Aging and MPTP Sensitivity Depend on Molecular and Ultrastructural Signatures of Astroglia and Microglia in Mice Substantia Nigra

Cell Mol Neurobiol. 2025 Jan 20;45(1):13. doi: 10.1007/s10571-024-01528-8.

Abstract

Both astroglia and microglia show region-specific distribution in CNS and often maladapt to age-associated alterations within their niche. Studies on autopsied substantia nigra (SN) of Parkinson's disease (PD) patients and experimental models propose gliosis as a trigger for neuronal loss. Epidemiological studies propose an ethnic bias in PD prevalence, since Caucasians are more susceptible than non-whites. Similarly, different mice strains are variably sensitive to MPTP. We had earlier likened divergent MPTP sensitivity of C57BL/6 J and CD-1 mice with differential susceptibility to PD, based on the numbers of SN neurons. We examined whether the variability was incumbent to inter-strain differences in glial features of male C57BL/6 J and CD-1 mice. Stereological counts showed relatively more microglia and fewer astrocytes in the SN of normal C57BL/6 J mice, suggesting persistence of an immune-vigilant state. MPTP-induced microgliosis and astrogliosis in both strains suggest their involvement in pathogenesis. ELISA of pro-inflammatory cytokines in the ventral-midbrain revealed augmentation of TNF-α and IL-6 at middle age in both strains that reduced at old age, suggesting middle age as a critical, inflamm-aging-associated time point. TNF-α levels were high in C57BL/6 J, through aging and post-MPTP, while IL-6 and IL-1β were upregulated at old age. CD-1 had higher levels of anti-inflammatory cytokine TGF-β. MPTP challenge caused upregulation of enzymes MAO-A, MAO-B, and iNOS in both strains. Post-MPTP enhancement in fractalkine and hemeoxygenase-1 may be neuron-associated compensatory signals. Ultrastructural observations of elongated astroglial/microglial mitochondria vis-à-vis the shrunken ones in neurons suggest a scale-up of their functions with neurotoxic consequences. Thus, astroglia and microglia may modulate aging and PD susceptibility.

Keywords: 1-Methyl-4-Phenyl-1, 2, 3, 6-Tetrahydropyridine (MPTP); CD-1 white mice; Cytokine ELISA; Monoamine oxidases a&b; Neuroinflammation; Parkinson’s disease; Substantia nigra pars compacta; Unbiased stereology, C57BL/6 J.

MeSH terms

  • 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine / pharmacology
  • Aging* / pathology
  • Animals
  • Astrocytes* / drug effects
  • Astrocytes* / metabolism
  • Astrocytes* / pathology
  • Astrocytes* / ultrastructure
  • Cytokines / metabolism
  • Gliosis / metabolism
  • Gliosis / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Microglia* / drug effects
  • Microglia* / metabolism
  • Microglia* / pathology
  • Microglia* / ultrastructure
  • Substantia Nigra* / drug effects
  • Substantia Nigra* / metabolism
  • Substantia Nigra* / pathology
  • Substantia Nigra* / ultrastructure

Substances

  • 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine
  • Cytokines