The perinuclear space of pancreatic acinar cells and the synthetic pathway of zymogen in Scorpaena scrofa L.: Ultrastructural aspects
Introduction
Cell biology texts commonly bring to readers the notion that the outer or external membrane of the nuclear envelope is part and in continuity with the cell rough endoplasmic reticulum or RER (Palade and Porter, 1954, Watson, 1955, Franke, 1974a, Franke, 1974b). Previous authors have suggested that the RER (Porter, 1961) and the annulate lamellae (Kessel, 1968, Franke, 1974b) could form the outer nuclear membrane (ONM). Alternatively, others have suggested that the nuclear outer membrane contributes to the endoplasmic reticulum (review by Kessel, 1968) or even produces Golgi cisterns (Weston et al., 1972). Previous illustrations have not clearly depicted the perinuclear space to be contributing to the secretory pathway despite old observations of the ONM being studded with ribosomes (Porter et al., 1945, Palade and Porter, 1954).
A serendipitous observation made during a study encompassing a comparative microscopic anatomy of the vertebrate hepato-biliary tract and gallbladder (Gilloteaux et al., 1995, Oldham-Ott and Gilloteaux, 1997) led to this report. Ultrastructural observations of pancreatic tissues attached to the gallbladder of Scorpaena allowed us to find supportive data illustrating that the perinuclear space is a part of the secretory pathway. Incidentally, the acinar cells’ morphology showed two functional cell morphologies. In the first one, the cells demonstrate perinuclear space swellings that burst into small secretory vesicles. Those vesicles are added to a main cytoplasmic pool of the same type made by the RER. These observations suggest the contribution of the perinuclear space to the expression of zymogenic secretory products. The other cell morphology illustrates the characteristic storage of large, apical zymogen vesicles after their production suggesting their ability to be released following an appropriate stimulus by the regulated pathway (Gilloteaux et al., 2007).
Section snippets
Material and methods
Fish Scorpaena scrofa L. (Class Actinopterigii, Family Scorpaenidae) is also known as hog-fish, red scorpionfish or large-scaled scorpionfish. It is omnivorous and it was captured outside the Banyuls Bay (France, Mediterranean gulf of the Lion), by net trailing between 50 and 60 m of depth along a NNW-SSE line facing Cape Béar to Cape of the Abeille (along and outside the nearby National Biological Marine Reserve). Following capture of several specimens, they were placed in running seawater
Results
Gross anatomical aspects of the scorpion fish pancreas shows delicate, branching projections similar to the ones found in mammals. The delicate branches of the organ consist of small lobes spread into a large area of the mesentery and attach to the adventitial tunic of the main body of the gallbladder and the intestine. In this lower vertebrate species, the exocrine pancreatic cells undergoing production of the zymogen vesicles surprisingly show many similar submicroscopic features as those
Discussion
Investigations of the exocrine pancreatic cells led cell biology pioneers to unravel many basic cell structures and functions by applying newly developed techniques (reviews by Hand, 1990, Scheele and Kern, 1993, Motta et al., 1997). Molecular pathways of cell secretion and most of the controlling steps associated with sorting and trafficking of zymogens, sequestered as content of secretory vesicles, have been clarified by many authors, especially by those associated with the group of Palade (
Acknowledgements
Supported by the Thomas R. Kelly M.D. fund, Summa Research Foundation, Akron, OH and the Scholarly Activity Committee of the AUC School of Medicine in St Maarten, N. A. as part of a Medical student research (RK and NY). The staff of the Observatoire Océanologique of Banuyls, France, Université Pierre et Marie Curie (Paris VI) and S. Getch, Communication Services, Summa Health System, Akron, OH, are thanked for technical assistance.
References (110)
The isolation of the envelopes of rat liver nuclei
Biochim. Biophys. Acta
(1972)COPII: a membrane coat that forms endoplasmic reticulum-derived vesicles
FEBS Lett.
(1995)- et al.
COPII: a membrane coat formed by sec proteins that drive vesicle budding from the endoplasmic reticulum
Cell
(1994) Formation of rough endoplasmic reticulum and nuclear membrane in normal and tumour cells
Cell Biol. Int. Rep.
(1986)Dilated cisternae of nuclear envelope and rough endoplasmic reticulum in the proventriculus of Drosophila auraria larvae
Biol. Int. Rep.
(1985)Interactions between endoplasmic reticulum and nuclear membranes of different types of cells during repair f damages amoeba nuclei
Exp. Cell Res.
(1978)Budding events in herpesvirus morphogenesis
Virus Res.
(2004)- et al.
Ultrastructural aspects of cytomegalovirus-infected fibroblastic stromal cells of human bone marrow
Tissue Cell
(1998) - et al.
Lumenal proteins of the mammalian endoplasmic reticulum are required to complete protein translocation
Cell
(1993) - et al.
The degree of coupling of nuclear rotation in binucleate 3T3 cells
Exp. Cell Res.
(1986)
Continuities between outer nuclear membrane and the rough endoplasmic reticulum increase in hippocampal neurons during seizure-induced protein synthesis
Brain Res.
Rotating nuclei in tissue cultures of adult human nasal mucosa
Exp. Cell Res.
The ground substance; observations from electron microscopy
Direct connection between myelinosomes, endoplasmic reticulum and nuclear envelope in mouse hepatocytes grown with the amphiphilic drug, quinacrine
Tissue Cell
Role of the envelope in synthesis, processing, and transport of membrane glycoproteins
J. Biol. Chem.
5 Alpha-reductase type 1 is localized to the outer nuclear membrane
Mol. Cell Endocrinol.
Studies on the guinea pig pancreas
J. Biol Chem.
Ultrastructure of the exocrine pancreas in the snake Waglerophis merremii (Wagler)
Ann. Anat.
Reconstitution of transport of vesicular stomatitis virus G protein from the endoplasmic reticulum to the Golgi complex using a cell-free system
J. Cell Biol.
Three-dimensional ultrastructure of the ring stage of Plasmodium falciparum: evidence for export pathways
Microsc. Microanal.
The organization of endoplasmic reticulum export complexes
J. Cell Biol.
Possible patterns of nuclear rotation in binucleate hepatocytes in vivo: static examination with fluorescence and electron microscopy
In Vivo
Proliferation of endoplasmic reticulum and formation with its enzyme, UDP-gluronyl-transferase in chick embryo liver during culture. Effect of phenobarbital
J. Cell Biol.
Immunoelectron microscopic studies of the intracellular transport of the membrane glycoprotein (G) of vesicular stomatitis virus in infected Chinese hamster ovary cells
J. Cell Biol.
Cell death. Triangle-Sandoz
J. Med. Sci.
Intracellular protein topogenesis
Proc. Natl. Acad. Sci. U.S.A.
Transfer of proteins across membranes. I. Presence of proteolyticaly processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma
J. Cell Biol.
Transfer of proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components
J. Cell Biol.
Intracellular protein topogenesis
Prog. Clin. Biol. Res.
Selective packaging of cargo molecules into endoplasmic reticulum-derived COPII vesicles
Proc. Natl. Acad. Sci. U.S.A.
Protein synthesis, storage, and discharge in the pancreatic exocrine cell
J. Cell Biol.
Unusual features of the nuclear envelope in human spermatogenic cells
Anat. Rec.
The ŋ isoform of protein kinase C is localized on rough endoplasmic reticulum
Mol. Cell. Biol.
Coupling of the nuclear and cytoplasm: role of the LINC complex
J. Cell Biol.
A Guided Tour of the Living Cell
Fine structure of the nuclear envelope of carcinoma cells
Nature
Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis
J. Cell Biol.
The fine structural organization of Rous tumour cells
J. Biophys. Biochem. Cytol.
Progress in unraveling pathways of Golgi traffic
Annu. Rev. Cell Biol.
The role of endoplasmic reticulum in the repair of amoeba nuclear envelopes damaged microsurgically
J. Cell Sci.
Nuclear envelopes. Structure and biochemistry of the nuclear envelope
Phil. Trans. R. Soc. Lond. B
Structure, biochemistry, and functions of the nuclear envelope
Int. Rev. Cytol. Suppl.
Pathways of nucleocytoplasmic translocation of ribonucleoproteins
Symp. Soc. Exp. Biol.
Ribosome substructure investigated by scanning force microscopy and image processing
J. Microsc.
Fibroblastic stromal cells of human bone marrow infected by cytomegalovirus
J. Submicrosc. Cytol. Pathol.
The biliary tract and the gallbladder morphologic diversity in fishes
Egress of Alphaherpesviruses: comparative ultrastructural study
J. Virol.
Cited by (17)
Effects of dietary arginine levels on intestinal morphology, digestive enzyme activity, antioxidant capacity and intestinal flora of hybrid snakehead(Channa maculata ♀×Channa argus ♂)
2022, Aquaculture ReportsCitation Excerpt :Growth performance is closely related to digestive and absorptive abilities in fish (Chen et al., 2012; Zhao et al., 2019). Proteases, lipases and amylases are the most common digestive enzymes found in the intestines, which are correlated with growth and intestinal development (Gilloteaux et al., 2008). Na+K+ -ATPase regulates the osmotic pressure inside and outside the cell, as well as the flow of glucose, amino acids, and other substances into the cell (Suhail, 2010).
Effects of dietary pantothenic acid on growth, antioxidant ability and innate immune response in juvenile black carp
2022, Aquaculture ReportsCitation Excerpt :Digestion of nutrients depends on the activities of digestive enzymes, which are responsible for breaking down and assimilating feed constituents (Klein et al., 2006; Debnath and Saikia, 2021). As the main digestive organ, the intestine contains several digestive enzymes, including α-amylase, trypsin, chymotrypsin and lipase (Zambonino Infante and Cahu, 2001; German et al., 2004; Gawlicka and Horn, 2006; Gilloteaux et al., 2008). In the current work, the latter enzymes showed enhanced activities with increasing dietary PA levels (Table 4), which indicated that dietary PA is important for improving the intestine’s digestive abilities in black carp.