3D-ultrastructure, functions and stress responses of gastropod (Biomphalaria glabrata) rhogocytes.

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",...

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Autores principales: Maria Kokkinopoulou, M Alptekin Güler, Bernhard Lieb, Mike Barbeck, Shahram Ghanaati, Jürgen Markl
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spelling oai:doaj.org-article:e51f1bc639ed44d4929a7746a960d14b2021-11-11T08:21:10Z3D-ultrastructure, functions and stress responses of gastropod (Biomphalaria glabrata) rhogocytes.1932-620310.1371/journal.pone.0101078https://doaj.org/article/e51f1bc639ed44d4929a7746a960d14b2014-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24971744/?tool=EBIhttps://doaj.org/toc/1932-6203Rhogocytes 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.Maria KokkinopoulouM Alptekin GülerBernhard LiebMike BarbeckShahram GhanaatiJürgen MarklPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 9, Iss 6, p e101078 (2014)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Maria Kokkinopoulou
M Alptekin Güler
Bernhard Lieb
Mike Barbeck
Shahram Ghanaati
Jürgen Markl
3D-ultrastructure, functions and stress responses of gastropod (Biomphalaria glabrata) rhogocytes.
description 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.
format article
author Maria Kokkinopoulou
M Alptekin Güler
Bernhard Lieb
Mike Barbeck
Shahram Ghanaati
Jürgen Markl
author_facet Maria Kokkinopoulou
M Alptekin Güler
Bernhard Lieb
Mike Barbeck
Shahram Ghanaati
Jürgen Markl
author_sort Maria Kokkinopoulou
title 3D-ultrastructure, functions and stress responses of gastropod (Biomphalaria glabrata) rhogocytes.
title_short 3D-ultrastructure, functions and stress responses of gastropod (Biomphalaria glabrata) rhogocytes.
title_full 3D-ultrastructure, functions and stress responses of gastropod (Biomphalaria glabrata) rhogocytes.
title_fullStr 3D-ultrastructure, functions and stress responses of gastropod (Biomphalaria glabrata) rhogocytes.
title_full_unstemmed 3D-ultrastructure, functions and stress responses of gastropod (Biomphalaria glabrata) rhogocytes.
title_sort 3d-ultrastructure, functions and stress responses of gastropod (biomphalaria glabrata) rhogocytes.
publisher Public Library of Science (PLoS)
publishDate 2014
url https://doaj.org/article/e51f1bc639ed44d4929a7746a960d14b
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