Counteracting neuroinflammation in experimental Parkinson's disease favors recovery of function: effects of Er-NPCs administration

J Neuroinflammation. 2018 Nov 30;15(1):333. doi: 10.1186/s12974-018-1375-2.

Abstract

Background: Parkinson's disease (PD) is the second most common neurodegenerative disease, presenting with midbrain dopaminergic neurons degeneration. A number of studies suggest that microglial activation may have a role in PD. It has emerged that inflammation-derived oxidative stress and cytokine-dependent toxicity may contribute to nigrostriatal pathway degeneration and exacerbate the progression of the disease in patients with idiopathic PD. Cell therapies have long been considered a feasible regenerative approach to compensate for the loss of specific cell populations such as the one that occurs in PD. We recently demonstrated that erythropoietin-releasing neural precursors cells (Er-NPCs) administered to MPTP-intoxicated animals survive after transplantation in the recipient's damaged brain, differentiate, and rescue degenerating striatal dopaminergic neurons. Here, we aimed to investigate the potential anti-inflammatory actions of Er-NPCs infused in an MPTP experimental model of PD.

Methods: The degeneration of dopaminergic neurons was caused by MPTP administration in C57BL/6 male mice. 2.5 × 105 GFP-labeled Er-NPCs were administered by stereotaxic injection unilaterally in the left striatum. Functional recovery was assessed by two independent behavioral tests. Neuroinflammation was investigated measuring the mRNAs levels of pro-inflammatory and anti-inflammatory cytokines, and immunohistochemistry studies were performed to evaluate markers of inflammation and the potential rescue of tyrosine hydroxylase (TH) projections in the striatum of recipient mice.

Results: Er-NPC administration promoted a rapid anti-inflammatory effect that was already evident 24 h after transplant with a decrease of pro-inflammatory and increase of anti-inflammatory cytokines mRNA expression levels. This effect was maintained until the end of the observational period, 2 weeks post-transplant. Here, we show that Er-NPCs transplant reduces macrophage infiltration, directly counteracting the M1-like pro-inflammatory response of murine-activated microglia, which corresponds to the decrease of CD68 and CD86 markers, and induces M2-like pro-regeneration traits, as indicated by the increase of CD206 and IL-10 expression. Moreover, we also show that this activity is mediated by Er-NPCs-derived erythropoietin (EPO) since the co-injection of cells with anti-EPO antibodies neutralizes the anti-inflammatory effect of the Er-NPCs treatment.

Conclusion: This study shows the anti-inflammatory actions exerted by Er-NPCs, and we suggest that these cells may represent good candidates for cellular therapy to counteract neuroinflammation in neurodegenerative disorders.

Keywords: Adult stem cells; Erythropoietin; Neural stem cells transplantation; Neuroinflammation; Parkinson’s disease; Regenerative medicine.

MeSH terms

  • 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine / pharmacology
  • Animals
  • Coculture Techniques
  • Corpus Striatum / metabolism
  • Corpus Striatum / surgery
  • Cytokines / metabolism
  • Disease Models, Animal
  • Dopamine Plasma Membrane Transport Proteins / metabolism
  • Encephalitis / etiology*
  • Encephalitis / surgery*
  • Erythropoietin / genetics
  • Erythropoietin / metabolism
  • Erythropoietin / therapeutic use*
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Muscle Strength / drug effects
  • Muscle Strength / physiology
  • Neural Stem Cells / physiology
  • Neural Stem Cells / transplantation*
  • Parkinsonian Disorders / complications*
  • Parkinsonian Disorders / etiology
  • Parkinsonian Disorders / pathology
  • Recovery of Function / drug effects
  • Recovery of Function / genetics
  • Recovery of Function / physiology*
  • Smell / drug effects
  • Smell / physiology
  • Tyrosine 3-Monooxygenase / metabolism

Substances

  • Cytokines
  • Dopamine Plasma Membrane Transport Proteins
  • Erythropoietin
  • Green Fluorescent Proteins
  • 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine
  • Tyrosine 3-Monooxygenase