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Repeated Forced Swim Exacerbates Methamphetamine-Induced Neurotoxicity: Neuroprotective Effects of Nanowired Delivery of 5-HT3-Receptor Antagonist Ondansetron

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Abstract

The possibility that stress associated with chronic forced swim (FS) may exacerbate methamphetamine (METH) neurotoxicity was examined in a rat model. Rats were subjected to FS in a pool (30 °C) for 15 min daily for 8 days. Control rats were kept at room temperature. METH was administered (9 mg/kg, s.c.) in both control and FS rats and allowed to survive 4 h after the drug injection. METH in FS rats exacerbated BBB breakdown to Evans blue albumin (EBA) by 150 to 220% and [131]-Iodine by 250 to 380% as compared to naive rats after METH. The METH-induced BBB leakage was most pronounced in the cerebral cortex followed by the hippocampus, cerebellum, thalamus, and hypothalamus in both FS and naive rats. The regional BBB changes were associated with a reduction in the local cerebral blood flow (CBF). Brain edema was also higher by 2 to 4% in FS rats after METH than in naive animals. Neuronal and glial cell injuries were aggravated by threefold to fivefold after METH in FS than the control group. Pretreatment with ondansetron (1 mg/kg, i.p.) 30 min before METH injection in naive rats reduced the brain pathology and improved the CBF. However, TiO2-nanowired delivery of ondansetron (1 mg/kg, i.p.) was needed to reduce METH-induced brain damage, BBB leakage, reduction in CBF, and edema formation in FS. Taken together, these observations are the first to show that METH exacerbates BBB breakdown leading to neurotoxicity in FS animals. This effect of METH-induced BBB breakdown and brain pathology in naive and FS rats is attenuated by ondansetron treatment indicating an involvement of 5-HT3 receptors, not reported earlier.

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Acknowledgements

This study is supported by grants from the Air Force Office of Scientific Research (EOARD, London, UK) and Air Force Material Command, USAF, under grant number FA8655-05-1-3065; the National Institutes of Health (R01 AG028679) Swedish Medical Research Council (Nr 2710-HSS), Göran Gustafsson Foundation, Stockholm, Sweden (HSS), Astra Zeneca, Mölndal, Sweden (HSS/AS), the University Grants Commission, New Delhi, India (HSS/AS), Ministry of Science & Technology, Govt. of India (HSS/AS), Indian Medical Research Council, New Delhi, India (HSS/AS), and India-EU Co-operation Program (RP/AS/HSS) and IT 901/16 (JVL), Government of Basque Country, and UFI 11/32 and PPG 17/51 (JVL) University of Basque Country, Spain, and Society for Neuroprotection and Neuroplasticity (SSNN), Romania. We thank Suraj Sharma, Uppsala, Sweden, for computer and graphic support. The US Government is authorized to reproduce and distribute reprints for Government purposes notwithstanding any copyright notation thereon. The views and conclusions contained herein are those of the authors and should not be interpreted as necessarily representing the official policies or endorsements, either expressed or implied, of the Air Force Office of Scientific Research or the US Government. We are grateful to anonymous reviewers for their very constructive comments that resulted in a significant increase in the quality of the revised manuscript.

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Authors and Affiliations

  1. LaNCE, Department of Neuroscience, University of the Basque Country (UPV/EHU), Leioa, Biscay, Spain

    José Vicente Lafuente, Aruna Sharma & Hari S. Sharma

  2. Nanoneurosurgery Group, BioCruces Health Research Institute, 48903, Barakaldo, Biscay, Spain

    José Vicente Lafuente

  3. Faculty of Health Science, Universidad Autónoma de Chile, Santiago de Chile, Chile

    José Vicente Lafuente

  4. Department of Surgical Sciences, Anesthesiology & Intensive Care Medicine, Uppsala University Hospital, Uppsala University, SE-75185, Uppsala, Sweden

    Aruna Sharma & Hari S. Sharma

  5. International Experimental CNS Injury & Repair (IECNSIR), University Hospital, Uppsala University, Frödingsgatan 12, Bldg. 28, SE-75421, Uppsala, Sweden

    Aruna Sharma & Hari S. Sharma

  6. “RoNeuro” Institute for Neurological Research and Diagnostic, 37 Mircea Eliade Street, 400364, Cluj-Napoca, Romania

    Dafin F. Muresanu

  7. Department of Clinical Neurosciences, University of Medicine & Pharmacy, Cluj-Napoca, Romania

    Dafin F. Muresanu

  8. Department of Biomedical Engineering, University of Arkansas, Fayetteville, AR, USA

    Asya Ozkizilcik

  9. Department of Chemistry and Biochemistry, J. William Fulbright College of Arts and Sciences, University of Arkansas, Fayetteville, AR, USA

    Z. Ryan Tian

  10. School of Biomedical Engineering, Department of Biomaterials, Indian Institute of technology, Banaras Hindu University, Varanasi, India

    Ranjana Patnaik

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  1. José Vicente Lafuente
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  2. Aruna Sharma
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  3. Dafin F. Muresanu
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  4. Asya Ozkizilcik
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  5. Z. Ryan Tian
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  6. Ranjana Patnaik
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  7. Hari S. Sharma
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Corresponding author

Correspondence to Hari S. Sharma.

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All experiments were carried out according to National Institutes of Health (NIH) Guide for the Care and Use of Laboratory Animals and approved by the Local Institutional Ethics Committee [44].

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Lafuente, J.V., Sharma, A., Muresanu, D.F. et al. Repeated Forced Swim Exacerbates Methamphetamine-Induced Neurotoxicity: Neuroprotective Effects of Nanowired Delivery of 5-HT3-Receptor Antagonist Ondansetron. Mol Neurobiol 55, 322–334 (2018). https://doi.org/10.1007/s12035-017-0744-7

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