Interaction of BDNF with cytokines in chronic schizophrenia

Brain, Behavior, and Immunity

Volumn 51, Issue , 2016, Pages 169-175

  Zhang, Xiang Yang ^a,b   Tan, Yun Long ^a   Chen, Da Chun ^a   Tan, Shu Ping ^a   Yang, Fu De ^a   Wu, Hanjing Emily ^b   Zunta Soares, Giovana B ^b   Huang, Xu Feng ^c   Kosten, Thomas R ^d   Soares, Jair C ^b  

^a PEKING UNIVERSITY   (China)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF WOLLONGONG   (Australia)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

BDNF; Cognition; Cytokine; Interaction; Schizophrenia; Symptom

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYTOKINE; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; TUMOR NECROSIS FACTOR; BRAIN-DERIVED NEUROTROPHIC FACTOR, HUMAN; IL6 PROTEIN, HUMAN; NEUROLEPTIC AGENT;

ADULT; AGED; ARTICLE; CLINICAL FEATURE; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; PATHOPHYSIOLOGY; POSITIVE AND NEGATIVE SYNDROME SCALE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; SCHIZOPHRENIA; BLOOD; COMPLICATION; MIDDLE AGED;

ADULT; ANTIPSYCHOTIC AGENTS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CYTOKINES; FEMALE; HUMANS; INTERLEUKIN-2; INTERLEUKIN-6; INTERLEUKIN-8; MALE; MIDDLE AGED; SCHIZOPHRENIA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84948800339     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.09.014     Document Type: Article

References (73)

1. Adachi, N., Numakawa, T., Richards, M., Nakajima, S., Kunugi, H., New insight in expression, transport, and secretion of brain-derived neurotrophic factor: implications in brain-related diseases. World J. Biol. Chem. 5:4 (2014), 409–428.
2. Al-Asmari, A.K., Khan, M.W., Inflammation and schizophrenia: alterations in cytokine levels and perturbation in antioxidative defense systems. Hum. Exp. Toxicol. 33:2 (2014), 115–122.
3. Altamura, A.C., Pozzoli, S., Fiorentini, A., Dell'osso, B., Neurodevelopment and inflammatory patterns in schizophrenia in relation to pathophysiology. Prog. Neuropsychopharmacol. Biol. Psychiatry 42 (2013), 63–70.
4. Anderson, G., Maes, M., Schizophrenia: linking prenatal infection to cytokines, the tryptophan catabolite (TRYCAT) pathway, NMDA receptor hypofunction, neurodevelopment and neuroprogression. Prog. Neuropsychopharmacol. Biol. Psychiatry 42 (2013), 5–19.
5. Bai, O., Chlan-Fourney, J., Bowen, R., Keegan, D., Li, X.M., Expression of brain-derived neurotrophic factor mRNA in rat hippocampus after treatment with antipsychotic drugs. J. Neurosci. Res. 71:1 (2003), 127–131.
6. Baker, I., Masserano, J., Wyatt, R.J., Serum cytokine concentrations in patients with schizophrenia. Schizophr. Res. 20 (1996), 199–203.
7. Baune, B.T., Konrad, C., Grotegerd, D., Suslow, T., Ohrmann, P., Bauer, J., Arolt, V., Heindel, W., Domschke, K., Schöning, S., Rauch, A.V., Sehlmeyer, C., Kugel, H., Dannlowski, U., Tumor necrosis factor gene variation predicts hippocampus volume in healthy individuals. Biol. Psychiatry 72:8 (2012), 655–662.
8. Borovcanin, M., Jovanovic, I., Radosavljevic, G., Djukic Dejanovic, S., Bankovic, D., Arsenijevic, N., Lukic, M.L., Elevated serum level of type-2 cytokine and low IL-17 in first episode psychosis and schizophrenia in relapse. J. Psychiatr. Res. 46:11 (2012), 1421–1426.
9. Borovcanin, M., Jovanovic, I., Radosavljevic, G., Djukic Dejanovic, S., Stefanovic, V., Arsenijevic, N., Lukic, M.L., Antipsychotics can modulate the cytokine profile in schizophrenia: attenuation of the type-2 inflammatory response. Schizophr. Res. 147:1 (2013), 103–109.
10. Brown, A.S., Hooton, J., Schaefer, C.A., Zhang, H., Petkova, E., Babulas, V., Perrin, M., Gorman, J.M., Susser, E.S., Elevated maternal interleukin-8 levels and risk of schizophrenia in adult off spring. Am. J. Psychiatry 161:5 (2004), 889–895.
11. Buckley, P.F., Pillai, A., Evans, D., Stirewalt, E., Mahadik, S., Brain derived neurotropic factor in first-episode psychosis. Schizophr. Res. 91:1–3 (2007), 1–5.
12. Buckley, P.F., Pillai, A., Howell, K.R., Brain-derived neurotrophic factor: findings in schizophrenia. Curr. Opin. Psychiatry 24:2 (2011), 122–127.
13. Calabrese, F., Rossetti, A.C., Racagni, G., Gass, P., Riva, M.A., Molteni, R., Brain-derived neurotrophic factor: a bridge between inflammation and neuroplasticity. Front. Cell. Neurosci., 8, 2014, 430.
14. Canetta, S.E., Brown, A.S., Prenatal infection, maternal immune activation, and risk for schizophrenia. Transl. Neurosci. 3:4 (2012), 320–327.
15. Cannella, B., Raine, C.S., Multiple sclerosis: cytokine receptors on oligodendrocytes predict innate regulation. Ann. Neurol. 55:1 (2004), 46–57.
16. Chen, D.C., Wang, J., Wang, B., Yang, S.C., Zhang, C.X., Zheng, Y.L., Li, Y.L., Wang, N., Yang, K.B., Xiu, M.H., Kosten, T.R., Zhang, X.Y., Decreased levels of serum brain-derived neurotrophic factor in drug-naïve first-episode schizophrenia: relationship to clinical phenotypes. Psychopharmacology 207:3 (2009), 375–380.
17. Drzyzga, L., Obuchowicz, E., Marcinowska, A., Herman, Z.S., Cytokines in schizophrenia and the effects of antipsychotic drugs. Brain Behav. Immun. 20:6 (2006), 532–545.
18. Dunjic-Kostic, B., Jasovic-Gasic, M., Ivkovic, M., Radonjic, N.V., Pantovic, M., Damjanovic, A., Poznanovic, S.T., Jovanovic, A., Nikolic, T., Petronijevic, N.D., Serum levels of interleukin-6 and tumor necrosis factor-alpha in exacerbation and remission phase of schizophrenia. Psychiat. Danub. 25 (2013), 55–61.
19. Favalli, G., Li, J., Belmonte-de-Abreu, P., Wong, A.H., Daskalakis, Z.J., The role of BDNF in the pathophysiology and treatment of schizophrenia. J. Psychiatr. Res. 46:1 (2012), 1–11.
20. Felderhoff-Mueser, U., Schmidt, O.I., Oberholzer, A., Bührer, C., Stahel, P.F., IL-18: a key player in neuroinflammation and neurodegeneration?. Trends Neurosci. 28:9 (2005), 487–493.
21. Fineberg, A.M., Ellman, L.M., Inflammatory cytokines and neurological and neurocognitive alterations in the course of schizophrenia. Biol. Psychiatry 73:10 (2013), 951–966.
22. Francesconi, L.P., Ceresér, K.M., Mascarenhas, R., Stertz, L., Gama, C.S., Belmonte-de-Abreu, P., Increased annexin-V and decreased TNF-α serum levels in chronic-medicated patients withschizophrenia. Neurosci. Lett. 502:3 (2011), 143–146.
23. Garay, P.A., McAllister, A.K., Novel roles for immune molecules in neural development: implications for neurodevelopmental disorders. Front. Synaptic Neurosci., 2, 2010, 136.
24. Green, M.J., Matheson, S.L., Shepherd, A., Weickert, C.S., Carr, V.J., Brain-derived neurotrophic factor levels in schizophrenia: a systematic review with meta-analysis. Mol. Psychiatry 16:9 (2011), 960–972.
25. Heese, K., Hock, C., Otten, U., Inflammatory signals induce neurotrophin expression in human microglial cells. J. Neurochem. 70:2 (1998), 699–707.
26. Kalmady, S.V., Venkatasubramanian, G., Shivakumar, V., Gautham, S., Subramaniam, A., Jose, D.A., Maitra, A., Ravi, V., Gangadhar, B.N., Relationship between interleukin-6 gene polymorphism and hippocampal volume in antipsychotic-naïve schizophrenia: evidence for differential susceptibility?. PLoS One, 9(5), 2014, e96021.
27. Kay, S.R., Fiszbein, A., Opler, L.A., The Positive and Negative Syndrome Scale (PANSS) for schizophrenia. Schizophr. Bull. 13 (1987), 261–276.
28. Keshavan, M.S., Development, disease and degeneration in schizophrenia: a unitary pathophysiological model. J. Psychiatr. Res. 33:6 (1999), 513–521.
29. Kim, Y.K., Myint, A.M., Verkerk, R., Scharpe, S., Steinbusch, H., Leonard, B., Cytokine changes and tryptophan metabolites in medication-naïve and medication-free schizophrenic patients. Neuropsychobiology 59:2 (2009), 123–129.
30. Klein, A.B., Williamson, R., Santini, M.A., Clemmensen, C., Ettrup, A., Rios, M., Knudsen, G.M., Aznar, S., Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int. J. Neuropsychopharmacol. 14:3 (2011), 347–353.
31. Kubistova, A., Horacek, J., Novak, T., Increased interleukin-6 and tumor necrosis factor alpha in first episode schizophrenia patients versus healthy controls. Psychiat. Danub. 24:Suppl 1 (2012), S153–S156.
32. Linker, R.A., Lee, D.H., Demir, S., Wiese, S., Kruse, N., Siglienti, I., Gerhardt, E., Neumann, H., Sendtner, M., Lühder, F., Gold, R., Functional role of brain-derived neurotrophic factor in neuroprotective autoimmunity: therapeutic implications in a model of multiple sclerosis. 133:Pt 8 (2010), 2248–2263.
33. Maes, M., Bocchio Chiavetto, L., Bignotti, S., Battisa Tura, G.J., Pioli, R., Boin, F., Kenis, G., Bosmans, E., de Jongh, R., Altamura, C.A., Increased serum interleukin-8 and interleukin-10 in schizophrenic patients resistant to treatment with neuroleptics and the stimulatory effects of clozapine on serum leukemia inhibitory factor receptor. Schizophr. Res. 54:3 (2002), 281–291.
34. 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 70:7 (2011), 663–671.
35. Miller, B.J., Culpepper, N., Rapaport, M.H., Buckley, P., Prenatal inflammation and neurodevelopment in schizophrenia: a review of human studies. Prog. Neuropsychopharmacol. Biol. Psychiatry 42 (2013), 92–100.
36. Müller, N., Immunology of schizophrenia. NeuroImmunoModulation 21:2–3 (2014), 109–116.
37. Na, K.S., Jung, H.Y., Kim, Y.K., The role of pro-inflammatory cytokines in the neuroinflammation and neurogenesis of schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 48 (2014), 277–286.
38. Nagahara, A.H., Tuszynski, M.H., Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat. Rev. Drug Discov. 10:3 (2011), 209–219.
39. Nawa, H., Takahashi, M., Patterson, P.H., Cytokine and growth factor involvement in schizophrenia – support for the developmental model. Mol. Psychiatry 5:6 (2000), 594–603.
40. Nieto, R., Kukuljan, M., Silva, H., BDNF and schizophrenia: from neurodevelopment to neuronal plasticity, learning, and memory. Front. Psychiatry, 4, 2013, 45.
41. Nurjono, M., Lee, J., Chong, S.A., A review of brain-derived neurotrophic factor as a candidate biomarker in schizophrenia. Clin. Psychopharmacol. Neurosci. 10:2 (2012), 61–70.
42. O'Brien, S.M., Scully, P., Dinan, T.G., Increased tumor necrosis factor-alpha concentrations with interleukin-4 concentrations in exacerbations of schizophrenia. Psychiatry Res. 160:3 (2008), 256–262.
43. Patas, K., Penninx, B.W., Bus, B.A., Vogelzangs, N., Molendijk, M.L., Elzinga, B.M., Bosker, F.J., Oude Voshaar, R.C., Association between serum brain-derived neurotrophic factor and plasma interleukin-6 in major depressive disorder with melancholic features. Brain Behav. Immun. 36 (2014), 71–79.
44. Pedrini, M., Chendo, I., Grande, I., Lobato, M.I., Belmonte-de-Abreu, P.S., Lersch, C., Walz, J., Kauer-Sant'anna, M., Kapczinski, F., Gama, C.S., Serum brain-derived neurotrophic factor and clozapine daily dose in patients with schizophrenia: a positive correlation. Neurosci. Lett. 491:3 (2011), 207–210.
45. Pillai, A., Kale, A., Joshi, S., Naphade, N., Raju, M.S., Nasrallah, H., Mahadik, S.P., Decreased BDNF levels in CSF of drug-naive first-episode psychotic subjects: correlation with plasma BDNF and psychopathology. Int. J. Neuropsychopharmacol. 13:4 (2010), 535–553.
46. Pirildar, S., Gönül, A.S., Taneli, F., Akdeniz, F., Low serum levels of brain-derived neurotrophic factor in patients with schizophrenia do not elevate after antipsychotic treatment. Prog. Neuropsychopharmacol. Biol. Psychiatry 28:4 (2004), 709–713.
47. Potvin, S., Stip, E., Sepehry, A.A., Gendron, A., Bah, R., Kouassi, E., Inflammatory cytokine alterations in schizophrenia: a systematic quantitative review. Biol. Psychiatry 63:8 (2008), 801–808.
48. Proost, P., Wuyts, A., van Damme, J., The role of chemokines in inflammation. Int. J. Clin. Lab. Res. 26:4 (1996), 211–223.
49. Rapoport, J.L., Giedd, J.N., Gogtay, N., Neurodevelopmental model of schizophrenia: update 2012. Mol. Psychiatry 17:12 (2012), 1228–1238.
50. Ray, M.T., Shannon Weickert, C., Webster, M.J., Decreased BDNF and TrkB mRNA expression in multiple cortical areas of patients with schizophrenia and mood disorders. Transl. Psychiatry, 4, 2014, e389.
51. Rizos, E., Rontos, I., Laskos, E., Arsenis, G., Michalopoulou, P., Vasilopoulos, D., Gournellis, R., Lykouras, L., Decreased serum levels of BDNF in first episode patients with schizophrenia and its psychopathological correlations. Schizophr. Res. 102:1–3 (2008), 208–209.
52. Rizos, E.N., Papadopoulou, A., Laskos, E., Michalopoulou, P.G., Kastania, A., Vasilopoulos, D., Katsafouros, K., Lykouras, L., Reduced serum BDNF levels in patients with chronic schizophrenic disorder in relapse, who were treated with typical or atypical antipsychotics. World J. Biol. Psychiatry 11:2 Pt 2 (2010), 251–255.
53. Rodriguez-Jimenez, R., Bagney, A., Mezquita, L., Martinez-Gras, I., Sanchez-Morla, E., Mesa, N., Ibanez, M., Diez-Martin, J., Jimenez-Arriero, M., Lobo, A., Santos, J., Palomo, T., PARG. Cognition and the five-factor model of the Positive and Negative Syndrome Scale in schizophrenia. Schizophr. Res. 143:1 (2013), 77–83.
54. Sasayama, D., Hattori, K., Wakabayashi, C., Teraishi, T., Hori, H., Ota, M., Yoshida, S., Arima, K., Higuchi, T., Amano, N., Kunugi, H., Increased cerebrospinal fluid interleukin-6 levels in patients with schizophrenia and those with major depressive disorder. J. Psychiatr. Res. 47:3 (2013), 401–406.
55. Schuhmann, B., Dietrich, A., Sel, S., Hahn, C., Klingenspor, M., Lommatzsch, M., Gudermann, T., Braun, A., Renz, H., Nockher, W.A., A role for brain-derived neurotrophic factor in B cell development. J. Neuroimmunol. 163:1–2 (2005), 15–23.
56. Schulte-Herbrüggen, O., Nassenstein, C., Lommatzsch, M., Quarcoo, D., Renz, H., Braun, A., Tumor necrosis factor-alpha and interleukin-6 regulate secretion of brain-derived neurotrophic factor in human monocytes. J. Neuroimmunol. 160:1–2 (2005), 204–209.
57. Singh, B., Bera, N.K., Nayak, C.R., Chaudhuri, T.K., Decreased serum levels of interleukin-2 and interleukin-6 in Indian Bengalee schizophrenic patients. Cytokine 47:1 (2009), 1–5.
58. Song, C., Zhang, Y., Dong, Y., Acute and subacute IL-1β administrations differentially modulate neuroimmune and neurotrophicsystems: possible implications for neuroprotection and neurodegeneration. J. Neuroinflammation, 10, 2013, 59.
59. Song, X., Fan, X., Zhang, J., Zheng, H., Li, X., Pang, L., Chen, X., Zhang, W., Harrington, A., Ziedonis, D., Lv, L., Prolactin serum levels correlate with inflammatory status in drug-naïve first-episode schizophrenia. World J. Biol. Psychiatry 15:7 (2014), 546–552.
60. Sperner-Unterweger, B., Fuchs, D., 2015. Schizophrenia and psychoneuroimmunology: an integrative view. Curr. Opin. Psychiatry [Epub ahead of print].
61. Tourjman, V., Kouassi, É., Koué, M.È., Rocchetti, M., Fortin-Fournier, S., Fusar-Poli, P., Potvin, S., Antipsychotics’ effects on blood levels of cytokines in schizophrenia: a meta-analysis. Schizophr. Res. 151:1–3 (2013), 43–47.
62. Upthegrove, R., Manzanares-Teson, N., Barnes, N.M., Cytokine function in medication-naive first episode psychosis: a systematic review and meta-analysis. Schizophr. Res. 155:1–3 (2014), 101–108.
63. Wallwork, R.S., Fortgang, R., Hashimoto, R., Weinberger, D.R., Dickinson, D., Searching for a consensus five-factor model of the Positive and Negative Syndrome Scale for schizophrenia. Schizophr. Res. 137:1–3 (2012), 246–250.
64. Xiong, H., Yamada, K., Han, D., Nabeshima, T., Enikolopov, G., Carnahan, J., Nawa, H., Mutual regulation between the intercellular messengers nitric oxide and brain-derived neurotrophic factor in rodent neocortical neurons. Eur. J. Neurosci. 11:5 (1999), 1567–1576.
65. Xiu, M.H., Hui, L., Dang, Y.F., Hou, T.D., Zhang, C.X., Zheng, Y.L., da Chen, C., Kosten, T.R., Zhang, X.Y., Decreased serum BDNF levels in chronic institutionalized schizophrenia on long-term treatment with typical and atypical antipsychotics. Prog. Neuropsychopharmacol. Biol. Psychiatry 33:8 (2009), 1508–1512.
66. Yang, Y.Q., Sun, S.L., Yu, Y.Q., Li, W.J., Zhang, X., Xiu, M.H., Chen, D.C., Yang, F.D., Liu, H.B., Li, C.B., Kosten, T.R., Zhang, X.Y., Decreased serum brain-derived neurotrophic factor levels in schizophrenic patients with tardive dyskinesia. Neurosci. Lett. 502:1 (2011), 37–40.
67. Yogeetha, B.S., Haupt, L.M., McKenzie, K., Sutherland, H.G., Okolicsyani, R.K., Lea, R.A., Maher, B.H., Chan, R.C., Shum, D.H., Griffiths, L.R., BDNF and TNF-α polymorphisms in memory. Mol. Biol. Rep. 40:9 (2013), 5483–5490.
68. Yoshimura, R., Hori, H., Sugita, A., Ueda, N., Kakihara, S., Umene, W., Nakano, Y., Shinkai, K., Mitoma, M., Ohta, M., Shinkai, T., Nakamura, J., Treatment with risperidone for 4 weeks increased plasma 3-methoxy-4-hydroxypnenylglycol (MHPG) levels, but did not alter plasma brain-derived neurotrophic factor (BDNF) levels in schizophrenic patients. Prog. Neuropsychopharmacol. Biol. Psychiatry 31:5 (2007), 1072–1077.
69. Zakharyan, R., Boyajyan, A., Inflammatory cytokine network in schizophrenia. World J. Biol. Psychiatry 15:3 (2014), 174–187.
70. Zhang, X.Y., Zhou, D.F., Zhang, P.Y., Wu, G.Y., Cao, L.Y., Shen, Y.C., Elevated interleukin-2, interleukin-6 and interleukin-8 serum levels in neuroleptic-free schizophrenia: association with psychopathology. Schizophr. Res. 57:2–3 (2002), 247–258.
71. 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 65:7 (2004), 940–947.
72. Zhang, X.Y., Liang, J., Chen da, C., Xiu, M.H., Yang, F.D., Kosten, T.A., Kosten, T.R., Low BDNF is associated with cognitive impairment in chronic patients with schizophrenia. Psychopharmacology 222:2 (2012), 277–284.
73. Zhang, X.Y., Zhang, W.F., Zhou, D.F., Chen, D.C., Xiu, M.H., Wu, H.R., Haile, C.N., Kosten, T.A., Kosten, T.R., Brain-derived neurotrophic factor levels and its Val66Met gene polymorphism predict tardive dyskinesia treatment response to ginkgo biloba. Biol. Psychiatry 72:8 (2012), 700–706.