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MeBib Suppressed Methamphetamine Self-Administration Response via Inhibition of BDNF/ERK/CREB Signal Pathway in the Hippocampus  

Kim, Buyun (College of Pharmacy, Keimyung University)
Jha, Sonam (College of Pharmacy, Keimyung University)
Seo, Ji Hae (Department of Biochemistry, School of Medicine, Keimyung University)
Jeong, Chul-Ho (College of Pharmacy, Keimyung University)
Lee, Sooyeun (College of Pharmacy, Keimyung University)
Lee, Sangkil (College of Pharmacy, Keimyung University)
Seo, Young Ho (College of Pharmacy, Keimyung University)
Park, Byoungduck (College of Pharmacy, Keimyung University)
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Biomolecules & Therapeutics / v.28, no.6, 2020 , pp. 519-526 More about this Journal
Methamphetamine (MA) is one of the most commonly abused drugs in the world by illegal drug users. Addiction to MA is a serious public health problem and effective therapies do not exist to date. It has also been reported that behavior induced by psychostimulants such as MA is related to histone deacetylase (HDAC). MeBib is an HDAC6 inhibitor derived from a benzimidazole scaffold. Many benzimidazole-containing compounds exhibit a wide range of pharmacological activity. In this study, we investigated whether HDAC6 inhibitor MeBib modulates the behavioral response in MA self-administered rats. Our results demonstrated that the number of active lever presses in MA self-administered rats was reduced by pretreatment with MeBib. In the hippocampus of rats, we also found MA administration promotes GluN2B, an NMDA receptor subunit, expression, which results in sequential activation of ERK/CREB/BDNF pathway, however, MeBib abrogated it. Collectively, we suggest that MeBib prevents the MA seeking response induced by MA administration and therefore, represents a potent candidate as an MA addiction inhibitor.
Methamphetamine; Self-administration; MeBib; HDAC6 inhibitor; Hippocampus;
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1 Galinato, M. H., Orio, L. and Mandyam, C. D. (2015) Methamphetamine differentially affects BDNF and cell death factors in anatomically defined regions of the hippocampus. Neuroscience 286, 97-108.   DOI
2 Go, B. S., Barry, S. M. and McGinty, J. F. (2016) Glutamatergic neurotransmission in the prefrontal cortex mediates the suppressive effect of intra-prelimbic cortical infusion of BDNF on cocaine-seeking. Eur. Neuropsychopharmacol. 26, 1989-1999.   DOI
3 Grace, C. E., Schaefer, T. L., Herring, N. R., Skelton, M. R., McCrea, A. E., Vorhees, C. V. and Williams, M. T. (2008) (+)-Methamphetamine increases corticosterone in plasma and BDNF in brain more than forced swim or isolation in neonatal rats. Synapse 62, 110-121.   DOI
4 Halpin, L. E., Northrop, N. A. and Yamamoto, B. K. (2014) Ammonia mediates methamphetamine-induced increases in glutamate and excitotoxicity. Neuropsychopharmacology 39, 1031-1038.   DOI
5 Huo, X. L., Min, J. J., Pan, C. Y., Zhao, C. C., Pan, L. L., Gui, F. F., Jin, L. and Wang, X. T. (2014) Efficacy of lovastatin on learning and memory deficits caused by chronic intermittent hypoxia-hypercapnia: through regulation of NR2B-containing NMDA receptor-ERK pathway. PLoS ONE 9, e94278.   DOI
6 Jang, E. Y., Ryu, Y. H., Lee, B. H., Chang, S. C., Yeo, M. J., Kim, S. H., Folsom, R. J., Schilaty, N. D., Kim, K. J., Yang, C. H., Steffensen, S. C. and Kim, H. Y. (2015) Involvement of reactive oxygen species in cocaine-taking behaviors in rats. Addict. Biol. 20, 663-675.   DOI
7 Jayanthi, S., McCoy, M. T., Chen, B., Britt, J. P., Kourrich, S., Yau, H. J., Ladenheim, B., Krasnova, I. N., Bonci, A. and Cadet, J. L. (2014) Methamphetamine downregulates striatal glutamate receptors via diverse epigenetic mechanisms. Biol. Psychiatry 76, 47-56.   DOI
8 Jing, D., Lee, F. S. and Ninan, I. (2017) The BDNF Val66Met polymorphism enhances glutamatergic transmission but diminishes activity-dependent synaptic plasticity in the dorsolateral striatum. Neuropharmacology 112, 84-93.   DOI
9 Kalivas, P. W. and Volkow, N. D. (2011) New medications for drug addiction hiding in glutamatergic neuroplasticity. Mol. Psychiatry 16, 974-986.   DOI
10 Kalda, A., Heidmets, L. T., Shen, H. Y., Zharkovsky, A. and Chen, J. F. (2007) Histone deacetylase inhibitors modulates the induction and expression of amphetamine-induced behavioral sensitization partially through an associated learning of the environment in mice. Behav. Brain Res. 181, 76-84.   DOI
11 Kim, D. J., Roh, S., Kim, Y., Yoon, S. J., Lee, H. K., Han, C. S. and Kim, Y. K. (2005) High concentrations of plasma brain-derived neurotrophic factor in methamphetamine users. Neurosci. Lett. 388, 112-115.   DOI
12 Krapivinsky, G., Krapivinsky, L., Manasian, Y., Ivanov, A., Tyzio, R., Pellegrino, C., Ben-Ari, Y., Clapham, D. E. and Medina, I. (2003) The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1. Neuron 40, 775-784.   DOI
13 Lin, S. Y., Wu, K., Levine, E. S., Mount, H. T., Suen, P. C. and Black, I. B. (1998) BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res. Mol. Brain Res. 55, 20-27.   DOI
14 Kuczenski, R., Everall, I. P., Crews, L., Adame, A., Grant, I. and Masliah, E. (2007) Escalating dose-multiple binge methamphetamine exposure results in degeneration of the neocortex and limbic system in the rat. Exp. Neurol. 207, 42-51.   DOI
15 Lazer, E. S., Matteo, M. R. and Possanza, G. J. (1987) Benzimidazole derivatives with atypical antiinflammatory activity. J. Med. Chem. 30, 726-729.   DOI
16 Li, L., Liu, X., Qiao, C., Chen, G. and Li, T. (2016) Ifenprodil attenuates methamphetamine-induced behavioral sensitization and activation of Ras-ERK-FosB pathway in the caudate putamen. Neurochem. Res. 41, 2636-2644.   DOI
17 Nash, J. F. and Yamamoto, B. K. (1992) Methamphetamine neurotoxicity and striatal glutamate release: comparison to 3,4-methylenedioxymethamphetamine. Brain Res. 581, 237-243.   DOI
18 Mishra, D., Pena-Bravo, J. I., Leong, K. C., Lavin, A. and Reichel, C. M. (2017) Methamphetamine self-administration modulates glutamate neurophysiology. Brain Struct. Funct. 222, 2031-2039.   DOI
19 Mizoguchi, H., Yamada, K., Mizuno, M., Mizuno, T., Nitta, A., Noda, Y. and Nabeshima, T. (2004) Regulations of methamphetamine reward by extracellular signal-regulated kinase 1/2/ets-like gene-1 signaling pathway via the activation of dopamine receptors. Mol. Pharmacol. 65, 1293-1301.   DOI
20 Moriguchi, S., Watanabe, S., Kita, H. and Nakanishi, H. (2002) Enhancement of N-methyl- D-aspartate receptor-mediated excitatory postsynaptic potentials in the neostriatum after methamphetamine sensitization. An in vitro slice study. Exp. Brain Res. 144, 238-246.   DOI
21 Ricoy, U. M. and Martinez, J. L., Jr. (2009) Local hippocampal methamphetamine-induced reinforcement. Front. Behav. Neurosci. 3, 47.   DOI
22 Nestler, E. J. (2001) Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2, 119-128.   DOI
23 Pickens, C. L., Airavaara, M., Theberge, F., Fanous, S., Hope, B. T. and Shaham, Y. (2011) Neurobiology of the incubation of drug craving. Trends Neurosci. 34, 411-420.   DOI
24 Qi, J., Han, W. Y., Yang, J. Y., Wang, L. H., Dong, Y. X., Wang, F., Song, M. and Wu, C. F. (2012) Oxytocin regulates changes of extracellular glutamate and GABA levels induced by methamphetamine in the mouse brain. Addict. Biol. 17, 758-769.   DOI
25 Rocher, C. and Gardier, A. M. (2001) Effects of repeated systemic administration of d-Fenfluramine on serotonin and glutamate release in rat ventral hippocampus: comparison with methamphetamine using in vivo microdialysis. Naunyn Schmiedebergs Arch. Pharmacol. 363, 422-428.   DOI
26 Seto, E. and Yoshida, M. (2014) Erasers of histone acetylation: the histone deacetylase enzymes. Cold Spring Harb. Perspect. Biol. 6, a018713.   DOI
27 Rosenblum, K., Dudai, Y. and Richter-Levin, G. (1996) Long-term potentiation increases tyrosine phosphorylation of the N-methyl-D-aspartate receptor subunit 2B in rat dentate gyrus in vivo. Proc. Natl. Acad. Sci. U.S.A. 93, 10457-10460.   DOI
28 Rostas, J. A., Brent, V. A., Voss, K., Errington, M. L., Bliss, T. V. and Gurd, J. W. (1996) Enhanced tyrosine phosphorylation of the 2B subunit of the N-methyl-D-aspartate receptor in long-term potentiation. Proc. Natl. Acad. Sci. U.S.A. 93, 10452-10456.   DOI
29 Sakamoto, K., Karelina, K. and Obrietan, K. (2011) CREB: a multifaceted regulator of neuronal plasticity and protection. J. Neurochem. 116, 1-9.   DOI
30 Scott, J. C., Woods, S. P., Matt, G. E., Meyer, R. A., Heaton, R. K., Atkinson, J. H. and Grant, I. (2007) Neurocognitive effects of methamphetamine: a critical review and meta-analysis. Neuropsychol. Rev. 17, 275-297.   DOI
31 Simoes, P. F., Silva, A. P., Pereira, F. C., Marques, E., Milhazes, N., Borges, F., Ribeiro, C. F. and Macedo, T. R. (2008) Methamphetamine changes NMDA and AMPA glutamate receptor subunit levels in the rat striatum and frontal cortex. Ann. N. Y. Acad. Sci. 1139, 232-241.   DOI
32 Simon, S. L., Dacey, J., Glynn, S., Rawson, R. and Ling, W. (2004) The effect of relapse on cognition in abstinent methamphetamine abusers. J. Subst. Abuse Treat. 27, 59-66.   DOI
33 Skelton, M. R., Williams, M. T., Schaefer, T. L. and Vorhees, C. V. (2007) Neonatal (+)-methamphetamine increases brain derived neurotrophic factor, but not nerve growth factor, during treatment and results in long-term spatial learning deficits. Psychoneuroendocrinology 32, 734-745.   DOI
34 Stucky, A., Bakshi, K. P., Friedman, E. and Wang, H. Y. (2016) Prenatal cocaine exposure upregulates BDNF-TrkB signaling. PLoS ONE 11, e0160585.   DOI
35 Yeh, G. C., Chen, J. C., Tsai, H. C., Wu, H. H., Lin, C. Y., Hsu, P. C. and Peng, Y. C. (2002) Amphetamine inhibits the N-methyl-D-aspartate receptor-mediated responses by directly interacting with the receptor/channel complex. J. Pharmacol. Exp. Ther. 300, 1008-1016.   DOI
36 Thomas, D. M., Walker, P. D., Benjamins, J. A., Geddes, T. J. and Kuhn, D. M. (2004) Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation. J. Pharmacol. Exp. Ther. 311, 1-7.   DOI
37 Torres, O. V., Ladenheim, B., Jayanthi, S., McCoy, M. T., Krasnova, I. N., Vautier, F. A. and Cadet, J. L. (2016) An acute methamphetamine injection downregulates the expression of several histone deacetylases (HDACs) in the mouse nucleus accumbens: potential regulatory role of HDAC2 expression. Neurotox. Res. 30, 32-40.   DOI
38 Vecsey, C. G., Hawk, J. D., Lattal, K. M., Stein, J. M., Fabian, S. A., Attner, M. A., Cabrera, S. M., McDonough, C. B., Brindle, P. K., Abel, T. and Wood, M. A. (2007) Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J. Neurosci. 27, 6128-6140.   DOI
39 Walz, C., Jungling, K., Lessmann, V. and Gottmann, K. (2006) Presynaptic plasticity in an immature neocortical network requires NMDA receptor activation and BDNF release. J. Neurophysiol. 96, 3512-3516.   DOI
40 Xing, A., Li, X., Jiang, C., Chen, Y., Wu, S., Zhang, J. and An, L. (2019) As a histone deacetylase inhibitor, gamma-aminobutyric acid upregulates GluR2 expression: an in vitro and in vivo study. Mol. Nutr. Food Res. 63, e1900001.
41 Zhang, S., Jin, Y., Liu, X., Yang, L., Ge, Z., Wang, H., Li, J. and Zheng, J. (2014) Methamphetamine modulates glutamatergic synaptic transmission in rat primary cultured hippocampal neurons. Brain Res. 1582, 1-11.   DOI
42 Brami-Cherrier, K., Valjent, E., Herve, D., Darragh, J., Corvol, J. C., Pages, C., Arthur, S. J., Girault, J. A. and Caboche, J. (2005) Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice. J. Neurosci. 25, 11444-11454.   DOI
43 Abekawa, T., Ohmori, T. and Koyama, T. (1994) Effects of repeated administration of a high dose of methamphetamine on dopamine and glutamate release in rat striatum and nucleus accumbens. Brain Res. 643, 276-281.   DOI
44 Ashabi, G., Sadat-Shirazi, M. S., Khalifeh, S., Elhampour, L. and Zarrindast, M. R. (2017) NMDA receptor adjusted co-administration of ecstasy and cannabinoid receptor-1 agonist in the amygdala via stimulation of BDNF/Trk-B/CREB pathway in adult male rats. Brain Res. Bull. 130, 221-230.   DOI
45 Berberich, S., Jensen, V., Hvalby, O., Seeburg, P. H. and Kohr, G. (2007) The role of NMDAR subtypes and charge transfer during hippocampal LTP induction. Neuropharmacology 52, 77-86.   DOI
46 Bhattacharya, S., Mukherjee, B., Dore, J. J. E., Yuan, Q., Harley, C. W. and McLean, J. H. (2017) Histone deacetylase inhibition induces odor preference memory extension and maintains enhanced AMPA receptor expression in the rat pup model. Learn. Mem. 24, 543-551.   DOI
47 Bowyer, J. F. and Ali, S. (2006) High doses of methamphetamine that cause disruption of the blood-brain barrier in limbic regions produce extensive neuronal degeneration in mouse hippocampus. Synapse 60, 521-532.   DOI
48 Cadet, J. L. (2016) Epigenetics of stress, addiction, and resilience: therapeutic implications. Mol. Neurobiol. 53, 545-560.   DOI
49 Caldeira, M. V., Melo, C. V., Pereira, D. B., Carvalho, R. F., Carvalho, A. L. and Duarte, C. B. (2007) BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons. Mol. Cell. Neurosci. 35, 208-219.   DOI
50 Cadet, J. L., Jayanthi, S., McCoy, M. T., Ladenheim, B., Saint-Preux, F., Lehrmann, E., De, S., Becker, K. G. and Brannock, C. (2013) Genome-wide profiling identifies a subset of methamphetamine (METH)-induced genes associated with METH-induced increased H4K5Ac binding in the rat striatum. BMC Genomics 14, 545.   DOI
51 da Silveira, F. P., Basso, C., Raupp, W., Dalpiaz, M., Bertoldi, K., Siqueira, I. R., Lago, P. D., de Souza, M. P. and Elsner, V. R. (2017) BDNF levels are increased in peripheral blood of middle-aged amateur runners with no changes on histone H4 acetylation levels. J. Physiol. Sci. 67, 681-687.   DOI
52 Cammarota, M., Bevilaqua, L. R., Medina, J. H. and Izquierdo, I. (2008) ERK1/2 and CaMKII-mediated events in memory formation: is 5HT regulation involved? Behav. Brain Res. 195, 120-128.   DOI
53 Cao, G., Zhu, J., Zhong, Q., Shi, C., Dang, Y., Han, W., Liu, X., Xu, M. and Chen, T. (2013) Distinct roles of methamphetamine in modulating spatial memory consolidation, retrieval, reconsolidation and the accompanying changes of ERK and CREB activation in hippocampus and prefrontal cortex. Neuropharmacology 67, 144-154.   DOI
54 Chen, G., Liu, Z., Zhang, Y., Shan, X., Jiang, L., Zhao, Y., He, W., Feng, Z., Yang, S. and Liang, G. (2013) Synthesis and anti-inflammatory evaluation of novel benzimidazole and imidazopyridine derivatives. ACS Med. Chem. Lett. 4, 69-74.   DOI
55 Easmon, J., Puerstinger, G., Roth, T., Fiebig, H. H., Jenny, M., Jaeger, W., Heinisch, G. and Hofmann, J. (2001) 2-benzoxazolyl and 2-benzimidazolyl hydrazones derived from 2-acetylpyridine: a novel class of antitumor agents. Int. J. Cancer 94, 89-96.   DOI
56 Fernandes, S., Salta, S. and Summavielle, T. (2015) Methamphetamine promotes alpha-tubulin deacetylation in endothelial cells: the protective role of acetyl-l-carnitine. Toxicol. Lett. 234, 131-138.   DOI
57 Eckroat, T. J., Mayhoub, A. S. and Garneau-Tsodikova, S. (2013) Amyloid-beta probes: review of structure-activity and brain-kinetics relationships. Beilstein J. Org. Chem. 9, 1012-1044.   DOI
58 Ersche, K. D., Clark, L., London, M., Robbins, T. W. and Sahakian, B. J. (2006) Profile of executive and memory function associated with amphetamine and opiate dependence. Neuropsychopharmacology 31, 1036-1047.   DOI