Electric signals counterbalanced posterior vs anterior PTEN signaling in directed migration of Dictyostelium

Bing Song; Yu Gu; Wenkai Jiang; Ying Li; Wayne Nishio Ayre; Zhipeng Liu; Tao Yin; Christopher Janetopoulos; Miho Iijima; Peter Devreotes; Min Zhao

doi:10.1186/s13578-021-00580-x

Electric signals counterbalanced posterior vs anterior PTEN signaling in directed migration of Dictyostelium

Bing Song, Yu Gu, Wenkai Jiang, Ying Li, Wayne Nishio Ayre, Zhipeng Liu, Tao Yin, Christopher Janetopoulos, Miho Iijima, Peter Devreotes, Min Zhao

School of Medicine

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

Abstract

Background: Cells show directed migration response to electric signals, namely electrotaxis or galvanotaxis. PI3K and PTEN jointly play counterbalancing roles in this event via a bilateral regulation of PIP3 signaling. PI3K has been proved essential in anterior signaling of electrotaxing cells, whilst the role of PTEN remains elusive. Methods: Dictyostelium cells with different genetic backgrounds were treated with direct current electric signals to investigate the genetic regulation of electrotaxis. Results: We demonstrated that electric signals promoted PTEN phosphatase activity and asymmetrical translocation to the posterior plasma membrane of the electrotaxing cells. Electric stimulation produced a similar but delayed rear redistribution of myosin II, immediately before electrotaxis started. Actin polymerization is required for the asymmetric membrane translocation of PTEN and myosin. PTEN signaling is also responsible for the asymmetric anterior redistribution of PIP3/F-actin, and a biased redistribution of pseudopod protrusion in the forwarding direction of electrotaxing cells. Conclusions: PTEN controls electrotaxis by coordinately regulating asymmetric redistribution of myosin to the posterior, and PIP3/F-actin to the anterior region of the directed migration cells.

Original language	English (US)
Article number	111
Journal	Cell and Bioscience
Volume	11
Issue number	1
DOIs	https://doi.org/10.1186/s13578-021-00580-x
State	Published - Dec 2021

Keywords

Cell migration
Electric field
Electrotaxis
F-actin
Galvanotaxis
Myosin
PH-Crac
PIP3
PTEN

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1186/s13578-021-00580-x

Cite this

@article{4fb1caf67b274e53a44dcb0c4330b7dc,

title = "Electric signals counterbalanced posterior vs anterior PTEN signaling in directed migration of Dictyostelium",

abstract = "Background: Cells show directed migration response to electric signals, namely electrotaxis or galvanotaxis. PI3K and PTEN jointly play counterbalancing roles in this event via a bilateral regulation of PIP3 signaling. PI3K has been proved essential in anterior signaling of electrotaxing cells, whilst the role of PTEN remains elusive. Methods: Dictyostelium cells with different genetic backgrounds were treated with direct current electric signals to investigate the genetic regulation of electrotaxis. Results: We demonstrated that electric signals promoted PTEN phosphatase activity and asymmetrical translocation to the posterior plasma membrane of the electrotaxing cells. Electric stimulation produced a similar but delayed rear redistribution of myosin II, immediately before electrotaxis started. Actin polymerization is required for the asymmetric membrane translocation of PTEN and myosin. PTEN signaling is also responsible for the asymmetric anterior redistribution of PIP3/F-actin, and a biased redistribution of pseudopod protrusion in the forwarding direction of electrotaxing cells. Conclusions: PTEN controls electrotaxis by coordinately regulating asymmetric redistribution of myosin to the posterior, and PIP3/F-actin to the anterior region of the directed migration cells.",

keywords = "Cell migration, Electric field, Electrotaxis, F-actin, Galvanotaxis, Myosin, PH-Crac, PIP3, PTEN",

author = "Bing Song and Yu Gu and Wenkai Jiang and Ying Li and Ayre, {Wayne Nishio} and Zhipeng Liu and Tao Yin and Christopher Janetopoulos and Miho Iijima and Peter Devreotes and Min Zhao",

note = "Funding Information: This work was supported by Wellcome Trust Grant (WT082887MA) to M.Z. and B.S.; Royal Society URF Award (UF051616) and European Research Council FP7 grant (No. 243261) to B.S.; AFOSR Multidisciplinary University Research Initiatives grant (FA9550-16–1-0052), NIH grants (EY019101), NEI core grant (P-30 EY012576), Karen Burns Cornea Research fund and an unrestricted grant from Research to Prevent Blindness, Inc., to M.Z.; CAMS Initiative for Innovative Medicine (CAMS-I2M, Grant No. 2016-I2M1-004) to T.Y.; and the National Natural Science Foundation of China (No. 81927806) to Z.L. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

doi = "10.1186/s13578-021-00580-x",

language = "English (US)",

volume = "11",

journal = "Cell and Bioscience",

issn = "2045-3701",

publisher = "Society of Chinese Bioscientists in America",

number = "1",

}

TY - JOUR

T1 - Electric signals counterbalanced posterior vs anterior PTEN signaling in directed migration of Dictyostelium

AU - Song, Bing

AU - Gu, Yu

AU - Jiang, Wenkai

AU - Li, Ying

AU - Ayre, Wayne Nishio

AU - Liu, Zhipeng

AU - Yin, Tao

AU - Janetopoulos, Christopher

AU - Iijima, Miho

AU - Devreotes, Peter

AU - Zhao, Min

N1 - Funding Information: This work was supported by Wellcome Trust Grant (WT082887MA) to M.Z. and B.S.; Royal Society URF Award (UF051616) and European Research Council FP7 grant (No. 243261) to B.S.; AFOSR Multidisciplinary University Research Initiatives grant (FA9550-16–1-0052), NIH grants (EY019101), NEI core grant (P-30 EY012576), Karen Burns Cornea Research fund and an unrestricted grant from Research to Prevent Blindness, Inc., to M.Z.; CAMS Initiative for Innovative Medicine (CAMS-I2M, Grant No. 2016-I2M1-004) to T.Y.; and the National Natural Science Foundation of China (No. 81927806) to Z.L. Publisher Copyright: © 2021, The Author(s).

PY - 2021/12

Y1 - 2021/12

N2 - Background: Cells show directed migration response to electric signals, namely electrotaxis or galvanotaxis. PI3K and PTEN jointly play counterbalancing roles in this event via a bilateral regulation of PIP3 signaling. PI3K has been proved essential in anterior signaling of electrotaxing cells, whilst the role of PTEN remains elusive. Methods: Dictyostelium cells with different genetic backgrounds were treated with direct current electric signals to investigate the genetic regulation of electrotaxis. Results: We demonstrated that electric signals promoted PTEN phosphatase activity and asymmetrical translocation to the posterior plasma membrane of the electrotaxing cells. Electric stimulation produced a similar but delayed rear redistribution of myosin II, immediately before electrotaxis started. Actin polymerization is required for the asymmetric membrane translocation of PTEN and myosin. PTEN signaling is also responsible for the asymmetric anterior redistribution of PIP3/F-actin, and a biased redistribution of pseudopod protrusion in the forwarding direction of electrotaxing cells. Conclusions: PTEN controls electrotaxis by coordinately regulating asymmetric redistribution of myosin to the posterior, and PIP3/F-actin to the anterior region of the directed migration cells.

AB - Background: Cells show directed migration response to electric signals, namely electrotaxis or galvanotaxis. PI3K and PTEN jointly play counterbalancing roles in this event via a bilateral regulation of PIP3 signaling. PI3K has been proved essential in anterior signaling of electrotaxing cells, whilst the role of PTEN remains elusive. Methods: Dictyostelium cells with different genetic backgrounds were treated with direct current electric signals to investigate the genetic regulation of electrotaxis. Results: We demonstrated that electric signals promoted PTEN phosphatase activity and asymmetrical translocation to the posterior plasma membrane of the electrotaxing cells. Electric stimulation produced a similar but delayed rear redistribution of myosin II, immediately before electrotaxis started. Actin polymerization is required for the asymmetric membrane translocation of PTEN and myosin. PTEN signaling is also responsible for the asymmetric anterior redistribution of PIP3/F-actin, and a biased redistribution of pseudopod protrusion in the forwarding direction of electrotaxing cells. Conclusions: PTEN controls electrotaxis by coordinately regulating asymmetric redistribution of myosin to the posterior, and PIP3/F-actin to the anterior region of the directed migration cells.

KW - Cell migration

KW - Electric field

KW - Electrotaxis

KW - F-actin

KW - Galvanotaxis

KW - Myosin

KW - PH-Crac

KW - PIP3

KW - PTEN

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U2 - 10.1186/s13578-021-00580-x

DO - 10.1186/s13578-021-00580-x

M3 - Article

C2 - 34127068

AN - SCOPUS:85107716688

SN - 2045-3701

VL - 11

JO - Cell and Bioscience

JF - Cell and Bioscience

IS - 1

M1 - 111

ER -

Electric signals counterbalanced posterior vs anterior PTEN signaling in directed migration of Dictyostelium

Abstract

Keywords

ASJC Scopus subject areas

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