Microglial production of TNF-alpha is a key element of sustained fear memory

Brain, Behavior, and Immunity

Volumn 59, Issue , 2017, Pages 313-321

  Yu, Zhiqian ^a,b   Fukushima, Hotaka ^c   Ono, Chiaki ^a   Sakai, Mai ^a,b   Kasahara, Yoshiyuki ^a,b   Kikuchi, Yoshie ^a   Gunawansa, Nicole ^a   Takahashi, Yuta ^b   Matsuoka, Hiroo ^b   Kida, Satoshi ^c   Tomita, Hiroaki ^a,b  

^a TOHOKU UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

Author keywords

Extinction; Fear memory; Retention; TNF alpha

Indexed keywords

CD206 ANTIGEN; CD209 ANTIGEN; MEMBRANE PROTEIN; MINOCYCLINE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; CYTOKINE; DC-SPECIFIC ICAM-3 GRABBING NONINTEGRIN; LECTIN; MANNOSE BINDING LECTIN; MANNOSE RECEPTOR;

ANALYSIS OF VARIANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA SYNTHESIS; FEAR; FOOTSHOCK; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; MICROGLIA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; ANIMAL; BIOSYNTHESIS; BLOOD; C57BL MOUSE; DRUG EFFECT; HIPPOCAMPUS; MACROPHAGE ACTIVATION; METABOLISM; REINFORCEMENT;

ANIMALS; CELL ADHESION MOLECULES; CYTOKINES; EXTINCTION, PSYCHOLOGICAL; FEAR; HIPPOCAMPUS; LECTINS, C-TYPE; MACROPHAGE ACTIVATION; MALE; MANNOSE-BINDING LECTINS; MEMORY; MICE; MICE, INBRED C57BL; MICROGLIA; MINOCYCLINE; RECEPTORS, CELL SURFACE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84997403823     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.08.011     Document Type: Article

References (47)

1. Acharjee, S., Nayani, N., Tsutsui, M., Hill, M.N., Ousman, S.S., Pittman, Q.J., Altered cognitive-emotional behavior in early experimental autoimmune encephalitis–cytokine and hormonal correlates. Brain Behav. Immun. 33 (2013), 164–172.
2. Agis-Balboa, R.C., Arcos-Diaz, D., Wittnam, J., Govindarajan, N., Blom, K., Burkhardt, S., Haladyniak, U., Agbemenyah, H.Y., Zovoilis, A., Salinas-Riester, G., Opitz, L., Sananbenesi, F., Fischer, A., A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. EMBO J. 30 (2011), 4071–4083.
3. Alberini, C.M., Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes?. Trends Neurosci. 28 (2005), 51–56.
4. Beattie, E.C., Stellwagen, D., Morishita, W., Bresnahan, J.C., Ha, B.K., Von Zastrow, M., Beattie, M.S., Malenka, R.C., Control of synaptic strength by glial TNFalpha. Science 295 (2002), 2282–2285.
5. Blandino, P. Jr., Barnum, C.J., Deak, T., The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1beta responses to stress. J. Neuroimmunol. 173 (2006), 87–95.
6. Blandino, P. Jr., Barnum, C.J., Solomon, L.G., Larish, Y., Lankow, B.S., Deak, T., Gene expression changes in the hypothalamus provide evidence for regionally-selective changes in IL-1 and microglial markers after acute stress. Brain Behav. Immun. 23 (2009), 958–968.
7. Boche, D., Perry, V.H., Nicoll, J.A., Review: activation patterns of microglia and their identification in the human brain. Neuropathol. Appl. Neurobiol. 39 (2013), 3–18.
8. Burton, M.D., Johnson, R.W., Interleukin-6 trans-signaling in the senescent mouse brain is involved in infection-related deficits in contextual fear conditioning. Brain Behav. Immun. 26 (2012), 732–738.
9. Durafourt, B.A., Moore, C.S., Zammit, D.A., Johnson, T.A., Zaguia, F., Guiot, M.C., Bar-Or, A., Antel, J.P., Comparison of polarization properties of human adult microglia and blood-derived macrophages. Glia 60 (2012), 717–727.
10. Frank, M.G., Thompson, B.M., Watkins, L.R., Maier, S.F., Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses. Brain Behav. Immun. 26 (2012), 337–345.
11. Fumagalli, M., Lecca, D., Abbracchio, M.P., Role of purinergic signalling in neuro-immune cells and adult neural progenitors. Front. Biosci. (Landmark Ed.) 16 (2011), 2326–2341.
12. Gill, J., Vythilingam, M., Page, G.G., Low cortisol, high DHEA, and high levels of stimulated TNF-alpha, and IL-6 in women with PTSD. J. Trauma. Stress 21 (2008), 530–539.
13. Goswami, S., Rodriguez-Sierra, O., Cascardi, M., Pare, D., Animal models of post-traumatic stress disorder: face validity. Front. Neurosci., 7, 2013, 89.
14. Grau, J.W., Huie, J.R., Lee, K.H., Hoy, K.C., Huang, Y.J., Turtle, J.D., Strain, M.M., Baumbauer, K.M., Miranda, R.M., Hook, M.A., Ferguson, A.R., Garraway, S.M., Metaplasticity and behavior: how training and inflammation affect plastic potential within the spinal cord and recovery after injury. Front. Neural Circuits, 8, 2014, 100.
15. Grinberg, Y.Y., Dibbern, M.E., Levasseur, V.A., Kraig, R.P., Insulin-like growth factor-1 abrogates microglial oxidative stress and TNF-alpha responses to spreading depression. J. Neurochem. 126 (2013), 662–672.
16. Guo, M., Liu, T., Guo, J.C., Jiang, X.L., Chen, F., Gao, Y.S., Study on serum cytokine levels in posttraumatic stress disorder patients. Asian Pac. J. Trop. Med. 5 (2012), 323–325.
17. Hao, Y., Jing, H., Bi, Q., Zhang, J., Qin, L., Yang, P., Intra-amygdala microinfusion of IL-6 impairs the auditory fear conditioning of rats via JAK/STAT activation. Behav. Brain Res. 275 (2014), 88–95.
18. Hu, X., Leak, R.K., Shi, Y., Suenaga, J., Gao, Y., Zheng, P., Chen, J., Microglial and macrophage polarization-new prospects for brain repair. Nat. Rev. Neurol. 11 (2015), 56–64.
19. Jing, H., Hao, Y., Bi, Q., Zhang, J., Yang, P., Intra-amygdala microinjection of TNF-alpha impairs the auditory fear conditioning of rats via glutamate toxicity. Neurosci. Res., 2014.
20. Jostock, T., Mullberg, J., Ozbek, S., Atreya, R., Blinn, G., Voltz, N., Fischer, M., Neurath, M.F., Rose-John, S., Soluble gp130 is the natural inhibitor of soluble interleukin-6 receptor transsignaling responses. Eur. J. Biochem. 268 (2001), 160–167.
21. Kobayashi, K., Imagama, S., Ohgomori, T., Hirano, K., Uchimura, K., Sakamoto, K., Hirakawa, A., Takeuchi, H., Suzumura, A., Ishiguro, N., Kadomatsu, K., Minocycline selectively inhibits M1 polarization of microglia. Cell Death Dis., 4, 2013, e525.
22. Lech, M., Susanti, H.E., Rommele, C., Grobmayr, R., Gunthner, R., Anders, H.J., Quantitative expression of C-type lectin receptors in humans and mice. Int. J. Mol. Sci. 13 (2012), 10113–10131.
23. Lee, S.M., Yune, T.Y., Kim, S.J., Kim, Y.C., Oh, Y.J., Markelonis, G.J., Oh, T.H., Minocycline inhibits apoptotic cell death via attenuation of TNF-alpha expression following iNOS/NO induction by lipopolysaccharide in neuron/glia co-cultures. J. Neurochem. 91 (2004), 568–578.
24. Lodge, P.A., Sriram, S., Regulation of microglial activation by TGF-beta, IL-10, and CSF-1. J. Leukoc. Biol. 60 (1996), 502–508.
25. Mamiya, N., Fukushima, H., Suzuki, A., Matsuyama, Z., Homma, S., Frankland, P.W., Kida, S., Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J. Neurosci. 29 (2009), 402–413.
26. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A., Locati, M., The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25 (2004), 677–686.
27. Marsicano, G., Wotjak, C.T., Azad, S.C., Bisogno, T., Rammes, G., Cascio, M.G., Hermann, H., Tang, J., Hofmann, C., Zieglgansberger, W., Di Marzo, V., Lutz, B., The endogenous cannabinoid system controls extinction of aversive memories. Nature 418 (2002), 530–534.
28. McCoy, M.K., Tansey, M.G., TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J. Neuroinflamm., 5, 2008, 45.
29. Miron, V.E., Boyd, A., Zhao, J.W., Yuen, T.J., Ruckh, J.M., Shadrach, J.L., van Wijngaarden, P., Wagers, A.J., Williams, A., Franklin, R.J., French-Constant, C., M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nat. Neurosci. 16 (2013), 1211–1218.
30. Nakazato, F., Tada, T., Sekiguchi, Y., Murakami, K., Yanagisawa, S., Tanaka, Y., Hongo, K., Disturbed spatial learning of rats after intraventricular administration of transforming growth factor-beta 1. Neurol. Med. Chir. (Tokyo) 42 (2002), 151–156 discussion 157.
31. O'Connor, K.A., Johnson, J.D., Hansen, M.K., Wieseler Frank, J.L., Maksimova, E., Watkins, L.R., Maier, S.F., Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res. 991 (2003), 123–132.
32. Parkhurst, C.N., Yang, G., Ninan, I., Savas, J.N., Yates, J.R. 3rd, Lafaille, J.J., Hempstead, B.L., Littman, D.R., Gan, W.B., Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155 (2013), 1596–1609.
33. Puffenbarger, R.A., Boothe, A.C., Cabral, G.A., Cannabinoids inhibit LPS-inducible cytokine mRNA expression in rat microglial cells. Glia 29 (2000), 58–69.
34. Pugh, C.R., Nguyen, K.T., Gonyea, J.L., Fleshner, M., Wakins, L.R., Maier, S.F., Rudy, J.W., Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation. Behav. Brain Res. 106 (1999), 109–118.
35. Quirk, G.J., Mueller, D., Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33 (2008), 56–72.
36. Raghavendra, V., Tanga, F., DeLeo, J.A., Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J. Pharmacol. Exp. Ther. 306 (2003), 624–630.
37. Rappocciolo, G., Jenkins, F.J., Hensler, H.R., Piazza, P., Jais, M., Borowski, L., Watkins, S.C., Rinaldo, C.R. Jr., DC-SIGN is a receptor for human herpesvirus 8 on dendritic cells and macrophages. J. Immunol. 176 (2006), 1741–1749.
38. Rescorla, R.A., Spontaneous recovery. Learn Mem. 11 (2004), 501–509.
39. Sanchez Mejia, R.O., Ona, V.O., Li, M., Friedlander, R.M., Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery 48 (2001), 1393–1399 discussion 1399–1401.
40. Shepherd, V.L., Abdolrasulnia, R., Garrett, M., Cowan, H.B., Down-regulation of mannose receptor activity in macrophages after treatment with lipopolysaccharide and phorbol esters. J. Immunol. 145 (1990), 1530–1536.
41. Sica, A., Mantovani, A., Macrophage plasticity and polarization: in vivo veritas. J. Clin. Invest. 122 (2012), 787–795.
42. Suzuki, A., Josselyn, S.A., Frankland, P.W., Masushige, S., Silva, A.J., Kida, S., Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J. Neurosci. 24 (2004), 4787–4795.
43. Vazquez-Mendoza, A., Carrero, J.C., Rodriguez-Sosa, M., Parasitic infections: a role for C-type lectins receptors. Biomed. Res. Int., 2013, 2013, 456352.
44. von Kanel, R., Hepp, U., Kraemer, B., Traber, R., Keel, M., Mica, L., Schnyder, U., Evidence for low-grade systemic proinflammatory activity in patients with posttraumatic stress disorder. J. Psychiatr. Res. 41 (2007), 744–752.
45. Wang, A.L., Yu, A.C., Lau, L.T., Lee, C., Wu le, M., Zhu, X., Tso, M.O., Minocycline inhibits LPS-induced retinal microglia activation. Neurochem. Int. 47 (2005), 152–158.
46. Yehuda, R., Post-traumatic stress disorder. N. Engl. J. Med. 346 (2002), 108–114.
47. Yu, Z., Ono, C., Aiba, S., Kikuchi, Y., Sora, I., Matsuoka, H., Tomita, H., Therapeutic concentration of lithium stimulates complement C3 production in dendritic cells and microglia via GSK-3 inhibition. Glia 63 (2015), 257–270.