CNS repair requires both effector and regulatory T cells with distinct temporal and spatial profiles

J Neurosci. 2014 Jul 30;34(31):10141-55. doi: 10.1523/JNEUROSCI.0076-14.2014.

Abstract

Monocyte-derived macrophages (mo-MΦs) and T cells have been shown to contribute to spinal cord repair. Recently, the remote brain choroid plexus epithelium (CP) was identified as a portal for monocyte recruitment, and its activation for leukocyte trafficking was found to be IFN-γ-dependent. Here, we addressed how the need for effector T cells can be reconciled with the role of inflammation-resolving immune cells in the repair process. Using an acute spinal cord injury model, we show that in mice deficient in IFN-γ-producing T cells, the CP was not activated, and recruitment of inflammation-resolving mo-MΦ to the spinal cord parenchyma was limited. We further demonstrate that mo-MΦ locally regulated recruitment of thymic-derived Foxp3(+) regulatory T (Treg) cells to the injured spinal cord parenchyma at the subacute/chronic phase. Importantly, an ablation protocol that resulted in reduced Tregs at this stage interfered with tissue remodeling, in contrast to Treg transient ablation, restricted to the 4 d period before the injury, which favored repair. The enhanced functional recovery observed following such a controlled decrease of Tregs suggests that reduced systemic immunosuppression at the time of the insult can enhance CNS repair. Overall, our data highlight a dynamic immune cell network needed for repair, acting in discrete compartments and stages, and involving effector and regulatory T cells, interconnected by mo-MΦ. Any of these populations may be detrimental to the repair process if their level or activity become dysregulated. Accordingly, therapeutic interventions must be both temporally and spatially controlled.

Keywords: T cells; Th1; Treg; immune resolution; monocyte-derived macrophages; spinal cord injury.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / metabolism
  • CD11c Antigen / genetics
  • CX3C Chemokine Receptor 1
  • Diphtheria Toxin / pharmacology
  • Disease Models, Animal
  • Forkhead Transcription Factors / genetics
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Macrophages / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Myelin-Oligodendrocyte Glycoprotein / immunology
  • Nerve Regeneration / genetics
  • Nerve Regeneration / immunology*
  • Peptide Fragments / immunology
  • Receptors, Chemokine / genetics
  • Recovery of Function / genetics
  • Recovery of Function / physiology*
  • Spinal Cord Injuries / physiopathology*
  • T-Box Domain Proteins / deficiency
  • T-Box Domain Proteins / genetics
  • T-Lymphocytes, Regulatory / physiology*
  • Vaccination

Substances

  • Antigens, CD
  • CD11c Antigen
  • CX3C Chemokine Receptor 1
  • Cx3cr1 protein, mouse
  • Diphtheria Toxin
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Myelin-Oligodendrocyte Glycoprotein
  • Peptide Fragments
  • Receptors, Chemokine
  • T-Box Domain Protein 2
  • T-Box Domain Proteins
  • myelin oligodendrocyte glycoprotein (35-55)
  • Green Fluorescent Proteins