Ketamine modulates hippocampal neurogenesis and pro-inflammatory cytokines but not stressor induced neurochemical changes

Neuropharmacology

Volumn 112, Issue , 2017, Pages 210-220

  Clarke, Melanie ^a   Razmjou, Sara ^a   Prowse, Natalie ^a   Dwyer, Zach ^a   Litteljohn, Darcy ^a   Pentz, Rowan ^a   Anisman, Hymie ^a   Hayley, Shawn ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

Cytokine; Depression; Ketamine; LPS; Neurogenesis; Stressor

Indexed keywords

4 HYDROXY 3 METHOXYPHENYLETHYLENE GLYCOL; 5 HYDROXYINDOLEACETIC ACID; CORTICOSTERONE; CYTOKINE; DOUBLECORTIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; KETAMINE; LIPOPOLYSACCHARIDE; NORADRENALIN; SEROTONIN; SUCROSE; TUMOR NECROSIS FACTOR; ANTIDEPRESSANT AGENT; BIOGENIC AMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BREGMA; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DENTATE GYRUS; DEPRESSION; DOSE RESPONSE; DRUG EFFECT; EXPOSURE; FORCED SWIM TEST; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; STRESS; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; CHEMICALLY INDUCED; COMPLICATION; DRUG EFFECTS; ENCEPHALITIS; EXERCISE; ILLNESS BEHAVIOR; MENTAL STRESS; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIDEPRESSIVE AGENTS; BIOGENIC MONOAMINES; CORTICOSTERONE; CYTOKINES; ENCEPHALITIS; HIPPOCAMPUS; ILLNESS BEHAVIOR; INTERLEUKIN-1BETA; KETAMINE; LIPOPOLYSACCHARIDES; MALE; MICE; NEUROGENESIS; NOREPINEPHRINE; RECEPTORS, N-METHYL-D-ASPARTATE; RESTRAINT, PHYSICAL; SEROTONIN; STRESS, PSYCHOLOGICAL; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84975513979     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.04.021     Document Type: Article

References (61)

1. Akinfiresoye, L., Tizabi, Y., Antidepressant effects of AMPA and ketamine combination: role of hippocampal BDNF, synapsin, and mTOR. Psychopharmacol. (Berl.) 230:2 (2013), 291–298.
2. Anisman, H., Hayley, S., Inflammatory factors contribute to depression and its comorbid conditions. Sci. Signal, 5(244), 2012 2; pe45.
3. Berlim, M.T., Turecki, G., What is the meaning of treatment resistant/refractory major depression (TRD)? A systematic review of current randomized trials. Eur. Neuropsychoparmacol. 17:11 (2007), 696–707.
4. Berman, R.M., Cappiello, A., Anand, A., Oren, D.A., Heninger, G.R., Charney, D.S., Krystal, J.H., Antidepressant effects of ketamine in depressed patients. Biol. Psychiatry 47:4 (2000), 351–354.
5. Berton, O., Nestler, E.J., New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 7:2 (2006), 137–151.
6. Blier, P., Zigman, D., Blier, J., On the safety and benefits of repeated intravenous injections of ketamine for depression. Biol. Psychiatry 72:4 (2012), e11–e12.
7. Chang, Y., Lee, J.J., Hsieh, C.Y., Hsiao, G., Chou, D.S., Sheu, J.R., Inhibitory effects of ketamine on lipopolysaccharide-induced microglial activation. Mediat. Inflamm., 2009, 2009, 705379, 10.1155/2009/705379.
8. Dantzer, R., Kelley, K.W., Twenty years of research on cytokine-induced sickness behavior. Brain Behav. Immun. 21:2 (2007 Feb), 153–160.
9. Donahue, R.J., Muschamp, J.W., Russo, S.J., Nestler, E.J., Carlezon, W.A. Jr., Effects of striatal ΔFosB overexpression and ketamine on social defeat stress-induced anhedonia in mice. Biol. Psychiatry 76:7 (2014 Oct 1), 550–558.
10. Duman, R.S., Li, N., Liu, R., Duric, V., Aghajanian, G., Signaling pathways underlying the rapid antidepressant actions of ketamine. Neuropharmacology 62:1 (2012), 35–41.
11. Dwyer, J.M., Duman, R.S., Activation of mammalian target of rapamycin and synaptogenesis: role in the actions of rapid-acting antidepressants. Biol. Psychiatry 73:12 (2013 Jun 15), 1189–1198.
12. Fava, M., Kendler, K.S., Major depressive disorder. Neuron 28:2 (2000), 335–341.
13. Fuster-Matanzo, A., Llorens-Martín, M., de Barreda, E.G., Ávila, J., Hernández, F., Different susceptibility to neurodegeneration of dorsal and ventral hippocampal dentate gyrus: a study with transgenic mice overexpressing GSK3β. PLoS One, 6(11), 2011, e27262.
14. Garcia, L.S., Comim, C.M., Valvassori, S.S., Reus, G.Z., Andreazza, A.C., Stertz, L., Fries, G.R., Gavioli, E.C., Kapczinski, F., Quevedo, J., Chronic administration of ketamine elicits antidepressant-like effects in rats without affecting hippocampal brain-derived neurotrophic factor protein levels. Basic Clin. Pharmacol. Toxicol. 103:6 (2008), 502–506.
15. Garcia, L.S., Comim, C.M., Valvassori, S.S., Reus, G.Z., Stertz, L., Kapczinski, F., Gavioli, E.C., Quevedo, J., Ketamine treatment reverses behavioral and physiological alterations induced by chronic mild stress in rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 33:3 (2009), 450–455.
16. Ghaemi, S.N., Why antidepressants are not antidepressants: STEP-BD, STAR*D, and the return of neurotic depression. Bipolar Disord. 10:8 (2008), 957–968.
17. Gibb, J., Hayley, S., Gandhi, R., Poulter, M.O., Anisman, H., Synergistic and additive actions of a psychosocial stressor and endotoxin challenge: circulating and brain cytokines, plasma corticosterone and behavioral changes in mice. Brain Behav. Immun. 22:4 (2008), 573–589.
18. Gibb, J., Hayley, S., Poulter, M.O., Anisman, H., Effects of stressors and immune activating agents on peripheral and central cytokines in mouse strains that differ in stressor responsivity. Brain Behav. Immun. 25:3 (2011), 468–482.
19. Harro, J., Animal models of depression vulnerability. Curr. Top. Behav. Neurosci. 14 (2013), 29–54.
20. Hayley, S., Scharf, J., Anisman, H., Central administration of murine interferon-α induces depressive-like behavioral, brain cytokine and neurochemical alterations in mice: a mini-review and original experiments. Brain Behav. Immun. 31 (2013), 115–127.
21. Hayley, S., Lacosta, S., Merali, Z., van Rooijen, N., Anisman, H., Central monoamine and plasma corticosterone changes induced by a bacterial endotoxin: sensitization and cross-sensitization effects. Eur. J. Neurosci. 13:6 (2001 Mar), 1155–1165.
22. Irwin, S.A., Iglewicz, A., Oral ketamine for the rapid treatment of depression and anxiety in patients receiving hospice care. J. Palliat. Med. 13:7 (2010), 903–908.
23. Kiu, H., Nicholson, S.E., Biology and significance of the JAK/STAT signalling pathways. Growth Factors 30:2 (2012), 88–106.
24. Koo, J.W., Russo, S.J., Ferguson, D., Nestler, E.J., Duman, R.S., Nuclear factor-kappaB is a critical mediator of stress-impaired neurogenesis and depressive behavior. Proc. Natl. Acad. Sci. 107:6 (2010), 2669–2674.
25. Krystal, J.H., Ketamine and the potential role for rapid-acting antidepressant medications. Swiss Med. Wkly. 137:15–16 (2007), 215–216.
26. Lally, N., Nugent, A.C., Luckenbaugh, D.A., Niciu, M.J., Roiser, J.P., Zarate, C.A. Jr., Neural correlates of change in major depressive disorder anhedonia following open-label ketamine. J. Psychopharmacol. 29:5 (2015 May), 596–607.
27. Lally, N., Nugent, A.C., Luckenbaugh, D.A., Ameli, R., Roiser, J.P., Zarate, C.A., Anti-anhedonic effect of ketamine and its neural correlates in treatment-resistant bipolar depression. Transl. Psychiatry, 4, 2014 Oct 14, e469.
28. Li, N., Lee, B., Liu, R., Banasr, M., Dwyer, J.M., Iwata, M., Li, X.Y., Aghajanian, G., Duman, R.S., mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329:5994 (2010), 959–964.
29. Li, N., Liu, R., Dwyer, J.M., Banasr, M., Lee, B., Son, H., Li, X.Y., Aghajamian, G., Duman, R.S., Glutamate N-methyl-D-aspartate receptor antagonists rapidly reverse behavioral and synaptic deficits caused by chronic stress exposure. Biol. Psychiatry 69:8 (2011), 754–761.
30. Lichtblau, N., Schmidt, F.M., Schumann, R., Kirkby, K.C., Himmerich, H., Cytokines as biomarkers in depressive disorder: current standing and prospects. Int. Rev. Psychiatry 25:5 (2013), 592–603.
31. Liebrenz, M., Borgeat, A., Leisinger, R., Stohler, R., Intravenous ketamine therapy in a patient with a treatment-resistant major depression. Swiss Med. Wkly. 137:15–16 (2007), 234–236.
32. Liu, G., Rustom, N., Litteljohn, D., Bobyn, J., Rudyk, C., Anisman, H., Hayley, S., Use of induced pluripotent stem cell derived neurons engineered to express BDNF for modulation of stressor related pathology. Front. Cell Neurosci., 8, 2014, 316.
33. Ma, X.C., Dang, Y.H., Jia, M., Ma, R., Wang, F., Wu, J., Gao, C.G., Hashimoto, K., Long-lasting antidepressant action of ketamine, but not glycogen synthase kinase-3 inhibitor SB216763, in the chronic mild stress model of mice. PLoS One, 8(2), 2013, e56053.
34. Machado-Vieira, R., Yuan, P., Brutsche, N., DiazGranados, N., Luckenbaugh, D., Manji, H.K., Zarate, C.A. Jr., Brain-derived neurotrophic factor and initial antidepressant response to an N-methyl-D-aspartate antagonist. J. Clin. Psychiatry 70:12 (2009), 1662–1666.
35. Malberg, J.E., Eisch, A.J., Nestler, E.J., Duman, R.S., Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20:24 (2000), 9104–9110.
36. Mathew, S.J., Murrough, J.W., aan het Rot, M., Collins, K.A., Reich, D.L., Charney, D.S., Riluzole for the relapse prevention following intravenous ketamine in treatment-resistant depression: a pilot randomized, placebo-controlled continuation trial. Int. J. Neuropsychopharmacol. 13:1 (2010), 71–82.
37. Mauri, M.C., Ferrrara, A., Boscati, L., Bravin, S., Zamberlan, F., Alecci, M., Invernizzi, G., Plasma and platelet amino acid concentrations in patients affected by major depression and under fluvoxamine treatment. Neuropsychobiology 37:3 (1998), 124–129.
38. Mercurio, F., Manning, A.M., Multiple signals converging on NF-κB. Curr. Opin. Cell Biol. 11:2 (1999), 226–232.
39. Murrough, J.W., Ketamine as a novel antidepressant: from synapse to behavior. Clin. Pharmacol. Ther. 91:2 (2011), 303–309.
40. Osborn, M., Rustom, N., Clarke, M., Litteljohn, D., Rudyk, C., Anisman, H., Hayley, S., Antidepressant-like effects of erythropoietin: a focus on behavioural and hippocampal processes. PLoS One, 8(9), 2013, e72813.
41. Parise, E.M., Alcantara, L.F., Warrn, B.L., Wright, K.N., Hadad, R., Sial, O.K., Kroeck, K.G., Iniguez, S.D., Bolanos-Guzman, C.A., Repeated ketamine exposure induces an enduring resilient phenotype in adolescent and adult rats. Biol. Psychiatry 74:10 (2013), 750–759.
42. Parker, K.J., Schatzberg, A.F., Lyons, D.M., Neuroendocrine aspects of hypercortisolism in major depression. Horm. Behav. 43:1 (2003), 60–66.
43. Phelps, L.E., Brutsche, N., Moral, J.R., Luckenbaugh, D.A., Manji, H.K., Zarate, C.A. Jr., Family history of alcohol dependence and initial antidepressant response to an N-methyl-D-aspartate antagonist. Biol. Psychiatry 65:2 (2009), 181–184.
44. Prikhozhan, A.V., Kovalev, G.I., Raevskii, K.S., Effects of antidepressive agents on glutamatergic autoregulatory presynaptic mechanism in the rat cerebral cortex. Bull. Eksp. Biol. Med. 110:12 (1990), 624–626.
45. Rezin, G.T., Gonçalves, C.L., Daufenbach, J.F., Fraga, D.B., Santos, P.M., Ferreira, G.K., Hermani, F.V., Comim, C.M., Quevedo, J., Streck, E.L., Acute administration of ketamine reverses the inhibition of mitochondrial respiratory chain induced by chronic mild stress. Brain Res. Bull. 79:6 (2009 Aug 14), 418–421.
46. Ruhe, H.G., Mason, N.S., Schene, A.H., Mood is indirectly related to serotonin, norepinephrine and dopamine levels in humans: a meta-analysis of monoamine depletion studies. Mol. Psychiatry 12:4 (2007), 331–359.
47. Rush, A.J., Trivedi, M.H., Wisniewski, S.R., Nierenberg, A.A., Stewart, J.W., Warden, D., Niederehe, G., Thase, M.E., Lavori, P.W., Lebowitz, B.D., McGrath, P.J., Rosenbaum, J.F., Sackeim, H.A., Kupfer, D.J., Luther, J., Fava, M., Acute and longer-term outcomes in depressed outpatients requiring one or several treatment steps: a STAR*D report. Am. J. Psychiatry 163:11 (2006), 1905–1917.
48. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C., Hen, R., Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:5634 (2003), 805–809.
49. Seguin, J.A., Brennan, J., Mangano, E., Hayley, S., Proinflammatory cytokines differentially influence adult hippocampal cell proliferation depending upon the route and chronicity of administration. Neuropsychiatr. Dis. Treat. 5 (2009), 5–14.
50. Soumier, A., Carter, R.M., Schoenfeld, T.J., Cameron, H.A., New hippocampal neurons mature rapidly in response to ketamine but are not required for its acute antidepressant effects on neophagia in rats. eNeuro, 3(2), 2016 Mar 31.
51. Sperner-Unterweger, B., Kohl, C., Fuchs, D., Immune changes and neurotransmitters: possible interactions in depression?. Prog. Neuropsychopharmacol. Biol. Psychiatry 48 (2014 Jan 3), 268–276.
52. Surget, A., Saxe, M., Leman, S., Ibarguen-Vargas, Y., Chalon, S., Griebel, G., Hen, R., Belzung, Z., Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol. Psychiatry 64:4 (2008), 293–301.
53. Thase, M.E., Haight, B.R., Richard, N., Rockett, C.B., Mitton, M., Modell, J.G., VanMeter, S., Harriett, A.E., Wang, Y., Remission rates following antidepressant therapy with bupropion or selective serotonin reuptake inhibitors: a meta-analysis of original data from 7 randomized controlled trials. J. Clin. Psychiatry 66:8 (2005), 974–981.
54. Trivedi, M.H., Rush, A.J., Wisniewski, S.R., Nierenberg, A.A., Warden, D., Ritz, L., Norquist, G., Howland, R.H., Lebowitz, B., McGrath, P.J., Shores-Wilson, K., Biggs, M.M., Balasubramani, G.K., Fava, M., Evaluation of outcomes with citalopram for depression using measurement-based care in STAR*D: implications for clinical practice. Am. J. Psychiatry 163:1 (2006), 28–40.
55. Van Bokhoven, P., Oomen, C.A., Hoogendijk, W.J., Smit, A.B., Lucassen, P.J., Spijker, S., Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment. Eur. J. Neurosci. 33:10 (2011), 1833–1840.
56. Walker, A.K., Budac, D.P., Bisulco, S., Lee, A.W., Smith, R.A., Beenders, B., Kelley, K.W., Dantzer, R., NMDA receptor blockade by ketamine abrogates lipopolysaccharide-induced depressive-like behavior in C57BL/6J mice. Neuropsychopharmacology 38:9 (2013), 1609–1616.
57. Ward, J.L., Harting, M.T., Cox, C.S. Jr., Mercer, D.W., Effects of ketamine on endotoxin and traumatic brain injury induced cytokine production in the rat. J. Trauma 70:6 (2011), 1471–1479.
58. Wesseling, H., Rahmoune, H., Tricklebank, M., Guest, P.C., Bahn, S., A targeted multiplexed proteomic investigation identifies ketamine-induced changes in immune markers in rat serum and expression changes in protein kinases/phosphatases in rat brain. J. Proteome Res. 14:1 (2015), 411–421.
59. Yang, J.J., Wang, N., Yang, C., Shi, J.Y., Yu, H.Y., Hashimoto, K., Serum interleukin-6 is a predictive biomarker for ketamine's antidepressant effect in treatment-resistant patients with major depression. Biol. Psychiatry 77:3 (2015), e19–20.
60. Zarate, C.A. Jr., Singh, J.B., Carlson, P.J., Brutsche, N.E., Ameli, R., Luckenbaugh, D.A., Charney, D.S., Manji, H.K., A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch. Gen. Psychiatry 63:8 (2006), 856–864.
61. Zhou, W., Wang, N., Yang, C., Li, X.M., Zhou, Z.Q., Yang, J.J., Ketamine-induced antidepressant effects are associated with AMPA receptors-mediated upregulation of mTOR and BDNF in rat hippocampus and prefrontal cortex. Eur. Psychiatry 29:7 (2014), 419–423.