Regulation of G protein-coupled receptor signaling: Specific dominant-negative effects of melanocortin 2 receptor accessory protein2

Science Signaling

Volumn 3, Issue 116, 2010, Pages

  Sebag, Julien A ^a   Hinkle, Patricia M ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSIME 3',5' MONOPHOSPHATE; CORTICOTROPIN; G PROTEIN COUPLED RECEPTOR; MELANOCORTIN 2 RECEPTOR; MELANOCORTIN 2 RECEPTOR ACCESSORY PROTEIN 2; PHOSPHATE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; GENE EXPRESSION; GENE SEQUENCE; HUMAN; MELANOCYTE; NONHUMAN; PRIORITY JOURNAL;

ADRENOCORTICOTROPIC HORMONE; ANALYSIS OF VARIANCE; ANIMALS; CARRIER PROTEINS; CHO CELLS; CLONING, MOLECULAR; CRICETINAE; CRICETULUS; CYCLIC AMP; DIMERIZATION; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; MEMBRANE PROTEINS; RECEPTOR, MELANOCORTIN, TYPE 2; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 77953867645     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000593     Document Type: Article

References (38)

1. T. A. Kohout, S. L. Nicholas, S. J. Perry, G. Reinhart, S. Junger, R. S. Struthers, Differential desensitization, receptor phosphorylation, β-arrestin recruitment, and ERK1/2 activation by the two endogenous ligands for the CC chemokine receptor 7. J. Biol. Chem. 279, 23214-23222 (2004).
2. C. Haskell-Luevano, E. K. Monck, Agouti-related protein functions as an inverse agonist at a constitutively active brain melanocortin-4 receptor. Regul. Pept. 99, 1-7 (2001).
3. W. A. Nijenhuis, J. Oosterom, R. A. Adan, AgRP (83-132) acts as an inverse agonist on the human-melanocortin-4 receptor. Mol. Endocrinol. 15, 164-171 (2001).
4. D. Lu, D. Willard, I. R. Patel, S. Kadwell, L. Overton, T. Kost, M. Luther, W. Chen, R. P. Woychik, W. O. Wilkison, R. D. Cone, Agouti protein is an antagonist of the melanocytestimulating-hormone receptor. Nature 371, 799-802 (1994).
5. R. D. Cone, Studies on the physiological functions of the melanocortin system. Endocr. Rev. 27, 736-749 (2006).
6. V. Bernier, D. G. Bichet, M. Bouvier, Pharmacological chaperone action on G-proteincoupled receptors. Curr. Opin. Pharmacol. 4, 528-533 (2004).
7. J. Bockaert, L. Fagni, A. Dumuis, P. Marin, GPCR interacting proteins (GIP). Pharmacol. Ther. 103, 203-221 (2004).
8. S. Bulenger, S. Marullo, M. Bouvier, Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol. Sci. 26, 131-137 (2005).
9. J. C. Bermak, M. Li, C. Bullock, Q. Y. Zhou, Regulation of transport of the dopamine D1 receptor by a new membrane-associated ER protein. Nat. Cell Biol. 3, 492-498 (2001).
10. D. L. Hay, D. R. Poyner, P. M. Sexton, GPCR modulation by RAMPs. Pharmacol. Ther. 109, 173-197 (2006).
11. L. M. McLatchie, N. J. Fraser, M. J. Main, A. Wise, J. Brown, N. Thompson, R. Solari, M. G. Lee, S. M. Foord, RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393, 333-339 (1998).
12. N. Parameswaran, W. S. Spielman, RAMPs: The past, present and future. Trends Biochem. Sci. 31, 631-638 (2006).
13. T. Bouschet, S. Martin, J. M. Henley, Receptor-activity-modifying proteins are required for forward trafficking of the calcium-sensing receptor to the plasma membrane. J. Cell Sci. 118, 4709-4720 (2005).
14. H. Saito, M. Kubota, R. W. Roberts, Q. Chi, H. Matsunami, RTP family members induce functional expression of mammalian odorant receptors. Cell 119, 679-691 (2004).
15. L. A. Metherell, J. P. Chapple, S. Cooray, A. David, C. Becker, F. Ruschendorf, D. Naville, M. Begeot, B. Khoo, P. Nurnberg, A. Huebner, M. E. Cheetham, A. J. Clark, Mutations in MRAP, encoding a new interacting partner of the ACTH receptor, cause familial glucocorticoid deficiency type 2. Nat. Genet. 37, 166-170 (2005).
16. A. J. Clark, L. McLoughlin, A. Grossman, Familial glucocorticoid deficiency associated with point mutation in the adrenocorticotropin receptor. Lancet 341, 461-462 (1993).
17. L. F. Chan, A. J. Clark, L. A. Metherell, Familial glucocorticoid deficiency: Advances in the molecular understanding of ACTH action. Horm. Res. 69, 75-82 (2008).
18. J. A. Sebag, P. M. Hinkle, Melanocortin-2 receptor accessory protein MRAP forms antiparallel homodimers. Proc. Natl. Acad. Sci. U. S. A. 104, 20244-20249 (2007).
19. J. A. Sebag, P. M. Hinkle, Regions of melanocortin 2 (MC2) receptor accessory protein necessary for dual topology and MC2 receptor trafficking and signaling. J. Biol. Chem. 284, 610-618 (2009).
20. J. A. Sebag, P. M. Hinkle, Opposite effects of the melanocortin-2 (MC2) receptor accessory protein MRAP on MC2 and MC5 receptor dimerization and trafficking. J. Biol. Chem. 284, 22641-22648 (2009).
21. T. R. Webb, L. Chan, S. N. Cooray, M. E. Cheetham, J. P. Chapple, A. J. Clark, Distinct melanocortin 2 receptor accessory protein domains are required for melanocortin 2 receptor interaction and promotion of receptor trafficking. Endocrinology 150, 720-726 (2009).
22. S. N. Cooray, I. Almiro Do Vale, K. Y. Leung, T. R. Webb, J. P. Chapple, M. Egertova, M. E. Cheetham, M. R. Elphick, A. J. Clark, The melanocortin 2 receptor accessory protein exists as a homodimer and is essential for the function of the melanocortin 2 receptor in the mouse Y1 cell line. Endocrinology 149, 1935-1941 (2008).
23. L. F. Chan, T. R. Webb, T. T. Chung, E. Meimaridou, S. N. Cooray, L. Guasti, J. P. Chapple, M. Egertova, M. R. Elphick, M. E. Cheetham, L. A. Metherell, A. J. Clark, MRAP and MRAP2 are bidirectional regulators of the melanocortin receptor family. Proc. Natl. Acad. Sci. U. S. A. 106, 6146-6151 (2009).
24. O. G. Chepurny, G. G. Holz, A novel cyclic adenosine monophosphate- responsive luciferase reporter incorporating a nonpalindromic cyclic adenosine monophosphate response element provides optimal performance for use in G protein-coupled receptor drug discovery efforts. J. Biomol. Screen. 12, 740-746 (2007).
25. A. Xu, K. L. Choi, Y. Wang, P. A. Permana, L. Y. Xu, C. Bogardus, G. J. Cooper, Identification of novel putative membrane proteins selectively expressed during adipose conversion of 3T3-L1 cells. Biochem. Biophys. Res. Commun. 293, 1161-1167 (2002).
26. T. Le, B. P. Schimmer, The regulation of MAPKs in Y1 mouse adrenocortical tumor cells. Endocrinology 142, 4282-4287 (2001).
27. C. D. Hu, Y. Chinenov, T. K. Kerppola, Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9, 789-798 (2002).
28. K. G. Mountjoy, I. M. Bird, W. E. Rainey, R. D. Cone, ACTH induces up-regulation of ACTH receptor mRNA in mouse and human adrenocortical cell lines. Mol. Cell. Endocrinol. 99, R17-R20 (1994).
29. B. P. Schimmer, M. Cordova, H. Cheng, A. Tsao, A. B. Goryachev, A. D. Schimmer, Q. Morris, Global profiles of gene expression induced by adrenocorticotropin in Y1 mouse adrenal cells. Endocrinology 147, 2357-2367 (2006).
30. S. Roy, B. Perron, N. Gallo-Payet, Role of asparagine-linked glycosylation in cell surface expression and function of the human adrenocorticotropin receptor (melanocortin 2 receptor) in 293/FRT cells. Endocrinology 151, 660-670 (2010).
31. D. Fridmanis, R. Petrovska, I. Kalnina, M. Slaidina, R. Peculis, H. B. Schiöth, J. Klovins, Identification of domains responsible for specific membrane transport and ligand specificity of the ACTH receptor (MC2R). Mol. Cell. Endocrinol., in press.
32. S. Roy, M. Rached, N. Gallo-Payet, Differential regulation of the human adrenocorticotropin receptor [melanocortin-2 receptor (MC2R)] by human MC2R accessory protein isoforms αand β in isogenic human embryonic kidney 293 cells. Mol. Endocrinol. 21, 1656-1669 (2007).
33. S. Srinivasan, C. Lubrano-Berthelier, C. Govaerts, F. Picard, P. Santiago, B. R. Conklin, C. Vaisse, Constitutive activity of the melanocortin-4 receptor is maintained by its N-terminal domain and plays a role in energy homeostasis in humans. J. Clin. Invest. 114, 1158-1164 (2004).
34. S. M. Mervine, E. A. Yost, J. L. Sabo, T. R. Hynes, C. H. Berlot, Analysis of G protein βγ dimer formation in live cells using multicolor bimolecular fluorescence complementation demonstrates preferences of β1 for particular γ subunits. Mol. Pharmacol. 70, 194-205 (2006).
35. B. W. Jones, P. M. Hinkle, β-Arrestin mediates desensitization and internalization but does not affect dephosphorylation of the thyrotropin-releasing hormone receptor. J. Biol. Chem. 280, 38346-38354 (2005).
36. B. W. Jones, G. J. Song, E. K. Greuber, P. M. Hinkle, 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 (2007).
37. -δδCT Method. Methods 25, 402-408 (2001).
38. Acknowledgments: The authors appreciate the valuable contributions of A. Jakubowski. Funding: This work was supported by NIH grant DK19974. Author contributions: Both authors made contributions to all aspects of this study. Competing interests: The authors declare no financial conflicts of interest. The University of Rochester Technology Transfer Office requires that a materials transfer agreement (MTA) be signed before the plasmids used in this study can be provided to other researchers.