Impaired β-arrestin recruitment and reduced desensitization by non-catechol agonists of the D1 dopamine receptor

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Gray, David L ^a   Allen, John A ^a,c   Mente, Scot ^a   O'connor, Rebecca E ^a   Demarco, George J ^a   Efremov, Ivan ^a   Tierney, Patrick ^a   Volfson, Dmitri ^a   Davoren, Jennifer ^a   Guilmette, Edward ^a   Salafia, Michelle ^a   Kozak, Rouba ^a   Ehlers, Michael D ^a,b  

^a PFIZER INC   (United States)

^b BIOGEN   (United States)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; 3 (1 ADAMANTYL) 1 AMINOMETHYL 3,4 DIHYDRO 5,6 DIHYDROXY 1H 2 BENZOPYRAN; ADENYLATE CYCLASE; BETA ARRESTIN; DOPAMINE 1 RECEPTOR; DOPAMINE 1 RECEPTOR STIMULATING AGENT; PF 2334; PF 6142; QUINPIROLE; UNCLASSIFIED DRUG; DOPAMINE RECEPTOR STIMULATING AGENT;

DRUG; GENE EXPRESSION; GENOME; MOLECULAR ANALYSIS; PROTEIN; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENCY; DRUG RECEPTOR BINDING; DRUG SELECTIVITY; HAPLORHINI; HUMAN; HUMAN CELL; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NONHUMAN; PARKINSON DISEASE; RAT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; CELL LINE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENETICS; HAMSTER; HEK293 CELL LINE; METABOLISM; MUTATION; PROCEDURES; RADIOASSAY; TUMOR CELL LINE;

RODENTIA;

ANIMALS; BETA-ARRESTINS; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; DOPAMINE AGONISTS; HEK293 CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; MOLECULAR STRUCTURE; MUTATION; RADIOLIGAND ASSAY; RECEPTORS, DOPAMINE D1;

EID: 85042094461     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-02776-7     Document Type: Article

References (76)

1. Beaulieu, J. M. & Gainetdinov, R. R. The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol. Rev. 63, 182-217 (2011).
2. Gershanik, O., Heikkila, R. E. & Duvoisin, R. C. Behavioral correlations of dopamine receptor activation. Neurology 33, 1489-1492 (1983).
3. O'Daly, O. G. et al. Amphetamine sensitization alters reward processing in the human striatum and amygdala. PLoS ONE 9, e93955 (2014).
4. Narayanan, N. S., Land, B. B., Solder, J. E., Deisseroth, K. & DiLeone, R. J. Prefrontal D1 dopamine signaling is required for temporal control. Proc. Natl Acad. Sci. USA 109, 20726-20731 (2012).
5. Waddington, J. L. Therapeutic potential of selective D-1 dopamine receptor agonists and antagonists in psychiatry and neurology. Gen. Pharmacol. 19, 55-60 (1988).
6. Sawaguchi, T. & Goldman-Rakic, P. S. D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science 251, 947-950 (1991).
7. Kalia, L. V. & Lang, A. E. Parkinson's disease. Lancet, https://doi.org/10.1016/ S0140-6736(14)61393-3 (2015).
8. Galvan, A. & Wichmann, T. Pathophysiology of parkinsonism. Clin. Neurophysiol. 119, 1459-1474 (2008).
9. Iversen, S. D. & Iversen, L. L. Dopamine: 50 years in perspective. Trends Neurosci. 30, 188-193 (2007).
10. Arnsten, A. F. The neurobiology of thought: the groundbreaking discoveries of Patricia Goldman-Rakic 1937-2003. Cereb. Cortex 23, 2269-2281 (2013).
11. Nutt, D. J., Lingford-Hughes, A., Erritzoe, D. & Stokes, P. R. The dopamine theory of addiction: 40 years of highs and lows. Nat. Rev. Neurosci. 16, 305-312 (2015).
12. Bush, G. Attention-deficit/hyperactivity disorder and attention networks. Neuropsychopharmacology 35, 278-300 (2010).
13. Buchanan, R. W., Freedman, R., Javitt, D. C., Abi-Dargham, A. & Lieberman, J. A. Recent advances in the development of novel pharmacological agents for the treatment of cognitive impairments in schizophrenia. Schizophr. Bull. 33, 1120-1130 (2007).
14. Lovenberg, T. W. et al. Dihydrexidine, a novel selective high potency full dopamine D-1 receptor agonist. Eur. J. Pharmacol. 166, 111-113 (1989).
15. Goldman-Rakic, P. S., Castner, S. A., Svensson, T. H., Siever, L. J. & Williams, G. V. Targeting the dopamine D1 receptor in schizophrenia: insights for cognitive dysfunction. Psychopharmacology 174, 3-16 (2004).
16. Kebabian, J. W. et al. A-77636: a potent and selective dopamine D1 receptor agonist with antiparkinsonian activity in marmosets. Eur. J. Pharmacol. 229, 203-209 (1992).
17. Kaiser, C. et al. Absolute stereochemistry and dopaminergic activity of enantiomers of 2,3,4,5-tetrahydro-7,8-dihydroxy-1-phenyl-1H-3-benzazepine. J. Med. Chem. 25, 697-703 (1982).
18. Neumeyer, J. L., Baindur, N., Niznik, H. B., Guan, H. C. & Seeman, P. (+/-)-3- Allyl-6-bromo-7,8-dihydroxy-1-phenyl-2,3,4,5-tetrahydro-1H-3- benzazepin, a new high-affinity D1 dopamine receptor ligand: synthesis and structureactivity relationship. J. Med. Chem. 34, 3366-3371 (1991).
19. Ring, A. M. et al. Adrenaline-activated structure of beta2-adrenoceptor stabilized by an engineered nanobody. Nature 502, 575-579 (2013).
20. Mente, S., Guilmette, E., Salafia, M. & Gray, D. Dopamine D1 receptor-agonist interactions: a mutagenesis and homology modeling study. Bioorg. Med. Chem. Lett. 25, 2106-2111 (2015).
21. Giardina, W. J. & Williams, M. Adrogolide HCl (ABT-431; DAS-431), a prodrug of the dopamine D1 receptor agonist, A-86929: preclinical pharmacology and clinical data. Cns. Drug. Rev. 7, 305-316 (2001).
22. Meanwell, N. A. Synopsis of some recent tactical application of bioisosteres in drug design. J. Med. Chem. 54, 2529-2591 (2011).
23. Taskinen, J. et al. Conjugation of catechols by recombinant human sulfotransferases, UDP-glucuronosyltransferases, and soluble catechol Omethyltransferase: structure-conjugation relationships and predictive models. Drug. Metab. Dispos. 31, 1187-1197 (2003).
24. Roe, D. L. From DOPA to Parkinson's disease: the early history of dopamine research. J. Hist. Neurosci. 6, 291-301 (1997).
25. Kim, O. J. et al. The role of phosphorylation in D1 dopamine receptor desensitization: evidence for a novel mechanism of arrestin association. J. Biol. Chem. 279, 7999-8010 (2004).
26. Jiang, D. & Sibley, D. R. Regulation of D(1) dopamine receptors with mutations of protein kinase phosphorylation sites: attenuation of the rate of agonist-induced desensitization. Mol. Pharmacol. 56, 675-683 (1999).
27. Kotowski, S. J., Hopf, F. W., Seif, T., Bonci, A. & von Zastrow, M. Endocytosis promotes rapid dopaminergic signaling. Neuron 71, 278-290 (2011).
28. Gainetdinov, R. R., Premont, R. T., Bohn, L. M., Lefkowitz, R. J. & Caron, M. G. Desensitization of G protein-coupled receptors and neuronal functions. Annu. Rev. Neurosci. 27, 107-144 (2004).
29. Morgan, D. J. et al. Mutation of putative GRK phosphorylation sites in the cannabinoid receptor 1 (CB1R) confers resistance to cannabinoid tolerance and hypersensitivity to cannabinoids in mice. J. Neurosci. 34, 5152-5163 (2014).
30. Bohn, L. M., Gainetdinov, R. R., Lin, F. T., Lefkowitz, R. J. & Caron, M. G. Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature 408, 720-723 (2000).
31. Blanchet, P. J., Grondin, R. & Bedard, P. J. Dyskinesia and wearing-off following dopamine D1 agonist treatment in drug-naive 1-methyl-4-phenyl- 1,2,3,6-tetrahydropyridine-lesioned primates. Mov. Disord. 11, 91-94 (1996).
32. Blanchet, P. J., Grondin, R., Bedard, P. J., Shiosaki, K. & Britton, D. R. Dopamine D1 receptor desensitization profile in MPTP-lesioned primates. Eur. J. Pharmacol. 309, 13-20 (1996).
33. Goulet, M., Grondin, R., Blanchet, P. J., Bedard, P. J. & Di Paolo, T. Dyskinesias and tolerance induced by chronic treatment with a D1 agonist administered in pulsatile or continuous mode do not correlate with changes of putaminal D1 receptors in drug-naive MPTP monkeys. Brain. Res. 719, 129-137 (1996).
34. Gulwadi, A. G. et al. Dinapsoline: characterization of a D1 dopamine receptor agonist in a rat model of Parkinson's disease. J. Pharmacol. Exp. Ther. 296, 338-344 (2001).
35. Munger, M. A. et al. Assessment of hemodynamic tolerance from a 24-hour intravenous infusion of fenoldopam mesylate in congestive heart failure. Am. J. Cardiol. 65, 206-210 (1990).
36. Wade, M. R. & Nomikos, G. G. Tolerance to the procholinergic action of the D1 receptor full agonist dihydrexidine. Psychopharmacology 182, 393-399 (2005).
37. Lefevre-Borg, F. et al. Studies on the mechanisms of the development of tolerance to the hypotensive effects of fenoldopam in rats. J. Cardiovasc. Pharmacol. 11, 444-455 (1988).
38. Bakken, G. A. et al. Shaping a screening file for maximal lead discovery efficiency and effectiveness: elimination of molecular redundancy. J. Chem. Inf. Model. 52, 2937-2949 (2012).
39. Ghose, A. K., Herbertz, T., Hudkins, R. L., Dorsey, B. D. & Mallamo, J. P. Knowledge-based, central nervous system (CNS) lead selection and lead optimization for CNS drug discovery. ACS Chem. Neurosci. 3, 50-68 (2012).
40. Wager, T. T., Hou, X., Verhoest, P. R. & Villalobos, A. Moving beyond rules: the development of a central nervous system multiparameter optimization (CNS MPO) approach to enable alignment of druglike properties. ACS Chem. Neurosci. 1, 435-449 (2010).
41. Sunahara, R. K. et al. Cloning of the gene for a human dopamine D5 receptor with higher affinity for dopamine than D1. Nature 350, 614-619 (1991).
42. Lefkowitz, R. J. G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. J. Biol. Chem. 273, 18677-18680 (1998).
43. Dumartin, B., Caille, I., Gonon, F. & Bloch, B. Internalization of D1 dopamine receptor in striatal neurons in vivo as evidence of activation by dopamine agonists. J. Neurosci. 18, 1650-1661 (1998).
44. Ng, G. Y. et al. Desensitization, phosphorylation and palmitoylation of the human dopamine D1 receptor. Eur. J. Pharmacol. 267, 7-19 (1994).
45. Shukla, A. K. et al. Structure of active beta-arrestin-1 bound to a G-proteincoupled receptor phosphopeptide. Nature 497, 137-141 (2013).
46. Malo, M., Brive, L., Luthman, K. & Svensson, P. Investigation of D(1) receptor-agonist interactions and D(1)/D(2) agonist selectivity using a combination of pharmacophore and receptor homology modeling. ChemMedChem 7, 483-494, 338 (2012).
47. Rasmussen, S. G. et al. Structure of a nanobody-stabilized active state of the beta(2) adrenoceptor. Nature 469, 175-180 (2011).
48. Lewis, M. M., Watts, V. J., Lawler, C. P., Nichols, D. E. & Mailman, R. B. Homologous desensitization of the D1A dopamine receptor: efficacy in causing desensitization dissociates from both receptor occupancy and functional potency. Pharmacol. Exp. Ther. 286, 345-353 (1998).
49. Conroy, J. L., Free, R. B. & Sibley, D. R. Identification of G protein-biased agonists that fail to recruit beta-arrestin or promote internalization of the D1 dopamine receptor. ACS Chem. Neurosci. 6, 681-692 (2015).
50. Colzato, L. S., van den Wildenberg, W. P., van Wouwe, N. C., Pannebakker, M. M. & Hommel, B. Dopamine and inhibitory action control: evidence from spontaneous eye blink rates. Exp. Brain Res. 196, 467-474 (2009).
51. Jutkiewicz, E. M. & Bergman, J. Effects of dopamine D1 ligands on eye blinking in monkeys: efficacy, antagonism, and D1/D2 interactions. J. Pharmacol. Exp. Ther. 311, 1008-1015 (2004).
52. Taylor, J. R. et al. Spontaneous blink rates correlate with dopamine levels in the caudate nucleus of MPTP-treated monkeys. Exp. Neurol. 158, 214-220 (1999).
53. Ungerstedt, U. 6-Hydroxy-dopamine induced degeneration of central monoamine neurons. Eur. J. Pharmacol. 5, 107-110 (1968).
54. Zhang, J., Xiong, B., Zhen, X. & Zhang, A. Dopamine D1 receptor ligands: where are we now and where are we going. Med. Res. Rev. 29, 272-294 (2009).
55. Reiter, E., Ahn, S., Shukla, A. K. & Lefkowitz, R. J. Molecular mechanism of beta-arrestin-biased agonism at seven-transmembrane receptors. Annu. Rev. Pharmacol. Toxicol. 52, 179-197 (2012).
56. Wacker, D. et al. Structural features for functional selectivity at serotonin receptors. Science 340, 615-619 (2013).
57. Allen, J. A. et al. Discovery of beta-arrestin-biased dopamine D2 ligands for probing signal transduction pathways essential for antipsychotic efficacy. Proc. Natl Acad. Sci. USA 108, 18488-18493 (2011).
58. Urban, J. D. et al. Functional selectivity and classical concepts of quantitative pharmacology. J. Pharmacol. Exp. Ther. 320, 1-13 (2007).
59. Bonner, L. A. et al. Mapping the catechol binding site in dopamine D(1) receptors: synthesis and evaluation of two parallel series of bicyclic dopamine analogues. ChemMedChem 6, 1024-1040 (2011).
60. Chemel, B. R., Bonner, L. A., Watts, V. J. & Nichols, D. E. Ligand-specific roles for transmembrane 5 serine residues in the binding and efficacy of dopamine D(1) receptor catechol agonists. Mol. Pharmacol. 81, 729-738 (2012).
61. Kalvass, J. C. & Maurer, T. S. Influence of nonspecific brain and plasma binding on CNS exposure: implications for rational drug discovery. Biopharm. Drug Dispos. 23, 327-338 (2002).
62. Di, L., Umland, J. P., Trapa, P. E. & Maurer, T. S. Impact of recovery on fraction unbound using equilibrium dialysis. J. Pharm. Sci. 101, 1327-1335 (2012).
63. Di, L. et al. Species independence in brain tissue binding using brain homogenates. Drug Metab. Dispos. 39, 1270-1277 (2011).
64. Barak, L. S., Ferguson, S. S., Zhang, J. & Caron, M. G. A beta-arrestin/green fluorescent protein biosensor for detecting G protein-coupled receptor activation. J. Biol. Chem. 272, 27497-27500 (1997).
65. Yudowski, G. A. & von Zastrow, M. Investigating G protein-coupled receptor endocytosis and trafficking by TIR-FM. Methods Mol. Biol. 756, 325-332 (2011).
66. Dougherty, E. R. & Lotufo, R. A. Hands-on Morphological Image Processing (SPIE Press-The International Society for Optical Engineering, Bellingham, WA, USA, 2003).
67. Nobuyuki, OtsuA threshold selection method from gray-level histograms. IEEE Trans. Sys., Man., Cyber 9, 62-66 (1979).
68. Garippa, R. J., Hoffman, A. F., Gradl, G. & Kirsch, A. High-throughput confocal microscopy for beta-arrestin-green fluorescent protein translocation G protein-coupled receptor assays using the Evotec Opera. Methods Enzymol. 414, 99-120 (2006).
69. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289-300 (1995).
70. R Core Team, 2014, R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, http://www.R-project. org, (2014).
71. Gehlhaar, D. K. et al. Molecular recognition of the inhibitor AG-1343 by HIV- 1 protease: conformationally flexible docking by evolutionary programming. Chem. Biol. 2, 317-324 (1995).
72. Dror, R. O. et al. Pathway and mechanism of drug binding to G-proteincoupled receptors. Proc. Natl Acad. Sci. USA 108, 13118-13123 (2011).
73. Python Software Foundation. Python Language Reference, Version 2.7. http://www.python.org.
74. G. R. Bradski & V. Pisarevsky. In Proceedings of IEEE Conference on Computer Vision and Pattern Recognition. Vol.2, 796-797 (2000).
75. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & Team, R. C. lme4: Linear and Nonlinear Mixed Effects Models. R Package Version 3.0.1, http://CRAN.Rproject. org/package=lme4 (2014).
76. Lenth, R. V. lsmeans: Least-Squares means. R Package Version 2.11, http:// CRAN.R-project.org/package=lsmeans (2014).