Glutamatergic dysfunction linked to energy and membrane lipid metabolism in frontal and anterior cingulate cortices of never treated first-episode schizophrenia patients

Schizophrenia Research

Volumn 168, Issue 1-2, 2015, Pages 322-329

  Smesny, Stefan ^a   Gussew, Alexander ^a   Biesel, Natalie Joan ^a   Schack, Stephan ^a   Walther, Mario ^a   Rzanny, Reinhard ^a   Milleit, Berko ^a,b   Gaser, Christian ^a   Sobanski, Thomas ^b   Schultz, Carl Christoph ^a   Amminger, Paul ^c,d   Hipler, Uta Christina ^a   Sauer, Heinrich ^a   Reichenbach, Jürgen R ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b ThUringen Kliniken   (Germany)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

1H MRS; 31P MRS; CSI; Energy metabolism; First episode psychosis; Glutamate; Phospholipids; Schizophrenia

Indexed keywords

GLUTAMIC ACID; PHOSPHOLIPID; ASPARTIC ACID; CREATINE; MEMBRANE LIPID; N-ACETYLASPARTATE; PHOSPHORUS; PROTON;

ADULT; AMINO ACID METABOLISM; ANTERIOR CINGULATE; ANTERIOR COMMISSURE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENERGY METABOLISM; FEMALE; FRONTAL CORTEX; GLUTAMATERGIC DYSFUNCTION; GRAY MATTER; HUMAN; LIPID MEMBRANE; LIPID METABOLISM; MALE; METABOLITE; NEUROLOGIC DISEASE; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; POSTERIOR COMMISSURE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SCHIZOPHRENIA; WHITE MATTER; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; CINGULATE GYRUS; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; PSYCHOLOGICAL RATING SCALE; YOUNG ADULT;

ADULT; ANALYSIS OF VARIANCE; ASPARTIC ACID; CREATINE; FEMALE; GLUTAMIC ACID; GYRUS CINGULI; HUMANS; LIPID METABOLISM; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MEMBRANE LIPIDS; PHOSPHOLIPIDS; PHOSPHORUS ISOTOPES; PROTONS; PSYCHIATRIC STATUS RATING SCALES; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84942371078     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2015.07.013     Document Type: Article

References (53)

1. Aoyama N., Theberge J., Drost D.J., Manchanda R., Northcott S., Neufeld R.W., Menon R.S., Rajakumar N., Pavlosky W.F., Densmore M., Schaefer B., Williamson P.C. Grey matter and social functioning correlates of glutamatergic metabolite loss in schizophrenia. Br. J. Psychiatry 2011, 198(6):448-456.
2. Bartha R., Williamson P.C., Drost D.J., Malla A., Carr T.J., Cortese L., Canaran G., Rylett R.J., Neufeld R.W. Measurement of glutamate and glutamine in the medial prefrontal cortex of never-treated schizophrenic patients and healthy controls by proton magnetic resonance spectroscopy. Arch. Gen. Psychiatry 1997, 54(10):959-965.
3. Berger G.E., Wood S.J., Wellard R.M., Proffitt T.M., McConchie M., Amminger G.P., Jackson G.D., Velakoulis D., Pantelis C., McGorry P.D. Ethyl-eicosapentaenoic acid in first-episode psychosis. A 1H-MRS study. Neuropsychopharmacology 2008, 33(10):2467-2473.
4. Bondi C., Matthews M., Moghaddam B. Glutamatergic animal models of schizophrenia. Curr. Pharm. Des. 2012, 18(12):1593-1604.
5. Coyle J.T. The GABA-glutamate connection in schizophrenia: which is the proximate cause?. Biochem. Pharmacol. 2004, 68(8):1507-1514.
6. de la Fuente-Sandoval C., Leon-Ortiz P., Azcarraga M., Stephano S., Favila R., Diaz-Galvis L., Alvarado-Alanis P., Ramirez-Bermudez J., Graff-Guerrero A. Glutamate levels in the associative striatum before and after 4weeks of antipsychotic treatment in first-episode psychosis: a longitudinal proton magnetic resonance spectroscopy study. JAMA Psychiatry 2013, 70(10):1057-1066.
7. Deicken R.F., Merrin E.L., Floyd T.C., Weiner M.W. Correlation between left frontal phospholipids and Wisconsin Card Sort Test performance in schizophrenia. Schizophr. Res. 1995, 14(2):177-181.
8. Erecinska M., Silver I.A. Metabolism and role of glutamate in mammalian brain. Prog. Neurobiol. 1990, 35(4):245-296.
9. Farooqui A.A., Horrocks L.A., Farooqui T. Glycerophospholipids in brain: their metabolism, incorporation into membranes, functions, and involvement in neurological disorders. Chem. Phys. Lipids 2000, 106(1):1-29.
10. Farooqui A.A., Ong W.Y., Horrocks L.A., Chen P., Farooqui T. Comparison of biochemical effects of statins and fish oil in brain: the battle of the titans. Brain Res. Rev. 2007, 56(2):443-471.
11. Finlay J.M., Zigmond M.J. The effects of stress on central dopaminergic neurons: possible clinical implications. Neurochem. Res. 1997, 22(11):1387-1394.
12. Gangadhar B.N., Jayakumar P.N., Subbakrishna D.K., Janakiramaiah N., Keshavan M.S. Basal ganglia high-energy phosphate metabolism in neuroleptic-naive patients with schizophrenia: a 31-phosphorus magnetic resonance spectroscopic study. Am. J. Psychiatry 2004, 161(7):1304-1306.
13. Grace A.A. Cortical regulation of subcortical dopamine systems and its possible relevance to schizophrenia. J. Neural Transm. Gen. Sect. 1993, 91(2-3):111-134.
14. Gussew A., Erdtel M., Hiepe P., Rzanny R., Reichenbach J.R. Absolute quantitation of brain metabolites with respect to heterogeneous tissue compositions in 1H-MR spectroscopic volumes. Magn. Reson. Mater. Phys. 2012, 25(5):321-333.
15. Hetherington H.P., Spencer D.D., Vaughan J.T., Pan J.W. Quantitative 31P spectroscopic imaging of human brain at 4 Tesla: assessment of gray and white matter differences of phosphocreatine and ATP. Magn. Reson. Med. 2001, 45:46-52.
16. Hoen W.P., Lijmer J.G., Duran M., Wanders R.J., van Beveren N.J., de Haan L. Red blood cell polyunsaturated fatty acids measured in red blood cells and schizophrenia: a meta-analysis. Psychiatry Res. 2013, 207(1-2):1-12.
17. Horrobin D.F. The membrane phospholipid hypothesis as a biochemical basis for the neurodevelopmental concept of schizophrenia. Schizophr. Res. 1998, 30(3):193-208.
18. Horrobin D.F., Glen A.I., Vaddadi K. The membrane hypothesis of schizophrenia. Schizophr. Res. 1994, 13(3):195-207.
19. Jayakumar P.N., Gangadhar B.N., Subbakrishna D.K., Janakiramaiah N., Srinivas J.S., Keshavan M.S. Membrane phospholipid abnormalities of basal ganglia in never-treated schizophrenia: a 31P magnetic resonance spectroscopy study. Biol. Psychiatry 2003, 54(4):491-494.
20. Jensen J.E., Miller J., Williamson P.C., Neufeld R.W., Menon R.S., Malla A., Manchanda R., Schaefer B., Densmore M., Drost D.J. Focal changes in brain energy and phospholipid metabolism in first-episode schizophrenia: 31P-MRS chemical shift imaging study at 4 Tesla. Br. J. Psychiatry 2004, 184:409-415.
21. Jensen J.E., Miller J., Williamson P.C., Neufeld R.W., Menon R.S., Malla A., Manchanda R., Schaefer B., Densmore M., Drost D.J. Grey and white matter differences in brain energy metabolism in first episode schizophrenia: 31P-MRS chemical shift imaging at 4 Tesla. Psychiatry Res. 2006, 146(2):127-135.
22. Kanai Y., Clemencon B., Simonin A., Leuenberger M., Lochner M., Weisstanner M., Hediger M.A. The SLC1 high-affinity glutamate and neutral amino acid transporter family. Mol. Asp. Med. 2013, 34(2-3):108-120.
23. Kantrowitz J., Javitt D.C. Glutamatergic transmission in schizophrenia: from basic research to clinical practice. Curr. Opin. Psychiatry 2012, 25(2):96-102.
24. Kato T., Shioiri T., Murashita J., Hamakawa H., Inubushi T., Takahashi S. Lateralized abnormality of high-energy phosphate and bilateral reduction of phosphomonoester measured by phosphorus-31 magnetic resonance spectroscopy of the frontal lobes in schizophrenia. Psychiatry Res. 1995, 61(3):151-160.
25. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 1987, 13(2):261-276.
26. Keshavan M.S. Development, disease and degeneration in schizophrenia: a unitary pathophysiological model. J. Psychiatr. Res. 1999, 33(6):513-521.
27. Keshavan M.S., Pettegrew J.W., Panchalingam K., Kaplan D., Brar J., Campbell K. In vivo 31P nuclear magnetic resonance (NMR) spectroscopy of the frontal lobe metabolism in neuroleptic naive first episode psychoses. Schizophr. Res. 1989, 2:122.
28. Keshavan M.S., Stanley J.A., Pettegrew J.W. Magnetic resonance spectroscopy in schizophrenia: methodological issues and findings-part II. Biol. Psychiatry 2000, 48(5):369-380.
29. Kraguljac N.V., White D.M., Reid M.A., Lahti A.C. Increased hippocampal glutamate and volumetric deficits in unmedicated patients with schizophrenia. JAMA Psychiatry 2013, 70(12):1294-1302.
30. Marsman A., van den Heuvel M.P., Klomp D.W., Kahn R.S., Luijten P.R., Hulshoff Pol H.E. Glutamate in schizophrenia: a focused review and meta-analysis of (1)H-MRS studies. Schizophr. Bull. 2013, 39(1):120-129.
31. Michaelis E.K. Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog. Neurobiol. 1998, 54(4):369-415.
32. Olney J.W., Newcomer J.W., Farber N.B. NMDA receptor hypofunction model of schizophrenia. J. Psychiatr. Res. 1999, 33(6):523-533.
33. Pettegrew J.W., Keshavan M.S., Panchalingam K., Strychor S., Kaplan D.B., Tretta M.G., Allen M. Alterations in brain high-energy phosphate and membrane phospholipid metabolism in first-episode, drug-naive schizophrenics. A pilot study of the dorsal prefrontal cortex by in vivo phosphorus 31 nuclear magnetic resonance spectroscopy. Arch. Gen. Psychiatry 1991, 48(6):563-568.
34. Plitman E., Nakajima S., de la Fuente-Sandoval C., Gerretsen P., Chakravarty M.M., Kobylianskii J., Chung J.K., Caravaggio F., Iwata Y., Remington G., Graff-Guerrero A. Glutamate-mediated excitotoxicity in schizophrenia: a review. Eur. Neuropsychopharmacol. 2014, 24(10):1591-1605.
35. Poels E.M., Kegeles L.S., Kantrowitz J.T., Slifstein M., Javitt D.C., Lieberman J.A., Abi-Dargham A., Girgis R.R. Imaging glutamate in schizophrenia: review of findings and implications for drug discovery. Mol. Psychiatry 2014, 19(1):20-29.
36. Provencher S.W. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson. Med. 1993, 30:672-679.
37. Reid M.S., Hsu K., Berger S.P. Cocaine and amphetamine preferentially stimulate glutamate release in the limbic system: studies on the involvement of dopamine. Synapse 1997, 27(2):95-105.
38. Ross B. Biochemical considerations in sup 1H spectroscopy: glutamate and glutamine myo-inositol and related metabolites. NMR Biomed. 1991, 4:59-63.
39. Shioiri T., Kato T., Inubushi T., Murashita J., Takahashi S. Correlations of phosphomonoesters measured by phosphorus-31 magnetic resonance spectroscopy in the frontal lobes and negative symptoms in schizophrenia. Psychiatry Res. 1994, 55(4):223-235.
40. Shioiri T., Someya T., Murashita J., Kato T., Hamakawa H., Fujii K., Inubushi T. Multiple regression analysis of relationship between frontal lobe phosphorus metabolism and clinical symptoms in patients with schizophrenia. Psychiatry Res. 1997, 76(2-3):113-122.
41. Smesny S., Rosburg T., Nenadic I., Fenk K.P., Kunstmann S., Rzanny R., Volz H.P., Sauer H. Metabolic mapping using 2D (31)P-MR spectroscopy reveals frontal and thalamic metabolic abnormalities in schizophrenia. Neuroimage 2007, 35(2):729-737.
42. Stanley J.A., Williamson P.C., Drost D.J., Carr T.J., Rylett R.J., Morrison-Stewart S., Thompson R.T. Membrane phospholipid metabolism and schizophrenia: an in vivo 31P-MR spectroscopy study. Schizophr. Res. 1994, 13(3):209-215.
43. Stanley J.A., Williamson P.C., Drost D.J., Carr T.J., Rylett R.J., Malla A., Thompson R.T. An in vivo study of the prefrontal cortex of schizophrenic patients at different stages of illness via phosphorus magnetic resonance spectroscopy. Arch. Gen. Psychiatry 1995, 52(5):399-406.
44. 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. Technol. 2009, 20:1-9.
45. Theberge J., Bartha R., Drost D.J., Menon R.S., Malla A., Takhar J., Neufeld R.W., Rogers J., Pavlosky W., Schaefer B., Densmore M., Al-Semaan Y., Williamson P.C. Glutamate and glutamine measured with 4.0T proton MRS in never-treated patients with schizophrenia and healthy volunteers. Am. J. Psychiatry 2002, 159(11):1944-1946.
46. Theberge J., Williamson K.E., Aoyama N., Drost D.J., Manchanda R., Malla A.K., Northcott S., Menon R.S., Neufeld R.W., Rajakumar N., Pavlosky W., Densmore M., Schaefer B., Williamson P.C. Longitudinal grey-matter and glutamatergic losses in first-episode schizophrenia. Br. J. Psychiatry 2007, 191:325-334.
47. Vanhamme L., van den Boogaart A., Van Huffel S.J. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. Magn. Reson. 1997, 129:35-43.
48. Vogt B.A. Structural organization of cingulate cortex: areas, neurons, and somatodendritic transmitter receptors. Neurobiology of Cingulate Cortex and Limbic Thalamus 1993, 19-70. Birkhauser, Boston. B.A. Vogt, M. Gabriel (Eds.).
49. Volz H.P., Hubner G., Rzanny R., Rossger G., Preussler B., Eichhorn M., Kreitschmann-Andermahr I., Kaiser W.A., Sauer H. High-energy phosphates in the frontal lobe correlate with Wisconsin Card Sort Test performance in controls, not in schizophrenics: a 31phosphorus magnetic resonance spectroscopic and neuropsychological investigation. Schizophr. Res. 1998, 31(1):37-47.
50. Volz H.R., Riehemann S., Maurer I., Smesny S., Sommer M., Rzanny R., Holstein W., Czekalla J., Sauer H. Reduced phosphodiesters and high-energy phosphates in the frontal lobe of schizophrenic patients: a (31)P chemical shift spectroscopic-imaging study. Biol. Psychiatry 2000, 47(11):954-961.
51. Williamson P.C., Brauer M., Leonard S., Thompson T., Drost D. 31P magnetic resonance spectroscopy studies in schizophrenia. Prostaglandins Leukot. Essent. Fatty Acids 1996, 55(1-2):115-118.
52. Wittchen H.-U., Fydrich T., Zaudig M. Strukturiertes Klinisches Interview für DSM-IV 1997, Göttingen Hogrefe Verlag.
53. Yin D.M., Chen Y.J., Sathyamurthy A., Xiong W.C., Mei L. Synaptic dysfunction in schizophrenia. Adv. Exp. Med. Biol. 2012, 970:493-516.