Advertisement

Psychopharmacology

, Volume 236, Issue 11, pp 3147–3158 | Cite as

Sigma-1 receptor ligand PD144418 and sigma-2 receptor ligand YUN-252 attenuate the stimulant effects of methamphetamine in mice

  • Melissa A. TapiaEmail author
  • John R. Lever
  • Susan Z. Lever
  • Matthew J. Will
  • Eric S. Park
  • Dennis K. Miller
Original Investigation

Abstract

Rationale

Previous research indicates that the selective sigma-1 receptor ligand PD144418 and the selective sigma-2 ligands YUN-252 can inhibit cocaine-induced hyperactivity. The effects of these ligands on other stimulants, such as methamphetamine, have not been reported.

Objectives

The present study examined the effects of PD144418 and YUN-252 pretreatment on methamphetamine-induced hyperactivity after acute treatment.

Methods

Mice (n = 8–14/group) were injected with PD144418 (3.16, 10, or 31.6 μmol/kg), YUN-252 (0.316, 3.16, 31.6 μmol/kg), or saline. After 15 min, mice injected with 2.69 μmol/kg methamphetamine or saline vehicle, where distance traveled during a 60-min period was recorded. Additionally, the effect of PD144418 on the initiation and expression of methamphetamine sensitization was determined by treating mice (n = 8–14/group) with PD144418, methamphetamine or saline repeatedly over a 5-day period, and testing said mice with a challenge dose after a 7-day withdrawal period.

Results

Results indicate that both PD144418 and YUN-252, in a dose-dependent manner, attenuated hyperactivity induced by an acute methamphetamine injection. Specifically, 10 μmol/kg or 31.6 μmol/kg of PD144418 and 31 μmol/kg of YUN-252 suppressed methamphetamine-induced hyperactivity. In regard to methamphetamine sensitization, while 10 μmol/kg PD144418 prevented the initiation of methamphetamine sensitization, it did not have an effect on the expression.

Conclusions

Overall, the current results suggest an intriguing potential for this novel sigma receptor ligand as a treatment for the addictive properties of methamphetamine. Future analysis of this novel sigma receptor ligand in assays directly measuring reinforcement properties will be critical.

Keywords

Sigma receptor Methamphetamine Locomotor activity 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Akunne HC et al (1997) The pharmacology of the novel and selective sigma ligand, PD 144418. Neuropharmacology 36:51–62CrossRefGoogle Scholar
  2. Alonso G, Phan V, Guillemain I, Saunier M, Legrand A, Anoal M, Maurice T (2000) Immunocytochemical localization of the sigma(1) receptor in the adult rat central nervous system. Neuroscience 97:155–170CrossRefGoogle Scholar
  3. Blasio A, Valenza M, Iyer MR, Rice KC, Steardo L, Hayashi T, Cottone P, Sabino V (2015) Sigma-1 receptor mediates acquisition of alcohol drinking and seeking behavior in alcohol-preferring rats. Behav Brain Res 287:315–322.  https://doi.org/10.1016/j.bbr.2015.03.065 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Calcagnetti DJ, Schechter MD (1993) Extinction of cocaine-induced place approach in rats: a validation of the "biased" conditioning procedure. Brain Res Bull 30:695–700CrossRefGoogle Scholar
  5. Ceci A, Smith M, French ED (1988) Activation of the A10 mesolimbic system by the sigma-receptor agonist (+)SKF 10,047 can be blocked by rimcazole, a novel putative antipsychotic. Eur J Pharmacol 154:53–57CrossRefGoogle Scholar
  6. Coughenour LL, McLean JR, Parker RB (1977) A new device for the rapid measurement of impaired motor function in mice. Pharmacol Biochem Behav 6:351–353CrossRefGoogle Scholar
  7. Derbez AE, Mody RM, Werling LL (2002) Sigma(2)-receptor regulation of dopamine transporter via activation of protein kinase C. J Pharmacol Exp Ther 301:306–314CrossRefGoogle Scholar
  8. Dluzen DE, Liu B (2008) Gender differences in methamphetamine use and responses: a review. Gend Med 5:24–35CrossRefGoogle Scholar
  9. Fukunaga K, Moriguchi S (2017) Stimulation of the Sigma-1 receptor and the effects on neurogenesis and depressive behaviors in mice. Adv Exp Med Biol 964:201–211.  https://doi.org/10.1007/978-3-319-50174-1_14 CrossRefPubMedGoogle Scholar
  10. Hashimoto, K. (2015). Activation of sigma-1 receptor chaperone in the treatment of neuropsychiatric diseases and its clinical implication. Journal of Pharmacological Sciences, 127(1), 6–9.  https://doi.org/10.1016/j.jphs.2014.11.010 CrossRefGoogle Scholar
  11. Hayashi T, Su TP (2004) Sigma-1 receptor ligands: potential in the treatment of neuropsychiatric disorders. CNS Drugs 18:269–284CrossRefGoogle Scholar
  12. Hayashi T, Su T (2005) The sigma receptor: evolution of the concept in neuropsychopharmacology. Curr Neuropharmacol 3:267–280CrossRefGoogle Scholar
  13. Hayashi T, Justinova Z, Hayashi E, Cormaci G, Mori T, Tsai SY, Barnes C, Goldberg SR, Su TP (2010) Regulation of sigma-1 receptors and endoplasmic reticulum chaperones in the brain of methamphetamine self-administering rats. J Pharmacol Exp Ther 332:1054–1063.  https://doi.org/10.1124/jpet.109.159244 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Ji LL, Peng JB, Fu CH, Cao D, Li D, Tong L, Wang ZY (2016) Activation of Sigma-1 receptor ameliorates anxiety-like behavior and cognitive impairments in a rat model of post-traumatic stress disorder. Behav Brain Res 311:408–415.  https://doi.org/10.1016/j.bbr.2016.05.056 CrossRefPubMedGoogle Scholar
  15. Katz JL, Hiranita T, Kopajtic TA, Rice KC, Mesangeau C, Narayanan S, Abdelazeem AH, McCurdy CR (2016) Blockade of cocaine or sigma receptor agonist self administration by subtype-selective sigma receptor antagonists. J Pharmacol Exp Ther 358:109–124.  https://doi.org/10.1124/jpet.116.232728 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kaushal N, Robson MJ, Vinnakota H, Narayanan S, Avery BA, McCurdy CR, Matsumoto RR (2011) Synthesis and pharmacological evaluation of 6-acetyl-3-(4-(4-(4-fluorophenyl)piperazin-1-yl)butyl)benzo[d]oxazol-2(3H)-one (SN79), a cocaine antagonist, in rodents. AAPS J 13:336–346.  https://doi.org/10.1208/s12248-011-9274-9 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Klawonn AM, Nilsson A, Rådberg CF, Lindström SH, Ericson M, Granseth B, Engblom D, Fritz M (2017) The Sigma-2 receptor selective agonist Siramesine (Lu 28-179) decreases cocaine-reinforced Pavlovian learning and alters glutamatergic and dopaminergic input to the striatum. Front Pharmacol 8:714.  https://doi.org/10.3389/fphar.2017.00714 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Lever JR, Miller DK, Fergason-Cantrell EA, Green CL, Watkinson LD, Carmack TL, Lever SZ (2014) Relationship between cerebral sigma-1 receptor occupancy and attenuation of cocaine's motor stimulatory effects in mice by PD144418. J Pharmacol Exp Ther 351:153–163.  https://doi.org/10.1124/jpet.114.216671 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Li Y, Vartanian AJ, White FJ, Xue CJ, Wolf ME (1997) Effects of the AMPA receptor antagonist NBQX on the development and expression of behavioral sensitization to cocaine and amphetamine. Psychopharmacology 134:266–276CrossRefGoogle Scholar
  20. Liu X, Fu Y, Yang H, Mavlyutov T, Li J, McCurdy CR, Guo LW, Pattnaik BR (2017) Potential independent action of sigma receptor ligands through inhibition of the Kv2. 1 channel. Oncotarget 8:59345–59358.  https://doi.org/10.18632/oncotarget.19581 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Mach RH, Huang Y, Freeman RA, Wu L, Vangveravong S, Luedtke RR (2004) Conformationally-flexible benzamide analogues as dopamine D3 and sigma 2 receptor ligands. Bioorg Med Chem Lett 14:195–202CrossRefGoogle Scholar
  22. Martin-Fardon R, Maurice T, Aujla H, Bowen WD, Weiss F (2007) Differential effects of sigma1 receptor blockade on self-administration and conditioned reinstatement motivated by cocaine vs natural reward. Neuropsychopharmacology 32:1967–1973.  https://doi.org/10.1038/sj.npp.1301323 CrossRefPubMedGoogle Scholar
  23. Matsumoto RR, Bowen WD, Tom MA, Vo VN, Truong DD, De Costa BR (1995) Characterization of two novel sigma receptor ligands: antidystonic effects in rats suggest sigma receptor antagonism. Eur J Pharmacol 280:301–310CrossRefGoogle Scholar
  24. Matsumoto RR, Pouw B, Mack AL, Daniels A, Coop A (2007) Effects of UMB24 and (+/−)-SM 21, putative sigma2-preferring antagonists, on behavioral toxic and stimulant effects of cocaine in mice. Pharmacol Biochem Behav 86:86–91.  https://doi.org/10.1016/j.pbb.2006.12.011 CrossRefPubMedGoogle Scholar
  25. Matsumoto RR, Shaikh J, Wilson LL, Vedam S, Coop A (2008) Attenuation of methamphetamine-induced effects through the antagonism of sigma (sigma) receptors: evidence from in vivo and in vitro studies. Eur Neuropsychopharmacol 18:871–881.  https://doi.org/10.1016/j.euroneuro.2008.07.006 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Maurice T, Martin-Fardon R, Romieu P, Matsumoto RR (2002) Sigma(1) (sigma(1)) receptor antagonists represent a new strategy against cocaine addiction and toxicity. Neurosci Biobehav Rev 26:499–527CrossRefGoogle Scholar
  27. Maurice T, Casalino M, Lacroix M, Romieu P (2003) Involvement of the sigma 1 receptor in the motivational effects of ethanol in mice. Pharmacol Biochem Behav 74:869–876CrossRefGoogle Scholar
  28. Miller DK, Oelrichs CE, Sage AS, Sun GY, Simonyi A (2013) Repeated resveratrol treatment attenuates methamphetamine-induced hyperactivity and [3H]dopamine overflow in rodents. Neurosci Lett 554:53–58.  https://doi.org/10.1016/j.neulet.2013.08.051 CrossRefPubMedGoogle Scholar
  29. Navarro G, Moreno E, Aymerich M, Marcellino D, McCormick PJ, Mallol J, Cortes A, Casado V, Canela EI, Ortiz J, Fuxe K, Lluis C, Ferre S, Franco R (2010) Direct involvement of sigma-1 receptors in the dopamine D1 receptor-mediated effects of cocaine. Proc Natl Acad Sci U S A 107:18676–18681.  https://doi.org/10.1073/pnas.1008911107 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Nguyen EC, McCracken KA, Liu Y, Pouw B, Matsumoto RR (2005) Involvement of sigma (sigma) receptors in the acute actions of methamphetamine: receptor binding and behavioral studies. Neuropharmacology 49:638–645.  https://doi.org/10.1016/j.neuropharm.2005.04.016 CrossRefPubMedGoogle Scholar
  31. Nguyen L, Robson MJ, Healy JR, Scandinaro AL, Matsumoto RR (2014) Involvement of sigma-1 receptors in the antidepressant-like effects of dextromethorphan. PLoS One 9:e89985.  https://doi.org/10.1371/journal.pone.0089985 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ohi K, Hashimoto R, Yasuda Y, Fukumoto M, Yamamori H, Umeda-Yano S, Kamino K, Ikezawa K, Azechi M, Iwase M, Kazui H, Kasai K, Takeda M (2011) The SIGMAR1 gene is associated with a risk of schizophrenia and activation of the prefrontal cortex. Prog Neuro-Psychopharmacol Biol Psychiatry 35:1309–1315.  https://doi.org/10.1016/j.pnpbp.2011.04.008 CrossRefGoogle Scholar
  33. Pierce RC, Kalivas PW (1997) A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res Brain Res Rev 25:192–216CrossRefGoogle Scholar
  34. Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18:247–291CrossRefGoogle Scholar
  35. Robson MJ, Noorbakhsh B, Seminerio MJ, Matsumoto RR (2012) Sigma-1 receptors: potential targets for the treatment of substance abuse. Curr Pharm Des 18:902–919CrossRefGoogle Scholar
  36. Rodvelt KR, Miller DK (2010) Could sigma receptor ligands be a treatment for methamphetamine addiction? Curr Drug Abuse Rev 3:156–162CrossRefGoogle Scholar
  37. Rodvelt KR, Lever SZ, Lever JR, Blount LR, Fan KH, Miller DK (2011) SA 4503 attenuates cocaine-induced hyperactivity and enhances methamphetamine substitution for a cocaine discriminative stimulus. Pharmacol Biochem Behav 97:676–682.  https://doi.org/10.1016/j.pbb.2010.11.016 CrossRefPubMedGoogle Scholar
  38. Romieu P, Phan VL, Martin-Fardon R, Maurice T (2002) Involvement of the sigma(1) receptor in cocaine-induced conditioned place preference: possible dependence on dopamine uptake blockade. Neuropsychopharmacology 26:444–455.  https://doi.org/10.1016/S0893-133X(01)00391-8 CrossRefPubMedGoogle Scholar
  39. Roth ME, Carroll ME (2004) Sex differences in the acquisition of IV methamphetamine self-administration and subsequent maintenance under a progressive ratio schedule in rats. Psychopharmacology 172:443–449.  https://doi.org/10.1007/s00213-003-1670-0 CrossRefPubMedGoogle Scholar
  40. Ruda-Kucerova J, Amchova P, Babinska Z, Dusek L, Micale V, Sulcova A (2015) Sex differences in the reinstatement of methamphetamine seeking after forced abstinence in Sprague-Dawley rats. Front Psychiatry 6:91.  https://doi.org/10.3389/fpsyt.2015.00091 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Sabino V, Cottone P, Parylak SL, Steardo L, Zorrilla EP (2009a) Sigma-1 receptor knockout mice display a depressive-like phenotype. Behav Brain Res 198:472–476.  https://doi.org/10.1016/j.bbr.2008.11.036 CrossRefPubMedGoogle Scholar
  42. Sabino V, Cottone P, Zhao Y, Iyer MR, Steardo L, Steardo L, Rice KC, Conti B, Koob GF, Zorrilla EP (2009b) The sigma-receptor antagonist BD-1063 decreases ethanol intake and reinforcement in animal models of excessive drinking. Neuropsychopharmacology 34:1482–1493.  https://doi.org/10.1038/npp.2008.192 CrossRefPubMedGoogle Scholar
  43. Sabino V, Cottone P, Blasio A, Iyer MR, Steardo L, Rice KC, Conti B, Koob GF, Zorrilla EP (2011) Activation of sigma-receptors induces binge-like drinking in Sardinian alcohol-preferring rats. Neuropsychopharmacology 36:1207–1218.  https://doi.org/10.1038/npp.2011.5 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Sage AS, Oelrichs CE, Davis DC, Fan KH, Nahas RI, Lever SZ, Lever JR, Miller DK (2013) Effects of N-phenylpropyl-N'-substituted piperazine sigma receptor ligands on cocaine-induced hyperactivity in mice. Pharmacol Biochem Behav 110:201–207.  https://doi.org/10.1016/j.pbb.2013.07.006 CrossRefPubMedGoogle Scholar
  45. Sambo DO, Lin M, Owens A, Lebowitz JJ, Richardson B, Jagnarine DA, Shetty M, Rodriquez M, Alonge T, Ali M, Katz J, Yan L, Febo M, Henry LK, Bruijnzeel AW, Daws L, Khoshbouei H (2017) The sigma-1 receptor modulates methamphetamine dysregulation of dopamine neurotransmission. Nat Commun 8:2228.  https://doi.org/10.1038/s41467-017-02087-x CrossRefPubMedPubMedCentralGoogle Scholar
  46. Sanchez C, Papp M (2000) The selective sigma2 ligand Lu 28-179 has an antidepressant-like profile in the rat chronic mild stress model of depression. Behav Pharmacol 11:117–124CrossRefGoogle Scholar
  47. Scott LL, Sahn JJ, Ferragud A, Yen RC, Satarasinghe PN, Wood MD, Hodges TR, Shi T, Prakash BA, Friese KM, Shen A, Sabino V, Pierce JT, Martin SF (2018) Small molecule modulators of sigma2R/Tmem97 reduce alcohol withdrawal-induced behaviors. Neuropsychopharmacology 43:1867–1875.  https://doi.org/10.1038/s41386-018-0067-z CrossRefPubMedPubMedCentralGoogle Scholar
  48. Shilling PD, Kelsoe JR, Segal DS (1997) Dopamine transporter mRNA is up-regulated in the substantia nigra and the ventral tegmental area of amphetamine-sensitized rats. Neurosci Lett 236:131–134CrossRefGoogle Scholar
  49. Stefanski R, Justinova Z, Hayashi T, Takebayashi M, Goldberg SR, Su TP (2004) Sigma1 receptor upregulation after chronic methamphetamine self-administration in rats: a study with yoked controls. Psychopharmacology 175:68–75.  https://doi.org/10.1007/s00213-004-1779-9 CrossRefPubMedGoogle Scholar
  50. Sulzer D, Sonders MS, Poulsen NW, Galli A (2005) Mechanisms of neurotransmitter release by amphetamines: a review. Prog Neurobiol 75:406–433.  https://doi.org/10.1016/j.pneurobio.2005.04.003 CrossRefPubMedGoogle Scholar
  51. Ujike H, Kanzaki A, Okumura K, Akiyama K, Otsuki S (1992) Sigma (sigma) antagonist BMY 14802 prevents methamphetamine-induced sensitization. Life Sci 50:PL129–PL134PubMedGoogle Scholar
  52. Ujike H, Kuroda S, Otsuki S (1996) Sigma receptor antagonists block the development of sensitization to cocaine. Eur J Pharmacol 296:123–128.  https://doi.org/10.1016/0014-2999(95)00693-1 CrossRefPubMedGoogle Scholar
  53. Vanderschuren LJ, Kalivas PW (2000) Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology 151:99–120CrossRefGoogle Scholar
  54. Wise RA, Bozarth MA (1987) A psychomotor stimulant theory of addiction. Psychol Rev 94:469–492CrossRefGoogle Scholar
  55. Witkin JM, Terry P, Menkel M, Hickey P, Pontecorvo M, Ferkany J, Katz JL (1993) Effects of the selective sigma receptor ligand, 6-[6-(4-hydroxypiperidinyl)hexyloxy]-3-methylflavone (NPC 16377), on behavioral and toxic effects of cocaine. J Pharmacol Exp Ther 266:473–482PubMedGoogle Scholar
  56. Xu YT, Kaushal N, Shaikh J, Wilson LL, Mesangeau C, McCurdy CR, Matsumoto RR (2010) A novel substituted piperazine, CM156, attenuates the stimulant and toxic effects of cocaine in mice. J Pharmacol Exp Ther 333:491–500.  https://doi.org/10.1124/jpet.109.161398 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Yasui Y, Su TP (2016) Potential molecular mechanisms on the role of the Sigma-1 receptor in the action of cocaine and methamphetamine. J Drug Alcohol Res 5:1–15.  https://doi.org/10.4303/jdar/235970 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Psychological SciencesUniversity of MissouriColumbiaUSA
  2. 2.Research Service, Harry S. Truman Memorial Veterans’ Hospital, Columbia, and Department of Radiology and Radiopharmaceutical Sciences InstituteUniversity of MissouriColumbiaUSA
  3. 3.Department of Chemistry and MU Research Reactor CenterUniversity of MissouriColumbiaUSA

Personalised recommendations