Dimers of the neuropeptide Y (NPY) Y2 receptor show asymmetry in agonist affinity and association with G proteins

Journal of Receptors and Signal Transduction

Volumn 28, Issue 5, 2008, Pages 437-451

  Parker, M S ^b   Sah, R ^c   Balasubramaniam, A ^c   Sallee, F R ^c   Sweatman, T ^a   Park, E A ^a   Parker, S L ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF MEMPHIS   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Receptor dimerization; Receptor monomer; Receptor protomer

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; NEUROPEPTIDE Y2 RECEPTOR;

ARTICLE; DIMERIZATION; HUMAN; HUMAN CELL; HUMAN TISSUE; PLASMA PROTEIN BINDING; PROTEIN BINDING; PROTEIN INTERACTION; RECEPTOR SOLUBILIZATION;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; ESTRENES; GTP-BINDING PROTEINS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; MICE; PHOSPHODIESTERASE INHIBITORS; PROTEIN MULTIMERIZATION; PYRROLIDINONES; RABBITS; RECEPTORS, NEUROPEPTIDE Y;

EID: 54349104938     PISSN: 10799893     EISSN: 15324281     Source Type: Journal    
DOI: 10.1080/10799890802447423     Document Type: Article

References (44)

1. Ridge KD, Palczewski K. Visual rhodopsin sees the light: Structure and mechanism of G protein signaling. J Biol Chem 2007, 282, 9297-9301.
2. Milligan G, Smith NJ. Allosteric modulation of heterodimeric G-protein-coupled receptors. Trends Pharmacol Sci 2007, 28, 615-620.
3. Milligan G. A day in the life of a G protein-coupled receptor: The contribution to function of G protein-coupled receptor dimerization. Br J Pharmacol 2007, 147, S46-S57.
4. Baneres JL, Parello J. Structure-based analysis of GPCR function: Evidence for a novel pentameric assembly between the dimeric leukotriene B4 receptor BLT1 and the G-protein. J Mol Biol 2003, 329, 815-829.
5. Herrick-Davis K, Grinde E, Harrigan TJ, Mazurkiewicz JE. Inhibition of serotonin 5-hydroxytryptamine2c receptor function through heterodimerization: Receptor dimers bind two molecules of ligand and one G-protein. J Biol Chem 2005, 280, 40144-40151.
6. Novi F, Stanasila L, Giorgi F, Corsini GU, Cotecchia S, Maggio R. Paired activation of two components within muscarinic M3 receptor dimers is required for recruitment of beta-arrestin-1 to the plasma membrane. J Biol Chem 2005, 280, 19768-19776.
7. Park PS, Filipek S, Wells JW, Palczewski K. Oligomerization of G protein-coupled receptors: Past, present, and future. Biochemistry 2004, 43, 15643-15656.
8. Dinger MC, Bader JE, Kobor AD, Kretzschmar AK, Beck-Sickinger AG. Homodimerization of neuropeptide y receptors investigated by fluorescence resonance energy transfer in living cells. J Biol Chem 2003, 278, 10562-10571.
9. Berglund MM, Schober DA, Esterman MA, Gehlert DR. Neuropeptide Y Y4 receptor homodimers dissociate upon agonist stimulation. J Pharmacol Exp Ther 2003, 307, 1120-1126.
10. Parker MS, Berglund MM, Lundell I, Parker SL. Blockade of pancreatic polypeptide-sensitive neuropeptide Y (NPY) receptors by agonist peptides is prevented by modulators of sodium transport. Implications for receptor signaling and regulation. Peptides 2001, 22, 887-898.
11. Sah R, Balasubramaniam A, Parker MS, Sallee F, Parker SL. Neuropeptide Y as a partial agonist of the Y1 receptor. Eur J Pharmacol 2005, 525, 60-68.
12. Dautzenberg FM, Neysari S. Irreversible binding kinetics of neuropeptide Y ligands to Y2 but not to Y1 and Y5 receptors. Pharmacology 2005, 75, 21-29.
13. Hilal-Dandan R, Villegas S, Gonzalez A, Brunton LL. The quasi-irreversible nature of endothelin binding and G protein-linked signaling in cardiac myocytes. J Pharmacol Exp Ther 1997, 281, 267-273.
14. Grantcharova E, Furkert J, Reusch HP, Krell HW, Papsdorf G, Beyermann M, Schulein R, Rosenthal W, Oksche A. The extracellular N terminus of the endothelin B (ETB) receptor is cleaved by a metalloprotease in an agonist-dependent process. J Biol Chem 2002, 277, 43933-43941.
15. Brighton PJ, Szekeres PG, Wise A, Willars GB. Signaling and ligand binding by recombinant neuromedin U receptors: Evidence for dual coupling to Galphaq/11 and Galphai and an irreversible ligand-receptor interaction. Mol Pharmacol 2004, 66, 1544-1556.
16. Liang Y, Fotiadis D, Filipek S, Saperstein DA, Palczewski K, Engel A. Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. J Biol Chem 2003, 278, 21655-21662.
17. Nobles M, Benians A, Tinker A. Heterotrimeric G proteins precouple with G protein-coupled receptors in living cells. Proc Natl Acad Sci USA 2005, 102, 18706-18711.
18. Parker SL, Parker MS, Sallee FR, Balasubramaniam A. Oligomerization of neuropeptide Y (NPY) Y2 receptors in CHO cells depends on functional pertussis toxin-sensitive G-proteins. Regul Pept 2007, 144, 72-81.
19. Salahpour A, Angers S, Mercier JF, Lagace M, Marullo S, Bouvier M. Homodimerization of the beta2-adrenergic receptor as a prerequisite for cell surface targeting. J Biol Chem 2004, 279, 33390-33397.
20. Dupre DJ, Robitaille M, Ethier N, Villeneuve LR, Mamarbachi AM, Hebert TE. Seven transmembrane receptor core signaling complexes are assembled prior to plasma membrane trafficking. J Biol Chem 2006, 281, 34561-34573.
21. Pidasheva S, Grant M, Canaff L, Ercan O, Kumar U, Hendy GN. Calcium-sensing receptor dimerizes in the endoplasmic reticulum: Biochemical and biophysical characterization of CASR mutants retained intracellularly. Hum Mol Genet 2006, 15, 2200-2209.
22. Parker SL, Parker MS, Sah R, Balasubramaniam A, Sallee FR. Pertussis toxin induces parallel loss of neuropeptide Y Y(1) receptor dimers and G(i) alpha subunit function in CHO cells. Eur J Pharmacol 2008, 579, 13-25.
23. Munson PJ, Rodbard D. LIGAND: A versatile computerized approach for characterization of ligand-binding proteins. Anal Biochem 1980, 107, 220-239.
24. Parker SL, Parker MS, Estes MA, Wong YY, Sah R, Sweatman T, Park EA, Balasubramaniam A, Sallee FR. The neuropeptide Y (NPY) Y2 receptors are largely dimeric in the kidney, but monomeric in the forebrain. Journal of Receptors and Signal Transduction 2008, 28, 245-263.
25. Jastrzebska B, Maeda T, Zhu L, Fotiadis D, Filipek S, Engel A, Stenkamp RE, Palczewski K. Functional characterization of rhodopsin monomers and dimers in detergents. J Biol Chem 2004, 279, 54663-54675.
26. Grierson JP, Meldolesi J. Calcium homeostasis in mouse fibroblast cells: Affected by U-73122, a putative phospholipase C beta blocker, via multiple mechanisms. Br J Pharmacol 1995, 115, 11-14.
27. Parker SL, Parker MS, Sweatman T, Crowley WR. Characterization of G protein and phospholipase C-coupled agonist binding to the Y1 neuropeptide Y receptor in rat brain: sensitivity to G protein activators and inhibitors and to inhibitors of phospholipase C. J Pharmacol Exp Ther 1998, 286, 382-391.
28. Misra S, Murthy KS, Zhou H, Grider JR. Coexpression of Y1, Y2, and Y4 receptors in smooth muscle coupled to distinct signaling pathways. J Pharmacol Exp Ther 2004, 311, 1154-1162.
29. Ben-Zeev O, Mao HZ, Doolittle MH. Maturation of lipoprotein lipase in the endoplasmic reticulum. Concurrent formation of functional dimers and inactive aggregates. J Biol Chem2002, 277, 10727-10738.
30. Cheng HH, Xu L, Kumagai H, Simoni RD. Oligomerization state influences the degradation rate of 3-hydroxy-3-methylglutaryl-CoA reductase. J Biol Chem 1999, 274, 17171-17178.
31. Kim SK, Jacobson KA. Computational prediction of homodimerization of the A3 adenosine receptor. J Mol Graph Model 2006, 25, 549-561.
32. Alexander SP, Mathie A, Peters JA. 7TM Receptors. Br J Pharmacol 2007, 150 (Suppl 1), S4-S81.
33. Filizola M, Wang SX, Weinstein H. Dynamic models of G-protein coupled receptor dimers: Indications of asymmetry in the rhodopsin dimer from molecular dynamics simulations in a POPC bilayer. J Comput Aided Mol Des 2006, 20, 405-416.
34. Kota P, Reeves PJ, Rajbhandary UL, Khorana HG. Opsin is present as dimers in COS1 cells: Identification of amino acids at the dimeric interface. Proc Natl Acad Sci USA 2006, 103, 3054-3059.
35. Leban JJ, Heyer D, Landavazo A, Matthews J, Aulabaugh A, Daniels AJ. Novel modified carboxy terminal fragments of neuropeptide Y with high affinity for Y2-type receptors and potent functional antagonism at a Y1-type receptor. J Med Chem 1995, 38, 1150-1157.
36. Gazi L, Nickolls SA, Strange PG. Functional coupling of the human dopamine D2 receptor with G alpha i1, G alpha i2, G alpha i3 and G alpha o G proteins: Evidence for agonist regulation of G protein selectivity. Br J Pharmacol 2003, 138, 775-786.
37. Walker P, Munoz M, Martinez R, Peitsch MC. Acidic residues in extracellular loops of the human Y1 neuropeptide Y receptor are essential for ligand binding. J Biol Chem 1994, 269, 2863-2869.
38. Guo W, Shi L, Filizola M, Weinstein H, Javitch JA. Crosstalk in G protein-coupled receptors: Changes at the transmembrane homodimer interface determine activation. Proc Natl Acad Sci USA 2005, 102, 17495-17500.
39. Berthouze M, Rivail L, Lucas A, Ayoub MA, Russo O, Sicsic S, Fischmeister R, Berque-Bestel I, Jockers R, Lezoualc'h F. Two transmembrane Cys residues are involved in 5-HT4 receptor dimerization. Biochem Biophys Res Commun 2007, 356, 642-647.
40. Baker JG, Hill SJ. Multiple GPCR conformations and signalling pathways: Implications for antagonist affinity estimates. Trends Pharmacol Sci 2007, 28, 374-381.
41. Hoare SR, Sullivan SK, Schwarz DA, Ling N, Vale WW, Crowe PD, Grigoriadis DE. Ligand affinity for amino-terminal and juxtamembrane domains of the corticotropin releasing factor type I receptor: regulation by G-protein and nonpeptide antagonists. Biochemistry 2004, 43, 3996-4011.
42. Alves ID, Ciano KA, Boguslavski V, Varga E, Salamon Z, Yamamura HI, Hruby VJ, Tollin G. Selectivity, cooperativity, and reciprocity in the interactions between the delta-opioid receptor, its ligands, and G-proteins. J Biol Chem 2004, 279, 44673-44682.
43. Tobin AB. G-protein-coupled receptor phosphorylation: Where, when and by whom. Br J Pharmacol 2008, 153(Suppl 1), S167-176.
44. Whorton MR, Jastrzebska B, Park PS, Fotiadis D, Engel A, Palczewski K, Sunahara RK. Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J Biol Chem 2008, 283, 4387-4394.