Glutathione in the human brain: Review of its roles and measurement by magnetic resonance spectroscopy

Analytical Biochemistry

Volumn 529, Issue , 2017, Pages 127-143

  Rae, Caroline D ^a,b   Williams, Stephen R ^c  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Brain; Glutathione; Glyoxalase; Magnetic resonance spectroscopy; Neurological disease; Psychiatric disease

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE REDUCTASE; GLUTATHIONE TRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; BRAIN; DEGENERATIVE DISEASE; DEPRESSION; DETOXIFICATION; EPILEPSY; GLUTATHIONE METABOLISM; HUMAN; MENINGIOMA; MENTAL DISEASE; MILD COGNITIVE IMPAIRMENT; MOTOR NEURON DISEASE; MULTIPLE SCLEROSIS; NEUROLOGIC DISEASE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION; PRIORITY JOURNAL; REDUCTION (CHEMISTRY); SCHIZOPHRENIA; SYNTHESIS; ANIMAL; BIOLOGICAL MODEL; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCEDURES;

ANIMALS; BRAIN; GLUTATHIONE; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, BIOLOGICAL;

EID: 85010006257     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2016.12.022     Document Type: Article

References (157)

1. Wu, G., Fang, Y.-Z., Yang, S., Lupton, J.R., Turner, N.D., Glutathione metabolism and its implications for health. J. Nutr. 134 (2004), 489–492.
2. Deponte, M., Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim. Biophys. Acta (BBA)-General Subj. 1830 (2013), 3217–3266.
3. Cooper, A.J.L., Kristal, B.S., Multiple roles of glutathione in the central nervous system. Biol. Chem. 378 (1997), 793–802.
4. Dringen, R., Metabolism and functions of glutathione in brain. Prog. Neurobiol. 62 (2000), 649–671.
5. Philbert, M.A., Beiswanger, C.M., Waters, D.K., Reuhl, K.R., Lowndes, H.E., Cellular and regional distribution of reduced glutathione in the nervous system of the rat: histochemical localization by mercury orange and o-phthaldialdehyde-induced histofluorescence. Toxicol. Appl. Pharmacol. 107 (1991), 215–227.
6. Slivka, A., Mytilineou, C., Cohen, G., Histochemical evaluation of glutathione in brain. Brain Res. 409 (1987), 275–284.
7. Sun, X., Shih, A.Y., Johannssen, H.C., Erb, H., Li, P., Murphy, T.H., Two-photon imaging of glutathione levels in intact brain indicates enhanced redox buffering in developing neurons and cells at the cerebrospinal fluid and blood-brain interface. J. Biol. Chem. 281 (2006), 17420–17431.
8. Sun, X., Two-photon Imaging of Glutathione Levels in Intact Brain Indicates Sites of Enhanced Redox Buffering. 2006, University of British Columbia.
9. Rice, M.E., Russo-Menna, I., Differential compartmentalization of brain ascorbate and glutathione between neurons and glia. Neurosci 82 (1998), 1213–1223.
10. Juurlink, B.H.J., Thorburne, S.K., Hertz, L., Peroxide-scavenging deficit underlies oligodendrocyte susceptibility to oxidative stress. Glia 22 (1998), 371–378.
11. Perry, T., Hansen, S., Berry, K., Mok, C., Lesk, D., Free amino acids and related compounds in biopsies of human brain. J. Neurochem. 18 (1971), 521–528.
12. Vitvitsky, V., Thomas, M., Ghorpade, A., Gendelman, H.E., Banerjee, R., A functional transsulfuration pathway in the brain links to glutathione homeostasis. J. Biol. Chem. 281 (2006), 35785–35793.
13. Slivka, A., Spina, M.B., Cohen, G., Reduced and oxidized glutathione in human and monkey brain. Neurosci. Lett. 74 (1987), 112–118.
14. Rehncrona, S., Folbergrova, J., Smith, D.S., Siesjo, B.K., Influence of complete and pronounced incomplete cerebral ischemia and subsequent recirculation on cortical concentrations of oxidized and reduced glutathione in the rat. J. Neurochem. 34 (1980), 477–486.
15. Cooper, A.J., Pulsinelli, W.A., Duffy, T.E., Glutathione and ascorbate during ischemia and postischemic reperfusion in rat brain. J. Neurochem. 35 (1980), 1242–1245.
16. Chauhan, A., Audhya, T., Chauhan, V., Brain region-specific glutathione redox imbalance in autism. Neurochem. Res. 37 (2012), 1681–1689.
17. Yang, C.-S., Chou, S.-T., Lin, N.-N., Liu, L., Tsai, P.-J., Kuo, J.-S., Lai, J.-S., Determination of extracellular glutathione in rat brain by microdialysis and high-performance liquid chromatography with fluorescence detection. J. Chromat B Biomed. Sci. Apps 661 (1994), 231–235.
18. Lada, M.W., Kennedy, R.T., In vivo monitoring of glutathione and cysteine in rat caudate nucleus using microdialysis on-line with capillary zone electrophoresis-laser induced fluorescence detection. J. Neurosci. Meth 72 (1997), 153–159.
19. Wallin, C., Weber, S.G., Sandberg, M., Glutathione efflux induced by NMDA and Kainate. J. Neurochem. 73 (1999), 1566–1572.
20. Seelig, G.F., Simondsen, R.P., Meister, A., Reversible dissociation of gamma-glutamylcysteine synthetase into two subunits. J. Biol. Chem. 259 (1984), 9345–9347.
21. Yang, Y., Dieter, M.Z., Chen, Y., Shertzer, H.G., Nebert, D.W., Dalton, T.P., Initial characterization of the glutamate-cysteine ligase modifier subunit Gclm(−/−) knockout mouse: novel mouse model system for a severely compromised oxidative stress response. J. Biol. Chem. 277 (2002), 49446–49452.
22. Chen, Y., Shertzer, H.G., Schneider, S.N., Nebert, D.W., Dalton, T.P., Glutamate Cysteine Ligase Catalysis: dependence on ATP and modifier subunit for regulation of tissue glutathione levels. J. Biol. Chem. 280 (2005), 33766–33774.
23. Tsuchiya, K., Mulcahy, R.T., Reid, L.L., Disteche, C.M., Kavanagh, T.J., Mapping of the glutamate-cysteine ligase catalytic subunit gene (GLCLC) to human chromosome 6p12 and mouse chromosome 9D-E and of the regulatory subunit gene (GLCLR) to human chromosome 1p21-p22 and mouse chromosome 3H1-3. Genomics 30 (1995), 630–632.
24. Tosic, M., Ott, J., Barral, S., Bovet, P., Deppen, P., Gheorghita, F., Matthey, M.-L., Parnas, J., Preisig, M., Saraga, M., Schizophrenia and oxidative stress: glutamate cysteine ligase modifier as a susceptibility gene. Am. J. Hum. Gen. 79 (2006), 586–592.
25. Butticaz, C., Werge, T., Beckmann, J.S., Cuénod, M., Do, K.Q., Rivolta, C., Mutation screening of the glutamate cysteine ligase modifier (GCLM) gene in patients with schizophrenia. Psychiatr. Gen. 19 (2009), 201–208.
26. Kishi, T., Ikeda, M., Kitajima, T., Yamanouchi, Y., Kinoshita, Y., Kawashima, K., Inada, T., Harano, M., Komiyama, T., Hori, T., Glutamate cysteine ligase modifier (GCLM) subunit gene is not associated with Methamphetamine-use disorder or schizophrenia in the Japanese population. Proc. Ann. N. Y. Acad. Sci. 1139 (2008), 63–69.
27. Berk, M., Johansson, S., Wray, N.R., Williams, L., Olsson, C., Haavik, J., Bjerkeset, O., Glutamate cysteine ligase (GCL) and self reported depression: an association study from the HUNT. J. Affect Disord. 131 (2011), 207–213.
28. Ottersen, O.P., Zhang, N., Walberg, F., Metabolic compartmentation of glutamate and glutamine: morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neurosci 46 (1992), 519–534.
29. Richman, P., Meister, A., Regulation of gamma-glutamyl-cysteine synthetase by nonallosteric feedback inhibition by glutathione. J. Biol. Chem. 250 (1975), 1422–1426.
30. Griffith, O.W., Meister, A., Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J. Biol. Chem. 254 (1979), 7558–7560.
31. Richman, P.G., Orlowski, M., Meister, A., Inhibition of γ-glutamylcysteine synthetase by L-methionine-S-sulfoximine. J. Biol. Chem. 248 (1973), 6684–6690.
32. Ronzio, R.A., Rowe, W.B., Meister, A., Mechanism of inhibition of glutamine synthetase by methionine sulfoximine. Biochem. 8 (1969), 1066–1075.
33. Jeitner, T.M., Cooper, A.J., Inhibition of human glutamine synthetase by L-methionine-S, R-sulfoximine—relevance to the treatment of neurological diseases. Metabol. Brain Dis. 29 (2014), 983–989.
34. Heales, R., Davies, S.E.C., Bates, T.E., Clark, J.B., Depletion of brain glutathione is accompanied by impaired micochondrial function and decreased N-acetyl aspartate concentration. Neurochem. Res. 20 (1995), 31–38.
35. Jain, A., Mårtensson, J., Stole, E., Auld, P., Meister, A., Glutathione deficiency leads to mitochondrial damage in brain. Proc. Natl. Acad. Sci. U. S. A. 88 (1991), 1913–1917.
36. Njälsson, R., Norgren, S., Physiological and pathological aspects of GSH metabolism. Acta Pædiatrica 94 (2005), 132–137.
37. Ristoff, E., Mayatepek, E., Larsson, A., Long-term clinical outcome in patients with glutathione synthetase deficiency. J. Pediatr. 139 (2001), 79–84.
38. Choi, I.-Y., Gruetter, R., Dynamic or inert metabolism? Turnover of N-acetyl aspartate and glutathione from d-[1-13C]glucose in the rat brain in vivo. J. Neurochem. 91 (2004), 778–787.
39. Koga, M., Serritella, A.V., Messmer, M.M., Hayashi-Takagi, A., Hester, L.D., Snyder, S.H., Sawa, A., Sedlak, T.W., Glutathione is a physiologic reservoir of neuronal glutamate. Biochem. Biophys. Res. Commun. 409 (2011), 596–602.
40. Janaky, R., Varga, V., Hermann, A., Saransaari, P., Oja, S.S., Mechanisms of L-cysteine neurotoxicity. Neurochem. Res. 25 (2000), 1397–1405.
41. Yudkoff, M., Pleasure, D., Cregar, L., Lin, Z.-P., Nissim, I., Stern, J., Nissim, I., Glutathione turnover in cultured astrocytes: studies with [15N]Glutamate. J. Neurochem. 55 (1990), 137–145.
42. Dringen, R., Hamprecht, B., N-acetylcysteine, but not methionine or 2-oxothiazolidine-4-carboxylate, serves as cysteine donor for the synthesis of glutathione in cultured neurons derived from embryonal rat brain. Neurosci. Lett. 259 (1999), 79–82.
43. Wang, X.F., Cynader, M.S., Astrocytes provide cysteine to neurons by releasing glutathione. J. Neurochem. 74 (2000), 1434–1442.
44. Olney, J.W., Zorumski, C., Price, M.T., Labruyere, J., L-cysteine, a bicarbonate-sensitive endogenous excitotoxin. Science 248 (1990), 596–599.
45. Chen, Y., Swanson, R.A., The glutamate transporters EAAT2 and EAAT3 mediate cysteine uptake in cortical neuron cultures. J. Neurochem. 84 (2003), 1332–1339.
46. Aoyama, K., Suh, S.W., Hamby, A.M., Liu, J., Chan, W.Y., Chen, Y., Swanson, R.A., Neuronal glutathione deficiency and age-dependent neurodegeneration in the EAAC1 deficient mouse. Nat. Neurosci. 9 (2006), 119–126.
47. Thorburne, S.K., Juurlink, B.H., Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J. Neurochem. 67 (1996), 1014–1022.
48. Meister, A., Anderson, M.E., Glutathione. Ann. Rev. Biochem. 52 (1983), 711–760.
49. Philbert, M., Beiswanger, C., Manson, M., Green, J., Novak, R., Primiano, T., Reuhl, K., Lowndes, H., Glutathione S-transferases and gamma-glutamyl transpeptidase in the rat nervous systems: a basis for differential susceptibility to neurotoxicants. Neurotoxicol 16 (1994), 349–362.
50. Maxwell, K., Berliner, J.A., Cancilla, P.A., Induction of γ-glutamyl transpeptidase in cultured cerebral endothelial cells by a product released by astrocytes. Brain Res. 410 (1987), 309–314.
51. Hotta, S.S., Glucose metabolism in brain tissue: the hexose monophosphate shunt and its role in glutathione reduction. J. Neurochem. 9 (1962), 43–51.
52. Gutterer, J.M., Dringen, R., Hirrlinger, J., Hamprecht, B., Purification of glutathione reductase from bovine brain, generation of an antiserum, and immunocytochemical localization of the enzyme in neural cells. J. Neurochem. 73 (1999), 1422–1430.
53. Bolanos, J.P., Almeida, A., Moncada, S., Glycolysis: a bioenergetic or a survival pathway?. Trends Biochem. Sci. 35 (2010), 145–149.
54. Bolanos, J.P., Almeida, A., The pentose-phosphate pathway in neuronal survival against nitrosative stress,. IUBMB Life 62 (2010), 14–18.
55. Dringen, R., Brandmann, M., Hohnholt, M.C., Blumrich, E.-M., Glutathione-dependent detoxification processes in astrocytes. Neurochem. Res. 40 (2015), 2570–2582.
56. Hirrlinger, J., König, J., Dringen, R., Expression of mRNAs of multidrug resistance proteins (Mrps) in cultured rat astrocytes, oligodendrocytes, microglial cells and neurones. J. Neurochem. 82 (2002), 716–719.
57. Minich, T., Riemer, J., Schulz, J.B., Wielinga, P., Wijnholds, J., Dringen, R., The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J. Neurochem. 97 (2006), 373–384.
58. Shawahna, R., Uchida, Y., Decleves, X., Ohtsuki, S., Yousif, S., Dauchy, S., Jacob, A., Chassoux, F., Daumas-Duport, C., Couraud, P.-O., Transcriptomic and quantitative proteomic analysis of transporters and drug metabolizing enzymes in freshly isolated human brain microvessels. Mol. Pharm. 8 (2011), 1332–1341.
59. Board, P.G., Menon, D., Glutathione transferases, regulators of cellular metabolism and physiology. Biochim. Biophys. Acta (BBA) - General Subj. 1830 (2013), 3267–3288.
60. Abramovitz, M., Homma, H., Ishigaki, S., Tansey, F., Cammer, W., Listowsky, I., Characterization and localization of glutathione-S-transferases in rat brain and binding of hormones, neurotransmitters and drugs. J. Neurochem. 50 (1988), 50–57.
61. Cammer, W., Tansey, F., Abramovitz, M., Ishigaki, S., Listowsky, I., Differential localization of glutathione-S-transferase Yp and Yb subunits in oligodendrocytes and astrocytes of rat brain. J. Neurochem. 52 (1989), 876–883.
62. Kannan, R., Kuhlenkamp, J.F., Jeandidier, E., Trinh, H., Ookhtens, M., Kaplowitz, N., Evidence for carrier-mediated transport of glutathione across the blood-brain barrier in the rat. J. Clin. Invest 85 (1990), 2009–2013.
63. Nies, A.T., Jedlitschky, G., König, J., Herold-Mende, C., Steiner, H.H., Schmitt, H.P., Keppler, D., Expression and immunolocalization of the multidrug resistance proteins, MRP1–MRP6 (ABCC1–ABCC6), in human brain. Neurosci 129 (2004), 349–360.
64. Kalvass, J.C., Polli, J.W., Bourdet, D.L., Feng, B., Huang, S.M., Liu, X., Smith, Q.R., Zhang, L.K., Zamek-Gliszczynski, M.J., C. International transporter, Why clinical modulation of efflux transport at the human blood–brain barrier is unlikely: the ITC evidence-based position. Clin. Pharmacol. Ther. 94 (2013), 80–94.
65. Richie, J.P., Skowronski, L., Abraham, P., Leutzinger, Y., Blood glutathione concentrations in a large-scale human study. Clin. Chem. 42 (1996), 64–70.
66. Zlokovic, B.V., Mackic, J.B., McComb, J.G., Weiss, M.H., Kaplowitz, N., Kannan, R., Evidence for transcapillary transport of reduced glutathione in vascular perfused Guinea-Pig brain. Biochem. Biophys. Res. Commun. 201 (1994), 402–408.
67. Kannan, R., Chakrabarti, R., Tang, D., Kim, K., Kaplowitz, N., GSH transport in human cerebrovascular endothelial cells and human astrocytes: evidence for luminal localization of Na+-dependent GSH transport in HCEC. Brain Res. 852 (2000), 374–382.
68. Kannan, R., Jian, R.Y., Tang, D., Li, Y., Zlokovic, B.V., Kaplowitz, N., Evidence for the existence of a sodium-dependent glutathione (GSH) transporter. J. Biol. Chem. 271 (1996), 9754–9758.
69. Agarwal, R., Shukla, G.S., Potential role of cerebral glutathione in the maintenance of blood-brain barrier integrity in rat. Neurochem. Res. 24 (1999), 1507–1514.
70. Hirrlinger, J., Schulz, J.B., Dringen, R., Glutathione release from cultured brain cells: multidrug resistance protein 1 mediates the release of GSH from rat astroglial cells. J. Neurosci. Res. 69 (2002), 318–326.
71. Rana, S., Dringen, R., Gap junction hemichannel-mediated release of glutathione from cultured rat astrocytes. Neurosci. Lett. 415 (2007), 45–48.
72. Griffith, O.W., Meister, A., Origin and turnover of mitochondrial glutathione. Proc. Natl. Acad. Sci. U. S. A., 82, 1985, 4668.
73. Mårtensson, J., Lai, J., Meister, A., High-affinity transport of glutathione is part of a multicomponent system essential for mitochondrial function. Proc. Natl. Acad. Sci. U. S. A. 87 (1990), 7185–7189.
74. McKernan, T.B., Woods, E.B., Lash, L.H., Uptake of glutathione by renal cortical mitochondria. Arch. Biochem. Biophys. 288 (1991), 653–663.
75. Chen, Z., Lash, L.H., Evidence for mitochondrial uptake of glutathione by dicarboxylate and 2-oxoglutarate carriers. J. Pharmacol. Exp. Ther. 285 (1998), 608–618.
76. Coll, O., Colell, A., García-Ruiz, C., Kaplowitz, N., Fernández-Checa, J.C., Sensitivity of the 2-oxoglutarate carrier to alcohol intake contributes to mitochondrial glutathione depletion. Hepatology 38 (2003), 692–702.
77. Racker, E., Glutathione as a coenzyme in intermediary metabolism. Glutathione, a Symp., 1954, 165–183.
78. Lohmann, K., A study of the enzymatic transformation of synthetic methylglyoxal to lactic acid. Biochem. Z 254 (1932), 332–354.
79. Rae, C., O'Donoghue, S.I., Bubb, W.A., Kuchel, P.W., Stereospecificity of substrate usage by glyoxalase 1: nuclear magnetic resonance studies of kinetics and hemithioacetal substrate conformation. Biochem. 33 (1994), 3548–3559.
80. Riddle, V., Lorenz, F., Nonenzymic, polyvalent anion-catalyzed formation of methylglyoxal as an explanation of its presence in physiological systems. J. Biol. Chem. 243 (1968), 2718–2724.
81. Richard, J.P., Kinetic parameters for the elimination reaction catalyzed by triosephosphate isomerase and an estimation of the reaction's physiological significance. Biochem. 30 (1991), 4581–4585.
82. Walsh, C., Enzymatic Reaction Mechanisms. 1979, W.H.Freeman, New York.
83. Rae, C., Bubb, W.A., Kuchel, P.W., Aldolase-catalyzed diketone phosphate formation from oxoaldehydes. NMR studies and metabolic significance. J. Biol. Chem. 267 (1992), 9713–9717.
84. Chen, F., Wollmer, M.A., Hoerndli, F., Münch, G., Kuhla, B., Rogaev, E.I., Tsolaki, M., Papassotiropoulos, A., Götz, J., Role for glyoxalase I in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 7687–7692.
85. Belanger, M., Yang, J.Y., Petit, J.M., Laroche, T., Magistretti, P.J., Allaman, I., Role of the glyoxalase system in astrocyte-mediated neuroprotection. J. Neurosci. 31 (2011), 18338–18352.
86. Mori, O., Haseba, T., Kameyama, K., Shimizu, H., Kudoh, M., Ohaki, Y., Arai, Y., Yamazaki, M., Asano, G., Histological distribution of class III alcohol dehydrogenase in human brain. Brain Res. 852 (2000), 186–190.
87. Rae, C.D., Davidson, J.E., Maher, A.D., Rowlands, B.D., Kashem, M.A., Nasrallah, F.A., Rallipalli, S.K., Cook, J.M., Balcar, V.J., Ethanol, not detectably metabolized in brain, significantly reduces brain metabolism, probably via action at specific GABA(A) receptors and has measureable metabolic effects at very low concentrations. J. Neurochem. 129 (2014), 304–314.
88. Boleda, M.D., Saubi, N., Farres, J., Pares, X., Physiological substrates for rat alcohol dehydrogenase classes: aldehydes of lipid peroxidation, ω-hydroxyfatty acids, and retinoids. Arch. Biochem. Biophys. 307 (1993), 85–90.
89. Galter, D., Carmine, A., Buervenich, S., Duester, G., Olson, L., Distribution of class I, III and IV alcohol dehydrogenase mRNAs in the adult rat, mouse and human brain. Eur. J. Biochem. 270 (2003), 1316–1326.
90. Tulpule, K., Dringen, R., Formaldehyde in brain: an overlooked player in neurodegeneration?. J. Neurochem. 127 (2013), 7–21.
91. Govindaraju, V., Young, K., Maudsley, A.A., Proton NMR chemical shifts and coupling constant for brain metabolites. NMR Biomed. 13 (2000), 129–153.
92. Kaiser, L.G., Marjanska, M., Matson, G.B., Iltis, I., Bush, S.D., Soher, B.J., Mueller, S., Young, K., (1)H MRS detection of glycine residue of reduced glutathione in vivo. J. Magn. Reson 202 (2010), 259–266.
93. York, M.J., Beilharz, G.R., Kuchel, P.W., Conformation of reduced glutathione in aqueous solution by 1H and 13C nmr. Int. J. Pept. Prot. Res. 29 (1987), 638–646.
94. R.J. Ordidge and R. Gordon, Methods and apparatus for obtaining localised NMR spectra, US Patent No. 4531094, 1985.
95. Bottomley, P.A., Spatial localization in NMR spectroscopy in vivo. Ann. N. Y. Acad. Sci. 508 (1987), 333–348.
96. Frahm, J., Merboldt, K.D., Hanicke, W., Localized proton spectroscopy using stimulated echoes. J. Magn. Reson 72 (1987), 502–508.
97. Moonen, C.T.W., Kienlin, M.V., Van Zijl, P.C.M., Cohen, J., Gillen, J., Daly, P., Wolf, G., Comparison of single-shot localization methods (steam and press) for in vivo proton NMR spectroscopy. NMR Biomed. 2 (1989), 201–208.
98. Trabesinger, A.H., Weber, O.M., Duc, C.O., Boesinger, P., Detection of glutathione in the human brain in vivo by means of double quantum coherence filtering. Magn. Reson Med. 42 (1999), 283–289.
99. Kreis, R., Hofmann, L., Kuhlmann, B., Boesch, C., Bossi, E., Hüppi, P.S., Brain metabolite composition during early human brain development as measured by quantitative in vivo 1H magnetic resonance spectroscopy. Magn. Reson Med. 48 (2002), 949–958.
100. Opstad, K., Provencher, S., Bell, B., Griffiths, J., Howe, F., Detection of elevated glutathione in meningiomas by quantitative in vivo 1H MRS. Magn. Reson Med. 49 (2003), 632–637.
101. Choi, I.Y., Lee, S.P., Denney, D.R., Lynch, S.G., Lower levels of glutathione (GSH) in the brains of secondary progressive multiple sclerosis patients measured by (1)H magnetic resonance chemical shift imaging at 3 T. Mult. Scler. 17 (2011), 289–296.
102. Zhao, T., Heberlein, K., Jonas, C., Jones, D.P., Hu, X., New double quantum coherence filter for localized detection of glutathione in vivo. Magn. Reson Med. 55 (2006), 676–680.
103. Mescher, M., Merkle, H., Kirsch, J., Garwood, M., Gruetter, R., Simultaneous in vivo spectral editing and water suppression. NMR Biomed. 11 (1998), 266–272.
104. Rothman, D.L., Behar, K.L., Hetherington, H.P., Shulman, R.G., Homonuclear H1 double resonance difference spectroscopy of the rat brain in vivo. Proc. Natl. Acad. Sci. U. S. A. - Biol. Sci. 81 (1984), 6330–6334.
105. Williams, S., Gadian, D., Proctor, E., A method for lactate detection in vivo by spectral editing without the need for double irradiation. J. Magn. Reson 66 (1986), 562–567.
106. Satoh, T., Yoshioka, Y., Contribution of reduced and oxidized glutathione to signals detected by magnetic resonance spectroscopy as indicators of local brain redox state. Neurosci. Res. 55 (2006), 34–39.
107. Terpstra, M., Henry, P.G., Gruetter, R., Measurement of reduced glutathione (GSH) in human brain using LCmodel analysis of difference-edited spectra. Magn. Reson Med. 50 (2003), 19–23.
108. Thomas, M.A., Yue, K., Binesh, N., Davanzo, P., Kumar, A., Siegel, B., Frye, M., Curran, J., Lufkin, R., Martin, P., Localized two-dimensional shift correlated MR spectroscopy of human brain. Magn. Reson Med. 46 (2001), 58–67.
109. Provencher, S.W., Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson Med. 30 (1993), 672–679.
110. Wijtenburg, S.A., Gaston, F.E., Spieker, E.A., Korenic, S.A., Kochunov, P., Hong, L.E., Rowland, L.M., Reproducibility of phase rotation STEAM at 3T: focus on glutathione. Magn. Reson Med. 72 (2014), 603–609.
111. Chitty, K.M., Lagopoulos, J., Hickie, I.B., Hermens, D.F., Risky alcohol use in young persons with emerging bipolar disorder is associated with increased oxidative stress. J. Affect Disord. 150 (2013), 1238–1241.
112. Chitty, K.M., Lagopoulos, J., Hickie, I.B., Hermens, D.F., The impact of alcohol and tobacco use on in vivo glutathione in youth with bipolar disorder: an exploratory study,. J. Psychiatr. Res. 55 (2014), 59–67.
113. Srinivasan, R., Ratiney, H., Hammond-Rosenbluth, K.E., Pelletier, D., Nelson, S.J., MR spectroscopic imaging of glutathione in the white and gray matter at 7 T with an application to multiple sclerosis. Magn. Reson Imag. 28 (2010), 163–170.
114. An, L., Li, S., Murdoch, J.B., Araneta, M.F., Johnson, C., Shen, J., Detection of glutamate, glutamine, and glutathione by radiofrequency suppression and echo time optimization at 7 Tesla. Magn. Reson Med. 73 (2015), 451–458.
115. Choi, C., Dimitrov, I.E., Douglas, D., Patel, A., Kaiser, L.G., Amezcua, C.A., Maher, E.A., Improvement of resolution for brain coupled metabolites by optimized 1H MRS at 7 T. NMR Biomed. 23 (2010), 1044–1052.
116. Payne, G.S., Single-voxel MR Spectroscopy, EMagRes. 2015, John Wiley & Sons, Ltd.
117. de Graaf, R.A., Rothman, D.L., Spectral Editing, EMagRes. 2015, John Wiley and Sons, Ltd.
118. Bogner, W., Hangel, G., Andronesi, O.C., 1D-spectral editing and 2D multispectral in vivo 1H-MRS and 1HMRSI - methods and applications. Anal. Biochem., 2016 In this issue.
119. Starčuk, Z. Jr., Starčuková, J., Quantum-mechanical simulations for in vivo MR spectroscopy: principles and possibilities demonstrated with the program NMRScopeB. Anal. Biochem., 2016 early view online http://dx.doi.org/10.1016/j.ab.2016.10.007 In this issue.
120. Gambarota, G., Optimization of metabolite detection by quantum mechanics simulations in magnetic resonance spectroscopy. Anal. Biochem., 2016 early view online http://dx.doi.org/10.1016/j.ab.2016.08.019 In this issue.
121. Xin, L., Tkáč, I., A practical guide to in vivo proton magnetic resonance spectroscopy at high magnetic fields. Anal. Biochem., 2016 early view online http://dx.doi.org/10.1016/j.ab.2016.10.019 In this issue.
122. An, L., Zhang, Y., Thomasson, D.M., Latour, L.L., Baker, E.H., Shen, J., Warach, S., Measurement of glutathione in normal volunteers and stroke patients at 3T using J-difference spectroscopy with minimized subtraction errors. J. Magn. Reson Imag. 30 (2009), 263–270.
123. Mullins, P.G., McGonigle, D.J., O'Gorman, R.L., Puts, N.A., Vidyasagar, R., Evans, C.J., Edden, R.A., Current practice in the use of MEGA-PRESS spectroscopy for the detection of GABA. Neuroimage 86 (2014), 43–52.
124. Waddell, K.W., Avison, M.J., Joers, J.M., Gore, J.C., A practical guide to robust detection of GABA in human brain by J-difference spectroscopy at 3 T using a standard volume coil. Magn. Reson. Imag. 25 (2007), 1032–1038.
125. Choi, I.Y., Lee, P., Doubly selective multiple quantum chemical shift imaging and T1 relaxation time measurement of glutathione (GSH) in the human brain in vivo. NMR Biomed. 26 (2013), 28–34.
126. Thomas, M.A., Yue, K., Binesh, N., Davanzo, P., Kumar, A., Siegel, B., Frye, M., Curran, J., Lufkin, R., Martin, P., Guze, B., Localised two-dimensional shift correlated MR spectroscopy of human brain. Magn. Reson. Med. 46 (2001), 58–67.
127. Hermens, D., Lagopoulos, J., Naismith, S., Tobias-Webb, J., Hickie, I., Distinct neurometabolic profiles are evident in the anterior cingulate of young people with major psychiatric disorders. Transl. Psychiatry, 2, 2012, e110.
128. Kreis, R., The trouble with quality filtering based on relative Cramér-Rao lower bounds. Magn. Reson. Med. 75 (2016), 15–18.
129. van Ormondt, D., Graveron-Demilly, D., Sima, D.M., Van Huffel, S., Williams, S.R., Time-Domain Methods for Quantifying MR Spectra, EMagRes. 2015, John Wiley & Sons, Ltd.
130. Terpstra, M., Vaughan, T.J., Ugurbil, K., Lim, K.O., Schulz, S.C., Gruetter, R., Validation of glutathione quantitation from STEAM spectra against edited H-1 NMR spectroscopy at 4T: application to schizophrenia. Magn. Reson Mat. Phys. Biol. Med. 18 (2005), 276–282.
131. Sanaei Nezhad, F., Anton, A., Parkes, L.M., Deakin, B., Williams, S.R., Quantification of glutathione in the human brain by MR spectroscopy at 3 Tesla: comparison of PRESS and MEGA-PRESS. Magn. Reson Med., 2016 early view online http://dx.doi.org/10.1002/mrm.26532.
132. Emir, U.E., Raatz, S., McPherson, S., Hodges, J.S., Torkelson, C., Tawfik, P., White, T., Terpstra, M., Noninvasive quantification of ascorbate and glutathione concentration in the elderly human brain. NMR Biomed. 24 (2011), 888–894.
133. Bednařík, P., Tkáč, I., Giove, F., DiNuzzo, M., Deelchand, D.K., Emir, U.E., Eberly, L.E., Mangia, S., Neurochemical and BOLD responses during neuronal activation measured in the human visual cortex at 7 Tesla. J. Cereb. Blood Flow. Metab. 35 (2015), 601–610.
134. Lin, Y., Stephenson, M.C., Xin, L., Napolitano, A., Morris, P.G., Investigating the metabolic changes due to visual stimulation using functional proton magnetic resonance spectroscopy at 7 T. J. Cereb. Blood Flow. Metab. 32 (2012), 1484–1495.
135. Terpstra, M., Torkelson, C., Emir, U., Hodges, J.S., Raatz, S., Noninvasive quantification of human brain antioxidant concentrations after an intravenous bolus of vitamin C. NMR Biomed. 24 (2011), 521–528.
136. Holmay, M.J., Terpstra, M., Coles, L.D., Mishra, U., Ahlskog, M., Öz, G., Cloyd, J.C., Tuite, P.J., N-acetylcysteine Boosts Brain and Blood Glutathione in Gaucher and Parkinson's Diseases. Clin. Neuropharmacol., 36, 2013, 103.
137. Choi, I.-Y., Lee, P., Denney, D.R., Spaeth, K., Nast, O., Ptomey, L., Roth, A.K., Lierman, J.A., Sullivan, D.K., Dairy intake is associated with brain glutathione concentration in older adults. Am. J. Clin. Nutr. 101 (2015), 287–293.
138. Mandal, P.K., Tripathi, M., Sugunan, S., Brain oxidative stress: Detection and mapping of anti-oxidant marker 'Glutathione' in different brain regions of healthy male/female, MCI and Alzheimer patients using non-invasive magnetic resonance spectroscopy. Biochem. Biophys. Res. Commun. 417 (2012), 43–48.
139. Weiduschat, N., Mao, X., Hupf, J., Armstrong, N., Kang, G., Lange, D., Mitsumoto, H., Shungu, D., Motor cortex glutathione deficit in ALS measured in vivo with the J-editing technique. Neurosci. Lett. 570 (2014), 102–107.
140. Mueller, S., Trabesinger, A., Boesiger, P., Wieser, H., Brain glutathione levels in patients with epilepsy measured by in vivo 1H-MRS. Neurol 57 (2001), 1422–1427.
141. Florian, C.L., Preece, N.E., Bhakoo, K.K., Williams, S.R., Noble, M.D., Cell type-specific fingerprinting of meningioma and meningeal cells by proton nuclear magnetic resonance spectroscopy. Cancer Res. 55 (1995), 420–427.
142. Duffy, S.L., Lagopoulos, J., Cockayne, N., Hermens, D.F., Hickie, I.B., Naismith, S.L., Oxidative stress and depressive symptoms in older adults: a magnetic resonance spectroscopy study. J. Affect Disord. 180 (2015), 29–35.
143. Duffy, S.L., Lagopoulos, J., Hickie, I.B., Diamond, K., Graeber, M.B., Lewis, S.J., Naismith, S.L., Glutathione relates to neuropsychological functioning in mild cognitive impairment. Alzheimers Demen 10 (2014), 67–75.
144. Lapidus, K.A., Gabbay, V., Mao, X., Johnson, A., Murrough, J.W., Mathew, S.J., Shungu, D.C., In vivo 1H MRS study of potential associations between glutathione, oxidative stress and anhedonia in major depressive disorder. Neurosci. Lett. 569 (2014), 74–79.
145. Shungu, D.C., Weiduschat, N., Murrough, J.W., Mao, X., Pillemer, S., Dyke, J.P., Medow, M.S., Natelson, B.H., Stewart, J.M., Mathew, S.J., Increased ventricular lactate in chronic fatigue syndrome. III. Relationships to cortical glutathione and clinical symptoms implicate oxidative stress in disorder pathophysiology. NMR Biomed. 25 (2012), 1073–1087.
146. Godlewska, B.R., Yip, S.W., Near, J., Goodwin, G.M., Cowen, P.J., Cortical glutathione levels in young people with bipolar disorder: a pilot study using magnetic resonance spectroscopy. Psychopharmacol 231 (2014), 327–332.
147. Mandal, P.K., Saharan, S., Tripathi, M., Murari, G., Brain glutathione levels–a novel biomarker for mild cognitive impairment and Alzheimer's disease. Biol. Psychiatry 78 (2015), 702–710.
148. Wood, S.J., Berger, G.E., Wellard, R.M., Proffitt, T.-M., McConchie, M., Berk, M., McGorry, P.D., Pantelis, C., Medial temporal lobe glutathione concentration in first episode psychosis: a 1 H-MRS investigation. Neurobiol. Dis. 33 (2009), 354–357.
149. Do, K., Trabesinger, A., Kirsten-Krüger, M., Lauer, C., Dydak, U., Hell, D., Holsboer, F., Boesiger, P., Cuenod, M., Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo. Eur. J. Neurosci. 12 (2000), 3721–3728.
150. Matsuzawa, D., Obata, T., Shirayama, Y., Nonaka, H., Kanazawa, Y., Yoshitome, E., Takanashi, J., Matsuda, T., Shimizu, E., Ikehira, H., Negative correlation between brain glutathione level and negative symptoms in schizophrenia: a 3T 1 H-MRS study. PLoS One, 3, 2008, e1944.
151. Monin, A., Baumann, P., Griffa, A., Xin, L., Mekle, R., Fournier, M., Butticaz, C., Klaey, M., Cabungcal, J.-H., Steullet, P., Glutathione deficit impairs myelin maturation: relevance for white matter integrity in schizophrenia patients. Mol. Psychiatry 20 (2014), 827–838.
152. Michels, L., Schulte-Vels, T., Schick, M., O'Gorman, R.L., Zeffiro, T., Hasler, G., Mueller-Pfeiffer, C., Prefrontal GABA and glutathione imbalance in posttraumatic stress disorder: preliminary findings. Psychiatry Res. 224 (2014), 288–295.
153. Durieux, A., Horder, J., Mendez, M.A., Egerton, A., Williams, S.C., Wilson, C.E., Spain, D., Murphy, C., Robertson, D., Barker, G.J., Cortical and subcortical glutathione levels in adults with autism spectrum disorder. Autism Res. 9 (2016), 429–435.
154. Stefan, D., Di Cesare, F., Andrasescu, A., Popa, E., Lazariev, A., Vescovo, E., Strbak, O., Williams, S., Starcuk, Z., Cabanas, M., van Ormondt, D., Graveron-Demilly, D., Quantitation of magnetic resonance spectroscopy signals: the jMRUI software package. Meas. Sci. Tech., 20, 2009.
155. Terpstra, M., Marjanska, M., Henry, P.G., Tkáč, I., Gruetter, R., Detection of an antioxidant profile in the human brain in vivo via double editing with MEGA-PRESS. Magn. Reson Med. 56 (2006), 1192–1199.
156. Emir, U.E., Auerbach, E.J., Moortele, P.F.V.D., Marjańska, M., Uğurbil, K., Terpstra, M., Tkáč, I., Öz, G., Regional neurochemical profiles in the human brain measured by 1H MRS at 7 T using local B1 shimming. NMR Biomed. 25 (2012), 152–160.
157. Chan, K.L., Puts, N.A., Snoussi, K., Harris, A.D., Barker, P.B., Edden, R.A., Echo time optimization for J-difference editing of glutathione at 3T. Magn. Reson. Med., 2016 early view online http://dx.doi.org/10.1002/mrm.26122.