Identification of serine 348 on the apelin receptor as a novel regulatory phosphorylation site in apelin-13-induced G protein-independent biased signaling

Journal of Biological Chemistry

Volumn 289, Issue 45, 2014, Pages 31173-31187

  Chen, Xiaoyu ^a,d   Bai, Bo ^b   Tian, Yanjun ^b   Du, Hui ^d   Chen, Jing ^b,c  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b JINING MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG FIRST MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; MASS SPECTROMETRY; PHOSPHORYLATION; SIGNALING;

CARDIAC HYPERTROPHY; CARDIOVASCULAR FUNCTION; G PROTEIN ACTIVATION; G-PROTEIN COUPLED RECEPTORS; INTRACELLULAR SIGNALING; PHOSPHORYLATION SITES; SIGNAL PATHWAYS; TANDEM MASS SPECTROMETRY;

PROTEINS;

APELIN; APELIN RECEPTOR; BETA ARRESTIN; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; SERINE; APELIN-13 PEPTIDE; APLNR PROTEIN, HUMAN; CALCIUM; SIGNAL PEPTIDE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENETIC TRANSFECTION; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; INTERNALIZATION; LIQUID CHROMATOGRAPHY; NUCLEOTIDE SEQUENCE; PALMITOYLATION; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TANDEM MASS SPECTROMETRY; AMINO ACID SEQUENCE; CELL MEMBRANE; CHEMISTRY; GENE EXPRESSION REGULATION; HEK293 CELL LINE; HYPERTROPHY; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; MUTATION; PHOSPHORYLATION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CALCIUM; CELL MEMBRANE; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; HYPERTROPHY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHOSPHORYLATION; RECEPTORS, G-PROTEIN-COUPLED; SEQUENCE HOMOLOGY, AMINO ACID; SERINE; SIGNAL TRANSDUCTION;

EID: 84909594474     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.574020     Document Type: Article

References (57)

1. Bockaert, J., and Pin, J. P. (1999) Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J. 18, 1723-1729
2. Pierce, K. L., Premont, R. T., and Lefkowitz, R. J. (2002) Seven-transmembrane receptors. Nat. Rev. Mol. Cell Biol. 3, 639-650
3. Ma, P., and Zemmel, R. (2002) Value of novelty? Nat. Rev. Drug Discov. 1, 571-572
4. Kohout, T. A., and Lefkowitz, R. J. (2003) Regulation of G protein-coupled receptor kinases and arrestins during receptor desensitization. Mol. Pharmacol. 63, 9-18
5. Luttrell, L. M., and Lefkowitz, R. J. (2002) The role of beta-arrestins in the termination and transduction of G-protein-coupled receptor signals. J. Cell Sci. 115, 455-465
6. DeWire, S. M., Ahn, S., Lefkowitz, R. J., and Shenoy, S. K. (2007) β-Arrestins and cell signaling. Annu. Rev. Physiol. 69, 483-510
7. DeFea, K. A., Zalevsky, J., Thoma, M. S., Déry, O., Mullins, R. D., and Bunnett, N. W. (2000) β-Arrestin-dependent endocytosis of proteinase-activated receptor 2 is required for intracellular targeting of activated ERK1/2. J. Cell Biol. 148, 1267-1281
8. Luttrell, L. M., Roudabush, F. L., Choy, E. W., Miller, W. E., Field, M. E., Pierce, K. L., and Lefkowitz, R. J. (2001) Activation and targeting of extracellular signal-regulated kinases by β-arrestin scaffolds. Proc. Natl. Acad. Sci. U.S.A. 98, 2449-2454
9. 125I]-(Pyr(1))Apelin-13 is a novel radioligand for localizing the APJ orphan receptor in human and rat tissues with evidence for a vasoconstrictor role in man. Br. J. Pharmacol. 132, 1255-1260
10. Reaux, A., De Mota, N., Skultetyova, I., Lenkei, Z., El Messari, S., Gallatz, K., Corvol, P., Palkovits, M., and Llorens-Cortès, C. (2001) Physiological role of a novel neuropeptide, apelin, and its receptor in the rat brain. J. Neurochem. 77, 1085-1096
11. Tatemoto, K., Hosoya, M., Habata, Y., Fujii, R., Kakegawa, T., Zou, M. X., Kawamata, Y., Fukusumi, S., Hinuma, S., Kitada, C., Kurokawa, T., Onda, H., and Fujino, M. (1998) Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem. Biophys. Res. Commun. 251, 471-476
12. Giddings, A. S. R., Thomas, J., Tajuba, J., Bortoff, K., and Maitra, R. (2010) Development of a functional HTS assay for the APJ receptor. Int. J. High Throughput Screening 1, 39-47
13. Castan-Laurell, I., Dray, C., Attané, C., Duparc, T., Knauf, C., and Valet, P. (2011) Apelin, diabetes, and obesity. Endocrine 40, 1-9
14. Scimia, M. C., Hurtado, C., Ray, S., Metzler, S., Wei, K., Wang, J., Woods, C. E., Purcell, N. H., Catalucci, D., Akasaka, T., Bueno, O. F., Vlasuk, G. P., Kaliman, P., Bodmer, R., Smith, L. H., Ashley, E., Mercola, M., Brown, J. H., and Ruiz-Lozano, P. (2012) APJ acts as a dual receptor in cardiac hypertrophy. Nature 488, 394-398
15. Masri, B., Morin, N., Pedebernade, L., Knibiehler, B., and Audigier, Y. (2006) The apelin receptor is coupled to Gi1 or Gi2 protein and is differentially desensitized by apelin fragments. J. Biol. Chem. 281, 18317-18326
16. Pals-Rylaarsdam, R., Gurevich, V. V., Lee, K. B., Ptasienski, J. A., Benovic, J. L., and Hosey, M. M. (1997) Internalization of the m2 muscarinic acetylcholine receptor: arrestin-independent and -dependent pathways. J. Biol. Chem. 272, 23682-23689
17. Qian, H., Pipolo, L., and Thomas, W. G. (2001) Association of β-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
18. Oakley, R. H., Laporte, S. A., Holt, J. A., Barak, L. S., and Caron, M. G. (1999) Association of β-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J. Biol. Chem. 274, 32248-32257
19. Bai, B., Tang, J., Liu, H., Chen, J., Li, Y., and Song, W. (2008) Apelin-13 induces ERK1/2 but not p38 MAPK activation through coupling of the human apelin receptor to the Gi2 pathway. Acta Biochim. Biophys. Sin. 40, 311-318
20. Blethrow, J. D., Tang, C., Deng, C., and Krutchinsky, A. N. (2007) Modular mass spectrometric tool for analysis of composition and phosphorylation of protein complexes. PloS One 2, e358
21. Choi, B. K., Cho, Y. M., Bae, S. H., Zoubaulis, C. C., and Paik, Y. K. (2003) Single-step perfusion chromatography with a throughput potential for enhanced peptide detection by matrix-assisted laser desorption/ionization-mass spectrometry. Proteomics 3, 1955-1961
22. Li, Y., Chen, J., Bai, B., Du, H., Liu, Y., and Liu, H. (2012) Heterodimerization of human apelin and κ opioid receptors: roles in signal transduction. Cell Signal. 24, 991-1001
23. Hawtin, S. R. (2005) Charged residues of the conserved DRY triplet of the vasopressin V1a receptor provide molecular determinants for cell surface delivery and internalization. Mol. Pharmacol. 68, 1172-1182
24. Chen, J., and Randeva, H. S. (2004) Genomic organization of mouse orexin receptors: characterization of two novel tissue-specific splice variants. Mol. Endocrinol. 18, 2790-2804
25. Wang, C., Pan, Y., Zhang, R., Bai, B., Chen, J., and Randeva, H. S. (2014) Heterodimerization of mouse orexin type 2 receptor variants and the effects on signal transduction. Biochim. Biophys. Acta 1843, 652-663
26. Blom, N., Gammeltoft, S., and Brunak, S. (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294, 1351-1362
27. See, H. B., Seeber, R. M., Kocan, M., Eidne, K. A., and Pfleger, K. D. (2011) Application of G protein-coupled receptor-heteromer identification technology to monitor β-arrestin recruitment to G protein-coupled receptor heteromers. Assay Drug Dev. Technol. 9, 21-30
28. Hasbi, A., Devost, D., Laporte, S. A., and Zingg, H. H. (2004) Real-time detection of interactions between the human oxytocin receptor and G protein-coupled receptor kinase-2. Mol. Endocrinol. 18, 1277-1286
29. Jorgensen, R., Holliday, N. D., Hansen, J. L., Vrecl, M., Heding, A., Schwartz, T. W., and Elling, C. E. (2008) Characterization of G-protein coupled receptor kinase interaction with the neurokinin-1 receptor using bioluminescence resonance energy transfer. Mol. Pharmacol. 73, 349-358
30. Namkung, Y., Dipace, C., Javitch, J. A., and Sibley, D. R. (2009) G protein-coupled receptor kinase-mediated phosphorylation regulates post-endocytic trafficking of the D2 dopamine receptor. J. Biol. Chem. 284, 15038-15051
31. Kocan, M., and Pfleger, K. D. (2009) Detection of GPCR/β-arrestin interactions in live cells using bioluminescence resonance energy transfer technology. Methods Mol Biol 552, 305-317
32. Habata, Y., Fujii, R., Hosoya, M., Fukusumi, S., Kawamata, Y., Hinuma, S., Kitada, C., Nishizawa, N., Murosaki, S., Kurokawa, T., Onda, H., Tatemoto, K., and Fujino, M. (1999) Apelin, the natural ligand of the orphan receptor APJ, is abundantly secreted in the colostrum. Biochim. Biophys. Acta 1452, 25-35
33. Masri, B., Lahlou, H., Mazarguil, H., Knibiehler, B., and Audigier, Y. (2002) Apelin(65-77) activates extracellular signal-regulated kinases via a PTX-sensitive G protein. Biochem. Biophys. Res. Commun. 290, 539-545
34. i, and AMPK-dependent mechanisms. Endocrinology 152, 59-68
35. Lefkowitz, R. J., and Shenoy, S. K. (2005) Transduction of receptor signals by β-arrestins. Science 308, 512-517
36. Lee, D. K., Ferguson, S. S., George, S. R., and O'Dowd, B. F. (2010) The fate of the internalized apelin receptor is determined by different isoforms of apelin mediating differential interaction with β-arrestin. Biochem. Biophys. Res. Commun. 395, 185-189
37. Oakley, R. H., Laporte, S. A., Holt, J. A., Barak, L. S., and Caron, M. G. (2001) Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor-β-arrestin complexes after receptor endocytosis. J. Biol. Chem. 276, 19452-19460
38. Butcher, A. J., Prihandoko, R., Kong, K. C., McWilliams, P., Edwards, J. M., Bottrill, A., Mistry, S., and Tobin, A. B. (2011) Differential G-protein-coupled receptor phosphorylation provides evidence for a signaling bar code. J. Biol. Chem. 286, 11506-11518
39. Tobin, A. B., Butcher, A. J., and Kong, K. C. (2008) Location, location, location: site-specific GPCR phosphorylation offers a mechanism for cell-type-specific signalling. Trends Pharmacol. Sci. 29, 413-420
40. Gurevich, E. V., and Gurevich, V. V. (2006) Arrestins: ubiquitous regulators of cellular signaling pathways. Genome Biol. 7, 236
41. Kule, C. E., Karoor, V., Day, J. N., Thomas, W. G., Baker, K. M., Dinh, D., Acker, K. A., and Booz, G. W. (2004) Agonist-dependent internalization of the angiotensin II type one receptor (AT1): role of C-terminus phosphorylation in recruitment of β-arrestins. Regul. Pept. 120, 141-148
42. Walther, C., Nagel, S., Gimenez, L. E., Mörl, K., Gurevich, V. V., and Beck-Sickinger, A. G. (2010) Ligand-induced internalization and recycling of the human neuropeptide Y2 receptor is regulated by its carboxyl-terminal tail. J. Biol. Chem. 285, 41578-41590
43. Jones, B. W., Song, G. J., Greuber, E. K., and Hinkle, P. M. (2007) Phosphorylation of the endogenous thyrotropin-releasing hormone receptor in pituitary GH3 cells and pituitary tissue revealed by phosphosite-specific antibodies. J. Biol. Chem. 282, 12893-12906
44. Zimmerman, B., Simaan, M., Akoume, M. Y., Houri, N., Chevallier, S., Séguéla, P., and Laporte, S. A. (2011) Role of ssarrestins in bradykinin B2 receptor-mediated signalling. Cell Signal. 23, 648-659
45. Ahn, S., Shenoy, S. K., Wei, H., and Lefkowitz, R. J. (2004) Differential kinetic and spatial patterns of β-arrestin and G protein-mediated ERK activation by the angiotensin II receptor. J. Biol. Chem. 279, 35518-35525
46. Luttrell, L. M., and Gesty-Palmer, D. (2010) Beyond desensitization: physiological relevance of arrestin-dependent signaling. Pharmacol. Rev. 62, 305-330
47. Reiter, E., Ahn, S., Shukla, A. K., and Lefkowitz, R. J. (2012) Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors. Annu. Rev. Pharmacol. Toxicol. 52, 179-197
48. Violin, J. D., DeWire, S. M., Yamashita, D., Rominger, D. H., Nguyen, L., Schiller, K., Whalen, E. J., Gowen, M., and Lark, M. W. (2010) Selectively engaging β-arrestins at the angiotensin II type 1 receptor reduces blood pressure and increases cardiac performance. J. Pharmacol. Exp. Ther. 335, 572-579
49. DeWire, S. M., Yamashita, D. S., Rominger, D. H., Liu, G., Cowan, C. L., Graczyk, T. M., Chen, X. T., Pitis, P. M., Gotchev, D., Yuan, C., Koblish, M., Lark, M. W., and Violin, J. D. (2013) A G protein-biased ligand at the μ-opioid receptor is potently analgesic with reduced gastrointestinal and respiratory dysfunction compared with morphine. J. Pharmacol. Exp. Ther. 344, 708-717
50. Wei, H., Ahn, S., Shenoy, S. K., Karnik, S. S., Hunyady, L., Luttrell, L. M., and Lefkowitz, R. J. (2003) Independent β-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
51. Gáborik, Z., Jagadeesh, G., Zhang, M., Spät, A., Catt, K. J., and Hunyady, L. (2003) The role of a conserved region of the second intracellular loop in AT1 angiotensin receptor activation and signaling. Endocrinology 144, 2220-2228
52. 2-adrenergic receptor. J. Biol. Chem. 281, 1261-1273
53. Szokodi, I., Tavi, P., Földes, G., Voutilainen-Myllylä, S., Ilves, M., Tokola, H., Pikkarainen, S., Piuhola, J., Rysä, J., Tóth, M., and Ruskoaho, H. (2002) Apelin, the novel endogenous ligand of the orphan receptor APJ, regulates cardiac contractility. Circ. Res. 91, 434-440
54. Ashley, E. A., Powers, J., Chen, M., Kundu, R., Finsterbach, T., Caffarelli, A., Deng, A., Eichhorn, J., Mahajan, R., Agrawal, R., Greve, J., Robbins, R., Patterson, A. J., Bernstein, D., and Quertermous, T. (2005) The endogenous peptide apelin potently improves cardiac contractility and reduces cardiac loading in vivo. Cardiovasc. Res. 65, 73-82
55. Jia, Y. X., Pan, C. S., Zhang, J., Geng, B., Zhao, J., Gerns, H., Yang, J., Chang, J. K., Tang, C. S., and Qi, Y. F. (2006) Apelin protects myocardial injury induced by isoproterenol in rats. Regul. Pept. 133, 147-154
56. Chun, H. J., Ali, Z. A., Kojima, Y., Kundu, R. K., Sheikh, A. Y., Agrawal, R., Zheng, L., Leeper, N. J., Pearl, N. E., Patterson, A. J., Anderson, J. P., Tsao, P. S., Lenardo, M. J., Ashley, E. A., and Quertermous, T. (2008) Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis. J. Clin. Invest. 118, 3343-3354
57. Siddiquee, K., Hampton, J., Khan, S., Zadory, D., Gleaves, L., Vaughan, D. E., and Smith, L. H. (2011) Apelin protects against angiotensin II-induced cardiovascular fibrosis and decreases plasminogen activator inhibitor type-1 production. J. Hypertens. 29, 724-731