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The Journal of Neuroscience, September 29, 2004, 24(39):8500-8509; doi:10.1523/JNEUROSCI.2451-04.2004

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Cellular/Molecular
CXCR3-Dependent Microglial Recruitment Is Essential for Dendrite Loss after Brain Lesion

Angelika Rappert,^1,3 * Ingo Bechmann,^2 * Tatyana Pivneva,³ Jacqueline Mahlo,² Knut Biber,⁴ Christiane Nolte,¹ Adam D. Kovac,² Craig Gerard,⁵ Hendrikus W. G. M. Boddeke,⁴ Robert Nitsch,² and Helmut Kettenmann¹

¹Department of Cellular Neuroscience, Max Delbrück Center for Molecular Medicine, 13092 Berlin, Germany, ²Center for Anatomy, Institute of Cell Biology and Neurobiology, Charité University Hospital, 10115 Berlin, Germany, ³Department of Cytology, Bogomoletz Institute of Physiology, 01024 Kiev, Ukraine, ⁴Department of Medical Physiology, University of Groningen, 9700 AD Groningen, The Netherlands, and ⁵Ina Sue Perlmutter Laboratory, Children's Hospital Boston, Harvard Medical School, Boston, Massachusetts 02115

Microglia are the resident macrophage population of the CNS and are considered its major immunocompetent elements. They are activated by any type of brain pathology and can migrate to the lesion site. The chemokine CXCL10 is expressed in neurons in response to brain injury and is a signaling candidate for activating microglia and directing them to the lesion site. We recently identified CXCR3, the corresponding receptor for CXCL10, in microglia and demonstrated that this receptor system controls microglial migration. We have now tested the impact of CXCR3 signaling on cellular responses after entorhinal cortex lesion. In wild-type mice, microglia migrate within the first 3 d after lesion into the zone of axonal degeneration, where 8 d after lesion denervated dendrites of interneurons are subsequently lost. In contrast, the recruitment of microglia was impaired in CXCR3 knock-out mice, and, strikingly, denervated distal dendrites were maintained in zones of axonal degeneration. No differences between wild-type and knock-out mice were observed after facial nerve axotomy, as a lesion model for assessing microglial proliferation. This shows that CXCR3 signaling is crucial in microglia recruitment but not proliferation, and this recruitment is an essential element for neuronal reorganization.

Key words: microglia; migration; chemokine; receptor; CXCL10; CXCR3; dendritic loss; entorhinal cortex lesion; facial nerve lesion

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Received Nov 11, 2003; accepted July 14, 2004.

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