Electron Microscopic Evidence for Multiple Types of Secretory Vesicles in Bovine Chromaffin Cells

Koval, L. M.; Yavorskaya, E. N.; Lukyanetz, E. A.

doi:10.1006/gcen.2000.7592

Cited by 29 publications

(41 citation statements)

References 71 publications

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“…Although artefactual events related to tissue fixation or osmication have been implicated in the ultrastructural morphology of chromaffin granules, interestingly, it has also been suggested that these findings may reflect granule function (Coupland 1965a, b). Evagination and budding of granule profiles, like those described by us in the present paper, have not been explicitly reported in the literature although some previously published pictures would suggest similar findings (Coupland 1965b;Rhodin 1975;Koval et al 2001). Of course, one should always take into account the possible influence of the method used in the formation of such pictures.…”

Section: Discussionsupporting

confidence: 67%

“…According to our ultrastructural evidence, this vesicle derives from chromaffin granules by a mechanism of evagination and detachment of the perigranular membrane coupled with removal of small packets of chromaffin substance. Interestingly, small dense-core vesicles have already been recognized in bovine chromaffin cells and, what is most remarkable, it has been proposed that such vesicles could originate from chromaffin granules by a budding process (Koval et al 2001).…”

Section: Discussionmentioning

confidence: 99%

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Fine ultrastructure of chromaffin granules in rat adrenal medulla indicative of a vesicle-mediated secretory process

et al. 2005

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Observation by transmission electron microscopy, coupled with morphometric analysis and estimation procedure, revealed unique ultrastructural features in 25.94% of noradrenaline (NA)-containing granules and 16.85% of adrenaline (A)-containing granules in the rat adrenal medulla. These consisted of evaginations of the granule limiting membrane to form budding structures having different morphology and extension. In 14.8% of NA granules and 12.0% of A granules, outpouches were relatively short, looked like small blebs emerging from the granule surface and generally contained electron-dense material. A proportion of 11.2% of NA granules and 4.9% of A granules revealed the most striking ultrastructural features. These secretory organelles presented thin, elongated, tail-like or stem-like appendages, which were variably filled by chromaffin substance and terminated with spherical expansions of different electron density. A cohort of vesicles of variable size (30-150 nm in diameter) and content was found either close to them or in the intergranular cytosol. Examination of adrenal medullary cells fixed by zinc iodide-osmium tetroxide (ZIO) revealed fine electron dense precipitates in chromaffin granules, budding structures as well as cytoplasmic vesicles. These data indicate that a common constituent is revealed by the ZIO histochemical reaction in chromaffin cells. As catecholic compounds are the main tissue targets of ZIO complexes, catecholamines are good candidates to be responsible for the observed ZIO reactivity. This study adds further to the hypothesis that release of secretory material from chromaffin granules may be accomplished by a vesiclular transport mechanism typical of piecemeal degranulation.

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Section: Discussionsupporting

confidence: 67%

Section: Discussionmentioning

confidence: 99%

Fine ultrastructure of chromaffin granules in rat adrenal medulla indicative of a vesicle-mediated secretory process

et al. 2005

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“…In addition, their limiting membranes express specific proteins, such as the vesicle receptor (vSNARE) VAMP2 (Dannies 1999;Burgoyne and Morgan 2003), which plays a key role in regulated exocytosis, and the Ca ++ sensor synaptotagmin I and II (Shin et al 2002). Hence a unifying concept including both LDCV and endocrine granules has been developed, and these structures are now often comprehensively referred to as large dense-core granules, irrespective of whether they are located in neurons or neuro-endocrine cells (Ho¨cker et al 1999;Kasai 1999;Koval et al 2001;Malosio et al 2004). Like LDCV, endocrine granules have been claimed to extrude their secretory content by exocytosis (Aunis 1998;Kasai 1999) but recently a particulate pattern of cell degranulation, called piecemeal degranulation (PMD), has been recognized in adrenal chromaffin cells and in endocrine cells of the gastro-intestinal epithelia (Crivellato et al 2002(Crivellato et al , 2003b(Crivellato et al , 2004(Crivellato et al , 2005).…”

Section: Introductionmentioning

confidence: 99%

Ultrastructural evidence of piecemeal degranulation in large dense-core vesicles of brain neurons

Crivellato

Nico

2005

Anat Embryol

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Large dense-core vesicles (LDCV) are a group of neuronal secretory organelles with different size and characteristically condensed morphology. LDCV release their specific cargo by regulated exocytosis, either in the form of "full fusion" or "kiss-and-run" exocytosis. In this paper, we provide ultrastructural evidence indicative of a slow and particulate mode of secretion from LDCV, called piecemeal degranulation (PMD). A number of LDCV in the nerve boutons of mouse brain presented marked increase in their size accompanied by reduction and also disappearance of content material. Residual secretory constituents in altered LDCV displayed eroded marginated patterns, leading to eccentric "haloed" morphologies. Remarkably, altered LDCV never appeared to be fused with each other or with the nerve plasma membrane. Very small vesicles, empty or apparently loaded with the same material making-up the LDCV content, could be seen near or attached to LDCV and the plasma membrane. First described in basophils, mast cells and eosinophils, PMD has recently been recognized in various neuro-endocrine cells, like adrenal chromaffin cells and endocrine cells of the gastro-intestinal epithelia. Here we suggest that PMD may be a hitherto unrecognized pathway of neuron secretion. It would represent the morphological correlate of a long-lasting and low-level process of neuro-transmitter release. It extends the patterns of neuron secretion and possibly opens new perspectives in understanding neuron plasticity.

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“…Different endocytic pathways have been described in chromaffin cells: the classical clathrin-dependent mechanism (4,12,25), a rapid endocytosis regulated by Ca 2ϩ and PKC (4,5,11), and an ultrarapid pathway (5). The speed at which secretory vesicles are recovered will depend on the pathway selected by the cell to retrieve its membrane.…”

mentioning

confidence: 99%

Rapid recovery of releasable vesicles and formation of nonreleasable endosomes follow intense exocytosis in chromaffin cells

Bay

Ibáñez²,

Marengo³

2007

American Journal of Physiology-Cell Physiology

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Perez Bay AE, Ibañ ez LI, Marengo FD. Rapid recovery of releasable vesicles and formation of nonreleasable endosomes follow intense exocytosis in chromaffin cells. Am J Physiol Cell Physiol 293: C1509-C1522, 2007. First published August 8, 2007 doi:10.1152/ajpcell.00632.2006.-Neurons and neuroendocrine cells must retrieve plasma membrane excess and refill vesicle pools depleted by exocytosis. To perform these tasks cells can use different endocytosis/recycling mechanisms whose selection will impact on vesicle recycling time and secretion performance. We used FM1-43 to evaluate in the same experiment exocytosis, endocytosis, and recovery of releasable vesicles on mouse chromaffin cells. Various exocytosis levels were induced by a variety of stimuli, and we discriminated the resultant endocytosis-recycling responses according to their ability to rapidly generate releasable vesicles. Exocytosis of Յ20% of plasma membrane (provoked by nicotine/acetylcholine) was followed by total recovery of releasable vesicles. If a stronger stimulus (50 mM K ϩ and 2 mM Ca 2ϩ ) provoking intense exocytosis (51 Ϯ 7%) was applied, endocytosis still retrieved all the fused membrane, but only a fraction (19 Ϯ 2%) was releasable by a second stimulus. Using ADVASEP-7 or bromophenol blue to quickly eliminate fluorescence from noninternalized FM1-43, we determined that this fraction became releasable in Ͻ2 min. The remaining nonreleasable fraction was distributed mainly as fluorescent spots (ϳ0.7 m) selectively labeled by 40-to 70-kDa dextrans and was suppressed by a phosphatidylinositol-3-phosphate kinase inhibitor, suggesting that it had been formed by a bulk retrieval mechanism. We concluded that chromaffin cells can rapidly recycle significant fractions of their total vesicle population, and that this pathway prevails when cholinergic agonists are used as secretagogues. When exocytosis exceeded ϳ20% of plasma membrane, an additional mechanism was activated, which was unable to produce secretory vesicles in our experimental time frame but appeared crucial to maintaining membrane surface homeostasis under extreme conditions. endocytosis; mouse chromaffin cells; calcium signal; FM1-43; ADVASEP-7; bromophenol blue

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Electron Microscopic Evidence for Multiple Types of Secretory Vesicles in Bovine Chromaffin Cells

Cited by 29 publications

References 71 publications

Fine ultrastructure of chromaffin granules in rat adrenal medulla indicative of a vesicle-mediated secretory process

Fine ultrastructure of chromaffin granules in rat adrenal medulla indicative of a vesicle-mediated secretory process

Ultrastructural evidence of piecemeal degranulation in large dense-core vesicles of brain neurons

Rapid recovery of releasable vesicles and formation of nonreleasable endosomes follow intense exocytosis in chromaffin cells

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