Caveolae Internalization Repairs Wounded Cells and Muscle Fibers

Overview

Journal Elife

Specialty Biology

Date 2013 Sep 21

PMID 24052812

Citations 90

Authors

Matthias Corrotte

Patricia E Almeida

Christina Tam

Thiago Castro-Gomes

Maria Cecilia Fernandes

Bryan A Millis

Mauro Cortez

Heather Miller

Wenxia Song

Timothy K Maugel

Norma W Andrews

Affiliations

Soon will be listed here.

Abstract

Rapid repair of plasma membrane wounds is critical for cellular survival. Muscle fibers are particularly susceptible to injury, and defective sarcolemma resealing causes muscular dystrophy. Caveolae accumulate in dystrophic muscle fibers and caveolin and cavin mutations cause muscle pathology, but the underlying mechanism is unknown. Here we show that muscle fibers and other cell types repair membrane wounds by a mechanism involving Ca(2+)-triggered exocytosis of lysosomes, release of acid sphingomyelinase, and rapid lesion removal by caveolar endocytosis. Wounding or exposure to sphingomyelinase triggered endocytosis and intracellular accumulation of caveolar vesicles, which gradually merged into larger compartments. The pore-forming toxin SLO was directly visualized entering cells within caveolar vesicles, and depletion of caveolin inhibited plasma membrane resealing. Our findings directly link lesion removal by caveolar endocytosis to the maintenance of plasma membrane and muscle fiber integrity, providing a mechanistic explanation for the muscle pathology associated with mutations in caveolae proteins. DOI:http://dx.doi.org/10.7554/eLife.00926.001.

Citing Articles

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.

Mechanical stretch leads to increased caveolin-1 content and mineralization potential in extracellular vesicles from vascular smooth muscle cells.

Shaver M, Gomez K, Kaiser K, Hutcheson J BMC Mol Cell Biol. 2024; 25(1):8.

PMID: 38486163 PMC: 10938675. DOI: 10.1186/s12860-024-00504-w.

Wound Repair of the Cell Membrane: Lessons from Cells.

Yumura S Cells. 2024; 13(4.

PMID: 38391954 PMC: 10886852. DOI: 10.3390/cells13040341.

Caveolae disassemble upon membrane lesioning and foster cell survival.

Stefl M, Takamiya M, Middel V, Tekpinar M, Nienhaus K, Beil T iScience. 2024; 27(2):108849.

PMID: 38303730 PMC: 10831942. DOI: 10.1016/j.isci.2024.108849.

LITAF protects against pore-forming protein-induced cell death by promoting membrane repair.

Stefani C, Bruchez A, Rosasco M, Yoshida A, Fasano K, Levan P Sci Immunol. 2024; 9(91):eabq6541.

PMID: 38181093 PMC: 11883904. DOI: 10.1126/sciimmunol.abq6541.

References

Bilderback T, Grigsby R, Dobrowsky R . Association of p75(NTR) with caveolin and localization of neurotrophin-induced sphingomyelin hydrolysis to caveolae. J Biol Chem. 1997; 272(16):10922-7. DOI: 10.1074/jbc.272.16.10922. View

Schissel S, Jiang X, Jeong T, Camejo E, Najib J, Rapp J . Secretory sphingomyelinase, a product of the acid sphingomyelinase gene, can hydrolyze atherogenic lipoproteins at neutral pH. Implications for atherosclerotic lesion development. J Biol Chem. 1998; 273(5):2738-46. DOI: 10.1074/jbc.273.5.2738. View

Fernandes M, Cortez M, Flannery A, Tam C, Mortara R, Andrews N . Trypanosoma cruzi subverts the sphingomyelinase-mediated plasma membrane repair pathway for cell invasion. J Exp Med. 2011; 208(5):909-21. PMC: 3092353. DOI: 10.1084/jem.20102518. View

Le P, Nabi I . Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J Cell Sci. 2003; 116(Pt 6):1059-71. DOI: 10.1242/jcs.00327. 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

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

Nichols B . Caveosomes and endocytosis of lipid rafts. J Cell Sci. 2003; 116(Pt 23):4707-14. DOI: 10.1242/jcs.00840. View

Yao Q, Chen J, Cao H, Orth J, McCaffery J, Stan R . Caveolin-1 interacts directly with dynamin-2. J Mol Biol. 2005; 348(2):491-501. DOI: 10.1016/j.jmb.2005.02.003. View

Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B . Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science. 2001; 293(5539):2449-52. DOI: 10.1126/science.1062688. View

10.

Hernandez-Deviez D, Howes M, Laval S, Bushby K, Hancock J, Parton R . Caveolin regulates endocytosis of the muscle repair protein, dysferlin. J Biol Chem. 2007; 283(10):6476-88. DOI: 10.1074/jbc.M708776200. View

11.

Opreanu M, Tikhonenko M, Bozack S, Lydic T, Reid G, McSorley K . The unconventional role of acid sphingomyelinase in regulation of retinal microangiopathy in diabetic human and animal models. Diabetes. 2011; 60(9):2370-8. PMC: 3161322. DOI: 10.2337/db10-0550. View

12.

Repetto S, Bado M, Broda P, Lucania G, Masetti E, Sotgia F . Increased number of caveolae and caveolin-3 overexpression in Duchenne muscular dystrophy. Biochem Biophys Res Commun. 1999; 261(3):547-50. DOI: 10.1006/bbrc.1999.1055. View

13.

Gazzerro E, Sotgia F, Bruno C, Lisanti M, Minetti C . Caveolinopathies: from the biology of caveolin-3 to human diseases. Eur J Hum Genet. 2009; 18(2):137-45. PMC: 2987183. DOI: 10.1038/ejhg.2009.103. View

14.

Holopainen J, Angelova M, Kinnunen P . Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys J. 2000; 78(2):830-8. PMC: 1300685. DOI: 10.1016/S0006-3495(00)76640-9. View

15.

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

16.

Zhu H, Lin P, De G, Choi K, Takeshima H, Weisleder N . Polymerase transcriptase release factor (PTRF) anchors MG53 protein to cell injury site for initiation of membrane repair. J Biol Chem. 2011; 286(15):12820-4. PMC: 3075629. DOI: 10.1074/jbc.C111.221440. View

17.

Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F . Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008; 319(5867):1244-7. DOI: 10.1126/science.1153124. View

18.

Sharma D, Brown J, Choudhury A, Peterson T, Holicky E, Marks D . Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol Biol Cell. 2004; 15(7):3114-22. PMC: 452569. DOI: 10.1091/mbc.e04-03-0189. View

19.

Kirkham M, Fujita A, Chadda R, Nixon S, Kurzchalia T, Sharma D . Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol. 2005; 168(3):465-76. PMC: 2171740. DOI: 10.1083/jcb.200407078. View

20.

Ferguson S, Ferguson S, Raimondi A, Paradise S, Shen H, Mesaki K . Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell. 2010; 17(6):811-22. PMC: 2861561. DOI: 10.1016/j.devcel.2009.11.005. View