Association between serum brain-derived neurotrophic factor and plasma interleukin-6 in major depressive disorder with melancholic features

Brain, Behavior, and Immunity

Volumn 36, Issue , 2014, Pages 71-79

  Patas, Konstantinos ^a,f   Penninx, Brenda W J H ^b   Bus, Boudewijn A A ^c   Vogelzangs, Nicole ^b   Molendijk, Marc L ^d,e   Elzinga, Bernet M ^d,e   Bosker, Fokko J ^a   Oude Voshaar, Richard C ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d LEIDEN UNIVERSITY   (Netherlands)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Brain derived neurotrophic factor; Depression; Inflammation; Interleukin 6; Melancholic

Indexed keywords

ANTIINFLAMMATORY AGENT; ANTIPYRETIC ANALGESIC AGENT; BRAIN DERIVED NEUROTROPHIC FACTOR; HYPERICUM PERFORATUM EXTRACT; INTERLEUKIN 6; SEROTONIN NORADRENALIN REUPTAKE INHIBITOR; SEROTONIN UPTAKE INHIBITOR; TETRACYCLIC ANTIDEPRESSANT AGENT; TRICYCLIC ANTIDEPRESSANT AGENT; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; AGITATION; ALCOHOL CONSUMPTION; ANOREXIA; ANXIETY DISORDER; ARTICLE; BLOOD SAMPLING; BODY HEIGHT; BODY MASS; BODY WEIGHT; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIAGNOSIS RELATED GROUP; DISEASE ASSOCIATION; DISEASE DURATION; DSM-IV; EXPLORATORY RESEARCH; FEMALE; HUMAN; LEUKOCYTE COUNT; LIFESTYLE; MAJOR CLINICAL STUDY; MAJOR DEPRESSION; MALE; MELANCHOLIA; MIDDLE AGED; NETHERLANDS; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PSYCHOMOTOR RETARDATION; SMOKING; WEIGHT REDUCTION; YOUNG ADULT;

BRAIN-DERIVED NEUROTROPHIC FACTOR; DEPRESSION; INFLAMMATION; INTERLEUKIN-6; MELANCHOLIC;

ADULT; BRAIN-DERIVED NEUROTROPHIC FACTOR; DEPRESSIVE DISORDER, MAJOR; FEMALE; HUMANS; INTERLEUKIN-6; MALE; MIDDLE AGED; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84891836330     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2013.10.007     Document Type: Article

References (72)

1. Audet M.C., Anisman H. Interplay between pro-inflammatory cytokines and growth factors in depressive illnesses. Front. Cell. Neurosci. 2013, 7:68.
2. Baune B.T., Konrad C., Grotegerd D., Suslow T., Birosova E., Ohrmann P., et al. Interleukin-6 gene (IL-6): a possible role in brain morphology in the healthy adult brain. J. Neuroinflamm. 2012, 9:125.
3. Besser M., Wank R. Cutting edge: clonally restricted production of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3 mRNA by human immune cells and Th1/Th2-polarized expression of their receptors. J. Immunol. 1999, 162(11):6303-6306.
4. Bocchio-Chiavetto L., Bagnardi V., Zanardini R., Molteni R., Nielsen M.G., Placentino A., et al. Serum and plasma BDNF levels in major depression: a replication study and meta-analyses. World J. Biol. Psychiatry 2010, 11(6):763-773.
5. Bus, B.A., Molendijk, M.L., Penninx, B.J., Buitelaar, J.K., Prickaerts, J., Elzinga, B.M., Oude Voshaar, R.C. (accepted for publication). Low serum BDNF levels in depressed patients cannot be attributed to individual depressive symptoms or symptom cluster. World J Biol Psychiatry.
6. Bus B.A., Molendijk M.L., Penninx B.J., Buitelaar J.K., Kenis G., Prickaerts J., et al. Determinants of serum brain-derived neurotrophic factor. Psychoneuroendocrinology 2011, 36(2):228-239.
7. Castren E., Rantamaki T. The role of BDNF and its receptors in depression and antidepressant drug action: Reactivation of developmental plasticity. Dev. Neurobiol. 2010, 70(5):289-297.
8. Cattaneo A., Bocchio-Chiavetto L., Zanardini R., Milanesi E., Placentino A., Gennarelli M. Reduced peripheral brain-derived neurotrophic factor mRNA levels are normalized by antidepressant treatment. Int. J. Neuropsychopharmacol. 2010, 13(1):103-108.
9. Cattaneo A., Gennarelli M., Uher R., Breen G., Farmer A., Aitchison K.J., et al. Candidate genes expression profile associated with antidepressants response in the GENDEP study: differentiating between baseline 'predictors' and longitudinal 'targets'. Neuropsychopharmacology 2013, 38(3):377-385.
10. Chaldakov G. The metabotrophic NGF and BDNF: an emerging concept. Arch. Ital. Biol. 2011, 149(2):257-263.
11. Chen G.Y., Nunez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 2010, 10(12):826-837.
12. Craig C.L., Marshall A.L., Sjostrom M., Bauman A.E., Booth M.L., Ainsworth B.E., et al. International physical activity questionnaire: 12-country reliability and validity. Med. Sci. Sports Exerc. 2003, 35(8):1381-1395.
13. Day C.V., Williams L.M. Finding a biosignature for melancholic depression. Expert Rev. Neurother. 2012, 12(7):835-847.
14. Dienz O., Rincon M. The effects of IL-6 on CD4 T cell responses. Clin. Immunol. 2009, 130(1):27-33.
15. Dowlati Y., Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., et al. A meta-analysis of cytokines in major depression. Biol. Psychiatry 2010, 67(5):446-457.
16. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 2006, 59(12):1116-1127.
17. Dunjic-Kostic B., Ivkovic M., Radonjic N.V., Petronijevic N.D., Pantovic M., Damjanovic A., et al. Melancholic and atypical major depression-connection between cytokines, psychopathology and treatment. Prog. Neuropsychopharmacol. Biol. Psychiatry 2013, 43:1-6.
18. Erdem M., Celik C., Cayci T., Ozdemir B., Kurt Y.G., Akgul E.O., et al. Serum haptoglobin levels in patients with melancholic and nonmelancholic major depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2011, 35(4):944-947.
19. Eyre H., Baune B.T. Neuroplastic changes in depression: a role for the immune system. Psychoneuroendocrinology 2012, 37(9):1397-1416.
20. Fauchais A.L., Lalloue F., Lise M.C., Boumediene A., Preud'homme J.L., Vidal E., et al. Role of endogenous brain-derived neurotrophic factor and sortilin in B cell survival. J. Immunol. 2008, 181(5):3027-3038.
21. Goldstein B.I., Collinger K.A., Lotrich F., Marsland A.L., Gill M.K., Axelson D.A., et al. Preliminary findings regarding proinflammatory markers and brain-derived neurotrophic factor among adolescents with bipolar spectrum disorders. J. Child Adolesc. Psychopharmacol. 2011, 21(5):479-484.
22. Hannestad J., DellaGioia N., Bloch M. The effect of antidepressant medication treatment on serum levels of inflammatory cytokines: a meta-analysis. Neuropsychopharmacology 2011, 36(12):2452-2459.
23. Howren M.B., Lamkin D.M., Suls J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med. 2009, 71(2):171-186.
24. Huang G.J., Smith A.L., Gray D.H., Cosgrove C., Singer B.H., Edwards A., et al. A genetic and functional relationship between T cells and cellular proliferation in the adult hippocampus. PLoS Biol. 2010, 8(12):e1000561.
25. Kauer-Sant'Anna M., Kapczinski F., Andreazza A.C., Bond D.J., Lam R.W., Young L.T., et al. Brain-derived neurotrophic factor and inflammatory markers in patients with early- vs. late-stage bipolar disorder. Int. J. Neuropsychopharmacol. 2009, 12(4):447-458.
26. Kerschensteiner M., Gallmeier E., Behrens L., Leal V.V., Misgeld T., Klinkert W.E., et al. Activated human T cells, B cells, and monocytes produce brain-derived neurotrophic factor in vitro and in inflammatory brain lesions: a neuroprotective role of inflammation?. J. Exp. Med. 1999, 189(5):865-870.
27. Khan A.Y., Carrithers J., Preskorn S.H., Lear R., Wisniewski S.R., John Rush A. Clinical and demographic factors associated with DSM-IV melancholic depression. Ann. Clin. Psychiatry 2006, 18(2):91-98.
28. Kotan Z., Sarandol E., Kirhan E., Ozkaya G., Kirli S. Serum brain-derived neurotrophic factor, vascular endothelial growth factor and leptin levels in patients with a diagnosis of severe major depressive disorder with melancholic features. Therapeutic Adv. Psychopharmacol. 2012, 2(2):65-74.
29. Kriegsman D.M., Penninx B.W., van Eijk J.T., Boeke A.J., Deeg D.J. Self-reports and general practitioner information on the presence of chronic diseases in community dwelling elderly. A study on the accuracy of patients' self-reports and on determinants of inaccuracy. J. Clin. Epidemiol. 1996, 49(12):1407-1417.
30. Lamers F., Vogelzangs N., Merikangas K.R., de Jonge P., Beekman A.T., Penninx B.W. Evidence for a differential role of HPA-axis function, inflammation and metabolic syndrome in melancholic versus atypical depression. Mol. Psychiatry 2013, 18(6):692-699.
31. Lang U.E., Hellweg R., Seifert F., Schubert F., Gallinat J. Correlation between serum brain-derived neurotrophic factor level and an in vivo marker of cortical integrity. Biol. Psychiatry 2007, 62(5):530-535.
32. Lanz T.A., Bove S.E., Pilsmaker C.D., Mariga A., Drummond E.M., Cadelina G.W., et al. Robust changes in expression of brain-derived neurotrophic factor (BDNF) mRNA and protein across the brain do not translate to detectable changes in BDNF levels in CSF or plasma. Biomarkers 2012, 17(6):524-531.
33. Linker R.A., Lee D.H., Demir S., Wiese S., Kruse N., Siglienti I., et al. Functional role of brain-derived neurotrophic factor in neuroprotective autoimmunity: therapeutic implications in a model of multiple sclerosis. Brain 2010, 133(Pt 8):2248-2263.
34. Liu Y., Ho R.C., Mak A. Interleukin (IL)-6, tumour necrosis factor alpha (TNF-alpha) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: a meta-analysis and meta-regression. J. Affect. Disord. 2012, 139(3):230-239.
35. Maes M., Stevens W., DeClerck L., Bridts C., Peeters D., Schotte C., et al. Immune disorders in depression: higher T helper/T suppressor-cytotoxic cell ratio. Acta Psychiatr. Scand. 1992, 86(6):423-431.
36. Maes M., Stevens W.J., DeClerck L.S., Bridts C.H., Peeters D., Schotte C., et al. A significantly increased number and percentage of B cells in depressed subjects: results of flow cytometric measurements. J. Affect. Disord. 1992, 24(3):127-134.
37. Maes M., Scharpe S., Meltzer H.Y., Bosmans E., Suy E., Calabrese J., et al. Relationships between interleukin-6 activity, acute phase proteins, and function of the hypothalamic-pituitary-adrenal axis in severe depression. Psychiatry Res. 1993, 49(1):11-27.
38. Maes M., Mihaylova I., Kubera M., Ringel K. Activation of cell-mediated immunity in depression: association with inflammation, melancholia, clinical staging and the fatigue and somatic symptom cluster of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2012, 36(1):169-175.
39. Maes M., Ringel K., Kubera M., Berk M., Rybakowski J. Increased autoimmune activity against 5-HT: a key component of depression that is associated with inflammation and activation of cell-mediated immunity, and with severity and staging of depression. J. Affect. Disord. 2012, 136(3):386-392.
40. Medzhitov R. Origin and physiological roles of inflammation. Nature 2008, 454(7203):428-435.
41. Miller A.H., Maletic V., Raison C.L. Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol. Psychiatry 2009, 65(9):732-741.
42. Molendijk M.L., Bus B.A., Spinhoven P., Penninx B.W., Kenis G., Prickaerts J., et al. Serum levels of brain-derived neurotrophic factor in major depressive disorder: state-trait issues, clinical features and pharmacological treatment. Mol. Psychiatry 2011, 16(11):1088-1095.
43. Morganti-Kossmann M.C., Satgunaseelan L., Bye N., Kossmann T. Modulation of immune response by head injury. Injury 2007, 38(12):1392-1400.
44. Neumann H., Misgeld T., Matsumuro K., Wekerle H. Neurotrophins inhibit major histocompatibility class II inducibility of microglia: involvement of the p75 neurotrophin receptor. Proc. Nat. Acad. Sci. USA 1998, 95(10):5779-5784.
45. O'Brien S.M., Scully P., Fitzgerald P., Scott L.V., Dinan T.G. Plasma cytokine profiles in depressed patients who fail to respond to selective serotonin reuptake inhibitor therapy. J. Psychiatr. Res. 2007, 41(3-4):326-331.
46. Pan W., Banks W.A., Fasold M.B., Bluth J., Kastin A.J. Transport of brain-derived neurotrophic factor across the blood-brain barrier. Neuropharmacology 1998, 37(12):1553-1561.
47. Penninx B.W., Beekman A.T., Smit J.H., Zitman F.G., Nolen W.A., Spinhoven P., et al. The Netherlands Study of Depression and Anxiety (NESDA): rationale, objectives and methods. Int. J. Methods Psychiatry Res. 2008, 17(3):121-140.
48. Popovich P.G., Longbrake E.E. Can the immune system be harnessed to repair the CNS?. Nat. Rev. Neurosci. 2008, 9(6):481-493.
49. Quinn C.R., Dobson-Stone C., Outhred T., Harris A., Kemp A.H. The contribution of BDNF and 5-HTT polymorphisms and early life stress to the heterogeneity of major depressive disorder: a preliminary study. Aust. N. Z. J. Psychiatry 2012, 46(1):55-63.
50. Raison C.L., Miller A.H. Is depression an inflammatory disorder?. Curr. Psychiatry Rep. 2011, 13(6):467-475.
51. Raison C.L., Rutherford R.E., Woolwine B.J., Shuo C., Schettler P., Drake D.F., et al. A randomized controlled trial of the tumor necrosis factor antagonist infliximab for treatment-resistant depression: the role of baseline inflammatory biomarkers. JAMA psychiatry 2013, 70(1):31-41.
52. Rasmussen P., Brassard P., Adser H., Pedersen M.V., Leick L., Hart E., et al. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp. Physiol. 2009, 94(10):1062-1069.
53. Rothermundt M., Arolt V., Wiesmann M., Missler U., Peters M., Rudolf S., et al. S-100B is increased in melancholic but not in non-melancholic major depression. J. Affect. Disord. 2001, 66(1):89-93.
54. Rush A.J., Gullion C.M., Basco M.R., Jarrett R.B., Trivedi M.H. The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychol. Med. 1996, 26(3):477-486.
55. Scheller J., Chalaris A., Schmidt-Arras D., Rose-John S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim. Biophys. Acta 2011, 1813(5):878-888.
56. Schlatter J., Ortuno F., Cervera-Enguix S. Lymphocyte subsets and lymphokine production in patients with melancholic versus nonmelancholic depression. Psychiatry Res. 2004, 128(3):259-265.
57. Schmidt H.D., Duman R.S. Peripheral BDNF produces antidepressant-like effects in cellular and behavioral models. Neuropsychopharmacology 2010, 35(12):2378-2391.
58. Schuhmann B., Dietrich A., Sel S., Hahn C., Klingenspor M., Lommatzsch M., et al. A role for brain-derived neurotrophic factor in B cell development. J. Neuroimmunol. 2005, 163(1-2):15-23.
59. Schulte-Herbruggen 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. 2005, 160(1-2):204-209.
60. Sen S., Duman R., Sanacora G. Serum brain-derived neurotrophic factor, depression, and antidepressant medications: meta-analyses and implications. Biol. Psychiatry 2008, 64(6):527-532.
61. Seppala J., Vanhala M., Kautiainen H., Eriksson J., Kampman O., Mantyselka P., et al. Prevalence of metabolic syndrome in subjects with melancholic and non-melancholic depressive symptoms. A Finnish population-based study. J. Affect. Disord. 2012, 136(3):543-549.
62. Shechter R., Schwartz M. CNS sterile injury: just another wound healing?. Trends Mol. Med. 2013, 19(3):135-143.
63. Spooren A., Kolmus K., Laureys G., Clinckers R., De Keyser J., Haegeman G., et al. Interleukin-6, a mental cytokine. Brain Res. Rev. 2011, 67(1-2):157-183.
64. Tabakman R., Lecht S., Sephanova S., Arien-Zakay H., Lazarovici P. Interactions between the cells of the immune and nervous system: neurotrophins as neuroprotection mediators in CNS injury. Prog. Brain Res. 2004, 146:387-401.
65. van Reedt Dortland A.K., Giltay E.J., van Veen T., van Pelt J., Zitman F.G., Penninx B.W. Associations between serum lipids and major depressive disorder: results from the Netherlands Study of Depression and Anxiety (NESDA). J. Clin. Psychiatry 2010, 71(6):729-736.
66. Vogelzangs N., Duivis H.E., Beekman A.T., Kluft C., Neuteboom J., Hoogendijk W., et al. Association of depressive disorders, depression characteristics and antidepressant medication with inflammation. Translational psychiatry 2012, 2:e79.
67. Wager-Smith K., Markou A. Depression: a repair response to stress-induced neuronal microdamage that can grade into a chronic neuroinflammatory condition?. Neurosci. Biobehav. Rev. 2011, 35(3):742-764.
68. Warner-Schmidt J.L., Vanover K.E., Chen E.Y., Marshall J.J., Greengard P. Antidepressant effects of selective serotonin reuptake inhibitors (SSRIs) are attenuated by antiinflammatory drugs in mice and humans. Proc. Nat. Acad. Sci. USA 2011, 108(22):9262-9267.
69. Wittchen H.U., Robins L.N., Cottler L.B., Sartorius N., Burke J.D., Regier D. Cross-cultural feasibility, reliability and sources of variance of the Composite International Diagnostic Interview (CIDI). The Multicentre WHO/ADAMHA Field Trials. Br. J. Psychiatry 1991, 159(645-653):658.
70. Wolf S.A., Steiner B., Akpinarli A., Kammertoens T., Nassenstein C., Braun A., et al. CD4-positive T lymphocytes provide a neuroimmunological link in the control of adult hippocampal neurogenesis. J. Immunol. 2009, 182(7):3979-3984.
71. Wong M.L., Kling M.A., Munson P.J., Listwak S., Licinio J., Prolo P., et al. Pronounced and sustained central hypernoradrenergic function in major depression with melancholic features: relation to hypercortisolism and corticotropin-releasing hormone. Proc. Nat. Acad. Sci. USA 2000, 97(1):325-330.
72. Yoshimura R., Hori H., Ikenouchi-Sugita A., Umene-Nakano W., Ueda N., Nakamura J. Higher plasma interleukin-6 (IL-6) level is associated with SSRI- or SNRI-refractory depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33(4):722-726.