Byrne M (2023), Morphological, Physiological and Mechanical Fea...

ECB-ART-51525

Mar Drugs 2023 Feb 21;213:. doi: 10.3390/md21030134.

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Morphological, Physiological and Mechanical Features of the Mutable Collagenous Tissues Associated with Autotomy and Evisceration in Dendrochirotid Holothuroids.

Byrne M .

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Evisceration in dendrochirotid sea cucumbers leads to expulsion of the digestive tract, pharyrngeal complex and coelomic fluid through rupture of the anterior body wall. This process involves failure of three mutable collagenous tissue (MCT) structures, the introvert, the pharyngeal retractor muscle tendon, and the intestine-cloacal junction. These are complex structures composed of several tissue strata. The MCT in the three autotomy structures contains collagen fibrils, unstriated microfibrils, and interfibrillar molecules. Neurosecretory-like processes (juxtaligamental-type) with large dense vesicles (LDVs) are prominent in the autotomy structures. Biomechanical tests show that these structures are not inherently weak. Failure of the autotomy structures can be elicited by manipulating the ionic environment and the changes are blocked by anaesthetics. Autotomy and evisceration are under neural control, but local neural elements and neurosecretory-like processes do not appear to be a source of factors that cause MCT destabilisation. The LDVs remain intact while the tissue destabilises. The coelomic fluid contains an evisceration inducing factor indicating a neurosecretory-like mediation of autotomy. This factor elicits muscle contraction and MCT destabilisation. As the autotomy structures are completely or partially surrounded by coelomic fluid, the agent(s) of change may be located in the coelom (systemic origin) as well as originate from cells within the MCT. The biochemistry and mechanism(s) of action of the evisceration factor are not known. This factor is a promising candidate for biodiscovery investigation.

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	Figure 1. (a) In situ image of Eupentacta quinquesemita showing the tentacles (T) that are used in suspension feeding and the supporting introvert (I). (b) Dissected individual showing the ossicles (O) of the pharyngeal complex, the introvert (I), the digestive tract (DT), and the pharyngeal retractor muscle (PM) and where it attaches (arrow) to the longitudinal body wall muscle. (c) Diagram showing the three autotomy structures; the introvert (I), pharyngeal retractor muscle (PM), tendon (Te), and the intestine-cloacal junction (arrow). C, cloaca; DT, digestive tract; L, longitudinal body wall muscle; O, ossicle ring; T, tentacles. (d) Evisceration involves softening of the introvert (I), which eventually dissolves into strands (arrow), note the broken end of the pharyngeal retractor muscles (PM). Scales: (a) = 1 cm (b,c) = 0.5 cm.
	Figure 2. Collagenous connective tissues of Eupentacta quinquesemita autotomy structures (a). Longitudinal section of collagen fibrils that differ in thickness and the unstriated fibrils (arrows) that cross between them. (b) Cross section showing collagen fibrils that differ in thickness. (c) Muscle bundle in the introvert connective tissue is surrounded by a band (CB) of collagen fibrils. (d) Collagen band that surrounds the muscle bundle. (e) Gut connective tissue layer with cells and small aggregations of material (arrow). (f) Unstriated fibril in introvert connective tissue. (g) Gut connective tissue layer with material (arrows) that may be coagulated haemal fluid. (h) Collagen fibrils (CF) in gut connective tissue layer. Scales: (a) = 0.1 µm, (b) and (d) = 0.5 µm, (c) = 2 µm, (e) = 1 µm (f–h) = 0.5 µm.
	Figure 3. Light (a,b) and transmission electron micrographs (c) of the intact introvert. (a,b) In cross section the introvert comprises a subepithelial connective tissue (SCT), a thin dense connective tissue layer (DCT), and is dominated by the inner loose connective tissue layer (LCT). The lumen of the tentacles (T), the radial nerve (N), and longitudinal body wall muscle (M) are evident. Arrow, oesophagus. (c) The dense connective region consists of collagen fibrils (CF), muscle (M) and occasional phagocytes (P). (d) Light micrograph showing morula cells (arrows) abundant in the subperitoneal connective tissue. (e) Electron micrograph of a morula cell filled with secretory vesicles. Scales: (a) = 2 mm, (b) = 0.2 mm (c–e) = 3 µm, (d) = 10 µm.
	Figure 4. (a–c) Transmission electron micrographs of the pharyngeal retractor muscle at the tendon connection to the body wall muscle. Collagenous tissue (CF) surrounds bundles of muscle cells (M. Processes containing large dense vesicles (arrows) in the connective tissue with some associated with muscle cells. P, peritoneum. Scales: (a) = 3 µm, (b,c) = 1 µm.
	Figure 5. (a–d) Transmission electron micrographs of a nerve bundle in the introvert connective tissue. The nerve bundle and associated cell are encased in a basal lamina (BL) and the axons contain clear vesicles (CV), small dense vesicles (SDV), dense core vesicles (DCV), and neurotubules (NT). CF, collagen fibrils; G, Golgi complex; GV, Golgi vesicles; P, phagocyte. Scales: (a,b) = 1 µm, (c,d) = 0.5 µm.
	Figure 6. Transmission electron micrographs of processes and cells containing dense vesicles that vary in size and shape. (a) Process in the dense connective tissue layer of the introvert where tangential sections (arrows) indicate that these profiles may be a part of an anastomosing process. Note the basal lamina (BL) cover. (b) Elongated (arrow) and round (arrowhead) vesicles in the same process in the introvert. (c) Cell body containing dense vesicles the introvert. (d) Dense vesicles apposed to collagen fibrils (CF) in the tendon. (e) Dense vesicle process in gut connective tissue. (f) Cell body in the tendon connective tissue containing dense vesicles that range in size and profile (arrows, round to elongate vesicles). G, Golgi complex, ER endoplasmic reticulum, M, mitochondrion. (a,c,f) = 1 µm, (b,d,e) = 0.5 µm.
	Figure 7. Transmission electron micrographs of autotomising MCT. (a) Collagen and unstriated fibrils in the introvert indicate some disarray but are intact. (b) Nerve-like profile in the loose connective tissue (LCT) with swollen cells (arrows). (c) Large dense granule processes in the dense connective tissue. Arrows show round and elongated vesicles. (d) Large dense granule processes in the dense connective tissue (DCT) tearing away (arrow) from the surrounding collagen, but the granules are intact. (e) Nerve bundle (N) and muscle cell (M) in introvert with tears evident (arrows). (f) Degenerating pharyngeal muscle cell (M) and associated axon-like processes remaining attached despite tissue disruption. Arrowhead shows round and elongated vesicles adjacent to each other. (g) Dense vesicles processes in the tendon connective tissue (h) Autotomised gut autotomy site with large and small granules (arrows) intact among disrupted tissue (a) = 0.3 µm (b) = 0.5 µm (c–e) = 1 µm, (f–h) = 2 µm.
	Figure 8. Hypothetical model of the sequence of events leading to autotomy and evisceration with involvement of a neurosecretory-like cascade and cell and tissue responses. It is proposed that the inducing stimulus (e.g., sea star predator) activates neurons which stimulate evisceration factor (EF) producing neurosecretory-endocrine cells resulting in release of EF into the coelomic fluid or directly activates EF producing cells. The process may also result in cell damage releasing EF into the coelom.

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