Preventive Effect of Low Intensity Pulsed Ultrasound against Experimental Cerebral Ischemia/Reperfusion Injury via Apoptosis Reduction and Brain-derived Neurotrophic Factor Induction

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Abstract

Stroke is known as the top 10 causes of death worldwide. Development of effectively neuroprotective or preventive strategies for ischemia stroke is imperative. For the purpose of stroke prevention, we tested the neuroprotective effects of low-intensity pulsed ultrasound (LIPUS) on ischemic stroke. Adult C57BL/6 mice were used to daily treatment with LIPUS for 5 days on left hemisphere before middle cerebral artery occlusion (MCAO)-induced cerebral ischemia/reperfusion injury. Western blotting and immunohistochemistry were performed to assess the protein expressions of signaling molecules. Pretreatment with LIPUS significantly ameliorated the brain ischemic damage, including the reduction of neurological deficit score, infarct area, histopathological score, and showed a better performance in neurological and behavior functions. LIPUS pretreatment could also significantly decrease the neuronal cell apoptosis and upregulation of apoptosis-related signaling molecules and downregulation of brain-derived neurotrophic factor (BDNF) in brain tissues of MCAO-treated mice. Furthermore, LIPUS significantly prevented the decreased cell viability, the increased caspase-3 cleavage, and the decreased BDNF expression in ischemia/reperfusion-treated microglial cells. These results demonstrate that LIPUS effectively prevented the cerebral ischemia/reperfusion injury through apoptosis reduction and BDNF induction in a MCAO mouse model. The neuroprotective potential of LIPUS may provide a novel preventive strategy for ischemic stroke in high-risk patients.

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Most cited references 37

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Neuroplasticity - exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects.

Kristel Knaepen, Maaike Goekint, Elsa Marie Heyman … (2010)

Exercise is known to induce a cascade of molecular and cellular processes that support brain plasticity. Brain-derived neurotrophic factor (BDNF) is an essential neurotrophin that is also intimately connected with central and peripheral molecular processes of energy metabolism and homeostasis, and could play a crucial role in these induced mechanisms. This review provides an overview of the current knowledge on the effects of acute exercise and/or training on BDNF in healthy subjects and in persons with a chronic disease or disability. A systematic and critical literature search was conducted. Articles were considered for inclusion in the review if they were human studies, assessed peripheral (serum and/or plasma) BDNF and evaluated an acute exercise or training intervention. Nine RCTs, one randomized trial, five non-randomized controlled trials, five non-randomized non-controlled trials and four retrospective observational studies were analysed. Sixty-nine percent of the studies in healthy subjects and 86% of the studies in persons with a chronic disease or disability, showed a 'mostly transient' increase in serum or plasma BDNF concentration following an acute aerobic exercise. The two studies regarding a single acute strength exercise session could not show a significant influence on basal BDNF concentration. In studies regarding the effects of strength or aerobic training on BDNF, a difference should be made between effects on basal BDNF concentration and training-induced effects on the BDNF response following an acute exercise. Only three out of ten studies on aerobic or strength training (i.e. 30%) found a training-induced increase in basal BDNF concentration. Two out of six studies (i.e. 33%) reported a significantly higher BDNF response to acute exercise following an aerobic or strength training programme (i.e. compared with the BDNF response to an acute exercise at baseline). A few studies of low quality (i.e. retrospective observational studies) show that untrained or moderately trained healthy subjects have higher basal BDNF concentrations than highly trained subjects. Yet, strong evidence still has to come from good methodological studies. Available results suggest that acute aerobic, but not strength exercise increases basal peripheral BDNF concentrations, although the effect is transient. From a few studies we learn that circulating BDNF originates both from central and peripheral sources. We can only speculate which central regions and peripheral sources in particular circulating BDNF originates from, where it is transported to and to what purpose it is used and/or stored at its final destination. No study could show a long-lasting BDNF response to acute exercise or training (i.e. permanently increased basal peripheral BDNF concentration) in healthy subjects or persons with a chronic disease or disability. It seems that exercise and/or training temporarily elevate basal BDNF and possibly upregulate cellular processing of BDNF (i.e. synthesis, release, absorption and degradation). From that point of view, exercise and/or training would result in a higher BDNF synthesis following an acute exercise bout (i.e. compared with untrained subjects). Subsequently, more BDNF could be released into the blood circulation which may, in turn, be absorbed more efficiently by central and/or peripheral tissues where it could induce a cascade of neurotrophic and neuroprotective effects.

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Transcranial pulsed ultrasound stimulates intact brain circuits.

Yusuf Tufail, Alexei Matyushov, Nathan Baldwin … (2010)

Electromagnetic-based methods of stimulating brain activity require invasive procedures or have other limitations. Deep-brain stimulation requires surgically implanted electrodes. Transcranial magnetic stimulation does not require surgery, but suffers from low spatial resolution. Optogenetic-based approaches have unrivaled spatial precision, but require genetic manipulation. In search of a potential solution to these limitations, we began investigating the influence of transcranial pulsed ultrasound on neuronal activity in the intact mouse brain. In motor cortex, ultrasound-stimulated neuronal activity was sufficient to evoke motor behaviors. Deeper in subcortical circuits, we used targeted transcranial ultrasound to stimulate neuronal activity and synchronous oscillations in the intact hippocampus. We found that ultrasound triggers TTX-sensitive neuronal activity in the absence of a rise in brain temperature (<0.01 degrees C). Here, we also report that transcranial pulsed ultrasound for intact brain circuit stimulation has a lateral spatial resolution of approximately 2 mm and does not require exogenous factors or surgical invasion. Copyright 2010 Elsevier Inc. All rights reserved.

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New insights in the biology of BDNF synthesis and release: implications in CNS function.

Baoji Xu, E. Peter Greenberg, Barbara L. Hempstead … (2009)

BDNF has pleiotropic effects on neuronal development and synaptic plasticity that underlie circuit formation and cognitive function. Recent breakthroughs reveal that neuronal activity regulates BDNF cell biology, including Bdnf transcription, dendritic targeting and trafficking of BDNF mRNA and protein, and secretion and extracellular conversion of proBDNF to mature BDNF. Defects in these mechanisms contribute differentially to cognitive dysfunction and anxiety-like behaviors. Here we review recent studies, presented at a symposium at Neuroscience 2009, that describe regulatory mechanisms that permit rapid and dynamic refinement of BDNF actions in neurons.

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Author and article information

Contributors

Chang-Mu Chen: cmchen10@ms27.hinet.net

Shing-Hwa Liu: shinghwaliu@ntu.eud.tw

Feng-Yi Yang: fyyang@ym.edu.tw

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 3 April 2018

Publication date PMC-release: 3 April 2018

Publication date Collection: 2018

Volume: 8

Electronic Location Identifier: 5568

Affiliations

[1 ]GRID grid.145695.a, Division of Neurosurgery, Department of Surgery, , National Taiwan University Hospital and National Taiwan University, College of Medicine, ; Taipei, Taiwan

[2 ]ISNI 0000 0004 0546 0241, GRID grid.19188.39, Institute of Toxicology, , College of Medicine, National Taiwan University, ; Taipei, Taiwan

[3 ]ISNI 0000 0004 0572 7815, GRID grid.412094.a, Department of Otolaryngology, , National Taiwan University Hospital, ; Taipei, Taiwan

[4 ]ISNI 0000 0004 0546 0241, GRID grid.19188.39, Department of Pediatrics, , College of Medicine and Hospital, National Taiwan University, ; Taipei, Taiwan

[5 ]Department of Medical Research, China Medical University Hospital, China Medical University, Taichung, Taiwan

[6 ]ISNI 0000 0001 0425 5914, GRID grid.260770.4, Department of Biomedical Imaging and Radiological Sciences, , National Yang-Ming University, ; Taipei, Taiwan

[7 ]ISNI 0000 0001 0425 5914, GRID grid.260770.4, Biophotonics and Molecular Imaging Research Center, , National Yang-Ming University, ; Taipei, Taiwan

Article

Publisher ID: 23929

DOI: 10.1038/s41598-018-23929-8

PMC ID: 5882812

PubMed ID: 29615782

SO-VID: 2ccf6be8-a73d-42e5-8e04-946fff84d967

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 19 January 2018

Date accepted : 20 March 2018

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Preventive Effect of Low Intensity Pulsed Ultrasound against Experimental Cerebral Ischemia/Reperfusion Injury via Apoptosis Reduction and Brain-derived Neurotrophic Factor Induction

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Probing cerebral hemodynamics with BOLD fMRI

Most cited references 37

Neuroplasticity - exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects.

Transcranial pulsed ultrasound stimulates intact brain circuits.

New insights in the biology of BDNF synthesis and release: implications in CNS function.

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Cited by 27

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