Systemic inflammation as a therapeutic target in acute ischemic stroke

References

• Medzhitov R. Origin and physiological roles of inflammation. Nature 2008;454:428-35
   PubMed Web of Science ®Google Scholar
• Dziedzic T. Clinical significance of acute phase reaction in stroke patients. Front Biosci 2008;13:2922-7
   PubMed Web of Science ®Google Scholar
• Dziedzic T, Slowik A, Szczudlik A. Interleukin-6 and stroke: cerebral ischemia versus nonspecific factors influencing interleukin-6. Stroke 2003;34:e229-30
   Web of Science ®Google Scholar
• Beamer NB, Coull BM, Clark WM, et al. Persistent inflammatory response in stroke survivors. Neurology 1998;50:1722-8
   PubMed Web of Science ®Google Scholar
• Cao JJ, Thach C, Manolio TA, et al. C-reactive protein, carotid intima-media thickness, and incidence of ischemic stroke in the elderly: the Cardiovascular Health Study. Circulation 2003;108:166-70
   PubMed Web of Science ®Google Scholar
• Rost NS, Wolf PA, Kase CS, et al. Plasma concentration of C-reactive protein and risk of ischemic stroke and transient ischemic attack: the Framingham study. Stroke 2001;32:2575-9
   PubMed Web of Science ®Google Scholar
• Beamer NB, Coull BM, Clark WM, et al. Interleukin-6 and interleukin-1 receptor antagonist in acute stroke. Ann Neurol 1995;37:800-5
   PubMed Web of Science ®Google Scholar
• Tarkowski E, Rosengren L, Blomstrand C, et al. Early intrathecal production of interleukin-6 predicts the size of brain lesion in stroke. Stroke 1995;26:1393-8
   PubMed Web of Science ®Google Scholar
• Fassbender K, Rossol S, Kammer T, et al. Proinflammatory cytokines in serum of patients with acute cerebral ischemia: kinetics of secretion and relation to the extent of brain damage and outcome of disease. J Neurol Sci 1994;122:135-9
   PubMed Web of Science ®Google Scholar
• Szczudlik A, Dziedzic T, Bartus S, et al. Serum interleukin-6 predicts cortisol release in acute stroke patients. J Endocrinol Invest 2004;27:37-41
   PubMed Web of Science ®Google Scholar
• Acalovschi D, Wiest T, Hartmann M, et al. Multiple levels of regulation of the interleukin-6 system in stroke. Stroke 2003;34:1864-9
   PubMed Web of Science ®Google Scholar
• Emsley HC, Smith CJ, Gavin CM, et al. An early and sustained peripheral inflammatory response in acute ischaemic stroke: relationships with infection and atherosclerosis. J Neuroimmunol 2003;139:93-101
   PubMed Web of Science ®Google Scholar
• Winbeck K, Poppert H, Etgen T, et al. Prognostic relevance of early serial C-reactive protein measurements after first ischemic stroke. Stroke 2002;33:2459-64
   PubMed Web of Science ®Google Scholar
• Marquardt L, Ruf A, Mansmann U, et al. Inflammatory response after acute ischemic stroke. J Neurol Sci 2005;236:65-71
   PubMed Web of Science ®Google Scholar
• Christensen H, Boysen G. C-reactive protein and white blood cell count increases in the first 24 hours after acute stroke. Cerebrovasc Dis 2004;18:214-19
   PubMed Web of Science ®Google Scholar
• Kim JS, Yoon SS, Kim YH, Ryu JS. Serial measurement of interleukin-6, transforming growth factor-beta, and S-100 protein in patients with acute stroke. Stroke 1996;27:1553-7
   PubMed Web of Science ®Google Scholar
• Waje-Andreassen U, Kråkenes J, Ulvestad E, et al. IL-6: an early marker for outcome in acute ischemic stroke. Acta Neurol Scand 2005;111:360-5
   PubMed Web of Science ®Google Scholar
• Tamam Y, Iltumur K, Apak I. Assessment of acute phase proteins in acute ischemic stroke. Tohoku J Exp Med 2005;206:91-8
   PubMed Web of Science ®Google Scholar
• Basic Kes V, Simundic AM, Nikolac N, et al. Pro-inflammatory and anti-inflammatory cytokines in acute ischemic stroke and their relation to early neurological deficit and stroke outcome. Clin Biochem 2008;41:1330-4
   PubMed Web of Science ®Google Scholar
• Worthmann H, Tryc AB, Goldbecker A, et al. The temporal profile of inflammatory markers and mediators in blood after acute ischemic stroke differs depending on stroke outcome. Cerebrovasc Dis 2010;30:85-92
   PubMed Web of Science ®Google Scholar
• Ormstad H, Aass HC, Lund-Sørensen N, et al. Serum levels of cytokines and C-reactive protein in acute ischemic stroke patients, and their relationship to stroke lateralization, type, and infarct volume. J Neurol 2011;258:677-85
   PubMed Web of Science ®Google Scholar
• Smith CJ, Emsley HC, Vail A, et al. Variability of the systemic acute phase response after ischemic stroke. J Neurol Sci 2006;251:77-81
   PubMed Web of Science ®Google Scholar
• Di Napoli M, Papa F, Bocola V. C-reactive protein in ischemic stroke: an independent prognostic factor. Stroke 2001;32:917-24
   PubMed Web of Science ®Google Scholar
• Audebert HJ, Rott MM, Eck T, Haberl RL. Systemic inflammatory response depends on initial stroke severity but is attenuated by successful thrombolysis. Stroke 2004;35:2128-33
   PubMed Web of Science ®Google Scholar
• Perini F, Morra M, Alecci M, et al. Temporal profile of serum anti-inflammatory and pro-inflammatory interleukins in acute ischemic stroke patients. Neurol Sci 2001;22:289-96
   PubMed Web of Science ®Google Scholar
• Dziedzic T, Gryz EA, Turaj W, et al. Serum interleukin-6 soluble receptor in relation to interleukin-6 in stroke patients. J Mol Neurosci 2004;24:293-8
   PubMed Web of Science ®Google Scholar
• Elkind MS, Tai W, Coates K, et al. High-sensitivity C-reactive protein, lipoprotein-associated phospholipase A2, and outcome after ischemic stroke. Arch Intern Med 2006;166:2073-80
   PubMed Web of Science ®Google Scholar
• Vila N, Castillo J, Dávalos A, Chamorro A. Proinflammatory cytokines and early neurological worsening in ischemic stroke. Stroke 2000;31:2325-9
   PubMed Web of Science ®Google Scholar
• Montaner J, Rovira A, Molina CA, et al. Plasmatic level of neuroinflammatory markers predict the extent of diffusion-weighted image lesions in hyperacute stroke. J Cereb Blood Flow Metab 2003;23:1403-7
   PubMed Web of Science ®Google Scholar
• Sotgiu S, Zanda B, Marchetti B, et al. Inflammatory biomarkers in blood of patients with acute brain ischemia. Eur J Neurol 2006;13:505-13
   PubMed Web of Science ®Google Scholar
• Intiso D, Zarrelli MM, Lagioia G, et al. Tumor necrosis factor alpha serum levels and inflammatory response in acute ischemic stroke patients. Neurol Sci 2004;24:390-6
   PubMed Web of Science ®Google Scholar
• Zaremba J, Losy J. Early TNF-alpha levels correlate with ischaemic stroke severity. Acta Neurol Scand 2001;104:288-95
   PubMed Web of Science ®Google Scholar
• Chapman KZ, Dale VQ, Dénes A, et al. A rapid and transient peripheral inflammatory response precedes brain inflammation after experimental stroke. J Cereb Blood Flow Metab 2009;29:1764-8
   PubMed Web of Science ®Google Scholar
• Haeusler KG, Schmidt WU, Föhring F, et al. Cellular immunodepression preceding infectious complications after acute ischemic stroke in humans. Cerebrovasc Dis 2008;25:50-8
   PubMed Web of Science ®Google Scholar
• Vogelgesang A, Grunwald U, Langner S, et al. Analysis of lymphocyte subsets in patients with stroke and their influence on infection after stroke. Stroke 2008;39:237-41
   PubMed Web of Science ®Google Scholar
• Urra X, Cervera A, Villamor N, et al. Harms and benefits of lymphocyte subpopulations in patients with acute stroke. Neuroscience 2009;158:1174-83
   PubMed Web of Science ®Google Scholar
• Liu ZJ, Chen C, Li FW, et al. Splenic responses in ischemic stroke: new insights into stroke pathology. CNS Neurosci Ther 2015;21(4):320-6
   PubMed Web of Science ®Google Scholar
• Denes A, McColl BW, Leow-Dyke SF, et al. Experimental stroke-induced changes in the bone marrow reveal complex regulation of leukocyte responses. J Cereb Blood Flow Metab 2011;31:1036-50
   PubMed Web of Science ®Google Scholar
• Grau AJ, Urbanek C, Palm F. Common infections and the risk of stroke. Nat Rev Neurol 2010;6:681-94
   PubMed Web of Science ®Google Scholar
• Emsley HC, Hopkins SJ. Acute ischaemic stroke and infection: recent and emerging concepts. Lancet Neurol 2008;7:341-53
   PubMed Web of Science ®Google Scholar
• Di Napoli M, Papa F, Bocola V. Prognostic influence of increased C-reactive protein and fibrinogen levels in ischemic stroke. Stroke 2001;32:133-8
   PubMed Web of Science ®Google Scholar
• Muir KW, Weir CJ, Alwan W, et al. C-reactive protein and outcome after ischemic stroke. Stroke 1999;30:981-5
   PubMed Web of Science ®Google Scholar
• Masotti L, Ceccarelli E, Forconi S, Cappelli R. Prognostic role of C-reactive protein in very old patients with acute ischaemic stroke. J Intern Med 2005;258:145-52
   PubMed Web of Science ®Google Scholar
• Rallidis LS, Vikelis M, Panagiotakos DB, et al. Inflammatory markers and in-hospital mortality in acute ischaemic stroke. Atherosclerosis 2006;189:193-7
   PubMed Web of Science ®Google Scholar
• Whiteley W, Jackson C, Lewis S, et al. Inflammatory markers and poor outcome after stroke: a prospective cohort study and systematic review of interleukin-6. PLoS Med 2009;6:e1000145
   PubMed Web of Science ®Google Scholar
• Montaner J, Fernandez-Cadenas I, Molina CA, et al. Poststroke C-reactive protein is a powerful prognostic tool among candidates for thrombolysis. Stroke 2006;37:1205-10
   PubMed Web of Science ®Google Scholar
• den Hertog HM, van Rossum JA, van der Worp HB, et al. C-reactive protein in the very early phase of acute ischemic stroke: association with poor outcome and death. J Neurol 2009;256:2003-8
   PubMed Web of Science ®Google Scholar
• Idicula TT, Brogger J, Naess H, et al. Admission C-reactive protein after acute ischemic stroke is associated with stroke severity and mortality: the ’Bergen stroke study’. BMC Neurol 2009;9:18
   PubMed Web of Science ®Google Scholar
• Castellanos M, Castillo J, García MM, et al. Inflammation-mediated damage in progressing lacunar infarctions: a potential therapeutic target. Stroke 2002;33:982-7
   PubMed Web of Science ®Google Scholar
• Leira R, Rodríguez-Yáñez M, Castellanos M, et al. Hyperthermia is a surrogate marker of inflammation-mediated cause of brain damage in acute ischaemic stroke. J Intern Med 2006;260:343-9
   PubMed Web of Science ®Google Scholar
• Johansson A, Ahrén B, Näsman B, et al. Cortisol axis abnormalities early after stroke–relationships to cytokines and leptin. J Intern Med 2000;247:179-87
   PubMed Web of Science ®Google Scholar
• Dziedzic T, Slowik A, Szczudlik A. Urine albumin excretion in acute ischaemic stroke is related to serum interleukin-6. Clin Chem Lab Med 2004;42:182-5
   PubMed Web of Science ®Google Scholar
• Urra X, Villamor N, Amaro S, et al. Monocyte subtypes predict clinical course and prognosis in human stroke. J Cereb Blood Flow Metab 2009;29:994-1002
   PubMed Web of Science ®Google Scholar
• Kim J, Song TJ, Park JH, et al. Different prognostic value of white blood cell subtypes in patients with acute cerebral infarction. Atherosclerosis 2012;222:464-7
   PubMed Web of Science ®Google Scholar
• Quan N, Banks WA. Brain-immune communication pathways. Brain Behav Immun 2007;21:727-35
   PubMed Web of Science ®Google Scholar
• Quan N. In-depth conversation: spectrum and kinetics of neuroimmune afferent pathways. Brain Behav Immun 2014;40:1-8
   PubMed Web of Science ®Google Scholar
• Dantzer R, O’Connor JC, Freund GG, et al. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008;9:46-56
   PubMed Web of Science ®Google Scholar
• Quan N, Stern EL, Whiteside MB, Herkenham M. Induction of pro-inflammatory cytokine mRNAs in the brain after peripheral injection of subseptic doses of lipopolysaccharide in the rat. J Neuroimmunol 1999;93:72-80
   PubMed Web of Science ®Google Scholar
• Qin L, Wu X, Block ML, et al. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007;55:453-62
   PubMed Web of Science ®Google Scholar
• Chen J, Buchanan JB, Sparkman NL, et al. Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain Behav Immun 2008;22:301-11
   PubMed Web of Science ®Google Scholar
• Cazareth J, Guyon A, Heurteaux C, et al. Molecular and cellular neuroinflammatory status of mouse brain after systemic lipopolysaccharide challenge: importance of CCR2/CCL2 signaling. J Neuroinflammation 2014;11:132
   PubMed Web of Science ®Google Scholar
• Capuron L, Miller AH. Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol Ther 2011;130:226-38
   PubMed Web of Science ®Google Scholar
• Serres S, Anthony DC, Jiang Y, et al. Systemic inflammatory response reactivates immune-mediated lesions in rat brain. J Neurosci 2009;29:4820-8
   PubMed Web of Science ®Google Scholar
• Moreno B, Jukes JP, Vergara-Irigaray N, et al. Systemic inflammation induces axon injury during brain inflammation. Ann Neurol 2011;70:932-42
   PubMed Web of Science ®Google Scholar
• Perry VH. Contribution of systemic inflammation to chronic neurodegeneration. Acta Neuropathol 2010;120:277-86
   PubMed Web of Science ®Google Scholar
• Godbout JP, Chen J, Abraham J, et al. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J 2005;19:1329-31
   PubMed Web of Science ®Google Scholar
• Godbout JP, Moreau M, Lestage J, et al. Aging exacerbates depressive-like behavior in mice in response to activation of the peripheral innate immune system. Neuropsychopharmacology 2008;33:2341-51
   PubMed Web of Science ®Google Scholar
• Schedlowski M, Engler H, Grigoleit JS. Endotoxin-induced experimental systemic inflammation in humans: a model to disentangle immune-to-brain communication. Brain Behav Immun 2014;35:1-8
   PubMed Web of Science ®Google Scholar
• McColl BW, Rothwell NJ, Allan SM. Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1- and neutrophil-dependent mechanisms. J Neurosci 2007;27:4403-12
   PubMed Web of Science ®Google Scholar
• McColl BW, Rothwell NJ, Allan SM. Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J Neurosci 2008;28:9451-62
   PubMed Web of Science ®Google Scholar
• Spencer SJ, Mouihate A, Pittman QJ. Peripheral inflammation exacerbates damage after global ischemia independently of temperature and acute brain inflammation. Stroke 2007;38:1570-7
   PubMed Web of Science ®Google Scholar
• Muhammad S, Haasbach E, Kotchourko M, et al. Influenza virus infection aggravates stroke outcome. Stroke 2011;42:783-91
   PubMed Web of Science ®Google Scholar
• Murray KN, Girard S, Holmes WM, et al. Systemic inflammation impairs tissue reperfusion through endothelin-dependent mechanisms in cerebral ischemia. Stroke 2014;45:3412-19
   PubMed Web of Science ®Google Scholar
• Dénes Á, Pradillo JM, Drake C, et al. Streptococcus pneumoniae worsens cerebral ischemia via interleukin 1 and platelet glycoprotein Ibα. Ann Neurol 2014;75:670-83
   PubMed Web of Science ®Google Scholar
• Gill R, Kemp JA, Sabin C, Pepys MB. Human C-reactive protein increases cerebral infarct size after middle cerebral artery occlusion in adult rats. J Cereb Blood Flow Metab 2004;24:1214-18
   PubMed Web of Science ®Google Scholar
• Terao S, Yilmaz G, Stokes KY, et al. Inflammatory and injury responses to ischemic stroke in obese mice. Stroke 2008;39:943-50
   PubMed Web of Science ®Google Scholar
• Sironi L, Tremoli E, Miller I, et al. Acute-phase proteins before cerebral ischemia in stroke-prone rats: identification by proteomics. Stroke 2001;32:753-60
   PubMed Web of Science ®Google Scholar
• Chiba T, Itoh T, Tabuchi M, et al. Interleukin-1β accelerates the onset of stroke in stroke-prone spontaneously hypertensive rats. Mediators Inflamm 2012;2012:701976
   PubMed Web of Science ®Google Scholar
• Chiba T, Ezaki O. Dietary restriction suppresses inflammation and delays the onset of stroke in stroke-prone spontaneously hypertensive rats. Biochem Biophys Res Commun 2010;399:98-103
   PubMed Web of Science ®Google Scholar
• de Beer FC, Baltz ML, Munn EA, et al. Isolation and characterization of C-reactive protein and serum amyloid P component in the rat. Immunology 1982;45:55-70
   PubMed Web of Science ®Google Scholar
• Black S, Kushner I, Samols D. C-reactive Protein. J Biol Chem 2004;279:48487-90
   PubMed Web of Science ®Google Scholar
• Prasad K. C-reactive protein (CRP)-lowering agents. Cardiovasc Drug Rev 2006;24:33-50
   PubMed Web of Science ®Google Scholar
• Scheller J, Garbers C, Rose-John S. Interleukin-6: from basic biology to selective blockade of pro-inflammatory activities. Semin Immunol 2014;26:2-12
   PubMed Web of Science ®Google Scholar
• Jones SA, Scheller J, Rose-John S. Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling. J Clin Invest 2011;121:3375-83
   PubMed Web of Science ®Google Scholar
• Emery P, Keystone E, Tony HP, et al. IL-6 receptor inhibition with tocilizumab improves treatment outcomes in patients with rheumatoid arthritis refractory to anti-tumour necrosis factor biologicals: results from a 24-week multicenter randomised placebo-controlled trial. Ann Rheum Dis 2008;67:1516-23
   PubMed Web of Science ®Google Scholar
• Sodenkamp J, Waetzig GH, Scheller J, et al. Therapeutic targeting of interleukin-6 trans-signaling does not affect the outcome of experimental tuberculosis. Immunobiology 2012;217:996-1004
   PubMed Web of Science ®Google Scholar
• Hoge J, Yan I, Jänner N, et al. IL-6 controls the innate immune response against Listeria monocytogenes via classical IL-6 signaling. J Immunol 2013;190:703-11
   PubMed Web of Science ®Google Scholar
• Emsley HC, Smith CJ, Georgiou RF, et al. A randomised phase II study of interleukin-1 receptor antagonist in acute stroke patients. J Neurol Neurosurg Psychiatry 2005;76:1366-72
   PubMed Web of Science ®Google Scholar
• Giles JA, Greenhalgh AD, Davies CL, et al. Requirement for interleukin-1 to drive brain inflammation reveals tissue-specific mechanisms of innate immunity. Eur J Immunol 2015;45:525-30
   PubMed Web of Science ®Google Scholar
• Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES. The sympathetic nerve – an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 2000;52:595-638
   PubMed Web of Science ®Google Scholar
• Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000;405:458-62
   PubMed Web of Science ®Google Scholar
• Rosas-Ballina M, Tracey KJ. Cholinergic control of inflammation. J Intern Med 2009;265:663-79
   PubMed Web of Science ®Google Scholar
• Wang YY, Lin SY, Chuang YH, et al. Adipose proinflammatory cytokine expression through sympathetic system is associated with hyperglycemia and insulin resistance in a rat ischemic stroke model. Am J Physiol Endocrinol Metab 2011;300:E155-63
   PubMed Web of Science ®Google Scholar
• Westendorp WF, Vermeij JD, Vermeij F, et al. Antibiotic therapy for preventing infections in patients with acute stroke. Cochrane Database Syst Rev 2012;1:CD008530
   PubMedGoogle Scholar
• Liesz A, Dalpke A, Mracsko E, et al. DAMP Signaling is a Key Pathway Inducing Immune Modulation after Brain Injury. J Neurosci 2015;35:583-98
   PubMed Web of Science ®Google Scholar