Astrocyte activation and wound healing in intact-skull mouse after focal brain injury

European Journal of Neuroscience

Volumn 36, Issue 12, 2012, Pages 3653-3664

  Suzuki, Takayuki ^a   Sakata, Honami ^b   Kato, Chiaki ^b   Connor, John A ^a   Morita, Mitsuhiro ^a,b  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b KOBE UNIVERSITY   (Japan)

Author keywords

Cranial window; Gliosis; Hemorrhage; Microglia; Nestin

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN G; NESTIN; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN INJURY; CELL ACTIVATION; CELL NUCLEUS; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; GLIOSIS; HISTOLOGY; LEUKOCYTE; LIGHT EXPOSURE; MALE; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKULL; TISSUE DEGENERATION; UPREGULATION; WOUND HEALING;

ANIMALS; ASTROCYTES; BRAIN INJURIES; CELL PROLIFERATION; CEREBRAL CORTEX; GENE EXPRESSION; GLIOSIS; IMMUNOGLOBULIN G; INTERMEDIATE FILAMENT PROTEINS; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; MICROGLIA; NERVE TISSUE PROTEINS; NEURONS; SKULL; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 84871322803     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08280.x     Document Type: Article

References (52)

1. Beurrier, C., Faideau, M., Bennouar, K.E., Escartin, C., Kerkerian-Le Goff, L., Bonvento, G. & Gubellini, P. (2010) Ciliary neurotrophic factor protects striatal neurons against excitotoxicity by enhancing glial glutamate uptake. PLoS ONE, 5, e8550.
2. Bouchama, A. & Knochel, J.P. (2002) Heat stroke. N. Engl. J. Med., 346, 1978-1988.
3. Buffo, A., Rite, I., Tripathi, P., Lepier, A., Colak, D., Horn, A.P., Mori, T. & Gotz, M. (2008) Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc. Natl. Acad. Sci. USA, 105, 3581-3586.
4. Bush, T.G., Puvanachandra, N., Horner, C.H., Polito, A., Ostenfeld, T., Svendsen, C.N., Mucke, L., Johnson, M.H. & Sofroniew, M.V. (1999) Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron, 23, 297-308.
5. Carmichael, S.T. (2005) Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx, 2, 396-409.
6. Chen, S., Pickard, J.D. & Harris, N.G. (2003) Time course of cellular pathology after controlled cortical impact injury. Exp. Neurol., 182, 87-102.
7. Cherian, L., Robertson, C.S. & Goodman, J.C. (1996) Secondary insults increase injury after controlled cortical impact in rats. J. Neurotrauma, 13, 371-383.
8. Chodobski, A., Chung, I., Kozniewska, E., Ivanenko, T., Chang, W., Harrington, J.F., Duncan, J.A. & Szmydynger-Chodobska, J. (2003) Early neutrophilic expression of vascular endothelial growth factor after traumatic brain injury. Neuroscience, 122, 853-867.
9. D'Ambrosio, R., Maris, D.O., Grady, M.S., Winn, H.R. & Janigro, D. (1998) Selective loss of hippocampal long-term potentiation, but not depression, following fluid percussion injury. Brain Res., 786, 64-79.
10. Davalos, D., Grutzendler, J., Yang, G., Kim, J.V., Zuo, Y., Jung, S., Littman, D.R., Dustin, M.L. & Gan, W.B. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci., 8, 752-758.
11. Escartin, C., Pierre, K., Colin, A., Brouillet, E., Delzescaux, T., Guillermier, M., Dhenain, M., Deglon, N., Hantraye, P., Pellerin, L. & Bonvento, G. (2007) Activation of astrocytes by CNTF induces metabolic plasticity and increases resistance to metabolic insults. J. Neurosci., 27, 7094-7104.
12. Faulkner, J.R., Herrmann, J.E., Woo, M.J., Tansey, K.E., Doan, N.B. & Sofroniew, M.V. (2004) Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci., 24, 2143-2155.
13. Fiehler, J., Foth, M., Kucinski, T., Knab, R., von Bezold, M., Weiller, C., Zeumer, H. & Rother, J. (2002) Severe ADC decreases do not predict irreversible tissue damage in humans. Stroke, 33, 79-86.
14. Finnie, J.W. & Blumbergs, P.C. (2002) Traumatic brain injury. Vet. Pathol., 39, 679-689.
15. Fitch, M.T. & Silver, J. (1997) Glial cell extracellular matrix: boundaries for axon growth in development and regeneration. Cell Tissue Res., 290, 379-384.
16. Hsu, J.Y., Bourguignon, L.Y., Adams, C.M., Peyrollier, K., Zhang, H., Fandel, T., Cun, C.L., Werb, Z. & Noble-Haeusslein, L.J. (2008) Matrix metalloproteinase-9 facilitates glial scar formation in the injured spinal cord. J. Neurosci., 28, 13467-13477.
17. Imai, Y., Ibata, I., Ito, D., Ohsawa, K. & Kohsaka, S. (1996) A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem. Biophys. Res. Commun., 224, 855-862.
18. Kaushal, V. & Schlichter, L.C. (2008) Mechanisms of microglia-mediated neurotoxicity in a new model of the stroke penumbra. J. Neurosci., 28, 2221-2230.
19. Kim, G.W., Gasche, Y., Grzeschik, S., Copin, J.C., Maier, C.M. & Chan, P.H. (2003) Neurodegeneration in striatum induced by the mitochondrial toxin 3-nitropropionic acid: role of matrix metalloproteinase-9 in early blood-brain barrier disruption? J. Neurosci., 23, 8733-8742.
20. Kovacs, Z., Ikezaki, K., Samoto, K., Inamura, T. & Fukui, M. (1996) VEGF and flt. Expression time kinetics in rat brain infarct. Stroke, 27, 1865-1872; discussion 1872-1863.
21. Krum, J.M. & Khaibullina, A. (2003) Inhibition of endogenous VEGF impedes revascularization and astroglial proliferation: roles for VEGF in brain repair. Exp. Neurol., 181, 241-257.
22. Lendahl, U., Zimmerman, L.B. & McKay, R.D. (1990) CNS stem cells express a new class of intermediate filament protein. Cell, 60, 585-595.
23. McGraw, J., Hiebert, G.W. & Steeves, J.D. (2001) Modulating astrogliosis after neurotrauma. J. Neurosci. Res., 63, 109-115.
24. McIntosh, T.K., Vink, R., Noble, L., Yamakami, I., Fernyak, S., Soares, H. & Faden, A.L. (1989) Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience, 28, 233-244.
25. Merrill, J.E. (1992) Tumor necrosis factor alpha, interleukin 1 and related cytokines in brain development: normal and pathological. Dev. Neurosci., 14, 1-10.
26. Merrill, J.E. & Benveniste, E.N. (1996) Cytokines in inflammatory brain lesions: helpful and harmful. Trends Neurosci., 19, 331-338.
27. Min, K.J., Jou, I. & Joe, E. (2003) Plasminogen-induced IL-1beta and TNF-alpha production in microglia is regulated by reactive oxygen species. Biochem. Biophys. Res. Commun., 312, 969-974.
28. Mitchell, J., Sundstrom, L.E. & Wheal, H.V. (1993) Microglial and astrocytic cell responses in the rat hippocampus after an intracerebroventricular kainic acid injection. Exp. Neurol., 121, 224-230.
29. Mitsias, P.D., Ewing, J.R., Lu, M., Khalighi, M.M., Pasnoor, M., Ebadian, H.B., Zhao, Q., Santhakumar, S., Jacobs, M.A., Papamitsakis, N., Soltanian-Zadeh, H., Hearshen, D., Patel, S.C. & Chopp, M. (2004) Multiparametric iterative self-organizing MR imaging data analysis technique for assessment of tissue viability in acute cerebral ischemia. AJNR Am. J. Neuroradiol., 25, 1499-1508.
30. Moppett, I.K. (2007) Traumatic brain injury: assessment, resuscitation and early management. Br. J. Anaesth., 99, 18-31.
31. Myer, D.J., Gurkoff, G.G., Lee, S.M., Hovda, D.A. & Sofroniew, M.V. (2006) Essential protective roles of reactive astrocytes in traumatic brain injury. Brain, 129, 2761-2772.
32. Nag, S., Takahashi, J.L. & Kilty, D.W. (1997) Role of vascular endothelial growth factor in blood-brain barrier breakdown and angiogenesis in brain trauma. J. Neuropathol. Exp. Neurol., 56, 912-921.
33. Norenberg, M.D. (1994) Astrocyte responses to CNS injury. J. Neuropathol. Exp. Neurol., 53, 213-220.
34. Oberheim, N.A., Tian, G.F., Han, X., Peng, W., Takano, T., Ransom, B. & Nedergaard, M. (2008) Loss of astrocytic domain organization in the epileptic brain. J. Neurosci., 28, 3264-3276.
35. Okada, S., Nakamura, M., Katoh, H., Miyao, T., Shimazaki, T., Ishii, K., Yamane, J., Yoshimura, A., Iwamoto, Y., Toyama, Y. & Okano, H. (2006) Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat. Med., 12, 829-834.
36. Ridet, J.L., Malhotra, S.K., Privat, A. & Gage, F.H. (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci., 20, 570-577.
37. Rosenberg, G.A., Cunningham, L.A., Wallace, J., Alexander, S., Estrada, E.Y., Grossetete, M., Razhagi, A., Miller, K. & Gearing, A. (2001) Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res., 893, 104-112.
38. Ruiz de Almodovar, C., Lambrechts, D., Mazzone, M. & Carmeliet, P. (2009) Role and therapeutic potential of VEGF in the nervous system. Physiol. Rev., 89, 607-648.
39. Sanders, M.J., Sick, T.J., Perez-Pinzon, M.A., Dietrich, W.D. & Green, E.J. (2000) Chronic failure in the maintenance of long-term potentiation following fluid percussion injury in the rat. Brain Res., 861, 69-76.
40. Schroeter, M., Jander, S. & Stoll, G. (2002) Non-invasive induction of focal cerebral ischemia in mice by photothrombosis of cortical microvessels: characterization of inflammatory responses. J. Neurosci. Methods, 117, 43-49.
41. Seiffert, E., Dreier, J.P., Ivens, S., Bechmann, I., Tomkins, O., Heinemann, U. & Friedman, A. (2004) Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J. Neurosci., 24, 7829-7836.
42. Shen, F., Su, H., Fan, Y., Chen, Y., Zhu, Y., Liu, W., Young, W.L. & Yang, G.Y. (2006) Adeno-associated viral-vector-mediated hypoxia-inducible vascular endothelial growth factor gene expression attenuates ischemic brain injury after focal cerebral ischemia in mice. Stroke, 37, 2601-2606.
43. Silver, J. & Miller, J.H. (2004) Regeneration beyond the glial scar. Nat. Rev. Neurosci., 5, 146-156.
44. Sminia, P., van der Zee, J., Wondergem, J. & Haveman, J. (1994) Effect of hyperthermia on the central nervous system: a review. Int. J. Hyperthermia, 10, 1-30.
45. Soares, H.D., Hicks, R.R., Smith, D. & McIntosh, T.K. (1995) Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J. Neurosci., 15, 8223-8233.
46. Sofroniew, M.V. (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci., 32, 638-647.
47. Suzuki, S., Namiki, J., Shibata, S., Mastuzaki, Y. & Okano, H. (2010) The neural stem/progenitor cell marker nestin is expressed in proliferative endothelial cells, but not in mature vasculature. J. Histochem. Cytochem., 58, 721-730.
48. Vanderveldt, G.M. & Regan, R.F. (2004) The neurotoxic effect of sickle cell hemoglobin. Free Radic. Res., 38, 431-437.
49. Werner, C. & Engelhard, K. (2007) Pathophysiology of traumatic brain injury. Br. J. Anaesth., 99, 4-9.
50. Xu, H.T., Pan, F., Yang, G. & Gan, W.B. (2007) Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex. Nat. Neurosci., 10, 549-551.
51. Xue, M., Hollenberg, M.D. & Yong, V.W. (2006) Combination of thrombin and matrix metalloproteinase-9 exacerbates neurotoxicity in cell culture and intracerebral hemorrhage in mice. J. Neurosci., 26, 10281-10291.
52. Zhou, Y., Lekic, T., Fathali, N., Ostrowski, R.P., Martin, R.D., Tang, J. & Zhang, J.H. (2010) Isoflurane posttreatment reduces neonatal hypoxic-ischemic brain injury in rats by the sphingosine-1-phosphate/phosphatidylinositol-3-kinase/Akt pathway. Stroke, 41, 1521-1527.