Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain

Journal of Neuroscience

Volumn 27, Issue 10, 2007, Pages 2596-2605

  Lalancette Hébert, Mélanie ^a   Gowing, Geneviève ^a   Simard, Alain ^a   Yuan, Cheng Weng ^a   Kriz, Jasna ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Glia; Growth factor; Ischemia; Mice; Neuroinflammation; Neuroprotection; Transgenic

Indexed keywords

CD11B ANTIGEN; COLONY STIMULATING FACTOR 1; GALECTIN 3; GANCICLOVIR; GREEN FLUORESCENT PROTEIN; MUTANT PROTEIN; SOMATOMEDIN C; THYMIDINE KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN INJURY; BRAIN ISCHEMIA; BRAIN NERVE CELL; BRAIN SURGERY; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE EXACERBATION; ENCEPHALITIS; GENE MUTATION; HERPES SIMPLEX VIRUS; IMMUNOFLUORESCENCE TEST; IN VIVO STUDY; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; MYELOID PROGENITOR CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FOLDING;

ANIMALS; ANTIGENS, CD11B; ANTIVIRAL AGENTS; APOPTOSIS; BRAIN; BRAIN ISCHEMIA; CELL PROLIFERATION; CEREBRAL INFARCTION; CYTOKINES; CYTOPROTECTION; GALECTIN 3; GANCICLOVIR; INFLAMMATION MEDIATORS; INSULIN-LIKE GROWTH FACTOR I; MACROPHAGE COLONY-STIMULATING FACTOR; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; MUTATION; NEURONS; SIMPLEXVIRUS; THYMIDINE KINASE; TISSUE DISTRIBUTION;

EID: 33847785649     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5360-06.2007     Document Type: Article

References (51)

1. Allan SM, Rothwell NJ (2001) Cytokines and acute neurodegeneration. Nat Rev Neurosci 2:734-744.
2. Batchelor PE, Liberatore GT, Wong JY, Porritt MJ, Frerichs F, Donnan GA, Howells DW (1999) Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor. J Neurosci 19:1708-1716.
3. Beaulieu JM, Kriz J, Julien JP (2002) Induction of peripherin expression in subsets of brain neurons after lesion injury or cerebral ischemia. Brain Res 946:153-161.
4. Beilharz EJ, Russo VC, Butler G, Baker NL, Connor B, Sirimanne ES, Dragunow M, Werther GA, Gluckman PD, Williams CE, Scheepens A (1998) Co-ordinated and cellular specific induction of the components of the IGF/IGFBP axis in the rat brain following hypoxic-ischemic injury. Brain Res Mol Brain Res 59:119-134.
5. Belayev L, Busto R, Zhao W, Fernandez G, Ginsberg MD (1999) Middle cerebral artery occlusion in the mouse by intraluminal suture coated with poly-L-lysine: neurological and histological validation. Brain Res 833:181-190.
6. Berezovskaya O, Maysinger D, Fedoroff S (1996) Colony stimulating factor-1 potentiates neuronal survival in cerebral cortex ischemic lesion. Acta Neuropathol (Berl) 92:479-486.
7. Black ME, Newcomb TG, Wilson HM, Loeb LA (1996) Creation of drug-specific herpes simplex virus type 1 thymidine kinase mutants for gene therapy. Proc Natl Acad Sci USA 93:3525-3529.
8. Blondeau N, Widmann C, Lazdunski M, Heurteaux C (2001) Activation of the nuclear factor-κB is a key event in brain tolerance. J Neurosci 21:4668-4677.
9. Clemens JA, Stephenson DT, Smalstig EB, Dixon EP, Little SP (1997) Global ischemia activates nuclear factor-kappa B in forebrain neurons of rats. Stroke 28:1073-1080.
10. del Zoppo GJ, Becker KJ, Hallenbeck JM (2001) Inflammation after stroke: is it harmful? Arch Neurol 58:669-672.
11. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22:391-397.
12. Dong S, Hughes RC (1997) Macrophage surface glycoproteins binding to galectin-3 (Mac-2-antigen). Glycoconj J 14:267-274.
13. Fedoroff S, Berezovskaya O, Maysinger D (1997) Role of colony stimulating factor-1 in brain damage caused by ischemia. Neurosci Biobehav Rev 21:187-191.
14. Feuerstein GZ, Wang X (2001) Inflammation and stroke: benefits without harm? Arch Neurol 58:672-674.
15. Gibson CL, Coughlan TC, Murphy SP (2005) Glial nitric oxide and ischemia. Glia 50:417-426.
16. Gowing G, Vallieres L, Julien JP (2006) Mouse model for ablation of proliferating microglia in acute CNS injuries. Glia 53:331-337.
17. Guan J, Williams C, Gunning M, Mallard C, Gluckman P (1993) The effects of IGF-1 treatment after hypoxic-ischemic brain injury in adult rats. J Cereb Blood Flow Metab 13:609-616.
18. Hanisch UK (2002) Microglia as a source and target of cytokines. Glia 40:140-155.
19. Hill JK, Gunion-Rinker L, Kulhanek D, Lessov N, Kim S, Clark WM, Dixon MP, Nishi R, Stenzel-Poore MP, Eckenstein FP (1999) Temporal modulation of cytokine expression following focal cerebral ischemia in mice. Brain Res 820:45-54.
20. Imai F, Suzuki H, Oda J, Ninomiya T, Ono K, Sano H, Sawada M (2006) Neuroprotective effect of exogenous microglia in global brain ischemia. J Cereb Blood Flow Metab.
21. Kempermann G, Neumann H (2003) Neuroscience. Microglia: the enemy within? Science 302:1689-1690.
22. Kitamura Y, Takata K, Inden M, Tsuchiya D, Yanagisawa D, Nakata J, Taniguchi T (2004) Intracerebroventricular injection of microglia protects against focal brain ischemia. J Pharmacol Sci 94:203-206.
23. Kitamura Y, Yanagisawa D, Inden M, Takata K, Tsuchiya D, Kawasaki T, Taniguchi T, Shimohama S (2005) Recovery of focal brain ischemia-induced behavioral dysfunction by intracerebroventricular injection of microglia. J Pharmacol Sci 97:289-293.
24. Kriz J, Nguyen MD, Julien JP (2002) Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 10:268-278.
25. Kriz J, Gowing G, Julien JP (2003) Efficient three-drug cocktail for disease induced by mutant superoxide dismutase. Ann Neurol 53:429-436.
26. Ladeby R, Wirenfeldt M, Garcia-Ovejero D, Fenger C, Dissing-Olesen L, Dalmau I, Finsen B (2005) Microglial cell population dynamics in the injured adult central nervous system. Brain Res Brain Res Rev 48:196-206.
27. Laflamme N, Rivest S (1999) Effects of systemic immunogenic insults and circulating proinflammatory cytokines on the transcription of the inhibitory factor kappaB alpha within specific cellular populations of the rat brain. J Neurochem 73:309-321.
28. Lo EH, Dalkara T, Moskowitz MA (2003) Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4:399-415.
29. Mitrasinovic OM, Grattan A, Robinson CC, Lapustea NB, Poon C, Ryan H, Phong C, Murphy Jr GM (2005) Microglia overexpressing the macrophage colony-stimulating factor receptor are neuroprotective in a microglial- hippocampal organotypic coculture system. J Neurosci 25:4442-4451.
30. Miwa T, Furukawa S, Nakajima K, Furukawa Y, Kohsaka S (1997) Lipopolysaccharide enhances synthesis of brain-derived neurotrophic factor in cultured rat microglia. J Neurosci Res 50:1023-1029.
31. Nakajima K, Kohsaka S (2004) Microglia: neuroprotective and neurotrophic cells in the central nervous system. Curr Drug Targets Cardiovasc Haematol Disord 4:65-84.
32. Nedergaard M, Dirnagl U (2005) Role of glial cells in cerebral ischemia. Glia 50:281-286.
33. Neumann J, Gunzer M, Gutzeit HO, Ullrich O, Reymann KG, Dinkel K (2006) Microglia provide neuroprotection after ischemia. FASEB J 20:714-716.
34. Nguyen MD, Julien JP, Rivest S (2002) Innate immunity: the missing link in neuroprotection and neurodegeneration? Nat Rev Neurosci 3:216-227.
35. O'Donnell SL, Frederick TJ, Krady JK, Vannucci SJ, Wood TL (2002) IGF-I and microglia/macrophage proliferation in the ischemic mouse brain. Glia 39:85-97.
36. Offner H, Subramanian S, Parker SM, Afentoulis ME, Vandenbark AA, Hurn PD (2006) Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab 26:654-665.
37. Priller J, Flugel A, Wehner T, Boentert M, Haas CA, Prinz M, Fernandez-Klett F, Prass K, Bechmann I, de Boer BA, Frotscher M, Kreutzberg GW, Persons DA, Dirnagl U (2001) Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat Med 7:1356-1361.
38. Raivich G, Moreno-Flores MT, Muller JC, Kreutzberg GW (1994) Regulation of microglial proliferation: colony-stimulating factors and their receptors. Neuropathol Appl Neurobiol 20:209-211.
39. Raivich G, Jones LL, Werner A, Bluthmann H, Doetschmann T, Kreutzberg GW (1999a) Molecular signals for glial activation: pro- and anti-inflammatory cytokines in the injured brain. Acta Neurochir [Suppl] 73:21-30.
40. Raivich G, Bohatschek M, Kloss CU, Werner A, Jones LL, Kreutzberg GW (1999b) Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 30:77-105.
41. Rogove AD, Lu W, Tsirka SE (2002) Microglial activation and recruitment, but not proliferation, suffice to mediate neurodegeneration. Cell Death Differ 9:801-806.
42. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S (2006) Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49:489-502.
43. Stoll G, Jander S (1999) The role of microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol 58:233-247.
44. Stoll G, Jander S, Schroeter M (1998) Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 56:149-171.
45. Streit WJ (2002) Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40:133-139.
46. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580-2588.
47. Vincent VA, Selwood SP, Murphy Jr GM (2002) Proinflammatory effects of M-CSF and A beta in hippocampal organotypic cultures. Neurobiol Aging 23:349-362.
48. Wyss-Coray T, Mucke L (2002) Inflammation in neurodegenerative disease - a double-edged sword. Neuron 35:419-432.
49. Yoshida H, Hayashi S, Kunisada T, Ogawa M, Nishikawa S, Okamura H, Sudo T, Shultz LD, Nishikawa S (1990) The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345:442-444.
50. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chan PH, Koistinaho J (1999) A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 96:13496-13500.
51. Weng YC, Kriz J (2007) Differential neuroprotective effects of a minocycline-based drug cocktail in transient and permanent focal cerebral ischemia. Exp Neurol, in press.