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Cells 2018, 7(12), 276; https://doi.org/10.3390/cells7120276

Gi Protein Modulation of the Potassium Channel TASK-2 Mediates Vesicle Osmotic Swelling to Facilitate the Fusion of Aquaporin-2 Water Channel Containing Vesicles

1
Department of Biosciences, Biotechnologies and Biopharmaceutics, University of Bari Aldo Moro, Bari 70125, Italy
2
Physics Department, University of Calabria, Rende 87036, Italy
3
Department of Chemistry and Chemical Technologies, University of Calabria, Rende 87036, Italy
4
Department of Biology, University of Bari Aldo Moro, Bari 70125, Italy
5
Institute of Nanotechnology-CNR (CNR-Nanotec), Cosenza Unit, Rende 87036, Italy
6
Sistema Tecnologico MaTeRIA, University of Calabria, Rende 87036, Italy
7
Interuniversitary Consortium “Istituto Nazionale Biostrutture e Biosistemi” (INBB), Rome 00136, Italy
8
Center of Excellence in Comparative Genomics (CEGBA), University of Bari Aldo Moro, Bari 70125, Italy
These authors contributed equally to this work.
*
Authors to whom correspondence should be addressed.
Received: 4 September 2018 / Revised: 13 December 2018 / Accepted: 13 December 2018 / Published: 19 December 2018
(This article belongs to the Special Issue Aquaporins)
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Abstract

Vesicle fusion is a fundamental cell biological process similar from yeasts to humans. For secretory vesicles, swelling is considered a step required for the expulsion of intravesicular content. Here this concept is revisited providing evidence that it may instead represent a general mechanism. We report the first example that non-secretory vesicles, committed to insert the Aquaporin-2 water channel into the plasma membrane, swell and this phenomenon is required for fusion to plasma membrane. Through an interdisciplinary approach, using atomic force microscope (AFM), a fluorescence-based assay of vesicle volume changes and NMR spectroscopy to measure water self-diffusion coefficient, we provide evidence that Gi protein modulation of potassium channel TASK-2 localized in AQP2 vesicles, is required for vesicle swelling. Estimated intravesicular K+ concentration in AQP2 vesicles, as measured by inductively coupled plasma mass spectrometry, was 5.3 mM, demonstrating the existence of an inwardly K+ chemical gradient likely generating an osmotic gradient causing vesicle swelling upon TASK-2 gating. Of note, abrogation of K+ gradient significantly impaired fusion between vesicles and plasma membrane. We conclude that vesicle swelling is a potentially important prerequisite for vesicle fusion to the plasma membrane and may be required also for other non-secretory vesicles, depicting a general mechanism for vesicle fusion. View Full-Text
Keywords: Gi protein; TASK-2; Aquaporin-2; exocytosis; swelling Gi protein; TASK-2; Aquaporin-2; exocytosis; swelling
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Centrone, M.; De Santo, M.P.; Nicotera, I.; Labate, C.; Ranieri, M.; Di Mise, A.; Mola, M.G.; Mastrodonato, M.; Elliani, R.; Barberi, R.; Formoso, V.; Tamma, G.; Valenti, G. Gi Protein Modulation of the Potassium Channel TASK-2 Mediates Vesicle Osmotic Swelling to Facilitate the Fusion of Aquaporin-2 Water Channel Containing Vesicles. Cells 2018, 7, 276.

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