Social isolation rearing in rats alters plasma tryptophan metabolism and is reversed by sub-chronic clozapine treatment

Neuropharmacology

Volumn 62, Issue 8, 2012, Pages 2499-2506

  Möller, Marisa ^a   Du Preez, Jan L ^a   Emsley, Robin ^b   Harvey, Brian H ^a  

^a NORTH WEST UNIVERSITY   (South Africa)

^b STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Anti inflammatory; Antioxidant; Clozapine; Kynurenic acid; Quinolinic acid; Schizophrenia; Social isolation rearing; Tryptophan metabolism

Indexed keywords

3 HYDROXYANTHRANILIC ACID; ANTHRANILIC ACID; CLOZAPINE; KYNURENINE; QUINOLINIC ACID; TRYPTOPHAN;

AMINO ACID BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; DRUG RESPONSE; ELECTROSPRAY MASS SPECTROMETRY; LIQUID CHROMATOGRAPHY; MALE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; REARING; SCHIZOPHRENIA; SINGLE DRUG DOSE; SOCIAL ISOLATION REARING; TRYPTOPHAN METABOLISM;

ANIMALS; ANTHRANILIC ACIDS; ANTIPSYCHOTIC AGENTS; CLOZAPINE; KYNURENINE; MALE; OXIDATIVE STRESS; QUINOLINIC ACID; RATS; RATS, SPRAGUE-DAWLEY; SOCIAL ISOLATION; TRYPTOPHAN;

EID: 84859709836     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.02.021     Document Type: Article

References (65)

1. Akyol, O., Herken, H., Uz, E., Fadillioglu, E., Unal, S., Sogut, S., Ozyurt, H., Savas, H.A., 2002. The indices of endogenous oxidative and antioxidative processes in plasma from schizophrenic patients. the possible role of oxidant/antioxidant imbalance. Prog. Neuropsychopharmacol. Biol. Psychiatry 26, 995-1005. (Pubitemid 35245568)
2. Allegri, G., Costa, C.V.L., Bertazzo, A., Biasiolo, M., Ragazzi, E., 2003. Enzyme activities of tryptophan metabolism along the kynurenine pathway in various species of animals. Il Farmaco 58, 829-836. (Pubitemid 37122654)
3. Amirkhani, A., Heldin, E., Markides, K.E., Bergquist, J., 2002. Quantitation of tryptophan, kynurenine and kynurenic acid in human plasma by capillary liquid chromatography-electrospray ionization tandem mass spectrometry. J. Chromatogr. B 780, 381-387. (Pubitemid 35223575)
4. Andreasen, N.C., O'Leary, D.S., Cizadlo, T., Arndt, S., Rezai, K., Ponto, L.L., Watkins, G.L., Hichwa, R.D., 1996. Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal-thalamic- cerebellar circuitry. Proc. Natl. Acad. Sci. U. S. A. 93, 9985-9990. (Pubitemid 26296722)
5. Atkins, M., Burgess, A., Bottomly, C., Riccio, M., 1997. Chlorpromazine equivalents: a concensus of opinion for both clinical and research applications. Psychiatr. Bull. 21, 224-226. (Pubitemid 27225823)
6. Ascher-Svanum, H., Nyhuis, A.W., Faries, D.E., Kinon, B.J., Baker, R.W., Shekhar, A., 2008. Clinical, functional, and economic ramifications of early nonresponse to antipsychotics in the naturalistic treatment of schizophrenia. Schizophr. Bull. 34, 1163-1171.
7. Barry, S., Clarke, G., Scully, P., Dinan, T., 2009. Kynurenine pathway in psychosis: evidence of increased tryptophan degradation. J. Psychopharmacol. 23, 287-294.
8. Bakshi, V.P., Swerdlow, N.R., Geyer, M.A., 1994. Clozapine antagonizes phencyclidine-induced deficits in sensorimotor gating of the startle response. J. Pharmacol. Exp. Ther. 271, 787-794. (Pubitemid 24377766)
9. Berk, M., Copolov, D., Dean, O., et al., 2008. N-acetyl cysteine as a glutathione precursor for Schizophrenia e a double-blind, randomized, placebo-controlled trial. Biol. Psychiatry 64, 361-368.
10. Bernstein, H.G., Bogerts, B., Keilhoff, G., 2005. The many faces of nitric oxide in schizophrenia. A review. Schizophr. Res. 78, 69-86. (Pubitemid 41188326)
11. Betzen, C., White, R., Zehendner, C.M., Pietrowski, E., Bender, B., Luhmann, H.J., Kuhlmann, C.R.W., 2009. Oxidative stress upregulates the NMDA receptor on cerebrovascular endothelium. Free Radic. Biol. Med. 47, 1212-1220.
12. Boussery, K., Lambrecht, S., Delaey, C., Van de Voorde, J., 2005. Clozapine directly relaxes bovine retinal arteries. Curr. Eye Res. 30, 139-146. (Pubitemid 40520504)
13. Byne, W., Kidkardnee, S., Tatusov, A., Yiannoulos, G., Buchsbaum, M.S., Haroutunian, V., 2006. Schizophrenia-associated reduction of neuronal and oligodendrocyte numbers in the anterior principal thalamic nucleus. Schizophr. Res. 85, 245-253. (Pubitemid 43947537)
14. Carlsson, A., Waters, N., Holm-Waters, S., Tedroff, J., Nilsson, M., Carlsson, M.L., 2001. Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. Annu. Rev. Pharmacol. Toxicol. 41, 237.
15. de Jong, W.H.A., Smit, R., Bakker, S.J.L., de Vries, E.G.E., Kema, I.P., 2009. Plasma tryptophan, kynurenine and 3-hydroxykynurenine measurement using automated on-line solid-phase extraction HPLC - tandem mass spectrometry. J. Chromatogr. B 877, 603-609.
16. Deutsch, S.I., Rosse, R.B., Schwartz, B.L., Mastropaolo, J., 2001. A revised excitotoxic hypothesis of schizophrenia: therapeutic implications. Clin. Neuropharmacol. 24, 43-49. (Pubitemid 32176480)
17. Evins, A.E., Amico, E., Posever, T.A., Toker, R., Goff, D.C., 2002. D-cycloserine added to risperidone in patients with primary negative symptoms of schizophrenia. Schizophr. Res. 56, 19-23. (Pubitemid 34655463)
18. Fone, K.C.F., Porkess, M.V., 2008. Behavioural and neurochemical effects of post-weaning social isolation in rodents - relevance to developmental neuropsychiatric disorders. Neurosci. Biobehav. Rev. 32, 1087-1102.
19. Ganzinelli, S., Borda, E., Sterin-Borda, L., 2010. Autoantibodies from schizophrenia patients induce cerebral cox-1/iNOS mRNA expression with NO/PGE2/MMP-3 production. Int. J. Neuropsychopharmacol. 13, 293-303.
20. Glantz, L.A., Lewis, D.A., 2000. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch. Gen. Psychiatry 57, 65-73. (Pubitemid 30035660)
21. Goff, D.C., Tsai, G., Levitt, J., Amico, E., Manoach, D., Schoenfeld, D.A., Hayden, D.L., McCarley, R., Coyle, J.T., 1999. A placebo-controlled trial of D-cycloserine added to conventional neuroleptics in patients with schizophrenia. Arch. Gen. Psychiatry 56, 21-27. (Pubitemid 29055046)
22. Guillemin, G.J., Cullen, K.M., Lim, C.K., Smythe, G.A., Garner, B., Kapoor, V., Takikawa, O., Brew, B.J., 2007. Characterization of the kynurenine pathway in human neurons. J. Neurosci. 27, 12884-12892. (Pubitemid 350161746)
23. Heyes, M.P., Chen, C.Y., Major, E.O., Saito, K., 1997. Different kynurenine pathway enzymes limit quinolinic acid formation by various human cell types. Biochem. J. 326 (Pt. 2), 351-356. (Pubitemid 27417209)
24. Hu, J., Lee, J.H., el-Fakahany, E.E., 1994. Inhibition of neuronal nitric oxide synthase by antipsychotic drugs. Psychopharmacology (Berl) 114, 161-166. (Pubitemid 24150534)
25. Hu, X., Zhou, H., Zhang, D., et al., 2011. Clozapine protects dopaminergic neurons from inflammation-induced damage by inhibiting microglial overactivation. J. Neuroimmune Pharmacol. doi:10.1007/s11481-011-9309-0.
26. Issa, F., Gerhardt, G.A., Bartko, J.J., Suddath, R.L., Lynch, M., Gamache, P.H., Freedman, R., Wyatt, R.J., Kirch, D.G., 1994. A multidimensional approach to analysis of cerebrospinal fluid biogenic amines in schizophrenia: I. comparisons with healthy control subjects and neuroleptic-treated/unmedicated pairs analyses. Psychiatry Res. 52, 237-249.
27. Javitt, D.C., 2010. Glutamatergic theories of schizophrenia. Isr. J. Psychiatry Relat. Sci. 47, 4-16.
28. Kantrowitz, J.T., Javitt, D.C., 2010. Thinking glutamatergically: changing concepts of schizophrenia based upon changing neurochemical models. Clin. Schizophr. Relat. Psychoses 4, 189-200.
29. Kapur, S., Arenovich, T., Agid, O., Zipursky, R., Lindborg, S., Jones, B., 2005. Evidence for onset of antipsychotic effects within the first 24 hours of treatment. Am. J. Psychiatry 162, 939-946. (Pubitemid 40676207)
30. Lavoie, S., Murray, M.M., Deppen, P., et al., 2008. Glutathione precursor, N-acetylcysteine, improves mismatch negativity in schizophrenia patients. Neuropsychopharmacology 33, 2187-2199. (Pubitemid 351992093)
31. Lin, A., Kenis, G., Bignotti, S., Tura, G., De Jong, R., Bosmans, E., Pioli, R., Altamura, C., Scharpé, S., Maes, M., 1998. The inflammatory response system in treatment-resistant schizophrenia: increased serum interleukin-6. Schizophr. Res. 32, 9-15. (Pubitemid 28338119)
32. Maes, M., Meltzer, H.Y., Bosmans, E., 1994. Immune-inflammatory markers in schizophrenia: comparison to normal controls and effects of clozapine. Acta Psychiatrica. Scand. 89, 346-351. (Pubitemid 24157957)
33. Magliaro, B.C., Saldanha, C.J., 2009. Clozapine protects PC-12 cells from death due to oxidative stress induced by hydrogen peroxide via a cell-type specific mechanism involving inhibition of extracellular signal-regulated kinase phosphorylation. Brain Res. 1283, 14-24.
34. Meltzer, H.Y., 1989. Clinical studies on the mechanism of action of clozapine: the dopamine-serotonin hypothesis of schizophrenia. Psychopharmacology 99 (Suppl.), S18-S27. (Pubitemid 19244134)
35. Meyer, U., Feldon, J., 2010. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog. Neurobiol. 90, 285-326.
36. Miller, C.L., Llenos, I.C., Dulay, J.R., Weis, S., 2006. Upregulation of the initiating step of the kynurenine pathway in postmortem anterior cingulate cortex from individuals with schizophrenia and bipolar disorder. Brain Res. 1073-1074, 25-37.
37. Miller, C.L., Llenos, I.C., Cwik, M., Walkup, J., Weis, S., 2008. Alterations in kynurenine precursor and product levels in schizophrenia and bipolar disorder. Neurochem. Int. 52, 1297-1303.
38. Möller, M., Du Preez, J.L., Emsley, R., Harvey, B.H., 2011. Isolation rearing-induced deficits in sensorimotor gating and social interaction in rats are related to cortico-striatal oxidative stress, and reversed by sub-chronic clozapine administration. Eur. Neuropsychopharmacol. 21, 471-483.
39. Möller, M., Du Preez, J. L., & Harvey, B. H., submitted for publication. Development and validation of a single analytical method for the determination of tryptophan, and its kynurenine metabolites in rat plasma. J. Chromatogr. B.
40. Myint, A., Kim, Y.K., Verkerk, R., Scharpé, S., Steinbusch, H., Leonard, B., 2007a. Kynurenine pathway in major depression: evidence of impaired neuroprotection. J. Affect. Disord. 98, 143-151. (Pubitemid 46048912)
41. Myint, A.M., Kim, Y.K., Verkerk, R., Park, S.H., Scharpe, S., Steinbusch, H.W., Leonard, B.E., 2007b. Tryptophan breakdown pathway in bipolar mania. J. Affect. Disord. 102, 65-72. (Pubitemid 47042175)
42. Myint, A.M., Schwarz, M.J., Verkerk, R., Mueller, H.H., Zach, J., Scharpé, S., Steinbusch, H.W.M., Leonard, B.E., Kim, Y.K., 2011. Reversal of imbalance between kynurenic acid and 3-hydroxykynurenine by antipsychotics in medication- naïve and medication-free schizophrenic patients. Brain Behav. Immun. 25, 1576-1581.
43. Nel, A., Harvey, B.H., 2003. Haloperidol-induced dyskinesia is associated with striatal NO synthase suppression: reversal with olanzapine. Behav. Pharmacol. 14, 251-255. (Pubitemid 36735159)
44. Ng, F., Berk, M., Dean, O., Bush, A.I., 2008. Oxidative stress in psychiatric disorders: evidence base and therapeutic implications. Int. J. Neuropsychopharmacol. 11, 851.
45. Potvin, S., Stip, E., Sepehry, A.A., Gendron, A., Bah, R., Kouassi, E., 2008. Inflammatory cytokine alterations in schizophrenia: a systematic quantitative review. Biol. Psychiatry 63, 801-808. (Pubitemid 351410515)
46. Ravikumar, A., Deepadevi, K.V., Arun, P., Manojkumar, V., Kurup, P.A., 2000. Tryptophan and tyrosine catabolic pattern in neuropsychiatric disorders. Neurol. India 48, 231-238.
47. Schwarcz, R., Whetsell Jr., W.O., Mangano, R.M., 1983. Quinolinic acid: an endogenous metabolite that produces axon-sparing lesions in rat brain. Science 219, 316-318. (Pubitemid 13222319)
48. Schwarcz, R., Rassoulpour, A., Wu, H.Q., Medoff, D., Tamminga, C.A., Roberts, R.C., 2001. Increased cortical kynurenate content in schizophrenia. Biol. Psychiatry 50, 521-530. (Pubitemid 32971883)
49. Schwarcz, R., 2004. The kynurenine pathway of tryptophan degradation as a drug target. Curr. Opin. Pharmacol. 4, 12-17. (Pubitemid 38145832)
50. Schwieler, L., Erhardt, S., 2003. Inhibitory action of clozapine on rat ventral tegmental area dopamine neurons following increased levels of endogenous kynurenic acid. Neuropsychopharmacology 28, 1770-1777. (Pubitemid 41070842)
51. Schwieler, L., Linderholm, K.R., Nilsson-Todd, L.K., Erhardt, S., Engberg, G., 2008. Clozapine interacts with the glycine site of the NMDA receptor: electrophysiological studies of dopamine neurons in the rat ventral tegmental area. Life Sci. 83, 170-175.
52. Stone, T.W., 2001. Kynurenines in the CNS: from endogenous obscurity to therapeutic importance. Prog. Neurobiol. 64, 185-218. (Pubitemid 32195412)
53. Stone, T.W., Darlington, L.G., 2002. Endogenous kynurenines as targets for drug discovery and development. Nat. Rev. Drug Discov. 1, 609.
54. Stone, T.W., Mackay, G.M., Forrest, C.M., Clark, C.J., Darlington, L.G., 2003. Tryptophan metabolites and brain disorders. Clin. Chem. Lab. Med. 41, 852-859. (Pubitemid 37010175)
55. Sugino, H., Futamura, T., Mitsumoto, Y., Maeda, K., Marunaka, Y., 2009. Atypical antipsychotics suppress production of proinflammatory cytokines and up-regulate interleukin-10 in lipopolysaccharide-treated mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 33, 303-307.
56. Theberge, J., Williamson, K.E., Aoyama, N., et al., 2007. Longitudinal grey-matter and glutamatergic losses in first-episode schizophrenia. Brit. J. Psychiatry 191, 325-334. (Pubitemid 47555981)
57. Torrey, E.F., Yolken, R.H., Zito, M., Heyes, M., 1998. Increased CSF and brain quinolinic acid in schizophrenia and bipolar disorder. Schizophr. Res. 29, 91-92.
58. Toua, C., Brand, L., Möller, M., Emsley, R.A., Harvey, B.H., 2010. The effects of subchronic clozapine and haloperidol administration on isolation rearing induced changes in frontal cortical N-methyl-D-aspartate and D1 receptor binding in rats. Neurosci 165, 492-499.
59. Wang, Y., Lawson, M.A., Kelley, K.W., Dantzer, R., 2010. Primary murine microglia are resistant to nitric oxide inhibition of indoleamine 2,3-dioxygenase. Brain Behav. Immun. 24, 1249-1253.
60. Weiss, I.C., Feldon, J., 2001. Environmental animal models for sensorimotor gating deficiencies in schizophrenia: a review. Psychopharmacology 156, 305-326. (Pubitemid 32702221)
61. Willinger, U., Heiden, A.M., Meszaros, K., Formann, A.K., Aschauer, H.N., 2001. Neurodevelopmental schizophrenia: obstetric complications, birth weight, premorbid social withdrawal and learning disabilities. Neuropsychobiology 43, 163-169. (Pubitemid 32268587)
62. Wright, I.C., Rabe-Hesketh, S., Woodruff, P.W., David, A.S., Murray, R.M., Bullmore, E.T., 2000. Meta-analysis of regional brain volumes in schizophrenia. Am. J. Psychiatry 157, 16-25. (Pubitemid 30027416)
63. Young, J.W., Zhou, X., Geyer, M.A., 2010. Animal models of schizophrenia. Curr. Top. Behav. Neurosci. 4, 391-433.
64. Zhang, W., Pouzet, B., Jongen-Rêlo, A.L., Weiner, I., Feldon, J., 1999. Disruption of prepulse inhibition following N-methyl-D-aspartate infusion into the ventral hippocampus is antagonized by clozapine but not by haloperidol: a possible model for the screening of atypical antipsychotics. Neuropharm. Neurotoxicol. 10, 2533-2538. (Pubitemid 29418132)
65. Zhang, X.R., Zhang, Z.J., Jenkins, T.A., Cheng, W.R., Reynolds, G.P., 2010. The effect of chronic antipsychotic drug administration on nitric oxide synthase activity and gene expression in rat penile tissues. Eur. Neuropsychopharmacol. 20, 211-217.