Caveolae as plasma membrane sensors, protectors and organizers (original) (raw)

• Palade, G. E. Fine structure of blood capillaries. J. Appl. Phys. 24, 1424 (1953).
  Google Scholar
• Yamada, E. The fine structures of the gall bladder epithelium of the mouse. J. Biophys. Biochem. Cytol. 1, 445–458 (1955).
  CAS PubMed PubMed Central Google Scholar
• Hayashi, Y. K. et al. Human PTRF mutations cause secondary deficiency of caveolins resulting in muscular dystrophy with generalized lipodystrophy. J. Clin. Invest. 119, 2623–2633 (2009).
  CAS PubMed PubMed Central Google Scholar
• Rajab, A. et al. 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 (2010). References 3 and 4 were the first papers showing that loss of cavins is associated with human disease.
  PubMed PubMed Central Google Scholar
• Parton, R. G. & Simons, K. The multiple faces of caveolae. Nature Rev. Mol. Cell Biol. 8, 185–194 (2007).
  CAS Google Scholar
• Pelkmans, L. & Zerial, M. Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436, 128–133 (2005).
  CAS PubMed Google Scholar
• Richter, T. et al. High-resolution 3D quantitative analysis of caveolar ultrastructure and caveola–cytoskeleton interactions. Traffic 9, 893–909 (2008).
  CAS PubMed Google Scholar
• Schlormann, W. et al. The shape of caveolae is omega-like after glutaraldehyde fixation and cup-like after cryofixation. Histochem. Cell Biol. 133, 223–228 (2010).
  PubMed Google Scholar
• Nixon, S. J. et al. Caveolin-1 is required for lateral line neuromast and notochord development. J. Cell Sci. 120, 2151–2161 (2007).
  CAS PubMed Google Scholar
• Peters, K. R., Carley, W. W. & Palade, G. E. Endothelial plasmalemmal vesicles have a characteristic striped bipolar surface structure. J. Cell Biol. 101, 2233–2238 (1985).
  CAS PubMed Google Scholar
• Rothberg, K. G. et al. Caveolin, a protein component of caveolae membrane coats. Cell 68, 673–682 (1992).
  CAS PubMed Google Scholar
• Zhuang, Z., Marshansky, V., Breton, S. & Brown, D. Is caveolin involved in normal proximal tubule function? Presence in model PT systems but absence in situ. Am. J. Physiol. Renal Physiol. 300, F199–F206 (2011).
  CAS PubMed Google Scholar
• Thorn, H. et al. Cell surface orifices of caveolae and localization of caveolin to the necks of caveolae in adipocytes. Mol. Biol. Cell 14, 3967–3976 (2003).
  CAS PubMed PubMed Central Google Scholar
• Rizzo, V., Morton, C., DePaola, N., Schnitzer, J. E. & Davies, P. F. Recruitment of endothelial caveolae into mechanotransduction pathways by flow conditioning in vitro. Am. J. Physiol. Heart Circ. Physiol. 285, H1720–H1729 (2003).
  CAS PubMed Google Scholar
• Scheiffele, P. et al. Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J. Cell Biol. 140, 795–806 (1998).
  CAS PubMed PubMed Central Google Scholar
• Parat, M. O., Anand-Apte, B. & Fox, P. L. Differential caveolin-1 polarization in endothelial cells during migration in two and three dimensions. Mol. Biol. Cell 14, 3156–3168 (2003).
  CAS PubMed PubMed Central Google Scholar
• Kurzchalia, T. V. et al. VIP21, a 21-kD membrane protein is an integral component of _trans_-Golgi-network-derived transport vesicles. J. Cell Biol. 118, 1003–1014 (1992).
  CAS PubMed Google Scholar
• Scherer, P. E. et al. Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Proc. Natl Acad. Sci. USA 93, 131–135 (1996).
  CAS PubMed PubMed Central Google Scholar
• Way, M. & Parton, R. G. M-caveolin, a muscle-specific caveolin-related protein. FEBS Lett. 376, 108–112 (1995).
  CAS PubMed Google Scholar
• Robenek, H., Weissen-Plenz, G. & Severs, N. J. Freeze-fracture replica immunolabelling reveals caveolin-1 in the human cardiomyocyte plasma membrane. J. Cell. Mol. Med. 12, 2519–2521 (2008).
  CAS PubMed PubMed Central Google Scholar
• Head, B. P. et al. Microtubules and actin microfilaments regulate lipid raft/caveolae localization of adenylyl cyclase signaling components. J. Biol. Chem. 281, 26391–26399 (2006).
  CAS PubMed Google Scholar
• Patel, H. H. et al. Mechanisms of cardiac protection from ischemia/reperfusion injury: a role for caveolae and caveolin-1. FASEB J. 21, 1565–1574 (2007).
  CAS PubMed Google Scholar
• Tomassian, T. et al. Caveolin-1 orchestrates TCR synaptic polarity, signal specificity, and function in CD8 T cells. J. Immunol. 187, 2993–3002 (2011).
  CAS PubMed Google Scholar
• Fernandez-Rojo, M. A. et al. Caveolin-1 orchestrates the balance between glucose and lipid-dependent energy metabolism: implications for liver regeneration. Hepatology 55, 1574–1584 (2012).
  CAS PubMed Google Scholar
• Head, B. P. et al. Neuron-targeted caveolin-1 protein enhances signaling and promotes arborization of primary neurons. J. Biol. Chem. 286, 33310–33321 (2011).
  CAS PubMed PubMed Central Google Scholar
• Head, B. P. et al. Loss of caveolin-1 accelerates neurodegeneration and aging. PLoS ONE 5, e15697 (2010).
  CAS PubMed PubMed Central Google Scholar
• Drab, M. et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293, 2449–2452 (2001).
  CAS PubMed Google Scholar
• Razani, B. et al. Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J. Biol. Chem. 277, 8635–8647 (2002).
  CAS PubMed Google Scholar
• Fra, A. M., Williamson, E., Simons, K. & Parton, R. G. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl Acad. Sci. USA 92, 8655–8659 (1995).
  CAS PubMed PubMed Central Google Scholar
• Walser, P. J. et al. Constitutive formation of caveolae in a bacterium. Cell 150, 752–763 (2012). Shows that caveolin expression in a prokaryotic system is sufficient to drive the formation of cytoplasmic vesicles analogous to mammalian caveolae. In this model system, caveolins can drive membrane curvature and fission from the membrane.
  CAS PubMed Google Scholar
• Hansen, C. G. & Nichols, B. J. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol. 20, 177–186 (2010).
  CAS PubMed Google Scholar
• Bastiani, M. et al. MURC/cavin-4 and cavin family members form tissue-specific caveolar complexes. J. Cell Biol. 185, 1259–1273 (2009).
  CAS PubMed PubMed Central Google Scholar
• Jansa, P., Mason, S. W., Hoffmann-Rohrer, U. & Grummt, I. Cloning and functional characterization of PTRF, a novel protein which induces dissociation of paused ternary transcription complexes. EMBO J. 17, 2855–2864 (1998).
  CAS PubMed PubMed Central Google Scholar
• Gustincich, S. & Schneider, C. Serum deprivation response gene is induced by serum starvation but not by contact inhibition. Cell Growth Differ. 4, 753–760 (1993).
  CAS PubMed Google Scholar
• Izumi, Y. et al. A protein kinase Cδ-binding protein SRBC whose expression is induced by serum starvation. J. Biol. Chem. 272, 7381–7389 (1997).
  CAS PubMed Google Scholar
• Ogata, T. et al. 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 (2008).
  CAS PubMed PubMed Central Google Scholar
• Tagawa, M. et al. MURC, a muscle-restricted coiled-coil protein, is involved in the regulation of skeletal myogenesis. Am. J. Physiol. Cell Physiol. 295, C490–C498 (2008).
  CAS PubMed Google Scholar
• Hill, M. M. et al. PTRF-cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132, 113–124 (2008).
  CAS PubMed PubMed Central Google Scholar
• Liu, L. et al. Deletion of cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab. 8, 310–317 (2008). Together with reference 33, the first demonstration of the crucial role of cavin 1 in regulating caveola formation in cells and whole animals.
  PubMed PubMed Central Google Scholar
• Hansen, C. G., Bright, N. A., Howard, G. & Nichols, B. J. SDPR induces membrane curvature and functions in the formation of caveolae. Nature Cell Biol. 11, 807–814 (2009).
  CAS PubMed Google Scholar
• McMahon, K. A. et al. SRBC/cavin-3 is a caveolin adapter protein that regulates caveolae function. EMBO J. 28, 1001–1015 (2009).
  CAS PubMed PubMed Central Google Scholar
• Hayer, A., Stoeber, M., Bissig, C. & Helenius, A. Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 11, 361–382 (2010). Identifies a Asp-X-Glu sequence in the N-terminal domain of CAV1 required for exit from the ER. Analyses the assembly of cavin 1 into caveolar domains.
  CAS PubMed Google Scholar
• Gustincich, S. et al. The human serum deprivation response gene (SDPR) maps to 2q32-q33 and codes for a phosphatidylserine-binding protein. Genomics 57, 120–129 (1999).
  CAS PubMed Google Scholar
• Fairn, G. D. et al. High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine. J. Cell Biol. 194, 257–275 (2011).
  CAS PubMed PubMed Central Google Scholar
• Wanaski, S. P., Ng, B. K. & Glaser, M. Caveolin scaffolding region and the membrane binding region of SRC form lateral membrane domains. Biochemistry 42, 42–56 (2003).
  CAS PubMed Google Scholar
• Sinha, B. et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 144, 402–413 (2011). Demonstrates reversible flattening of caveolae and caveolin–cavin dissociation in response to acute mechanical stimuli and shows the importance of the caveolar system in the protection of cells against mechanical stress.
  CAS PubMed PubMed Central Google Scholar
• Breen, M. R., Camps, M., Carvalho-Simoes, F., Zorzano, A. & Pilch, P. F. Cholesterol depletion in adipocytes causes caveolae collapse concomitant with proteosomal degradation of cavin-2 in a switch-like fashion. PLoS ONE 7, e34516 (2012).
  CAS PubMed PubMed Central Google Scholar
• Naslavsky, N. & Caplan, S. EHD proteins: key conductors of endocytic transport. Trends Cell Biol. 21, 122–131 (2011).
  CAS PubMed Google Scholar
• Daumke, O. et al. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449, 923–927 (2007).
  CAS PubMed Google Scholar
• Moren, B. et al. EHD2 regulates caveolar dynamics via ATP-driven targeting and oligomerization. Mol. Biol. Cell 23, 1316–1329 (2012).
  CAS PubMed PubMed Central Google Scholar
• Stoeber, M. et al. Oligomers of the ATPase EHD2 confine caveolae to the plasma membrane through association with actin. EMBO J. 31, 2350–2364 (2012). Identifies, together with reference 50, the ATPase EHD2 as a new component of caveolae. Shows that EHD2 has a role in the regulation of caveolar dynamics.
  CAS PubMed PubMed Central Google Scholar
• Fujita, A., Cheng, J., Tauchi-Sato, K., Takenawa, T. & Fujimoto, T. A distinct pool of phosphatidylinositol 4,5-bisphosphate in caveolae revealed by a nanoscale labeling technique. Proc. Natl Acad. Sci. USA 106, 9256–9261 (2009).
  CAS PubMed PubMed Central Google Scholar
• Henley, J. R., Krueger, E. W., Oswald, B. J. & McNiven, M. A. Dynamin-mediated internalization of caveolae. J. Cell Biol. 141, 85–99 (1998).
  CAS PubMed PubMed Central Google Scholar
• Oh, P., McIntosh, D. P. & Schnitzer, J. E. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J. Cell Biol. 141, 101–114 (1998).
  CAS PubMed PubMed Central Google Scholar
• Hansen, C. G., Howard, G. & Nichols, B. J. Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis. J. Cell Sci. 124, 2777–2785 (2011). Demonstrates a role for the F-BAR domain protein PACSIN2 in caveola formation.
  CAS PubMed Google Scholar
• Senju, Y., Itoh, Y., Takano, K., Hamada, S. & Suetsugu, S. Essential role of PACSIN2/syndapin-II in caveolae membrane sculpting. J. Cell Sci. 124, 2032–2040 (2011).
  CAS PubMed Google Scholar
• Parton, R. G., Molero, J. C., Floetenmeyer, M., Green, K. M. & James, D. E. Characterization of a distinct plasma membrane macrodomain in differentiated adipocytes. J. Biol. Chem. 277, 46769–46778 (2002).
  CAS PubMed Google Scholar
• del Pozo, M. A. et al. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nature Cell Biol. 7, 901–908 (2005).
  CAS PubMed Google Scholar
• Millan, J. et al. Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nature Cell Biol. 8, 113–123 (2006).
  CAS PubMed Google Scholar
• Echarri, A. et al. Caveolar domain organization and trafficking is regulated by Abl kinases and mDia1. J. Cell Sci. 125, 309–3113 (2012). Identifies the actin polymerization pathway that links caveolae to stress fibres and shows that adhesion strength and actin fibres modulate caveola plasticity from flattened structures to caveolar rosettes.
  Google Scholar
• Echarri, A. & Del Pozo, M. A. Caveolae. Curr. Biol. 22, R114–R116 (2012).
  CAS PubMed Google Scholar
• Parton, R. G., Way, M., Zorzi, N. & Stang, E. Caveolin-3 associates with developing T-tubules during muscle differentiation. J. Cell Biol. 136, 137–154 (1997).
  CAS PubMed PubMed Central Google Scholar
• Pelkmans, L., Kartenbeck, J. & Helenius, A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nature Cell Biol. 3, 473–483 (2001).
  CAS PubMed Google Scholar
• Ewers, H. et al. GM1 structure determines SV40-induced membrane invagination and infection. Nature Cell Biol. 12, 11–18 (2010).
  CAS PubMed Google Scholar
• Damm, E. M. et al. Clathrin- and caveolin1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 168, 477–488 (2005).
  CAS PubMed PubMed Central Google Scholar
• Oh, P. et al. Live dynamic imaging of caveolae pumping targeted antibody rapidly and specifically across endothelium in the lung. Nature Biotech. 25, 327–337 (2007).
  CAS Google Scholar
• Rippe, B., Rosengren, B. I., Carlsson, O. & Venturoli, D. Transendothelial transport: the vesicle controversy. J. Vasc. Res. 39, 375–390 (2002).
  CAS PubMed Google Scholar
• Pelkmans, L., Burli, T., Zerial, M. & Helenius, A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118, 767–780 (2004).
  CAS PubMed Google Scholar
• Hayer, A. et al. Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J. Cell Biol. 191, 615–629 (2010).
  CAS PubMed PubMed Central Google Scholar
• Boucrot, E., Howes, M. T., Kirchhausen, T. & Parton, R. G. Redistribution of caveolae during mitosis. J. Cell Sci. 124, 1965–1972 (2011).
  CAS PubMed PubMed Central Google Scholar
• Parton, R. G., Joggerst, B. & Simons, K. Regulated internalization of caveolae. J. Cell Biol. 127, 1199–1215 (1994).
  CAS PubMed Google Scholar
• Le Lay, S. et al. Cholesterol-induced caveolin targeting to lipid droplets in adipocytes: a role for caveolar endocytosis. Traffic 7, 549–561 (2006).
  CAS PubMed Google Scholar
• Sharma, D. K. et al. Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol. Biol. Cell 15, 3114–3122 (2004).
  CAS PubMed PubMed Central Google Scholar
• Muriel, O. et al. Phosphorylated filamin A regulates actin-linked caveolae dynamics. J. Cell Sci. 124, 2763–2776 (2011). Shows, using high-spatio-temporal resolution particle tracking, that filamin A mediates stable arrest of CAV1 vesicles in confined areas and subsequent internalization.
  CAS PubMed Google Scholar
• Balasubramanian, N., Scott, D. W., Castle, J. D., Casanova, J. E. & Schwartz, M. A. Arf6 and microtubules in adhesion-dependent trafficking of lipid rafts. Nature Cell Biol. 9, 1381–1391 (2007).
  CAS PubMed Google Scholar
• Ritz, D. et al. Endolysosomal sorting of ubiquitylated caveolin-1 is regulated by VCP and UBXD1 and impaired by VCP disease mutations. Nature Cell Biol. 13, 1116–1123 (2011). Identifies monoubiquitylated oligomeric caveolin as a binding partner of the VCP–UBXD1 complex and links caveolin turnover to human degenerative diseases associated with VCP mutations.
  CAS PubMed Google Scholar
• Yamanaka, K., Sasagawa, Y. & Ogura, T. Recent advances in p97/VCP/Cdc48 cellular functions. Biochim. Biophys. Acta 1823, 130–137 (2011).
  PubMed Google Scholar
• Stahlhut, M. & van Deurs, B. Identification of filamin as a novel ligand for caveolin-1: evidence for the organization of caveolin-1-associated membrane domains by the actin cytoskeleton. Mol. Biol. Cell 11, 325–337 (2000).
  CAS PubMed PubMed Central Google Scholar
• Wickstrom, S. A. et al. Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Dev. Cell 19, 574–588 (2010). Demonstrates a loss of caveolae in mice lacking β1 integrins or ILK and identifies the underlying cause as the defective microtubule-dependent trafficking of caveolae to the plasma membrane.
  PubMed PubMed Central Google Scholar
• Singh, R. D. et al. Gangliosides and β1-integrin are required for caveolae and membrane domains. Traffic 11, 348–360 (2010).
  CAS PubMed Google Scholar
• Sverdlov, M., Shinin, V., Place, A. T., Castellon, M. & Minshall, R. D. Filamin A regulates caveolae internalization and trafficking in endothelial cells. Mol. Biol. Cell 20, 4531–4540 (2009).
  CAS PubMed PubMed Central Google Scholar
• Sharma, P. et al. β-dystroglycan binds caveolin-1 in smooth muscle: a functional role in caveolae distribution and Ca2+ release. J. Cell Sci. 123, 3061–3070 (2010).
  CAS PubMed Google Scholar
• Lee, J. & Schmid-Schonbein, G. W. Biomechanics of skeletal muscle capillaries: hemodynamic resistance, endothelial distensibility, and pseudopod formation. Ann. Biomed. Eng. 23, 226–246 (1995).
  CAS PubMed Google Scholar
• Dulhunty, A. F. & Franzini-Armstrong, C. 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 (1975). References 83 and 84 use elegant quantitative electron microscopy and different experimental systems to demonstrate flattening of caveolae in response to plasma membrane deformation.
  CAS PubMed PubMed Central Google Scholar
• Kozera, L., White, E. & Calaghan, S. Caveolae act as membrane reserves which limit mechanosensitive _I_Cl, swell channel activation during swelling in the rat ventricular myocyte. PLoS ONE 4, e8312 (2009).
  PubMed PubMed Central Google Scholar
• Czarny, M. & Schnitzer, J. E. Neutral sphingomyelinase inhibitor scyphostatin prevents and ceramide mimics mechanotransduction in vascular endothelium. Am J. Physiol. Heart Circ. Physiol. 287, H1344–H1352 (2004).
  CAS PubMed Google Scholar
• Rizzo, V., Sung, A., Oh, P. & Schnitzer, J. E. Rapid mechanotransduction in situ at the luminal cell surface of vascular endothelium and its caveolae. J. Biol. Chem. 273, 26323–26329 (1998).
  CAS PubMed Google Scholar
• Sedding, D. G. et al. Caveolin-1 facilitates mechanosensitive protein kinase B (Akt) signaling in vitro and in vivo. Circ. Res. 96, 635–642 (2005).
  CAS PubMed Google Scholar
• Yu, J. et al. Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J. Clin. Invest. 116, 1284–1291 (2006).
  CAS PubMed PubMed Central Google Scholar
• Zhang, B. et al. Caveolin-1 phosphorylation is required for stretch-induced EGFR and Akt activation in mesangial cells. Cell. Signal. 19, 1690–1700 (2007).
  CAS PubMed Google Scholar
• Joshi, B. et al. Phosphocaveolin-1 is a mechanotransducer that induces caveola biogenesis via Egr1 transcriptional regulation. J. Cell Biol. 199, 425–435 (2012).
  CAS PubMed PubMed Central Google Scholar
• Radel, C. & Rizzo, V. Integrin mechanotransduction stimulates caveolin-1 phosphorylation and recruitment of Csk to mediate actin reorganization. Am. J. Physiol. Heart Circ. Physiol. 288, H936–H945 (2005).
  CAS PubMed Google Scholar
• Grande-Garcia, A. et al. Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J. Cell Biol. 177, 683–694 (2007).
  CAS PubMed PubMed Central Google Scholar
• Goetz, J. G. et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 146, 148–163 (2011). First direct demonstration of the role of CAV1 in mechanical regulation of the extracellular environment and its role in tumour invasion.
  CAS PubMed PubMed Central Google Scholar
• Yang, B., Radel, C., Hughes, D., Kelemen, S. & Rizzo, V. p190 RhoGTPase-activating protein links the β1 integrin/caveolin-1 mechanosignaling complex to RhoA and actin remodeling. Arterioscler. Thromb. Vasc. Biol. 31, 376–383 (2011).
  CAS PubMed Google Scholar
• Boettcher, J. P. et al. Tyrosine-phosphorylated caveolin-1 blocks bacterial uptake by inducing Vav2–RhoA-mediated cytoskeletal rearrangements. PLoS Biol. 8, e1000457 (2010). Shows that CAV1 is Tyr phosphorylated in response to bacterial uptake, which induces actin cytoskeletal reorganization via VAV2 and RHOA.
  PubMed PubMed Central Google Scholar
• Bai, L. et al. Regulation of cellular senescence by the essential caveolar component PTRF/cavin-1. Cell Res. 21, 1088–1101 (2011).
  CAS PubMed PubMed Central Google Scholar
• Hasegawa, T. et al. 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 (2000).
  CAS PubMed PubMed Central Google Scholar
• Albinsson, S., Nordstrom, I., Sward, K. & Hellstrand, P. Differential dependence of stretch and shear stress signaling on caveolin-1 in the vascular wall. Am. J. Physiol. Cell Physiol. 294, C271–C279 (2008).
  CAS PubMed Google Scholar
• Bernatchez, P. N., Sharma, A., Kodaman, P. & Sessa, W. C. Myoferlin is critical for endocytosis in endothelial cells. Am. J. Physiol. Cell Physiol. 297, C484–C492 (2009).
  CAS PubMed PubMed Central Google Scholar
• Cai, C. et al. Membrane repair defects in muscular dystrophy are linked to altered interaction between MG53, caveolin-3, and dysferlin. J. Biol. Chem. 284, 15894–15902 (2009).
  CAS PubMed PubMed Central Google Scholar
• Zhu, H. et al. Polymerase transcriptase release factor (PTRF) anchors MG53 protein to cell injury site for initiation of membrane repair. J. Biol. Chem. 286, 12820–12824 (2011).
  CAS PubMed PubMed Central Google Scholar
• Ohsawa, Y. et al. Muscular atrophy of caveolin 3-deficient mice is rescued by myostatin inhibition. J. Clin. Invest. 116, 2924–2934 (2006).
  CAS PubMed PubMed Central Google Scholar
• Ohsawa, Y. et al. Overexpression of P104L mutant caveolin-3 in mice develops hypertrophic cardiomyopathy with enhanced contractility in association with increased endothelial nitric oxide synthase activity. Hum. Mol. Genet. 13, 151–157 (2004).
  CAS PubMed Google Scholar
• Cerezo, A. et al. The absence of caveolin-1 increases proliferation and anchorage- independent growth by a Rac-dependent, Erk-independent mechanism. Mol. Cell. Biol. 29, 5046–5059 (2009).
  CAS PubMed PubMed Central Google Scholar
• Borza, C. M. et al. Integrin α1β1 promotes caveolin-1 dephosphorylation by activating T cell protein-tyrosine phosphatase. J. Biol. Chem. 285, 40114–40124 (2010).
  CAS PubMed PubMed Central Google Scholar
• Wary, K. K., Mariotti, A., Zurzolo, C. & Giancotti, F. G. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent growth. Cell 94, 625–634 (1998).
  CAS PubMed Google Scholar
• Du, J. et al. Integrin activation and internalization on soft ECM as a mechanism of induction of stem cell differentiation by ECM elasticity. Proc. Natl Acad. Sci. USA 108, 9466–9471 (2011).
  CAS PubMed PubMed Central Google Scholar
• Goetz, J. G. et al. Concerted regulation of focal adhesion dynamics by galectin-3 and tyrosine-phosphorylated caveolin-1. J. Cell Biol. 180, 1261–1275 (2008).
  CAS PubMed PubMed Central Google Scholar
• Paszek, M. J. et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241–254 (2005).
  CAS PubMed Google Scholar
• Sanz-Moreno, V. et al. ROCK and JAK1 signaling cooperate to control actomyosin contractility in tumor cells and stroma. Cancer Cell 20, 229–245 (2011).
  CAS PubMed Google Scholar
• Levental, K. R. et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891–906 (2009).
  CAS PubMed PubMed Central Google Scholar
• Gaggioli, C. et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nature Cell Biol. 9, 1392–1400 (2007).
  CAS PubMed Google Scholar
• Couet, J., Li, S., Okamoto, T., Ikezu, T. & Lisanti, M. P. Identification of peptide and protein ligands for the caveolin- scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J. Biol. Chem. 272, 6525–6533 (1997).
  CAS PubMed Google Scholar
• Okamoto, T., Schlegel, A., Scherer, P. E. & Lisanti, M. P. Caveolins, a family of scaffolding proteins for organizing “preassembled signaling complexes” at the plasma membrane. J. Biol. Chem. 273, 5419–5422 (1998).
  CAS PubMed Google Scholar
• Collins, B. M., Davis, M. J., Hancock, J. F. & Parton, R. G. Structure-based reassessment of the caveolin signaling model: do caveolae regulate signaling through caveolin–protein interactions? Dev. Cell 23, 11–20 (2012).
  CAS PubMed PubMed Central Google Scholar
• Byrne, D. P., Dart, C. & Rigden, D. J. Evaluating caveolin interactions: do proteins interact with the caveolin scaffolding domain through a widespread aromatic residue-rich motif? PLoS ONE 7, e44879 (2012).
  CAS PubMed PubMed Central Google Scholar
• Garcia-Cardena, G. et al. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the NOS caveolin binding domain in vivo. J. Biol. Chem. 272, 25437–25440 (1997).
  CAS PubMed Google Scholar
• Sowa, G., Pypaert, M. & Sessa, W. C. Distinction between signaling mechanisms in lipid rafts versus caveolae. Proc. Natl Acad. Sci. USA 98, 14072–14077 (2001).
  CAS PubMed PubMed Central Google Scholar
• Bucci, M. et al. In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nature Med. 6, 1362–1367 (2000).
  CAS PubMed Google Scholar
• Place, A. T. et al. Cooperative role of caveolin-1 and C-terminal Src kinase binding protein in C-terminal Src kinase-mediated negative regulation of c-Src. Mol. Pharmacol. 80, 665–672 (2011).
  CAS PubMed PubMed Central Google Scholar
• Kronstein, R. et al. Caveolin-1 opens endothelial cell junctions by targeting catenins. Cardiovasc. Res. 93, 130–140 (2012).
  CAS PubMed Google Scholar
• Blouin, C. M. et al. Plasma membrane subdomain compartmentalization contributes to distinct mechanisms of ceramide action on insulin signaling. Diabetes 59, 600–610 (2010).
  CAS PubMed Google Scholar
• Mattsson, C. L., Csikasz, R. I., Shabalina, I. G., Nedergaard, J. & Cannon, B. Caveolin-1-ablated mice survive in cold by nonshivering thermogenesis despite desensitized adrenergic responsiveness. Am. J. Physiol. Endocrinol. Metab. 299, e374–e383 (2010).
  CAS PubMed Google Scholar
• Gonzalez-Munoz, E. et al. Caveolin-1 loss of function accelerates glucose transporter 4 and insulin receptor degradation in 3T3-L1 adipocytes. Endocrinology 150, 3493–3502 (2009).
  CAS PubMed Google Scholar
• Hernandez-Deviez, D. J. et al. Caveolin regulates endocytosis of the muscle repair protein, dysferlin. J. Biol. Chem. 283, 6476–6488 (2008).
  CAS PubMed Google Scholar
• Marchiando, A. M. et al. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J. Cell Biol. 189, 111–126 (2010).
  CAS PubMed PubMed Central Google Scholar
• Orlichenko, L. et al. Caveolae mediate growth factor-induced disassembly of adherens junctions to support tumor cell dissociation. Mol. Biol. Cell 20, 4140–4152 (2009).
  CAS PubMed PubMed Central Google Scholar
• Upla, P. et al. Clustering induces a lateral redistribution of α2 β1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol. Biol. Cell 15, 625–636 (2004).
  CAS PubMed PubMed Central Google Scholar
• Shi, F. & Sottile, J. Caveolin-1-dependent β1 integrin endocytosis is a critical regulator of fibronectin turnover. J. Cell Sci. 121, 2360–2371 (2008).
  CAS PubMed Google Scholar
• Arjonen, A., Alanko, J., Veltel, S. & Ivaska, J. Distinct recycling of active and inactive β1 integrins. Traffic 13, 610–625 (2012).
  CAS PubMed PubMed Central Google Scholar
• Pellinen, T. et al. Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev. Cell 15, 371–385 (2008).
  CAS PubMed Google Scholar
• Guo, J. et al. Cell surface expression of human ether-a-go-go-related gene (hERG) channels is regulated by caveolin-3 protein via the ubiquitin ligase Nedd4-2. J. Biol. Chem. 287, 33132–33141 (2012).
  CAS PubMed PubMed Central Google Scholar
• Lee, I. H. et al. The activity of the epithelial sodium channels is regulated by caveolin-1 via a Nedd4-2-dependent mechanism. J. Biol. Chem. 284, 12663–12669 (2009).
  CAS PubMed PubMed Central Google Scholar
• Otsu, K. et al. Caveolin gene transfer improves glucose metabolism in diabetic mice. Am. J. Physiol. Cell Physiol. 298, C450–C456 (2010).
  CAS PubMed Google Scholar
• Gervasio, O. L., Whitehead, N. P., Yeung, E. W., Phillips, W. D. & Allen, D. G. TRPC1 binds to caveolin-3 and is regulated by Src kinase — role in Duchenne muscular dystrophy. J. Cell Sci. 121, 2246–2255 (2008).
  CAS PubMed Google Scholar
• Langlois, S., Cowan, K. N., Shao, Q., Cowan, B. J. & Laird, D. W. Caveolin-1 and -2 interact with connexin43 and regulate gap junctional intercellular communication in keratinocytes. Mol. Biol. Cell 19, 912–928 (2008).
  CAS PubMed PubMed Central Google Scholar
• Pani, B. et al. Activation of TRPC1 by STIM1 in ER–PM microdomains involves release of the channel from its scaffold caveolin-1. Proc. Natl Acad. Sci. USA 106, 20087–20092 (2009).
  CAS PubMed PubMed Central Google Scholar
• Sundivakkam, P. C. et al. Caveolin-1 scaffold domain interacts with TRPC1 and IP3R3 to regulate Ca2+ store release-induced Ca2+ entry in endothelial cells. Am. J. Physiol. Cell Physiol. 296, C403–C413 (2009).
  CAS PubMed Google Scholar
• Fuhs, S. R. & Insel, P. A. Caveolin-3 undergoes SUMOylation by the SUMO E3 ligase PIASy: sumoylation affects G-protein-coupled receptor desensitization. J. Biol. Chem. 286, 14830–14841 (2011).
  CAS PubMed PubMed Central Google Scholar
• Nethe, M. et al. Focal-adhesion targeting links caveolin-1 to a Rac1-degradation pathway. J. Cell Sci. 123, 1948–1958 (2010).
  CAS PubMed Google Scholar
• Hezel, M., de Groat, W. C. & Galbiati, F. Caveolin-3 promotes nicotinic acetylcholine receptor clustering and regulates neuromuscular junction activity. Mol. Biol. Cell 21, 302–310 (2010).
  CAS PubMed PubMed Central Google Scholar
• Isshiki, M. et al. Endothelial Ca2+ waves preferentially originate at specific loci in caveolin-rich cell edges. Proc. Natl Acad. Sci. USA 95, 5009–5014 (1998).
  CAS PubMed PubMed Central Google Scholar
• Yamamoto, K. et al. Visualization of flow-induced ATP release and triggering of Ca2+ waves at caveolae in vascular endothelial cells. J. Cell Sci. 124, 3477–3483 (2011). Demonstrates that localized release of calcium in response to shear stress occurs in caveolin-rich areas of the plasma membrane and is lost in CAV1-deficient cells.
  CAS PubMed Google Scholar
• Vassilopoulos, S. et al. Caveolin 3 is associated with the calcium release complex and is modified via in vivo triadin modification. Biochemistry 49, 6130–6135 (2010).
  CAS PubMed Google Scholar
• Adebiyi, A., Narayanan, D. & Jaggar, J. H. Caveolin-1 assembles type 1 inositol 1,4,5-trisphosphate receptors and canonical transient receptor potential 3 channels into a functional signaling complex in arterial smooth muscle cells. J. Biol. Chem. 286, 4341–4348 (2011).
  CAS PubMed Google Scholar
• Hoffmann, C. et al. Caveolin limits membrane microdomain mobility and integrin-mediated uptake of fibronectin-binding pathogens. J. Cell Sci. 123, 4280–4291 (2010). Provides evidence for a general effect of CAV1 on membrane properties as indicated by the effects on membrane microdomain mobility and the consequences for pathogen entry.
  CAS PubMed Google Scholar
• Gaus, K., Le Lay, S., Balasubramanian, N. & Schwartz, M. A. Integrin-mediated adhesion regulates membrane order. J. Cell Biol. 174, 725–734 (2006).
  CAS PubMed PubMed Central Google Scholar
• Roy, S. et al. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nature Cell Biol. 1, 98–105 (1999).
  CAS PubMed Google Scholar
• Lingwood, D. & Simons, K. Lipid rafts as a membrane-organizing principle. Science 327, 46–50 (2010).
  CAS PubMed Google Scholar
• Carozzi, A. J. et al. Inhibition of lipid raft-dependent signaling by a dystrophy-associated mutant of caveolin-3. J. Biol. Chem. 277, 17944–17949 (2002).
  CAS PubMed Google Scholar
• Kirkham, M. et al. Evolutionary analysis and molecular dissection of caveola biogenesis. J. Cell Sci. 121, 2075–2086 (2008).
  CAS PubMed Google Scholar
• Ortegren, U. et al. Lipids and glycosphingolipids in caveolae and surrounding plasma membrane of primary rat adipocytes. Eur. J. Biochem. 271, 2028–2036 (2004).
  PubMed Google Scholar
• Sharma, D. K. et al. The glycosphingolipid, lactosylceramide, regulates β1-integrin clustering and endocytosis. Cancer Res. 65, 8233–8241 (2005).
  CAS PubMed Google Scholar
• Sharma, D. K. et al. Glycosphingolipids internalized via caveolar-related endocytosis rapidly merge with the clathrin pathway in early endosomes and form microdomains for recycling. J. Biol. Chem. 278, 7564–7572 (2003).
  CAS PubMed Google Scholar
• Prinetti, A. et al. GM3 synthase overexpression results in reduced cell motility and in caveolin-1 upregulation in human ovarian carcinoma cells. Glycobiology 20, 62–77 (2010).
  CAS PubMed Google Scholar
• Murata, M. et al. VIP21/caveolin is a cholesterol-binding protein. Proc. Natl Acad. Sci. USA 92, 10339–10343 (1995).
  CAS PubMed PubMed Central Google Scholar
• Trigatti, B. L., Anderson, R. G. & Gerber, G. E. Identification of caveolin-1 as a fatty acid binding protein. Biochem. Biophys. Res. Commun. 255, 34–39 (1999).
  CAS PubMed Google Scholar
• Brasaemle, D. L., Dolios, G., Shapiro, L. & Wang, R. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes. J. Biol. Chem. 279, 46835–46842 (2004).
  CAS PubMed Google Scholar
• Martin, S. & Parton, R. G. Caveolin, cholesterol, and lipid bodies. Semin. Cell Dev. Biol. 16, 163–174 (2005).
  CAS PubMed Google Scholar
• Pol, A. et al. 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 (2004).
  CAS PubMed PubMed Central Google Scholar
• Pol, A. et al. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J. Cell Biol. 152, 1057–1070 (2001).
  CAS PubMed PubMed Central Google Scholar
• Bosch, M. et al. Caveolin-1 deficiency causes cholesterol-dependent mitochondrial dysfunction and apoptotic susceptibility. Curr. Biol. 21, 681–686 (2011). Identifies mitochondrial dysfunction due to aberrant cholesterol accumulation as a common feature in CAV1-deficient cells.
  CAS PubMed PubMed Central Google Scholar
• Asterholm, I. W., Mundy, D. I., Weng, J., Anderson, R. G. & Scherer, P. E. Altered mitochondrial function and metabolic inflexibility associated with loss of caveolin-1. Cell. Metab. 15, 171–185 (2012).
  PubMed PubMed Central Google Scholar
• Meshulam, T., Simard, J. R., Wharton, J., Hamilton, J. A. & Pilch, P. F. Role of caveolin-1 and cholesterol in transmembrane fatty acid movement. Biochemistry 45, 2882–2893 (2006).
  CAS PubMed Google Scholar
• Simard, J. R. et al. Caveolins sequester fatty acids on the cytoplasmic leaflet of the plasma membrane, augment triglyceride formation and protect cells from lipotoxicity. J. Lipid Res. 51, 914–922 (2009).
  Google Scholar
• Pohl, J. et al. Long-chain fatty acid uptake into adipocytes depends on lipid raft function. Biochemistry 43, 4179–4187 (2004).
  CAS PubMed Google Scholar
• Cohen, A. W. et al. Caveolin-1-deficient mice show insulin resistance and defective insulin receptor protein expression in adipose tissue. Am. J. Physiol. Cell Physiol. 285, C222–C235 (2003).
  CAS PubMed Google Scholar
• Frank, P. G. et al. Caveolin-1 and regulation of cellular cholesterol homeostasis. Am. J. Physiol. Heart Circ. Physiol. 291, H677–H686 (2006).
  CAS PubMed Google Scholar
• Cohen, A. W. et al. Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation. Diabetes 53, 1261–1270 (2004).
  CAS PubMed Google Scholar
• Fernandez, M. A. et al. Caveolin-1 is essential for liver regeneration. Science 313, 1628–1632 (2006).
  CAS PubMed Google Scholar
• Siasos, G. et al. Adiponectin and cardiovascular disease: mechanisms and new therapeutic approaches. Curr. Med. Chem. 19, 1193–1209 (2012).
  CAS PubMed Google Scholar
• Pilch, P. F. & Liu, L. Fat caves: caveolae, lipid trafficking and lipid metabolism in adipocytes. Trends Endocrinol. Metab. 22, 318–324 (2011).
  CAS PubMed PubMed Central Google Scholar
• Martin, S. et al. Caveolin-1 deficiency leads to increased susceptibility to cell death and fibrosis in white adipose tissue: characterization of a lipodystrophic model. PLoS ONE 7, e46242 (2012).
  CAS PubMed PubMed Central Google Scholar
• Khan, T. et al. Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol. Cell. Biol. 29, 1575–1591 (2009).
  CAS PubMed Google Scholar
• Berchtold, D. et al. Plasma membrane stress induces relocalization of Slm proteins and activation of TORC2 to promote sphingolipid synthesis. Nature Cell Biol. 14, 542–547 (2012). In yeast cells, mechanical stretching of the plasma membrane causes redistribution of Slm proteins and activation of TORC2, leading to changes in the lipid composition of the plasma membrane possibly analogous to those occurring in mammalian cells upon disassembly of caveolae.
  CAS PubMed Google Scholar
• Styers, M. L., O'Connor, A. K., Grabski, R., Cormet-Boyaka, E. & Sztul, E. Depletion of β-COP reveals a role for COP-I in compartmentalization of secretory compartments and in biosynthetic transport of caveolin-1. Am. J. Physiol. Cell Physiol. 294, C1485–C1498 (2008).
  CAS PubMed Google Scholar
• Pol, A. et al. Cholesterol and fatty acids regulate dynamic caveolin trafficking through the Golgi complex and between the cell surface and lipid bodies. Mol. Biol. Cell 16, 2091–2105 (2005).
  CAS PubMed PubMed Central Google Scholar
• Tagawa, A. et al. Assembly and trafficking of caveolar domains in the cell: caveolae as stable, cargo-triggered, vesicular transporters. J. Cell Biol. 170, 769–779 (2005).
  CAS PubMed PubMed Central Google Scholar
• Manninen, A. et al. Caveolin-1 is not essential for biosynthetic apical membrane transport. Mol. Cell. Biol. 25, 10087–10096 (2005).
  CAS PubMed PubMed Central Google Scholar
• Aung, C. S., Hill, M. M., Bastiani, M., Parton, R. G. & Parat, M. O. PTRF-cavin-1 expression decreases the migration of PC3 prostate cancer cells: role of matrix metalloprotease 9. Eur. J. Cell Biol. 90, 136–142 (2011).
  CAS PubMed Google Scholar
• Gould, M. L., Williams, G. & Nicholson, H. D. Changes in caveolae, caveolin, and polymerase 1 and transcript release factor (PTRF) expression in prostate cancer progression. Prostate 70, 1609–1621 (2010).
  CAS PubMed Google Scholar
• Doyon, J. B. et al. Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nature Cell Biol. 13, 331–337 (2011).
  CAS PubMed Google Scholar
• Nassoy, P. & Lamaze, C. Stressing caveolae new role in cell mechanics. Trends Cell Biol. 22, 381–389 (2012).
  PubMed Google Scholar
• Vorgerd, M. et al. A sporadic case of rippling muscle disease caused by a de novo caveolin-3 mutation. Neurology 57, 2273–2277 (2001).
  CAS PubMed Google Scholar
• McNally, E. M. et al. Caveolin-3 in muscular dystrophy. Hum. Mol. Genet. 7, 871–877 (1998).
  CAS PubMed Google Scholar
• Woodman, S. E., Sotgia, F., Galbiati, F., Minetti, C. & Lisanti, M. P. Caveolinopathies: mutations in caveolin-3 cause four distinct autosomal dominant muscle diseases. Neurology 62, 538–543 (2004).
  CAS PubMed Google Scholar
• Minetti, C. et al. Mutations in the caveolin-3 gene cause autosomal dominant limb-girdle muscular dystrophy. Nature Genet. 18, 365–368 (1998).
  CAS PubMed Google Scholar
• Matsuda, C. et al. The sarcolemmal proteins dysferlin and caveolin-3 interact in skeletal muscle. Hum. Mol. Genet. 10, 1761–1766 (2001).
  CAS PubMed Google Scholar
• Bansal, D. & Campbell, K. P. Dysferlin and the plasma membrane repair in muscular dystrophy. Trends Cell Biol. 14, 206–213 (2004).
  CAS PubMed Google Scholar
• Vatta, M. et al. Mutant caveolin-3 induces persistent late sodium current and is associated with long-QT syndrome. Circulation 114, 2104–2112 (2006).
  CAS PubMed Google Scholar
• Cao, H., Alston, L., Ruschman, J. & Hegele, R. A. Heterozygous CAV1 frameshift mutations (MIM 601047) in patients with atypical partial lipodystrophy and hypertriglyceridemia. Lipids Health Dis. 7, 3 (2008).
  PubMed PubMed Central Google Scholar
• Dwianingsih, E. K. et al. A Japanese child with asymptomatic elevation of serum creatine kinase shows _PTRF_-CAVIN mutation matching with congenital generalized lipodystrophy type 4. Mol. Genet. Metab. 101, 233–237 (2010).
  CAS PubMed Google Scholar
• Shastry, S. et al. Congenital generalized lipodystrophy, type 4 (CGL4) associated with myopathy due to novel PTRF mutations. Am. J. Med. Genet. A 152A, 2245–2253 (2010).
  CAS PubMed PubMed Central Google Scholar
• Lee, S. W., Reimer, C. L., Oh, P., Campbell, D. B. & Schnitzer, J. E. Tumor cell growth inhibition by caveolin re-expression in human breast cancer cells. Oncogene 16, 1391–1397 (1998).
  CAS PubMed Google Scholar
• Capozza, F. et al. Absence of caveolin-1 sensitizes mouse skin to carcinogen-induced epidermal hyperplasia and tumor formation. Am. J. Pathol. 162, 2029–2039 (2003).
  CAS PubMed PubMed Central Google Scholar
• Witkiewicz, A. K. et al. An absence of stromal caveolin-1 expression predicts early tumor recurrence and poor clinical outcome in human breast cancers. Am. J. Pathol. 174, 2023–2034 (2009).
  CAS PubMed PubMed Central Google Scholar
• Koleske, A. J., Baltimore, D. & Lisanti, M. P. Reduction of caveolin and caveolae in oncogenically transformed cells. Proc. Natl Acad. Sci. USA 92, 1381–1385 (1995).
  CAS PubMed PubMed Central Google Scholar
• Sunaga, N. et al. Different roles for caveolin-1 in the development of non-small cell lung cancer versus small cell lung cancer. Cancer Res. 64, 4277–4285 (2004).
  CAS PubMed Google Scholar
• Patani, N. et al. Non-existence of caveolin-1 gene mutations in human breast cancer. Breast Cancer Res. Treat. 131, 307–310 (2012).
  CAS PubMed Google Scholar
• Hayashi, K. et al. Invasion activating caveolin-1 mutation in human scirrhous breast cancers. Cancer Res. 61, 2361–2364 (2001).
  CAS PubMed Google Scholar
• Felicetti, F. et al. Caveolin-1 tumor-promoting role in human melanoma. Int. J. Cancer 125, 1514–1522 (2009).
  CAS PubMed PubMed Central Google Scholar
• Thompson, T. C., Timme, T. L., Li, L. & Goltsov, A. Caveolin-1, a metastasis-related gene that promotes cell survival in prostate cancer. Apoptosis 4, 233–237 (1999).
  CAS PubMed Google Scholar
• Yang, G., Timme, T. L., Frolov, A., Wheeler, T. M. & Thompson, T. C. Combined c-Myc and caveolin-1 expression in human prostate carcinoma predicts prostate carcinoma progression. Cancer 103, 1186–1194 (2005).
  CAS PubMed Google Scholar
• Capozza, F. et al. Genetic ablation of Cav1 differentially affects melanoma tumor growth and metastasis in mice. Role of Cav1 in Shh heterotypic signaling and transendothelial migration. Cancer Res. 72, 2262–2274 (2012).
  CAS PubMed PubMed Central Google Scholar
• Trimmer, C. et al. CAV1 inhibits metastatic potential in melanomas through suppression of the integrin/Src/FAK signaling pathway. Cancer Res. 70, 7489–7499 (2010).
  CAS PubMed PubMed Central Google Scholar
• Xu, X. L. et al. Inactivation of human SRBC, located within the 11p15.5-p15.4 tumor suppressor region, in breast and lung cancers. Cancer Res. 61, 7943–7949 (2001).
  CAS PubMed Google Scholar
• Zochbauer-Muller, S. et al. Expression of the candidate tumor suppressor gene hSRBC is frequently lost in primary lung cancers with and without DNA methylation. Oncogene 24, 6249–6255 (2005).
  PubMed Google Scholar
• Bai, L. et al. Down-regulation of the cavin family proteins in breast cancer. J. Cell Biochem. 113, 322–328 (2012).
  CAS PubMed Google Scholar
• Parton, R. G., Hanzal-Bayer, M. & Hancock, J. F. Biogenesis of caveolae: a structural model for caveolin-induced domain formation. J. Cell Sci. 119, 787–796 (2006).
  CAS PubMed Google Scholar