Granule matrix property and rapid “kiss-and-run” exocytosis contribute to the different kinetics of catecholamine release from carotid glomus and adrenal chromaffin cells at matched quantal size

• Published in: Canadian journal of physiology and pharmacology 2012-06, Vol.90 (6), p.791-801
• Main Authors: NAN WANG, LEE, Andy K, LEI YAN, SIMPSON, Michael R, TSE, Amy, TSE, Frederick W
• Format: Article
• Language: English
• Subjects: Adrenal Glands - metabolism; Adrenal Glands - physiology; amperometry; ampérométrie; Animals; Biological and medical sciences; Calcium; Calcium (intracellular); Calcium - metabolism; carbon fibre electrode; Carotid body; Catecholamines; Catecholamines - metabolism; Cells; cellule chromaffine; Chemoreception; chromaffin cell; Chromaffin cells; Chromaffin Cells - metabolism; Chromaffin Cells - physiology; Chromaffin Granules - metabolism; Chromaffin Granules - physiology; Comparative analysis; corps carotidien; Data processing; dense core granule; Dialysis; exocytose; Exocytosis; Exocytosis - physiology; Fundamental and applied biological sciences. Psychology; fusion pore; Glomus; Glomus cells; granule matrix; granule à cœur dense; Granules; Health aspects; Kinetics; Male; matrice du granule; Membrane fusion; Neurons; Osmolar Concentration; osmolarity; osmolarité; Pharmacokinetics; Physiological aspects; pore de fusion; Rats; Rats, Sprague-Dawley; Vertebrates: anatomy and physiology, studies on body, several organs or systems; électrode à fibre de carbone
• ISSN: 0008-4212; 1205-7541
• DOI: 10.1139/y2012-040

Catecholamine-containing small dense core granules (SDCGs, vesicular diameter of ∼100 nm) are prominent in carotid glomus (chemosensory) cells and some neurons, but the release kinetics from individual SDCGs has not been studied in detail. In this study, we compared the amperometric signals from glomus cells with those from adrenal chromaffin cells, which also secrete catecholamine but via large dense core granules (LDCGs, vesicular diameter of ∼200–250 nm). When exocytosis was triggered by whole-cell dialysis (which raised the concentration of intracellular Ca 2+ ([Ca 2+ ] i ) to ∼0.5 µmol/L), the proportion of the type of signal that represents a flickering fusion pore was 9-fold higher for glomus cells. Yet, at the same range of quantal size (Q, the total amount of catecholamine that can be released from a granule), the kinetics of every phase of the amperometric spike signals from glomus cells was faster. Our data indicate that the last phenomenon involved at least 2 mechanisms: (i) the granule matrix of glomus cells can supply a higher concentration of free catecholamine during exocytosis; (ii) a modest elevation of [Ca 2+ ] i triggers a form of rapid “kiss-and-run” exocytosis, which is very prevalent among glomus SDCGs and leads to incomplete release of their catecholamine content (and underestimation of their Q value).