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Circulating heparan sulfate fragments mediate septic cognitive dysfunction.

Joseph A Hippensteel1, Brian J Anderson2, James E Orfila3

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The Journal of Clinical Investigation
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Summary
This summary is machine-generated.

Sepsis survivors experience cognitive impairment due to circulating heparan sulfate fragments inhibiting brain-derived neurotrophic factor (BDNF) signaling, impacting learning and memory.

Keywords:
Extracellular matrixGlycobiologyNeurosciencegrowth factors

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Area of Science:

  • Neuroscience
  • Molecular Biology
  • Immunology

Background:

  • Sepsis frequently causes persistent cognitive impairment.
  • The mechanisms underlying sepsis-induced cognitive deficits, particularly effects on learning and memory, are not fully understood.
  • Brain-derived neurotrophic factor (BDNF) signaling is crucial for spatial memory formation via long-term potentiation (LTP).

Purpose of the Study:

  • To investigate the impact of sepsis on electrophysiological and molecular mechanisms of learning.
  • To identify the specific molecular factors contributing to persistent cognitive impairment after sepsis.
  • To explore the role of heparan sulfate fragments in sepsis-associated cognitive dysfunction.

Main Methods:

  • Sepsis and endotoxemia models in mice.
  • Electrophysiological recordings of hippocampal long-term potentiation (LTP).
  • Analysis of brain-derived neurotrophic factor (BDNF) content and signaling.
  • Glycoarray analysis of heparan sulfate binding affinities.
  • Measurement of heparan sulfate sulfation patterns in plasma of septic mice and humans.
  • Correlation of plasma heparan sulfate patterns with cognitive outcomes.

Main Results:

  • Sepsis survivors exhibited impaired hippocampal LTP and spatial memory deficits.
  • These impairments were linked to circulating heparan sulfate fragments that inhibited BDNF-mediated LTP.
  • Heparan sulfate fragments with specific 2-O- and N-sulfation patterns were found in endotoxemic mice and septic humans.
  • The presence of these specific sulfated heparan sulfate fragments in ICU patients predicted persistent cognitive impairment.

Conclusions:

  • Circulating heparan sulfate fragments, particularly those with 2-O- and N-sulfation, contribute to cognitive impairment following sepsis.
  • These fragments inhibit BDNF signaling in the hippocampus, disrupting learning and memory processes.
  • Plasma levels of specific sulfated heparan sulfate fragments may serve as a biomarker for predicting persistent cognitive deficits in septic patients.