11,317
Views
67
CrossRef citations to date
0
Altmetric
Review Article

Epigenetic regulation in bacterial infections: targeting histone deacetylases

&
Pages 336-350 | Received 28 Jun 2017, Accepted 25 Aug 2017, Published online: 03 Oct 2017

References

  • Angiolilli C, Grabiec AM, Ferguson BS, Ospelt C, Malvar Fernandez B, van Es IE, van Baarsen LGM, Gay S, McKinsey TA, Tak PP, et al. 2016. Inflammatory cytokines epigenetically regulate rheumatoid arthritis fibroblast-like synoviocyte activation by suppressing HDAC5 expression. Ann Rheum Dis. 75:430–438.
  • Archin NM, Liberty AL, Kashuba AD, Choudhary SK, Kuruc JD, Crooks AM, Parker DC, Anderson EM, Kearney MF, Strain MC, et al. 2012. Administration of vorinostat disrupts HIV-1 latency in patients on antiretroviral therapy. Nature. 487:482–485.
  • Ariffin JK, das Gupta K, Kapetanovic R, Iyer A, Reid RC, Fairlie DP, Sweet MJ. 2015. Histone deacetylase inhibitors promote mitochondrial reactive oxygen species production and bacterial clearance by human macrophages. Antimicrob Agents Chemother. 60:1521–1529.
  • Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, Rudensky AY. 2013. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 504:451–455.
  • Bandyopadhaya A, Tsurumi A, Maura D, Jeffrey KL, Rahme LG. 2016. A quorum-sensing signal promotes host tolerance training through HDAC1-mediated epigenetic reprogramming. Nat Microbiol. 1:16174.
  • Beier UH, Wang L, Han R, Akimova T, Liu Y, Hancock WW. 2012. Histone deacetylases 6 and 9 and sirtuin-1 control foxp3+ regulatory T cell function through shared and isoform-specific mechanisms. Sci Signal. 5:ra45.
  • Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A. 2009. An operational definition of epigenetics. Genes Dev. 23:781–783.
  • Bierne H, Hamon M, Cossart P. 2012. Epigenetics and bacterial infections. Cold Spring Harb Perspect Med. 2:a010272.
  • Bobetsis YA, Barros SP, Lin DM, Weidman JR, Dolinoy DC, Jirtle RL, Boggess KA, Beck JD, Offenbacher S. 2007. Bacterial infection promotes DNA hypermethylation. J Dent Res. 86:169–174.
  • Cantley MD, Bartold PM, Marino V, Fairlie DP, Le GT, Lucke AJ, Haynes DR. 2011. Histone deacetylase inhibitors and periodontal bone loss. J Periodont Res. 46:697–703.
  • Cantley MD, Dharmapatni AA, Algate K, Crotti TN, Bartold PM, Haynes DR. 2016. Class I and II histone deacetylase expression in human chronic periodontitis gingival tissue. J Periodont Res. 51:143–151.
  • Cardoso F, Castro F, Moreira-Teixeira L, Sousa J, Torrado E, Silvestre R, Castro AG, Saraiva M, Pais TF, Cardona P-J. 2015. Myeloid sirtuin 2 expression does not impact long-term Mycobacterium tuberculosis control. PLoS One. 10:e0131904.
  • Chang M-C, Tsai Y-L, Chen Y-W, Chan C-P, Huang C-F, Lan W-C, Lin C-C, Lan W-H, Jeng J-H. 2013. Butyrate induces reactive oxygen species production and affects cell cycle progression in human gingival fibroblasts. J Periodont Res. 48:66–73.
  • Chen X, Lu Y, Zhang Z, Wang J, Yang H, Liu G. 2015. Intercellular interplay between Sirt1 signalling and cell metabolism in immune cell biology. Immunology. 145:455–467.
  • Cheng CY, Gutierrez NM, Marzuki MB, Lu X, Foreman TW, Paleja B, Lee B, Balachander A, Chen J, Tsenova L, et al. 2017. Host sirtuin 1 regulates mycobacterial immunopathogenesis and represents a therapeutic target against tuberculosis. Sci Immunol. 2:eaaj1789.
  • Choi SW, Braun T, Chang L, Ferrara JLM, Pawarode A, Magenau JM, Hou G, Beumer JH, Levine JE, Goldstein S, et al. 2014. Vorinostat plus tacrolimus and mycophenolate to prevent graft-versus-host disease after related-donor reduced-intensity conditioning allogeneic haemopoietic stem-cell transplantation: a phase 1/2 trial. Lancet Oncol. 15:87–95.
  • Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M. 2009. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 325:834–840.
  • Ciarlo E, Savva A, Roger T. 2013. Epigenetics in sepsis: targeting histone deacetylases. Int J Antimicrob Agents. 42(Suppl): S8–S12.
  • Corrêa-Oliveira R, Fachi JL, Vieira A, Sato FT, Vinolo MAR. 2016. Regulation of immune cell function by short-chain fatty acids. Clin Transl Immunology. 5:e73.
  • Corrêa RO, Vieira A, Sernaglia EM, Lancellotti M, Vieira AT, Avila-Campos MJ, Rodrigues HG, Vinolo MAR. 2017. Bacterial short-chain fatty acid metabolites modulate the inflammatory response against infectious bacteria. Cell Microbiol. 19:e12720.
  • Crotty Alexander LE, Marsh BJ, Timmer AM, Lin AE, Zainabadi K, Czopik A, Guarente L, Nizet V. 2013. Myeloid cell sirtuin-1 expression does not alter host immune responses to Gram-negative endotoxemia or Gram-positive bacterial infection. PLoS One. 8:e84481.
  • Dinarello CA, Fossati G, Mascagni P. 2011. Histone deacetylase inhibitors for treating a spectrum of diseases not related to cancer. Mol Med. 17:333–352.
  • Ding S-Z, Fischer W, Kaparakis-Liaskos M, Liechti G, Merrell DS, Grant PA, Ferrero RL, Crowe SE, Haas R, Hatakeyama M, Goldberg JB. 2010. Helicobacter pylori-induced histone modification, associated gene expression in gastric epithelial cells, and its implication in pathogenesis. PLoS One. 5:e9875.
  • Doss M, White MR, Tecle T, Hartshorn KL. 2010. Human defensins and LL-37 in mucosal immunity. J Leukoc Biol. 87:79–92.
  • Eskandarian HA, Impens F, Nahori M-A, Soubigou G, Coppée J-Y, Cossart P, Hamon MA. 2013. A role for SIRT2-dependent histone H3K18 deacetylation in bacterial infection. Science. 341:1238858.
  • Fehri LF, Rechner C, Janssen S, Mak TN, Holland C, Bartfeld S, Brüggemann H, Meyer TF. 2009. Helicobacter pylori-induced modification of the histone H3 phosphorylation status in gastric epithelial cells reflects its impact on cell cycle regulation. Epigenetics. 4:577–586.
  • Fischer N, Sechet E, Friedman R, Amiot A, Sobhani I, Nigro G, Sansonetti PJ, Sperandio B. 2016. Histone deacetylase inhibition enhances antimicrobial peptide but not inflammatory cytokine expression upon bacterial challenge. Proc Natl Acad Sci USA. 113:E2993–E3001.
  • Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, et al. 2013. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 504:446–450.
  • Ganesan R, Hos NJ, Gutierrez S, Fischer J, Stepek JM, Daglidu E, Krönke M, Robinson N. 2017. Salmonella Typhimurium disrupts Sirt1/AMPK checkpoint control of mTOR to impair autophagy. PLoS Pathog. 13:e1006227.
  • Garcia-Garcia JC, Barat NC, Trembley SJ, Dumler JS. 2009. Epigenetic silencing of host cell defense genes enhances intracellular survival of the rickettsial pathogen Anaplasma phagocytophilum. PLoS Pathog. 5:e1000488.
  • Gardner KE, Allis CD, Strahl BD. 2011. Operating on chromatin, a colorful language where context matters. J Mol Biol. 409:36–46.
  • GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. 2016. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet (London, England). 388:1545–1602.
  • Glaser KB, Staver MJ, Waring JF, Stender J, Ulrich RG, Davidsen SK. 2003. Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. Mol Cancer Ther. 2:151–163.
  • Glozak MA, Sengupta N, Zhang X, Seto E. 2005. Acetylation and deacetylation of non-histone proteins. Gene. 363:15–23.
  • Grabiec AM, Reedquist KA. 2013. The ascent of acetylation in the epigenetics of rheumatoid arthritis. Nat Rev Rheumatol. 9:311–318.
  • Grabiec AM, Tak PP, Reedquist KA. 2008. Targeting histone deacetylase activity in rheumatoid arthritis and asthma as prototypes of inflammatory disease: should we keep our HATs on? Arthritis Res Ther. 10:226.
  • Grabiec AM, Tak PP, Reedquist KA. 2011. Function of histone deacetylase inhibitors in inflammation. Crit Rev Immunol. 31:233–263.
  • Ha S-D, Han CY, Reid C, Kim SO. 2014. HDAC8-mediated epigenetic reprogramming plays a key role in resistance to anthrax lethal toxin-induced pyroptosis in macrophages. J Immunol. 193:1333–1343.
  • Ha S-D, Reid C, Meshkibaf S, Kim SO. 2016. Inhibition of Interleukin 1β (IL-1β) expression by anthrax lethal toxin (LeTx) is reversed by histone deacetylase 8 (HDAC8) inhibition in murine macrophages. J Biol Chem. 291:8745–8755.
  • Hamon MA, Batsché E, Régnault B, Tham TN, Seveau S, Muchardt C, Cossart P. 2007. Histone modifications induced by a family of bacterial toxins. Proc Natl Acad Sci USA. 104:13467–13472.
  • Hamon MA, Cossart P. 2008. Histone modifications and chromatin remodeling during bacterial infections. Cell Host Microbe. 4:100–109.
  • Imai K, Inoue H, Tamura M, Cueno ME, Inoue H, Takeichi O, Kusama K, Saito I, Ochiai K. 2012. The periodontal pathogen Porphyromonas gingivalis induces the Epstein-Barr virus lytic switch transactivator ZEBRA by histone modification. Biochimie. 94:839–846.
  • Imai K, Ochiai K, Okamoto T. 2009. Reactivation of latent HIV-1 infection by the periodontopathic bacterium Porphyromonas gingivalis involves histone modification. J Immunol. 182:3688–3695.
  • Jones PA. 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 13:484–492.
  • Jüngel A, Baresova V, Ospelt C, Simmen BR, Michel BA, Gay RE, Gay S, Seemayer CA, Neidhart M. 2006. Trichostatin A sensitises rheumatoid arthritis synovial fibroblasts for TRAIL-induced apoptosis. Ann Rheum Dis. 65:910–912.
  • Kawabata T, Nishida K, Takasugi K, Ogawa H, Sada K, Kadota Y, Inagaki J, Hirohata S, Ninomiya Y, Makino H. 2010. Increased activity and expression of histone deacetylase 1 in relation to tumor necrosis factor-alpha in synovial tissue of rheumatoid arthritis. Arthritis Res Ther. 12:R133.
  • Kim G-W, Yang X-J. 2011. Comprehensive lysine acetylomes emerging from bacteria to humans. Trends Biochem Sci. 36:211–220.
  • Klein K, Kabala PA, Grabiec AM, Gay RE, Kolling C, Lin L-L, Gay S, Tak PP, Prinjha RK, Ospelt C, Reedquist KA. 2016. The bromodomain protein inhibitor I-BET151 suppresses expression of inflammatory genes and matrix degrading enzymes in rheumatoid arthritis synovial fibroblasts. Ann Rheum Dis. 75:422–429.
  • Krautkramer KA, Rey FE, Denu JM. 2017. Chemical signaling between gut microbiota and host chromatin: what is your gut really saying? J Biol Chem. 292:8582–8593.
  • Li T, Lu Q, Wang G, Xu H, Huang H, Cai T, Kan B, Ge J, Shao F. 2013. SET-domain bacterial effectors target heterochromatin protein 1 to activate host rDNA transcription. EMBO Rep. 14:733–740.
  • Li T, Zhang J, Feng J, Li Q, Wu L, Ye Q, Sun J, Lin Y, Zhang M, Huang R, et al. 2013. Resveratrol reduces acute lung injury in a LPS-induced sepsis mouse model via activation of Sirt1. Mol Med Rep. 7:1889–1895.
  • Li Y, Zhao T, Liu B, Halaweish I, Mazitschek R, Duan X, Alam HB. 2015. Inhibition of histone deacetylase 6 improves long-term survival in a lethal septic model. J Trauma Acute Care Surg. 78:378–385.
  • Liu Q, Liu J, Roschmann KI, van Egmond D, Golebski K, Fokkens W, Wang D, van Drunen C. 2013. Histone deacetylase inhibitors up-regulate LL-37 expression independent of toll-like receptor mediated signalling in airway epithelial cells. J Inflamm. 10:15.
  • Lugrin J, Ciarlo E, Santos A, Grandmaison G, dos Santos I, Le Roy D, Roger T. 2013. The sirtuin inhibitor cambinol impairs MAPK signaling, inhibits inflammatory and innate immune responses and protects from septic shock. Biochim Biophys Acta. 1833:1498–1510.
  • Maekita T, Nakazawa K, Mihara M, Nakajima T, Yanaoka K, Iguchi M, Arii K, Kaneda A, Tsukamoto T, Tatematsu M, et al. 2006. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin Cancer Res. 12:989–995.
  • Mandomando I, Jaintilal D, Pons MJ, Valles X, Espasa M, Mensa L, Sigauque B, Sanz S, Sacarlal J, Macete E, et al. 2009. Antimicrobial susceptibility and mechanisms of resistance in Shigella and Salmonella isolates from children under five years of age with diarrhea in rural Mozambique. Antimicrob Agents Chemother. 53:2450–2454.
  • Martins MD, Jiao Y, Larsson L, Almeida LO, Garaicoa-Pazmino C, Le JM, Squarize CH, Inohara N, Giannobile WV, Castilho RM. 2016. Epigenetic modifications of histones in periodontal disease. J Dent Res. 95:215–222.
  • Masaki T, Qu J, Cholewa-Waclaw J, Burr K, Raaum R, Rambukkana A. 2013. Reprogramming adult Schwann cells to stem cell-like cells by leprosy bacilli promotes dissemination of infection. Cell. 152:51–67.
  • Matalon S, Rasmussen TA, Dinarello CA. 2011. Histone deacetylase inhibitors for purging HIV-1 from the latent reservoir. Mol Med. 17:466–472.
  • Meng S, Zhang L, Tang Y, Tu Q, Zheng L, Yu L, Murray D, Cheng J, Kim SH, Zhou X, Chen J. 2014. BET inhibitor JQ1 blocks inflammation and bone destruction. J Dent Res. 93:657–662.
  • Miraglia E, Nylén F, Johansson K, Arnér E, Cebula M, Farmand S, Ottosson H, Strömberg R, Gudmundsson GH, Agerberth B, Bergman P. 2016. Entinostat up-regulates the CAMP gene encoding LL-37 via activation of STAT3 and HIF-1α transcription factors. Sci Rep. 6:33274.
  • Mombelli M, Lugrin J, Rubino I, Chanson A-L, Giddey M, Calandra T, Roger T. 2011. Histone deacetylase inhibitors impair antibacterial defenses of macrophages. J Infect Dis. 204:1367–1374.
  • Mujtaba S, Winer BY, Jaganathan A, Patel J, Sgobba M, Schuch R, Gupta YK, Haider S, Wang R, Fischetti VA. 2013. Anthrax SET protein: a potential virulence determinant that epigenetically represses NF-κB activation in infected macrophages. J Biol Chem. 288:23458–23472.
  • Nakamura T, Kukita T, Shobuike T, Nagata K, Wu Z, Ogawa K, Hotokebuchi T, Kohashi O, Kukita A. 2005. Inhibition of histone deacetylase suppresses osteoclastogenesis and bone destruction by inducing IFN-beta production. J Immunol. 175:5809–5816.
  • Niederman R, Buyle-Bodin Y, Lu BY, Naleway C, Robinson P, Kent R. 1996. The relationship of gingival crevicular fluid short chain carboxylic acid concentration to gingival inflammation. J Clin Periodontol. 23:743–749.
  • Niederman R, Buyle-Bodin Y, Lu BY, Robinson P, Naleway C. 1997. Short-chain carboxylic acid concentration in human gingival crevicular fluid. J Dent Res. 76:575–579.
  • Niller HH, Minarovits J. 2016. Patho-epigenetics of infectious diseases caused by intracellular bacteria. Adv Exp Med Biol. 879:107–130.
  • Nishida K, Komiyama T, Miyazawa S-I, Shen Z-N, Furumatsu T, Doi H, Yoshida A, Yamana J, Yamamura M, Ninomiya Y. 2004. Histone deacetylase inhibitor suppression of autoantibody-mediated arthritis in mice via regulation of p16INK4a and p21(WAF1/Cip1) expression. Arthritis Rheum. 50:3365–3376.
  • Peart MJ, Smyth GK, van Laar RK, Bowtell DD, Richon VM, Marks PA, Holloway AJ, Johnstone RW. 2005. Identification and functional significance of genes regulated by structurally different histone deacetylase inhibitors. Proc Natl Acad Sci USA. 102:3697–3702.
  • Pennini ME, Pai RK, Schultz DC, Boom WH, Harding CV. 2006. Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-gamma-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J Immunol. 176:4323–4330.
  • Pereira JM, Hamon MA, Cossart P. 2016. A lasting impression: epigenetic memory of bacterial infections? Cell Host Microbe. 19:579–582.
  • Piekarz RL, Frye R, Turner M, Wright JJ, Allen SL, Kirschbaum MH, Zain J, Prince HM, Leonard JP, Geskin LJ, et al. 2009. Phase II multi-institutional trial of the histone deacetylase inhibitor romidepsin as monotherapy for patients with cutaneous T-cell lymphoma. J Clin Oncol. 27:5410–5417.
  • Prinjha RK, Witherington J, Lee K. 2012. Place your BETs: the therapeutic potential of bromodomains. Trends Pharmacol Sci. 33:146–153.
  • Rahman MM, Kukita A, Kukita T, Shobuike T, Nakamura T, Kohashi O. 2003. Two histone deacetylase inhibitors, trichostatin A and sodium butyrate, suppress differentiation into osteoclasts but not into macrophages. Blood. 101:3451–3459.
  • Raqib R, Sarker P, Bergman P, Ara G, Lindh M, Sack DA, Nasirul Islam KM, Gudmundsson GH, Andersson J, Agerberth B. 2006. Improved outcome in shigellosis associated with butyrate induction of an endogenous peptide antibiotic. Proc Natl Acad Sci USA. 103:9178–9183.
  • Raqib R, Sarker P, Mily A, Alam NH, Arifuzzaman ASM, Rekha RS, Andersson J, Gudmundsson GH, Cravioto A, Agerberth B. 2012. Efficacy of sodium butyrate adjunct therapy in shigellosis: a randomized, double-blind, placebo-controlled clinical trial. BMC Infect Dis. 12:111
  • Raymond B, Batsche E, Boutillon F, Wu Y-Z, Leduc D, Balloy V, Raoust E, Muchardt C, Goossens PL, Touqui L. 2009. Anthrax lethal toxin impairs IL-8 expression in epithelial cells through inhibition of histone H3 modification. PLoS Pathog. 5:e1000359.
  • Rennoll-Bankert KE, Garcia-Garcia JC, Sinclair SH, Dumler JS. 2015. Chromatin-bound bacterial effector ankyrin A recruits histone deacetylase 1 and modifies host gene expression. Cell Microbiol. 17:1640–1652.
  • Roger T, Lugrin J, Le Roy D, Goy G, Mombelli M, Koessler T, Ding XC, Chanson A-L, Reymond MK, Miconnet I, et al. 2011. Histone deacetylase inhibitors impair innate immune responses to Toll-like receptor agonists and to infection. Blood. 117:1205–1217.
  • Rolando M, Gomez-Valero L, Buchrieser C. 2015. Bacterial remodelling of the host epigenome: functional role and evolution of effectors methylating host histones. Cell Microbiol. 17:1098–1107.
  • Rolando M, Sanulli S, Rusniok C, Gomez-Valero L, Bertholet C, Sahr T, Margueron R, Buchrieser C. 2013. Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe. 13:395–405.
  • de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg ABP. 2003. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J. 370:737–749.
  • Sabari BR, Zhang D, Allis CD, Zhao Y. 2017. Metabolic regulation of gene expression through histone acylations. Nat Rev Mol Cell Biol. 18:90–101.
  • Saeed S, Quintin J, Kerstens HH, Rao NA, Aghajanirefah A, Matarese F, Cheng S-C, Ratter J, Berentsen K, van der Ent MA, et al. 2014. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science. 345:1251086.
  • Sawicka A, Seiser C. 2012. Histone H3 phosphorylation – a versatile chromatin modification for different occasions. Biochimie. 94:2193–2201.
  • Schauber J, Svanholm C, Termén S, Iffland K, Menzel T, Scheppach W, Melcher R, Agerberth B, Lührs H, Gudmundsson GH. 2003. Expression of the cathelicidin LL-37 is modulated by short chain fatty acids in colonocytes: relevance of signalling pathways. Gut. 52:735–741.
  • Shakespear MR, Halili MA, Irvine KM, Fairlie DP, Sweet MJ. 2011. Histone deacetylases as regulators of inflammation and immunity. Trends Immunol. 32:335–343.
  • Shames SR, Bhavsar AP, Croxen MA, Law RJ, Mak SHC, Deng W, Li Y, Bidshari R, de Hoog CL, Foster LJ, Finlay BB. 2011. The pathogenic Escherichia coli type III secreted protease NleC degrades the host acetyltransferase p300. Cell Microbiol. 13:1542–1557.
  • Singh SK, Ellenrieder V. 2013. Senescence in pancreatic carcinogenesis: from signalling to chromatin remodelling and epigenetics. Gut. 62:1364–1372.
  • Steinmann J, Halldórsson S, Agerberth B, Gudmundsson GH. 2009. Phenylbutyrate induces antimicrobial peptide expression. Antimicrob Agents Chemother. 53:5127–5133.
  • Tolg C, Sabha N, Cortese R, Panchal T, Ahsan A, Soliman A, Aitken KJ, Petronis A, Bägli DJ. 2011. Uropathogenic E. coli infection provokes epigenetic downregulation of CDKN2A (p16INK4A) in uroepithelial cells. Lab Investig. 91:825–836.
  • Tsuda H, Ochiai K, Suzuki N, Otsuka K. 2010. Butyrate, a bacterial metabolite, induces apoptosis and autophagic cell death in gingival epithelial cells. J Periodontal Res. 45:626–634.
  • Vachharajani VT, Liu T, Brown CM, Wang X, Buechler NL, Wells JD, Yoza BK, McCall CE. 2014. SIRT1 inhibition during the hypoinflammatory phenotype of sepsis enhances immunity and improves outcome. J Leukoc Biol. 96:785–796.
  • Verdin E, Ott M. 2015. 50 years of protein acetylation: from gene regulation to epigenetics, metabolism and beyond. Nat Rev Mol Cell Biol. 16:258–264.
  • Wang Y, Curry HM, Zwilling BS, Lafuse WP. 2005. 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. 174:5687–5694.
  • Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, Zhao K. 2009. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell. 138:1019–1031.
  • Woo V, Alenghat T. 2017. Host-microbiota interactions: epigenomic regulation. Curr Opin Immunol. 44:52–60.
  • Xia G, Schneider-Stock R, Diestel A, Habold C, Krueger S, Roessner A, Naumann M, Lendeckel U. 2008. Helicobacter pylori regulates p21(WAF1) by histone H4 acetylation. Biochem Biophys Res Commun. 369:526–531.
  • Xu S, Gao Y, Zhang Q, Wei S, Chen Z, Dai X, Zeng Z, Zhao K-S. 2016. SIRT1/3 activation by resveratrol attenuates acute kidney injury in a septic rat model. Oxid Med Cell Longev. 2016:7296092.
  • Yedery R, Jerse A. 2015. Augmentation of cationic antimicrobial peptide production with histone deacetylase inhibitors as a novel epigenetic therapy for bacterial infections. Antibiotics (Basel). 4:44–61.
  • Yin L, Chung WO. 2011. Epigenetic regulation of human β-defensin 2 and CC chemokine ligand 20 expression in gingival epithelial cells in response to oral bacteria. Mucosal Immunol. 4:409–419.
  • Yu X, Shahir A-M, Sha J, Feng Z, Eapen B, Nithianantham S, Das B, Karn J, Weinberg A, Bissada NF, Ye F. 2014. Short-chain fatty acids from periodontal pathogens suppress histone deacetylases, ezh2, and suv39h1 to promote Kaposi's sarcoma-associated herpesvirus replication. J Virol. 88:4466–4479.
  • Zhang Z, Zhang R. 2015. Epigenetics in autoimmune diseases: pathogenesis and prospects for therapy. Autoimmun Rev. 14:854–863.
  • Zhao T, Li Y, Liu B, Pan B, Cheng X, Georgoff P, Alam HB. 2016. Inhibition of histone deacetylase 6 restores innate immune cells in the bone marrow in a lethal septic model. J Trauma Acute Care Surg. 80:34–40.