Depression, Cytokine, and Cytokine by Treatment Interactions Modulate Gene Expression in Antipsychotic Naïve First Episode Psychosis

Molecular Neurobiology

Volumn 53, Issue 8, 2016, Pages 5701-5709

  Noto, Cristiano ^a,b   Ota, Vanessa Kiyomi ^a   Santoro, Marcos Leite ^a   Gouvea, Eduardo Sauerbronn ^a,b   Silva, Patricia Natalia ^a   Spindola, Leticia Maria ^a   Cordeiro, Quirino ^a,b   Bressan, Rodrigo Affonseca ^a   Gadelha, Ary ^a   Brietzke, Elisa ^a   Belangero, Sintia Iole ^a   Maes, Michael ^c,d  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b FACULDADE DE CIÊNCIAS MÉDICAS DA SANTA CASA DE SÃO PAULO   (Brazil)

^c STATE UNIVERSITY OF LONDRINA   (Brazil)

^d CHULALONGKORN UNIVERSITY   (Thailand)

Author keywords

Antipsychotic na ve; Depression; First episode psychosis; Gene expression; Immune; Inflammation; Neuroprogression; Schizophrenia

Indexed keywords

CATECHOL METHYLTRANSFERASE; CYTOKINE; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 6; MESSENGER RNA; MICRORNA; MYELIN BASIC PROTEIN; RISPERIDONE; TUMOR NECROSIS FACTOR; BIOLOGICAL MARKER; NEUROLEPTIC AGENT;

ADULT; AKT1 GENE; ARTICLE; CALGARY DEPRESSION SCALE; COMT GENE; CONTROLLED STUDY; DEPRESSION; DICER1 GENE; DISC1 GENE; DROSHA GENE; FEMALE; GENE; GENE EXPRESSION; HUMAN; INTERLEUKIN 2 GENE; INTERLEUKIN 6 GENE; MAJOR CLINICAL STUDY; MALE; MBP GENE; NDEL1 GENE; POSITIVE AND NEGATIVE SYNDROME SCALE; PSYCHOSIS; UFD1L GENE; BLOOD; CASE CONTROL STUDY; DEMOGRAPHY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; STATISTICAL MODEL;

ANTIPSYCHOTIC AGENTS; BIOMARKERS; CASE-CONTROL STUDIES; CYTOKINES; DEMOGRAPHY; DEPRESSION; GENE EXPRESSION REGULATION; HUMANS; LOGISTIC MODELS; PSYCHOTIC DISORDERS; RNA, MESSENGER;

EID: 84944929790     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-015-9489-3     Document Type: Article

References (59)

1. Whiteford HA, Degenhardt L, Rehm J, Baxter AJ, Ferrari AJ, Erskine HE, Charlson FJ, Norman RE et al (2013) Global burden of disease attributable to mental and substance use disorders: findings from the Global Burden of Disease Study 2010. Lancet 382(9904):1575–1586. doi:10.1016/S0140-6736(13)61611-6
2. Arnedo J, Svrakic DM, Del Val C, Romero-Zaliz R, Hernandez-Cuervo H, Molecular Genetics of Schizophrenia C, Fanous AH, Pato MT et al (2014) Uncovering the hidden risk architecture of the schizophrenias: confirmation in three independent genome-wide association studies. Am J Psychiatry. doi:10.1176/appi.ajp.2014.14040435
3. Davis J, Moylan S, Harvey BH, Maes M, Berk M (2014) Neuroprogression in schizophrenia: pathways underpinning clinical staging and therapeutic corollaries. Austral N Z J Psychiatr 48(6):512–529. doi:10.1177/0004867414533012
4. Sullivan PF, Kendler KS, Neale MC (2003) Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. Arch Gen Psychiatry 60(12):1187–1192. doi:10.1001/archpsyc.60.12.1187
5. Bodmer W, Bonilla C (2008) Common and rare variants in multifactorial susceptibility to common diseases. Nat Genet 40(6):695–701. doi:10.1038/ng.f.136
6. Schizophrenia Working Group of the Psychiatric Genomics C (2014) Biological insights from 108 schizophrenia-associated genetic loci. Nature 511(7510):421–427. doi:10.1038/nature13595
7. Anderson G, Berk M, Dodd S, Bechter K, Altamura AC, Dell’osso B, Kanba S, Monji A et al (2013) Immuno-inflammatory, oxidative and nitrosative stress, and neuroprogressive pathways in the etiology, course and treatment of schizophrenia. Prog Neuro-Psychopharmacol Biol Psychiatry 42:1–4. doi:10.1016/j.pnpbp.2012.10.008
8. Ripke S, O’Dushlaine C, Chambert K, Moran JL, Kahler AK, Akterin S, Bergen SE, Collins AL et al (2013) Genome-wide association analysis identifies 13 new risk loci for schizophrenia. Nat Genet 45(10):1150–1159. doi:10.1038/ng.2742
9. Meyer U (2013) Developmental neuroinflammation and schizophrenia. Prog Neuro-Psychopharmacol Biol Psychiatry 42:20–34. doi:10.1016/j.pnpbp.2011.11.003
10. Miller BJ, Buckley P, Seabolt W, Mellor A, Kirkpatrick B (2011) Meta-analysis of cytokine alterations in schizophrenia: clinical status and antipsychotic effects. Biol Psychiatry 70(7):663–671. doi:10.1016/j.biopsych.2011.04.013
11. Park KM, Bowers WJ (2010) Tumor necrosis factor-alpha mediated signaling in neuronal homeostasis and dysfunction. Cell Signal 22(7):977–983. doi:10.1016/j.cellsig.2010.01.010
12. Pan W, Zadina JE, Harlan RE, Weber JT, Banks WA, Kastin AJ (1997) Tumor necrosis factor-alpha: a neuromodulator in the CNS. Neurosci Biobehav Rev 21(5):603–613
13. Dunn AJ, Wang J, Ando T (1999) Effects of cytokines on cerebral neurotransmission. Comparison with the effects of stress. Adv Exp Med Biol 461:117–127. doi:10.1007/978-0-585-37970-8_8
14. Thompson CD, Zurko JC, Hanna BF, Hellenbrand DJ, Hanna A (2013) The therapeutic role of interleukin-10 after spinal cord injury. J Neurotrauma 30(15):1311–1324. doi:10.1089/neu.2012.2651
15. Calabrese F, Rossetti AC, Racagni G, Gass P, Riva MA, Molteni R (2014) Brain-derived neurotrophic factor: a bridge between inflammation and neuroplasticity. Front Cell Neurosci 8:430. doi:10.3389/fncel.2014.00430
16. Song XQ, Lv LX, Li WQ, Hao YH, Zhao JP (2009) The interaction of nuclear factor-kappa B and cytokines is associated with schizophrenia. Biol Psychiatry 65(6):481–488. doi:10.1016/j.biopsych.2008.10.018
17. Mattson MP, Culmsee C, Yu Z, Camandola S (2000) Roles of nuclear factor kappaB in neuronal survival and plasticity. J Neurochem 74(2):443–456
18. Hodge DR, Xiao W, Clausen PA, Heidecker G, Szyf M, Farrar WL (2001) Interleukin-6 regulation of the human DNA methyltransferase (HDNMT) gene in human erythroleukemia cells. J Biol Chem 276(43):39508–39511. doi:10.1074/jbc.C100343200
19. Saradalekshmi KR, Neetha NV, Sathyan S, Nair IV, Nair CM, Banerjee M (2014) DNA methyl transferase (DNMT) gene polymorphisms could be a primary event in epigenetic susceptibility to schizophrenia. PLoS One 9(5):e98182. doi:10.1371/journal.pone.0098182
20. Wockner LF, Noble EP, Lawford BR, Young RM, Morris CP, Whitehall VL, Voisey J (2014) Genome-wide DNA methylation analysis of human brain tissue from schizophrenia patients. Translat Psychiatr 4:e339. doi:10.1038/tp.2013.111
21. Noto C, Ota VK, Gouvea ES, Rizzo LB, Spindola LM, Honda PH, Cordeiro Q, Belangero SI et al (2014) Effects of risperidone on cytokine profile in drug-naive first-episode psychosis. Int J Neuropsychopharmacol / Off Sci J Coll Int Neuropsychopharmacol 18 (4). doi:10.1093/ijnp/pyu042
22. Noto C, Ota VK, Gadelha A, Noto MN, Barbosa DS, Bonifacio KL, Nunes SO, Cordeiro Q et al (2015) Oxidative stress in drug naive first episode psychosis and antioxidant effects of risperidone. J Psychiatr Res 68:210–216. doi:10.1016/j.jpsychires.2015.07.003
23. Ota VK, Noto C, Gadelha A, Santoro ML, Ortiz BB, Andrade EH, Tasso BC, Spindola LM et al (2014) Evaluation of neurotransmitter receptor gene expression identifies GABA receptor changes: a follow-up study in antipsychotic-naive patients with first-episode psychosis. J Psychiatr Res 56:130–136. doi:10.1016/j.jpsychires.2014.05.012
24. Ota VK, Noto C, Gadelha A, Santoro ML, Spindola LM, Gouvea ES, Stilhano RS, Ortiz BB et al (2014) Changes in gene expression and methylation in the blood of patients with first-episode psychosis. Schizophr Res. doi:10.1016/j.schres.2014.09.008
25. Ota VK, Noto C, Gadelha A, Santoro ML, Silva PN, Melaragno MI, Smith Mde A, Cordeiro Q et al (2013) Neurotransmitter receptor and regulatory gene expression in peripheral blood of Brazilian drug-naive first-episode psychosis patients before and after antipsychotic treatment. Psychiatry Res 210(3):1290–1292. doi:10.1016/j.psychres.2013.09.016
26. Gozdzik-Zelazny A, Borecki L, Pokorski M (2011) Depressive symptoms in schizophrenic patients. Europ J Med Res 16(12):549–552
27. Upthegrove R, Birchwood M, Ross K, Brunett K, McCollum R, Jones L (2010) The evolution of depression and suicidality in first episode psychosis. Acta Psychiatr Scand 122(3):211–218. doi:10.1111/j.1600-0447.2009.01506.x
28. Noto C, Gadelha A, Belangero SI, Spindola LM, Rocha NP, de Miranda AS, Teixeira AL, Cardoso Smith MA et al (2013) Circulating levels of sTNFR1 as a marker of severe clinical course in schizophrenia. J Psychiatr Res 47(4):467–471. doi:10.1016/j.jpsychires.2012.12.010
29. Vessoni AL (1993) Adaptação e estudo de confiabilidade da escala de avaliação das síndromes positiva e negativa para a esquizofrenia no Brasil. Escola Paulista de Medicina, São Paulo
30. Addington D, Addington J, Maticka-Tyndale E (1993) Assessing depression in schizophrenia: the Calgary Depression Scale. British J Psychiatr Suppl 22:39–44
31. Hayashi MA, Portaro FC, Tambourgi DV, Sucupira M, Yamane T, Fernandes BL, Ferro ES, Reboucas NA et al (2000) Molecular and immunochemical evidences demonstrate that endooligopeptidase A is the predominant cytosolic oligopeptidase of rabbit brain. Biochem Biophys Res Commun 269(1):7–13. doi:10.1006/bbrc.2000.2243
32. Rampino A, Walker RM, Torrance HS, Anderson SM, Fazio L, Di Giorgio A, Taurisano P, Gelao B et al (2014) Expression of DISC1-interactome members correlates with cognitive phenotypes related to schizophrenia. PLoS One 9(6):e99892. doi:10.1371/journal.pone.0099892
33. Gadelha A, Machado MF, Yonamine CM, Sato JR, Juliano MA, Oliveira V, Bressan RA, Hayashi MA (2013) Plasma Ndel1 enzyme activity is reduced in patients with schizophrenia—a potential biomarker? J Psychiatr Res 47(5):657–663. doi:10.1016/j.jpsychires.2013.01.009
34. Kumarasinghe N, Beveridge NJ, Gardiner E, Scott RJ, Yasawardene S, Perera A, Mendis J, Suriyakumara K et al (2013) Gene expression profiling in treatment-naive schizophrenia patients identifies abnormalities in biological pathways involving AKT1 that are corrected by antipsychotic medication. Int J Neuropsychopharmacol 16(7):1483–1503. doi:10.1017/S1461145713000035
35. Kamiya A, Tomoda T, Chang J, Takaki M, Zhan C, Morita M, Cascio MB, Elashvili S et al (2006) DISC1-NDEL1/NUDEL protein interaction, an essential component for neurite outgrowth, is modulated by genetic variations of DISC1. Hum Mol Genet 15(22):3313–3323. doi:10.1093/hmg/ddl407
36. Hayashi MA, Portaro FC, Bastos MF, Guerreiro JR, Oliveira V, Gorrao SS, Tambourgi DV, Sant’Anna OA et al (2005) Inhibition of NUDEL (nuclear distribution element-like)-oligopeptidase activity by disrupted-in-schizophrenia 1. Proc Natl Acad Sci U S A 102(10):3828–3833. doi:10.1073/pnas.0500330102
37. Hayashi MA, Guerreiro JR, Charych E, Kamiya A, Barbosa RL, Machado MF, Campeiro JD, Oliveira V et al (2010) Assessing the role of endooligopeptidase activity of Ndel1 (nuclear-distribution gene E homolog like-1) in neurite outgrowth. Mol Cell Neurosci 44(4):353–361. doi:10.1016/j.mcn.2010.04.006
38. Ira E, Zanoni M, Ruggeri M, Dazzan P, Tosato S (2013) COMT, neuropsychological function and brain structure in schizophrenia: a systematic review and neurobiological interpretation. J Psychiatr Neurosci: JPN 38(6):366–380. doi:10.1503/jpn.120178
39. Sonmez N, Rossberg JI, Evensen J, Barder HE, Haahr U, Ten Velden HW, Joa I, Johannessen JO et al (2014) Depressive symptoms in first-episode psychosis: a 10-year follow-up study. Early Interven Psychiatr. doi:10.1111/eip.12163
40. Talarowska M, Szemraj J, Berk M, Maes M, Galecki P (2015) Oxidant/antioxidant imbalance is an inherent feature of depression. BMC Psychiatr 15:71. doi:10.1186/s12888-015-0454-5
41. Al-Hakeim HK, Al-Rammahi DA, Al-Dujaili AH (2015) IL-6, IL-18, sIL-2R, and TNFalpha proinflammatory markers in depression and schizophrenia patients who are free of overt inflammation. J Affect Disord 182:106–114. doi:10.1016/j.jad.2015.04.044
42. Noto C, Ota VK, Santoro ML, Ortiz BB, Rizzo LB, Higuchi CH, Cordeiro Q, Belangero SI et al (2015) Effects of depression on the cytokine profile in drug naive first-episode psychosis. Schizophr Res. doi:10.1016/j.schres.2015.01.026
43. Kim S, Hwang Y, Webster MJ, Lee D (2015) Differential activation of immune/inflammatory response-related co-expression modules in the hippocampus across the major psychiatric disorders. Mol Psychiatry. doi:10.1038/mp.2015.79
44. Beveridge NJ, Cairns MJ (2012) MicroRNA dysregulation in schizophrenia. Neurobiol Dis 46(2):263–271. doi:10.1016/j.nbd.2011.12.029
45. Sun E, Shi Y (2014) MicroRNAs: small molecules with big roles in neurodevelopment and diseases. Exp Neurol. doi:10.1016/j.expneurol.2014.08.005
46. Balu DT, Coyle JT (2011) Neuroplasticity signaling pathways linked to the pathophysiology of schizophrenia. Neurosci Biobehav Rev 35(3):848–870. doi:10.1016/j.neubiorev.2010.10.005
47. Chalecka-Franaszek E, Chuang DM (1999) Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc Natl Acad Sci U S A 96(15):8745–8750
48. De Sarno P, Li X, Jope RS (2002) Regulation of Akt and glycogen synthase kinase-3 beta phosphorylation by sodium valproate and lithium. Neuropharmacology 43(7):1158–1164
49. Emamian ES, Hall D, Birnbaum MJ, Karayiorgou M, Gogos JA (2004) Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat Genet 36(2):131–137. doi:10.1038/ng1296
50. Kim JY, Duan X, Liu CY, Jang MH, Guo JU, Pow-anpongkul N, Kang E, Song H et al (2009) DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 63(6):761–773. doi:10.1016/j.neuron.2009.08.008
51. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P et al (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425(6956):415–419. doi:10.1038/nature01957
52. Aggarwal S, Yurlova L, Simons M (2011) Central nervous system myelin: structure, synthesis and assembly. Trends Cell Biol 21(10):585–593. doi:10.1016/j.tcb.2011.06.004
53. Matthews PR, Eastwood SL, Harrison PJ (2012) Reduced myelin basic protein and actin-related gene expression in visual cortex in schizophrenia. PLoS One 7(6):e38211. doi:10.1371/journal.pone.0038211
54. Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB, Starkey M, Webster MJ et al (2003) Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 362(9386):798–805. doi:10.1016/S0140-6736(03)14289-4
55. Santoro ML, Gadelha A, Ota VK, Cunha GR, Asevedo E, Noto CS, Spindola LM, Pan PM et al (2015) Gene expression analysis in blood of ultra-high risk subjects compared to first-episode of psychosis patients and controls. World J Biol Psychiatr:1–6. doi:10.3109/15622975.2015.1048724
56. Santarelli DM, Beveridge NJ, Tooney PA, Cairns MJ (2011) Upregulation of dicer and microRNA expression in the dorsolateral prefrontal cortex Brodmann area 46 in schizophrenia. Biol Psychiatry 69(2):180–187. doi:10.1016/j.biopsych.2010.09.030
57. Beveridge NJ, Gardiner E, Carroll AP, Tooney PA, Cairns MJ (2010) Schizophrenia is associated with an increase in cortical microRNA biogenesis. Mol Psychiatry 15(12):1176–1189. doi:10.1038/mp.2009.84
58. Sanders AR, Goring HH, Duan J, Drigalenko EI, Moy W, Freda J, He D, Shi J et al (2013) Transcriptome study of differential expression in schizophrenia. Hum Mol Genet 22(24):5001–5014. doi:10.1093/hmg/ddt350
59. Giraldez AJ, Cinalli RM, Glasner ME, Enright AJ, Thomson JM, Baskerville S, Hammond SM, Bartel DP et al (2005) MicroRNAs regulate brain morphogenesis in zebrafish. Science 308(5723):833–838. doi:10.1126/science.1109020