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The Journal of Neuroscience, October 8, 2008, 28(41):10187-10199; doi:10.1523/JNEUROSCI.3510-08.2008

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Neurobiology of Disease
Rod-Shaped Monocytes Patrol the Brain Vasculature and Give Rise to Perivascular Macrophages under the Influence of Proinflammatory Cytokines and Angiopoietin-2

Julie Audoy-Rémus,¹ Jean-François Richard,¹ Denis Soulet,² Hong Zhou,³ Paul Kubes,³ and Luc Vallières¹

¹Department of Oncology and Molecular Endocrinology, Laval University Hospital Research Center, Quebec City, Quebec, Canada G1V 4G2, ²Neuronal Survival Unit, Department of Experimental Medical Science, Wallenberg Neuroscience Center, Lund University, 221 84 Lund, Sweden, and ³Immunology Research Group, Department of Physiology and Biophysics, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada T2N 4N1

Correspondence should be addressed to Luc Vallières, Department of Oncology and Molecular Endocrinology, Laval University Hospital Research Center, 2705 Laurier Boulevard, T3-67, Quebec City, Quebec, Canada G1V 4G2. Email: luc.vallieres{at}crchul.ulaval.ca

The nervous system is constantly infiltrated by blood-derived sentinels known as perivascular macrophages. Their immediate precursors have not yet been identified in situ and the mechanism that governs their recruitment is mostly unknown. Here, we provide evidence that CD68⁺GR1^– monocytes can give rise to perivascular macrophages in mice suffering from endotoxemia. After adhesion to the endothelium, these monocytes start to crawl, adopt a rod-shaped morphology when passing through capillaries, and can manifest the ability to proliferate and form a long cytoplasmic protuberance. They are attracted in greater numbers during endotoxemia by a combination of vasoregulatory molecules, including TNF (tumor necrosis factor), interleukin-1β, and angiopoietin-2. After a period of several hours, some of them cross the endothelium to expand the population of perivascular macrophages. Depletion of adherent monocytes and perivascular macrophages can be achieved by injection of anti-angiopoietin-2 peptide-Fc fusion protein. This study extends our understanding of the behavior of monocytes at the blood–brain interface and provides a way to block their infiltration into the nervous tissue under inflammatory conditions.

Key words: neuroinflammation; macrophage; microglia; endothelial; blood–brain barrier; cytokine

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Received July 25, 2008; revised Aug. 26, 2008; accepted Aug. 30, 2008.

Correspondence should be addressed to Luc Vallières, Department of Oncology and Molecular Endocrinology, Laval University Hospital Research Center, 2705 Laurier Boulevard, T3-67, Quebec City, Quebec, Canada G1V 4G2. Email: luc.vallieres{at}crchul.ulaval.ca

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