Morpho-functional characterisation of cœlomocytes in the aquacultivated sea cucumber Holothuria scabra: From cell diversity to transcriptomic immune response.
[en] Holothuria scabra is one of the most valuable species of sea cucumber owing to its exploitation as a seafood product. This study aims to describe the main molecular and cellular actors in the immunology of this species. First, a detailed description of the immune cells - the cœlomocytes - is provided, highlighting five main cell types including phagocytes, small round cells (SRCs), spherulocytes, fusiform cells, and crystal cells, with a further five subtypes identified using transmission electron microscopy. Cœlomocyte aggregates were also described morphologically, yielding two main types, one comprising three successive maturation stages. A comparison of the concentration and proportion of cell populations was carried out between the two main body fluids, namely the hydrovascular fluid of the Polian vesicle (HF) and the perivisceral fluid of the general cavity (PF), and no clear relation could be highlighted. Next, the cœlomocyte immune response was studied 24 h after lipopolysaccharide (LPS) injection in the two body fluids. Firstly, the fluctuation in cell populations was assessed, and despite a high inter-individual variability, it shows a decrease in the phagocyte proportion and an increase in the SRC proportion. Secondly, the differential gene expression of PF cœlomocytes was studied by de novo RNA-sequencing between LPS-injected and control-injected individuals: 945 genes were differentially expressed, including 673 up-regulated and 272 down-regulated in the LPS-injected individuals. Among these genes, 80 had a presumed function in immunity based on their annotation, covering a wide range of immune mechanisms. Overall, this study reveals a complex immune system at both molecular and cellular levels and constitutes a baseline reference on H. scabra immunity, which may be useful for the development of sustainable aquaculture and provides valuable data for comparative immunology.
Disciplines :
Zoology
Author, co-author :
Wambreuse, Noé ; Biology of Marine Organisms and Biomimetics Unit, Research Institute for Biosciences, University of Mons (UMONS), 7000, Mons, Belgium, Belaza Marine Station (IH.SM-UMONS-ULB-ULIEGE), Toliara, 601, Madagascar. Electronic address: Noe.Wambreuse@umons.ac.be
Caulier, Guillaume ; Université de Mons - UMONS > Faculté des Sciences > Service de Biologie des Organismes Marins et Biomimétisme
Eeckhaut, Igor ; Université de Mons - UMONS > Faculté des Sciences > Service de Biologie des Organismes Marins et Biomimétisme
Borrello, Laura; Biology of Marine Organisms and Biomimetics Unit, Research Institute for Biosciences, University of Mons (UMONS), 7000, Mons, Belgium
Bureau, Fabrice; Laboratory of Cellular and Molecular Immunology, GIGA Research, University of Liège, 4000, Liège, Belgium
Fievez, Laurence; Laboratory of Cellular and Molecular Immunology, GIGA Research, University of Liège, 4000, Liège, Belgium
Delroisse, Jérôme ; Biology of Marine Organisms and Biomimetics Unit, Research Institute for Biosciences, University of Mons (UMONS), 7000, Mons, Belgium, Laboratory of Cellular and Molecular Immunology, GIGA Research, University of Liège, 4000, Liège, Belgium
Language :
English
Title :
Morpho-functional characterisation of cœlomocytes in the aquacultivated sea cucumber Holothuria scabra: From cell diversity to transcriptomic immune response.
Purcell, S.W., Value, market preferences and trade of beche-de-mer from Pacific Island sea cucumbers. PLoS One, 9, 2014, e95075, 10.1371/journal.pone.0095075.
Hamel, J.-F., Eeckhaut, I., Conand, C., Sun, J., Caulier, G., Mercier, A., Global knowledge on the commercial sea cucumber Holothuria scabra. Adv. Mar. Biol., 2022, Elsevier, 1–286, 10.1016/bs.amb.2022.04.001.
Delroisse, J., Van Wayneberghe, K., Flammang, P., Gillan, D., Gerbaux, P., Opina, N., Todinanahary, G.G.B., Eeckhaut, I., Epidemiology of a SKin ulceration disease (SKUD) in the sea cucumber Holothuria scabra with a review on the SKUDs in holothuroidea (Echinodermata). Sci. Rep., 10, 2020, 22150, 10.1038/s41598-020-78876-0.
Smith, L.C., Arizza, V., Barela Hudgell, M.A., Barone, G., Bodnar, A.G., Buckley, K.M., Cunsolo, V., Dheilly, N.M., Franchi, N., Fugmann, S.D., Furukawa, R., Garcia-Arraras, J., Henson, J.H., Hibino, T., Irons, Z.H., Li, C., Lun, C.M., Majeske, A.J., Oren, M., Pagliara, P., Pinsino, A., Raftos, D.A., Rast, J.P., Samasa, B., Schillaci, D., Schrankel, C.S., Stabili, L., Stensväg, K., Sutton, E., Echinodermata: the complex immune system in echinoderms. Cooper, E.L., (eds.) Adv. Comp. Immunol., 2018, Springer International Publishing, Cham, 409–501, 10.1007/978-3-319-76768-0_13.
Caulier, G., Hamel, J.-F., Mercier, A., From coelomocytes to colored aggregates: cellular components and processes involved in the immune response of the holothuroid Cucumaria frondosa. Biol. Bull. 239 (2020), 95–114, 10.1086/710355.
Eliseikina, M.G., Magarlamov, T.Yu, Coelomocyte morphology in the holothurians Apostichopus japonicus (Aspidochirota: Stichopodidae) and Cucumaria japonica (Dendrochirota: Cucumariidae). Russ. J. Mar. Biol. 28 (2002), 197–202, 10.1023/A:1016801521216.
Xing, K., Yang, H., Chen, M., Morphological and ultrastructural characterization of the coelomocytes in Apostichopus japonicus. Aquat. Biol. 2 (2008), 85–92, 10.3354/ab00038.
Hetzel, H.R., Studies on Holothurian Coelomocytes, I., A Survey of coelomocyte types. Biol. Bull. 125 (1963), 289–301, 10.2307/1539404.
Prompoon, Y., Weerachatyanukul, W., Withyachumnarnkul, B., Lectin-based profiling of coelomocytes in Holothuria scabra and expression of superoxide dismutase in purified coelomocytes. Zoolog. Sci., 32, 2015, 345, 10.2108/zs140285.
Oomen, R.A., Hutchings, J.A., Transcriptomic responses to environmental change in fishes: insights from RNA sequencing. FACETS 2 (2017), 610–641, 10.1139/facets-2017-0015.
Gao, Q., Liao, M., Wang, Y., Li, B., Zhang, Z., Rong, X., Chen, G., Wang, L., Transcriptome analysis and discovery of genes involved in immune pathways from coelomocytes of sea cucumber (Apostichopus japonicus) after Vibrio splendidus challenge. Int. J. Mol. Sci. 16 (2015), 16347–16377, 10.3390/ijms160716347.
Dong, Y., Sun, H., Zhou, Z., Yang, A., Chen, Z., Guan, X., Gao, S., Wang, B., Jiang, B., Jiang, J., Expression analysis of immune related genes identified from the coelomocytes of sea cucumber (Apostichopus japonicus) in response to LPS challenge. Int. J. Mol. Sci. 15 (2014), 19472–19486, 10.3390/ijms151119472.
Smith, L.C., Hawley, T.S., Henson, J.H., Majeske, A.J., Oren, M., Rosental, B., Methods for collection, handling, and analysis of sea urchin coelomocytes. Methods Cell Biol., 2019, Elsevier, 357–389, 10.1016/bs.mcb.2018.11.009.
Zhou, Z.C., Dong, Y., Sun, H.J., Yang, A.F., Chen, Z., Gao, S., Jiang, J.W., Guan, X.Y., Jiang, B., Wang, B., Transcriptome sequencing of sea cucumber (Apostichopus japonicus) and the identification of gene-associated markers. Mol. Ecol. Resour 14 (2014), 127–138, 10.1111/1755-0998.12147.
Xue, Z., Li, H., Wang, X., Li, X., Liu, Y., Sun, J., Liu, C., A review of the immune molecules in the sea cucumber. Fish Shellfish Immunol. 44 (2015), 1–11, 10.1016/j.fsi.2015.01.026.
Hibino, T., Loza-Coll, M., Messier, C., Majeske, A.J., Cohen, A.H., Terwilliger, D.P., Buckley, K.M., Brockton, V., Nair, S.V., Berney, K., Fugmann, S.D., Anderson, M.K., Pancer, Z., Cameron, R.A., Smith, L.C., Rast, J.P., The immune gene repertoire encoded in the purple sea urchin genome. Dev. Biol. 300 (2006), 349–365, 10.1016/j.ydbio.2006.08.065.
Terrana, L., Eeckhaut, I., Taxonomic description and 3D modelling of a new species of myzostomid (Annelida, Myzostomida) associated with black corals from Madagascar. Zootaxa, 4244, 2017, 10.11646/zootaxa.4244.2.9.
Li, Q., rong Qi, R., nan Wang, Y., gen Ye, S., Qiao, G., Li, H., Comparison of cells free in coelomic and water-vascular system of sea cucumber, Apostichopus japonicus. Fish Shellfish Immunol. 35 (2013), 1654–1657, 10.1016/j.fsi.2013.07.020.
Canicatti, C., D'Ancona, G., Farina‐ Lipari, E., The coelomocytes of Holothuria polii (Echinodermata). I. light and electron microscopy. Bolletino Zool. 56 (1989), 29–36, 10.1080/11250008909355618.
Queiroz, V., Mauro, M., Arizza, V., Custódio, M.R., Vazzana, M., The use of an integrative approach to identify coelomocytes in three species of the genus Holothuria (Echinodermata). Invertebr. Biol., 141, 2022, 10.1111/ivb.12357.
Caulier, G., Jobson, S., Wambreuse, N., Borrello, L., Delroisse, J., Eeckhaut, I., Mercier, A., Hamel, J.-F., Vibratile cells and hemocytes in sea cucumbers—clarifications and new paradigms. World Sea Cucumbers, 2024, Elsevier, 403–412, 10.1016/B978-0-323-95377-1.00024-2.
Li, Q., Ren, Y., Luan, L., Zhang, J., Qiao, G., Wang, Y., Ye, S., Li, R., Localization and characterization of hematopoietic tissues in adult sea cucumber, Apostichopus japonicus. Fish Shellfish Immunol. 84 (2019), 1–7, 10.1016/j.fsi.2018.09.058.
Dubovskiy, I.M., Kryukova, N.A., Glupov, V.V., Ratcliffe, N.A., Encapsulation and nodulation in insects. Invertebr. Surviv. J., 2016, 229–246, 10.25431/1824-307X/ISJ.V13I1.229-246.
Jobson, S., Hamel, J.-F., Mercier, A., Rainbow bodies: revisiting the diversity of coelomocyte aggregates and their synthesis in echinoderms. Fish Shellfish Immunol. 122 (2022), 352–365, 10.1016/j.fsi.2022.02.009.
Matranga, V., Toia, G., Bonaventura, R., Müller, W.E.G., Cellular and biochemical responses to environmental and experimentally induced stress in sea urchin coelomocytes. Cell Stress Chaperones, 5, 2000, 113, 10.1379/1466-1268(2000)005<0113:CABRTE>2.0.CO;2.
Hamel, J., Sun, J., Gianasi, B.L., Montgomery, E.M., Kenchington, E.L., Burel, B., Rowe, S., Winger, P.D., Mercier, A., Active buoyancy adjustment increases dispersal potential in benthic marine animals. J. Anim. Ecol. 88 (2019), 820–832, 10.1111/1365-2656.12943.
Wu, X., Chen, T., Huo, D., Yu, Z., Ruan, Y., Cheng, C., Jiang, X., Ren, C., Transcriptomic analysis of sea cucumber (Holothuria leucospilota) coelomocytes revealed the echinoderm cytokine response during immune challenge. BMC Genom., 21, 2020, 306, 10.1186/s12864-020-6698-6.
Chiaramonte, M., Russo, R., The echinoderm innate humoral immune response. Ital. J. Zool. 82 (2015), 300–308, 10.1080/11250003.2015.1061615.
Korn, T., Bettelli, E., Oukka, M., Kuchroo, V.K., IL-17 and Th17 cells. Annu. Rev. Immunol. 27 (2009), 485–517, 10.1146/annurev.immunol.021908.132710.
Meunier, E., Broz, P., Evolutionary convergence and divergence in NLR function and structure. Trends Immunol. 38 (2017), 744–757, 10.1016/j.it.2017.04.005.
Li, L.X., Liu, X.H., Wang, H., Wang, L., Han, B., Chang, Y.Q., Ding, J., Molecular characterization and expression of NLRP10 in the antibacterial host defense of the sea cucumber (Apostichopus japonicus). Gene 675 (2018), 110–118, 10.1016/j.gene.2018.06.072.
Lv, Z., Wei, Z., Zhang, Z., Li, C., Shao, Y., Zhang, W., Zhao, X., Li, Y., Duan, X., Xiong, J., Characterization of NLRP3-like gene from Apostichopus japonicus provides new evidence on inflammation response in invertebrates. Fish Shellfish Immunol. 68 (2017), 114–123, 10.1016/j.fsi.2017.07.024.
Gowda, N.M., Goswami, U., Islam Khan, M., T-antigen binding lectin with antibacterial activity from marine invertebrate, sea cucumber (Holothuria scabra): possible involvement in differential recognition of bacteria. J. Invertebr. Pathol. 99 (2008), 141–145, 10.1016/j.jip.2008.04.003.
Wei, X., Liu, X., Yang, J., Wang, S., Sun, G., Yang, J., Critical roles of sea cucumber C-type lectin in non-self recognition and bacterial clearance. Fish Shellfish Immunol. 45 (2015), 791–799, 10.1016/j.fsi.2015.05.037.
Elenbaas, J.S., Pudupakkam, U., Ashworth, K.J., Kang, C.J., Patel, V., Santana, K., Jung, I.-H., Lee, P.C., Burks, K.H., Amrute, J.M., Mecham, R.P., Halabi, C.M., Alisio, A., Di Paola, J., Stitziel, N.O., SVEP1 is an endogenous ligand for the orphan receptor PEAR1. Nat. Commun., 14, 2023, 850, 10.1038/s41467-023-36486-0.
Verstrepen, L., Carpentier, I., Beyaert, R., The biology of A20-binding inhibitors of NF-κB activation (ABINS). Ferran, C., (eds.) Mult. Ther. Targets A20, 2014, Springer New York, New York, NY, 13–31, 10.1007/978-1-4939-0398-6_2.
Xu, C., Zheng, P., Shen, S., Xu, Y., Wei, L., Gao, H., Wang, S., Zhu, C., Tang, Y., Wu, J., Zhang, Q., Shi, Y., NMR structure and regulated expression in APL cell of human SH3BGRL3. FEBS Lett. 579 (2005), 2788–2794, 10.1016/j.febslet.2005.04.011.
Wang, Y., Diao, J., Wang, B., Xu, X., Gui, M., Li, C., Guo, M., A second FADD mediates coelomocyte apoptosis response to Vibrio splendidus infection in sea cucumber Apostichopus japonicus. Fish Shellfish Immunol. 127 (2022), 396–404, 10.1016/j.fsi.2022.06.046.
Rodriguez, J.M., Glozak, M.A., Ma, Y., Cress, W.D., Bok, bcl-2-related ovarian killer, is cell cycle-regulated and sensitizes to stress-induced apoptosis. J. Biol. Chem. 281 (2006), 22729–22735, 10.1074/jbc.M604705200.
Hillier, B.J., Vacquier, V.D., Amassin, an olfactomedin protein, mediates the massive intercellular adhesion of sea urchin coelomocytes. J. Cell Biol. 160 (2003), 597–604, 10.1083/jcb.200210053.
D'Andrea-Winslow, L., Radke, D.W., Utecht, T., Kaneko, T., Akasaka, K., Sea urchin coelomocyte arylsulfatase: a modulator of the echinoderm clotting pathway. Integr. Zool. 7 (2012), 61–73, 10.1111/j.1749-4877.2011.00279.x.
Ponczek, M.B., Bijak, M.Z., Nowak, P.Z., Evolution of thrombin and other hemostatic proteases by survey of protochordate, hemichordate, and echinoderm genomes. J. Mol. Evol. 74 (2012), 319–331, 10.1007/s00239-012-9509-0.
Wang, Z., Li, C., Xing, R., Shao, Y., Zhao, X., Zhang, W., Guo, M., β-Integrin mediates LPS-induced coelomocyte apoptosis in sea cucumber Apostichopus japonicus via the integrin/FAK/caspase-3 signaling pathway. Dev. Comp. Immunol. 91 (2019), 26–36, 10.1016/j.dci.2018.10.004.
Wallin, R.P.A., Lundqvist, A., Moré, S.H., Von Bonin, A., Kiessling, R., Ljunggren, H.-G., Heat-shock proteins as activators of the innate immune system. Trends Immunol. 23 (2002), 130–135, 10.1016/S1471-4906(01)02168-8.
Zhao, H., Yang, H., Zhao, H., Chen, M., Wang, T., The molecular characterization and expression of heat shock protein 90 (Hsp90) and 26 (Hsp26) cDNAs in sea cucumber (Apostichopus japonicus). Cell Stress Chaperones 16 (2011), 481–493, 10.1007/s12192-011-0260-z.
Battin, E.E., Brumaghim, J.L., Antioxidant activity of sulfur and selenium: a review of reactive oxygen species scavenging, glutathione peroxidase, and metal-binding antioxidant mechanisms. Cell Biochem. Biophys. 55 (2009), 1–23, 10.1007/s12013-009-9054-7.
Ba, H., Yao, F., Yang, L., Qin, T., Luan, H., Li, Z., Zou, X., Hou, L., Identification and expression patterns of extracellular matrix-associated genes fibropellin-ia and tenascin involved in regeneration of sea cucumber Apostichopus japonicus. Gene 565 (2015), 96–105, 10.1016/j.gene.2015.03.071.
Mehta, K., Shahid, U., Malavasi, F., Human CD38, a cell‐surface protein with multiple functions. Faseb. J. 10 (1996), 1408–1417, 10.1096/fasebj.10.12.8903511.
Cerenius, L., Söderhäll, K., Immune properties of invertebrate phenoloxidases. Dev. Comp. Immunol., 122, 2021, 104098, 10.1016/j.dci.2021.104098.
Jiang, J., Zhou, Z., Dong, Y., Sun, H., Chen, Z., Yang, A., Gao, S., Wang, B., Jiang, B., Guan, X., Phenoloxidase from the sea cucumber Apostichopus japonicus: cDNA cloning, expression and substrate specificity analysis. Fish Shellfish Immunol. 36 (2014), 344–351, 10.1016/j.fsi.2013.12.001.
Wang, Z., Fan, X., Li, Z., Guo, L., Ren, Y., Li, Q., Comparative analysis for immune response of coelomic fluid from coelom and polian vesicle in Apostichopus japonicus to Vibrio splendidus infection. Fish Shellfish Immunol. Rep., 4, 2023, 100074, 10.1016/j.fsirep.2022.100074.
Liu, C., Yang, C., Wang, M., Jiang, S., Yi, Q., Wang, W., Wang, L., Song, L., A CD63 homolog specially recruited to the fungi-contained phagosomes is involved in the cellular immune response of oyster Crassostrea gigas. Front. Immunol., 11, 2020, 1379, 10.3389/fimmu.2020.01379.
Yu, K., Zhao, X., Xiang, Y., Li, C., Phenotypic and functional characterization of two coelomocyte subsets in Apostichopus japonicus. Fish Shellfish Immunol., 132, 2023, 108453, 10.1016/j.fsi.2022.108453.
Wilkins, G.T., Using Novel Sequence Assembly Strategies to Resolve the Transformer Gene Family., 2020, Macquarie University Doctoral Thesis.
Chen, K., Zhang, S., Shao, Y., Guo, M., Zhang, W., Li, C., A unique NLRC4 receptor from echinoderms mediates Vibrio phagocytosis via rearrangement of the cytoskeleton and polymerization of F-actin. PLoS Pathog., 17, 2021, e1010145, 10.1371/journal.ppat.1010145.
Li, X.-J., Yang, L., Li, D., Zhu, Y.-T., Wang, Q., Li, W.-W., Pathogen-specific binding soluble down syndrome cell adhesion molecule (Dscam) regulates phagocytosis via membrane-bound Dscam in crab. Front. Immunol., 9, 2018, 801, 10.3389/fimmu.2018.00801.
