Regulation of intracellular signaling and function by caveolin

FASEB Journal

Volumn 28, Issue 9, 2014, Pages 3823-3831

  Fridolfsson, Heidi N ^a,b   Roth, David M ^a,b   Insel, Paul A ^c,d   Patel, Hemal H ^a,b  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b University of California   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d San Diego   (United States)

Author keywords

Cell physiology; Cellular organelles; Cholesterol

Indexed keywords

CAVEOLIN 1; CAVEOLIN 2; CAVEOLIN 3; FAT DROPLET; LIPID; CAVEOLIN;

CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL NUCLEUS; CHOLESTEROL TRANSPORT; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; EXOCYTOSIS; GOLGI MEMBRANE; HUMAN; INTRACELLULAR SIGNALING; LYSOSOME; MITOCHONDRION; NONHUMAN; PEROXISOME; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION; TRANSCYTOSIS; ANIMAL; INTRACELLULAR MEMBRANE; METABOLISM;

ANIMALS; CAVEOLINS; HUMANS; INTRACELLULAR MEMBRANES; MEMBRANE MICRODOMAINS; SIGNAL TRANSDUCTION;

EID: 84907221124     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-252320     Document Type: Review

References (104)

1. Palade, G. (1953) Fine structure of blood capillaries. J. Appl. Phys. 24, 1424
2. Williams, T. M., and Lisanti, M. P. (2004) The caveolin proteins. Genome Biol. 5, 214
3. Song, K. S., Scherer, P. E., Tang, Z., Okamoto, T., Li, S., Chafel, M., Chu, C., Kohtz, D. S., and Lisanti, M. P. (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
4. Head, B. P., Patel, H. H., Tsutsumi, Y. M., Hu, Y., Mejia, T., Mora, R. C., Insel, P. A., Roth, D. M., Drummond, J. C., and Patel, P. M. (2008) Caveolin-1 expression is essential for N-methyl-D-aspartate receptor-mediated Src and extracellular signal-regulated kinase 1/2 activation and protection of primary neurons from ischemic cell death. FASEB J. 22, 828-840
5. Patel, H. H., Murray, F., and Insel, P. A. (2008) Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu. Rev. Pharmacol. Toxicol. 48, 359-391
6. Tagawa, A., Mezzacasa, A., Hayer, A., Longatti, A., Pelkmans, L., and Helenius, A. (2005) Assembly and trafficking of caveolar domains in the cell: caveolae as stable, cargo-triggered, vesicular transporters. J. Cell Biol. 170, 769-779
7. Smart, E. J., Ying, Y. S., Conrad, P. A., and Anderson, R. G. (1994) Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 127, 1185-1197
8. Gkantiragas, I., Brugger, B., Stuven, E., Kaloyanova, D., Li, X. Y., Lohr, K., Lottspeich, F., Wieland, F. T., and Helms, J. B. (2001) Sphingomyelin-enriched microdomains at the Golgi complex. Mol. Biol. Cell 12, 1819-1833
9. Li, W. P., Liu, P., Pilcher, B. K., and Anderson, R. G. (2001) Cell-specific targeting of caveolin-1 to caveolae, secretory vesicles, cytoplasm or mitochondria. J. Cell Sci. 114, 1397-1408
10. Fridolfsson, H. N., Kawaraguchi, Y., Ali, S. S., Panneerselvam, M., Niesman, I. R., Finley, J. C., Kellerhals, S. E., Migita, M. Y., Okada, H., Moreno, A. L., Jennings, M., Kidd, M. W., Bonds, J. A., Balijepalli, R. C., Ross, R. S., Patel, P. M., Miyanohara, A., Chen, Q., Lesnefsky, E. J., Head, B. P., Roth, D. M., Insel, P. A., and Patel, H. H. (2012) Mitochondria-localized caveolin in adaptation to cellular stress and injury. FASEB J. 26, 4637-4649
11. Jeong, K., Kwon, H., Lee, J., Jang, D., Hwang, E. M., Park, J. Y., and Pak, Y. (2012) Rab6-mediated retrograde transport regulates inner nuclear membrane targeting of caveolin-2 in response to insulin. Traffic 13, 1218-1233
12. Pol, A., Calvo, M., and Enrich, C. (1998) Isolated endosomes from quiescent rat liver contain the signal transduction machinery. Differential distribution of activated Raf-1 and Mek in the endocytic compartment. FEBS Lett. 441, 34-38
13. Mundy, D. I., Li, W. P., Luby-Phelps, K., and Anderson, R. G. (2012) Caveolin targeting to late endosome/lysosomal membranes is induced by perturbations of lysosomal pH and cholesterol content. Mol. Biol. Cell 23, 864-880
14. Woudenberg, J., Rembacz, K. P., van den Heuvel, F. A., Woudenberg-Vrenken, T. E., Buist-Homan, M., Geuken, M., Hoekstra, M., Deelman, L. E., Enrich, C., Henning, R. H., Moshage, H., and Faber, K. N. (2010) Caveolin-1 is enriched in the peroxisomal membrane of rat hepatocytes. Hepatology 51, 1744-1753
15. Ostermeyer, A. G., Paci, J. M., Zeng, Y., Lublin, D. M., Munro, S., and Brown, D. A. (2001) Accumulation of caveolin in the endoplasmic reticulum redirects the protein to lipid storage droplets. J. Cell Biol. 152, 1071-1078
16. Monier, S., Parton, R. G., Vogel, F., Behlke, J., Henske, A., and Kurzchalia, T. V. (1995) VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol. Biol. Cell 6, 911-927
17. Monier, S., Dietzen, D. J., Hastings, W. R., Lublin, D. M., and Kurzchalia, T. V. (1996) Oligomerization of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol. FEBS Lett. 388, 143-149
18. Hayer, A., Stoeber, M., Bissig, C., and Helenius, A. (2010) Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 11, 361-382
19. Pol, A., Martin, S., Fernandez, M. A., Ingelmo-Torres, M., Ferguson, C., Enrich, C., and Parton, R. G. (2005) 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
20. Hill, M. M., Bastiani, M., Luetterforst, R., Kirkham, M., Kirkham, A., Nixon, S. J., Walser, P., Abankwa, D., Oorschot, V. M., Martin, S., Hancock, J. F., and Parton, R. G. (2008) PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132, 113-124
21. Liu, L., Brown, D., McKee, M., Lebrasseur, N. K., Yang, D., Albrecht, K. H., Ravid, K., and Pilch, P. F. (2008) Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell. Metab. 8, 310-317
22. Liu, L., and Pilch, P. F. (2008) A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J. Biol. Chem. 283, 4314-4322
23. Okamoto, T., Schlegel, A., Scherer, P. E., and Lisanti, M. P. (1998) Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J. Biol. Chem. 273, 5419-5422
24. Couet, J., Li, S., Okamoto, T., Ikezu, T., and Lisanti, M. P. (1997) 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
25. Garcia-Cardena, G., Martasek, P., Masters, B. S., Skidd, P. M., Couet, J., Li, S., Lisanti, M. P., and Sessa, W. C. (1997) 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
26. Feron, O., Belhassen, L., Kobzik, L., Smith, T. W., Kelly, R. A., and 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
27. Shaul, P. W., Smart, E. J., Robinson, L. J., German, Z., Yuhanna, I. S., Ying, Y., Anderson, R. G., and Michel, T. (1996) Acylation targets endothelial nitric-oxide synthase to plasmalemmal caveolae. J. Biol. Chem. 271, 6518-6522
28. Ju, H., Zou, R., Venema, V. J., and Venema, R. C. (1997) Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J. Biol. Chem. 272, 18522-18525
29. Bucci, M., Gratton, J. P., Rudic, R. D., Acevedo, L., Roviezzo, F., Cirino, G., and Sessa, W. C. (2000) In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat. Med. 6, 1362-1367
30. Maniatis, N. A., Shinin, V., Schraufnagel, D. E., Okada, S., Vogel, S. M., Malik, A. B., and Minshall, R. D. (2008) Increased pulmonary vascular resistance and defective pulmonary artery filling in caveolin-1-/- mice. Am. J. Physiol. Lung. Cell. Mol. Physiol. 294, L865-873
31. Roth, D. M., and Patel, H. H. (2011) Role of caveolae in cardiac protection. Pediatr. Cardiol. 32, 329-333
32. Hausenloy, D. J., and Yellon, D. M. (2007) Reperfusion injury salvage kinase signalling: taking a RISK for cardioprotection. Heart Fail. Rev. 12, 217-234
33. Peart, J. N., and Headrick, J. P. (2009) Clinical cardioprotection and the value of conditioning responses. Am. J. Physiol. Heart Circ. Physiol. 296, H1705-1720
34. Krajewska, W. M., and Maslowska, I. (2004) Caveolins: structure and function in signal transduction. Cell. Mol. Biol. Lett. 9, 195-220
35. Patel, H. H., Tsutsumi, Y. M., Head, B. P., Niesman, I. R., Jennings, M., Horikawa, Y., Huang, D., Moreno, A. L., Patel, P. M., Insel, P. A., and Roth, D. M. (2007) Mechanisms of cardiac protection from ischemia/reperfusion injury: a role for caveolae and caveolin-1. FASEB J. 21, 1565-1574
36. Razani, B., Zhang, X. L., Bitzer, M., von Gersdorff, G., Bottinger, E. P., and Lisanti, M. P. (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
37. Di Guglielmo, G. M., Le Roy, C., Goodfellow, A. F., and Wrana, J. L. (2003) Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat. Cell Biol. 5, 410-421
38. Del Pozo, M. A., Balasubramanian, N., Alderson, N. B., Kiosses, W. B., Grande-Garcia, A., Anderson, R. G., and Schwartz, M. A. (2005) Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat. Cell Biol. 7, 901-908
39. Marchiando, A. M., Shen, L., Graham, W. V., Weber, C. R., Schwarz, B. T., Austin, J. R., 2nd, Raleigh, D. R., Guan, Y., Watson, A. J., Montrose, M. H., and Turner, J. R. (2010) Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J. Cell Biol. 189, 111-126
40. Orlichenko, L., Weller, S. G., Cao, H., Krueger, E. W., Awoniyi, M., Beznoussenko, G., Buccione, R., and McNiven, M. A. (2009) Caveolae mediate growth factor-induced disassembly of adherens junctions to support tumor cell dissociation. Mol. Biol. Cell 20, 4140-4152
41. Gervasio, O. L., Whitehead, N. P., Yeung, E. W., Phillips, W. D., and Allen, D. G. (2008) TRPC1 binds to caveolin-3 and is regulated by Src kinase - role in Duchenne muscular dystrophy. J. Cell Sci. 121, 2246-2255
42. Schubert, W., Frank, P. G., Razani, B., Park, D. S., Chow, C. W., and Lisanti, M. P. (2001) Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J. Biol. Chem. 276, 48619-48622
43. Minshall, R. D., Tiruppathi, C., Vogel, S. M., and Malik, A. B. (2002) Vesicle formation and trafficking in endothelial cells and regulation of endothelial barrier function. Histochem. Cell. Biol. 117, 105-112
44. Hu, G., Vogel, S. M., Schwartz, D. E., Malik, A. B., and Minshall, R. D. (2008) Intercellular adhesion molecule-1-dependent neutrophil adhesion to endothelial cells induces caveolae-mediated pulmonary vascular hyperpermeability. Circ. Res. 102, e120-131
45. Minshall, R. D., Sessa, W. C., Stan, R. V., Anderson, R. G., and Malik, A. B. (2003) Caveolin regulation of endothelial function. Am. J. Physiol. Lung Cell. Mol. Physiol. 285, L1179-1183
46. Sun, Y., Hu, G., Zhang, X., and Minshall, R. D. (2009) Phosphorylation of caveolin-1 regulates oxidant-induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ. Res. 105, 676-685, 615 p following 685
47. Murata, M., Peranen, J., Schreiner, R., Wieland, F., Kurzchalia, T. V., and Simons, K. (1995) VIP21/caveolin is a cholesterol-binding protein. Proc. Natl. Acad. Sci. U. S. A. 92, 10339-10343
48. Pol, A., Luetterforst, R., Lindsay, M., Heino, S., Ikonen, E., and Parton, R. G. (2001) A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J. Cell Biol. 152, 1057-1070
49. Fielding, P. E., and Fielding, C. J. (1995) Plasma membrane caveolae mediate the efflux of cellular free cholesterol. Biochemistry 34, 14288-14292
50. Meshulam, T., Simard, J. R., Wharton, J., Hamilton, J. A., and Pilch, P. F. (2006) Role of caveolin-1 and cholesterol in transmembrane fatty acid movement. Biochemistry 45, 2882-2893
51. Le Lay, S., Hajduch, E., Lindsay, M. R., Le Liepvre, X., Thiele, C., Ferre, P., Parton, R. G., Kurzchalia, T., Simons, K., and Dugail, I. (2006) Cholesterol-induced caveolin targeting to lipid droplets in adipocytes: a role for caveolar endocytosis. Traffic 7, 549-561
52. Liu, P., Li, W. P., Machleidt, T., and Anderson, R. G. (1999) Identification of caveolin-1 in lipoprotein particles secreted by exocrine cells. Nat. Cell Biol. 1, 369-375
53. 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, S. P., Garcia-Ruiz, C., Perez-Navarro, E., Fernandez-Checa, J. C., and Pol, A. (2011) Caveolin-1 deficiency causes cholesterol-dependent mitochondrial dysfunction and apoptotic susceptibility. Curr. Biol. 21, 681-686
54. DeGrella, R. F., and Simoni, R. D. (1982) Intracellular transport of cholesterol to the plasma membrane. J. Biol. Chem. 257, 14256-14262
55. Urbani, L., and Simoni, R. D. (1990) Cholesterol and vesicular stomatitis virus G protein take separate routes from the endoplasmic reticulum to the plasma membrane. J. Biol. Chem. 265, 1919-1923
56. Smart, E. J., Ying, Y., Donzell, W. C., and Anderson, R. G. (1996) A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J. Biol. Chem. 271, 29427-29435
57. Lange, Y. (1994) Cholesterol movement from plasma membrane to rough endoplasmic reticulum. Inhibition by progesterone. J. Biol. Chem. 269, 3411-3414
58. Conrad, P. A., Smart, E. J., Ying, Y. S., Anderson, R. G., and Bloom, G. S. (1995) Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J. Cell Biol. 131, 1421-1433
59. Munro, S. (1998) Localization of proteins to the Golgi apparatus. Trends Cell Biol. 8, 11-15
60. Sasai, K., Ikeda, Y., Ihara, H., Honke, K., and Taniguchi, N. (2003) Caveolin-1 regulates the functional localization of N-acetylglucosaminyltransferase III within the Golgi apparatus. J. Biol. Chem. 278, 25295-25301
61. Razani, B., and Lisanti, M. P. (2001) Caveolin-deficient mice: insights into caveolar function human disease. J. Clin. Invest. 108, 1553-1561
62. Hayashi, T., Rizzuto, R., Hajnoczky, G., and Su, T. P. (2009) MAM: more than just a housekeeper. Trends Cell Biol. 19, 81-88
63. Sano, R., Annunziata, I., Patterson, A., Moshiach, S., Gomero, E., Opferman, J., Forte, M., and d'Azzo, A. (2009) GM1-ganglioside accumulation at the mitochondria-associated ER membranes links ER stress to Ca(2+)-dependent mitochondrial apoptosis. Mol. Cell. 36, 500-511
64. Razani, B., Combs, T. P., Wang, X. B., Frank, P. G., Park, D. S., Russell, R. G., Li, M., Tang, B., Jelicks, L. A., Scherer, P. E., and Lisanti, M. P. (2002) Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J. Biol. Chem. 277, 8635-8647
65. Cohen, A. W., Razani, B., Wang, X. B., Combs, T. P., Williams, T. M., Scherer, P. E., and Lisanti, M. P. (2003) Caveolin-1-deficient mice show insulin resistance and defective insulin receptor protein expression in adipose tissue. Am. J. Physiol. Cell. Physiol. 285, C222-C235
66. Cohen, A. W., Razani, B., Schubert, W., Williams, T. M., Wang, X. B., Iyengar, P., Brasaemle, D. L., Scherer, P. E., and Lisanti, M. P. (2004) Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation. Diabetes 53, 1261-1270
67. Asterholm, I. W., Mundy, D. I., Weng, J., Anderson, R. G., and Scherer, P. E. (2012) Altered mitochondrial function and metabolic inflexibility associated with loss of caveolin-1. Cell. Metab. 15, 171-185
68. Mastrodonato, M., Calamita, G., Rossi, R., Mentino, D., Bonfrate, L., Portincasa, P., Ferri, D., and Liquori, G. E. (2011) Altered distribution of caveolin-1 in early liver steatosis. Eur. J. Clin. Invest. 41, 642-651
69. Cohen, A. W., Schubert, W., Brasaemle, D. L., Scherer, P. E., and Lisanti, M. P. (2005) Caveolin-1 expression is essential for proper nonshivering thermogenesis in brown adipose tissue. Diabetes 54, 679-686
70. Horikawa, Y. T., Panneerselvam, M., Kawaraguchi, Y., Tsutsumi, Y. M., Ali, S. S., Balijepalli, R. C., Murray, F., Head, B. P., Niesman, I. R., Rieg, T., Vallon, V., Insel, P. A., Patel, H. H., and Roth, D. M. (2011) Cardiac-specific overexpression of caveolin-3 attenuates cardiac hypertrophy and increases natriuretic peptide expression and signaling. J. Am. Coll. Cardiol. 57, 2273-2283
71. Tsutsumi, Y. M., Horikawa, Y. T., Jennings, M. M., Kidd, M. W., Niesman, I. R., Yokoyama, U., Head, B. P., Hagiwara, Y., Ishikawa, Y., Miyanohara, A., Patel, P. M., Insel, P. A., Patel, H. H., and Roth, D. M. (2008) Cardiac-specific overexpression of caveolin-3 induces endogenous cardiac protection by mimicking ischemic preconditioning. Circulation 118, 1979-1988
72. Moroianu, J., and Riordan, J. F. (1994) Nuclear translocation of angiogenin in proliferating endothelial cells is essential to its angiogenic activity. Proc. Natl. Acad. Sci. U. S. A. 91, 1677-1681
73. Rakowicz-Szulczynska, E. M., Rodeck, U., Herlyn, M., and Koprowski, H. (1986) Chromatin binding of epidermal growth factor, nerve growth factor, and platelet-derived growth factor in cells bearing the appropriate surface receptors. Proc. Natl. Acad. Sci. U. S. A. 83, 3728-3732
74. Ferrara, N., and Davis-Smyth, T. (1997) The biology of vascular endothelial growth factor. Endocr. Rev. 18, 4-25
75. Feng, Y., Venema, V. J., Venema, R. C., Tsai, N., Behzadian, M. A., and Caldwell, R. B. (1999) VEGF-induced permeability increase is mediated by caveolae. Invest. Ophthalmol. Vis. Sci. 40, 157-167
76. Feng, Y., Venema, V. J., Venema, R. C., Tsai, N., and Caldwell, R. B. (1999) VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem. Biophys. Res. Commun. 256, 192-197
77. Kwon, H., Jeong, K., and Pak, Y. (2009) Identification of pY19-caveolin-2 as a positive regulator of insulin-stimulated actin cytoskeleton-dependent mitogenesis. J. Cell. Mol. Med. 13, 1549-1564
78. Kwon, H., Jeong, K., Hwang, E. M., Park, J. Y., and Pak, Y. (2011) A novel domain of caveolin-2 that controls nuclear targeting: regulation of insulin-specific ERK activation and nuclear translocation by caveolin-2. J. Cell. Mol. Med. 15, 888-908
79. Kwon, H., Jeong, K., Hwang, E. M., Park, J. Y., Hong, S. G., Choi, W. S., and Pak, Y. (2009) Caveolin-2 regulation of STAT3 transcriptional activation in response to insulin. Biochim. Biophys. Acta 1793, 1325-1333
80. Engelman, J. A., Zhang, X. L., Galbiati, F., and Lisanti, M. P. (1998) Chromosomal localization, genomic organization, and developmental expression of the murine caveolin gene family (Cav-1, -2, and -3). Cav-1 and Cav-2 genes map to a known tumor suppressor locus (6-A2/7q31). FEBS Lett. 429, 330-336
81. Fiucci, G., Ravid, D., Reich, R., and Liscovitch, M. (2002) Caveolin-1 inhibits anchorage-independent growth, anoikis and invasiveness in MCF-7 human breast cancer cells. Oncogene 21, 2365-2375
82. Bagnoli, M., Tomassetti, A., Figini, M., Flati, S., Dolo, V., Canevari, S., and Miotti, S. (2000) Downmodulation of caveolin-1 expression in human ovarian carcinoma is directly related to alpha-folate receptor overexpression. Oncogene 19, 4754-4763
83. Koleske, A. J., Baltimore, D., and Lisanti, M. P. (1995) Reduction of caveolin and caveolae in oncogenically transformed cells. Proc. Natl. Acad. Sci. U. S. A. 92, 1381-1385
84. Engelman, J. A., Wykoff, C. C., Yasuhara, S., Song, K. S., Okamoto, T., and Lisanti, M. P. (1997) Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J. Biol. Chem. 272, 16374-16381
85. Lee, S. W., Reimer, C. L., Oh, P., Campbell, D. B., and Schnitzer, J. E. (1998) Tumor cell growth inhibition by caveolin re-expression in human breast cancer cells. Oncogene 16, 1391-1397
86. Sanna, E., Miotti, S., Mazzi, M., De Santis, G., Canevari, S., and Tomassetti, A. (2007) Binding of nuclear caveolin-1 to promoter elements of growth-associated genes in ovarian carcinoma cells. Exp. Cell. Res. 313, 1307-1317
87. Jackle, S., Runquist, E. A., Miranda-Brady, S., and Havel, R. J. (1991) Trafficking of the epidermal growth factor receptor and transferrin in three hepatocytic endosomal fractions. J. Biol. Chem. 266, 1396-1402
88. Baass, P. C., Di Guglielmo, G. M., Authier, F., Posner, B. I., and Bergeron, J. J. (1995) Compartmentalized signal transduction by receptor tyrosine kinases. Trends Cell Biol. 5, 465-470
89. Butler, J. D., Blanchette-Mackie, J., Goldin, E., O'Neill, R. R., Carstea, G., Roff, C. F., Patterson, M. C., Patel, S., Comly, M. E., Cooney, A., and et al. (1992) Progesterone blocks cholesterol translocation from lysosomes. J. Biol. Chem. 267, 23797-23805
90. Lazarow, P. B. (1978) Rat liver peroxisomes catalyze the beta oxidation of fatty acids. J. Biol. Chem. 253, 1522-1528
91. Pedersen, J. I., and Gustafsson, J. (1980) Conversion of 3 alpha, 7 alpha, 12 alpha-trihydroxy-5 beta-cholestanoic acid into cholic acid by rat liver peroxisomes. FEBS Lett. 121, 345-348
92. Fujimoto, T., Kogo, H., Ishiguro, K., Tauchi, K., and Nomura, R. (2001) Caveolin-2 is targeted to lipid droplets, a new "membrane domain" in the cell. J. Cell Biol. 152, 1079-1085
93. Blouin, C. M., Le Lay, S., Eberl, A., Kofeler, H. C., Guerrera, I. C., Klein, C., Le Liepvre, X., Lasnier, F., Bourron, O., Gautier, J. F., Ferre, P., Hajduch, E., and Dugail, I. (2010) Lipid droplet analysis in caveolin-deficient adipocytes: alterations in surface phospholipid composition and maturation defects. J. Lipid Res. 51, 945-956
94. Pol, A., Martin, S., Fernandez, M. A., Ferguson, C., Carozzi, A., Luetterforst, R., Enrich, C., and Parton, R. G. (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
95. Van Meer, G. (2001) Caveolin, cholesterol, and lipid droplets? J. Cell Biol. 152, F29-34
96. Fuhs, S. R., and Insel, P. A. (2011) Caveolin-3 undergoes SUMOylation by the SUMO E3 ligase PIASy: sumoylation affects G-protein-coupled receptor desensitization. J. Biol. Chem. 286, 14830-14841
97. Kirchner, P., Bug, M., and Meyer, H. (2013) Ubiquitination of the N-terminal region of caveolin-1 regulates endosomal sorting by the VCP/p97 AAA-ATPase. J. Biol. Chem. 288, 7363-7372
98. Hayer, A., Stoeber, M., Ritz, D., Engel, S., Meyer, H. H., and Helenius, A. (2010) Caveolin-1 is ubiquitinated and targeted to intralumenal vesicles in endolysosomes for degradation. J. Cell Biol. 191, 615-629
99. Glenney, J. R., Jr., and Soppet, D. (1992) Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 89, 10517-10521
100. Dietzen, D. J., Hastings, W. R., and Lublin, D. M. (1995) Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae. J. Biol. Chem. 270, 6838-6842
101. Head, B. P., Patel, H. H., and Insel, P. A. (2014) Interaction of membrane/lipid rafts with the cytoskeleton: impact on signaling and function: membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signaling. Biochim. Biophys. Acta 1838, 532-545
102. Niesman, I. R., Zemke, N., Fridolfsson, H. N., Haushalter, K. J., Levy, K., Grove, A., Schnoor, R., Finley, J. C., Patel, P. M., Roth, D. M., Head, B. P., and Patel, H. H. (2013) Caveolin isoform switching as a molecular, structural, and metabolic regulator of microglia. Mol. Cell. Neurosci. 56, 283-297
103. Boscher, C., and Nabi, I. R. (2013) Galectin-3- and phosphocaveolin-1-dependent outside-in integrin signaling mediates the EGF motogenic response in mammary cancer cells. Mol. Biol. Cell 24, 2134-2145
104. Shiroto, T., Romero, N., Sugiyama, T., Sartoretto, J. L., Kalwa, H., Yan, Z., Shimokawa, H., and Michel, T. (2014) Caveolin-1 is a critical determinant of autophagy, metabolic switching, and oxidative stress in vascular endothelium. PLoS One 9, e87871