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Role of the Endocytosis of Caveolae in Intracellular Signaling and Metabolism

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Endocytosis and Signaling

Part of the book series: Progress in Molecular and Subcellular Biology ((PMSB,volume 57))

Abstract

Caveolae are 60–80 nm invaginated plasma membrane (PM) nanodomains, with a specific lipid and protein composition, which assist and regulate multiple processes in the plasma membrane—ranging from the organization of signalling complexes to the mechanical adaptation to changes in PM tension. However, since their initial descriptions, these structures have additionally been found tightly linked to internalization processes, mechanoadaptation, to the regulation of signalling events and of endosomal trafficking. Here, we review caveolae biology from this perspective, and its implications for cell physiology and disease.

Muriel, Sánchez-Álvarez, Strippoli—These authors contributed equally to this work.

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References

  • Aboulaich N, Vainonen JP, Stralfors P, Vener AV (2004) Vectorial proteomics reveal targeting, phosphorylation and specific fragmentation of polymerase I and transcript release factor (PTRF) at the surface of caveolae in human adipocytes. Biochem J 383:237–248

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Abulrob A, Giuseppin S, Andrade MF, McDermid A, Moreno M, Stanimirovic D (2004) Interactions of EGFR and caveolin-1 in human glioblastoma cells: evidence that tyrosine phosphorylation regulates EGFR association with caveolae. Oncogene 23:6967–6979

    Article  PubMed  CAS  Google Scholar 

  • Almeida RA, Dunlap JR, Oliver SP (2010) Binding of host factors influences internalization and intracellular trafficking of streptococcus uberis in bovine mammary epithelial cells. Vet Med Int 2010:319192

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Anderson RG (1998) The caveolae membrane system. Annu Rev Biochem 67:199–225

    Article  PubMed  CAS  Google Scholar 

  • Ariotti N, Fernandez-Rojo MA, Zhou Y, Hill MM, Rodkey TL, Inder KL, Tanner LB, Wenk MR, Hancock JF, Parton RG (2014) Caveolae regulate the nanoscale organization of the plasma membrane to remotely control Ras signaling. J Cell Biol 204:777–792

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ariotti N, Rae J, Leneva N, Ferguson C, Loo D, Okano S, Hill MM, Walser P, Collins BM, Parton RG (2015) Molecular characterization of caveolin-induced membrane curvature. J Biol Chem 290:24875–24890

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bai L, Deng X, Li J, Wang M, Li Q, An WAD, Cong YS (2011) Regulation of cellular senescence by the essential caveolar component PTRF/Cavin-1. Cell Res 21:1088–1101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bass MD, Williamson RC, Nunan RD, Humphries JD, Byron A, Morgan MR, Martin P, Humphries MJ (2011) A syndecan-4 hair trigger initiates wound healing through caveolin- and RhoG-regulated integrin endocytosis. Dev Cell 21:681–693

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bastiani M, Liu L, Hill MM, Jedrychowski MP, Nixon SJ, Lo HP, Abankwa D, Luetterforst R, Fernandez-Rojo M, Breen MR, Gygi SP, Vinten J, Walser PJ, North KN, Hancock JF, Pilch PF, Parton RG (2009) MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol 185:1259–1273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Benga L, Goethe R, Rohde M, Valentin-Weigand P (2004) Non-encapsulated strains reveal novel insights in invasion and survival of Streptococcus suis in epithelial cells. Cell Microbiol 6:867–881

    Article  PubMed  CAS  Google Scholar 

  • Bernatchez PN, Bauer PM, Yu J, Prendergast JS, He P, Sessa WC (2005) Dissecting the molecular control of endothelial NO synthase by caveolin-1 using cell-permeable peptides. Proc Natl Acad Sci USA 102:761–766

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bitsikas V, Correa IR, Jr., Nichols BJ (2014) Clathrin-independent pathways do not contribute significantly to endocytic flux. eLife 3:e03970

    Google Scholar 

  • Bosch M, Mari M, Gross SP, Fernandez-Checa JC, Pol A (2011a) Mitochondrial cholesterol: a connection between caveolin, metabolism, and disease. Traffic 12:1483–1489

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bosch M, Mari M, Herms A, Fernandez A, Fajardo A, Kassan A, Giralt A, Colell A, Balgoma D, Barbero E, Gonzalez-Moreno E, Matias N, Tebar F, Balsinde J, Camps M, Enrich C, Gross SP, Garcia-Ruiz C, Perez-Navarro E, Fernandez-Checa JC et al (2011b) Caveolin-1 deficiency causes cholesterol-dependent mitochondrial dysfunction and apoptotic susceptibility. Current Biol 21:681–686

    Article  CAS  Google Scholar 

  • Boucrot E, Howes MT, Kirchhausen T, Parton RG (2011) Redistribution of caveolae during mitosis. J Cell Sci 124:1965–1972

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bruno C, Sotgia F, Gazzerro M, Minetti C, Lisanti MP (1993) Caveolinopathies. Synonym: Caveolin-3 Deficiency. GeneReviews- University of Washington, Seattle. PMID: 20301559

    Google Scholar 

  • Bucci M, Gratton JP, Rudic RD, Acevedo L, Roviezzo F, Cirino G, Sessa WC (2000) In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat Med 6:1362–1367

    Article  PubMed  CAS  Google Scholar 

  • Burgermeister E, Friedrich T, Hitkova I, Regel I, Einwachter H, Zimmermann W, Rocken C, Perren A, Wright MB, Schmid RM, Seger R, Ebert MP (2011) The Ras inhibitors caveolin-1 and docking protein 1 activate peroxisome proliferator-activated receptor gamma through spatial relocalization at helix 7 of its ligand-binding domain. Mol Cell Biol 31:3497–3510

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Byrne DP, Dart C, Rigden DJ (2012) Evaluating caveolin interactions: do proteins interact with the caveolin scaffolding domain through a widespread aromatic residue-rich motif? PLoS ONE 7:e44879

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cao H, Courchesne WE, Mastick CC (2002) A phosphotyrosine-dependent protein interaction screen reveals a role for phosphorylation of caveolin-1 on tyrosine 14: Recruitment of C- terminal Src kinase. J Biol Chem 22:22

    Google Scholar 

  • Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, Nagle J, Polymeropoulos MH, Sturley SL, Ioannou YA, Higgins ME, Comly M, Cooney A, Brown A, Kaneski CR, Blanchette-Mackie EJ et al (1997) Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277:228–231

    Article  PubMed  CAS  Google Scholar 

  • Cerezo A, Guadamillas MC, Goetz JG, Sanchez-Perales S, Klein E, Assoian RK, del Pozo MA (2009) The absence of caveolin-1 increases proliferation and anchorage- independent growth by a Rac-dependent, Erk-independent mechanism. Mol Cell Biol 29:5046–5059

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Collins BM, Davis MJ, Hancock JF, Parton RG (2012) Structure-based reassessment of the caveolin signaling model: do caveolae regulate signaling through caveolin-protein interactions? Dev Cell 23:11–20

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Conrad PA, Smart EJ, Ying YS, Anderson RG, Bloom GS (1995) Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J Cell Biol 131:1421–1433

    Article  PubMed  CAS  Google Scholar 

  • Cota CD, Davidson B (2015) Mitotic membrane turnover coordinates differential induction of the heart progenitor lineage. Dev Cell 34:505–519

    Article  PubMed  CAS  Google Scholar 

  • Couet J, Sargiacomo M, Lisanti MP (1997) Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J Biol Chem 272:30429–30438

    Article  PubMed  CAS  Google Scholar 

  • Czarny M, Schnitzer JE (2004) Neutral sphingomyelinase inhibitor scyphostatin prevents and ceramide mimics mechanotransduction in vascular endothelium. Am J Physiol Heart Circ Physiol 287:H1344–H1352

    Article  PubMed  CAS  Google Scholar 

  • Chaudhary N, Gomez GA, Howes MT, Lo HP, McMahon KA, Rae JA, Schieber NL, Hill MM, Gaus K, Yap AS, Parton RG (2014) Endocytic crosstalk: cavins, caveolins, and caveolae regulate clathrin-independent endocytosis. PLoS Biol 12:e1001832

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen XW, Wang H, Bajaj K, Zhang P, Meng ZX, Ma D, Bai Y, Liu HH, Adams E, Baines A, Yu G, Sartor MA, Zhang B, Yi Z, Lin J, Young SG, Schekman R, Ginsburg D (2013) SEC24A deficiency lowers plasma cholesterol through reduced PCSK9 secretion. eLife 2:e00444

    Google Scholar 

  • Cheng JP, Nichols BJ (2016) Caveolae: one function or many? Trends Cell Biol 26:177–189

    Article  PubMed  CAS  Google Scholar 

  • Chevallier J, Chamoun Z, Jiang G, Prestwich G, Sakai N, Matile S, Parton RG, Gruenberg J (2008) Lysobisphosphatidic acid controls endosomal cholesterol levels. J Biol Chem 283:27871–27880

    Article  PubMed  CAS  Google Scholar 

  • Chidlow JH Jr, Sessa WC (2010) Caveolae, caveolins, and cavins: complex control of cellular signalling and inflammation. Cardiovasc Res 86:219–225

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Damm EM, Pelkmans L, Kartenbeck J, Mezzacasa A, Kurzchalia T, Helenius A (2005) Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168:477–488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, McMahon HT (2007) Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449:923–927

    Article  PubMed  CAS  Google Scholar 

  • Del Galdo F, Lisanti MP, Jimenez SA (2008) Caveolin-1, transforming growth factor-beta receptor internalization, and the pathogenesis of systemic sclerosis. Curr Opin Rheumatol 20:713–719

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • del Pozo MA, Balasubramanian N, Alderson NB, Kiosses WB, Grande-Garcia A, Anderson RG, Schwartz MA (2005) Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat Cell Biol 7:901–908

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Del Pozo MA, Schwartz MA (2007) Rac, membrane heterogeneity, caveolin and regulation of growth by integrins. Trends Cell Biol 17:246–250

    Article  PubMed  CAS  Google Scholar 

  • Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL (2003) Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 5:410–421

    Article  PubMed  CAS  Google Scholar 

  • Dietzen DJ, Hastings WR, Lublin DM (1995) Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae. J Biol Chem 270:6838–6842

    Article  PubMed  CAS  Google Scholar 

  • Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV (2001) Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293:2449–2452

    Article  PubMed  CAS  Google Scholar 

  • Dupree P, Parton RG, Raposo G, Kurzchalia TV, Simons K (1993) Caveolae and sorting in the trans-Golgi network of epithelial cells. EMBO J 12:1597–1605

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Echarri A, Del Pozo MA (2015) Caveolae - mechanosensitive membrane invaginations linked to actin filaments. J C Sci

    Google Scholar 

  • Echarri A, Muriel O, Del Pozo MA (2007) Intracellular trafficking of raft/caveolae domains: insights from integrin signaling. Semin Cell Dev Biol 18:627–637

    Article  PubMed  CAS  Google Scholar 

  • Echarri A, Muriel O, Pavon DM, Azegrouz H, Escolar F, Terron MC, Sanchez-Cabo F, Martinez F, Montoya MC, Llorca O, Del Pozo MA (2012) Caveolar domain organization and trafficking is regulated by Abl kinases and mDia1. J Cell Sci 125:3097–3113

    Article  PubMed  CAS  Google Scholar 

  • Eden ER, Sanchez-Heras E, Tsapara A, Sobota A, Levine TP, Futter CE (2016) Annexin A1 tethers membrane contact sites that mediate ER to endosome cholesterol transport. Dev Cell 37:473–483

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ewers H, Romer W, Smith AE, Bacia K, Dmitrieff S, Chai W, Mancini R, Kartenbeck J, Chambon V, Berland L, Oppenheim A, Schwarzmann G, Feizi T, Schwille P, Sens P, Helenius A, Johannes L (2010) GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 12(Supplementary 11–18):1–12

    Google Scholar 

  • Feng S, Wang Y, Wang X, Wang Z, Cui Y, Liu J, Zhao C, Jin M, Zou W (2010) Caveolin-1 gene silencing promotes the activation of PI3K/AKT dependent on Erα36 and the transformation of MCF10ACE. Sci China Life Sci 53:598–605

    Article  PubMed  CAS  Google Scholar 

  • Feron O, Belhassen L, Kobzik L, Smith TW, Kelly RA, Michel T (1996) Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem 271:22810–22814

    Article  PubMed  CAS  Google Scholar 

  • Frank PG, Lee H, Park DS, Tandon NN, Scherer PE, Lisanti MP (2004) Genetic ablation of caveolin-1 confers protection against atherosclerosis. Arterioscler Thromb Vasc Biol 24:98–105

    Article  PubMed  CAS  Google Scholar 

  • Frank PG, Pavlides S, Lisanti MP (2009) Caveolae and transcytosis in endothelial cells: role in atherosclerosis. Cell Tissue Res 335:41–47

    Article  PubMed  CAS  Google Scholar 

  • Fu Y, Hoang A, Escher G, Parton RG, Krozowski Z, Sviridov D (2004) Expression of caveolin-1 enhances cholesterol efflux in hepatic cells. J Biol Chem 279:14140–14146

    Article  PubMed  CAS  Google Scholar 

  • Fujita A, Cheng J, Tauchi-Sato K, Takenawa T, Fujimoto T (2009) A distinct pool of phosphatidylinositol 4,5-bisphosphate in caveolae revealed by a nanoscale labeling technique. Proc Natl Acad Sci USA 106:9256–9561

    Article  PubMed  PubMed Central  Google Scholar 

  • Galbiati F, Volonte D, Engelman JA, Watanabe G, Burk R, Pestell RG, Lisanti MP (1998) Targeted downregulation of caveolin-1 is sufficient to drive cell transformation and hyperactivate the p42/44 MAP kinase cascade. EMBO J 17:6633–6648

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garcia-Cardena G, Oh P, Liu J, Schnitzer JE, Sessa WC (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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Glenney JR Jr (1989) Tyrosine phosphorylation of a 22-kDa protein is correlated with transformation by Rous sarcoma virus. J Biol Chem 264:20163–20166

    PubMed  CAS  Google Scholar 

  • Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E, Tello M, Osteso-Ibanez T, Pellinen T, Echarri A, Cerezo A, Klein-Szanto AJ, Garcia R, Keely PJ, Sanchez-Mateos P, Cukierman E, Del Pozo MA (2011) Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 146:148–163

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gottlieb-Abraham E, Shvartsman DE, Donaldson JC, Ehrlich M, Gutman O, Martin GS, Henis YI (2013) Src-mediated caveolin-1 phosphorylation affects the targeting of active Src to specific membrane sites. Mol Biol Cell 24:3881–3895

    Article  PubMed  PubMed Central  Google Scholar 

  • Grande-Garcia A, Echarri A, de Rooij J, Alderson NB, Waterman-Storer CM, Valdivielso JM, del Pozo MA (2007) Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J Cell Biol 177:683–694

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guan JL (2004) Cell biology. Integrins, rafts, Rac, and Rho. Science 303:773–774

    Article  PubMed  CAS  Google Scholar 

  • Hansen CG, Bright NA, Howard G, Nichols BJ (2009) SDPR induces membrane curvature and functions in the formation of caveolae. Nat Cell Biol 11:807–814

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hansen CG, Howard G, Nichols BJ (2011) Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis. J Cell Sci 124:2777–2785

    Article  PubMed  CAS  Google Scholar 

  • Hansen CG, Shvets E, Howard G, Riento K, Nichols BJ (2013) Deletion of cavin genes reveals tissue-specific mechanisms for morphogenesis of endothelial caveolae. Nat Communications 4:1831

    Article  CAS  Google Scholar 

  • Hasegawa T, Takeuchi A, Miyaishi O, Xiao H, Mao J, Isobe K (2000) PTRF (polymerase I and transcript-release factor) is tissue-specific and interacts with the BFCOL1 (binding factor of a type-I collagen promoter) zinc-finger transcription factor which binds to the two mouse type-I collagen gene promoters. Biochem J 347(Pt 1):55–59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayer A, Stoeber M, Bissig C, Helenius A (2010a) Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 11:361–382

    Article  PubMed  CAS  Google Scholar 

  • Hayer A, Stoeber M, Ritz D, Engel S, Meyer HH, Helenius A (2010b) Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J Cell Biol 191:615–629

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • He K, Yan X, Li N, Dang S, Xu L, Zhao B, Li Z, Lv Z, Fang X, Zhang Y, Chen YG (2015) Internalization of the TGF-beta type I receptor into caveolin-1 and EEA1 double-positive early endosomes. Cell Res 25:738–752

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Head BP, Patel HH, Roth DM, Murray F, Swaney JS, Niesman IR, Farquhar MG, Insel PA (2006) Microtubules and actin microfilaments regulate lipid raft/caveolae localization of adenylyl cyclase signaling components. J Biol Chem 281:26391–26399

    Article  PubMed  CAS  Google Scholar 

  • Henley JR, Krueger EW, Oswald BJ, McNiven MA (1998) Dynamin-mediated internalization of caveolae. J Cell Biol 141:85–99

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hernandez VJ, Weng J, Ly P, Pompey S, Dong H, Mishra L, Schwarz M, Anderson RG, Michaely P (2013) Cavin-3 dictates the balance between ERK and Akt signaling. eLife 2:e00905

    Google Scholar 

  • Hertzog M, Monteiro P, Le Dez G, Chavrier P (2012) Exo70 subunit of the exocyst complex is involved in adhesion-dependent trafficking of caveolin-1. PLoS ONE 7:e52627

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hill MM, Bastiani M, Luetterforst R, Kirkham M, Kirkham A, Nixon SJ, Walser P, Abankwa D, Oorschot VM, Martin S, Hancock JF, Parton RG (2008) PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132:113–124

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoernke M, Mohan J, Larsson E, Blomberg J, Kahra D, Westenhoff S, Schwieger C, Lundmark R (2017) EHD2 restrains dynamics of caveolae by an ATP-dependent, membrane-bound, open conformation. Proc Natl Acad Sci USA 114:E4360–E4369

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Howe AK, Juliano RL (2000) Regulation of anchorage-dependent signal transduction by protein kinase A and p21-activated kinase. Nat Cell Biol 2:593–600

    Article  PubMed  CAS  Google Scholar 

  • Ishibashi S, Brown MS, Goldstein JL, Gerard RD, Hammer RE, Herz J (1993) Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest 92:883–893

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Izumi Y, Hirai S, Tamai Y, Fujise-Matsuoka A, Nishimura Y, Ohno S (1997) A protein kinase Cδ-binding protein SRBC whose expression is induced by serum starvation. J Biol Chem 272:7381–7389

    Article  PubMed  CAS  Google Scholar 

  • Jansa P, Mason SW, Hoffmann-Rohrer U, Grummt I (1998) Cloning and functional characterization of PTRF, a novel protein which induces dissociation of paused ternary transcription complexes. EMBO J 17:2855–2864

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joshi B, Bastiani M, Strugnell SS, Boscher C, Parton RG, Nabi IR (2012) Phosphocaveolin-1 is a mechanotransducer that induces caveola biogenesis via Egr1 transcriptional regulation. J Cell Biol 199:425–435

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang YS, Ko YG, Seo JS (2000) Caveolin internalization by heat shock or hyperosmotic shock. Exp Cell Res 255:221–228

    Article  PubMed  CAS  Google Scholar 

  • Kim CA, Delepine M, Boutet E, El Mourabit H, Le Lay S, Meier M, Nemani M, Bridel E, Leite CC, Bertola DR, Semple RK, O’Rahilly S, Dugail I, Capeau J, Lathrop M, Magre J (2008) Association of a homozygous nonsense caveolin-1 mutation with Berardinelli-Seip congenital lipodystrophy. J Clin Endocrinol Metab 93:1129–1134

    Article  PubMed  CAS  Google Scholar 

  • Kirkham M, Fujita A, Chadda R, Nixon SJ, Kurzchalia TV, Sharma DK, Pagano RE, Hancock JF, Mayor S, Parton RG (2005) Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J Cell Biol 168:465–476

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kirkham M, Nixon SJ, Howes MT, Abi-Rached L, Wakeham DE, Hanzal-Bayer M, Ferguson C, Hill MM, Fernandez-Rojo M, Brown DA, Hancock JF, Brodsky FM, Parton RG (2008) Evolutionary analysis and molecular dissection of caveola biogenesis. J Cell Sci 121:2075–2086

    Article  PubMed  CAS  Google Scholar 

  • Koch D, Westermann M, Kessels MM, Qualmann B (2012) Ultrastructural freeze-fracture immunolabeling identifies plasma membrane-localized syndapin II as a crucial factor in shaping caveolae. Histochem Cell Biol 138:215–230

    Article  PubMed  CAS  Google Scholar 

  • Kozera L, White E, Calaghan S (2009) Caveolae act as membrane reserves which limit mechanosensitive I(Cl, swell) channel activation during swelling in the rat ventricular myocyte. PLoS ONE 4:e8312

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kurzchalia TV, Parton RG (1999) Membrane microdomains and caveolae. Curr Opin Cell Biol 11:424–431

    Article  PubMed  CAS  Google Scholar 

  • Labrecque L, Nyalendo C, Langlois S, Durocher Y, Roghi C, Murphy G, Gingras D, Beliveau R (2004) Src-mediated tyrosine phosphorylation of caveolin-1 induces its association with membrane type 1 matrix metalloproteinase. J Biol Chem 279:52132–52140

    Article  PubMed  CAS  Google Scholar 

  • Lai YC, Kondapalli C, Lehneck R, Procter JB, Dill BD, Woodroof HI, Gourlay R, Peggie M, Macartney TJ, Corti O, Corvol JC, Campbell DG, Itzen A, Trost M, Muqit MM (2015) Phosphoproteomic screening identifies Rab GTPases as novel downstream targets of PINK1. EMBO J 34:2840–2861

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lajoie P, Partridge EA, Guay G, Goetz JG, Pawling J, Lagana A, Joshi B, Dennis JW, Nabi IR (2007) Plasma membrane domain organization regulates EGFR signaling in tumor cells. J Cell Biology 179:341–356

    Article  CAS  Google Scholar 

  • Lamaze C, Tardif N, Dewulf M, Vassilopoulos S, Blouin CM (2017) The caveolae dress code: structure and signaling. Curr Opin Cell Biol 47:117–125

    Article  PubMed  CAS  Google Scholar 

  • Lamaze C, Torrino S (2015) Caveolae and cancer: a new mechanical perspective. Biomed J 38:367–379

    Article  PubMed  Google Scholar 

  • Lang AB, John Peter AT, Walter P, Kornmann B (2015) ER-mitochondrial junctions can be bypassed by dominant mutations in the endosomal protein Vps13. J Cell Biol 210:883–890

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lapierre LA, Ducharme NA, Drake KR, Goldenring JR, Kenworthy AK (2012) Coordinated regulation of caveolin-1 and Rab11a in apical recycling compartments of polarized epithelial cells. Exp Cell Res 318:103–113

    Article  PubMed  CAS  Google Scholar 

  • Le Roy C, Wrana JL (2005) Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 6:112–126

    Article  PubMed  CAS  Google Scholar 

  • Lee H, Volonte D, Galbiati F, Iyengar P, Lublin DM, Bregman DB, Wilson MT, Campos-Gonzalez R, Bouzahzah B, Pestell RG, Scherer PE, Lisanti MP (2000) Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol Endocrinol 14:1750–1775

    Article  PubMed  CAS  Google Scholar 

  • Lee H, Xie L, Luo Y, Lee SY, Lawrence DS, Wang XB, Sotgia F, Lisanti MP, Zhang ZY (2006) Identification of phosphocaveolin-1 as a novel protein tyrosine phosphatase 1B substrate. Biochemistry 45:234–240

    Article  PubMed  CAS  Google Scholar 

  • Li G, D’Souza-Schorey C, Barbieri MA, Roberts RL, Klippel A, Williams LT, Stahl PD (1995) Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. Proc Natl Acad Sci USA 92:10207–10211

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li S, Couet J, Lisanti MP (1996) Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J Biol Chem 271:29182–29190

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Pilch PF (2008) A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J Biol Chem 283:4314–4322

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Brown D, McKee M, Lebrasseur NK, Yang D, Albrecht KH, Ravid K, Pilch PF (2008) Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab 8:310–317

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu L, Pilch PF (2016) PTRF/Cavin-1 promotes efficient ribosomal RNA transcription in response to metabolic challenges. eLife 5

    Google Scholar 

  • Lu Z, Ghosh S, Wang Z, Hunter T (2003) Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 4:499–515

    Article  PubMed  CAS  Google Scholar 

  • Ludwig A, Howard G, Mendoza-Topaz C, Deerinck T, Mackey M, Sandin S, Ellisman MH, Nichols BJ (2013) Molecular composition and ultrastructure of the caveolar coat complex. PLoS Biol 11:e1001640

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ludwig A, Nichols BJ, Sandin S (2016) Architecture of the caveolar coat complex. J Cell Sci 129:3077–3083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mari M, Morales A, Colell A, Garcia-Ruiz C, Fernandez-Checa JC (2009) Mitochondrial glutathione, a key survival antioxidant. Antioxid Redox Signal 11:2685–2700

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maxwell KN, Breslow JL (2005) Proprotein convertase subtilisin kexin 9: the third locus implicated in autosomal dominant hypercholesterolemia. Curr Opin Lipidol 16:167–172

    Article  PubMed  CAS  Google Scholar 

  • Maxwell KN, Fisher EA, Breslow JL (2005) Overexpression of PCSK9 accelerates the degradation of the LDLR in a post-endoplasmic reticulum compartment. Proc Natl Acad Sci USA 102:2069–2074

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McLelland GL, Soubannier V, Chen CX, McBride HM, Fon EA (2014) Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J 33:282–295

    PubMed  PubMed Central  CAS  Google Scholar 

  • McMahon KA, Zajicek H, Li WP, Peyton MJ, Minna JD, Hernandez VJ, Luby-Phelps K, Anderson RG (2009) SRBC/cavin-3 is a caveolin adapter protein that regulates caveolae function. EMBO J 28:1001–1015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mercier I, Jasmin JF, Pavlides S, Minetti C, Flomenberg N, Pestell RG, Frank PG, Sotgia F, Lisanti MP (2009) Clinical and translational implications of the caveolin gene family: lessons from mouse models and human genetic disorders. Lab Invest 89:614–623

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mercier I, Camacho J, Titchen K, Gonzales DM, Quann K, Bryant KG, Molchansky A, Milliman JN, Whitaker-Menezes D, Sotgia F, Jasmin JF, Schwarting R, Pestell RG, Blagosklonny MV, Lisanti MP (2012) Caveolin-1 and accelerated host aging in the breast tumor microenvironment: chemoprevention with rapamycin, an mTOR inhibitor and anti-aging drug. Am J Pathol 181:278–293

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Michel JB, Feron O, Sase K, Prabhakar P, Michel T (1997) Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. J Biol Chem 272:25907–25912

    Article  PubMed  CAS  Google Scholar 

  • Mineo C, Ying YS, Chapline C, Jaken S, Anderson RG (1998) Targeting of protein kinase Calpha to caveolae. J Cell Biol 141:601–610

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Minshall RD, Tiruppathi C, Vogel SM, Niles WD, Gilchrist A, Hamm HE, Malik AB (2000) Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i)-coupled Src kinase signaling pathway. J Cell Biol 150:1057–1070

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mohan J, Moren B, Larsson E, Holst MR, Lundmark R (2015) Cavin3 interacts with cavin1 and caveolin1 to increase surface dynamics of caveolae. J Cell Sci 128:979–991

    Article  PubMed  CAS  Google Scholar 

  • Monier S, Dietzen DJ, Hastings WR, Lublin DM, Kurzchalia TV (1996) Oligomerization of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol. FEBS Lett 388:143–149

    Article  PubMed  CAS  Google Scholar 

  • Monier S, Parton RG, Vogel F, Behlke J, Henske A, Kurzchalia TV (1995) VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol Biol Cell 6:911–927

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moren B, Shah C, Howes MT, Schieber NL, McMahon HT, Parton RG, Daumke O, Lundmark R (2012) EHD2 regulates caveolar dynamics via ATP-driven targeting and oligomerization. Mol Biol Cell 23:1316–1329

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moreno-Caceres J, Caja L, Mainez J, Mayoral R, Martin-Sanz P, Moreno-Vicente R, Del Pozo MA, Dooley S, Egea G, Fabregat I (2014) Caveolin-1 is required for TGF-beta-induced transactivation of the EGF receptor pathway in hepatocytes through the activation of the metalloprotease TACE/ADAM17. Cell Death Dis 5:e1326

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mundy DI, Machleidt T, Ying YS, Anderson RG, Bloom GS (2002) Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J Cell Sci 115:4327–4339

    Article  PubMed  CAS  Google Scholar 

  • Murata T, Lin MI, Huang Y, Yu J, Bauer PM, Giordano FJ, Sessa WC (2007) Reexpression of caveolin-1 in endothelium rescues the vascular, cardiac, and pulmonary defects in global caveolin-1 knockout mice. J Exp Med 204:2373–2382

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Muriel O, Echarri A, Hellriegel C, Pavon DM, Beccari L, Del Pozo MA (2011) Phosphorylated filamin A regulates actin-linked caveolae dynamics. J Cell Sci 124:2763–2776

    Article  PubMed  CAS  Google Scholar 

  • Musiol A, Gran S, Ehrhardt C, Ludwig S, Grewal T, Gerke V, Rescher U (2013) Annexin A6-balanced late endosomal cholesterol controls influenza A replication and propagation. MBio 4:e00608–e00613

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nabi IR (2009) Cavin fever: regulating caveolae. Nat Cell Biol 11:789–791

    Article  PubMed  CAS  Google Scholar 

  • Nakanishi N, Ogata T, Naito D, Miyagawa K, Taniguchi T, Hamaoka T, Maruyama N, Kasahara T, Nishi M, Matoba S, Ueyama T (2016) MURC deficiency in smooth muscle attenuates pulmonary hypertension. Nat Commun 7:12417

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nassoy P, Lamaze C (2012) Stressing caveolae new role in cell mechanics. Trends Cell Biol 22:381–389

    Article  PubMed  Google Scholar 

  • Nichols B (2003) Caveosomes and endocytosis of lipid rafts. J Cell Sci 116:4707–4714

    Article  PubMed  CAS  Google Scholar 

  • Nixon SJ, Carter A, Wegner J, Ferguson C, Floetenmeyer M, Riches J, Key B, Westerfield M, Parton RG (2007) Caveolin-1 is required for lateral line neuromast and notochord development. J Cell Sci 120:2151–2161

    Article  PubMed  CAS  Google Scholar 

  • Norambuena A, Schwartz MA (2011) Effects of integrin-mediated cell adhesion on plasma membrane lipid raft components and signaling. Mol Biol Cell 22:3456–3464

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nystrom FH, Chen H, Cong LN, Li Y, Quon MJ (1999) Caveolin-1 interacts with the insulin receptor and can differentially modulate insulin signaling in transfected Cos-7 cells and rat adipose cells. Mol Endocrinol 13:2013–2024

    Article  PubMed  CAS  Google Scholar 

  • Ogata T, Ueyama T, Isodono K, Tagawa M, Takehara N, Kawashima T, Harada K, Takahashi T, Shioi T, Matsubara H, Oh H (2008) MURC, a muscle-restricted coiled-coil protein that modulates the Rho/ROCK pathway, induces cardiac dysfunction and conduction disturbance. Mol Cell Biol 28:3424–3436

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ogata T, Naito D, Nakanishi N, Hayashi YK, Taniguchi T, Miyagawa K, Hamaoka T, Maruyama N, Matoba S, Ikeda K, Yamada H, Oh H, Ueyama T (2014) MURC/Cavin-4 facilitates recruitment of ERK to caveolae and concentric cardiac hypertrophy induced by α1-adrenergic receptors. Proc Natl Acad Sci USA 111:3811–3816

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Okamoto T, Schlegel A, Scherer PE, Lisanti MP (1998) Caveolins, a family of scaffolding proteins for organizing “preassembled signaling complexes” at the plasma membrane. J Biol Chem 273:5419–5422

    Article  PubMed  CAS  Google Scholar 

  • Orlichenko L, Huang B, Krueger E, McNiven MA (2006) Epithelial growth factor-induced phosphorylation of caveolin 1 at tyrosine 14 stimulates caveolae formation in epithelial cells. J Biol Chem 281:4570–4579

    Article  PubMed  CAS  Google Scholar 

  • Osmani N, Pontabry J, Comelles J, Fekonja N, Goetz JG, Riveline D, Georges-Labouesse E, Labouesse M (2017) An Arf6- and caveolae-dependent pathway links hemidesmosome remodeling and mechanoresponse. Mol Biol Cell

    Google Scholar 

  • Palade GE (1953) An electron microscope study of the mitochondrial structure. J Histochem Cytochem 1:188–211

    Article  PubMed  CAS  Google Scholar 

  • Parat MO, Anand-Apte B, Fox PL (2003) Differential caveolin-1 polarization in endothelial cells during migration in two and three dimensions. Mol Biol Cell 14:3156–3168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parton RG, del Pozo MA (2013) Caveolae as plasma membrane sensors, protectors and organizers. Nat Rev Mol Cell Biol 14:98–112

    Article  PubMed  CAS  Google Scholar 

  • Parton RG, Howes MT (2010) Revisiting caveolin trafficking: the end of the caveosome. J Cell Biol 191:439–441

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parton RG, Simons K (2007) The multiple faces of caveolae. Nat Rev Mol Cell Biol 8:185–194

    Article  PubMed  CAS  Google Scholar 

  • Parton RG, Joggerst B, Simons K (1994) Regulated internalization of caveolae. J Cell Biol 127:1199–1215

    Article  PubMed  CAS  Google Scholar 

  • Parton RG, Molero JC, Floetenmeyer M, Green KM, James DE (2002) Characterization of a distinct plasma membrane macrodomain in differentiated adipocytes. J Biol Chem 277:46769–46778

    Article  PubMed  CAS  Google Scholar 

  • Patel HH, Tsutsumi YM, Head BP, Niesman IR, Jennings M, Horikawa Y, Huang D, Moreno AL, Patel PM, Insel PA, Roth DM (2007) Mechanisms of cardiac protection from ischemia/reperfusion injury: a role for caveolae and caveolin-1. FASEB J Official Publ Fed Am Soc Exp Biol 21:1565–1574

    CAS  Google Scholar 

  • Pelkmans L, Helenius A (2002) Endocytosis via caveolae. Traffic 3:311–320

    Article  PubMed  CAS  Google Scholar 

  • Pelkmans L, Kartenbeck J, Helenius A (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3:473–483

    Article  PubMed  CAS  Google Scholar 

  • Pelkmans L, Zerial M (2005) Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436:128–133

    Article  PubMed  CAS  Google Scholar 

  • Pilch PF, Liu L (2011) Fat caves: caveolae, lipid trafficking and lipid metabolism in adipocytes. Trends Endocrinol Metab 22:318–324

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pol A, Martin S, Fernandez MA, Ferguson C, Carozzi A, Luetterforst R, Enrich C, Parton RG (2004) Dynamic and regulated association of caveolin with lipid bodies: modulation of lipid body motility and function by a dominant negative mutant. Mol Biol Cell 15:99–110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Predescu SA, Predescu DN, Timblin BK, Stan RV, Malik AB (2003) Intersectin regulates fission and internalization of caveolae in endothelial cells. Mol Biol Cell 14:4997–5010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Prieto-Sanchez RM, Berenjeno IM, Bustelo XR (2006) Involvement of the Rho/Rac family member RhoG in caveolar endocytosis. Oncogene 25:2961–2973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rahman A, Sward K (2009) The role of caveolin-1 in cardiovascular regulation. Acta Physiol (Oxf) 195:231–245

    Article  CAS  Google Scholar 

  • Rauch MC, Ocampo ME, Bohle J, Amthauer R, Yanez AJ, Rodriguez-Gil JE, Slebe JC, Reyes JG, Concha II (2006) Hexose transporters GLUT1 and GLUT3 are colocalized with hexokinase I in caveolae microdomains of rat spermatogenic cells. J Cell Physiol 207:397–406

    Article  PubMed  CAS  Google Scholar 

  • Razani B, Lisanti MP (2001) Two distinct caveolin-1 domains mediate the functional interaction of caveolin-1 with protein kinase A. Am J Physiol Cell Physiol 281:C1241–C1250

    Article  PubMed  CAS  Google Scholar 

  • Razani B, Zhang XL, Bitzer M, von Gersdorff G, Bottinger EP, Lisanti MP (2001) Caveolin-1 regulates transforming growth factor (TGF)-beta/SMAD signaling through an interaction with the TGF-beta type I receptor. J Biol Chem 276:6727–6738

    Article  PubMed  CAS  Google Scholar 

  • Razani B, Woodman SE, Lisanti MP (2002) Caveolae: from cell biology to animal physiology. Pharmacol Rev 54:431–467

    Article  PubMed  CAS  Google Scholar 

  • Richter T, Floetenmeyer M, Ferguson C, Galea J, Goh J, Lindsay MR, Morgan GP, Marsh BJ, Parton RG (2008) High-resolution 3D quantitative analysis of caveolar ultrastructure and caveola-cytoskeleton interactions. Traffic 9:893–909

    Article  PubMed  CAS  Google Scholar 

  • Ritz D, Vuk M, Kirchner P, Bug M, Schutz S, Hayer A, Bremer S, Lusk C, Baloh RH, Lee H, Glatter T, Gstaiger M, Aebersold R, Weihl CC, Meyer H (2011) Endolysosomal sorting of ubiquitylated caveolin-1 is regulated by VCP and UBXD1 and impaired by VCP disease mutations. Nat Cell Biol 13:1116–1123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rizzo V, Morton C, DePaola N, Schnitzer JE, Davies PF (2003) Recruitment of endothelial caveolae into mechanotransduction pathways by flow conditioning in vitro. Am J Physiol Heart Circ Physiol 285:H1720–H1729

    Article  PubMed  CAS  Google Scholar 

  • Rizzo V, Sung A, Oh P, Schnitzer JE (1998) Rapid mechanotransduction in situ at the luminal cell surface of vascular endothelium and its caveolae. J Biol Chem 273:26323–26329

    Article  PubMed  CAS  Google Scholar 

  • Robenek H, Weissen-Plenz G, Severs NJ (2008) Freeze-fracture replica immunolabelling reveals caveolin-1 in the human cardiomyocyte plasma membrane. J Cell Mol Med 12:2519–2521

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68:673–682

    Article  PubMed  CAS  Google Scholar 

  • Sala-Vila A, Navarro-Lerida I, Sanchez-Alvarez M, Bosch M, Calvo C, Lopez JA, Calvo E, Ferguson C, Giacomello M, Serafini A, Scorrano L, Enriquez JA, Balsinde J, Parton RG, Vazquez J, Pol A, Del Pozo MA (2016) Interplay between hepatic mitochondria-associated membranes, lipid metabolism and caveolin-1 in mice. Sci Rep 6:27351

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sanguinetti AR, Mastick CC (2003) c-Abl is required for oxidative stress-induced phosphorylation of caveolin-1 on tyrosine 14. Cell Signal 15:289–298

    Article  PubMed  CAS  Google Scholar 

  • Sanguinetti AR, Cao H, Corley Mastick C (2003) Fyn is required for oxidative- and hyperosmotic-stress-induced tyrosine phosphorylation of caveolin-1. Biochem J 376:159–168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Santibanez JF, Blanco FJ, Garrido-Martin EM, Sanz-Rodriguez F, del Pozo MA, Bernabeu C (2008) Caveolin-1 interacts and cooperates with the transforming growth factor-beta type I receptor ALK1 in endothelial caveolae. Cardiovasc Res 77:791–799

    Article  PubMed  CAS  Google Scholar 

  • Sarkar S, Carroll B, Buganim Y, Maetzel D, Ng AH, Cassady JP, Cohen MA, Chakraborty S, Wang H, Spooner E, Ploegh H, Gsponer J, Korolchuk VI, Jaenisch R (2013) Impaired autophagy in the lipid-storage disorder Niemann-Pick type C1 disease. Cell reports 5:1302–1315

    Article  PubMed  Google Scholar 

  • Scott CC, Vossio S, Vacca F, Snijder B, Larios J, Schaad O, Guex N, Kuznetsov D, Martin O, Chambon M, Turcatti G, Pelkmans L, Gruenberg J (2015) Wnt directs the endosomal flux of LDL-derived cholesterol and lipid droplet homeostasis. EMBO Rep 16:741–752

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scheiffele P, Verkade P, Fra AM, Virta H, Simons K, Ikonen E (1998) Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J Cell Biol 140:795–806

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scherer PE, Lisanti MP, Baldini G, Sargiacomo M, Mastick CC, Lodish HF (1994) Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles. J Cell Biol 127:1233–1243

    Article  PubMed  CAS  Google Scholar 

  • Scherer PE, Okamoto T, Chun M, Nishimoto I, Lodish HF, Lisanti MP (1996) Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Proc Natl Acad Sci USA 93:131–135

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scherer PE, Lewis RY, Volonte D, Engelman JA, Galbiati F, Couet J, Kohtz DS, van Donselaar E, Peters P, Lisanti MP (1997) Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in vivo. J Biol Chem 272:29337–29346

    Article  PubMed  CAS  Google Scholar 

  • Schlegel A, Schwab RB, Scherer PE, Lisanti MP (1999) A role for the caveolin scaffolding domain in mediating the membrane attachment of caveolin-1. The caveolin scaffolding domain is both necessary and sufficient for membrane binding in vitro. J Biol Chem 274:22660–22667

    Article  PubMed  CAS  Google Scholar 

  • Schlegel A, Arvan P, Lisanti MP (2001) Caveolin-1 binding to endoplasmic reticulum membranes and entry into the regulated secretory pathway are regulated by serine phosphorylation. Protein sorting at the level of the endoplasmic reticulum. J Biol Chem 276:4398–4408

    Article  PubMed  CAS  Google Scholar 

  • Schlormann W, Steiniger F, Richter W, Kaufmann R, Hause G, Lemke C, Westermann M (2010) The shape of caveolae is omega-like after glutaraldehyde fixation and cup-like after cryofixation. Histochem Cell Biol 133:223–228

    Article  PubMed  CAS  Google Scholar 

  • Schwartz EA, Reaven E, Topper JN, Tsao PS (2005) Transforming growth factor-beta receptors localize to caveolae and regulate endothelial nitric oxide synthase in normal human endothelial cells. Biochem J 390:199–206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sedding DG, Hermsen J, Seay U, Eickelberg O, Kummer W, Schwencke C, Strasser RH, Tillmanns H, Braun-Dullaeus RC (2005) Caveolin-1 facilitates mechanosensitive protein kinase B (Akt) signaling in vitro and in vivo. Circ Res 96:635–642

    Article  PubMed  CAS  Google Scholar 

  • Seemann E, Sun M, Krueger S, Troger J, Hou W, Haag N, Schuler S, Westermann M, Huebner CA, Romeike B, Kessels MM, Qualmann B (2017) Deciphering caveolar functions by syndapin III KO-mediated impairment of caveolar invagination. eLife 6

    Google Scholar 

  • Senju Y, Itoh Y, Takano K, Hamada S, Suetsugu S (2011) Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. J Cell Sci 124:2032–2040

    Article  PubMed  CAS  Google Scholar 

  • Shack S, Wang XT, Kokkonen GC, Gorospe M, Longo DL, Holbrook NJ (2003) Caveolin-induced activation of the phosphatidylinositol 3-kinase/Akt pathway increases arsenite cytotoxicity. Mol Cell Biol 23:2407–2414

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shajahan AN, Timblin BK, Sandoval R, Tiruppathi C, Malik AB, Minshall RD (2004) Role of Src-induced dynamin-2 phosphorylation in caveolae-mediated endocytosis in endothelial cells. J Biol Chem 279:20392–20400

    Article  PubMed  CAS  Google Scholar 

  • Sharma P, Ghavami S, Stelmack GL, McNeill KD, Mutawe MM, Klonisch T, Unruh H, Halayko AJ (2010) β-Dystroglycan binds caveolin-1 in smooth muscle: a functional role in caveolae distribution and Ca2+ release. J Cell Sci 123:3061–3070

    Article  PubMed  CAS  Google Scholar 

  • Shaul PW, Anderson RG (1998) Role of plasmalemmal caveolae in signal transduction. Am J Physiol 275:L843–L851

    PubMed  CAS  Google Scholar 

  • Shi F, Sottile J (2008) Caveolin-1-dependent β1 integrin endocytosis is a critical regulator of fibronectin turnover. J Cell Sci 121:2360–2371

    Article  PubMed  CAS  Google Scholar 

  • Shin JS, Gao Z, Abraham SN (2000) Involvement of cellular caveolae in bacterial entry into mast cells. Science 289:785–788

    Article  PubMed  CAS  Google Scholar 

  • Shvets E, Bitsikas V, Howard G, Hansen CG, Nichols BJ (2015) Dynamic caveolae exclude bulk membrane proteins and are required for sorting of excess glycosphingolipids. Nat Commun 6:6867

    Article  PubMed  CAS  Google Scholar 

  • Siddiqi S, Sheth A, Patel F, Barnes M, Mansbach CM 2nd (2013) Intestinal caveolin-1 is important for dietary fatty acid absorption. Biochim Biophys Acta 1831:1311–1321

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31–39

    Article  PubMed  CAS  Google Scholar 

  • Sinha B, Koster D, Ruez R, Gonnord P, Bastiani M, Abankwa D, Stan RV, Butler-Browne G, Vedie B, Johannes L, Morone N, Parton RG, Raposo G, Sens P, Lamaze C, Nassoy P (2011) Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 144:402–413

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smart EJ, Ying Y, Donzell WC, Anderson RG (1996) A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 271:29427–29435

    Article  PubMed  CAS  Google Scholar 

  • Smart EJ, Ying YS, Anderson RG (1995) Hormonal regulation of caveolae internalization. J Cell Biol 131:929–938

    Article  PubMed  CAS  Google Scholar 

  • Song KS, Sargiacomo M, Galbiati F, Parenti M, Lisanti MP (1997) Targeting of a G alpha subunit (Gi1 alpha) and c-Src tyrosine kinase to caveolae membranes: clarifying the role of N-myristoylation. Cell Mol Biol (Noisy-le-grand) 43:293–303

    Google Scholar 

  • Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, Lisanti MP (1996) Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 271:15160–15165

    Article  PubMed  CAS  Google Scholar 

  • Stoeber M, Stoeck IK, Hanni C, Bleck CK, Balistreri G, Helenius A (2012) Oligomers of the ATPase EHD2 confine caveolae to the plasma membrane through association with actin. EMBO J 31:2350–2364

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stoeber M, Schellenberger P, Siebert CA, Leyrat C, Helenius A, Grunewald K (2016) Model for the architecture of caveolae based on a flexible, net-like assembly of Cavin1 and Caveolin discs. Proc Natl Acad Sci USA 113:E8069–E8078

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Strippoli R, Loureiro J, Moreno V, Benedicto I, Perez Lozano ML, Barreiro O, Pellinen T, Minguet S, Foronda M, Osteso MT, Calvo E, Vazquez J, Lopez Cabrera M, del Pozo MA (2014) Caveolin-1 deficiency induces a MEK-ERK1/2-Snail-1-dependent epithelial-mesenchymal transition and fibrosis during peritoneal dialysis. EMBO Mol Med 7:102–123

    Article  CAS  PubMed Central  Google Scholar 

  • Strippoli R, Loureiro J, Moreno V, Benedicto I, Perez Lozano ML, Barreiro O, Pellinen T, Minguet S, Foronda M, Osteso MT, Calvo E, Vazquez J, Lopez Cabrera M, del Pozo MA (2015) Caveolin-1 deficiency induces a MEK-ERK1/2-Snail-1-dependent epithelial-mesenchymal transition and fibrosis during peritoneal dialysis. EMBO Mol Med 7:102–123

    Article  PubMed  CAS  Google Scholar 

  • Sverdlov M, Shinin V, Place AT, Castellon M, Minshall RD (2009) Filamin A regulates caveolae internalization and trafficking in endothelial cells. Mol Biol Cell 20:4531–4540

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tagawa M, Ueyama T, Ogata T, Takehara N, Nakajima N, Isodono K, Asada S, Takahashi T, Matsubara H, Oh H (2008) MURC, a muscle-restricted coiled-coil protein, is involved in the regulation of skeletal myogenesis. Am J Physiol Cell Physiol 295:C490–C498

    Article  PubMed  CAS  Google Scholar 

  • Tang Z, Scherer PE, Okamoto T, Song K, Chu C, Kohtz DS, Nishimoto I, Lodish HF, Lisanti MP (1996) Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. J Biol Chem 271:2255–2261

    Article  PubMed  CAS  Google Scholar 

  • Tang W, Feng X, Zhang S, Ren Z, Liu Y, Yang B, lv B, Cai Y, Xia J, Ge N (2015) Caveolin-1 confers resistance of hepatoma cells to anoikis by activating IGF-1 pathway. Cell Physiol Biochem 36:1223–1236

    Article  PubMed  CAS  Google Scholar 

  • Thorn H, Stenkula KG, Karlsson M, Ortegren U, Nystrom FH, Gustavsson J, Stralfors P (2003) Cell surface orifices of caveolae and localization of caveolin to the necks of caveolae in adipocytes. Mol Biol Cell 14:3967–3976

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tourkina E, Richard M, Gooz P, Bonner M, Pannu J, Harley R, Bernatchez PN, Sessa WC, Silver RM, Hoffman S (2008) Antifibrotic properties of caveolin-1 scaffolding domain in vitro and in vivo. Am J Physiol Lung Cell Mol Physiol 294:L843–L861

    Article  PubMed  CAS  Google Scholar 

  • Uittenbogaard A, Smart EJ (2000) Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae. J Biol Chem 275:25595–25599

    Article  PubMed  CAS  Google Scholar 

  • Villasenor R, Kalaidzidis Y, Zerial M (2016) Signal processing by the endosomal system. Curr Opin Cell Biol 39:53–60

    Article  PubMed  CAS  Google Scholar 

  • Vinten J, Johnsen AH, Roepstorff P, Harpoth J, Tranum-Jensen J (2005) Identification of a major protein on the cytosolic face of caveolae. Biochim Biophys Acta 1717:34–40

    Article  PubMed  CAS  Google Scholar 

  • Walser PJ, Ariotti N, Howes M, Ferguson C, Webb R, Schwudke D, Leneva N, Cho KJ, Cooper L, Rae J, Floetenmeyer M, Oorschot VM, Skoglund U, Simons K, Hancock JF, Parton RG (2012) Constitutive formation of caveolae in a bacterium. Cell 150:752–763

    Article  PubMed  CAS  Google Scholar 

  • Wang XM, Zhang Y, Kim HP, Zhou Z, Feghali-Bostwick CA, Liu F, Ifedigbo E, Xu X, Oury TD, Kaminski N, Choi AM (2006) Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J Exp Med 203:2895–2906

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wickstrom SA, Lange A, Hess MW, Polleux J, Spatz JP, Kruger M, Pfaller K, Lambacher A, Bloch W, Mann M, Huber LA, Fassler R (2010) Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Dev Cell 19:574–858

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Williams TM, Lisanti MP (2005) Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am J Physiol Cell Physiol 288:C494–C506

    Article  PubMed  CAS  Google Scholar 

  • Williams TM, Medina F, Badano I, Hazan RB, Hutchinson J, Muller WJ, Chopra NG, Scherer PE, Pestell RG, Lisanti MP (2004) Caveolin-1 gene disruption promotes mammary tumorigenesis and dramatically enhances lung metastasis in vivo. Role of Cav-1 in cell invasiveness and matrix metalloproteinase (MMP-2/9) secretion. J Biol Chem 279:51630–51646

    Article  PubMed  CAS  Google Scholar 

  • Xu XL, Wu LC, Du F, Davis A, Peyton M, Tomizawa Y, Maitra A, Tomlinson G, Gazdar AF, Weissman BE, Bowcock AM, Baer R, Minna JD (2001) Inactivation of human SRBC, located within the 11p15.5-p15.4 tumor suppressor region, in breast and lung cancers. Cancer Res 61:7943–7949

    PubMed  CAS  Google Scholar 

  • Yamada E (1955) The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol 1:445–458

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamaguchi T, Lu C, Ida L, Yanagisawa K, Usukura J, Cheng J, Hotta N, Shimada Y, Isomura H, Suzuki M, Fujimoto T, Takahashi T (2016) ROR1 sustains caveolae and survival signalling as a scaffold of cavin-1 and caveolin-1. Nat Commun 7:10060

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamamoto M, Toya Y, Jensen RA, Ishikawa Y (1999) Caveolin is an inhibitor of platelet-derived growth factor receptor signaling. Exp Cell Res 247:380–388

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto M, Toya Y, Schwencke C, Lisanti MP, Myers MG Jr, Ishikawa Y (1998) Caveolin is an activator of insulin receptor signaling. J Biol Chem 273:26962–26968

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto H, Komekado H, Kikuchi A (2006) Caveolin is necessary for Wnt-3a-dependent internalization of LRP6 and accumulation of beta-catenin. Dev Cell 11:213–223

    Article  PubMed  CAS  Google Scholar 

  • Yeh YC, Parekh AB (2015) Distinct structural domains of caveolin-1 independently regulate Ca2+ release-activated Ca2+ channels and Ca2+ microdomain-dependent gene expression. Mol Cell Biol 35:1341–1349

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yeow I, Howard G, Chadwick J, Mendoza-Topaz C, Hansen CG, Nichols BJ, Shvets E (2017) EHD proteins cooperate to generate caveolar clusters and to maintain caveolae during repeated mechanical stress. Curr Biol 27(19):2951–2962

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yu J, Bergaya S, Murata T, Alp IF, Bauer MP, Lin MI, Drab M, Kurzchalia TV, Stan RV, Sessa WC (2006) Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J Clin Invest 116:1284–1291

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yuan T, Hong S, Yao Y, Liao K (2007) Glut-4 is translocated to both caveolae and non-caveolar lipid rafts, but is partially internalized through caveolae in insulin-stimulated adipocytes. Cell Res 17:772–782

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Peng F, Wu D, Ingram AJ, Gao B, Krepinsky JC (2007) Caveolin-1 phosphorylation is required for stretch-induced EGFR and Akt activation in mesangial cells. Cell Signal 19:1690–1700

    Article  PubMed  CAS  Google Scholar 

  • Zhang M, Dwyer NK, Love DC, Cooney A, Comly M, Neufeld E, Pentchev PG, Blanchette-Mackie EJ, Hanover JA (2001) Cessation of rapid late endosomal tubulovesicular trafficking in Niemann-Pick type C1 disease. Proc Natl Acad Sci USA 98:4466–4471

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zilberberg A, Yaniv A, Gazit A (2004) The low density lipoprotein receptor-1, LRP1, interacts with the human frizzled-1 (HFz1) and down-regulates the canonical Wnt signaling pathway. J Biol Chem 279:17535–17542

    Article  PubMed  CAS  Google Scholar 

  • Zimnicka AM, Husain YS, Shajahan AN, Sverdlov M, Chaga O, Chen Z, Toth PT, Klomp J, Karginov AV, Tiruppathi C, Malik AB, Minshall RD (2016) Src-dependent phosphorylation of caveolin-1 Tyr-14 promotes swelling and release of caveolae. Mol Biol Cell 27:2090–2106

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by grants SAF2011-25047 and CSD2009-0016 from Spanish Ministry of Science and Innovation (MICINN), SAF2014-51876-R from Spanish Ministry of Economy and Competitiveness (MINECO) and co-funded by FEDER funds, 674/C/2013 from Fundació La Marató de TV3, and AICR 15-0404 from the Worldwide Cancer Research Foundation (to M.A.dP.). The CNIC is supported by the Ministry of Economy, Industry and Competitiveness (MEIC), and the Pro CNIC Foundation, and is a Severo Ochoa Center of Excellence (SEV-2015-0505).

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The authors declare no competing financial interests exist.

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Authors and Affiliations

  1. Mechanoadaptation and Caveolae Biology Lab, Cell and Developmental Biology Area, Centro Nacional de Investigaciones Cardiovasculares, 28029, Madrid, Spain

    Olivia Muriel, Miguel Sánchez-Álvarez, Raffaele Strippoli & Miguel Angel del Pozo

  2. Department of Fundamental Microbiology, University of Lausanne, Quartier UNIL-Sorge. Bâtiment Biophore, 1015, Lausanne, Switzerland

    Olivia Muriel

  3. Istituto Pasteur Italia-Fondazione Cenci Bolognetti, Department of Cellular Biotechnologies and Hematology, Sapienza University of Rome, Rome, Italy

    Raffaele Strippoli

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  1. Olivia Muriel
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  2. Miguel Sánchez-Álvarez
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  3. Raffaele Strippoli
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  4. Miguel Angel del Pozo
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Correspondence to Miguel Angel del Pozo .

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Editors and Affiliations

  1. Membrane Dynamics and Mechanics of Intracellular Signaling Laboratory, CNRS UMR3666, INSERM U1143, Institut Curie—Centre de Recherche, PSL Research University, Paris, France

    Christophe Lamaze

  2. Department of Cellular and Molecular Physiology, Institute of Translational Medicine, University of Liverpool, Liverpool, United Kingdom

    Ian Prior

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Muriel, O., Sánchez-Álvarez, M., Strippoli, R., del Pozo, M.A. (2018). Role of the Endocytosis of Caveolae in Intracellular Signaling and Metabolism. In: Lamaze, C., Prior, I. (eds) Endocytosis and Signaling. Progress in Molecular and Subcellular Biology, vol 57. Springer, Cham. https://doi.org/10.1007/978-3-319-96704-2_8

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