Neuron death and inflammation in a rat model of intracerebral hemorrhage: Effects of delayed minocycline treatment

Brain Research

Volumn 1136, Issue 1, 2007, Pages 208-218

  Wasserman, Jason K ^a,b   Schlichter, Lyanne C ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Hemorrhage; Microglia; Minocycline; Neurodegeneration; Striatum; Stroke

Indexed keywords

MINOCYCLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN HEMORRHAGE; CELL DEATH; CONTROLLED STUDY; CORPUS STRIATUM; DRUG EFFICACY; DRUG MECHANISM; INFLAMMATION; MACROPHAGE ACTIVATION; MALE; MICROGLIA; NERVE CELL; NERVE CELL LESION; NERVE DEGENERATION; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RAT; THERAPY DELAY;

ANIMALS; BLOOD CIRCULATION; CELL COUNT; CELL DEATH; CEREBRAL HEMORRHAGE; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; FUNCTIONAL LATERALITY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MINOCYCLINE; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SPECTROPHOTOMETRY; TIME FACTORS;

RATTUS;

EID: 33846849030     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2006.12.035     Document Type: Article

References (64)

1. Andes D., and Craig W.A. Pharmacodynamics of the new des-f(6)-quinolone garenoxacin in a murine thigh infection model. Antimicrob. Agents Chemother. 47 (2003) 3935-3941
2. Arvin K.L., Han B.H., Du Y., Lin S.Z., Paul S.M., and Holtzman D.M. Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann. Neurol. 52 (2002) 54-61
3. Barone F.C., and Feuerstein G.Z. Inflammatory mediators and stroke: new opportunities for novel therapeutics. J. Cereb. Blood Flow Metab. 19 (1999) 819-834
4. Blum D., Chtarto A., Tenenbaum L., Brotchi J., and Levivier M. Clinical potential of minocycline for neurodegenerative disorders. Neurobiol. Dis. 17 (2004) 359-366
5. Castillo J., Davalos A., varez-Sabin J., Pumar J.M., Leira R., Silva Y., Montaner J., and Kase C.S. Molecular signatures of brain injury after intracerebral hemorrhage. Neurology 58 (2002) 624-629
6. Chan P.H. Reactive oxygen radicals in signaling and damage in the ischemic brain. J. Cereb. Blood Flow Metab. 21 (2001) 2-14
7. Choi S.H., Joe E.H., Kim S.U., and Jin B.K. Thrombin-induced microglial activation produces degeneration of nigral dopaminergic neurons in vivo. J. Neurosci. 23 (2003) 5877-5886
8. Colovic M., and Caccia S. Liquid chromatographic determination of minocycline in brain-to-plasma distribution studies in the rat. J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 791 (2003) 337-343
9. Cunningham L.A., Wetzel M., and Rosenberg G.A. Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia 50 (2005) 329-339
10. Del Bigio M.R., Yan H.J., Buist R., and Peeling J. Experimental intracerebral hemorrhage in rats. Magnetic resonance imaging and histopathological correlates. Stroke 27 (1996) 2312-2319
11. Diguet E., Gross C.E., Tison F., and Bezard E. Rise and fall of minocycline in neuroprotection: need to promote publication of negative results. Exp. Neurol. 189 (2004) 1-4
12. Fagan S.C., Edwards D.J., Borlongan C.V., Xu L., Arora A., Feuerstein G., and Hess D.C. Optimal delivery of minocycline to the brain: implication for human studies of acute neuroprotection. Exp. Neurol. 186 (2004) 248-251
13. Fan L.W., Lin S., Pang Y., Rhodes P.G., and Cai Z. Minocycline attenuates hypoxia-ischemia-induced neurological dysfunction and brain injury in the juvenile rat. Eur. J. Neurosci. 24 (2006) 341-350
14. Felberg R.A., Grotta J.C., Shirzadi A.L., Strong R., Narayana P., Hill-Felberg S.J., and Aronowski J. Cell death in experimental intracerebral hemorrhage: the "black hole" model of hemorrhagic damage. Ann. Neurol. 51 (2002) 517-524
15. Fisher M., and Ratan R. New perspectives on developing acute stroke therapy. Ann. Neurol. 53 (2003) 10-20
16. Fujii Y., Tanaka R., Takeuchi S., Koike T., Minakawa T., and Sasaki O. Hematoma enlargement in spontaneous intracerebral hemorrhage. J. Neurosurg. 80 (1994) 51-57
17. Gebel Jr. J.M., Jauch E.C., Brott T.G., Khoury J., Sauerbeck L., Salisbury S., Spilker J., Tomsick T.A., Duldner J., and Broderick J.P. Natural history of perihematomal edema in patients with hyperacute spontaneous intracerebral hemorrhage. Stroke 33 (2002) 2631-2635
18. Giuliani F., Metz L.M., Wilson T., Fan Y., Bar-Or A., and Yong V.W. Additive effect of the combination of glatiramer acetate and minocycline in a model of MS. J. Neuroimmunol. 158 (2005) 213-221
19. Gong C., Hoff J.T., and Keep R.F. Acute inflammatory reaction following experimental intracerebral hemorrhage in rat. Brain Res. 871 (2000) 57-65
20. Gong C., Boulis N., Qian J., Turner D.E., Hoff J.T., and Keep R.F. Intracerebral hemorrhage-induced neuronal death. Neurosurgery 48 (2001) 875-882
21. Hanisch U.K. Microglia as a source and target of cytokines. Glia 40 (2002) 140-155
22. Hewlett K.A., and Corbett D. Delayed minocycline treatment reduces long-term functional deficits and histological injury in a rodent model of focal ischemia. Neuroscience 141 (2006) 27-33
23. Jeong S.W., Chu K., Jung K.H., Kim S.U., Kim M., and Roh J.K. Human neural stem cell transplantation promotes functional recovery in rats with experimental intracerebral hemorrhage. Stroke 34 (2003) 2258-2263
24. Jian L.K., and Rosenberg G.A. Matrix metalloproteinases and free radicals in cerebral ischemia. Free Radical Biol. Med. 39 (2005) 71-80
25. Kazui S., Naritomi H., Yamamoto H., Sawada T., and Yamaguchi T. Enlargement of spontaneous intracerebral hemorrhage. Incidence and time course. Stroke 27 (1996) 1783-1787
26. Leira R., Davalos A., Silva Y., Gil-Peralta A., Tejada J., Garcia M., and Castillo J. Early neurologic deterioration in intracerebral hemorrhage: predictors and associated factors. Neurology 63 (2004) 461-467
27. Lind D., Franken S., Kappler J., Jankowski J., and Schilling K. Characterization of the neuronal marker NeuN as a multiply phosphorylated antigen with discrete subcellular localization. J. Neurosci. Res. 79 (2005) 295-302
28. Machado L.S., Kozak A., Ergul A., Hess D.C., Borlongan C.V., and Fagan S.C. Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci. 17 (2006) 56
29. MacLellan C.L., Girgis J., and Colbourne F. Delayed onset of prolonged hypothermia improves outcome after intracerebral hemorrhage in rats. J. Cereb. Blood Flow Metab. 24 (2004) 432-440
30. MacLellan C.L., Grams J., Adams K., and Colbourne F. Combined use of a cytoprotectant and rehabilitation therapy after severe intracerebral hemorrhage in rats. Brain Res. 1063 (2005) 40-47
31. MacLellan C.L., Auriat A.M., McGie S.C., Yan R.H., Huynh H.D., De Butte M.F., and Colbourne F. Gauging recovery after hemorrhagic stroke in rats: implications for cytoprotection studies. J. Cereb. Blood Flow Metab. 26 (2006) 1031-1042
32. MacLellan C.L., Davies L.M., Fingas M.S., and Colbourne F. The influence of hypothermia on outcome after intracerebral hemorrhage in rats. Stroke 37 (2006) 1266-1270
33. Maier C.M., Hsieh L., Crandall T., Narasimhan P., and Chan P.H. Evaluating therapeutic targets for reperfusion-related brain hemorrhage. Ann. Neurol. 59 (2006) 929-938
34. Matsushita K., Meng W., Wang X., Asahi M., Asahi K., Moskowitz M.A., and Lo E.H. Evidence for apoptosis after intercerebral hemorrhage in rat striatum. J. Cereb. Blood Flow Metab. 20 (2000) 396-404
35. Mayne M., Fotheringham J., Yan H.J., Power C., Del Bigio M.R., Peeling J., and Geiger J.D. Adenosine A2A receptor activation reduces proinflammatory events and decreases cell death following intracerebral hemorrhage. Ann. Neurol. 49 (2001) 727-735
36. Mayne M., Ni W., Yan H.J., Xue M., Johnston J.B., Del Bigio M.R., Peeling J., and Power C. Antisense oligodeoxynucleotide inhibition of tumor necrosis factor-alpha expression is neuroprotective after intracerebral hemorrhage. Stroke 32 (2001) 240-248
37. Morimoto N., Shimazawa M., Yamashima T., Nagai H., and Hara H. Minocycline inhibits oxidative stress and decreases in vitro and in vivo ischemic neuronal damage. Brain Res. 1044 (2005) 8-15
38. Mullen R.J., Buck C.R., and Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116 (1992) 201-211
39. Peeling J., Yan H.J., Chen S.G., Campbell M., and Del Bigio M.R. Protective effects of free radical inhibitors in intracerebral hemorrhage in rat. Brain Res. 795 (1998) 63-70
40. Peeling J., Del Bigio M.R., Corbett D., Green A.R., and Jackson D.M. Efficacy of disodium 4-[(tert-butylimino)methyl]benzene-1,3-disulfonate N-oxide (NXY-059), a free radical trapping agent, in a rat model of hemorrhagic stroke. Neuropharmacology 40 (2001) 433-439
41. Peeling J., Yan H.J., Corbett D., Xue M., and Del Bigio M.R. Effect of FK-506 on inflammation and behavioral outcome following intracerebral hemorrhage in rat. Exp. Neurol. 167 (2001) 341-347
42. Power C., Henry S., Del Bigio M.R., Larsen P.H., Corbett D., Imai Y., Yong V.W., and Peeling J. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann. Neurol. 53 (2003) 731-742
43. Qureshi A.I., Tuhrim S., Broderick J.P., Batjer H.H., Hondo H., and Hanley D.F. Spontaneous intracerebral hemorrhage. N. Engl. J. Med. 344 (2001) 1450-1460
44. Qureshi A.I., Suri M.F., Ostrow P.T., Kim S.H., Ali Z., Shatla A.A., Guterman L.R., and Hopkins L.N. Apoptosis as a form of cell death in intracerebral hemorrhage. Neurosurgery 52 (2003) 1041-1047
45. Rincon F., and Mayer S.A. Novel therapies for intracerebral hemorrhage. Curr. Opin. Crit. Care 10 (2004) 94-100
46. Saivin S., and Houin G. Clinical pharmacokinetics of doxycycline and minocycline. Clin. Pharmacokinet. 15 (1988) 355-366
47. Sarnat H.B., Nochlin D., and Born D.E. Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in early human fetal nervous system. Brain Dev. 20 (1998) 88-94
48. Schmued L.C., and Hopkins K.J. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 874 (2000) 123-130
49. Song E.C., Chu K., Jeong S.W., Jung K.H., Kim S.H., Kim M., and Yoon B.W. Hyperglycemia exacerbates brain edema and perihematomal cell death after intracerebral hemorrhage. Stroke 34 (2003) 2215-2220
50. Streit W.J. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40 (2002) 133-139
51. Streit W.J., Walter S.A., and Pennell N.A. Reactive microgliosis. Prog. Neurobiol. 57 (1999) 563-581
52. Szymanska A., Biernaskie J., Laidley D., Granter-Button S., and Corbett D. Minocycline and intracerebral hemorrhage: influence of injury severity and delay to treatment. Exp. Neurol. 197 (2006) 189-196
53. Tomas-Camardiel M., Rite I., Herrera A.J., de Pablos R.M., Cano J., Machado A., and Venero J.L. Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood-brain barrier, and damage in the nigral dopaminergic system. Neurobiol. Dis. 16 (2004) 190-201
54. Unal-Cevik I., Kilinc M., Gursoy-Ozdemir Y., Gurer G., and Dalkara T. Loss of NeuN immunoreactivity after cerebral ischemia does not indicate neuronal cell loss: a cautionary note. Brain Res. 1015 (2004) 169-174
55. Wang J., and Tsirka S.E. Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain 128 (2005) 1622-1633
56. Wang J., and Tsirka S.E. Tuftsin fragment 1-3 is beneficial when delivered after the induction of intracerebral hemorrhage. Stroke 36 (2005) 613-618
57. Wolf H.K., Buslei R., Schmidt-Kastner R., Schmidt-Kastner P.K., Pietsch T., Wiestler O.D., and Blumcke I. NeuN: a useful neuronal marker for diagnostic histopathology. J. Histochem. Cytochem. 44 (1996) 1167-1171
58. Wu D.C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D.K., Ischiropoulos H., and Przedborski S. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22 (2002) 1763-1771
59. Wu J., Hua Y., Keep R.F., Nakamura T., Hoff J.T., and Xi G. Iron and iron-handling proteins in the brain after intracerebral hemorrhage. Stroke 34 (2003) 2964-2969
60. Xu L., Fagan S.C., Waller J.L., Edwards D., Borlongan C.V., Zheng J., Hill W.D., Feuerstein G., and Hess D.C. Low dose intravenous minocycline is neuroprotective after middle cerebral artery occlusion-reperfusion in rats. BMC Neurol. 4 (2004) 7
61. Xue M., and Del Bigio M.R. Intracerebral injection of autologous whole blood in rats: time course of inflammation and cell death. Neurosci. Lett. 283 (2000) 230-232
62. Yong V.W., Wells J., Giuliani F., Casha S., Power C., and Metz L.M. The promise of minocycline in neurology. Lancet Neurol. 3 (2004) 744-751
63. Yrjanheikki J., Keinanen R., Pellikka M., Hokfelt T., and Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 15769-15774
64. Yrjanheikki J., Tikka T., Keinanen R., Goldsteins G., Chan P.H., and Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13496-13500