Altered interleukin-18 levels are associated with cognitive impairment in chronic schizophrenia

Journal of Psychiatric Research

Volumn 76, Issue , 2016, Pages 9-15

  Wu, Jing Qin ^a,b,c   Chen, Da Chun ^c   Tan, Yun Long ^c   Tan, Shu Ping ^c   Xiu, Mei Hong ^c   Wang, Zhi Ren ^c   De Yang, Fu ^c   Soares, Jair C ^d   Zhang, Xiang Yang ^c,d  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b SCHIZOPHRENIA RESEARCH INSTITUTE   (Australia)

^c PEKING UNIVERSITY   (China)

^d UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Behavior; Biological psychiatry; Cytokines; Neuropsychiatry; Schizophrenia

Indexed keywords

INTERLEUKIN 18;

ADULT; ARTICLE; ASSESSMENT OF HUMANS; CHRONIC PATIENT; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DELAYED MEMORY; EDUCATIONAL STATUS; FEMALE; HUMAN; IMMUNE RESPONSE; MAJOR CLINICAL STUDY; MALE; MEMORY; MENTAL PERFORMANCE; NEUROLOGIC EXAMINATION; POSITIVE AND NEGATIVE SYNDROME SCALE; PRIORITY JOURNAL; REPEATABLE BATTERY FOR THE ASSESSMENT OF NEUROPSYCHOLOGICAL STATUS; SCHIZOPHRENIA; SHORT TERM MEMORY; AGED; ANALYSIS OF VARIANCE; BLOOD; CHRONIC DISEASE; COGNITION DISORDERS; COMPLICATION; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; PSYCHOLOGICAL RATING SCALE; STATISTICS;

ADULT; AGED; ANALYSIS OF VARIANCE; CHRONIC DISEASE; COGNITION DISORDERS; FEMALE; HUMANS; INTERLEUKIN-18; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PSYCHIATRIC STATUS RATING SCALES; SCHIZOPHRENIA; STATISTICS AS TOPIC;

EID: 84960108707     PISSN: 00223956     EISSN: 18791379     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2016.01.013     Document Type: Article

References (70)

1. Aberg K., Adkins D.E., Bukszar J., Webb B.T., Caroff S.N., Miller D.D., et al. Genomewide association study of movement-related adverse antipsychotic effects. Biol. Psychiatry 2010, 67:279-282.
2. Alboni S., Cervia D., Sugama S., Conti B. Interleukin 18 in the CNS. J. Neuroinflammation 2010, 7:9.
3. Altshuler L.L., Ventura J., van Gorp W.G., Green M.F., Theberge D.C., Mintz J. Neurocognitive function in clinically stable men with bipolar I disorder or schizophrenia and normal control subjects. Biol. Psychiatry 2004, 56:560-569.
4. Anderson G., Maes M. Schizophrenia: linking prenatal infection to cytokines, the tryptophan catabolite (TRYCAT) pathway, NMDA receptor hypofunction, neurodevelopment and neuroprogression. Prog. Neuro Psychopharmacol. Biol. Psychiatry 2013, 42:5-19.
5. Baune B.T., Ponath G., Golledge J., Varga G., Arolt V., Rothermundt M., et al. Association between IL-8 cytokine and cognitive performance in an elderly general population-the MEMO-Study. Neurobiol. Aging 2008, 29:937-944.
6. Bossu P., Ciaramella A., Salani F., Bizzoni F., Varsi E., Di Iulio F., et al. Interleukin-18 produced by peripheral blood cells is increased in Alzheimer's disease and correlates with cognitive impairment. Brain Behav. Immun. 2008, 22:487-492.
7. Chandrasekar B., Vemula K., Surabhi R.M., Li-Weber M., Owen-Schaub L.B., Jensen L.E., et al. Activation of intrinsic and extrinsic proapoptotic signaling pathways in interleukin-18-mediated human cardiac endothelial cell death. J. Biol. Chem. 2004, 279:20221-20233.
8. Condray R., Yao J.K. Cognition, dopamine and bioactive lipids in schizophrenia. Front. Biosci. Sch. Ed. 2011, 3:298-330.
9. Curran B., O'Connor J.J. The pro-inflammatory cytokine interleukin-18 impairs long-term potentiation and NMDA receptor-mediated transmission in the rat hippocampus in vitro. Neuroscience 2001, 108:83-90.
10. Curran B.P., Murray H.J., O'Connor J.J. A role for c-Jun N-terminal kinase in the inhibition of long-term potentiation by interleukin-1beta and long-term depression in the rat dentate gyrus in vitro. Neuroscience 2003, 118:347-357.
11. del Rey A., Balschun D., Wetzel W., Randolf A., Besedovsky H.O. A cytokine network involving brain-borne IL-1beta, IL-1ra, IL-18, IL-6, and TNFalpha operates during long-term potentiation and learning. Brain Behav. Immun. 2013, 33:15-23.
12. Dickerson F., Boronow J.J., Stallings C., Origoni A.E., Cole S.K., Yolken R.H. Cognitive functioning in schizophrenia and bipolar disorder: comparison of performance on the repeatable battery for the assessment of neuropsychological status. Psychiatry Res. 2004, 129:45-53.
13. Dinarello C.A., Fantuzzi G. Interleukin-18 and host defense against infection. J. Infect. Dis. 2003, 187(Suppl. 2):S370-S384.
14. Fan X., Pristach C., Liu E.Y., Freudenreich O., Henderson D.C., Goff D.C. Elevated serum levels of C-reactive protein are associated with more severe psychopathology in a subgroup of patients with schizophrenia. Psychiatry Res. 2007, 149:267-271.
15. Felderhoff-Mueser U., Schmidt O.I., Oberholzer A., Buhrer C., Stahel P.F. IL-18: a key player in neuroinflammation and neurodegeneration?. Trends Neurosci. 2005, 28:487-493.
16. Fillman S.G., Cloonan N., Miller L.C., Weickert C.S. Markers of inflammation in the prefrontal cortex of individuals with schizophrenia. Mol. Psychiatry 2013, 18:133.
17. Fillman S.G., Weickert T.W., Lenroot R.K., Catts S.V., Bruggemann J.M., Catts V.S., et al. Elevated peripheral cytokines characterize a subgroup of people with schizophrenia displaying poor verbal fluency and reduced Broca's area volume. Molecular Psychiatry 2015.
18. Frodl T., Amico F. Is there an association between peripheral immune markers and structural/functional neuroimaging findings?. Prog. Neuro Psychopharmacol. Biol. Psychiatry 2014, 48:295-303.
19. Harvey P.D., Green M.F., Keefe R.S., Velligan D.I. Cognitive functioning in schizophrenia: a consensus statement on its role in the definition and evaluation of effective treatments for the illness. J. Clin. Psychiatry 2004, 65:361-372.
20. Heaton R.K., Gladsjo J.A., Palmer B.W., Kuck J., Marcotte T.D., Jeste D.V. Stability and course of neuropsychological deficits in schizophrenia. Arch. General Psychiatry 2001, 58:24-32.
21. Heinrichs R.W., Zakzanis K.K. Neurocognitive deficit in schizophrenia: a quantitative review of the evidence. Neuropsychology 1998, 12:426-445.
22. Huang W.X., Huang P., Hillert J. Increased expression of caspase-1 and interleukin-18 in peripheral blood mononuclear cells in patients with multiple sclerosis. Mult. Scler. 2004, 10:482-487.
23. Iannello A., Samarani S., Debbeche O., Tremblay C., Toma E., Boulassel M.R., et al. Role of interleukin-18 in the development and pathogenesis of AIDS. AIDS Rev. 2009, 11:115-125.
24. Kanno T., Nagata T., Yamamoto S., Okamura H., Nishizaki T. Interleukin-18 stimulates synaptically released glutamate and enhances postsynaptic AMPA receptor responses in the CA1 region of mouse hippocampal slices. Brain Res. 2004, 1012:190-193.
25. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 1987, 13:261-276.
26. Kim Y.K., Kim L., Lee M.S. Relationships between interleukins, neurotransmitters and psychopathology in drug-free male schizophrenics. Schizophrenia Res. 2000, 44:165-175.
27. Kirkpatrick B., Miller B.J. Inflammation and schizophrenia. Schizophr. Bull. 2013, 39:1174-1179.
28. Kneeland R.E., Fatemi S.H. Viral infection, inflammation and schizophrenia. Prog. Neuro Psychopharmacol. Biol. Psychiatry 2013, 42:35-48.
29. Lehman A.F., Lieberman J.A., Dixon L.B., McGlashan T.H., Miller A.L., Perkins D.O., et al. Practice guideline for the treatment of patients with schizophrenia, second edition. Am. J. Psychiatry 2004, 161:1-56.
30. Leza J.C., Garcia-Bueno B., Bioque M., Arango C., Parellada M., Do K., et al. Inflammation in schizophrenia: a question of balance. Neurosci. Biobehav. Rev. 2015, 55:612-626.
31. Li Z., Qu J., Xu X., Zhou X., Zou H., Wang N., et al. A genome-wide association study reveals association between common variants in an intergenic region of 4q25 and high-grade myopia in the Chinese Han population. Hum. Mol. Genet. 2011, 20:2861-2868.
32. Liu J., Liu J., Zhou Y., Li S., Li Y., Song X., et al. Association between promoter variants of interleukin-18 and schizophrenia in a Han Chinese population. DNA Cell Biol. 2011, 30:913-917.
33. Losy J., Niezgoda A. IL-18 in patients with multiple sclerosis. Acta Neurol. Scand. 2001, 104:171-173.
34. Lu L.X., Guo S.Q., Chen W., Li Q., Cheng J., Guo J.H. Effect of clozapine and risperidone on serum cytokine levels in patients with first-episode paranoid schizophrenia. Di Yi Jun Yi Da Xue Xue Bao 2004, 24:1251-1254.
35. McAllister C.G., van Kammen D.P., Rehn T.J., Miller A.L., Gurklis J., Kelley M.E., et al. Increases in CSF levels of interleukin-2 in schizophrenia: effects of recurrence of psychosis and medication status. Am. J. Psychiatry 1995, 152:1291-1297.
36. Meyer U. Developmental neuroinflammation and schizophrenia. Prog. Neuro Psychopharmacol. Biol. Psychiatry 2013, 42:20-34.
37. Miller B.J., Buckley P., Seabolt W., Mellor A., Kirkpatrick B. Meta-analysis of cytokine alterations in schizophrenia: clinical status and antipsychotic effects. Biol. Psychiatry 2011, 70:663-671.
38. Miller B.J., Culpepper N., Rapaport M.H. C-reactive protein levels in schizophrenia: a review and meta-analysis. Clin. Schizophr. Relat. Psychoses 2014, 7:223-230.
39. Miller B.J., Mellor A., Buckley P. Interleukin-6 and cognition in non-affective psychosis. Schizophr. Bull. 2013, 39.
40. Mondelli V., Cattaneo A., Belvederi Murri M., Di Forti M., Handley R., Hepgul N., et al. Stress and inflammation reduce brain-derived neurotrophic factor expression in first-episode psychosis: a pathway to smaller hippocampal volume. J. Clin. Psychiatry 2011, 72:1677-1684.
41. Muller N., Dobmeier P., Empl M., Riedel M., Schwarz M., Ackenheil M. Soluble IL-6 receptors in the serum and cerebrospinal fluid of paranoid schizophrenic patients. Eur. Psychiatry 1997, 12:294-299.
42. Muller N., Schwarz M. Schizophrenia as an inflammation-mediated dysbalance of glutamatergic neurotransmission. Neurotox. Res. 2006, 10:131-148.
43. Nakanishi K., Yoshimoto T., Tsutsui H., Okamura H. Interleukin-18 regulates both Th1 and Th2 responses. Annu. Rev. Immunol. 2001, 19:423-474.
44. Nicoletti F., Di Marco R., Mangano K., Patti F., Reggio E., Nicoletti A., et al. Increased serum levels of interleukin-18 in patients with multiple sclerosis. Neurology 2001, 57:342-344.
45. Ojala J., Alafuzoff I., Herukka S.K., van Groen T., Tanila H., Pirttila T. Expression of interleukin-18 is increased in the brains of Alzheimer's disease patients. Neurobiol. Aging 2009, 30:198-209.
46. Ojala J.O., Sutinen E.M., Salminen A., Pirttila T. Interleukin-18 increases expression of kinases involved in tau phosphorylation in SH-SY5Y neuroblastoma cells. J. Neuroimmunol. 2008, 205:86-93.
47. Palladino I., Salani F., Ciaramella A., Rubino I.A., Caltagirone C., Fagioli S., et al. Elevated levels of circulating IL-18BP and perturbed regulation of IL-18 in schizophrenia. J. Neuroinflammation 2012, 9:206.
48. Palmer B.W., Dawes S.E., Heaton R.K. What do we know about neuropsychological aspects of schizophrenia?. Neuropsychol. Rev. 2009, 19:365-384.
49. Potvin S., Stip E., Sepehry A.A., Gendron A., Bah R., Kouassi E. Inflammatory cytokine alterations in schizophrenia: a systematic quantitative review. Biol. Psychiatry 2008, 63:801-808.
50. Purcell S.M., Wray N.R., Stone J.L., Visscher P.M., O'Donovan M.C., Sullivan P.F., et al. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 2009, 460:748-752.
51. Rajji T.K., Mulsant B.H. Nature and course of cognitive function in late-life schizophrenia: a systematic review. Schizophrenia Res. 2008, 102:122-140.
52. Randolph C., Tierney M.C., Mohr E., Chase T.N. The repeatable battery for the assessment of neuropsychological status (RBANS): preliminary clinical validity. J. Clin. Exp. Neuropsychol. 1998, 20:310-319.
53. Reale M., Patruno A., De Lutiis M.A., Pesce M., Felaco M., Di Giannantonio M., et al. Dysregulation of chemo-cytokine production in schizophrenic patients versus healthy controls. BMC Neurosci. 2011, 12:13.
54. Ripke S., Neale B.M., Corvin A., Walters J.T., Farh K.H., Holmans P.A., et al. Biological insights from 108 schizophrenia-associated genetic loci. Nature 2014, 511:421-427.
55. Ripke S., Sanders R.A., Kendler K.S., Levinson D.F., Sklar P., Holmans P.A., et al. Genome-wide association study identifies five new schizophrenia loci. Nat. Genet. 2011, 43:969-976.
56. Sharma T., Antonova L. Cognitive function in schizophrenia. Deficits, functional consequences, and future treatment. Psychiatr. Clin. N. Am. 2003, 26:25-40.
57. Shi J., Levinson D.F., Duan J., Sanders A.R., Zheng Y., Pe'er I., et al. Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 2009, 460:753-757.
58. Shirts B.H., Wood J., Yolken R.H., Nimgaonkar V.L. Comprehensive evaluation of positional candidates in the IL-18 pathway reveals suggestive associations with schizophrenia and herpes virus seropositivity. Am. J. Med. Genet. Part B Neuropsychiatric Genet. 2008, 147:343-350.
59. Stefansson H., Ophoff R.A., Steinberg S., Andreassen O.A., Cichon S., Rujescu D., et al. Common variants conferring risk of schizophrenia. Nature 2009, 460:744-747.
60. Sutinen E.M., Pirttila T., Anderson G., Salminen A., Ojala J.O. Pro-inflammatory interleukin-18 increases Alzheimer's disease-associated amyloid-beta production in human neuron-like cells. J. Neuroinflamm. 2012, 9:199.
61. Tanaka K.F., Shintani F., Fujii Y., Yagi G., Asai M. Serum interleukin-18 levels are elevated in schizophrenia. Psychiatry Res. 2000, 96:75-80.
62. Toyooka K., Watanabe Y., Iritani S., Shimizu E., Iyo M., Nakamura R., et al. A decrease in interleukin-1 receptor antagonist expression in the prefrontal cortex of schizophrenic patients. Neurosci. Res. 2003, 46:299-307.
63. Watanabe Y., Someya T., Nawa H. Cytokine hypothesis of schizophrenia pathogenesis: evidence from human studies and animal models. Psychiatry Clin. Neurosci. 2010, 64:217-230.
64. Wheeler R.D., Culhane A.C., Hall M.D., Pickering-Brown S., Rothwell N.J., Luheshi G.N. Detection of the interleukin 18 family in rat brain by RT-PCR. Brain Res. Mol. Brain Res. 2000, 77:290-293.
65. Woods S.W. Chlorpromazine equivalent doses for the newer atypical antipsychotics. J. Clin. Psychiatry 2003, 64:663-667.
66. Xiu M.H., Chen da C., Wang D., Zhang K., Dong A., Tang W., et al. Elevated interleukin-18 serum levels in chronic schizophrenia: association with psychopathology. J. Psychiatr. Res. 2012, 46:1093-1098.
67. Yaffe K., Lindquist K., Penninx B.W., Simonsick E.M., Pahor M., Kritchevsky S., et al. Inflammatory markers and cognition in well-functioning African-American and white elders. Neurology 2003, 61:76-80.
68. Zhang B.H., Tan Y.L., Zhang W.F., Wang Z.R., Yang G.G., Shi C., et al. Repeatable battery for the assessment of neuropsychological status (RBANS) as a Screening test in chinese: reliability and validity. Chin. Ment. Health J. 2009, 28:865-869.
69. Zhang X.Y., Tang W., Xiu M.H., Chen da C., Yang F.D., Tan Y.L., et al. Interleukin 18 and cognitive impairment in first episode and drug naive schizophrenia versus healthy controls. Brain Behav. Immun. 2013, 32:105-111.
70. Zhang X.Y., Zhou D.F., Cao L.Y., Zhang P.Y., Wu G.Y., Shen Y.C. Changes in serum interleukin-2, -6, and -8 levels before and during treatment with risperidone and haloperidol: relationship to outcome in schizophrenia. J. Clin. Psychiatry 2004, 65:940-947.