Activation of the kappa opioid receptor in the dorsal raphe nucleus mediates the aversive effects of stress and reinstates drug seeking

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 45, 2009, Pages 19168-19173

  Land, Benjamin B ^a,b   Bruchas, Michael R ^a   Schattauer, Selena ^a   Giardino, William J ^a   Aita, Megumi ^a   Messinger, Daniel ^a   Hnasko, Thomas S ^a,b   Palmiter, Richard D ^a,b   Chavkin, Charles ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Depression; Drug addiction; Dynorphin; Serotonin

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; COCAINE; DOPAMINE; DYNORPHIN; KAPPA OPIATE RECEPTOR; LENTIVIRUS VECTOR; MITOGEN ACTIVATED PROTEIN KINASE P38;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVERSIVE BEHAVIOR; CONTROLLED STUDY; DOPAMINE RELEASE; DORSAL RAPHE NUCLEUS; GENE EXPRESSION; LIMBIC SYSTEM; MALE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PLACE PREFERENCE; PRIORITY JOURNAL; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; SIGNAL TRANSDUCTION;

3,4-DICHLORO-N-METHYL-N-(2-(1-PYRROLIDINYL)-CYCLOHEXYL)-BENZENEACETAMIDE, (TRANS)-ISOMER; ANALYSIS OF VARIANCE; ANIMALS; COCAINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; LENTIVIRUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NALTREXONE; RAPHE NUCLEI; RECEPTORS, OPIOID, KAPPA; STRESS, PHYSIOLOGICAL; VENTRAL TEGMENTAL AREA;

MUS;

EID: 73149124507     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0910705106     Document Type: Article

References (46)

1. Krishnan V, Nestler EJ (2008) The molecular neurobiology of depression. Nature 455:894-902.
2. Nestler EJ, et al. (2002) Neurobiology of depression. Neuron 34:13-25.
3. Volkow ND, Li TK (2004) Drug addiction: The neurobiology of behaviour gone awry. Nat Rev Neurosci 5:963-970.
4. MüllerMB,et al. (2003) Limbic corticotropin-releasing factorhormonereceptor1mediates anxiety-related behavior and hormonal adaptation to stress. Nat Neurosci 6:1100-1107.
5. Land BB, et al. (2008) The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J Neurosci 28:407-414.
6. Redila VA, Chavkin C (2008) Stress-induced reinstatement of cocaine seeking is mediated by the kappa opioid system. Psychopharmacology (Berl) 200:59-70.
7. Carey AN, Borozny K, Aldrich JV, McLaughlin JP (2007) Reinstatement of cocaine placeconditioning prevented by the peptide kappa-opioid receptor antagonist arodyn. Eur J Pharmacol 569:84-89.
8. McLaughlin JP, Li S, Valdez J, Chavkin TA, Chavkin C (2006) Social defeat stress-induced behavioral responses are mediated by the endogenous kappa opioid system. Neuropsychopharmacology 31:1241-1248.
9. Beardsley PM, Howard JL, Shelton KL, Carroll FI (2005) Differential effects of the novel kappa opioid receptor antagonist JDTic on reinstatement of cocaine-seeking induced by footshock vs cocaine primes and its antidepressant-like effects in rats. Psychopharmacology 183:118-126.
10. Koob GF (2008) A role for brain stress systems in addiction. Neuron 59:11-34.
11. Wise RA (2004) Dopamine learning and motivation. Nat Rev Neurosci 6:483-496.
12. Hnasko TS, Sotak BN, Palmiter RD (2005) Morphine reward in dopamine-deficient mice. Nature 438:854-857.
13. Hnasko TS, Sotak BN, Palmiter RD (2007) Cocaine-conditioned place preference by dopamine-deficient mice is mediated by serotonin. J Neurosci 27:12484-12488.
14. Amat J, et al. (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365-371.
15. Zhao ZQ, et al. (2007) Central serotonergic neurons are differentially required for opioid analgesia but not for morphine tolerance or morphine reward. Proc Natl Acad Sci USA 104:14519-14524.
16. Bals-Kubik R, Ableitner A, Herz A, Shippenberg TS (1993) Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J Pharmacol Exp Ther 264:489-495.
17. Margolis EB, HjelmstadGO,Bonci A, FieldsHL(2003) Kappa-opioid agonists directly inhibit midbrain dopaminergic neurons. J Neuro 23:9981-9986.
18. Hnasko TS, et al. (2006) Cre recombinase-mediated restoration of nigrostriatal dopamine in dopamine-deficient mice reverses hypophagia and bradykinesia. Proc Natl Acad SciUSA 103:8858-8863.
19. Horan P, Taylor J, Yamamura HI, Porreca F (1992) Extremely long-lasting antagonistic actions of nor-binaltorphimine (nor-BNI) in the mouse tail-flick test. J Pharmacol Exp Ther 260:1237-1243.
20. Bruchas MR, et al. (2007) Long-acting kappa opioid antagonists disrupt receptor signaling and produce noncompetitive effects by activating c-Jun N-terminal kinase. J Biol Chem 282:29803-29811.
21. McLaughlin JP, Xu M, Mackie K, Chavkin C (2003) Phosphorylation of a carboxyl-terminal serine within the kappa-opioid receptor produces desensitization and internalization. J Biol Chem 278:34631-34640.
22. Maskos U, et al. (2005) Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 436:103-107.
23. Hough LB, et al. (2000) Improgan a cimetidine analog induces morphine-like antinociception in opioid receptor-knockout mice. Brain Res 880:102-108.
24. Bruchas MR, Macey TA, Lowe JD, Chavkin C(2006)Kappaopioid receptor activation of p38 MAPKis GRK3- and arrestin-dependent in neurons and astrocytes. J BiolChem281:18081-18089.
25. Bruchas MR, et al. (2007) Stress-induced p38 mitogen-activated protein kinase activation mediates kappa-opioid-dependent dysphoria. J Neurosci 27:11614-11623.
26. Belcheva MM, et al. (1998) Opioid modulation of extracellular signal-regulated protein kinase activity is ras-dependent and involvesGbetagammasubunits. J Neurochem 70:635-645.
27. Reynolds SM, Berridge KC (2002) Positive and negative motivation in nucleus accumbens shell: Bivalent rostrocaudal gradients for GABA-elicited eating taste ''liking''/''disliking'' reactions place preference/avoidance and fear. J Neurosci 22:7308-7320.
28. Shirayama Y, et al. (2004) Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. J Neurochem 90:1258-1268.
29. Sora I, et al. (2001) Molecular mechanisms of cocaine reward: Combined dopamine and serotonin transporter knockouts eliminate cocaine place preference. Proc Natl Acad Sci USA 98:5300-5305.
30. Neumaier JF, Vincow ES Arvanitogiannis A, Wise RA, Carlezon WA Jr (2002) Elevated expression of 5-HT1B receptors in nucleus accumbens efferents sensitizes animals to cocaine. J Neurosci 22:10856-10863.
31. Le AD, et al. (2002) The role of corticotropin-releasing factor in the median raphe nucleus in relapse to alcohol. J Neurosci 22:7844-7849.
32. Tao R, Auerbach SB (2002) Opioid receptor subtypes differentially modulate serotonin efflux in the rat central nervous system. J Pharmacol Exp Ther 303:549-556.
33. Grudt TJ, Williams JT (1995) Opioid receptors and the regulation of ion conductances. Rev Neurosci 6:279-286.
34. Shippenberg TS, Herz A (1987) Place preference conditioning reveals involvement of D1-dopamine receptors in the motivational properties of mu and kappa-opioid agonists. Brain Res 436:169-172.
35. Shippenberg TS, Herz A (1988) Motivational effects of opioids: Influence of D1 vs D2 receptor antagonists. Euro J Pharmacol 151:233-242.
36. Prasad HC, et al. (2005) Human serotonin transporter variants display altered sensitivity to protein kinase G and p38-mitogen-activated protein kinase. Proc Natl Acad Sci USA 102:11545-11550.
37. Thomas GM, Huganir RL (2004) MAPK signaling and synaptic plasticity. Nat Rev Neurosci 5:173-183.
38. Rumbaugh G, Adams JP, Kim JH, Huganir RL (2006) SynGAP regulates synaptic strength and mitogen-activated protein kinases in cultured neurons. Proc Natl Acad Sci USA 103:4344-4351.
39. Pfeiffer A, Brantl V, Herz A, EmrichHM(1986) Psychotomimesis mediated by kappa opiate receptors. Science 233:774-776.
40. Shippenberg TS, Herz A (1986) Differential effects of mu and kappa opioid systems on motivational processes. NIDA Res Monogr 75:563-566.
41. Wittmann W, et al. (2009) Prodynorphin-derived peptides are critical modulators of anxiety and regulate neurochemistry and corticosterone. Neuropsychopharmacology 34:775-785.
42. McLaughlin JP, Marton-Popovici M, Chavkin C (2003) Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23:5674-5683.
43. Walker BM, Koob GF (2008) Pharmacological evidence for a motivational role of kappaopioid systems in ethanol dependence. Neuropsychopharmacology 33:643-652.
44. Sirven A, et al. (2001) Enhanced transgene expression in cord blood CD34(+)-derived hematopoietic cells including developing T cells and NOD/SCID mouse repopulating cells following transduction with modified trip lentiviral vectors. Mol Ther 3:438-448.
45. Zufferey A, et al. (1998) Self-inactivating lentivirus vector for safeandefficient in vivogene delivery. J Virol 72:9873-9880.
46. Zennou V, et al. (2001) The HIV-1 DNA flap stimulates HIV vector-mediated cell transduction in the brain. Nat Biotechnol 19:446-450.