TNF-alpha reduces cerebral blood volume and disrupts tissue homeostasis via an endothelin- and TNFR2-dependent pathway

Brain. 2002 Nov;125(Pt 11):2446-59. doi: 10.1093/brain/awf256.

Abstract

TNF-alpha expression is elevated in a variety of neuropathologies, including multiple sclerosis, cerebral malaria and HIV encephalitis. However, the consequences of such high cerebral TNF-alpha expression remain unresolved. Here, using MRI, we demonstrate that a focal intrastriatal injection of TNF-alpha causes a significant, acute reduction (15-30%) in cerebral blood volume (CBV), which is dependent on TNF-alpha-type 2 receptor (TNFR2) activation, and can be ameliorated by pre-treatment with a non-specific endothelin (ET) receptor antagonist. An acute breakdown of the blood-cerebrospinal fluid barrier (B-CSF-B) and a delayed breakdown of the blood-brain barrier (BBB) were also observed using contrast-enhanced MRI. Furthermore, a significant reduction in tissue water diffusion was apparent 24 h after intrastriatal injection of TNF-alpha injection, which may indicate compromise of tissue energy metabolism. Prolonged expression of endogenous TNF-alpha, achieved through the use of an adenoviral vector expressing TNF-alpha cDNA (Ad5TNF-alpha(m)), caused a sustained depression in CBV in accordance with the single TNF-alpha bolus data. These findings identify vasoconstriction, disrupted tissue homeostasis and damage to the BBBs as adverse effects of TNF-alpha within the brain, and suggest that antagonists of the endothelin and TNF-alpha type 2 receptors may be therapeutic in TNF-alpha-associated neuropathologies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / metabolism*
  • Blood-Brain Barrier / drug effects*
  • Blood-Brain Barrier / physiology
  • Brain / drug effects*
  • Brain / metabolism
  • Brain / pathology
  • Central Nervous System Diseases / drug therapy
  • Central Nervous System Diseases / metabolism*
  • Central Nervous System Diseases / physiopathology
  • Cerebrospinal Fluid / drug effects
  • Cerebrospinal Fluid / metabolism
  • Cerebrovascular Circulation / drug effects*
  • Cerebrovascular Circulation / physiology
  • Drug Administration Schedule
  • Endothelins / antagonists & inhibitors
  • Endothelins / metabolism*
  • Energy Metabolism / drug effects
  • Energy Metabolism / physiology
  • Homeostasis / drug effects
  • Homeostasis / physiology
  • Magnetic Resonance Imaging
  • Male
  • Neostriatum / drug effects
  • Neostriatum / metabolism
  • Neostriatum / pathology
  • Rats
  • Rats, Wistar
  • Receptors, Tumor Necrosis Factor / metabolism*
  • Receptors, Tumor Necrosis Factor, Type II
  • Recombinant Fusion Proteins / pharmacology
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism*
  • Tumor Necrosis Factor-alpha / pharmacology
  • Water-Electrolyte Balance / drug effects
  • Water-Electrolyte Balance / physiology

Substances

  • Antigens, CD
  • Endothelins
  • Receptors, Tumor Necrosis Factor
  • Receptors, Tumor Necrosis Factor, Type II
  • Recombinant Fusion Proteins
  • Tumor Necrosis Factor-alpha