Abnormal fatty acid pattern in the superior temporal gyrus distinguishes bipolar disorder from major depression and schizophrenia and resembles multiple sclerosis

Psychiatry Research

Volumn 215, Issue 3, 2014, Pages 560-567

  McNamara, Robert K ^a   Rider, Therese ^a   Jandacek, Ronald ^a   Tso, Patrick ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Bipolar disorder; Lithium; Major depressive disorder; Multiple sclerosis; Schizophrenia; Valproic acid

Indexed keywords

ADRENIC ACID; ANTIDEPRESSANT AGENT; ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; DOCOSAPENTAENOIC ACID; FATTY ACID; GAMMA LINOLENIC ACID; LINOLEIC ACID; LITHIUM; MONOUNSATURATED FATTY ACID; MYRISTIC ACID; NEUROLEPTIC AGENT; OLEIC ACID; PALMITIC ACID; PALMITOLEIC ACID; POLYUNSATURATED FATTY ACID; SATURATED FATTY ACID; STEARIC ACID; VACCENIC ACID; VALPROIC ACID; UNSATURATED FATTY ACID;

ADULT; ARTICLE; AUTOPSY; BIPOLAR DISORDER; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DIFFERENTIAL DIAGNOSIS; FEMALE; GAS CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; LIPID COMPOSITION; MAJOR DEPRESSION; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; SCHIZOPHRENIA; SUPERIOR TEMPORAL GYRUS; CASE CONTROL STUDY; METABOLISM; PATHOLOGY; POSTMORTEM CHANGE; PSYCHOLOGY; TEMPORAL LOBE;

ADULT; BIPOLAR DISORDER; CASE-CONTROL STUDIES; DEPRESSIVE DISORDER, MAJOR; FATTY ACIDS; FATTY ACIDS, UNSATURATED; FEMALE; HUMANS; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS; POSTMORTEM CHANGES; SCHIZOPHRENIA; TEMPORAL LOBE;

EID: 84900354593     PISSN: 01651781     EISSN: 18727123     Source Type: Journal    
DOI: 10.1016/j.psychres.2013.12.022     Document Type: Article

References (84)

1. Alling C., Vanier M.T., Svennerholm L. Lipid alterations in apparently normal white matter in multiple sclerosis. Brain Research 1971, 35:325-336.
2. Allison T., Puce A., McCarthy G. Social perception from visual cues: role of the STS region. Trends in Cognitive Sciences 2000, 4:267-278.
3. Amminger G.P., Schäfer M.R., Papageorgiou K., Klier C.M., Cotton S.M., Harrigan S.M., Mackinnon A., McGorry P.D., Berger G.E. Long-chain omega-3 fatty acids for indicated prevention of psychotic disorders: a randomized, placebo-controlled trial. Archives of General Psychiatry 2010, 67:146-154.
4. Appleton K.M., Rogers P.J., Ness A.R. Updated systematic review and meta-analysis of the effects of n-3 long-chain polyunsaturated fatty acids on depressed mood. American Journal of Clinical Nutrition 2010, 91:757-770.
5. Arnsten A.F., Rubia K. Neurobiological circuits regulating attention, cognitive control, motivation, and emotion: disruptions in neurodevelopmental psychiatric disorders. Journal of the American Academy of Child and Adolescent Psychiatry 2012, 51:356-367.
6. Arvindakshan M., Ghate M., Ranjekar P.K., Evans D.R., Mahadik S.P. Supplementation with a combination of omega-3 fatty acids and antioxidants (vitamins E and C) improves the outcome of schizophrenia. Schizophrenia Research 2003, 62:195-204.
7. Bazinet R.P., Rao J.S., Chang L., Rapoport S.I., Lee H.J. Chronic valproate does not alter the kinetics of docosahexaenoic acid within brain phospholipids of the unanesthetized rat. Psychopharmacology 2005, 182:180-185.
8. Bazinet R.P., Rao J.S., Chang L., Rapoport S.I., Lee H.J. Chronic valproate does not alter the kinetics of docosahexaenoic acid within brain phospholipids of the unanesthetized rat. Psychopharmacology 2005, 182:180-185.
9. Beasley C.L., Chana G., Honavar M., Landau S., Everall I.P., Cotter D. Evidence for altered neuronal organisation within the planum temporale in major psychiatric disorders. Schizophrenia Research 2005, 73:69-78.
10. Beasley C.L., Honavar M., Everall I.P., Cotter D. Two-dimensional assessment of cytoarchitecture in the superior temporal white matter in schizophrenia, major depressive disorder and bipolar disorder. Schizophrenia Research 2009, 115:156-162.
11. Bellani M., Perlini C., Ferro A., Cerruti S., Rambaldelli G., Isola M., Cerini R., Dusi N., Andreone N., Balestrieri M., Pozzi Mucelli R., Tansella M., Brambilla P. White matter microstructure alterations in bipolar disorder. Functional Neurology 2012, 27:29-34.
12. Bourre J.M., Dumont O.L., Clément M.E., Durand G.A. Endogenous synthesis cannot compensate for absence of dietary oleic acid in rats. Journal of Nutrition 1997, 127:488-493.
13. Breunis M.N., Kupka R.W., Nolen W.A., Suppes T., Denicoff K.D., Leverich G.S., Post R.M. Drexhage HA. High numbers of circulating activated T cells and raised levels of serum IL-2 receptor in bipolar disorder. Biological Psychiatry 2003, 53:157-165.
14. Byatt N., Rothschild A.J., Riskind P., Ionete C., Hunt A.T. Relationships between multiple sclerosis and depression. Journal of Neuropsychiatry and Clinical Neurosciences 2011, 23:198-200.
15. Carver J.D., Benford V.J., Han B., Cantor A.B. The relationship between age and the fatty acid composition of cerebral cortex and erythrocytes in human subjects. Brain Research Bulletin 2001, 56:79-85.
16. Chang M.C., Grange E., Rabin O., Bell J.M., Allen D.D., Rapoport S.I. Lithium decreases turnover of arachidonate in several brain phospholipids. Neuroscience Letters 1996, 220:171-174.
17. Chang M.C., Contreras M.A., Rosenberger T.A., Rintala J.J., Bell J.M., Rapoport S.I. Chronic valproate treatment decreases the in vivo turnover of arachidonic acid in brain phospholipids: a possible common effect of mood stabilizers. Journal of Neurochemistry 2001, 77:796-803.
18. Chen H.H, Nicoletti M.A., Hatch J.P., Sassi R.B., Axelson D., Brambilla P., Monkul E.S., Keshavan M.S., Ryan N.D., Birmaher B., Soares J.C. Abnormal left superior temporal gyrus volumes in children and adolescents with bipolar disorder: a magnetic resonance imaging study. Neuroscience Letters 2004, 363:65-68.
19. Chiu C.C., Huang S.Y., Su K.P., Lu M.L., Huang M.C., Chen C.C., Shen W.W. Polyunsaturated fatty acid deficit in patients with bipolar mania. European Neuropsychopharmacology 2003, 13:99-103.
20. Conklin S.M., Runyan C.A., Leonard S., Reddy R.D., Muldoon M.F., Yao J.K. Age-related changes of n-3 and n-6 polyunsaturated fatty acids in the anterior cingulate cortex of individuals with major depressive disorder. Prostaglandins, Leukotrienes and Essential Fatty Acids 2010, 82:111-119.
21. Diau G.Y., Hsieh A.T., Sarkadi-Nagy E.A., Wijendran V., Nathanielsz P.W., Brenna J.T. The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system. BMC Medical 2005, 3:11.
22. Dullemeijer C., Zock P.L., Coronel R., Den Ruijter H.M., Katan M.B., Brummer R.J., Kok F.J., Beekman J., Brouwer I.A. Differences in fatty acid composition between cerebral brain lobes in juvenile pigs after fish oil feeding. British Journal of Nutrition 2008, 100:794-800.
23. Edwards L.J., Constantinescu C.S. A prospective study of conditions associated with multiple sclerosis in a cohort of 658 consecutive outpatients attending a multiple sclerosis clinic. Multiple Sclerosis 2004, 10:575-581.
24. Emsley R., Myburgh C., Oosthuizen P., van Rensburg S.J. Randomized, placebo-controlled study of ethyl-eicosapentaenoic acid as supplemental treatment in schizophrenia. American Journal of Psychiatry 2002, 159:1596-1598.
25. Farooqui A.A., Horrocks L.A. Brain phospholipases A2: a perspective on the history. Prostaglandins, Leukotrienes and Essential Fatty Acids 2004, 71:161-169.
26. Fitzgerald P.B., Laird A.R., Maller J., Daskalakis Z.J. A meta-analytic study of changes in brain activation in depression. Human Brain Mapping 2008, 29:683-695.
27. Freeman M.P., Hibbeln J.R., Wisner K.L., Davis J.M., Mischoulon D., Peet M., Keck P.E., Marangell L.B., Richardson A.J., Lake J., Stoll A.L. Omega-3 fatty acids: evidence basis for treatment and future research in psychiatry. Journal of Clinical Psychiatry 2006, 67:1954-1967.
28. Galeazzi G.M., Ferrari S., Giaroli G., Mackinnon A., Merelli E., Motti L., Rigatelli M. Psychiatric disorders and depression in multiple sclerosis outpatients: impact of disability and interferon beta therapy. Neurological Sciences 2005, 26:255-262.
29. Garbay B., Boiron-Sargueil F., Shy M., Chbihi T., Jiang H., Kamholz J., Cassagne C. Regulation of oleoyl-CoA synthesis in the peripheral nervous system: demonstration of a link with myelin synthesis. Journal of Neurochemistry 1998, 71:1719-1726.
30. Hamazaki K., Choi K.H., Kim H.Y. Phospholipid profile in the postmortem hippocampus of patients with schizophrenia and bipolar disorder: no changes in docosahexaenoic acid species. Journal of Psychiatric Research 2010, 44:688-693.
31. Hamazaki K., Hamazaki T., Inadera H. Fatty acid composition in the postmortem amygdala of patients with schizophrenia, bipolar disorder, and major depressive disorder. Journal of Psychiatric Research 2012, 46:1024-1028.
32. Hamazaki K., Hamazaki T., Inadera H. Abnormalities in the fatty acid composition of the postmortem entorhinal cortex of patients with schizophrenia, bipolar disorder, and major depressive disorder. Psychiatry Research 2013, 210:346-350.
33. Homa S.T., Belin J., Smith A.D., Monro J.A., Zilkha K.J. Levels of linoleate and arachidonate in red blood cells of healthy individuals and patients with multiple sclerosis. Journal of Neurology, Neurosurgery, and Psychiatry 1980, 43:106-110.
34. Horrobin D.F., Manku M.S., Hillman H., Iain A., Glen M. Fatty acid levels in the brains of schizophrenics and normal controls. Biological Psychiatry 1991, 30:795-805.
35. Igarashi M., Ma K., Gao F., Kim H.W., Greenstein D., Rapoport S.I., Rao J.S. Brain lipid concentrations in bipolar disorder. Journal of Psychiatric Research 2010, 44:177-182.
36. Joffe R.T., Lippert G.P., Gray T.A., Sawa G., Horvath Z. Mood disorder and multiple sclerosis. Archives of Neurology 1987, 44:376-378.
37. 3H]arachidonic acid from blood in rat brain synaptosomal fractions before and after cholinergic stimulation. Journal of Neurochemistry 1996, 67:822-829.
38. Jones L.D., Payne M.E., Messer D.F., Beyer J.L., MacFall J.R., Krishnan K.R., Taylor W.D. Temporal lobe volume in bipolar disorder: relationship with diagnosis and antipsychotic medication use. Journal of Affective Disorders 2009, 114:50-57.
39. Landén M., Davidsson P., Gottfries C.G., Månsson J.E., Blennow K. Reduction of the synaptophysin level but normal levels of glycerophospholipids in the gyrus cinguli in schizophrenia. Schizophrenia Research 2002, 55:83-88.
40. Lee C.H., Hajra A.K. Molecular species of diacylglycerols and phosphoglycerides and the postmortem changes in the molecular species of diacylglycerols in rat brains. Journal of Neurochemistry 1991, 56:370-379.
41. Lin P.Y., Huang S.Y., Su K.P. A meta-analytic review of polyunsaturated fatty acid compositions in patients with depression. Biological Psychiatry 2010, 68:140-147.
42. Lin P.Y., Su K.P. A meta-analytic review of double-blind, placebo-controlled trials of antidepressant efficacy of omega-3 fatty acids. Journal of Clinical Psychiatry 2007, 68:1056-1061.
43. Liu Y., Jandacek R., Rider T., Tso P., McNamara R.K. Elevated delta-6 desaturase (FADS2) gene expression in the postmortem prefrontal cortex of schizophrenic patients: Relationship with fatty acid composition. Schizophrenia Research 2009, 109:113-120.
44. Liu Y., McNamara R.K. Elevated delta-6 desaturase (FADS2) gene expression in the prefrontal cortex of patients with bipolar disorder. Journal of Psychiatric Research 2011, 45:269-272.
45. Mahon K., Burdick K.E., Ikuta T., Braga R.J., Gruner P., Malhotra A.K., Szeszko P.R. Abnormal temporal lobe white matter as a biomarker for genetic risk of bipolar disorder. Biological Psychiatry 2013, 73:177-182.
46. Martins J.G. EPA but not DHA appears to be responsible for the efficacy of omega-3 long chain polyunsaturated fatty acid supplementation in depression: evidence from a meta-analysis of randomized controlled trials. Journal of the American College of Nutrition 2009, 28:525-542.
47. McNamara R.K., Ostrander M., Abplanalp W., Richtand N.M., Benoit S., Clegg D. Modulation of phosphoinositide-protein kinase C signal transduction by omega-3 fatty acids: Implications for the pathophysiology and treatment of recurrent neuropsychiatric illness. Prostaglandins, Leukotrienes and Essential Fatty Acids 2006, 75:237-257.
48. McNamara R.K., Jandacek R., Rider T., Tso P., Richtand N.M., Stanford K. Abnormalities in the fatty acid composition of the postmortem orbitofrontal cortex of schizophrenic patients: Gender differences and partial normalization with antipsychotic medications. Schizophrenia Research 2007, 91:37-50.
49. McNamara R.K., Hahn C-G., Jandacek R., Rider T., Tso P., Stanford K., Richtand N.M. Selective deficits in the omega-3 fatty acid docosahexaenoic acid in the postmortem orbitofrontal cortex of patients with major depressive disorder. Biological Psychiatry 2007, 62:17-24.
50. McNamara R.K., Jandacek R., Rider T., Tso P., Stanford K., Hahn C-G., Richtand N.M. Deficits in docosahexaenoic acid and associated elevations in the metabolism of arachidonic acid and saturated fatty acids in the postmortem orbitofrontal cortex of patients with bipolar disorder. Psychiatry Research 2008, 160:285-299.
51. McNamara R.K., Liu Y., Jandacek R., Rider T., Tso P. The aging human orbitofrontal cortex: Decreasing polyunsaturated fatty acid composition and associated increases in lipogenic gene expression and stearoyl-CoA desaturase activity. Prostaglandins, Leukotrienes and Essential Fatty Acids 2008, 78:293-304.
52. McNamara R.K., Sullivan J., Richtand N.M. Omega-3 fatty acid deficiency augments amphetamine-induced behavioral sensitization in adult mice: Prevention by chronic lithium treatment. Journal of Psychiatric Research 2008, 42:458-468.
53. McNamara R.K., Jandacek R., Rider T., Tso P., Dwivedi Y., Pandey G.N. Selective deficits in erythrocyte docosahexaenoic acid composition in adult patients with bipolar disorder and major depressive disorder. Journal of Affective Disorders 2010, 126:303-311.
54. McNamara R.K., Jandacek R. Investigation of postmortem brain polyunsaturated fatty acid composition in psychiatric disorders: Limitations, challenges, and future directions. Journal of Psychiatric Research 2011, 45:44-46.
55. McNamara R.K., Lotrich F.E. Elevated immune-inflammatory signaling in mood disorders: A new therapeutic target?. Expert Review of Neurotherapeutics 2012, 12:1143-1161.
56. McNamara R.K., Jandacek R., Tso P., Dwivedi Y., Ren X., Pandey G.N. Lower docosahexaenoic acid concentrations in the postmortem prefrontal cortex of adult depressed suicide victims compared with controls without cardiovascular disease. Journal of Psychiatric Research 2013, 47:1187-1191.
57. McNamara R.K. Deciphering the role of docosahexaenoic acid in brain maturation and pathology with magnetic resonance imaging. Prostaglandins, Leukotrienes and Essential Fatty Acids 2013, 88:33-42.
58. Navarro X., Segura R. Red blood cell fatty acids in multiple sclerosis. Acta Neurologica Scandinavica 1989, 79:32-37.
59. Nightingale S., Woo E., Smith A.D., French J.M., Gale M.M., Sinclair H.M., Bates D., Shaw D.A. Red blood cell and adipose tissue fatty acids in mild inactive multiple sclerosis. Acta Neurologica Scandinavica 1990, 82:43-50.
60. Ntambi J.M. Regulation of stearoyl-CoA desaturase by polyunsaturated fatty acids and cholesterol. Journal of Lipid Research 1999, 40:1549-1558.
61. Nudmamud S., Reynolds L.M., Reynolds G.P. N-acetylaspartate and N-Acetylaspartylglutamate deficits in superior temporal cortex in schizophrenia and bipolar disorder: a postmortem study. Biological Psychiatry 2003, 53:1138-1141.
62. Ohler B., Graf K., Bragg R., Lemons T., Coe R., Genain C., Israelachvili J., Husted C. Role of lipid interactions in autoimmune demyelination. Biochimica et Biophysica Acta 2004, 1688:10-17.
63. Padmos R.C., Bekris L., Knijff E.M., Tiemeier H., Kupka R.W., Cohen D., Nolen W.A., Lernmark A., Drexhage H.A. A high prevalence of organ-specific autoimmunity in patients with bipolar disorder. Biological Psychiatry 2004, 56:476-482.
64. Padmos R.C., Hillegers M.H., Knijff E.M., Vonk R., Bouvy A., Staal F.J., de Ridder D., Kupka R.W., Nolen W.A., Drexhage H.A. A discriminating messenger RNA signature for bipolar disorder formed by an aberrant expression of inflammatory genes in monocytes. Archives of General Psychiatry 2008, 65:395-407.
65. Paton C.M., Ntambi J.M. Biochemical and physiological function of stearoyl-CoA desaturase. American Journal of Physiology, Endocrinology, and Metabolism 2009, 297:28-37.
66. Rao J.S., Ertley R.N., DeMar J.C., Rapoport S.I., Bazinet R.P., Lee H.J. Dietary n-3 PUFA deprivation alters expression of enzymes of the arachidonic and docosahexaenoic acid cascades in rat frontal cortex. Molecular Psychiatry 2007, 12:151-157.
67. Rao J.S., Keleshian V.L., Klein S., Rapoport S.I. Epigenetic modifications in frontal cortex from Alzheimer's disease and bipolar disorder patients. Translational Psychiatry 2012, 2:e132.
68. Sarris J., Mischoulon D., Schweitzer I. Omega-3 for bipolar disorder: meta-analyses of use in mania and bipolar depression. Journal of Clinical Psychiatry 2012, 73:81-86.
69. Schiffer R.B., Wineman N.M., Weitkamp L.R. Association between bipolar affective disorder and multiple sclerosis. American Journal of Psychiatry 1986, 143:94-95.
70. Sublette M.E., Milak M.S., Hibbeln J.R., Freed P.J., Oquendo M.A., Malone K.M., Parsey R.V., Mann J.J. Plasma polyunsaturated fatty acids and regional cerebral glucose metabolism in major depression. Prostaglandins, Leukotrienes and Essential Fatty Acids 2009, 80:57-64.
71. Sublette M.E., Ellis S.P., Geant A.L., Mann J.J. Meta-analysis of the effects of eicosapentaenoic acid (EPA) in clinical trials in depression. Journal of Clinical Psychiatry 2011, 72:1577-1584.
72. Suzuki H., Manabe S., Wada O., Crawford M.A. Rapid incorporation of docosahexaenoic acid from dietary sources into brain microsomal, synaptosomal and mitochondrial membranes in adult mice. International Journal of Vitamin and Nutrition Research 1997, 67:272-278.
73. Taha A.Y., Cheon Y., Ma K., Rapoport S.I., Rao J.S. Altered fatty acid concentrations in prefrontal cortex of schizophrenic patients. Journal of Psychiatric Research 2013, 47:636-643.
74. Takahashi T., Malhi G.S., Wood S.J., Yücel M., Walterfang M., Kawasaki Y., Suzuki M., Pantelis C. Gray matter reduction of the superior temporal gyrus in patients with established bipolar I disorder. Journal of Affective Disorders 2010, 123:276-282.
75. Takahashi T., Wood S.J., Yung A.R., Soulsby B., McGorry P.D., Suzuki M., Kawasaki Y., Phillips L.J., Velakoulis D., Pantelis C. Progressive gray matter reduction of the superior temporal gyrus during transition to psychosis. Archives of General Psychiatry 2009, 66:366-376.
76. Tatebayashi Y., Nihonmatsu-Kikuchi N., Hayashi Y., Yu X., Soma M., Ikeda K. Abnormal fatty acid composition in the frontopolar cortex of patients with affective disorders. Translational Psychiatry 2012, 2:e204.
77. Torrey E.F., Webster M., Knable M., Johnston N., Yolken R.H. The stanley foundation brain collection and neuropathology consortium. Schizophrenia Research 2000, 44:151-155.
78. Umhau J.C., Zhou W., Carson R.E., Rapoport S.I., Polozova A., Demar J., Hussein N., Bhattacharjee A.K., Ma K., Esposito G., Majchrzak S., Herscovitch P., Eckelman W.C., Kurdziel K.A., Salem N. Imaging incorporation of circulating docosahexaenoic acid into the human brain using positron emission tomography. Journal of Lipid Research 2009, 50:1259-1268.
79. van der Kemp W.J., Klomp D.W., Kahn R.S., Luijten P.R., Hulshoff Pol H.E. A meta-analysis of the polyunsaturated fatty acid composition of erythrocyte membranes in schizophrenia. Schizophrenia Research 2012, 141:153-161.
80. Wilson R., Bell M.V. Molecular species composition of glycerophospholipids from white matter of human brain. Lipids 1993, 28:13-17.
81. Wilson R., Tocher D.R. Lipid and fatty acid composition is altered in plaque tissue from multiple sclerosis brain compared with normal brain white matter. Lipids 1991, 26:9-15.
82. Woelk H., Borri P. Lipid and fatty acid composition of myelin purified from normal and MS brains. European Neurology 1973, 10:250-260.
83. Xiao Y., Huang Y., Chen Z.Y. Distribution, depletion and recovery of docosahexaenoic acid are region-specific in rat brain. British Journal of Nutrition 2005, 94:544-550.
84. Yao J.K., Leonard S., Reddy R.D. Membrane phospholipid abnormalities in postmortem brains from schizophrenic patients. Schizophrenia Research 2000, 42:7-17.