A role for the mu opioid receptor in the antidepressant effects of buprenorphine

Behavioural Brain Research

Volumn 319, Issue , 2017, Pages 96-103

  Robinson, Shivon A ^a   Erickson, Rebecca L ^a   Browne, Caroline A ^a   Lucki, Irwin ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Antidepressant; Buprenorphine; Endogenous opioid system; Novelty induced hypophagia

Indexed keywords

BUPRENORPHINE; CYPRODIME; MU OPIATE RECEPTOR; NALTREXONE; ANTIDEPRESSANT AGENT; KAPPA OPIATE RECEPTOR; MORPHINAN DERIVATIVE; NARCOTIC ANTAGONIST; OPRM PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANTIDEPRESSANT ACTIVITY; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DEPRESSION; GENE DELETION; LATENT PERIOD; MALE; MOUSE; NONHUMAN; NOVELTY INDUCED HYPOPHAGIA TEST; NOVELTY SUPPRESSED FEEDING TEST; PRIORITY JOURNAL; TASK PERFORMANCE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; DEFICIENCY; DRUG EFFECTS; EATING DISORDER; FEEDING BEHAVIOR; GENETICS; KNOCKOUT MOUSE; METABOLISM; PAIN MEASUREMENT; REACTION TIME;

ANIMALS; ANTIDEPRESSIVE AGENTS; BEHAVIOR, ANIMAL; BUPRENORPHINE; FEEDING AND EATING DISORDERS; FEEDING BEHAVIOR; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MORPHINANS; NALTREXONE; NARCOTIC ANTAGONISTS; PAIN MEASUREMENT; REACTION TIME; RECEPTORS, OPIOID, KAPPA; RECEPTORS, OPIOID, MU;

EID: 84995900524     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2016.10.050     Document Type: Article

References (48)

1. [1] Almatroudi, A., Husbands, S.M., Bailey, C.P., Bailey, S.J., Combined administration of buprenorphine and naltrexone produces antidepressant-like effects in mice. J. Psychopharmacol. 29 (2015), 812–821.
2. [2] Bansinath, M., Ramabadran, K., Turndorf, H., Puig, M.M., Effects of the benzomorphan kappa-opiate, MR 2266 and its (+) enantiomer MR 2267, on thermonociceptive reactions in different strains of mice. Neurosci. Lett. 117 (1990), 212–217.
3. [3] Bodkin, J.A., Zomberg, G.L., Lukas, S.E., Cole, J.O., Buprenorphine treatment of refractory depression. J. Clin. Psychopharmacol. 15 (1995), 49–57.
4. [4] Bodnoff, S.R., Suranyi-Cadotte, B., Quirion, R., Meaney, M.J., A comparison of the effects of diazepam versus several typical and atypical anti-depressant drugs in an animal model of anxiety. Psychopharmacology 97 (1989), 277–279.
5. [5] Bodnoff, S.R., Suranyi-Cadotte, B., Aitken, D.H., Quirion, R., Meaney, M.J., The effects of chronic antidepressant treatment in an animal model of anxiety. Psychopharmacology 95 (1988), 298–302.
6. [6] Browne, C.A., van Nest, D.S., Lucki, I., Antidepressant-like effects of buprenorphine in rats are strain dependent. Behav. Brain Res. 278 (2015), 385–392.
7. [7] Bruchas, M.R., Land, B.B., Chavkin, C., The dynorphin/kappa opioid system as a modulator of stress-induced and pro-addictive behaviors. Brain Res. 1314 (2010), 44–55.
8. [8] Bruchas, M.R., Land, B.B., Lemos, J.C., Chavkin, C., CRF1-R activation of the dynorphin/kappa opioid system in the mouse basolateral amygdala mediates anxiety-like behavior. PLoS One, 4, 2009, e8528.
9. [9] Carlezon, W.A. Jr., Beguin, C., DiNieri, J.A., Baumann, M.H., Richards, M.R., Todtenkopf, M.S., Rothman, R.B., Ma, Z., Lee, D.Y., Cohen, B.M., Depressive-like effects of the kappa-opioid receptor agonist salvinorin A on behavior and neurochemistry in rats. J. Pharmacol. Exp. Therap. 316 (2006), 440–447.
10. [10] Carr, G.V., Bangasser, D.A., Bethea, T., Young, M., Valentino, R.J., Lucki, I., Antidepressant-like effects of kappa-opioid receptor antagonists in Wistar Kyoto rats. Neuropsychopharmacology 35 (2010), 752–763.
11. [11] Contet, C., Kieffer, B.L., Befort, K., Mu opioid receptor: a gateway to drug addiction. Curr. Opin. Neurobiol. 14 (2004), 370–378.
12. [12] Cowan, A., Lewis, J.W., Macfarlane, I.R., Agonist and antagonist properties of buprenorphine, a new antinociceptive agent. Br. J. Pharmacol. 60 (1977), 537–545.
13. [13] Devine, D.P., Leone, P., Wise, R.A., Mesolimbic dopamine neurotransmission is increased by administration of mu-opioid receptor antagonists. Eur. J. Pharmacol. 243 (1993), 55–64.
14. [14] Dulawa, S.C., Hen, R., Recent advances in animal models of chronic antidepressant effects: the novelty-induced hypophagia test. Neurosci. Biobehav. Rev. 29 (2005), 771–783.
15. [15] Ehrich, E., Turncliff, R., Leigh-Pemberton, R., Fernandez, E., Jones, R., Fava, M., Evaluation of opioid modulation in major depressive disorder. Neuropsychopharmacology 40 (2015), 1448–1455.
16. [16] Falcon, E., Maier, K., Robinson, S.A., Hill-Smith, T.E., Lucki, I., Effects of buprenorphine on behavioral tests for antidepressant and anxiolytic drugs in mice. Psychopharmacology 232 (2015), 907–915.
17. [17] Falcon, E., Browne, C.A., Leon, R.M., Fleites, V.C., Sweeney, R., Kirby, L.G., Lucki, I., Antidepressant-like effects of buprenorphine are mediated by kappa opioid receptors. Neuropsychopharmacology 41 (2016), 2344–2351.
18. [18] Filliol, D., Ghozland, S., Chluba, J., Martin, M., Matthes, H.W., Simonin, F., Befort, K., Gaveriaux-Ruff, C., Dierich, A., LeMeur, M., Valverde, O., Maldonado, R., Kieffer, B.L., Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses. Nat. Gen. 25 (2000), 195–200.
19. [19] Gamble-George, J.C., Baldi, R., Halladay, L., Kocharian, A., Hartley, N., Silva, C.G., Roberts, H., Haymer, A., Marnett, L.J., Holmes, A., Patel, S., Cyclooxygenase-2 inhibition reduces stress-induced affective pathology. eLife, 5, 2016, e14137.
20. [20] Gomes, I., Jordan, B.A., Gupta, A., Trapaidze, N., Nagy, V., Devi, L.A., Heterodimerization of mu and delta opioid receptors: a role in opiate synergy. J. Neurosci., 20, 2000, RC110.
21. [21] Huang, P., Yakovleva, T., Aldrich, J.V., Tunis, J., Parry, C., Liu-Chen, L.Y., Two short-acting kappa opioid receptor antagonists (zyklophin and LY2444296) exhibited different behavioral effects from the long-acting antagonist norbinaltorphimine in mouse anxiety tests. Neurosci. Lett. 615 (2016), 15–20.
22. [22] Ide, S., Sora, I., Ikeda, K., Minami, M., Uhl, G.R., Ishihara, K., Reduced emotional and corticosterone responses to stress in mu-opioid receptor knockout mice. Neuropharmacology 58 (2010), 241–247.
23. [23] Johnson, S.W., North, R.A., Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 12 (1992), 483–488.
24. [24] Kieffer, B.L., Gaveriaux-Ruff, C., Exploring the opioid system by gene knockout. Prog. Neurobiol. 66 (2002), 285–306.
25. [25] Knoll, A.T., Meloni, E.G., Thomas, J.B., Carroll, F.I., Carlezon, W.A. Jr., Anxiolytic-like effects of kappa-opioid receptor antagonists in models of unlearned and learned fear in rats. J. Pharmacol. Exp. Therap. 323 (2007), 838–845.
26. [26] Lalanne, L., Ayranci, G., Kieffer, B.L., Lutz, P.E., The kappa opioid receptor: from addiction to depression, and back. Front Psychiatry, 5, 2014, 170.
27. [27] Latagliata, E.C., Valzania, A., Pascucci, T., Campus, P., Cabib, S., Puglisi-Allegra, S., Stress-induced activation of ventral tegmental mu-opioid receptors reduces accumbens dopamine tone by enhancing dopamine transmission in the medial pre-frontal cortex. Psychopharmacology 231 (2014), 4099–4108.
28. [28] Lutfy, K., Cowan, A., Buprenorphine: a unique drug with complex pharmacology. Curr. Neuropharmacol. 2 (2004), 395–402.
29. [29] Lutz, P.E., Kieffer, B.L., The multiple facets of opioid receptor function: implications for addiction. Curr. Opin. Neurobiol. 23 (2013), 473–479.
30. [30] Mague, S.D., Pliakas, A.M., Todtenkopf, M.S., Tomasiewicz, H.C., Zhang, Y., Stevens, W.C. Jr., Jones, R.M., Portoghese, P.S., Carlezon, W.A. Jr., Antidepressant-like effects of kappa-opioid receptor antagonists in the forced swim test in rats. J. Pharmacol. Exp. Therap. 305 (2003), 323–330.
31. [31] Marki, A., Monory, K., Otvos, F., Toth, G., Krassnig, R., Schmidhammer, H., Traynor, J.R., Roques, B.P., Maldonado, R., Borsodi, A., Mu-opioid receptor specific antagonist cyprodime: characterization by in vitro radioligand and [35S]GTPgammaS binding assays. Eur. J. Pharmacol. 383 (1999), 209–214.
32. [32] Matthes, H.W., Maldonado, R., Simonin, F., Valverde, O., Slowe, S., Kitchen, I., Befort, K., Dierich, A., Le Meur, M., Dolle, P., Tzavara, E., Hanoune, J., Roques, B.P., Kieffer, B.L., Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383 (1996), 819–823.
33. [33] McLaughlin, J.P., Marton-Popovici, M., Chavkin, C., Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J. Neurosci. 23 (2003), 5674–5683.
34. [34] McLaughlin, J.P., Land, B.B., Li, S., Pintar, J.E., Chavkin, C., Prior activation of kappa opioid receptors by U50,488 mimics repeated forced swim stress to potentiate cocaine place preference conditioning. Neuropsychopharmacology 31 (2006), 787–794.
35. [35] McLaughlin, J.P., Li, S., Valdez, J., Chavkin, T.A., Chavkin, C., Social defeat stress-Induced behavioral responses are mediated by the endogenous kappa opioid system. Neuropsychopharmacology 31 (2006), 1241–1248.
36. [36] Menzies, J.R., Skibicka, K.P., Leng, G., Dickson, S.L., Ghrelin, reward and motivation. Endocr. Dev. 25 (2013), 101–111.
37. [37] Nyhuis, P.W., Gastpar, M., Scherbaum, N., Opiate treatment in depression refractory to antidepressants and electroconvulsive therapy. J. Clin. Psychopharmacol. 28 (2008), 593–595.
38. [38] Papaleo, F., Kieffer, B.L., Tabarin, A., Contarino, A., Decreased motivation to eat in mu-opioid receptor-deficient mice. Eur. J. Neurosci. 25 (2007), 3398–3405.
39. [39] Redila, V.A., Chavkin, C., Stress-induced reinstatement of cocaine seeking is mediated by the kappa opioid system. Psychopharmacology 200 (2008), 59–70.
40. [40] Shirayama, Y., Ishida, H., Iwata, M., Hazama, G.I., Kawahara, R., Duman, R.S., Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. J. Neurochem. 90 (2004), 1258–1268.
41. [41] Slowe, S.J., Simonin, F., Kieffer, B., Kitchen, I., Quantitative autoradiography of mu-,delta- and kappa1 opioid receptors in kappa-opioid receptor knockout mice. Brain Res. 818 (1999), 335–345.
42. [42] Spanagel, R., Herz, A., Shippenberg, T.S., Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. PNAS 89 (1992), 2046–2050.
43. [43] Walker, E.A., Zering, G., Woods, J.H., Buprenorphine antagonism of mu opioids in the rhesus monkey tail-withdrawal procedure. J. Pharmacol. Exp. Therap. 273 (1995), 1345–1352.
44. [44] Wiley, M.D., Poveromo, L.B., Antapasis, J., Herrera, C.M., Bolanos Guzman, C.A., Kappa-opioid system regulates the long-lasting behavioral adaptations induced by early-life exposure to methylphenidate. Neuropsychopharmacology 34 (2009), 1339–1350.
45. [45] Wilson, M.A., Junor, L., The role of amygdalar mu-opioid receptors in anxiety-related responses in two rat models. Neuropsychopharmacology 33 (2008), 2957–2968.
46. [46] Wittmann, W., Schunk, E., Rosskothen, I., Gaburro, S., Singewald, N., Herzog, H., Schwarzer, C., Prodynorphin-derived peptides are critical modulators of anxiety and regulate neurochemistry and corticosterone. Neuropsychopharmacology 34 (2009), 775–785.
47. [47] Yoshida, M., Ohdo, S., Takane, H., Tomiyoshi, Y., Matsuo, A., Yukawa, E., Higuchi, S., Chronopharmacology of analgesic effect and its tolerance induced by morphine in mice. J. Pharmacol. Exp. Therap. 305 (2003), 1200–1205.
48. [48] Yovell, Y., Bar, G., Mashiah, M., Baruch, Y., Briskman, I., Asherov, J., Lotan, A., Rigbi, A., Panksepp, J., Ultra-low-dose buprenorphine as a time-limited treatment for severe suicidal ideation: a randomized controlled trial. Am. J. Psychiatry 173 (2015), 491–498.