Caveolin-1 and lipid microdomains regulate Gs trafficking and attenuate Gs/adenylyl cyclase signaling

Molecular Pharmacology

Volumn 76, Issue 5, 2009, Pages 1082-1093

  Allen, John A ^a,c   Yu, Jiang Z ^a   Dave, Rahul H ^a   Bhatnagar, Anushree ^b   Roth, Bryan L ^c   Rasenick, Mark M ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ALUMINUM TETRAFLUORIDE; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CAVEOLIN 1; CAVEOLIN 2; CHOLESTEROL; CYCLIC AMP; FLUORIDE; FORSKOLIN; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; ISOPRENALINE; LIPID; METHYL BETA CYCLODEXTRIN; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN; THYROTROPIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN MEMBRANE; CAVEOLA; CELL MEMBRANE; CHELATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GLIOMA CELL; IMAGING; INTERNALIZATION; LIPID RAFT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STIMULATION;

ADENYLATE CYCLASE; ANIMALS; CAVEOLIN 1; CELL LINE, TUMOR; GENE KNOCKDOWN TECHNIQUES; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; MALE; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 70350449242     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.109.060160     Document Type: Article

References (53)

1. Allen JA, Halverson-Tamboli RA, and Rasenick MM (2007) Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci 8:128-140.
2. s internalization through lipid rafts: a study in living cells. Mol Pharmacol 67:1493-1504.
3. q-coupled protein receptors. J Biol Chem 279:34614-34623.
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
5. Brown DA (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 21:430-439.
6. Cohen AW, Hnasko R, Schubert W, and Lisanti MP (2004) Role of caveolae and caveolins in health and disease. Physiol Rev 84:1341-1379. (Pubitemid 39287953)
7. Daaka Y, Luttrell LM, and Lefkowitz RJ (1997) Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A. Nature 390:88-91. (Pubitemid 27494762)
8. Debernardi MA, Munshi R, Yoshimura M, Cooper DM, and Brooker G (1993) Predominant expression of type-VI adenylate cyclase in C6-2B rat glioma cells may account for inhibition of cyclic AMP accumulation by calcium. Biochem J 293:325-328. (Pubitemid 23233907)
9. s alpha localization in lipid raft domains where it is less likely to activate adenylyl cyclase. J Neurosci 28:3042-3050.
10. Donati RJ and Rasenick MM (2005) Chronic antidepressant treatment prevents accumulation of gsalpha in cholesterol-rich, cytoskeletal-associated, plasma membrane domains (lipid rafts). Neuropsychopharmacology 30:1238-1245.
11. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, et al. (2001) Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293:2449-2452. (Pubitemid 32917325)
12. Evanko DS, Thiyagarajan MM, Siderovski DP, and Wedegaertner PB (2001) Gbeta gamma isoforms selectively rescue plasma membrane localization and palmitoylation of mutant Galphas and Galphaq. J Biol Chem 276:23945-23953.
13. 2+ entry requires localization in cholesterol- rich domains. J Biol Chem 275:26530-26537.
14. Fra AM, Williamson E, Simons K, and Parton RG (1995) De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci U S A 92:8655-8659.
15. Francesconi A, Kumari R, and Zukin RS (2009) Regulation of group I metabotropic glutamate receptor trafficking and signaling by the caveolar/lipid raft pathway. J Neurosci 29:3590-3602.
16. Frank PG, Cheung MW, Pavlides S, Llaverias G, Park DS, and Lisanti MP (2006) Caveolin-1 and regulation of cellular cholesterol homeostasis. Am J Physiol Heart Circ Physiol 291:H677-H686. (Pubitemid 44175073)
17. Hanson MA, Cherezov V, Griffith MT, Roth CB, Jaakola VP, Chien EY, Velasquez J, Kuhn P, and Stevens RC (2008) A specific cholesterol binding site is established by the 2.8 A structure of the human beta2-adrenergic receptor. Structure 16:897-905. (Pubitemid 351778384)
18. Head BP, Patel HH, Roth DM, Lai NC, Niesman IR, Farquhar MG, and Insel PA (2005) G-protein-coupled receptor signaling components localize in both sarcolemmal and intracellular caveolin-3-associated microdomains in adult cardiac myocytes. J Biol Chem 280:31036-31044.
19. Head BP, Patel HH, Roth DM, Murray F, Swaney JS, Niesman IR, Farquhar MG, and Insel PA (2006) Microtubules and actin microfilaments regulate lipid raft/ caveolae localization of adenylyl cyclase signaling components. J Biol Chem 281: 26391-26399. (Pubitemid 44401847)
20. Hines LM, Tabakoff B, and WHO/ISBRA Study on State and Trait Markers of Alcohol Use and Dependence Investigators (2005) Platelet adenylyl cyclase activity: a biological marker for major depression and recent drug use. Biol Psychiatry 58:955-962.
21. s and the beta2-adrenergic receptor demonstrates that both alphas and beta1gamma7 internalize upon stimulation and exhibit similar trafficking patterns that differ from that of the beta2-adrenergic receptor. J Biol Chem 279: 44101-44112.
22. Insel PA and Ostrom RS (2003) Forskolin as a tool for examining adenylyl cyclase expression, regulation, and G protein signaling. Cell Mol Neurobiol 23:305-314.
23. Layden BT, Saengsawang W, Donati RJ, Yang S, Mulhearn DC, Johnson ME, and Rasenick MM (2008) Structural model of a complex between the heterotrimeric G protein, Gsalpha, and tubulin. Biochim Biophys Acta 1783:964-973.
24. Le Roy C and Wrana JL (2005) Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 6:112-126. (Pubitemid 40215807)
25. s in intact cells alters its abundance, rate of degradation, and membrane avidity. J Cell Biol 119:1297-1307.
26. Marrari Y, Crouthamel M, Irannejad R, and Wedegaertner PB (2007) Assembly and trafficking of heterotrimeric G proteins. Biochemistry 46:7665-7677.
27. Miura Y, Hanada K, and Jones TL (2001) G(s) signaling is intact after disruption of lipid rafts. Biochemistry 40:15418-15423. (Pubitemid 33151958)
28. Mizrachi D and Segaloff DL (2004) Intracellularly located misfolded glycoprotein hormone receptors associate with different chaperone proteins than their cognate wild-type receptors. Mol Endocrinol 18:1768-1777. (Pubitemid 38859582)
29. Murata M, Peränen J, Schreiner R, Wieland F, Kurzchalia TV, and Simons K (1995) VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci U S A 92: 10339-10343.
30. Oh P and Schnitzer JE (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. (Pubitemid 33052021)
31. Ostrom RS, Gregorian C, Drenan RM, Xiang Y, Regan JW, and Insel PA (2001) Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J Biol Chem 276:42063-42069. (Pubitemid 37371111)
32. Ostrom RS and Insel PA (2004) The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol 143:235-245.
33. s to rat synaptic membrane adenylate cyclase is enhanced subsequent to chronic antidepressant treatment. Mol Pharmacol 36:803-808.
34. Patel HH, Murray F, and Insel PA (2008) Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 48: 359-391. (Pubitemid 351738158)
35. 2- adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction. J Biol Chem 283:24659-24672.
36. Rajendran L and Simons K (2005) Lipid rafts and membrane dynamics. J Cell Sci 118:1099-1102.
37. Ransnäs LA, Svoboda P, Jasper JR, and Insel PA (1989) Stimulation of betaadrenergic receptors of S49 lymphoma cells redistributes the alpha subunit of the stimulatory G protein between cytosol and membranes. Proc Natl Acad Sci U S A 86:7900-7903. (Pubitemid 19265290)
38. Rasenick MM, Stein PJ, and Bitensky MW (1981) The regulatory subunit of adenylate cyclase interacts with cytoskeletal components. Nature 294:560-562.
39. Rasenick MM, Wheeler GL, Bitensky MW, Kosack CM, Malina RL, and Stein PJ (1984) Photoaffinity identification of colchicine-solubilized regulatory subunit from rat brain adenylate cyclase. J Neurochem 43:1447-1454. (Pubitemid 15205904)
40. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, et al. (2001) Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276: 38121-38138. (Pubitemid 37384066)
41. Rodbell M (1985) Programmable messengers: a new theory of hormone action. Trends Biochem Sci 10:461-464.
42. Rybin VO, Xu X, Lisanti MP, and Steinberg SF (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. (Pubitemid 32054981)
43. Salomon Y (1979) Adenylate cyclase assay. Adv Cyclic Nucleotide Res 10:35-55.
44. Smart EJ, Ying Y, Donzell WC, and Anderson RG (1996) A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 271:29427-29435. (Pubitemid 26382662)
45. Sutkowski EM, Tang WJ, Broome CW, Robbins JD, and Seamon KB (1994) Regulation of forskolin interactions with type I, II, V, and VI adenylyl cyclases by Gs alpha. Biochemistry 33:12852-12859. (Pubitemid 24352876)
46. s alpha from plasma membrane. J Neurochem 73:1114-1120.
47. s alpha and Gi alpha 1. J Biol Chem 265:1239-1242.
48. Watts VJ and Neve KA (1996) Sensitization of endogenous and recombinant adenylate cyclase by activation of D2 dopamine receptors. Mol Pharmacol 50:966-976.
49. s alpha. Mol Biol Cell 7:1225-1233.
50. 2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol Rev 87:965-1010.
51. Xiang Y, Rybin VO, Steinberg SF, and Kobilka B (2002) Caveolar localization dictates physiologic signaling of beta 2-adrenoceptors in neonatal cardiac myocytes. J Biol Chem 277:34280-34286. (Pubitemid 35056250)
52. s acts as an intracellular messenger to increase microtubule dynamics and promote neurite outgrowth. J Biol Chem 284:10462-10472.
53. s: dissociation of the activated G protein from plasma membrane. Mol Pharmacol 61:352-359.