Post-conditioning with lipopolysaccharide reduces the inflammatory infiltrate to the injured brain and spinal cord: A potential neuroprotective treatment

European Journal of Neuroscience

Volumn 22, Issue 10, 2005, Pages 2441-2450

  Davis, Andrew E M ^a   Campbell, Sandra J ^a   Wilainam, Panop ^a   Anthony, Daniel C ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Endotoxin; IL 1 ; Inflammation; Neutrophil; Priming; Rat

Indexed keywords

INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN; BRAIN INJURY; CELL DEATH; CONTROLLED STUDY; INFLAMMATORY INFILTRATE; LEUKOCYTE; MALE; MONOCYTE; NEUROPROTECTION; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD; SPINAL CORD INJURY;

ACUTE-PHASE REACTION; ANIMALS; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; INFLAMMATION; LEUKOCYTE COUNT; LEUKOCYTOSIS; LIPOPOLYSACCHARIDES; MALE; NEUROPROTECTIVE AGENTS; RATS; RATS, WISTAR; SPINAL CORD; SPINAL CORD COMPRESSION;

EID: 28744454151     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04447.x     Document Type: Article

References (44)

1. Ahmed, S.H., He, Y.Y., Nassief, A., Xu, J., Xu, X.M., Hsu, C.Y. & Faraci, F.M. (2000) Effects of lipopolysaccharide priming on acute ischemic brain injury. Stroke, 31, 193-199.
2. Aihara, N., Tanno, H., Hall, J.J., Pitts, L.H. & Noble, L.J. (1994) Immunocytochemical localization of immunoglobulins in the rat brain: relationship to the blood-brain barrier. J. Comp. Neurol., 342, 481-496.
3. Alves-Rosa, F., Vulcano, M., Beigier-Bompadre, M., Fernandez, G., Palermo, M. & Isturiz, M.A. (2002) Interleukin-1beta induces in vivo tolerance to lipopolysaccharide in mice. Clin. Exp. Immunol., 128, 221-228.
4. Andersson, P.B., Perry, V.H. & Gordon, S. (1992) The acute inflammatory response to lipopolysaccharide in CNS parenchyma differs from that in other body tissues. Neuroscience, 48, 169-186.
5. Anthony, D.C., Bolton, S.J., Fearn, S. & Perry, V.H. (1997) Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats. Brain, 120, 435-444.
6. Anthony, D.C. & Campbell, S.J. (2003) Developmental influences on inflammation in the brain. In Rothwell, N.J.L.S., (Ed), Immune and Inflammatory Responses in the Central Nervous System, 2nd Edn. Oxford University Press, Oxford pp. 1-13.
7. Anthony, D., Dempster, R., Fearn, S., Clements, J., Wells, G., Perry, V.H. & Walker, K. (1998) CXC chemokines generate age-related increases in neutrophil-mediated brain inflammation and blood-brain barrier breakdown. Curr. Biol., 8, 923-926.
8. Bartholdi, D. & Schwab, M.E. (1997) Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: An in situ hybridization study. Eur. J. Neurosci., 9, 1422-1438.
9. Bastide, M., Gele, P., Petrault, O., Pu, Q., Caliez, A., Robin, E., Deplanque, D., Duriez, P. & Bordet, R. (2003) Delayed cerebrovascular protective effect of lipopolysaccharide in parallel to brain ischemic tolerance. J. Cereb. Blood Flow Metab., 23, 399-405.
10. Beeson, P. (1946) Development of tolerance to typhoid bacterial pyrogen and its abolition by reticuloendothelial blockade. Soc. Exp. Biol. Med., 61, 248-250.
11. Bernardes-Silva, M., Anthony, D.C., Issekutz, A.C. & Perry, V.H. (2001) Recruitment of neutrophils across the blood-brain barrier: the role of E- and P-selectins. J. Cereb. Blood Flow Metab., 21, 1115-1124.
12. Blond, D., Campbell, S.J., Butchart, A.G., Perry, V.H. & Anthony, D.C. (2002) Differential induction of interleukin-1 beta and tumour necrosis factor-alpha may account for specific patterns of leukocyte recruitment in the brain. Brain Res., 958, 89-99.
13. Boche, D., Cunningham, C., Gauldie, J. & Perry, V.H. (2003) Transforming growth factor-beta 1-mediated neuroprotection against excitotoxic injury in vivo. J. Cereb. Blood Flow Metab., 23, 1174-1182.
14. Bordet, R., Deplanque, D., Maboudou, P., Puisieux, F., Pu, Q., Robin, E., Martin, A., Bastide, M., Leys, D., Lhermitte, M. & Dupuis, B. (2000) Increase in endogenous brain superoxide dismutase as a potential mechanism of lipopolysaccharide-induced brain ischemic tolerance. J. Cereb. Blood Flow Metab., 20, 1190-1196.
15. Campbell, S.J., Hughes, P.M., Iredale, J.P., Wilcockson, D.C., Waters, S., Docagne, F., Perry, V.H. & Anthony, D.C. (2003) CINC-1 is identified as an acute-phase protein induced by focal brain injury causing leukocyte mobilization and liver injury. FASEB J., 17, 1168-1170.
16. Campbell, S.J., Perry, V.H., Pitossi, F.J., Butchart, A.G., Chertoff, M., Waters, S., Dempster, R. & Anthony, D.C. (2005) Central nervous system injury triggers hepatic CC and CXC chemokine expression that is associated with leukocyte mobilization and recruitment to both the central nervous system and the liver. Am. J. Pathol., 166, 1487-1497.
17. Combrinck, M.I., Perry, V.H. & Cunningham, C. (2002) Peripheral infection evokes exaggerated sickness behaviour in pre-clinical murine prion disease. Neuroscience, 112, 7-11.
18. De La Garza, R. 2nd (2005) Endotoxin- or pro-inflammatory cytokine-induced sickness behavior as an animal model of depression: focus on anhedonia. Neurosci. Biobehav. Rev., 29, 761-770.
19. Dobrovolskaia, M.A., Medvedev, A.E., Thomas, K.E., Cuesta, N., Toshchakov, V., Ren, T., Cody, M.J., Michalek, S.M., Rice, N.R. & Vogel, S.N. (2003) Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR 'homotolerance' versus 'heterotolerance' on NF-kappa B signaling pathway components. J. Immunol., 170, 508-519.
20. Eklind, S., Mallard, C., Arvidsson, P. & Hagberg, H. (2005) Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain. Pediatr. Res., 58, 112-116.
21. Fan, H. & Cook, J.A. (2004) Molecular mechanisms of endotoxin tolerance. J. Endotoxin Res., 10, 71-84.
22. de Haas, C.J., van Leeuwen, E.M., van Bommel, T., Verhoef, J., van Kessel, K.P. & van Strijp, J.A. (2000) Serum amyloid P component bound to gram-negative bacteria prevents lipopolysaccharide-mediated classical pathway complement activation. Infect. Immun., 68, 1753-1759.
23. Jones, T.B., McDaniel, E.E. & Popovich, P.G. (2005) Inflammatory-mediated injury and repair in the traumatically injured spinal cord. Curr. Pharm. Des, 11, 1223-1236.
24. Liu, J., Ginis, I., Spatz, M. & Hallenbeck, J.M. (2000) Hypoxic preconditioning protects cultured neurons against hypoxic stress via TNF-alpha and ceramide. Am. J. Physiol. Cell Physiol., 278, C144-C153.
25. Loddick, S.A. & Rothwell, N.J. (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.
26. Matyszak, M.K. & Perry, V.H. (1995) Demyelination in the central nervous system following a delayed-type hypersensitivity response to bacillus Calmette-Guerin. Neuroscience, 64, 967-977.
27. Nawashiro, H., Tasaki, K., Ruetzler, C.A. & Hallenbeck, J.M. (1997) TNF-alpha pretreatment induces protective effects against focal cerebral ischemia in mice. J. Cereb. Blood Flow Metab., 17, 483-490.
28. Puisieux, F., Deplanque, D., Pu, Q., Souil, E., Bastide, M. & Bordet, R. (2000) Differential role of nitric oxide pathway and heat shock protein in preconditioning and lipopolysaccharide-induced brain ischemic tolerance. Eur. J. Pharmacol., 389, 71-78.
29. Qureshi, S.T., Lariviere, L., Leveque, G., Clermont, S., Moore, K.J., Gros, P. & Malo, D. (1999) Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J. Exp. Med., 189, 615-625.
30. Rosenzweig, H.L., Lessov, N.S., Henshall, D.C., Minami, M., Simon, R.P. & Stenzel-Poore, M.P. (2004) Endotoxin preconditioning prevents cellular inflammatory response during ischemic neuroprotection in mice. Stroke, 35, 2576-2581.
31. Saville, L.R., Pospisil, C.H., Mawhinney, L.A., Bao, F., Simedrea, F.C., Peters, A.A., O'Connell, P.J., Weaver, L.C. & Dekaban, G.A. (2004) A monoclonal antibody to CD11d reduces the inflammatory infiltrate into the injured spinal cord: a potential neuroprotective treatment. J. Neuroimmunol., 156, 42-57.
32. Schnell, L., Fearn, S., Schwab, M.E., Perry, V.H. & Anthony, D.C. (1999) Cytokine-induced acute inflammation in the brain and spinal cord. J. Neuropathol. Exp. Neurol., 58, 245-254.
33. Stroemer, R.P. & Rothwell, N.J. (1998) Exacerbation of ischemic brain damage by localized striatal injection of interleukin-1beta in the rat. J. Cereb. Blood Flow Metab., 18, 833-839.
34. Subramaniam, S., Stansberg, C. & Cunningham, C. (2004) The interleukin 1 receptor family. Dev. Comp. Immunol., 28, 415-428.
35. Tanno, H., Nockels, R.P., Pitts, L.H. & Noble, L.J. (1992) Breakdown of the blood-brain barrier after fluid percussion brain injury in the rat: Part 2: Effect of hypoxia on permeability to plasma proteins. J. Neurotrauma, 9, 335-347.
36. Tasaki, K., Ruetzler, C.A., Ohtsuki, T., Martin, D., Nawashiro, H. & Hallenbeck, J.M. (1997) Lipopolysaccharide pre-treatment induces resistance against subsequent focal cerebral ischemic damage in spontaneously hypertensive rats. Brain Res., 748, 267-270.
37. Tobias, P.S., Soldau, K., Gegner, J.A., Mintz, D. & Ulevitch, P.J. (1995) Lipopolysaccharide binding protein-mediated complexation of lipopolysaccharide with soluble CD14. J. Biol. Chem., 270, 10482-10488.
38. Toyoda, T., Kassell, N.F. & Lee, K.S. (2000) Induction of tolerance against ischemia/reperfusion injury in the rat brain by preconditioning with the endotoxin analog diphosphoryl lipid A. J. Neurosurg., 92, 435-441.
39. Wang, C.X., Olschowka, J.A. & Wrathall, J.R. (1997) Increase of interleukin-1 beta mRNA and protein in the spinal cord following experimental traumatic injury in the rat. Brain Res., 759, 190-196.
40. Wheeler, R.D., Young, E.A., Rothwell, N.J., Hall, M.D. & Luheshi, G.N. (2003) Up-regulation of IL-18 BP, but not IL-18 mRNA in rat liver by LPS. Cytokine, 21, 161-166.
41. Wright, J.L. & Merchant, R.E. (1994) Blood-brain barrier changes following intracerebral injection of human recombinant tumor necrosis factor-alpha in the rat. J. Neurooncol., 20, 17-25.
42. Yamasaki, Y., Matsuura, N., Shozuhara, H., Onodera, H., Itoyama, Y. & Kogure, K. (1995) Interleukin-1 as a pathogenetic mediator of ischemic brain damage in rats. Stroke, 26, 676-680; discussion 681.
43. Zarember, K.A. & Godowski, P.J. (2002) Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J. Immunol., 168, 554-561.
44. Zimmermann, C., Ginis, I., Furuya, K., Klimanis, D., Ruetzler, C., Spatz, M. & Hallenbeck, J.M. (2001) Lipopolysaccharide-induced ischemic tolerance is associated with increased levels of ceramide in brain and in plasma. Brain Res., 895, 59-65.