Blood glutamate scavenging: Insight into neuro protection

International Journal of Molecular Sciences

Volumn 13, Issue 8, 2012, Pages 10041-10066

  Leibowitz, Akiva ^a   Boyko, Matthew ^a   Shapira, Yoram ^a   Zlotnik, Alexander ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Brain ischemia; Glutamate; Neuroprotection; Scavenging; Traumatic brain injury

Indexed keywords

ALANINE AMINOTRANSFERASE; ANTIDEPRESSANT AGENT; ASPARTATE AMINOTRANSFERASE; BLOOD GLUTAMATE SCAVENGER; ESTROGEN; GLUCAGON; GLUTAMATE RECEPTOR; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; INSULIN; LAMOTRIGINE; NEUROPROTECTIVE AGENT; OXALOACETIC ACID; PROGESTERONE; PYRUVIC ACID; UNCLASSIFIED DRUG; ZIDOVUDINE;

ACUTE STRESS RESPONSE; AMINO ACID BLOOD LEVEL; AMINO ACID METABOLISM; AMINO ACID TRANSPORT; APOPTOSIS; ASTROCYTE; AUTOREGULATION; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; BRAIN INJURY; BRAIN NERVE CELL; CELL DEATH; CELL SWELLING; CENTRAL NERVOUS SYSTEM DISEASE; CENTRAL NERVOUS SYSTEM INJURY; DEPRESSION; DISEASE EXACERBATION; EPILEPSY; EXTRACELLULAR FLUID; EXTRACORPOREAL CIRCULATION; GLIA CELL; GLUTAMATE METABOLISM; HEMODIALYSIS; HEMOFILTRATION; HUMAN; HYPOTHERMIA; INTERSTITIUM; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; PERITONEAL DIALYSIS; PLACENTA; REVIEW; STRESS; TRAUMATIC BRAIN INJURY; ANIMAL; METABOLISM; NERVOUS SYSTEM DISEASES;

ANIMALS; GLUTAMIC ACID; HUMANS; NERVOUS SYSTEM DISEASES; NEUROPROTECTIVE AGENTS;

EID: 84864976081     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms130810041     Document Type: Review

References (178)

1. Hawkins, R.A. The blood-brain barrier and glutamate. Am. J. Clin. Nutr. 2009, 90, 867S-874S.
2. Nakanishi, S. Molecular diversity of glutamate receptors and implications for brain function. Science 1992, 258, 597-603.
3. Matsui, K.; Jahr, C.E.; Rubio, M.E. High-concentration rapid transients of glutamate mediate neural-glial communication via ectopic release. J. Neurosci. 2005, 25, 7538-7547.
4. Filosa, A.; Paixao, S.; Honsek, S.D.; Carmona, M.A.; Becker, L.; Feddersen, B.; Gaitanos, L.; Rudhard, Y.; Schoepfer, R.; Klopstock, T., et al. Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport. Nat. Neurosci. 2009, 12, 1285-1292.
5. Hedberg, T.G.; Stanton, P.K. Long-term plasticity in cingulate cortex requires both NMDA and metabotropic glutamate receptor activation. Eur. J. Pharmacol. 1996, 310, 19-27.
6. Hardingham, G.E.; Bading, H. The Yin and Yang of NMDA receptor signalling. Trends Neurosci. 2003, 26, 81-89.
7. Richards, D.A.; Tolias, C.M.; Sgouros, S.; Bowery, N.G. Extra cellular glutamine to glutamate ratio may predict outcome in the injured brain: A clinical microdialysis study in children. Pharmacol. Res. 2003, 48, 101-109.
8. Hawkins, R.A.; Mokashi, A.; Dejoseph, M.R.; Vina, J.R.; Fernstrom, J.D. Glutamate ermeability at the blood-brain barrier in insulinopenic and insulin-resistant rats. Metabolism 2010, 59, 258-266.
9. Rossi, D.J.; Oshima, T.; Attwell, D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 2000, 403, 316-321.
10. Jensen, A.M.; Chiu, S.Y. Differential intracellular calcium responses to glutamate in type 1 and type 2 cultured brain astrocytes. J. Neurosci. 1991, 11, 1674-1684.
11. Kato, B.M.; Lachica, E.A.; Rubel, E.W. Glutamate modulates intracellular Ca2+ stores in brain stem auditory neurons. J. Neurophysiol. 1996, 76, 646-650.
12. Castillo, J.; Davalos, A.; Naveiro, J.; Noya, M. Neuroexcitatory amino acids and their relation to infarct size and neurological deficit in ischemic stroke. Stroke 1996, 27, 1060-1065.
13. Zauner, A.; Bullock, R.; Kuta, A.J.; Woodward, J.; Young, H.F. Glutamate release and cerebral blood flow after severe human head injury. Acta Neurochir. Suppl. 1996, 67, 40-44.
14. Castillo, J.; Davalos, A.; Alvarez-Sabin, J.; Pumar, J.M.; Leira, R.; Silva, Y.; Montaner, J.; Kase, C.S. Molecular signatures of brain injury after intra cerebral hemorrhage. Neurology 2002, 58, 624-629.
15. Johnston, M.V.; Trescher, W.H.; Ishida, A.; Nakajima, W. Neuro biology of hypoxic-ischemic injury in the developing brain. Pediatr. Res. 2001, 49, 735-741.
16. Andreadou, E.; Kapaki, E.; Kokotis, P.; Paraskevas, G.P.; Katsaros, N.; Libitaki, G.; Petropoulou, O.; Zis, V.; Sfagos, C.; Vassilopoulos, D. Plasma glutamate and glycine levels in patients with amyotrophic lateral sclerosis. In Vivo 2008, 22, 137-141.
17. Bunting, H.; Still, R.; Williams, D.R.; Gravenor, M.; Austin, M.W. Evaluation of plasma glutamate levels in normal tension glaucoma. Ophthalmic Res. 2010, 43, 197-200.
18. Espey, M.G.; Basile, A.S.; Heaton, R.K.; Ellis, R.J. Increased glutamate in CSF and plasma of patients with HIV dementia. Neurology 2002, 58, 1439-1440.
19. Takano, T.; Lin, J.H.; Arcuino, G.; Gao, Q.; Yang, J.; Nedergaard, M. Glutamate release promotes growth of malignant gliomas. Nat. Med. 2001, 7, 1010-1015.
20. Hassel, B.; Bachelard, H.; Jones, P.; Fonnum, F.; Sonnewald, U. Trafficking of amino acids between neurons and glia in vivo. Effects of inhibition of glial metabolism by fluoroacetate. J. Cereb. Blood Flow Metab. 1997, 17, 1230-1238.
21. Hertz, L.; Dringen, R.; Schousboe, A.; Robinson, S.R. Astro cytes: Glutamate producers for neurons. J. Neurosci. Res. 1999, 57, 417-428.
22. Hutchison, H.T.; Eisenberg, H.M.; Haber, B. High-affinity transport of glutamate in rat brain microvessels. Exp. Neurol. 1985, 87, 260-269.
23. Lee, W.J.; Hawkins, R.A.; Vina, J.R.; Peterson, D.R. Glutamine transport by the blood-brain barrier: A possible mechanism for nitrogen removal. Am. J. Physiol. 1998, 274, C1101-C1107.
24. O'Kane, R.L.; Martinez-Lopez, I.; DeJoseph, M.R.; Vina, J.R.; Hawkins, R.A. Na+-dependent glutamate transporters (EAAT1, EAAT2, and EAAT3) of the blood-brain barrier. A mechanism for glutamate removal. J. Biol. Chem. 1999, 274, 31891-31895.
25. Cohen-Kashi-Malina, K.; Cooper, I.; Teichberg, V.I. Mechanisms of glutamate efflux at the blood-brain barrier: Involvement of glial cells. J. Cereb. Blood Flow Metab. 2012, 32, 177-189.
26. Al-sarraf, H.; Preston, J.E.; Segal, M.B. Changes in the kinetics of the acidic amino acid brain and CSF uptake during development in the rat. Brain Res. Dev. Brain Res. 1997, 102, 127-134.
27. Al-Sarraf, H.; Preston, J.E.; Segal, M.B. Acidic amino acid accumulation by rat choroid plexus during development. Brain Res. Dev. Brain Res. 1997, 102, 47-52.
28. Helms, H.C.; Madelung, R.; Waagepetersen, H.S.; Nielsen, C.U.; Brodin, B. In vitro evidence for the brain glutamate efflux hypothesis: Brain endothelial cells cocultured with astrocytes display a polarized brain-to-blood transport of glutamate. Glia 2012, 60, 882-893.
29. Danbolt, N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65, 1-105.
30. Berl, S.; Lajtha, A.; Waelsch, H. Amino acid and protein metabolism of the brain. VI. Cerebral compartments of glutamic acid metabolism. J. Neurochem. 1961, 7, 186-197.
31. Gottlieb, M.; Wang, Y.; Teichberg, V.I. Blood-mediated scavenging of cerebrospinal fluid glutamate. J. Neurochem. 2003, 87, 119-126.
32. Hosoya, K.; Sugawara, M.; Asaba, H.; Terasaki, T. Blood-brain barrier produces significant efflux of L-aspartic acid but not D-aspartic acid: In vivo evidence using the brain efflux index method. J. Neurochem. 1999, 73, 1206-1211.
33. Bickel, U.; Yoshikawa, T.; Pardridge, W.M. Delivery of peptides and proteins through the blood-brain barrier. Adv. Drug Deliv. Rev. 2001, 46, 247-279.
34. Pawlik, G.; Rackl, A.; Bing, R.J. Quantitative capillary topography and blood flow in the cerebral cortex of cats: An in vivo microscopic study. Brain Res. 1981, 208, 35-58.
35. Schlageter, K.E.; Molnar, P.; Lapin, G.D.; Groothuis, D.R. Micro vessel organization and structure in experimental brain tumors: Micro vessel populations with distinctive structural and functional properties. Micro vasc. Res. 1999, 58, 312-328.
36. Buchan, A.M.; Lesiuk, H.; Barnes, K.A.; Li, H.; Huang, Z.G.; Smith, K.E.; Xue, D. AMPA antagonists: Do they hold more promise for clinical stroke trials than NMDA antagonists? Stroke 1993, 24, I148- I152.
37. Morris, G.F.; Juul, N.; Marshall, S.B.; Benedict, B.; Marshall, L.F. Neurological deterioration as a potential alternative endpoint in human clinical trials of experimental pharmacological agents for treatment of severe traumatic brain injuries. Executive Committee of the International Selfotel Trial. Neurosurgery 1998, 43, 1369-1372.
38. Muir, K.W. Glutamate-based therapeutic approaches: Clinical trials with NMDA antagonists. Curr. Opin. Pharmacol. 2006, 6, 53-60.
39. Ikonomidou, C.; Turski, L. Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury? Lancet Neurol. 2002, 1, 383-386.
40. Bertrand, G.; Gross, R.; Puech, R.; Loubatieres-Mariani, M.M.; Bockaert, J. Evidence for a glutamate receptor of the AMPA subtype which mediates insulin release from rat perfused pancreas. Br. J. Pharmacol. 1992, 106, 354-359.
41. Gonoi, T.; Mizuno, N.; Inagaki, N.; Kuromi, H.; Seino, Y.; Miyazaki, J.; Seino, S. Functional neuronal ionotropic glutamate receptors are expressed in the non-neuronal cell line MIN6. J. Biol. Chem. 1994, 269, 16989-16992.
42. Molnar, E.; Varadi, A.; McIlhinney, R.A.; Ashcroft, S.J. Identification of functional ionotropic glutamate receptor proteins in pancreatic beta-cells and in islets of Langerhans. FEBS Lett. 1995, 371, 253-257.
43. Inagaki, N.; Kuromi, H.; Gonoi, T.; Okamoto, Y.; Ishida, H.; Seino, Y.; Kaneko, T.; Iwanaga, T.; Seino, S. Expression and role of ionotropic glutamate receptors in pancreatic islet cells. FASEB J. 1995, 9, 686-691.
44. Weaver, C.D.; Yao, T.L.; Powers, A.C.; Verdoorn, T.A. Differential expression of glutamate receptor subtypes in rat pancreatic islets. J. Biol. Chem. 1996, 271, 12977-12984.
45. Teichberg, V.I. From the liver to the brain across the blood-brain barrier. Proc. Natl. Acad. Sci. USA 2007, 104, 7315-7316.
46. Teichberg, V.I.; Cohen-Kashi-Malina, K.; Cooper, I.; Zlotnik, A. Homeostasis of glutamate in brain fluids: An accelerated brain-to-blood efflux of excess glutamate is produced by blood glutamate scavenging and offers protection from neuropathologies. Neuroscience 2009, 158, 301-308.
47. Zlotnik, A.; Ohayon, S.; Gruenbaum, B.F.; Gruenbaum, S.E.; Mohar, B.; Boyko, M.; Klin, Y.; Sheiner, E.; Shaked, G.; Shapira, Y., et al. Determination of factors affecting glutamate concentrations in the whole blood of healthy human volunteers. J. Neurosurg. Anesthesiol. 2011, 23, 45-49.
48. Zlotnik, A.; Gruenbaum, B.F.; Mohar, B.; Kuts, R.; Gruenbaum, S.E.; Ohayon, S.; Boyko, M.; Klin D; Sheiner, E.; Shaked, G., et al. The effects of estrogen and progesterone on blood glutamate evels: Evidence from changes of blood glutamate levels during the menstrual cycle in women. Biol. Reprod. 2011, 84, 581-586.
49. Davson, H.; Hollingsworth, J.G.; Carey, M.B.; Fenstermacher, J.D. Ventriculo-cisternal perfusion of twelve amino acids in the rabbit. J. Neurobiol. 1982, 13, 293-318.
50. Al-Sarraf, H.; Preston, J.E.; Segal, M.B. Acidic amino acid clearance from CSF in the neonatal versus adult rat using ventriculo-cisternal perfusion. J. Neurochem. 2000, 74, 770-776.
51. Campos, F.; Sobrino, T.; Ramos-Cabrer, P.; Argibay, B.; Agulla, J.; Perez-Mato, M.; Rodriguez-Gonzalez, R.; Brea, D.; Castillo, J. Neuro protection by glutamate oxaloacetate transaminase in ischemic stroke: An experimental study. J. Cereb. Blood Flow Metab. 2011, 31. 1378-1386.
52. Fanne, R.A.; Nassar, T.; Heyman, S.N.; Hijazi, N.; Higazi, A.A. Insulin and glucagon share the same mechanism of neuroprotection in diabetic rats: Role of glutamate. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301, R668-R673.
53. Fanne, R.A.; Nassar, T.; Mazuz, A.; Waked, O.; Heyman, S.N.; Hijazi, N.; Goelman, G.; Higazi, A.A. Neuroprotection by glucagon: Role of gluconeogenesis. J. Neurosurg. 2010, 114, 85-91.
54. Stover, J.F.; Kempski, O.S. Anesthesia increases circulating glutamate in neurosurgical patients. Acta Neurochir. (Wien.) 2005, 147, 847-853.
55. Alfredsson, G.; Wiesel, F.A.; Tylec, A. Relationships between glutamate and monoamine metabolites in cerebrospinal fluid and serum in healthy volunteers. Biol. Psychiatry 1988, 23, 689-697
56. Ferrarese, C.; Aliprandi, A.; Tremolizzo, L.; Stanzani, L.; de Micheli, A.; Dolara, A.; Frattola, L. Increased glutamate in CSF and plasma of patients with HIV dementia. Neurology 2001, 57, 671-675.
57. Castillo, J.; Davalos, A.; Noya, M. Progression of ischaemic stroke and excitotoxic aminoacids. The Lancet 1997, 349, 79-83.
58. Shulman, Y.; Grant, S.; Seres, P.; Hanstock, C.; Baker, G.; Tibbo, P. The relation between peripheral and central glutamate and glutamine in healthy male volunteers. J. Psychiatry Neurosci. 2006, 31, 406-410.
59. Zlotnik, A.; Gurevich, B.; Tkachov, S.; Maoz, I.; Shapira, Y.; Teichberg, V.I. Brain neuroprotection by scavenging blood glutamate. Exp. Neurol. 2007, 203, 213-220.
60. Zlotnik, A.; Gruenbaum, S.E.; Artru, A.A.; Rozet, I.; Dubilet, M.; Tkachov, S.; Brotfain, E.; Klin, Y.; Shapira, Y.; Teichberg, V.I. The neuroprotective effects of oxaloacetate in closed head injury in rats is mediated by its blood glutamate scavenging activity: Evidence from the use of maleate. J. Neurosurg. Anesthesiol. 2009, 21, 235-241.
61. Zlotnik, A.; Gurevich, B.; Cherniavsky, E.; Tkachov, S.; Matuzani-Ruban, A.; Leon, A.; Shapira, Y.; Teichberg, V.I. The contribution of the blood glutamate scavenging activity of pyruvate to its neuroprotective properties in a rat model of closed head injury. Neurochem. Res. 2008, 33, 1044-1050.
62. Zlotnik, A.; Klin, Y.; Kotz, R.; Dubilet, M.; Boyko, M.; Ohayon, S.; Shapira, Y.; Teichberg, V.I. Regulation of blood L-glutamate levels by stress as a possible brain defense mechanism. Exp. Neurol. 2010, 224, 465-471.
63. Zlotnik, A.; Klin, Y.; Gruenbaum, B.F.; Gruenbaum, S.E.; Ohayon, S.; Boyko, M.; Sheiner, E.; Aricha-Tamir, B.; Shapira, Y.; Teichberg, V.I. The activation of beta2-adrenergic receptors in naive rats causes a reduction of blood glutamate levels: Relevance to stress and neuroprotection. Neurochem. Res. 2011, 36, 732-738.
64. Vuille-Dit-Bille, R.N.; Ha-Huy, R.; Tanner, M.; Stover, J.F. Changes in calculated arterio-jugular venous glutamate difference and SjvO2 in patients with severe traumatic brain injury. Minerva Anestesiol. 2011, 77, 870-876.
65. Boyko, M.; Zlotnik, A.; Gruenbaum, B.F.; Gruenbaum, S.E.; Ohayon, S.; Kuts, R.; Melamed, I.; Regev, A.; Shapira, Y.; Teichberg, V.I. Pyruvate's blood glutamate scavenging activity contributes to the spectrum of its neuro protective mechanisms in a rat model of stroke. Eur. J. Neurosci. 2011, 34, 1432-1441.
66. Puig, N.; Davalos, A.; Adan, J.; Piulats, J.; Martinez, J.M.; Castillo, J. Serum amino acid levels after permanent middle cerebral artery occlusion in the rat. Cerebrovasc. Dis. 2000, 10, 449-454.
67. Aliprandi, A.; Longoni, M.; Stanzani, L.; Tremolizzo, L.; Vaccaro, M.; Begni, B.; Galimberti, G.; Garofolo, R.; Ferrarese, C. Increased plasma glutamate in stroke patients might be linked to altered platelet release and uptake. J. Cereb. Blood Flow Metab. 2005, 25, 513-519.
68. Campos, F.; Sobrino, T.; Ramos-Cabrer, P.; Castellanos, M.; Blanco, M.; Rodriguez-Yanez, M.; Serena, J.; Leira, R.; Castillo, J. High blood glutamate oxaloacetate transaminase levels are associated with good functional outcome in acute ischemic stroke. J. Cereb. Blood Flow Metab. 2011, 31, 1387-1393.
69. Divino Filho, J.C.; Barany, P.; Stehle, P.; Furst, P.; Bergstrom, J. Free amino-acid levels simultaneously collected in plasma, muscle, and erythrocytes of uraemic patients. Nephrol. Dial. Transplant. 1997, 12, 2339-2348.
70. Ikizler, T.A.; Flakoll, P.J.; Parker, R.A.; Hakim, R.M. Amino acid and albumin losses during hemodialysis. Kidney Int. 1994, 46, 830-837.
71. Choi, J.Y.; Yoon, Y.J.; Choi, H.J.; Park, S.H.; Kim, C.D.; Kim, I.S.; Kwon, T.H.; Do, J.Y.; Kim, S.H.; Ryu, D.H., et al. Dialysis modality-dependent changes in serum metabolites: Accumulation of inosine and hypoxanthine in patients on haemodialysis. Nephrol. Dial. Transplant. 2011, 26, 1304-1313.
72. Filho, J.C.; Hazel, S.J.; Anderstam, B.; Bergstrom, J.; Lewitt, M.; Hall, K. Effect of protein intake on plasma and erythrocyte free amino acids and serum IGF-I and IGFBP-1 levels in rats. Am. J. Physiol. 1999, 277, E693-E701.
73. Rogachev, B.O.S.; Saad, A.; Vorobiovsky, V.; Gruenbaum, B.F.; Leibowitz, A.; Boyko, M.; Shapira, Y.; Shnaider, A.; Zlotnik, M.; Azab, A.N., et al. The effects of hemodialysis on blood glutamate levels in chronic renal failure-implementation for neuroprotection. J. Crit. Care 2012, in press.
74. Sumiyoshi, H.; Mantani, A.; Nishiyama, S.; Fujiwaki, S.; Ohta, S.; Masuda, Y.; Tomita, Y.; Tarumoto, N.; Yamawaki, S. Yokukansan treatment in chronic renal failure patients with dementia receiving hemodialysis: An open label study. Am. J. Geriatr. Psychiatry 2011, 19, 906-907.
75. Seifter, J.L.; Samuels, M.A. Uremic encephalopathy and other brain disorders associated with renal failure. Semin. Neurol. 2011, 31, 139-143.
76. Mitani, H.; Shirayama, Y.; Yamada, T.; Maeda, K.; Ashby, C.R., Jr.; Kawahara, R. Correlation between plasma levels of glutamate, alanine and serine with severity of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2006, 30, 1155-1158.
77. Kucukibrahimoglu, E.; Saygin, M.Z.; Caliskan, M.; Kaplan, O.K.; Unsal, C.; Goren, M.Z. The change in plasma GABA, glutamine and glutamate levels in fluoxetine- or S-citalopram-treated female patients with major depression. Eur. J. Clin. Pharmacol. 2009, 65, 571-577.
78. Mauri, M.C.; Ferrara, A.; Boscati, L.; Bravin, S.; Zamberlan, F.; Alecci, M.; Invernizzi, G. Plasma and platelet amino acid concentrations in patients affected by major depression and under fluvoxamine treatment. Neuropsychobiology 1998, 37, 124-129.
79. Altamura, C.; Maes, M.; Dai, J.; Meltzer, H.Y. Plasma concentrations of excitatory amino acids, serine, glycine, taurine and histidine in major depression. Eur. Neuropsychopharmacol. 1995, 5 71-75.
80. Eck, H.P.; Mertens, T.; Rosokat, H.; Fatkenheuer, G.; Pohl, C.; Schrappe, M.; Daniel, V.; Naher, H.; Petzoldt, D.; Drings, P., et al. T4+ cell numbers are correlated with plasma glutamate and cystine levels: association of hyper glutamataemia with immunodeficiency in diseases with different aetiologies. Int. Immunol. 1992, 4, 7-13.
81. Alfredsson, G.; Wiesel, F.A. Relationships between clinical effects and monoamine metabolites and amino acids in sulpiride-treated schizophrenic patients. Psychopharmacology 1990, 101, 324-331.
82. Van der Heijden, F.M.; Tuinier, S.; Fekkes, D.; Sijben, A.E.; Kahn, R.S.; Verhoeven, W.M. Atypical antipsychotics and the relevance of glutamate and serotonin. Eur. Neuropsychopharmacol. 2004, 14, 259-265.
83. Paraskevas, G.P.; Triantafyllou, N.I.; Kapaki, E.; Limpitaki, G.; Petropoulou, O.; Vassilopoulos, D. Add-on lamotrigine treatment and plasma glutamate levels in epilepsy: Relation to treatment response. Epilepsy. Res. 2006, 70, 184-189.
84. Spreux-Varoquaux, O.; Bensimon, G.; Lacomblez, L.; Salachas, F.; Pradat, P.F.; Le Forestier, N.; Marouan, A.; Dib, M.; Meininger, V. Glutamate levels in cerebrospinal fluid in amyotrophic lateral sclerosis: A reappraisal using a new HPLC method with coulometric detection in a large cohort of patients. J. Neurol. Sci. 2002, 193, 73-78.
85. Andreadou, E.; Kapaki, E.; Kokotis, P.; Paraskevas, G.P.; Katsaros, N.; Libitaki, G.; Zis, V.; Sfagos, C.; Vassilopoulos, D. Plasma glutamate and glycine levels in patients with amyotrophic lateral sclerosis: The effect of riluzole treatment. Clin. Neurol. Neurosurg. 2008, 110, 222-226.
86. Iwasaki, Y.; Ikeda, K.; Kinoshita, M. Plasma amino acid levels in patients with amyotrophic lateral sclerosis. J. Neurol. Sci. 1992, 107, 219-222.
87. Hajati, A.K.; Alstergren, P.; Nasstrom, K.; Bratt, J.; Kopp, S. Endogenous glutamate in association with inflammatory and hormonal factors modulates bone tissue resorption of the temporomandibular joint in patients with early rheumatoid arthritis. J. Oral Maxillofac. Surg. 2009, 67, 1895-1903.
88. Hajati, A.K.; Nasstrom, K.; Alstergren, P.; Bratt, J.; Kopp, S. Temporomandibular joint bone tissue resorption in patients with early rheumatoid arthritis can be predicted by joint crepitus and plasma glutamate level. Mediators Inflamm. 2010, 2010, 627803.
89. Babu, G.N.; Bawari, M.; Mathur, V.N.; Kalita, J.; Misra, U.K. Blood glutamate levels in patients with motor neuron disease. Clin. Chim. Acta 1998, 273, 195-200.
90. Tominaga, T.; Suzuki, H.; Mizuno, H.; Kouno, M.; Suzuki, M.; Kato, Y.; Sato, A.; Okabe, K.; Miyashita, M. Clinical significance of measuring plasma concentrations of glutamine and glutamate in alcoholic liver diseases. Alcohol Alcohol. Suppl. 1993, 1A, 103-109.
91. Yi, J.S.; Kim, T.Y.; Kyu Kim, D.; Koh, J.Y. Systemic pyruvate administration markedly reduces infarcts and motor deficits in rat models of transient and permanent focal cerebral ischemia. Neurobiol. Dis. 2007, 26, 94-104.
92. Zlotnik, A.; Sinelnikov, I.; Gruenbaum, B.F.; Gruenbaum, S.E.; Dubilet, M.; Dubilet, E.; Leibowitz, A.; Ohayon, S.; Regev, A.; Boyko, M.; Shapira, Y.; Teichberg, V.I. Effect of glutamate and blood glutamate scavengers oxaloacetate and pyruvate on neurological outcome and pathohistology of the hippocampus after traumatic brain injury in rats. Anesthesiology 2012, 116, 73-83.
93. Desagher, S.; Glowinski, J.; Premont, J. Pyruvate protects neurons against hydrogen peroxide-induced toxicity. J. Neurosci. 1997, 17, 9060-9067.
94. Crestanello, J.A.; Lingle, D.M.; Millili, J.; Whitman, G.J. Pyruvate improves myocardial tolerance to reperfusion injury by acting as an antioxidant: A chemiluminescence study. Surgery 1998, 124, 92-99.
95. Varma, S.D.; Devamanoharan, P.S.; Ali, A.H. Prevention of intracellular oxidative stress to lens by pyruvate and its ester. Free Radic. Res. 1998, 28, 131-135.
96. Mongan, P.D.; Capacchione, J.; Fontana, J.L.; West, S.; Bunger, R. Pyruvate improves cerebral metabolism during hemorrhagic shock. Am. J. Physiol. Heart Circ. Physiol. 2001, 281, H854- H864.
97. Burckhardt, B.C.; Lorenz, J.; Kobbe, C.; Burckhardt, G. Substrate specificity of the human renal sodium dicarboxylate cotransporter, hNaDC-3, under voltage-clamp conditions. Am. J. Physiol. Renal Physiol. 2005, 288, F792-F799.
98. Pajor, A.M.; Gangula, R.; Yao, X. Cloning and functional characterization of a high-affinity Na+/dicarboxylate cotransporter from mouse brain. Am. J. Physiol. Cell Physiol. 2001, 280, C1215-C1223.
99. Smith, Q.R. Transport of glutamate and other amino acids at the blood-brain barrier. J. Nutr. 2000, 130, 1016S-1022S.
100. Ronne Engstrom, E.; Hillered, L.; Enblad, P.; Karlsson, T. Cerebral interstitial levels of glutamate and glutamine after intravenous administration of nutritional amino acids in neurointensive care patients. Neurosci. Lett. 2005, 384, 7-10.
101. Faden, A.I.; Demediuk, P.; Panter, S.S.; Vink, R. The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 1989, 244, 798-800.
102. Farooque, M.; Hillered, L.; Holtz, A.; Olsson, Y. Changes of extracellular levels of amino acids after graded compression trauma to the spinal cord: An experimental study in the rat using microdialysis. J. Neurotrauma 1996, 13, 537-548.
103. Guyot, L.L.; Diaz, F.G.; O'Regan, M.H.; McLeod, S.; Park, H.; Phillis, J.W. Real-time measurement of glutamate release from the ischemic penumbra of the rat cerebral cortex using a focal middle cerebral artery occlusion model. Neurosci. Lett. 2001, 299, 37-40.
104. Phillis, J.W.; Smith-Barbour, M.; O'Regan, M.H. Changes in extracellular amino acid neurotransmitters and purines during and following ischemias of different durations in the rat cerebral cortex. Neurochem. Int. 1996, 29, 115-120.
105. Rose, M.E.; Huerbin, M.B.; Melick, J.; Marion, D.W.; Palmer, A.M.; Schiding, J.K.; Kochanek, P.M.; G raham, S.H. Regulation of interstitial excitatory amino acid concentrations after cortical contusion injury. Brain Res. 2002, 943, 15-22.
106. Alves, O.L.; Bullock, R.; Clausen, T.; Reinert, M.; Reeves, T.M. Concurrent monitoring of cerebral electrophysiology and metabolism after traumatic brain injury: An experimental and clinical study. J. Neurotrauma 2005, 22, 733-749.
107. Singh, I.N.; Sullivan, P.G.; Deng, Y.; Mbye, L.H.; Hall, E.D. Time course of post-traumatic mitochondrial oxidative damage and dysfunction in a mouse model of focal traumatic brain injury: Implications for neuroprotective therapy. J. Cereb. Blood Flow Metab. 2006, 26, 1407-1418.
108. Takamatsu, H.; Kondo, K.; Ikeda, Y.; Umemura, K. Hydroxyl radical generation after the third hour following ischemia contributes to brain damage. Eur. J. Pharmacol. 1998, 352, 165-169.
109. Xiong, Y.; Shie, F.S.; Zhang, J.; Lee, C.P.; Ho, Y.S. Prevention of mitochondrial dysfunction in post-traumatic mouse brain by superoxide dismutase. J. Neurochem. 2005, 95, 732-744.
110. Barzo, P.; Marmarou, A.; Fatouros, P.; Corwin, F.; Dunbar, J. Magnetic resonance imaging- monitored acute blood-brain barrier changes in experimental traumatic brain injury. J. Neurosurg. 1996, 85, 1113-1121.
111. Teichberg, V.I. GOT to rid the body of excess glutamate. J. Cereb. Blood Flow Metab. 2011, 31, 1376-1377.
112. Tsai, P.J.; Huang, P.C. Circadian variations in plasma and erythrocyte glutamate concentrations in adult men consuming a diet with and without added monosodium glutamate. J. Nutr. 2000, 130, 1002S-1004S.
113. Thomassen, A.R.; Mortensen, P.T.; Nielsen, T.T.; Falstie-Jensen, N.; Thygesen, K.; Henningsen, P. Altered plasma concentrations of glutamate, alanine and citrate in the early phase of acute myocardial infarction in man. Eur. Heart J. 1986, 7, 773-778.
114. Rosner, M.J.; Newsome, H.H.; Becker, D.P. Mechanical brain injury: The sympathoadrenal response. J. Neurosurg. 1984, 61, 76-86.
115. Clifton, G.L.; Ziegler, M.G.; Grossman, R.G. Circulating catecholamines and sympathetic activity after head injury. Neurosurgery 1981, 8, 10-14.
116. Zlotnik, A.; Gruenbaum, B.F.; Klin, Y.; Gruenbaum, S.E.; Ohayon, S.; Sheiner, E.; Kuts, R.; Boyko, M.; Bichovsky, Y.; Shapira, Y., et al. The effects of insulin, glucagon, glutamate, and glucose infusion on blood glutamate and plasma glucose levels in naive rats. J. Neurosurg. Anesthesiol. 2011, 23, 323-328.
117. Klin, Y.; Zlotnik, A.; Boyko, M.; Ohayon, S.; Shapira, Y.; Teichberg, V.I. Distribution of radiolabeled L-glutamate and D-aspartate from blood into peripheral tissues in naive rats: Significance for brain neuroprotection. Biochem. Biophys. Res. Commun. 2010, 399, 694-698.
118. Arakawa, H.; Kodama, H.; Matsuoka, N.; Yamaguchi, I. Stress increases plasma enzyme activity in rats: Differential effects of adrenergic and cholinergic blockades. J. Pharmacol. Exp. Ther. 1997, 280, 1296-1303.
119. Woolf, P.D.; Hamill, R.W.; Lee, L.A.; Cox, C.; McDonald, J.V. The predictive value of catecholamines in assessing outcome in traumatic brain injury. J. Neurosurg. 1987, 66, 875-882.
120. Aoki, T.T.; Brennan, M.F.; Muller, W.A.; Moore, F.D.; Cahill, G.F., Jr. Effect of insulin on muscle glutamate uptake. Whole blood versus plasma glutamate analysis. J. Clin. Invest. 1972, 51, 2889-2894.
121. Leweling, H.; Breitkreutz, R.; Behne, F.; Staedt, U.; Striebel, J.P.; Holm, E. Hyperammonemia-induced depletion of glutamate and branched-chain amino acids in muscle and plasma. J. Hepatol. 1996, 25, 756-762.
122. Felig, P.; Wahren, J.; Sherwin, R.; Hendler, R. Insulin, glucagon, and somatostatin in normal physiology and diabetes mellitus. Diabetes 1976, 25, 1091-1099.
123. Thomassen, A.; Nielsen, T.T.; Bagger, J.P.; Henningsen, P. Effects of intravenous glutamate on substrate availability and utilization across the human heart and leg. Metabolism 1991, 40, 378- 384.
124. Bertrand, G.; Gross, R.; Puech, R.; Loubatieres-Mariani, M.M.; Bockaert, J. Glutamate stimulates glucagon secretion via an excitatory amino acid receptor of the AMPA subtype in rat pancreas. Eur. J. Pharmacol. 1993, 237, 45-50.
125. Assan, R.; Attali, J.R.; Ballerio, G.; Boillot, J.; Girard, J.R. Glucagon secretion induced by natural and artificial amino acids in the perfused rat pancreas. Diabetes 1977, 26, 300-307.
126. Floyd, J.C., Jr.; Fajans, S.S.; Conn, J.W.; Knopf, R.F.; Rull, J. Stimulation of insulin secretion by amino acids. J. Clin. Invest. 1966, 45, 1487-1502.
127. Bertrand, G.; Puech, R.; Loubatieres-Mariani, M.M.; Bockaert, J. Glutamate stimulates insulin secretion and improves glucose tolerance in rats. Am. J. Physiol. 1995, 269, E551-E556.
128. Graham, T.E.; Sgro, V.; Friars, D.; Gibala, M.J. Glutamate ingestion: The plasma and muscle free amino acid pools of resting humans. Am. J. Physiol. Endocrinol. Metab. 2000, 278, E83-E89.
129. Bomont, L.; MacKenzie, E.T. Neuroprotection after focal cerebral ischaemia in hyperglycaemic and diabetic rats. Neurosci. Lett. 1995, 197, 53-56.
130. LeMay, D.R.; Gehua, L.; Zelenock, G.B.; D'Alecy, L.G. Insulin administration protects neurologic function in cerebral ischemia in rats. Stroke 1988, 19, 1411-1419.
131. Behl, C.; Manthey, D. Neuroprotective activities of estrogen: An update. J. Neurocytol. 2000, 29, 351-358.
132. Slooter, A.J.; Bronzova, J.; Witteman, J.C.; van Broeckhoven, C.; Hofman, A.; van Duijn, C.M. Estrogen use and early onset Alzheimer's disease: A population-based study. J. Neurol. Neurosurg. Psychiatry 1999, 67, 779-781.
133. Behl, C. Oestrogen as a neuroprotective hormone. Neuroscience 2002, 3, 433-442.
134. Tang, M.X.; Jacobs, D.; Stern, Y.; Marder, K.; Schofield, P.; Gurland, B.; Andrews, H.; Mayeux, R. Effect of oestrogen during menopause on risk and age at onset of Alzheimer's disease. Lancet 1996, 348, 429-432.
135. Waring, S.C.; Rocca, W.A.; Petersen, R.C.; O'Brien, P.C.; Tangalos, E.G.; Kokmen, E. Postmenopausal estrogen replacement therapy and risk of AD: A population-based study. Neurology 1999, 52, 965-970.
136. Yang, S.H.; Shi, J.; Day, A.L.; Simpkins, J.W. Estradiol exerts neuroprotective effects when administered after ischemic insult. Stroke 2000, 31, 745-749; discussion 749-750.
137. Green, P.S.; Simpkins, J.W. Neuro protective effects of estrogens: Potential mechanisms of action. Int. J. Dev. Neurosci. 2000, 18, 347-358.
138. Alkayed, N.J.; Murphy, S.J.; Traystman, R.J.; Hurn, P.D.; Miller, V.M. Neuro protective effects of female gonadal steroids in reproductively senescent female rats. Stroke 2000, 31, 161-168.
139. Wang, Q.; Santizo, R.; Baughman, V.L.; Pelligrino, D.A.; Iadecola, C. Estrogen provides neuroprotection in transient forebrain ischemia through perfusion-independent mechanisms in rats. Stroke 1999, 30, 630-637.
140. Dubal, D.B.; Shughrue, P.J.; Wilson, M.E.; Merchenthaler, I.; Wise, P.M. Estradiol modulates bcl-2 in cerebral ischemia: A potential role for estrogen receptors. J. Neurosci. 1999, 19, 6385-6393.
141. Dubal, D.B.; Kashon, M.L.; Pettigrew, L.C.; Ren, J.M.; Finklestein, S.P.; Rau, S.W.; Wise, P.M. Estradiol protects against ischemic injury. J. Cereb. Blood Flow Metab. 1998, 18, 1253-1258.
142. Rocca, W.A.; Bower, J.H.; Maraganore, D.M.; Ahlskog, J.E.; Grossardt, B.R.; de Andrade, M.; Melton, L.J., Increased risk of cognitive impairment or dementia in women who underwent ophorectomy before menopause. Neurology 2007, 69, 1074-1083.
143. Wright, D.W.; Bauer, M.E.; Hoffman, S.W.; Stein, D.G. Serum progesterone levels correlate with decreased cerebral edema after traumatic brain injury in male rats. J. Neurotrauma 2001, 18, 901-909.
144. Roof, R.L.; Duvdevani, R.; Heyburn, J.W.; Stein, D.G. Progesterone rapidly decreases brain edema: Treatment delayed up to 24 hours is still effective. Exp. Neurol. 1996, 138, 246-251.
145. Stein, D.G. Progesterone exerts neuroprotective effects after brain injury. Brain Res. Rev. 2008, 57, 386-397.
146. Roof, R.L.; Duvdevani, R.; Braswell, L.; Stein, D.G. Progesterone facilitates cognitive recovery and reduces secondary neuronal loss caused by cortical contusion injury in male rats. Exp. Neurol. 1994, 129, 64-69.
147. Roof, R.L.; Hall, E.D. Gender differences in acute CNS trauma and stroke: Neuroprotective effects of estrogen and progesterone. J. Neuro trauma 2000, 17, 367-388.
148. Punnonen, R.; Nummi, S.; Ylikorkala, O.; Alapiessa, U.; Karvonen, P.; Vinikka, L. A composite picture of the normal menstrual cycle. Acta Obstet. Gynecol. Scand. Suppl. 1976, 51, 63-70.
149. Abraham, G.E.; Odell, W.D.; Swerdloff, R.S.; Hopper, K. Simultaneous radioimmunoassay of plasma FSH, LH, progesterone, 17-hydroxyprogesterone, and estradiol-17 beta during the menstrual cycle. J. Clin. Endocrinol. Metab. 1972, 34, 312-318.
150. Zlotnik, A.; Leibowitz, A.; Gurevich, B.; Ohayon, S.; Boyko, M.; Klein, M.; Knyazer, B.; Shapira, Y.; Teichberg, V.I. Effect of estrogens on blood glutamate levels in relation to neurological outcome after TBI in male rats. Intensive Care Med. 2012, 38, 137-144.
151. Koivusalo, A.M.; Teikari, T.; Hockerstedt, K.; Isoniemi, H. Albumin dialysis has a favorable effect on amino acid profile in hepatic encephalopathy. Metab. Brain Dis. 2008, 23, 387-398.
152. Hachimi-Idrissi, S.; Corne, L.; Huyghens, L. The effect of mild hypothermia and induced hypertension on long term survival rate and neurological outcome after asphyxial cardiac arrest in rats. Resuscitation 2001, 49, 73-82.
153. Kollmar, R.; Schwab, S. Therapeutic hypothermia in neurological critical care. Dtsch Med. Wochenschr 2010, 135, 2361-2365.
154. Maekawa, T.; Tateishi, A.; Sadamitsu, D.; Kuroda, Y.; Soejima, Y.; Kashiwagi, S.; Yamashita, T.; Ito, H. Clinical application of mild hypothermia in neurological disorders. Minerva Anestesiol. 1994, 60, 537-540.
155. Maier, C.M.; Sun, G.H.; Kunis, D.; Yenari, M.A.; Steinberg, G.K. Delayed induction and long-term effects of mild hypothermia in a focal model of transient cerebral ischemia: Neurological outcome and infarct size. J. Neurosurg. 2001, 94, 90-96.
156. Moore, E.M.; Nichol, A.D.; Bernard, S.A.; Bellomo, R. Therapeutic hypothermia: Benefits, mechanisms and potential clinical applications in neurological, cardiac and kidney injury. Injury 2011, 42, 843-854.
157. Polderman, K.H. Induced hypothermia and fever control for prevention and treatment of neurological injuries. Lancet 2008, 371, 1955-1969.
158. Rees, K.; Beranek-Stanley, M.; Burke, M.; Ebrahim, S. Hypothermia to reduce neurological damage following coronary artery bypass surgery. Cochrane Database Syst. Rev. 2001, CD002138.
159. Wennervirta, J.E.; Ermes, M.J.; Tiainen, S.M.; Salmi, T.K.; Hynninen, M.S.; Sarkela, M.O.; Hynynen, M.J.; Stenman, U.H.; Viertio-Oja, H.E.; Saastamoinen, K.P., et al. Hypothermia-treated cardiac arrest patients with good neurological outcome differ early inquantitative variables of EEG suppression and epileptiform activity. Crit. Care Med. 2009, 37, 2427-2435.
160. Zeiner, A.; Holzer, M.; Sterz, F.; Behringer, W.; Schorkhuber, W.; Mullner, M.; Frass, M.; Siostrzonek, P.; Ratheiser, K.; Kaff, A., et al. Mild resuscitative hypothermia to improve neurological outcome after cardiac arrest. A clinical feasibility trial. Hypothermia After CardiacArrest (HACA) Study Group. Stroke 2000, 31, 86-94.
161. Zornow, M.H. Inhibition of glutamate release: A possible mechanism of hypothermic neuroprotection. J. Neurosurg. Anesthesiol. 1995, 7, 148-151.
162. Stover, J.F.; Kroppenstedt, S.N.; Thomale, U.W.; Kempski, O.S.; Unterberg, A.W. Isoflurane doubles plasma glutamate and increases posttraumatic brain edema. Acta Neurochir. Suppl. 2000, 76, 375-378.
163. Rutten, E.P.; Engelen, M.P.; Wouters, E.F.; Deutz, N.E.; Schols, A.M. Effect of glutamate ingestion on whole-body glutamate turnover in healthy elderly and patients with chronic obstructive pulmonary disease. Nutrition 2006, 22, 496-503.
164. Hackl, S.; van den Hoven, R.; Zickl, M.; Spona, J.; Zentek, J. The effects of short intensive exercise on plasma free amino acids in standardbred trotters. J. Anim. Physiol. Anim. Nutr. (Berl.) 2009, 93, 165-173.
165. Blomstrand, E.; Essen-Gustavsson, B. Changes in amino acid concentration in plasma and type I and type II fibres during resistance exercise and recovery in human subjects. Amino Acids 2009, 37, 629-636.
166. Newsholme, E.A.; Blomstrand, E. The plasma level of some amino acids and physical and mental fatigue. Experientia 1996, 52, 413-415.
167. Blomstrand, E.; Celsing, F.; Newsholme, E.A. Changes in plasma concentrations of aromatic and branched-chain amino acids during sustained exercise in man and their possible role in fatigue. Acta Physiol. Scand. 1988, 133, 115-121.
168. Yan, B.A.J.; Wang, G.; Lu, H.; Huang, X.; Liu, Y.; Zha, W.; Hao, H.; Zhang, Y.; Liu, L.; Gu, S., et al. Metabolomic investigation into variation of endogenous metabolites in professional athletes subject to strength-endurance training. J. Appl. Physiol. 2009, 106, 531-538.
169. Zlotnik, A.; Gurevich, B.; Artru, A.A.; Gruenbaum, S.E.; Dubilet, M.; Leibowitz, A.; Shaked, G.; Ohayon, S.; Shapira, Y.; Teichberg, V.I. The effect of hyperthermia on blood glutamate levels. Anesth. Analg. 2010, 111, 1497-1504.
170. De Cristobal, J.; Madrigal, J.L.; Lizasoain, I.; Lorenzo, P.; Leza, J.C.; Moro, M.A. Aspirin inhibits stress-induced increase in plasma glutamate, brain oxidative damage and ATP fall in rats. Neuro report 2002, 13, 217-221.
171. Mochizuki, A.; Lee, Y.P. Effects of thyroid hormone on amino acid and protein metabolism. 3. Influence of hydrocortisone on blood plasma and tissue glutamate levels of the rat in various thyroid hormone states. Endocrinology 1971, 89, 618-621.
172. Fernholm, R.; Thoren, M.; Hoybye, C.; Anderstam, B.; Pernow, Y.; Saaf, M.; Hall, K. Amino acid profiles in adults with growth hormone (GH) deficiency before and during GH replacement therapy. Growth Horm. IGF Res. 2009, 19, 206-211.
173. Khashaba, M.T.; Shouman, B.O.; Shaltout, A.A.; Al-Marsafawy, H.M.; Abdel-Aziz, M.M.; Patel, K.; Aly, H. Excitatory amino acids and magnesium sulfate in neonatal asphyxia. Brain Dev. 2006, 28, 375-379.
174. Jensen, A.; Garnier, Y.; Middelanis, J.; Berger, R. Perinatal brain damage-From thophysiology to prevention. Eur. J. Obstet. Gynecol. Reprod. Biol. 2003, 110, S70-S79.
175. Hagberg, H. Hypoxic-ischemic damage in the neonatal brain: Excitatory amino acids. Dev. Pharmacol. Ther. 1992, 18, 139-144.
176. Noorlander, C.W.; de Graan, P.N.E.; Nikkels, P.G.J.; Schrama, L.H.; Visser, G.H.A. Distribution of glutamate transporters in the human placenta. Placenta 2004, 25, 489-495.
177. Cetin, I.; de Santis, M.S.N.; Taricco, E.; Radaelli, T.; Teng, C.; Ronzoni, S.; Spada, E.; Milani, S.; Pardi, G. Maternal and fetal amino acid concentrations in normal pregnancies and in pregnancies with gestational diabetes mellitus. Am. J. Obstet. Gynecol. 2005, 192, 610-617.
178. Young, M.; Prenton, M.A. Maternal and fetal plasma amino acid concentrations during gestation and in retarded fetal growth. J. Obstet. Gynaecol. Br. Commonw. 1969, 76, 333-334.