Cortical Actin Contributes to Spatial Organization of ER-PM Junctions

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2017 Sep 29

PMID 28954864

Citations 28

Authors

Ting-Sung Hsieh

Yu-Ju Chen

Chi-Lun Chang

Wan-Ru Lee

Jen Liou

Affiliations

Soon will be listed here.

Abstract

Endoplasmic reticulum-plasma membrane (ER-PM) junctions mediate crucial activities ranging from Ca signaling to lipid metabolism. Spatial organization of ER-PM junctions may modulate the extent and location of these cellular activities. However, the morphology and distribution of ER-PM junctions are not well characterized. Using photoactivated localization microscopy, we reveal that the contact area of single ER-PM junctions is mainly oblong with the dimensions of ∼120 nm × ∼80 nm in HeLa cells. Using total internal reflection fluorescence microscopy and structure illumination microscopy, we show that cortical actin contributes to spatial distribution and stability of ER-PM junctions. Further functional assays suggest that intact F-actin architecture is required for phosphatidylinositol 4,5-bisphosphate homeostasis mediated by Nir2 at ER-PM junctions. Together, our study provides quantitative information on spatial organization of ER-PM junctions that is in part regulated by F-actin. We envision that functions of ER-PM junctions can be differentially regulated through dynamic actin remodeling during cellular processes.

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References

Tinevez J, Perry N, Schindelin J, Hoopes G, Reynolds G, Laplantine E . TrackMate: An open and extensible platform for single-particle tracking. Methods. 2016; 115:80-90. DOI: 10.1016/j.ymeth.2016.09.016. View

Nicovich P, Owen D, Gaus K . Turning single-molecule localization microscopy into a quantitative bioanalytical tool. Nat Protoc. 2017; 12(3):453-460. DOI: 10.1038/nprot.2016.166. View

Wu Y, Whiteus C, Xu C, Hayworth K, Weinberg R, Hess H . Contacts between the endoplasmic reticulum and other membranes in neurons. Proc Natl Acad Sci U S A. 2017; 114(24):E4859-E4867. PMC: 5474793. DOI: 10.1073/pnas.1701078114. View

Chang C, Hsieh T, Yang T, Rothberg K, Azizoglu D, Volk E . Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep. 2013; 5(3):813-25. DOI: 10.1016/j.celrep.2013.09.038. View

Xu K, Babcock H, Zhuang X . Dual-objective STORM reveals three-dimensional filament organization in the actin cytoskeleton. Nat Methods. 2012; 9(2):185-8. PMC: 3304438. DOI: 10.1038/nmeth.1841. View

Giordano F, Saheki Y, Idevall-Hagren O, Colombo S, Pirruccello M, Milosevic I . PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell. 2013; 153(7):1494-509. PMC: 3716012. DOI: 10.1016/j.cell.2013.05.026. View

Zhang D, Bidone T, Vavylonis D . ER-PM Contacts Define Actomyosin Kinetics for Proper Contractile Ring Assembly. Curr Biol. 2016; 26(5):647-53. PMC: 4783277. DOI: 10.1016/j.cub.2015.12.070. View

Kiskowski M, Hancock J, Kenworthy A . On the use of Ripley's K-function and its derivatives to analyze domain size. Biophys J. 2009; 97(4):1095-103. PMC: 2726315. DOI: 10.1016/j.bpj.2009.05.039. View

Liou J, Kim M, Heo W, Jones J, Myers J, Ferrell Jr J . STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol. 2005; 15(13):1235-41. PMC: 3186072. DOI: 10.1016/j.cub.2005.05.055. View

10.

Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N . Computer control of microscopes using µManager. Curr Protoc Mol Biol. 2010; Chapter 14:Unit14.20. PMC: 3065365. DOI: 10.1002/0471142727.mb1420s92. View

11.

Tarantino N, Tinevez J, Crowell E, Boisson B, Henriques R, Mhlanga M . TNF and IL-1 exhibit distinct ubiquitin requirements for inducing NEMO-IKK supramolecular structures. J Cell Biol. 2014; 204(2):231-45. PMC: 3897181. DOI: 10.1083/jcb.201307172. View

12.

van Vliet A, Giordano F, Gerlo S, Segura I, Van Eygen S, Molenberghs G . The ER Stress Sensor PERK Coordinates ER-Plasma Membrane Contact Site Formation through Interaction with Filamin-A and F-Actin Remodeling. Mol Cell. 2017; 65(5):885-899.e6. DOI: 10.1016/j.molcel.2017.01.020. View

13.

Stauffer T, Ahn S, Meyer T . Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr Biol. 1998; 8(6):343-6. DOI: 10.1016/s0960-9822(98)70135-6. View

14.

West M, Zurek N, Hoenger A, Voeltz G . A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J Cell Biol. 2011; 193(2):333-46. PMC: 3080256. DOI: 10.1083/jcb.201011039. View

15.

Kim Y, Guzman-Hernandez M, Wisniewski E, Balla T . Phosphatidylinositol-Phosphatidic Acid Exchange by Nir2 at ER-PM Contact Sites Maintains Phosphoinositide Signaling Competence. Dev Cell. 2015; 33(5):549-61. PMC: 4476625. DOI: 10.1016/j.devcel.2015.04.028. View

16.

Levet F, Hosy E, Kechkar A, Butler C, Beghin A, Choquet D . SR-Tesseler: a method to segment and quantify localization-based super-resolution microscopy data. Nat Methods. 2015; 12(11):1065-71. DOI: 10.1038/nmeth.3579. View

17.

Morone N, Fujiwara T, Murase K, Kasai R, Ike H, Yuasa S . Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography. J Cell Biol. 2006; 174(6):851-62. PMC: 2064339. DOI: 10.1083/jcb.200606007. View

18.

Chen Y, Chang C, Lee W, Liou J . RASSF4 controls SOCE and ER-PM junctions through regulation of PI(4,5)P. J Cell Biol. 2017; 216(7):2011-2025. PMC: 5496610. DOI: 10.1083/jcb.201606047. View

19.

Orci L, Ravazzola M, Le Coadic M, Shen W, Demaurex N, Cosson P . From the Cover: STIM1-induced precortical and cortical subdomains of the endoplasmic reticulum. Proc Natl Acad Sci U S A. 2009; 106(46):19358-62. PMC: 2775999. DOI: 10.1073/pnas.0911280106. View

20.

Wu M, Buchanan J, Luik R, Lewis R . Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol. 2006; 174(6):803-13. PMC: 2064335. DOI: 10.1083/jcb.200604014. View