Chronic clozapine reduces rat brain arachidonic acid metabolism by reducing plasma arachidonic acid availability

Journal of Neurochemistry

Volumn 124, Issue 3, 2013, Pages 376-387

  Modi, Hiren R ^a   Taha, Ameer Y ^a   Kim, Hyung Wook ^a   Chang, Lisa ^a   Rapoport, Stanley I ^a   Cheon, Yewon ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

antipsychotic; arachidonic acid; bipolar disorder; clozapine; phospholipid; rat brain

Indexed keywords

ACYL COENZYME A; ARACHIDONIC ACID; CARBON 14; CLOZAPINE; OLANZAPINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; PHOSPHOLIPID; PROSTAGLANDIN SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARACHIDONIC ACID METABOLISM; ARTICLE; BIOAVAILABILITY; BIPOLAR DISORDER; BLOOD SAMPLING; BRAIN TISSUE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ESTERIFICATION; IN VIVO STUDY; KINETICS; LIPID BRAIN LEVEL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STEADY STATE; TREATMENT DURATION;

ANIMALS; ANTIPSYCHOTIC AGENTS; ARACHIDONIC ACID; BRAIN; CLOZAPINE; DOWN-REGULATION; MALE; RATS; RATS, INBRED F344;

RATTUS;

EID: 84872069674     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12078     Document Type: Article

References (88)

1. Albaugh V. L., Henry C. R., Bello N. T., Hajnal A., Lynch S. L., Halle B., and, Lynch C. J., (2006) Hormonal and metabolic effects of olanzapine and clozapine related to body weight in rodents. Obesity (Silver Spring) 14, 36-51.
2. Albaugh V. L., Judson J. G., She P., Lang C. H., Maresca K. P., Joyal J. L., and, Lynch C. J., (2011) Olanzapine promotes fat accumulation in male rats by decreasing physical activity, repartitioning energy and increasing adipose tissue lipogenesis while impairing lipolysis. Mol. Psychiatry 16, 569-581.
3. Albaugh V. L., Vary T. C., Ilkayeva O., Wenner B. R., Maresca K. P., Joyal J. L., Breazeale S., Elich T. D., Lang C. H., and, Lynch C. J., (2012) Atypical antipsychotics rapidly and inappropriately switch peripheral fuel utilization to lipids, impairing metabolic flexibility in rodents. Schizophr. Bull. 38, 153-166.
4. Baldessarini R. J., Centorrino F., Flood J. G., Volpicelli S. A., Huston-Lyons D., and, Cohen B. M., (1993) Tissue concentrations of clozapine and its metabolites in the rat. Neuropsychopharmacology 9, 117-124.
5. Basselin M., Chang L., Bell J. M., and, Rapoport S. I., (2006) Chronic lithium chloride administration attenuates brain NMDA receptor-initiated signaling via arachidonic acid in unanesthetized rats. Neuropsychopharmacology 31, 1659-1674.
6. Basselin M., Villacreses N. E., Lee H. J., Bell J. M., and, Rapoport S. I., (2007) Chronic lithium administration attenuates up-regulated brain arachidonic acid metabolism in a rat model of neuroinflammation. J. Neurochem. 102, 761-772.
7. Basselin M., Kim H. W., Chen M., Ma K., Rapoport S. I., Murphy R. C., and, Farias S. E., (2010) Lithium modifies brain arachidonic and docosahexaenoic metabolism in rat lipopolysaccharide model of neuroinflammation. J. Lipid Res. 51, 1049-1056.
8. Bazinet R. P., Lee H. J., Felder C. C., Porter A. C., Rapoport S. I., and, Rosenberger T. A., (2005a) Rapid high-energy microwave fixation is required to determine the anandamide (N-arachidonoylethanolamine) concentration of rat brain. Neurochem. Res. 30, 597-601.
9. Bazinet R. P., Rao J. S., Chang L., Rapoport S. I., and, Lee H. J., (2005b) Chronic valproate does not alter the kinetics of docosahexaenoic acid within brain phospholipids of the unanesthetized rat. Psychopharmacology 182, 180-185.
10. Bazinet R. P., Rao J. S., Chang L., Rapoport S. I., and, Lee H. J., (2006) Chronic carbamazepine decreases the incorporation rate and turnover of arachidonic acid but not docosahexaenoic acid in brain phospholipids of the unanesthetized rat: relevance to bipolar disorder. Biol. Psychiatry 59, 401-407.
11. Bhattacharjee A. K., Chang L., Lee H. J., Bazinet R. P., Seemann R., and, Rapoport S. I., (2005) D2 but not D1 dopamine receptor stimulation augments brain signaling involving arachidonic acid in unanesthetized rats. Psychopharmacology 180, 735-742.
12. Bosetti F., Rintala J., Seemann R., Rosenberger T. A., Contreras M. A., Rapoport S. I., and, Chang M. C., (2002) Chronic lithium downregulates cyclooxygenase-2 activity and prostaglandin E(2) concentration in rat brain. Mol. Psychiatry 7, 845-850.
13. Bosetti F., Weerasinghe G. R., Rosenberger T. A., and, Rapoport S. I., (2003) Valproic acid down-regulates the conversion of arachidonic acid to eicosanoids via cyclooxygenase-1 and -2 in rat brain. J. Neurochem. 85, 690-696.
14. Bowden C. L., Calabrese J. R., McElroy S. L., et al,. (2000) A randomized, placebo-controlled 12-month trial of divalproex and lithium in treatment of outpatients with bipolar I disorder. Divalproex maintenance study group. Arch. Gen. Psychiatry 57, 481-489.
15. Calabrese J. R., Kimmel S. E., Woyshville M. J., Rapport D. J., Faust C. J., Thompson P. A., and, Meltzer H. Y., (1996) Clozapine for treatment-refractory mania. Am. J. Psychiatry 153, 759-764.
16. Calabrese J. R., Bowden C. L., Sachs G., et al,. (2003) A placebo-controlled 18-month trial of lamotrigine and lithium maintenance treatment in recently depressed patients with bipolar I disorder. J. Clin. Psychiatry 64, 1013-1024.
17. Chang M. C., Grange E., Rabin O., Bell J. M., Allen D. D., and, Rapoport S. I., (1996) Lithium decreases turnover of arachidonate in several brain phospholipids. Neurosci. Lett. 220, 171-174.
18. Chang M. C., Contreras M. A., Rosenberger T. A., Rintala J. J., Bell J. M., and, Rapoport S. I., (2001) Chronic valproate treatment decreases the in vivo turnover of arachidonic acid in brain phospholipids: a possible common effect of mood stabilizers. J. Neurochem. 77, 796-803.
19. Cheon Y., Park J. Y., Modi H. R., Kim H. W., Lee H. J., Chang L., Rao J. S., and, Rapoport S. I., (2011) Chronic olanzapine treatment decreases arachidonic acid turnover and prostaglandin E(2) concentration in rat brain. J. Neurochem. 119, 364-376.
20. Cipriani A., Rendell J., and, Geddes J. R., (2010) Olanzapine in the long-term treatment of bipolar disorder: a systematic review and meta-analysis. J. Psychopharmacol. 24, 1729-1738.
21. Cooper G. D., Harrold J. A., Halford J. C., and, Goudie A. J., (2008) Chronic clozapine treatment in female rats does not induce weight gain or metabolic abnormalities but enhances adiposity: implications for animal models of antipsychotic-induced weight gain. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 428-436.
22. DeGeorge J. J., Noronha J. G., Bell J., Robinson P., and, Rapoport S. I., (1989) Intravenous injection of [1-14C]arachidonate to examine regional brain lipid metabolism in unanesthetized rats. J. Neurosci. Res. 24, 413-423.
23. Demar J. C. Jr, Ma K., Chang L., Bell J. M., and, Rapoport S. I., (2005) alpha-Linolenic acid does not contribute appreciably to docosahexaenoic acid within brain phospholipids of adult rats fed a diet enriched in docosahexaenoic acid. J. Neurochem. 94, 1063-1076.
24. DeMar J. C. Jr, Lee H. J., Ma K., Chang L., Bell J. M., Rapoport S. I., and, Bazinet R. P., (2006) Brain elongation of linoleic acid is a negligible source of the arachidonate in brain phospholipids of adult rats. Biochim. Biophys. Acta 1761, 1050-1059.
25. Deutsch J., Grange E., Rapoport S. I., and, Purdon A. D., (1994) Isolation and quantitation of long-chain acyl-coenzyme A esters in brain tissue by solid-phase extraction. Anal. Biochem. 220, 321-323.
26. Deutsch J., Rapoport S. I., and, Purdon A. D., (1997) Relation between free fatty acid and acyl-CoA concentrations in rat brain following decapitation. Neurochem. Res. 22, 759-765.
27. Duncan R. E., Sarkadi-Nagy E., Jaworski K., Ahmadian M., and, Sul H. S., (2008) Identification and functional characterization of adipose-specific phospholipase A2 (AdPLA). J. Biol. Chem. 283, 25428-25436.
28. Farde L., and, Nordstrom A. L., (1992) PET analysis indicates atypical central dopamine receptor occupancy in clozapine-treated patients. Br. J. Psychiatry Suppl. 17, 30-33.
29. Fell M. J., Anjum N., Dickinson K., Marshall K. M., Peltola L. M., Vickers S., Cheetham S., and, Neill J. C., (2007) The distinct effects of subchronic antipsychotic drug treatment on macronutrient selection, body weight, adiposity, and metabolism in female rats. Psychopharmacology 194, 221-231.
30. Ferno J., Vik-Mo A. O., Jassim G., et al,. (2009) Acute clozapine exposure in vivo induces lipid accumulation and marked sequential changes in the expression of SREBP, PPAR, and LXR target genes in rat liver. Psychopharmacology 203, 73-84.
31. Folch J., Lees M., and, Sloane Stanley G. H., (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509.
32. Frye M. A., Ketter T. A., Altshuler L. L., Denicoff K., Dunn R. T., Kimbrell T. A., Cora-Locatelli G., and, Post R. M., (1998) Clozapine in bipolar disorder: treatment implications for other atypical antipsychotics. J. Affect. Disord. 48, 91-104.
33. Gavino V. C., and, Gavino G. R., (1992) Adipose hormone-sensitive lipase preferentially releases polyunsaturated fatty acids from triglycerides. Lipids 27, 950-954.
34. Geddes J. R., Goodwin G. M., Rendell J., Azorin J. M., Cipriani A., Ostacher M. J., Morriss R., Alder N., and, Juszczak E., (2010) Lithium plus valproate combination therapy versus monotherapy for relapse prevention in bipolar I disorder (BALANCE): a randomised open-label trial. Lancet 375, 385-395.
35. Ghelardoni S., Tomita Y. A., Bell J. M., Rapoport S. I., and, Bosetti F., (2004) Chronic carbamazepine selectively downregulates cytosolic phospholipase A2 expression and cyclooxygenase activity in rat brain. Biol. Psychiatry 56, 248-254.
36. Ghelardoni S., Bazinet R. P., Rapoport S. I., and, Bosetti F., (2005) Topiramate does not alter expression in rat brain of enzymes of arachidonic acid metabolism. Psychopharmacology 180, 523-529.
37. Greil W., Ludwig-Mayerhofer W., Erazo N., et al,. (1997) Lithium versus carbamazepine in the maintenance treatment of bipolar disorders-a randomised study. J. Affect. Disord. 43, 151-161.
38. Halim N. D., Weickert C. S., McClintock B. W., Weinberger D. R., and, Lipska B. K., (2004) Effects of chronic haloperidol and clozapine treatment on neurogenesis in the adult rat hippocampus. Neuropsychopharmacology 29, 1063-1069.
39. Hegerl U., (2012) Review: risperidone, olanzapine and haloperidol are the most effective drugs for acute mania in adults with bipolar I disorder. Evid. Based Ment. Health 15, 45.
40. Holman R. T., (1986) Control of polyunsaturated acids in tissue lipids. J. Am. Coll. Nutr. 5, 183-211.
41. Igarashi M., Ma K., Chang L., Bell J. M., Rapoport S. I., and, DeMar J. C., Jr, (2006) Low liver conversion rate of alpha-linolenic to docosahexaenoic acid in awake rats on a high-docosahexaenoate-containing diet. J. Lipid Res. 47, 1812-1822.
42. Igarashi M., Ma K., Gao F., Kim H. W., Greenstein D., Rapoport S. I., and, Rao J. S., (2010) Brain lipid concentrations in bipolar disorder. J. Psychiatr. Res. 44, 177-182.
43. Janowsky A., Neve K. A., Kinzie J. M., Taylor B., de Paulis T., and, Belknap J. K., (1992) Extrastriatal dopamine D2 receptors: distribution, pharmacological characterization and region-specific regulation by clozapine. J. Pharmacol. Exp. Ther. 261, 1282-1290.
44. Jutila A., Soderlund T., Pakkanen A. L., Huttunen M., and, Kinnunen P. K., (2001) Comparison of the effects of clozapine, chlorpromazine, and haloperidol on membrane lateral heterogeneity. Chem. Phys. Lipids 112, 151-163.
45. Kabbani N., and, Levenson R., (2006) Antipsychotic-induced alterations in D2 dopamine receptor interacting proteins within the cortex. NeuroReport 17, 299-301.
46. Kaddurah-Daouk R., McEvoy J., Baillie R. A., Lee D., Yao J. K., Doraiswamy P. M., and, Krishnan K. R., (2007) Metabolomic mapping of atypical antipsychotic effects in schizophrenia. Mol. Psychiatry 12, 934-945.
47. Kim H. W., Rapoport S. I., and, Rao J. S., (2010) Altered expression of apoptotic factors and synaptic markers in postmortem brain from bipolar disorder patients. Neurobiol. Dis. 37, 596-603.
48. Kim H. W., Rao J. S., Rapoport S. I., and, Igarashi M., (2011a) Dietary n-6 PUFA deprivation downregulates arachidonate but upregulates docosahexaenoate metabolizing enzymes in rat brain. Biochim. Biophys. Acta 1811, 111-117.
49. Kim H. W., Rapoport S. I., and, Rao J. S., (2011b) Altered arachidonic acid cascade enzymes in postmortem brain from bipolar disorder patients. Mol. Psychiatry 16, 419-428.
50. Kim H. W., Cheon Y., Modi H. R., Rapoport S. I., and, Rao J. S., (2012) Effects of chronic clozapine administration on markers of arachidonic acid cascade and synaptic integrity in rat brain. Psychopharmacology 222, 663-674.
51. Kirkilionis M., (2010) Exploration of cellular reaction systems. Brief. Bioinform. 11, 153-178.
52. Kontkanen O., Lakso M., Wong G., and, Castren E., (2002) Chronic antipsychotic drug treatment induces long-lasting expression of fos and jun family genes and activator protein 1 complex in the rat prefrontal cortex. Neuropsychopharmacology 27, 152-162.
53. Kushner S. F., Khan A., Lane R., and, Olson W. H., (2006) Topiramate monotherapy in the management of acute mania: results of four double-blind placebo-controlled trials. Bipolar Disord. 8, 15-27.
54. Lee H. J., Gheraldoni S., Chang L., Bosetti F., Rapoport S. I., and, Bazinet R. P., (2005) Topiramate does not alter the kinetics of arachidonic or docosahexaenoic acid in brain phospholipids of unanesthetized rats. Neurochem. Res. 30, 677-683.
55. Lee H. J., Rao J. S., Chang L., Rapoport S. I., and, Bazinet R. P., (2008) Chronic N-methyl-D-aspartate administration increases the turnover of arachidonic acid within brain phospholipids of the unanesthetized rat. J. Lipid Res. 49, 162-168.
56. Lee H. J., Rao J. S., Chang L., Rapoport S. I., and, Kim H. W., (2010) Chronic imipramine but not bupropion increases arachidonic acid signaling in rat brain: is this related to 'switching' in bipolar disorder? Mol. Psychiatry 15, 602-614.
57. Levant B., Crane J. F., and, Carlson S. E., (2006) Sub-chronic antipsychotic drug treatment does not alter brain phospholipid fatty acid composition in rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 30, 728-732.
58. Lidow M. S., and, Goldman-Rakic P. S., (1997) Differential regulation of D2 and D4 dopamine receptor mRNAs in the primate cerebral cortex vs. neostriatum: effects of chronic treatment with typical and atypical antipsychotic drugs. J. Pharmacol. Exp. Ther. 283, 939-946.
59. Meshul C. K., Bunker G. L., Mason J. N., Allen C., and, Janowsky A., (1996) Effects of subchronic clozapine and haloperidol on striatal glutamatergic synapses. J. Neurochem. 67, 1965-1973.
60. Minet-Ringuet J., Even P. C., Lacroix M., Tome D., and, de Beaurepaire R., (2006) A model for antipsychotic-induced obesity in the male rat. Psychopharmacology 187, 447-454.
61. Modi H. R., Cheon Y., Kim H. W., Chang L., Rao J. S., and, Rapoport S. I., (2011) Effect of chronic administration of clozapine on arachidonic acid (AA) turnover. Society of Biological Psychiatry 66th Annual Meeting 2011, 12-14 May 2011, 740.
62. Ossowska K., Pietraszek M., Wardas J., Dziedzicka-Wasylewska M., Nowicka D., and, Wolfarth S., (2002) Chronic treatments with haloperidol and clozapine alter the level of NMDA-R1 mRNA in the rat brain: an in situ hybridization study. Pol. J. Pharmacol. 54, 1-9.
63. Parry M. J., Alakoskela J. M., Khandelia H., Kumar S. A., Jaattela M., Mahalka A. K., and, Kinnunen P. K., (2008) High-affinity small molecule-phospholipid complex formation: binding of siramesine to phosphatidic acid. J. Am. Chem. Soc. 130, 12953-12960.
64. 2. J. Lipid Mediat. 6, 433-443.
65. Purdon D., Arai T., and, Rapoport S., (1997) No evidence for direct incorporation of esterified palmitic acid from plasma into brain lipids of awake adult rat. J. Lipid Res. 38, 526-530.
66. Raclot T., (2003) Selective mobilization of fatty acids from adipose tissue triacylglycerols. Prog. Lipid Res. 42, 257-288.
67. Ramadan E., Basselin M., Taha A. Y., Cheon Y., Chang L., Chen M., and, Rapoport S. I., (2011) Chronic valproate treatment blocks D2-like receptor-mediated brain signaling via arachidonic acid in rats. Neuropharmacology 61, 1256-1264.
68. Rao J. S., Harry G. J., Rapoport S. I., and, Kim H. W., (2010) Increased excitotoxicity and neuroinflammatory markers in postmortem frontal cortex from bipolar disorder patients. Mol. Psychiatry 15, 384-392.
69. Rao J. S., Kellom M., Reese E. A., Rapoport S. I., and, Kim H. W., (2012) Dysregulated glutamate and dopamine transporters in postmortem frontal cortex from bipolar and schizophrenic patients. J. Affect. Disord. 136, 63-71.
70. Rapoport S. I., Fitzhugh R., Pettigrew K. D., Sundaram U., and, Ohno K., (1982) Drug entry into and distribution within brain and cerebrospinal fluid: 14C-urea pharmacokinetics. Amer. J. Physiol. 242, R339-R348.
71. Rapoport S. I., (2008) Brain arachidonic and docosahexaenoic acid cascades are selectively altered by drugs, diet and disease. Prostaglandins Leukot. Essent. Fatty Acids 79, 153-156.
72. Rapoport S. I., and, Bosetti F., (2002) Do lithium and anticonvulsants target the brain arachidonic acid cascade in bipolar disorder? Arch. Gen. Psychiatry 59, 592-596.
73. Rapoport S. I., Basselin M., Kim H. W., and, Rao J. S., (2009) Bipolar disorder and mechanisms of action of mood stabilizers. Brain Res. Rev. 61, 185-209.
74. Robinson P. J., Noronha J., DeGeorge J. J., Freed L. M., Nariai T., and, Rapoport S. I., (1992) A quantitative method for measuring regional in vivo fatty-acid incorporation into and turnover within brain phospholipids: review and critical analysis. Brain Res. Brain Res. Rev. 17, 187-214.
75. Scherk H., Pajonk F. G., and, Leucht S., (2007) Second-generation antipsychotic agents in the treatment of acute mania: a systematic review and meta-analysis of randomized controlled trials. Arch. Gen. Psychiatry 64, 442-455.
76. Shimizu T., and, Wolfe L. S., (1990) Arachidonic acid cascade and signal transduction. J. Neurochem. 55, 1-15.
77. Shimshoni J. A., Basselin M., Li L. O., Coleman R. A., Rapoport S. I., and, Modi H. R., (2011) Valproate uncompetitively inhibits arachidonic acid acylation by rat acyl-CoA synthetase 4: relevance to valproate's efficacy against bipolar disorder. Biochim. Biophys. Acta 1811, 163-169.
78. Silvestri S., Seeman M. V., Negrete J. C., et al,. (2000) Increased dopamine D2 receptor binding after long-term treatment with antipsychotics in humans: a clinical PET study. Psychopharmacology 152, 174-180.
79. Skipski V. P., Barclay M., Reichman E. S., and, Good J. J., (1967) Separation of acidic phospholipids by one-dimensional thin-layer chromatography. Biochim. Biophys. Acta 137, 80-89.
80. Skipski V. P., Good J. J., Barclay M., and, Reggio R. B., (1968) Quantitative analysis of simple lipid classes by thin-layer chromatography. Biochim. Biophys. Acta 152, 10-19.
81. Soderlund T., Jutila A., and, Kinnunen P. K., (1999) Binding of adriamycin to liposomes as a probe for membrane lateral organization. Biophys. J. 76, 896-907.
82. Sun G. Y., and, MacQuarrie R. A., (1989) Deacylation-reacylation of arachidonoyl groups in cerebral phospholipids. Ann. N. Y. Acad. Sci. 559, 37-55.
83. Tarazi F. I., Florijn W. J., and, Creese I., (1997) Differential regulation of dopamine receptors after chronic typical and atypical antipsychotic drug treatment. Neuroscience 78, 985-996.
84. Thambisetty M., Gallardo K. A., Liow J. S., et al,. (2012) The utility of (11)C-arachidonate PET to study in vivo dopaminergic neurotransmission in humans. J. Cereb. Blood Flow Metab. 32, 676-684.
85. Tulipano G., Rizzetti C., Bianchi I., Fanzani A., Spano P., and, Cocchi D., (2007) Clozapine-induced alteration of glucose homeostasis in the rat: the contribution of hypothalamic-pituitary-adrenal axis activation. Neuroendocrinology 85, 61-70.
86. Vidarsdottir S., de Leeuw van Weenen J. E., Frolich M., Roelfsema F., Romijn J. A., and, Pijl H., (2010) Effects of olanzapine and haloperidol on the metabolic status of healthy men. J. Clin. Endocrinol. Metab. 95, 118-125.
87. Washizaki K., Smith Q. R., Rapoport S. I., and, Purdon A. D., (1994) Brain arachidonic acid incorporation and precursor pool specific activity during intravenous infusion of unesterified [3H]arachidonate in the anesthetized rat. J. Neurochem. 63, 727-736.
88. Zarate C. A. Jr, Tohen M., and, Baldessarini R. J., (1995) Clozapine in severe mood disorders. J. Clin. Psychiatry 56, 411-417.