Nanoscale Amperometry Reveals that Only a Fraction of Vesicular Serotonin Content is Released During Exocytosis from Beta Cells

Amir Hatamie; Lin Ren; Haiqiang Dou; Nikhil R. Gandasi; Patrik Rorsman; Andrew Ewing

doi:10.1002/anie.202015902

Nanoscale Amperometry Reveals that Only a Fraction of Vesicular Serotonin Content is Released During Exocytosis from Beta Cells

Amir Hatamie, Lin Ren, Haiqiang Dou, Nikhil R. Gandasi, Patrik Rorsman, Andrew Ewing

Research output: Contribution to journal › Article › peer-review

29 Citations (Scopus)

108 Downloads (Pure)

Abstract

Recent work has shown that chemical release during the fundamental cellular process of exocytosis in model cell lines is not all-or-none. We tested this theory for vesicular release from single pancreatic beta cells. The vesicles in these cells release insulin, but also serotonin, which is detectible with amperometric methods. Traditionally, it is assumed that exocytosis in beta cells is all-or-none. Here, we use a multidisciplinary approach involving nanoscale amperometric chemical methods to explore the chemical nature of insulin exocytosis. We amperometrically quantified the number of serotonin molecules stored inside of individual nanoscale vesicles (39 317±1611) in the cell cytoplasm before exocytosis and the number of serotonin molecules released from single cells (13 310±1127) for each stimulated exocytosis event. Thus, beta cells release only one-third of their granule content, clearly supporting partial release in this system. We discuss these observations in the context of type-2 diabetes.

Original language	English
Pages (from-to)	7593-7596
Number of pages	4
Journal	Angewandte Chemie - International Edition
Volume	60
Issue number	14
Early online date	19 Dec 2020
DOIs	https://doi.org/10.1002/anie.202015902
Publication status	Published (in print/issue) - 29 Mar 2021

Bibliographical note

Funding Information:
We acknowledge funding from the European Research Council (Advanced Grant), the Knut and Alice Wallenberg Foundation, the Swedish Research Council (VR). AH acknowledges funding from Sweden's Innovation Agency (Vinnova) and the Swedish Strategy Group for EU‐coordination. Also, AH thanks Alicia Lork for critical comments on the manuscript. NRG was supported by the European Foundation for the Study of Diabetes‐Rising Star Program and Novo Nordisk Foundation‐Young Investigator Program.

Publisher Copyright:
© 2020 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH

Keywords

beta cells
electrochemical analysis
exocytosis
nanoelectrodes
partial release

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1002/anie.202015902

anie.202015902Final published version, 835 KBLicence: CC BY-NC-ND

Cite this

@article{4dd4d4423d5b4ee892a641454de675a4,

title = "Nanoscale Amperometry Reveals that Only a Fraction of Vesicular Serotonin Content is Released During Exocytosis from Beta Cells",

abstract = "Recent work has shown that chemical release during the fundamental cellular process of exocytosis in model cell lines is not all-or-none. We tested this theory for vesicular release from single pancreatic beta cells. The vesicles in these cells release insulin, but also serotonin, which is detectible with amperometric methods. Traditionally, it is assumed that exocytosis in beta cells is all-or-none. Here, we use a multidisciplinary approach involving nanoscale amperometric chemical methods to explore the chemical nature of insulin exocytosis. We amperometrically quantified the number of serotonin molecules stored inside of individual nanoscale vesicles (39 317±1611) in the cell cytoplasm before exocytosis and the number of serotonin molecules released from single cells (13 310±1127) for each stimulated exocytosis event. Thus, beta cells release only one-third of their granule content, clearly supporting partial release in this system. We discuss these observations in the context of type-2 diabetes.",

keywords = "beta cells, electrochemical analysis, exocytosis, nanoelectrodes, partial release",

author = "Amir Hatamie and Lin Ren and Haiqiang Dou and Gandasi, {Nikhil R.} and Patrik Rorsman and Andrew Ewing",

note = "Funding Information: We acknowledge funding from the European Research Council (Advanced Grant), the Knut and Alice Wallenberg Foundation, the Swedish Research Council (VR). AH acknowledges funding from Sweden's Innovation Agency (Vinnova) and the Swedish Strategy Group for EU‐coordination. Also, AH thanks Alicia Lork for critical comments on the manuscript. NRG was supported by the European Foundation for the Study of Diabetes‐Rising Star Program and Novo Nordisk Foundation‐Young Investigator Program. Publisher Copyright: {\textcopyright} 2020 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH",

year = "2021",

month = mar,

day = "29",

doi = "10.1002/anie.202015902",

language = "English",

volume = "60",

pages = "7593--7596",

journal = "Angewandte Chemie - International Edition",

issn = "1433-7851",

publisher = "John Wiley & Sons, Inc.",

number = "14",

}

TY - JOUR

T1 - Nanoscale Amperometry Reveals that Only a Fraction of Vesicular Serotonin Content is Released During Exocytosis from Beta Cells

AU - Hatamie, Amir

AU - Ren, Lin

AU - Dou, Haiqiang

AU - Gandasi, Nikhil R.

AU - Rorsman, Patrik

AU - Ewing, Andrew

N1 - Funding Information: We acknowledge funding from the European Research Council (Advanced Grant), the Knut and Alice Wallenberg Foundation, the Swedish Research Council (VR). AH acknowledges funding from Sweden's Innovation Agency (Vinnova) and the Swedish Strategy Group for EU‐coordination. Also, AH thanks Alicia Lork for critical comments on the manuscript. NRG was supported by the European Foundation for the Study of Diabetes‐Rising Star Program and Novo Nordisk Foundation‐Young Investigator Program. Publisher Copyright: © 2020 The Authors. Angewandte Chemie International Edition published by Wiley-VCH GmbH

PY - 2021/3/29

Y1 - 2021/3/29

N2 - Recent work has shown that chemical release during the fundamental cellular process of exocytosis in model cell lines is not all-or-none. We tested this theory for vesicular release from single pancreatic beta cells. The vesicles in these cells release insulin, but also serotonin, which is detectible with amperometric methods. Traditionally, it is assumed that exocytosis in beta cells is all-or-none. Here, we use a multidisciplinary approach involving nanoscale amperometric chemical methods to explore the chemical nature of insulin exocytosis. We amperometrically quantified the number of serotonin molecules stored inside of individual nanoscale vesicles (39 317±1611) in the cell cytoplasm before exocytosis and the number of serotonin molecules released from single cells (13 310±1127) for each stimulated exocytosis event. Thus, beta cells release only one-third of their granule content, clearly supporting partial release in this system. We discuss these observations in the context of type-2 diabetes.

AB - Recent work has shown that chemical release during the fundamental cellular process of exocytosis in model cell lines is not all-or-none. We tested this theory for vesicular release from single pancreatic beta cells. The vesicles in these cells release insulin, but also serotonin, which is detectible with amperometric methods. Traditionally, it is assumed that exocytosis in beta cells is all-or-none. Here, we use a multidisciplinary approach involving nanoscale amperometric chemical methods to explore the chemical nature of insulin exocytosis. We amperometrically quantified the number of serotonin molecules stored inside of individual nanoscale vesicles (39 317±1611) in the cell cytoplasm before exocytosis and the number of serotonin molecules released from single cells (13 310±1127) for each stimulated exocytosis event. Thus, beta cells release only one-third of their granule content, clearly supporting partial release in this system. We discuss these observations in the context of type-2 diabetes.

KW - beta cells

KW - electrochemical analysis

KW - exocytosis

KW - nanoelectrodes

KW - partial release

UR - http://www.scopus.com/inward/record.url?scp=85101629109&partnerID=8YFLogxK

U2 - 10.1002/anie.202015902

DO - 10.1002/anie.202015902

M3 - Article

C2 - 33340209

AN - SCOPUS:85101629109

SN - 1433-7851

VL - 60

SP - 7593

EP - 7596

JO - Angewandte Chemie - International Edition

JF - Angewandte Chemie - International Edition

IS - 14

ER -

Nanoscale Amperometry Reveals that Only a Fraction of Vesicular Serotonin Content is Released During Exocytosis from Beta Cells

Abstract

Bibliographical note

Keywords

UN SDGs

Access to Document

Other files and links

Fingerprint

Cite this