Learned helplessness activates hippocampal microglia in rats: A potential target for the antidepressant imipramine

Pharmacology Biochemistry and Behavior

Volumn 150-151, Issue , 2016, Pages 138-146

  Iwata, Masaaki ^a   Ishida, Hisahito ^a   Kaneko, Koichi ^a   Shirayama, Yukihiko ^b  

^a TOTTORI UNIVERSITY   (Japan)

^b TEIKYO UNIVERSITY CHIBA MEDICAL CENTER   (Japan)

Author keywords

Antidepressants; Depression; Hippocampus; Learned helplessness; Microglia

Indexed keywords

FLUVOXAMINE; IMIPRAMINE; ANTIDEPRESSANT AGENT;

ANIMAL EXPERIMENT; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; GRANULE CELL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; LEARNED HELPLESSNESS; MALE; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; HIPPOCAMPUS; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIDEPRESSIVE AGENTS; HELPLESSNESS, LEARNED; HIPPOCAMPUS; IMIPRAMINE; MALE; MICROGLIA; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84994322980     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2016.10.005     Document Type: Article

References (41)

1. Arakawa, S., Shirayama, Y., Fujita, Y., Ishima, T., Horio, M., Muneoka, K., Iyo, M., Hashimoto, K., Minocycline produced antidepressant-like effects on the learned helplessness rats with alterations in levels of monoamine in the amygdala and no changes in BDNF levels in the hippocampus at baseline. Pharmacol. Biochem. Behav. 100 (2012), 601–606.
2. Berk, M., Williams, L.J., Jacka, F.N., O'Neil, A., Pasco, J.A., Moylan, S., Allen, N.B., Stuart, A.L., Hayley, A.C., Byrne, M.L., Maes, M., So depression is an inflammatory disease, but where does the inflammation come from?. BMC Med., 11, 2013, 200.
3. Bremner, J.D., Narayan, M., Anderson, E.R., Staib, L.H., Miller, H.L., Charney, D.S., Hippocampal volume reduction in major depression. Am. J. Psychiatry 157 (2000), 115–118.
4. Capuron, L., Miller, A.H., Cytokines and psychopathology: lessons from interferon-alpha. Biol. Psychiatry 56 (2004), 819–824.
5. Dantzer, R., O'Connor, J.C., Freund, G.G., Johnson, R.W., Kelley, K.W., From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 9 (2008), 46–57.
6. Duman, R.S., Heninger, G.R., Nestler, E.J., A molecular and cellular theory of depression. Arch. Gen. Psychiatry 54 (1997), 597–606.
7. Dunn, A.J., Swiergiel, A.H., de Beaurepaire, R., Cytokines as mediators of depression: what can we learn from animal studies?. Neurosci. Biobehav. Rev. 29 (2005), 891–909.
8. Gustin, A., Kirchmeyer, M., Koncina, E., Felten, P., Losciuto, S., Heurtaux, T., Tardivel, A., Heuschling, P., Dostert, C., NLRP3 inflammasome is expressed and functional in mouse brain microglia but not in astrocytes. PLoS One, 10, 2015, e0130624.
9. Hanisch, U.K., Microglia as a source and target of cytokines. Glia 40 (2002), 140–155.
10. Horikawa, H., Kato, T.A., Mizoguchi, Y., Monji, A., Seki, Y., Ohkuri, T., Gotoh, L., Yonaha, M., Ueda, T., Hashioka, S., Kanba, S., Inhibitory effects of SSRIs on IFN-gamma induced microglial activation through the regulation of intracellular calcium. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 34 (2010), 1306–1316.
11. Iwata, M., Shirayama, Y., Ishida, H., Kawahara, R., Hippocampal synapsin I, growth-associated protein-43, and microtubule-associated protein-2 immunoreactivity in learned helplessness rats and antidepressant-treated rats. Neuroscience 141 (2006), 1301–1313.
12. Iwata, M., Shirayama, Y., Ishida, H., Hazama, G.I., Nakagome, K., Hippocampal astrocytes are necessary for antidepressant treatment of learned helplessness rats. Hippocampus 21 (2011), 877–884.
13. Iwata, M., Ota, K.T., Duman, R.S., The inflammasome: pathways linking psychological stress, depression, and systemic illnesses. Brain Behav. Immun. 31 (2013), 105–114.
14. Iwata, M., Ota, K.T., Li, X.Y., Sakaue, F., Li, N., Dutheil, S., Banasr, M., Duric, V., Yamanashi, T., Kaneko, K., Rasmussen, K., Glasebrook, A., Koester, A., Song, D., Jones, K.A., Zorn, S., Smagin, G., Duman, R.S., Psychological stress activates the inflammasome via release of adenosine triphosphate and stimulation of the purinergic type 2X7 receptor. Biol. Psychiatry 80 (2016), 12–22.
15. Jeong, H.K., Ji, K., Min, K., Joe, E.H., Brain inflammation and microglia: facts and misconceptions. Exp. Neurobiol. 22 (2013), 59–67.
16. Kettenmann, H., Hanisch, U.K., Noda, M., Verkhratsky, A., Physiology of microglia. Physiol. Rev. 91 (2011), 461–553.
17. Kigerl, K.A., Gensel, J.C., Ankeny, D.P., Alexander, J.K., Donnelly, D.J., Popovich, P.G., Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 29 (2009), 13435–13444.
18. Koo, J.W., Duman, R.S., IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 751–756.
19. Koo, J.W., Duman, R.S., Evidence for IL-1 receptor blockade as a therapeutic strategy for the treatment of depression. Curr. Opin. Investig. Drugs 10 (2009), 664–671.
20. 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. U. S. A. 107 (2010), 2669–2674.
21. Kreutzberg, G.W., Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19 (1996), 312–318.
22. Matsui, H., Ohgomori, T., Natori, T., Miyamoto, K., Kusunoki, S., Sakamoto, K., Ishiguro, N., Imagama, S., Kadomatsu, K., Keratan sulfate expression in microglia is diminished in the spinal cord in experimental autoimmune neuritis. Cell Death Dis., 4, 2013, e946.
23. Monje, M.L., Toda, H., Palmer, T.D., Inflammatory blockade restores adult hippocampal neurogenesis. Science 302 (2003), 1760–1765.
24. Musselman, D.L., Lawson, D.H., Gumnick, J.F., Manatunga, A.K., Penna, S., Goodkin, R.S., Greiner, K., Nemeroff, C.B., Miller, A.H., Paroxetine for the prevention of depression induced by high-dose interferon alfa. N. Engl. J. Med. 344 (2001), 961–966.
25. Nakagawa, Y., Chiba, K., Role of microglial m1/m2 polarization in relapse and remission of psychiatric disorders and diseases. Pharm. (Basel) 7 (2014), 1028–1048.
26. Obuchowicz, E., Kowalski, J., Labuzek, K., Krysiak, R., Pendzich, J., Herman, Z.S., Amitriptyline and nortriptyline inhibit interleukin-1 release by rat mixed glial and microglial cell cultures. Int. J. Neuropsychopharmacol. 9 (2006), 27–35.
27. Pan, Y., Chen, X.Y., Zhang, Q.Y., Kong, L.D., Microglial NLRP3 inflammasome activation mediates IL-1beta-related inflammation in prefrontal cortex of depressive rats. Brain Behav. Immun., 2014.
28. Qin, L., Liu, Y., Cooper, C., Liu, B., Wilson, B., Hong, J.S., Microglia enhance beta-amyloid peptide-induced toxicity in cortical and mesencephalic neurons by producing reactive oxygen species. J. Neurochem. 83 (2002), 973–983.
29. Rial, D., Lemos, C., Pinheiro, H., Duarte, J.M., Goncalves, F.Q., Real, J.I., Prediger, R.D., Goncalves, N., Gomes, C.A., Canas, P.M., Agostinho, P., Cunha, R.A., Depression as a glial-based synaptic dysfunction. Front. Cell. Neurosci., 9, 2015, 521.
30. Seligman, M.E., Beagley, G., Learned helplessness in the rat. J. Comp. Physiol. Psychol. 88 (1975), 534–541.
31. Setiawan, E., Wilson, A.A., Mizrahi, R., Rusjan, P.M., Miler, L., Rajkowska, G., Suridjan, I., Kennedy, J.L., Rekkas, P.V., Houle, S., Meyer, J.H., Role of translocator protein density, a marker of neuroinflammation, in the brain during major depressive episodes. JAMA Psychiat. 72 (2015), 268–275.
32. 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. 93 (1996), 3908–3913.
33. Shirayama, Y., Chen, A.C., Nakagawa, S., Russell, D.S., Duman, R.S., Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 22 (2002), 3251–3261.
34. Sudo, S., Tanaka, J., Toku, K., Desaki, J., Matsuda, S., Arai, T., Sakanaka, M., Maeda, N., Neurons induce the activation of microglial cells in vitro. Exp. Neurol. 154 (1998), 499–510.
35. Vavakova, M., Durackova, Z., Trebaticka, J., Markers of oxidative stress and neuroprogression in depression disorder. Oxidative Med. Cell. Longev., 2015, 2015, 898393.
36. Vila, M., Jackson-Lewis, V., Guegan, C., Wu, D.C., Teismann, P., Choi, D.K., Tieu, K., Przedborski, S., The role of glial cells in Parkinson's disease. Curr. Opin. Neurol. 14 (2001), 483–489.
37. Wake, H., Moorhouse, A.J., Jinno, S., Kohsaka, S., Nabekura, J., Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29 (2009), 3974–3980.
38. Wake, H., Moorhouse, A.J., Miyamoto, A., Nabekura, J., Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci. 36 (2013), 209–217.
39. Weber, M.D., Frank, M.G., Tracey, K.J., Watkins, L.R., Maier, S.F., Stress induces the danger-associated molecular pattern HMGB-1 in the hippocampus of male Sprague Dawley rats: a priming stimulus of microglia and the NLRP3 inflammasome. J. Neurosci. 35 (2015), 316–324.
40. Wu, C.H., Chien, H.F., Chang, C.Y., Chen, S.H., Huang, Y.S., Response of amoeboid and differentiating ramified microglia to glucocorticoids in postnatal rats: a lectin histochemical and ultrastructural study. Neurosci. Res. 40 (2001), 235–244.
41. Yirmiya, R., Rimmerman, N., Reshef, R., Depression as a microglial disease. Trends Neurosci. 38 (2015), 637–658.