Human neutrophils communicate remotely via calcium-dependent glutamate-induced glutamate release

Olga Kopach; Sergyi Sylantyev; Lucie Bard; Piotr Michaluk; Janosch P. Heller; Ana Gutierrez del Arroyo; Gareth L. Ackland; Alexander V. Gourine; Dmitri A. Rusakov

doi:10.1016/j.isci.2023.107236

Human neutrophils communicate remotely via calcium-dependent glutamate-induced glutamate release

Olga Kopach^*, Sergyi Sylantyev^*, Lucie Bard, Piotr Michaluk, Janosch P. Heller, Ana Gutierrez del Arroyo, Gareth L. Ackland, Alexander V. Gourine, Dmitri A. Rusakov^*

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

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

2 Downloads (Pure)

Abstract

Neutrophils are white blood cells that are critical to acute inflammatory and adaptive immune responses. Their swarming-pattern behavior is controlled by multiple cellular cascades involving calcium-dependent release of various signaling molecules. Previous studies have reported that neutrophils express glutamate receptors and can release glutamate but evidence of direct neutrophil-neutrophil communication has been elusive. Here, we hold semi-suspended cultured human neutrophils in patch-clamp whole-cell mode to find that calcium mobilization induced by stimulating one neutrophil can trigger an N-methyl-D-aspartate (NMDA) receptor-driven membrane current and calcium signal in neighboring neutrophils. We employ an enzymatic-based imaging assay to image, in real time, glutamate release from neutrophils induced by glutamate released from their neighbors. These observations provide direct evidence for a positive-feedback inter-neutrophil communication that could contribute to mechanisms regulating communal neutrophil behavior.

Original language	English
Article number	107236
Journal	iScience
Volume	26
Issue number	7
Early online date	12 Jul 2023
DOIs	https://doi.org/10.1016/j.isci.2023.107236
Publication status	Published - 21 Jul 2023

Bibliographical note

Funding Information:
Wellcome Trust Principal Fellowship ( 212251_Z_18_Z ), MRC Research Grant ( MR/W019752/1 ), NC3Rs Research Grant ( NC/X001067/1 ), and ERC Advanced Grant ( 323113 ) to D.A.R.

Publisher Copyright:
© 2023 The Authors

Data Availability Statement

•
Data reported in this paper will be shared by the lead contact upon request.

•
This manuscript contains no original programming code.

•
Any additional information required to reanalyse the data reported in this paper is available from the lead upon request.

Keywords

biological sciences
cell biology
immunology
molecular biology
neuroscience

Access to Document

10.1016/j.isci.2023.107236

Kopach_etal_IS_Human_Neutrophils_Communicated_VOR
iScience 26, 107236, July 21, 2023 ª 2023 The Authors. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Final published version, 3.59 MBLicence: CC BY

Cite this

@article{c533805aa6ce41f684118cbda3127e1b,

title = "Human neutrophils communicate remotely via calcium-dependent glutamate-induced glutamate release",

abstract = "Neutrophils are white blood cells that are critical to acute inflammatory and adaptive immune responses. Their swarming-pattern behavior is controlled by multiple cellular cascades involving calcium-dependent release of various signaling molecules. Previous studies have reported that neutrophils express glutamate receptors and can release glutamate but evidence of direct neutrophil-neutrophil communication has been elusive. Here, we hold semi-suspended cultured human neutrophils in patch-clamp whole-cell mode to find that calcium mobilization induced by stimulating one neutrophil can trigger an N-methyl-D-aspartate (NMDA) receptor-driven membrane current and calcium signal in neighboring neutrophils. We employ an enzymatic-based imaging assay to image, in real time, glutamate release from neutrophils induced by glutamate released from their neighbors. These observations provide direct evidence for a positive-feedback inter-neutrophil communication that could contribute to mechanisms regulating communal neutrophil behavior.",

keywords = "biological sciences, cell biology, immunology, molecular biology, neuroscience",

author = "Olga Kopach and Sergyi Sylantyev and Lucie Bard and Piotr Michaluk and Heller, {Janosch P.} and {Gutierrez del Arroyo}, Ana and Ackland, {Gareth L.} and Gourine, {Alexander V.} and Rusakov, {Dmitri A.}",

note = "Funding Information: Wellcome Trust Principal Fellowship ( 212251_Z_18_Z ), MRC Research Grant ( MR/W019752/1 ), NC3Rs Research Grant ( NC/X001067/1 ), and ERC Advanced Grant ( 323113 ) to D.A.R. Publisher Copyright: {\textcopyright} 2023 The Authors",

year = "2023",

month = jul,

day = "21",

doi = "10.1016/j.isci.2023.107236",

language = "English",

volume = "26",

journal = "iScience",

issn = "2589-0042",

publisher = "Elsevier Inc.",

number = "7",

}

TY - JOUR

T1 - Human neutrophils communicate remotely via calcium-dependent glutamate-induced glutamate release

AU - Kopach, Olga

AU - Sylantyev, Sergyi

AU - Bard, Lucie

AU - Michaluk, Piotr

AU - Heller, Janosch P.

AU - Gutierrez del Arroyo, Ana

AU - Ackland, Gareth L.

AU - Gourine, Alexander V.

AU - Rusakov, Dmitri A.

N1 - Funding Information: Wellcome Trust Principal Fellowship ( 212251_Z_18_Z ), MRC Research Grant ( MR/W019752/1 ), NC3Rs Research Grant ( NC/X001067/1 ), and ERC Advanced Grant ( 323113 ) to D.A.R. Publisher Copyright: © 2023 The Authors

PY - 2023/7/21

Y1 - 2023/7/21

N2 - Neutrophils are white blood cells that are critical to acute inflammatory and adaptive immune responses. Their swarming-pattern behavior is controlled by multiple cellular cascades involving calcium-dependent release of various signaling molecules. Previous studies have reported that neutrophils express glutamate receptors and can release glutamate but evidence of direct neutrophil-neutrophil communication has been elusive. Here, we hold semi-suspended cultured human neutrophils in patch-clamp whole-cell mode to find that calcium mobilization induced by stimulating one neutrophil can trigger an N-methyl-D-aspartate (NMDA) receptor-driven membrane current and calcium signal in neighboring neutrophils. We employ an enzymatic-based imaging assay to image, in real time, glutamate release from neutrophils induced by glutamate released from their neighbors. These observations provide direct evidence for a positive-feedback inter-neutrophil communication that could contribute to mechanisms regulating communal neutrophil behavior.

AB - Neutrophils are white blood cells that are critical to acute inflammatory and adaptive immune responses. Their swarming-pattern behavior is controlled by multiple cellular cascades involving calcium-dependent release of various signaling molecules. Previous studies have reported that neutrophils express glutamate receptors and can release glutamate but evidence of direct neutrophil-neutrophil communication has been elusive. Here, we hold semi-suspended cultured human neutrophils in patch-clamp whole-cell mode to find that calcium mobilization induced by stimulating one neutrophil can trigger an N-methyl-D-aspartate (NMDA) receptor-driven membrane current and calcium signal in neighboring neutrophils. We employ an enzymatic-based imaging assay to image, in real time, glutamate release from neutrophils induced by glutamate released from their neighbors. These observations provide direct evidence for a positive-feedback inter-neutrophil communication that could contribute to mechanisms regulating communal neutrophil behavior.

KW - biological sciences

KW - cell biology

KW - immunology

KW - molecular biology

KW - neuroscience

UR - http://www.scopus.com/inward/record.url?scp=85165080516&partnerID=8YFLogxK

U2 - 10.1016/j.isci.2023.107236

DO - 10.1016/j.isci.2023.107236

M3 - Article

AN - SCOPUS:85165080516

SN - 2589-0042

VL - 26

JO - iScience

JF - iScience

IS - 7

M1 - 107236

ER -

Human neutrophils communicate remotely via calcium-dependent glutamate-induced glutamate release

Abstract

Bibliographical note

Data Availability Statement

Keywords

Access to Document

Other files and links

Fingerprint

Cite this