The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: Implications for molecular pharmacology

British Journal of Pharmacology

Volumn 143, Issue 2, 2004, Pages 235-245

  Ostrom, Rennolds S ^a   Insel, Paul A ^b,c,d  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b University of California San Diego   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

adrenergic receptors; Adenylyl cyclase; Caveolae; Compartmentation; G protein coupled receptors; G proteins; Lipid rafts

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; GUANOSINE TRIPHOSPHATE; NEUROTRANSMITTER; PROTEIN SUBUNIT;

CAVEOLA; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL MATURATION; CELL SPECIFICITY; CELL TYPE; GENE LOCATION; HORMONE RESPONSE; HUMAN; HUMAN CELL; LIPID MEMBRANE; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RECEPTOR GENE; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; SYSTEMATIC REVIEW;

CAVEOLAE; CHOLESTEROL; HUMANS; LIPIDS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SPHINGOLIPIDS;

EID: 4744346615     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0705930     Document Type: Review

References (124)

1. ALOUSI, A.A., JASPER, J.R., INSEL, P.A. & MOTULSKY, H.J. (1991). Stoichiometry of receptor-Gs-adenylate cyclase interactions. FASEB J., 5, 2300-2303.
2. ANDERSON, R.G. (1998). The caveolae membrane system. Annu. Rev. Biochem., 67, 199-225.
3. ANDERSON, R.G. & JACOBSON, K. (2002). A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science, 296, 1821-1825.
4. AWASTHI-KALIA, M., SCHNETKAMP, P.P. & DEANS, J.P. (2001). Differential effects of filipin and methyl-beta-cyclodextrin on B cell receptor signaling. Biochem. Biophys. Res. Commun., 287, 77-82.
5. BAILLIE, G.S., SOOD, A., MCPHEE, I., GALL, I., PERRY, S.J., LEFKOWITZ, R.J. & HOUSLAY, M.D. (2003). beta-Arrestin-mediated PDE4 cAMP phosphodiesterase recruitment regulates beta-adrenoceptor switching from Gs to Gi. Proc. Natl. Acad. Sci. U.S.A., 100, 940-945.
6. BERGDAHL, A., GOMEZ, M.F., DREJA, K., XU, S.Z., ADNER, M., BEECH, D.J., BROMAN, J., HELLSTRAND, P. & SWARD, K. (2003). Cholesterol depletion impairs vascular reactivity to endothelin-1 by reducing store-operated Ca2+ entry dependent on TRPC1. Circ. Res., 93, 839-847.
7. BOCKAERT, J., MARIN, P., DUMUIS, A. & FAGNI, L. (2003). The 'magic tail' of G protein-coupled receptors: an anchorage for functional protein networks. FEBS Lett., 546, 65-72.
8. BRADY, J.D., RICH, T.C., LE, X., STAFFORD, K., FOWLER, C.J., LYNCH, L., KARPEN, J.W., BROWN, R.L. & MARTENS, J.R. (2004). Functional role of lipid raft microdomains in cyclic nucleotide-gated channel activation. Mol. Pharmacol., 65, 503-511.
9. CARMAN, C.V., LISANTI, M.P. & BENOVIC, J.L. (1999). Regulation of G protein-coupled receptor kinases by caveolin. J. Biol. Chem., 274, 8858-8864.
10. CHUN, M., LIYANAGE, U.K., LISANTI, M.P. & LODISH, H.F. (1994). Signal transduction of a G protein-coupled receptor in caveolae: colocalization of endothelin and its receptor with caveolin. Proc. Natl. Acad. Sci. U.S.A., 91, 11728-11732.
11. CLAPHAM, D.E. & NEER, E.J. (1997). G protein beta gamma subunits. Annu. Rev. Pharmacol. Toxicol., 37, 167-203.
12. CLAPHAM, D.E., RUNNELS, L.W. & STRUBING, C. (2001). The TRP ion channel family. Nat. Rev. Neurosci., 2, 387-396.
13. COOPER, D.M. (2003). Molecular and cellular requirements for the regulation of adenylate cyclases by calcium. Biochem. Soc. Trans., 31, 912-915.
14. COUET, J., SARGIACOMO, M. & LISANTI, M.P. (1997). Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J. Biol. Chem., 272, 30429-30438.
15. DARBY, P.J., KWAN, C.Y. & DANIEL, E.E. (2000). Caveolae from canine airway smooth muscle contain the necessary components for a role in Ca(2+) handling. Am. J. Physiol. Lung Cell. Mol. Physiol., 279, L1226-L1235.
16. DE WEERD, W.F. & LEEB-LUNDBERG, L.M. (1997). Bradykinin sequesters B2 bradykinin receptors and the receptor-coupled Galpha subunits Galphaq and Galphai in caveolae in DDT1 MF-2 smooth muscle cells. J. Biol. Chem., 272, 17858-17866.
17. DOHLMAN, H.G. & THORNER, J. (1997). RGS proteins and signaling by heterotrimeric G proteins. J. Biol. Chem., 272, 3871-3874.
18. ENGELMAN, J.A., CHU, C., LIN, A., JO, H., IKEZU, T., OKAMOTO, T., KOHTZ, D.S. & LISANTI, M.P. (1998). Caveolin-mediated regulation of signaling along the p42/44 MAP kinase cascade in vivo. A role for the caveolin-scaffolding domain. FEBS Lett., 428, 205-211.
19. FAGAN, K.A., SMITH, K.E. & COOPER, D.M. (2000). Regulation of the Ca2+-inhibitable adenylyl cyclase type VI by capacitative Ca2+ entry requires localization in cholesterol-rich domains. J. Biol. Chem., 275, 26530-26537.
20. FERGUSON, S.S. (2001). Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol. Rev., 53, 1-24.
21. FERON, O., SALDANA, F., MICHEL, J.B. & MICHEL, T. (1998). The endothelial nitric-oxide synthase-caveolin regulatory cycle. J. Biol. Chem., 273, 3125-3128.
22. FERON, O., SMITH, T.W., MICHEL, T. & KELLY, R.A. (1997). Dynamic targeting of the agonist-stimulated m2 muscarinic acetylcholine receptor to caveolae in cardiac myocytes. J. Biol. Chem., 272, 17744-17748.
23. FREDRIKSSON, R., LAGERSTROM, M.C., LUNDIN, L.G. & SCHIOTH, H.B. (2003). The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol., 63, 1256-1272.
24. GAGNON, A.W., KALLAL, L. & BENOVIC, J.L. (1998). Role of clathrin-mediated endocytosis in agonist-induced down-regulation of the beta2-adrenergic receptor. J. Biol. Chem., 273, 6976-6981.
25. GALBIATI, F., RAZANI, B. & LISANTI, M.P. (2001). Emerging themes in lipid rafts and caveolae. Cell, 106, 403-411.
26. GARCÍA-CARDEÑA, G., MARTASEK, P., MASTERS, B.S., SKIDD, P.M., COUET, J., LI, S., LISANTI, M.P. & 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.
27. GOODMAN JR, O.B., KRUPNICK, J.G., SANTINI, F., GUREVICH, V.V., PENN, R.B., GAGNON, A.W., KEEN, J.H. & BENOVIC, J.L. (1996). Beta-arrestin acts as a clathrin adaptor in endocytosis of the beta2-adrenergic receptor. Nature, 383, 447-450.
28. GUZZI, F., ZANCHETTA, D., CASSONI, P., GUZZI, V., FRANCOLINI, M., PARENTI, M. & CHINI, B. (2002). Localization of the human oxytocin receptor in caveolin-1 enriched domains turns the receptor-mediated inhibition of cell growth into a proliferative response. Oncogene, 21, 1658-1667.
29. HAKAK, Y., SHRESTHA, D., GOEGEL, M.C., BEHAN, D.P. & CHALMERS, D.T. (2003). Global analysis of G-protein-coupled receptor signaling in human tissues. FEBS Lett., 550, 11-17.
30. HALL, R.A., PREMONT, R.T. & LEFKOWITZ, R.J. (1999). Heptahelical receptor signaling: beyond the G protein paradigm. J. Cell Biol., 145, 927-932.
31. HANOUNE, J. & DEFER, N. (2001). Regulation and role of adenylyl cyclase isoforms. Annu. Rev. Pharmacol. Toxicol., 41, 145-174.
32. HERMANS, E. (2003). Biochemical and pharmacological control of the multiplicity of coupling at G-protein-coupled receptors. Pharmacol. Ther., 99, 25-44.
33. HILL, J., HOWLETT, A. & KLEIN, C. (2000). Nitric oxide selectively inhibits adenylyl cyclase isoforms 5 and 6. Cell Signal, 12, 233-237.
34. HNASKO, R. & LISANTI, M.P. (2003). The biology of caveolae: lessons from caveolin knockout mice and implications for human disease. Mol. Interventions, 3, 445-464.
35. HOOPER, N.M. (1999). Detergent-insoluble glycosphingolipid/cholesterol- rich membrane domains, lipid rafts and caveolae (review). Mol. Membr. Biol., 16, 145-156.
36. INSEL, P.A. (2003). Location, location, location. Trends Endocrinol. Metab., 14, 100-102.
37. KAWASAKI, H., SPRINGETT, G.M., MOCHIZUKI, N., TOKI, S., NAKAYA, M., MATSUDA, M., HOUSMAN, D.E. & GRAYBIEL, A.M. (1998). A family of cAMP-binding proteins that directly activate Rap1. Science, 282, 2275-2279.
38. KENAKIN, T. (2001). Inverse, protean, and ligand-selective agonism: matters of receptor conformation. FASEB J., 15, 598-611.
39. KENAKIN, T. (2003). Ligand-selective receptor conformations revisited: the promise and the problem. Trends Pharmacol. Sci., 24, 346-354.
40. KOHOUT, T.A. & LEFKOWITZ, R.J. (2003). Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization. Mol. Pharmacol., 63, 9-18.
41. KOPPERUD, R., KRAKSTAD, C., SELHEIM, F. & DOSKELAND, S.O. (2003). cAMP effector mechanisms. Novel twists for an 'old' signaling system. FEBS Lett., 546, 121-126.
42. KRUPNICK, J.G. & BENOVIC, J.L. (1998). The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu. Rev. Pharmacol. Toxicol., 38, 289-319.
43. LAHTINEN, U., HONSHO, M., PARTON, R.G., SIMONS, K. & VERKADE, P. (2003). Involvement of caveolin-2 in caveolar biogenesis in MDCK cells. FEBS Lett., 538, 85-88.
44. LEFKOWITZ, R.J. (1998). G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. J. Biol. Chem., 273, 18677-18680.
45. LEVITZKI, A. & BAR-SINAI, A. (1991). The regulation of adenylyl cyclase by receptor-operated G proteins. Pharmacol. Ther., 50, 271-283.
46. LLOYD, P.G. & HARDIN, C.D. (2001). Caveolae and the organization of carbohydrate metabolism in vascular smooth muscle. J. Cell. Biochem., 82, 399-408.
47. LOCKWICH, T.P., LIU, X., SINGH, B.B., JADLOWIEC, J., WEILAND, S. & AMBUDKAR, I.S. (2000). Assembly of Trp1 in a signaling complex associated with caveolin-scaffolding lipid raft domains. J. Biol. Chem., 275, 11934-11942.
48. LOHN, M., FURSTENAU, M., SAGACH, V., ELGER, M., SCHULZE, W., LUFT, F.C., HALLER, H. & GOLLASCH, M. (2000). Ignition of calcium sparks in arterial and cardiac muscle through caveolae. Circ. Res., 87, 1034-1039.
49. LUDWIG, M.G. & SEUWEN, K. (2002). Characterization of the human adenylyl cyclase gene family: cDNA, gene structure, and tissue distribution of the nine isoforms. J. Recept. Signal Transduct. Res., 22, 79-110.
50. LUTTRELL, L.M. & LEFKOWITZ, R.J. (2002). The role of beta-arrestins in the termination and transduction of G-protein-coupled receptor signals. J. Cell. Sci., 115, 455-465.
51. MARTENS, J.R., O'CONNELL, K. & TAMKUN, M. (2004). Targeting of ion channels to membrane microdomains: localization of KV channels to lipid rafts. Trends Pharmacol. Sci., 25, 16-21.
52. MARTENS, J.R., SAKAMOTO, N., SULLIVAN, S.A., GROBASKI, T.D. & TAMKUN, M.M. (2000). Isoform-specific localization of voltage-gated K+ channels to distinct lipid raft populations: targeting of Kv1.5 to caveolae. J. Biol. Chem., 13, 13.
53. MCVEY, M., HILL, J., HOWLETT, A. & KLEIN, C. (1999). Adenylyl cyclase, a coincidence detector for nitric oxide. J. Biol. Chem., 274, 18887-18892.
54. MICHEL, J.J. & SCOTT, J.D. (2002). AKAP mediated signal transduction. Annu. Rev. Pharmacol. Toxicol., 42, 235-257.
55. MILLIGAN, G. (1996). The stoichiometry of expression of protein components of the stimulatory adenylyl cyclase cascade and the regulation of information transfer. Cell Signal, 8, 87-95.
56. MILLIGAN, G., GRASSIE, M.A., WISE, A., MACEWAN, D.J., MAGEE, A.I. & PARENTI, M. (1995). G-protein palmitoylation: regulation and functional significance. Biochem. Soc. Trans., 23, 583-587.
57. MUMBY, S.M. (1997). Reversible palmitoylation of signaling proteins. Curr. Opin. Cell Biol., 9, 148-154.
58. NAIR, K.S., BALASUBRAMANIAN, N. & SLEPAK, V.Z. (2002). Signal-dependent translocation of transducin, RGS9-1-Gbeta5L complex, and arrestin to detergent-resistant membrane rafts in photoreceptors. Curr. Biol., 12, 421-425.
59. OH, P. & SCHNITZER, J.E. (1999). Immunoisolation of caveolae with high affinity antibody binding to the oligomeric caveolin cage. Toward understanding the basis of purification. J. Biol. Chem., 274, 23144-23154.
60. OH, P. & SCHNITZER, J.E. (2001). Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas g(i) and g(s) target lipid rafts by default. Mol. Biol. Cell, 12, 685-698.
61. OKA, N., YAMAMOTO, M., SCHWENCKE, C., KAWABE, J., EBINA, T., OHNO, S., COUET, J., LISANTI, M.P. & 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.
62. OKAMOTO, T., SCHLEGEL, A., SCHERER, P.E. & 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.
63. ORLANDI, P.A. & FISHMAN, P.H. (1998). Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol., 141, 905-915.
64. OSTROM, R.S., BUNDEY, R.A. & INSEL, P.A. (2004). Nitric oxide inhibition of adenylyl cyclase type 6 activity is dependent upon lipid rafts and caveolin signaling complexes. J. Biol. Chem, 279, 19846-19853.
65. OSTROM, R.S., GREGORIAN, C., DRENAN, R.M., XIANG, Y., REGAN, J.W. & INSEL, P.A. (2001). Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J. Biol. Chem., 276, 42063-42069.
66. OSTROM, R.S., LIU, X., HEAD, B.P., GREGORIAN, C., SEASHOLTZ, T.M. & INSEL, P.A. (2002). Localization of adenylyl cyclase isoforms and G protein-coupled receptors in vascular smooth muscle cells: expression in caveolin-rich and noncaveolin domains. Mol. Pharmacol., 62, 983-992.
67. OSTROM, R.S., NAUGLE, J.E., HASE, M., GREGORIAN, C., SWANEY, J.S., INSEL, P.A., BRUNTON, L.L. & MESZAROS, J.G. (2003). Angiotensin II enhances adenylyl cyclase signaling via Ca2+/ calmodulin. Gq-Gs cross-talk regulates collagen production in cardiac fibroblasts. J. Biol. Chem., 278, 24461-24468.
68. OSTROM, R.S., POST, S.R. & INSEL, P.A. (2000a). Stoichiometry and compartmentation in G protein-coupled receptor signaling: implications for therapeutic interventions involving Gs. J. Pharmacol. Exp. Ther., 294, 407-412.
69. OSTROM, R.S., VIOLIN, J.D., COLEMAN, S. & INSEL, P.A. (2000b). Selective enhancement of beta-adrenergic receptor signaling by overexpression of adenylyl cyclase type 6: colocalization of receptor and adenylyl cyclase in caveolae of cardiac myocytes. Mol. Pharmacol., 57, 1075-1079.
70. PAGE, E., WINTERFIELD, J., GOINGS, G., BASTAWROUS, A. & UPSHAW-EARLEY, J. (1998). Water channel proteins in rat cardiac myocyte caveolae: osmolarity-dependent reversible internalization. Am. J. Physiol., 274, H1988-H2000.
71. PAPOUCHEVA, E., DUMUIS, A., SEBBEN, M., RICHTER, D.W. & PONIMASKIN, E.G. (2004). The 5-hydroxytryptamine(1A) receptor is stably palmitoylated, and acylation is critical for communication of receptor with Gi-protein. J. Biol. Chem., 279, 3280-3291.
72. PERRY, S.J., BAILLIE, G.S., KOHOUT, T.A., MCPHEE, I., MAGIERA, M.M., ANG, K.L., MILLER, W.E., MCLEAN, A.J., CONTI, M., HOUSLAY, M.D. & LEFKOWITZ, R.J. (2002). Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by beta-arrestins. Science, 298, 834-836.
73. PIERCE, K.L., LUTTRELL, L.M. & LEFKOWITZ, R.J. (2001). New mechanisms in heptahelical receptor signaling to mitogen activated protein kinase cascades. Oncogene, 20, 1532-1539.
74. PIKE, L.J. (2003). Lipid rafts: bringing order to chaos. J. Lipid Res., 44, 655-667.
75. POST, S.R., HILAL-DANDAN, R., URASAWA, K., BRUNTON, L.L. & INSEL, P.A. (1995). Quantification of signalling components and amplification in the beta-adrenergic-receptor-adenylate cyclase pathway in isolated adult rat ventricular myocytes. Biochem. J., 311, 75-80.
76. RAPACCIUOLO, A., SUVARNA, S., BARKI-HARRINGTON, L., LUTTRELL, L.M., CONG, M., LEFKOWITZ, R.J. & ROCKMAN, H.A. (2003). Protein kinase A and G protein-coupled receptor kinase phosphorylation mediates beta-1 adrenergic receptor endocytosis through different pathways. J. Biol. Chem., 278, 35403-35411.
77. 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. & LISANTI, M.P. (2002a). Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J. Biol. Chem., 277, 8635-8647.
78. RAZANI, B. & LISANTI, M.P. (2001). Caveolin-deficient mice: insights into caveolar function human disease. J. Clin. Invest., 108, 1553-1561.
79. RAZANI, B., RUBIN, C.S. & LISANTI, M.P. (1999). Regulation of cAMP-mediated signal transduction via interaction of caveolins with the catalytic subunit of protein kinase A. J. Biol. Chem., 274, 26353-26360.
80. RAZANI, B., WANG, X.B., ENGELMAN, J.A., BATTISTA, M., LAGAUD, G., ZHANG, X.L., KNEITZ, B., HOU JR, H., CHRIST, G.J., EDELMANN, W. & LISANTI, M.P. (2002b). Caveolin-2-deficient mice show evidence of severe pulmonary dysfunction without disruption of caveolae. Mol. Cell. Biol., 22, 2329-2344.
81. RAZANI, B., WOODMAN, S.E. & LISANTI, M.P. (2002c). Caveolae: from cell biology to animal physiology. Pharmacol. Rev., 54, 431-467.
82. ROSS, E.M. & WILKIE, T.M. (2000). GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu. Rev. Biochem., 69, 795-827.
83. RYBIN, V.O., GRABHAM, P.W., ELOUARDIGHI, H. & STEINBERG, S.F. (2003). Caveolae-associated proteins in cardiomyocytes: caveolin-2 expression and interactions with caveolin-3. Am. J. Physiol. Heart Circ. Physiol., 285, H325-H332.
84. RYBIN, V.O., XU, X., LISANTI, M.P. & STEINBERG, S.F. (2000). Differential targeting of beta-adrenergic receptor subtypes and adenylyl cyclase to cardiomyocyte caveolae. A mechanism to functionally regulate the cAMP signaling pathway. J. Biol. Chem., 275, 41447-41457.
85. RYBIN, V.O., XU, X. & STEINBERG, S.F. (1999). Activated protein kinase C isoforms target to cardiomyocyte caveolae: stimulation of local protein phosphorylation. Circ. Res., 84, 980-988.
86. SCHERER, P.E., LEWIS, R.Y., VOLONTÉ, D., ENGELMAN, J.A., GALBIATI, F., COUET, J., KOHTZ, D.S., VAN DONSELAAR, E., PETERS, P. & LISANTI, M.P. (1997). Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in vivo. J. Biol. Chem., 272, 29337-29346.
87. SCHERER, P.E., OKAMOTO, T., CHUN, M., NISHIMOTO, I., LODISH, H.F. & LISANTI, M.P. (1996). Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Proc. Natl. Acad. Sci. U.S.A., 93, 131-135.
88. SCHNITZER, J.E. & OH, P. (1996). Aquaporin-1 in plasma membrane and caveolae provides mercury-sensitive water channels across lung endothelium. Am. J. Physiol., 270, H416-H422.
89. SCHNITZER, J.E., OH, P., PINNEY, E. & ALLARD, J. (1994). Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J. Cell. Biol., 127, 1217-1232.
90. SCHUBERT, W., FRANK, P.G., WOODMAN, S.E., HYOGO, H., COHEN, D.E., CHOW, C.W. & LISANTI, M.P. (2002). Microvascular hyper-permeability in caveolin-1 (-/-) knock-out mice: treatment with a specific NOS inhibitor, L-NAME, restores normal microvascular permeability in Cav-1 null mice. J. Biol. Chem., 277, 40091-40098.
91. SCHWENCKE, C., OKUMURA, S., YAMAMOTO, M., GENG, Y.J. & ISHIKAWA, Y. (1999a). Colocalization of beta-adrenergic receptors and caveolin within the plasma membrane. J. Cell. Biochem., 75, 64-72.
92. SCHWENCKE, C., YAMAMOTO, M., OKUMURA, S., TOYA, Y., KIM, S.J. & ISHIKAWA, Y. (1999b). Compartmentation of cyclic adenosine 3′,5′- monophosphate signaling in caveolae. Mol. Endocrinol., 13, 1061-1070.
93. SHAUL, P.W., SMART, E.J., ROBINSON, L.J., GERMAN, Z., YUHANNA, I.S., YING, Y., ANDERSON, R.G, & MICHEL, T. (1996). Acylation targets endothelial nitric-oxide synthase to plasmalemmal caveolae. J. Biol. Chem., 271, 6518-6522.
94. SMART, E.J., YING, Y.S., MINEO, C. & ANDERSON, R.G. (1995). A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc. Natl. Acad. Sci. U.S.A., 92, 10104-10108.
95. SMITH, K.E., GU, C., FAGAN, K.A., HU, B. & COOPER, D.M. (2002). Residence of adenylyl cyclase type 8 in caveolae is necessary but not sufficient for regulation by capacitative Ca2+ entry. J. Biol. Chem., 277, 6025-6031.
96. SONG, K.S., SARGIACOMO, M., GALBIATI, F., PARENTI, M. & LISANTI, M.P. (1997). Targeting of a G alpha subunit (Gi1 alpha) and c-Src tyrosine kinase to caveolae membranes: clarifying the role of N-myristoylation. Cell Mol. Biol. (Noisy-le-grand), 43, 293-303.
97. SONG, K.S., SCHERER, P.E., TANG, Z., OKAMOTO, T., LI, S., CHAFEL, M., CHU, C., KOHTZ, D.S. & LISANTI, M.P. (1996a). Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and cofractionates with dystrophin and dystrophin-associated glycoproteins. J. Biol. Chem., 271, 15160-15165.
98. SONG, S.K., LI, S., OKAMOTO, T., QUILLIAM, L.A., SARGIACOMO, M. & LISANTI, M.P. (1996b). Co-purification 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.
99. SOWA, G., PYPAERT, M. & SESSA, W.C. (2001). Distinction between signaling mechanisms in lipid rafts vs caveolae. Proc. Natl. Acad. Sci. U.S.A., 98, 14072-14077.
100. STEINBERG, S.F. & BRUNTON, L.L. (2001). Compartmentation of g protein-coupled signaling pathways in cardiac myocytes. Annu. Rev. Pharmacol. Toxicol., 41, 751-773.
101. TANG, C.M. & INSEL, P.A. (2004). GPCR expression in the heart; 'new' receptors in myocytes and fibroblasts. Trends Cardiovasc. Med., 14, 94-99.
102. TANG, Z., SCHERER, P.E., OKAMOTO, T., SONG, K., CHU, C., KOHTZ, D.S., NISHIMOTO, I., LODISH, H.F. & LISANTI, M.P. (1996). Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. J. Biol. Chem., 271, 2255-2261.
103. TASKEN, K. & AANDAHL, E.M. (2004). Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol. Rev., 84, 137-167.
104. TORIHASHI, S., FUJIMOTO, T., TROST, C. & NAKAYAMA, S. (2002). Calcium oscillation linked to pacemaking of interstitial cells of Cajal: requirement of calcium influx and localization of TRP4 in caveolae. J. Biol. Chem., 277, 19191-19197.
105. TOYA, Y., SCHWENCKE, C., COUET, J., LISANTI, M.P. & ISHIKAWA, Y. (1998). Inhibition of adenylyl cyclase by caveolin peptides. Endocrine, 139, 2025-2031.
106. VALLEJO, J. & HARDIN, C.D. (2004). Metabolic organization in vascular smooth muscle: distribution and localization of caveolin-1 and phosphofructokinase. Am. J. Physiol. Cell. Physiol., 286, C43-C54.
107. VASSILATIS, D.K., HOHMANN, J.G., ZENG, H., LI, F., RANCHALIS, J.E., MORTRUD, M.T., BROWN, A., RODRIGUEZ, S.S., WELLER, J.R., WRIGHT, A.C., BERGMANN, J.E. & GAITANARIS, G.A. (2003). The G protein-coupled receptor repertoires of human and mouse. Proc. Natl. Acad. Sci. U.S.A., 100, 4903-4908.
108. VON ZASTROW, M. (2003). Mechanisms regulating membrane trafficking of G protein-coupled receptors in the endocytic pathway. Life Sci., 74, 217-224.
109. WILLIAMS, T.M. & LISANTI, M.P. (2004). The caveolin proteins. Genome Biol., 5, 214.
110. WONG, W. & SCHLICHTER, L.C. (2004). Differential recruitment of Kv1.4 and Kv4.2 to lipid rafts by PSD-95. J. Biol. Chem., 279, 444-452.
111. WOODMAN, S.E., PARK, D.S., COHEN, A.W., CHEUNG, M., CHANDRA, M., SHIRANI, J., TANG, B., JELICKS, L.A., KITSIS, R.N., CHRIST, G.J., FACTOR, S.M., TANOWITZ, H.B. & LISANTI, M.P. (2002). Caveolin-3 knock-out mice develop a progressive cardiomyopathy and show hyperactivation of the p42/44 MAP kinase cascade. J. Biol. Chem, 277, 38988-38997.
112. XIANG, Y., DEVIC, E. & KOBILKA, B. (2002a). The PDZ binding motif of the beta1 adrenergic receptor modulates receptor trafficking and signaling in cardiac myocytes. J. Biol. Chem., 277, 33783-33790.
113. XIANG, Y. & KOBILKA, B. (2003). The PDZ-binding motif of the beta2-adrenoceptor is essential for physiologic signaling and trafficking in cardiac myocytes. Proc. Natl. Acad. Sci. U.S.A., 100, 10776-10781.
114. XIANG, Y., RYBIN, V.O., STEINBERG, S.S. & KOBILKA, B. (2002b). Caveolar localization dictates physiologic signaling of beta2 adrenoceptors in neonatal cardiac myocytes. J. Biol. Chem., 277, 34280-34286.
115. XIAO, R.P., AVDONIN, P., ZHOU, Y.Y., CHENG, H., AKHTER, S.A., ESCHENHAGEN, T., LEFKOWITZ, R.J., KOCH, W.J. & LAKATTA, E.G. (1999). Coupling of beta2-adrenoceptor to Gi proteins and its physiological relevance in murine cardiac myocytes. Circ. Res., 84, 43-52.
116. XIAO, R.P., HOHL, C., ALTSCHULD, R., JONES, L., LIVINGSTON, B., ZIMAN, B., TANTINI, B. & LAKATTA, E.G. (1994). Beta 2-adrenergic receptor-stimulated increase in cAMP in rat heart cells is not coupled to changes in Ca2+ dynamics, contractility, or phospholamban phosphorylation. J. Biol. Chem., 269, 19151-19156.
117. YAMABHAI, M. & ANDERSON, R.G. (2002). Second cysteine-rich region of epidermal growth factor receptor contains targeting information for caveolae/rafts. J. Biol. Chem., 277, 24843-24846.
118. YARBROUGH, T.L., LU, T., LEE, H.C. & SHIBATA, E.F. (2002). Localization of cardiac sodium channels in caveolin-rich membrane domains: regulation of sodium current amplitude. Circ. Res., 90, 443-449.
119. YATANI, A., TAJIMA, Y. & GREEN, S.A. (1999). Coupling of beta-adrenergic receptors to cardiac L-type Ca2+ channels: preferential coupling of the beta1 versus beta2 receptor subtype and evidence for PKA-independent activation of the channel. Cell Signal, 11, 337-342.
120. ZACCOLO, M. & POZZAN, T. (2002). Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science, 295, 1711-1715.
121. ZACHARIAS, D.A., VIOLIN, J.D., NEWTON, A.C. & TSIEN, R.Y. (2002). Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science, 296, 913-916.
122. ZHENG, B., DE VRIES, L. & GIST FARQUHAR, M. (1999). Divergence of RGS proteins: evidence for the existence of six mammalian RGS subfamilies. Trends Biochem. Sci., 24, 411-414.
123. ZHENG, B., MA, Y.C., OSTROM, R.S., LAVOIE, C., GILL, G.N., INSEL, P.A., HUANG, X.Y. & FARQUHAR, M.G. (2001). RGS-PX1, a GAP for Galpha s and sorting Nexin in vesicular trafficking. Science, 294, 1939-1942.
124. ZHONG, H., WADE, S.M., WOOLF, P.J., LINDERMAN, J.J., TRAYNOR, J.R. & NEUBIG, R.R. (2003). A spatial focusing model for G protein signals. Regulator of G protein signaling (RGS) protein-mediated kinetic scaffolding. J. Biol. Chem., 278, 7278-7284.