The short life of the Hoyle organ of Sepia officinalis: formation, differentiation and degradation by programmed cell death

Abstract

Cephalopods encapsulate their eggs in protective egg envelopes. To hatch from this enclosure, most cephalopod embryos release egg shell-digesting choriolytic enzymes produced by the Hoyle organ (HO). After hatching, this gland becomes inactive and rapidly degrades by programmed cell death. We aim to characterize morphologically the development, maturation and degradation of the gland throughout embryonic and first juvenile stages in Sepia officinalis. Special focus is laid on cell death mechanisms and the presence of nitric oxide synthase during gland degradation. Hatching enzyme has been examined in view of metallic contents, commonly amplifying enzyme effectiveness. HO gland cells are first visualized at embryonic stage 23; secretion is observed from stage 27 onwards. Degradation of the HO occurs after hatching within two days by the rarely observed autophagic process, recognized for the first time in cephalopods. Nitric oxide synthase immunopositivity was not found in the HO cells after hatching, suggesting a possible NO role in cell death signalling. Although the HO 'life course' chronology in S. officinalis is similar to other cephalopods, gland degradation occurs by autophagy instead of necrosis. Eggs that combine a large perivitelline space and multi-layered integument seem to require a more complex and large gland system.

Evaluation of X‐ray tomography contrast agents: A review of production, protocols, and biological applications

“…The protocol helped to obtain detailed 3D visualization of embryos, and development and facial formation steps were assessed. Morphological characterization pertaining to the development, maturation, and degradation of the gland throughout embryonic and first juvenile stages of Sepia officinalis using CT methods were published by Cyran et al (). The samples were the glutaraldehyde‐fixed and washed, and dehydrated in varying concentrations of ethanol.…”

Digital Three-Dimensional Imaging Techniques Provide New Analytical Pathways for Malacological Research

“…Studies that previously have analyzed molluscan taxa using contrast-enhanced μCT comprise experiments on the general suitability of all higher molluscan taxa for this approach using different contrast agents (Golding and Jones 2007, Faulwetter et al 2012, Cándas et al 2015, Cándas et al 2016. In addition, more specifi c studies have focused on odontophoral cartilage morphology in selected gastropods (Golding et al 2009), changes in ganglionic system anatomy during cephalopod ontogeny (Kerbl et al 2013), the internal anatomy of a larval cephalopod (Xavier et al 2015), the reproductive system of a nudibranch (Cándas et al 2017), the anatomy of Hoyle's organ in a cephalopod (Cyran et al 2018), or the visualization of internal and external organs of selected gastropod species (Pedrouzo et al 2018). Furthermore, contrast-enhanced μCT was performed in a methodological study on correlative imaging using a bivalve (Handschuh et al 2013), to describe several new nudibranch species (Moles et al 2016, Moles et al 2017, and to illustrate the internal anatomy of numerous bivalve species (Machado et al 2018).…”

A practical staging atlas to study embryonic development of Octopus vulgaris under controlled laboratory conditions

“…b The morphological axes in cephalopod embryos correspond to the axes in other mollusks. In this orientation, the location of the funnel is posterior, the embryonic mouth is anterior, the arms are ventral and the mantle is dorsal enzymes that dissolve the chorion locally, making the egg integument permeable to water, which increases the osmotic pressure within the perivitelline space [5,[18][19][20]. Afterwards, the mantle is extruded due to a release of pressure and the Kölliker organs (hard bristle-like structures spread over the skin) make sure that the embryo does not slip back into the chorion so it can move freely from the egg during hatching [9,20,21].…”