Minocycline, an antibiotic with inhibitory effect on microglial activation, attenuates the maintenance and reinstatement of methamphetamine-seeking behavior in rat

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 53, Issue , 2014, Pages 142-148

  Attarzadeh Yazdi, Ghassem ^a,b   Arezoomandan, Reza ^c   Haghparast, Abbas ^b,c  

^a HORMOZGAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b Iran National Science Foundation   (Iran)

^c SHAHID BEHESHTI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Glial cell activity; Methamphetamine maintenance; Minocycline; Nucleus accumbens; Reinstatement

Indexed keywords

METHAMPHETAMINE; MINOCYCLINE; ANTIINFECTIVE AGENT; CENTRAL STIMULANT AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CONDITIONED PLACE PREFERENCE TEST; CONDITIONING; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG SEEKING BEHAVIOR; INTRA-ACCUMBAL DRUG ADMINISTRATION; LOCOMOTION; MALE; METHAMPHETAMINE DEPENDENCE; MICROGLIA; NONHUMAN; RAT; RECURRENCE RISK; REINFORCEMENT; RISK REDUCTION; ANIMAL; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; INSTRUMENTAL CONDITIONING; SUBSTANCE-RELATED DISORDERS; WISTAR RAT;

ANIMALS; ANTI-BACTERIAL AGENTS; CENTRAL NERVOUS SYSTEM STIMULANTS; CONDITIONING, OPERANT; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG-SEEKING BEHAVIOR; EXTINCTION, PSYCHOLOGICAL; MALE; METHAMPHETAMINE; MINOCYCLINE; RATS; RATS, WISTAR; REINFORCEMENT (PSYCHOLOGY); SUBSTANCE-RELATED DISORDERS;

EID: 84899755767     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2014.04.008     Document Type: Article

References (58)

1. Aguilar M.A., Rodríguez-Arias M., Miñarro J. Neurobiological mechanisms of the reinstatement of drug-conditioned place preference. Brain Res Rev 2009, 59:253-277.
2. Beardsley P.M., Shelton K.L., Hendrick E., Johnson K.W. The glial cell modulator and phosphodiesterase inhibitor, AV411 (ibudilast), attenuates prime- and stress-induced methamphetamine relapse. Eur J Pharmacol 2010, 637:102-108.
3. Blum D., Chtarto A., Tenenbaum L., Brotchi J., Levivier M. Clinical potential of minocycline for neurodegenerative disorders. Neurobiol Dis 2004, 17:359-366.
4. Bowyer J.F., Clausing P., Gough B., Slikker W., Holson R.R. Nitric oxide regulation of methamphetamine-induced dopamine release in caudate/putamen. Brain Res 1995, 699:62-70.
5. Chen H., Uz T., Manev H. Minocycline affects cocaine sensitization in mice. Neurosci Lett 2009, 452:258-261.
6. Chen H., Wu J., Zhang J., Hashimoto K. Recent topics on pharmacotherapy for amphetamine-type stimulants abuse and dependence. Curr Drug Abuse Rev 2010, 3:222-238.
7. Chen X., Ma L., Jiang Y., Chen S., Zhu C., Liu M., et al. Minocycline up-regulates the expression of brain-derived neurotrophic factor and nerve growth factor in experimental autoimmune encephalomyelitis. Eur J Pharmacol 2012, 686:124-129.
8. Cooper Z.D., Jones J.D., Comer S.D. Glial modulators: a novel pharmacological approach to altering the behavioral effects of abused substances. Expert Opin Investig Drugs 2012, 21:169-178.
9. Cretzmeyer M., Sarrazin M.V., Huber D.L., Block R.I., Hall J.A. Treatment of methamphetamine abuse: research findings and clinical directions. J Subst Abuse Treat 2003, 24:267-277.
10. DeLeo J.A., Colburn R.W. Proinflammatory cytokines and glial cells: their role in neuropathic pain. Cytokines and Pain 1999, 159-181. Springer.
11. Domercq M., Matute C. Neuroprotection by tetracyclines. Trends Pharmacol Sci 2004, 25:609-612.
12. Elkashef A., Vocci F., Hanson G., White J., Wickes W., Tiihonen J. Pharmacotherapy of methamphetamine addiction: an update. Subst Abus 2008, 29:31-49.
13. Fujita Y., Kunitachi S., Iyo M., Hashimoto K. The antibiotic minocycline prevents methamphetamine-induced rewarding effects in mice. Pharmacol Biochem Behav 2012, 101:303-306.
14. Hashimoto K. Minocycline as a therapeutic drug for methamphetamine use disorders. Nihon Shinkei Seishin Yakurigaku Zasshi 2008, 28:19-22.
15. Hashimoto K., Tsukada H., Nishiyama S., Fukumoto D., Kakiuchi T., Iyo M. Protective effects of minocycline on the reduction of dopamine transporters in the striatum after administration of methamphetamine: a positron emission tomography study in conscious monkeys. Biol Psychiatry 2007, 61:577-581.
16. He D.-Y., McGough N.N., Ravindranathan A., Jeanblanc J., Logrip M.L., Phamluong K., et al. Glial cell line-derived neurotrophic factor mediates the desirable actions of the anti-addiction drug ibogaine against alcohol consumption. J Neurosci 2005, 25:619-628.
17. Heneka M.T., Rodríguez J.J., Verkhratsky A. Neuroglia in neurodegeneration. Brain Res Rev 2010, 63:189-211.
18. Hutchinson M.R., Northcutt A.L., Chao L.W., Kearney J.J., Zhang Y., Berkelhammer D.L., et al. Minocycline suppresses morphine-induced respiratory depression, suppresses morphine-induced reward, and enhances systemic morphine-induced analgesia. Brain Behav Immun 2008, 22:1248-1256.
19. Itzhak Y. Modulation of cocaine- and methamphetamine-induced behavioral sensitization by inhibition of brain nitric oxide synthase. J Pharmacol Exp Ther 1997, 282:521-527.
20. Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D.-K., et al. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 2002, 22:1763-1771.
21. United Nations Office on Drugs and Crime (UNODC) World drug report (United Nations Publication, sales no. E.11.XI.10) 2011.
22. Karimi S., Attarzadeh-Yazdi G., Yazdi-Ravandi S., Hesam S., Azizi P., Razavi Y., et al. Forced swim stress but not exogenous corticosterone could induce the reinstatement of extinguished morphine conditioned place preference in rats: involvement of glucocorticoid receptors in the basolateral amygdala. Behav Brain Res 2014, 264:43-50.
23. Kofman O., Van Embden S., Alpert C., Fuchs I. Central and peripheral minocycline suppresses motor activity in rats. Pharmacol Biochem Behav 1993, 44:397-402.
24. Lee S.M., Yune T.Y., Kim S.J., Kim Y.C., Oh Y.J., Markelonis G.J., et al. Minocycline inhibits apoptotic cell death via attenuation of TNF-α expression following iNOS/NO induction by lipopolysaccharide in neuron/glia co-cultures. J Neurochem 2004, 91:568-578.
25. Levkovitz Y., Mendlovich S., Riwkes S., Braw Y., Levkovitch-Verbin H., Gal G., et al. A double-blind, randomized study of minocycline for the treatment of negative and cognitive symptoms in early-phase schizophrenia. J Clin Psychiatry 2010, 71:138-149.
26. Licata S.C., Pierce R.C. The roles of calcium/calmodulin-dependent and Ras/mitogen-activated protein kinases in the development of psychostimulant-induced behavioral sensitization. J Neurochem 2003, 85:14-22.
27. Lin K.-Y., Cherng C.G., Yang F.-R., Lin L.-C., Lu R.-B., Yu L. Memantine abolishes the formation of cocaine-induced conditioned place preference possibly via its IL-6-modulating effect in medial prefrontal cortex. Behav Brain Res 2011, 220:126-131.
28. Miguel-Hidalgo J.J. The role of glial cells in drug abuse. Curr Drug Abuse Rev 2009, 2:76-82.
29. Miyaoka T. Clinical potential of minocycline for schizophrenia. CNS Neurol Disord Drug Targets 2008, 7:376-381.
30. Narita M., Miyatake M., Narita M., Shibasaki M., Shindo K., Nakamura A., et al. Direct evidence of astrocytic modulation in the development of rewarding effects induced by drugs of abuse. Neuropsychopharmacology 2006, 31:2476-2488.
31. Paxinos G., Watson C.R. The rat brain in stereotaxic coordinates 2005, Elsevier Academic Press, San Diego, p. 62-65.
32. Pennartz C., Groenewegen H.J., Da Silva F.L. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 1994, 42:719-761.
33. Pi R., Li W., Lee N.T., Chan H.H., Pu Y., Chan L.N., et al. Minocycline prevents glutamate-induced apoptosis of cerebellar granule neurons by differential regulation of p38 and Akt pathways. J Neurochem 2004, 91:1219-1230.
34. Pubill D., Canudas A.M., Pallàs M., Camins A., Camarasa J., Escubedo E. Different glial response to methamphetamine- and methylenedioxymethamphetamine-induced neurotoxicity. Naunyn Schmiedebergs Arch Pharmacol 2003, 367:490-499.
35. Pudiak C.M., Bozarth M.A. L-NAME and MK-801 attenuate sensitization to the locomotor-stimulating effect of cocaine. Life Sci 1993, 53:1517-1524.
36. Rawson R.A., Condon T.P. Why do we need an addiction supplement focused on methamphetamine?. Addiction 2007, 102:1-4.
37. Rocha A., Kalivas P.W. Role of the prefrontal cortex and nucleus accumbens in reinstating methamphetamine seeking. Eur J Neurosci 2010, 31:903-909.
38. Romieu P., Meunier J., Garcia D., Zozime N., Martin-Fardon R., Bowen W.D., et al. The sigma1 (σ1) receptor activation is a key step for the reactivation of cocaine conditioned place preference by drug priming. Psychopharmacology 2004, 175:154-162.
39. Rothman R.B., Baumann M.H., Dersch C.M., Romero D.V., Rice K.C., Carroll F.I., et al. Amphetamine-type central nervous system stimulants release norepinephrine more potently than they release dopamine and serotonin. Synapse 2001, 39:32-41.
40. Samandari R., Chizari A., Hassanpour R., Mousavi Z., Haghparast A. Streptozotocin-induced diabetes affects the development and maintenance of morphine reward in rats. Neurosci Lett 2013, 543:90-94.
41. Seiden L.S., Sabol K.E., Ricaurte G.A. Amphetamine: effects on catecholamine systems and behavior. Annu Rev Pharmacol Toxicol 1993, 33:639-676.
42. Snider S.E., Hendrick E.S., Beardsley P.M. Glial cell modulators attenuate methamphetamine self-administration in the rat. Eur J Pharmacol 2013, 701:124-130.
43. Sofuoglu M. Cognitive enhancement as a pharmacotherapy target for stimulant addiction. Addiction 2010, 105:38-48.
44. Sofuoglu M., Waters A.J., Mooney M., O'Malley S.S. Minocycline reduced craving for cigarettes but did not affect smoking or intravenous nicotine responses in humans. Pharmacol Biochem Behav 2009, 92:135-140.
45. Stirling D.P., Koochesfahani K.M., Steeves J.D., Tetzlaff W. Minocycline as a neuroprotective agent. Neuroscientist 2005, 11:308-322.
46. Suk K. Minocycline suppresses hypoxic activation of rodent microglia in culture. Neurosci Lett 2004, 366:167-171.
47. Tanibuchi Y., Shimagami M., Fukami G., Sekine Y., Iyo M., Hashimoto K. A case of methamphetamine use disorder treated with the antibiotic drug minocycline. Gen Hosp Psychiatry 2010, 32:559. [e 1-3].
48. Thomas D.M., Dowgiert J., Geddes T.J., Francescutti-Verbeem D., Liu X., Kuhn D.M. Microglial activation is a pharmacologically specific marker for the neurotoxic amphetamines. Neurosci Lett 2004, 367:349-354.
49. Tikka T., Fiebich B.L., Goldsteins G., Keinänen R., Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 2001, 21:2580-2588.
50. Toolaney G.H. New Research on Methamphetamine Abuse 2007, Nova Publishers.
51. Vijayaraghavan S. Glial-neuronal interactions-implications for plasticity and drug addiction. AAPS 2009, 11:123-132.
52. Wei X., Zhao L., Liu J., Dodel R., Farlow M., Du Y. Minocycline prevents gentamicin-induced ototoxicity by inhibiting p38 MAP kinase phosphorylation and caspase 3 activation. Neuroscience 2005, 131:513-521.
53. Yan Y., Yamada K., Niwa M., Nagai T., Nitta A., Nabeshima T. Enduring vulnerability to reinstatement of methamphetamine-seeking behavior in glial cell line-derived neurotrophic factor mutant mice. FASEB 2007, 21:1994-2004.
54. Yirmiya R., Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 2011, 25:181-213.
55. Yong V.W., Wells J., Giuliani F., Casha S., Power C., Metz L.M. The promise of minocycline in neurology. Lancet 2004, 3:744-751.
56. Zhang L., Kitaichi K., Fujimoto Y., Nakayama H., Shimizu E., Iyo M., et al. Protective effects of minocycline on behavioral changes and neurotoxicity in mice after administration of methamphetamine. Prog Neuropsychopharmacol Biol Psychiatry 2006, 30:1381-1393.
57. Zhang L., Shirayama Y., Shimizu E., Iyo M., Hashimoto K. Protective effects of minocycline on 3, 4-methylenedioxymethamphetamine-induced neurotoxicity in serotonergic and dopaminergic neurons of mouse brain. Eur J Pharmacol 2006, 544:1-9.
58. Zhang X.-Q., Cui Y., Cui Y., Chen Y., Na X.-D., Chen F.-Y., et al. Activation of p38 signaling in the microglia in the nucleus accumbens contributes to the acquisition and maintenance of morphine-induced conditioned place preference. Brain Behav Immun 2012, 26:318-325.