Role of matrix metalloproteinase and tissue inhibitor of MMP in methamphetamine-induced behavioral sensitization and reward: Implications for dopamine receptor down-regulation and dopamine release

Hiroyuki Mizoguchi, Kiyofumi Yamada, Akihiro Mouri, Minae Niwa, Tomoko Mizuno, Yukihiro Noda, Atsumi Nitta, Shigeyoshi Itohara, Yoshiko Banno, Toshitaka Nabeshima

Research output: Contribution to journalArticle

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Abstract

Matrix metalloproteinases (MMPs) and its inhibitors (TIMPs) function to remodel the pericellular environment. We have demonstrated that methamphetamine (METH)-induced behavioral sensitization and reward were markedly attenuated in MMP-2- and MMP-9 deficient [MMP-2-(-/-) and MMP-9-(-/-)] mice compared with those in wild-type mice, suggesting that METH-induced expression of MMP-2 and MMP-9 in the brain plays a role in the development of METH-induced sensitization and reward. In the present study, we investigated the changes in TIMP-2 expression in the brain after repeated METH treatment. Furthermore, we studied a role of MMP/TIMP system in METH-induced behavioral changes and dopamine neurotransmission. Repeated METH treatment induced behavioral sensitization, which was accompanied by an increase in TIMP-2 expression. Antisense TIMP-2 oligonucleotide (TIMP-AS) treatment enhanced the sensitization, which was associated with the potentiation of METH-induced dopamine release in the nucleus accumbens (NAc). On the other hand, MMP-2/-9 inhibitors blocked the METH-induced behavioral sensitization and conditioned place preference, a measure of the rewarding effect, and reduced the METH-increased dopamine release in the NAc. Dopamine receptor agonist-stimulated [35S]GTPγS binding was reduced in the frontal cortex of sensitized rats. TIMP-AS treatment potentiated, while MMP-2/-9 inhibitor attenuated, the reduction of dopamine D2 receptor agonist-stimulated [35S]GTPγS binding. Repeated METH treatment also reduced dopamine D2 receptor agonist-stimulated [ 35S]GTPγS binding in wild-type mice, but such changes were significantly attenuated in MMP-2-(-/-) and MMP-9-(-/-) mice. These results suggest that the MMP/TIMP system is involved in METH-induced behavioral sensitization and reward, by regulating dopamine release and receptor signaling.

Original languageEnglish
Pages (from-to)1548-1560
Number of pages13
JournalJournal of Neurochemistry
Volume102
Issue number5
DOIs
Publication statusPublished - 01-09-2007

Fingerprint

Tissue Inhibitor of Metalloproteinases
Matrix Metalloproteinase Inhibitors
Methamphetamine
Dopamine Receptors
Matrix Metalloproteinases
Reward
Dopamine
Down-Regulation
Tissue
Matrix Metalloproteinase 2
Matrix Metalloproteinase 9
Tissue Inhibitor of Metalloproteinase-2
Dopamine Agonists
Dopamine D2 Receptors
Nucleus Accumbens
Brain
Frontal Lobe
Oligonucleotides
Synaptic Transmission
Rats

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Cellular and Molecular Neuroscience

Cite this

Mizoguchi, Hiroyuki ; Yamada, Kiyofumi ; Mouri, Akihiro ; Niwa, Minae ; Mizuno, Tomoko ; Noda, Yukihiro ; Nitta, Atsumi ; Itohara, Shigeyoshi ; Banno, Yoshiko ; Nabeshima, Toshitaka. / Role of matrix metalloproteinase and tissue inhibitor of MMP in methamphetamine-induced behavioral sensitization and reward : Implications for dopamine receptor down-regulation and dopamine release. In: Journal of Neurochemistry. 2007 ; Vol. 102, No. 5. pp. 1548-1560.
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Role of matrix metalloproteinase and tissue inhibitor of MMP in methamphetamine-induced behavioral sensitization and reward : Implications for dopamine receptor down-regulation and dopamine release. / Mizoguchi, Hiroyuki; Yamada, Kiyofumi; Mouri, Akihiro; Niwa, Minae; Mizuno, Tomoko; Noda, Yukihiro; Nitta, Atsumi; Itohara, Shigeyoshi; Banno, Yoshiko; Nabeshima, Toshitaka.

In: Journal of Neurochemistry, Vol. 102, No. 5, 01.09.2007, p. 1548-1560.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Role of matrix metalloproteinase and tissue inhibitor of MMP in methamphetamine-induced behavioral sensitization and reward

T2 - Implications for dopamine receptor down-regulation and dopamine release

AU - Mizoguchi, Hiroyuki

AU - Yamada, Kiyofumi

AU - Mouri, Akihiro

AU - Niwa, Minae

AU - Mizuno, Tomoko

AU - Noda, Yukihiro

AU - Nitta, Atsumi

AU - Itohara, Shigeyoshi

AU - Banno, Yoshiko

AU - Nabeshima, Toshitaka

PY - 2007/9/1

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N2 - Matrix metalloproteinases (MMPs) and its inhibitors (TIMPs) function to remodel the pericellular environment. We have demonstrated that methamphetamine (METH)-induced behavioral sensitization and reward were markedly attenuated in MMP-2- and MMP-9 deficient [MMP-2-(-/-) and MMP-9-(-/-)] mice compared with those in wild-type mice, suggesting that METH-induced expression of MMP-2 and MMP-9 in the brain plays a role in the development of METH-induced sensitization and reward. In the present study, we investigated the changes in TIMP-2 expression in the brain after repeated METH treatment. Furthermore, we studied a role of MMP/TIMP system in METH-induced behavioral changes and dopamine neurotransmission. Repeated METH treatment induced behavioral sensitization, which was accompanied by an increase in TIMP-2 expression. Antisense TIMP-2 oligonucleotide (TIMP-AS) treatment enhanced the sensitization, which was associated with the potentiation of METH-induced dopamine release in the nucleus accumbens (NAc). On the other hand, MMP-2/-9 inhibitors blocked the METH-induced behavioral sensitization and conditioned place preference, a measure of the rewarding effect, and reduced the METH-increased dopamine release in the NAc. Dopamine receptor agonist-stimulated [35S]GTPγS binding was reduced in the frontal cortex of sensitized rats. TIMP-AS treatment potentiated, while MMP-2/-9 inhibitor attenuated, the reduction of dopamine D2 receptor agonist-stimulated [35S]GTPγS binding. Repeated METH treatment also reduced dopamine D2 receptor agonist-stimulated [ 35S]GTPγS binding in wild-type mice, but such changes were significantly attenuated in MMP-2-(-/-) and MMP-9-(-/-) mice. These results suggest that the MMP/TIMP system is involved in METH-induced behavioral sensitization and reward, by regulating dopamine release and receptor signaling.

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