Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior

J Neurosci. 2013 Aug 21;33(34):13820-33. doi: 10.1523/JNEUROSCI.1671-13.2013.

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(+)/SSC(lo)/Ly6C(hi)) and brain macrophages (CD11b(+)/SSC(lo)/CD45(hi)). 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 (CCR2(KO)) or fractalkine receptor knockout (CX3CR1(KO))] 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 CCR2(KO) or CX3CR1(KO) 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.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antigens, CD / metabolism
  • Anxiety Disorders / etiology*
  • Anxiety Disorders / immunology
  • Anxiety Disorders / pathology*
  • Bone Marrow / pathology*
  • Brain / pathology*
  • Calcium-Binding Proteins / metabolism
  • Cell Movement / genetics
  • Cell Movement / immunology
  • Cytokines / genetics
  • Cytokines / metabolism
  • Disease Models, Animal
  • Exploratory Behavior
  • Gene Expression Regulation
  • Green Fluorescent Proteins / genetics
  • Macrophages / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Microfilament Proteins / metabolism
  • Microglia / physiology
  • Monocytes / physiology*
  • Muramidase / genetics
  • Muramidase / metabolism
  • Receptors, CCR2 / deficiency
  • Receptors, CCR2 / genetics
  • Receptors, Interleukin-8A / genetics
  • Receptors, Interleukin-8B / deficiency
  • Receptors, Interleukin-8B / genetics
  • Stress, Psychological / complications*
  • Stress, Psychological / immunology
  • Time Factors

Substances

  • Aif1 protein, mouse
  • Antigens, CD
  • Calcium-Binding Proteins
  • Ccr2 protein, mouse
  • Cytokines
  • Microfilament Proteins
  • Receptors, CCR2
  • Receptors, Interleukin-8A
  • Receptors, Interleukin-8B
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Muramidase
  • lysozyme M, mouse