Kappa-opioid receptors, dynorphin, and cocaine addiction: a positron emission tomography study.
Adult
Brain
/ diagnostic imaging
Carbon Radioisotopes
Case-Control Studies
Choice Behavior
Cocaine
/ administration & dosage
Cocaine Smoking
Cocaine-Related Disorders
/ diagnostic imaging
Dynorphins
/ metabolism
Humans
Male
Middle Aged
Naltrexone
/ pharmacology
Narcotic Antagonists
/ pharmacology
Neostriatum
/ diagnostic imaging
Piperazines
Positron-Emission Tomography
Pyrrolidines
Receptors, Opioid, kappa
/ metabolism
Stress, Psychological
/ psychology
Journal
Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
ISSN: 1740-634X
Titre abrégé: Neuropsychopharmacology
Pays: England
ID NLM: 8904907
Informations de publication
Date de publication:
09 2019
09 2019
Historique:
received:
21
09
2018
accepted:
16
04
2019
revised:
28
03
2019
pubmed:
27
4
2019
medline:
17
3
2020
entrez:
27
4
2019
Statut:
ppublish
Résumé
Animal studies indicate that the kappa-opioid receptor/dynorphin system plays an important role in cocaine binges and stress-induced relapse. Our goal was to investigate changes in kappa-opioid receptor (KOR) availability in the human brain using positron emission tomography (PET), before and after a cocaine binge. We also investigated the correlation between KOR and stress-induced cocaine self-administration. PET imaging was performed with the KOR selective agonist [
Identifiants
pubmed: 31026862
doi: 10.1038/s41386-019-0398-4
pii: 10.1038/s41386-019-0398-4
pmc: PMC6785004
doi:
Substances chimiques
Carbon Radioisotopes
0
Narcotic Antagonists
0
OPRK1 protein, human
0
Piperazines
0
Pyrrolidines
0
Receptors, Opioid, kappa
0
GR 89696
126766-32-3
Naltrexone
5S6W795CQM
Dynorphins
74913-18-1
Cocaine
I5Y540LHVR
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
1720-1727Subventions
Organisme : NCATS NIH HHS
ID : UL1 TR001863
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR000142
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA027777
Pays : United States
Références
Koob GF. Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology. 2009;56:18–31.
doi: 10.1016/j.neuropharm.2008.07.043
Trifilieff P, Martinez D. Kappa-opioid receptor signaling in the striatum as a potential modulator of dopamine transmission in cocaine dependence. Front Psychiatry. 2013;4:44.
doi: 10.3389/fpsyt.2013.00044
Shippenberg TS, Herz A. Differential effects of mu and kappa opioid systems on motivational processes. NIDA Res Monogr. 1986;75:563–6.
pubmed: 2829003
Sivam SP. Cocaine selectively increases striatonigral dynorphin levels by a dopaminergic mechanism. J Pharmacol Exp Ther. 1989;250:818–24.
pubmed: 2476548
Smiley PL, Johnson M, Bush L, Gibb JW, Hanson GR. Effects of cocaine on extrapyramidal and limbic dynorphin systems. J Pharmacol Exp Ther. 1990;253:938–43.
pubmed: 1972755
Daunais JB, Roberts DC, McGinty JF. Cocaine self-administration increases preprodynorphin, but not c-fos, mRNA in rat striatum. Neuroreport. 1993;4:543–6.
doi: 10.1097/00001756-199305000-00020
Daunais JB, Roberts DC, McGinty JF. Short-term cocaine self administration alters striatal gene expression. Brain Res Bull. 1995b;37:523–7.
doi: 10.1016/0361-9230(95)00049-K
Jenab S, Festa ED, Russo SJ, Wu HB, Inturrisi CE, Quinones-Jenab V. MK-801 attenuates cocaine induction of c-fos and preprodynorphin mRNA levels in Fischer rats. Brain Res Mol Brain Res. 2003;117:237–9.
doi: 10.1016/S0169-328X(03)00319-X
Schlussman SD, Zhang Y, Yuferov V, LaForge KS, Ho A, Kreek MJ. Acute ‘binge’ cocaine administration elevates dynorphin mRNA in the caudate putamen of C57BL/6J but not 129/J mice. Brain Res. 2003;974:249–53.
doi: 10.1016/S0006-8993(03)02561-7
Schlussman SD, Zhou Y, Bailey A, Ho A, Kreek MJ. Steady-dose and escalating-dose “binge” administration of cocaine alter expression of behavioral stereotypy and striatal preprodynorphin mRNA levels in rats. Brain Res Bull. 2005;67:169–75.
doi: 10.1016/j.brainresbull.2005.04.018
Spangler R, Ho A, Zhou Y, Maggos CE, Yuferov V, Kreek MJ. Regulation of kappa opioid receptor mRNA in the rat brain by “binge’ pattern cocaine administration and correlation with preprodynorphin mRNA. Brain Res Mol Brain Res. 1996;38:71–6.
doi: 10.1016/0169-328X(95)00319-N
Spangler R, Unterwald E, Kreek M. Binge cocaine administration induces a sustained increase of prodynorphin mRNA in rat caudate-putamen. Brain Res Mol Brain Res. 1993;19:323–7.
doi: 10.1016/0169-328X(93)90133-A
Zhou Y, Spangler R, Schlussman SD, Yuferov VP, Sora I, Ho A, et al. Effects of acute “binge” cocaine on preprodynorphin, preproenkephalin, proopiomelanocortin, and corticotropin-releasing hormone receptor mRNA levels in the striatum and hypothalamic-pituitary-adrenal axis of mu-opioid receptor knockout mice. Synapse. 2002;45:220–9.
doi: 10.1002/syn.10101
Daunais JB, McGinty JF. Cocaine binges differentially alter striatal preprodynorphin and zif/268 mRNAs. Brain Res Mol Brain Res. 1995a;29:201–10.
doi: 10.1016/0169-328X(94)00246-B
Daunais JB, McGinty JF. The effects of D1 or D2 dopamine receptor blockade on zif/268 and preprodynorphin gene expression in rat forebrain following a short-term cocaine binge. Brain Res Mol Brain Res. 1996;35:237–48.
doi: 10.1016/0169-328X(95)00226-I
Hurd YL, Herkenham M. Molecular alterations in the neostriatum of human cocaine addicts. Synapse. 1993;13:357–69.
doi: 10.1002/syn.890130408
Mash DC, Staley JK. D3 dopamine and kappa opioid receptor alterations in human brain of cocaine-overdose victims. Ann N Y Acad Sci. 1999;877:507–22.
doi: 10.1111/j.1749-6632.1999.tb09286.x
Staley JK, Rothman RB, Rice KC, Partilla J, Mash DC. Kappa2 opioid receptors in limbic areas of the human brain are upregulated by cocaine in fatal overdose victims. J Neurosci. 1997;17:8225–33.
doi: 10.1523/JNEUROSCI.17-21-08225.1997
Muschamp JW, Carlezon WA Jr. Roles of nucleus accumbens CREB and dynorphin in dysregulation of motivation. Cold Spring Harb Perspect Med. 2013;3:a012005.
doi: 10.1101/cshperspect.a012005
Bruchas MR, Land BB, Chavkin C. The dynorphin/kappa opioid system as a modulator of stress-induced and pro-addictive behaviors. Brain Res. 2010;1314:44–55.
doi: 10.1016/j.brainres.2009.08.062
Wee S, Koob GF. The role of the dynorphin-kappa opioid system in the reinforcing effects of drugs of abuse. Psychopharmacology. 2010;210:121–35.
doi: 10.1007/s00213-010-1825-8
Chavkin C, Koob GF. Dynorphin, dysphoria, and dependence: the stress of addiction. Neuropsychopharmacology. 2016;41:373–4.
doi: 10.1038/npp.2015.258
Nabulsi NB, Zheng MQ, Ropchan J, Labaree D, Ding YS, Blumberg L, et al. [11C]GR103545: novel one-pot radiosynthesis with high specific activity. Nucl Med Biol. 2011;38:215–21.
doi: 10.1016/j.nucmedbio.2010.08.014
Naganawa M, Jacobsen LK, Zheng MQ, Lin SF, Banerjee A, Byon W, et al. Evaluation of the agonist PET radioligand [(1)(1)C]GR103545 to image kappa opioid receptor in humans: kinetic model selection, test-retest reproducibility and receptor occupancy by the antagonist PF-04455242. NeuroImage. 2014;99:69–79.
doi: 10.1016/j.neuroimage.2014.05.033
Schoultz BW, Hjornevik T, Willoch F, Marton J, Noda A, Murakami Y, et al. Evaluation of the kappa-opioid receptor-selective tracer [(11)C]GR103545 in awake rhesus macaques. Eur J Nucl Med Mol Imaging. 2010;37:1174–80.
doi: 10.1007/s00259-010-1384-6
Back SE, Brady KT, Jackson JL, Salstrom S, Zinzow H. Gender differences in stress reactivity among cocaine-dependent individuals. Psychopharmacology. 2005;180:169–76.
doi: 10.1007/s00213-004-2129-7
Compton MA. Cold-pressor pain tolerance in opiate and cocaine abusers: correlates of drug type and use status. J Pain Symptom Manag. 1994;9:462–73.
doi: 10.1016/0885-3924(94)90203-8
Talbot PS, Narendran R, Butelman ER, Huang Y, Ngo K, Slifstein M, et al. 11C-GR103545, a radiotracer for imaging kappa-opioid receptors in vivo with PET: synthesis and evaluation in baboons. J Nucl Med. 2005;46:484–94.
pubmed: 15750163
Peng XM, Knapp BI, Bidlack JM, Neumeyer JL. Pharmacological properties of bivalent ligands containing butorphan linked to nalbuphine, naltrexone, and naloxone at mu, delta, and kappa opioid receptors. J Med Chem. 2007;50:2254–8.
doi: 10.1021/jm061327z
Butelman ER, Rus S, Prisinzano TE, Kreek MJ. The discriminative effects of the kappa-opioid hallucinogen salvinorin A in nonhuman primates: dissociation from classic hallucinogen effects. Psychopharmacology. 2010;210:253–62.
doi: 10.1007/s00213-009-1771-5
Martinez D, Slifstein M, Broft A, Mawlawi O, Hwang DR, Huang Y, et al. Imaging human mesolimbic dopamine transmission with positron emission tomography. Part II: amphetamine-induced dopamine release in the functional subdivisions of the striatum. J Cereb Blood Flow Metab. 2003;23:285–300.
doi: 10.1097/01.WCB.0000048520.34839.1A
Abi-Dargham A, Martinez D, Mawlawi O, Simpson N, Hwang DR, Slifstein M, et al. Measurement of striatal and extrastriatal dopamine D1 receptor binding potential with [11C]NNC 112 in humans: validation and reproducibility. J Cereb Blood Flow Metab. 2000;20:225–43.
doi: 10.1097/00004647-200002000-00003
Girgis RR, Xu X, Gil RB, Hackett E, Ojeil N, Lieberman JA, et al. Antipsychotic binding to the dopamine-3 receptor in humans: a PET study with [(11)C]-(+)-PHNO. Schizophr Res. 2015;168:373–6.
doi: 10.1016/j.schres.2015.06.027
Ichise M, Toyama H, Innis RB, Carson RE. Strategies to improve neuroreceptor parameter estimation by linear regression analysis. J Cereb Blood Flow Metab. 2002;22:1271–81.
doi: 10.1097/01.WCB.0000038000.34930.4E
Slifstein M, van de Giessen E, Van Snellenberg J, Thompson JL, Narendran R, Gil R, et al. Deficits in prefrontal cortical and extrastriatal dopamine release in schizophrenia: a positron emission tomographic functional magnetic resonance imaging study. JAMA Psychiatry. 2015;72:316–24.
doi: 10.1001/jamapsychiatry.2014.2414
Foltin RW, Fischman MW. Residual effects of repeated cocaine smoking in humans. Drug Alcohol Depend. 1997;47:117–24.
doi: 10.1016/S0376-8716(97)00093-8
Haney M, Rubin E, Foltin RW. Aripiprazole maintenance increases smoked cocaine self-administration in humans. Psychopharmacology. 2011;216:379–87.
doi: 10.1007/s00213-011-2231-6
Martinez D, Slifstein M, Narendran R, Foltin RW, Broft A, Hwang DR, et al. Dopamine D1 receptors in cocaine dependence measured with PET and the choice to self-administer cocaine. Neuropsychopharmacology. 2009;34:1774–82.
doi: 10.1038/npp.2008.235
Ward AS, Haney M, Fischman MW, Foltin RW. Binge cocaine self-administration by humans: smoked cocaine. Behav Pharmacol. 1997;8:736–44.
doi: 10.1097/00008877-199712000-00009
Kowalczyk WJ, Evans SM, Bisaga AM, Sullivan MA, Comer SD. Sex differences and hormonal influences on response to cold pressor pain in humans. J Pain. 2006;7:151–60.
doi: 10.1016/j.jpain.2005.10.004
Vadhan NP, Hart CL, Haney M, van Gorp WG, Foltin RW. Decision-making in long-term cocaine users: effects of a cash monetary contingency on Gambling task performance. Drug Alcohol Depend. 2009;102:95–101.
doi: 10.1016/j.drugalcdep.2009.02.003
Foltin RW, Ward AS, Collins ED, Haney M, Hart CL, Fischman MW. The effects of venlafaxine on the subjective, reinforcing, and cardiovascular effects of cocaine in opioid-dependent and non-opioid-dependent humans. Exp Clin Psychopharmacol. 2003;11:123–30.
doi: 10.1037/1064-1297.11.2.123
Cunningham VJ, Rabiner EA, Slifstein M, Laruelle M, Gunn RN. Measuring drug occupancy in the absence of a reference region: the Lassen plot re-visited. J Cereb Blood Flow Metab. 2010;30:46–50.
doi: 10.1038/jcbfm.2009.190
Groblewski PA, Zietz C, Willuhn I, Phillips PE, Chavkin C. Repeated stress exposure causes strain-dependent shifts in the behavioral economics of cocaine in rats. Addict Biol. 2015;20:297–301.
doi: 10.1111/adb.12123
Polter AM, Bishop RA, Briand LA, Graziane NM, Pierce RC, Kauer JA. Poststress block of kappa opioid receptors rescues long-term potentiation of inhibitory synapses and prevents reinstatement of cocaine seeking. Biol Psychiatry. 2014;76:785–93.
doi: 10.1016/j.biopsych.2014.04.019
Fagergren P, Smith HR, Daunais JB, Nader MA, Porrino LJ, Hurd YL. Temporal upregulation of prodynorphin mRNA in the primate striatum after cocaine self-administration. Eur J Neurosci. 2003;17:2212–8.
doi: 10.1046/j.1460-9568.2003.02636.x
Frankel PS, Alburges ME, Bush L, Hanson GR, Kish SJ. Striatal and ventral pallidum dynorphin concentrations are markedly increased in human chronic cocaine users. Neuropharmacology. 2008;55:41–6.
doi: 10.1016/j.neuropharm.2008.04.019
Placzek MS, Schroeder FA, Che T, Wey HY, Neelamegam R, Wang C, et al. Discrepancies in kappa opioid agonist binding revealed through PET imaging. ACS Chem Neurosci. 2018;10:384–95.
doi: 10.1021/acschemneuro.8b00293
Placzek MS, Van de Bittner GC, Wey HY, Lukas SE, Hooker JM. Immediate and persistent effects of salvinorin A on the kappa opioid receptor in rodents, monitored in vivo with PET. Neuropsychopharmacology. 2015;40:2865–72.
doi: 10.1038/npp.2015.159
Laruelle M. Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. J Cereb Blood Flow Metab. 2000;20:423–51.
doi: 10.1097/00004647-200003000-00001
Placzek MS, Zhao W, Wey HY, Morin TM, Hooker JM. PET neurochemical imaging modes. Semin Nucl Med. 2016;46:20–27.
doi: 10.1053/j.semnuclmed.2015.09.001
Tejeda HA, Bonci A. Dynorphin/kappa-opioid receptor control of dopamine dynamics: Implications for negative affective states and psychiatric disorders. Brain Res. 2018;pii: S0006-8993:30488-8.
Tejeda HA, Natividad LA, Orfila JE, Torres OV, O’Dell LE. Dysregulation of kappa-opioid receptor systems by chronic nicotine modulate the nicotine withdrawal syndrome in an age-dependent manner. Psychopharmacology. 2012;224:289–301.
doi: 10.1007/s00213-012-2752-7
Walker BM, Zorrilla EP, Koob GF. Systemic kappa-opioid receptor antagonism by nor-binaltorphimine reduces dependence-induced excessive alcohol self-administration in rats. Addict Biol. 2011;16:116–9.
doi: 10.1111/j.1369-1600.2010.00226.x
Whitfield TW Jr., Schlosburg JE, Wee S, Gould A, George O, Grant Y, et al. kappa Opioid receptors in the nucleus accumbens shell mediate escalation of methamphetamine intake. J Neurosci. 2015;35:4296–305.
doi: 10.1523/JNEUROSCI.1978-13.2015