Caveolae and caveolae-like membrane domains in cellular signaling and disease: Identification of downstream targets for the tumor suppressor protein caveolin-1

Biological Research

Volumn 35, Issue 2, 2002, Pages 151-167

  Bender, Florent ^b   Montoya, Margarita ^a   Monardes, Virginia ^a   Leyton, Lisette ^a   Quest, Andrew F G ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Caveolae; Caveolae like domains; Caveolin 1; Colon carcinoma cells; Lipid rafts; Microarray analysis; Tumor suppressor

Indexed keywords

CAVEOLIN 1; CHOLESTEROL; DETERGENT; EPIDERMAL GROWTH FACTOR RECEPTOR; GLYCOSPHINGOLIPID; GLYCOSYLPHOSPHATIDYLINOSITOL; GUANINE NUCLEOTIDE BINDING PROTEIN; INSULIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE SYNTHASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE C; T LYMPHOCYTE RECEPTOR; TRANSFERRIN RECEPTOR;

ARTICLE; CARCINOMA CELL; CAVEOLA; CELL COMMUNICATION; CELL FUNCTION; CELL MEMBRANE; CHOLESTEROL TRANSPORT; COLON CARCINOGENESIS; COLON CARCINOMA; CONTROLLED STUDY; DNA MICROARRAY; DOWNSTREAM PROCESSING; GENE TARGETING; HUMAN; IN VIVO STUDY; KNOCKOUT MOUSE; MAMMAL CELL; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; SOLUBILITY; TRANSCYTOSIS;

MAMMALIA;

EID: 0036403111     PISSN: 07169760     EISSN: None     Source Type: Journal    
DOI: 10.4067/S0716-97602002000200006     Document Type: Article

References (124)

1. ANDERSON RG (1998). The caveolae membrane system. Annu Rev Biochem 67:199-225
2. ANDERSON RG, KAMEN BA, ROTHBERG KG, LACEY SW (1992) Potocytosis: sequestration and transport of small molecules by caveolae. Science 255: 410-411
3. BENDER FC, REYMOND MA, BRON C, QUEST AFG (2000) Caveolin-1 levels are down-regulated in human colon tumors, and ectopic expression of caveolin-1 in colon carcinoma cell lines reduces cell tumorigenicity. Cancer Res 60: 5870-5878
4. BICKEL PE, SCHERER PE, SCHNITZER JE, OH P, LISANTI MP, LODISH HF (1997) Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J Biol Chem 272: 13793-13802
5. BISHOP JM (1991) Molecular themes in oncogenesis. Cell 64: 235-248
6. BOHUSLAV J, CINEK T, HOREJSI V (1993) Large, detergent-resistant complexes containing murine antigens Thy-1 and Ly-6 and protein tyrosine kinase p56lck. Eur J Immunol 23: 825-831
7. BROWN DA, LONDON E (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14, 111-136
8. BROWN DA, ROSE JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68, 533-544
9. 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 277, 8771-8774
10. CHANG WJ, ROTHBERG KG, KAMEN BA, ANDERSON RG (1992) Lowering the cholesterol content of MA104 cells inhibits receptor-mediated transport of folate. J Cell Biol 118, 63-69
11. CHANG WJ, YING YS, ROTHBERG KG, HOOPER NM, TURNER AJ, GAMBLIEL HA, DE GUNZBURG J, MUMBY SM, GILMAN AG, ANDERSON RG (1994) Purification and characterization of smooth muscle cell caveolae. J Cell Biol 126: 127-138
12. 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
13. COUET J, LI S, OKAMOTO T, IKEZU T, LISANTI MP (1997a) Identification of peptide and protein ligands for the caveolin-1 scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 272: 6525-6533
14. COUET J, SARGIACOMO M, LISANTI MP (1997b) 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
15. 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
16. 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
17. 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
18. ENGELMAN JA, LEE RJ, KARNEZIS A, BEARSS DJ, WEBSTER M, SIEGEL P, MULLER WJ, WINDLE JJ, PESTELL RG, LISANTI MP (1998) Reciprocal regulation of neu tyrosine kinase activity and caveolin-1 protein expression in vitro and in vivo. Implications for human breast cancer. J Biol Chem 273: 20448-20455
19. ENGELMAN JA, WYKOFF CC, YASUHARA S, SONG KS, OKAMOTO T, LISANTI MP (1997) Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J Biol Chem 272: 16374-16381
20. FAROUDI M, ZARU R, FAVIER B, VALITUTTI S (2002) New insights to the functional role of the T cell-Antigen Presenting Cell immunological synapse, Biol Res 35: 133-137
21. FEARON ER, VOGELSTEIN B (1990). A genetic model for colorectal tumorigenesis. Cell 61: 759-767
22. FELLEY-BOSCO E, BENDER F, QUEST AFG (2002) Caveolin-1-mediated post-transcriptional regulation of inducible nitric oxide synthase in human colon carcinoma cells. Biol Res 35: 169-175
23. FELLEY-BOSCO E, BENDER FC, COURJAULT-GAUTIER F, BRON C, QUEST AFG (2000) Caveolin-1 down-regulates inducible nitric oxide synthase via the proteasome pathway in human colon carcinoma cells. Proc Natl Acad Sci USA 97: 14334-14339
24. FERON O, SMITH TW, MICHEL T, KELLY RA (1997) Dynamic targeting of the agonist-stimulated m2 muscarinic acetylcholine receptor to caveolae in cardiac myocytes. J Biol Chem 272: 17744-17748
25. FIELDING CJ, FIELDING PE (1997) Intracellular cholesterol transport. J Lipid Res 38: 1503-1521
26. FRA AM, WILLIAMSON E, SIMONS K, PARTON RG (1995) De novo formation of caveolae in lymphocytes by expression of VIP21 - caveolin. Proc Natl Acad Sci USA 92: 8655-8659
27. FURUCHI T, ANDERSON RG (1998) Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK). J Biol Chem 273: 21099-21104
28. 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
29. GARCIA-CARDENA G, FAN R, STERN DF, LIU J, SESSA WC (1996a) Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem 271: 27237-27240
30. GARCIA-CARDENA G, OH P, LIU J, SCHNITZER JE, SESSA WC (1996b) Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc Natl Acad Sci USA 93: 6448-6453
31. GHOSH S, GACHHUI R, CROOKS C, WU C, LISANTI MP, STUEHR DJ (1998) Interaction between caveolin-1 and the reductase domain of endothelial nitric-oxide synthase. Consequences for catalysis. J Biol Chem 273: 22267-22271
32. GLENNEY JR, 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 USA 89: 10517-10521
33. GOLDSTEIN JL, BROWN MS, ANDERSON RG, RUSSELL DW, SCHNEIDER WJ (1985). Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu Rev Cell Biol 1: 1-39
34. GOLSTEIN P, GORIDIS C, SCHMITT-VERHULST AM, HAYOT B, PIERRES A, VAN AGTHOVEN A, KAUFMANN Y, ESHHAR Z, PIERRES M (1982) Lymphoid cell surface interaction structures detected using cytolysis- inhibiting monoclonal antibodies. Immunol. Rev 68: 5-42
35. GORODINSKY A, HARRIS DA (1995) Glycolipid-anchored proteins in neuroblastoma cells form detergent- resistant complexes without caveolin. J Cell Biol 129: 619-627
36. HAILSTONES D, SLEER LS, PARTON RG, STANLEY KK (1998) Regulation of caveolin and caveolae by cholesterol in MDCK cells. J Lipid Res 39: 369-379
37. HARDER T, SCHEIFFELE P, VERKADE P, SIMONS K (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141: 929-942
38. HETZ CA, MUNROE D, GALLEGUILLOS D, LISBOA P, MONARDES V, MONTOYA M. NEIRA M, LEYTON L, QUEST AFG (2001) Identification by ranscription profiling of genes in human colon carcinoma cells regulated by the tumor suppressor caveolin-1. Biol Res 34: R-37
39. HOPE HR, PIKE LJ (1996) Phosphoinositides and phosphoinositide-utilizing enzymes in detergent-insoluble lipid domains. Mol Biol Cell 7: 843-851
40. HUANG C, HEPLER JR, CHEN LT, GILMAN AG, ANDERSON RGW, MUMBY SM (1997) Organization of G Proteins and Adenylyl Cyclase at the Plasma Membrane. Mol Biol Cell 8: 2365-2378
41. HUNZIKER W, MELLMAN I (1989) Expression of macrophage-lymphocyte Fc receptors in Madin-Darby canine kidney cells: polarity and transcytosis differ for isoforms with or without coated pit localization domains. J Cell Biol 109: 3291-3302
42. JU H, ZOU R, VENEMA VJ, VENEMA RC (1997) Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 272: 18522-18525
43. KING KL, CIDLOWSKI JA (1998) Cell cycle regulation and apoptosis. Annu Rev Physiol 60: 601-617
44. KOGO H, FUJIMOTO T (2000) Caveolin-1 isoforms are encoded by distinct mRNAs. Identification of mouse caveolin-1 mRNA variants caused by alternative transcription initiation and splicing. FEBS Lett 465: 119-123
45. KOLESKE AJ, BALTIMORE D, LISANTI MP (1995). Reduction of caveolin and caveolae in oncogenically transformed cells. Proc Natl Acad Sci USA 92: 1381-1385
46. KURZCHALIA TV, PARTON RG (1996) And still they are moving.... dynamic properties of caveolae. FEBS Lett 389: 52-54
47. LANG DM, LOMMEL S, JUNG M, ANKERHOLD R, PETRAUSCH B, LAESSING U, WIECHERS MF, PLATTNER H, STUERMER CA (1998) Identification of reggie-1 and reggie-2 as plasma membrane-associated proteins which cocluster with activated GPI-anchored cell adhesion molecules in non-caveolar micropatches in neurons. J Neurobiol 37: 502-523
48. LANGE Y, SWAISGOOD MH, RAMOS BV, STECK TL (1989) Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. J Biol Chem 264: 3786-3793
49. 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
50. LEE H, WOODMAN SE, ENGELMAN JA, VOLONTE D, GALBIATI F, KAUFMAN HL, LUBLIN DM, LISANTI MP (2001) Palmitoylation of caveolin-1 at a single site (Cys-156) controls its coupling to the c-Src tyrosine kinase: targeting of dually acylated molecules (GPI-linked, transmembrane, or cytoplasmic) to caveolae effectively uncouples c-Src and caveolin-1 (TYR-14). J Biol Chem 276: 35150-35158
51. LEE SW, REIMER CL, OH P, CAMPBELL DB, SCHNITZER JE (1998) Tumor cell growth inhibition by caveolin re-expression in human breast cancer cells. Oncogene 16: 1391-1397
52. LENGAUER C, KINZLER KW, VOGELSTEIN B (1998) Genetic instabilities in human cancers. Nature 396: 643-649
53. LI S, COUET J, LISANTI MP (1996a) 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
54. LI S, OKAMOTO T, CHUN M, SARGIACOMO M, CASANOVA JE, HANSEN SH, NISHIMOTO I, LISANTI MP (1995) Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem 270: 15693-15701
55. LI S, SEITZ R, LISANTI MP (1996b) Phosphorylation of caveolin by src tyrosine kinases. The alpha-isoform of caveolin is selectively phosphorylated by v-Src in vivo. J Biol Chem 271: 3863-3868
56. LI S, SONG KS, LISANTI MP (1996c) Expression and characterization of recombinant caveolin. Purification by polyhistidine tagging and cholesterol-dependent incorporation into defined lipid membranes. J Biol Chem 271: 568-573
57. LIPARDI C, MORA R, COLOMER V, PALADINO S, NITSCH L, RODRIGUEZ-BOULAN E, ZURZOLO C (1998) Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI)-anchored proteins in epithelial cells. J Cell Biol 140: 617-626
58. LISANTI MP, SCHERER PE, VIDUGIRIENE J, TANG Z, HERMANOWSKI-VOSATKA A, TU YH, COOK RF, SARGIACOMO M (1994) Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J Cell Biol 126: 111-126
59. LIU J, OH P, HORNER T, ROGERS RA, SCHNITZER JE (1997) Organized endothelial cell surface signal transduction in caveolae distinct from glycosylphosphatidylinositol-anchored protein microdomains. J Biol Chem 272: 7211-7222
60. LIU J, GARCIA-CARDENA G, SESSA WC (1996a) Palmitoylation of endothelial nitric oxide synthase is necessary for optimal stimulated release of nitric oxide: implications for caveolae localization. Biochemistry 35: 13277-13281
61. LIU P, ANDERSON RG (1995) Compartmentalized production of ceramide at the cell surface. J Biol Chem 270: 27179-27185
62. LIU P, YING Y, KO YG, ANDERSON RG (1996b) Localization of platelet-derived growth factor-stimulated phosphorylation cascade to caveolae. J Biol Chem 271: 10299-10303
63. MAGEE T, PIRINER N, ADLER J, PAGAKIS SN, PARMRYD I (2002) Lipid rafts: cell surface platforms for T cell signaling. Biol Res 35: 127-131
64. MICHEL JB, FERON O, SACKS D, MICHEL T (1997) Reciprocal regulation of endothelial nitric-oxide synthase by Ca2+- calmodulin and caveolin. J Biol Chem 272: 15583-15586
65. MIDGLEY R, KERR D (1999) Colorectal cancer. Lancet 353: 391-399
66. MINEO C, JAMES GL, SMART EJ, ANDERSON RG (1996) Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane. J Biol Chem 271: 11930-11935
67. MONARDES V, LEYTON L, QUEST AFG (2001) Caveolin-1 promotes phorbol ester-induced translocation of Protein Kinas C (PKC)α to detergent-insoluble rafts of HT-29 colon carcinoma cells. Biol Res 34: R-79
68. 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
69. MONTIXI C, LANGLET C, BERNARD AM, THIMONIER J, DUBOIS C, WURBEL MA, CHAUVIN JP, PIERRES M, HE HT (1998) Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J 17: 5334-5348
70. MURATA M, PERANEN J, SCHREINER R, WIELAND F, KURZCHALIA TV, SIMONS K. (1995). VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA 92: 10339-10343
71. OKA N, YAMAMOTO M, SCHWENCKE C, KAWABE J, EBINA T, OHNO S, COUET J, LISANTI MP, ISHIKAWA Y (1997) Caveolin interaction with protein kinase C. Isoenzyme-dependent regulation of kinase activity by the caveolin scaffolding domain peptide. J Biol Chem 272: 33416-33421
72. 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
73. ORAM JF (1986) Receptor-mediated transport of cholesterol between cultured cells and high-density lipoproteins. Methods Enzymol 129: 645-659
74. PARTON RG (1996) Caveolae and caveolins. Curr Opin Cell Biol 8: 542-548
75. PARTON RG, JOGGERST B, SIMONS K (1994) Regulated internalization of caveolae. J Cell Biol 127: 1199-1215
76. PARTON RG, SIMONS K (1995) Digging into caveolae. Science 269: 1398-1399
77. PETERS DJ, MCGREW BR, PERRON DC, LIPTAK LM, LAUDANO AP (1990) In vivo phosphorylation and membrane association of the fyn proto-oncogene product in IM-9 human lymphoblasts. Oncogene 5: 1313-1319
78. PATTERSON SI (2002) Posttranslational protein S-palmitoylation and the compartmentalization of signaling molecules in neurons. Biol Res 35: 139-150
79. PIKE LJ, CASEY L (1996) Localization and turnover of phosphatidylinositol 4,5-bisphosphate in caveolin-enriched membrane domains. J Biol Chem 271:26453-26456
80. RACINE C, BELANGER M, HIRABAYASHI H, BOUCHER M, CHAKIR J, COUET J (1999) Reduction of caveolin 1 gene expression in lung carcinoma cell lines. Biochem Biophys Res Commun 255: 580-586
81. RAZANI B, ENGELMAN JA, WANG XB, SCHUBERT W, ZHANG XL, MARKS CB, MACALUSO F, RUSSELL RG, LI M, PESTELL RG, DI VIZIO D, HOU H, JR., KNEITZ B, LAGAUD G, CHRIST GJ, EDELMANN W, LISANTI MP (2001) Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276: 38121-38138
82. RODGERS W, CRISE B, ROSE JK (1994) Signals determining protein tyrosine kinase and glycosyl-phosphatidylinositol-anchored protein targeting to a glycolipid- enriched membrane fraction. Mol Cell Biol 14: 5384-5391
83. RODGERS W, ROSE JK (1996) Exclusion of CD45 inhibits activity of p56lck associated with glycolipid-enriched membrane domains. J Cell Biol 135: 1515-1523
84. 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
85. ROTHBLAT GH, BAMBERGER M, PHILLIPS MC (1986) Reverse cholesterol transport. Methods Enzymol 129: 628-644
86. ROY S, LUETTERFORST R, HARDING A, APOLLONI A, ETHERIDGE M, STANG E, ROLLS B, HANCOCK JF, PARTON RG (1999) Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nature Cell Biol 1: 98-105
87. SARGIACOMO M, SUDOL M, TANG Z, LISANTI MP (1993) Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol 122: 789-807
88. SCHLEGEL A, LISANTI MP (2000) A molecular dissection of caveolin-1 membrane attachment and oligomerization. Two separate regions of the caveolin-1 C-terminal domain mediate membrane binding and oligomer/oligomer interactions in vivo. J Biol Chem 275: 21605-21617
89. SCHLEGEL A, LISANTI MP (2001) The caveolin triad: caveolae biogenesis, cholesterol trafficking, and signal transduction. Cytokine Growth Factor Rev 12: 41-51
90. SCHNITZER JE, OH P, MCINTOSH DP (1996) Role of GTP hydrolysis in fission of caveolae directly from plasma membranes (published erratum appears in Science 1996 Nov 15;274(5290):1069]. Science 274: 239-242
91. SCHULTE T, PASCHKE KA, LAESSING U, LOTTSPEICH F, STUERMER CA (1997) Reggie-1 and reggie-2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development 124: 577-587
92. SEVERS NJ (1988) Caveolae: static inpocketings of the plasma membrane, dynamic vesicles or plain artifact? J Cell Sci 90: 341-348
93. SHAUL PW (2002) Regulation of endothelial nitric oxide synthase: location, location, location. Annu Rev Physiol 64: 749-774
94. SHAUL PW, SMART EJ, ROBINSON LJ, GERMAN Z, YUHANNA IS, YING Y, ANDERSON RG, MICHEL T (1996) Acylation targets emdothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem 271: 6518-6522
95. SHENOY-SCARIA AM, GAUEN LK, KWONG J, SHAW AS, LUBLIN DM (1993) Palmitylation of an amino-terminal cysteine motif of protein tyrosine kinases p56lck and p59fyn mediates interaction with glycosyl-phosphatidylinositol-anchored proteins. Mol Cell Biol 13: 6385-6392
96. SHIN JS, ABRAHAM SN (2001) Cell biology. Caveolae - not just craters in the cellular landscape. Science 293: 1447-1448
97. SIMIONESCU N, SIMIONESCU M, PALADE GE (1973) Permeability of muscle capillaries to exogenous myoglobin. J Cell Biol 57: 424-452
98. SIMONS K, IKONEN E. (1997). Functional rafts in cell membranes. Nature 387: 569-572
99. SIMONS K, TOOMRE D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31-39
100. SMART EJ, GRAF GA, MCNIVEN MA, SESSA WC, ENGELMAN JA, SCHERER PE, OKAMOTO T, LISANTI MP (1999) Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol 19: 7289-7304
101. SMART EJ, MINEO C, ANDERSON RG (1996a) Clustered folate receptors deliver 5-methyltetrahydrofolate to cytoplasm of MA104 cells. J Cell Biol 134: 1169-1177
102. SMART EJ, YING Y, DONZELL WC, ANDERSON RG (1996b) A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 271: 29427-29435
103. SMART EJ, YING YS, ANDERSON RG (1995a) Hormonal regulation of caveolae internalization. J Cell Biol 131: 929-938
104. SMART EJ, YING YS, MINEO C, ANDERSON RG (1995b) A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc Natl Acad Sci USA 92: 10104-10108
105. SOLOMON S, MASILAMANI M, RAJENDRAN L, BASTMEYER M, STUERMER CA, ILLGES H (2002) The lipid raft microdomain-associated protein reggie-1/flotillin-2 is expressed in human B cells and localized at the plasma membrane and centrosome in PBMCs. Immunobiology 205: 108-119
106. SONG SK, LI S, OKAMOTO T, QUILLIAM LA, SARGIACOMO M, LISANTI MP (1996) Copurification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J Biol Chem 271: 9690-9697
107. SOTGIA F, LEE JK, DAS K, BEDFORD M, PETRUCCI TC, MACIOCE P, SARGIACOMO M, BRICARELLI FD, MINETTI C, SUDOL M, LISANTI MP (2000) Caveolin-3 directly interacts with the C-terminal tail of beta-dystroglycan. Identification of a central WW-like domain within caveolin family members. J Biol Chem 275: 38048-38058
108. STANG E, KARTENBECK J, PARTON RG (1997) Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol Biol Cell 8: 47-57
109. STUERMER CA, LANG DM, KIRSCH F, WIECHERS M, DEININGER SO, PLATTNER H (2001). Glycosylphosphatidyl inositol-anchored proteins and fyn kinase assemble in noncaveolar plasma membrane microdomains defined by reggie-1 and -2. Mol Biol Cell 12: 3031-3045
110. STULNIG TM, BERGER M, SIGMUND T, STOCKINGER H, HOREJSI V, WALDHAUSL W (1997) Signal transduction via glycosyl phosphatidylinositol-anchored proteins in T cells is inhibited by lowering cellular cholesterol. J Biol Chem 272: 19242-19247
111. TANG Z, OKAMOTO T, BOONTRAKULPOONTAWEE P, KATADA T, OTSUKA AJ, LISANTI MP (1997) Identification, sequence, and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegans. Implications for the molecular evolution of mammalian caveolin genes. J Biol Chem 272: 2437-2445
112. TKACHENKO E, SIMONS M (2002) Clustering induces redistribution of syndecan-4 core protein into raft membrane domains. J Biol Chem 277: 19946-19951
113. VAN MEER G, SIMONS K (1988) Lipid polarity and sorting in epithelial cells. J Cell Biochem 36: 51-58
114. VIOLA A, SCHROEDER S, SAKAKIBARA Y, LANZAVECCHIA A (1999) T lymphocyte costimulation mediated by reorganization of membrane microdomains. Science 283: 680-682
115. VOGELSTEIN B, FEARON ER, HAMILTON SR, KERN SE, PREISINGER AC, LEPPERT M, NAKAMURA Y, WHITE R, SMITS AM, BOS JL (1988) Genetic alterations during colorectal-tumor development. N Engl J Med 319: 525-532
116. VOLONTE D, GALBIATI F, LI S, NISHIYAMA K, OKAMOTO T, LISANTI MP (1999) Flotillins/cavatellins are differentially expressed in cells and tissues and form a hetero-oligomeric complex with caveolins in vivo. Characterization and epitope-mapping of a novel flotillin-1 monoclonal antibody probe. J Biol Chem 274: 12702-12709
117. VOLONTE D, GALBIATI F, PESTELL RG, LISANTI MP (2001) Cellular stress induces the tyrosine phosphorylation of caveolin-1 (Tyr(14)) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress. J Biol Chem 276: 8094-8103
118. WARY KK, MARIOTTI A, ZURZOLO C, GIANCOTTI FG (1998) A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94. 625-634
119. WIECHEN K, DIATCHENKO L, AGOULNIK A, SCHARFF KM, SCHOBER H, ARLT K, ZHUMABAYEVA B, SIEBERT PD, DIETEL M, SCHAFER R, SERS C (2001a) Caveolin-1 is down-regulated in human ovarian carcinoma and acts as a candidate tumor suppressor gene. Am J Pathol 159: 1635-1643
120. WIECHEN K, SERS C, AGOULNIK A, ARLT K, DIETEL M, SCHLAG PM, SCHNEIDER U (2001b) Down-regulation of caveolin-1, a candidate tumor suppressor gene, in sarcomas. Am J Pathol 158: 833-839
121. WU C, BUTZ S, YING Y, ANDERSON RG (1997) Tyrosine kinase receptors concentrated in caveolae-like domains from neuronal plasma membrane. J Biol Chem 272: 3554-3559
122. XAVIER R, BRENNAN T, LI Q, MCCORMACK C, SEED B (1998) Membrane compartmentation is required for efficient T cell activation. Immunity 8: 723-732
123. YANG G, TRUONG LD, TIMME TL, REN C, WHEELER TM, PARK SH, NASU Y, BANGMA CH, KATTAN MW, SCARDINO PT, THOMPSON TC (1998) Elevated expression of caveolin is associated with prostate and breast cancer. Clin Cancer Res 4: 1873-1880
124. ZURZOLO C, VANT HOF W, VAN MEER G, RODRIGUEZ-BOULAN E (1994) VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO J 13: 42-53