Role of neutrophils in exacerbation of brain injury after focal cerebral ischemia in hyperlipidemic mice

Stroke

Volumn 46, Issue 10, 2015, Pages 2916-2925

  Herz, Josephine ^a   Sabellek, Pascal ^a   Lane, Thomas E ^b   Gunzer, Matthias ^a   Hermann, Dirk M ^a   Doeppner, Thorsten R ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Brain injury; CXCR2; Hyperlipidemia; Inflammation; Neutrophils; Stroke

Indexed keywords

1 (2 BROMOPHENYL) 3 (2 HYDROXY 4 NITROPHENYL)UREA; CATALASE; CHEMOKINE RECEPTOR CXCR2; INDUCIBLE NITRIC OXIDE SYNTHASE; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; APOLIPOPROTEIN E; CARBANILAMIDE DERIVATIVE; CHOLESTEROL INTAKE; CYBB PROTEIN, MOUSE; MEMBRANE PROTEIN; MESSENGER RNA; NOS2 PROTEIN, MOUSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BLOOD; BLOOD BRAIN BARRIER; BONE MARROW; BRAIN; BRAIN INJURY; BRAIN ISCHEMIA; CHOLESTEROL DIET; CONTROLLED STUDY; DISEASE EXACERBATION; DNA DAMAGE; FLOW CYTOMETRY; FOCAL CEREBRAL ISCHEMIA; HYPERLIPIDEMIA; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE SUBPOPULATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL COUNT; NEUTROPHILIA; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN DIET; ANIMAL; ANTAGONISTS AND INHIBITORS; CEREBRAL ARTERY DISEASE; CHOLESTEROL INTAKE; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; APOLIPOPROTEINS E; BRAIN ISCHEMIA; CHOLESTEROL, DIETARY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HYPERLIPIDEMIAS; IMMUNOHISTOCHEMISTRY; INFARCTION, MIDDLE CEREBRAL ARTERY; INFLAMMATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; NADPH OXIDASE; NEUTROPHILS; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PHENYLUREA COMPOUNDS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, INTERLEUKIN-8B; RNA, MESSENGER;

EID: 84942927426     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.115.010620     Document Type: Article

References (32)

1. Macrez R, Ali C, Toutirais O, Le Mauff B, Defer G, Dirnagl U, et al. Stroke and the immune system: from pathophysiology to new therapeutic strategies. Lancet Neurol. 2011;10:471-480. doi: 10.1016/S1474-4422(11)70066-7.
2. Enlimomab Acute Stroke Trial Investigators. Use of anti-ICAM-1 therapy in ischemic stroke: results of the Enlimomab Acute Stroke Trial. Neurology. 2001;57:1428-1434.
3. ElAli A, Doeppner TR, Zechariah A, Hermann DM. Increased blood-brain barrier permeability and brain edema after focal cerebral ischemia induced by hyperlipidemia: role of lipid peroxidation and calpain-1/2, matrix metalloproteinase-2/9, and RhoA overactivation. Stroke. 2011;42:3238-3244. doi: 10.1161/STROKEAHA.111.615559.
4. Herz J, Hagen SI, Bergmüller E, Sabellek P, Göthert JR, Buer J, et al. Exacerbation of ischemic brain injury in hypercholesterolemic mice is associated with pronounced changes in peripheral and cerebral immune responses. Neurobiol Dis. 2014;62:456-468. doi: 10.1016/j. nbd.2013.10.022.
5. Kim E, Tolhurst AT, Qin LY, Chen XY, Febbraio M, Cho S. CD36/fatty acid translocase, an infammatory mediator, is involved in hyper-lipidemia-induced exacerbation in ischemic brain injury. J Neurosci. 2008;28:4661-4670. doi: 10.1523/JNEUROSCI.0982-08.2008.
6. Drechsler M, Megens RT, van Zandvoort M, Weber C, Soehnlein O. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation. 2010;122:1837-1845. doi: 10.1161/CIRCULATIONAHA.110.961714.
7. McColl BW, Allan SM, Rothwell NJ. Systemic infection, infammation and acute ischemic stroke. Neuroscience. 2009;158:1049-1061. doi: 10.1016/j.neuroscience.2008.08.019.
8. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999;22:391-397.
9. Barone FC, Hillegass LM, Price WJ, White RF, Lee EV, Feuerstein GZ, et al. Polymorphonuclear leukocyte infltration into cerebral focal isch-emic tissue: myeloperoxidase activity assay and histologic verifcation. J Neurosci Res. 1991;29:336-345. doi: 10.1002/jnr.490290309.
10. Connolly ES Jr, Winfree CJ, Springer TA, Naka Y, Liao H, Yan SD, et al. Cerebral protection in homozygous null ICAM-1 mice after middle cerebral artery occlusion. Role of neutrophil adhesion in the pathogenesis of stroke. J Clin Invest. 1996;97:209-216. doi: 10.1172/JCI118392.
11. Neumann J, Riek-Burchardt M, Herz J, Doeppner TR, König R, Hütten H, et al. Very-late-antigen-4 (VLA-4)-mediated brain invasion by neu-trophils leads to interactions with microglia, increased ischemic injury and impaired behavior in experimental stroke. Acta Neuropathol. 2015;129:259-277. doi: 10.1007/s00401-014-1355-2.
12. Prestigiacomo CJ, Kim SC, Connolly ES Jr, Liao H, Yan SF, Pinsky DJ. CD18-mediated neutrophil recruitment contributes to the pathogenesis of reperfused but not nonreperfused stroke. Stroke. 1999;30:1110-1117.
13. Veenstra M, Ransohoff RM. Chemokine receptor CXCR2: physiology regulator and neuroinfammation controller? J Neuroimmunol. 2012;246:1-9. doi: 10.1016/j.jneuroim.2012.02.016.
14. Köhler A, De Filippo K, Hasenberg M, van den Brandt C, Nye E, Hosking MP, et al. G-CSF-mediated thrombopoietin release triggers neutrophil motility and mobilization from bone marrow via induction of Cxcr2 ligands. Blood. 2011;117:4349-4357. doi: 10.1182/blood-2010-09-308387.
15. Hosking MP, Liu L, Ransohoff RM, Lane TE. A protective role for ELR+ chemokines during acute viral encephalomyelitis. PLoS Pathog. 2009;5:e1000648. doi: 10.1371/journal.ppat.1000648.
16. Doeppner TR, Kaltwasser B, Bähr M, Hermann DM. Effects of neural progenitor cells on post-stroke neurological impairment-a detailed and comprehensive analysis of behavioral tests. Front Cell Neurosci. 2014;8:338. doi: 10.3389/fncel.2014.00338.
17. Herz J, Reitmeir R, Hagen SI, Reinboth BS, Guo Z, Zechariah A, et al. Intracerebroventricularly delivered VEGF promotes contralesional corti-corubral plasticity after focal cerebral ischemia via mechanisms involving anti-infammatory actions. Neurobiol Dis. 2012;45:1077-1085. doi: 10.1016/j.nbd.2011.12.026.
18. Enzmann G, Mysiorek C, Gorina R, Cheng YJ, Ghavampour S, Hannocks MJ, et al. The neurovascular unit as a selective barrier to polymorphonuclear granulocyte (PMN) infltration into the brain after ischemic injury. Acta Neuropathol. 2013;125:395-412. doi: 10.1007/s00401-012-1076-3.
19. Cuartero MI, Ballesteros I, Moraga A, Nombela F, Vivancos J, Hamilton JA, et al. N2 neutrophils, novel players in brain infammation after stroke: modulation by the PPARγ agonist rosiglitazone. Stroke. 2013;44:3498-3508. doi: 10.1161/STROKEAHA.113.002470.
20. Huo Y, Schober A, Forlow SB, Smith DF, Hyman MC, Jung S, et al. Circulating activated platelets exacerbate atherosclerosis in mice def-cient in apolipoprotein E. Nat Med. 2003;9:61-67. doi: 10.1038/nm810.
21. Sreeramkumar V, Adrover JM, Ballesteros I, Cuartero MI, Rossaint J, Bilbao I, et al. Neutrophils scan for activated platelets to initiate infam-mation. Science. 2014;346:1234-1238. doi: 10.1126/science.1256478.
22. Dunican A, Grutkoski P, Leuenroth S, Ayala A, Simms HH. Neutrophils regulate their own apoptosis via preservation of CXC receptors. J Surg Res. 2000;90:32-38. doi: 10.1006/jsre.2000.5829.
23. Auten RL, Richardson RM, White JR, Mason SN, Vozzelli MA, Whorton MH. Nonpeptide CXCR2 antagonist prevents neutrophil accumulation in hyperoxia-exposed newborn rats. J Pharmacol Exp Ther. 2001;299:90-95.
24. Beray-Berthat V, Croci N, Plotkine M, Margaill I. Polymorphonuclear neutrophils contribute to infarction and oxidative stress in the cortex but not in the striatum after ischemia-reperfusion in rats. Brain Res. 2003;987:32-38.
25. Jin R, Yang G, Li G. Infammatory mechanisms in ischemic stroke: role of infammatory cells. J Leukoc Biol. 2010;87:779-789. doi: 10.1189/jlb.1109766.
26. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011;11:519-531. doi: 10.1038/nri3024.
27. Denes A, Pradillo JM, Drake C, Buggey H, Rothwell NJ, Allan SM. Surgical manipulation compromises leukocyte mobilization responses and infammation after experimental cerebral ischemia in mice. Front Neurosci. 2013;7:271. doi: 10.3389/fnins.2013.00271.
28. Brait VH, Rivera J, Broughton BR, Lee S, Drummond GR, Sobey CG. Chemokine-related gene expression in the brain following ischemic stroke: no role for CXCR2 in outcome. Brain Res. 2011;1372:169-179. doi: 10.1016/j.brainres.2010.11.087.
29. Copin JC, da Silva RF, Fraga-Silva RA, Capettini L, Quintao S, Lenglet S, et al. Treatment with Evasin-3 reduces atherosclerotic vulnerability for ischemic stroke, but not brain injury in mice. J Cereb Blood Flow Metab. 2013;33:490-498. doi: 10.1038/jcbfm.2012.198.
30. Gelderblom M, Weymar A, Bernreuther C, Velden J, Arunachalam P, Steinbach K, et al. Neutralization of the IL-17 axis diminishes neutro-phil invasion and protects from ischemic stroke. Blood. 2012;120:3793-3802. doi: 10.1182/blood-2012-02-412726.
31. Perez-de-Puig I, Miro-Mur F, Ferrer-Ferrer M, Gelpi E, Pedragosa J, Justicia C, et al. Neutrophil recruitment to the brain in mouse and human ischemic stroke. Acta Neuropathol. 2015;129:239-257.
32. Gliem M, Mausberg AK, Lee JI, Simiantonakis I, van Rooijen N, Hartung HP, et al. Macrophages prevent hemorrhagic infarct transformation in murine stroke models. Ann Neurol. 2012;71:743-752. doi: 10.1002/ana.23529.