Natural cyclic degeneration by a sequence of programmed cell death modes in Semibalanus balanoides (Linnaeus, 1767) (Crustacea, Cirripedia Thoracica)

Klepal, Waltraud; Gruber, Daniela; Pflugfelder, Bettina

doi:10.1007/s00435-007-0050-4

Cited by 9 publications

(5 citation statements)

References 37 publications

(36 reference statements)

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“…The ultrastructural observations further confirm the expected accompanying features relating to ACD, such as the secondary enlarged Golgi bodies and the loss of microvilli and junctional complexes (Clarke, 1990;Berry & Baehrecke, 2007;Klepal et al, 2008).…”

Section: Bipartite Granulessupporting

confidence: 67%

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

et al. 2017

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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.

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Section: Bipartite Granulessupporting

confidence: 67%

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

et al. 2017

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“…It is also evident that apoptosis and autophagy can occur simultaneously in the same tissue or even in the same cell (Bursch, 2001;Klepal et al, 2008).…”

Section: Pathways Of Programmed Cell Deathmentioning

confidence: 98%

“…Certainly apoptosis as cell death pathway can be excluded because of the lack of some typical indications as chromatin condensation, nuclear fragmentation, plasma membrane blebbing, or membrane coated cytoplasm fragments and stacks of membranes (Altmann and Bannasch, 1966;Kerr et al, 1972;Klepal et al, 2008).…”

Section: Pathways Of Programmed Cell Deathmentioning

confidence: 99%

Alterations in the mantle epithelium during transition from hatching gland to adhesive organ of Idiosepius pygmaeus (Mollusca, Cephalopoda)

Cyran

Klepal

Städler

et al. 2015

Mechanisms of Development

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Epithelial gland systems play an important role in marine molluscs in fabricating lubricants, repellents, fragrances, adhesives or enzymes. In cephalopods the typically single layered epithelium provides a highly dynamic variability and affords a rapid rebuilding of gland cells. While the digestive hatching gland (also named Hoyle organ) is obligatory for most cephalopods, only four genera (Nautilus, Sepia, Euprymna and Idiosepius) produce adhesive secretions by means of glandular cells in an adhesive area on the mantle or tentacles. In Idiosepius this adhesive organ is restricted to the posterior part of the fin region on the dorsal mantle side and well developed in the adult stage. Two gland cell types could be distinguished, which produce different contents of the adhesive. During the embryonic development the same body area is occupied by the temporary hatching gland. The question arises, in which way the hatching gland degrades and is replaced by the adhesive gland. Ultrastructural analyses as well as computer tomography scans were performed to monitor the successive post hatching transformation in the mantle epithelium from hatching gland degradation to the formation of the adhesive organ. According to our investigations the hatching gland cells degrade within about 1 day after hatching by a type of programmed cell death and leave behind a temporary cellular gap in this area. First glandular cells of the adhesive gland arise 7 days after hatching and proceed evenly over the posterior mantle epithelium. In contrast, the accompanying reduction of a part of the dorsal mantle musculature is already established before hatching. The results demonstrate a distinct independence between the two gland systems and illustrate the early development of the adhesive organ as well as the corresponding modifications within the mantle.

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“…No TUNEL or antibody staining was observed on any of the negative-control sections. Additionally, for positive controls, semithin section of Semibalanus balanoides (Crustacea, Cirripedia Thoracica), which is known to show various types of cell death in the degenerating penis tissue, were examined and revealed positive TUNEL and anti-AIF and anti-LC3 staining (see Klepal et al 2008). …”

Section: Immunohistochemistrymentioning

confidence: 99%

Dynamics of cell proliferation and apoptosis reflect different life strategies in hydrothermal vent and cold seep vestimentiferan tubeworms

2009

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Deep-sea vestimentiferan tubeworms, which live in symbiosis with bacteria, exhibit different life strategies according to their habitat. At unstable and relatively short-lived hydrothermal vents, they grow extremely fast, whereas their close relatives at stable and long-persisting cold seeps grow slowly and live up to 300 years. Growth and age differences are thought to occur because of ecological and physiological adaptations. However, the underlying mechanisms of cell proliferation and death, which are closely linked to homeostasis, growth, and longevity, are unknown. Here, we show by immunohistochemical and ultrastructural cell cycle analyses that cell proliferation activities of the two species studied are higher than in any other characterized invertebrate, being only comparable with tumor and wound-healing processes. The slow growth in Lamellibrachia luymesi from cold seeps results from balanced activities of proliferation and apoptosis in the epidermis. In contrast, Riftia pachyptila from hydrothermal vents grows fast because apoptosis is down-regulated in this tissue. The symbiont-housing organ, the trophosome, exhibits a complex cell cycle and terminal differentiation pattern in both species, and growth is regulated by proliferation. These mechanisms have similarities to the up- and down-regulation of proliferation or apoptosis in various types of tumor, although they occur in healthy animals in this study, thus providing significant insights into the underlying mechanisms of growth and longevity.

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Natural cyclic degeneration by a sequence of programmed cell death modes in Semibalanus balanoides (Linnaeus, 1767) (Crustacea, Cirripedia Thoracica)

Cited by 9 publications

References 37 publications

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

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

Alterations in the mantle epithelium during transition from hatching gland to adhesive organ of Idiosepius pygmaeus (Mollusca, Cephalopoda)

Dynamics of cell proliferation and apoptosis reflect different life strategies in hydrothermal vent and cold seep vestimentiferan tubeworms

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