In vivo temporal and spatial profile of leukocyte adhesion and migration after experimental traumatic brain injury in mice

Journal of Neuroinflammation

Volumn 10, Issue , 2013, Pages

  Schwarzmaier, Susanne M ^a,b   Zimmermann, Ricarda ^a   McGarry, Niamh B ^b   Trabold, Raimund ^a   Kim, Seong Woong ^a,b   Plesnila, Nikolaus ^a,b  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

Author keywords

2 photon microscopy; Brain trauma; In vivo; Inflammation; Intravital microscopy; Leukocyte adhesion; Leukocyte platelet aggregates; Leukocytes; Mice; Secondary brain damage

Indexed keywords

2 PHOTON MICROSCOPY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN CORTEX; BRAIN RADIOGRAPHY; CELL INTERACTION; CONTROLLED STUDY; ENDOTHELIUM CELL; FLUORESCENCE MICROSCOPY; IN VIVO STUDY; INTRAVITAL FLUORESCENCE MICROSCOPY; LEUKOCYTE ADHERENCE; LEUKOCYTE MIGRATION; MALE; MICROSCOPY; MOUSE; NEUROIMAGING; NONHUMAN; PIA ARTERY; THROMBOCYTE AGGREGATION; TRAUMATIC BRAIN INJURY; VASCULAR ENDOTHELIUM; VENULE;

ANIMALS; BRAIN INJURIES; CELL ADHESION; CELL MOVEMENT; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; MICROCIRCULATION; TIME FACTORS;

EID: 84874380718     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-10-32     Document Type: Article

References (59)

1. Feuerstein GZ, Wang X, Barone FC. Inflammatory gene expression in cerebral ischemia and trauma. Potential new therapeutic targets. Ann NY Acad Sci 1997, 825:179-193. 10.1111/j.1749-6632.1997.tb48428.x, 9369986.
2. van Buul JD, Hordijk PL. Signaling in leukocyte transendothelial migration. Arterioscler Thromb Vasc Biol 2004, 24:824-833. 10.1161/01.ATV.0000122854.76267.5c, 14976004.
3. Chopp M, Zhang RL, Chen H, Li Y, Jiang N, Rusche JR. Postischemic administration of an anti-Mac-1 antibody reduces ischemic cell damage after transient middle cerebral artery occlusion in rats. Stroke 1994, 25:869-875. 10.1161/01.STR.25.4.869, 8160235.
4. Zhang RL, Chopp M, Li Y, Zaloga C, Jiang N, Jones ML, Miyasaka M, Ward PA. Anti-ICAM-1 antibody reduces ischemic cell damage after transient middle cerebral artery occlusion in the rat. Neurology 1994, 44:1747-1751. 10.1212/WNL.44.9.1747, 7936308.
5. Soriano SG, Lipton SA, Wang YF, Xiao M, Springer TA, Gutierrez-Ramos JC, Hickey PR. Intercellular adhesion molecule-1-deficient mice are less susceptible to cerebral ischemia-reperfusion injury. Ann Neurol 1996, 39:618-624. 10.1002/ana.410390511, 8619547.
6. Soriano SG, Coxon A, Wang YF, Frosch MP, Lipton SA, Hickey PR, Mayadas TN. Mice deficient in Mac-1 (CD11b/CD18) are less susceptible to cerebral ischemia/reperfusion injury. Stroke 1999, 30:134-139. 10.1161/01.STR.30.1.134, 9880401.
7. Scallan J, Huxley VH, Korthuis RJ. Capillary Fluid Exchange: Regulation, Functions, and Pathology 2010, San Rafael (CA): Morgan & Claypool Life Sciences.
8. Zhuang J, Shackford SR, Schmoker JD, Anderson ML. The association of leukocytes with secondary brain injury. J Trauma 1993, 35:415-422. 10.1097/00005373-199309000-00014, 8371301.
9. Knoblach SM, Faden AI. Administration of either anti-intercellular adhesion molecule-1 or a nonspecific control antibody improves recovery after traumatic brain injury in the rat. J Neurotrauma 2002, 19:1039-1050. 10.1089/089771502760341956, 12482117.
10. Fee D, Crumbaugh A, Jacques T, Herdrich B, Sewell D, Auerbach D, Piaskowski S, Hart MN, Sandor M, Fabry Z. Activated/effector CD4+ T cells exacerbate acute damage in the central nervous system following traumatic injury. J Neuroimmunol 2003, 136:54-66. 10.1016/S0165-5728(03)00008-0, 12620643.
11. Utagawa A, Bramlett HM, Daniels L, Lotocki G, Dekaban GA, Weaver LC, Dietrich WD. Transient blockage of the CD11d/CD18 integrin reduces contusion volume and macrophage infiltration after traumatic brain injury in rats. Brain Res 2008, 1207:155-163. 2435262, 18374312.
12. Kenne E, Erlandsson A, Lindbom L, Hillered L, Clausen F. Neutrophil depletion reduces edema formation and tissue loss following traumatic brain injury in mice. J Neuroinflammation 2012, 9:17. 10.1186/1742-2094-9-17, 3292978, 22269349.
13. Hartl R, Medary M, Ruge M, Arfors KE, Ghajar J. Blood-brain barrier breakdown occurs early after traumatic brain injury and is not related to white blood cell adherence. Acta Neurochir Suppl 1997, 70:240-242.
14. Hartl R, Medary MB, Ruge M, Arfors KE, Ghajar J. Early white blood cell dynamics after traumatic brain injury: effects on the cerebral microcirculation. JCereb Blood Flow Metab 1997, 17:1210-1220.
15. Whalen MJ, Carlos TM, Kochanek PM, Clark RS, Heineman S, Schiding JK, Franicola D, Memarzadeh F, Lo W, Marion DW, Dekosky ST. Neutrophils do not mediate blood-brain barrier permeability early after controlled cortical impact in rats. J Neurotrauma 1999, 16:583-594. 10.1089/neu.1999.16.583, 10447070.
16. Whalen MJ, Carlos TM, Dixon CE, Robichaud P, Clark RS, Marion DW, Kochanek PM. Reduced brain edema after traumatic brain injury in mice deficient in P-selectin and intercellular adhesion molecule-1. J LeukocBiol 2000, 67:160-168.
17. Zweckberger K, Stoffel M, Baethmann A, Plesnila N. Effect of decompression craniotomy on increase of contusion volume and functional outcome after controlled cortical impact in mice. J Neurotrauma 2003, 20:1307-1314. 10.1089/089771503322686102, 14748979.
18. Schwarzmaier SM, Kim SW, Trabold R, Plesnila N. Temporal profile of thrombogenesis in the cerebral microcirculation after traumatic brain injury in mice. J Neurotrauma 2010, 27:121-130. 10.1089/neu.2009.1114, 19803784.
19. Kataoka H, Kim SW, Plesnila N. Leukocyte-endothelium interactions during permanent focal cerebral ischemia in mice. J Cereb Blood Flow Metab 2004, 24:668-676.
20. Thal SC, Plesnila N. Non-invasive intraoperative monitoring of blood pressure and arterial pCO2 during surgical anesthesia in mice. J Neurosci Methods 2007, 159:261-267. 10.1016/j.jneumeth.2006.07.016, 16945419.
21. Zweckberger K, Eros C, Zimmermann R, Kim SW, Engel D, Plesnila N. Effect of early and delayed decompressive craniectomy on secondary brain damage after controlled cortical impact in mice. J Neurotrauma 2006, 23:1083-1093. 10.1089/neu.2006.23.1083, 16866621.
22. Helmchen F, Denk W. Deep tissue two-photon microscopy. Nat Methods 2005, 2:932-940. 10.1038/nmeth818, 16299478.
23. Plesnila N, von Baumgarten L, Retiounskaia M, Engel D, Ardeshiri A, Zimmermann R, Hoffmann F, Landshamer S, Wagner E, Culmsee C. Delayed neuronal death after brain trauma involves p53-dependent inhibition of NF-kappaB transcriptional activity. Cell Death Differ 2007, 14:1529-1541. 10.1038/sj.cdd.4402159, 17464322.
24. Engel DC, Mies G, Terpolilli NA, Trabold R, Loch A, De Zeeuw CI, Weber JT, Maas AI, Plesnila N. Changes of cerebral blood flow during the secondary expansion of a cortical contusion assessed by 14C-iodoantipyrine autoradiography in mice using a non-invasive protocol. J Neurotrauma 2008, 25:739-753. 10.1089/neu.2007.0480, 18627253.
25. Groger M, Lebesgue D, Pruneau D, Relton J, Kim SW, Nussberger J, Plesnila N. Release of bradykinin and expression of kinin B2 receptors in the brain: role for cell death and brain edema formation after focal cerebral ischemia in mice. J Cereb Blood Flow Metab 2005, 25:978-989. 10.1038/sj.jcbfm.9600096, 15815587.
26. Kunkel EJ, Dunne JL, Ley K. Leukocyte arrest during cytokine-dependent inflammation in vivo. J Immunol 2000, 164:3301-3308.
27. Sahuquillo J, Poca MA, Amoros S. Current aspects of pathophysiology and cell dysfunction after severe head injury. Curr Pharm Des 2001, 7:1475-1503. 10.2174/1381612013397311, 11562294.
28. Morganti-Kossmann MC, Rancan M, Otto VI, Stahel PF, Kossmann T. Role of cerebral inflammation after traumatic brain injury: a revisited concept. Shock 2001, 16:165-177. 10.1097/00024382-200116030-00001, 11531017.
29. Shojo H, Kaneko Y, Mabuchi T, Kibayashi K, Adachi N, Borlongan CV. Genetic and histologic evidence implicates role of inflammation in traumatic brain injury-induced apoptosis in the rat cerebral cortex following moderate fluid percussion injury. Neuroscience 2010, 171:1273-1282. 10.1016/j.neuroscience.2010.10.018, 20950674.
30. McKeating EG, Andrews PJ, Mascia L. Leukocyte adhesion molecule profiles and outcome after traumatic brain injury. Acta Neurochir Suppl 1998, 71:200-202.
31. Morganti-Kossmann MC, Rancan M, Stahel PF, Kossmann T. Inflammatory response in acute traumatic brain injury: a double-edged sword. Curr Opin Crit Care 2002, 8:101-105. 10.1097/00075198-200204000-00002, 12386508.
32. Hall ED, Bryant YD, Cho W, Sullivan PG. Evolution of post-traumatic neurodegeneration after controlled cortical impact traumatic brain injury in mice and rats as assessed by the de Olmos silver and fluorojade staining methods. J Neurotrauma 2008, 25:235-247. 10.1089/neu.2007.0383, 18352837.
33. Harlan JM. Leukocyte-endothelial interactions. Blood 1985, 65:513-525.
34. Chen T, Liu W, Chao X, Zhang L, Qu Y, Huo J, Fei Z. Salvianolic acid B attenuates brain damage and inflammation after traumatic brain injury in mice. Brain Res Bull 2011, 84:163-168. 10.1016/j.brainresbull.2010.11.015, 21134421.
35. Qu C, Mahmood A, Ning R, Xiong Y, Zhang L, Chen J, Jiang H, Chopp M. The treatment of traumatic brain injury with velcade. J Neurotrauma 2010, 27:1625-1634. 10.1089/neu.2010.1359, 2966855, 20649468.
36. Whalen MJ, Carlos TM, Dixon CE, Schiding JK, Clark RS, Baum E, Yan HQ, Marion DW, Kochanek PM. Effect of traumatic brain injury in mice deficient in intercellular adhesion molecule-1: assessment of histopathologic and functional outcome. J Neurotrauma 1999, 16:299-309. 10.1089/neu.1999.16.299, 10225216.
37. Rothlein R. Overview of leukocyte adhesion. Neurology 1997, 49(Suppl 4):S3-S4.
38. Diamond MS, Springer TA. A subpopulation of Mac-1 (CD11b/CD18) molecules mediates neutrophil adhesion to ICAM-1 and fibrinogen. J Cell Biol 1993, 120:545-556. 10.1083/jcb.120.2.545, 2119505, 7678422.
39. Edens HA, Parkos CA. Modulation of epithelial and endothelial paracellular permeability by leukocytes. Adv Drug Deliv Rev 2000, 41:315-328. 10.1016/S0169-409X(00)00049-1, 10854689.
40. Johnson-Leger C, Aurrand-Lions M, Imhof BA. The parting of the endothelium: miracle, or simply a junctional affair?. J Cell Sci 2000, 113:921-933.
41. Elalamy I, Chakroun T, Gerotziafas GT, Petropoulou A, Robert F, Karroum A, Elgrably F, Samama MM, Hatmi M. Circulating platelet-leukocyte aggregates: a marker of microvascular injury in diabetic patients. Thromb Res 2008, 121:843-848. 10.1016/j.thromres.2007.07.016, 17825880.
42. He P, Zhang H, Zhu L, Jiang Y, Zhou X. Leukocyte-platelet aggregate adhesion and vascular permeability in intact microvessels: role of activated endothelial cells. Am J Physiol Heart CircPhysiol 2006, 291:H591-H599.
43. Lehr HA, Olofsson AM, Carew TE, Vajkoczy P, von Andrian UH, Hubner C, Berndt MC, Steinberg D, Messmer K, Arfors KE. P-selectin mediates the interaction of circulating leukocytes with platelets and microvascular endothelium in response to oxidized lipoprotein in vivo. Lab Invest 1994, 71:380-386.
44. Moore KL, Patel KD, Bruehl RE, Li F, Johnson DA, Lichenstein HS, Cummings RD, Bainton DF, McEver RP. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J Cell Biol 1995, 128:661-671. 10.1083/jcb.128.4.661, 2199883, 7532174.
45. Ishikawa M, Kusaka G, Yamaguchi N, Sekizuka E, Nakadate H, Minamitani H, Shinoda S, Watanabe E. Platelet and leukocyte adhesion in the microvasculature at the cerebral surface immediately after subarachnoid hemorrhage. Neurosurgery 2009, 64:546-553. 10.1227/01.NEU.0000337579.05110.F4, 19240618.
46. van der Sande JJ, Emeis JJ, Lindeman J. Intravascular coagulation: a common phenomenon in minor experimental head injury. J Neurosurg 1981, 54:21-25. 10.3171/jns.1981.54.1.0021, 7463116.
47. Holmin S, Soderlund J, Biberfeld P, Mathiesen T. Intracerebral inflammation after human brain contusion. Neurosurgery 1998, 42:291-298. 10.1097/00006123-199802000-00047, 9482179.
48. Clark RS, Schiding JK, Kaczorowski SL, Marion DW, Kochanek PM. Neutrophil accumulation after traumatic brain injury in rats: comparison of weight drop and controlled cortical impact models. J Neurotrauma 1994, 11:499-506. 10.1089/neu.1994.11.499, 7861443.
49. Carlos TM, Clark RS, Franicola-Higgins D, Schiding JK, Kochanek PM. Expression of endothelial adhesion molecules and recruitment of neutrophils after traumatic brain injury in rats. J Leukoc Biol 1997, 61:279-285.
50. Holmin S, Mathiesen T, Shetye J, Biberfeld P. Intracerebral inflammatory response to experimental brain contusion. Acta Neurochir(Wien) 1995, 132:110-119.
51. Soares HD, Hicks RR, Smith D, McIntosh TK. Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J Neurosci 1995, 15:8223-8233.
52. Arumugam TV, Salter JW, Chidlow JH, Ballantyne CM, Kevil CG, Granger DN. Contributions of LFA-1 and Mac-1 to brain injury and microvascular dysfunction induced by transient middle cerebral artery occlusion. Am J Physiol Heart Circ Physiol 2004, 287:H2555-H2560. 10.1152/ajpheart.00588.2004, 15308480.
53. Matsuo Y, Onodera H, Shiga Y, Shozuhara H, Ninomiya M, Kihara T, Tamatani T, Miyasaka M, Kogure K. Role of cell adhesion molecules in brain injury after transient middle cerebral artery occlusion in the rat. Brain Res 1994, 656:344-352. 10.1016/0006-8993(94)91478-8, 7820595.
54. Prestigiacomo CJ, Kim SC, Connolly ES, Liao H, Yan SF, Pinsky DJ. CD18-mediated neutrophil recruitment contributes to the pathogenesis of reperfused but not nonreperfused stroke. Stroke 1999, 30:1110-1117. 10.1161/01.STR.30.5.1110, 10229752.
55. Bramlett HM, Dietrich WD. Pathophysiology of cerebral ischemia and brain trauma: similarities and differences. J Cereb Blood Flow Metab 2004, 24:133-150.
56. Lighthall JW, Dixon CE, Anderson TE. Experimental models of brain injury. J Neurotrauma 1989, 6:83-97. 10.1089/neu.1989.6.83, 2671392.
57. Carbonell WS, Maris DO, McCall T, Grady MS. Adaptation of the fluid percussion injury model to the mouse. J Neurotrauma 1998, 15:217-229. 10.1089/neu.1998.15.217, 9528921.
58. Dietrich WD, Alonso O, Halley M. Early microvascular and neuronal consequences of traumatic brain injury: a light and electron microscopic study in rats. J Neurotrauma 1994, 11:289-301. 10.1089/neu.1994.11.289, 7996583.
59. Dixon CE, Clifton GL, Lighthall JW, Yaghmai AA, Hayes RL. A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Methods 1991, 39:253-262. 10.1016/0165-0270(91)90104-8, 1787745.