Surfactant protein C is associated with perineuronal nets and shows age-dependent changes of brain content and hippocampal deposits in wildtype and 3xTg mice

J Chem Neuroanat. 2021 Dec:118:102036. doi: 10.1016/j.jchemneu.2021.102036. Epub 2021 Oct 7.

Abstract

Surfactant protein C (SP-C) modulates cerebrospinal fluid (CSF) rheology. During ageing, its declining levels are accompanied by an increased burden of white matter lesions. Pulmonary SP-C intermediates harbouring the BRICHOS-domain prevent protein misfolding in the lungs. Thus, cerebral SP-C intermediates may counteract cerebral β-amyloidosis, a hallmark of Alzheimer's disease (AD). However, data on the molecular neuroanatomy of SP-C and its alterations in wildtype and triple transgenic (3xTg) mice, featuring essential elements of AD-neuropathology, are lacking. Therefore, this study investigated SP-C-containing structures in murine forebrains and their spatial relationships with vascular, glial and neuronal components of the neurovascular unit. Fluorescence labelling demonstrated neuronal SP-C in the medial habenula, the indusium griseum and the hippocampus. Glial counterstaining elucidated astrocytes in the corpus callosum co-expressing SP-C and S100β. Notably, perineuronal nets were associated with SP-C in the nucleus reticularis thalami, the lateral hypothalamus and the retrosplenial cortex. In the hippocampus of aged 3xTg mice, an increased number of dot-like depositions containing SP-C and Reelin, but devoid of BRICHOS-immunoreactivity were observed apart from AD-like lesions. Wildtype and 3xTg mice revealed an age-dependent increase of such deposits markedly pronounced in about 24-month-old 3xTg mice. SP-C levels of the intracellular and extracellular compartments in each group revealed an inverse correlation of SP-C and Reelin, with reduced SP-C and increased Reelin in an age-dependent fashion especially in 3xTg mice. Taken together, extracellular SP-C, as modulator of glymphatic clearance and potential ligand of PNs, declines in 3xTg mice, which show an accumulation of extracellular Reelin depositions during ageing.

Keywords: Extracellular matrix; Hippocampus; Hyperphosphorylated tau; Neurovascular unit; Perineuronal net; Reelin; S100β; SP-C; VGLUT2; WFA; β-amyloid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / metabolism
  • Animals
  • Astrocytes / metabolism
  • Brain Chemistry / physiology*
  • Extracellular Space / metabolism
  • Female
  • Glymphatic System / metabolism
  • Hippocampus / metabolism*
  • Humans
  • Male
  • Mice
  • Mice, Transgenic
  • Nerve Net / growth & development
  • Nerve Net / metabolism*
  • Neuroglia / metabolism
  • Neurovascular Coupling / physiology
  • Pulmonary Surfactant-Associated Protein C / metabolism*
  • Reelin Protein / metabolism
  • S100 Calcium Binding Protein beta Subunit / metabolism

Substances

  • Pulmonary Surfactant-Associated Protein C
  • Reelin Protein
  • S100 Calcium Binding Protein beta Subunit
  • S100b protein, mouse
  • Sftpc protein, mouse
  • Reln protein, mouse