Vorinostat, a histone deacetylase inhibitor, suppresses dendritic cell function and ameliorates experimental autoimmune encephalomyelitis

Experimental Neurology

Volumn 241, Issue 1, 2013, Pages 56-66

  Ge, Zhenzhen ^a   Da, Yurong ^a   Xue, Zhenyi ^a   Zhang, Kai ^a   Zhuang, Hao ^a   Peng, Meiyu ^a   Li, Yan ^a   Li, Wen ^a   Simard, Alain ^b   Hao, Junwei ^a   Yao, Zhi ^a   Zhang, Rongxin ^a  

^a TIANJIN MEDICAL UNIVERSITY   (China)

^b UNIVERSITÉ DE MONCTON   (Canada)

Author keywords

Dendritic cells; Experimental autoimmune encephalomyelitis; HDAC inhibitors; Inflammation; Multiple sclerosis; Vorinostat

Indexed keywords

CD14 ANTIGEN; CYTOKINE; VORINOSTAT;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEMYELINATION; DENDRITIC CELL; DRUG EFFICACY; DRUG MECHANISM; ENDOCYTOSIS; FEMALE; GROWTH INHIBITION; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; METABOLIC INHIBITION; MONOCYTE; MOUSE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TH1 CELL; TH17 CELL;

ANIMALS; ANTIGENS, CD; CELL COUNT; CELL DIFFERENTIATION; CELL POLARITY; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; PEPTIDE FRAGMENTS; RNA, MESSENGER;

EID: 84872318428     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.12.006     Document Type: Article

References (54)

1. Acosta-Rodriguez E.V., Napolitani G., Lanzavecchia A., Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 2007, 8:942-949.
2. Adachi H., Katsuno M., Minamiyama M., Sang C., Pagoulatos G., Angelidis C., Kusakabe M., Yoshiki A., Kobayashi Y., Doyu M., Sobue G. Heat shock protein 70 chaperone overexpression ameliorates phenotypes of the spinal and bulbar muscular atrophy transgenic mouse model by reducing nuclear-localized mutant androgen receptor protein. J. Neurosci. 2003, 23:2203-2211.
3. Banchereau J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y.J., Pulendran B., Palucka K. Immunobiology of dendritic cells. Annu. Rev. Immunol. 2000, 18:767-811.
4. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., Weiner H.L., Kuchroo V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-238.
5. Beutler B. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 2004, 430:257-263.
6. Bosisio D., Vulcano M., Del Prete A., Sironi M., Salvi V., Salogni L., Riboldi E., Leoni F., Dinarello C.A., Girolomoni G., Sozzani S. Blocking TH17-polarizing cytokines by histone deacetylase inhibitors in vitro and in vivo. J. Leukoc. Biol. 2008, 84:1540-1548.
7. Bright J.J., Musuro B.F., Du C., Sriram S. Expression of IL-12 in CNS and lymphoid organs of mice with experimental allergic encephalitis. J. Neuroimmunol. 1998, 82:22-30.
8. Burgoon M.P., Gilden D.H., Owens G.P. B cells in multiple sclerosis. Front. Biosci. 2004, 9:786-796.
9. Butler Lisa M., Agus David B., Scher Howard I., Higgins Brian, Rose Adam, Cordon-Cardo Carlos, Thaler Howard T., Rifkind Richard A., Marks Paul A., Richon Victoria M. Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo. Cancer Res. 2000, 60:5165-5170.
10. Camelo S., Iglesias A.H., Hwang D., Due B., Ryu H., Smith K., Gray S.G., Imitola J., Duran G., Assaf B., Langley B., Khoury S.J., Stephanopoulos G., De Girolami U., Ratan R.R., Ferrante R.J., Dangond F. Transcriptional therapy with the histone deacetylase inhibitor trichostatin A ameliorates experimental autoimmune encephalomyelitis. J. Neuroimmunol. 2005, 164:10-21.
11. 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.
12. Dangond F., Gullans S.R. Differential expression of human histone deacetylase mRNAs in response to immune cell apoptosis induction by trichostatin A and butyrate. Biochem. Biophys. Res. Commun. 1998, 247:833-837.
13. Dangond F., Hafler D.A., Tong J.K., Randall J., Kojima R., Utku N., Gullans S.R. Differential display cloning of a novel human histone deacetylase (HDAC3) cDNA from PHA-activated immune cells. Biochem. Biophys. Res. Commun. 1998, 242:648-652.
14. Dangond F., Foerznler D., Weremowicz S., Morton C.C., Beier D.R., Gullans S.R. Cloning and expression of a murine histone deacetylase 3 (mHdac3) cDNA and mapping to a region of conserved synteny between murine chromosome 18 and human chromosome 5. Mol. Cell Biol. Res. Commun. 1999, 2:91-96.
15. Diveu C., McGeachy M.J., Cua D.J. Cytokines that regulate autoimmunity. Curr. Opin. Immunol. 2008, 20:663-668.
16. 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. 2009, 36(2):269-279.
17. Glauben R., Batra A., Fedke I., Zeitz M., Lehr H.A., Leoni F., Mascagni P., Fantuzzi G., Dinarello C.A., Siegmund B. Histone hyperacetylation is associated with amelioration of experimental colitis in mice. J. Immunol. 2006, 176:5015-5022.
18. Gray S.G., De Meyts P. Role of histone and transcription factor acetylation in diabetes pathogenesis. Diabetes Metab. Res. Rev. 2005, 21:416-433.
19. Johnson C.A., White D.A., Lavender J.S., O'Neill L.P., Turner B.M. Human class I histone deacetylase complexes show enhanced catalytic activity in the presence of ATP and co-immunoprecipitate with the ATP-dependent chaperone protein Hsp70. J. Biol. Chem. 2002, 277:9590-9597.
20. Kebir H., Ifergan I., Alvarez J.I., Bernard M., Poirier J., Arbour N., Duquette P., Prat A. Preferential recruitment of interferon-gamma-expressing TH17 cells in multiple sclerosis. Ann. Neurol. 2009, 66:390-402.
21. Klampfer L., Huang J., Swaby L.A., Augenlicht L. Requirement of histone deacetylase activity for signaling by STAT1. J. Biol. Chem. 2004, 279(29):30358-30368.
22. Koenen H.J., Smeets R.L., Vink P.M., van Rijssen E., Boots A.M., Joosten I. Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 2008, 112:2340-2352.
23. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., McClanahan T., Kastelein R.A., Cua D.J. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005, 201:233-240.
24. Leng C., Gries M., Ziegler J., Lokshin A., Mascagni P., Lentzsch S., Mapara M.Y. Reduction of graft-versus-host disease by histone deacetylase inhibitor suberonylanilide hydroxamic acid is associated with modulation of inflammatory cytokine milieu and involves inhibition of STAT1. Exp. Hematol. 2006, 34:776-787.
25. 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. U.S.A. 2002, 99:2995-3000.
26. Lizcano F., Koibuchi N., Fukuda H., Dangond F., Chin W.W. Cell type-specific roles of histone deacetylase in TR ligand-independent transcriptional repression. Mol. Cell. Endocrinol. 2001, 172:13-20.
27. Lock C., Hermans G., Pedotti R., Brendolan A., Schadt E., Garren H., Langer-Gould A., Strober S., Cannella B., Allard J., Klonowski P., Austin A., Lad N., Kaminski N., Galli S.J., Oksenberg J.R., Raine C.S., Heller R., Steinman L. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 2002, 8:500-508.
28. Lucchinetti C., Bruck W., Parisi J., Scheithauer B., Rodriguez M., Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann. Neurol. 2000, 47:707-717.
29. Macagno A., Napolitani G., Lanzavecchia A., Sallusto F. Duration, combination and timing: the signal integration model of dendritic cell activation. Trends Immunol. 2007, 28:227-233.
30. Mahlknecht U., Will J., Varin A., Hoelzer D., Herbein G. Histone deacetylase 3, a class I histone deacetylase, suppresses MAPK11-mediated activating transcription factor-2 activation and represses TNF gene expression. J. Immunol. 2004, 173(6):3979-3990.
31. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., Hatton R.D., Wahl S.M., Schoeb T.R., Weaver C.T. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006, 441:231-234.
32. Martin B.K., Frelinger J.G., Ting J.P. Combination gene therapy with CD86 and the MHC class II transactivator in the control of lung tumor growth. J. Immunol. 1999, 162:6663-6670.
33. Minucci S., Pelicci P.G. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer 2006, 6:38-51.
34. 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. 2007, 13:3933-3941.
35. Noseworthy J.H., Lucchinetti C., Rodriguez M., Weinshenker B.G. Multiple sclerosis. N. Engl. J. Med. 2000, 343:938-952.
36. Reddy P., Maeda Y., Hotary K., Liu C., Reznikov L.L., Dinarello C.A., Ferrara J.L. Histone deacetylase inhibitor suberoylanilide hydroxamic acid reduces acute graft-versus-host disease and preserves graft-versus-leukemia effect. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:3921-3926.
37. Reddy P., Sun Y., Toubai T., Duran-Struuck R., Clouthier S.G., Weisiger E., Maeda Y., Tawara I., Krijanovski O., Gatza E., Liu C., Malter C., Mascagni P., Dinarello C.A., Ferrara J.L. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J. Clin. Invest. 2008, 118:2562-2573.
38. Reilly C.M., Farrelly L.W., Viti D., Redmond S.T., Hutchison F., Ruiz P., Manning P., Connor J., Gilkeson G.S. Modulation of renal disease in MRL/lpr mice by pharmacologic inhibition of inducible nitric oxide synthase. Kidney Int. 2002, 61:839-846.
39. Reilly C.M., Mishra N., Miller J.M., Joshi D., Ruiz P., Richon V.M., Marks P.A., Gilkeson G.S. Modulation of renal disease in MRL/lpr mice by suberoylanilide hydroxamic acid. J. Immunol. 2004, 173:4171-4178.
40. Reis e Sousa C. Activation of dendritic cells: translating innate into adaptive immunity. Curr. Opin. Immunol. 2004, 16:21-25.
41. Rolak L.A. Multiple sclerosis treatment 2001. Neurol. Clin. 2001, 19:107-118.
42. Saemann M.D., Bohmig G.A., Osterreicher C.H., Burtscher H., Parolini O., Diakos C., Stockl J., Horl W.H., Zlabinger G.J. Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J. 2000, 14:2380-2382.
43. Segain J.P., Raingeard de la Blétière D., Bourreille A., Leray V., Gervois N., Rosales C., Ferrier L., Bonnet C., Blottière H.M., Galmiche J.P. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease. Gut 2000, 47(3):397-403.
44. Sercarz E.E. Driver clones and determinant spreading. J. Autoimmun. 2000, 14:275-277.
45. Shen Z., Reznikoff G., Dranoff G., Rock K.L. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 1997, 158:2723-2730.
46. Steinman L., Zamvil S.S. How to successfully apply animal studies in experimental allergic encephalomyelitis to research on multiple sclerosis. Ann. Neurol. 2006, 60:12-21.
47. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006, 24:179-189.
48. Visintin A., Mazzoni A., Spitzer J.H., Wyllie D.H., Dower S.K., Segal D.M. Regulation of Toll-like receptors in human monocytes and dendritic cells. J. Immunol. 2001, 166:249-255.
49. Wang B., Morinobu A., Horiuchi M., Liu J., Kumagai S. Butyrate inhibits functional differentiation of human monocyte-derived dendritic cells. Cell. Immunol. 2008, 253:54-58.
50. Wekerle H. Lessons from multiple sclerosis: models, concepts, observations. Ann. Rheum. Dis. 2008, 67(Suppl. 3):iii56-iii60.
51. Wilson N.J., Boniface K., Chan J.R., McKenzie B.S., Blumenschein W.M., Mattson J.D., Basham B., Smith K., Chen T., Morel F., Lecron J.C., Kastelein R.A., Cua D.J., McClanahan T.K., Bowman E.P., de Waal Malefyt R. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 2007, 8:950-957.
52. Windhagen A., Newcombe J., Dangond F., Strand C., Woodroofe M.N., Cuzner M.L., Hafler D.A. Expression of costimulatory molecules B7-1 (CD80), B7-2 (CD86), and interleukin 12 cytokine in multiple sclerosis lesions. J. Exp. Med. 1995, 182:1985-1996.
53. Woan K.V., Sahakian E., Sotomayor E.M., Seto E., Villagra A. Modulation of antigen-presenting cells by HDAC inhibitors: implications in autoimmunity and cancer. Immunol. Cell Biol. 2012, 90:55-65.
54. Yoo C.B., Jones P.A. Epigenetic therapy of cancer: past, present and future. Nat. Rev. Drug Discov. 2006, 5:37-50.