Biased signaling of the angiotensin II type 1 receptor can be mediated through distinct mechanisms

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Bonde, Marie Mi ^a,b   Hansen, Jonas Tind ^b,c   Sanni, Samra Joke ^c   Haunsø, Stig ^a   Gammeltoft, Steen ^c   Lyngsø, Christina ^b,c   Hansen, Jakob Lerche ^a,b,d  

^a Mental Health Services CPH   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c GLOSTRUP UNIVERSITY HOSPITAL   (Denmark)

^d NOVO NORDISK A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; BETA ARRESTIN 2; GUANINE NUCLEOTIDE BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; BETA ARRESTIN; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; HYBRID PROTEIN; LUCIFERASE; RETINA S ANTIGEN;

ARTICLE; BINDING AFFINITY; BINDING COMPETITION; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTERNALIZATION; MUTATION; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; CELL STRAIN COS1; CELL STRAIN HEK293; CERCOPITHECUS; GENETIC TRANSFECTION; GENETICS; KINETICS; LUMINESCENCE; METABOLISM; METHODOLOGY; PROTEIN BINDING;

ANGIOTENSIN II; ANIMALS; ARRESTINS; BINDING, COMPETITIVE; CERCOPITHECUS AETHIOPS; COS CELLS; GREEN FLUORESCENT PROTEINS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HEK293 CELLS; HUMANS; KINETICS; LUCIFERASES; LUMINESCENT MEASUREMENTS; MUTATION; PROTEIN BINDING; RECEPTOR, ANGIOTENSIN, TYPE 1; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 78649869175     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014135     Document Type: Article

References (61)

1. Aplin M, Christensen GL, Hansen JL (2008) Pharmacologic perspectives of functional selectivity by the angiotensin II type 1 receptor. Trends Cardiovasc Med 18: 305-312.
2. Kendall RT, Luttrell LM (2009) Diversity in arrestin function. Cell Mol Life Sci 66: 2953-2973.
3. Nygaard R, Frimurer TM, Holst B, Rosenkilde MM, Schwartz TW (2009) Ligand binding and micro-switches in 7TM receptor structures. Trends Pharmacol Sci 30: 249-259.
4. Rosenbaum DM, Rasmussen SG, Kobilka BK (2009) The structure and function of G-protein-coupled receptors. Nature 459: 356-363.
5. Ballesteros JA, Shi L, Javitch JA (2001) Structural mimicry in G protein-coupled receptors: implications of the high-resolution structure of rhodopsin for structure-function analysis of rhodopsin-like receptors. Mol Pharmacol 60: 1-19.
6. Urban JD, Clarke WP, von Zastrow M, Nichols DE, Kobilka BK, et al. (2006) Functional selectivity and classical concepts of quantitative pharmacology. J Pharmacol Exp Ther.
7. Aplin M, Bonde MM, Hansen JL (2009) Molecular determinants of angiotensin II type 1 receptor functional selectivity. J Mol Cell Cardiol 46: 15-24.
8. Tohgo A, Pierce KL, Choy EW, Lefkowitz RJ, Luttrell LM (2002) Beta-Arrestin scaffolding of the ERK cascade enhances cytosolic ERK activity but inhibits ERK-mediated transcription following angiotensin AT1a receptor stimulation. J Biol Chem 277:9429-9436.
9. Aplin M, Christensen GL, Schneider M, Heydorn A, Gammeltoft S, et al. (2007) Differential extracellular signal-regulated kinases 1 and 2 activation by the angiotensin type 1 receptor supports distinct phenotypes of cardiac myocytes. Basic Clin Pharmacol Toxicol 100: 296-301.
10. Aplin M, Christensen GL, Schneider M, Heydorn A, Gammeltoft S, et al. (2007) The angiotensin type 1 receptor activates extracellular signal-regulated kinases 1 and 2 by G protein-dependent and -independent pathways in cardiac myocytes and langendorff-perfused hearts. Basic Clin Pharmacol Toxicol 100: 289-295.
11. Ahn S, Shenoy SK, Wei H, Lefkowitz RJ (2004) Differential kinetic and spatial patterns of beta-arrestin and G protein-mediated ERK activation by the angiotensin II receptor. J Biol Chem 279: 35518-35525.
12. Wei H, Ahn S, Shenoy SK, Karnik SS, Hunyady L, et al. (2003) Independent beta-arrestin 2 and G protein-mediated pathways for angiotensin II activation of extracellular signal-regulated kinases 1 and 2. Proc Natl Acad Sci U S A 100: 10782-10787.
13. Hunyady L, Catt KJ (2006) Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol Endocrinol 20: 953-970.
14. Mehta PK, Griendling KK (2007) Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 292: C82-97.
15. Weir MR (2007) Effects of renin-angiotensin system inhibition on end-organ protection: can we do better? Clin Ther 29: 1803-1824.
16. Bihoreau C, Monnot C, Davies E, Teutsch B, Bernstein KE, et al. (1993) Mutation of Asp74 of the rat angiotensin II receptor confers changes in antagonist affinities and abolishes G-protein coupling. Proc Natl Acad Sci U S A 90: 5133-5137.
17. Gaborik Z, Jagadeesh G, Zhang M, Spat A, Catt KJ, et al. (2003) The role of a conserved region of the second intracellular loop in AT1 angiotensin receptor activation and signaling. Endocrinology 144: 2220-2228.
18. Hines J, Fluharty SJ, Yee DK (2003) Structural determinants for the activation mechanism of the angiotensin II type 1 receptor differ for phosphoinositide hydrolysis and mitogen-activated protein kinase pathways. Biochem Pharmacol 66: 251-262.
19. Hunyady L, Baukal AJ, Balla T, Catt KJ (1994) Independence of type I angiotensin II receptor endocytosis from G protein coupling and signal transduction. J Biol Chem 269: 24798-24804.
20. Hunyady L, Bor M, Baukal AJ, Balla T, Catt KJ (1995) A conserved NPLFY sequence contributes to agonist binding and signal transduction but is not an internalization signal for the type 1 angiotensin II receptor. J Biol Chem 270: 16602-16609.
21. Holloway AC, Qian H, Pipolo L, Ziogas J, Miura S, et al. (2002) Side-chain substitutions within angiotensin II reveal different requirements for signaling, internalization, and phosphorylation of type 1A angiotensin receptors. Mol Pharmacol 61: 768-777.
22. Oakley RH, Laporte SA, Holt JA, Caron MG, Barak LS (2000) Differential affinities of visual arrestin, beta arrestin1, and beta arrestin2 for G proteincoupled receptors delineate two major classes of receptors. J Biol Chem 275: 17201-17210.
23. Zhang J, Barak LS, Anborgh PH, Laporte SA, Caron MG, et al. (1999) Cellular trafficking of G protein-coupled receptor/beta-arrestin endocytic complexes. J Biol Chem 274: 10999-11006.
24. Conchon S, Peltier N, Corvol P, Clauser E (1998) A noninternalized nondesensitized truncated AT1A receptor transduces an amplified ANG II signal. Am J Physiol 274: E336-345.
25. Qian H, Pipolo L, Thomas WG (2001) Association of beta-Arrestin 1 with the type 1A angiotensin II receptor involves phosphorylation of the receptor carboxyl terminus and correlates with receptor internalization. Mol Endocrinol 15: 1706-1719.
26. Hunyady L, Bor M, Balla T, Catt KJ (1994) Identification of a cytoplasmic Ser-Thr-Leu motif that determines agonist-induced internalization of the AT1 angiotensin receptor. J Biol Chem 269: 31378-31382.
27. Oakley RH, Laporte SA, Holt JA, Barak LS, Caron MG (2001) Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor-beta-arrestin complexes after receptor endocytosis*. J Biol Chem 276: 19452-19460.
28. Smith RD, Hunyady L, Olivares-Reyes JA, Mihalik B, Jayadev S, et al. (1998) Agonist-induced phosphorylation of the angiotensin AT1a receptor is localized to a serine/threonine-rich region of its cytoplasmic tail. Mol Pharmacol 54: 935-941.
29. Wei H, Ahn S, Barnes WG, Lefkowitz RJ (2004) Stable interaction between beta-arrestin 2 and angiotensin type 1A receptor is required for beta-arrestin 2-mediated activation of extracellular signal-regulated kinases 1 and 2. J Biol Chem 279: 48255-48261.
30. Marie J, Maigret B, Joseph MP, Larguier R, Nouet S, et al. (1994) Tyr292 in the seventh transmembrane domain of the AT1A angiotensin II receptor is essential for its coupling to phospholipase C. J Biol Chem 269: 20815-20818.
31. Laporte SA, Servant G, Richard DE, Escher E, Guillemette G, et al. (1996) The tyrosine within the NPXnY motif of the human angiotensin II type 1 receptor is involved in mediating signal transduction but is not essential for internalization. Mol Pharmacol 49: 89-95.
32. Heckman KL, Pease LR (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc 2: 924-932.
33. Benned-Jensen T, Rosenkilde MM (2008) Structural motifs of importance for the constitutive activity of the orphan 7TM receptor EBI2: analysis of receptor activation in the absence of an agonist. Mol Pharmacol 74: 1008-1021.
34. Hansen JL, Aplin M, Hansen JT, Christensen GL, Bonde MM, et al. (2008) The human angiotensin AT(1) receptor supports G protein-independent extracellular signal-regulated kinase 1/2 activation and cellular proliferation. Eur J Pharmacol 590: 255-263.
35. Bonde MM, Yao R, Ma JN, Madabushi S, Haunso S, et al. (2010) An angiotensin II type 1 receptor activation switch patch revealed through evolutionary trace analysis. Biochem Pharmacol 80: 86-94.
36. Hansen JL, Haunso S, Brann MR, Sheikh SP, Weiner DM (2004) Loss-offunction polymorphic variants of the human angiotensin II type 1 receptor. Mol Pharmacol 65: 770-777.
37. Gaborik Z, Mihalik B, Jayadev S, Jagadeesh G, Catt KJ, et al. (1998) Requirement of membrane-proximal amino acids in the carboxyl-terminal tail for expression of the rat AT1a angiotensin receptor. FEBS Lett 428: 147-151.
38. Sanni SJ, Hansen JT, Bonde MM, Speerschneider T, Christensen GL, et al. Beta-Arrestin 1 and 2 stabilize the angiotensin II type I receptor in distinct highaffinity conformations. Br J Pharmacol 161: 150-161.
39. Feng YH, Ding Y, Ren S, Zhou L, Xu C, et al. (2005) Unconventional homologous internalization of the angiotensin II type-1 receptor induced by Gprotein-independent signals. Hypertension 46: 419-425.
40. Ohyama K, Yamano Y, Sano T, Nakagomi Y, Wada M, et al. (2002) Role of the conserved DRY motif on G protein activation of rat angiotensin II receptor type 1A. Biochem Biophys Res Commun 292: 362-367.
41. Seta K, Nanamori M, Modrall JG, Neubig RR, Sadoshima J (2002) AT1 receptor mutant lacking heterotrimeric G protein coupling activates the Src-Ras-ERK pathway without nuclear translocation of ERKs. J Biol Chem 277: 9268.
42. Shibata T, Suzuki C, Ohnishi J, Murakami K, Miyazaki H (1996) Identification of regions in the human angiotensin II receptor type 1 responsible for Gi and Gq coupling by mutagenesis study. Biochem Biophys Res Commun 218: 383-389.
43. Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauss N, et al. (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455: 497-502.
44. Gurevich VV, Pals-Rylaarsdam R, Benovic JL, Hosey MM, Onorato JJ (1997) Agonist-receptor-arrestin, an alternative ternary complex with high agonist affinity. J Biol Chem 272: 28849-28852.
45. Sanni SJ, Hansen JT, Bonde MM, Speerschneider T, Christensen GL, et al. (2010) Beta-Arrestin 1 and 2 stabilize the angiotensin II type I receptor in distinct high-affinity conformations. Br J Pharmacol 161:150-161.
46. Yee DK, Suzuki A, Luo L, Fluharty SJ (2006) Identification of structural determinants for G protein-independent activation of mitogen-activated protein kinases in the seventh transmembrane domain of the angiotensin II type 1 receptor. Mol Endocrinol 20: 1924-1934.
47. Kule CE, Karoor V, Day JN, Thomas WG, Baker KM, et al. (2004) Agonistdependent internalization of the angiotensin II type one receptor (AT1): role of C-terminus phosphorylation in recruitment of beta-arrestins. Regul Pept 120: 141-148.
48. Kenakin T (2007) Functional selectivity through protean and biased agonism: who steers the ship? Mol Pharmacol 72: 1393-1401.
49. Christensen GL, Kelstrup CD, Lyngso C, Sarwar U, Bogebo R, et al. (2010) Quantitative phosphoproteomics dissection of seven-transmembrane receptor signaling using full and biased agonists. Mol Cell Proteomics 9: 1540-1553.
50. Xiao K, Sun J, Kim J, Rajagopal S, Zhai B, et al. (2010) Global phosphorylation analysis of beta-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR). Proc Natl Acad Sci U S A 107: 15299-15304.
51. Mirzadegan T, Benko G, Filipek S, Palczewski K (2003) Sequence analyses of Gprotein- coupled receptors: similarities to rhodopsin. Biochemistry 42: 2759-2767.
52. Li J, Edwards PC, Burghammer M, Villa C, Schertler GF (2004) Structure of bovine rhodopsin in a trigonal crystal form. J Mol Biol 343: 1409-1438.
53. Murakami M, Kouyama T (2008) Crystal structure of squid rhodopsin. Nature 453: 363-367.
54. Nikiforovich GV, Zhang M, Yang Q, Jagadeesh G, Chen HC, et al. (2006) Interactions between conserved residues in transmembrane helices 2 and 7 during angiotensin AT1 receptor activation. Chem Biol Drug Des 68: 239-249.
55. Rosenbaum DM, Cherezov V, Hanson MA, Rasmussen SG, Thian FS, et al. (2007) GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function. Science 318: 1266-1273.
56. Sealfon SC, Chi L, Ebersole BJ, Rodic V, Zhang D, et al. (1995) Related Contribution of Specific Helix 2 and 7 Residues to Conformational Activation of the Serotonin 5-HT2A Receptor. J Biol Chem 270: 16683-16688.
57. Zhou W, Flanagan C, Ballesteros JA, Konvicka K, Davidson JS, et al. (1994) A reciprocal mutation supports helix 2 and helix 7 proximity in the gonadotropinreleasing hormone receptor. Mol Pharmacol 45: 165-170.
58. Urizar E, Claeysen S, Deupi X, Govaerts C, Costagliola S, et al. (2005) An activation switch in the rhodopsin family of G protein-coupled receptors: the thyrotropin receptor. J Biol Chem 280: 17135-17141.
59. Barak LS, Menard L, Ferguson SS, Colapietro AM, Caron MG (1995) The conserved seven-transmembrane sequence NP(X)2,3Y of the G-protein-coupled receptor superfamily regulates multiple properties of the beta 2-adrenergic receptor. Biochemistry 34: 15407-15414.
60. Gripentrog JM, Jesaitis AJ, Miettinen HM (2000) A single amino acid substitution (N297A) in the conserved NPXXY sequence of the human Nformyl peptide receptor results in inhibition of desensitization and endocytosis, and a dose-dependent shift in p42/44 mitogen-activated protein kinase activation and chemotaxis. Biochem J 352 Pt 2: 399-407.
61. Hofmann KP, Scheerer P, Hildebrand PW, Choe HW, Park JH, et al. (2009) A G protein-coupled receptor at work: the rhodopsin model. Trends Biochem Sci 34: 540-552.