Endophilin-A2-dependent Tubular Endocytosis Promotes Plasma Membrane Repair and Parasite Invasion

Overview

Journal J Cell Sci

Specialty Cell Biology

Date 2020 Oct 23

PMID 33093240

Citations 9

Authors

Matthias Corrotte

Mark Cerasoli

Fernando Y Maeda

Norma W Andrews

Affiliations

Soon will be listed here.

Abstract

Endocytosis of caveolae has previously been implicated in the repair of plasma membrane wounds. Here, we show that caveolin-1-deficient fibroblasts lacking caveolae upregulate a tubular endocytic pathway and have a reduced capacity to reseal after permeabilization with pore-forming toxins compared with wild-type cells. Silencing endophilin-A2 expression inhibited fission of endocytic tubules and further reduced plasma membrane repair in cells lacking caveolin-1, supporting a role for tubular endocytosis as an alternative pathway for the removal of membrane lesions. Endophilin-A2 was visualized in association with cholera toxin B-containing endosomes and was recruited to recently formed intracellular vacuoles containing , a parasite that utilizes the plasma membrane wounding repair pathway to invade host cells. Endophilin-A2 deficiency inhibited invasion, and fibroblasts deficient in both caveolin-1 and endophilin-A2 did not survive prolonged exposure to the parasites. These findings reveal a novel crosstalk between caveolin-1 and endophilin-A2 in the regulation of clathrin-independent endocytosis and plasma membrane repair, a process that is subverted by parasites for cell invasion.

Citing Articles

The invasion pore induced by .

Kegawa Y, Male F, Jimenez-Munguia I, Blank P, Mekhedov E, Ward G bioRxiv. 2024; .

PMID: 39416144 PMC: 11482919. DOI: 10.1101/2024.10.11.617945.

Membrane Tension Regulation is Required for Wound Repair.

Raj N, Weiss M, Vos B, Weischer S, Brinkmann F, Betz T Adv Sci (Weinh). 2024; 11(48):e2402317.

PMID: 39360573 PMC: 11672324. DOI: 10.1002/advs.202402317.

Endophilin A2 controls touch and mechanical allodynia via kinesin-mediated Piezo2 trafficking.

Xie M, Lai R, Xiao Y, Zhang X, Cao X, Tian X Mil Med Res. 2024; 11(1):17.

PMID: 38475827 PMC: 10929226. DOI: 10.1186/s40779-024-00520-z.

Mechanisms of Endothelial Cell Membrane Repair: Progress and Perspectives.

Zha D, Wang S, Monaghan-Nichols P, Qian Y, Sampath V, Fu M Cells. 2023; 12(22).

PMID: 37998383 PMC: 10670313. DOI: 10.3390/cells12222648.

Plasma membrane repair empowers the necrotic survivors as innate immune modulators.

Xu S, Yang T, Xu S, Gong Y Semin Cell Dev Biol. 2023; 156:93-106.

PMID: 37648621 PMC: 10872800. DOI: 10.1016/j.semcdb.2023.08.001.

References

Ambroso M, Hegde B, Langen R . Endophilin A1 induces different membrane shapes using a conformational switch that is regulated by phosphorylation. Proc Natl Acad Sci U S A. 2014; 111(19):6982-7. PMC: 4024918. DOI: 10.1073/pnas.1402233111. View

Pelkmans L, Helenius A . Endocytosis via caveolae. Traffic. 2002; 3(5):311-20. DOI: 10.1034/j.1600-0854.2002.30501.x. View

Fra A, Williamson E, Simons K, Parton R . Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J Biol Chem. 1994; 269(49):30745-8. View

Miller H, Castro-Gomes T, Corrotte M, Tam C, Maugel T, Andrews N . Lipid raft-dependent plasma membrane repair interferes with the activation of B lymphocytes. J Cell Biol. 2015; 211(6):1193-205. PMC: 4687878. DOI: 10.1083/jcb.201505030. View

McDade J, Archambeau A, Michele D . Rapid actin-cytoskeleton-dependent recruitment of plasma membrane-derived dysferlin at wounds is critical for muscle membrane repair. FASEB J. 2014; 28(8):3660-70. PMC: 4101652. DOI: 10.1096/fj.14-250191. View

Sibley L, Andrews N . Cell invasion by un-palatable parasites. Traffic. 2001; 1(2):100-6. DOI: 10.1034/j.1600-0854.2000.010202.x. View

Corrotte M, Fernandes M, Tam C, Andrews N . Toxin pores endocytosed during plasma membrane repair traffic into the lumen of MVBs for degradation. Traffic. 2012; 13(3):483-94. PMC: 3356596. DOI: 10.1111/j.1600-0854.2011.01323.x. View

Lakshminarayan R, Wunder C, Becken U, Howes M, Benzing C, Arumugam S . Galectin-3 drives glycosphingolipid-dependent biogenesis of clathrin-independent carriers. Nat Cell Biol. 2014; 16(6):595-606. DOI: 10.1038/ncb2970. View

Parton R, Simons K . The multiple faces of caveolae. Nat Rev Mol Cell Biol. 2007; 8(3):185-94. DOI: 10.1038/nrm2122. View

10.

Burleigh B, Andrews N . The mechanisms of Trypanosoma cruzi invasion of mammalian cells. Annu Rev Microbiol. 1995; 49:175-200. DOI: 10.1146/annurev.mi.49.100195.001135. View

11.

Togo T, Krasieva T, Steinhardt R . A decrease in membrane tension precedes successful cell-membrane repair. Mol Biol Cell. 2000; 11(12):4339-46. PMC: 15076. DOI: 10.1091/mbc.11.12.4339. View

12.

Idone V, Tam C, Andrews N . Two-way traffic on the road to plasma membrane repair. Trends Cell Biol. 2008; 18(11):552-9. PMC: 2593466. DOI: 10.1016/j.tcb.2008.09.001. View

13.

Simunovic M, Manneville J, Renard H, Evergren E, Raghunathan K, Bhatia D . Friction Mediates Scission of Tubular Membranes Scaffolded by BAR Proteins. Cell. 2017; 170(1):172-184.e11. PMC: 5576516. DOI: 10.1016/j.cell.2017.05.047. View

14.

Kjaerulff O, Brodin L, Jung A . The structure and function of endophilin proteins. Cell Biochem Biophys. 2010; 60(3):137-54. DOI: 10.1007/s12013-010-9137-5. View

15.

Swaggart K, Demonbreun A, Vo A, Swanson K, Kim E, Fahrenbach J . Annexin A6 modifies muscular dystrophy by mediating sarcolemmal repair. Proc Natl Acad Sci U S A. 2014; 111(16):6004-9. PMC: 4000833. DOI: 10.1073/pnas.1324242111. View

16.

Keefe D, Shi L, Feske S, Massol R, Navarro F, Kirchhausen T . Perforin triggers a plasma membrane-repair response that facilitates CTL induction of apoptosis. Immunity. 2005; 23(3):249-62. DOI: 10.1016/j.immuni.2005.08.001. View

17.

Renard H, Simunovic M, Lemiere J, Boucrot E, Daniela Garcia-Castillo M, Arumugam S . Endophilin-A2 functions in membrane scission in clathrin-independent endocytosis. Nature. 2014; 517(7535):493-6. PMC: 4342003. DOI: 10.1038/nature14064. View

18.

Boucrot E, Ferreira A, Almeida-Souza L, Debard S, Vallis Y, Howard G . Endophilin marks and controls a clathrin-independent endocytic pathway. Nature. 2014; 517(7535):460-5. DOI: 10.1038/nature14067. View

19.

Wah Hak L, Khan S, Di Meglio I, Law A, Lucken-Ardjomande Hasler S, Quintaneiro L . FBP17 and CIP4 recruit SHIP2 and lamellipodin to prime the plasma membrane for fast endophilin-mediated endocytosis. Nat Cell Biol. 2018; 20(9):1023-1031. PMC: 6122583. DOI: 10.1038/s41556-018-0146-8. View

20.

Maeda F, van Haaren J, Langley D, Christ D, Andrews N, Song W . Surface-associated antigen induces permeabilization of primary mouse B-cells and lysosome exocytosis facilitating antigen uptake and presentation to T-cells. Elife. 2021; 10. PMC: 8589448. DOI: 10.7554/eLife.66984. View