Rapid-mix flow cytometry measurements of subsecond regulation of G protein-coupled receptor ternary complex dynamics by guanine nucleotides

Analytical Biochemistry

Volumn 371, Issue 1, 2007, Pages 10-20

  Wu, Yang ^a,b   Buranda, Tione ^a   Simons, Peter C ^a   Lopez, Gabriel P ^b   McIntire, William E ^c   Garrison, James C ^c   Prossnitz, Eric R ^a   Sklar, Larry A ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^b University of New Mexico   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Detergent solubilized receptors; Dissociation kinetics; G protein coupled receptor; Guanine nucleotide; Rapid mix flow cytometer

Indexed keywords

CHEMICAL ACTIVATION; DISSOCIATION; FLOW CYTOMETRY; PEPTIDES; POSITIVE IONS;

DISSOCIATION KINETICS; FLOW-CYTOMETER; FORMYL PEPTIDE RECEPTOR; G PROTEIN COUPLED RECEPTORS; GREEN FLUORESCENT PROTEIN FUSION; GUANINE NUCLEOTIDES; TERNARY COMPLEX; TIME RESOLUTION;

NUCLEOTIDES;

GLUCORECEPTOR; GREEN FLUORESCENT PROTEIN; GUANINE NUCLEOTIDE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; TERNARY COMPLEX FACTOR;

ARTICLE; CELL ACTIVATION; CELL STRAIN U937; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

EID: 34548399654     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2007.08.011     Document Type: Article

References (55)

1. Robishaw J.D., and Berlot C.H. Translating G protein subunit diversity into functional specificity. Curr. Opin. Cell Biol. 16 (2004) 206-209
2. Venter J.C., Adams M.D., Myers E.W., Li P.W., Mural R.J., et al. The sequence of the human genome. Science 291 (2001) 1304-1351
3. Hamm H.E. How activated receptors couple to G proteins. Proc. Natl. Acad. Sci. USA 98 (2001) 4819-4821
4. Cabrera-Vera T.M., Vanhauwe J., Thomas T.O., Medkova M., Preininger A., et al. Insights into G protein structure, function, and regulation. Endocrine Rev. 24 (2003) 765-781
5. Klein S., Reuveni H., and Levitzki A. Signal transduction by a nondissociable heterotrimeric yeast G protein. Proc. Natl. Acad. Sci. USA 97 (2000) 3219-3223
6. Levitzki A., and Klein S. G-protein subunit dissociation is not an integral part of G-protein action. Chembiochem 3 (2002) 815-818
7. Hoffmann C., Gaietta G., Bunemann M., Adams S.R., Oberdorff-Maass S., et al. A FlAsH-based FRET approach to determine G protein-coupled receptor activation in living cells. Nat. Methods 2 (2005) 171-176
8. Frank M., Thumer L., Lohse M.J., and Bunemann M. G protein activation without subunit dissociation depends on a G alpha(i)-specific region. J. Biol. Chem. 280 (2005) 24584-24590
9. Bunemann M., Frank M., and Lohse M.J. Gi protein activation in intact cells involves subunit rearrangement rather than dissociation. Proc. Natl. Acad. Sci. USA 100 (2003) 16077-16082
10. Gao J.L., Becker E.L., Freer R.J., Muthukumaraswamy N., and Murphy P.M. A high potency nonformylated peptide agonist for the phagocyte N -formylpeptide chemotactic receptor. J. Exp. Med. 180 (1994) 2191-2197
11. Prossnitz E.R., and Ye R.D. The N -formyl peptide receptor: a model for the study of chemoattractant receptor structure and function. Pharmacol. Ther. 74 (1997) 73-102
12. Bennett T.A., Key T.A., Gurevich V.V., Neubig R., Prossnitz E.R., et al. Real-time analysis of G protein-coupled receptor reconstitution in a solubilized system. J. Biol. Chem. 276 (2001) 22453-22460
13. Simons P.C., Shi M., Foutz T., Cimino D.F., Lewis J., et al. Ligand-receptor-G-protein molecular assemblies on beads for mechanistic studies and screening by flow cytometry. Mol. Pharmacol. 64 (2003) 1227-1238
14. Simons P.C., Biggs S.M., Waller A., Foutz T., Cimino D.F., et al. Real-time analysis of ternary complex on particles: direct evidence for partial agonism at the agonist-receptor-G-protein complex assembly step of signal transduction. J. Biol. Chem. 279 (2004) 13514-13521
15. Kenakin T. Efficacy at G-protein-coupled receptors. Nat. Rev. Drug Discov. 1 (2002) 103-110
16. Buranda T., Jones G., Nolan J., Keij J., Lopez G.P., et al. Ligand receptor dynamics at streptavidin coated particle surfaces: a flow cytometric and spectrofluorimetric study. J. Phys. Chem. B 103 (1999) 3399-3410
17. Graves S.W., Nolan J.P., Jett J.H., Martin J.C., and Sklar L.A. Nozzle design parameters and their effects on rapid sample delivery in flow cytometry. Cytometry 47 (2002) 127-137
18. Wu Y., Zwartz G., Lopez G.P., Sklar L.A., and Buranda T. Small-volume rapid-mix device for subsecond kinetic analysis in flow cytometry. Cytometry Part A 67A (2005) 37-44
19. Hein P., Frank M., Hoffmann C., Lohse M.J., and Bunemann M. Dynamics of receptor/G protein coupling in living cells. EMBO J. 24 (2005) 4106-4114
20. McIntire W.E., MacCleery G., and Garrison J.C. The G protein beta subunit is a determinant in the coupling of G(s) to the beta(1)-adrenergic and A2a adenosine receptors. J. Biol. Chem. 276 (2001) 15801-15809
21. Shi M., Bennett T.A., Cimino D.F., Maestas D.C., Foutz T.D., et al. Functional capabilities of an N -formyl peptide receptor-G(alpha i2) fusion protein: assemblies with G proteins and arrestins. Biochemistry 42 (2003) 7283-7293
22. Buranda T., Lopez G.P., Simons P., Pastuszyn A., and Sklar L.A. Detection of epitope-tagged proteins in flow cytometry: fluorescence resonance energy transfer-based assays on beads with femtomole resolution. Anal. Biochem. 298 (2001) 151-162
23. McIntire W.E., Myung C.S., MacCleery G., Wang Q., and Garrison J.C. Reconstitution of G protein-coupled receptors with recombinant G protein alpha and beta gamma subunits. G Protein Pathways Pt. A Receptors 343 (2002) 372-393
24. Buranda T., Waller A., Wu Y., Simons P., Biggs S.M., et al. Some mechanistic insights into GPCR activation from detergent solubilized ternary complexes on beads. In: Sprang S.R. (Ed). Advances in Protein Chemistry Vol. 74 (2007), Elsevier, San Diego 96-135
25. Wu Y., Campos S.K., Lopez G.P., Ozbun M.A., Sklar L.A., et al. The development of quantum dot calibration beads and quantitative multicolor bioassays in flow cytometry and microscopy. Anal. Biochem. 364 (2007) 180-192
26. Sarvazyan N.A., Remmers A.E., and Neubig R.R. Determinants of G(i1)alpha and beta gamma binding : measuring high affinity interactions in a lipid environment using flow cytometry. J. Biol. Chem. 273 (1998) 7934-7940
27. 2+ "lock" after GTP/GDP exchange. Biochemistry 40 (2001) 9647-9656
28. Goody R., Frech M., and Wittinghofer A. Affinity of guanine nucleotide binding-proteins for their ligands: facts and artifacts. Trends Biochem. Sci. 16 (1991) 32-328
29. Coleman D.E., Berghuis A.M., Lee E., Linder M.E., Gilman A.G., et al. Structures of active conformations of G(I-Alpha-1) and the mechanism of GTP hydrolysis. Science 265 (1994) 1405-1412
30. Noel J.P., Hamm H.E., and Sigler P.B. The 2.2-angstrom crystal-structure of transducin-alpha complexed with GTP-gamma-S. Nature 366 (1993) 654-663
31. Bigay J., Deterre P., Pfister C., and Chabre M. Fluoroaluminates activate transducin-Gdp by mimicking the gamma-phosphate of Gtp in its binding-site. FEBS Lett. 191 (1985) 181-185
32. Tesmer J.J.G., Berman D.M., Gilman A.G., and Sprang S.R. Structure of RGS4 bound to AlF4-activated G(i alpha 1): stabilization of the transition state for GTP hydrolysis. Cell 89 (1997) 251-261
33. Hamm H.E. The many faces of G protein signaling. J. Biol. Chem. 273 (1998) 669-672
34. Davis T.L., Bonacci T.M., Sprang S.R., and Smrcka A.V. Structural and molecular characterization of a preferred protein interaction surface on G protein beta gamma subunits. Biochemistry 44 (2005) 10593-10604
35. Tesmer V.M., Kawano T., Shankaranarayanan A., Kozasa T., and Tesmer J.J.G. Snapshot of activated G proteins at the membrane: the G alpha(q)-GRK2-G beta gamma complex. Science 310 (2005) 1686-1690
36. Cherfils J., and Chabre M. Activation of G-protein G alpha subunits by receptors through G alpha-G beta and G alpha-G gamma interactions. Trends Biochem. Sci. 28 (2003) 13-17
37. Nanoff C., Koppensteiner R., Yang Q., Fuerst E., Ahorn H., et al. The carboxyl terminus of the G alpha-subunit is the latch for triggered activation of heterotrimeric G proteins. Mol. Pharmacol. 69 (2006) 397-405
38. Rebois R.V., Warner D.R., and Basi N.S. Does subunit dissociation necessarily accompany the activation of all heterotrimeric G proteins?. Cell. Signal. 9 (1997) 141-151
39. Rebois R.V., and Hebert T.E. Protein complexes involved in heptahelical receptor-mediated signal transduction. Recept. Channels 9 (2003) 169-194
40. Ridge K.D., Abdulaev N.G., Zhang C., Ngo T., Brabazon D.M., et al. Conformational changes associated with receptor-stimulated guanine nucleotide exchange in a heterotrimeric G-protein alpha-subunit: NMR analysis of GTP gamma S-bound states. J. Biol. Chem. 281 (2006) 7635-7648
41. Lambright D.G., Sondek J., Bohm A., Skiba N.P., Hamm H.E., et al. The 2.0 angstrom crystal structure of a heterotrimeric G protein. Nature 379 (1996) 311-319
42. Sprang S.R. G protein mechanisms: insights from structural analysis. Annu. Rev. Biochem. 66 (1997) 639-678
43. Rondard P., Iiri T., Srinivasan S., Meng E., Fujita T., et al. Mutant G protein alpha subunit activated by G beta gamma: a model for receptor activation?. Proc. Natl. Acad. Sci. USA 98 (2001) 6150-6155
44. Abbott A.J., and Nelsestuen G.L. The collisional limit: an important consideration for membrane-associated enzymes and receptors. FASEB J 2 (1988) 2858-2866
45. Christopoulos A., and Kenakin T. G protein-coupled receptor allosterism and complexing. Pharmacol. Rev. 54 (2002) 323-374
46. Shea L.D., Omann G.M., and Linderman J.J. Calculation of diffusion-limited kinetics for the reactions in collision coupling and receptor cross-linking. Biophys J. 73 (1997) 2949-2959
47. Neubig R.R. Membrane organization in G-protein mechanisms. FASEB J. 8 (1994) 939-946
48. Head B.P., Patel H.H., Roth D.M., Lai N.C., Niesman I.R., et al. G-protein-coupled receptor signaling components localize in both sarcolemmal and intracellular caveolin-3-associated microdomains in adult cardiac myocytes. J. Biol. Chem. 280 (2005) 31036-31044
49. Gross W., and Lohse M.J. Mechanism of activation of A2 adenosine receptors: 2. A restricted collision-coupling model of receptor-effector interaction. Mol. Pharmacol. 39 (1991) 524-530
50. Vetter I.R., and Wittinghofer A. Signal transduction: the guanine nucleotide-binding switch in three dimensions. Science 294 (2001) 1299-1304
51. Vauquelin G., and Liefde I.V. G protein-coupled receptors: a count of 1001 conformations. Fundam. Clin. Pharmacol. 19 (2005) 45-56
52. Kimura N., and Shimada N. GDP does not mediate but rather inhibits hormonal signal to adenylate-cyclase. J. Biol. Chem. 258 (1983) 2278-2283
53. Kikkawa S., Takahashi K., Takahashi K., Shimada N., Ui M., et al. Kinase on the GTP-binding proteins. J. Biol. Chem. 265 (1990) 21536-21540
54. Ugur O., Oner S., Molinari P., Ambrosio C., Sayar K., et al. Guanine nucleotide exchange-independent activation of G(s) protein by beta(2)-adrenoceptor. Mol. Pharm. 68 (2005) 720-728
55. Sunahara R.K., Dessauer C.W., Whisnant R.E., Kleuss C., and Gilman A.G. Interaction of Gsa with the cytosolic domains of mammalian adenylyl cyclase. J. Biol. Chem. 272 (1997) 22265-22271