Endothelial activation and chemoattractant expression are early processes in isolated blast brain injury

NeuroMolecular Medicine

Volumn 16, Issue 3, 2014, Pages 606-619

  Risdall, Jane E ^a   Carter, Alun J ^b   Kirkman, Emrys ^b   Watts, Sarah A ^b   Taylor, Christopher ^b   Menon, David K ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b Biomedical Sciences   (United Kingdom)

Author keywords

Blast; Cerebral inflammation; Cytokines; Endothelial integrins; Traumatic brain injury

Indexed keywords

CCL2 PROTEIN, RAT; CELL ADHESION MOLECULE; CYTOKINE; ERYTHROPOIETIN; INTEGRIN; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL; BIOSYNTHESIS; BLAST INJURY; BRAIN INJURIES; ENCEPHALITIS; GENE EXPRESSION REGULATION; GENETICS; HEMODYNAMICS; MALE; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; RAT; T LYMPHOCYTE; VASCULAR ENDOTHELIUM; WISTAR RAT;

ANIMALS; BLAST INJURIES; BRAIN INJURIES; CELL ADHESION MOLECULES; CHEMOKINE CCL2; CHEMOTAXIS, LEUKOCYTE; CYTOKINES; ENCEPHALITIS; ENDOTHELIUM, VASCULAR; ERYTHROPOIETIN; GENE EXPRESSION REGULATION; HEMODYNAMICS; INTEGRINS; MALE; RANDOM ALLOCATION; RATS; RATS, WISTAR; T-LYMPHOCYTES;

EID: 84906083217     PISSN: 15351084     EISSN: 15591174     Source Type: Journal    
DOI: 10.1007/s12017-014-8313-y     Document Type: Article

References (65)

1. Babcock, A. A., Kuziel, W. A., Rivest, S., & Owens, T. (2003). Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. [Research Support, Non-U.S. Gov't]. Journal of Neuroscience, 23(21), 7922-7930.
2. Bauman, R. A., Ling, G., Tong, L., Januszkiewicz, A., Agoston, D., Delanerolle, N., et al. (2009). An introductory characterization of a combat-casualty-care relevant swine model of closed head injury resulting from exposure to explosive blast. Journal of Neurotrauma, 26(6), 841-860. doi: 10.1089/neu.2009-0898.
3. Camous, L., Roumenina, L., Bigot, S., Fremeaux-Bacchi, V., Lesavre, P., & Halbwachs-Mecarelli, L. (2011). Complement alternative pathway acts as a positive feedback amplification of neutrophil activation. Blood, 117(4), 1340-1349. doi: 10.1182/blood-2010-05-283564.
4. Carlos, T. M., Clark, R. S., Franicola-Higgins, D., Schiding, J. K., & Kochanek, P. M. (1997). Expression of endothelial adhesion molecules and recruitment of neutrophils after traumatic brain injury in rats. [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.]. Journal of Leukocyte Biology, 61(3), 279-285.
5. Cernak, I. (2010). The importance of systemic response in the pathobiology of blast-induced neurotrauma. Frontiers of Neurology, 1, 151. doi: 10.3389/fneur.2010.00151.
6. Cernak, I., Merkle, A. C., Koliatsos, V. E., Bilik, J. M., Luong, Q. T., Mahota, T. M., et al. (2011). The pathobiology of blast injuries and blast-induced neurotrauma as identified using a new experimental model of injury in mice. [Research Support, Non-U.S. Gov't Validation Studies]. Neurobiology of Disease, 41(2), 538-551. doi: 10.1016/j.nbd.2010.10.025.
7. Cernak, I., & Noble-Haeusslein, L. J. (2010). Traumatic brain injury: An overview of pathobiology with emphasis on military populations. Journal of Cerebral Blood Flow and Metabolism, 30, 255-266. doi: 10.1038/jcbfm.2009.203.
8. Cernak, I., Stoica, B., Byrnes, K. R., Di Giovanni, S., & Faden, A. I. (2005). Role of the cell cycle in the pathobiology of central nervous system trauma. [Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.]. Cell Cycle, 4(9), 1286-1293.
9. Cernak, I., Wang, Z., Jiang, J., Bian, X., & Savic, J. (2001). Ultrastructural and functional characteristics of blast injury-induced neurotrauma. Journal of Trauma, 50(4), 695-706.
10. Chen, Y., Hallenbeck, J. M., Ruetzler, C., Bol, D., THomas, K., Berman, N. E. J., et al. (2003). Overexpression of monocyte chemoattractant protein 1 in the brain exacerbates ischemic brain injury and is associated with recruitment of inflammatory cells. Journal of Cerebral Blood Flow and Metabolism, 23, 748-755. doi: 10.1097/01.WBC.0000071885.63724.20.
11. Chong, Z. Z., Kang, J. Q., & Maiese, K. (2002). Hematopoietic factor erythropoietin fosters neuroprotection through novel signal transduction cascades. Journal of Cerebral Blood Flow and Metabolism, 22, 503-514.
12. Courtney, A. C., & Courtney, M. W. (2009). A thoracic mechanism of mild traumatic brain injury due to blast pressure waves. Medical Hypotheses, 72, 76-83. doi: 10.1016/j.mehy.2008.09.015.
13. Cox, A. L., Coles, A. J., Nortje, J., Bradley, P. G., Chatfield, D. A., Thompson, S. J., et al. (2006). An investigation of auto-reactivity after head injury. Journal of Neuroimmunology, 174, 180-186. doi: 10.1016/j.jneuroim.2006. 01.007.
14. Dalgard, C. L., Cole, J. T., Kean, W. S., Lucky, J. J., Sukumar, G., McMullen, D. C., et al. (2012). The cytokine temporal profile in rat cortex after controlled cortical impact. Frontiers in Molecular Neuroscience, 5, 6. doi: 10.3389/fnmol.2012.00006.
15. Dalle Lucca, J. J., Chavko, M., Dubick, M. A., Adeeb, S., Falabella, M. J., Slack, J. L., et al. (2012). Blast-induced moderate neurotrauma (BINT) elicits early complement activation and tumor necrosis factor alpha (TNFalpha) release in rat brain. Journal of Neurological Science, 318, 146-154. doi: 10.1016/jns.2012.02.002.
16. Digicaylioglu, M., & Lipton, S. A. (2001). Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature, 412(6847), 641-647.
17. Dimitrijevic, O. B., Stamatovic, S. M., Keep, R. F., & Andjelkovic, A. V. (2007). Absence of the chemokine receptor CCR2 protects against cerebral ischemia/reperfusion injury in mice. [Research Support, N.I.H., Extramural]. Stroke, 38(4), 1345-1353. doi: 10.1161/01.STR.0000259709.16654.8f.
18. Feuerstein, G. Z., Wang, X., & Barone, F. C. (1998). The role of cytokines in the neuropathology of stroke and neurotrauma. [Review]. NeuroImmunoModulation, 5(3-4), 143-159.
19. Gentleman, S. M., Leclercq, P. D., Moyes, L., Graham, D. I., Smith, C., Griffin, W. S., et al. (2004). Long-term intracerebral inflammatory response after traumatic brain injury. [Research Support, N.I.H., Extramural]. Forensic Science International, 146(2-3), 97-104. doi: 10.1016/j.forsciint.2004.06.027.
20. Glabinski, A. R., Balasingam, V., Tani, M., Kunkel, S. L., Strieter, R. M., Yong, V. W., et al. (1996). Chemokine monocyte chemoattractant protein-1 is expressed by astrocytes after mechanical injury to the brain. [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.]. Journal of Immunology, 156(11), 4363-4368.
21. Goldstein, L. E., Fisher, A. M., Tagge, C. A., Zhang, X. L., Velisek, L., Sullivan, J. A., et al. (2012). Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.]. Science Translational Medicine, 4(134), 134ra160. doi: 10.1126/scitranslmed.3003716.
22. Guy, R. J., Kirkman, E., Watkins, P. E., & Cooper, G. J. (1998). Physiologic responses to primary blast. Journal of Trauma, 45(6), 983-987.
23. Hailer, N. P. (2008). Immunosuppression after traumatic or ischemic CNS damage: It is neuroprotective and illuminates the role of microglial cells. [Review]. Progress of Neurobiology, 84(3), 211-233. doi: 10.1016/j.pneurobio. 2007.12.001.
24. Helmy, A., Carpenter, K. L. H., Menon, D. K., Pickard, J. D., & Hutchinson, P. J. A. (2011). The cytokine response to human traumatic brain injury: Temporal profiles and evidence for cerebral parenchymal production. Journal of Cerebral Blood Flow and Metabolism, 31, 658-670. doi: 10.1038/jcbfm2010.142.
25. Hutchinson, P. J., O'Connell, M. T., Rothwell, N. J., Hopkins, S. J., Nortje, J., Carpenter, K. L., et al. (2007). Inflammation in human brain injury: intracerebral concentrations of IL-1alpha, IL-1beta, and their endogenous inhibitor IL-1ra. [Research Support, Non-U.S. Gov't]. Journal of Neurotrauma, 24(10), 1545-1557. doi: 10.1089/neu.2007.0295.
26. Isaksson, J., Lewen, A., Hillered, L., & Olsson, Y. (1997). Up-regulation of intercellular adhesion molecule 1 in cerebral microvessels after cortical contusion trauma in a rat model. [Comparative Study Research Support, Non-U.S. Gov't]. Acta Neuropathologica, 94(1), 16-20.
27. Jaffin, J. H., McKinney, L., Kinney, R. C., Cunningham, J. A., Moritz, D. M., Kraimer, J. M., et al. (1987). A laboratory model for studying blast overpressure injury. Journal of Trauma, 27(4), 349-356.
28. Kato, K., Fujimura, M., Nakagawa, A., Saito, A., Ohki, T., Takayama, K., et al. (2007). Pressure-dependent effect of shock waves on rat brain: Induction of neuronal apoptosis mediated by a caspase-dependent pathway. Journal of Neurosurgery, 106(4), 667-676. doi: 10.3171/jns.2007.106.4.667.
29. Knoblach, S. M., Fan, L., & Faden, A. I. (1999). Early neuronal expression of tumor necrosis factor-alpha after experimental brain injury contributes to neurological impairment. [Research Support, U.S. Gov't, P.H.S.]. Journal of Neuroimmunology, 95(1-2), 115-125.
30. Lee, S. J., & Benveniste, E. N. (1999). Adhesion molecule expression and regulation on cells of the central nervous system. [Research Support, U.S. Gov't, P.H.S. Review]. Journal of Neuroimmunology, 98(2), 77-88.
31. Leow-Dyke, S., Allen, C., Denes, A., Nilsson, O., Maysami, S., Bowie, A. G., et al. (2012). Neuronal toll-like receptor 4 signaling induces brain endothelial activation and neutrophil transmigration in vitro. Journal of Neuroinflammation, 9, 230. doi: 10.1186/1742-2094-9-230.
32. Lin, F. K., Suggs, S., Lin, C. H., Browne, J. K., Smalling, R., Egrie, J. C., et al. (1985). Cloning and expression of the human erythropoietin gene. Proceedings of the National Academy of Sciences USA, 82, 7580-7584.
33. McKeating, E. G., Andrews, P. J., & Mascia, L. (1998). Leukocyte adhesion molecule profiles and outcome after traumatic brain injury. Acta Neurochirurgica Supplement, 71, 200-202.
34. Mellor, S. G. (1988). The pathogenesis of blast injury and its management. British Journal of Hospital Medicine, 39(6), 536-539.
35. Moss, W. C., King, M. J., & Blackman, E. G. (2009). Skull flexure from blast waves: A mechanism for brain injury with implications for helmet design. Physical Review Letters, 103(10), 108702.
36. Mukherjee, S., Katki, K., Arisi, G. M., Foresti, M. L., & Shapiro, L. A. (2011). EarlyTBI-induced cytokine alterations are similarly detected by two distinct methods of multiplex assay. Frontiers in Molecular Neuroscience, 4, 1-7. doi: 10.3389/fnmol.2011.00021.
37. Muller, M., Carter, S., Hofer, M. J., & Campbell, I. L. (2010). Review: The chemokine receptor CXCR3 and its ligands CXCL9, CXCL10 and CXCL11 in neuroimmunity - a tale of conflict and conundrum. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review]. Neuropathology and Applied Neurobiology, 36(5), 368-387. doi: 10.1111/j.1365-2990.2010.01089.x.
38. Neumann, J., Sauerzweig, S., Rönicke, R., Gunzer, F., Dinkel, K., Ullrich, O., et al. (2008). Microglia cells protect neurons by direct engulfment of invading neutrophil granulocytes: A new mechanism of CNS immune privilege. The Journal of Neuroscience, 28(23), 5965-5975.
39. Ohnishi, M., Kirkman, E., Guy, R. J., & Watkins, P. E. (2001). Reflex nature of the cardiorespiratory response to primary thoracic blast injury in the anaesthetised rat. Experimental Physiology, 86(3), 357-364. doi: 10.1113/eph8602145.
40. Ponce, L. L., Navarro, J. C., Ahmed, O., & Robertson, C. S. (2013). Erythropoietin neuroprotection with traumatic brain injury. Pathophysiology, 20, 31-38. doi: 10.1016/j.pathophys.2012.02.005.
41. Rancan, M., Otto, V. I., Hans, V. H., Gerlach, I., Jork, R., Trentz, O., et al. (2001). Upregulation of ICAM-1 and MCP-1 but not of MIP-2 and sensorimotor deficit in response to traumatic axonal injury in rats. [Research Support, Non-U.S. Gov't]. Journal of Neuroscience Research, 63(5), 438-446.
42. Raza, S. S., Khan, M. M., Ahmad, A., Ashafaq, M., Khuwaja, G., Tabassum, R., et al. (2011). Hesperidin ameliorates functional and histological outcome and reduces neuroinflammation in experimental stroke. [Research Support, Non-U.S. Gov't]. Brain Research, 1420, 93-105. doi: 10.1016/j.brainres.2011.08. 047.
43. Reichel, C. A., Puhr-Westerheide, D., Zuchtriegel, G., Uhl, B., Berberich, N., Zahler, S., et al. (2012). C-C motif chemokine CCL3 and canonical neutrophil attractants promote neutrophil extravasation through common and distinct mechanisms. [Research Support, Non-U.S. Gov't]. Blood, 120(4), 880-890. doi: 10.1182/blood-2012-01-402164.
44. Rhind, S. G., Crnko, N. T., Baker, A. J., Morrison, L. J., Shek, P. N., Scarpelini, S., et al. (2010). Prehospital resuscitation with hypertonic saline-dextran modulates inflammatory, coagulation and endothelial activation marker profiles in severe traumatic brain injured patients. [Clinical Trial Randomized Controlled Trial Research Support, Non-U.S. Gov't]. Journal of Neuroinflammation, 7, 5. doi: 10.1186/1742-2094-7-5.
45. Risdall, J. E., & Menon, D. K. (2011). Traumatic brain injury. Philosophical Transactions of the Royal Society B, 366, 241-250. doi: 10.1098/rstb.20.10.0230.
46. Risling, M., Plantman, S., Angeria, M., Rostami, E., Bellander, B. M., Kirkegaard, M., et al. (2011). Mechanisms of blast induced brain injuries, experimental studies in rats. [Research Support, Non-U.S. Gov't]. Neuroimage, 54(Suppl 1), S89-s97. doi: 10.1016/j.neuroimage.2010.05.031.
47. Sawdon, M., Ohnishi, M., Watkins, P. E., & Kirkman, E. (2002). The effects of primary thoracic blast injury and morphine on the response to haemorrhage in the anaesthetised rat. Experimental Physiology, 87(6), 683-689.
48. Schultzberg, M., Lindberg, C., Aronsson, A. F., Hjorth, E., Spulber, S. D., & Oprica, M. (2007). Inflammation in the nervous system - physiological and pathophysiological aspects. [Research Support, Non-U.S. Gov't]. Physiology & Behavior, 92(1-2), 121-128. doi: 10.1016/j.physbeh.2007.05.050.
49. Schwartz, M., London, A., & Shechter, R. (2009). Boosting T-call immunity as a therapeutic approach for neurodegenerative conditions: The role of innate immunity. Neuroscience, 158, 1133-1142. doi: 10.1016/j.neuroscience. 2008.12.013.
50. Scouten, C. (2010). Frozen section technique in the animal research setting. In A. Practical (Ed.), Guide to frozen section technique. New York: Springer.
51. Semple, B. D., Bye, N., Rancan, M., Ziebell, J. M., & Morganti-Kossmann, M. C. (2010a). Role of CCL2 (MCP-1) in traumatic brain injury (TBI): Evidence from severe TBI patients and CCL2-/- mice. [Research Support, Non-U.S. Gov't]. Journal of Cerebral Blood Flow and Metabolism, 30(4), 769-782. doi: 10.1038/jcbfm.2009.262.
52. Semple, B. D., Frugier, T., & Morganti-Kossmann, M. C. (2010b). CCL2 modulates cytokine production in cultured mouse astrocytes. [Research Support, Non-U.S. Gov't]. Journal of Neuroinflammation, 7, 67. doi: 10.1186/1742-2094-7- 67.
53. Semple, B. D., Kossmann, T., & Morganti-Kossmann, M. C. (2010c). Role of chemokines in CNS health and pathology: A focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. [Research Support, Non-U.S. Gov't Review]. Journal of Cerebral Blood Flow and Metabolism, 30(3), 459-473. doi: 10.1038/jcbfm.2009.240.
54. Sewell, D., Nacewicz, B., Liu, F., Macvilay, S., Erdei, A., Lambris, J., et al. (2004). Complement C3 and C5 play critical roles in traumatic brain cryoinjury: Blocking effects on neutrophil extravasation by C5a receptor antagonist. Journal of Neuroimmunology, 155, 55-63. doi: 10.1016/j.jneuroim. 2004.06.003.
55. Shlosberg, D., Benifla, M., Kaufer, D., & Friedman, A. (2010). Blood-brain barrier breakdown as a therapeutic target in traumatic brain injury. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review]. Nature of Review Neurology, 6(7), 393-403. doi: 10.1038/nrneurol.2010.74.
56. Siren, A. L., Fratelli, M., Brines, M., Goemans, C., Casagrande, S., Lewczuk, P., et al. (2001). Erthropoietin prevents neuronal apoptosis after cerebral ischaemia and metabolic stress. Proceedings of the National Academy of Sciences USA, 98(7), 4044-4049.
57. Skaper, S. D. (2007). The brain as a target for inflammatory processes and neuroprotective strategies. [Review]. Annal of New York Academy of Science, 1122, 23-34. doi: 10.1196/annals.1403.002.
58. Sligh, J. E, Jr, Ballantyne, C. M., Rich, S. S., Hawkins, H. K., Smith, C. W., Bradley, A., et al. (1993). Inflammatory and immune responses are impaired in mice deficient in intercellular adhesion molecule 1. [Research Support, U.S. Gov't, P.H.S.]. Proceedings of the National Academy of Sciences USA, 90(18), 8529-8533.
59. Sola, A., Wen, T. C., Hamrick, S. E., & Ferriero, D. M. (2005). Potential for protection and repair following injury to the developing brain: A role for erythropoietin? Pediatric Research, 57(5 pt 2), 110R-117R.
60. Stamatovic, S. M., Shakui, P., Keep, R. F., Moore, B. B., Kunkel, S. L., Van Rooijen, N., et al. (2005). Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.]. Journal of Cerebral Blood Flow and Metabolism, 25(5), 593-606. doi: 10.1038/sj.jcbfm.9600055.
61. Szmydynger-Chodobska, J., Strazielle, N., Gandy, J. R., Keefe, T. H., Zink, B. J., Ghersi-Egea, J. F., et al. (2012). Posttraumatic invasion of monocytes across the blood-cerebrospinal fluid barrier. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't]. Journal of Cerebral Blood Flow and Metabolism, 32(1), 93-104. doi: 10.1038/jcbfm.2011.111.
62. Wang, H., Lynch, J. R., Song, P., Yang, H. J., Yates, R. B., Mace, B., et al. (2007). Simvastatin and atorvastatin improve behavioral outcome, reduce hippocampal degeneration, and improve cerebral blood flow after experimental traumatic brain injury. Experimental of Neurology, 206(1), 59-69. doi: 10.1016/j.expneurol.2007.03.031.
63. Wolf, S. J., Bebarta, V. S., Bonnett, C. J., Pons, P. T., & Cantrill, S. V. (2009). Blast injuries. [Review]. Lancet, 374(9687), 405-415. doi: 10.1016/S0140-6736(09)60257-9.
64. Yamamoto, Y., & Gaynor, R. B. (2001). Role of the NF-kappaB pathway in the pathogenesis of human disease states. Current Molecular Medicine, 1(3), 287-296.
65. Zuckerman, S. (1940). Experimental study of blast injuries to the lungs. Lancet, 2, 219-224.