Localization of the mouse 5-hydroxytryptamine1A receptor in lipid microdomains depends on its palmitoylation and is involved in receptor-mediated signaling

Molecular Pharmacology

Volumn 72, Issue 3, 2007, Pages 502-513

  Renner, Ute ^a,b   Glebov, Konstantin ^a   Lang, Thorsten ^c   Papusheva, Ekaterina ^a,b,c   Balakrishnan, Saju ^a   Keller, Bernhard ^a   Richter, Diethelm W ^a,b   Jahn, Reinhard ^c   Ponimaskin, Evgeni ^a,b,c  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b DFG Research Center for Molecular Physiology of the Brain   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; SEROTONIN 1A RECEPTOR; YELLOW FLUORESCENT PROTEIN;

ACYLATION; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CENTRIFUGATION; CONTROLLED STUDY; CYTOPLASM; EMBRYO; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; BIOTINYLATION; CALCIUM; CELL LINE, TUMOR; ENZYME ACTIVATION; FLUORESCENT DYES; GREEN FLUORESCENT PROTEINS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; LUMINESCENT PROTEINS; MEMBRANE MICRODOMAINS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUTATION; NEUROBLASTOMA; NIH 3T3 CELLS; PALMITIC ACID; PHOSPHORYLATION; RADIOLIGAND ASSAY; RECEPTOR, SEROTONIN, 5-HT1A; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 34548303255     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.107.037085     Document Type: Article

References (62)

1. Alousi AA, Jasper JR, Insel PA, and Motulsky HJ (1991) Stoichiometry of receptor-Gs-adenylate cyclase interactions. FASEB J 5:2300-2303.
2. Anderson RG (1998) The caveolae membrane system. Annu Rev Biochem 67:199-225.
3. Andrade R, Malenka RC, and Nicoll RA (1986) A G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science 234:1261-1265.
4. Arni S, Keilbaugh SA, Ostermeyer AG, and Brown DA (1998) Association of GAP-43 with detergent-resistant membranes requires two palmitoylated cysteine residues. J Biol Chem 273:28478-28485.
5. Aune TM, McGrath KM, Sarr T, Bombara MP, and Kelley KA (1993) Expression of 5HT1a receptors on activated human T cells. Regulation of cyclic AMP levels and T cell proliferation by 5-hydroxytryptamine. J Immunol 151:1175-1183.
6. Avery J, Ellis DJ, Lang T, Holroyd P, Riedel D, Henderson RM, Edwardson JM, and Jahn R (2000) A cell-free system for regulated exocytosis in PC12 cells. J Cell Biol 148:317-324.
7. Brown DA and London E (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14:111-136.
8. Burnet PW, Mefford IN, Smith CC, Gold PW and Sternberg EM (1996) Hippocampal 5-HT1A receptor binding site densities, 5-HT1A receptor messenger ribonucleic acid abundance and serotonin levels parallel the activity of the hypothalamo-pituitary-adrenal axis in rats. Behav Brain Res 73:365-368.
9. Chini B, and Parenti M (2004) G-protein coupled receptors in lipid rafts and caveolae: how, when and why do they go there? J Mol Endocrinol 32:325-338.
10. Chudakov DM, Lukyanov S, and Lukyanov KA (2005) Fluorescent proteins as a toolkit for in vivo imaging. Trends Biotechnol 23:605-613.
11. Claeysen S, Sebben M, Becamel C, Bockaert J, and Dumuis A (1999) Novel brains-pecific 5-HT4 receptor splice variants show marked constitutive activity: role of the C-terminal intracellular domain. Mol Pharmacol 55:910-920.
12. Cowen DS, Sowers RS, and Manning DR (1996) Activation of a mitogen-activated protein kinase (ERK2) by the 5-hydroxytryptamine1A receptor is sensitive not only to inhibitors of phosphatidylinositol 3-kinase, but to an inhibitor of phosphatidylcholine hydrolysis. J Biol Chem 271:22297-22300.
13. De Vivo M and Maayani S (1986) Characterization of the 5-hydroxytryptamine1a receptor-mediated inhibition of forskolin-stimulated adenylate cyclase activity in guinea pig and rat hippocampal membranes. J Pharmacol Exp Ther 238:248-253.
14. Dietzen DJ, Hastings WR, and 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.
15. Dumuis A, Sebben M, and Bockaert J (1988) Pharmacology of 5-hydroxytryptamine-1A receptors which inhibit cAMP production in hippocampal and cortical neurons in primary culture. Mol Pharmacol 33:178-186.
16. Emerit MB, el Mestikawy S, Gozlan H, Rouot B, and Hamon M (1990) Physical evidence of the coupling of solubilized 5-HT1A binding sites with G regulatory proteins. Biochem Pharmacol 39:7-18.
17. Eroglu C, Brugger B, Wieland F, and Sinning I (2003) Glutamate-binding affinity of Drosophila metabotropic glutamate receptor is modulated by association with lipid rafts. Proc Natl Acad Sci U S A 100:10219-10224.
18. Fargin A, Yamamoto K, Cotecchia S, Goldsmith PK, Spiegel AM, Lapetina EG, Caron MG, and Lefkowitz RJ (1991) Dual coupling of the cloned 5-HT1A receptor to both adenylyl cyclase and phospholipase C is mediated via the same Gi protein. Cell Signal 3:547-557.
19. Foster LJ, De Hoog CL, and Mann M (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci U S A 100:5813-5818.
20. Garnovskaya MN, van Biesen T, Hawe B, Casanas Ramos S, Lefkowitz RJ, and Raymond JR (1996) Ras-dependent activation of fibroblast mitogen-activated protein kinase by 5-HT1A receptor via a G protein beta gamma-subunit-initiated pathway. Biochemistry 35:13716-13722.
21. Gordon JA and Hen R (2004) The serotonergic system and anxiety. Neuromol Med 5:27-40.
22. Harder T, Scheiffele P, Verkade P, and Simons K (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141:929-942.
23. q-green fluorescent protein fusion in living cells. Association with the plasma membrane is disrupted by mutational activation and by elimination of palmitoylation sites, but not be activation mediated by receptors or AlF4. J Biol Chem 276:4227-4235.
24. Hur EM and Kim KT (2002) G protein-coupled receptor signalling and cross-talk: achieving rapidity and specificity. Cell Signal 14:397-405.
25. Janetopoulos C, Jin T, and Devreotes P (2001) Receptor-mediated activation of heterotrimeric G-proteins in living cells. Science 291:2408-2411.
26. Kallal L and Benovic JL (2000) Using green fluorescent proteins to study G-protein-coupled receptor localization and trafficking. Trends Pharmacol Sci 21:175-180.
27. Lang T, Bruns D, Wenzel D, Riedel D, Holroyd P, Thiele C, and Jahn R (2001) SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J 20:2202-2213.
28. Leaney JL, Benians A, Graves FM, and Tinker A (2002) A novel strategy to engineer functional fluorescent inhibitory G-protein α subunits. J Biol Chem 277:28803-28809.
29. Levis MJ and Bourne HR (1992) Activation of the alpha subunit of Gs in intact cells alters its abundance, rate of degradation, and membrane avidity. J Cell Biol 119:1297-1307.
30. Liu YF and Albert PR (1991) Cell-specific signaling of the 5-HT1A receptor. Modulation by protein kinases C and A. J Biol Chem 266:23689-23697.
31. Mañes S, Ana Lacalle R, Gomez-Mouton C, and Martinez AC (2003) From rafts to crafts: membrane asymmetry in moving cells. Trends Immunol 24:320-326.
32. Melkonian KA, Ostermeyer AG, Chen JZ, Roth MG, and Brown DA (1999) Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J Biol Chem 274:3910-3917.
33. 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.
34. Milligan G (2004) Applications of bioluminescence and fluorescence resonance energy transfer to drug discovery at G protein-coupled receptors. Eur J Pharm Sci 21:397-405.
35. Moffett S, Brown DA, and Linder ME (2000) Lipid-dependent targeting of G proteins into rafts. J Biol Chem 275:2191-2198.
36. Nebigil CG, Garnovskaya MN, Casanas SJ, Mulheron JG, Parker EM, Gettys TW, and Raymond JR (1995) Agonist-induced desensitization and phosphorylation of human 5-HT1A receptor expressed in Sf9 insect cells. Biochemistry 34:11954-11962.
37. 3H]-S 15535: definition of its binding profile using agonists, antagonists and inverse agonists. Naunyn Schmiedebergs Arch Pharmacol 357:205-217.
38. s target lipid rafts by default. Mol Biol Cell 12:685-698.
39. Okamoto T, Schlegel A, Scherer PE, and Lisanti MP (1998) Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem 273:5419-5422.
40. s. J Pharmacol Exp Ther 294:407-412.
41. Overstreet DH (2002) Behavioral characteristics of rat lines selected for differential hypothermic responses to cholinergic or serotonergic agonists. Behav Genet 32:335-348.
42. 1A receptor is stably palmitoylated, and acylation is critical for communication of receptor with Gi protein. J Biol Chem 279:3280-3291.
43. 2+ responses in Chinese hamster ovary-K1 cells demonstrate an atypical pattern of ligand-induced 5-HT1A receptor activation. J Pharmacol Exp Ther 307:608-614.
44. Pierce KL, Premont RT, and Lefkowitz RJ (2002) Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3:639-650.
45. 1A receptors from bovine hippocampus. Biochim Biophys Acta 1663:188-200.
46. Pucadyil TJ, Kalipatnapu S, Harikumar KG, Rangaraj N, Karnik SS, and Chattopadhyay A (2004) G-protein-dependent cell surface dynamics of the human serotonin1A receptor tagged to yellow fluorescent protein. Biochemistry 43:15852-15862.
47. Radley JJ and Jacobs BL (2002) 5-HT1A receptor antagonist administration decreases cell proliferation in the dentate gyrus. Brain Res 955:264-267.
48. Riad M, Watkins KC, Doucet E, Hamon M, and Descarries L(2001) Agonist-induced internalization of serotonin-1a receptors in the dorsal raphe nucleus (autoreceptors) but not hippocampus (heteroreceptors). J Neurosci 21:8378-8386.
49. Richter DW, Manzke T, Wilken B, and Ponimaskin E (2003) Serotonin receptors: guardians of stable breathing. Trends Mol Med 9:542-548.
50. Sambrook J, Fritsch E, and Maniatis T, eds (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
51. Shaul PW, Smart EJ, Robinson LJ, German Z, Yuhanna IS, Ying Y, Anderson RG, and Michel T (1996) Acylation targets endothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem 271:6518-6522.
52. Shenoy-Scaria AM, Dietzen DJ, Kwong J, Link DC, and Lublin DM (1994) Cysteine3 of Src family protein tyrosine kinase determines palmitoylation and localization in caveolae. J Cell Biol 126:353-363.
53. 1A receptors in mood disorders: a combined genetic and genomic approach. Behav Pharmacol 12:429-438.
54. Simons K and Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31-39.
55. Simons K and Vaz WL (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33:269-295.
56. Song KS, Sargiacomo M, Galbiati F, Parenti M, and Lisanti MP (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 43:293-303.
57. Spiegel S, Kassis S, Wilchek M, and Fishman PH (1984) Direct visualization of redistribution and capping of fluorescent gangliosides on lymphocytes. J Cell Biol 99:1575-1581.
58. Sprong H, van der Sluijs P, and van Meer G (2001) How proteins move lipids and lipids move proteins. Nat Rev Mol Cell Biol 2:504-513.
59. van Duyl BY, Rijkers DT, de Kruijff B, and Killian JA (2002) Influence of hydrophobic mismatch and palmitoylation on the association of transmembrane alpha-helical peptides with detergent-resistant membranes. FEBS Lett 523:79-84.
60. Wedegaertner PB, Bourne HR, and von Zastrow M (1996) Activation-induced subcellular redistribution of Gs alpha. Mol Biol Cell 7:1225-1233.
61. s: dissociation of the activated G protein from plasma membrane. Mol Pharmacol 61:352-359.
62. Zacharias DA, Violin JD, Newton AC, and Tsien RY (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296:913-916.