemocytes and their mechanisms against pathogen invasions are unclear in invertebrates. In the present study, a population of hemocytes in the Pacific oyster labeled with a fluorescein isothiocyanate (FITC)-conjugated Arg-Gly-Asp (RGD)-containing peptide was sorted. RGD hemocytes were characterized by a smaller cell size and cytoplasmic-nucleo ratio, fewer cytoplasmic granules, and higher levels of myeloperoxidase, reactive oxygen species, and intracellular free calcium concentration. RGD hemocytes exhibited a high level of migration activity, which was further induced after infection. Transcriptome analysis revealed that RGD hemocytes highly expressed a series of migration-related genes, which together with migration-promoting genes were significantly upregulated after infection. The neuroendocrine system was also proven to regulate the migration activity of RGD hemocytes, especially with the excitatory neuroendocrine factor dopamine, which promoted migration activity as confirmed by receptor blocking assays. Meanwhile, RGD hemocytes could highly express immunomodulatory factor interleukin (IL)-17s and their receptor genes, which was positively related to the production of antimicrobial peptides in whole hemocytes after infection. Collectively, this study identified a specific hemocyte population, i.e., RGD hemocytes, that shows high migration activity in response to pathogen infection and exerts a potential immunomodulatory role by highly expressing IL-17s that might enhance the hemocytes' antimicrobial peptide production in oysters.

Citing Articles

Hallmarks of crustacean immune hemocytes at single-cell resolution.

Xin F, Zhang X Front Immunol. 2023; 14:1121528.

PMID: 36761772 PMC: 9902875. DOI: 10.3389/fimmu.2023.1121528.

References

van Rees D, Szilagyi K, Kuijpers T, Matlung H, van den Berg T . Immunoreceptors on neutrophils. Semin Immunol. 2016; 28(2):94-108. PMC: 7129252. DOI: 10.1016/j.smim.2016.02.004. View

Bhusal R, Foster S, Stone M . Structural basis of chemokine and receptor interactions: Key regulators of leukocyte recruitment in inflammatory responses. Protein Sci. 2019; 29(2):420-432. PMC: 6954698. DOI: 10.1002/pro.3744. View

Nagaosa K, Okada R, Nonaka S, Takeuchi K, Fujita Y, Miyasaka T . Integrin βν-mediated phagocytosis of apoptotic cells in Drosophila embryos. J Biol Chem. 2011; 286(29):25770-7. PMC: 3138285. DOI: 10.1074/jbc.M110.204503. View

Conti H, Shen F, Nayyar N, Stocum E, Sun J, Lindemann M . Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med. 2009; 206(2):299-311. PMC: 2646568. DOI: 10.1084/jem.20081463. View

Parsons B, Foley E . Cellular immune defenses of Drosophila melanogaster. Dev Comp Immunol. 2016; 58:95-101. DOI: 10.1016/j.dci.2015.12.019. View

Xin L, Zhang H, Du X, Li Y, Li M, Wang L . The systematic regulation of oyster CgIL17-1 and CgIL17-5 in response to air exposure. Dev Comp Immunol. 2016; 63:144-55. DOI: 10.1016/j.dci.2016.06.001. View

Jin T, Zhang N, Long Y, Parent C, Devreotes P . Localization of the G protein betagamma complex in living cells during chemotaxis. Science. 2000; 287(5455):1034-6. DOI: 10.1126/science.287.5455.1034. View

Song L, Wang L, Qiu L, Zhang H . Bivalve immunity. Adv Exp Med Biol. 2011; 708:44-65. DOI: 10.1007/978-1-4419-8059-5_3. View

Wang L, Zhang H, Wang M, Zhou Z, Wang W, Liu R . The transcriptomic expression of pattern recognition receptors: Insight into molecular recognition of various invading pathogens in Oyster Crassostrea gigas. Dev Comp Immunol. 2018; 91:1-7. DOI: 10.1016/j.dci.2018.09.021. View

10.

Mitroulis I, Alexaki V, Kourtzelis I, Ziogas A, Hajishengallis G, Chavakis T . Leukocyte integrins: role in leukocyte recruitment and as therapeutic targets in inflammatory disease. Pharmacol Ther. 2014; 147:123-135. PMC: 4324083. DOI: 10.1016/j.pharmthera.2014.11.008. View

11.

Johansson M . Cell adhesion molecules in invertebrate immunity. Dev Comp Immunol. 1999; 23(4-5):303-15. DOI: 10.1016/s0145-305x(99)00013-0. View

12.

Mak M, Spill F, Kamm R, Zaman M . Single-Cell Migration in Complex Microenvironments: Mechanics and Signaling Dynamics. J Biomech Eng. 2015; 138(2):021004. PMC: 4844084. DOI: 10.1115/1.4032188. View

13.

Li B, Song K, Meng J, Li L, Zhang G . Integrated application of transcriptomics and metabolomics provides insights into glycogen content regulation in the Pacific oyster Crassostrea gigas. BMC Genomics. 2017; 18(1):713. PMC: 5594505. DOI: 10.1186/s12864-017-4069-8. View

14.

Plows L, Cook R, Davies A, Walker A . Integrin engagement modulates the phosphorylation of focal adhesion kinase, phagocytosis, and cell spreading in molluscan defence cells. Biochim Biophys Acta. 2006; 1763(8):779-86. DOI: 10.1016/j.bbamcr.2006.04.008. View

15.

Du Y, Zhang L, Xu F, Huang B, Zhang G, Li L . Validation of housekeeping genes as internal controls for studying gene expression during Pacific oyster (Crassostrea gigas) development by quantitative real-time PCR. Fish Shellfish Immunol. 2013; 34(3):939-45. DOI: 10.1016/j.fsi.2012.12.007. View

16.

Hirahara K, Nakayama T . CD4+ T-cell subsets in inflammatory diseases: beyond the Th1/Th2 paradigm. Int Immunol. 2016; 28(4):163-71. PMC: 4889886. DOI: 10.1093/intimm/dxw006. View

17.

Lv Z, Qiu L, Wang W, Liu Z, Liu Q, Wang L . The Members of the Highly Diverse Integrin Family Cooperate for the Generation of Various Immune Responses. Front Immunol. 2020; 11:1420. PMC: 7390872. DOI: 10.3389/fimmu.2020.01420. View

18.

Klein J . Dynamic Interactions Between the Immune System and the Neuroendocrine System in Health and Disease. Front Endocrinol (Lausanne). 2021; 12:655982. PMC: 8020567. DOI: 10.3389/fendo.2021.655982. View

19.

Chen X, Conti P, Moats R . In vivo near-infrared fluorescence imaging of integrin alphavbeta3 in brain tumor xenografts. Cancer Res. 2004; 64(21):8009-14. DOI: 10.1158/0008-5472.CAN-04-1956. View

20.

Devreotes P, Horwitz A . Signaling networks that regulate cell migration. Cold Spring Harb Perspect Biol. 2015; 7(8):a005959. PMC: 4526752. DOI: 10.1101/cshperspect.a005959. View