Vascular amyloid alters astrocytic water and potassium channels in mouse models and humans with Alzheimer's disease

Neuroscience. 2009 Mar 31;159(3):1055-69. doi: 10.1016/j.neuroscience.2009.01.023. Epub 2009 Jan 19.

Abstract

The neurovascular unit (NVU) comprises cerebral blood vessels and surrounding astrocytes, neurons, perivascular microglia and pericytes. Astrocytes associated with the NVU are responsible for maintaining cerebral blood flow and ionic and osmotic balances in the brain. A significant proportion of individuals with Alzheimer's disease (AD) have vascular amyloid deposits (cerebral amyloid angiopathy, CAA) that contribute to the heterogeneous nature of the disease. To determine whether NVU astrocytes are affected by the accumulation of amyloid at cerebral blood vessels we examined astrocytic markers in four transgenic mouse models of amyloid deposition. These mouse models represent mild CAA, moderate CAA with disease progression to tau pathology and neuron loss, severe CAA and severe CAA with disease progression to tau pathology and neuron loss. We found that CAA and disease progression both resulted in distinct NVU astrocytic changes. CAA causes a loss of apparent glial fibrillary acidic protein (GFAP)-positive astrocytic end-feet and loss of water channels (aquaporin 4) localized to astrocytic end feet. The potassium channels Kir4.1, an inward rectifying potassium channel, and BK, a calcium-sensitive large-conductance potassium channel, were also lost. The anchoring protein, dystrophin 1, is common to these channels and was reduced in association with CAA. Disease progression was associated with a phenotypic switch in astrocytes indicated by a loss of GFAP-positive cells and a gain of S100 beta-positive cells. Aquaporin 4, Kir4.1 and dystrophin 1 were also reduced in autopsied brain tissue from individuals with AD that also display moderate and severe CAA. Together, these data suggest that damage to the neurovascular unit may be a factor in the pathogenesis of Alzheimer's disease.

Publication types

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

MeSH terms

  • Aged, 80 and over
  • Alzheimer Disease / physiopathology*
  • Amyloid beta-Protein Precursor / genetics
  • Animals
  • Aquaporin 4 / metabolism*
  • Astrocytes / pathology
  • Astrocytes / physiology*
  • Brain / blood supply
  • Brain / physiopathology
  • Cerebral Amyloid Angiopathy / physiopathology*
  • Disease Models, Animal
  • Dystrophin / metabolism
  • Female
  • Glial Fibrillary Acidic Protein / metabolism
  • Humans
  • Kv1.6 Potassium Channel
  • Male
  • Mice
  • Mice, Transgenic
  • Nitric Oxide Synthase Type II / genetics
  • Potassium Channels / metabolism*
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Protease Nexins
  • RNA, Messenger
  • Receptors, Cell Surface / genetics
  • Shaker Superfamily of Potassium Channels / metabolism

Substances

  • AQP4 protein, human
  • Amyloid beta-Protein Precursor
  • Aquaporin 4
  • Dystrophin
  • Glial Fibrillary Acidic Protein
  • KCNA6 protein, human
  • Kcnj10 (channel)
  • Kv1.6 Potassium Channel
  • Potassium Channels
  • Potassium Channels, Inwardly Rectifying
  • Protease Nexins
  • RNA, Messenger
  • Receptors, Cell Surface
  • Shaker Superfamily of Potassium Channels
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse