Rapid brain penetration of interleukin-1 receptor antagonist in rat cerebral ischaemia: Pharmacokinetics, distribution, protection

British Journal of Pharmacology

Volumn 160, Issue 1, 2010, Pages 153-159

  Greenhalgh, A D ^a   Galea, J ^b   Denes A ^a   Tyrrell, P J ^b   Rothwell, N J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b SALFORD ROYAL NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Brain penetration; Cerebral ischaemia; Inflammation; Interleukin 1 receptor antagonist; Neuroprotection

Indexed keywords

RECOMBINANT INTERLEUKIN 1 RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; BRAIN TISSUE; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG CEREBROSPINAL FLUID LEVEL; DRUG DISTRIBUTION; DRUG PENETRATION; IMMUNOHISTOCHEMISTRY; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SINGLE DRUG DOSE; SPRAGUE DAWLEY RAT; TISSUE DISTRIBUTION;

EID: 77950932320     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.00684.x     Document Type: Article

References (44)

1. Alexander SPH, Mathie A, Peters JA (2008). Guide to Receptors and Channels (GRAC), 3rd edn. Br J Pharmacol 153 : S1.
2. Allan SM, Tyrrell PJ, Rothwell NJ (2005). Interleukin-1 and neuronal injury. Nat Rev Immunol 5 : 629 640.
3. Banks W, Kastin A, Broadwell R (1995). Passage of cytokines across the blood-brain barrier. Neuroimmunomodulation 2 : 241 248.
4. Belayev L, Busto R, Zhao W, Ginsberg MD (1996). Quantitative evaluation of blood-brain barrier permeability following middle cerebral artery occlusion in rats. Brain Res 739 : 88 96.
5. Bernardes-Silva M, Anthony DC, Issekutz AC, Perry VH (2001). Recruitment of neutrophils across the blood-brain barrier: the role of E- and P-selectins. J Cereb Blood Flow Metab 21 : 1115 1124.
6. Chaichana KL, Pradilla G, Huang J, Tamargo RJ (2009). Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. Surg Neurol (in press).
7. Chapman KZ, Dale VQ, Denes A, Bennett G, Rothwell NJ, Allan SM et al. (2009). A rapid and transient peripheral inflammatory response precedes brain inflammation after experimental stroke. J Cereb Blood Flow Metab 29 : 1764 1768.
8. Clark SR, McMahon CJ, Gueorguieva I, Rowland M, Scarth S, Georgiou R et al. (2008). Interleukin-1 receptor antagonist penetrates human brain at experimentally therapeutic concentrations. J Cereb Blood Flow Metab 28 : 387 394.
9. Denes A, Ferenczi S, Halasz J, Kornyei Z, Kovacs KJ (2008). Role of CX3CR1 (fractalkine receptor) in brain damage and inflammation induced by focal cerebral ischemia in mouse. J Cereb Blood Flow Metab 28 : 1707 1721.
10. Donnan GA (2008). The 2007 Feinberg lecture: a new road map for neuroprotection. Stroke 39 : 242
11. Durukan A, Marinkovic I, Strbian D, Pitkonen M, Pedrono E, Soinne L et al. (2009). Post-ischemic blood-brain barrier leakage in rats: one-week follow-up by MRI. Brain Res 1280 : 158 165.
12. Emsley HCA, Smith CJ, Georgiou RF, Vail A, Hopkins SJ, Rothwell NJ et al. (2005). A randomised phase II study of interleukin-1 receptor antagonist in acute stroke patients. J Neurol Neurosurg Psychiatry 76 : 1366 1372.
13. Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA, Savitz SI et al. (2009). Update of the Stroke Therapy Academic Industry Roundtable Preclinical Recommendations. Stroke 40 : 2244 2250.
14. Gueorguieva I, Clark SR, McMahon CJ, Scarth S, Rothwell NJ, Tyrell PJ et al. (2007). Pharmacokinetic modelling of interleukin-1 receptor antagonist in plasma and cerebrospinal fluid of patients following subarachnoid haemorrhage. Br J Clin Pharmacol 65 : 317 325.
15. Gutierrez E, Banks W, Kastin A (1994). Blood-borne interleukin-1 receptor antagonist crosses the blood-brain barrier. J Neuroimmunol 55 : 153 160.
16. Hankey G (2003). Long-term outcome after ischaemic stroke/transient ischaemic attack. Cerebrovasc Dis 16 : 14 19.
17. Hannum C, Wilcox C, Arend W, Joslin F, Dripps D, Heimdal P et al. (1990). Interleukin-1 receptor antagonist activity of a human interleukin-1 inhibitor. Nature 343 : 336 340. (Pubitemid 120028524)
18. Huang P, Chen C-H, Yang Y-H, Lin R-T, Lin F-C, Liu C-K (2006). Eligibility for recombinant tissue plasminogen activator in acute ischemic stroke. Cerebrovasc Dis 22 : 423 428.
19. 2, and their endogenous inhibitor IL-1ra. J Neurotrauma 24 : 1545 1557.
20. Konsman J, Vigues S, Mackerlova L, Bristow A, Blomqvist A (2004). Rat brain vascular distribution of interleukin-1 type-1 receptor immunoreactivity: relationship to patterns of inducible cyclooxygenase expression by peripheral inflammatory stimuli. J Comp Neurol 472 : 113 129.
21. Korherr C, Hofmeister R, Wesche H, Falk W (1997). A critical role for interleukin-1 receptor accessory protein in interleukin-1 signaling. Eur J Immunol 27 : 262 267. (Pubitemid 27046087)
22. Kuroiwa T, Ting P, Martinez H, Klatzo I (1985). The biphasic opening of the blood-brain barrier to proteins following temporary middle cerebral artery occlusion. Acta Neuropathol 68 : 122 129. (Pubitemid 16242137)
23. Latour L, Kang D-W, Ezzeddine M, Chalela J, Warach S (2004). Early blood-brain barrier disruption in human focal brain ischemia. Ann Neurol 56 : 468 477. (Pubitemid 39319336)
24. Loddick SA, Rothwell NJ (1996). Neuroprotective effects of human recombinant interleukin-1 receptor antagonist in focal cerebral ischaemia in the rat. J Cereb Blood Flow Metab 16 : 932 940. (Pubitemid 26292060)
25. McColl BW, Rothwell NJ, Allan SM (2007). 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 27 : 4403 4412.
26. McColl BW, Rothwell NJ, Allan SM (2008). Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J Neurosci 28 : 9451 9462.
27. McColl BW, Allan SM, Rothwell NJ (2009). Systemic infection, inflammation and acute ischemic stroke. Neuroscience 158 : 1049 1061.
28. Macleod MR, Fisher M, O'Collins V, Sena ES, Dirnagl U, Bath PMW et al. (2009). Good laboratory practice: preventing introduction of bias at the bench. Stroke 40 : e50 52
29. Mulcahy NJ, Ross J, Rothwell NJ, Loddick SA (2003). Delayed administration of interleukin-1 receptor antagonist protects against transient cerebral ischaemia in the rat. Br J Pharmacol 140 : 471 476. (Pubitemid 37330491)
30. Offner H, Subramanian S, Parker SM, Afentoulis ME, Vandenbark AA, Hurn PD (2005). Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab 26 : 654 665.
31. Philip M, Benatar M, Fisher M, Savitz SI (2009). Methodological quality of animal studies of neuroprotective agents currently in phase II/III acute ischemic stroke trials. Stroke 40 : 577 581.
32. Pillai DR, Dittmar MS, Baldaranov D, Heidemann RM, Henning EC, Schuierer G et al. (2009). Cerebral ischemia-reperfusion injury in rats[mdash]A 3 T MRI study on biphasic blood-brain barrier opening and the dynamics of edema formation. J Cereb Blood Flow Metab 29 : 1846 1855.
33. Price CJS, Warburton EA, Menon DK (2003). Human cellular inflammation in the pathology of acute cerebral ischaemia. J Neurol Neurosurg Psychiatry 74 : 1476 1484. (Pubitemid 37392868)
34. Quiniou C, Kooli E, Joyal J-S, Sapieha P, Sennlaub F, Lahaie I et al. (2008). Interleukin-1 and ischemic brain injury in the newborn: development of a small molecule inhibitor of IL-1 receptor. Semin Perinatol 32 : 325 333.
35. Relton JK, Martin D, Thompson RC, Russell DA (1996). Peripheral administration of interleukin-1 receptor antagonist inhibits brain damage after focal cerebral ischemia in the rat. Exp Neurol 138 : 206 213. (Pubitemid 26135199)
36. Savitz S, Fisher M (2007). Future of neuroprotection for acute stroke: in the aftermath of the SAINT trials. Ann Neurol 61 : 396 402. (Pubitemid 46878767)
37. Schoch B, Regel JP, Wichert M, Gasser T, Volbracht L, Stolke D (2007). Analysis of intrathecal interleukin-6 as a potential predictive factor for vasospasm in subarachnoid hemorrhage. Neurosurgery 60 : 828 836. 810.1227/1201.NEU.0000255440.0000221495.0000255480.
38. Skinner RA, Gibson RM, Rothwell NJ, Pinteaux E, Penny JI (2009). Transport of interleukin-1 across cerebromicrovascular endothelial cells. Br J Pharmacol 156 : 1115 1123.
39. Smith DE, Lipsky BP, Russell C, Ketchem RR, Kirchner J, Hensley K et al. (2009). A central nervous system-restricted isoform of the interleukin-1 receptor accessory protein modulates neuronal responses to interleukin-1. Immunity 30 : 817 831.
40. Strbian D, Durukan A, Pitkonen M, Marinkovic I, Tatlisumak E, Pedrono E et al. (2008). The blood-brain barrier is continuously open for several weeks following transient focal cerebral ischemia. Neuroscience 153 : 175 181.
41. Summers L, Kielty C, Pinteaux E (2009). Adhesion to fibronectin regulates interleukin-1 beta expression in microglial cells. Mol Cell Neurosci 41 : 148 155.
42. Thornton P, Pinteaux E, Allan SM, Rothwell NJ (2008). Matrix metalloproteinase-9 and urokinase plasminogen activator mediate interleukin-1-induced neurotoxicity. Mol Cell Neurosci 37 : 135 142. (Pubitemid 350299999)
43. Wang Q, Tang XN, Yenari MA (2007). The inflammatory response in stroke. J Neuroimmunol 184 : 53 68. (Pubitemid 46365991)
44. Warach S, Latour LL (2004). Evidence of reperfusion injury, exacerbated by thrombolytic therapy, in human focal brain ischemia using a novel imaging marker of early blood-brain barrier disruption. Stroke 35 : 2659 2661. (Pubitemid 39458362)