On the functions of the pore cells in the connective tissue of terrestrial pulmonate molluscs

Skelding, J. M.; Newell, P. F.

doi:10.1007/bf00225366

Cited by 28 publications

(24 citation statements)

References 7 publications

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“…When we started our experiments, the situation in gastropods was rather unclear. In the pulmonate gastropods Lymnaea stagnalis, Helix aspersa and Arion hortensis, "pore cells" (recently renamed "rhogocytes", for review, see Haszprunar 1996) scattered among the connective tissue have been proposed as candidates for the site of hemocyanin biosynthesis, from electron-microscopic images showing the presence of intracellular hemocyanin-like particles (Sminia 1972;Sminia and Boer 1973;Skelding and Newell 1975;Sminia and Vlugt van Daalen 1977). In contrast, similar experiments with tissues of opisthobranch species indicated the presence of intracellular hemocyanin in the socalled "blood gland" (Schmekel and Weischer 1973).…”

Section: Introductionmentioning

confidence: 79%

Rhogocytes (pore cells) as the site of hemocyanin biosynthesis in the marine gastropod Haliotis tuberculata

Albrecht¹,

Keller²,

Gebauer³

et al. 2001

Cell and Tissue Research

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Rhogocytes (pore cells) are specific molluscan cell types that are scattered throughout the connective tissues of diverse body parts. We have identified rhogocytes in large numbers in tissue taken from mantle, foot and midgut gland of the abalone Haliotis tuberculata (Vetigastropoda). Within cisternae of the endoplasmic reticulum, particles are visible that resemble, in shape and size, hemocyanin molecules, the respiratory protein of many molluscs. Immunohistochemical experiments using hemocyanin-specific antibodies demonstrated that these cells contain hemocyanin. In situ hybridization with a cDNA probe specific for Haliotis hemocyanin showed that hemocyanin-specific mRNA is present in rhogocytes, which confirmed that they are the site of hemocyanin biosynthesis in this gastropod. A possible path of hemocyanin release into the hemolymph is discussed. Also in the vetigastropod Megathura crenulata, many rhogocytes could be detected. However, they lacked hemocyanin molecules which, together with published data, indicates a seasonal expression of hemocyanin in this animal.

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Section: Introductionmentioning

confidence: 79%

Rhogocytes (pore cells) as the site of hemocyanin biosynthesis in the marine gastropod Haliotis tuberculata

Albrecht¹,

Keller²,

Gebauer³

et al. 2001

Cell and Tissue Research

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“…If the slit diaphragm is indeed a molecular sieve for size-selective inward passage of hemolymph components, which is also deduced from its similarity to the diaphragm in podocytes and nephrocytes [1], [14], the outward passage of the freshly synthesized, and exocytosed, hemoglobin and/or hemocyanin requires a gating mechanism. We speculate that a chemical signal released during exocytosis stimulates the actin bundles at either side of the diaphragmatic slits to interact with motor proteins which temporarily enlarges the holes of the sieve.…”

Section: Discussionmentioning

confidence: 99%

“…Since gastropod rhogocytes often contain, in lacunae of the endoplasmic reticulum, large amounts of the extracellular oxygen carrier hemocyanin, these cells have been addressed as the site of hemocyanin biosynthesis [14]–[17]. Hemocyanin is a multimeric blue copper protein and structurally known in detail (for review, see [18]).…”

Section: Introductionmentioning

confidence: 99%

3D-Ultrastructure, Functions and Stress Responses of Gastropod (Biomphalaria glabrata) Rhogocytes

et al. 2014

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Rhogocytes are pore cells scattered among the connective tissue of different body parts of gastropods and other molluscs, with great variation in their number, shape and size. They are enveloped by a lamina of extracellular matrix. Their most characteristic feature is the “slit apparatus”, local invaginations of the plasma membrane bridged by cytoplasmic bars, forming slits of ca. 20 nm width. A slit diaphragm creates a molecular sieve with permeation holes of 20×20 nm. In blue-blooded gastropods, rhogocytes synthesize and secrete the respiratory protein hemocyanin, and it has been proposed–though not proven–that in the rare red-blooded snail species they might synthesize and secrete the hemoglobin. However, the cellular secretion pathway for respiratory proteins, and the functional role(s) of the enigmatic rhogocyte slit apparatus are still unclear. Additional functions for rhogocytes have been proposed, notably a role in protein uptake and degradation, and in heavy metal detoxification. Here we provide new structural and functional information on the rhogocytes of the red-blooded freshwater snail Biomphalaria glabrata. By in situ hybridization of mantle tissues, we prove that rhogocytes indeed synthesize hemoglobin. By electron tomography, the first three dimensional (3D) reconstructions of the slit apparatus are provided, showing detail of highly dense material in the cytoplasmic bars close to the slits. By immunogold labelling, we collected evidence that a major component of this material is actin. By genome databank mining, the complete sequence of a B. glabrata nephrin was obtained, and localized to the rhogocytes by immunofluorescence microscopy. The presence of both proteins fit the ultrastructure-based hypothesis that rhogocytes are related to mammalian podocytes and insect nephrocytes. Reactions of the rhogocytes to deprivation of food and cadmium toxification are also documented, and a possible secretion pathway of newly synthesized respiratory proteins through the slit apparatus is discussed.

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“…(Sundermann 1980). In the connective tissue of gastropods, comparable endocytotic-active cells, called pore cells, were also described to be a component of the defense system (Wondrak 1969;Sminia 1972;Skelding and Newell 1975;Sminia 1981;Sminia and van der Knaap 1987). In this study, we prefer the name rhogocyte as proposed for all molluscs by Witmer (1974) and Haszprunar (1996), respectively.…”

Section: Introductionmentioning

confidence: 91%

Hemocyanin and the branchial heart complex of Sepia officinalis : are the hemocytes involved in hemocyanin metabolism of coleoid cephalopods?

Beuerlein

Ruth

Westermann

et al. 2002

Cell and Tissue Research

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Cytobiological experiments using isotopic- and cytochemical-labeled Sepia hemocyanin as well as immunocytochemical localization of the respiratory pigment were carried out to investigate the function of the hemocytes in hemocyanin metabolism of the common cuttlefish Sepia officinalis. For comparison, the rhogocytes (ovoid cells) of the branchial heart complex were included in this study. Hemocyanin molecules were immunocytochemically detected in the lysosomal compartment of the rhogocytes and, at lower levels, in adhesive and circulating hemocytes. (125)I-labeled Sepia hemocyanin was taken up by the rhogocytes only, whereas gold- and/or fluorescein-labeled Sepia hemocyanin was solely taken up by the adhesive and the circulating hemocytes, even though the level of uptake is different. There are also differences in the uptake of pure gold particles and/or fluorescein between rhogocytes and hemocytes. These findings give evidence that circulating and adhesive hemocytes of the branchial heart complex are not involved in hemocyanin turnover, but are a component of the cellular defense and detoxification system of adult coleoid cephalopods.

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On the functions of the pore cells in the connective tissue of terrestrial pulmonate molluscs

Cited by 28 publications

References 7 publications

Rhogocytes (pore cells) as the site of hemocyanin biosynthesis in the marine gastropod Haliotis tuberculata

Rhogocytes (pore cells) as the site of hemocyanin biosynthesis in the marine gastropod Haliotis tuberculata

3D-Ultrastructure, Functions and Stress Responses of Gastropod (Biomphalaria glabrata) Rhogocytes

Hemocyanin and the branchial heart complex of Sepia officinalis : are the hemocytes involved in hemocyanin metabolism of coleoid cephalopods?

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