Fluorescent protein complementation assays: New tools to study G protein-coupled receptor oligomerization and GPCR-mediated signaling

Molecular and Cellular Endocrinology

Volumn 331, Issue 2, 2011, Pages 185-193

  Vidi, Pierre Alexandre ^a   Ejendal, Karin F K ^b   Przybyla, Julie A ^b   Watts, Val J ^b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

BiFC; Dimerization; Fluorescence; G protein coupled receptor; Imaging; Signaling

Indexed keywords

ADENOSINE A2A RECEPTOR; ADENYLATE CYCLASE; CALCITONIN RECEPTOR LIKE RECEPTOR; DOPAMINE 2 RECEPTOR; G PROTEIN COUPLED RECEPTOR; RECEPTOR ACTIVITY MODIFYING PROTEIN;

CELL MEMBRANE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; DIMERIZATION; FLUORESCENCE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT PROTEIN COMPLEMENTATION ASSAY; HIGH THROUGHPUT SCREENING; HUMAN; MOLECULAR DYNAMICS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE; FLUORESCENCE; GENETIC COMPLEMENTATION TEST; HUMANS; LUMINESCENT MEASUREMENTS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 78650270722     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.07.011     Document Type: Review

References (94)

1. Antonelli T., Fuxe K., Agnati L., Mazzoni E., Tanganelli S., Tomasini M.C., Ferraro L. Experimental studies and theoretical aspects on A2A/D2 receptor interactions in a model of Parkinson's disease. Relevance for L-dopa induced dyskinesias. J. Neurol. Sci. 2006, 248:16-22.
2. Armstrong D., Strange P.G. Dopamine D2 receptor dimer formation: evidence from ligand binding. J. Biol. Chem. 2001, 276:22621-22629.
3. Baragli A., Grieco M.L., Trieu P., Villeneuve L.R., Hebert T.E. Heterodimers of adenylyl cyclases 2 and 5 show enhanced functional responses in the presence of Galpha s. Cell. Signal. 2008, 20:480-492.
4. Bulenger S., Marullo S., Bouvier M. Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol. Sci. 2005, 26:131-137.
5. Cabello N., Gandia J., Bertarelli D.C., Watanabe M., Lluis C., Franco R., Ferre S., Lujan R., Ciruela F. Metabotropic glutamate type 5, dopamine D2 and adenosine A2a receptors form higher-order oligomers in living cells. J. Neurochem. 2009, 109:1497-1507.
6. Canals M., Burgueno J., Marcellino D., Cabello N., Canela E.I., Mallol J., Agnati L., Ferre S., Bouvier M., Fuxe K., Ciruela F., Lluis C., Franco R. Homodimerization of adenosine A2A receptors: qualitative and quantitative assessment by fluorescence and bioluminescence energy transfer. J. Neurochem. 2004, 88:726-734.
7. Canals M., Marcellino D., Fanelli F., Ciruela F., de Benedetti P., Goldberg S.R., Neve K., Fuxe K., Agnati L.F., Woods A.S., Ferre S., Lluis C., Bouvier M., Franco R. Adenosine A2A-dopamine D2 receptor-receptor heteromerization: qualitative and quantitative assessment by fluorescence and bioluminescence energy transfer. J. Biol. Chem. 2003, 278:46741-46749.
8. Cao X., Liang L., Hadcock J.R., Iredale P.A., Griffith D.A., Menniti F.S., Factor S., Greenamyre J.T., Papa S.M. Blockade of cannabinoid type 1 receptors augments the antiparkinsonian action of levodopa without affecting dyskinesias in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated rhesus monkeys. J. Pharmacol. Exp. Ther. 2007, 323:318-326.
9. Carriba P., Navarro G., Ciruela F., Ferre S., Casado V., Agnati L., Cortes A., Mallol J., Fuxe K., Canela E.I., Lluis C., Franco R. Detection of heteromerization of more than two proteins by sequential BRET-FRET. Nat. Methods 2008, 5:727-733.
10. 2+ channel Cav1.2. Science 2001, 293:98-101.
11. Dessauer C.W. Adenylyl cyclase - a-kinase anchoring protein complexes: the next dimension in cAMP signaling. Mol. Pharmacol. 2009, 76:935-941.
12. Ding Z., Liang J., Lu Y., Yu Q., Songyang Z., Lin S.Y., Mills G.B. A retrovirus-based protein complementation assay screen reveals functional AKT1-binding partners. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:15014-15019.
13. Dupre D.J., Robitaille M., Rebois R.V., Hebert T.E. The role of Gbetagamma subunits in the organization, assembly, and function of GPCR signaling complexes. Annu. Rev. Pharmacol. Toxicol. 2009, 49:31-56.
14. Eglen R.M. Enzyme fragment complementation: a flexible high throughput screening assay technology. Assay Drug Dev. Technol. 2002, 1:97-104.
15. Eglen R.M. Assessing GPCR activation using protein complementation: a novel technique for HTS. Biochem. Soc. Trans. 2007, 35:746-748.
16. Fan J.Y., Cui Z.Q., Wei H.P., Zhang Z.P., Zhou Y.F., Wang Y.P., Zhang X.E. Split mCherry as a new red bimolecular fluorescence complementation system for visualizing protein-protein interactions in living cells. Biochem. Biophys. Res. Commun. 2008, 367:47-53.
17. Ferre S., Goldberg S.R., Lluis C., Franco R. Looking for the role of cannabinoid receptor heteromers in striatal function. Neuropharmacology 2009, 56(Suppl. 1):226-234.
18. Fuxe K., Canals M., Torvinen M., Marcellino D., Terasmaa A., Genedani S., Leo G., Guidolin D., Diaz-Cabiale Z., Rivera A., Lundstrom L., Langel U., Narvaez J., Tanganelli S., Lluis C., Ferre S., Woods A., Franco R., Agnati L.F. Intramembrane receptor-receptor interactions: a novel principle in molecular medicine. J. Neural Transm. 2007, 114:49-75.
19. Galperin E., Verkhusha V.V., Sorkin A. Three-chromophore FRET microscopy to analyze multiprotein interactions in living cells. Nat. Methods 2004, 1:209-217.
20. Gandia J., Galino J., Amaral O.B., Soriano A., Lluis C., Franco R., Ciruela F. Detection of higher-order G protein-coupled receptor oligomers by a combined BRET-BiFC technique. FEBS Lett. 2008, 582:2979-2984.
21. Gazi L., Lopez-Gimenez J.F., Rudiger M.P., Strange P.G. Constitutive oligomerization of human D2 dopamine receptors expressed in Spodoptera frugiperda 9 (Sf9) and in HEK293 cells. Analysis using co-immunoprecipitation and time-resolved fluorescence resonance energy transfer. Eur. J. Biochem. 2003, 270:3928-3938.
22. Giese B., Roderburg C., Sommerauer M., Wortmann S.B., Metz S., Heinrich P.C., Muller-Newen G. Dimerization of the cytokine receptors gp130 and LIFR analysed in single cells. J. Cell Sci. 2005, 118:5129-5140.
23. Glass M., Felder C.C. Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors augments cAMP accumulation in striatal neurons: evidence for a Gs linkage to the CB1 receptor. J. Neurosci. 1997, 17:5327-5333.
24. Gu C., Cali J.J., Cooper D.M. Dimerization of mammalian adenylate cyclases. Eur. J. Biochem. 2002, 269:413-421.
25. Guo W., Shi L., Filizola M., Weinstein H., Javitch J.A. Crosstalk in G protein-coupled receptors: changes at the transmembrane homodimer interface determine activation. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17495-17500.
26. Guo W., Urizar E., Kralikova M., Mobarec J.C., Shi L., Filizola M., Javitch J.A. Dopamine D2 receptors form higher order oligomers at physiological expression levels. EMBO J. 2008, 27:2293-2304.
27. Gurevich V.V., Gurevich E.V., Cleghorn W.M. Arrestins as multi-functional signaling adaptors. Handb. Exp. Pharmacol. 2008, 15-37.
28. Hacker B.M., Tomlinson J.E., Wayman G.A., Sultana R., Chan G., Villacres E., Disteche C., Storm D.R. Cloning, chromosomal mapping, and regulatory properties of the human type 9 adenylyl cyclase (ADCY9). Genomics 1998, 50:97-104.
29. Heroux M., Hogue M., Lemieux S., Bouvier M. Functional calcitonin gene-related peptide receptors are formed by the asymmetric assembly of a calcitonin receptor-like receptor homo-oligomer and a monomer of receptor activity-modifying protein-1. J. Biol. Chem. 2007, 282:31610-31620.
30. Hillion J., Canals M., Torvinen M., Casado V., Scott R., Terasmaa A., Hansson A., Watson S., Olah M.E., Mallol J., Canela E.I., Zoli M., Agnati L.F., Ibanez C.F., Lluis C., Franco R., Ferre S., Fuxe K. Coaggregation, cointernalization, and codesensitization of adenosine A2A receptors and dopamine D2 receptors. J. Biol. Chem. 2002, 277:18091-18097.
31. Hu C.D., Chinenov Y., Kerppola T.K. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 2002, 9:789-798.
32. Hu C.D., Grinberg A.V., Kerppola T.K. Visualization of protein interactions in living cells using bimolecular fluorescence complementation (BiFC) analysis. Curr. Protoc. Cell Biol. 2006, (Chapter 21, Unit 21 3).
33. Hu C.D., Kerppola T.K. Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat. Biotechnol. 2003, 21:539-545.
34. Hynes T.R., Mervine S.M., Yost E.A., Sabo J.L., Berlot C.H. Live cell imaging of Gs and the beta2-adrenergic receptor demonstrates that both alphas and beta1gamma7 internalize upon stimulation and exhibit similar trafficking patterns that differ from that of the beta2-adrenergic receptor. J. Biol. Chem. 2004, 279:44101-44112.
35. Hynes T.R., Yost E., Mervine S., Berlot C.H. Multicolor BiFC analysis of competition among G protein beta and gamma subunit interactions. Methods 2008, 45:207-213.
36. Jarrahian A., Watts V.J., Barker E.L. D2 dopamine receptors modulate Galpha-subunit coupling of the CB1 cannabinoid receptor. J. Pharmacol. Exp. Ther. 2004, 308:880-886.
37. Johnston C.A., Beazely M.A., Bilodeau M.L., Andrisani O., Watts V.J. Differentiation-induced alterations in cyclic AMP signaling in the Cath: differentiated (CAD) neuronal cell line. J. Neurochem. 2004, 88:1497-1508.
38. Kamiya T., Saitoh O., Yoshioka K., Nakata H. Oligomerization of adenosine A2A and dopamine D2 receptors in living cells. Biochem. Biophys. Res. Commun. 2003, 306:544-549.
39. Kearn C.S., Blake-Palmer K., Daniel E., Mackie K., Glass M. Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: a mechanism for receptor cross-talk?. Mol. Pharmacol. 2005, 67:1697-1704.
40. Kerppola T.K. Visualization of molecular interactions by fluorescence complementation. Nat. Rev. Mol. Cell Biol. 2006, 7:449-456.
41. Lavine N., Ethier N., Oak J.N., Pei L., Liu F., Trieu P., Rebois R.V., Bouvier M., Hebert T.E., Van Tol H.H. G protein-coupled receptors form stable complexes with inwardly rectifying potassium channels and adenylyl cyclase. J. Biol. Chem. 2002, 277:46010-46019.
42. Lee S.P., O'Dowd B.F., Ng G.Y., Varghese G., Akil H., Mansour A., Nguyen T., George S.R. Inhibition of cell surface expression by mutant receptors demonstrates that D2 dopamine receptors exist as oligomers in the cell. Mol. Pharmacol. 2000, 58:120-128.
43. Lee S.P., O'Dowd B.F., Rajaram R.D., Nguyen T., George S.R. D2 dopamine receptor homodimerization is mediated by multiple sites of interaction, including an intermolecular interaction involving transmembrane domain 4. Biochemistry 2003, 42:11023-11031.
44. Lin M.Z., McKeown M.R., Ng H.L., Aguilera T.A., Shaner N.C., Campbell R.E., Adams S.R., Gross L.A., Ma W., Alber T., Tsien R.Y. Autofluorescent proteins with excitation in the optical window for intravital imaging in mammals. Chem. Biol. 2009, 16:1169-1179.
45. Lopez-Gimenez J.F., Canals M., Pediani J.D., Milligan G. The alpha1b-adrenoceptor exists as a higher-order oligomer: effective oligomerization is required for receptor maturation, surface delivery, and function. Mol. Pharmacol. 2007, 71:1015-1029.
46. MacDonald M.L., Lamerdin J., Owens S., Keon B.H., Bilter G.K., Shang Z., Huang Z., Yu H., Dias J., Minami T., Michnick S.W., Westwick J.K. Identifying off-target effects and hidden phenotypes of drugs in human cells. Nat. Chem. Biol. 2006, 2:329-337.
47. Marcellino D., Carriba P., Filip M., Borgkvist A., Frankowska M., Bellido I., Tanganelli S., Muller C.E., Fisone G., Lluis C., Agnati L.F., Franco R., Fuxe K. Antagonistic cannabinoid CB1/dopamine D2 receptor interactions in striatal CB1/D2 heteromers. A combined neurochemical and behavioral analysis. Neuropharmacology 2008, 54:815-823.
48. Marullo S., Bouvier M. Resonance energy transfer approaches in molecular pharmacology and beyond. Trends Pharmacol. Sci. 2007, 28:362-365.
49. McIntire W.E. Structural determinants involved in the formation and activation of G protein betagamma dimers. Neurosignals 2009, 17:82-99.
50. McLatchie L.M., Fraser N.J., Main M.J., Wise A., Brown J., Thompson N., Solari R., Lee M.G., Foord S.M. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 1998, 393:333-339.
51. Mercier J.F., Salahpour A., Angers S., Breit A., Bouvier M. Quantitative assessment of beta 1- and beta 2-adrenergic receptor homo- and heterodimerization by bioluminescence resonance energy transfer. J. Biol. Chem. 2002, 277:44925-44931.
52. Mervine S.M., Yost E.A., Sabo J.L., Hynes T.R., Berlot C.H. Analysis of G protein betagamma dimer formation in live cells using multicolor bimolecular fluorescence complementation demonstrates preferences of beta1 for particular gamma subunits. Mol. Pharmacol. 2006, 70:194-205.
53. Milligan G. G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function. Br. J. Pharmacol. 2009, 158:5-14.
54. Milligan G., Bouvier M. Methods to monitor the quaternary structure of G protein-coupled receptors. FEBS J. 2005, 272:2914-2925.
55. Morell M., Espargaro A., Aviles F.X., Ventura S. Study and selection of in vivo protein interactions by coupling bimolecular fluorescence complementation and flow cytometry. Nat. Protoc. 2008, 3:22-33.
56. Morelli M., Di Paolo T., Wardas J., Calon F., Xiao D., Schwarzschild M.A. Role of adenosine A2A receptors in parkinsonian motor impairment and l-DOPA-induced motor complications. Prog. Neurobiol. 2007, 83:293-309.
57. Nagai T., Ibata K., Park E.S., Kubota M., Mikoshiba K., Miyawaki A. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 2002, 20:87-90.
58. Navarro G., Carriba P., Gandia J., Ciruela F., Casado V., Cortes A., Mallol J., Canela E.I., Lluis C., Franco R. Detection of heteromers formed by cannabinoid CB1, dopamine D2, and adenosine A2A G-protein-coupled receptors by combining bimolecular fluorescence complementation and bioluminescence energy transfer. ScientificWorldJournal 2008, 8:1088-1097.
59. Nimchinsky E.A., Hof P.R., Janssen W.G., Morrison J.H., Schmauss C. Expression of dopamine D3 receptor dimers and tetramers in brain and in transfected cells. J. Biol. Chem. 1997, 272:29229-29237.
60. Park P.S., Wells J.W. Oligomeric potential of the M2 muscarinic cholinergic receptor. J. Neurochem. 2004, 90:537-548.
61. Paulmurugan R., Gambhir S.S. Combinatorial library screening for developing an improved split-firefly luciferase fragment-assisted complementation system for studying protein-protein interactions. Anal. Chem. 2007, 79:2346-2353.
62. Pin J.P., Neubig R., Bouvier M., Devi L., Filizola M., Javitch J.A., Lohse M.J., Milligan G., Palczewski K., Parmentier M., Spedding M. International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers. Pharmacol. Rev. 2007, 59:5-13.
63. Pontier S.M., Percherancier Y., Galandrin S., Breit A., Gales C., Bouvier M. Cholesterol-dependent separation of the beta2-adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction. J. Biol. Chem. 2008, 283:24659-24672.
64. Przybyla J.A., Watts V.J. Ligand-induced regulation and localization of cannabinoid CB1 and dopamine D2L receptor heterodimers. J. Pharmacol. Exp. Ther. 2010, 332:710-719.
65. Rebois R.V., Robitaille M., Gales C., Dupre D.J., Baragli A., Trieu P., Ethier N., Bouvier M., Hebert T.E. Heterotrimeric G proteins form stable complexes with adenylyl cyclase and Kir3.1 channels in living cells. J. Cell Sci. 2006, 119:2807-2818.
66. Rebois R.V., Robitaille M., Petrin D., Zylbergold P., Trieu P., Hebert T.E. Combining protein complementation assays with resonance energy transfer to detect multipartner protein complexes in living cells. Methods 2008, 45:214-218.
67. Remy I., Michnick S.W. A highly sensitive protein-protein interaction assay based on Gaussia luciferase. Nat. Methods 2006, 3:977-979.
68. Rizzo M.A., Springer G.H., Granada B., Piston D.W. An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 2004, 22:445-449.
69. Rowe L., Dikici E., Daunert S. Engineering bioluminescent proteins: expanding their analytical potential. Anal. Chem. 2009, 81:8662-8668.
70. Sadana R., Dascal N., Dessauer C.W. N terminus of type 5 adenylyl cyclase scaffolds gs heterotrimer. Mol. Pharmacol. 2009, 76:1256-1264.
71. Schwarzschild M.A., Agnati L., Fuxe K., Chen J.F., Morelli M. Targeting adenosine A2A receptors in Parkinson's disease. Trends Neurosci. 2006, 29:647-654.
72. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N., Palmer A.E., Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 2004, 22:1567-1572.
73. Sharma S.K., Klee W.A., Nirenberg M. Dual regulation of adenylate cyclase accounts for narcotic dependence and tolerance. Proc. Natl. Acad. Sci. U.S.A. 1975, 72:3092-3096.
74. Shu X., Royant A., Lin M.Z., Aguilera T.A., Lev-Ram V., Steinbach P.A., Tsien R.Y. Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 2009, 324:804-807.
75. Shyu Y.J., Hiatt S.M., Duren H.M., Ellis R.E., Kerppola T.K., Hu C.D. Visualization of protein interactions in living Caenorhabditis elegans using bimolecular fluorescence complementation analysis. Nat. Protoc. 2008, 3:588-596.
76. Shyu Y.J., Hu C.D. Fluorescence complementation: an emerging tool for biological research. Trends Biotechnol. 2008, 26:622-630.
77. Shyu Y.J., Liu H., Deng X., Hu C.D. Identification of new fluorescent protein fragments for bimolecular fluorescence complementation analysis under physiological conditions. Biotechniques 2006, 40:61-66.
78. Shyu Y.J., Suarez C.D., Hu C.D. Visualization of AP-1 NF-kappaB ternary complexes in living cells by using a BiFC-based FRET. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:151-156.
79. Stefan E., Aquin S., Berger N., Landry C.R., Nyfeler B., Bouvier M., Michnick S.W. Quantification of dynamic protein complexes using Renilla luciferase fragment complementation applied to protein kinase A activities in vivo. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:16916-16921.
80. Tang W.J., Stanzel M., Gilman A.G. Truncation and alanine-scanning mutants of type I adenylyl cyclase. Biochemistry 1995, 34:14563-14572.
81. van der Stelt M., Fox S.H., Hill M., Crossman A.R., Petrosino S., Di Marzo V., Brotchie J.M. A role for endocannabinoids in the generation of parkinsonism and levodopa-induced dyskinesia in MPTP-lesioned non-human primate models of Parkinson's disease. FASEB J. 2005, 19:1140-1142.
82. Vidi P.A., Chemel B.R., Hu C.D., Watts V.J. Ligand-dependant oligomerization of dopamine D2 and adenosine A2A receptors in living neuronal cells. Mol. Pharmacol. 2008, 74:544-551.
83. Vidi P.A., Chen J., Irudayaraj J.M., Watts V.J. Adenosine A(2A) receptors assemble into higher-order oligomers at the plasma membrane. FEBS Lett. 2008, 582:3985-3990.
84. Vidi P.A., Przybyla J.A., Hu C.D., Watts V.J. Visualization of G protein-coupled receptor (GPCR) interactions in living cells using bimolecular fluorescence complementation (BiFC). Curr. Protoc. Neurosci. 2010, (Chapter 5, Unit 5 29).
85. Vidi P.A., Watts V.J. Fluorescent and bioluminescent protein-fragment complementation assays in the study of G protein-coupled receptor oligomerization and signaling. Mol. Pharmacol. 2009, 75:733-739.
86. Villar V.A., Jones J.E., Armando I., Palmes-Saloma C., Yu P., Pascua A.M., Keever L., Arnaldo F.B., Wang Z., Luo Y., Felder R.A., Jose P.A. G protein-coupled receptor kinase 4 (GRK4) regulates the phosphorylation and function of the dopamine D3 receptor. J. Biol. Chem. 2009, 284:21425-21434.
87. Vortherms T.A., Watts V.J. Sensitization of neuronal A2A adenosine receptors after persistent D2 dopamine receptor activation. J. Pharmacol. Exp. Ther. 2004, 308:221-227.
88. Walters D.E., Carr L.A. Changes in brain catecholamine mechanisms following perinatal exposure to marihuana. Pharmacol. Biochem. Behav. 1986, 25:763-768.
89. Wang X., Dow-Edwards D., Anderson V., Minkoff H., Hurd Y.L. In utero marijuana exposure associated with abnormal amygdala dopamine D2 gene expression in the human fetus. Biol. Psychiatry 2004, 56:909-915.
90. Watanabe N., Bodin L., Pandey M., Krause M., Coughlin S., Boussiotis V.A., Ginsberg M.H., Shattil S.J. Mechanisms and consequences of agonist-induced talin recruitment to platelet integrin alphaIIbbeta3. J. Cell Biol. 2008, 181:1211-1222.
91. Watts V.J., Neve K.A. Sensitization of adenylate cyclase by Galpha i/o-coupled receptors. Pharmacol. Ther. 2005, 106:405-421.
92. Wreggett K.A., Wells J.W. Cooperativity manifest in the binding properties of purified cardiac muscarinic receptors. J. Biol. Chem. 1995, 270:22488-22499.
93. Yost E.A., Mervine S.M., Sabo J.L., Hynes T.R., Berlot C.H. Live cell analysis of G protein beta5 complex formation, function, and targeting. Mol. Pharmacol. 2007, 72:812-825.
94. Zhao X., Jones A., Olson K.R., Peng K., Wehrman T., Park A., Mallari R., Nebalasca D., Young S.W., Xiao S.H. A homogeneous enzyme fragment complementation-based beta-arrestin translocation assay for high-throughput screening of G-protein-coupled receptors. J. Biomol. Screen. 2008, 13:737-747.