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Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology

Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries... Elimination of interstitial fluid and solutes plays a role in homeostasis in the brain, but the pathways are unclear. Previous work suggests that interstitial fluid drains along the walls of arteries. Aims: to define the pathways within the walls of capillaries and arteries for drainage of fluid and solutes out of the brain. Methods: Fluorescent soluble tracers, dextran (3 kDa) and ovalbumin (40 kDa), and particulate fluospheres (0.02 μm and 1.0 μm in diameter) were injected into the corpus striatum of mice. Brains were examined from 5 min to 7 days by immunocytochemistry and confocal microscopy. Results: soluble tracers initially spread diffusely through brain parenchyma and then drain out of the brain along basement membranes of capillaries and arteries. Some tracer is taken up by vascular smooth muscle cells and by perivascular macrophages. No perivascular drainage was observed when dextran was injected into mouse brains following cardiac arrest. Fluospheres expand perivascular spaces between vessel walls and surrounding brain, are ingested by perivascular macrophages but do not appear to leave the brain even following an inflammatory challenge with lipopolysaccharide or kainate. Conclusions: capillary and artery basement membranes act as ‘lymphatics of the brain’ for drainage of fluid and solutes; such drainage appears to require continued cardiac output as it ceases following cardiac arrest. This drainage pathway does not permit migration of cells from brain parenchyma to the periphery. Amyloid‐β is deposited in basement membrane drainage pathways in cerebral amyloid angiopathy, and may impede elimination of amyloid‐β and interstitial fluid from the brain in Alzheimer's disease. Soluble antigens, but not cells, drain from the brain by perivascular pathways. This atypical pattern of drainage may contribute to partial immune privilege of the brain and play a role in neuroimmunological diseases such as multiple sclerosis. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Neuropathology & Applied Neurobiology Wiley

Solutes, but not cells, drain from the brain parenchyma along basement membranes of capillaries and arteries: significance for cerebral amyloid angiopathy and neuroimmunology

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Publisher
Wiley
Copyright
2007 Blackwell Publishing Ltd
ISSN
0305-1846
eISSN
1365-2990
DOI
10.1111/j.1365-2990.2007.00926.x
pmid
18208483
Publisher site
See Article on Publisher Site

Abstract

Elimination of interstitial fluid and solutes plays a role in homeostasis in the brain, but the pathways are unclear. Previous work suggests that interstitial fluid drains along the walls of arteries. Aims: to define the pathways within the walls of capillaries and arteries for drainage of fluid and solutes out of the brain. Methods: Fluorescent soluble tracers, dextran (3 kDa) and ovalbumin (40 kDa), and particulate fluospheres (0.02 μm and 1.0 μm in diameter) were injected into the corpus striatum of mice. Brains were examined from 5 min to 7 days by immunocytochemistry and confocal microscopy. Results: soluble tracers initially spread diffusely through brain parenchyma and then drain out of the brain along basement membranes of capillaries and arteries. Some tracer is taken up by vascular smooth muscle cells and by perivascular macrophages. No perivascular drainage was observed when dextran was injected into mouse brains following cardiac arrest. Fluospheres expand perivascular spaces between vessel walls and surrounding brain, are ingested by perivascular macrophages but do not appear to leave the brain even following an inflammatory challenge with lipopolysaccharide or kainate. Conclusions: capillary and artery basement membranes act as ‘lymphatics of the brain’ for drainage of fluid and solutes; such drainage appears to require continued cardiac output as it ceases following cardiac arrest. This drainage pathway does not permit migration of cells from brain parenchyma to the periphery. Amyloid‐β is deposited in basement membrane drainage pathways in cerebral amyloid angiopathy, and may impede elimination of amyloid‐β and interstitial fluid from the brain in Alzheimer's disease. Soluble antigens, but not cells, drain from the brain by perivascular pathways. This atypical pattern of drainage may contribute to partial immune privilege of the brain and play a role in neuroimmunological diseases such as multiple sclerosis.

Journal

Neuropathology & Applied NeurobiologyWiley

Published: Apr 1, 2008

References

  • Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology
    Abbott, Abbott
  • CSF drains directly from the subarachnoid space into nasal lymphatics in the rat. Anatomy, histology and immunological significance
    Kida, Kida; Pantazis, Pantazis; Weller, Weller
  • Drainage of interstitial fluid from different regions of rat brain
    Szentistvanyi, Szentistvanyi; Patlak, Patlak; Ellis, Ellis; Cserr, Cserr
  • Factors and signals that govern the migration of dendritic cells via lymphatics: recent advances
    Randolph, Randolph; Sanchez‐Schmitz, Sanchez‐Schmitz; Angeli, Angeli
  • Differential blood–brain barrier breakdown and leucocyte recruitment following excitotoxic lesions in juvenile and adult rats
    Bolton, Bolton; Perry, Perry
  • Mechanisms to explain the reverse perivascular transport of solutes out of the brain
    Schley, Schley; Carare‐Nnadi, Carare‐Nnadi; Please, Please; Perry, Perry; Weller, Weller
  • Perivascular spaces in the basal ganglia of the human brain: their relationship to lacunes
    Pollock, Pollock; Hutchings, Hutchings; Weller, Weller; Zhang, Zhang
  • Giant tumefactive perivascular spaces
    Salzman, Salzman; Osborn, Osborn; House, House; Jinkins, Jinkins; Ditchfield, Ditchfield; Cooper, Cooper; Weller, Weller

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