Homologous desensitization of signalling by the beta (β) isoform of the human thromboxane A2 receptor

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1761, Issue 9, 2006, Pages 1114-1131

  Kelley Hickie, Leanne P ^a   Kinsella, B Therese ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Arrestin; Beta; Desensitization; G protein coupled receptor; G protein coupled receptor kinase; Phospholipase C; Phosphorylation; Thromboxane receptor

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; BETA ARRESTIN; G PROTEIN COUPLED RECEPTOR KINASE; GUANINE NUCLEOTIDE BINDING PROTEIN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; INOSITOL 1,3,4 TRISPHOSPHATE; INOSITOL DERIVATIVE; PROTEIN KINASE C; RECEPTOR PROTEIN; SERINE; THROMBOXANE A2 RECEPTOR; THROMBOXANE A2 RECEPTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; INTERNALIZATION; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TARGETING; SECOND MESSENGER; SMOOTH MUSCLE CONTRACTION; THROMBOCYTE AGGREGATION; VASCULAR DISEASE;

15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; AMINO ACID SEQUENCE; ARRESTINS; CALCIUM; CELL LINE; G-PROTEIN-COUPLED RECEPTOR KINASE 3; HUMANS; INDOLES; INOSITOL 1,4,5-TRISPHOSPHATE; MALEIMIDES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, THROMBOXANE A2, PROSTAGLANDIN H2; SECOND MESSENGER SYSTEMS; SERINE; SIGNAL TRANSDUCTION;

EID: 33748450161     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2006.07.012     Document Type: Article

References (57)

1. Pierce K.L., Premont R.T., and Lefkowitz R.J. Seven-transmembrane receptors. Nat. Rev., Mol. Cell Biol. 3 9 (2002) 639-650
2. Lefkowitz R.J. G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. J. Biol. Chem. 273 30 (1998) 18677-18680
3. Shenoy S.K., and Lefkowitz R.J. Multifaceted roles of beta-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signalling. Biochem J. 375 Pt 3 (2003) 503-515
4. Penn R.B., Pronin A.N., and Benovic J.L. Regulation of G protein-coupled receptor kinases. Trends Cardiovasc. Med. 10 2 (2000) 81-89
5. Lefkowitz R.J., and Shenoy S.K. Transduction of receptor signals by beta-arrestins. Science 308 5721 (2005) 512-517
6. Shenoy S.K., and Lefkowitz R.J. Receptor regulation: beta-arrestin moves up a notch. Nat. Cell Biol. 7 12 (2005) 1059-1061
7. Shenoy S.K., Drake M.T., Nelson C.D., Houtz D.A., Xiao K., Madabushi S., Reiter E., Premont R.T., Lichtarge O., and Lefkowitz R.J. beta-arrestin-dependent, G protein-independent ERK1/2 activation by the beta2 adrenergic receptor. J. Biol. Chem. 281 2 (2006) 1261-1273
8. Narumiya S., Sugimoto Y., and Ushikubi F. Prostanoid receptors: structures, properties, and functions. Physiol. Rev. 79 4 (1999) 1193-1226
9. Oates J.A., FitzGerald G.A., Branch R.A., Jackson E.K., Knapp H.R., and Roberts II L.J. Clinical implications of prostaglandin and thromboxane A2 formation (1). N. Engl. J. Med. 319 11 (1988) 689-698
10. Fitzgerald D.J., Rocki W., Murray R., Mayo G., and FitzGerald G.A. Thromboxane A2 synthesis in pregnancy-induced hypertension. Lancet 335 8692 (1990) 751-754
11. Kinsella B.T. Thromboxane A2 signalling in humans: a 'Tail' of two receptors. Biochem. Soc. Trans. 29 Pt 6 (2001) 641-654
12. Hirata M., Hayashi Y., Ushikubi F., Yokota Y., Kageyama R., Nakanishi S., and Narumiya S. Cloning and expression of cDNA for a human thromboxane A2 receptor. Nature 349 6310 (1991) 617-620
13. Raychowdhury M.K., Yukawa M., Collins L.J., McGrail S.H., Kent K.C., and Ware J.A. Alternative splicing produces a divergent cytoplasmic tail in the human endothelial thromboxane A2 receptor. J. Biol. Chem. 269 30 (1994) 19256-19261
14. Raychowdhury M.K., Yukawa M., Collins L.J., McGrail S.H., Kent K.C., and Ware J.A. Alternative splicing produces a divergent cytoplasmic tail in the human endothelial thromboxane A2 receptor. J. Biol. Chem. 270 12 (1995) 7011 Published erratum.
15. Habib A., Vezza R., Creminon C., Maclouf J., and FitzGerald G.A. Rapid, agonist-dependent phosphorylation in vivo of human thromboxane receptor isoforms. Minimal involvement of protein kinase C. J. Biol. Chem. 272 11 (1997) 7191-7200
16. Walsh M.T., Foley J.F., and Kinsella B.T. Characterization of the role of N-linked glycosylation on the cell signaling and expression of the human thromboxane A2 receptor alpha and beta isoforms. J. Pharmacol. Exp. Ther. 286 2 (1998) 1026-1036
17. Walsh M., Foley J.F., and Kinsella B.T. Investigation of the role of the carboxyl-terminal tails of the alpha and beta isoforms of the human thromboxane A(2) receptor (TP) in mediating receptor:effector coupling. Biochim Biophys Acta 1496 2-3 (2000) 164-182
18. Hirata T., Ushikubi F., Kakizuka A., Okuma M., and Narumiya S. Two thromboxane A2 receptor isoforms in human platelets. Opposite coupling to adenylyl cyclase with different sensitivity to Arg60 to Leu mutation. J. Clin. Invest. 97 4 (1996) 949-956
19. Vezza R., Habib A., and FitzGerald G.A. Differential signaling by the thromboxane receptor isoforms via the novel GTP-binding protein, Gh. J. Biol. Chem. 274 18 (1999) 12774-12779
20. Miggin S.M., and Kinsella B.T. Expression and tissue distribution of the mRNAs encoding the human thromboxane A2 receptor (TP) alpha and beta isoforms. Biochim. Biophys. Acta 1425 3 (1998) 543-559
21. Miggin S.M., and Kinsella B.T. Thromboxane A(2) receptor mediated activation of the mitogen activated protein kinase cascades in human uterine smooth muscle cells. Biochim. Biophys. Acta 1539 1-2 (2001) 147-162
22. Habib A., FitzGerald G.A., and Maclouf J. Phosphorylation of the thromboxane receptor alpha, the predominant isoform expressed in human platelets. J. Biol. Chem. 274 5 (1999) 2645-2651
23. Coyle A.T., Miggin S.M., and Kinsella B.T. Characterization of the 5′ untranslated region of alpha and beta isoforms of the human thromboxane A2 receptor (TP). Differential promoter utilization by the TP isoforms. Eur. J. Biochem. 269 16 (2002) 4058-4073
24. Coyle A.T., and Kinsella B.T. Characterization of promoter 3 of the human thromboxane A receptor gene. A functional AP-1 and octamer motif are required for basal promoter activity. FEBS J. 272 4 (2005) 1036-1053
25. Coyle A.T., O'Keeffe M.B., and Kinsella B.T. 15-Deoxy Delta-prostaglandin J suppresses transcription by promoter 3 of the human thromboxane A receptor gene through peroxisome proliferator-activated receptor gamma in human erythroleukemia cells. FEBS J. 272 18 (2005) 4754-4773
26. Coyle A.T., and Kinsella B.T. Synthetic peroxisome proliferator-activated receptor gamma agonists rosiglitazone and troglitazone suppress transcription by promoter 3 of the human thromboxane A(2) receptor gene in human erythroleukemia cells. Biochem. Pharmacol. 71 9 (2006) 1308-1323
27. Walsh M.T., Foley J.F., and Kinsella B.T. The alpha, but not the beta, isoform of the human thromboxane A2 receptor is a target for prostacyclin-mediated desensitization. J. Biol. Chem. 275 27 (2000) 20412-20423
28. Foley J.F., Kelley L.P., and Kinsella B.T. Prostaglandin D(2) receptor-mediated desensitization of the alpha isoform of the human thromboxane A(2) receptor. Biochem. Pharmacol. 62 2 (2001) 229-239
29. Reid H.M., and Kinsella B.T. The alpha, but not the beta, isoform of the human thromboxane A2 receptor is a target for nitric oxide-mediated desensitization. Independent modulation of Tp alpha signaling by nitric oxide and prostacyclin. J. Biol. Chem. 278 51 (2003) 51190-51202
30. Parent J.L., Labrecque P., Orsini M.J., and Benovic J.L. Internalization of the TXA2 receptor alpha and beta isoforms. Role of the differentially spliced cooh terminus in agonist-promoted receptor internalization. J. Biol. Chem. 274 13 (1999) 8941-8948
31. Parent J.L., Labrecque P., Driss Rochdi M., and Benovic J.L. Role of the differentially spliced carboxyl terminus in thromboxane A2 receptor trafficking: identification of a distinct motif for tonic internalization. J. Biol. Chem. 276 10 (2001) 7079-7085
32. Laroche G., Rochdi M.D., Laporte S.A., and Parent J.L. Involvement of actin in agonist-induced endocytosis of the G protein-coupled receptor for thromboxane A2: overcoming of actin disruption by arrestin-3 but not arrestin-2. J. Biol. Chem. 280 24 (2005) 23215-23224
33. Hamelin E., Theriault C., Laroche G., and Parent J.L. The intracellular trafficking of the G protein-coupled receptor TPbeta depends on a direct interaction with Rab11. J. Biol. Chem. 280 43 (2005) 36195-36205
34. Kinsella B.T., O'Mahony D.J., and Fitzgerald G.A. The human thromboxane A2 receptor alpha isoform (TP alpha) functionally couples to the G proteins Gq and G11 in vivo and is activated by the isoprostane 8-epi prostaglandin F2 alpha. J. Pharmacol. Exp. Ther. 281 2 (1997) 957-964
35. Kelley-Hickie L.P., and Kinsella B.T. EP1-and FP-mediated cross-desensitization of the alpha (alpha) and beta (beta) isoforms of the human thromboxane A2 receptor. Br. J. Pharmacol. 142 1 (2004) 203-221
36. Koch W.J., Hawes B.E., Inglese J., Luttrell L.M., and Lefkowitz R.J. Cellular expression of the carboxyl terminus of a G protein-coupled receptor kinase attenuates G beta gamma-mediated signaling. J. Biol. Chem. 269 8 (1994) 6193-6197
37. Gorman C.M., Gies D., and McCray G. Transient production of proteins using an adenovirus transformed cell line. DNA Protein Eng. Tech. 2 (1990) 3-10
38. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
39. Grynkiewicz G., Poenic M., and Tsien R. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260 (1985) 3440-3450
40. Godfrey P. Inositol lipids and phosphates. In: Milligan G. (Ed). Signal Transduction: A practical approach (1992), Irl Press, Oxford 105-122
41. Freedman N.J., Ament A.S., Oppermann M., Stoffel R.H., Exum S.T., and Lefkowitz R.J. Phosphorylation and desensitization of human endothelin A and B receptors. Evidence for G protein-coupled receptor kinase specificity. J. Biol. Chem. 272 28 (1997) 17734-17743
42. Miggin S.M., Lawler O.A., and Kinsella B.T. Investigation of a functional requirement for isoprenylation by the human prostacyclin receptor. Eur. J. Biochem. 269 6 (2002) 1714-1725
43. Blom N., Kreegipuu A., and Brunak S. PhosphoBase: a database of phosphorylation sites. Nucleic Acids Res. 26 1 (1998) 382-386
44. Onorato J.J., Palczewski K., Regan J.W., Caron M.G., Lefkowitz R.J., and Benovic J.L. Role of acidic amino acids in peptide substrates of the beta-adrenergic receptor kinase and rhodopsin kinase. Biochemistry 30 21 (1991) 5118-5125
45. Wang Q., Zhao J., Brady A.E., Feng J., Allen P.B., Lefkowitz R.J., Greengard P., and Limbird L.E. Spinophilin blocks arrestin actions in vitro and in vivo at G protein-coupled receptors. Science 304 5679 (2004) 1940-1944
46. Theriault C., Rochdi M.D., and Parent J.L. Role of the Rab11-associated intracellular pool of receptors formed by constitutive endocytosis of the beta isoform of the thromboxane A2 receptor (TP beta). Biochemistry 43 19 (2004) 5600-5607
47. Sugimoto Y. [Physiological functions of prostanoid receptors and their subtypes]. Nippon Yakurigaku Zasshi 115 3 (2000) 131-141
48. Narumiya S., and FitzGerald G.A. Genetic and pharmacological analysis of prostanoid receptor function. J. Clin. Invest. 108 1 (2001) 25-30
49. Spurney R.F., and Coffman T.M. The C-terminus of the thromboxane receptor contributes to coupling and desensitization in a mouse mesangial cell line. J. Pharmacol. Exp. Ther. 283 1 (1997) 207-215
50. Spurney R.F. Effect of receptor number on desensitization of the mouse thromboxane receptor. Biochem. Pharmacol. 55 8 (1998) 1271-1281
51. Spurney R.F. Role of C-terminal serines in desensitization and phosphorylation of the mouse thromboxane receptor. J. Biol. Chem. 273 43 (1998) 28496-28503
52. Rockman H.A., Choi D.J., Akhter S.A., Jaber M., Giros B., Lefkowitz R.J., Caron M.G., and Koch W.J. Control of myocardial contractile function by the level of beta-adrenergic receptor kinase 1 in gene-targeted mice. J. Biol. Chem. 273 29 (1998) 18180-18184
53. Koch W.J., Rockman H.A., Samama P., Hamilton R.A., Bond R.A., Milano C.A., and Lefkowitz R.J. Cardiac function in mice overexpressing the beta-adrenergic receptor kinase or a beta ARK inhibitor. Science 268 5215 (1995) 1350-1353
54. Wess J. Physiological roles of G-protein-coupled receptor kinases revealed by gene-targeting technology. Trends Pharmacol. Sci. 21 10 (2000) 364-367
55. Ungerer M., Bohm M., Elce J.S., Erdmann E., and Lohse M.J. Altered expression of beta-adrenergic receptor kinase and beta 1-adrenergic receptors in the failing human heart. Circulation 87 2 (1993) 454-463
56. Gros R., Benovic J.L., Tan C.M., and Feldman R.D. G-protein-coupled receptor kinase activity is increased in hypertension. J. Clin. Invest. 99 9 (1997) 2087-2093
57. Kim O.J., Gardner B.R., Williams D.B., Marinec P.S., Cabrera D.M., Peters J.D., Mak C.C., Kim K.M., and Sibley D.R. The role of phosphorylation in D1 dopamine receptor desensitization: evidence for a novel mechanism of arrestin association. J. Biol. Chem. 279 9 (2004) 7999-8010