Reactive oxygen species regulate M-CSF-induced monocyte/macrophage proliferation through SHP1 oxidation

Han Kyoung Choi; Tae Hee Kim; Gil Ja Jhon; Soo Young Lee

doi:10.1016/j.cellsig.2011.05.017

Reactive oxygen species regulate M-CSF-induced monocyte/macrophage proliferation through SHP1 oxidation

Han Kyoung Choi, Tae Hee Kim, Gil Ja Jhon, Soo Young Lee

Life Sciences

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

25 Scopus citations

Abstract

Macrophage colony-stimulating factor (M-CSF) stimulation results in the production of reactive oxygen species (ROS) that participate in the proliferation of monocyte/macrophage. However, the molecular mechanisms whereby ROS modulate the signaling processes of M-CSF remain poorly defined. We report here that the redox-sensitive Src homology region 2 domain-containing phosphatase 1 (SHP1) is a critical regulator of M-CSF-mediated signaling in bone marrow monocyte/macrophage lineage cells (BMMs). Application of diphenylene iodonium (DPI) inhibited the responses of BMMs to M-CSF, including ROS production, cell proliferation, and phosphorylation of c-Fms as well as Akt kinase, but not of MAP kinases such as ERK, p38, and JNK. Dysregulation of SHP1 by overexpression or RNA interference in BMMs showed that SHP1 specifically regulates PI3 kinase (PI3K)/Akt signaling, but not MAP kinases in a redox-dependent manner, thereby regulating proliferation of BMMs through cyclins D1 and D2. These findings demonstrate that M-CSF-mediated ROS generation leads to SHP1 oxidation, which promotes cell proliferation through the PI3K/Akt-dependent signaling pathway.

Original language	English
Pages (from-to)	1633-1639
Number of pages	7
Journal	Cellular Signalling
Volume	23
Issue number	10
DOIs	https://doi.org/10.1016/j.cellsig.2011.05.017
State	Published - Oct 2011

Bibliographical note

Funding Information:
We thank T. Kitamura for PLAT-E cells and K. Mizuno for pSPORT6-SHP1. This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea Government (MEST) ( R0A-2008-000-20001-0 ; R31-2008-000-10010-0 ; No. 2011–0006244 ; No. 2010–0020577 ). H.C. was supported by the second stage of the Brain Korea 21 Project.

Keywords

M-CSF
Monocyte/macrophage
Oxidation
PI3K/Akt signaling
Proliferation
SHP1

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10.1016/j.cellsig.2011.05.017

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title = "Reactive oxygen species regulate M-CSF-induced monocyte/macrophage proliferation through SHP1 oxidation",

abstract = "Macrophage colony-stimulating factor (M-CSF) stimulation results in the production of reactive oxygen species (ROS) that participate in the proliferation of monocyte/macrophage. However, the molecular mechanisms whereby ROS modulate the signaling processes of M-CSF remain poorly defined. We report here that the redox-sensitive Src homology region 2 domain-containing phosphatase 1 (SHP1) is a critical regulator of M-CSF-mediated signaling in bone marrow monocyte/macrophage lineage cells (BMMs). Application of diphenylene iodonium (DPI) inhibited the responses of BMMs to M-CSF, including ROS production, cell proliferation, and phosphorylation of c-Fms as well as Akt kinase, but not of MAP kinases such as ERK, p38, and JNK. Dysregulation of SHP1 by overexpression or RNA interference in BMMs showed that SHP1 specifically regulates PI3 kinase (PI3K)/Akt signaling, but not MAP kinases in a redox-dependent manner, thereby regulating proliferation of BMMs through cyclins D1 and D2. These findings demonstrate that M-CSF-mediated ROS generation leads to SHP1 oxidation, which promotes cell proliferation through the PI3K/Akt-dependent signaling pathway.",

keywords = "M-CSF, Monocyte/macrophage, Oxidation, PI3K/Akt signaling, Proliferation, SHP1",

author = "Choi, {Han Kyoung} and Kim, {Tae Hee} and Jhon, {Gil Ja} and Lee, {Soo Young}",

note = "Funding Information: We thank T. Kitamura for PLAT-E cells and K. Mizuno for pSPORT6-SHP1. This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea Government (MEST) ( R0A-2008-000-20001-0 ; R31-2008-000-10010-0 ; No. 2011–0006244 ; No. 2010–0020577 ). H.C. was supported by the second stage of the Brain Korea 21 Project.",

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AU - Choi, Han Kyoung

AU - Kim, Tae Hee

AU - Jhon, Gil Ja

AU - Lee, Soo Young

N1 - Funding Information: We thank T. Kitamura for PLAT-E cells and K. Mizuno for pSPORT6-SHP1. This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea Government (MEST) ( R0A-2008-000-20001-0 ; R31-2008-000-10010-0 ; No. 2011–0006244 ; No. 2010–0020577 ). H.C. was supported by the second stage of the Brain Korea 21 Project.

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N2 - Macrophage colony-stimulating factor (M-CSF) stimulation results in the production of reactive oxygen species (ROS) that participate in the proliferation of monocyte/macrophage. However, the molecular mechanisms whereby ROS modulate the signaling processes of M-CSF remain poorly defined. We report here that the redox-sensitive Src homology region 2 domain-containing phosphatase 1 (SHP1) is a critical regulator of M-CSF-mediated signaling in bone marrow monocyte/macrophage lineage cells (BMMs). Application of diphenylene iodonium (DPI) inhibited the responses of BMMs to M-CSF, including ROS production, cell proliferation, and phosphorylation of c-Fms as well as Akt kinase, but not of MAP kinases such as ERK, p38, and JNK. Dysregulation of SHP1 by overexpression or RNA interference in BMMs showed that SHP1 specifically regulates PI3 kinase (PI3K)/Akt signaling, but not MAP kinases in a redox-dependent manner, thereby regulating proliferation of BMMs through cyclins D1 and D2. These findings demonstrate that M-CSF-mediated ROS generation leads to SHP1 oxidation, which promotes cell proliferation through the PI3K/Akt-dependent signaling pathway.

AB - Macrophage colony-stimulating factor (M-CSF) stimulation results in the production of reactive oxygen species (ROS) that participate in the proliferation of monocyte/macrophage. However, the molecular mechanisms whereby ROS modulate the signaling processes of M-CSF remain poorly defined. We report here that the redox-sensitive Src homology region 2 domain-containing phosphatase 1 (SHP1) is a critical regulator of M-CSF-mediated signaling in bone marrow monocyte/macrophage lineage cells (BMMs). Application of diphenylene iodonium (DPI) inhibited the responses of BMMs to M-CSF, including ROS production, cell proliferation, and phosphorylation of c-Fms as well as Akt kinase, but not of MAP kinases such as ERK, p38, and JNK. Dysregulation of SHP1 by overexpression or RNA interference in BMMs showed that SHP1 specifically regulates PI3 kinase (PI3K)/Akt signaling, but not MAP kinases in a redox-dependent manner, thereby regulating proliferation of BMMs through cyclins D1 and D2. These findings demonstrate that M-CSF-mediated ROS generation leads to SHP1 oxidation, which promotes cell proliferation through the PI3K/Akt-dependent signaling pathway.

KW - M-CSF

KW - Monocyte/macrophage

KW - Oxidation

KW - PI3K/Akt signaling

KW - Proliferation

KW - SHP1

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JO - Cellular Signalling

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ER -

Reactive oxygen species regulate M-CSF-induced monocyte/macrophage proliferation through SHP1 oxidation

Abstract

Bibliographical note

Keywords

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