Imaging the cannabinoid CB1 receptor in humans with [11C] OMAR: Assessment of kinetic analysis methods, test-retest reproducibility, and gender differences

Journal of Cerebral Blood Flow and Metabolism

Volumn 35, Issue 8, 2015, Pages 1313-1322

  Normandin, Marc D ^a,f   Zheng, Ming Qiang ^a   Lin, Kuo Shyan ^b   Mason, N Scott ^c   Lin, Shu Fei ^a   Ropchan, Jim ^a   Labaree, David ^a   Henry, Shannan ^a   Williams, Wendol A ^a   Carson, Richard E ^a   Neumeister, Alexander ^d,e   Huang, Yiyun ^a  

^a YALE UNIVERSITY   (United States)

^b BRITISH COLUMBIA CANCER AGENCY   (Canada)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NEW YORK UNIVERSITY   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

cannabinoid CB1 receptor; gender differences; human; kinetic modeling; positron emission tomography; test retest

Indexed keywords

CANNABINOID 1 RECEPTOR; OMAR C 11; RADIOPHARMACEUTICAL AGENT; UNCLASSIFIED DRUG; CARBON;

ADULT; AGED; ARTICLE; BODY WEIGHT; CLINICAL ARTICLE; COMPARTMENT MODEL; CONTROLLED STUDY; FEMALE; HUMAN; IN VIVO STUDY; KINETICS; MALE; NUCLEAR MAGNETIC RESONANCE; PLASMA CLEARANCE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REPRODUCIBILITY; SEX DIFFERENCE; TEST RETEST RELIABILITY; VOLUME OF DISTRIBUTION; ADOLESCENT; BRAIN; BRAIN ANGIOGRAPHY; CLINICAL TRIAL; METABOLISM; MIDDLE AGED; MULTICENTER STUDY; PROCEDURES; RADIOGRAPHY; SEXUAL DEVELOPMENT;

ADOLESCENT; ADULT; AGED; BRAIN; CARBON ISOTOPES; CEREBRAL ANGIOGRAPHY; FEMALE; HUMANS; MALE; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; RECEPTOR, CANNABINOID, CB1; SEX CHARACTERISTICS;

EID: 84938741069     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2015.46     Document Type: Article

References (40)

1. Devane WA, Dysarz FA 3rd, Johnson MR, Melvin LS, Howlett AC. Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol 1988; 34: 605-613
2. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990; 346: 561-564
3. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993; 365: 61-65
4. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR et al. Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 1990; 87: 1932-1936
5. Glass M, Dragunow M, Faull RL. Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 1997; 77: 299-318
6. Mechoulam R, Parker LA. The endocannabinoid system and the brain. Annu Rev Psychol 2013; 64: 21-47
7. Horti AG, Van Laere K. Development of radioligands for in vivo imaging of type 1 cannabinoid receptors (CB1) in human brain. Curr Pharm Des 2008; 14: 3363-3383
8. Terry GE, Liow JS, Zoghbi SS, Hirvonen J, Farris AG, Lerner A et al. Quantitation of cannabinoid CB1 receptors in healthy human brain using positron emission tomography and an inverse agonist radioligand. Neuroimage 2009; 48: 362-370
9. Terry GE, Hirvonen J, Liow JS, Zoghbi SS, Gladding R, Tauscher JT et al. Imaging and quantitation of cannabinoid CB1 receptors in human and monkey brains using [18F]-labeled inverse agonist radioligands. J Nucl Med 2010; 51: 112-120
10. Burns HD, Van Laere K, Sanabria-Bohorquez S, Hamill TG, Bormans G, Eng WS et al. [18F]MK-9470, a positron emission tomography (PET) tracer for in vivo human PET brain imaging of the cannabinoid-1 receptor. Proc Natl Acad Sci USA 2007; 104: 9800-9805
11. Tsujikawa T, Zoghbi SS, Hong J, Donohue SR, Jenko KJ, Gladding RL et al. In vitro and in vivo evaluation of 11C-SD5024, a novel PET radioligand for human brain imaging of cannabinoid CB1 receptors. Neuroimage 2014; 84: 733-741
12. Horti AG, Fan H, Kuwabara H, Hilton J, Ravert HT, Holt DP et al. 11C-JHU75528: a radiotracer for PET imaging of CB1 cannabinoid receptors. J Nucl Med 2006; 47: 1689-1696
13. Wong DF, Kuwabara H, Horti AG, Raymont V, Brasic J, Guevara M et al. Quantification of cerebral cannabinoid receptors subtype 1 (CB1) in healthy subjects and schizophrenia by the novel PET radioligand [11C]OMAR. Neuroimage 2010; 52: 1505-1513
14. Logan J, Fowler JS, Volkow ND, Wolf AP, Dewey SL, Schlyer DJ et al. Graphical analysis of reversible radioligand binding from time-Activity measurements applied to [N-11C-methyl]-(-)-cocaine PET studies in human subjects. J Cereb Blood Flow Metab 1990; 10: 740-747
15. Carson RE, Barker WC, Liow JS, Johnson C. Design of a motion-compensation OSEM list-mode algorithm for resolution-recovery reconstruction for the HRRT. IEEE Nucl Sci Symp Conf Rec 2004; 5: 3281-3285
16. Hilton J, Yokoi F, Dannals RF, Ravert HT, Szabo Z, Wong DF. Column-switching HPLC for the analysis of plasma in PET imaging studies. Nucl Med Biol 2000; 27: 627-630
17. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002; 17: 825-841
18. Papademetris X, Jackowski MP, Rajeevan N, DiStasio M, Okuda H, Constable RT et al. BioImage Suite: an integrated medical image analysis suite: an update. Insight J 2006; 2006: 209
19. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002; 15: 273-289
20. Innis RB, Cunningham VJ, Delforge J, Fujita M, Gjedde A, Gunn RN et al. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J Cereb Blood Flow Metab 2007; 27: 1533-1539
21. Ichise M, Toyama H, Innis RB, Carson RE. Strategies to improve neuroreceptor parameter estimation by linear regression analysis. J Cereb Blood Flow Metab 2002; 22: 1271-1281
22. Akaike H. A new look at the statistical model identification. IEEE Trans Automatic Control 1974; 19: 716-723
23. Schwarz G. Estimating the dimension of a model. Ann Stat 1978; 6: 461-464
24. Van Laere K, Goffin K, Casteels C, Dupont P, Mortelmans L, de Hoon J et al. Genderdependent increases with healthy aging of the human cerebral cannabinoid-Type 1 receptor binding using [18F]MK-9470 PET. Neuroimage 2008; 39: 1533-1541
25. Slifstein M, Laruelle M. Effects of statistical noise on graphic analysis of PET neuroreceptor studies. J Nucl Med 2000; 41: 2083-2088
26. Neumeister A, Normandin MD, Murrough JW, Henry S, Bailey CR, Luckenbaugh DA et al. Positron emission tomography shows elevated cannabinoid CB1 receptor binding in men with alcohol dependence. Alcohol Clin Exp Res 2012; 36: 2104-2109
27. Neumeister A, Normandin MD, Pietrzak RH, Piomelli D, Zheng MQ, Gujarro-Anton A et al. Elevated brain cannabinoid CB1 receptor availability in post-Traumatic stress disorder: a positron emission tomography study. Mol Psychiatry 2013; 18: 1034-1040
28. Sanabria-Bohorquez SM, Hamill TG, Goffin K, De Lepeleire I, Bormans G, Burns HD et al. Kinetic analysis of the cannabinoid-1 receptor PET tracer [18F]MK-9470 in human brain. Eur J Nucl Med Mol Imaging 2010; 37: 920-933
29. Hirvonen J, Terry GE, Halldin C, Pike VW, Innis RB. Approaches to quantify radioligands that wash out slowly from target organs. Eur J Nucl Med Mol Imaging 2010; 37: 917-919
30. Fattore L, Fratta W. How important are sex differences in cannabinoid action?. Br J Pharmacol 2010; 160: 544-548
31. Van Der Schueren BJ, Van Laere K, Gerard N, Bormans G, De Hoon JN. Interictal type 1 cannabinoid receptor binding is increased in female migraine patients. Headache 2012; 52: 433-440
32. Hirvonen J, Zanotti-Fregonara P, Umhau JC, George DT, Rallis-Frutos D, Lyoo CH et al. Reduced cannabinoid CB1 receptor binding in alcohol dependence measured with positron emission tomography. Mol Psychiatry 2013; 18: 916-921
33. Gerard N, Pieters G, Goffin K, Bormans G, Van Laere K. Brain type 1 cannabinoid receptor availability in patients with anorexia and bulimia nervosa. Biol Psychiatry 2011; 70: 777-784
34. Ceccarini J, De Hert M, Van Winkel R, Peuskens J, Bormans G, Kranaster L et al. Increased ventral striatal CB1 receptor binding is related to negative symptoms in drug-free patients with schizophrenia. Neuroimage 2013; 79: 304-312
35. Van Laere K, Casteels C, Lunskens S, Goffin K, Grachev ID, Bormans G et al. Regional changes in type 1 cannabinoid receptor availability in Parkinson's disease in vivo. Neurobiol Aging 2012; 33: 620. e1-e8
36. Van Laere K, Goffin K, Bormans G, Casteels C, Mortelmans L, de Hoon J et al. Relationship of type 1 cannabinoid receptor availability in the human brain to novelty-seeking temperament. Arch Gen Psychiatry 2009; 66: 196-204
37. Riebe CJ, Hill MN, Lee TT, Hillard CJ, Gorzalka BB. Estrogenic regulation of limbic cannabinoid receptor binding. Psychoneuroendocrinology 2010; 35: 1265-1269
38. Casteels C, Gerard N, Van Kuyck K, Pottel L, Nuttin B, Bormans G et al. Small animal PET imaging of the type 1 cannabinoid receptor in a rodent model for anorexia nervosa. Eur J Nucl Med Mol Imaging 2014; 41: 308-321
39. Castelli MP, Fadda P, Casu A, Spano MS, Casti A, Fratta W et al. Male and female rats differ in brain cannabinoid CB1 receptor density and function and in behavioural traits predisposing to drug addiction: effect of ovarian hormones. Curr Pharm Des 2014; 20: 2100-2113
40. Rodriguez de Fonseca F, Cebeira M, Ramos JA, Martin M, Fernandez-Ruiz JJ. Cannabinoid receptors in rat brain areas: sexual differences, fluctuations during estrous cycle and changes after gonadectomy and sex steroid replacement. Life Sci 1994; 54: 159-170