Regulation of corticotropin-releasing hormone receptor type 1α signaling: Structural determinants for G protein-coupled receptor kinase-mediated phosphorylation and agonist-mediated desensitization

Molecular Endocrinology

Volumn 19, Issue 2, 2005, Pages 474-490

  Teli, Thalia ^a   Markovic, Danijela ^a   Levine, Michael A ^b   Hillhouse, Edward W ^c   Grammatopoulos, Dimitris K ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b LERNER RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; AMINO ACID DERIVATIVE; BETA ARRESTIN; CORTICOTROPHIN RELEASING HORMONE RECEPTOR TYPE 1 ALPHA; CORTICOTROPIN RELEASING FACTOR; G PROTEIN COUPLED RECEPTOR KINASE; G PROTEIN COUPLED RECEPTOR KINASE 3; G PROTEIN COUPLED RECEPTOR KINASE 6; HORMONE RECEPTOR; PROTEIN KINASE; PROTEIN SUBUNIT; SERINE DERIVATIVE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; DESENSITIZATION; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; GENE TRANSLOCATION; HORMONAL REGULATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MYOMETRIUM; PREMEDICATION; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

ADENYLATE CYCLASE; ANIMALS; ARRESTINS; CELL LINE; CYCLIC AMP; DIMERIZATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENDOCYTOSIS; FEMALE; HEPARIN; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MUSCLE CELLS; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; SERINE; SHEEP; SIGNAL TRANSDUCTION; THREONINE; TIME FACTORS; TRANSFECTION; TYROSINE;

EID: 13544261496     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2004-0275     Document Type: Article

References (54)

1. Chen R, Lewis KA, Perrin MH, Vale WW 1993 Expression cloning of a human corticotropin-releasing-factor receptor. Proc Natl Acad Sci USA 90:8967-6971
2. Liaw CW, Lovenberg TW, Barry G, Oltersdorf T, Grigoriadis DE, De Souza EB 1995 Cloning and characterization of the human corticotropin-releasing factor-2 receptor complementary deoxyribonucleic acid. Endocrinology 137:72-77
3. Grammatopoulos DK, Chrousos GP 2002 Functional characteristics of CRH receptors and potential clinical applications of CRH-receptor antagonists. Trends Endocrinol Metab 10:436-444
4. Timpl P, Spanagel R, Sillaber I, Kresse A, Reul JM, Stalla GK, Blanquet V, Steckler T, Holsboer F, Wurst W 1998 Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nat Genet 19:162-166
5. Seres J, Bornstein SR, Seres P, Willenberg HS, Schulte KM, Scherbaum WA, Ehrhart-Bornstein M 2004 Corticotropin-releasing hormone system in human adipose tissue. J Clin Endocrinol Metab 89:965-970
6. Slominski A, Pisarchik A, Tobin DJ, Mazurkiewicz JE, Wortsman J 2004 Differential expression of a cutaneous corticotropin-releasing hormone system. Endocrinology 145:941-950
7. Grammatopoulos D, Dai Y, Chen J, Karteris E, Papadopoulou N, Easton AJ, Hillhouse EW 1998 Human corticotropin-releasing hormone receptor: differences in subtype expression between pregnant and nonpregnant myometria. J Clin Endocrinol Metab 83:2539-2544
8. Grammatopoulos DK, Randeva HS, Levine MA, Kanellopoulou KA, Hillhouse EW 2001 Rat cerebral cortex corticotropin-releasing hormone receptors: evidence for receptor coupling to multiple G-proteins. J Neurochem 76:509-519
9. Karteris E, Grammatopoulos D, Randeva H, Hillhouse EW 2000 Signal transduction characteristics of the corticotropin-releasing hormone receptors in the feto-placental unit. J Clin Endocrinol Metab 85:1989-1996
10. Blank T, Nijholt I, Grammatopoulos DK, Randeva HS, Hillhouse EW, Spiess J 2003 Corticotropin-releasing factor receptors couple to multiple G-proteins to activate diverse intracellular signaling pathways in mouse hippocampus: role in neuronal excitability and associative learning. J Neurosci 23:700-707
11. Riley SC, Walton JC, Herlick JM, Challis JR 1991 The localisation and distribution of CRH in the human placenta and fetal membranes throughout gestation. J Clin Endocrinol Metab 72:1001-1007
12. Petraglia F, Florio P, Gallo R, Simoncini T, Saviozzi M, Di Blasio AM, Vaughan J, Vale W 1996 Human placenta and fetal membranes express human urocortin mRNA and peptide. J Clin Endocrinol Metab 81:3807-3810
13. McLean M, Bisits A, Davies J, Woods R, Lowry P, Smith R 1995 A placental clock controlling the length of human pregnancy. Nat Med 1:460-463
14. Hillhouse EW, Grammatopoulos D 2001 Control of intracellular signalling by corticotropin-releasing hormone (CRH) in human myometrium. Front Horm Res 27:66-74
15. Grammatopoulos D, Stirrat GM, Williams SA, Hillhouse EW 1996 The biological activity of the corticotropin-releasing hormone receptor-adenylate cyclase complex in human myometrium is reduced at the end of pregnancy. J Clin Endocrinol Metab 81:745-751
16. Aggelidou E, Hillhouse EW, Grammatopoulos D 2002 Up-regulation of nitric oxide synthase and modulation of the guanylate cyclase activity by corticotropin releasing hormone but not urocortin II or urocortin III in cultured human pregnant myometrial cells. Proc Natl Acad Sci USA 99:3300-3305
17. Word RA, Casey ML, Kamm KE, Stull JT 1991 Effects of cGMP on [Ca2+]i, myosin light chain phosphorylation, and contraction in human myometrium. Am J Physiol 260:C861-C867
18. Grammatopoulos DK, Randeva HS, Levine MA, Katsanou ES, Hillhouse EW 2000 Urocortin, but not corticotropin-releasing hormone (CRH), activates the mitogen-activated protein kinase signal transduction pathway in human pregnant myometrium: an effect mediated via R1α and R2β CRH receptor subtypes and stimulation of Gq-proteins. Mol Endocrinol 14:2076-2091
19. 301 for signalling switch and selectivity. Mol Endocrinol 18:624-639
20. Grammatopoulos D, Hillhouse EW 1999 Role of corticotropin-releasing hormone in the onset of labour. Lancet 353:1546-1549
21. Freedman NJ, Lefkowitz RJ 1996 Desensitization of G protein-coupled receptors. Recent Prog Horm Res 51:319-351
22. Claing A, Laporte SA, Caron MG, Lefkowitz RJ 2002 Endocytosis of G protein-coupled receptors: roles of G protein-coupled receptor kinases and β-arrestin proteins. Prog Neurobiol 66:61-79
23. Hauger RL, Smith RD, Braun S, Dautzenberg FM, Catt KJ 2000 Rapid agonist-induced phosphorylation of the human CRF receptor, type 1: a potential mechanism for homologous desensitization. Biochem Biophys Res Commun 268:572-576
24. Dautzenberg FM, Braun S, Hauger RL 2001 GRK3 mediates desensitization of CRF1 receptors: a potential mechanism regulating stress adaptation. Am J Physiol Regul Integr Comp Physiol 280:R935-R946
25. Hauger RL, Dautzenberg FM, Flaccus A, Liepold T, Spiess J 1997 Regulation of corticotropin-releasing factor receptor function in human Y-79 retinoblastoma cells: rapid and reversible homologous desensitization but prolonged recovery. J Neurochem 68:2308-2316
26. Dieterich KD, Grigoriadis DE, De Souza EB 1996 Homologous desensitization of human corticotropin-releasing factor 1 receptor in stable transfected mouse fibroblast cells. Brain Res 710:287-292
27. Dayes BA, Lye SJ 1990 Characterization of myometrial desensitization to β-adrenergic agonists. Can J Physiol Pharmacol 68:1377-1384
28. Kohout TA, Lefkowitz RJ 2003 Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization. Mol Pharmacol 63:9-18
29. Krupnick JG, Santini F, Gagnon AW, Keen JH, Benovic JL 1997 Modulation of the arrestin-clathrin interaction in cells. Characterization of β-arrestin dominant-negative mutants. J Biol Chem 272:32507-32512
30. Lazari MF, Liu X, Nakamura K, Benovic JL, Ascoli M 1999 Role of G protein-coupled receptor kinases on the agonist-induced phosphorylation and internalization of the follitropin receptor. Mol Endocrinol 13:866-878
31. Daaka Y, Pitcher JA, Richardson M, Stoffel RH, Robishaw JD, Lefkowitz RJ 1997 Receptor and G βγ isoform-specific interactions with G protein-coupled receptor kinases. Proc Natl Acad Sci USA 94:2180-2185
32. Khac LD, Naze S, Harbon S 1994 Endothelin receptor type A signals both the accumulation of inositol phosphates and the inhibition of cyclic AMP generation in rat myometrium: stimulation and desensitization. Mol Pharmacol 46:485-494
33. Robinson C, Schumann R, Zhang P, Young RC 2003 Oxytocin-induced desensitization of the oxytocin receptor. Am J Obstet Gynecol 188:497-502
34. de Gasparo M, Whitebread S, Kalenga MK, de Hertogh R, Crevoisier P, Thomas K 1994 Down regulation of the angiotensin II receptor subtype AT2 in human myometrium during pregnancy. Regul Pept 53:39-45
35. Berg G, Andersson RG, Ryden G 1985 β-Adrenergic receptors in human myometrium during pregnancy: changes in the number of receptors after β-mimetic treatment. Am J Obstet Gynecol 151:392-396
36. Engelhardt S, Zieger W, Kassubek J, Michel MC, Lohse MJ, Brodde OE 1997 Tocolytic therapy with fenoterol induces selective down-regulation of β-adrenergic receptors in human myometrium. J Clin Endocrinol Metab 82:1235-1242
37. Aiyar N, Disa J, Dang K, Pronin AN, Benovic JL, Nambi P 2000 Involvement of G protein-coupled receptor kinase-6 in desensitization of CGRP receptors. Eur J Pharmacol 403:1-7
38. Roseboom PH, Urben CM, Kalin NH 2001 Persistent corticotropin-releasing factor(1) receptor desensitization and downregulation in the human neuroblastoma cell line IMR-32. Brain Res Mol Brain Res 2001 92:115-127
39. Lefkowitz RJ 1998 G protein-coupled receptors. III. New roles for receptor kinases and β-arrestins in receptor signaling and desensitization. J Biol Chem 273:18677-18680
40. Hauger RL, Olivares-Reyes JA, Braun S, Catt KJ, Dautzenberg FM 2003 Mediation of corticotropin releasing factor type 1 receptor phosphorylation and desensitization by protein kinase C: a possible role in stress adaptation. J Pharmacol Exp Ther 306:794-803
41. Grammatopoulos DK, Hillhouse EW 1999 Activation of protein kinase C by oxytocin inhibits the biological activity of the human myometrial corticotropin-releasing hormone receptor at term. Endocrinology 140:585-594
42. Benovic JL, Stone WC, Caron MG, Lefkowitz RJ 1989 Inhibition of the β-adrenergic receptor kinase by polyanions. J Biol Chem 264:6707-6710
43. Shayo C, Fernandez N, Legnazzi BL, Monczor F, Mladovan A, Baldi A, Davio C 2001 Histamine H2 receptor desensitization: involvement of a select array of G protein-coupled receptor kinases. Mol Pharmacol 60:1049-1056
44. Pitcher JA, Freedman NJ, Lefkowitz RJ 1998 G-protein receptor kinases. Ann Rev Biochem 67:653-692
45. Brenninkmeijer CB, Price SA, Lopez Bernal A, Phaneuf S 1999 Expression of G-protein-coupled receptor kinases in pregnant term and non-pregnant human myometrium. J Endocrinol 162:401-418
46. Simon V, Robin MT, Legrand C, Cohen-Tannoudji J 2003 Endogenous G protein-coupled receptor kinase 6 triggers homologous β-adrenergic receptor desensitization in primary uterine smooth muscle cells. Endocrinology 144:3058-3066
47. Onorato JJ, Palczewski K, Regan JW, Caron MG, Lefkowitz RJ, Benovic JL 1991 Role of acidic amino acids in peptide substrates of the β-adrenergic receptor kinase and rhodopsin kinase. Biochemistry 30:5118-5125
48. Fredericks ZL, Pitcher JA, Lefkowitz RJ 1996 Identification of the G protein-coupled receptor kinase phosphorylation sites in the human β2-adrenergic receptor. J Biol Chem 1271:13796-13803
49. Lefkowitz RJ, Hausdorff WP, Caron MG 1990 Role of phosphorylation in desensitization of the β-adrenoceptor. Trends Pharmacol Sci 11:190-194
50. Tang H, Guo DF, Porter JP, Wanaka Y, Inagami T 1998 Role of cytoplasmic tail of the type 1A angiotensin II receptor in agonist- and phorbol ester-induced desensitization. Circ Res 82:523-531
51. Innamorati G, Sadeghi HM, Tran NT, Birnbaumer M 1998 A serine cluster prevents recycling of the V2 vasopressin receptor. Proc Natl Acad Sci USA 95:2222-2226
52. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR 1989 Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59
53. McPherson G 1983 A practical computer based approach to the analysis of radioligand binding experiments. Prog Biomed 17:107-114
54. Munson P, Rodgbard O 1980 LIGAND: a versatile computerised approach for characterization of ligand binding systems. Anal Biochem 107:220-239