Imipramine reverses alterations in cytokines and BDNF levels induced by maternal deprivation in adult rats

Behavioural Brain Research

Volumn 242, Issue 1, 2013, Pages 40-46

  Réus, Gislaine Z ^a   dos Santos, Maria Augusta B ^a   Abelaira, Helena M ^a   Ribeiro, Karine F ^a   Petronilho, Fabrícia ^c   Vuolo, Francieli ^a   Colpo, Gabriela D ^b   Pfaffenseller, Bianca ^b   Kapczinski, Flávio ^b   Dal Pizzol, Felipe ^a   Quevedo, João ^a  

^a UNIVERSIDADE DO EXTREMO SUL CATARINENSE   (Brazil)

^b HOSPITAL DE CLÍNICAS DE PORTO ALEGRE   (Brazil)

^c UNIVERSITY OF SOUTHERN SANTA CATARINA   (Brazil)

Author keywords

BDNF; Depression; IL 1 ; IL 10; Imipramine; Maternal deprivation; TNF

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYTOKINE; IMIPRAMINE; INTERLEUKIN 10; INTERLEUKIN 1BETA; SODIUM CHLORIDE; TUMOR NECROSIS FACTOR ALPHA;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FORCED SWIMMING TEST; HIPPOCAMPUS; IMMOBILIZATION; IMMUNOMODULATION; MALE; MATERNAL DEPRIVATION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CEREBROSPINAL FLUID LEVEL; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANTIDEPRESSIVE AGENTS, TRICYCLIC; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CYTOKINES; FEMALE; GENE EXPRESSION REGULATION; IMIPRAMINE; MALE; MATERNAL DEPRIVATION; PREGNANCY; RATS; RATS, WISTAR;

EID: 84872402713     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.11.044     Document Type: Article

References (81)

1. Anda R.F., Felitti V.J., Bremner J.D., Walker J.D., Whitfield C., Perry B.D., et al. The enduring effects of abuse and related adverse experiences in childhood. A convergence of evidence from neurobiology and epidemiology. European Archives of Psychiatry and Clinical Neuroscience 2006, 256:174-186.
2. Kendler K.S., Karkowski L.M., Prescott C.A. Causal relationship between stressful life events and the onset of major depression. American Journal of Psychiatry 1999, 156:837-841.
3. Kessler R.C. The effects of stressful life events on depression. Annual Review of Psychology 1997, 48:191-214.
4. Kosten T.A., Lee H.J., Kim J.J. Neonatal handling alters learning in adult male and female rats in a task-specific manner. Brain Research 2007, 18:144-153.
5. Matthews K., Robbins T.W. Early experience as a determinant of adult behavioural responses to reward: the effects of repeated maternal separation in the rat. Neuroscience and Biobehavioral Reviews 2003, 27:45-55.
6. Francis D.D., Caldji C., Champagne F., Plotsky P.M., Meaney M.J. The role of corticotropin-releasing factor-norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biological Psychiatry 1999, 46:1153-1166.
7. Hall F.S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Critical Reviews in Neurobiology 1998, 12:129-162.
8. Berk M., Wadee A.A., Kuschke R.H., O'Neill-Kerr A. Acute phase proteins in major depression. Journal of Psychosomatic Research 1997, 43:529-534.
9. Maes M., Scharpe S., Van Grootel L., Uyttenbroeck W., Cooreman W., Cosyns P., et al. Higher alpha 1-antitrypsin, haptoglobin, ceruloplasmin and lower retinol binding protein plasma levels during depression: further evidence for the existence of an inflammatory response during that illness. Journal of Affective Disorders 1992, 24:183-192.
10. Maes M. Evidence for an immune response in major depression: a review and hypothesis. Progress in Neuro-Psychopharmacology and Biological Psychiatry 1995, 19:11-38.
11. Raison C.L., Capuron L., Miller A.H. Cytokines sing the blues: inflammation and the pathogenesis of major depression. Trends in Immunology 2006, 27:24-31.
12. Zorilla E.P., Luborsky L., McKay J.R., Roesnthal R., Houldin A., Tax A., et al. The relationship of depression and stressors to immunological assays: a meta-analytic review. Brain, Behavior, and Immunity 2001, 15:199-226.
13. Kubera M., Obuchowicz E., Goehler L., Brzeszcz J., Maes M. In animal models, psychosocial stress-induced (neuro)inflammation, apoptosis and reduced neurogenesis are associated to the onset of depression. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2011, 35:744-759.
14. Vismari L., Alves G.J., Muscará M.N., Palermo-Neto J. A possible role to nitric oxide in the anti-inflammatory effects of amitriptyline. Immunopharmacology and Immunotoxicology 2012, 34:578-585.
15. Xia Z., DePierre J.W., Nassberger L. Tricyclic antidepressants inhibit IL-6, IL-beta and TNF-alpha release in human blood monocytes and IL-2 and interferon-gamma in T cells. Immunopharmacology 1996, 34:27-37.
16. Huang E.J., Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annual Review of Neuroscience 2001, 24:677-736.
17. Abelaira H.A., Réus G.Z., Ribeiro K.F., Zappellini G., Cipriano A.L., Scaini G., et al. Lamotrigine treatment reverses depressive-like behavior and alters BDNF levels in the brains of maternally deprived adult rats. Pharmacology Biochemistry and Behavior 2012, 101:348-353.
18. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biological Psychiatry 2006, 59:1116-1127.
19. Réus G.Z., Abelaira H.M., Stringari R.B., Fries G.R., Kapczinski F., Quevedo J. Memantine treatment reverses anhedonia, normalizes corticosterone levels and increases BDNF levels in the prefrontal cortex induced by chronic mild stress in rats. Metabolic Brain Disease 2012, 27:175-182.
20. Abelaira H.M., Réus G.Z., Ribeiro K.F., Zappellini G., Ferreira G.F., Gomes L.M., et al. Effects of acute and chronic treatment elicited by lamotrigine on behavior, energy metabolism, neurotrophins and signaling cascades in rats. Neurochemistry International 2011, 59:1163-1174.
21. Ceretta L.B., Réus G.Z., Stringari R.B., Ribeiro K.F., Zappellini G., Aguiar B.W., et al. Imipramine treatment reverses depressive-like behavior in alloxan-diabetic rats. Diabetes/Metabolism Research and Reviews 2012, 28:139-144.
22. Réus G.Z., Stringari R.B., Ribeiro K.F., Ferraro A.K., Vitto M.F., Cesconetto P., et al. Ketamine plus imipramine treatment induces antidepressant-like behavior and increases CREB and BDNF protein levels and PKA and PKC phosphorylation in rat brain. Behavioural Brain Research 2011, 221:166-171.
23. Lin Y., Ro L., Wang H., Chen J. Up-regulation of dorsal root ganglia BDNF and trkB receptor in inflammatory pain: an in vivo and in vitro study. Journal of Neuroinflammation 2011, 8:126.
24. Zhao J., Seereeram A., Nassar M.A., Levato A., Pezet S., Hathaway G., et al. Nociceptor-derived brain derived neurotrophic factor regulates acute and inflammatory but not neuropathic pain. Molecular and Cellular Neurosciences 2006, 31:539-548.
25. Heim C., Nemeroff C.B. The impact of early adverse experiences on brain systems involved in the pathophysiology of anxiety and affective disorders. Biological Psychiatry 1999, 46:1509-1522.
26. Réus G.Z., Stringari R.B., Ribeiro K.F., Cipriano A.L., Panizzutti B.S., Stertz L., et al. Maternal deprivation induces depressive-like behaviour and alters neurotrophin levels in the rat brain. Neurochemical Research 2011, 36:460-466.
27. Rattiner L.M., Davis M., French C.T., Kessler K.J. Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdale-dependant fear conditioning. Journal of Neuroscience 2004, 24:4796-4806.
28. Mello P.B. Physical exercise can reverse the deficit in fear memory induced by maternal deprivation. Neurobiology of Learning and Memory 2009, 92:364-369.
29. Fortunato J.J., Réus G.Z., Kirsch T.R., Stringari R.B., Fries G.R., Kapczinski F., et al. Chronic administration of harmine elicits antidepressant-like effects and increases BDNF levels in rat hippocampus. Journal of Neural Transmission 2010, 117:1131-1137.
30. Réus G.Z., Stringari R.B., Kirsch T.R., Fries G.R., Kapczinski F., Roesler R., et al. Neurochemical and behavioural effects of acute and chronic memantine administration in rats: further support for NMDA as a new pharmacological target for the treatment of depression. Brain Research Bulletin 2010, 81:585-589.
31. Garcia L.S., Comim C.M., Valvassori S.S., Réus G.Z., Barbosa L.M., Andreazza A.C., et al. Acute administration of ketamine induces antidepressant-like effects in the forced swimming test and increases BDNF levels in the rat hippocampus. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2008, 321:140-144.
32. Garcia L.S., Comim C.M., Valvassori S.S., Réus G.Z., Andreazza A.C., Stertz L., et al. Chronic administration of ketamine elicits antidepressant-like effects in rats without affecting hippocampal brain-derived neurotrophic factor protein levels. Basic & Clinical Pharmacology & Toxicology 2008, 103:502-506.
33. Porsolt R.D., Le Pichon M., Jalfre M. Animal model of depression. Nature 1977, 266:730-732.
34. Paxinos G., Watson C. The rat brain: stereotaxic coordinates 1986, Academic Press, Australia. 2nd ed.
35. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 1951, 193:265-275.
36. Agid O., Shapira B., Zislin J., Ritsner M., Hanin B., Murad H., et al. Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Molecular Psychiatry 1999, 4:163-172.
37. Stephan M., Straub R.H., Breivik T., Pabst R., von Hörsten S. Postnatal maternal deprivation aggravates experimental autoimmune encephalomyelitis in adult Lewis rats: reversal by chronic imipramine treatment. International Journal of Developmental Neuroscience 2002, 20:125-132.
38. MacQueen G.M., Ramakrishnan K., Ratnasingan R., Chen B., Young L.T. Desipramine treatment reduces the long-term behavioural and neurochemical sequelae of early-life maternal separation. International Journal of Neuropsychopharmacology 2003, 6:391-396.
39. Campbell S., MacQueen G. An update on regional brain volume differences associated with mood disorders. Current Opinion in Psychiatry 2006, 19:25-33.
40. McKinnon M.C., Yucel K., Nazarov A., MacQueen G.M. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. Journal of Psychiatry and Neuroscience 2009, 34:41-54.
41. Cunha A.B., Frey B.N., Andreazza A.C., Goi J.D., Rosa A.R., Goncalves C.A., et al. Serum brain-derived neurotrophic factor is decreased in bipolar disorder during depressive and manic episodes. Neuroscience Letters 2006, 398:215-219.
42. Kapczinski F., Frey B.N., Andreazza A.C., Kauer-Sant'Anna M., Cunha A.B., Post R.M. Increased oxidative stress as a mechanism for decreased BDNF levels in acute manic episodes. Revista Brasileira de Psiquiatria 2008, 30:243-245.
43. Palomino A., Vallejo-Illarramendi A., Gonzalez-Pinto A., Aldama A., Gonzalez-Gomez C., Mosquera F., et al. Decreased levels of plasma BDNF in first-episode schizophrenia and bipolar disorder patients. Schizophrenia Research 2006, 86:321-322.
44. Réus G.Z., Stringari R.B., Ribeiro K.F., Luft T., Abelaira H.M., Fries G.R., et al. Administration of cannabidiol and imipramine induces antidepressant-like effects in the forced swimming test and increases brain-derived neurotrophic factor levels in the rat amygdala. Acta Neuropsychiatrica 2011, 23:241-248.
45. Fanous S., Hammer R.P., Nikulina E.M. Short- and long-term effects of intermittent social defeat stress on brain-derived neurotrophic factor expression in mesocorticolimbic brain regions. Neuroscience 2010, 167:598-607.
46. Pizarro J.M., Lumley L.A., Medina W., Robison C.L., Chang W.E., Alagappan A., et al. Acute social defeat reduces neurotrophin expression in brain cortical and subcortical areas in mice. Brain Research 2004, 1025:10-20.
47. Yu H., Chen Z. The role of BDNF in depression on the basis of its location in the neural circuity. Acta Pharmacologica Sinica 2011, 32:3-11.
48. Vyas A., Mitra R., Shankaranarayana Rao B.S., Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. Journal of Neuroscience 2002, 22:6810-6818.
49. Pawlak R., Rao B.S., Melchor J.P., Chattarji S., McEwen B., Strickland S. Tissue plasminogen activator and plasminogen mediate stress induced decline of neuronal and cognitive functions in the mouse hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:18201-18206.
50. de Pablos R.M., Villaran R.F., Arguelles S., Herrera A.J., Venero J.L., Ayala A., et al. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology 1995, 121:66-72.
51. Bilbo S.D., Barrientos R.M., Eads A.S., Northcutt A., Watkins L.R., Rudy J.W., et al. Early-life infection leads to altered BDNF and IL-1b mRNA expression in rat hippocampus following learning in adulthood. Brain, Behavior, and Immunity 2008, 22:451-455.
52. Tong L., Balazs R., Soiampornkul R., Thangnipon W., Cotman C.W. Interleukin-1beta impairs brain derived neurotrophic factorinduced signal transduction. Neurobiology of Aging 2007, 29:1380-1393.
53. Elomaa A.P., Niskanen L., Herzig K., Viinamäki H., Hintikka J., Koivumaa-Honkanen H., et al. Elevated levels of serum IL-5 are associated with an increased likelihood of major depressive disorder. BMC Psychiatry 2012, 12:2.
54. Haastrup E., Bukh J.D., Bock C., Vinberg M., Thørner L.W., Hansen T., et al. Promoter variants in IL18 are associated with onset of depression in patients previously exposed to stressful-life events. Journal of Affective Disorders 2012, 136:134-138.
55. Anisman H., Poulter M.O., Gandhi R., Merali Z., Hayley S. Interferon-alpha effects are exaggerated when administered on a psychosocial stressor backdrop: cytokine, corticosterone and brain monoamine variations. Journal of Neuroimmunology 2007, 186:45-53.
56. Anisman H., Prakash P., Merali Z., Poulter M.O. Corticotropin releasing hormone receptor alterations elicited by acute and chronic unpredictable stressor challenges in stressor-susceptible and resilient strains of mice. Behavioural Brain Research 2007, 181:180-190.
57. 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, Behavior, and Immunity 2008, 22:573-589.
58. Nelson T., Ur C., Gruol D. Chronic interleukin-6 exposure alters electrophysiological properties and calcium signaling in developing cerebellar purkinje neurons in culture. Journal of Neurophysiology 2002, 88:475-486.
59. Tsao C.W., Lin Y.S., Chen C.C., Bai C.H., Wu S.R. Cytokines and serotonin transporter in patients with major depression. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2006, 30:899-905.
60. Nadjar A., Bluthé R.M., May M.J., Dantzer R., Parnet P. Inactivation of the cerebral NFkappaB pathway inhibits interleukin-1beta-induced sickness behavior and c-Fos expression in various brain nuclei. Neuropsychopharmacology 2005, 30:1492-1499.
61. Capuron L., Pagnoni G., Demetrashvili M., Woolwine B.J., Nemeroff C.B., Berns G.S., et al. Anterior cingulate activation and error processing during interferon-alpha treatment. Biological Psychiatry 2005, 58:190-196.
62. Capuron L., Pagnoni G., Demetrashvili M.F., Lawson D.H., Fornwalt F.B., Woolwine B., et al. Basal ganglia hypermetabolism and symptoms of fatigue during interferon-alpha therapy. Neuropsychopharmacology 2007, 32:2384-2392.
63. McAfoose J., Baune B.T. Evidence for a cytokine model of cognitive function. Neuroscience and Biobehavioral Reviews 2009, 33:355-366.
64. Pace T.W.W., Hu F., Miller A.H. Cytokine-effects on glucocorticoid receptor function: relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression. Brain, Behavior, and Immunity 2007, 21:9-19.
65. Brenhouse H.C., Andersen S.L. Nonsteroidal anti-inflammatory treatment prevents delayed effects of early life stress in rats. Biological Psychiatry 2011, 70:434-440.
66. Dimatelis J.J., Pillay N.S., Mutyaba A.K., Russell V.A., Daniels W.M., Stein D.J. Early maternal separation leads to down-regulation of cytokine gene expression. Metabolic Brain Disease 2012, 27:393-397.
67. Carboni L., Becchi S., Piubelli C., Mallei A., Giambelli R., Razzoli M., et al. Early-life stress and antidepressants modulate peripheral biomarkers in a gene-environment rat model of depression. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2010, 34:1037-1048.
68. Loftis J.M., Huckans M., Morasco B.J. Neuroimmune mechanisms of cytokine-induced depression: current theories and novel treatment strategies. Neurobiology of Disease 2010, 37:519-533.
69. Qin L., Wu X., Block M.L., Liu Y., Breese G.R., Hong J.S., et al. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462.
70. Boka G., Anglade P., Wallach D., Javoy-Agid F., Agid Y., Hirsch E.C. Immunocytochemical analysis of tumor necrosis factor and its receptors in Parkinson's disease. Neuroscience Letters 1994, 172:151-154.
71. Khairova R.A., Machado-Vieira R., Du J., Manji H.K. A potential role for proinflammatory cytokines in regulating synaptic plasticity in major depressive disorder. International Journal of Neuropsychopharmacology 2009, 12:561-578.
72. Parnet P., Amindari S., Wu C., Brunke-Reese D., Goujon E., Weyhenmeyer J.A., et al. Expression of type I and type II interleukin-1 receptors in mouse brain. Brain Research. Molecular Brain Research 1994, 27:63-70.
73. Schobitz B., de Kloet E.R., Sutanto W., Holsboer F. Cellular localization of interleukin 6 mRNA and interleukin 6 receptor mRNA in rat brain. European Journal of Neuroscience 1993, 5:1426-1435.
74. Campbell S.J., Deacon R.M., Jiang Y., Ferrari C., Pitossi F.J., Anthony D.C. Overexpression of IL-1beta by adenoviral-mediated gene transfer in the rat brain causes a prolonged hepatic chemokine response, axonal injury and the suppression of spontaneous behaviour. Neurobiology of Disease 2007, 27:151-163.
75. Butler M.P., O'Connor J.J., Moynagh P.N. Dissection of tumor-necrosis factor alpha inhibition of long-term potentiation (LTP) reveals a p38 mitogen-activated protein kinase-dependent mechanism which maps to early-but not late-phase LTP. Neuroscience 2004, 124:319-326.
76. Cunningham A.J., Murray C.A., O'Neill L.A., Lynch M.A., O'Connor J.J. Interleukin-1 beta (IL-1 beta) and tumour necrosis factor (TNF) inhibit long-term potentiation in the rat dentate gyrus in vitro. Neuroscience Letters 1996, 203:17-20.
77. Martensson U., Nassberger L. Influence of antidepressants on mitogen stimulation of human lymphocytes. Toxicology In Vitro 1993, 7:241-245.
78. Sacerdote P., Bianchi M., Panerai A.E. Chlorimipramine and nortriptyline but not fluoxetine and fluvoxamine inhibit human polymorphonuclear cell chemotaxis in vitro. General Pharmacology 1994, 25:409-412.
79. Song C., Halbreich U., Han C., Leonard B.E., Luo H. Imbalance between pro and anti-inflammatory cytokines, and between Th1 and Th2 cytokines in depressed patients: the effect of electroacupuncture or fluoxetine treatment. Pharmacopsychiatry 2009, 42:182-188.
80. Song C., Zhang X.Y., Manku M. Increased phospholipase A2 activity and inflammatory response but decreased nerve growth factor expression in the olfactory bulbectomized rat model of depression: effects of chronic ethyleicosapentaenoate treatment. Journal of Neuroscience 2009, 29:14-22.
81. Tynan R.J., Weidenhofer J., Hinwood M., Cairns M.J., Day T.A., Walker F.R. A comparative examination of the anti-inflammatory effects of SSRI and SNRI antidepressants on LPS stimulated microglia. Brain, Behavior, and Immunity 2012, 26:469-479.