The glial cell modulator and phosphodiesterase inhibitor, AV411 (ibudilast), attenuates prime- and stress-induced methamphetamine relapse

European Journal of Pharmacology

Volumn 637, Issue 1-3, 2010, Pages 102-108

  Beardsley, Patrick M ^a   Shelton, Keith L ^a   Hendrick, Elizabeth ^a   Johnson, Kirk W ^b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b Avigen Inc   (United States)

Author keywords

AV411; Glial; Ibudilast; Methamphetamine; Relapse; Self administration

Indexed keywords

IBUDILAST; METHAMPHETAMINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG DEPENDENCE; DRUG EFFICACY; DRUG MECHANISM; FOOTSHOCK; GLIA CELL; LONG EVANS RAT; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REINFORCEMENT; RELAPSE; STRESS; TREATMENT DURATION; WITHDRAWAL SYNDROME;

AMPHETAMINE-RELATED DISORDERS; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; INJECTIONS, INTRAPERITONEAL; MALE; METHAMPHETAMINE; NEUROGLIA; PHOSPHODIESTERASE INHIBITORS; PYRIDINES; RATS; RATS, LONG-EVANS; RECURRENCE; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 77953289024     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2010.04.010     Document Type: Article

References (63)

1. Anggadiredja K., Nakamichi M., Hiranita T., Tanaka H., Shoyama Y., Watanabe S., Yamamoto T. Endocannabinoid system modulates relapse to methamphetamine seeking: possible mediation by the arachidonic acid cascade. Neuropsychopharmacology 2004, 29:1470-1478.
2. Anonymous Avigen Announces Positive Data for AV411 in Pain Relief and Drug Addiction 2009, GlobeNewswire. GlobeNewswire, Inc., Los Angeles, CA.
3. Benz B., Grima G., Do K.Q. Glutamate-induced homocysteic acid release from astrocytes: possible implication in glia-neuron signaling. Neuroscience 2004, 124:377-386.
4. Bezzi P., Carmignoto G., Pasti L., Vesce S., Rossi D., Rizzini B.L., Pozzan T., Volterra A. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 1998, 391:281-285.
5. Boger H.A., Middaugh L.D., Patrick K.S., Ramamoorthy S., Denehy E.D., Zhu H., Pacchioni A.M., Granholm A.C., McGinty J.F. Long-term consequences of methamphetamine exposure in young adults are exacerbated in glial cell line-derived neurotrophic factor heterozygous mice. J. Neurosci. 2007, 27:8816-8825.
6. Camacho A., Massieu L. Role of glutamate transporters in the clearance and release of glutamate during ischemia and its relation to neuronal death. Arch. Med. Res. 2006, 37:11-18.
7. Cass W.A. GDNF selectively protects dopamine neurons over serotonin neurons against the neurotoxic effects of methamphetamine. J. Neurosci. 1996, 16:8132-8139.
8. Cass W.A., Walker D.J., Manning M.W. Augmented methamphetamine-induced overflow of striatal dopamine 1day after GDNF administration. Brain Res. 1999, 827:104-112.
9. Cass W.A., Manning M.W., Bailey S.L. Restorative effects of GDNF on striatal dopamine release in rats treated with neurotoxic doses of methamphetamine. Ann. NY Acad. Sci. 2000, 914:127-136.
10. Cass W.A., Peters L.E., Harned M.E., Seroogy K.B. Protection by GDNF and other trophic factors against the dopamine-depleting effects of neurotoxic doses of methamphetamine. Ann. NY Acad. Sci. 2006, 1074:272-281.
11. Davidson C., Gopalan R., Ahn C., Chen Q., Mannelli P., Patkar A.A., Weese G.D., Lee T.H., Ellinwood E.H. Reduction in methamphetamine induced sensitization and reinstatement after combined pergolide plus ondansetron treatment during withdrawal. Eur. J. Pharmacol. 2007, 565:113-118.
12. Escubedo E., Guitart L., Sureda F.X., Jimenez A., Pubill D., Pallas M., Camins A., Camarasa J. Microgliosis and down-regulation of adenosine transporter induced by methamphetamine in rats. Brain Res. 1998, 814:120-126.
13. Fantegrossi W.E., Woolverton W.L., Kilbourn M., Sherman P., Yuan J., Hatzidimitriou G., Ricaurte G.A., Woods J.H., Winger G. Behavioral and neurochemical consequences of long-term intravenous self-administration of MDMA and its enantiomers by rhesus monkeys. Neuropsychopharmacology 2004, 29:1270-1281.
14. Fumagalli M., Brambilla R., D'Ambrosi N., Volonte C., Matteoli M., Verderio C., Abbracchio M.P. Nucleotide-mediated calcium signaling in rat cortical astrocytes: role of P2X and P2Y receptors. Glia 2003, 43:218-230.
15. Gibson L.C., Hastings S.F., McPhee I., Clayton R.A., Darroch C.E., Mackenzie A., Mackenzie F.L., Nagasawa M., Stevens P.A., Mackenzie S.J. The inhibitory profile of Ibudilast against the human phosphodiesterase enzyme family. Eur. J. Pharmacol. 2006, 538:39-42.
16. Guilarte T.R., Nihei M.K., McGlothan J.L., Howard A.S. Methamphetamine-induced deficits of brain monoaminergic neuronal markers: distal axotomy or neuronal plasticity. Neuroscience 2003, 122:499-513.
17. Hamdy M.M., Mamiya T., Noda Y., Sayed M., Assi A.A., Gomaa A., Yamada K., Nabeshima T. A selective phosphodiesterase IV inhibitor, rolipram blocks both withdrawal behavioral manifestations, and c-Fos protein expression in morphine dependent mice. Behav. Brain Res. 2001, 118:85-93.
18. Hiranita T., Anggadiredja K., Fujisaki C., Watanabe S., Yamamoto T. Nicotine attenuates relapse to methamphetamine-seeking behavior (craving) in rats. Ann. NY Acad. Sci. 2004, 1025:504-507.
19. Hiranita T., Nawata Y., Sakimura K., Anggadiredja K., Yamamoto T. Suppression of methamphetamine-seeking behavior by nicotinic agonists. Proc. Natl Acad. Sci. USA 2006, 103:8523-8527.
20. Hutchinson M.R., Bland S.T., Johnson K.W., Rice K.C., Maier S.F., Watkins L.R. Opioid-induced glial activation: mechanisms of activation and implications for opioid analgesia, dependence, and reward. Sci. World J. 2007, 7:98-111.
21. Hutchinson M.R., Lewis S.S., Coats B.D., Skyba D.A., Crysdale N.Y., Berkelhammer D.L., Brzeski A., Northcutt A., Vietz C.M., Judd C.M., Maier S.F., Watkins L.R., Johnson K.W. Reduction of opioid withdrawal and potentiation of acute opioid analgesia by systemic AV411 (ibudilast). Brain Behav. Immun. 2009, 23:240-250.
22. Iyo M., Maeda Y., Inada T., Kitao Y., Sasaki H., Fukui S. The effects of a selective cAMP phosphodiesterase inhibitor, rolipram, on methamphetamine-induced behavior. Neuropsychopharmacology 1995, 13:33-39.
23. Iyo M., Bi Y., Hashimoto K., Inada T., Fukui S. Prevention of methamphetamine-induced behavioral sensitization in rats by a cyclic AMP phosphodiesterase inhibitor, rolipram. Eur. J. Pharmacol. 1996, 312:163-170.
24. Kang J., Jiang L., Goldman S.A., Nedergaard M. Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat. Neurosci. 1998, 1:683-692.
25. Kawanokuchi J., Mizuno T., Kato H., Mitsuma N., Suzumura A. Effects of interferon-beta on microglial functions as inflammatory and antigen presenting cells in the central nervous system. Neuropharmacology 2004, 46:734-742.
26. Khan Z.U., Koulen P., Rubinstein M., Grandy D.K., Goldman-Rakic P.S. An astroglia-linked dopamine D2-receptor action in prefrontal cortex. Proc. Natl Acad. Sci. USA 2001, 98:1964-1969.
27. Kukley M., Barden J.A., Steinhauser C., Jabs R. Distribution of P2X receptors on astrocytes in juvenile rat hippocampus. Glia 2001, 36:11-21.
28. LaVoie M.J., Card J.P., Hastings T.G. Microglial activation precedes dopamine terminal pathology in methamphetamine-induced neurotoxicity. Exp. Neurol. 2004, 187:47-57.
29. Ledeboer A., Liu T., Shumilla J.A., Mahoney J.H., Vijay S., Gross M.I., Vargas J.A., Sultzbaugh L., Claypool M.D., Sanftner L.M., Watkins L.R., Johnson K.W. The glial modulatory drug AV411 attenuates mechanical allodynia in rat models of neuropathic pain. Neuron Glia Biol. 2006, 2:279-291.
30. Ledeboer A., Hutchinson M.R., Watkins L.R., Johnson K.W. Ibudilast (AV-411). A new class therapeutic candidate for neuropathic pain and opioid withdrawal syndromes. Expert Opin. Investig. Drugs 2007, 16:935-950.
31. Mamiya T., Noda Y., Ren X., Hamdy M., Furukawa S., Kameyama T., Yamada K., Nabeshima T. Involvement of cyclic AMP systems in morphine physical dependence in mice: prevention of development of morphine dependence by rolipram, a phosphodiesterase 4 inhibitor. Br. J. Pharmacol. 2001, 132:1111-1117.
32. Melega W.P., Lacan G., Desalles A.A., Phelps M.E. Long-term methamphetamine-induced decreases of [(11)C]WIN 35, 428 binding in striatum are reduced by GDNF: PET studies in the vervet monkey. Synapse 2000, 35:243-249.
33. Messer C.J., Eisch A.J., Carlezon W.A., Whisler K., Shen L., Wolf D.H., Westphal H., Collins F., Russell D.S., Nestler E.J. Role for GDNF in biochemical and behavioral adaptations to drugs of abuse. Neuron 2000, 26:247-257.
34. Mizoguchi H., Takuma K., Fukakusa A., Ito Y., Nakatani A., Ibi D., Kim H.C., Yamada K. Improvement by minocycline of methamphetamine-induced impairment of recognition memory in mice. Psychopharmacology (Berl) 2008, 196:233-241.
35. Mizuno T., Kurotani T., Komatsu Y., Kawanokuchi J., Kato H., Mitsuma N., Suzumura A. Neuroprotective role of phosphodiesterase inhibitor ibudilast on neuronal cell death induced by activated microglia. Neuropharmacology 2004, 46:404-411.
36. Moffett M.C., Goeders N.E. CP-154, 526, a CRF type-1 receptor antagonist, attenuates the cue-and methamphetamine-induced reinstatement of extinguished methamphetamine-seeking behavior in rats. Psychopharmacology (Berl) 2007, 190:171-180.
37. Mori T., Baba J., Ichimaru Y., Suzuki T. Effects of rolipram, a selective inhibitor of phosphodiesterase 4, on hyperlocomotion induced by several abused drugs in mice. Jpn. J. Pharmacol. 2000, 83:113-118.
38. Narita M., Miyatake M., Shibasaki M., Shindo K., Nakamura A., Kuzumaki N., Nagumo Y., Suzuki T. Direct evidence of astrocytic modulation in the development of rewarding effects induced by drugs of abuse. Neuropsychopharmacology 2006, 31:2476-2488.
39. Nitta A., Nishioka H., Fukumitsu H., Furukawa Y., Sugiura H., Shen L., Furukawa S. Hydrophobic dipeptide Leu-Ile protects against neuronal death by inducing brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor synthesis. J. Neurosci. Res. 2004, 78:250-258.
40. Niwa M., Nitta A., Shen L., Noda Y., Nabeshima T. Involvement of glial cell line-derived neurotrophic factor in inhibitory effects of a hydrophobic dipeptide Leu-Ile on morphine-induced sensitization and rewarding effects. Behav. Brain Res. 2007, 179:167-171.
41. Niwa M., Nitta A., Yamada Y., Nakajima A., Saito K., Seishima M., Noda Y., Nabeshima T. Tumor necrosis factor-alpha and its inducer inhibit morphine-induced rewarding effects and sensitization. Biol. Psychiatry 2007, 62:658-668.
42. Niwa M., Nitta A., Yamada Y., Nakajima A., Saito K., Seishima M., Shen L., Noda Y., Furukawa S., Nabeshima T. An inducer for glial cell line-derived neurotrophic factor and tumor necrosis factor-alpha protects against methamphetamine-induced rewarding effects and sensitization. Biol. Psychiatry 2007, 61:890-901.
43. Parpura V., Basarsky T.A., Liu F., Jeftinija K., Jeftinija S., Haydon P.G. Glutamate-mediated astrocyte-neuron signalling. Nature 1994, 369:744-747.
44. Pubill D., Verdaguer E., Sureda F.X., Camins A., Pallas M., Camarasa J., Escubedo E. Carnosine prevents methamphetamine-induced gliosis but not dopamine terminal loss in rats. Eur. J. Pharmacol. 2002, 448:165-168.
45. Pubill D., Canudas A.M., Pallas M., Camins A., Camarasa J., Escubedo E. Different glial response to methamphetamine- and methylenedioxymethamphetamine-induced neurotoxicity. Naunyn Schmiedebergs Arch. Pharmacol. 2003, 367:490-499.
46. Qi J., Yang J.Y., Wang F., Zhao Y.N., Song M., Wu C.F. Effects of oxytocin on methamphetamine-induced conditioned place preference and the possible role of glutamatergic neurotransmission in the medial prefrontal cortex of mice in reinstatement. Neuropharmacology 2009, 56:856-865.
47. Rolan P., Gibbons J.A., He L., Chang E., Jones D., Gross M.I., Davidson J.B., Sanftner L.M., Johnson K.W. Ibudilast in healthy volunteers: safety, tolerability and pharmacokinetics with single and multiple doses. Br. J. Clin. Pharmacol. 2008, 66:792-801.
48. Rolan P., Hutchinson M., Johnson K. Ibudilast: a review of its pharmacology, efficacy and safety in respiratory and neurological disease. Expert Opin. Pharmacother. 2009, 10:2897-2904.
49. Shelton K.L., Beardsley P.M. Effect of drug-paired exteroceptive stimulus presentations on methamphetamine reinstatement in rats. Pharmacol. Biochem. Behav. 2008, 90:434-440.
50. Shepard J.D., Bossert J.M., Liu S.Y., Shaham Y. The anxiogenic drug yohimbine reinstates methamphetamine seeking in a rat model of drug relapse. Biol. Psychiatry 2004, 55:1082-1089.
51. Sheskin D. Handbook of Parametric and Nonparametric Statistical Procedures 2007, Chapman & Hall/CRC, Boca Raton. 4th ed.
52. Song P., Zhao Z.Q. The involvement of glial cells in the development of morphine tolerance. Neurosci. Res. 2001, 39:281-286.
53. Suzuki T., Shindo K., Miyatake M., Kurokawa K., Higashiyama K., Suzuki M., Narita M. Lack of development of behavioral sensitization to methylphenidate in mice: correlation with reversible astrocytic activation. Eur. J. Pharmacol. 2007, 574:39-48.
54. Suzumura A., Ito A., Yoshikawa M., Sawada M. Ibudilast suppresses TNFalpha production by glial cells functioning mainly as type III phosphodiesterase inhibitor in the CNS. Brain Res. 1999, 837:203-212.
55. 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.
56. Thomas D.M., Walker P.D., Benjamins J.A., Geddes T.J., Kuhn D.M. Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation. J. Pharmacol. Exp. Ther. 2004, 311:1-7.
57. Thompson B.E., Sachs B.D., Kantak K.M., Cherry J.A. The Type IV phosphodiesterase inhibitor rolipram interferes with drug-induced conditioned place preference but not immediate early gene induction in mice. Eur. J. Neurosci. 2004, 19:2561-2568.
58. Ullian E.M., Christopherson K.S., Barres B.A. Role for glia in synaptogenesis. Glia 2004, 47:209-216.
59. Watkins L.R., Hutchinson M.R., Johnston I.N., Maier S.F. Glia: novel counter-regulators of opioid analgesia. Trends Neurosci. 2005, 28:661-669.
60. Watkins L.R., Hutchinson M.R., Ledeboer A., Wieseler-Frank J., Milligan E.D., Maier S.F. Norman Cousins lecture. Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids. Brain Behav. Immun. 2007, 21:131-146.
61. Yan Y., Nitta A., Mizuno T., Nakajima A., Yamada K., Nabeshima T. Discriminative-stimulus effects of methamphetamine and morphine in rats are attenuated by cAMP-related compounds. Behav. Brain Res. 2006, 173:39-46.
62. 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 J. 2007, 21:1994-2004.
63. Zhang L., Kitaichi K., Fujimoto Y., Nakayama H., Shimizu E., Iyo M., Hashimoto K. Protective effects of minocycline on behavioral changes and neurotoxicity in mice after administration of methamphetamine. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30:1381-1393.