Markers of neuroinflammation and neuronal injury in bipolar disorder: Relation to prospective clinical outcomes

Brain, Behavior, and Immunity

Volumn 65, Issue , 2017, Pages 195-201

  Isgren, Anniella ^a   Sellgren, Carl ^b,c   Ekman, Carl Johan ^d   Holmén Larsson, Jessica ^a   Blennow, Kaj ^a,e   Zetterberg, Henrik ^a,e,f   Jakobsson, Joel ^a   Landén, Mikael ^a,d  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

^e SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Bipolar disorder; Cerebrospinal fluid; Cytokines; Disease progression; Microglia; Neuroinflammation

Indexed keywords

BIOLOGICAL MARKER; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; NF L PROTEIN; UNCLASSIFIED DRUG; YKL 40 PROTEIN; CCL2 PROTEIN, HUMAN; CHI3L1 PROTEIN, HUMAN; CHITINASE 3 LIKE PROTEIN 1; CYTOKINE; IL8 PROTEIN, HUMAN; NEUROFILAMENT PROTEIN; NEUROFILAMENT PROTEIN L;

ADAPTIVE IMMUNITY; ADULT; ARTICLE; BIPOLAR DISORDER; BRAIN INJURY; CEREBROSPINAL FLUID; CLINICAL OUTCOME; CONTROLLED STUDY; DEPRESSION; DISEASE ASSOCIATION; FEMALE; FOLLOW UP; GLOBAL ASSESSMENT OF FUNCTIONING; HOSPITAL PATIENT; HUMAN; HUMAN TISSUE; HYPOMANIA; IMMUNOPATHOGENESIS; INCIDENCE; MAJOR CLINICAL STUDY; MALE; MANIA; MINI INTERNATIONAL NEUROPSYCHIATRIC INTERVIEW; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NEURONAL INJURY; PATIENT CARE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PSYCHOSIS; SUICIDE ATTEMPT; SURVIVAL RATE; BLOOD; IMMUNOLOGY; IMMUNOMODULATION; LONGITUDINAL STUDY; METABOLISM; MIDDLE AGED; PHYSIOLOGY; PROGNOSIS; TREATMENT OUTCOME;

ADULT; BIOMARKERS; BIPOLAR DISORDER; CHEMOKINE CCL2; CHITINASE-3-LIKE PROTEIN 1; CYTOKINES; FEMALE; HUMANS; INTERLEUKIN-8; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; NEUROFILAMENT PROTEINS; NEUROIMMUNOMODULATION; NEURONS; PROGNOSIS; PROSPECTIVE STUDIES; PSYCHOTIC DISORDERS; TREATMENT OUTCOME;

EID: 85019130221     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2017.05.002     Document Type: Article

References (45)

1. Andersson, M., Alvarez-Cermeno, J., Bernardi, G., Cogato, I., Fredman, P., Frederiksen, J., Fredrikson, S., Gallo, P., Grimaldi, L.M., Gronning, M., et al. Cerebrospinal fluid in the diagnosis of multiple sclerosis: a consensus report. J. Neurol. Neurosurg. Psychiatry 57:8 (1994), 897–902.
2. Barbosa, I.G., Bauer, M.E., Machado-Vieira, R., Teixeira, A.L., Cytokines in bipolar disorder: paving the way for neuroprogression. Neural Plast., 2014, 2014, 360481.
3. Becking, K., Boschloo, L., Vogelzangs, N., Haarman, B.C., Riemersma-van der Lek, R., Penninx, B.W., Schoevers, R.A., The association between immune activation and manic symptoms in patients with a depressive disorder. Transl. Psychiatry, 3, 2013, e314.
4. Belmaker, R.H., Bipolar disorder. N. Engl. J. Med. 351:5 (2004), 476–486.
5. Benedetti, F., Poletti, S., Hoogenboezem, T.A., Mazza, E., Ambree, O., de Wit, H., Wijkhuijs, A.J., Locatelli, C., Bollettini, I., Colombo, C., Arolt, V., Drexhage, H.A., Inflammatory cytokines influence measures of white matter integrity in Bipolar Disorder. J. Affect Disord. 202 (2016), 1–9.
6. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57 (1995), 289–300.
7. Beumer, W., Gibney, S.M., Drexhage, R.C., Pont-Lezica, L., Doorduin, J., Klein, H.C., Steiner, J., Connor, T.J., Harkin, A., Versnel, M.A., Drexhage, H.A., The immune theory of psychiatric diseases: a key role for activated microglia and circulating monocytes. J. Leukoc. Biol. 92:5 (2012), 959–975.
8. Bhattacharya, A., Derecki, N.C., Lovenberg, T.W., Drevets, W.C., Role of neuro-immunological factors in the pathophysiology of mood disorders. Psychopharmacology (Berl) 233:9 (2016), 1623–1636.
9. Bond, D.J., Andreazza, A.C., Hughes, J., Dhanoa, T., Torres, I.J., Kozicky, J.M., Young, L.T., Lam, R.W., Yatham, L.N., Association of peripheral inflammation with body mass index and depressive relapse in bipolar disorder. Psychoneuroendocrinology 65 (2016), 76–83.
10. Bonneh-Barkay, D., Bissel, S.J., Wang, G., Fish, K.N., Nicholl, G.C., Darko, S.W., Medina-Flores, R., Murphey-Corb, M., Rajakumar, P.A., Nyaundi, J., Mellors, J.W., Bowser, R., Wiley, C.A., YKL-40, a marker of simian immunodeficiency virus encephalitis, modulates the biological activity of basic fibroblast growth factor. Am. J. Pathol. 173:1 (2008), 130–143.
11. Bonneh-Barkay, D., Bissel, S.J., Kofler, J., Starkey, A., Wang, G., Wiley, C.A., Astrocyte and macrophage regulation of YKL-40 expression and cellular response in neuroinflammation. Brain Pathol. 22:4 (2012), 530–546.
12. Bose, S., Cho, J., Role of chemokine CCL2 and its receptor CCR2 in neurodegenerative diseases. Arch. Pharm. Res. 36:9 (2013), 1039–1050.
13. Bromander, S., Anckarsater, R., Kristiansson, M., Blennow, K., Zetterberg, H., Anckarsater, H., Wass, C.E., Changes in serum and cerebrospinal fluid cytokines in response to non-neurological surgery: an observational study. J. Neuroinflamm., 9(1), 2012, 242.
14. Cekanaviciute, E., Buckwalter, M.S., Astrocytes: integrative regulators of neuroinflammation in stroke and other neurological diseases. Neurotherapeutics 13:4 (2016), 685–701.
15. Colombo, E., Farina, C., Astrocytes: key regulators of neuroinflammation. Trends Immunol. 37:9 (2016), 608–620.
16. Estes, M.L., McAllister, A.K., Alterations in immune cells and mediators in the brain: it's not always neuroinflammation!. Brain Pathol. 24:6 (2014), 623–630.
17. Haarman, B.C., Riemersma-Van der Lek, R.F., Burger, H., Netkova, M., Drexhage, R.C., Bootsman, F., Mesman, E., Hillegers, M.H., Spijker, A.T., Hoencamp, E., Drexhage, H.A., Nolen, W.A., Relationship between clinical features and inflammation-related monocyte gene expression in bipolar disorder – towards a better understanding of psychoimmunological interactions. Bipolar Disord. 16:2 (2014), 137–150.
18. Haarman, B.C., Burger, H., Doorduin, J., Renken, R.J., Sibeijn-Kuiper, A.J., Marsman, J.B., de Vries, E.F., de Groot, J.C., Drexhage, H.A., Mendes, R., Nolen, W.A., Riemersma-Van der Lek, R.F., Volume, metabolites and neuroinflammation of the hippocampus in bipolar disorder – a combined magnetic resonance imaging and positron emission tomography study. Brain Behav. Immun. 56 (2016), 21–33.
19. Haroon, E., Raison, C.L., Miller, A.H., Psychoneuroimmunology meets neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology 37:1 (2012), 137–162.
20. Isgren, A., Jakobsson, J., Palsson, E., Ekman, C.J., Johansson, A.G., Sellgren, C., Blennow, K., Zetterberg, H., Landen, M., Increased cerebrospinal fluid interleukin-8 in bipolar disorder patients associated with lithium and antipsychotic treatment. Brain Behav. Immun. 43 (2015), 198–204.
21. Jakobsson, J., Bjerke, M., Ekman, C.J., Sellgren, C., Johansson, A.G., Zetterberg, H., Blennow, K., Landen, M., Elevated concentrations of neurofilament light chain in the cerebrospinal fluid of bipolar disorder patients. Neuropsychopharmacology 39:10 (2014), 2349–2356.
22. Jakobsson, J., Bjerke, M., Sahebi, S., Isgren, A., Ekman, C.J., Sellgren, C., Olsson, B., Zetterberg, H., Blennow, K., Palsson, E., Landen, M., Monocyte and microglial activation in patients with mood-stabilized bipolar disorder. J. Psychiatry Neurosci. 40:4 (2015), 250–258.
23. Janelidze, S., Ventorp, F., Erhardt, S., Hansson, O., Minthon, L., Flax, J., Samuelsson, M., Traskman-Bendz, L., Brundin, L., Altered chemokine levels in the cerebrospinal fluid and plasma of suicide attempters. Psychoneuroendocrinology 38:6 (2013), 853–862.
24. Janelidze, S., Suchankova, P., Ekman, A., Erhardt, S., Sellgren, C., Samuelsson, M., Westrin, A., Minthon, L., Hansson, O., Traskman-Bendz, L., Brundin, L., Low IL-8 is associated with anxiety in suicidal patients: genetic variation and decreased protein levels. Acta Psychiatr. Scand. 131:4 (2015), 269–278.
25. Junker, N., Johansen, J.S., Hansen, L.T., Lund, E.L., Kristjansen, P.E., Regulation of YKL-40 expression during genotoxic or microenvironmental stress in human glioblastoma cells. Cancer Sci. 96:3 (2005), 183–190.
26. Karanti, A., Bobeck, C., Osterman, M., Kardell, M., Tidemalm, D., Runeson, B., Lichtenstein, P., Landen, M., Gender differences in the treatment of patients with bipolar disorder: a study of 7354 patients. J. Affect. Disord. 174 (2015), 303–309.
27. Kraneveld, A.D., de Theije, C.G., van Heesch, F., Borre, Y., de Kivit, S., Olivier, B., Korte, M., Garssen, J., The neuro-immune axis: prospect for novel treatments for mental disorders. Basic Clin. Pharmacol. Toxicol. 114:1 (2014), 128–136.
28. Leckman, J.F., Sholomskas, D., Thompson, W.D., Belanger, A., Weissman, M.M., Best estimate of lifetime psychiatric diagnosis: a methodological study. Arch Gen. Psychiatry 39:8 (1982), 879–883.
29. Maier, B., Laurer, H.L., Rose, S., Buurman, W.A., Marzi, I., Physiological levels of pro- and anti-inflammatory mediators in cerebrospinal fluid and plasma: a normative study. J. Neurotrauma 22:7 (2005), 822–835.
30. McAfoose, J., Baune, B.T., Evidence for a cytokine model of cognitive function. Neurosci. Biobehav. Rev. 33:3 (2009), 355–366.
31. Mesman, E., Hillegers, M.H., Ambree, O., Arolt, V., Nolen, W.A., Drexhage, H.A., Monocyte activation, brain-derived neurotrophic factor (BDNF), and S100B in bipolar offspring: a follow-up study from adolescence into adulthood. Bipolar Disord. 17:1 (2015), 39–49.
32. Munkholm, K., Vinberg, M., Vedel Kessing, L., Cytokines in bipolar disorder: a systematic review and meta-analysis. J. Affect. Disord. 144:1–2 (2013), 16–27.
33. Nakagawa, Y., Chiba, K., Diversity and plasticity of microglial cells in psychiatric and neurological disorders. Pharmacol. Ther. 154 (2015), 21–35.
34. O'Callaghan, J.P., Sriram, K., Miller, D.B., Defining “neuroinflammation”. Ann. N.Y. Acad. Sci. 1139 (2008), 318–330.
35. Pae, C.U., The potential role of monocyte chemoattractant protein-1 for major depressive disorder. Psychiatry Investig. 11:3 (2014), 217–222.
36. Rolstad, S., Jakobsson, J., Sellgren, C., Ekman, C.J., Blennow, K., Zetterberg, H., Palsson, E., Landen, M., Cognitive performance and cerebrospinal fluid biomarkers of neurodegeneration: a study of patients with bipolar disorder and healthy controls. PLoS One, 10(5), 2015, e0127100.
37. Rolstad, S., Jakobsson, J., Sellgren, C., Isgren, A., Ekman, C.J., Bjerke, M., Blennow, K., Zetterberg, H., Palsson, E., Landen, M., CSF neuroinflammatory biomarkers in bipolar disorder are associated with cognitive impairment. Eur. Neuropsychopharmacol. 25:8 (2015), 1091–1098.
38. Rosenblat, J.D., Cha, D.S., Mansur, R.B., McIntyre, R.S., Inflamed moods: a review of the interactions between inflammation and mood disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry 53 (2014), 23–34.
39. Roy, M.A., Lanctot, G., Merette, C., Cliche, D., Fournier, J.P., Boutin, P., Rodrigue, C., Charron, L., Turgeon, M., Hamel, M., Montgrain, N., Nicole, L., Pires, A., Wallot, H., Ponton, A.M., Garneau, Y., Dion, C., Lavallee, J.C., Potvin, A., Szatmari, P., Maziade, M., Clinical and methodological factors related to reliability of the best-estimate diagnostic procedure. Am. J. Psychiatry 154:12 (1997), 1726–1733.
40. Ryden, E., Thase, M.E., Straht, D., Aberg-Wistedt, A., Bejerot, S., Landen, M., A history of childhood attention-deficit hyperactivity disorder (ADHD) impacts clinical outcome in adult bipolar patients regardless of current ADHD. Acta Psychiatry Scand. 120:3 (2009), 239–246.
41. Sachs, G.S., Thase, M.E., Otto, M.W., Bauer, M., Miklowitz, D., Wisniewski, S.R., Lavori, P., Lebowitz, B., Rudorfer, M., Frank, E., Nierenberg, A.A., Fava, M., Bowden, C., Ketter, T., Marangell, L., Calabrese, J., Kupfer, D., Rosenbaum, J.F., Rationale, design, and methods of the systematic treatment enhancement program for bipolar disorder (STEP-BD). Biol. Psychiatry 53:11 (2003), 1028–1042.
42. SDM-ProjectWeb, 2010. “Neuroimaging software library including meta-analytic methods for fMRI, VBM, DTI and PET and other tools.” 2016, from http://www.sdmproject.com/utilities/?show=FDR.
43. Sellgren, C.M., Kegel, M.E., Bergen, S.E., Ekman, C.J., Olsson, S., Larsson, M., Vawter, M.P., Backlund, L., Sullivan, P.F., Sklar, P., Smoller, J.W., Magnusson, P.K., Hultman, C.M., Walther-Jallow, L., Svensson, C.I., Lichtenstein, P., Schalling, M., Engberg, G., Erhardt, S., Landen, M., A genome-wide association study of kynurenic acid in cerebrospinal fluid: implications for psychosis and cognitive impairment in bipolar disorder. Mol. Psychiatry, 2015.
44. Semple, B.D., Kossmann, T., Morganti-Kossmann, M.C., Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J. Cereb. Blood Flow Metab. 30:3 (2010), 459–473.
45. Sheehan, D.V., Lecrubier, Y., Sheehan, K.H., Amorim, P., Janavs, J., Weiller, E., Hergueta, T., Baker, R., Dunbar, G.C., The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J. Clin. Psychiatry 59:Suppl. 20 (1998), 22–33 quiz 34-57.