Resident microglia, rather than blood-derived macrophages, contribute to the earlier and more pronounced inflammatory reaction in the immature compared with the adult hippocampus after hypoxia-ischemia

GLIA

Volumn 63, Issue 12, 2015, Pages 2220-2230

  Umekawa, Takashi ^a,b   Osman, Ahmed M ^a   Han, Wei ^a   Ikeda, Tomoaki ^b   Blomgren, Klas ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

CCL2; Galectin 3; Hypoxic ischemic encephalopathy; Neuroinflammation

Indexed keywords

CD16 ANTIGEN; CD206 ANTIGEN; CD32 ANTIGEN; CELL ANTIGEN; GALECTIN 3; MONOCYTE CHEMOTACTIC PROTEIN 1; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; CALCIUM BINDING PROTEIN; CCR2 PROTEIN, MOUSE; CELL SURFACE RECEPTOR; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR2; CX3CR1 PROTEIN, HUMAN; FC RECEPTOR; FCGR2B PROTEIN, MOUSE; FCGR3 PROTEIN, MOUSE; KI 67 ANTIGEN; LECTIN; MANNOSE BINDING LECTIN; MANNOSE RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; BRAIN INJURY; CELL ACTIVATION; CELL COUNT; CELL MATURATION; CELL PROLIFERATION; ENCEPHALITIS; HIPPOCAMPUS; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MACROPHAGE; MALE; MICROGLIA; MOUSE; NEWBORN; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; TIME FACTOR; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; CALCIUM-BINDING PROTEINS; CELL COUNT; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HYPOXIA-ISCHEMIA, BRAIN; KI-67 ANTIGEN; LECTINS, C-TYPE; MACROPHAGES; MALE; MANNOSE-BINDING LECTINS; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MICROGLIA; RECEPTORS, CCR2; RECEPTORS, CELL SURFACE; RECEPTORS, CHEMOKINE; RECEPTORS, IGG; TIME FACTORS;

EID: 84943526945     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22887     Document Type: Article

References (33)

1. Biber K, Owens T, Boddeke E. 2014. What is microglia neurotoxicity (Not)? Glia 62:841-854.
2. Burguillos MA, Svensson M, Schulte T, Boza-Serrano A, Garcia-Quintanilla A, Kavanagh E, Santiago M, Viceconte N, Oliva-Martin MJ, Osman AM, Salomonsson E, Amar L, Persson A, Blomgren K, Achour A, Englund E, Leffler H, Venero JL, Joseph B, Deierborg T. 2015. Microglia-secreted galectin-3 acts as a toll-like receptor 4 ligand and contributes to microglial activation. Cell Rep. 10:1626-1638.
3. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee J-C, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM. 2006. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917-924.
4. Dénes Á, Ferenczi S, Halász J, Környei Z, Kovács KJ. 2008. Role of CX3CR1 (fractalkine receptor) in brain damage and inflammation induced by focal cerebral ischemia in mouse. J Cereb Blood Flow Metab 28:1707-1721.
5. Denker SP, Ji S, Dingman A, Lee SY, 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.
6. Fanselow MS, Dong H-W. 2010. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19.
7. Fernández-López D, Faustino J, Daneman R, Zhou L, Lee SY, Derugin N, Wendland MF, Vexler ZS. 2012. Blood-brain barrier permeability is increased after acute adult stroke but not neonatal stroke in the rat. J Neurosci 32:9588-9600.
8. Fernández-López D, Natarajan N, Ashwal S, Vexler ZS. 2014. Mechanisms of perinatal arterial ischemic stroke. J Cereb Blood Flow Metab 34:921-932.
9. Gliem M, Mausberg AK Lee J-I, Simiantonakis I, van Rooijen N, Hartung H-P Jander S. 2012. Macrophages prevent hemorrhagic infarct transformation in murine stroke models. Ann Neurol 71:743-752.
10. Gordon S, Taylor PR. 2005. Monocyte and macrophage heterogeneity. Nat Rev Immunol 5:953-964.
11. Hagberg H, Wilson MA, Matsushita H, Zhu C, Lange M, Gustavsson M, Poitras MF, Dawson TM, Dawson VL, Northington F, Johnston MV. 2004. PARP-1 gene disruption in mice preferentially protects males from perinatal brain injury. J Neurochem 90:1068-1075.
12. Hanisch U-K, Kettenmann H. 2007. Microglia: Active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394.
13. Hu X, Li P, Guo Y, Wang H, Leak RK, Chen S, Gao Y, Chen J. 2012. Microglia/macrophage polarization dynamics reveal novel mechanism of injury expansion after focal cerebral ischemia. Stroke 43:3063-3070.
14. Iadecola C, Anrather J. 2011. The immunology of stroke: From mechanisms to translation. Nat Med 17:796-808.
15. Ivacko JA, Sun R, Silverstein FS. 1996. Hypoxic-ischemic brain injury induces an acute microglial reaction in perinatal rats1. Pediatr Res 39:39-47.
16. Jin R, Yang G, Li G. 2010. Inflammatory mechanisms in ischemic stroke: Role of inflammatory cells. J Leukoc Biol 87:779-789.
17. Kadam SD, Chen H, Markowitz GJ, Raja S, George S, Shotwell E, Loechelt B, Johnston MV, Kamani N, Fatemi A, Comi AM. 2015. Systemic injection of CD34(+)-enriched human cord blood cells modulates poststroke neural and glial response in a sex-dependent manner in CD1 mice. Stem Cells Dev 24:51-66.
18. Lalancette-Hébert M, Swarup V, Beaulieu JM, Bohacek I, Abdelhamid E, Weng YC, Sato S, Kriz J. 2012. Galectin-3 is required for resident microglia activation and proliferation in response to ischemic injury. J Neurosci 32:10383-10395.
19. Li H, Li Q, Du X, Sun Y, Wang X, Kroemer G, Blomgren K, Zhu C. 2011. Lithium-mediated long-term neuroprotection in neonatal rat hypoxia-ischemia is associated with antiinflammatory effects and enhanced proliferation and survival of neural stem/progenitor cells. J Cereb Blood Flow Metab 31:2106-2115.
20. Li T, Pang S, Yu Y, Wu X, Guo J, Zhang S. 2013. Proliferation of parenchymal microglia is the main source of microgliosis after ischaemic stroke. Brain J Neurol 136:3578-3588.
21. Muramatsu K, Fukuda A, Togari H, Wada Y, Nishino H. 1997. Vulnerability to cerebral hypoxic-ischemic insult in neonatal but not in adult rats is in parallel with disruption of the blood-brain barrier. Stroke 28:2281-2289.
22. Osman AM, Zhou K, Zhu C, Blomgren K. 2014. Transplantation of enteric neural stem/progenitor cells into the irradiated young mouse hippocampus. Cell Transplant 23:1657-1671.
23. Perego C, Fumagalli S, De Simoni M-G. 2011. Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J Neuroinflammation 8:174.
24. Qiu L, Zhu C, Wang X, Xu F, Eriksson PS, Nilsson M, Cooper-Kuhn CM, Kuhn HG, Blomgren K. 2007. Less neurogenesis and inflammation in the immature than in the juvenile brain after cerebral hypoxia-ischemia. J Cereb Blood Flow Metab 27:785-794.
25. Rice JE, Vannucci RC, Brierley JB. 1981. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 9:131-141.
26. Saederup N, Cardona AE, Croft K, Mizutani M, Cotleur AC, Tsou C-L, Ransohoff RM, Charo IF. 2010. Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PloS One 5:e13693.
27. Schilling M, Besselmann M, Leonhard C, Mueller M, Ringelstein EB, Kiefer R. 2003. Microglial activation precedes and predominates over macrophage infiltration in transient focal cerebral ischemia: A study in green fluorescent protein transgenic bone marrow chimeric mice. Exp Neurol 183:25-33.
28. Stamatovic SM, Shakui P, Keep RF, Moore BB, Kunkel SL, Van Rooijen N, Andjelkovic AV. 2005. Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. J Cereb Blood Flow Metab 25:593-606.
29. Tanaka R, Komine-Kobayashi M, Mochizuki H, Yamada M, Furuya T, Migita M, Shimada T, Mizuno Y, Urabe T. 2003. Migration of enhanced green fluorescent protein expressing bone marrow-derived microglia/macrophage into the mouse brain following permanent focal ischemia. Neuroscience 117:531-539.
30. Vexler ZS, Yenari MA. 2009. Does inflammation after stroke affect the developing brain differently than adult brain? Dev Neurosci 31:378-393.
31. Wang Q, Tang XN, Yenari MA. 2007. The inflammatory response in stroke. J Neuroimmunol 184:53-68.
32. Yan Y-P, Lang BT, Vemuganti R, Dempsey RJ. 2009. Galectin-3 mediates post-ischemic tissue remodeling. Brain Res 1288:116-124.
33. Zhu C, Wang X, Xu F, Bahr BA Shibata M, Uchiyama Y, Hagberg H Blomgren K. 2005. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ 12:162-176.