Stereotactic Administration of Edaravone Ameliorates Collagenase‐Induced Intracerebral Hemorrhage in Rat

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Summary

Background

Edaravone is widely used for treating ischemic stroke, but it is not still confirmed in intracerebral hemorrhage ( ICH) as an ideal medication targeting the brain parenchyma. We aimed to investigate the neuroprotective effects of stereotactic administration of edaravone ( SI) into the brain parenchyma.

Methods

Intracerebral hemorrhage rat models were established by infusion of collagenase into the caudate nucleus. Neural functional recovery was assessed using modified neurological severity scores ( mNSS). A comparative study of therapeutic effects between SI and intraperitoneal injection of edaravone ( IP) involved in cerebral edema, blood–brain barrier ( BBB) permeability, hematoma absorption, inflammatory response and neuronal apoptosis.

Results

Compared with IP, the mNSS was significantly ( P < 0.05) improved by SI; cerebral edema and BBB permeability were dramatically ameliorated ( P < 0.05); IL‐4 and IL‐10 levels increased, but IL‐1β and TNF‐α levels significantly decreased; neuron apoptosis decreased markedly ( P < 0.05); and caspase‐3 and Bax expression significantly dropped, but Bcl‐2 increased in SI group ( P < 0.05).

Conclusion

SI markedly improved neurological deficits in ICH rat models via antiinflammatory and antiapoptosis mechanisms and promoted M2‐type microglia differentiation. SI was effective in rats with collagenase‐induced ICH.

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Most cited references 36

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TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease

Melissa McCoy, Malú G. Tansey (2008)

The role of tumor necrosis factor (TNF) as an immune mediator has long been appreciated but its function in the brain is still unclear. TNF receptor 1 (TNFR1) is expressed in most cell types, and can be activated by binding of either soluble TNF (solTNF) or transmembrane TNF (tmTNF), with a preference for solTNF; whereas TNFR2 is expressed primarily by microglia and endothelial cells and is preferentially activated by tmTNF. Elevation of solTNF is a hallmark of acute and chronic neuroinflammation as well as a number of neurodegenerative conditions including ischemic stroke, Alzheimer's (AD), Parkinson's (PD), amyotrophic lateral sclerosis (ALS), and multiple sclerosis (MS). The presence of this potent inflammatory factor at sites of injury implicates it as a mediator of neuronal damage and disease pathogenesis, making TNF an attractive target for therapeutic development to treat acute and chronic neurodegenerative conditions. However, new and old observations from animal models and clinical trials reviewed here suggest solTNF and tmTNF exert different functions under normal and pathological conditions in the CNS. A potential role for TNF in synaptic scaling and hippocampal neurogenesis demonstrated by recent studies suggest additional in-depth mechanistic studies are warranted to delineate the distinct functions of the two TNF ligands in different parts of the brain prior to large-scale development of anti-TNF therapies in the CNS. If inactivation of TNF-dependent inflammation in the brain is warranted by additional pre-clinical studies, selective targeting of TNFR1-mediated signaling while sparing TNFR2 activation may lessen adverse effects of anti-TNF therapies in the CNS.

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Collagenase-induced intracerebral hemorrhage in rats.

Jennifer Wesley, Nicole Bryce, Aaron Rosenberg … (1990)

Intracranial bleeding is an important cause of brain masses and edema. To study the pathophysiology of intracerebral hemorrhage, we produced experimental hemorrhages in 53 rats and characterized the lesion by histology, brain water content, and behavior. Adult rats had 2 microliters saline containing 0.5 unit bacterial collagenase infused into the left caudate nucleus. Histologically, erythrocytes were seen around blood vessels at the needle puncture site within the first hour. By 4 hours there were hematomas, the size of which depended on the amount of collagenase injected. Necrotic masses containing fluid, blood cells, and fibrin were seen at 24 hours. Lipid-filled macrophages were observed at 7 days and cysts at 3 weeks. Water content was significantly increased 4, 24, and 48 hours after infusion at the needle puncture site and for 24 hours in posterior brain sections. Behavioral abnormalities were present for 48 hours, with recovery of function occurring during the first week. Brain tissue contains Type IV collagen in the basal lamina. Collagenase, which occurs in an inactive form in cells, is released and activated during injury, leading to disruption of the extracellular matrix. Collagenase-induced intracerebral hemorrhage is a reproducible animal model for the study of the effects of the hematoma and brain edema.

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Transplantation of human bone marrow-derived mesenchymal stem cells promotes behavioral recovery and endogenous neurogenesis after cerebral ischemia in rats.

Wenbin Ma, Chuan Qin, Ming Feng … (2011)

Mesenchymal stem cells (MSCs) have been successfully used for the treatment of experimental stroke. However, the neurorestorative mechanisms by which MSCs improve neurological functional recovery are not fully understood. Endogenous cell proliferation in the subventricular zone (SVZ) after stroke is well known, but most of newly formed cells underwent apoptosis. In the present study, we tested the hypothesis that neurotrophic factors secreted by human bone marrow-derived MSCs (hBMSCs) promote endogenous neurogenesis, reduce apoptosis, and improve functional recovery. Adult rats subjected to 2-h middle cerebral artery occlusion (MCAO) were transplanted with hBMSCs or saline into the ipsilateral brain parenchyma at 3days after ischemia. There was a significant recovery of behavior in the hBMSCs-treated rats beginning at 14days after MCAO compared with the control animals. Higher levels of brain-derived neurotrophic factor (BDNF), neurotrophin-3 (NT-3), and vascular endothelial growth factor (VEGF) were detected in the hBMSCs-treated rat brain than the control. Human BMSCs treatment also enhanced endogenous cell proliferation both in the SVZ and in the subgranular zone (SGZ) of the hippocampus. In addition, more neuronal progenitor cells migrated from the SVZ to the ischemic boundary zone (IBZ) and differentiated into mature neurons with less apoptosis in rats treated with hBMSCs. Overall, these data suggest an essential role for hBMSCs in promoting endogenous neurogenesis, protecting newly formed cells, and improving functional recovery after ischemia in rats. Copyright © 2010 Elsevier B.V. All rights reserved.

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Author and article information

Contributors

Hong‐Tian Zhang: zhanghongtian2016@126.com

Ru‐Xiang Xu: brain_xu@126.com

Journal

Journal ID (nlm-ta): CNS Neurosci Ther

Journal ID (iso-abbrev): CNS Neurosci Ther

Journal ID (doi): 10.1111/(ISSN)1755-5949

Journal ID (publisher-id): CNS

Title: CNS Neuroscience & Therapeutics

Publisher: John Wiley and Sons Inc. (Hoboken )

ISSN (Print): 1755-5930

ISSN (Electronic): 1755-5949

Publication date (Electronic): 08 July 2016

Publication date (Print): October 2016

Volume: 22

Issue: 10 ( doiID: 10.1111/cns.2016.22.issue-10 )

Pages: 824-835

Affiliations

[ ¹ ]The Third Military Medical University ChongqingChina

[ ² ] Affiliated Bayi Brain HospitalArmy General Hospital of PLA BeijingChina

[ ³ ]The Neurosurgical Research Center of Beijing Military Region BeijingChina

[ ⁴ ]Department of Ultrapathology of Beijing Neurosurgical Institute BeijingChina

Author notes

[*] [* ] Correspondence

Prof. Ru‐Xiang Xu, Affiliated Bayi Brain Hospital, Army General Hospital of PLA, The Neurosurgical Research Center of Beijing Military Region, NO.5, Nanmencang, Dongsishitiao Street, Dongcheng District, Beijing 100700, China.

Tel.: +86‐10‐64021575;

Fax: +86‐10‐66399833;

E‐mail: brain_xu@ 123456126.com

and

Dr. Hong‐Tian Zhang, Affiliated Bayi Brain Hospital, Army General Hospital of PLA, The Neurosurgical Research Center of Beijing Military Region, NO.5, Nanmencang, Dongsishitiao Street, Dongcheng District, Beijing 100700, China.

Tel.: +86‐10‐66721204;

Fax: +86‐10‐66399833;

E‐mail: zhanghongtian2016@ 123456126.com

Article

Publisher ID: CNS12584

DOI: 10.1111/cns.12584

PMC ID: 5095785

PubMed ID: 27390192

SO-VID: 75c6689a-0521-4847-9f21-f40d70398122

License:

This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial‐NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

History

Date received : 25 April 2016

Date revision received : 18 May 2016

Date accepted : 04 June 2016

Page count

Figures: 6, Tables: 0, Pages: 12, Words: 7578

Funding

Funded by: National Natural Scientific Research funds of China

Award ID: 81371345

Funded by: Beijing Nova program

Award ID: XX2013059

Custom metadata

source-schema-version-number 2.0

component-id cns12584

cover-date October 2016

details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.6 mode:remove_FC converted:04.11.2016

ScienceOpen disciplines: Neurosciences

Keywords: edaravone,intracerebral hemorrhage,intraperitoneal injection,stereotactic administration

Data availability:

ScienceOpen disciplines: Neurosciences

Keywords: edaravone, intracerebral hemorrhage, intraperitoneal injection, stereotactic administration

Stereotactic Administration of Edaravone Ameliorates Collagenase‐Induced Intracerebral Hemorrhage in Rat

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Summary

Background

Methods

Results

Conclusion

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Neuronal Signaling

Most cited references 36

TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease

Collagenase-induced intracerebral hemorrhage in rats.

Transplantation of human bone marrow-derived mesenchymal stem cells promotes behavioral recovery and endogenous neurogenesis after cerebral ischemia in rats.

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