Microglial cells contribute to endogenous brain defenses after acute neonatal focal stroke

Journal of Neuroscience

Volumn 31, Issue 36, 2011, Pages 12992-13001

  Faustino, Joel V ^a   Wang, Xia ^a,b   Johnson, Cali E ^a   Klibanov, Alexander ^c   Derugin, Nikita ^a   Wendland, Michael F ^a   Vexler, Zinaida S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CD68 ANTIGEN; CLODRONIC ACID; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; GLUTATHIONE; INTERLEUKIN 18; INTERLEUKIN 1BETA; LIPOSOME; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ISCHEMIA; BRAIN LEVEL; CELL COUNT; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE RESISTANCE; FEMALE; INJURY SEVERITY; LIPID RAFT; MACROPHAGE; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL; NERVE CELL NECROSIS; NEUROPROTECTION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PHAGOCYTOSIS; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BRAIN; CASPASE 3; CELL DEATH; CHEMOKINES; CYTOKINES; ECHO-PLANAR IMAGING; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GLUTATHIONE; INFLAMMATION; LIPID METABOLISM; MAGNETIC RESONANCE IMAGING; MALE; MICROGLIA; PHAGOCYTOSIS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; STROKE;

EID: 80052561392     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2102-11.2011     Document Type: Article

References (42)

1. Aderem A (2002) How to eat something bigger than your head. Cell 110:5-8.
2. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, Pluchino S, Martino G, Schwartz M (2006) Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31:149-160.
3. Chéret C, Gervais A, Lelli A, Colin C, Amar L, Ravassard P, Mallet J, Cumano A, Krause KH, Mallat M (2008) Neurotoxic activation of microglia is promoted by a nox1-dependent NADPH oxidase. J Neurosci 28:12039-12051.
4. Cho S, Park EM, Febbraio M, Anrather J, Park L, Racchumi G, Silverstein RL, Iadecola C (2005) The class B scavenger receptor CD36 mediates free radical production and tissue injury in cerebral ischemia. J Neurosci 25:2504-2512.
5. Cuschieri J, Maier RV (2007) Oxidative stress, lipid rafts, and macrophage reprogramming. Antioxid Redox Signal 9:1485-1497.
6. Denker SP, Ji S, Lee SY, Dingman A, Derugin N, Wendland MF, Vexler ZS (2007) Macrophages are comprised of resident brain microglia not infiltrating peripheral monocytes acutely after neonatal stroke. J Neurochem 100:893-904
7. Derugin N, Ferriero DM, Vexler ZS (1998) Neonatal reversible focal cerebral ischemia: a new model. Neurosci Res 32:349-353.
8. Derugin N, Dingman A, Wendland MF, Fox C, Bollen A, Vexler ZS (2005) Magnetic resonance imaging as a surrogate measure for histological subchronic endpoint in a neonatal rat stroke model. Brain Res 1066:49-56.
9. Dingman A, Lee SY, Derugin N, Wendland MF, Vexler ZS (2006) Aminoguanidine inhibits caspase-3 and calpain activation without affecting microglial activation following neonatal transient ischemia. J Neurochem 96:1467-1479.
10. Doverhag C, Keller M, Karlsson A, Hedtjarn M, Nilsson U, Kapeller E, Sarkozy G, Klimaschewski L, Humpel C, Hagberg H, Simbruner G, Gressens P, Savman K (2008) Pharmacological and genetic inhibition of NADPH oxidase does not reduce brain damage in different models of perinatal brain injury in newborn mice. Neurobiol Dis 31:133-144.
11. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P, Lysiak JJ, Harden TK, Leitinger N, Ravichandran KS (2009) Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461:282-286.
12. Fullerton HJ, Ditelberg JS, Chen SF, Sarco DP, Chan PH, Epstein CJ, Ferriero DM (1998) Copper/zinc superoxide dismutase transgenic brain accumulates hydrogen peroxide after perinatal hypoxia ischemia. Ann Neurol 44:357-364.
13. Han BH, DeMattos RB, Dugan LL, Kim-Han JS, Brendza RP, Fryer JD, Kierson M, Cirrito J, Quick K, Harmony JA, Aronow BJ, Holtzman DM (2001) Clusterin contributes to caspase-3-independent brain injury following neonatal hypoxia-ischemia. Nat Med 7:338-343.
14. Haynes SE, Hollopeter G, Yang G, Kurpius D, Dailey ME, Gan WB, Julius D (2006) The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci 9:1512-1519.
15. Hedtjärn M, Mallard C, Hagberg H (2004) Inflammatory gene profiling in the developing mouse brain after hypoxia-ischemia. J Cereb Blood Flow Metab 24:1333-1351.
16. Helming L, Gordon S (2009) Molecular mediators of macrophage fusion. Trends Cell Biol 19:514-522.
17. Ikonomidou C, Mosinger JL, Salles KS, Labruyere J, Olney JW (1989) Sensitivity of the developing rat brain to hypobaric/ischemic damage parallels sensitivity to N-methyl-aspartate neurotoxicity. J Neurosci 9:2809-2818.
18. Imai F, Suzuki H, Oda J, Ninomiya T, Ono K, Sano H, Sawada M (2007) Neuroprotective effect of exogenous microglia in global brain ischemia. J Cereb Blood Flow Metab 27:488-500.
19. Jain A, Mårtensson J, Stole E, Auld PA, Meister A (1991) Glutathione deficiency leads to mitochondrial damage in brain. Proc Natl Acad Sci U S A 88:1913-1917.
20. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318.
21. Kunz A, Abe T, Hochrainer K, Shimamura M, Anrather J, Racchumi G, Zhou P, Iadecola C (2008) Nuclear factor-kappaB activation and postischemic inflammation are suppressed in CD36-null mice after middle cerebral artery occlusion. J Neurosci 28:1649-1658.
22. Lafemina MJ, Sheldon RA, Ferriero DM (2006) Acute hypoxia-ischemia results in hydrogen peroxide accumulation in neonatal but not adult mouse brain. Pediatr Res 59:680-683.
23. Lalancette-Hébert M, Gowing G, Simard A, Weng YC, Kriz J (2007) Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J Neurosci 27:2596-2605.
24. Lalancette-Hébert M, Moquin A, Choi AO, Kriz J, Maysinger D (2010) Lipopolysaccharide-QD micelles induce marked induction of TLR2 and lipid droplet accumulation in olfactory bulb microglia. Mol Pharm 7:1183-1194.
25. Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, Bluethmann H, Faergeman NJ, Meldgaard M, Deierborg T, Finsen B (2009) Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 29:1319-1330.
26. Lauber K, Bohn E, Kröber SM, Xiao YJ, Blumenthal SG, Lindemann RK, Marini P, Wiedig C, Zobywalski A, Baksh S, Xu Y, Autenrieth IB, Schulze-Osthoff K, Belka C, Stuhler G, Wesselborg S (2003) Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113:717-730.
27. Lauber K, Blumenthal SG, Waibel M, Wesselborg S (2004) Clearance of apoptotic cells: getting rid of the corpses. Mol Cell 14:277-287.
28. Lucas M, Stuart LM, Zhang A, Hodivala-Dilke K, Febbraio M, Silverstein R, Savill J, Lacy-Hulbert A (2006) Requirements for apoptotic cell contact in regulation of macrophage responses. J Immunol 177:4047-4054.
29. Mallat M, Marín-Teva JL, Chéret C (2005) Phagocytosis in the developing CNS: more than clearing the corpses. Curr Opin Neurobiol 15:101-107.
30. Manabat C, Han BH, Wendland M, Derugin N, Fox CK, Choi J, Holtzman DM, Ferriero DM, Vexler ZS (2003) Reperfusion differentially induces caspase-3 activation in ischemic core and penumbra after stroke in immature brain. Stroke 34:207-213.
31. Marín-Teva JL, Dusart I, Colin C, Gervais A, van Rooijen N, Mallat M (2004) Microglia promote the death of developing Purkinje cells. Neuron 41:535-547.
32. Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760-1765.
33. Petersen MA, Dailey ME (2004) Diverse microglial motility behaviors during clearance of dead cells in hippocampal slices. Glia 46:195-206.
34. Qiu H, Edmunds T, Baker-Malcolm J, Karey KP, Estes S, Schwarz C, Hughes H, Van Patten SM (2003) Activation of human acid sphingomyelinase through modification or deletion of C-terminal cysteine. J Biol Chem 278:32744-32752.
35. Santambrogio L, Belyanskaya SL, Fischer FR, Cipriani B, Brosnan CF, Ricciardi-Castagnoli P, Stern LJ, Strominger JL, Riese R (2001) Developmental plasticity of CNS microglia. Proc Natl Acad Sci U S A 98:6295-6300.
36. Schmitz G, Grandl M (2007) Role of redox regulation and lipid rafts in macrophages during Ox-LDL-mediated foam cell formation. Antioxid Redox Signal 9:1499-1518.
37. Sheldon RA, Jiang X, Francisco C, Christen S, Vexler ZS, Täuber MG, Ferriero DM (2004) Manipulation of antioxidant pathways in neonatal murine brain. Pediatr Res 56:656-662.
38. Szoka F Jr, Papahadjopoulos D (1978) Procedure for preparation of liposomes with large internal aqueous space and high capture by reversephase evaporation. Proc Natl Acad Sci U S A 75:4194-4198.
39. Vexler ZS, Wong A, Francisco C, Manabat C, Christen S, Täuber M, Ferriero DM, Gregory G (2003) Fructose-1,6-bisphosphate preserves intracellular glutathione and protects cortical neurons against oxidative stress. Brain Res 960:90-98.
40. Zhang AY, Yi F, Zhang G, Gulbins E, Li PL (2006) Lipid raft clustering and redox signaling platform formation in coronary arterial endothelial cells. Hypertension 47:74-80.
41. Zhang Y, Li X, Grassmé H, Döring G, Gulbins E (2010) Alterations in ceramide concentration and pH determine the release of reactive oxygen species by Cftr-deficient macrophages on infection. J Immunol 184:5104-5111.
42. Zito MA, Koennecke LA, McAuliffe MJ, McNally B, van Rooijen N, Heyes MP (2001) Depletion of systemic macrophages by liposome-encapsulated clodronate attenuates striatal macrophage invasion and neurodegeneration following local endotoxin infusion in gerbils. Brain Res 892:13-26.