Taguchi M et al. (2022), Establishment of the immunological self in juve...

ECB-ART-51093

Front Immunol 2022 Dec 06;13:1056027. doi: 10.3389/fimmu.2022.1056027.

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Establishment of the immunological self in juvenile Patiria pectinifera post-metamorphosis.

Taguchi M , Minakata K , Tame A , Furukawa R .

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Ontogeny of the immune system is a fundamental immunology issue. One indicator of immune system maturation is the establishment of the immunological self, which describes the ability of the immune system to distinguish allogeneic individuals (allorecognition ability). However, the timing of immune system maturation during invertebrate ontogeny is poorly understood. In the sea star Patiria pectinifera, cells that have dissociated from the embryos and larvae are able to reconstruct larvae. This reconstruction phenomenon is possible because of a lack of allorecognition capability in the larval immune system, which facilitates the formation of an allogeneic chimera. In this study, we revealed that the adult immune cells of P. pectinifera (coelomocytes) have allorecognition ability. Based on a hypothesis that allorecognition ability is acquired before and after metamorphosis, we conducted detailed morphological observations and survival time analysis of metamorphosis-induced chimeric larvae. The results showed that all allogeneic chimeras died within approximately two weeks to one month of reaching the juvenile stage. In these chimeras, the majority of the epidermal cell layer was lost and the mesenchymal region expanded, but cell death appeared enhanced in the digestive tract. These results indicate that the immunological self of P. pectinifera is established post-metamorphosis during the juvenile stage. This is the first study to identify the timing of immune system maturation during echinodermal ontogenesis. As well as establishing P. pectinifera as an excellent model for studies on self- and non-self-recognition, this study enhances our understanding of the ontogeny of the immune system in invertebrates.

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	Figure 1. Patiria pectinifera coelomocytes. (A) Coelomocytes smear stained by MG. (B–F) Five identified cell types: (B) amoebocyte; (C) discoidal phagocyte; (D) agranulocyte; (E) progenitor cell; (F) morula cell. Fi, filopodia; La, lamellipodia; Ru: membrane ruffling, Arrows: granules. Scale bars: 20 µm (A), 10 µm (B–F).
	Figure 2. Dynamics of coelomocyte aggregate formation in response to injected allogeneic coelomocytes. (A) Time course of allorecognition response to allogeneic coelomocytes. Arrow heads indicate coelomocyte aggregates. Scale bar: 500 µm. (B) Magnified image of coelomocyte aggregate in response to fluorescently labeled allogeneic coelomocytes. Scale bar: 100 µm. (C) Temporal change in the size of coelomocyte aggregates, shown in (A), after injection of allogeneic coelomocytes. Horizontal bars indicate the median size at each time interval. (D) Temporal change in the number of coelomocyte aggregates after injection of allogeneic coelomocytes in each recipient.
	Figure 3. Internal morphology of coelomocyte aggregates in response to allogeneic coelomocytes. (A) Outer edge of aggregate. (B) Coelomocytes that phagocytosed other coelomocytes. Asterisks indicate the nuclei of phagocytosed coelomocytes. (C) Coelomocyte during digestion of the phagocytosed cell. A secondary lysosome (SL) that fused with the endosome was also observed. Scale bars: 5 µm (A), 2 µm (B), 1 µm (C).
	Figure 4. Developmental process of chimeric larvae. (A) Fluorescent labeled blastulae before dissociation. Images of differential interference contrast (left), stained by CMFDA (middle), stained by CFDA (right). Scale bar: 100 µm. (B) Developmental processes of reconstructed chimeras. Arrows: adult rudiment. Scale bars: 40 µm (dissociated cells to reconstructed embryo), 200 µm (gastrula and bipinnaria), 500 µm (brachiolaria and juvenile).
	Figure 5. Abnormal morphologies and survival time analysis of allogeneic chimera juveniles. (A) Allogeneic chimera showing abnormal morphologies. Left: view of back bridge form from above. Middle: bent in half. Right: swelling like balloons. DS, dorsal side; VS, ventral side; Arrowheads: five arms. Arrows: mouth. Scale bar: 500 µm. (B) Survival time curve of the juvenile stage using the Kaplan–Meier method.
	Figure 6. Internal morphology of chimeric juveniles. (A) Light microscopic and transmission electron microscopic images of semi-thin sections of juveniles. Left column: whole juvenile sections stained by toluidine blue. Sibling chimeras and healthy individual are 5 dpm, abnormal individual is 14 dpm, and death occurred at 30 dpm. Ventral side is downwards. Enlarged portion of the black box is shown in the right column. Pink lines indicate that part of the epidermal cell layer was lost. C, coelomic cavity; DT, digestive tract; ECL, epidermal cell layer; HL, hyalin layer; MC, mesenchyme cell; MR, mesenchymal region. (B) Phagocytosis in areas of severe damage in epidermal cell layer of abnormal-morphology individual. Arrows: cells containing phagosome-like vesicles. Arrowheads: vesicles. Scale bars: 100 µm (left column in A and B), 10 µm (right column in A and B).
	Figure 7. Abnormal morphologies of digestive tract in chimeric juveniles. Sibling chimera (A, B) and dead allogeneic chimera (C–E) shown in Figure 6 . LD, lipid droplet. Black boxes in A, C are shown enlarged in B, D, respectively. (E) Cell indicated by arrow in (C) Arrowheads: segmented nuclear membrane. Scale bars: 10 µm (A), 2 µm (B, E).

References [+] :

Bertheussen, The cytotoxic reaction in allogeneic mixtures of echinoid phagocytes. 1979, Pubmed, Echinobase