Surgical manipulation compromises leukocyte mobilization responses and inflammation after experimental cerebral ischemia in mice

Frontiers in Neuroscience

Volumn , Issue 8 JAN, 2014, Pages

  Denes, Adam ^a,b   Pradillo, Jesus M ^a   Drake, Caroline ^a   Buggey, Hannah ^a   Rothwell, Nancy J ^a   Allan, Stuart M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Anaesthesia; Bone marrow; CXCR2; Experimental stroke; Granulocyte

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; CYTOKINE; ISOFLURANE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; BONE MARROW; BONE MARROW CELL; BRAIN TISSUE; CELL CULTURE; CHEMOPROPHYLAXIS; CONTROLLED STUDY; CRANIOTOMY; CXCR2+ GRANULOCYTE; CYTOKINE RESPONSE; DRUG ACTIVITY; EXPERIMENTAL CEREBRAL ISCHEMIA; EXPERIMENTAL STROKE; EXTRACRANIAL TISSUE; FOCAL CEREBRAL ISCHEMIA; GRANULOCYTE; GRANULOCYTE FUNCTION; GRANULOCYTE MOBILIZATION; IMMUNE DEFICIENCY; IN VITRO STUDY; INJURY SEVERITY; LEUKOCYTE ACTIVATION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOLECULAR INTERACTION; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OUTCOME ASSESSMENT; PROTECTION; SHAM PROCEDURE; SPLEEN; STROKE PATIENT; SURGICAL STRESS; TISSUE INJURY; VASCULAR PROTECTION;

EID: 84898023591     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00271     Document Type: Article

References (31)

1. Brait, V. H., Rivera, J., Broughton, B. R., Lee, S., Drummond, G. R., and Sobey, C. G. (2011). Chemokine-related gene expression in the brain following ischemic stroke: no role for CXCR2 in outcome. Brain Res. 1372, 169-179. doi: 10.1016/j.brainres.2010.11.087.
2. Carbo, C., Yuki, K., Demers, M., Wagner, D. D., and Shimaoka, M. (2013). Isoflurane inhibits neutrophil recruitment in the cutaneous Arthus reaction model. J. Anesth. 27, 261-268. doi: 10.1007/s00540-012-1508-1.
3. Chapman, K. Z., Dale, V. Q., Denes, A., Bennett, G., Rothwell, N. J., Allan, S. M., et al. (2009). A rapid and transient peripheral inflammatory response precedes brain inflammation after experimental stroke. J. Cereb. Blood Flow Metab. 29, 1764-1768. doi: 10.1038/jcbfm.2009.113.
4. Denes, A., Humphreys, N., Lane, T. E., Grencis, R., and Rothwell, N. (2010a). Chronic systemic infection exacerbates ischemic brain damage via a CCL5 (regulated on activation, normal T-cell expressed and secreted)-mediated proinflammatory response in mice. J. Neurosci. 30, 10086-10095. doi: 10.1523/JNEUROSCI.1227-10.2010.
5. Denes, A., Thornton, P., Rothwell, N. J., and Allan, S. M. (2010b). Inflammation and brain injury: acute cerebral ischaemia, peripheral and central inflammation. Brain Behav. Immun. 24, 708-723. doi: 10.1016/j.bbi.2009.09.010.
6. Denes, A., McColl, B. W., Leow-Dyke, S. F., Chapman, K. Z., Humphreys, N. E., Grencis, R. K., et al. (2011). Experimental stroke-induced changes in the bone marrow reveal complex regulation of leukocyte responses. J. Cereb. Blood Flow Metab. 31, 1036-1050. doi: 10.1038/jcbfm.2010.198.
7. Dirnagl, U., Klehmet, J., Braun, J. S., Harms, H., Meisel, C., Ziemssen, T., et al. (2007). Stroke-induced immunodepression: experimental evidence and clinical relevance. Stroke 38, 770-773. doi: 10.1161/01.STR.0000251441.89665.bc.
8. Eash, K. J., Greenbaum, A. M., Gopalan, P. K., and Link, D. C. (2010). CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J. Clin. Invest. 120, 2423-2431. doi: 10.1172/JCI41649.
9. Elenkov, I. J., Wilder, R. L., Chrousos, G. P., and Vizi, E. S. (2000). The sympathetic nerve-an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev. 52, 595-638.
10. Fisher, M., Feuerstein, G., Howells, D. W., Hurn, P. D., Kent, T. A., Savitz, S. I., et al. (2009). Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 40, 2244-2250. doi: 10.1161/STROKEAHA.108.541128.
11. Iadecola, C., and Anrather, J. (2011). The immunology of stroke: from mechanisms to translation. Nat. Med. 17, 796-808. doi: 10.1038/nm.2399.
12. Inada, T., Yamanouchi, Y., Jomura, S., Sakamoto, S., Takahashi, M., Kambara, T., et al. (2004). Effect of propofol and isoflurane anaesthesia on the immune response to surgery. Anaesthesia 59, 954-959. doi: 10.1111/j.1365-2044.2004.03837.x.
13. Kawaguchi, M., Furuya, H., and Patel, P. M. (2005). Neuroprotective effects of anesthetic agents. J. Anesth. 19, 150-156. doi: 10.1007/s00540-005-0305-5.
14. Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., and Altman, D. G. (2010). Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 8:e1000412. doi: 10.1371/journal.pbio.1000412.
15. Koedel, U., Merbt, U. M., Schmidt, C., Angele, B., Popp, B., Wagner, H., et al. (2007). Acute brain injury triggers MyD88-dependent, TLR2/4-independent inflammatory responses. Am. J. Pathol. 171, 200-213. doi: 10.2353/ajpath.2007.060821.
16. Leuschner, F., Rauch, P. J., Ueno, T., Gorbatov, R., Marinelli, B., Lee, W. W., et al. (2012). Rapid monocyte kinetics in acute myocardial infarction are sustained by extramedullary monocytopoiesis. J. Exp. Med. 209, 123-137. doi: 10.1084/jem.20111009.
17. Martin, C., Burdon, P. C., Bridger, G., Gutierrez-Ramos, J. C., Williams, T. J., and Rankin, S. M. (2003). Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 19, 583-593. doi: 10.1016/S1074-7613(03)00263-2.
18. Matzer, S. P., Rodel, F., Strieter, R. M., Rollinghoff, M., and Beuscher, H. U. (2004). Constitutive expression of CXCL2/MIP-2 is restricted to a Gr-1high, CD11b+, CD62Lhigh subset of bone marrow derived granulocytes. Int. Immunol. 16, 1675-1683. doi: 10.1093/intimm/dxh169.
19. McColl, B. W., Rothwell, N. J., and Allan, S. M. (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. doi: 10.1523/JNEUROSCI.5376-06.2007.
20. Murray, K. N., Buggey, H. F., Denes, A., and Allan, S. M. (2013). Systemic immune activation shapes stroke outcome. Mol. Cell. Neurosci. 53, 14-25. doi: 10.1016/j.mcn.2012.09.004.
21. Offner, H., Subramanian, S., Parker, S. M., Afentoulis, M. E., Vandenbark, A. A., and Hurn, P. D. (2006a). Experimental stroke induces massive, rapid activation of the peripheral immune system. J. Cereb. Blood Flow Metab. 26, 654-665. doi: 10.1038/sj.jcbfm.9600217.
22. Offner, H., Subramanian, S., Parker, S. M., Wang, C., Afentoulis, M. E., Lewis, A., et al. (2006b). Splenic atrophy in experimental stroke is accompanied by increased regulatory T cells and circulating macrophages. J. Immunol. 176, 6523-6531.
23. Pradillo, J. M., Denes, A., Greenhalgh, A. D., Boutin, H., Drake, C., McColl, B. W., et al. (2012). Delayed administration of interleukin-1 receptor antagonist reduces ischemic brain damage and inflammation in comorbid rats. J. Cereb. Blood Flow Metab. 32, 1810-1819. doi: 10.1038/jcbfm.2012.101.
24. Pradillo, J. M., Fernandez-Lopez, D., Garcia-Yebenes, I., Sobrado, M., Hurtado, O., Moro, M. A., et al. (2009). Toll-like receptor 4 is involved in neuroprotection afforded by ischemic preconditioning. J. Neurochem. 109, 287-294. doi: 10.1111/j.1471-4159.2009.05972.x.
25. Prass, K., Meisel, C., Hoflich, C., Braun, J., Halle, E., Wolf, T., et al. (2003). Stroke-induced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J. Exp. Med. 198, 725-736. doi: 10.1084/jem.20021098.
26. Smith, C. J., Lawrence, C. B., Rodriguez-Grande, B., Kovacs, K. J., Pradillo, J. M., and Denes, A. (2013). The immune system in stroke: clinical challenges and their translation to experimental research. J. Neuroimmune Pharmacol. 8, 867-887. doi: 10.1007/s11481-013-9469-1.
27. Swirski, F. K., Nahrendorf, M., Etzrodt, M., Wildgruber, M., Cortez-Retamozo, V., Panizzi, P., et al. (2009). Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325, 612-616. doi: 10.1126/science.1175202.
28. Veenstra, M., and Ransohoff, R. M. (2012). Chemokine receptor CXCR2: physiology regulator and neuroinflammation controller? J. Neuroimmunol. 246, 1-9. doi: 10.1016/j.jneuroim.2012.02.016.
29. Vogelgesang, A., Grunwald, U., Langner, S., Jack, R., Broker, B. M., Kessler, C., et al. (2008). Analysis of lymphocyte subsets in patients with stroke and their influence on infection after stroke. Stroke 39, 237-241. doi: 10.1161/STROKEAHA.107.493635.
30. White, J. R., Lee, J. M., Young, P. R., Hertzberg, R. P., Jurewicz, A. J., Chaikin, M. A., et al. (1998). Identification of a potent, selective non-peptide CXCR2 antagonist that inhibits interleukin-8-induced neutrophil migration. J. Biol. Chem. 273, 10095-10098. doi: 10.1074/jbc.273.17.10095.
31. Yuki, K., Bu, W., Xi, J., Sen, M., Shimaoka, M., and Eckenhoff, R. G. (2012). Isoflurane binds and stabilizes a closed conformation of the leukocyte function-associated antigen-1. FASEB J. 26, 4408-4417. doi: 10.1096/fj.12-212746.