The Behavioral Effects of the Antidepressant Tianeptine Require the Mu-Opioid Receptor

Neuropsychopharmacology

Volumn 42, Issue 10, 2017, Pages 2052-2063

  Samuels, Benjamin Adam ^a   Nautiyal, Katherine M ^b   Kruegel, Andrew C ^c   Levinstein, Marjorie R ^b   Magalong, Valerie M ^b   Gassaway, Madalee M ^c   Grinnell, Steven G ^b   Han, Jaena ^c   Ansonoff, Michael A ^d   Pintar, John E ^d   Javitch, Jonathan A ^b   Sames, Dalibor ^c   Hen, René ^b  

^a RUTGERS UNIVERSITY   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c Howard Hughes Medical Institute   (United States)

^d RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MORPHINE; MU OPIATE RECEPTOR; NARCOTIC ANALGESIC AGENT; OPRM PROTEIN, MOUSE; OPRM1 PROTEIN, HUMAN; THIAZEPINE DERIVATIVE; TIANEPTINE; TRICYCLIC ANTIDEPRESSANT AGENT;

AGONISTS; ANIMAL; C57BL MOUSE; CHEMICAL STRUCTURE; DEPRESSION; DOSE RESPONSE; DRUG TOLERANCE; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM;

ANALGESICS, OPIOID; ANIMALS; ANTIDEPRESSIVE AGENTS, TRICYCLIC; DEPRESSIVE DISORDER; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG TOLERANCE; HEK293 CELLS; HUMANS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR STRUCTURE; MORPHINE; RECEPTORS, OPIOID, MU; THIAZEPINES;

EID: 85017625656     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2017.60     Document Type: Article

References (68)

1. Aleksandrovskii Iu A, Avedisova AS, Boev IV, Bukhanovkskii AO, Voloshin VM, Tsygankov BD et al (2005). Efficacy and tolerability of coaxil (tianeptine) in the therapy of posttraumatic stress disorder. Zh Nevrol Psikhiatr Im S S Korsakova 105: 24–29.
2. Almatroudi A, Husbands SM, Bailey CP, Bailey SJ (2015). Combined administration of buprenorphine and naltrexone produces antidepressant-like effects in mice. J Psychopharmacol 29: 812–821. DOI: 10.1177/0269881115586937
3. Atmaca M, Kuloglu M, Tezcan E, Buyukbayram A (2003). Switching to tianeptine in patients with antidepressant-induced sexual dysfunction. Hum Psychopharmacol 18: 277–280. DOI: 10.1002/hup.479
4. Belknap JK, Noordewier B, Lame M (1989). Genetic dissociation of multiple morphine effects among C57BL/6J, DBA/2J and C3H/HeJ inbred mouse strains. Physiol Behav 46: 69–74. DOI: 10.1016/0031-9384(89)90324-7
5. Belknap JK, Riggan J, Cross S, Young ER, Gallaher EJ, Crabbe JC (1998). Genetic determinants of morphine activity and thermal responses in 15 inbred mouse strains. Pharmacol Biochem Behav 59: 353–360. DOI: 10.1016/S0091-3057(97)00421-8
6. Berman RM, Cappiello A, Anand A, Oren DA, Heninger GR, Charney DS et al (2000). Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 47: 351–354. DOI: 10.1016/S0006-3223(99)00230-9
7. Bernard K, Penelaud PF, Mocaer E, Donazzolo Y (2011). Absence of psychostimulant effects of a supratherapeutic dose of tianeptine: a placebo-controlled study versus methylphenidate in young healthy volunteers. J Clin Psychopharmacol 31: 441–448. DOI: 10.1097/JCP.0b013e3182217a50
8. Brady KT, McCauley JL, Back SE (2016). Prescription Opioid Misuse, Abuse, and Treatment in the United States: An Update. Am J Psychiatry 173: 18–26. DOI: 10.1176/appi.ajp.2015.15020262
9. Brase DA, Loh HH, Way EL (1977). Comparison of the effects of morphine on locomotor activity, analgesia and primary and protracted physical dependence in six mouse strains. J Pharmacol Exp Ther 201: 368–374.
10. Broom DC, Jutkiewicz EM, Folk JE, Traynor JR, Rice KC, Woods JH (2002). Nonpeptidic delta-opioid receptor agonists reduce immobility in the forced swim assay in rats. Neuropsychopharmacology 26: 744–755. DOI: 10.1016/S0893-133X(01)00413-4
11. Carlezon WA Jr, Beguin C, Knoll AT, Cohen BM (2009). Kappa-opioid ligands in the study and treatment of mood disorders. Pharmacol Ther 123: 334–343. DOI: 10.1016/j.pharmthera.2009.05.008
12. Carr GV, Bangasser DA, Bethea T, Young M, Valentino RJ, Lucki I (2010). Antidepressant-like effects of kappa-opioid receptor antagonists in Wistar Kyoto rats. Neuropsychopharmacology 35: 752–763. DOI: 10.1038/npp.2009.183
13. Chavkin C (2011). The therapeutic potential of kappa-opioids for treatment of pain and addiction. Neuropsychopharmacology 36: 369–370. DOI: 10.1038/npp.2010.137
14. Couet W, Girault J, Latrille F, Salvadori C, Fourtillan JB (1990). Kinetic profiles of tianeptine and its MC5 metabolite in plasma, blood and brain after single and chronic intraperitoneal administration in the rat. Eur J Drug Metab Pharmacokinet 15: 69–74. DOI: 10.1007/BF03190130
15. Cryan JF, Lucki I (2000). Antidepressant-like behavioral effects mediated by 5-Hydroxytryptamine(2C) receptors. J Pharmacol Exp Ther 295: 1120–1126.
16. Cryan JF, Valentino RJ, Lucki I (2005). Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 29: 547–569. DOI: 10.1016/j.neubiorev.2005.03.008
17. David DJ, Samuels BA, Rainer Q, Wang J-W, Marsteller D, Mendez I et al (2009a). Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62: 479–493. DOI: 10.1016/j.neuron.2009.04.017
18. David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D, Mendez I et al (2009b). Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62: 479–493. DOI: 10.1016/j.neuron.2009.04.017
19. Ehrich E, Turncliff R, Du Y, Leigh-Pemberton R, Fernandez E, Jones R et al (2015). Evaluation of opioid modulation in major depressive disorder. Neuropsychopharmacology 40: 1448–1455. DOI: 10.1038/npp.2014.330
20. Fava M, Memisoglu A, Thase ME, Bodkin JA, Trivedi MH, de Somer M et al (2016). Opioid modulation with buprenorphine/samidorphan as adjunctive treatment for inadequate response to antidepressants: a randomized double-blind placebo-controlled trial. Am J Psychiatry 173: 499–508. DOI: 10.1176/appi.ajp.2015.15070921
21. Filliol D, Ghozland S, Chluba J, Martin M, Matthes HW, Simonin F et al (2000). Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses. Nature genetics 25: 195–200. DOI: 10.1038/76061
22. Furey ML, Drevets WC (2006). Antidepressant efficacy of the antimuscarinic drug scopolamine: a randomized, placebo-controlled clinical trial. Arch Gen Psychiatry 63: 1121–1129. DOI: 10.1001/archpsyc.63.10.1121
23. Gassaway MM, Rives ML, Kruegel AC, Javitch JA, Sames D (2014). The atypical antidepressant and neurorestorative agent tianeptine is a mu-opioid receptor agonist. Transl Psychiatry 4: e411. DOI: 10.1038/tp.2014.30
24. Grislain L, Gele P, Bertrand M, Luijten W, Bromet N, Salvadori C et al (1990). The metabolic pathways of tianeptine, a new antidepressant, in healthy volunteers. Drug Metab Dispos 18: 804–808.
25. Guillem E, Lepine JP (2003). Does addiction to antidepressants exist? About a case of one addiction to tianeptine. Encephale 29: 456–459.
26. Hsu DT, Sanford BJ, Meyers KK, Love TM, Hazlett KE, Walker SJ et al (2015). It still hurts: altered endogenous opioid activity in the brain during social rejection and acceptance in major depressive disorder. Mol Psychiatry 20: 193–200. DOI: 10.1038/mp.2014.185
27. Hsu DT, Sanford BJ, Meyers KK, Love TM, Hazlett KE, Wang H et al (2013a). Response of the mu-opioid system to social rejection and acceptance. Mol Psychiatry 18: 1211–1217. DOI: 10.1038/mp.2013.96
28. Hsu DT, Sanford BJ, Meyers KK, Love TM, Hazlett KE, Wang H et al (2013b). Social feedback activates the endogenous opioid system. Mol Psychiatry 18: 1147. DOI: 10.1038/mp.2013.139
29. Karpukhin IB (2009). Use of Coaxil (tianeptine) in elderly patients with combined mild cognitive and depressive-anxiety disorders. Neurosci Behav Physiol 39: 53–56. DOI: 10.1007/s11055-008-9099-x
30. Kasper S, McEwen BS (2008). Neurobiological and clinical effects of the antidepressant tianeptine. CNS Drugs 22: 15–26. DOI: 10.2165/00023210-200822010-00002
31. Lee NM, Smith AP (2002). Opioid receptor polymorphisms and opioid abuse. Pharmacogenomics 3: 219–227. DOI: 10.1517/14622416.3.2.219
32. Leterme L, Singlan YS, Auclair V, Le Boisselier R, Frimas V (2003). Misuse of tianeptine: five cases of abuse. Ann Med Interne (Paris) 154 Spec No 2: S58–S63.
33. Levin OS (2007). Coaxil (tianeptine) in the treatment of depression in Parkinson's disease. Neurosci Behav Physiol 37: 419–424. DOI: 10.1007/s11055-007-0029-0
34. Levine AS, Morley JE, Gosnell BA, Billington CJ, Bartness TJ (1985). Opioids and consummatory behavior. Brain Res Bull 14: 663–672. DOI: 10.1016/0361-9230(85)90116-9
35. Lotsch J, Geisslinger G (2005). Are mu-opioid receptor polymorphisms important for clinical opioid therapy? Trends Mol Med 11: 82–89. DOI: 10.1016/j.molmed.2004.12.006
36. Lutz PE, Kieffer BL (2013). Opioid receptors: distinct roles in mood disorders. Trends Neurosci 36: 195–206.
37. Mague SD, Pliakas AM, Todtenkopf MS, Tomasiewicz HC, Zhang Y, Stevens WC Jr et al (2003). Antidepressant-like effects of kappa-opioid receptor antagonists in the forced swim test in rats. J Pharmacol Exp Ther 305: 323–330. DOI: 10.1124/jpet.102.046433
38. Marki A, Monory K, Otvos F, Toth G, Krassnig R, Schmidhammer H et al (1999). Mu-opioid receptor specific antagonist cyprodime: characterization by in vitro radioligand and [35S]GTPgammaS binding assays. Eur J Pharmacol 383: 209–214. DOI: 10.1016/S0014-2999(99)00610-X
39. McEwen BS, Chattarji S, Diamond DM, Jay TM, Reagan LP, Svenningsson P et al (2010). The neurobiological properties of tianeptine (Stablon): from monoamine hypothesis to glutamatergic modulation. Mol Psychiatry 15: 237–249. DOI: 10.1038/mp.2009.80
40. 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. DOI: 10.1523/JNEUROSCI.23-13-05674.2003
41. Naidu PS, Lichtman AH, Archer CC, May EL, Harris LS, Aceto MD (2007). NIH 11082 produces anti-depressant-like activity in the mouse tail-suspension test through a delta-opioid receptor mechanism of action. Eur J Pharmacol 566: 132–136. DOI: 10.1016/j.ejphar.2007.03.031
42. Negri A, Rives ML, Caspers MJ, Prisinzano TE, Javitch JA, Filizola M (2013). Discovery of a novel selective kappa-opioid receptor agonist using crystal structure-based virtual screening. J Chem Inf Model 53: 521–526. DOI: 10.1021/ci400019t
43. Newton SS, Thome J, Wallace TL, Shirayama Y, Schlesinger L, Sakai N et al (2002). Inhibition of cAMP response element-binding protein or dynorphin in the nucleus accumbens produces an antidepressant-like effect. J Neurosci 22: 10883–10890. DOI: 10.1523/JNEUROSCI.22-24-10883.2002
44. Oliverio A, Castellano C (1974a). Experience modifies morphine-induced behavioral excitation of mice. Nature 252: 229–230. DOI: 10.1038/252229a0
45. Oliverio A, Castellano C (1974b). Genotype-dependent sensitivity and tolerance to morphine and heroin: dissociation between opiate-induced running and analgesia in the mouse. Psychopharmacologia 39: 13–22. DOI: 10.1007/BF00421454
46. Onder E, Tural U, Aker T (2006). A comparative study of fluoxetine, moclobemide, and tianeptine in the treatment of posttraumatic stress disorder following an earthquake. Eur Psychiatry 21: 174–179. DOI: 10.1016/j.eurpsy.2005.03.007
47. Porsolt RD, Bertin A, Jalfre M (1977). Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodynam Ther 229: 327–336.
48. Richards EM, Mathews DC, Luckenbaugh DA, Ionescu DF, Machado-Vieira R, Niciu MJ et al (2016). A randomized, placebo-controlled pilot trial of the delta opioid receptor agonist AZD2327 in anxious depression. Psychopharmacology 233: 1119–1130. DOI: 10.1007/s00213-015-4195-4
49. Rives ML, Rossillo M, Liu-Chen LY, Javitch JA (2012). 6'-Guanidinonaltrindole (6'-GNTI) is a G protein-biased kappa-opioid receptor agonist that inhibits arrestin recruitment. J Biol Chem 287: 27050–27054. DOI: 10.1074/jbc.C112.387332
50. Rush AJ, Trivedi MH, Wisniewski SR, Nierenberg AA, Stewart JW, Warden D et al (2006). Acute and longer-term outcomes in depressed outpatients requiring one or several treatment steps: a STAR*D report. Am J Psychiatry 163: 1905–1917. DOI: 10.1176/ajp.2006.163.11.1905
51. Saatcioglu O, Erim R, Cakmak D (2006). A case of tianeptine abuse. Turk Psikiyatri Derg 17: 72–75.
52. Saitoh A, Kimura Y, Suzuki T, Kawai K, Nagase H, Kamei J (2004). Potential anxiolytic and antidepressant-like activities of SNC80, a selective delta-opioid agonist, in behavioral models in rodents. J Pharmacol Sci 95: 374–380. DOI: 10.1254/jphs.FPJ04014X
53. Samuels BA, Hen R. Chapter 7: Novelty-suppressed feeding in the mouse. Mood and anxiety related phenotypes in mice: characterization using behavioral tests. Todd D. Gould (ed). Volume 2. Springer Protocols Neuromethods. 2012, p 107–121.
54. Sanacora G, Smith MA, Pathak S, Su HL, Boeijinga PH, McCarthy DJ et al (2014). Lanicemine: a low-trapping NMDA channel blocker produces sustained antidepressant efficacy with minimal psychotomimetic adverse effects. Mol Psychiatry 19: 978–985. DOI: 10.1038/mp.2013.130
55. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S et al (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301: 805–809. DOI: 10.1126/science.1083328
56. Schuller AG, King MA, Zhang J, Bolan E, Pan YX, Morgan DJ et al (1999). Retention of heroin and morphine-6 beta-glucuronide analgesia in a new line of mice lacking exon 1 of MOR-1. Nat Neurosci 2: 151–156. DOI: 10.1038/5706
57. Shirayama Y, Ishida H, Iwata M, Hazama GI, Kawahara R, Duman RS (2004). Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. J Neurochem 90: 1258–1268. DOI: 10.1111/j.1471-4159.2004.02589.x
58. Smith K (2014). Mental health: a world of depression. Nature 515: 181.
59. Svenningsson P, Bateup H, Qi H, Takamiya K, Huganir RL, Spedding M et al (2007). Involvement of AMPA receptor phosphorylation in antidepressant actions with special reference to tianeptine. Eur J Neurosci 26: 3509–3517. DOI: 10.1111/j.1460-9568.2007.05952.x
60. Tejedor-Real P, Mico JA, Smadja C, Maldonado R, Roques BP, Gilbert-Rahola J (1998). Involvement of delta-opioid receptors in the effects induced by endogenous enkephalins on learned helplessness model. Eur J Pharmacol 354: 1–7. DOI: 10.1016/S0014-2999(98)00423-3
61. Torregrossa MM, Jutkiewicz EM, Mosberg HI, Balboni G, Watson SJ, Woods JH (2006). Peptidic delta opioid receptor agonists produce antidepressant-like effects in the forced swim test and regulate BDNF mRNA expression in rats. Brain Res 1069: 172–181. DOI: 10.1016/j.brainres.2005.11.005
62. Vadachkoria D, Gabunia L, Gambashidze K, Pkhaladze N, Kuridze N (2009). Addictive potential of Tianeptine—the threatening reality. Georgian Med News 174: 92–94.
63. Vandel P, Regina W, Bonin B, Sechter D, Bizouard P (1999). Abuse of tianeptine. A case report. Encephale 25: 672–673.
64. Voikar V, Koks S, Vasar E, Rauvala H (2001). Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol Behav 72: 271–281. DOI: 10.1016/S0031-9384(00)00405-4
65. Warden D, Rush AJ, Trivedi MH, Fava M, Wisniewski SR (2007). The STAR*D Project results: a comprehensive review of findings. Curr Psychiatry Rep 9: 449–459. DOI: 10.1007/s11920-007-0061-3
66. Wenger GR (1989). The role of control activity levels in the reported strain differences to the behavioral effects of drugs in mice. Pharmacol Biochem Behav 32: 241–247. DOI: 10.1016/0091-3057(89)90240-2
67. Woo YS, Bahk WM, Jeong JH, Lee SH, Sung HM, Pae CU et al (2013). Tianeptine combination for partial or non-response to selective serotonin re-uptake inhibitor monotherapy. Psychiatry Clin Neurosci 67: 219–227. DOI: 10.1111/pcn.12042
68. Zarate CA, Singh JB, Carlson PJ, Brutsche NE, Ameli R, Luckenbaugh DA et al (2006). A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 63: 856–864. DOI: 10.1001/archpsyc.63.8.856