Neutrophil elastase inhibition effectively rescued angiopoietin-1 decrease and inhibits glial scar after spinal cord injury

After spinal cord injury (SCI), neutrophil elastase (NE) released at injury site disrupts vascular endothelium integrity and stabilization. Angiopoietins (ANGPTs) are vascular growth factors that play an important role in vascular stabilization. We hypothesized that neutrophil elastase is one of the...

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Published inActa neuropathologica communications Vol. 6; no. 1; pp. 73 - 18
Main Authors Kumar, Hemant, Choi, Hyemin, Jo, Min-Jae, Joshi, Hari Prasad, Muttigi, Manjunatha, Bonanomi, Dario, Kim, Sung Bum, Ban, Eunmi, Kim, Aeri, Lee, Soo-Hong, Kim, Kyoung-Tae, Sohn, Seil, Zeng, Xiang, Han, Inbo
Format Journal Article
LanguageEnglish
Published England BioMed Central Ltd 07.08.2018
BioMed Central
BMC
Subjects
Angiogenesis
Angiopoietin-1 - metabolism
Angiopoietin-2 - metabolism
Angiopoietins
Animals
Apoptosis
Blood-brain barrier
Cicatrix - drug therapy
Cicatrix - etiology
Cytokines - metabolism
Disease Models, Animal
Endothelial Cells - drug effects
Endothelial Cells - metabolism
Endothelium
Female
Functional recovery
Gene Expression Regulation - genetics
Gene Expression Regulation - physiology
Glial scar
Glycine - analogs & derivatives
Glycine - pharmacology
Growth factors
Hostages
Humans
Ischemia
Laminin - metabolism
Leukocyte Elastase - metabolism
Leukocyte Elastase - pharmacology
Neovascularization
Nerve Tissue Proteins - metabolism
Neuropathic pain
Neutrophil elastase
Neutrophils
Nociceptin
Occludin - metabolism
Opioid Peptides - drug effects
Proteolysis
Rats
Rats, Sprague-Dawley
Recovery of Function - drug effects
Serine Proteinase Inhibitors - pharmacology
Spinal cord injuries
Spinal Cord Injuries - complications
Spinal Cord Injuries - pathology
Spinal cord injury
Sulfonamides - pharmacology
Transforming Growth Factor beta1 - metabolism
Wound healing
Zonula Occludens-1 Protein - metabolism
Neutrophil elastase
Functional recovery
Glial scar
Spinal cord injury
Angiopoietins
Neuropathic pain
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Abstract After spinal cord injury (SCI), neutrophil elastase (NE) released at injury site disrupts vascular endothelium integrity and stabilization. Angiopoietins (ANGPTs) are vascular growth factors that play an important role in vascular stabilization. We hypothesized that neutrophil elastase is one of the key determinants of vascular endothelium disruption/destabilization and affects angiopoietins expression after spinal cord injury. To test this, tubule formation and angiopoietins expression were assessed in endothelial cells exposed to different concentrations of recombinant neutropil elastase. Then, the expression of angiopoietin-1, angiopoietin-2, and neutrophil elastase was determined at 3 h and at 1, 3, 5, 7, 14, 21, and 28 days in a clinically relevant model of moderate compression (35 g for 5 min at T10) spinal cord injury. A dichotomy between the levels of angiopoietin-1 and angiopoietin-2 was observed; thus, we utilized a specific neutrophil elastase inhibitor (sivelestat sodium; 30 mg/kg, i.p., b.i.d.) after spinal cord injury. The expression levels of neutropil elastase and angiopoietin-2 increased, and that of angiopoietin-1 decreased after spinal cord injury in rats. The sivelestat regimen, optimized via a pharmacokinetics study, had potent effects on vascular stabilization by upregulating angiopoietin-1 via the AKT pathway and preventing tight junction protein degradation. Moreover, sivelestat attenuated the levels of inflammatory cytokines and chemokines after spinal cord injury and hence subsequently alleviated secondary damage observed as a reduction in glial scar formation and the promotion of blood vessel formation and stabilization. As a result, hindlimb locomotor function significantly recovered in the sivelestat-treated animals as determined by the Basso, Beattie, and Bresnahan scale and footprint analyses. Furthermore, sivelestat treatment attenuated neuropathic pain as assessed by responses to von Frey filaments after spinal cord injury. Thus, our result suggests that inhibiting neutropil elastase by administration of sivelestat is a promising therapeutic strategy to inhibit glial scar and promote functional recovery by upregulating angiopoietin-1 after spinal cord injury.
AbstractList Abstract After spinal cord injury (SCI), neutrophil elastase (NE) released at injury site disrupts vascular endothelium integrity and stabilization. Angiopoietins (ANGPTs) are vascular growth factors that play an important role in vascular stabilization. We hypothesized that neutrophil elastase is one of the key determinants of vascular endothelium disruption/destabilization and affects angiopoietins expression after spinal cord injury. To test this, tubule formation and angiopoietins expression were assessed in endothelial cells exposed to different concentrations of recombinant neutropil elastase. Then, the expression of angiopoietin-1, angiopoietin-2, and neutrophil elastase was determined at 3 h and at 1, 3, 5, 7, 14, 21, and 28 days in a clinically relevant model of moderate compression (35 g for 5 min at T10) spinal cord injury. A dichotomy between the levels of angiopoietin-1 and angiopoietin-2 was observed; thus, we utilized a specific neutrophil elastase inhibitor (sivelestat sodium; 30 mg/kg, i.p., b.i.d.) after spinal cord injury. The expression levels of neutropil elastase and angiopoietin-2 increased, and that of angiopoietin-1 decreased after spinal cord injury in rats. The sivelestat regimen, optimized via a pharmacokinetics study, had potent effects on vascular stabilization by upregulating angiopoietin-1 via the AKT pathway and preventing tight junction protein degradation. Moreover, sivelestat attenuated the levels of inflammatory cytokines and chemokines after spinal cord injury and hence subsequently alleviated secondary damage observed as a reduction in glial scar formation and the promotion of blood vessel formation and stabilization. As a result, hindlimb locomotor function significantly recovered in the sivelestat-treated animals as determined by the Basso, Beattie, and Bresnahan scale and footprint analyses. Furthermore, sivelestat treatment attenuated neuropathic pain as assessed by responses to von Frey filaments after spinal cord injury. Thus, our result suggests that inhibiting neutropil elastase by administration of sivelestat is a promising therapeutic strategy to inhibit glial scar and promote functional recovery by upregulating angiopoietin-1 after spinal cord injury.
After spinal cord injury (SCI), neutrophil elastase (NE) released at injury site disrupts vascular endothelium integrity and stabilization. Angiopoietins (ANGPTs) are vascular growth factors that play an important role in vascular stabilization. We hypothesized that neutrophil elastase is one of the key determinants of vascular endothelium disruption/destabilization and affects angiopoietins expression after spinal cord injury. To test this, tubule formation and angiopoietins expression were assessed in endothelial cells exposed to different concentrations of recombinant neutropil elastase. Then, the expression of angiopoietin-1, angiopoietin-2, and neutrophil elastase was determined at 3 h and at 1, 3, 5, 7, 14, 21, and 28 days in a clinically relevant model of moderate compression (35 g for 5 min at T10) spinal cord injury. A dichotomy between the levels of angiopoietin-1 and angiopoietin-2 was observed; thus, we utilized a specific neutrophil elastase inhibitor (sivelestat sodium; 30 mg/kg, i.p., b.i.d.) after spinal cord injury. The expression levels of neutropil elastase and angiopoietin-2 increased, and that of angiopoietin-1 decreased after spinal cord injury in rats. The sivelestat regimen, optimized via a pharmacokinetics study, had potent effects on vascular stabilization by upregulating angiopoietin-1 via the AKT pathway and preventing tight junction protein degradation. Moreover, sivelestat attenuated the levels of inflammatory cytokines and chemokines after spinal cord injury and hence subsequently alleviated secondary damage observed as a reduction in glial scar formation and the promotion of blood vessel formation and stabilization. As a result, hindlimb locomotor function significantly recovered in the sivelestat-treated animals as determined by the Basso, Beattie, and Bresnahan scale and footprint analyses. Furthermore, sivelestat treatment attenuated neuropathic pain as assessed by responses to von Frey filaments after spinal cord injury. Thus, our result suggests that inhibiting neutropil elastase by administration of sivelestat is a promising therapeutic strategy to inhibit glial scar and promote functional recovery by upregulating angiopoietin-1 after spinal cord injury.
The sivelestat regimen, optimized via a pharmacokinetics study, had potent effects on vascular stabilization by upregulating angiopoietin-1 via the AKT pathway and preventing tight junction protein degradation. [...]sivelestat attenuated the levels of inflammatory cytokines and chemokines after spinal cord injury and hence subsequently alleviated secondary damage observed as a reduction in glial scar formation and the promotion of blood vessel formation and stabilization. [...]hindlimb locomotor function significantly recovered in the sivelestat-treated animals as determined by the Basso, Beattie, and Bresnahan scale and footprint analyses. Furthermore, sivelestat treatment attenuated neuropathic pain as assessed by responses to von Frey filaments after spinal cord injury. [...]our result suggests that inhibiting neutropil elastase by administration of sivelestat is a promising therapeutic strategy to inhibit glial scar and promote functional recovery by upregulating angiopoietin-1 after spinal cord injury. Injury group NE inhibition attenuates the expression of inflammatory cytokines and chemokines after SCI We and others have shown that the peak expression of inflammatory markers (cytokines and chemokines) occurs in the acute phase of SCI [48]. [...]we determined the effect of NE inhibition on inflammatory parameters using spinal cord samples from sham, injured untreated (Injury), and injured sivelestat-treated (two doses) animals prepared on DPI-1.
After spinal cord injury (SCI), neutrophil elastase (NE) released at injury site disrupts vascular endothelium integrity and stabilization. Angiopoietins (ANGPTs) are vascular growth factors that play an important role in vascular stabilization. We hypothesized that neutrophil elastase is one of the key determinants of vascular endothelium disruption/destabilization and affects angiopoietins expression after spinal cord injury. To test this, tubule formation and angiopoietins expression were assessed in endothelial cells exposed to different concentrations of recombinant neutropil elastase. Then, the expression of angiopoietin-1, angiopoietin-2, and neutrophil elastase was determined at 3 h and at 1, 3, 5, 7, 14, 21, and 28 days in a clinically relevant model of moderate compression (35 g for 5 min at T10) spinal cord injury. A dichotomy between the levels of angiopoietin-1 and angiopoietin-2 was observed; thus, we utilized a specific neutrophil elastase inhibitor (sivelestat sodium; 30 mg/kg, i.p., b.i.d.) after spinal cord injury. The expression levels of neutropil elastase and angiopoietin-2 increased, and that of angiopoietin-1 decreased after spinal cord injury in rats. The sivelestat regimen, optimized via a pharmacokinetics study, had potent effects on vascular stabilization by upregulating angiopoietin-1 via the AKT pathway and preventing tight junction protein degradation. Moreover, sivelestat attenuated the levels of inflammatory cytokines and chemokines after spinal cord injury and hence subsequently alleviated secondary damage observed as a reduction in glial scar formation and the promotion of blood vessel formation and stabilization. As a result, hindlimb locomotor function significantly recovered in the sivelestat-treated animals as determined by the Basso, Beattie, and Bresnahan scale and footprint analyses. Furthermore, sivelestat treatment attenuated neuropathic pain as assessed by responses to von Frey filaments after spinal cord injury. Thus, our result suggests that inhibiting neutropil elastase by administration of sivelestat is a promising therapeutic strategy to inhibit glial scar and promote functional recovery by upregulating angiopoietin-1 after spinal cord injury.
After spinal cord injury (SCI), neutrophil elastase (NE) released at injury site disrupts vascular endothelium integrity and stabilization. Angiopoietins (ANGPTs) are vascular growth factors that play an important role in vascular stabilization. We hypothesized that neutrophil elastase is one of the key determinants of vascular endothelium disruption/destabilization and affects angiopoietins expression after spinal cord injury. To test this, tubule formation and angiopoietins expression were assessed in endothelial cells exposed to different concentrations of recombinant neutropil elastase. Then, the expression of angiopoietin-1, angiopoietin-2, and neutrophil elastase was determined at 3 h and at 1, 3, 5, 7, 14, 21, and 28 days in a clinically relevant model of moderate compression (35 g for 5 min at T10) spinal cord injury. A dichotomy between the levels of angiopoietin-1 and angiopoietin-2 was observed; thus, we utilized a specific neutrophil elastase inhibitor (sivelestat sodium; 30 mg/kg, i.p., b.i.d.) after spinal cord injury. The expression levels of neutropil elastase and angiopoietin-2 increased, and that of angiopoietin-1 decreased after spinal cord injury in rats. The sivelestat regimen, optimized via a pharmacokinetics study, had potent effects on vascular stabilization by upregulating angiopoietin-1 via the AKT pathway and preventing tight junction protein degradation. Moreover, sivelestat attenuated the levels of inflammatory cytokines and chemokines after spinal cord injury and hence subsequently alleviated secondary damage observed as a reduction in glial scar formation and the promotion of blood vessel formation and stabilization. As a result, hindlimb locomotor function significantly recovered in the sivelestat-treated animals as determined by the Basso, Beattie, and Bresnahan scale and footprint analyses. Furthermore, sivelestat treatment attenuated neuropathic pain as assessed by responses to von Frey filaments after spinal cord injury. Thus, our result suggests that inhibiting neutropil elastase by administration of sivelestat is a promising therapeutic strategy to inhibit glial scar and promote functional recovery by upregulating angiopoietin-1 after spinal cord injury. Keywords: Neutrophil elastase, Spinal cord injury, Glial scar, Angiopoietins, Functional recovery, Neuropathic pain
ArticleNumber 73
Audience Academic
Author Han, Inbo
Kumar, Hemant
Lee, Soo-Hong
Zeng, Xiang
Bonanomi, Dario
Sohn, Seil
Joshi, Hari Prasad
Kim, Kyoung-Tae
Kim, Sung Bum
Choi, Hyemin
Jo, Min-Jae
Kim, Aeri
Ban, Eunmi
Muttigi, Manjunatha
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  surname: Ban
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  organization: College of Pharmacy, CHA University, Seongnam-si, Gyeonggi-do, Republic of Korea
– sequence: 9
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  fullname: Kim, Aeri
  organization: College of Pharmacy, CHA University, Seongnam-si, Gyeonggi-do, Republic of Korea
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  givenname: Soo-Hong
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  fullname: Lee, Soo-Hong
  organization: Department of Biomedical Science, CHA University, Seongnam-si, Gyeonggi-do, Republic of Korea
– sequence: 11
  givenname: Kyoung-Tae
  surname: Kim
  fullname: Kim, Kyoung-Tae
  organization: Department of Neurosurgery, School of Medicine,Kyungpook National University, 130, Dongdeok-ro, Jung-gu, Daegu, 41944, Republic of Korea
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  surname: Sohn
  fullname: Sohn, Seil
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  givenname: Xiang
  surname: Zeng
  fullname: Zeng, Xiang
  email: zengx33@mail.sysu.edu.cn
  organization: Department of Histology and Embryology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, 510080, Guangdong Province, China. zengx33@mail.sysu.edu.cn
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  email: hanib@cha.ac.kr
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Cites_doi 10.1038/srep02217
10.4103/2152-7806.83732
10.1016/0006-8993(89)90542-8
10.1038/74725
10.1093/brain/awq034
10.1007/s12035-017-0509-3
10.1038/nrn1824
10.1016/j.mcn.2004.06.007
10.1016/j.mcn.2004.10.008
10.1093/rheumatology/kes093.
10.1016/j.jaci.2004.06.045
10.1089/neu.2010.1403
10.1046/j.1460-9568.2000.00226.x
10.1016/j.neuroscience.2011.09.058
10.1172/JCI5928
10.1038/nm0598-615
10.1152/japplphysiol.00567.2004
10.1182/blood-2008-12-196584
10.1016/j.bbrc.2008.05.025
10.1038/nrn1326
10.1016/S0014-2999(02)02182-9
10.1089/neu.2000.17.203
10.2174/156720208786413433
10.1074/jbc.M300351200
10.1073/pnas.96.5.1904
10.1093/brain/awp121
10.1124/pr.57.2.4
10.1038/sj.mn.7800185
10.1016/S0169-328X(00)00253-9
10.2174/156720210793180756
10.1158/0008-5472.CAN-15-1227
10.1536/ihj.54.149
10.1007/s12035-016-9910-6
10.1089/neu.2013.3034
10.1002/cne.10168
10.4049/jimmunol.172.7.4493
10.1089/neu.2011.1860
10.1242/dev.127.21.4531
10.1126/science.aaa2958
10.1016/j.expneurol.2015.07.012
10.1189/jlb.69.2.241
10.1172/JCI112426
10.1007/s10456-009-9147-3
10.1002/(SICI)1096-9861(19961223)376:4<542::AID-CNE4>3.0.CO;2-1
10.1016/0896-6273(90)90089-X
10.1038/sj.jcbfm.9600475
10.1038/labinvest.3700325
10.1186/2045-8118-8-4
10.1523/JNEUROSCI.21-23-09334.2001
10.1161/01.RES.87.7.603
10.1111/j.1742-4658.2009.07174.x
10.1093/cvr/cvs254
10.1161/HYPERTENSIONAHA.110.155556
10.4049/jimmunol.1400401
10.1083/jcb.125.4.917
10.2147/TCRM.S65066
10.1164/ajrccm/150.6_Pt_2.S114
10.1152/ajpgi.00061.2004
10.1016/j.bbrc.2008.11.052
10.2147/DDDT.S36436
10.1016/S0002-9343(88)80068-8
10.1002/jnr.21362
10.1002/jnr.10759
10.1523/JNEUROSCI.3444-07.2007
10.1006/exnr.1996.0196
10.1111/j.1460-9568.1997.tb01497.x
10.1152/physrev.00035.2003
10.1046/j.1471-4159.2001.00488.x
10.1182/blood-2004-09-3531
10.1016/S0002-9440(10)64786-4
10.1111/j.1432-2277.2003.tb00310.x
10.1523/JNEUROSCI.17-14-05395.1997
10.1038/nm1505
10.1007/s00441-004-1068-2
10.1016/S0006-8993(98)00459-4
10.1016/j.expneurol.2015.03.001
10.1186/s12974-014-0150-2
10.1038/nm1351
10.1056/NEJMra043632
10.1111/j.1750-3639.2007.00067.x
10.1510/icvts.2008.197244
10.1097/01.LAB.0000082383.40635.FE
10.1186/1744-8069-10-26
10.1002/glia.10074
10.1007/s002689900366
10.1006/exnr.2001.7827
10.1038/sj.bjp.0705259
10.1016/j.nbd.2014.12.003
10.1097/00003246-200210000-00011
10.3171/jns.1997.86.3.0483
10.1089/neu.1995.12.1
10.1038/hr.2010.58
10.1016/j.neuron.2008.01.003
10.1016/j.neuroscience.2008.07.001
10.1038/jcbfm.2008.76
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Issue 1
Keywords Neutrophil elastase
Functional recovery
Glial scar
Spinal cord injury
Angiopoietins
Neuropathic pain
Language English
License Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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References SN McGill (576_CR60) 1998; 22
PC Maisonpierre (576_CR57) 1990; 5
N Aikawa (576_CR5) 2014; 10
G Bazzoni (576_CR12) 2004; 84
D Bartholdi (576_CR9) 1997; 9
M Thomas (576_CR86) 2009; 12
Y Bai (576_CR8) 2009; 378
JV Coumans (576_CR19) 2001; 21
PJ Newman (576_CR65) 1999; 103
JA Russell (576_CR78) 2006; 355
DP Ankeny (576_CR6) 2009; 158
XZ Liu (576_CR55) 1997; 17
MB Leal-Filho (576_CR50) 2011; 2
C Feistritzer (576_CR25) 2004; 114
J Kosacka (576_CR47) 2005; 320
576_CR49
MJ Donovan (576_CR20) 2000; 127
TM Hansen (576_CR31) 2008; 5
576_CR48
G Doring (576_CR21) 1994; 150
576_CR45
H Kim (576_CR46) 2008; 372
NJ Abbott (576_CR1) 2006; 7
A Blesch (576_CR16) 2004; 27
CH Tator (576_CR85) 1997; 86
HS Lee (576_CR51) 2009; 276
Y Taoka (576_CR84) 1998; 799
WD Whetstone (576_CR93) 2003; 74
RP Bonin (576_CR17) 2014; 10
K Nakatani (576_CR62) 2001; 69
S Rossignol (576_CR76) 2007; 27
N Nourhaghighi (576_CR68) 2003; 83
C Lemieux (576_CR53) 2005; 105
K Okajima (576_CR69) 2004; 287
BV Zlokovic (576_CR99) 2008; 57
JJ Herrera (576_CR35) 2010; 27
CV Ionescu (576_CR39) 2003; 10
J Silver (576_CR82) 2004; 5
576_CR63
M Hayashi (576_CR33) 2000; 17
S Han (576_CR30) 2010; 133
576_CR66
M Oubaha (576_CR70) 2009; 114
N Inoue (576_CR38) 2013; 54
J Ruschel (576_CR77) 2015; 348
DM Basso (576_CR10) 1995; 12
H Ueno (576_CR91) 2002; 30
EJ Battegay (576_CR11) 1994; 125
S Iwamoto (576_CR41) 2009; 8
B Aube (576_CR7) 2014; 193
T Tonai (576_CR88) 2001; 78
L Pizurki (576_CR72) 2003; 139
L Acarin (576_CR2) 2000; 12
SM Lee (576_CR52) 2011; 28
LJ Noble (576_CR67) 1989; 482
A Zacharek (576_CR98) 2007; 27
B Hermant (576_CR34) 2003; 278
S Man (576_CR58) 2007; 17
BD Semple (576_CR81) 2015; 74
RE Young (576_CR97) 2004; 172
M Agudo (576_CR3) 2005; 28
G Gopinathan (576_CR29) 2015; 75
T Matsushita (576_CR59) 2015; 267
K Satake (576_CR79) 2000; 85
Y Tsuboko (576_CR90) 2012; 6
JJ Yang (576_CR96) 1996; 149
LA Smedly (576_CR83) 1986; 77
J Xu (576_CR95) 2012; 96
Y Ikegame (576_CR37) 2010; 33
JC Durham-Lee (576_CR22) 2012; 202
MF Ritz (576_CR74) 2010; 7
U Fiedler (576_CR26) 2006; 12
DN Loy (576_CR56) 2002; 445
V Neirinckx (576_CR64) 2014; 11
G Thurston (576_CR87) 2000; 6
JR Gamble (576_CR28) 2000; 87
E Jablonska (576_CR42) 2001; 49
A Belaaouaj (576_CR14) 1998; 4
J Travis (576_CR89) 1988; 84
K Kawabata (576_CR44) 2002; 451
X Ling (576_CR54) 2007; 85
AE Ropper (576_CR75) 2015; 271
PK Houtz (576_CR36) 2004; 97
S Nag (576_CR61) 2005; 85
WD Whetstone (576_CR94) 2003; 74
T Oya (576_CR71) 2002; 38
H Beck (576_CR13) 2000; 157
M Scali (576_CR80) 2013; 3
RL Benton (576_CR15) 2008; 28
PG Popovich (576_CR73) 1996; 142
S Ahmad (576_CR4) 2010; 56
BT Hawkins (576_CR32) 2005; 57
JW Fawcett (576_CR24) 2009; 132
SA Figley (576_CR27) 2014; 31
B Engelhardt (576_CR23) 2011; 8
S Kaneko (576_CR43) 2006; 12
GT Casella (576_CR18) 2002; 173
N Ishikawa (576_CR40) 2003; 16
DM Valenzuela (576_CR92) 1999; 96
References_xml – volume: 3
  start-page: 2217
  year: 2013
  ident: 576_CR80
  publication-title: Sci Rep
  doi: 10.1038/srep02217
  contributor:
    fullname: M Scali
– volume: 2
  start-page: 112
  year: 2011
  ident: 576_CR50
  publication-title: Surg Neurol Int
  doi: 10.4103/2152-7806.83732
  contributor:
    fullname: MB Leal-Filho
– volume: 482
  start-page: 57
  year: 1989
  ident: 576_CR67
  publication-title: Brain Res
  doi: 10.1016/0006-8993(89)90542-8
  contributor:
    fullname: LJ Noble
– volume: 6
  start-page: 460
  year: 2000
  ident: 576_CR87
  publication-title: Nat Med
  doi: 10.1038/74725
  contributor:
    fullname: G Thurston
– volume: 133
  start-page: 1026
  year: 2010
  ident: 576_CR30
  publication-title: Brain
  doi: 10.1093/brain/awq034
  contributor:
    fullname: S Han
– ident: 576_CR48
  doi: 10.1007/s12035-017-0509-3
– volume: 7
  start-page: 41
  year: 2006
  ident: 576_CR1
  publication-title: Nat Rev Neurosci
  doi: 10.1038/nrn1824
  contributor:
    fullname: NJ Abbott
– volume: 27
  start-page: 190
  year: 2004
  ident: 576_CR16
  publication-title: Mol Cell Neurosci
  doi: 10.1016/j.mcn.2004.06.007
  contributor:
    fullname: A Blesch
– volume: 28
  start-page: 475
  year: 2005
  ident: 576_CR3
  publication-title: Mol Cell Neurosci
  doi: 10.1016/j.mcn.2004.10.008
  contributor:
    fullname: M Agudo
– volume: 49
  start-page: 63
  year: 2001
  ident: 576_CR42
  publication-title: Arch Immunol Ther Exp (Warsz)
  contributor:
    fullname: E Jablonska
– ident: 576_CR45
  doi: 10.1093/rheumatology/kes093.
– volume: 114
  start-page: 1077
  year: 2004
  ident: 576_CR25
  publication-title: J Allergy Clin Immunol
  doi: 10.1016/j.jaci.2004.06.045
  contributor:
    fullname: C Feistritzer
– volume: 27
  start-page: 2067
  year: 2010
  ident: 576_CR35
  publication-title: J Neurotrauma
  doi: 10.1089/neu.2010.1403
  contributor:
    fullname: JJ Herrera
– volume: 12
  start-page: 3505
  year: 2000
  ident: 576_CR2
  publication-title: Eur J Neurosci
  doi: 10.1046/j.1460-9568.2000.00226.x
  contributor:
    fullname: L Acarin
– volume: 202
  start-page: 454
  year: 2012
  ident: 576_CR22
  publication-title: Neuroscience
  doi: 10.1016/j.neuroscience.2011.09.058
  contributor:
    fullname: JC Durham-Lee
– volume: 103
  start-page: 5
  year: 1999
  ident: 576_CR65
  publication-title: J Clin Invest
  doi: 10.1172/JCI5928
  contributor:
    fullname: PJ Newman
– volume: 149
  start-page: 1617
  year: 1996
  ident: 576_CR96
  publication-title: Am J Pathol
  contributor:
    fullname: JJ Yang
– volume: 4
  start-page: 615
  year: 1998
  ident: 576_CR14
  publication-title: Nat Med
  doi: 10.1038/nm0598-615
  contributor:
    fullname: A Belaaouaj
– volume: 97
  start-page: 2139
  year: 2004
  ident: 576_CR36
  publication-title: J Appl Physiol (1985)
  doi: 10.1152/japplphysiol.00567.2004
  contributor:
    fullname: PK Houtz
– volume: 114
  start-page: 3343
  year: 2009
  ident: 576_CR70
  publication-title: Blood
  doi: 10.1182/blood-2008-12-196584
  contributor:
    fullname: M Oubaha
– volume: 372
  start-page: 243
  year: 2008
  ident: 576_CR46
  publication-title: Biochem Biophys Res Commun
  doi: 10.1016/j.bbrc.2008.05.025
  contributor:
    fullname: H Kim
– volume: 5
  start-page: 146
  year: 2004
  ident: 576_CR82
  publication-title: Nat Rev Neurosci
  doi: 10.1038/nrn1326
  contributor:
    fullname: J Silver
– volume: 451
  start-page: 1
  year: 2002
  ident: 576_CR44
  publication-title: Eur J Pharmacol
  doi: 10.1016/S0014-2999(02)02182-9
  contributor:
    fullname: K Kawabata
– volume: 17
  start-page: 203
  year: 2000
  ident: 576_CR33
  publication-title: J Neurotrauma
  doi: 10.1089/neu.2000.17.203
  contributor:
    fullname: M Hayashi
– volume: 5
  start-page: 236
  year: 2008
  ident: 576_CR31
  publication-title: Curr Neurovasc Res
  doi: 10.2174/156720208786413433
  contributor:
    fullname: TM Hansen
– volume: 278
  start-page: 14002
  year: 2003
  ident: 576_CR34
  publication-title: J Biol Chem
  doi: 10.1074/jbc.M300351200
  contributor:
    fullname: B Hermant
– volume: 96
  start-page: 1904
  year: 1999
  ident: 576_CR92
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.96.5.1904
  contributor:
    fullname: DM Valenzuela
– volume: 132
  start-page: 1417
  year: 2009
  ident: 576_CR24
  publication-title: Brain
  doi: 10.1093/brain/awp121
  contributor:
    fullname: JW Fawcett
– volume: 57
  start-page: 173
  year: 2005
  ident: 576_CR32
  publication-title: Pharmacol Rev
  doi: 10.1124/pr.57.2.4
  contributor:
    fullname: BT Hawkins
– volume: 10
  start-page: 205
  year: 2003
  ident: 576_CR39
  publication-title: Microcirculation
  doi: 10.1038/sj.mn.7800185
  contributor:
    fullname: CV Ionescu
– volume: 85
  start-page: 114
  year: 2000
  ident: 576_CR79
  publication-title: Brain Res Mol Brain Res
  doi: 10.1016/S0169-328X(00)00253-9
  contributor:
    fullname: K Satake
– volume: 7
  start-page: 301
  year: 2010
  ident: 576_CR74
  publication-title: Curr Neurovasc Res
  doi: 10.2174/156720210793180756
  contributor:
    fullname: MF Ritz
– volume: 75
  start-page: 3098
  year: 2015
  ident: 576_CR29
  publication-title: Cancer Res
  doi: 10.1158/0008-5472.CAN-15-1227
  contributor:
    fullname: G Gopinathan
– volume: 54
  start-page: 149
  year: 2013
  ident: 576_CR38
  publication-title: Int Heart J
  doi: 10.1536/ihj.54.149
  contributor:
    fullname: N Inoue
– ident: 576_CR49
  doi: 10.1007/s12035-016-9910-6
– volume: 31
  start-page: 541
  year: 2014
  ident: 576_CR27
  publication-title: J Neurotrauma
  doi: 10.1089/neu.2013.3034
  contributor:
    fullname: SA Figley
– volume: 445
  start-page: 308
  year: 2002
  ident: 576_CR56
  publication-title: J Comp Neurol
  doi: 10.1002/cne.10168
  contributor:
    fullname: DN Loy
– volume: 172
  start-page: 4493
  year: 2004
  ident: 576_CR97
  publication-title: J Immunol
  doi: 10.4049/jimmunol.172.7.4493
  contributor:
    fullname: RE Young
– volume: 28
  start-page: 1893
  year: 2011
  ident: 576_CR52
  publication-title: J Neurotrauma
  doi: 10.1089/neu.2011.1860
  contributor:
    fullname: SM Lee
– volume: 127
  start-page: 4531
  year: 2000
  ident: 576_CR20
  publication-title: Development
  doi: 10.1242/dev.127.21.4531
  contributor:
    fullname: MJ Donovan
– volume: 348
  start-page: 347
  year: 2015
  ident: 576_CR77
  publication-title: Science
  doi: 10.1126/science.aaa2958
  contributor:
    fullname: J Ruschel
– volume: 271
  start-page: 515
  year: 2015
  ident: 576_CR75
  publication-title: Exp Neurol
  doi: 10.1016/j.expneurol.2015.07.012
  contributor:
    fullname: AE Ropper
– volume: 69
  start-page: 241
  year: 2001
  ident: 576_CR62
  publication-title: J Leukoc Biol
  doi: 10.1189/jlb.69.2.241
  contributor:
    fullname: K Nakatani
– volume: 77
  start-page: 1233
  year: 1986
  ident: 576_CR83
  publication-title: J Clin Invest
  doi: 10.1172/JCI112426
  contributor:
    fullname: LA Smedly
– volume: 12
  start-page: 125
  year: 2009
  ident: 576_CR86
  publication-title: Angiogenesis
  doi: 10.1007/s10456-009-9147-3
  contributor:
    fullname: M Thomas
– ident: 576_CR66
  doi: 10.1002/(SICI)1096-9861(19961223)376:4<542::AID-CNE4>3.0.CO;2-1
– volume: 5
  start-page: 501
  year: 1990
  ident: 576_CR57
  publication-title: Neuron
  doi: 10.1016/0896-6273(90)90089-X
  contributor:
    fullname: PC Maisonpierre
– volume: 27
  start-page: 1684
  year: 2007
  ident: 576_CR98
  publication-title: J Cereb Blood Flow Metab
  doi: 10.1038/sj.jcbfm.9600475
  contributor:
    fullname: A Zacharek
– volume: 85
  start-page: 1189
  year: 2005
  ident: 576_CR61
  publication-title: Lab Invest
  doi: 10.1038/labinvest.3700325
  contributor:
    fullname: S Nag
– volume: 8
  start-page: 4
  year: 2011
  ident: 576_CR23
  publication-title: Fluids Barriers CNS
  doi: 10.1186/2045-8118-8-4
  contributor:
    fullname: B Engelhardt
– volume: 21
  start-page: 9334
  year: 2001
  ident: 576_CR19
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.21-23-09334.2001
  contributor:
    fullname: JV Coumans
– volume: 87
  start-page: 603
  year: 2000
  ident: 576_CR28
  publication-title: Circ Res
  doi: 10.1161/01.RES.87.7.603
  contributor:
    fullname: JR Gamble
– volume: 276
  start-page: 4622
  year: 2009
  ident: 576_CR51
  publication-title: FEBS J
  doi: 10.1111/j.1742-4658.2009.07174.x
  contributor:
    fullname: HS Lee
– volume: 96
  start-page: 308
  year: 2012
  ident: 576_CR95
  publication-title: Cardiovasc Res
  doi: 10.1093/cvr/cvs254
  contributor:
    fullname: J Xu
– volume: 56
  start-page: 477
  year: 2010
  ident: 576_CR4
  publication-title: Hypertension
  doi: 10.1161/HYPERTENSIONAHA.110.155556
  contributor:
    fullname: S Ahmad
– volume: 193
  start-page: 2438
  year: 2014
  ident: 576_CR7
  publication-title: J Immunol
  doi: 10.4049/jimmunol.1400401
  contributor:
    fullname: B Aube
– volume: 125
  start-page: 917
  year: 1994
  ident: 576_CR11
  publication-title: J Cell Biol
  doi: 10.1083/jcb.125.4.917
  contributor:
    fullname: EJ Battegay
– volume: 10
  start-page: 621
  year: 2014
  ident: 576_CR5
  publication-title: Ther Clin Risk Manag
  doi: 10.2147/TCRM.S65066
  contributor:
    fullname: N Aikawa
– volume: 150
  start-page: S114
  year: 1994
  ident: 576_CR21
  publication-title: Am J Respir Crit Care Med
  doi: 10.1164/ajrccm/150.6_Pt_2.S114
  contributor:
    fullname: G Doring
– volume: 287
  start-page: G1116
  year: 2004
  ident: 576_CR69
  publication-title: Am J Physiol Gastrointest Liver Physiol
  doi: 10.1152/ajpgi.00061.2004
  contributor:
    fullname: K Okajima
– volume: 378
  start-page: 296
  year: 2009
  ident: 576_CR8
  publication-title: Biochem Biophys Res Commun
  doi: 10.1016/j.bbrc.2008.11.052
  contributor:
    fullname: Y Bai
– volume: 6
  start-page: 273
  year: 2012
  ident: 576_CR90
  publication-title: Drug Des Devel Ther
  doi: 10.2147/DDDT.S36436
  contributor:
    fullname: Y Tsuboko
– volume: 84
  start-page: 37
  year: 1988
  ident: 576_CR89
  publication-title: Am J Med
  doi: 10.1016/S0002-9343(88)80068-8
  contributor:
    fullname: J Travis
– volume: 85
  start-page: 2175
  year: 2007
  ident: 576_CR54
  publication-title: J Neurosci Res
  doi: 10.1002/jnr.21362
  contributor:
    fullname: X Ling
– volume: 74
  start-page: 227
  year: 2003
  ident: 576_CR93
  publication-title: J Neurosci Res
  doi: 10.1002/jnr.10759
  contributor:
    fullname: WD Whetstone
– volume: 27
  start-page: 11782
  year: 2007
  ident: 576_CR76
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.3444-07.2007
  contributor:
    fullname: S Rossignol
– volume: 142
  start-page: 258
  year: 1996
  ident: 576_CR73
  publication-title: Exp Neurol
  doi: 10.1006/exnr.1996.0196
  contributor:
    fullname: PG Popovich
– volume: 9
  start-page: 1422
  year: 1997
  ident: 576_CR9
  publication-title: Eur J Neurosci
  doi: 10.1111/j.1460-9568.1997.tb01497.x
  contributor:
    fullname: D Bartholdi
– volume: 84
  start-page: 869
  year: 2004
  ident: 576_CR12
  publication-title: Physiol Rev
  doi: 10.1152/physrev.00035.2003
  contributor:
    fullname: G Bazzoni
– volume: 78
  start-page: 1064
  year: 2001
  ident: 576_CR88
  publication-title: J Neurochem
  doi: 10.1046/j.1471-4159.2001.00488.x
  contributor:
    fullname: T Tonai
– volume: 105
  start-page: 1523
  year: 2005
  ident: 576_CR53
  publication-title: Blood
  doi: 10.1182/blood-2004-09-3531
  contributor:
    fullname: C Lemieux
– volume: 157
  start-page: 1473
  year: 2000
  ident: 576_CR13
  publication-title: Am J Pathol
  doi: 10.1016/S0002-9440(10)64786-4
  contributor:
    fullname: H Beck
– volume: 16
  start-page: 341
  year: 2003
  ident: 576_CR40
  publication-title: Transpl Int
  doi: 10.1111/j.1432-2277.2003.tb00310.x
  contributor:
    fullname: N Ishikawa
– volume: 17
  start-page: 5395
  year: 1997
  ident: 576_CR55
  publication-title: J Neurosci
  doi: 10.1523/JNEUROSCI.17-14-05395.1997
  contributor:
    fullname: XZ Liu
– volume: 12
  start-page: 1380
  year: 2006
  ident: 576_CR43
  publication-title: Nat Med
  doi: 10.1038/nm1505
  contributor:
    fullname: S Kaneko
– volume: 320
  start-page: 11
  year: 2005
  ident: 576_CR47
  publication-title: Cell Tissue Res
  doi: 10.1007/s00441-004-1068-2
  contributor:
    fullname: J Kosacka
– volume: 799
  start-page: 264
  year: 1998
  ident: 576_CR84
  publication-title: Brain Res
  doi: 10.1016/S0006-8993(98)00459-4
  contributor:
    fullname: Y Taoka
– volume: 267
  start-page: 152
  year: 2015
  ident: 576_CR59
  publication-title: Exp Neurol
  doi: 10.1016/j.expneurol.2015.03.001
  contributor:
    fullname: T Matsushita
– volume: 11
  start-page: 150
  year: 2014
  ident: 576_CR64
  publication-title: J Neuroinflammation
  doi: 10.1186/s12974-014-0150-2
  contributor:
    fullname: V Neirinckx
– volume: 12
  start-page: 235
  year: 2006
  ident: 576_CR26
  publication-title: Nat Med
  doi: 10.1038/nm1351
  contributor:
    fullname: U Fiedler
– volume: 355
  start-page: 1699
  year: 2006
  ident: 576_CR78
  publication-title: N Engl J Med
  doi: 10.1056/NEJMra043632
  contributor:
    fullname: JA Russell
– volume: 17
  start-page: 243
  year: 2007
  ident: 576_CR58
  publication-title: Brain Pathol
  doi: 10.1111/j.1750-3639.2007.00067.x
  contributor:
    fullname: S Man
– volume: 8
  start-page: 606
  year: 2009
  ident: 576_CR41
  publication-title: Interact Cardiovasc Thorac Surg
  doi: 10.1510/icvts.2008.197244
  contributor:
    fullname: S Iwamoto
– volume: 83
  start-page: 1211
  year: 2003
  ident: 576_CR68
  publication-title: Lab Invest
  doi: 10.1097/01.LAB.0000082383.40635.FE
  contributor:
    fullname: N Nourhaghighi
– volume: 10
  start-page: 26
  year: 2014
  ident: 576_CR17
  publication-title: Mol Pain
  doi: 10.1186/1744-8069-10-26
  contributor:
    fullname: RP Bonin
– volume: 38
  start-page: 303
  year: 2002
  ident: 576_CR71
  publication-title: Glia
  doi: 10.1002/glia.10074
  contributor:
    fullname: T Oya
– volume: 22
  start-page: 171
  year: 1998
  ident: 576_CR60
  publication-title: World J Surg
  doi: 10.1007/s002689900366
  contributor:
    fullname: SN McGill
– volume: 173
  start-page: 63
  year: 2002
  ident: 576_CR18
  publication-title: Exp Neurol
  doi: 10.1006/exnr.2001.7827
  contributor:
    fullname: GT Casella
– volume: 139
  start-page: 329
  year: 2003
  ident: 576_CR72
  publication-title: Br J Pharmacol
  doi: 10.1038/sj.bjp.0705259
  contributor:
    fullname: L Pizurki
– volume: 74
  start-page: 263
  year: 2015
  ident: 576_CR81
  publication-title: Neurobiol Dis
  doi: 10.1016/j.nbd.2014.12.003
  contributor:
    fullname: BD Semple
– volume: 30
  start-page: 2242
  year: 2002
  ident: 576_CR91
  publication-title: Crit Care Med
  doi: 10.1097/00003246-200210000-00011
  contributor:
    fullname: H Ueno
– volume: 86
  start-page: 483
  year: 1997
  ident: 576_CR85
  publication-title: J Neurosurg
  doi: 10.3171/jns.1997.86.3.0483
  contributor:
    fullname: CH Tator
– volume: 74
  start-page: 227
  year: 2003
  ident: 576_CR94
  publication-title: J Neurosci Res
  doi: 10.1002/jnr.10759
  contributor:
    fullname: WD Whetstone
– volume: 12
  start-page: 1
  year: 1995
  ident: 576_CR10
  publication-title: J Neurotrauma
  doi: 10.1089/neu.1995.12.1
  contributor:
    fullname: DM Basso
– volume: 33
  start-page: 703
  year: 2010
  ident: 576_CR37
  publication-title: Hypertens Res
  doi: 10.1038/hr.2010.58
  contributor:
    fullname: Y Ikegame
– volume: 57
  start-page: 178
  year: 2008
  ident: 576_CR99
  publication-title: Neuron
  doi: 10.1016/j.neuron.2008.01.003
  contributor:
    fullname: BV Zlokovic
– volume: 158
  start-page: 1112
  year: 2009
  ident: 576_CR6
  publication-title: Neuroscience
  doi: 10.1016/j.neuroscience.2008.07.001
  contributor:
    fullname: DP Ankeny
– volume: 28
  start-page: 1771
  year: 2008
  ident: 576_CR15
  publication-title: J Cereb Blood Flow Metab
  doi: 10.1038/jcbfm.2008.76
  contributor:
    fullname: RL Benton
– ident: 576_CR63
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Snippet After spinal cord injury (SCI), neutrophil elastase (NE) released at injury site disrupts vascular endothelium integrity and stabilization. Angiopoietins...
The sivelestat regimen, optimized via a pharmacokinetics study, had potent effects on vascular stabilization by upregulating angiopoietin-1 via the AKT pathway...
Abstract After spinal cord injury (SCI), neutrophil elastase (NE) released at injury site disrupts vascular endothelium integrity and stabilization....
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SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
StartPage 73
SubjectTerms Angiogenesis
Angiopoietin-1 - metabolism
Angiopoietin-2 - metabolism
Angiopoietins
Animals
Apoptosis
Blood-brain barrier
Cicatrix - drug therapy
Cicatrix - etiology
Cytokines - metabolism
Disease Models, Animal
Endothelial Cells - drug effects
Endothelial Cells - metabolism
Endothelium
Female
Functional recovery
Gene Expression Regulation - genetics
Gene Expression Regulation - physiology
Glial scar
Glycine - analogs & derivatives
Glycine - pharmacology
Growth factors
Hostages
Humans
Ischemia
Laminin - metabolism
Leukocyte Elastase - metabolism
Leukocyte Elastase - pharmacology
Neovascularization
Nerve Tissue Proteins - metabolism
Neuropathic pain
Neutrophil elastase
Neutrophils
Nociceptin
Occludin - metabolism
Opioid Peptides - drug effects
Proteolysis
Rats
Rats, Sprague-Dawley
Recovery of Function - drug effects
Serine Proteinase Inhibitors - pharmacology
Spinal cord injuries
Spinal Cord Injuries - complications
Spinal Cord Injuries - pathology
Spinal cord injury
Sulfonamides - pharmacology
Transforming Growth Factor beta1 - metabolism
Wound healing
Zonula Occludens-1 Protein - metabolism
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Title Neutrophil elastase inhibition effectively rescued angiopoietin-1 decrease and inhibits glial scar after spinal cord injury
URI https://www.ncbi.nlm.nih.gov/pubmed/30086801
https://www.proquest.com/docview/2090618761
https://pubmed.ncbi.nlm.nih.gov/PMC6080383
https://doaj.org/article/ce2e28e8dfd64f55b561f5a692c30fa6
Volume 6
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