Histone deacetylase inhibitors suppress immune activation in primary mouse microglia

Journal of Neuroscience Research

Volumn 91, Issue 9, 2013, Pages 1133-1142

  Kannan, Vishnu ^a   Brouwer, Nieske ^a   Hanisch, Uwe Karsten ^b   Regen, Tommy ^b   Eggen, Bart J L ^a   Boddeke, Hendrikus W G M ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Innate immunity; Lipopolysaccharide; M1 M2 activation markers; Primary microglia and astrocytes

Indexed keywords

GAMMA INTERFERON; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL CULTURE; CELL FUNCTION; CELL MIGRATION; CELL STIMULATION; COMPETITIVE INHIBITION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INNATE IMMUNITY; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

INNATE IMMUNITY; LIPOPOLYSACCHARIDE; M1-M2 ACTIVATION MARKERS; PRIMARY MICROGLIA AND ASTROCYTES;

ANIMALS; ANTIGENS, SURFACE; ASTROCYTES; BRAIN; CELLS, CULTURED; CHEMOTACTIC FACTORS; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HYDROXAMIC ACIDS; INTERFERON-GAMMA; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICROGLIA; RNA, MESSENGER; SIRTUIN 1; SIRTUIN 2; TIME FACTORS;

EID: 84880514164     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23221     Document Type: Article

References (50)

1. Aloisi F. 2001. Immune function of microglia. Glia 36:165-179.
2. Ashburner BP, Westerheide SD, Baldwin AS Jr. 2001. The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol Cell Biol 21:7065-7077.
3. Aung HT, Schroder K, Himes SR, Brion K, van Zuylen W, Trieu A, Suzuki H, Hayashizaki Y, Hume DA, Sweet MJ, Ravasi T. 2006. LPS regulates proinflammatory gene expression in macrophages by altering histone deacetylase expression. FASEB J 20:1315-1327.
4. Beurel E. 2011. HDAC6 regulates LPS-tolerance in astrocytes. PLoS One 6:e25804.
5. Biber K, Sauter A, Brouwer N, Copray SC, Boddeke HW. 2001. Ischemia-induced neuronal expression of the microglia attracting chemokine secondary lymphoid-tissue chemokine (SLC). Glia 34:121-133.
6. Block ML, Hong JS. 2005. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 76:77-98.
7. Bode KA, Schroder K, Hume DA, Ravasi T, Heeg K, Sweet MJ, Dalpke AH. 2007. Histone deacetylase inhibitors decrease Toll-like receptor-mediated activation of proinflammatory gene expression by impairing transcription factor recruitment. Immunology 122:596-606.
8. Chen Z, Jalabi W, Shpargel KB, Farabaugh KT, Dutta R, Yin X, Kidd GJ, Bergmann CC, Stohlman SA, Trapp BD. 2012. Lipopolysaccharide-induced microglial activation and neuroprotection against experimental brain injury is independent of hematogenous TLR4. J Neurosci 32:11706-11715.
9. Choo QY, Ho PC, Tanaka Y, Lin HS. 2010. Histone deacetylase inhibitors MS-275 and SAHA induced growth arrest and suppressed lipopolysaccharide-stimulated NF-kappaB p65 nuclear accumulation in human rheumatoid arthritis synovial fibroblastic E11 cells. Rheumatology 49:1447-1460.
10. Chung IY, Benveniste EN. 1990. Tumor necrosis factor-alpha production by astrocytes. Induction by lipopolysaccharide, 1990 IFN-gamma, and IL-1 beta. J Immunol 15:2999-3007.
11. Colton CA. 2009. Heterogeneity of microglial activation in the innate immune response in the brain. J Neuroimmune Pharmacol 4:399-418.
12. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB. 2005. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-758.
13. de Haas AH, Boddeke HW, Biber K. 2008. Region-specific expression of immunoregulatory proteins on microglia in the healthy CNS. Glia 56:888-894.
14. de Jong EK, Dijkstra IM, Hensens M, Brouwer N, van Amerongen M, Liem RS, Boddeke HW, Biber K. 2005. Vesicle-mediated transport and release of CCL21 in endangered neurons: a possible explanation for microglia activation remote from a primary lesion. J Neurosci 25:7548-7557.
15. Dijkstra IM, Hulshof S, van der Valk P, Boddeke HW, Biber K. 2004. Cutting edge: activity of human adult microglia in response to CC chemokine ligand 21. J Immunol 172:2744-2747.
16. Dokmanovic M, Clarke C, Marks PA. 2007. Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 5:981-989.
17. Dong Y, Benveniste EN. 2001. Immune function of astrocytes. Glia 36:180-190.
18. Faraco G, Pittelli M, Cavone L, Fossati S, Porcu M, Mascagni P, Fossati G, Moroni F, Chiarugi A. 2009. Histone deacetylase (HDAC) inhibitors reduce the glial inflammatory response in vitro and in vivo. Neurobiol Dis 36:269-279.
19. Gonzalez-Scarano F, Baltuch G. 1999. Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22:219-240.
20. Halili MA, Andrews MR, Labzin LI, Schroder K, Matthias G, Cao C, Lovelace E, Reid RC, Le GT, Hume DA, Irvine KM, Matthias P, Fairlie DP, Sweet MJ. 2010. Differential effects of selective HDAC inhibitors on macrophage inflammatory responses to the Toll-like receptor 4 agonist LPS. J Leukoc Biol 87:1103-1114.
21. Han SB, Lee JK. 2009. Anti-inflammatory effect of trichostatin-A on murine bone marrow-derived macrophages. Arch Pharm Res 32:613-624.
22. Hanisch UK, Kettenmann H. 2007. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394.
23. Holling TM, Bergevoet MW, Wilson L, Van Eggermond MC, Schooten E, Steenbergen RD, Snijders PJ, Jager MJ, Van den Elsen PJ. 2007. A role for EZH2 in silencing of IFN-gamma inducible MHC2TA transcription in uveal melanoma. J Immunol 179:5317-5325.
24. Huuskonen J, Suuronen T, Nuutinen T, Kyrylenko S, Salminen A. 2004. Regulation of microglial inflammatory response by sodium butyrate and short-chain fatty acids. Br J Pharmacol 141:874-880.
25. Kim SU, de Vellis J. 2005. Microglia in health and disease. J Neurosci Res 81:302-313.
26. Kraft AD, Harry GJ. 2011. Features of microglia and neuroinflammation relevant to environmental exposure and neurotoxicity. Int J Environ Res Public Health 8:2980-3018.
27. Leoni F, Zaliani A, Bertolini G, Porro G, Pagani P, Pozzi P, Dona G, Fossati G, Sozzani S, Azam T, Bufler P, Fantuzzi G, Goncharov I, Kim SH, Pomerantz BJ, Reznikov LL, Siegmund B, Dinarello CA, Mascagni P. 2002. The antitumor histone deacetylase inhibitor suberoylanilide hydroxamic acid exhibits antiinflammatory properties via suppression of cytokines. Proc Natl Acad Sci U S A 99:2995-3000.
28. Li Y, Liu B, Zhao H, Sailhamer EA, Fukudome EY, Zhang X, Kheirbek T, Finkelstein RA, Velmahos GC, deMoya M, Hales CA, Alam HB. 2009. Protective effect of suberoylanilide hydroxamic acid against LPS-induced septic shock in rodents. Shock 32:517-523.
29. Liu J, Casaccia P. 2010. Epigenetic regulation of oligodendrocyte identity. Trends Neurosci 33:193-201.
30. T) method. Methods 25:402-408.
31. Mander P, Brown GC. 2005. Activation of microglial NADPH oxidase is synergistic with glial iNOS expression in inducing neuronal death: a dual-key mechanism of inflammatory neurodegeneration. J Neuroinflamm 2:20.
32. Miller AM, Stella N. 2009. Microglial cell migration stimulated by ATP and C5a involve distinct molecular mechanisms: quantification of migration by a novel near-infrared method. Glia 57:875-883.
33. Mullican SE, Gaddis CA, Alenghat T, Nair MG, Giacomin PR, Everett LJ, Feng D, Steger DJ, Schug J, Artis D, Lazar MA. 2011. Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev 25:2480-2488.
34. Nimmerjahn A, Kirchhoff F, Helmchen F. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314-1318.
35. Ransohoff RM, Brown MA. 2012. Innate immunity in the central nervous system. J Clin Invest 122:1164-1171.
36. Saijo K, Glass CK. 2011. Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol 11:775-787.
37. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, Gage FH, Glass CK. 2009. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137:47-59.
38. Shahbazian MD, Grunstein M. 2007. Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76:75-100.
39. Shakespear MR, Halili MA, Irvine KM, Fairlie DP, Sweet MJ. 2011. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol 32:335-343.
40. Sher F, Boddeke E, Copray S. 2011. Ezh2 expression in astrocytes induces their dedifferentiation toward neural stem cells. Cell Reprogram 13:1-6.
41. Shuttleworth SJ, Bailey SG, Townsend PA. 2010. Histone deacetylase inhibitors: new promise in the treatment of immune and inflammatory diseases. Curr Drug Targets 11:1430-1438.
42. Suuronen T, Huuskonen J, Pihlaja R, Kyrylenko S, Salminen A. 2003. Regulation of microglial inflammatory response by histone deacetylase inhibitors. J Neurochem 87:407-416.
43. Suuronen T, Huuskonen J, Nuutinen T, Salminen A. 2006. Characterization of the pro-inflammatory signaling induced by protein acetylation in microglia. Neurochem Int 49:610-618.
44. Thiagalingam S, Cheng KH, Lee HJ, Mineva N, Thiagalingam A, Ponte JF. 2003. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann N Y Acad Sci 983:84-100.
45. Thurn KT, Thomas S, Moore A, Munster PN. 2011. Rational therapeutic combinations with histone deacetylase inhibitors for the treatment of cancer. Future Oncol 7:263-283.
46. van der Putten C, Zuiderwijk-Sick EA, van Straalen L, de Geus ED, Boven LA, Kondova I, IJzerman AP, Bajramovic JJ. 2009. Differential expression of adenosine A3 receptors controls adenosine A2A receptor-mediated inhibition of TLR responses in microglia. J Immunol 182:7603-7612.
47. Villagra A, Cheng F, Wang HW, Suarez I, Glozak M, Maurin M, Nguyen D, Wright KL, Atadja PW, Bhalla K, Pinilla-Ibarz J, Seto E, Sotomayor EM. 2009. The histone deacetylase HDAC11 regulates the expression of interleukin 10 and immune tolerance. Nat Immunol 10:92-100.
48. Wang H, Cheng F, Woan K, Sahakian E, Merino O, Rock-Klotz J, Vicente-Suarez I, Pinilla-Ibarz J, Wright KL, Seto E, Bhalla K, Villagra A, Sotomayor EM. 2011. Histone deacetylase inhibitor LAQ824 augments inflammatory responses in macrophages through transcriptional regulation of IL-10. J Immunol 186:3986-3996.
49. Wang J, Du JR, Wang Y, Kuang X, Wang CY. 2010. Z-ligustilide attenuates lipopolysaccharide-induced proinflammatory response via inhibiting NF-kappaB pathway in primary rat microglia. Acta Pharmacol Sin 31:791-797.
50. Yao YL, Yang WM. 2011. Beyond histone and deacetylase: an overview of cytoplasmic histone deacetylases and their nonhistone substrates. J Biomed Biotechnol 2011:146493.