Structural and functional analysis of the c-terminus of Gαq in complex with the human thromboxane A2 receptor provides evidence of constitutive activity

Biochemistry

Volumn 49, Issue 30, 2010, Pages 6365-6374

  Chillar, Annirudha ^a   Wu, Jiaxin ^a   Cervantes, Vanessa ^a   Ruan, Ke He ^a  

^a UNIVERSITY OF HOUSTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACULOVIRUS EXPRESSION SYSTEMS; BINDING AFFINITIES; C-TERMINAL DOMAINS; C-TERMINUS; CALCIUM SIGNALING; CONTROL-CELL; FLUORESCENCE BINDING; G PROTEIN; HEK293 CELLS; INTRACELLULAR CALCIUM LEVELS; LIGAND-FREE; NMR SPECTROSCOPY; PHOSPHOLIPASE C; PLATELET AGGREGATION; PURIFIED RECEPTORS; SPECTROSCOPIC STUDIES; STABLE CELL LINES;

BINDING ENERGY; CALCIUM; CELL CULTURE; FLUORESCENCE; GENE TRANSFER; LIGANDS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PLANTS (BOTANY); PURIFICATION; SIGNALING; SPECTROSCOPIC ANALYSIS;

PEPTIDES;

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; G ALPHA Q PROTEIN; G PROTEIN COUPLED RECEPTOR; THROMBOXANE A2 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; BINDING AFFINITY; BINDING ASSAY; CALCIUM SIGNALING; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; CHEMICAL INTERACTION; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; FLUORESCENCE; GENE TRANSFER; GENETIC SELECTION; HUMAN; HUMAN CELL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STABLE EXPRESSION; STRUCTURE ACTIVITY RELATION; SYNTHESIS;

15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; CALCIUM SIGNALING; CELL LINE; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, PROSTAGLANDIN; RECEPTORS, THROMBOXANE A2, PROSTAGLANDIN H2; SPECTROMETRY, FLUORESCENCE;

EID: 77955048623     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100047n     Document Type: Article

References (51)

1. Funk, C. D. (2001) Prostaglandins and leukotrienes: Advances in eicosanoid biology Science 294, 1871-1875
2. Majerus, P. W. (1983) Arachidonate metabolism in vascular disorders J. Clin. Invest. 72, 1521-1525
3. Miller, D. K., Sadowski, S., Soderman, D. D., and Kuehl, F. A., Jr. (1985) Endothelial cell prostacyclin production induced by activated neutrophils J. Biol. Chem. 260, 1006-1014
4. Negishi, M., Sugimoto, Y., and Ichikawa, A. (1995) Molecular mechanisms of diverse actions of prostanoid receptors Biochim. Biophys. Acta 1259, 109-120
5. Coleman, R. A., Kennedy, I., Humphrey, P. P. A., Bunce, K., and Kumley, P. (1990) Prostanoid and their receptor. In Comprehensive Medicinal Chemistry (Hansch, C., Sammes, P. G., Taylor, J. B., and Emmett, J. C., Eds.) Vol. 3, pp 643 - 714, Pergamon Press, Oxford, U.K.
6. Ushikubi, F., Nakajima, M., Hirata, M., Okuma, M., Fujiwara, M., and Narumiya, S. (1989) Purification of the thromboxane A2/prostaglandin H2 receptor from human blood platelets J. Biol. Chem. 264, 16496-16501
7. Hirata, M., Hayashi, Y., Ushikubi, F., Yokata, Y., Kageyama, R., Nakanishi, S., and Narumiya, S. (1991) Cloning and expression of cDNA for a human thromboxane A2 receptor Nature 349, 617-620 (Pubitemid 21912117)
8. Raychowdhury, M. K., Yukawa, M., Collins, L. J., McGrail, S. H., Kent, K. C., and Ware, J. A. (1994) Alternative splicing produces a divergent cytoplasmic tail in the human endothelial thromboxane A2 receptor J. Biol. Chem. 269, 19256-19261
9. Huang, J. S., Ramamurthy, S. K., Lin, X., and Le Breton, G. C. (2004) Cell signaling through thromboxane A2 receptors Cell. Signalling 16, 521-533
10. 2 receptor (TP) in mediating receptor: Effector coupling Biochim. Biophys. Acta 1496, 164-182
11. Kenakin, T. (2004) Principles: Receptor theory in pharmacology Trends Pharmacol. Sci. 25, 186-192
12. Kisselev, O. G., Kao, J., Ponder, J. W., Fann, Y. C., Gautam, N., and Marshall, G. R. (1998) Light-activated rhodopsin induces structural binding motif in G protein α subunit Proc. Natl. Acad. Sci. U.S.A. 95, 4270-4275
13. Tesmer, V. M., Kawano, T., Shankaranarayanan, A., Kozasa, T., and Tesmer, J. J. (2005) Snapshot of activated G proteins at the membrane: The Gαq-GRK2-Gβ complex Science 310, 1686-1690
14. Lutz, S., Shankaranarayanan, A., Coco, C., Ridilla, M., Nance, M. R., Vettel, C., Baltus, D., Evelyn, C. R., Neubig, R. R., Wieland, T., and Tesmer, J. J. (2007) Structure of Gαq-p63RhoGEF-RhoA complex reveals a pathway for the activation of RhoA by GPCRs Science 318, 1923-1927
15. Dratz, E. A., Furstenau, J. E., Lambert, C. G., Thireault, D. L., Rarick, H., Schepers, T., Pakhlevaniants, S., and Hamm, H. E. (1993) NMR structure of a receptor-bound G-protein peptide Nature 363, 276-281
16. Ridge, K. D., Marino, J. P., Ngo, T., Ramon, E., Brabazon, D. M., and Abdulaev, N. G. (2006) NMR analysis of rhodopsin-transducin interactions Vision Res. 46, 4482-4492
17. Abdulaev, N. G., Ngo, T., Zhang, C., Dinh, A., Brabazon, D. M., Ridge, K. D., and Marino, J. P. (2005) Heterotrimeric G-protein α-subunit adopts a "preactivated" conformation when associated with -subunits J. Biol. Chem. 280, 38071-38080
18. Ridge, K. D., Abdulaev, N. G., Zhang, C., Ngo, T., Brabazon, D. M., and Marino, J. P. (2006) Conformational changes associated with receptor-stimulated guanine nucleotide exchange in a heterotrimeric G-protein α-subunit: NMR analysis of GTP'S-bound states J. Biol. Chem. 281, 7635-7648
19. Piscitelli, C. L., Angel, T. E., Bailey, B. W., Hargrave, P., Dratz, E. A., and Lawrence, C. M. (2006) Equilibrium between metarhodopsin-I and metarhodopsin-II is dependent on the conformation of the third cytoplasmic loop J. Biol. Chem. 281, 6813-6825
20. Conklin, B. R., Farfel, Z., Lustig, K. D., Julius, D., and Bourne, H. R. (1993) Substitution of three amino acids switches receptor specificity of Gqα to that of Giα Nature 363, 274-276
21. Ruan, K. H., Cervantes, V., and Wu, J. (2008) A simple, quick, and high-yield preparation of the human thromboxane A2 receptor in full size for structural studies Biochemistry 47, 6819-6826
22. Hamm, H. E., Deretic, D., Arendt, A., Hargrave, P. A., Koenig, B., and Hofmann, K. P. (1998) Site of G protein binding to rhodopsin mapped with synthetic peptides from the α subunit Science 241, 832-835
23. Albrizio, S., Caliendo, G., D'errico, G., Novellino, E., Rovero, P., and D'ursi, A. M. (2005) Gα(s) protein C-terminal α-helix at the interface: Does the plasma membrane play a critical role in the Gα(s) protein functionality? J. Pept. Sci. 11, 617-626
24. Sunahara, R. K., Tesmer, J. J., Gilman, A. G., and Sprang, S. R. (1997) Crystal structure of the adenylyl cyclase activator Gsα Science 278, 1943-1947
25. s protein C-terminal region J. Pept. Sci. 8, 476-488
26. S proteins Biopolymers 54, 186-194
27. 2A adenosine receptor Mol. Pharmacol. 58, 226-236
28. Masters, S. B., Sullivan, K. A., Miller, R. T., Beiderman, B., Lopez, N. G., Ramachandran, J., and Bourne, H. R. (1988) Carboxyl terminal domain of Gsα specifies coupling of receptors to stimulation of adenylyl cyclase Science 241, 448-451
29. Rasenick, M. M., Watanabe, M., Lazarevic, M. B., Hatta, S., and Hamm, H. E. (1994) Synthetic peptides as probes for G protein function. Carboxyl-terminal Gαs peptides mimic Gs and evoke high affinity agonist binding to β-adrenergic receptors J. Biol. Chem. 269, 21519-21525
30. s carboxyl terminus J. Biol. Chem. 277, 28631-28640
31. Zhang, L., Huang, G., Wu, J., and Ruan, K. H. (2005) A profile of the residues in the first intracellular loop critical for Gs-mediated signaling of human prostacyclin receptor characterized by an integrative approach of NMR-experiment and mutagenesis Biochemistry 44, 11389-11401
32. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley, New York.
33. Lippens, R. M., Cerf, C., and Hallenga, K. (1992) Theory and experimental results of transfer-NOE experiments. The influence of the off rate versus cross-relaxation rates J. Magn. Reson. 99, 268-281
34. Landy, S. B. and Rao, B. D. N. (1989) Dynamical NOE in multiple-spin systems undergoing chemical exchange J. Magn. Reson. 81, 371-377
35. Ruan, K. H., Wu, J., and Wang, L. H. (2005) Solution structure of a common substrate mimetic of cyclooxygenase-downstream synthases bound to an engineered thromboxane A2 synthase using a high-resolution NMR technique Arch. Biochem. Biophys. 444, 165-173
36. Ruan, K. H., Wu, J., and Cervantes, V. (2008) Characterization of the substrate mimic bound to engineered prostacyclin synthase in solution using high-resolution NMR spectroscopy and mutagenesis: Implication of the molecular mechanism in biosynthesis of prostacyclin Biochemistry 47, 680-688
37. Callihan, D., West, J., Kumar, S., Schweitzer, B. I., and Logan, T. M. (1996) Simple, distortion-free homonuclear spectra of peptides and nucleic acids in water using excitation sculpting J. Magn. Reson., Ser. B 112, 82-85
38. Marion, D., Ikura, M., Tschudin, R., and Bax, A. (1989) Rapid recording of 2D NMR spectra withoutphase cycling. Application to the study of hydrogen exchange in proteins J. Magn. Reson. 85, 393-399
39. Ruan, K. H., Deng, H., and So, S. P. (2006) Engineering of a protein with cyclooxygenase and prostacyclin synthase activities that converts arachidonic acid to prostacyclin Biochemistry 45, 14003-14011
40. Gilchrist, A., Vanhauwe, J. F., Li, A., Thomas, T. O., Voyno-Yasenetskaya, T., and Hamm, H. E. (2001) Gα minigenes expressing C-terminal peptides serve as specific inhibitors of thrombin-mediated endothelial activation J. Biol. Chem. 276, 25672-25679
41. Ruan, K. H., So, S. P., Cervantes, V., Wu, H., Wijaya, C., and Jentzen, R. R. (2008) An active triple-catalytic hybrid enzyme engineered by linking cyclo-oxygenase isoform-1 to prostacyclin synthase that can constantly biosynthesize prostacyclin, the vascular protector FEBS J. 275, 5820-5829
42. Pinto, A., Gillard, S., Moss, F., Whyte, K., Brust, P., Williams, M., Stauderman, K., Harpold, M., Lang, B., Newsom-Davis, J., Bleakman, D., Lodge, D., and Boot, J. (1998) Human autoantibodies specific for the a1A calcium channel subunit reduce both P-type and Q-type calcium currents in cerebellar neurons Proc. Natl. Acad. Sci. U.S.A. 95, 8328-8333
43. Kao, J. P., Harootunian, A. T., and Tsien, R. Y. (1989) Photochemically Generated Cytosolic Calcium Pulses and Their Detection by Fluo-3 J. Biol. Chem. 264, 8179-8184
44. Huang, J., Hamasaki, T., and Ozoe, Y. (2009) Pharmacological characterization of a Bombyx mori α-adrenergic-like octopamine receptor stably expressed in a mammalian cell line Arch. Insect Biochem. Physiol. 73, 74-86
45. De Lean, A., Stadel, J. M., and Lefkowitz, R. J. (1980) A ternary complex model explains the agonist-specific binding properties of the adenylate cyclase-coupled β-adrenergic receptor J. Biol. Chem. 255, 7108-7117
46. Costa, T. and Herz, A. (1989) Antagonists with negative intrinsic activity at δ opioid receptors coupled to GTP-binding proteins Proc. Natl. Acad. Sci. U.S.A. 86, 7321-7325
47. Samama, P., Cotecchia, S., Costa, T., and Lefkowitz, R. J. (1993) A mutation-induced activated state of the β2-adrenergic receptor. Extending the ternary complex model J. Biol. Chem. 26, 4625-4636
48. 3H-Naloxone benzoylhydrazone binding in MOR-1-transfected Chinese hamster ovary cells: Evidence for G-protein-dependent antagonist binding J. Pharmacol. Exp. Ther. 286, 376-381
49. Cherezov, V., Rosenbaum, D. M., Hanson, M. A., Rasmussen, S. G., Thian, F. S., Kobilka, T. S., Choi, H. J., Kuhn, P., Weis, W. I., Kobilka, B. K., and Stevens, R. C. (2007) High-resolution crystal structure of an engineered human β2-adrenergic G protein-coupled receptor Science 318, 1258-1265
50. Rasmussen, S. G., Choi, H. J., Rosenbaum, D. M., Kobilka, T. S., Thian, F. S., Edwards, P. C., Burghammer, M., Ratnala, V. R., Sanishvili, R., Fischetti, R. F., Schertler, G. F., Weis, W. I., and Kobilka, B. K. (2007) Crystal structure of the human β2 adrenergic G-protein-coupled receptor Nature 450, 383-387
51. 2+-indicator dyes Cell Calcium 27, 97-106