Abstract
Methamphetamine (METH) abuse is a serious social and health problem worldwide. At present, there are no effective medications to treat METH addiction1. Here, we report that aggregated single-walled carbon nanotubes (aSWNTs) significantly inhibited METH self-administration, METH-induced conditioned place preference and METH- or cue-induced relapse to drug-seeking behaviour in mice. The use of aSWNTs alone did not significantly alter the mesolimbic dopamine system, whereas pretreatment with aSWNTs attenuated METH-induced increases in extracellular dopamine in the ventral striatum. Electrochemical assays suggest that aSWNTs facilitated dopamine oxidation. In addition, aSWNTs attenuated METH-induced increases in tyrosine hydroxylase or synaptic protein expression. These findings suggest that aSWNTs may have therapeutic effects for treatment of METH addiction by oxidation of METH-enhanced extracellular dopamine in the striatum.
Similar content being viewed by others
References
Vocci, F. J. & Appel, N. M. Approaches to the development of medications for the treatment of methamphetamine dependence. Addiction 102, 96–106 (2007).
Giraldo, J. P. et al. A ratiometric sensor using single chirality near-infrared fluorescent carbon nanotubes: application to in vivo monitoring. Small 11, 3973–3984 (2015).
Khan, A. A. et al. Tunable scattering from liquid crystal devices using carbon nanotubes network electrodes. Nanoscale 7, 330–336 (2015).
Xue, X. et al. Single-walled carbon nanotubes alleviate autophagic/lysosomal defects in primary glia from a mouse model of Alzheimer's disease. Nano Lett. 14, 5110–5117 (2014).
Lee, H. J. et al. Amine-modified single-walled carbon nanotubes protect neurons from injury in a rat stroke model. Nature Nanotech. 6, 121–125 (2011).
Ma, X. W. et al. Single-walled carbon nanotubes alter cytochrome c electron transfer and modulate mitochondrial function. ACS Nano 6, 10486–10496 (2012).
Wang, L. R. et al. Structure-dependent mitochondrial dysfunction and hypoxia induced with single-walled carbon nanotubes. Small. 10, 2859–2869 (2014).
Figueiredo-Filho, L. C., Silva, T. A., Vicentini, F. C. & Fatibello-Filho, O. Simultaneous voltammetric determination of dopamine and epinephrine in human body fluid samples using a glassy carbon electrode modified with nickel oxide nanoparticles and carbon nanotubes within a dihexadecylphosphate film. Analyst 139, 2842–2849 (2014).
Tiwari, J. N., Vij, V., Kemp, K. C. & Kim, K. S. Engineered carbon-nanomaterial-based electrochemical sensors for biomolecules. ACS Nano 10, 46–80 (2016).
Yang, C., Denno, M. E., Pyakurel, P. & Venton, B. J. Recent trends in carbon nanomaterial-based electrochemical sensors for biomolecules: A review. Anal. Chim. Acta. 887, 17–37 (2015).
Wise, R. A. Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotox. Res. 14, 169–183 (2008).
Chiu, V. M. & Schenk, J. O. Mechanism of action of methamphetamine within the catecholamine and serotonin areas of the central nervous system. Curr. Drug Abuse Rev. 5, 227–242 (2012).
O'Brien, C. P. & Gardner, E. L. Critical assessment of how to study addiction and its treatment: Human and non-human animal models. Pharmacol. Ther. 108, 18–58 (2005).
Pickens, C. L. et al. Neurobiology of the incubation of drug craving. Trends Neurosci. 34, 411–420 (2011).
Keller, C. M. et al. Biphasic dopamine regulation in mesoaccumbens pathway in response to non-contingent binge and escalating methamphetamine regimens in the Wistar rat. Psychopharmacology 215, 513–526 (2011).
Shepard, J. D., Chuang, D. T., Shaham, Y. & Morales, M. Effect of methamphetamine self-administration on tyrosine hydroxylase and dopamine transporter levels in mesolimbic and nigrostriatal dopamine pathways of the rat. Psychopharmacology 185, 505–513 (2006).
Zhu, J. et al. Distinct roles of dopamine D3 receptors in modulating methamphetamine-induced behavioral sensitization and ultrastructural plasticity in the shell of the nucleus accumbens. J. Neurosci. Res. 90, 895–904 (2012).
Robinson, T. E. & Kolb, B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47, 33–46 (2004).
Song, R. et al. Increased vulnerability to cocaine in mice lacking dopamine D3 receptors. Proc. Natl Acad. Sci. USA 109, 17675–17680 (2012).
Xi, Z. X. et al. Brain cannabinoid CB2 receptors modulate cocaine's actions in mice. Nature Neurosci. 14, 1160–1166 (2011).
Arnold, M. S., Green, A. A., Hulvat, J. F., Stupp, S. I. & Hersam, M. C. Sorting carbon nanotubes by electronic structure using density differentiation. Nature Nanotech. 1, 60–65 (2006).
Edwards, S. L., Werkmeister, J. A. & Ramshaw, J. A. M. Carbon nanotubes in scaffolds for tissue engineering. Expert Rev. Med. Devices 6, 499–505 (2009).
Keefer, E. W., Botterman, B. R., Romero, M. I., Rossi, A. F. & Gross, G. W. Carbon nanotube coating improves neuronal recordings. Nature Nanotech. 3, 434–439 (2008).
Suzuki, I., Fukuda, M., Shirakawa, K., Jiko, H. & Gotoh, M. Carbon nanotube multi-electrode array chips for noninvasive real-time measurement of dopamine, action potentials, and postsynaptic potentials. Biosens. Bioelectron. 49, 270–275 (2013).
Bardi, G. et al. Functionalized carbon nanotubes in the brain: cellular internalization and neuroinflammatory responses. PLoS ONE 8, e80964 (2013).
Wang, L., Zhang, L., Xue, X., Ge, G. L. & Liang, X. J. Enhanced dispersibility and cellular transmembrane capability of single-wall carbon nanotubes by polycyclic organic compounds as chaperon. Nanoscale 4, 3983–3989 (2012).
Qi, J. et al. Inhibition by oxytocin of methamphetamine-induced hyperactivity related to dopamine turnover in the mesolimbic region in mice. N. S. Arch. Pharmacol. 376, 441–448 (2008).
Qi, J. et al. 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 56, 856–865 (2009).
Han, W. Y. et al. Oxytocin via its receptor affects restraint stress-induced methamphetamine CPP reinstatement in mice: involvement of the medial prefrontal cortex and dorsal hippocampus glutamatergic system. Pharmacol. Biochem. Behav. 119, 80–87 (2013).
Qi, J. et al. A glutamatergic reward input from the dorsal raphe to ventral tegmental area dopamine neurons. Nature Commun. 5, 5390 (2014).
Colonnier, M. & Beaulieu, C. An empirical assessment of stereological formulae applied to the counting of synaptic disks in the cerebral cortex. J. Comp. Neurol. 231, 175–179 (1985).
DeFelipe, J., Marco, P., Busturia, I. & Merchan-Perez, A. Estimation of the number of synapses in the cerebral cortex: methodological considerations. Cereb. Cortex. 9, 722–732 (1999).
Acknowledgements
This work was supported by the National Key Scientific Project for New Drug Discovery and Development (2013ZX09301305), the National Natural Science Foundation key project (31430031), the National Distinguished Young Scholars grant (31225009) and the National Natural Science Foundation (No. 81373383) in China. This work was also supported by State High-Tech Development Plan (2012AA020804 and SS2014AA020708) and the National Institute on Drug Abuse (NIDA), Intramural Research Program (IRP), National Institutes of Health (NIH) in the United States of America. We also gratefully acknowledge support from the Chinese Academy of Sciences (CAS), Hundred Talents Program (07165111ZX), the CAS Knowledge Innovation Program, the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA09030301) and the external collaboration program of BIC, Chinese Academy of Science (121D11KYSB20130006). We thank I. Hanson for English editing services.
Author information
Authors and Affiliations
Contributions
X.X., J.-Y.Y., Y.H., G.-L.G., Z.-X.X., C.-F.W. and X.-J.L. conceived and designed the experiments. X.X., Y.H., L.-R.W., P.L., L.-S.Y., G.-H.B., M.-M.Z., Y.-Y.L., X.-T.Y., X.-Y.F., X.-M.W. and W.C. performed the experiments. X.X., J.-Y.Y., Y.H., L.-R.W., R.-W.X., J.Q., H.-J.Z., Z.-X.X. and X.-J.L. analyzed the data. X.X. and L.-R.W. contributed materials/analysis tools. X.X., J.-Y.Y., Y.H., T.W., Z.-X.X. C.-F.W. and X.-J.L. wrote the paper. All authors discussed the results and commented on the manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary information
Supplementary information (PDF 1375 kb)
Rights and permissions
About this article
Cite this article
Xue, X., Yang, JY., He, Y. et al. Aggregated single-walled carbon nanotubes attenuate the behavioural and neurochemical effects of methamphetamine in mice. Nature Nanotech 11, 613–620 (2016). https://doi.org/10.1038/nnano.2016.23
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nnano.2016.23
- Springer Nature Limited
This article is cited by
-
Astrocyte-derived lactate/NADH alters methamphetamine-induced memory consolidation and retrieval by regulating neuronal synaptic plasticity in the dorsal hippocampus
Brain Structure and Function (2022)
-
Ascorbic acid derived carbon dots promote circadian rhythm and contribute to attention deficit hyperactivity disorder
Nano Research (2022)
-
Iron-sulphur cluster biogenesis factor LYRM4 is a novel prognostic biomarker associated with immune infiltrates in hepatocellular carcinoma
Cancer Cell International (2021)
-
The neuroprotective effect of pretreatment with carbon dots from Crinis Carbonisatus (carbonized human hair) against cerebral ischemia reperfusion injury
Journal of Nanobiotechnology (2021)
-
Carbon Nanotubes in Biomedicine
Topics in Current Chemistry (2020)