TNF-alpha inhibition prevents cognitive decline and maintains hippocampal BDNF levels in the unpredictable chronic mild stress rat model of depression

Behavioural Brain Research

Volumn 292, Issue , 2015, Pages 233-240

  Şahin, Tuğçe Demirtaş ^a   Karson, Ayşe ^a   Balci, Fuat ^b   Yazir, Yusufhan ^a   Bayramgürler, Dilek ^a   Utkan, Tijen ^a  

^a KOCAELI UNIVERSITY   (Turkey)

^b KOÇ UNIVERSITY   (Turkey)

Author keywords

BDNF; Chronic stress; Cognitive function; Hippocampus; TNF alpha

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; INFLIXIMAB; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CHRONIC DRUG ADMINISTRATION; CHRONIC STRESS; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; DOWN REGULATION; DRUG EFFECT; EMOTIONALITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; LATENT PERIOD; LOCOMOTION; MALE; MEMORY DISORDER; MENTAL DETERIORATION; MENTAL PERFORMANCE; MENTAL STRESS; MORRIS WATER MAZE TEST; NEUROPROTECTION; NONHUMAN; PASSIVE AVOIDANCE TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPATIAL MEMORY; UNPREDICTABLE CHRONIC MILD STRESS; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; CHRONIC DISEASE; COGNITION; DISEASE MODEL; DRUG EFFECTS; EMOTION; HIPPOCAMPUS; INFLAMMATION; METABOLISM; PHYSIOLOGICAL STRESS; WISTAR RAT;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CHRONIC DISEASE; COGNITION; COGNITION DISORDERS; DEPRESSION; DISEASE MODELS, ANIMAL; EMOTIONS; HIPPOCAMPUS; INFLAMMATION; INFLIXIMAB; MALE; MEMORY DISORDERS; RATS, WISTAR; STRESS, PHYSIOLOGICAL; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84934780297     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.05.062     Document Type: Article

References (61)

1. 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.
2. Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., Lanctôt K.L. A meta-analysis of cytokines in major depression. Biol. Psychiatry 2010, 67(5):446-457.
3. 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.
4. Hu T.M., Subeq Y.M., Yang F.L., Hsu B.G., Lin N.T., Lee R.P. The use of a selective serotonin reuptake inhibitor decreases heavy alcohol exposure-induced inflammatory response and tissue damage in rats. J. Psychopharmacol. 2013, 27(10):940-946.
5. Ohgi Y., Futamura T., Kikuchi T., Hashimoto K. Effects of antidepressants on alternations in serum cytokines and depressive-like behavior in mice after lipopolysaccharide administration. Pharmacol. Biochem. Behav. 2013, 103(4):853-859.
6. Müller N., Schwarz M.J., Dehning S., Douhe A., Cerovecki A., Goldstein-Müller B., et al. The cyclooxygenase-2 inhibitor celecoxib has therapeutic effects in major depression: results of a double-blind, randomized, placebo controlled, add-on pilot study to reboxetine. Mol. Psychiatry 2006, 11(7):680-684.
7. Karson A., Demirtaş T., Bayramgürler D., Balci F., Utkan T. Chronic administration of infliximab (TNF-α inhibitor) decreases depression and anxiety-like behavior in rat model of chronic mild stress. Basic Clin. Pharmacol. Toxicol. 2013, 112(5):335-340.
8. Bian Y., Pan Z., Hou Z., Huang C., Li W., Zhao B. Learning, memory, and glial cell changes following recovery from chronic unpredictable stress. Brain Res. Bull. 2012, 88(5):471-476.
9. Li S., Wang C., Wang W., Dong H., Hou P., Tang Y. Chronic mild stress impairs cognition in mice: from brain homeostasis to behavior. Life Sci. 2008, 82(17-18):934-942.
10. Liu D., Wang Z., Gao Z., Xie K., Zhang Q., Jiang H., et al. Effects of curcumin on learning and memory deficits, BDNF, and ERK protein expression in rats exposed to chronic unpredictable stress. Behav. Brain Res. 2014, 271:116-121.
11. Yirmiya R., Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav. Immun. 2011, 25(2):181-213.
12. Triantafillidis J.K., Papalois A.E., Parasi A., Anagnostakis E., Burnazos S., Gikas A., et al. Favorable response to subcutaneous administration of infliximab in rats with experimental colitis. World J. Gastroenterol. 2005, 11:6843-6847.
13. Güzel A., Günaydin M., Alaçam H., Murat N., Gacar A., Güvenç T. Infliximab attenuates activated charcoal and polyethylene glycol aspiration-induced lung injury in rats. Exp. Lung Res. 2012, 38(3):147-156.
14. Kumar B., Kuhad A., Chopra K. Neuropsychopharmacological effect of sesamol in unpredictable chronic mild stress model of depression: behavioral and biochemical evidences. Psychopharmacol. (Berl.) 2011, 214(4):819-828.
15. Yazir Y., Utkan T., Aricioglu F. Inhibition of neuronal nitric oxide synthase and soluble guanylate cyclase prevents depression-like behaviour in rats exposed to chronic unpredictable mild stress. Basic Clin. Pharmacol. Toxicol. 2012, 111(3):154-160.
16. Altman H.J., Stone W.S., Ogren S.O. Evidence for a possible functional interaction between serotonergic and cholinergic mechanisms in memory retrieval. Behav. Neural. Biol. 1987, 48(1):49-62.
17. Monleón S., Urquiza A., Carmen Arenas M., Vinader-Caerols C., Parra A. Chronic administration of fluoxetine impairs inhibitory avoidance in male but not female mice. Behav. Brain Res. 2002, 136(2):483-488.
18. Pothion S., Bizot J.C., Trovero F., Belzung C. Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav. Brain Res. 2004, 155(1):135-146.
19. Cachard-Chastel M., Devers S., Sicsic S., Langlois M., Lezoualc'h F., Gardier A.M., et al. Prucalopride and donepezil act synergistically to reverse scopolamine-induced memory deficit in C57Bl/6j mice. Behav. Brain Res. 2008, 187(2):455-461.
20. Austin M.P., Mitchell P., Goodwin G.M. Cognitive deficits in depression: possible implications for functional neuropathology. Br. J. Psychiatry 2001, 178:200-206.
21. Kang H., Zhao F., You L., Giorgetta C.D.V., Sarkhel S., Prakash R. Pseudo-dementia. A neuropsychological review. Ann. Indian Acad. Neurol. 2014, 17(2):147-154.
22. Peselow E.D., Corwin J., Fieve R.R., Rotrosen J., Cooper T.B. Disappearance of memory deficits in outpatient depressives responding to imipramine. J. Affect. Disord. 1991, 21(3):173-183.
23. Sheline Y.I., Wang P.W., Gado M.H., Csernansky J.G., Vannier M.W. Hippocampal atrophy in recurrent major depression. Proc. Natl. Acad. Sci. U. S. A. 1996, 93(9):3908-3913.
24. Kempermann G. Regulation of adult hippocampal neurogenesis-implications for novel theories of major depression. Bipolar. Disord. 2002, 4(1):17-33.
25. Conrad C.D. Chronic stress-induced hippocampal vulnerability: the glucocorticoid vulnerability hypothesis. Rev. Neurosci. 2008, 19(6):395-411.
26. Machado A., Herrera A.J., de Pablos R.M., Espinosa-Oliva A.M., Sarmiento M., Ayala A., et al. Chronic stress as a risk factor for Alzheimer's disease. Rev. Neurosci. 2014, 25(6):785-804.
27. Joëls M., Karst H., Alfarez D., Heine V.M., Qin Y., van Riel E., et al. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 2004, 7(4):221-231.
28. Willner P. Validity reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacol. (Berl.) 1997, 134(4):319-329.
29. Kallarackal A.J., Kvarta M.D., Cammarata E., Jaberi L., Cai X., Bailey A.M., et al. Chronic stress induces a selective decrease in AMPA receptor-mediated synaptic excitation at hippocampal temporoammonic-CA1 synapses. J. Neurosci. 2013, 33(40):15669-15674.
30. Bisaz R., Schachner M., Sandi C. Causal evidence for the involvement of the neural cell adhesion molecule, NCAM, in chronic stress-induced cognitive impairments. Hippocampus 2011, 21(1):56-71.
31. Borcel E., Pérez-Alvarez L., Herrero A.I., Brionne T., Varea E., Berezin V., et al. Chronic stress in adulthood followed by intermittent stress impairs spatial memory and the survival of newborn hippocampal s in aging animals: prevention by FGL, a peptide mimetic of neural adhesion molecule. Behav. Pharmacol. 2008, 19(1):41-49.
32. Liao M.J., Lin L.F., Zhou X., Zhou X.W., Xu X., Cheng X., et al. Daphnetin prevents chronic unpredictable stress-induced cognitive deficits. Fundam. Clin. Pharmacol. 2013, 27(5):510-516.
33. Gu H.F., Nie Y.X., Tong Q.Z., Tang Y.L., Zeng Y., Jing K.Q., et al. Epigallocatechin-3-gallate attenuates impairment of learning and memory in chronic unpredictable mild stress-treated rats by restoring hippocampal autophagic flux. PLoS One 2014, 9(11):e112683.
34. Rinwa P., Kumar A. Modulation of nitrergic signalling pathway by American ginseng attenuates chronic unpredictable stress-induced cognitive impairment, neuroinflammation, and biochemical alterations. Naunyn Schmiedebergs Arch. Pharmacol. 2014, 387(2):129-141.
35. Cammarota M., Bevilaqua L.R., Rossato J.I., Lima R.H., Medina J.H., Izquierdo I. Parallel memory processing by the CA1 region of the dorsal hippocampus and the basolateral amygdala. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(30):10279-10284.
36. Bonini J.S., Rodrigues L., Kerr D.S., Bevilaqua L.R., Cammarota M., Izquierdo I. AMPA/kainate and group-I metabotropic receptor antagonists infused into different brain areas impair memory formation of inhibitory avoidance in rats. Behav. Pharmacol. 2003, 14(2).
37. Farmer G.E., Thompson L.T. Learning-dependent plasticity of hippocampal CA1 pyramidal neuron postburst afterhyperpolarizations and increased excitability after inhibitory avoidance learning depend upon basolateral amygdala inputs. Hippocampus 2012, 22(8):1703-1719.
38. Henningsen K., Andreasen J.T., Bouzinova E.V., Jayatissa M.N., Jensen M.S., Redrobe J.P., et al. Cognitive deficits in the rat chronic mild stress model for depression: relation to anhedonic-like responses. Behav. Brain Res. 2009, 198(1):136-141.
39. Palumbo M.L., Zorrilla Zubilete M.A., Cremaschi G.A., Genaro A.M. Different effect of chronic stress on learning and memory in BALB/c and C57BL/6 inbred mice: involvement of hippocampal NO production and PKC activity. Stress 2009, 12(4):350-361.
40. Zhang Z.H., Wu L.N., Song J.G., Li W.Q. Correlations between cognitive impairment and brain-derived neurotrophic factor expression in the hippocampus of post-stroke depression rats. Mol. Med. Rep. 2012, 6(4):889-893.
41. Yazir Y., Utkan T., Gacar N., Aricioglu F. Resveratrol exerts anti-inflammatory and neuroprotective effects to prevent memory deficits in rats exposed to chronic unpredictable mild stress. Physiol. Behav. 2015, 138:297-304.
42. Kim H., Park H.J., Shim H.S., Han S.M., Hahm D.H., Lee H., et al. The effects of acupuncture (PC6) on chronic mild stress-induced memory loss. Neurosci. Lett. 2011, 488(3):225-228.
43. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol. Learn. Mem. 2002, 78(3):578-595.
44. Zhang Y., Gu F., Chen J., Dong W. Chronic antidepressant administration alleviates frontal and hippocampal BDNF deficits in CUMS rat. Brain Res. 2010, 1366:141-148.
45. Izquierdo I., Bevilaqua L.R., Rossato J.I., da Silva W.C., Bonini J., Medina J.H., et al. The molecular cascades of long-term potentiation underlie memory consolidation of one-trial avoidance in the CA1 region of the dorsal hippocampus, but not in the basolateral amygdala or the neocortex. Neurotoxic. Res. 2008, 14(2-3):273-294.
46. Beer Z., Chwiesko C., Sauvage M.M. Processing of spatial and non-spatial information reveals functional homogeneity along the dorso-ventral axis of CA3, but not CA1. Neurobiol. Learn. Mem. 2014, 111:56-64.
47. Song L., Che W., Min-Wei W., Murakami Y., Matsumoto K. Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacol. Biochem. Behav. 2006, 83(2):186-193.
48. Duman R.S. Pathophysiology of depression and innovative treatments: remodeling glutamatergic synaptic connections. Dialogues Clin. Neurosci. 2014, 16(1):11-27.
49. 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. Neurosci. Cell. 2014, 8:430.
50. Haase J., Brown E. Integrating the monoamine, neurotrophin and cytokine hypotheses of depression-a central role for the serotonin transporter?. Pharmacol. Ther. 2015, 147:1-11.
51. Belarbi K., Jopson T., Tweedie D., Arellano C., Luo W., Greig N.H., et al. TNF-α protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. J. Neuroinflamm. 2012, 9:23.
52. Manikowska K., Mikołajczyk M., Mikołajczak P.Ł., Bobkiewicz-Kozłowska T. The influence of mianserin on TNF-α, IL-6 and IL-10 serum levels in rats under chronic mild stress. Pharmacol. Rep. 2014, 66(1):22-27.
53. Bayramgürler D., Karson A., Ozer C., Utkan T. Effects of long-term etanercept treatment on anxiety- and depression-like neurobehaviors in rats. Physiol. Behav. 2013, 119:145-148.
54. Takeda S., Sato N., Morishita R. Systemic inflammation, blood-brain barrier vulnerability and cognitive/non-cognitive symptoms in Alzheimer disease: relevance to pathogenesis and therapy. Front Aging Neurosci. 2014, 6:171.
55. Takeda S., Sato N., Ikimura K., Nishino H., Rakugi H., Morishita R. Increased blood-brain barrier vulnerability to systemic inflammation in an Alzheimer disease mouse model. Neurobiol. Aging 2013, 34(8):2064-2070.
56. Swardfager W., Lanctôt K., Rothenburg L., Wong A., Cappell J., Herrmann N. A meta-analysis of cytokines in Alzheimer's disease. Biol. Psychiatry 2010, 68(10):930-941.
57. Baune B.T., Smith E., Reppermund S., Air T., Samaras K., Lux O., et al. Inflammatory biomarkers predict depressive, but not anxiety symptoms during aging: the prospective Sydney memory and aging study. Psychoneuroendocrinology 2012, 37(9):1521-1530.
58. Bermejo P., Martín-Aragón S., Benedí J., Susín C., Felici E., Gil P., et al. Differences of peripheral inflammatory markers between mild cognitive impairment and Alzheimer's disease. Immunol. Lett. 2008, 117(2):198-202.
59. Motta M., Imbesi R., Di Rosa M., Stivala F., Malaguarnera L. Altered plasma cytokine levels in Alzheimer's disease: correlation with the disease progression. Immunol. Lett. 2007, 114(1):46-51.
60. Kahn M.S., Kranjac D., Alonzo C.A., Haase J.H., Cedillos R.O., McLinden K.A., et al. Prolonged elevation in hippocampal Aβ and cognitive deficits following repeated endotoxin exposure in the mouse. Behav. Brain Res. 2012, 229(1):176-184.
61. Krstic D., Madhusudan A., Doehner J., Vogel P., Notter T., Imhof C., et al. Systemic immune challenges trigger and drive Alzheimer-like neuropathology in mice. J. Neuroinflamm. 2012, 9:151.