Caveolae protect endothelial cells from membrane rupture during increased cardiac output

Journal of Cell Biology

Volumn 211, Issue 1, 2015, Pages 53-61

  Cheng, Jade P X ^a   Mendoza Topaz, Carolina ^a   Howard, Gillian ^a   Chadwick, Jessica ^a   Shvets, Elena ^a   Cowburn, Andrew S ^a   Dunmore, Benjamin J ^a   Crosby, Alexi ^a   Morrell, Nicholas W ^a   Nichols, Benjamin J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSAY; BIOCHEMICAL ASSAY; CAPILLARY ENDOTHELIAL CELL; CARDIAC MUSCLE; CAVEOLA; CELL CULTURE; CELL MEMBRANE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; FORCE; HEART OUTPUT; HEMODYNAMICS; IMAGING; IN VIVO STUDY; LUNG; MEMBRANE RUPTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TWO PHOTON IMAGING; ANIMAL; BIOMECHANICS; C57BL MOUSE; ENDOCYTOSIS; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; BIOMECHANICAL PHENOMENA; CARDIAC OUTPUT; CAVEOLAE; CAVEOLIN 1; CELL MEMBRANE; CELLS, CULTURED; ENDOCYTOSIS; ENDOTHELIAL CELLS; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84980350780     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201504042     Document Type: Article

References (47)

1. Albinsson, S., I. Nordström, K. Swärd, and P. Hellstrand. 2008. Differential dependence of stretch and shear stress signaling on caveolin-1 in the vascular wall. Am. J. Physiol. Cell Physiol. 294:C271-C279. http://dx.doi.org/10.1152/ajpcell.00297.2007
2. Andrews, N.W., P.E. Almeida, and M. Corrotte. 2014. Damage control: cellular mechanisms of plasma membrane repair. Trends Cell Biol. 24:734-742. http://dx.doi.org/10.1016Zj.tcb.2014.07.008
3. Ardissone, A., C. Bragato, L. Caffi, F. Blasevich, S. Maestrini, M.L. Bianchi, L. Morandi, I. Moroni, and M. Mora. 2013. Novel PTRF mutation in a child with mild myopathy and very mild congenital lipodystrophy. BMC Med. Genet. 14:89. http://dx.doi.org/10.1186/1471-2350-14-89
4. Austin, E.D., L. Ma, C. LeDuc, E. Berman Rosenzweig, A. Borczuk, J.A. Phillips III, T. Palomero, P. Sumazin, H.R. Kim, M.H. Talati, et al. 2012. Whole exome sequencing to identify a novel gene (caveolin-1) associated with human pulmonary arterial hypertension. Circ Cardiovasc Genet. 5:336-343. http://dx.doi.org/10.1161/CIRCGENETICS.111.961888
5. Bitsikas, V., I.R. Correa Jr., and B.J. Nichols. 2014. Clathrin-independent pathways do not contribute significantly to endocytic flux. eLife. 3:e03970.
6. Chang, S.H., D. Feng, J.A. Nagy, T.E. Sciuto, A.M. Dvorak, and H.F. Dvorak. 2009. Vascular permeability and pathological angiogenesis in caveolin-1-null mice. Am. J. Pathol. 175:1768-1776. http://dx.doi.org/10.2353/ajpath.2009.090171
7. Collins, B.M., M.J. Davis, J.F. Hancock, and R.G. Parton. 2012. Structure-based reassessment of the caveolin signaling model: do caveolae regulate signaling through caveolin-protein interactions? Dev. Cell. 23:11-20. http://dx.doi.org/10.1016/j.devcel.2012.06.012
8. Corrotte, M., P.E. Almeida, C. Tam, T. Castro-Gomes, M.C. Fernandes, B. A. Millis, M. Cortez, H. Miller, W. Song, T.K. Maugel, et al. 2013. Caveolae internalization repairs wounded cells and muscle fibers. eLife. 2:e00926. http://dx.doi.org/10.7554/eLife.00926
9. Cruz, J.A., E.M. Bauer, A.I. Rodriguez, A. Gangopadhyay, N.S. Zeineh, Y. Wang, S. Shiva, H.C. Champion, and P.M. Bauer. 2012. Chronic hypoxia induces right heart failure in caveolin-1-/-mice. Am. J. Physiol. Heart Circ. Physiol. 302:H2518-H2527. http://dx.doi.org/10.1152/ajpheart.01140.2011
10. del Pozo, M.A., N. Balasubramanian, N.B. Alderson, W.B. Kiosses, A. Grande-García, R.G. Anderson, and M.A. Schwartz. 2005. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat. Cell Biol. 7:901-908. http://dx.doi.org/10.1038/ncb1293
11. Desai, K.H., R. Sato, E. Schauble, G.S. Barsh, B.K. Kobilka, and D. Bernstein. 1997. Cardiovascular indexes in the mouse at rest and with exercise: new tools to study models of cardiac disease. Am. J. Physiol. 272:H1053-H1061.
12. Drab, M., P. Verkade, M. Elger, M. Kasper, M. Lohn, B. Lauterbach, J. Menne, C. Lindschau, F. Mende, F.C. Luft, et al. 2001. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science. 293:2449-2452. http://dx.doi.org/10.1126/science.1062688
13. Dulhunty, A.F., and C. Franzini-Armstrong. 1975. The relative contributions of the folds and caveolae to the surface membrane of frog skeletal muscle fibres at different sarcomere lengths. J. Physiol. 250:513-539. http://dx.doi.org/10.1113/jphysiol.1975.sp011068
14. Galbiati, F., J.A. Engelman, D. Volonte, X.L. Zhang, C. Minetti, M. Li, H. Hou Jr., B. Kneitz, W. Edelmann, and M.P. Lisanti. 2001a. Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and T-tubule abnormalities. J. Biol. Chem. 276:21425-21433. http://dx.doi.org/10.1074/jbc.M100828200
15. Galbiati, F., B. Razani, and M.P. Lisanti. 2001b. Caveolae and caveolin-3 in muscular dystrophy. Trends Mol. Med. 7:435-441. http://dx.doi.org/10.1016/S1471-4914(01)02105-0
16. Gambin, Y., N. Ariotti, K.A. McMahon, M. Bastiani, E. Sierecki, O. Kovtun, M.E. Polinkovsky, A. Magenau, W. Jung, S. Okano, et al. 2014. Singlemolecule analysis reveals self assembly and nanoscale segregation of two distinct cavin subcomplexes on caveolae. eLife. 3:e01434. http://dx.doi.org/10.7554/eLife.01434
17. García-Cardeña, G., P. Oh, J. Liu, J.E. Schnitzer, and W.C. Sessa. 1996. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc. Natl. Acad. Sci. USA. 93:6448-6453. http://dx.doi.org/10.1073/pnas.93.13.6448
18. Han, R. 2011. Muscle membrane repair and inflammatory attack in dysferlinopathy. Skelet. Muscle. 1:10.
19. Hansen, C.G., E. Shvets, G. Howard, K. Riento, and B.J. Nichols. 2013. Deletion of cavin genes reveals tissue-specific mechanisms for morphogenesis of endothelial caveolae. Nat. Commun. 4:1831. http://dx.doi.org/10.1038/ncomms2808
20. Hayer, A., M. Stoeber, C. Bissig, and A. Helenius. 2010. Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic. 11:361-382. http://dx.doi.org/10.1111/j.1600-0854.2009.01023.x
21. Hill, M.M., M. Bastiani, R. Luetterforst, M. Kirkham, A. Kirkham, S.J. Nixon, P. Walser, D. Abankwa, V.M. Oorschot, S. Martin, et al. 2008. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell. 132:113-124. http://dx.doi.org/10.1016/j.cell.2007.11.042
22. Jimenez, A.J., P. Maiuri, J. Lafaurie-Janvore, S. Divoux, M. Piel, and F. Perez. 2014. ESCRT machinery is required for plasma membrane repair. Science. 343:1247136. http://dx.doi.org/10.1126/science.1247136
23. Jones, L.J., and V.L. Singer. 2001. Fluorescence microplate-based assay for tumor necrosis factor activity using SYTOX Green stain. Anal. Biochem. 293:8-15. http://dx.doi.org/10.1006/abio.2001.5116
24. Joshi, B., M. Bastiani, S.S. Strugnell, C. Boscher, R.G. Parton, and I.R. Nabi. 2012. Phosphocaveolin-1 is a mechanotransducer that induces caveola biogenesis via Egr1 transcriptional regulation. J. Cell Biol. 199:425-435. http://dx.doi.org/10.1083/jcb.201207089
25. Lammerding, J., and R.T. Lee. 2007. Torn apart: membrane rupture in muscular dystrophies and associated cardiomyopathies. J. Clin. Invest. 117:1749-1752. http://dx.doi.org/10.1172/JC132686
26. Lee, J., and G.W. Schmid-Schonbein. 1995. Biomechanics of skeletal muscle capillaries: hemodynamic resistance, endothelial distensibility, and pseudopod formation. Ann. Biomed. Eng. 23:226-246. http://dx.doi.org/10.1007/BF02584425
27. Liu, L., and P.F. Pilch. 2008. A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J. Biol. Chem. 283:4314-4322. http://dx.doi.org/10.1074/jbc.M707890200
28. Liu, L., D. Brown, M. McKee, N.K. Lebrasseur, D. Yang, K.H. Albrecht, K. Ravid, and P.F. Pilch. 2008. Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab. 8:310-317. http://dx.doi.org/10.1016Zj.cmet.2008.07.008
29. Ludwig, A., G. Howard, C. Mendoza-Topaz, T. Deerinck, M. Mackey, S. Sandin, M.H. Ellisman, and B.J. Nichols. 2013. Molecular composition and ultrastructure of the caveolar coat complex. PLoS Biol. 11:e1001640. http://dx.doi.org/10.1371/journal.pbio.1001640
30. Marcovitz, P.A., and W.F. Armstrong. 1991. Dobutamine stress echocardiography: diagnostic utility. Herz. 16:372-378.
31. Mathew, R. 2014. Pathogenesis of pulmonary hypertension: a case for caveolin-1 and cell membrane integrity. Am. J. Physiol. Heart Circ. Physiol. 306:H15-H25.
32. Oh, P., P. Borgstrom, H. Witkiewicz, Y. Li, B.J. Borgstrom, A. Chrastina, K. Iwata, K.R. Zinn, R. Baldwin, J.E. Testa, et al. 2007. Live dynamic imaging of caveolae pumping targeted antibody rapidly and specifically across endothelium in the lung. Nat. Biotechnol. 25:327-337. http://dx.doi.org/10.1038/nbt1292
33. Parker, S., H.S. Peterkin, and H.A. Baylis. 2007. Muscular dystrophy associated mutations in caveolin-1 induce neurotransmission and locomotion defects in Caenorhabditis elegans. Invert. Neurosci. 7:157-164. http://dx.doi.org/10.1007/s10158-007-0051-5
34. Parton, R.G., and M.A. del Pozo. 2013. Caveolae as plasma membrane sensors, protectors and organizers. Nat. Rev Mol. Cell Biol. 14:98-112. http://dx.doi.org/10.1038/nrm3512
35. Parton, R.G., and K. Simons. 2007. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8:185-194. http://dx.doi.org/10.1038/nrm2122
36. Pilch, P.F., and L. Liu. 2011. Fat caves: caveolae, lipid trafficking and lipid metabolism in adipocytes. Trends Endocrinol. Metab. 22:318-324. http://dx.doi.org/10.1016/j.tem.2011.04.001
37. Predescu, S.A., D.N. Predescu, and A.B. Malik. 2007. Molecular determinants of endothelial transcytosis and their role in endothelial permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 293:L823-L842. http://dx.doi.org/10.1152/ajplung.00436.2006
38. Rajab, A., V. Straub, L.J. McCann, D. Seelow, R. Varon, R. Barresi, A. Schulze, B. Lucke, S. Lützkendorf, M. Karbasiyan, et al. 2010. Fatal cardiac arrhythmia and long-QT syndrome in a new form of congenital generalized lipodystrophy with muscle rippling (CGL4) due to PTRF-CAVIN mutations. PLoS Genet. 6:e1000874. http://dx.doi.org/10.1371/journal.pgen.1000874
39. Razani, B., J.A. Engelman, X.B. Wang, W. Schubert, X.L. Zhang, C.B. Marks, F. Macaluso, R.G. Russell, M. Li, R.G. Pestell, et al. 2001. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J. Biol. Chem. 276:38121-38138.
40. Schubert, W., P.G. Frank, S.E. Woodman, H. Hyogo, D.E. Cohen, C.W. Chow, and M.P. Lisanti. 2002. Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice. Treatment with a specific nitric-oxide synthase inhibitor, L-NAME, restores normal microvascular permeability in Cav-1 null mice. J. Biol. Chem. 277:40091-40098. http://dx.doi.org/10.1074/jbc.M205948200
41. Shvets, E., V. Bitsikas, G. Howard, C.G. Hansen, and B.J. Nichols. 2015. Dynamic caveolae exclude bulk membrane proteins and are required for sorting of excess glycosphingolipids. Nat. Commun. 6:6867. http://dx.doi.org/10.1038/ncomms7867
42. Siddiqui, M.R., Y.A. Komarova, S.M. Vogel, X. Gao, M.G. Bonini, J. Rajasingh, Y.Y. Zhao, V. Brovkovych, and A.B. Malik. 2011. Caveolin-1-eNOS signaling promotes p190RhoGAP-A nitration and endothelial permeability. J. Cell Biol. 193:841-850. http://dx.doi.org/10.1083/jcb.201012129
43. Sinha, B., D. Köster, R. Ruez, P. Gonnord, M. Bastiani, D. Abankwa, R.V. Stan, G. Butler-Browne, B. Vedie, L. Johannes, et al. 2011. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell. 144:402-413. http://dx.doi.org/10.1016/j.cell.2010.12.031
44. Tse, D., and R.V. Stan. 2010. Morphological heterogeneity of endothelium. Semin. Thromb. Hemost. 36:236-245. http://dx.doi.org/10.1055/s-0030-1253447
45. 14) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress. J. Biol. Chem. 276:8094-8103. http://dx.doi.org/10.1074/jbc.M009245200
46. Woodman, S.E., F. Sotgia, F. Galbiati, C. Minetti, and M.P. Lisanti. 2004. Caveolinopathies: mutations in caveolin-3 cause four distinct autosomal dominant muscle diseases. Neurology. 62:538-543. http://dx.doi.org/10.1212/WNL.62.4.538
47. Zhao, Y.Y., Y Liu, R.V. Stan, L. Fan, Y. Gu, N. Dalton, PH. Chu, K. Peterson, J. Ross Jr., and K.R. Chien. 2002. Defects in caveolin-1 cause dilated cardiomyopathy and pulmonary hypertension in knockout mice. Proc. Natl. Acad. Sci. USA. 99:11375-11380. http://dx.doi.org/10.1073/pnas.172360799