Leukocyte Cytoskeleton Polarization Is Initiated by Plasma Membrane Curvature from Cell Attachment.


Journal

Developmental cell
ISSN: 1878-1551
Titre abrégé: Dev Cell
Pays: United States
ID NLM: 101120028

Informations de publication

Date de publication:
22 04 2019
Historique:
received: 15 03 2018
revised: 15 01 2019
accepted: 25 02 2019
pubmed: 2 4 2019
medline: 7 1 2020
entrez: 2 4 2019
Statut: ppublish

Résumé

Cell polarization is important for various biological processes. However, its regulation, particularly initiation, is incompletely understood. Here, we investigated mechanisms by which neutrophils break their symmetry and initiate their cytoskeleton polarization from an apolar state in circulation for their extravasation during inflammation. We show here that a local increase in plasma membrane (PM) curvature resulting from cell contact to a surface triggers the initial breakage of the symmetry of an apolar neutrophil and is required for subsequent polarization events induced by chemical stimulation. This local increase in PM curvature recruits SRGAP2 via its F-BAR domain, which in turn activates PI4KA and results in PM PtdIns4P polarization. Polarized PM PtdIns4P is targeted by RPH3A, which directs PIP5K1C90 and subsequent phosphorylated myosin light chain polarization, and this polarization signaling axis regulates neutrophil firm attachment to endothelium. Thus, this study reveals a mechanism for the initiation of cell cytoskeleton polarization.

Identifiants

pubmed: 30930167
pii: S1534-5807(19)30146-7
doi: 10.1016/j.devcel.2019.02.023
pmc: PMC6482112
mid: NIHMS1525314
pii:
doi:

Substances chimiques

Actins 0
GTPase-Activating Proteins 0
Minor Histocompatibility Antigens 0
Myosin Light Chains 0
Phosphatidylinositol Phosphates 0
SRGAP2 protein, human 0
phosphatidylinositol 4-phosphate 0
Phosphotransferases (Alcohol Group Acceptor) EC 2.7.1.-
phosphatidylinositol phosphate 4-kinase EC 2.7.1.67

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

206-219.e7

Subventions

Organisme : NCATS NIH HHS
ID : UL1 TR001863
Pays : United States
Organisme : NHLBI NIH HHS
ID : R35 HL135805
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL125885
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM108954
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS113236
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM114513
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL145152
Pays : United States

Informations de copyright

Copyright © 2019 Elsevier Inc. All rights reserved.

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Auteurs

Chunguang Ren (C)

Department of Pharmacology, Vascular Biology and Therapeutic Program, Yale University, New Haven, CT 06520, USA.

Qianying Yuan (Q)

Department of Pharmacology, Vascular Biology and Therapeutic Program, Yale University, New Haven, CT 06520, USA.

Martha Braun (M)

Department of Cellular and Molecular Physiology, Yale University, New Haven, CT 06520, USA; Nanobiology Institute, Yale University, New Haven, CT 06520, USA; Department of Molecular Biophysics and Biochemistry, Yale School of Medicine, Yale University, New Haven, CT 06520, USA.

Xia Zhang (X)

Department of Geriatrics, the First affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, Zhejiang, China.

Björn Petri (B)

Snyder Institute for Chronic Diseases Mouse Phenomics Resource Laboratory, University of Calgary, Calgary AB T2N 4N1, Canada; Department of Microbiology, Immunology, and Infectious Diseases, University of Calgary, Calgary AB T2N 4N1, Canada.

Jiasheng Zhang (J)

Department of Internal Medicine, Yale University, New Haven, CT 06520, USA.

Dongjoo Kim (D)

Department of Biomedical Engineering, Yale University, New Haven, CT 06520, USA.

Julia Guez-Haddad (J)

The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Wenzhi Xue (W)

Shanghai Institute of Nutrition and Health, Shanghai Institutes for Biological Sciences, University of Chinese Academy of Sciences, Chinese Academy of Sciences (CAS), Shanghai, China.

Weijun Pan (W)

Shanghai Institute of Nutrition and Health, Shanghai Institutes for Biological Sciences, University of Chinese Academy of Sciences, Chinese Academy of Sciences (CAS), Shanghai, China.

Rong Fan (R)

Department of Biomedical Engineering, Yale University, New Haven, CT 06520, USA.

Paul Kubes (P)

Snyder Institute for Chronic Diseases Mouse Phenomics Resource Laboratory, University of Calgary, Calgary AB T2N 4N1, Canada; Department of Physiology and Pharmacology, Cumming School of Medicine, and Calvin, Phoebe, and Joan Snyder Institute for Chronic Diseases, University of Calgary, Calgary AB T2N 4N1, Canada.

Zhaoxia Sun (Z)

Department of Genetics, Yale University, New Haven, CT 06520, USA.

Yarden Opatowsky (Y)

The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 5290002, Israel.

Franck Polleux (F)

Department of Neuroscience, Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY 10025, USA.

Erdem Karatekin (E)

Department of Cellular and Molecular Physiology, Yale University, New Haven, CT 06520, USA; Nanobiology Institute, Yale University, New Haven, CT 06520, USA; Department of Molecular Biophysics and Biochemistry, Yale School of Medicine, Yale University, New Haven, CT 06520, USA; Centre National de la Recherche Scientifique (CNRS), Paris, France. Electronic address: erdem.karatekin@yale.edu.

Wenwen Tang (W)

Department of Pharmacology, Vascular Biology and Therapeutic Program, Yale University, New Haven, CT 06520, USA. Electronic address: wenwen.tang@yale.edu.

Dianqing Wu (D)

Department of Pharmacology, Vascular Biology and Therapeutic Program, Yale University, New Haven, CT 06520, USA. Electronic address: dan.wu@yale.edu.

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Classifications MeSH