Glutamate Turnover and Energy Metabolism in Brain Injury: Clinical and Experimental Studies

During brain activity neurons release the major excitatory transmitter glutamate, which is taken up by astrocytes and converted to glutamine. Glutamine returns to neurons for re-conversion to glutamate. This glutamate-glutamine cycle is energy demanding. Glutamate turnover in injured brain was studied using an animal iron-induced posttraumatic epilepsy model and using neurointensive care data from 33 patients with spontaneous subarachnoid hemorrhage (SAH). Immunoblotting revealed that the functional form of the major astrocytic glutamate uptake protein GLT-1 was decreased 1-5 days following a cortical epileptogenic iron-injection, presumably due to oxidation-induced aggregation. Using microdialysis it was shown that the GLT-1 decrease was associated with increased interstitial glutamate levels and decreased interstitial glutamine levels. The results indicate a possible posttraumatic and post-stroke epileptogenic mechanism. Analysing 3600 microdialysis hours from patients it was found that the interstitial lactate/pyruvate (L/P) ratio correlate with the glutamine/glutamate ratio (r =-0.66). This correlation was as strong as the correlation between L/P and glutamate (r=0.68) and between lactate and glutamate (r=0.65). Pyruvate and glutamine correlated linearly (r=0.52). Energy failure periods, defined as L/P>40, were associated with high interstitial glutamate levels. Glutamine increased or decreased during energy failure periods depending on pyruvate. Energy failure periods were clinically associated with delayed ischemic neurological deficits (DIND) or development of radiologically verified infarcts, confirming that L/P>40 is a pathological microdialysis pattern that can predict ischemic deterioration after SAH. DIND-associated microdialysis patterns were L/P elevations and surges in interstitial glutamine. Glutamine and pyruvate correlated with the cerebral perfusion pressure (r=0.25, r=0.24). Glutamine and the glutamine/glutamate ratio correlated with the intracranial pressure (r=-0.29, r=0.40). Glutamine surges appeared upon substantial lowering of the intracranial pressure by increased cerebrospinal fluid drainage. Increased interstitial glutamine and pyruvate levels may reflect augmented astrocytic glycolysis in recovering brain tissue with increased energy demand due to a high glutamate-glutamine turnover.

Contents

Introduction
Acute brain injuries
Epidemiology
Neurointensive monitoring and care
Brain blood flow and energy metabolism
Ischemia
Seizures
Glutamatergic neurotransmission
Glutamate uptake
The glutamate-glutamine cycle
The role of glutamate and GLT-1 in the injured brain
Microdialysis
The technique
Recovery
What and where does microdialysis measure?
Microdialysis to monitor brain energy metabolism
Aims of the Study
Materials and Methods
Animals (Paper I & II)
Iron-induced posttraumatic epilepsy model
Microdialysis in animals
EEG
Immunoblotting
PBN analysis of blood
Patients (Paper III-V)
Microdialysis in patients
Computerized multimodality monitoring
Recording of clinical status and clinical course of events
Classification of microdialysis pattern
Statistics
Ethics
Results & Discussion
Time dependent protein alterations at the iron-induced epileptogenic lesion
Significance and reproducibility of the animal model
There is oxidation-induced aggregation of GLT-1 at the epileptogenic lesion
The interstitial glutamine/glutamate ratio is altered at the epileptogenic lesion
Human interstitial brain glutamate and glutamine relate to the energy metabolism
L/P ratios above 40 are associated with clinical criteria of ischemia
Where was the probe, where should it have been and why?
Interstitial glutamine increase over time and glutamine surges may signal hard-working astrocytes
DINDs are associated with glutamine surges
Glutamine surges appear when ICP is lowered
Interstitial glutamine relate to the clinical admittance status
Cessation of sedation does not explain the glutamine surges
Intracranial hemodynamics and microdialysis measurements
Interstitial glutamine what does it mean?
Origin of low glutamine/glutamate ratios in animals and humans
Methodological and statistical considerations
Concluding remarks
Acknowledgements
References

Author: Samuelsson, Carolina

Source: Uppsala University Library

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