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Articles, Neurobiology of Disease

Stress-Induced Recruitment of Bone Marrow-Derived Monocytes to the Brain Promotes Anxiety-Like Behavior

Eric S. Wohleb, Nicole D. Powell, Jonathan P. Godbout and John F. Sheridan
Journal of Neuroscience 21 August 2013, 33 (34) 13820-13833; DOI: https://doi.org/10.1523/JNEUROSCI.1671-13.2013
Eric S. Wohleb
1Division of Oral Biology,
2Department of Neuroscience,
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Nicole D. Powell
1Division of Oral Biology,
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Jonathan P. Godbout
2Department of Neuroscience,
3Institute for Behavioral Medicine Research,
4Center for Brain and Spinal Cord Repair, The Ohio State University, Columbus, Ohio 43210
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John F. Sheridan
1Division of Oral Biology,
3Institute for Behavioral Medicine Research,
4Center for Brain and Spinal Cord Repair, The Ohio State University, Columbus, Ohio 43210
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Abstract

Social stress is associated with altered immunity and higher incidence of anxiety-related disorders. Repeated social defeat (RSD) is a murine stressor that primes peripheral myeloid cells, activates microglia, and induces anxiety-like behavior. Here we show that RSD-induced anxiety-like behavior corresponded with an exposure-dependent increase in circulating monocytes (CD11b+/SSClo/Ly6Chi) and brain macrophages (CD11b+/SSClo/CD45hi). Moreover, RSD-induced anxiety-like behavior corresponded with brain region-dependent cytokine and chemokine responses involved with myeloid cell recruitment. Next, LysM-GFP+ and GFP+ bone marrow (BM)-chimeric mice were used to determine the neuroanatomical distribution of peripheral myeloid cells recruited to the brain during RSD. LysM-GFP+ mice showed that RSD increased recruitment of GFP+ macrophages to the brain and increased their presence within the perivascular space (PVS). In addition, RSD promoted recruitment of GFP+ macrophages into the PVS and parenchyma of the prefrontal cortex, amygdala, and hippocampus of GFP+ BM-chimeric mice. Furthermore, mice deficient in chemokine receptors associated with monocyte trafficking [chemokine receptor-2 knockout (CCR2KO) or fractalkine receptor knockout (CX3CR1KO)] failed to recruit macrophages to the brain and did not develop anxiety-like behavior following RSD. Last, RSD-induced macrophage trafficking was prevented in BM-chimeric mice generated with CCR2KO or CX3CR1KO donor cells. These findings indicate that monocyte recruitment to the brain in response to social stress represents a novel cellular mechanism that contributes to the development of anxiety.

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The Journal of Neuroscience: 33 (34)
Journal of Neuroscience
Vol. 33, Issue 34
21 Aug 2013
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Stress-Induced Recruitment of Bone Marrow-Derived Monocytes to the Brain Promotes Anxiety-Like Behavior
Eric S. Wohleb, Nicole D. Powell, Jonathan P. Godbout, John F. Sheridan
Journal of Neuroscience 21 August 2013, 33 (34) 13820-13833; DOI: 10.1523/JNEUROSCI.1671-13.2013

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Stress-Induced Recruitment of Bone Marrow-Derived Monocytes to the Brain Promotes Anxiety-Like Behavior
Eric S. Wohleb, Nicole D. Powell, Jonathan P. Godbout, John F. Sheridan
Journal of Neuroscience 21 August 2013, 33 (34) 13820-13833; DOI: 10.1523/JNEUROSCI.1671-13.2013
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