The Role of APC-mediated Actin Assembly in Microtubule Capture and Focal Adhesion Turnover

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2019 Sep 1

PMID 31471457

Citations 24

Authors

M Angeles Juanes

Daniel Isnardon

Ali Badache

Sophie Brasselet

Manos Mavrakis

Bruce L Goode

Affiliations

Soon will be listed here.

Abstract

Focal adhesion (FA) turnover depends on microtubules and actin. Microtubule ends are captured at FAs, where they induce rapid FA disassembly. However, actin's roles are less clear. Here, we use polarization-resolved microscopy, FRAP, live cell imaging, and a mutant of Adenomatous polyposis coli (APC-m4) defective in actin nucleation to investigate the role of actin assembly in FA turnover. We show that APC-mediated actin assembly is critical for maintaining normal F-actin levels, organization, and dynamics at FAs, along with organization of FA components. In WT cells, microtubules are captured repeatedly at FAs as they mature, but once a FA reaches peak maturity, the next microtubule capture event leads to delivery of an autophagosome, triggering FA disassembly. In APC-m4 cells, microtubule capture frequency and duration are altered, and there are long delays between autophagosome delivery and FA disassembly. Thus, APC-mediated actin assembly is required for normal feedback between microtubules and FAs, and maintaining FAs in a state "primed" for microtubule-induced turnover.

Citing Articles

APC orchestrates microtubule dynamics by acting as a positive regulator of KIF2A and a negative regulator of CLASPs.

Wang Y, Liu X, Liu Z, Hua S, Jiang K Cell Insight. 2024; 4(1):100210.

PMID: 39640087 PMC: 11617872. DOI: 10.1016/j.cellin.2024.100210.

The role and regulation of integrins in cell migration and invasion.

Chastney M, Kaivola J, Leppanen V, Ivaska J Nat Rev Mol Cell Biol. 2024; 26(2):147-167.

PMID: 39349749 DOI: 10.1038/s41580-024-00777-1.

From Crypts to Cancer: A Holistic Perspective on Colorectal Carcinogenesis and Therapeutic Strategies.

Gharib E, Robichaud G Int J Mol Sci. 2024; 25(17).

PMID: 39273409 PMC: 11395697. DOI: 10.3390/ijms25179463.

Focal adhesions are controlled by microtubules through local contractility regulation.

Aureille J, Prabhu S, Barnett S, Farrugia A, Arnal I, Lafanechere L EMBO J. 2024; 43(13):2715-2732.

PMID: 38769437 PMC: 11217342. DOI: 10.1038/s44318-024-00114-4.

Actin Cytoskeleton Remodeling Accompanied by Redistribution of Adhesion Proteins Drives Migration of Cells in Different EMT States.

Ilnitskaya A, Litovka N, Rubtsova S, Zhitnyak I, Gloushankova N Cells. 2024; 13(9.

PMID: 38727316 PMC: 11083118. DOI: 10.3390/cells13090780.

References

Kaverina I, Krylyshkina O, Small J . Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J Cell Biol. 1999; 146(5):1033-44. PMC: 2169483. DOI: 10.1083/jcb.146.5.1033. View

Geiger B, Yamada K . Molecular architecture and function of matrix adhesions. Cold Spring Harb Perspect Biol. 2011; 3(5). PMC: 3101841. DOI: 10.1101/cshperspect.a005033. View

Moseley J, Bartolini F, Okada K, Wen Y, Gundersen G, Goode B . Regulated binding of adenomatous polyposis coli protein to actin. J Biol Chem. 2007; 282(17):12661-8. DOI: 10.1074/jbc.M610615200. View

Jackson W, Giddings Jr T, Taylor M, Mulinyawe S, Rabinovitch M, Kopito R . Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 2005; 3(5):e156. PMC: 1084330. DOI: 10.1371/journal.pbio.0030156. View

Efimov A, Schiefermeier N, Grigoriev I, Ohi R, Brown M, Turner C . Paxillin-dependent stimulation of microtubule catastrophes at focal adhesion sites. J Cell Sci. 2008; 121(Pt 2):196-204. PMC: 3164837. DOI: 10.1242/jcs.012666. View

Breitsprecher D, Jaiswal R, Bombardier J, Gould C, Gelles J, Goode B . Rocket launcher mechanism of collaborative actin assembly defined by single-molecule imaging. Science. 2012; 336(6085):1164-8. PMC: 3613992. DOI: 10.1126/science.1218062. View

Ezratty E, Partridge M, Gundersen G . Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol. 2005; 7(6):581-90. DOI: 10.1038/ncb1262. View

Juanes M, Bouguenina H, Eskin J, Jaiswal R, Badache A, Goode B . Adenomatous polyposis coli nucleates actin assembly to drive cell migration and microtubule-induced focal adhesion turnover. J Cell Biol. 2017; 216(9):2859-2875. PMC: 5584174. DOI: 10.1083/jcb.201702007. View

Jaiswal R, Stepanik V, Rankova A, Molinar O, Goode B, McCartney B . Drosophila homologues of adenomatous polyposis coli (APC) and the formin diaphanous collaborate by a conserved mechanism to stimulate actin filament assembly. J Biol Chem. 2013; 288(19):13897-905. PMC: 3650425. DOI: 10.1074/jbc.M113.462051. View

10.

Falcon-Perez J, Nazarian R, Sabatti C, DellAngelica E . Distribution and dynamics of Lamp1-containing endocytic organelles in fibroblasts deficient in BLOC-3. J Cell Sci. 2005; 118(Pt 22):5243-55. DOI: 10.1242/jcs.02633. View

11.

Kenific C, Debnath J . NBR1-dependent selective autophagy is required for efficient cell-matrix adhesion site disassembly. Autophagy. 2016; 12(10):1958-1959. PMC: 5079663. DOI: 10.1080/15548627.2016.1212789. View

12.

Mogensen M, Tucker J, Mackie J, Prescott A, Nathke I . The adenomatous polyposis coli protein unambiguously localizes to microtubule plus ends and is involved in establishing parallel arrays of microtubule bundles in highly polarized epithelial cells. J Cell Biol. 2002; 157(6):1041-8. PMC: 2174057. DOI: 10.1083/jcb.200203001. View

13.

Valades Cruz C, Shaban H, Kress A, Bertaux N, Monneret S, Mavrakis M . Quantitative nanoscale imaging of orientational order in biological filaments by polarized superresolution microscopy. Proc Natl Acad Sci U S A. 2016; 113(7):E820-8. PMC: 4763786. DOI: 10.1073/pnas.1516811113. View

14.

Svitkina T, Bulanova E, Chaga O, Vignjevic D, Kojima S, Vasiliev J . Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol. 2003; 160(3):409-21. PMC: 2172658. DOI: 10.1083/jcb.200210174. View

15.

Sharifi M, Mowers E, Drake L, Collier C, Chen H, Zamora M . Autophagy Promotes Focal Adhesion Disassembly and Cell Motility of Metastatic Tumor Cells through the Direct Interaction of Paxillin with LC3. Cell Rep. 2016; 15(8):1660-72. PMC: 4880529. DOI: 10.1016/j.celrep.2016.04.065. View

16.

Krylyshkina O, Anderson K, Kaverina I, Upmann I, Manstein D, Small J . Nanometer targeting of microtubules to focal adhesions. J Cell Biol. 2003; 161(5):853-9. PMC: 2172972. DOI: 10.1083/jcb.200301102. View

17.

Stehbens S, Paszek M, Pemble H, Ettinger A, Gierke S, Wittmann T . CLASPs link focal-adhesion-associated microtubule capture to localized exocytosis and adhesion site turnover. Nat Cell Biol. 2014; 16(6):561-73. PMC: 4108447. DOI: 10.1038/ncb2975. View

18.

Carramusa L, Ballestrem C, Zilberman Y, Bershadsky A . Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherin-mediated cell-cell junctions. J Cell Sci. 2007; 120(Pt 21):3870-82. DOI: 10.1242/jcs.014365. View

19.

Thery M, Pepin A, Dressaire E, Chen Y, Bornens M . Cell distribution of stress fibres in response to the geometry of the adhesive environment. Cell Motil Cytoskeleton. 2006; 63(6):341-55. DOI: 10.1002/cm.20126. View

20.

Swaminathan V, Kalappurakkal J, Mehta S, Nordenfelt P, Moore T, Koga N . Actin retrograde flow actively aligns and orients ligand-engaged integrins in focal adhesions. Proc Natl Acad Sci U S A. 2017; 114(40):10648-10653. PMC: 5635867. DOI: 10.1073/pnas.1701136114. View