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The Journal of Neuroscience, June 4, 2008, 28(23):5965-5975; doi:10.1523/JNEUROSCI.0060-08.2008

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Neurobiology of Disease
Microglia Cells Protect Neurons by Direct Engulfment of Invading Neutrophil Granulocytes: A New Mechanism of CNS Immune Privilege

Jens Neumann,¹ Steven Sauerzweig,¹ Raik Rönicke,¹ Frank Gunzer,³ Klaus Dinkel,¹ Oliver Ullrich,^2,4 Matthias Gunzer,^2,5 * and Klaus G. Reymann^1,6 *

¹Leibniz Institute for Neurobiology, Project Group Neuropharmacology, and ²Institute of Immunology, Otto von Guericke University Magdeburg, 39118 Magdeburg, Germany, ³German University in Cairo, 11771 Cairo, Egypt, ⁴Institute of Anatomy, Faculty of Medicine, University Zurich, CH-8057 Zurich, Switzerland, ⁵Helmholtz Centre for Infection Research, Junior Research Group Immunodynamics, 38124 Braunschweig, Germany, and ⁶Institute for Applied Neuroscience (Institute für Angewandte Neurowissenschaften FAN gGmbH), 39120 Magdeburg, Germany

Correspondence should be addressed to one of the following: Klaus G. Reymann or Jens Neumann, Leibniz Institute for Neurobiology, Project Group Neuropharmacology, Brenneckestrasse 6, D-39118 Magdeburg, Germany, Email: reymann{at}fan-neuroscience.com or Email: jens.neumann{at}sciencetoday.de; or Matthias Gunzer, Institute of Clinical and Molecular Immunology, Otto von Guericke University Magdeburg, Leipziger Strasse 44, D-39120 Magdeburg, Germany, E-mail: Email: matthias.gunzer{at}med.ovgu.de

Microglial cells maintain the immunological integrity of the healthy brain and can exert protection from traumatic injury. During ischemic tissue damage such as stroke, peripheral immune cells acutely infiltrate the brain and may exacerbate neurodegeneration. Whether and how microglia can protect from this insult is unknown. Polymorphonuclear neutrophils (PMNs) are a prominent immunologic infiltrate of ischemic lesions in vivo. Here, we show in organotypic brain slices that externally applied invading PMNs massively enhance ischemic neurotoxicity. This, however, is counteracted by additional application of microglia. Time-lapse imaging shows that microglia exert protection by rapid engulfment of apoptotic, but, strikingly, also viable, motile PMNs in cell culture and within brain slices. PMN engulfment is mediated by integrin- and lectin-based recognition. Interference with this process using RGDS peptides and N-acteyl-glucosamine blocks engulfment of PMNs and completely abrogates the neuroprotective function of microglia. Thus, engulfment of invading PMNs by microglia may represent an entirely new mechanism of CNS immune privilege.

Key words: neuroinflammation; stroke; microglia; polymorphonuclear granulocytes; PMN; phagocytosis; time-lapse imaging

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Received Jan. 7, 2008; revised Feb. 28, 2008; accepted April 1, 2008.

Correspondence should be addressed to one of the following: Klaus G. Reymann or Jens Neumann, Leibniz Institute for Neurobiology, Project Group Neuropharmacology, Brenneckestrasse 6, D-39118 Magdeburg, Germany, Email: reymann{at}fan-neuroscience.com or Email: jens.neumann{at}sciencetoday.de; or Matthias Gunzer, Institute of Clinical and Molecular Immunology, Otto von Guericke University Magdeburg, Leipziger Strasse 44, D-39120 Magdeburg, Germany, E-mail: Email: matthias.gunzer{at}med.ovgu.de

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