Imaging Agonist-Induced D2/D3 Receptor Desensitization and Internalization In Vivo with PET/fMRI

Neuropsychopharmacology

Volumn 41, Issue 5, 2016, Pages 1427-1436

  Sander, Christin Y ^a,b   Hooker, Jacob M ^a,b   Catana, Ciprian ^a,b   Rosen, Bruce R ^a,b,c   Mandeville, Joseph B ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; PROCHLORPERAZINE; QUINPIROLE; ROPINIROLE; DOPAMINE 2 RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR STIMULATING AGENT; INDOLE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISSOCIATION; DOSE RESPONSE; DRUG DOSE INCREASE; DRUG EFFICACY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; IN VIVO STUDY; INTERNALIZATION; MALE; NEUROPHARMACOLOGY; NEUROVASCULAR COUPLING; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RECEPTOR OCCUPANCY; RHESUS MONKEY; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; BRAIN; DRUG EFFECTS; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCEDURES;

ANIMALS; BRAIN; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; DOPAMINE D2 RECEPTOR ANTAGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; INDOLES; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; POSITRON-EMISSION TOMOGRAPHY; PROCHLORPERAZINE; QUINPIROLE; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3;

EID: 84960885454     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2015.296     Document Type: Article

References (59)

1. Alpert NM, Badgaiyan RD, Livni E, Fischman AJ (2003). A novel method for noninvasive detection of neuromodulatory changes in specific neurotransmitter systems. NeuroImage 19: 1049-1060.
2. Arnsten AF, Cai JX, Steere JC, Goldman-Rakic PS (1995). Dopamine D2 receptor mechanisms contribute to age-related cognitive decline: the effects of quinpirole on memory and motor performance in monkeys. J Neurosci 15: 3429-3439.
3. Bartlett SE, Enquist J, Hopf FW, Lee JH, Gladher F, Kharazia V et al (2005). Dopamine responsiveness is regulated by targeted sorting of D2 receptors. Proc Natl Acad Sci USA 102: 11521-11526.
4. Beaulieu J-M, Del'Guidice T, Sotnikova T, Lemasson M, Gainetdinov R (2011). Beyond cAMP: the regulation of Akt and GSK3 by dopamine receptors. Front Mol Neurosci 4: 38.
5. Beaulieu J-M, Gainetdinov RR (2011). The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol Rev 63: 182-217.
6. Bhattacharyya S, Raote I, Bhattacharya A, Miledi R, Panicker MM (2006). Activation, internalization, and recycling of the serotonin 2A receptor by dopamine. Proc Natl Acad Sci USA 103: 15248-15253.
7. Bolaños-Jiménez R, Arizmendi-Vargas J, Martínez-Zavala N, Carrillo-Ruiz J, Damián CÁ-TJ, Luis J-PF et al (2011). Quinpirole effects on the dopaminergic system. Br J Pharmacol Toxicol 2: 310.
8. Breier A, Su T-P, Saunders R, Carson RE, Kolachana BS, de Bartolomeis A et al (1997). Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: Evidence from a novel positron emission tomography method. Proc Natl Acad Sci USA 94: 2569-2574.
9. Carson RE, Channing MA, Blasberg RG, Dunn BB, Cohen RM, Rice KC et al (1993). Comparison of bolus and infusion methods for receptor quantitation: application to [18f]cyclofoxy and positron emission tomography. J Cereb Blood Flow Metab 13: 24-42.
10. Catana C, van der Kouwe A, Benner T, Michel CJ, Hamm M, Fenchel M et al (2010). Toward implementing an MRI-based PET attenuation-correction method for neurologic studies on the MRPET brain prototype. J Nucl Med 51: 1431-1438.
11. Chen YCI, Galpern WR, Brownell A-L, Matthews RT, Bogdanov M, Isacson O et al (1997). Detection of dopaminergic neurotransmitter activity using pharmacologic MRI: correlation with PET, microdialysis, and behavioral data. Magn Reson Med 38: 389-398.
12. Chen YI, Brownell AL, Galpern W, Isacson O, Bogdanov M, Beal MF et al (1999). Detection of dopaminergic cell loss and neural transplantation using pharmacological MRI, PET and behavioral assessment. Neuroreport 10: 2881-2886.
13. Choi J-K, Chen YI, Hamel E, Jenkins BG (2006). Brain hemodynamic changes mediated by dopamine receptors: role of the cerebral microvasculature in dopamine-mediated neurovascular coupling. NeuroImage 30: 700-712.
14. Chugani DC, Ackermann RF, Phelps ME (1988). In vivo [3H] spiperone binding: evidence for accumulation in corpus striatum by agonist-mediated receptor internalization. J Cereb Blood Flow Metab 8: 291-303.
15. Clark AJ (1937). General Pharmacology. Springer-Verlag: Berlin, New York.
16. Coldwell MC, Boyfield I, Brown T, Hagan JJ, Middlemiss DN (1999). Comparison of the functional potencies of ropinirole and other dopamine receptor agonists at human D2(long), D3 and D4.4 receptors expressed in Chinese hamster ovary cells. Br J Pharmacol 127: 1696-1702.
17. Cox RW (2012). AFNI: what a long strange trip it's been. Neuroimage 62: 743-747.
18. Cumming P (2011). Absolute abundances and affinity states of dopamine receptors in mammalian brain: a review. Synapse 65: 892-909.
19. Eilam D, Szechtman H (1989). Biphasic effect of D-2 agonist quinpirole on locomotion and movements. Eur J Pharmacol 161: 151-157.
20. Gardner B, Strange PG (1998). Agonist action at D2(long) dopamine receptors: ligand binding and functional assays. Br J Pharmacol 124: 978-984.
21. Ginovart N (2005). Imaging the dopamine system with in vivo [11C]raclopride displacement studies: understanding the true mechanism. Mol Imaging Biol 7: 45-52.
22. Goggi JL, Sardini A, Egerton A, Strange PG, Grasby PM (2007). Agonist-dependent internalization of D2 receptors: imaging quantification by confocal microscopy. Synapse 61: 231-241.
23. Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J et al (2002). Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47: 1202-1210.
24. Gründer G, Yokoi F, Offord SJ, Ravert HT, Dannals RF, Salzmann JK et al (1997). Time course of 5-HT2A Receptor occupancy in the human brain after a single oral dose of the putative antipsychotic drug MDL 100,907 measured by positron emission tomography. Neuropsychopharmacology 17: 175-185.
25. Guo N, Guo W, Kralikova M, Jiang M, Schieren I, Narendran R et al (2009). Impact of D2 receptor internalization on binding affinity of neuroimaging radiotracers. Neuropsychopharmacology 35: 806-817.
26. Hall J, Trent S, Thomas KL, O'Donovan MC, Owen MJ (2015). Genetic risk for schizophrenia: convergence on synaptic pathways involved in plasticity. Biol Psychiatry 77: 52-58.
27. Ichise M, Liow J-S, Lu J-Q, Takano A, Model K, Toyama H et al (2003). Linearized reference tissue parametric imaging methods: application to [11C]DASB positron emission tomography studies of the serotonin transporter in human brain. J Cereb Blood Flow Metab 23: 1096-1112.
28. Ko F, Seeman P, Sun WS, Kapur S (2002). Dopamine D2 receptors internalize in their low-affinity state. Neuroreport 13: 1017-1020.
29. Lammertsma AA, Hume SP (1996). Simplified reference tissue model for PET receptor studies. Neuroimage 4: 153-158.
30. Lane DA, Chan J, Fitzgerald ML, Kearn CS, Mackie K, Pickel VM (2012). Quinpirole elicits differential in vivo changes in the preand postsynaptic distributions of dopamine D2 receptors in mouse striatum: relation to cannabinoid-1 (CB1) receptor targeting. Psychopharmacology (Berl) 221: 101-113.
31. Laruelle M (2000). Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. J Cereb Blood Flow Metab 20: 423-451.
32. Laruelle M, Iyer RN, Al-Tikriti MS, Zea-Ponce Y, Malison R, Zoghbi SS et al (1997). Microdialysis and SPECT measurements of amphetamine-induced dopamine release in nonhuman primates. Synapse 25: 1-14.
33. Lefkowitz RJ, Shenoy SK (2005). Transduction of receptor signals by ß-arrestins. Science 308: 512-517.
34. Levant B, Grigoriadis DE, DeSouza EB (1992). Characterization of [3H]quinpirole binding to D2-like dopamine receptors in rat brain. J Pharmacol Exp Ther 262: 929-935.
35. Maehle A-H, Prüll C-R, Halliwell RF (2002). The emergence of the drug receptor theory. Nat Rev Drug Discov 1: 637-641.
36. Mandeville JB (2012). IRON fMRI measurements of CBV and implications for BOLD signal. Neuroimage 62: 1000-1008.
37. Mandeville JB, Marota JJA, Kosofsky BE, Keltner JR, Weissleder R, Rosen BR et al (1998). Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation. Magn Reson Med 39: 615-624.
38. Mandeville JB, Sander CYM, Jenkins BG, Hooker JM, Catana C, Vanduffel W et al (2013). A receptor-based model for dopamineinduced fMRI signal. Neuroimage 75: 46-57.
39. McLaren DG, Kosmatka KJ, Oakes TR, Kroenke CD, Kohama SG, Matochik JA et al (2009). A population-average MRI-based atlas collection of the rhesus macaque. Neuroimage 45: 52-59.
40. Narendran R, Slifstein M, Guillin O, Hwang Y, Hwang D-R, Scher E et al (2006). Dopamine (D2/3) receptor agonist positron emission tomography radiotracer [11C]-(+)-PHNO is a D3 receptor preferring agonist in vivo. Synapse 60: 485-495.
41. Normandin MD, Schiffer WK, Morris ED (2012). A linear model for estimation of neurotransmitter response profiles from dynamic PET data. Neuroimage 59: 2689-2699.
42. Perachon S, Schwartz J-C, Sokoloff P (1999). Functional potencies of new antiparkinsonian drugs at recombinant human dopamine D1, D2 and D3 receptors. Eur J Pharmacol 366: 293-300.
43. Saleem KS, Logothetis NK (2006). A Combined MRI and Histology Atlas of the Rhesus Monkey Brain. Elsevier: Burlington, USA.
44. Sander CY, Cramer A, Keil B, Mareyam A, Rosen BR, Wald LL (2013a). Low 511 keV-attenuation array coil setup for simultaneous PET/MR imaging of the monkey brain. Proc Intl Soc Mag Reson Med 21.
45. Sander CY, Hooker JM, Catana C, Normandin MD, Alpert NM, Knudsen GM et al (2013b). Neurovascular coupling to D2/D3 dopamine receptor occupancy using simultaneous PET/functional MRI. Proc Natl Acad Sci USA 201220512.
46. Seeman MV, Seeman P (2014). Is schizophrenia a dopamine supersensitivity psychotic reaction? Prog Neuropsychopharmacol Biol Psychiatry 48: 155-160.
47. Seeman P (2011). All roads to schizophrenia lead to dopamine supersensitivity and elevated dopamine D2high receptors. CNS Neurosci Ther 17: 118-132.
48. Seeman P (2013). Are dopamine D2 receptors out of control in psychosis? Prog Neuropsychopharmacol Biol Psychiatry 46: 146-152.
49. Seeman P, Guan H-C, Niznik HB (1989). Endogenous dopamine lowers the dopamine D2 receptor density as measured by [3H] raclopride: implications for positron emission tomography of the human brain. Synapse 3: 96-97.
50. Seeman P, Wilson A, Gmeiner P, Kapur S (2006). Dopamine D2 and D3 receptors in human putamen, caudate nucleus, and globus pallidus. Synapse 60: 205-211.
51. Skinbjerg M, Liow J-S, Seneca N, Hong J, Lu S, Thorsell A et al (2010). D2 dopamine receptor internalization prolongs the decrease of radioligand binding after amphetamine: a PET study in a receptor internalization-deficient mouse model. Neuroimage 50: 1402-1407.
52. Sokoloff P, Giros B, Martres M-P, Bouthenet M-L, Schwartz J-C (1990). Molecular cloning and characterization of a novel dopamine receptor (D3) as a target for neuroleptics. Nature 347: 146-151.
53. Sun W, Ginovart N, Ko F, Seeman P, Kapur S (2003). In vivo evidence for dopamine-mediated internalization of D2-receptors after amphetamine: differential findings with [3H]raclopride versus [3H]spiperone. Mol Pharmacol 63: 456-462.
54. Trevor Young L, Wong DF, Goldman S, Minkin E, Chen C, Matsumura K et al (1991). Effects of endogenous dopamine on kinetics of [3H]N-methylspiperone and [3H]raclopride binding in the rat brain. Synapse 9: 188-194.
55. Tsukada H, Harada N, Nishiyama S, Ohba H, Sato K, Fukumoto D et al (2000). Ketamine decreased striatal [11C]raclopride binding with no alterations in static dopamine concentrations in the striatal extracellular fluid in the monkey brain: multiparametric PET studies combined with microdialysis analysis. Synapse 37: 95-103.
56. Tsukada H, Nishiyama S, Kakiuchi T, Ohba H, Sato K, Harada N (1999). Is synaptic dopamine concentration the exclusive factor which alters the in vivo binding of [11C]raclopride?: PET studies combined with microdialysis in conscious monkeys. Brain Res 841: 160-169.
57. Williams JT, Ingram SL, Henderson G, Chavkin C, von Zastrow M, Schulz S et al (2013). Regulation of μ-opioid receptors: desensitization, phosphorylation, internalization, and tolerance. Pharmacol Rev 65: 223-254.
58. Winstanley CA, Zeeb FD, Bedard A, Fu K, Lai B, Steele C et al (2010). Dopaminergic modulation of the orbitofrontal cortex affects attention, motivation and impulsive responding in rats performing the five-choice serial reaction time task. Behav Brain Res 210: 263-272.
59. Worsley KJ, Liao CH, Aston J, Petre V, Duncan GH, Morales F et al (2002). A general statistical analysis for fMRI data. Neuroimage 15: 1-15.