Placental ischemia-induced increases in brain water content and cerebrovascular permeability: role of TNF-α

Am J Physiol Regul Integr Comp Physiol. 2015 Dec 1;309(11):R1425-31. doi: 10.1152/ajpregu.00372.2015. Epub 2015 Sep 23.

Abstract

Cerebrovascular complications and increased risk of encephalopathies are characteristic of preeclampsia and contribute to 40% of preeclampsia/eclampsia-related deaths. Circulating tumor necrosis factor-α (TNF-α) is elevated in preeclamptic women, and infusion of TNF-α into pregnant rats mimics characteristics of preeclampsia. While this suggests that TNF-α has a mechanistic role to promote preeclampsia, the impact of TNF-α on the cerebral vasculature during pregnancy remains unclear. We tested the hypothesis that TNF-α contributes to cerebrovascular abnormalities during placental ischemia by first infusing TNF-α in pregnant rats (200 ng/day ip, from gestational day 14 to 19) at levels to mimic those reported in preeclamptic women. TNF-α increased mean arterial pressure (MAP, P < 0.05) and brain water content in the anterior cerebrum (P < 0.05); however, TNF-α infusion had no effect on blood-brain barrier (BBB) permeability in the anterior cerebrum or posterior cerebrum. We then assessed the role of endogenous TNF-α in mediating these abnormalities in a model of placental ischemia induced by reducing uterine perfusion pressure followed by treatment with the soluble TNF-α receptor (etanercept, 0.8 mg/kg sc) on gestational day 18. Etanercept reduced placental ischemia-mediated increases in MAP, anterior brain water content (P < 0.05), and BBB permeability (202 ± 44% in placental ischemic rats to 101 ± 28% of normal pregnant rats). Our results indicate that TNF-α mechanistically contributes to cerebral edema by increasing BBB permeability and is an underlying factor in the development of cerebrovascular abnormalities associated with preeclampsia complicated by placental ischemia.

Keywords: BBB permeability; cerebrovascular abnormalities; edema; preeclampsia; pregnancy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Pressure
  • Body Water / metabolism*
  • Brain / drug effects
  • Brain / metabolism*
  • Brain / physiopathology
  • Brain Edema / etiology*
  • Brain Edema / metabolism
  • Brain Edema / physiopathology
  • Brain Edema / prevention & control
  • Capillary Permeability* / drug effects
  • Cerebrovascular Disorders / etiology*
  • Cerebrovascular Disorders / metabolism
  • Cerebrovascular Disorders / physiopathology
  • Cerebrovascular Disorders / prevention & control
  • Disease Models, Animal
  • Etanercept / administration & dosage
  • Female
  • Gestational Age
  • Ischemia / complications*
  • Ischemia / drug therapy
  • Ischemia / metabolism
  • Ischemia / physiopathology
  • Placenta / blood supply*
  • Pre-Eclampsia / etiology*
  • Pre-Eclampsia / metabolism
  • Pre-Eclampsia / physiopathology
  • Pre-Eclampsia / prevention & control
  • Pregnancy
  • Rats, Sprague-Dawley
  • Tumor Necrosis Factor-alpha / administration & dosage
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / metabolism*

Substances

  • Tumor Necrosis Factor-alpha
  • Etanercept