Beyond receptors and signaling: Epigenetic factors in the regulation of innate immunity

Immunology and Cell Biology

Volumn 93, Issue 3, 2015, Pages 233-244

  Mehta, Stuti ^a   Jeffrey, Kate L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; BROMODOMAIN INHIBITOR; DNA; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HISTONE DEMETHYLASE; HISTONE METHYLTRANSFERASE; OXYGENASE INHIBITOR; TOLL LIKE RECEPTOR 4; UNTRANSLATED RNA; HISTONE;

ADAPTIVE IMMUNITY; ANTIINFLAMMATORY ACTIVITY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CPG ISLAND; DNA METHYLATION; ENHANCER REGION; ENZYME ACTIVE SITE; EPIGENETICS; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE PHOSPHORYLATION; HISTONE UBIQUITINATION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL MEMORY; IMMUNOREGULATION; INNATE IMMUNITY; MACROPHAGE; NONHUMAN; PROMOTER REGION; PROTEIN DOMAIN; REVIEW; TRANSCRIPTION ELONGATION; TRANSCRIPTION REGULATION; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLULAR MICROENVIRONMENT; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTONES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; IMMUNOMODULATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, UNTRANSLATED; SIGNAL TRANSDUCTION;

EID: 84925039208     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2014.101     Document Type: Review

References (109)

1. Hargreaves DC, Horng T, Medzhitov R. Control of inducible gene expression by signaldependent transcriptional elongation. Cell 2009; 138: 129-145
2. Fang TC, Schaefer U, Mecklenbrauker I, Stienen A, Dewell S, Chen MS, et al. Histone H3 lysine 9 di-methylation as an epigenetic signature of the interferon response. J Exp Med 2012; 209: 661-669
3. Foster SL, Hargreaves DC, Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 2007; 447: 972-978
4. Ostuni R, Piccolo V, Barozzi I, Polletti S, Termanini A, Bonifacio S, et al. Latent enhancers activated by stimulation in differentiated cells. Cell 2013; 152: 157-171
5. Cheng SC, Quintin J, Cramer RA, Shepardson KM, Saeed S, Kumar V, et al. mTORand HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 2014; 345: 1250684
6. Quintin J, Saeed S, Martens JH, Giamarellos-Bourboulis EJ, Ifrim DC, Logie C, et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 2012; 12: 223-232
7. Kleinnijenhuis J, Quintin J, Preijers F, Joosten LA, Ifrim DC, Saeed S, et al. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc Natl Acad Sci USA 2012; 109: 17537-17542
8. Carpenter S, Aiello D, Atianand MK, Ricci EP, Gandhi P, Hall LL, et al. A long noncoding RNA mediates both activation and repression of immune response genes. Science 2013; 341: 789-792
9. Jenuwein T, Allis CD. Translating the histone code. Science 2001; 293: 1074-1080
10. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012; 13: 484-492
11. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324: 930-935
12. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011; 333: 1300-1303
13. Tan M, Luo H, Lee S, Jin F, Yang JS, Montellier E, et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 2011; 146: 1016-1028
14. Ram O, Goren A, Amit I, Shoresh N, Yosef N, Ernst J, et al. Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells. Cell 2011; 147: 1628-1639
15. Greer EL, Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 2012; 13: 343-357
16. Gaffney DJ, McVicker G, Pai AA, Fondufe-Mittendorf YN, Lewellen N, Michelini K, et al. Controls of nucleosome positioning in the human genome. PLoS Genet 2012; 8: e1003036
17. Sarai N, Nimura K, Tamura T, Kanno T, Patel MC, Heightman TD, et al. WHSC1 links transcription elongation to HIRA-mediated histone H3.3 deposition. EMBO J 2013; 32: 2392-2406
18. Trojer P, Reinberg D. Histone lysine demethylases and their impact on epigenetics. Cell 2006; 125: 213-217
19. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, Natoli G. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycombmediated gene silencing. Cell 2007; 130: 1083-1094
20. De Santa F, Narang V, Yap ZH, Tusi BK, Burgold T, Austenaa L, et al. Jmjd3 contributes to the control of gene expression in LPS-Activated macrophages. EMBO J2009; 28: 3341-3352
21. Satoh T, Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, Kumagai Y, et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol 2010; 11: 936-944
22. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 2001; 292: 110-113
23. Saccani S, Natoli G. Dynamic changes in histone H3 Lys 9 methylation occurring at tightly regulated inducible inflammatory genes. Genes Dev 2002; 16: 2219-2224
24. Garber M, Yosef N, Goren A, Raychowdhury R, Thielke A, Guttman M, et al. A highthroughput chromatin immunoprecipitation approach reveals principles of dynamic gene regulation in mammals. Mol Cell 2012; 47: 810-822
25. Nicodeme E, Jeffrey KL, Schaefer U, Beinke S, Dewell S, Chung CW, et al. Suppression of inflammation by a synthetic histone mimic. Nature 2010; 468: 1119-1123
26. Filippakopoulos P, Picaud S, Mangos M, Keates T, Lambert JP, Barsyte-Lovejoy D, et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 2012; 149: 214-231
27. Jang MK, Mochizuki K, Zhou M, Jeong HS, Brady JN, Ozato K. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol Cell 2005; 19: 523-534
28. Patel MC, Debrosse M, Smith M, Dey A, Huynh W, Sarai N, et al. BRD4 coordinates recruitment of pause release factor P-TEFb and the pausing complex NELF/DSIF to regulate transcription elongation of interferon-stimulated genes. Mol Cell Biol 2013; 33: 2497-2507
29. Huang B, Yang XD, Zhou MM, Ozato K, Chen LF. Brd4 coactivates transcriptional activation of NF-kappaB via specific binding to acetylated RelA. Mol Cell Biol 2009; 29: 1375-1387
30. Dawson MA, Prinjha RK, Dittmann A, Giotopoulos G, Bantscheff M, Chan WI, et al. Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 2011; 478: 529-533
31. Carpenter S, Ricci EP, Mercier BC, Moore MJ, Fitzgerald KA. Post-Transcriptional regulation of gene expression in innate immunity. Nat Rev Immunol 2014; 14: 361-376
32. Peng X, Gralinski L, Armour CD, Ferris MT, Thomas MJ, Proll S, et al. Unique signatures of long noncoding RNA expression in response to virus infection and altered innate immune signaling. MBio 2010; 1: pii: e00206-10
33. Kambara H, Niazi F, Kostadinova L, Moonka DK, Siegel CT, Post AB, et al. Negative regulation of the interferon response by an interferon-induced long non-coding RNA. Nucleic acids Res 2014; 42: 10668-10680
34. Ramirez-Carrozzi VR, Braas D, Bhatt DM, Cheng CS, Hong C, Doty KR, et al. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell 2009; 138: 114-128
35. Ramirez-Carrozzi VR, Nazarian AA, Li CC, Gore SL, Sridharan R, Imbalzano AN, et al. Selective and antagonistic functions of SWI/SNF and Mi-2beta nucleosome remodeling complexes during an inflammatory response. Genes Dev 2006; 20: 282-296
36. Boehm T, McCurley N, Sutoh Y, Schorpp M, Kasahara M, Cooper MD. VLR-based adaptive immunity. Annu Rev Immunol 2012; 30: 203-220
37. Kurtz J. Specific memory within innate immune systems. Trends Immunol 2005; 26: 186-192
38. Sun JC, Ugolini S, Vivier E. Immunological memory within the innate immune system. EMBO J 2014; 33: 1295-1303
39. Sun JC, Beilke JN, Lanier LL. Immune memory redefined: characterizing the longevity of natural killer cells. Immunol Rev 2010; 236: 83-94
40. Narni-Mancinelli E, Campisi L, Bassand D, Cazareth J, Gounon P, Glaichenhaus N, et al. Memory CD8+ T cells mediate antibacterial immunity via CCL3 activation of TNF/ROI+ phagocytes. J Exp Med 2007; 204: 2075-2087
41. Jeffrey K. Rechallenging immunological memory. Nat Med 2007; 13: 1142
42. Soudja SM, Chandrabos C, Yakob E, Veenstra M, Palliser D, Lauvau G. Memory-T-cellderived interferon-gamma instructs potent innate cell activation for protective immunity. Immunity 2014; 40: 974-988
43. Strutt TM, McKinstry KK, Dibble JP, Winchell C, Kuang Y, Curtis JD, et al. Memory CD4+ T cells induce innate responses independently of pathogen. Nat Med 2010; 16: 558-564 1p following 564
44. Schenkel JM, Fraser KA, Beura LK, Pauken KE, Vezys V, Masopust D. Resident memory CD8 T cells trigger protective innate and adaptive immune responses. Science 2014; 346: 98-101
45. Duggan JM, You D, Cleaver JO, Larson DT, Garza RJ, Guzman Pruneda FA, et al. Synergistic interactions of TLR2/6 and TLR9 induce a high level of resistance to lung infection in mice. J Immunol 2011; 186: 5916-5926
46. Tuvim MJ, Gilbert BE, Dickey BF, Evans SE. Synergistic TLR2/6 and TLR9 activation protects mice against lethal influenza pneumonia. PLoS ONE 2012; 7: e30596
47. Mishra PK, Patel N, Wu W, Bleich D, Gause WC. Prevention of type 1 diabetes through infection with an intestinal nematode parasite requires IL-10 in the absence of a Th2-Type response. Mucosal Immunol 2013; 6: 297-308
48. Saeed S, Quintin J, Kerstens HH, Rao NA, Aghajanirefah A, Matarese F, et al. Epigenetic programming of monocyte-To-macrophage differentiation and trained innate immunity. Science 2014; 345: 1251086
49. Kaelin WG Jr, McKnight SL. Influence of metabolism on epigenetics and disease. Cell 2013; 153: 56-69
50. Cyr AR, Domann FE. The redox basis of epigenetic modifications: from mechanisms to functional consequences. Antioxid Redox Signal 2011; 15: 551-589
51. Everts B, Amiel E, Huang SC, Smith AM, Chang CH, Lam WY, et al. TLR-driven early glycolytic reprogramming via the kinases TBK1-IKKvarepsilon supports the anabolic demands of dendritic cell activation. Nat Immunol 2014; 15: 323-332
52. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, et al. Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature 2013; 496: 238-242
53. Davies LC, Jenkins SJ, Allen JE, Taylor PR. Tissue-resident macrophages. Nat Immunol 2013; 14: 986-995
54. Abreu MT, Thomas LS, Arnold ET, Lukasek K, Michelsen KS, Arditi M. TLR signaling at the intestinal epithelial interface. J Endotoxin Res 2003; 9: 322-330
55. Abreu MT, Vora P, Faure E, Thomas LS, Arnold ET, Arditi M. Decreased expression of toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. J Immunol 2001; 167: 1609-1616
56. Hamon MA, Batsche E, Regnault B, Tham TN, Seveau S, Muchardt C, et al. Histone modifications induced by a family of bacterial toxins. Proc Natl Acad Sci USA 2007; 104: 13467-13472
57. Hamon MA, Cossart P. K+ efflux is required for histone H3 dephosphorylation by Listeria monocytogenes listeriolysin O and other pore-forming toxins. Infect Immun 2011; 79: 2839-2846
58. Eskandarian HA, Impens F, Nahori M-A, Soubigou G, Coppée J-Y, Cossart P, et al. A role for SIRT2-dependent histone H3K18 deacetylation in bacterial infection. Science 2013; 341: 1238858
59. Arbibe L, Kim DW, Batsche E, Pedron T, Mateescu B, Muchardt C, et al. An injected bacterial effector targets chromatin access for transcription factor NF-kappaB to alter transcription of host genes involved in immune responses. Nat Immunol 2007; 8: 47-56
60. Leng J, Butcher BA, Egan CE, Abi Abdallah DS, Denkers EY. Toxoplasma gondii prevents chromatin remodeling initiated by TLR-Triggered macrophage activation. J Immunol 2009; 182: 489-497
61. Leng J, Denkers EY. Toxoplasma gondii inhibits covalent modification of histone H3 at the IL-10 promoter in infected macrophages. PLoS ONE 2009; 4: e7589
62. Pennini ME, Pai RK, Schultz DC, Boom WH, Harding CV. Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-gamma-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J Immunol. 2006; 176: 4323-4330
63. Wang Y, Curry HM, Zwilling BS, Lafuse WP. Mycobacteria inhibition of IFN-gamma induced HLA-DR gene expression by up-regulating histone deacetylation at the promoter region in human THP-1 monocytic cells. J Immunol 2005; 174: 5687-5694
64. Lebreton A, Job V, Ragon M, Le Monnier A, Dessen A, Cossart P, et al. Structural basis for the inhibition of the chromatin repressor BAHD1 by the bacterial nucleomodulin LntA. MBio 2014; 5: e00775-13
65. Lebreton A, Lakisic G, Job V, Fritsch L, Tham TN, Camejo A, et al. A bacterial protein targets the BAHD1 chromatin complex to stimulate type III interferon response. Science 2011; 331: 1319-1321
66. Rolando M, Sanulli S, Rusniok C, Gomez-Valero L, Bertholet C, Sahr T, et al. Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe 2013; 13: 395-405
67. Mujtaba S, Winer BY, Jaganathan A, Patel J, Sgobba M, Schuch R, et al. Anthrax SET protein: a potential virulence determinant that epigenetically represses NF-kappaB activation in infected macrophages. J Biol Chem 2013; 288: 23458-23472
68. Rennoll-Bankert KE, Dumler JS. Lessons from Anaplasma phagocytophilum: chromatin remodeling by bacterial effectors. Infect Disord Drug Targets 2012; 12: 380-387
69. Garcia-Garcia JC, Rennoll-Bankert KE, Pelly S, Milstone AM, Dumler JS. Silencing of host cell CYBB gene expression by the nuclear effector anka of the intracellular pathogen Anaplasma phagocytophilum. Infect Immun 2009; 77: 2385-2391
70. Marazzi I, Ho JSY, Kim J, Manicassamy B, Dewell S, Albrecht RA, et al. Suppression of the antiviral response by an influenza histone mimic. Nature 2012; 483: 428-433
71. Shanmugam MK, Sethi G. Role of epigenetics in inflammation-Associated diseases. Subcell Biochem 2013; 61: 627-657
72. Liu A, La Cava A. Epigenetic dysregulation in systemic lupus erythematosus. Autoimmunity 2014; 47: 215-219
73. Rakyan VK, Beyan H, Down TA, Hawa MI, Maslau S, Aden D, et al. Identification of type 1 diabetes-Associated DNA methylation variable positions that precede disease diagnosis. PLoS Genet 2011; 7: e1002300
74. Javierre BM, Fernandez AF, Richter J, Al-Shahrour F, Martin-Subero JI, Rodriguez-Ubreva J, et al. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res 2010; 20: 170-179
75. Runyon RS, Cachola LM, Rajeshuni N, Hunter T, Garcia M, Ahn R, et al. Asthma discordance in twins is linked to epigenetic modifications of T cells. PLoS ONE 2012; 7: e48796
76. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, et al. Genome-wide meta-Analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 2010; 42: 1118-1125
77. Sawcer S, Hellenthal G, Pirinen M, Spencer CC, Patsopoulos NA, Moutsianas L, et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature 2011; 476: 214-219
78. Pointon JJ, Harvey D, Karaderi T, Appleton LH, Farrar C, Wordsworth BP. The histone demethylase JARID1A is associated with susceptibility to ankylosing spondylitis. Genes Immun 2011; 12: 395-398
79. Kruidenier L, Chung CW, Cheng Z, Liddle J, Che K, Joberty G, et al. A selective jumonji H3K27 demethylase inhibitor modulates the proinflammatory macrophage response. Nature 2012; 488: 404-408
80. Stasevich TJ, Hayashi-Takanaka Y, Sato Y, Maehara K, Ohkawa Y, Sakata-Sogawa K, et al. Regulation of RNA polymerase II activation by histone acetylation in single living cells. Nature 2014 advance online publication
81. Segain JP, de la Blétière DR, Bourreille A, Leray V, Gervois N, Rosales C, et al. Butyrate inhibits inflammatory responses through NF?B inhibition: implications for Crohn's disease. Gut 2000; 47: 397-403
82. Luhrs H, Gerke T, Muller JG, Melcher R, Schauber J, Boxberge F, et al. Butyrate inhibits NF-kappaB activation in lamina propria macrophages of patients with ulcerative colitis. Scand J Gastroenterol 2002; 37: 458-466
83. Vojinovic J, Damjanov N. HDAC inhibition in rheumatoid arthritis and juvenile idiopathic arthritis. Mol Med. 2011; 17: 397-403
84. Chung YL, Lee MY, Wang AJ, Yao LF. A therapeutic strategy uses histone deacetylase inhibitors to modulate the expression of genes involved in the pathogenesis of rheumatoid arthritis. Mol Ther 2003; 8: 707-717
85. Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci USA 2014; 111: 2247-2252
86. Adcock IM. HDAC inhibitors as anti-inflammatory agents. Br J Pharmacol 2007; 150: 829-831
87. Seal J, Lamotte Y, Donche F, Bouillot A, Mirguet O, Gellibert F, et al. Identification of a novel series of BET family bromodomain inhibitors: binding mode and profile of I-BET151 (GSK1210151A). Bioorg Med Chem Lett 2012; 22: 2968-2972
88. Belkina AC, Nikolajczyk BS, Denis GV. BET protein function is required for inflammation: Brd2 genetic disruption and BET inhibitor JQ1 impair mouse macrophage inflammatory responses. J Immunol 2013; 190: 3670-3678
89. Zhang G, Plotnikov AN, Rusinova E, Shen T, Morohashi K, Joshua J, et al. Structureguided design of potent diazobenzene inhibitors for the BET bromodomains. J Med Chem 2013; 56: 9251-9264
90. Bisgrove DA, Mahmoudi T, Henklein P, Verdin E. Conserved P-TEFb-interacting domain of BRD4 inhibits HIV transcription. Proc Natl Acad Sci USA 2007; 104: 13690-13695
91. Kundu M, Guermah M, Roeder RG, Amini S, Khalili K. Interaction between cell cycle regulator, E2F-1, and NF-kappaB mediates repression of HIV-1 gene transcription. J Biol Chem 1997; 272: 29468-29474
92. Zhu J, Gaiha GD, John SP, Pertel T, Chin CR, Gao G, et al. Reactivation of latent HIV-1 by inhibition of BRD4. Cell reports 2012; 2: 807-816
93. Halper-Stromberg A, Lu C-L, Klein F, Horwitz Joshua A, Bournazos S, Nogueira L, et al. Broadly neutralizing antibodies and viral inducers decrease rebound from HIV-1 latent reservoirs in humanized mice. Cell 2014; 158: 989-999
94. Pennini ME, Liu Y, Yang J, Croniger CM, Boom WH, Harding CV. CCAAT/enhancerbinding protein beta and delta binding to CIITA promoters is associated with the inhibition of CIITA expression in response to Mycobacterium tuberculosis 19-kDa lipoprotein. J Immunol 2007; 179: 6910-6918
95. Pennini ME, Perrinet S, Dautry-Varsat A, Subtil A. Histone methylation by NUE, a novel nuclear effector of the intracellular pathogen Chlamydia trachomatis. PLoS Pathog 2010; 6: e1000995
96. Garcia-Garcia JC, Barat NC, Trembley SJ, Dumler JS. Epigenetic silencing of host cell defense genes enhances intracellular survival of the rickettsial pathogen Anaplasma phagocytophilum. PLoS Pathog 2009; 5: e1000488
97. Lang C, Hildebrandt A, Brand F, Opitz L, Dihazi H, Luder CG. Impaired chromatin remodelling at STAT1-regulated promoters leads to global unresponsiveness of Toxoplasma gondii-infected macrophages to IFN-gamma. PLoS Pathog 2012; 8: e1002483
98. Agarwal S, Agarwal S, Jin H, Pancholi P, Pancholi V. Serine/threonine phosphatase (SP-STP), secreted from Streptococcus pyogenes, is a pro-Apoptotic protein. J Biol Chem 2012; 287: 9147-9167
99. Glauben R, Batra A, Fedke I, Zeitz M, Lehr HA, Leoni F, et al. Histone hyperacetylation is associated with amelioration of experimental colitis in mice. J Immunol 2006; 176: 5015-5022
100. Lin HS, Hu CY, Chan HY, Liew YY, Huang HP, Lepescheux L, et al. Anti-rheumatic activities of histone deacetylase (HDAC) inhibitors in vivo in collagen-induced arthritis in rodents. Br J Pharmacol 2007; 150: 862-872
101. Chung Y-L, Lee M-Y, Wang A-J, Yao L-F. A therapeutic strategy uses histone deacetylase inhibitors to modulate the expression of genes involved in the pathogenesis of rheumatoid arthritis. Mol Ther 2003; 8: 707-717
102. Hsieh IN, Liou JP, Lee HY, Lai MJ, Li YH, Yang CR. Preclinical anti-Arthritic study and pharmacokinetic properties of a potent histone deacetylase inhibitor MPT0G009. Cell Death Dis 2014; 5: e1166
103. Hara N, Alkanani AK, Dinarello CA, Zipris D. Histone deacetylase inhibitor suppresses virus-induced proinflammatory responses and type 1 diabetes. J Mol Med (Berl) 2014; 92: 93-102
104. Zhang Z-Y, Schluesener HJ. HDAC inhibitor MS-275 attenuates the inflammatory reaction in rat experimental autoimmune prostatitis. Prostate 2012; 72: 90-99
105. Cantley MD, Bartold PM, Marino V, Fairlie DP, Le GT, Lucke AJ, et al. Histone deacetylase inhibitors and periodontal bone loss. J Periodontal Res 2011; 46: 697-703
106. Gillespie J, Savic S, Wong C, Hempshall A, Inman M, Emery P, et al. Histone deacetylases are dysregulated in rheumatoid arthritis and a novel histone deacetylase 3-selective inhibitor reduces interleukin-6 production by peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Rheum 2012; 64: 418-422
107. Kruidenier L, Chung C-w, Cheng Z, Liddle J, Che K, Joberty G, et al. A selective jumonji H3K27 demethylase inhibitor modulates the proinflammatory macrophage response. Nature 2012; 488: 404-408
108. Zhang G, Liu R, Zhong Y, Plotnikov AN, Zhang W, Zeng L, et al. Down-regulation of NF-?B transcriptional activity in HIV-Associated kidney disease by BRD4 inhibition. J Biol Chem 2012; 287: 28840-28851
109. Zhang ZY, Zhang Z, Schluesener HJ. MS-275, an histone deacetylase inhibitor, reduces the inflammatory reaction in rat experimental autoimmune neuritis. Neuroscience 2010; 169: 370-377