The P2×7 receptor is a master regulator of microparticle and mitochondria exchange in mouse microglia

Simonetta Falzoni; Valentina Vultaggio-Poma; Paola Chiozzi; Mario Tarantini; Elena Adinolfi; Paola Boldrini; Anna Lisa Giuliani; Giampaolo Morciano; Yong Tang; Darek Gorecki; Francesco Di Virgilio

doi:10.1093/function/zqae019

The P2×7 receptor is a master regulator of microparticle and mitochondria exchange in mouse microglia

Simonetta Falzoni, Valentina Vultaggio-Poma, Paola Chiozzi, Mario Tarantini, Elena Adinolfi, Paola Boldrini, Anna Lisa Giuliani, Giampaolo Morciano, Yong Tang, Darek Gorecki, Francesco Di Virgilio

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Abstract

Microparticles (MPs) are secreted by all cells where they play a key role in intercellular communication, differentiation, inflammation, and cell energy transfer. P2×7 receptor (P2×7R) activation by extracellular ATP (eATP) causes a large MP release and affects their contents in a cell-specific fashion. We investigated MP release and functional impact in microglial cells from P2×7R-WT or P2×7R-KO mice, as well as mouse microglial cell lines characterized for high (N13-P2×7RHigh) or low (N13-P2×7RLow) P2×7R expression. P2×7R stimulation promoted release of a mixed MP population enriched with naked mitochondria. Released mitochondria were taken up and incorporated into the mitochondrial network of the recipient cells in a P2×7R-dependent fashion. NLRP3 and the P2×7R itself were also delivered to the recipient cells. MP transfer increased the energy level of the recipient cells and conferred a pro-inflammatory phenotype. These data show that the P2×7R is a master regulator of intercellular organelle and MP trafficking in immune cells.

Original language	English
Article number	zqae019
Number of pages	16
Journal	Function
Volume	5
Issue number	4
Early online date	17 Apr 2024
DOIs	https://doi.org/10.1093/function/zqae019
Publication status	Published - 1 Jul 2024

Keywords

P2X7 receptor
microparticles
mitochondria
microglia
inflammation

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10.1093/function/zqae019

The P2X7 Receptor FINALFinal published version, 2.24 MBLicence: CC BY-NC

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title = "The P2×7 receptor is a master regulator of microparticle and mitochondria exchange in mouse microglia",

abstract = "Microparticles (MPs) are secreted by all cells where they play a key role in intercellular communication, differentiation, inflammation, and cell energy transfer. P2×7 receptor (P2×7R) activation by extracellular ATP (eATP) causes a large MP release and affects their contents in a cell-specific fashion. We investigated MP release and functional impact in microglial cells from P2×7R-WT or P2×7R-KO mice, as well as mouse microglial cell lines characterized for high (N13-P2×7RHigh) or low (N13-P2×7RLow) P2×7R expression. P2×7R stimulation promoted release of a mixed MP population enriched with naked mitochondria. Released mitochondria were taken up and incorporated into the mitochondrial network of the recipient cells in a P2×7R-dependent fashion. NLRP3 and the P2×7R itself were also delivered to the recipient cells. MP transfer increased the energy level of the recipient cells and conferred a pro-inflammatory phenotype. These data show that the P2×7R is a master regulator of intercellular organelle and MP trafficking in immune cells.",

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author = "Simonetta Falzoni and Valentina Vultaggio-Poma and Paola Chiozzi and Mario Tarantini and Elena Adinolfi and Paola Boldrini and Giuliani, {Anna Lisa} and Giampaolo Morciano and Yong Tang and Darek Gorecki and {Di Virgilio}, Francesco",

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AU - Falzoni, Simonetta

AU - Vultaggio-Poma, Valentina

AU - Chiozzi, Paola

AU - Tarantini, Mario

AU - Adinolfi, Elena

AU - Boldrini, Paola

AU - Giuliani, Anna Lisa

AU - Morciano, Giampaolo

AU - Tang, Yong

AU - Gorecki, Darek

AU - Di Virgilio, Francesco

PY - 2024/7/1

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N2 - Microparticles (MPs) are secreted by all cells where they play a key role in intercellular communication, differentiation, inflammation, and cell energy transfer. P2×7 receptor (P2×7R) activation by extracellular ATP (eATP) causes a large MP release and affects their contents in a cell-specific fashion. We investigated MP release and functional impact in microglial cells from P2×7R-WT or P2×7R-KO mice, as well as mouse microglial cell lines characterized for high (N13-P2×7RHigh) or low (N13-P2×7RLow) P2×7R expression. P2×7R stimulation promoted release of a mixed MP population enriched with naked mitochondria. Released mitochondria were taken up and incorporated into the mitochondrial network of the recipient cells in a P2×7R-dependent fashion. NLRP3 and the P2×7R itself were also delivered to the recipient cells. MP transfer increased the energy level of the recipient cells and conferred a pro-inflammatory phenotype. These data show that the P2×7R is a master regulator of intercellular organelle and MP trafficking in immune cells.

AB - Microparticles (MPs) are secreted by all cells where they play a key role in intercellular communication, differentiation, inflammation, and cell energy transfer. P2×7 receptor (P2×7R) activation by extracellular ATP (eATP) causes a large MP release and affects their contents in a cell-specific fashion. We investigated MP release and functional impact in microglial cells from P2×7R-WT or P2×7R-KO mice, as well as mouse microglial cell lines characterized for high (N13-P2×7RHigh) or low (N13-P2×7RLow) P2×7R expression. P2×7R stimulation promoted release of a mixed MP population enriched with naked mitochondria. Released mitochondria were taken up and incorporated into the mitochondrial network of the recipient cells in a P2×7R-dependent fashion. NLRP3 and the P2×7R itself were also delivered to the recipient cells. MP transfer increased the energy level of the recipient cells and conferred a pro-inflammatory phenotype. These data show that the P2×7R is a master regulator of intercellular organelle and MP trafficking in immune cells.

KW - P2X7 receptor

KW - microparticles

KW - mitochondria

KW - microglia

KW - inflammation

U2 - 10.1093/function/zqae019

DO - 10.1093/function/zqae019

M3 - Article

VL - 5

JO - Function

JF - Function

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M1 - zqae019

ER -

The P2×7 receptor is a master regulator of microparticle and mitochondria exchange in mouse microglia

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Keywords

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