Behavioral disturbances in adult mice following neonatal virus infection or kynurenine treatment - Role of brain kynurenic acid

Brain, Behavior, and Immunity

Volumn 36, Issue , 2014, Pages 80-89

  Liu, Xi Cong ^a   Holtze, Maria ^a   Powell, Susan B ^b   Terrando, Niccolò ^a   Larsson, Markus K ^a   Persson, Anna ^a   Olsson, Sara K ^a   Orhan, Funda ^a   Kegel, Magdalena ^a   Asp, Linnea ^a   Goiny, Michel ^a   Schwieler, Lilly ^a   Engberg, Göran ^a   Karlsson, Håkan ^a   Erhardt, Sophie ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amphetamine; Immune activation; Kynurenine; Locomotor activity; Microdialysis; Neurodevelopment; Postnatal; Prepulse inhibition; Schizophrenia

Indexed keywords

AMPHETAMINE; BUNGAROTOXIN RECEPTOR; DEXAMPHETAMINE; KYNURENIC ACID; KYNURENINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RELEASE; INFLUENZA VIRUS A; LEARNING; LOCOMOTION; MALE; MEMORY; MOUSE; NEWBORN INFECTION; NONHUMAN; PERINATAL PERIOD; PREPULSE INHIBITION; PRIORITY JOURNAL; STARTLE REFLEX; VIRUS INFECTION;

AMPHETAMINE; IMMUNE ACTIVATION; KYNURENINE; LOCOMOTOR ACTIVITY; MICRODIALYSIS; NEURODEVELOPMENT; POSTNATAL; PREPULSE INHIBITION; SCHIZOPHRENIA;

AMPHETAMINE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BRAIN; BRAIN CHEMISTRY; CONDITIONING (PSYCHOLOGY); DOPAMINE; DOPAMINE AGENTS; FEMALE; INFLUENZA A VIRUS; KYNURENIC ACID; KYNURENINE; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; ORTHOMYXOVIRIDAE INFECTIONS;

EID: 84891827968     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2013.10.010     Document Type: Article

References (87)

1. Abi-Dargham A., Gil R., Krystal J., Baldwin R.M., Seibyl J.P., Bowers M., van Dyck C.H., Charney D.S., Innis R.B., Laruelle M. Increased striatal dopamine transmission in schizophrenia: confirmation in a second cohort. Am. J. Psychiatry 1998, 155:761-767.
2. Adler C.M., Malhotra A.K., Elman I., Goldberg T., Egan M., Pickar D., Breier A. Comparison of ketamine-induced thought disorder in healthy volunteers and thought disorder in schizophrenia. Am. J. Psychiatry 1999, 156:1646-1649.
3. Alexander K.S., Pocivavsek A., Wu H.Q., Pershing M.L., Schwarcz R., Bruno J.P. Early developmental elevations of brain kynurenic acid impair cognitive flexibility in adults: reversal with galantamine. Neuroscience 2013, 238:19-28.
4. Amori L., Guidetti P., Pellicciari R., Kajii Y., Schwarcz R. On the relationship between the two branches of the kynurenine pathway in the rat brain in vivo. J. Neurochem. 2009, 109:316-325.
5. Amori L., Wu H.Q., Marinozzi M., Pellicciari R., Guidetti P., Schwarcz R. Specific inhibition of kynurenate synthesis enhances extracellular dopamine levels in the rodent striatum. Neuroscience 2009, 159:196-203.
6. Andreasen N.C. Symptoms, signs, and diagnosis of schizophrenia. Lancet 1995, 346:477-481.
7. Angrist B.M., Gershon S. The phenomenology of experimentally induced amphetamine psychosis-preliminary observations. Biol. Psychiatry 1970, 2:95-107.
8. Asp L., Nellaker C., Karlsson H. Influenza A virus transactivates the mouse envelope gene encoding syncytin B and its regulator, glial cells missing 1. J. Neurovirol. 2007, 13:29-37.
9. Asp L., Beraki S., Kristensson K., Ogren S.O., Karlsson H. Neonatal infection with neurotropic influenza A virus affects working memory and expression of type III Nrg1 in adult mice. Brain Behav. Immun. 2009, 23:733-741.
10. -/- mice. Int. J. Neuropsychopharmacol. 2010, 13:475-485.
11. Atlas A., Gisslen M., Nordin C., Lindstrom L., Schwieler L. Acute psychotic symptoms in HIV-1 infected patients are associated with increased levels of kynurenic acid in cerebrospinal fluid. Brain Behav. Immun. 2007, 21:86-91.
12. Blomström A., Karlsson H., Wicks S., Yang S., Yolken R.H., Dalman C. Maternal antibodies to infectious agents and risk for non-affective psychoses in the offspring - a matched case-control study. Schizophr. Res. 2012, 140:25-30.
13. Braff D.L., Geyer M.A., Swerdlow N.R. Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl.) 2001, 156:234-258.
14. Breier A., Su T.P., Saunders R., Carson R.E., Kolachana B.S., de Bartolomeis A., Weinberger D.R., Weisenfeld N., Malhotra A.K., Eckelman W.C., Pickar D. Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. Proc. Natl. Acad. Sci. USA 1997, 94:2569-2574.
15. Brown A.S., Derkits E.J. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am. J. Psychiatry 2010, 167:261-280.
16. Carlsson A., Carlsson M.L. A dopaminergic deficit hypothesis of schizophrenia: the path to discovery. Dialogues Clin. Neurosci. 2006, 8:137-142.
17. Carlsson A., Lindqvist M. Effect of chlorpromazine or haloperidol on formation of 3-methoxytyramine and normetanephrine in mouse brain. Acta Pharmacol. Toxicol. (Copenh.) 1963, 20:140-144.
18. Carlsson A., Waters N., Holm-Waters S., Tedroff J., Nilsson M., Carlsson M.L. Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. Annu. Rev. Pharmacol. Toxicol. 2001, 41:237-260.
19. Chess A.C., Landers A.M., Bucci D.J. l-kynurenine treatment alters contextual fear conditioning and context discrimination but not cue-specific fear conditioning. Behav. Brain Res. 2009, 201:325-331.
20. Cibelli M., Fidalgo A.R., Terrando N., Ma D., Monaco C., Feldmann M., Takata M., Lever I.J., Nanchahal J., Fanselow M.S., Maze M. Role of interleukin-1beta in postoperative cognitive dysfunction. Ann. Neurol. 2010, 68:360-368.
21. Costall B., Jones B.J., Kelly M.E., Naylor R.J., Tomkinks D.M. Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacol. Biochem. Behav. 1988, 31:777-785.
22. Crnic L.S., Pizer L.I. Behavioral effects of neonatal herpes simplex type 1 infection of mice. Neurotoxicol. Teratol. 1988, 10:381-386.
23. Cruickshank C.C., Dyer K.R. A review of the clinical pharmacology of methamphetamine. Addiction 2009, 104:1085-1099.
24. Dalman C., Allebeck P., Gunnell D., Harrison G., Kristensson K., Lewis G., Lofving S., Rasmussen F., Wicks S., Karlsson H. Infections in the CNS during childhood and the risk of subsequent psychotic illness: a cohort study of more than one million Swedish subjects. Am. J. Psychiatry 2008, 165:59-65.
25. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
26. Ellman L.M., Yolken R.H., Buka S.L., Torrey E.F., Cannon T.D. Cognitive functioning prior to the onset of psychosis: the role of fetal exposure to serologically determined influenza infection. Biol. Psychiatry 2009, 65:1040-1047.
27. Engel J.A., Zhang J., Bergstrom T., Conradi N., Forkstam C., Liljeroth A., Svensson L. Neonatal herpes simplex virus type 1 brain infection affects the development of sensorimotor gating in rats. Brain Res. 2000, 863:233-240.
28. Erhardt S., Blennow K., Nordin C., Skogh E., Lindström L.H., Engberg G. Kynurenic acid levels are elevated in the cerebrospinal fluid of patients with schizophrenia. Neurosci. Lett. 2001, 313:96-98.
29. Erhardt S., Öberg H., Mathe J.M., Engberg G. Pharmacological elevation of endogenous kynurenic acid levels activates nigral dopamine neurons. Amino Acids 2001, 20:353-362.
30. Erhardt S., Schwieler L., Emanuelsson C., Geyer M. Endogenous kynurenic acid disrupts prepulse inhibition. Biol. Psychiatry 2004, 56:255-260.
31. Erhardt S., Schwieler L., Nilsson L., Linderholm K., Engberg G. The kynurenic acid hypothesis of schizophrenia. Physiol. Behav. 2007, 92:203-209.
32. Erhardt S., Olsson S.K., Engberg G. Pharmacological manipulation of kynurenic acid: potential in the treatment of psychiatric disorders. CNS Drugs 2009, 23:91-101.
33. Erhardt S., Lim C.K., Linderholm K.R., Janelidze S., Lindqvist D., Samuelsson M., Lundberg K., Postolache T.T., Träskman-Bendz L., Guillemin G.J., Brundin L. Connecting inflammation with glutamate agonism in suicidality. Neuropsychopharmacology 2013, 38:743-752.
34. Fredriksson A., Ponten E., Gordh T., Eriksson P. Neonatal exposure to a combination of N-methyl-d-aspartate and gamma-aminobutyric acid type A receptor anesthetic agents potentiates apoptotic neurodegeneration and persistent behavioral deficits. Anesthesiology 2007, 107:427-436.
35. Gold L.H., Brot M.D., Polis I., Schroeder R., Tishon A., de la Torre J.C., Oldstone M.B., Koob G.F. Behavioral effects of persistent lymphocytic choriomeningitis virus infection in mice. Behav. Neural. Biol. 1994, 62:100-109.
36. Griffith J.D., Cavanaugh J., Held J., Oates J.A. Dextroamphetamine. Evaluation of psychomimetic properties in man. Arch. Gen. Psychiatry 1972, 26:97-100.
37. Guidetti P., Eastman C.L., Schwarcz R. Metabolism of [5-3H]kynurenine in the rat brain in vivo: evidence for the existence of a functional kynurenine pathway. J. Neurochem. 1995, 65:2621-2632.
38. Han C.J., O'Tuathaigh C.M., van Trigt L., Quinn J.J., Fanselow M.S., Mongeau R., Koch C., Anderson D.J. Trace but not delay fear conditioning requires attention and the anterior cingulate cortex. Proc. Natl. Acad. Sci. USA 2003, 100:13087-13092.
39. Harris L.W., Sharp T., Gartlon J., Jones D.N., Harrison P.J. Long-term behavioural, molecular and morphological effects of neonatal NMDA receptor antagonism. Eur. J. Neurosci. 2003, 18:1706-1710.
40. Heyes M.P., Saito K., Crowley J.S., Davis L.E., Demitrack M.A., Der M., Dilling L.A., Elia J., Kruesi M.J., Lackner A., et al. Quinolinic acid and kynurenine pathway metabolism in inflammatory and non-inflammatory neurological disease. Brain 1992, 115:1249-1273.
41. Hoffman H.S., Ison J.R. Reflex modification in the domain of startle: I. Some empirical findings and their implications for how the nervous system processes sensory input. Psychol. Rev. 1980, 87:175-189.
42. Holtze M., Asp L., Schwieler L., Engberg G., Karlsson H. Induction of the kynurenine pathway by neurotropic influenza A virus infection. J. Neurosci. Res. 2008, 86:3674-3683.
43. Holtze M., Mickiené A., Atlas A., Lindquist L., Schwieler L. Elevated cerebrospinal fluid kynurenic acid levels in patients with tick-borne encephalitis. J. Intern. Med. 2012, 272:394-401.
44. Ikonomidou C. Triggers of apoptosis in the immature brain. Brain Dev. 2009, 31:488-492.
45. Ikonomidou C., Bosch F., Miksa M., Bittigau P., Vockler J., Dikranian K., Tenkova T.I., Stefovska V., Turski L., Olney J.W. Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 1999, 283:70-74.
46. Javitt D.C. Glutamate as a therapeutic target in psychiatric disorders. Mol. Psychiatry 2004, 9(984-997):979.
47. Javitt D.C., Zukin S.R. Recent advances in the phencyclidine model of schizophrenia. Am. J. Psychiatry 1991, 148:1301-1308.
48. Jentsch J.D., Roth R.H. The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1999, 20:201-225.
49. Kessler M., Terramani T., Lynch G., Baudry M. A glycine site associated with N-methyl-d-aspartic acid receptors: characterization and identification of a new class of antagonists. J. Neurochem. 1989, 52:1319-1328.
50. Kim J.J., Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 1992, 256:675-677.
51. King N.J., Thomas S.R. Molecules in focus: indoleamine 2,3-dioxygenase. Int. J. Biochem. Cell Biol. 2007, 39:2167-2172.
52. Laruelle M., Abi-Dargham A., van Dyck C.H., Gil R., D'Souza C.D., Erdos J., McCance E., Rosenblatt W., Fingado C., Zoghbi S.S., Baldwin R.M., Seibyl J.P., Krystal J.H., Charney D.S., Innis R.B. Single photon emission computerized tomography imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects. Proc. Natl. Acad. Sci. USA 1996, 93:9235-9240.
53. Lavebratt C., Olsson S., Backlund L., Frisén L., Sellgren C., Priebe L., Nikamo P., Träskman-Bendz L., Cichon S., Vawter M.P., Osby U., Engberg G., Landén M., Erhardt S., Schalling M. The KMO allele encoding Arg452 is associated with psychotic features in bipolar disorder type 1, and with increased CSF KYNA level and reduced KMO expression. Mol. Psychiatry 2013, 10.1038/mp.2013.11.
54. Linderholm K.R., Andersson A., Olsson S., Olsson E., Snodgrass R., Engberg G., Erhardt S. Activation of rat ventral tegmental area dopamine neurons by endogenous kynurenic acid: a pharmacological analysis. Neuropharmacology 2007, 53:918-924.
55. Linderholm K.R., Skogh E., Olsson S.K., Dahl M.L., Holtze M., Engberg G., Samuelsson M., Erhardt S. Increased levels of kynurenine and kynurenic acid in the CSF of patients with schizophrenia. Schizophr. Bull. 2012, 38:426-432.
56. Lister R.G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 1987, 92:180-185.
57. Lu L., Mamiya T., Lu P., Toriumi K., Mouri A., Hiramatsu M., Kim H.C., Zou L.B., Nagai T., Nabeshima T. Prenatal exposure to phencyclidine produces abnormal behaviour and NMDA receptor expression in postpubertal mice. Int. J. Neuropsychopharmacol. 2010, 13:877-889.
58. Luby E.D., Cohen B.D., Rosenbaum G., Gottlieb J.S., Kelley R. Study of a new schizophrenomimetic drug; sernyl. AMA Arch. Neurol. Psychiatry 1959, 81:363-369.
59. Marenco S., Weinberger D.R. The neurodevelopmental hypothesis of schizophrenia: following a trail of evidence from cradle to grave. Dev. Psychopathol. 2000, 12:501-527.
60. Meyer U., Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog. Neurobiol. 2010, 90:285-326.
61. Mohn A.R., Gainetdinov R.R., Caron M.G., Koller B.H. Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 1999, 98:427-436.
62. Mouri A., Noda Y., Enomoto T., Nabeshima T. Phencyclidine animal models of schizophrenia: approaches from abnormality of glutamatergic neurotransmission and neurodevelopment. Neurochem. Int. 2007, 51:173-184.
63. Nilsson L.K., Linderholm K.R., Engberg G., Paulson L., Blennow K., Lindström L.H., Nordin C., Karanti A., Persson P., Erhardt S. Elevated levels of kynurenic acid in the cerebrospinal fluid of male patients with schizophrenia. Schizophr. Res. 2005, 80:315-322.
64. Olney J.W. New insights and new issues in developmental neurotoxicology. Neurotoxicology 2002, 23:659-668.
65. Olney J.W., Farber N.B. Glutamate receptor dysfunction and schizophrenia. Arch. Gen. Psychiatry 1995, 52:998-1007.
66. Olsson S.K., Andersson A.S., Linderholm K.R., Holtze M., Nilsson-Todd L.K., Schwieler L., Olsson E., Larsson K., Engberg G., Erhardt S. Elevated levels of kynurenic acid change the dopaminergic response to amphetamine: implications for schizophrenia. Int. J. Neuropsychopharmacol. 2009, 12:501-512.
67. Olsson S.K., Samuelsson M., Saetre P., Lindstrom L., Jonsson E.G., Nordin C., Engberg G., Erhardt S., Landen M. Elevated levels of kynurenic acid in the cerebrospinal fluid of patients with bipolar disorder. J. Psychiatry Neurosci. 2010, 35:195-199.
68. Olsson S.K., Larsson M.K., Erhardt S. Subchronic elevation of brain kynurenic acid augments amphetamine-induced locomotor response in mice. J. Neural Transm. 2012, 119:155-163.
69. Olsson S.K., Sellgren C., Engberg G., Landén M., Erhardt S. Cerebrospinal fluid kynurenic acid is associated with manic and psychotic features in patients with bipolar I disorder. Bipolar Disord. 2012, 14:719-726.
70. Pocivavsek A., Wu H.Q., Elmer G.I., Bruno J.P., Schwarcz R. Pre- and postnatal exposure to kynurenine causes cognitive deficits in adulthood. Eur. J. Neurosci. 2012, 35:1605-1612.
71. Powell S.B., Sejnowski T.J., Behrens M.M. Behavioral and neurochemical consequences of cortical oxidative stress on parvalbumin-interneuron maturation in rodent models of schizophrenia. Neuropharmacology 2012, 62:1322-1331.
72. Raison C.L., Dantzer R., Kelley K.W., Lawson M.A., Woolwine B.J., Vogt G., Spivey J.R., Saito K., Miller A.H. CSF concentrations of brain tryptophan and kynurenines during immune stimulation with IFN-alpha: relationship to CNS immune responses and depression. Mol. Psychiatry 2010, 15:393-403.
73. Rice, D., Barone Jr., S., 2000. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 108, S3, 511-533.
74. Ross R.G., Stevens K.E., Proctor W.R., Leonard S., Kisley M.A., Hunter S.K., Freedman R., Adams C.E. Research review: cholinergic mechanisms, early brain development, and risk for schizophrenia. J. Child Psychol. Psychiatry 2010, 51:535-549.
75. Rudin M., Ben-Abraham R., Gazit V., Tendler Y., Tashlykov V., Katz Y. Single-dose ketamine administration induces apoptosis in neonatal mouse brain. J. Basic Clin. Physiol. Pharmacol. 2005, 16:231-243.
76. Runyan J.D., Moore A.N., Dash P.K. A role for prefrontal cortex in memory storage for trace fear conditioning. J. Neurosci. 2004, 24:1288-1295.
77. Sathyasaikumar K.V., Stachowski E.K., Wonodi I., Roberts R.C., Rassoulpour A., McMahon R.P., Schwarcz R. Impaired kynurenine pathway metabolism in the prefrontal cortex of individuals with schizophrenia. Schizophr. Bull. 2011, 37:1147-1156.
78. Schwarcz R., Rassoulpour A., Wu H.Q., Medoff D., Tamminga C.A., Roberts R.C. Increased cortical kynurenate content in schizophrenia. Biol. Psychiatry 2001, 50:521-530.
79. Schwarcz R., Bruno J.P., Muchowski P.J., Wu H.Q. Kynurenines in the mammalian brain: when physiology meets pathology. Nat. Rev. Neurosci. 2012, 13(7):465-477.
80. Schwieler L., Linderholm K.R., Nilsson-Todd L.K., Erhardt S., Engberg G. Clozapine interacts with the glycine site of the NMDA receptor: electrophysiological studies of dopamine neurons in the rat ventral tegmental area. Life Sci. 2008, 83:170-175.
81. Soderlund J., Schroder J., Nordin C., Samuelsson M., Walther-Jallow L., Karlsson H., Erhardt S., Engberg G. Activation of brain interleukin-1beta in schizophrenia. Mol. Psychiatry 2009, 14:1069-1071.
82. Terrando N., Monaco C., Ma D., Foxwell B.M., Feldmann M., Maze M. Tumor necrosis factor-alpha triggers a cytokine cascade yielding postoperative cognitive decline. Proc. Natl. Acad. Sci. USA 2010, 107:20518-20522.
83. Tohmi M., Tsuda N., Watanabe Y., Kakita A., Nawa H. Perinatal inflammatory cytokine challenge results in distinct neurobehavioral alterations in rats: implication in psychiatric disorders of developmental origin. Neurosci. Res. 2004, 50:67-75.
84. Yates J.W., Meij J.T., Sullivan J.R., Richtand N.M., Yu L. Bimodal effect of amphetamine on motor behaviors in C57BL/6 mice. Neurosci. Lett. 2007, 427:66-70.
85. Yolken R.H., Torrey E.F. Are some cases of psychosis caused by microbial agents? A review of the evidence. Mol. Psychiatry 2008, 13:470-479.
86. Yoon T., Okada J., Jung M.W., Kim J.J. Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learn. Mem. 2008, 15:97-105.
87. Young C., Jevtovic-Todorovic V., Qin Y.Q., Tenkova T., Wang H., Labruyere J., Olney J.W. Potential of ketamine and midazolam, individually or in combination, to induce apoptotic neurodegeneration in the infant mouse brain. Br. J. Pharmacol. 2005, 146:189-197.