Sodium butyrate abolishes lipopolysaccharide-induced depression-like behaviors and hippocampal microglial activation in mice

Brain Research

Volumn 1680, Issue , 2018, Pages 13-38

  Yamawaki, Yosuke ^a,b   Yoshioka, Norika ^a   Nozaki, Kanako ^b   Ito, Hikaru ^b   Oda, Keisuke ^a   Harada, Kana ^a   Shirawachi, Satomi ^b   Asano, Satoshi ^b   Aizawa, Hidenori ^b   Yamawaki, Shigeto ^b   Kanematsu, Takashi ^b   Akagi, Hiroyuki ^a  

^a HIROSHIMA INTERNATIONAL UNIVERSITY   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Epigenetics; Hippocampus; Histone deacetylase inhibitor; Inflammation; Microglia

Indexed keywords

BUTYRIC ACID; COMPLEMENTARY DNA; HISTONE H3; HISTONE H4; LIPOPOLYSACCHARIDE; MESSENGER RNA; ACTIN BINDING PROTEIN; AIF1 PROTEIN, MOUSE; ANTIDEPRESSANT AGENT; CALCIUM BINDING PROTEIN; CYTOKINE; HISTONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIDEPRESSANT ACTIVITY; ARTICLE; CALCIUM BINDING; CELL ACTIVATION; CONTROLLED STUDY; DISEASE SEVERITY; DNA METHYLATION; EPIGENETICS; FORCED SWIM TEST; GENE EXPRESSION; HIPPOCAMPUS; HISTONE ACETYLATION; HISTONE MODIFICATION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MAJOR DEPRESSION; MENTAL STRESS; MICROGLIA; MOUSE; NONHUMAN; OVERLAPPING GENE; PRIORITY JOURNAL; REPEATED DRUG DOSE; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CYTOLOGY; DEPRESSION; DISEASE MODEL; DNA MICROARRAY; DOSE RESPONSE; DRUG EFFECT; EXPLORATORY BEHAVIOR; GENETICS; METABOLISM; PSYCHOLOGY; SWIMMING;

ANIMALS; ANTIDEPRESSIVE AGENTS; BUTYRIC ACID; CALCIUM-BINDING PROTEINS; CYTOKINES; DEPRESSION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; GENE EXPRESSION; HIPPOCAMPUS; HISTONES; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; MICROGLIA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; SWIMMING;

EID: 85038841468     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2017.12.004     Document Type: Article

References (53)

1. Almeida-Suhett, C.P., Graham, A., Chen, Y., Deuster, P., Behavioral changes in male mice fed a high-fat diet are associated with IL-1beta expression in specific brain regions. Physiol. Behav. 169 (2017), 130–140.
2. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios, M., Monteggia, L.M., Self, D.W., Nestler, E.J., Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006), 864–868.
3. Berton, O., Nestler, E.J., New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 7 (2006), 137–151.
4. Bianchi, R., Adami, C., Giambanco, I., Donato, R., S100B binding to RAGE in microglia stimulates COX-2 expression. J. Leukoc. Biol. 81 (2007), 108–118.
5. Blazek, K., Eames, H.L., Weiss, M., Byrne, A.J., Perocheau, D., Pease, J.E., Doyle, S., McCann, F., Williams, R.O., Udalova, I.A., IFN-lambda resolves inflammation via suppression of neutrophil infiltration and IL-1beta production. J. Exp. Med. 212 (2015), 845–853.
6. Boitard, C., Cavaroc, A., Sauvant, J., Aubert, A., Castanon, N., Laye, S., Ferreira, G., Impairment of hippocampal-dependent memory induced by juvenile high-fat diet intake is associated with enhanced hippocampal inflammation in rats. Brain Behav. Immun. 40 (2014), 9–17.
7. Chen, P.S., Peng, G.S., Li, G., Yang, S., Wu, X., Wang, C.C., Wilson, B., Lu, R.B., Gean, P.W., Chuang, D.M., Hong, J.S., Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol. Psychiatry 11 (2006), 1116–1125.
8. Chen, P.S., Wang, C.C., Bortner, C.D., Peng, G.S., Wu, X., Pang, H., Lu, R.B., Gean, P.W., Chuang, D.M., Hong, J.S., Valproic acid and other histone deacetylase inhibitors induce microglial apoptosis and attenuate lipopolysaccharide-induced dopaminergic neurotoxicity. Neuroscience 149 (2007), 203–212.
9. Covington, H.E. 3rd, Vialou, V.F., LaPlant, Q., Ohnishi, Y.N., Nestler, E.J., Hippocampal-dependent antidepressant-like activity of histone deacetylase inhibition. Neurosci. Lett. 493 (2011), 122–126.
10. 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), 46–56.
11. Ding, S., Khoury-Hanold, W., Iwasaki, A., Robek, M.D., Epigenetic reprogramming of the type III interferon response potentiates antiviral activity and suppresses tumor growth. PLoS Biol., 12, 2014, e1001758.
12. Faraco, G., Pittelli, M., Cavone, L., Fossati, S., Porcu, M., Mascagni, P., Fossati, G., Moroni, F., Chiarugi, A., Histone deacetylase (HDAC) inhibitors reduce the glial inflammatory response in vitro and in vivo. Neurobiol. Dis. 36 (2009), 269–279.
13. Fekadu, A., Wooderson, S.C., Markopoulo, K., Donaldson, C., Papadopoulos, A., Cleare, A.J., What happens to patients with treatment-resistant depression? A systematic review of medium to long term outcome studies. J. Affect. Disord. 116 (2009), 4–11.
14. Frenois, F., Moreau, M., O'Connor, J., Lawson, M., Micon, C., Lestage, J., Kelley, K.W., Dantzer, R., Castanon, N., Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 32 (2007), 516–531.
15. Fuchikami, M., Morinobu, S., Kurata, A., Yamamoto, S., Yamawaki, S., Single immobilization stress differentially alters the expression profile of transcripts of the brain-derived neurotrophic factor (BDNF) gene and histone acetylation at its promoters in the rat hippocampus. Int. J. Neuropsychopharmacol. 12 (2009), 73–82.
16. Fuchikami, M., Morinobu, S., Segawa, M., Okamoto, Y., Yamawaki, S., Ozaki, N., Inoue, T., Kusumi, I., Koyama, T., Tsuchiyama, K., Terao, T., DNA methylation profiles of the brain-derived neurotrophic factor (BDNF) gene as a potent diagnostic biomarker in major depression. PLoS One, 6, 2011, e23881.
17. Imai, Y., Ibata, I., Ito, D., Ohsawa, K., Kohsaka, S., A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem. Biophys. Res. Commun. 224 (1996), 855–862.
18. Ito, D., Imai, Y., Ohsawa, K., Nakajima, K., Fukuuchi, Y., Kohsaka, S., Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res. Mol. Brain Res. 57 (1998), 1–9.
19. Kauer-Sant'Anna, M., Kapczinski, F., Andreazza, A.C., Bond, D.J., Lam, R.W., Young, L.T., Yatham, L.N., Brain-derived neurotrophic factor and inflammatory markers in patients with early- vs. late-stage bipolar disorder. Int. J. Neuropsychopharmacol. 12 (2009), 447–458.
20. Kohda, K., Jinde, S., Iwamoto, K., Bundo, M., Kato, N., Kato, T., Maternal separation stress drastically decreases expression of transthyretin in the brains of adult rat offspring. Int. J. Neuropsychopharmacol. 9 (2006), 201–208.
21. 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.
22. 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.
23. Lawson, L.J., Perry, V.H., Dri, P., Gordon, S., Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39 (1990), 151–170.
24. Lee, C., Kim, B.G., Kim, J.H., Chun, J., Im, J.P., Kim, J.S., Sodium butyrate inhibits the NF-kappa B signaling pathway and histone deacetylation, and attenuates experimental colitis in an IL-10 independent manner. Int. Immunopharmacol. 51 (2017), 47–56.
25. Lin, H., Geng, X., Dang, W., Wu, B., Dai, Z., Li, Y., Yang, Y., Zhang, H., Shi, J., Molecular mechanisms associated with the antidepressant effects of the class I histone deacetylase inhibitor MS-275 in the rat ventrolateral orbital cortex. Brain Res. 1447 (2012), 119–125.
26. Liu, Y., Beyer, A., Aebersold, R., On the dependency of cellular protein levels on mRNA abundance. Cell 165 (2016), 535–550.
27. Lu, N., Wang, L., Cao, H., Liu, L., Van Kaer, L., Washington, M.K., Rosen, M.J., Dube, P.E., Wilson, K.T., Ren, X., Hao, X., Polk, D.B., Yan, F., Activation of the epidermal growth factor receptor in macrophages regulates cytokine production and experimental colitis. J. Immunol. 192 (2014), 1013–1023.
28. Machado, R.A., Constantino Lde, S., Tomasi, C.D., Rojas, H.A., Vuolo, F.S., Vitto, M.F., Cesconetto, P.A., de Souza, C.T., Ritter, C., Dal-Pizzol, F., Sodium butyrate decreases the activation of NF-kappaB reducing inflammation and oxidative damage in the kidney of rats subjected to contrast-induced nephropathy. Nephrol. Dial. Transplant. 27 (2012), 3136–3140.
29. Mathew, S.J., Treatment-resistant depression: recent developments and future directions. Depress Anxiety 25 (2008), 989–992.
30. McGowan, P.O., Sasaki, A., D'Alessio, A.C., Dymov, S., Labonte, B., Szyf, M., Turecki, G., Meaney, M.J., Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12 (2009), 342–348.
31. Mello, B.S., Monte, A.S., McIntyre, R.S., Soczynska, J.K., Custodio, C.S., Cordeiro, R.C., Chaves, J.H., Vasconcelos, S.M., Nobre, H.V. Jr., Florenco de Sousa, F.C., Hyphantis, T.N., Carvalho, A.F., Macedo, D.S., Effects of doxycycline on depressive-like behavior in mice after lipopolysaccharide (LPS) administration. J. Psychiatr. Res. 47 (2013), 1521–1529.
32. Monteggia, L.M., Barrot, M., Powell, C.M., Berton, O., Galanis, V., Gemelli, T., Meuth, S., Nagy, A., Greene, R.W., Nestler, E.J., Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc. Natl. Acad. Sci. U.S.A. 101 (2004), 10827–10832.
33. Nibuya, M., Morinobu, S., Duman, R.S., Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neurosci. 15 (1995), 7539–7547.
34. Ohgidani, M., Kato, T.A., Sagata, N., Hayakawa, K., Shimokawa, N., Sato-Kasai, M., Kanba, S., TNF-alpha from hippocampal microglia induces working memory deficits by acute stress in mice. Brain Behav. Immun., 2015.
35. Ohsawa, K., Imai, Y., Kanazawa, H., Sasaki, Y., Kohsaka, S., Involvement of Iba1 in membrane ruffling and phagocytosis of macrophages/microglia. J. Cell Sci. 113:Pt 17 (2000), 3073–3084.
36. Payne, S.H., The utility of protein and mRNA correlation. Trends Biochem. Sci. 40 (2015), 1–3.
37. Peng, G.S., Li, G., Tzeng, N.S., Chen, P.S., Chuang, D.M., Hsu, Y.D., Yang, S., Hong, J.S., Valproate pretreatment protects dopaminergic neurons from LPS-induced neurotoxicity in rat primary midbrain cultures: role of microglia. Brain Res. Mol. Brain Res. 134 (2005), 162–169.
38. Peters, V.A., Joesting, J.J., Freund, G.G., IL-1 receptor 2 (IL-1R2) and its role in immune regulation. Brain Behav. Immun. 32 (2013), 1–8.
39. Porsolt, R.D., Bertin, A., Jalfre, M., Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 229 (1977), 327–336.
40. Post, R.M., Fleming, J., Kapczinski, F., Neurobiological correlates of illness progression in the recurrent affective disorders. J. Psychiatr. Res. 46 (2012), 561–573.
41. Qin, L., Wu, X., Block, M.L., Liu, Y., Breese, G.R., Hong, J.S., Knapp, D.J., Crews, F.T., Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55 (2007), 453–462.
42. Raison, C.L., Capuron, L., Miller, A.H., Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol. 27 (2006), 24–31.
43. Sasaki, Y., Ohsawa, K., Kanazawa, H., Kohsaka, S., Imai, Y., Iba1 is an actin-cross-linking protein in macrophages/microglia. Biochem. Biophys. Res. Commun. 286 (2001), 292–297.
44. Schramm, N.L., McDonald, M.P., Limbird, L.E., The alpha(2a)-adrenergic receptor plays a protective role in mouse behavioral models of depression and anxiety. J. Neurosci. 21 (2001), 4875–4882.
45. Schroeder, F.A., Lin, C.L., Crusio, W.E., Akbarian, S., Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol. Psychiatry 62 (2007), 55–64.
46. Shebl, F.M., Pinto, L.A., Garcia-Pineres, A., Lempicki, R., Williams, M., Harro, C., Hildesheim, A., Comparison of mRNA and protein measures of cytokines following vaccination with human papillomavirus-16 L1 virus-like particles. Cancer Epidemiol. Biomarkers Prev. 19 (2010), 978–981.
47. Siwek, M., Sowa-Kucma, M., Dudek, D., Styczen, K., Szewczyk, B., Kotarska, K., Misztakk, P., Pilc, A., Wolak, M., Nowak, G., Oxidative stress markers in affective disorders. Pharmacol. Rep. 65 (2013), 1558–1571.
48. Sullivan, G.M., Mann, J.J., Oquendo, M.A., Lo, E.S., Cooper, T.B., Gorman, J.M., Low cerebrospinal fluid transthyretin levels in depression: correlations with suicidal ideation and low serotonin function. Biol. Psychiatry 60 (2006), 500–506.
49. Takeuchi, F., Isono, M., Katsuya, T., Yamamoto, K., Yokota, M., Sugiyama, T., Nabika, T., Fujioka, A., Ohnaka, K., Asano, H., Yamori, Y., Yamaguchi, S., Kobayashi, S., Takayanagi, R., Ogihara, T., Kato, N., Blood pressure and hypertension are associated with 7 loci in the Japanese population. Circulation 121 (2010), 2302–2309.
50. Tsankova, N., Renthal, W., Kumar, A., Nestler, E.J., Epigenetic regulation in psychiatric disorders. Nat. Rev. Neurosci. 8 (2007), 355–367.
51. Weaver, I.C., Cervoni, N., Champagne, F.A., D'Alessio, A.C., Sharma, S., Seckl, J.R., Dymov, S., Szyf, M., Meaney, M.J., Epigenetic programming by maternal behavior. Nat. Neurosci. 7 (2004), 847–854.
52. Yamawaki, Y., Kimura, H., Hosoi, T., Ozawa, K., MyD88 plays a key role in LPS-induced Stat3 activation in the hypothalamus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298 (2010), R403–R410.
53. Yamawaki, Y., Fuchikami, M., Morinobu, S., Segawa, M., Matsumoto, T., Yamawaki, S., Antidepressant-like effect of sodium butyrate (HDAC inhibitor) and its molecular mechanism of action in the rat hippocampus. World J. Biol. Psychiatry. 13 (2012), 458–467.