Improvement of malignant pleural mesothelioma immunotherapy by epigenetic modulators

[en] In the absence of a satisfactory treatment of malignant pleural mesothelioma (MPM), novel therapeutic strategies are urgently needed. Among these, immunotherapy offers a series of advantages such as tumor specificity and good tolerability. Unfortunately, MPM immunotherapy is frequently limited by incomplete cell differentiation or feedback loop regulatory mechanisms. In this review, we describe different components of the innate immune system and discuss strategies to improve MPM immunotherapy by using epigenetic modulators.

Research center :

Department of AgroBioChem, University of Liege, 5030, Gembloux, Belgium

Disciplines :

Biochemistry, biophysics & molecular biology
Oncology
Immunology & infectious disease

Author, co-author :

Hamaïdia, Malik ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Biologie cell. et moléc.

Staumont, Bernard ; Université de Liège > GIGA-R : Epigénétique Cellulaire et Moléculaire

Duysinx, Bernard ; Centre Hospitalier Universitaire de Liège - CHU > > Service de pneumologie - allergologie ; Centre Hospitalier Universitaire de Liège - CHU > Pneumologie-Allergologie

Louis, Renaud ; Centre Hospitalier Universitaire de Liège - CHU > > Service de pneumologie - allergologie ; Centre Hospitalier Universitaire de Liège - CHU > Pneumologie-Allergologie

Willems, Luc ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Biologie cell. et moléc.

Language :

English

Title :

Improvement of malignant pleural mesothelioma immunotherapy by epigenetic modulators

Alternative titles :

[en] Improvement of malignant pleural mesothelioma immunotherapy by epigenetic modulators

Publication date :

2016

Journal title :

Current Topics in Medicinal Chemistry

ISSN :

1568-0266

eISSN :

1873-4294

Publisher :

Bentham Science Publishers Ltd., San Francisco, United States - California

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://benthamscience.com/journals/current-topics-in-medicinal-chemistry/article/134323/
http://www.ncbi.nlm.nih.gov/pubmed/26303419

Available on ORBi :

since 29 September 2015

Statistics

Number of views

162 (47 by ULiège)

Number of downloads

14 (13 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Cornelissen, R., Heuvers, M.E., Maat, A.P., Hendriks, R.W., Hoogsteden, H.C., Aerts, J.G., Hegmans, J.P., New roads open up for implementing immunotherapy in mesothelioma. Clin. Dev. Immunol., 2012, 2012, 927240.
Ismail-Khan, R., Robinson, L.A., Williams, C.C., Jr., Garrett, C.R., Bepler, G., Simon, G.R., Malignant pleural mesothelioma: a com prehensive review. Cancer Control: J. Moffitt Cancer Center, 2006, 13, (4), 255-263.
Bianchi, C., Bianchi, T., Malignant Mesothelioma: Global Incidence and Relationship with Asbestos. Ind. Health, 2007, 45, (3), 379-387.
Creaney, J., Robinson, B.W., Serum and pleural fluid biomarkers for mesothelioma. Curr. Opin Pulmonary Med., 2009, 15, (4), 366-370.
Grigoriu, B., Chahine, B., Zerimech, F., Gregoire, M., Balduyck, M., Copin, M.C., Devos, P., Lassalle, P., Scherpereel, A., Serum mesothelin has a higher diagnostic utility than hyaluronic acid in malignant mesothelioma. Clin. Biochem., 2009, 42, (10-11), 1046-1050.
Gueugnon, F., Leclercq, S., Blanquart, C., Sagan, C., Cellerin, L., Padieu, M., Perigaud, C., Scherpereel, A., Gregoire, M., Identification of novel markers for the diagnosis of malignant pleural mesothelioma. Am. J. Pathol., 2011, 178, (3), 1033-1042.
Gibbs, A.R., Stephens, M., Griffiths, D.M., Blight, B.J., Pooley, F.D., Fibre distribution in the lungs and pleura of subjects with asbestos related diffuse pleural fibrosis. Br. J. Ind. Med., 1991, 48, (11), 762-770.
Donaldson, K., Murphy, F.A., Duffin, R., Poland, C.A., Asbestos, carbon nanotubes and the pleural mesothelium: a review of the hypothesis regarding the role of long fibre retention in the parietal pleura, inflammation and mesothelioma. Particle Fibre Toxicol., 2010, 7, 5.
Dostert, C., Petrilli, V., Van Bruggen, R., Steele, C., Mossman, B.T., Tschopp, J., Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science, 2008, 320, (5876), 674-677.
Izzi, V., Masuelli, L., Tresoldi, I., Foti, C., Modesti, A., Bei, R., Immunity and malignant mesothelioma: from mesothelial cell damage to tumor development and immune response-based therapies. Cancer Lett., 2012, 322, (1), 18-34.
Sumimoto, H., Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J., 2008, 275, (13), 3249-3277.
Amati, M., Tomasetti, M., Scartozzi, M., Mariotti, L., Alleva, R., Pignotti, E., Borghi, B., Valentino, M., Governa, M., Neuzil, J., Santarelli, L., Profiling tumor-associated markers for early detection of malignant mesothelioma: an epidemiologic study. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology, 2008, 17, (1), 163-170.
Suzuki, Y., Murakami, H., Kawaguchi, K., Tanigushi, T., Fujii, M., Shinjo, K., Kondo, Y., Osada, H., Shimokata, K., Horio, Y., Hasegawa, Y., Hida, T., Sekido, Y., Activation of the PI3K-AKT pathway in human malignant mesothelioma cells. Mol. Med. Rep., 2009, 2, (2), 181-188.
Ziegler-Heitbrock, L., Ancuta, P., Crowe, S., Dalod, M., Grau, V., Hart, D.N., Leenen, P.J., Liu, Y.J., MacPherson, G., Randolph, G.J., Scherberich, J., Schmitz, J., Shortman, K., Sozzani, S., Strobl, H., Zembala, M., Austyn, J.M., Lutz, M.B., Nomenclature of monocytes and dendritic cells in blood. Blood, 2010, 116, (16), e74-80.
Lee, H.W., Choi, H.J., Ha, S.J., Lee, K.T., Kwon, Y.G., Recruitment of monocytes/macrophages in different tumor microenvironments. Biochim. Biophys. Acta, 2013, 1835, (2), 170-179.
Ziegler-Heitbrock, L., The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J. Leukocyte Biol., 2007, 81, (3), 584-592.
Merad, M., Sathe, P., Helft, J., Miller, J., Mortha, A., The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Ann. Rev. Immunol., 2013, 31, 563-604.
Condon, T.V., Sawyer, R.T., Fenton, M.J., Riches, D.W., Lung dendritic cells at the innate-adaptive immune interface. J. Leukocyte Biol., 2011, 90, (5), 883-895.
Rutella, S., Danese, S., Leone, G., Tolerogenic dendritic cells: cytokine modulation comes of age. Blood, 2006, 108, (5), 1435-1440.
Zou, W., Restifo, N.P., T(H)17 cells in tumour immunity and immunotherapy. Nat. Rev. Immunol., 2010, 10, (4), 248-256.
Kim, R., Emi, M., Tanabe, K., Arihiro, K., Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res., 2006, 66, (11), 5527-5536.
Li, Q., Guo, Z., Xu, X., Xia, S., Cao, X., Pulmonary stromal cells induce the generation of regulatory DC attenuating T-cell-mediated lung inflammation. Eur. J. Immunol., 2008, 38, (10), 2751-2761.
Torres-Aguilar, H., Aguilar-Ruiz, S.R., Gonzalez-Perez, G., Munguia, R., Bajana, S., Meraz-Rios, M.A., Sanchez-Torres, C., Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells. J. Immunol., 2010, 184, (4), 1765-1775.
Ahmadzadeh, M., Johnson, L.A., Heemskerk, B., Wunderlich, J.R., Dudley, M.E., White, D.E., Rosenberg, S.A., Tumor antigenspecific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood, 2009, 114, (8), 1537-1544.
Manicassamy, S., Pulendran, B., Dendritic cell control of tolerogenic responses. Immunol. Rev., 2011, 241, (1), 206-227.
Singh, A.K., Stock, P., Akbari, O., Role of PD-L1 and PD-L2 in allergic diseases and asthma. Allergy, 2011, 66, (2), 155-162.
Murray, P.J., Wynn, T.A., Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol., 2011, 11, (11), 723-737.
Lawrence, T., Natoli, G., Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nature Rev. Immunol., 2011, 11, (11), 750-761.
Piccinini, A.M., Midwood, K.S., DAMPening inflammation by modulating TLR signalling. Mediators of inflammation, 2010, 2010.
Kaarteenaho-Wiik, R., Soini, Y., Pollanen, R., Paakko, P., Kinnula, V.L., Over-expression of tenascin-C in malignant pleural mesothelioma. Histopathology, 2003, 42, (3), 280-291.
Jube, S., Rivera, Z.S., Bianchi, M.E., Powers, A., Wang, E., Pagano, I., Pass, H.I., Gaudino, G., Carbone, M., Yang, H., Cancer cell secretion of the DAMP protein HMGB1 supports progression in malignant mesothelioma. Cancer Res., 2012, 72, (13), 3290-3301.
Yanai, H., Ban, T., Taniguchi, T., High-mobility group box family of proteins: ligand and sensor for innate immunity. Trends Immunol., 2012, 33, (12), 633-640.
Di Virgilio, F., Purines, purinergic receptors, and cancer. Cancer research, 2012, 72, (21), 5441-5447.
Blum, J.S., Wearsch, P.A., Cresswell, P., Pathways of antigen processing. Ann. Rev. Immunol., 2013, 31, 443-473.
Long, E.O., Kim, H.S., Liu, D., Peterson, M.E., Rajagopalan, S., Controlling natural killer cell responses: integration of signals for activation and inhibition. Ann. Rev. Immunol., 2013, 31, 227-258.
Lecker, S.H., Goldberg, A.L., Mitch, W.E., Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. JASN, 2006, 17, (7), 1807-1819.
Neri, M., Betta, P., Marroni, P., Filiberti, R., Cafferata, M., Mereu, C., Ivaldi, G., Montanaro, F., Puntoni, R., Paganuzzi, M., Serum anti-p53 autoantibodies in pleural malignant mesothelioma, lung cancer and non-neoplastic lung diseases. Lung Cancer, 2003, 39, (2), 165-172.
Gregoire, M., What’s the place of immunotherapy in malignant mesothelioma treatments? Cell Adhesion Migration, 2010, 4, (1), 153-161.
Boisgerault, N., Guillerme, J.B., Pouliquen, D., Mesel-Lemoine, M., Achard, C., Combredet, C., Fonteneau, J.F., Tangy, F., Gregoire, M., Natural oncolytic activity of live-attenuated measles virus against human lung and colorectal adenocarcinomas. BioMed Res. Int., 2013, 2013, 387362.
Fonteneau, J.F., Guillerme, J.B., Tangy, F., Gregoire, M., Attenuated measles virus used as an oncolytic virus activates myeloid and plasmacytoid dendritic cells. Oncoimmunology, 2013, 2, (5), e24212.
Amin, K.M., Litzky, L.A., Smythe, W.R., Mooney, A.M., Morris, J.M., Mews, D.J., Pass, H.I., Kari, C., Rodeck, U., Rauscher, F.J., III, et al., Wilms’ tumor 1 susceptibility (WT1) gene products are selectively expressed in malignant mesothelioma. Am. J. Pathol. 1995, 146, (2), 344-356.
Nishida, S., Koido, S., Takeda, Y., Homma, S., Komita, H., Takahara, A., Morita, S., Ito, T., Morimoto, S., Hara, K., Tsuboi, A., Oka, Y., Yanagisawa, S., Toyama, Y., Ikegami, M., Kitagawa, T., Eguchi, H., Wada, H., Nagano, H., Nakata, J., Nakae, Y., Hosen, N., Oji, Y., Tanaka, T., Kawase, I., Kumanogoh, A., Sakamoto, J., Doki, Y., Mori, M., Ohkusa, T., Tajiri, H., Sugiyama, H., Wilms tumor gene (WT1) peptide-based cancer vaccine combined with gemcitabine for patients with advanced pancreatic cancer. J. Immunother., 2014, 37, (2), 105-114.
Hassan, R., Bullock, S., Premkumar, A., Kreitman, R.J., Kindler, H., Willingham, M.C., Pastan, I., Phase I study of SS1P, a recombinant anti-mesothelin immunotoxin given as a bolus I.V. infusion to patients with mesothelin-expressing mesothelioma, ovarian, and pancreatic cancers. Clin. Cancer Res.: An fficial journal of the American Association for Cancer Research, 2007, 13, (17), 5144-5149.
Houot, R., Kohrt, H.E., Marabelle, A., Levy, R., Targeting immune effector cells to promote antibody-induced cytotoxicity in cancer immunotherapy. Trends Immunol., 2011, 32, (11), 510-516.
Hegmans, J.P., Hemmes, A., Aerts, J.G., Hoogsteden, H.C., Lambrecht, B.N., Immunotherapy of murine malignant mesothelioma using tumor lysate-pulsed dendritic cells. Am. J. Respiratory Crit. Care Med., 2005, 171, (10), 1168-1177.
Jackaman, C., Bundell, C.S., Kinnear, B.F., Smith, A.M., Filion, P., van Hagen, D., Robinson, B.W., Nelson, D.J., IL-2 intratumoral immunotherapy enhances CD8+ T cells that mediate destruction of tumor cells and tumor-associated vasculature: a novel mechanism for IL-2. J. Immunol., 2003, 171, (10), 5051-5063.
Mao, C., Wang, S., Jiang, Q., Tong, J., Ma, J., Yang, M., Xu, X., Qiu, G., Shao, Q., Li, L., Xu, H., Increased CD4CD25+FOXP3+ regulatory T Cells in cancer patients from conversion of CD4+CD25-T cells through tumor-derived factors. Onkologie, 2008, 31, (5), 243-248.
Ye, Z.J., Zhou, Q., Zhang, J.C., Li, X., Wu, C., Qin, S.M., Xin, J.B., Shi, H.Z., CD39+ regulatory T cells suppress generation and differentiation of Th17 cells in human malignant pleural effusion via a LAP-dependent mechanism. Respiratory Res., 2011, 12, 77.
Esquerre, M., Tauzin, B., Guiraud, M., Muller, S., Saoudi, A., Valitutti, S., Human regulatory T cells inhibit polarization of T helper cells toward antigen-presenting cells via a TGF-betadependent mechanism. Proc. Natl. Acad. Sci. USA, 2008, 105, (7), 2550-2555.
Hegmans, J.P., Hemmes, A., Hammad, H., Boon, L., Hoogsteden, H.C., Lambrecht, B.N., Mesothelioma environment comprises cytokines and T-regulatory cells that suppress immune responses. Eur. Respiratory J., 2006, 27, (6), 1086-1095.
Curran, M.A., Kim, M., Montalvo, W., Al-Shamkhani, A., Allison, J.P., Combination CTLA-4 blockade and 4-1BB activation enhances tumor rejection by increasing T-cell infiltration, proliferation, and cytokine production. PloS One, 2011, 6, (4), e19499.
Broomfield, S.A., van der Most, R.G., Prosser, A.C., Mahendran, S., Tovey, M.G., Smyth, M.J., Robinson, B.W., Currie, A.J., Locally administered TLR7 agonists drive systemic antitumor immune responses that are enhanced by anti-CD40 immunotherapy. J. Immunol., 2009, 182, (9), 5217-5224.
Bowdridge, S., Gause, W.C., Regulation of alternative macrophage activation by chromatin remodeling. Nat. Immunol., 2010, 11, (10), 879-881.
Helin, K., Dhanak, D., Chromatin proteins and modifications as drug targets. Nature, 2013, 502, (7472), 480-488.
Mullican, S.E., Gaddis, C.A., Alenghat, T., Nair, M.G., Giacomin, P.R., Everett, L.J., Feng, D., Steger, D.J., Schug, J., Artis, D., Lazar, M.A., Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev., 2011, 25, (23), 2480-2488.
Shakespear, M.R., Hohenhaus, D.M., Kelly, G.M., Kamal, N.A., Gupta, P., Labzin, L.I., Schroder, K., Garceau, V., Barbero, S., Iyer, A., Hume, D.A., Reid, R.C., Irvine, K.M., Fairlie, D.P., Sweet, M.J., Histone deacetylase 7 promotes Toll-like receptor 4-dependent proinflammatory gene expression in macrophages. J. Biol. Chem., 2013, 288, (35), 25362-25374.
Sigalotti, L., Fratta, E., Coral, S., Maio, M., Epigenetic drugs as immunomodulators for combination therapies in solid tumors. Pharmacol. Ther., 2014, 142, (3), 339-350.
Heninger, E., Krueger, T.E., Lang, J.M., Augmenting antitumor immune responses with epigenetic modifying agents. Frontiers Immunol., 2015, 6, 29.
Sigalotti, L., Coral, S., Altomonte, M., Natali, L., Gaudino, G., Cacciotti, P., Libener, R., Colizzi, F., Vianale, G., Martini, F., Tognon, M., Jungbluth, A., Cebon, J., Maraskovsky, E., Mutti, L., Maio, M., Cancer testis antigens expression in mesothelioma: role of DNA methylation and bioimmunotherapeutic implications. Br. J. Cancer, 2002, 86, (6), 979-982.
Leclercq, S., Gueugnon, F., Boutin, B., Guillot, F., Blanquart, C., Rogel, A., Padieu, M., Pouliquen, D., Fonteneau, J.F., Gregoire, M., A 5-aza-2’-deoxycytidine/valproate combination induces cytotoxic T-cell response against mesothelioma. Eur. Respiratory J., 2011, 38, (5), 1105-1116.
Coral, S., Parisi, G., Nicolay, H.J., Colizzi, F., Danielli, R., Fratta, E., Covre, A., Taverna, P., Sigalotti, L., Maio, M., Immunomodulatory activity of SGI-110, a 5-aza-2’-deoxycytidine-containing demethylating dinucleotide. Cancer Immunol. Immunother.,: CII, 2013, 62, (3), 605-614.
Schafer, A., Schomacher, L., Barreto, G., Doderlein, G., Niehrs, C., Gemcitabine functions epigenetically by inhibiting repair mediated DNA demethylation. PloS One, 2010, 5, (11), e14060.
Gray, S.G., Baird, A.M., O’Kelly, F., Nikolaidis, G., Almgren, M., Meunier, A., Dockry, E., Hollywood, D., Ekstrom, T.J., Perry, A.S., O’Byrne, K.J. Gemcitabine reactivates epigenetically silenced genes and functions as a DNA methyltransferase inhibitor. Int. J. Mol. Med., 2012, 30, (6), 1505-1511.
Cheng, C., Huang, C., Ma, T.T., Bian, E.B., He, Y., Zhang, L., Li, J., SOCS1 hypermethylation mediated by DNMT1 is associated with lipopolysaccharide-induced inflammatory cytokines in macrophages. Toxicol. Lett., 2014, 225, (3), 488-497.
Davie, J.R., Inhibition of histone deacetylase activity by butyrate. J. Nutrition, 2003, 133, (7 Suppl), 2485S-2493S.
Saemann, M.D., Parolini, O., Bohmig, G.A., Kelemen, P., Krieger, P.M., Neumuller, J., Knarr, K., Kammlander, W., Horl, W.H., Diakos, C., Stuhlmeier, K., Zlabinger, G.J., Bacterial metabolite interference with maturation of human monocyte-derived dendritic cells. J. Leukocyte Biol., 2002, 71, (2), 238-246.
Liu, L., Li, L., Min, J., Wang, J., Wu, H., Zeng, Y., Chen, S., Chu, Z., Butyrate interferes with the differentiation and function of human monocyte-derived dendritic cells. Cell. Immunol., 2012, 277, (1-2), 66-73.
Chang, P.V., 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, (6), 2247-2252.
Diakos, C., Prieschl, E.E., Saemann, M., Novotny, V., Bohmig, G., Csonga, R., Baumruker, T., Zlabinger, G.J., Novel mode of interference with nuclear factor of activated T-cells regulation in T-cells by the bacterial metabolite n-butyrate. J. Biol. Chem., 2002, 277, (27), 24243-24251.
Arpaia, N., Campbell, C., Fan, X., Dikiy, S., van der Veeken, J., deRoos, P., Liu, H., Cross, J.R., Pfeffer, K., Coffer, P.J., Rudensky, A.Y., Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature, 2013, 504, (7480), 451-455.
Furusawa, Y., Obata, Y., Fukuda, S., Endo, T.A., Nakato, G., Takahashi, D., Nakanishi, Y., Uetake, C., Kato, K., Kato, T., Takahashi, M., Fukuda, N.N., Murakami, S., Miyauchi, E., Hino, S., Atarashi, K., Onawa, S., Fujimura, Y., Lockett, T., Clarke, J.M., Topping, D.L., Tomita, M., Hori, S., Ohara, O., Morita, T., Koseki, H., Kikuchi, J., Honda, K., Hase, K., Ohno, H., Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature, 2013, 504, (7480), 446-450.
Yoshida, M., Horinouchi, S., Beppu, T., Trichostatin A and trapoxin: novel chemical probes for the role of histone acetylation in chromatin structure and function. BioEssays: News Revi. Mol. Cell. Dev. Biol., 1995, 17, (5), 423-430.
Yoshida, M., Kijima, M., Akita, M., Beppu, T., Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J. Biol. Chem., 1990, 265, (28), 17174-17179.
Bode, K.A., Schroder, K., Hume, D.A., Ravasi, T., Heeg, K., Sweet, M.J., Dalpke, A.H., Histone deacetylase inhibitors decrease Toll-like receptor-mediated activation of proinflammatory gene expression by impairing transcription factor recruitment. Immunology, 2007, 122, (4), 596-606.
Han, S.B., Lee, J.K., Anti-inflammatory effect of Trichostatin-A on murine bone marrow-derived macrophages. Arch. Pharmacal Res., 2009, 32, (4), 613-624.
Halili, M.A., Andrews, M.R., Labzin, L.I., Schroder, K., Matthias, G., Cao, C., Lovelace, E., Reid, R.C., Le, G.T., Hume, D.A., Irvine, K.M., Matthias, P., Fairlie, D.P., Sweet, M.J., Differential effects of selective HDAC inhibitors on macrophage inflammatory responses to the Toll-like receptor 4 agonist LPS. J. Leukocyte Biol., 2010, 87, (6), 1103-1114.
Mombelli, M., Lugrin, J., Rubino, I., Chanson, A.L., Giddey, M., Calandra, T., Roger, T., Histone deacetylase inhibitors impair antibacterial defenses of macrophages. J. Infect. Dis., 2011, 204, (9), 1367-1374.
Misaki, K., Morinobu, A., Saegusa, J., Kasagi, S., Fujita, M., Miyamoto, Y., Matsuki, F., Kumagai, S. Histone deacetylase inhibition alters dendritic cells to assume a tolerogenic phenotype and ameliorates arthritis in SKG mice. Arthritis Res. Ther., 2011, 13, (3), R77.
Stepanek, I., Indrova, M., Bieblova, J., Fucikova, J., Spisek, R., Bubenik, J., Reinis, M., Effects of 5-azacytidine and trichostatin A on dendritic cell maturation. J. Biol. Regulators Homeostatic Agents, 2011, 25, (4), 517-529.
Salvi, V., Bosisio, D., Mitola, S., Andreoli, L., Tincani, A., Sozzani, S., Trichostatin A blocks type I interferon production by activated plasmacytoid dendritic cells. Immunobiology, 2010, 215, (9-10), 756-761.
Donas, C., Fritz, M., Manriquez, V., Tejon, G., Bono, M.R., Loyola, A., Rosemblatt, M., Trichostatin A promotes the generation and suppressive functions of regulatory T cells. Clin. Dev. Immunology, 2013, 2013, 679804.
Choi, Y., Park, S.K., Kim, H.M., Kang, J.S., Yoon, Y.D., Han, S.B., Han, J.W., Yang, J.S., Han, G., Histone deacetylase inhibitor KBH-A42 inhibits cytokine production in RAW 264.7 macrophage cells and in vivo endotoxemia model. Exp. Mol. Med., 2008, 40, (5), 574-581.
Chong, W., Li, Y., Liu, B., Zhao, T., Fukudome, E.Y., Liu, Z., Smith, W.M., Velmahos, G.C., deMoya, M.A., Alam, H.B., Histone deacetylase inhibitor suberoylanilide hydroxamic acid attenuates Toll-like receptor 4 signaling in lipopolysaccharide-stimulated mouse macrophages. J. Surg. Res., 2012, 178, (2), 851-859.
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, S.H., Pomerantz, B.J., Reznikov, L.L., Siegmund, B., Dinarello, C.A., Mascagni, P., The antitumor histone deacetylase inhibitor suberoylanilide hydroxamic acid exhibits antiinflammatory properties via suppression of cytokines. Proc. Natl. Acad. Sci. USA, 2002, 99, (5), 2995-3000.
Shi, Z.J., Ouyang, D.Y., Zhu, J.S., Xu, L.H., He, X.H., Histone deacetylase inhibitor suberoylanilide hydroxamic acid exhibits antiinflammatory activities through induction of mitochondrial damage and apoptosis in activated lymphocytes. Int. Immunopharmacol., 2012, 12, (4), 580-587.
Zhang, Z., Zhang, Z.Y., Fauser, U., Schluesener, H.J., Valproic acid attenuates inflammation in experimental autoimmune neuritis. Cellular and molecular life sciences: CMLS, 2008, 65, (24), 4055-4065.
Brogdon, J.L., Xu, Y., Szabo, S.J., An, S., Buxton, F., Cohen, D., Huang, Q., Histone deacetylase activities are required for innate immune cell control of Th1 but not Th2 effector cell function. Blood, 2007, 109, (3), 1123-1130.
Roger, T., Lugrin, J., Le Roy, D., Goy, G., Mombelli, M., Koessler, T., Ding, X.C., Chanson, A.L., Reymond, M.K., Miconnet, I., Schrenzel, J., Francois, P., Calandra, T., Histone deacetylase inhibitors impair innate immune responses to Toll-like receptor agonists and to infection. Blood, 2011, 117, (4), 1205-1217.
Wu, C., Li, A., Leng, Y., Li, Y., Kang, J., Histone deacetylase inhibition by sodium valproate regulates polarization of macrophage subsets. DNA Cell Biol., 2012, 31, (4), 592-599.
Chauvistre, H., Kustermann, C., Rehage, N., Klisch, T., Mitzka, S., Felker, P., Rose-John, S., Zenke, M., Sere, K.M., Dendritic cell development requires histone deacetylase activity. Eur. J. Immunol., 2014, 44, (8), 2478-2488.
Frikeche, J., Simon, T., Brissot, E., Gregoire, M., Gaugler, B., Mohty, M., Impact of valproic acid on dendritic cells function. Immunobiology, 2012, 217, (7), 704-710.
Nencioni, A., Beck, J., Werth, D., Grunebach, F., Patrone, F., Ballestrero, A., Brossart, P. Histone deacetylase inhibitors affect dendritic cell differentiation and immunogenicity. Clin. Cancer Res.: an official journal of the American Association for Cancer Research, 2007, 13, (13), 3933-3941.
Lagneaux, L., Gillet, N., Stamatopoulos, B., Delforge, A., Dejeneffe, M., Massy, M., Meuleman, N., Kentos, A., Martiat, P., Willems, L., Bron, D., Valproic acid induces apoptosis in chronic lymphocytic leukemia cells through activation of the death receptor pathway and potentiates TRAIL response. Exp. Hematol., 2007, 35, (10), 1527-1537.
Vandermeers, F., Hubert, P., Delvenne, P., Mascaux, C., Grigoriu, B., Burny, A., Scherpereel, A., Willems, L., Valproate, in combination with pemetrexed and cisplatin, provides additional efficacy to the treatment of malignant mesothelioma. Clinical Cancer Res.: an official journal of the American Association for Cancer Research, 2009, 15, (8), 2818-2828.
Scherpereel, A., Berghmans, T., Lafitte, J.J., Colinet, B., Richez, M., Bonduelle, Y., Meert, A.P., Dhalluin, X., Leclercq, N., Paesmans, M., Willems, L., Sculier, J.P., European Lung Cancer Working, P., Valproate-doxorubicin: promising therapy for progressing mesothelioma. A phase II study. Eur. Tespiratory J., 2011, 37, (1), 129-135.
Hubaux, R., Vandermeers, F., Crisanti, M.C., Kapoor, V., Burny, A., Mascaux, C., Albelda, S.M., Willems, L., Preclinical evidence for a beneficial impact of valproate on the response of small cell lung cancer to first-line chemotherapy. Eur. J. Cancer, 2010, 46, (9), 1724-1734.
Suzuki, T., Terao, S., Acharya, B., Naoe, M., Yamamoto, S., Okamura, H., Gotoh, A., The antitumour effect of {gamma}{delta} Tcells is enhanced by valproic acid-induced up-regulation of NKG2D ligands. Anticancer Res., 2010, 30, (11), 4509-4513.
Zhang, Z.Y., Zhang, Z., Schluesener, H.J., MS-275, an histone deacetylase inhibitor, reduces the inflammatory reaction in rat experimental autoimmune neuritis. Neuroscience, 2010, 169, (1), 370-377.
Zhang, Z.Y., Schluesener, H.J., HDAC inhibitor MS-275 attenuates the inflammatory reaction in rat experimental autoimmune prostatitis. Prostate, 2012, 72, (1), 90-99.
Filippakopoulos, P., Knapp, S., Targeting bromodomains: epigenetic readers of lysine acetylation. Nat. Rev. Drug Discov., 2014, 13, (5), 337-356.
Nicodeme, E., Jeffrey, K.L., Schaefer, U., Beinke, S., Dewell, S., Chung, C.W., Chandwani, R., Marazzi, I., Wilson, P., Coste, H., White, J., Kirilovsky, J., Rice, C.M., Lora, J.M., Prinjha, R.K., Lee, K., Tarakhovsky, A., Suppression of inflammation by a synthetic histone mimic. Nature, 2010, 468, (7327), 1119-1123.
Bandukwala, H.S., Gagnon, J., Togher, S., Greenbaum, J.A., Lamperti, E.D., Parr, N.J., Molesworth, A.M., Smithers, N., Lee, K., Witherington, J., Tough, D.F., Prinjha, R.K., Peters, B., Rao, A., Selective inhibition of CD4+ T-cell cytokine production and autoimmunity by BET protein and c-Myc inhibitors. Proc. Natl. Acad. Sci. USA, 2012, 109, (36), 14532-14537.
Barrett, E., Brothers, S., Wahlestedt, C., Beurel, E., I-BET151 selectively regulates IL-6 production. Biochim. Biophys. Acta, 2014, 1842, (9), 1549-1555.
Belkina, A.C., Nikolajczyk, B.S., Denis, G.V., BET protein function is required for inflammation: Brd2 genetic disruption and BET inhibitor JQ1 impair mouse macrophage inflammatory responses. J. Immunol. 2013, 190, (7), 3670-3678.
Wienerroither, S., Rauch, I., Rosebrock, F., Jamieson, A.M., Bradner, J., Muhar, M., Zuber, J., Muller, M., Decker, T., Regulation of NO synthesis, local inflammation, and innate immunity to pathogens by BET family proteins. Mol. Cellular Biol. 2014, 34, (3), 415-427.
Kemp, C.D., Rao, M., Xi, S., Inchauste, S., Mani, H., Fetsch, P., Filie, A., Zhang, M., Hong, J.A., Walker, R.L., Zhu, Y.J., Ripley, R.T., Mathur, A., Liu, F., Yang, M., Meltzer, P.A., Marquez, V.E., De Rienzo, A., Bueno, R., Schrump, D.S., Polycomb repressor complex-2 is a novel target for mesothelioma therapy. Clin. Cancer Res.: an official journal of the American Association for Cancer Research, 2012, 18, (1), 77-90.
Imai, K., Togami, H., Okamoto, T., Involvement of histone H3 lysine 9 (H3K9) methyltransferase G9a in the maintenance of HIV-1 latency and its reactivation by BIX01294. J. Biol. Chem., 2010, 285, (22), 16538-16545.
Ke, X.X., Zhang, D., Zhu, S., Xia, Q., Xiang, Z., Cui, H., Inhibition of H3K9 Methyltransferase G9a Repressed Cell Proliferation and Induced Autophagy in Neuroblastoma Cells. PloS One, 2014, 9, (9), e106962.
De Santa, F., Narang, V., Yap, Z.H., Tusi, B.K., Burgold, T., Austenaa, L., Bucci, G., Caganova, M., Notarbartolo, S., Casola, S., Testa, G., Sung, W.K., Wei, C.L., Natoli, G., Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J., 2009, 28, (21), 3341-3352.
Satoh, T., Takeuchi, O., Vandenbon, A., Yasuda, K., Tanaka, Y., Kumagai, Y., Miyake, T., Matsushita, K., Okazaki, T., Saitoh, T., Honma, K., Matsuyama, T., Yui, K., Tsujimura, T., Standley, D.M., Nakanishi, K., Nakai, K., Akira, S., The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat. Immunol., 2010, 11, (10), 936-944.
Wang, K., Bodempudi, V., Liu, Z., Borrego-Diaz, E., Yamoutpoor, F., Meyer, A., Woo, R.A., Pan, W., Dudek, A.Z., Olyaee, M.S., Esfandyari, T., Farassati, F., Inhibition of mesothelin as a novel strategy for targeting cancer cells. PloS One, 2012, 7, (4), e33214.
Benetatos, L., Voulgaris, E., Vartholomatos, G., Hatzimichael, E., Non-coding RNAs and EZH2 interactions in cancer: long and short tales from the transcriptome. Int. J. Cancer, 2013, 133, (2), 267-274.