Histone deacetylase inhibitors repress macrophage migration inhibitory factor (MIF) expression by targeting MIF gene transcription through a local chromatin deacetylation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 11, 2009, Pages 1749-1758

  Lugrin, Jérôme ^a   Ding, Xavier C ^a   Le Roy, Didier ^a   Chanson, Anne Laure ^a   Sweep, Fred C G J ^b   Calandra, Thierry ^a   Roger, Thierry ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Chromatin; Histone deacetylase inhibitor; Macrophage migration inhibitory factor; Transcription factor; Trichostatin A

Indexed keywords

ADENOVIRUS VECTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; HISTONE H4; MACROPHAGE MIGRATION INHIBITION FACTOR; RNA POLYMERASE II; TRANSCRIPTION FACTOR SP1; TRICHOSTATIN A;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL PROLIFERATION; CHROMATIN; CONTROLLED STUDY; DEACETYLATION; DRUG POTENCY; DRUG TARGETING; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC TRANSDUCTION; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; HYPOTHESIS; IN VIVO STUDY; INFLAMMATION; INHIBITION KINETICS; METASTASIS POTENTIAL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REPORTER GENE;

ANIMALS; ANTINEOPLASTIC AGENTS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HELA CELLS; HISTONE DEACETYLASE INHIBITORS; HL-60 CELLS; HUMANS; HYDROXAMIC ACIDS; INTRAMOLECULAR OXIDOREDUCTASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MICE; MICE, INBRED BALB C; RNA POLYMERASE II; SP1 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; U937 CELLS;

ADENOVIRIDAE;

EID: 71749112935     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2009.09.007     Document Type: Article

References (62)

1. Bloom B.R., and Bennett B. Mechanism of a reaction in vitro associated with delayed-type hypersensitivity. Science 153 (1966) 80-82
2. David J.R. Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc. Natl. Acad. Sci. U. S. A. 56 (1966) 72-77
3. Calandra T., and Roger T. Macrophage migration inhibitory factor: a regulator of innate immunity. Nat. Rev. Immunol. 3 (2003) 791-800
4. Mitchell R.A., Metz C.N., Peng T., and Bucala R. Sustained mitogen-activated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF). Regulatory role in cell proliferation and glucocorticoid action. J. Biol. Chem. 274 (1999) 18100-18106
5. Swant J.D., Rendon B.E., Symons M., and Mitchell R.A. Rho GTPase-dependent signaling is required for macrophage migration inhibitory factor-mediated expression of cyclin D1. J. Biol. Chem. 280 (2005) 23066-23072
6. Hudson J.D., Shoaibi M.A., Maestro R., Carnero A., Hannon G.J., and Beach D.H. A proinflammatory cytokine inhibits p53 tumor suppressor activity. J. Exp. Med. 190 (1999) 1375-1382
7. Petrenko O., Fingerle-Rowson G., Peng T., Mitchell R.A., and Metz C.N. Macrophage migration inhibitory factor deficiency is associated with altered cell growth and reduced susceptibility to Ras-mediated transformation. J. Biol. Chem. 278 (2003) 11078-11085
8. Petrenko O., and Moll U.M. Macrophage migration inhibitory factor MIF interferes with the Rb-E2F pathway. Mol. Cell 17 (2005) 225-236
9. Lue H., Thiele M., Franz J., Dahl E., Speckgens S., Leng L., Fingerle-Rowson G., Bucala R., Luscher B., and Bernhagen J. Macrophage migration inhibitory factor (MIF) promotes cell survival by activation of the Akt pathway and role for CSN5/JAB1 in the control of autocrine MIF activity. Oncogene 26 (2007) 5046-5059
10. Wilson J.M., Coletta P.L., Cuthbert R.J., Scott N., MacLennan K., Hawcroft G., Leng L., Lubetsky J.B., Jin K.K., Lolis E., Medina F., Brieva J.A., Poulsom R., Markham A.F., Bucala R., and Hull M.A. Macrophage migration inhibitory factor promotes intestinal tumorigenesis. Gastroenterology 129 (2005) 1485-1503
11. Abe R., Peng T., Sailors J., Bucala R., and Metz C.N. Regulation of the CTL response by macrophage migration inhibitory factor. J. Immunol. 166 (2001) 747-753
12. Krockenberger M., Dombrowski Y., Weidler C., Ossadnik M., Honig A., Hausler S., Voigt H., Becker J.C., Leng L., Steinle A., Weller M., Bucala R., Dietl J., and Wischhusen J. Macrophage migration inhibitory factor contributes to the immune escape of ovarian cancer by down-regulating NKG2D. J. Immunol. 180 (2008) 7338-7348
13. Repp A.C., Mayhew E.S., Apte S., and Niederkorn J.Y. Human uveal melanoma cells produce macrophage migration-inhibitory factor to prevent lysis by NK cells. J. Immunol. 165 (2000) 710-715
14. Zhou Q., Yan X., Gershan J., Orentas R.J., and Johnson B.D. Expression of macrophage migration inhibitory factor by neuroblastoma leads to the inhibition of antitumor T cell reactivity in vivo. J. Immunol. 181 (2008) 1877-1886
15. Nemajerova A., Mena P., Fingerle-Rowson G., Moll U.M., and Petrenko O. Impaired DNA damage checkpoint response in MIF-deficient mice. EMBO J. 26 (2007) 987-997
16. Rendon B.E., Roger T., Teneng I., Zhao M., Al-Abed Y., Calandra T., and Mitchell R.A. Regulation of human lung adenocarcinoma cell migration and invasion by macrophage migration inhibitory factor. J. Biol. Chem. 282 (2007) 29910-29918
17. Bucala R., and Donnelly S.C. Macrophage migration inhibitory factor: a probable link between inflammation and cancer. Immunity 26 (2007) 281-285
18. Mitchell R.A. Mechanisms and effectors of MIF-dependent promotion of tumourigenesis. Cell. Signal. 16 (2004) 13-19
19. Bolden J.E., Peart M.J., and Johnstone R.W. Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov. 5 (2006) 769-784
20. Glozak M.A., and Seto E. Histone deacetylases and cancer. Oncogene 26 (2007) 5420-5432
21. Minucci S., and Pelicci P.G. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer 6 (2006) 38-51
22. Hebbes T.R., Thorne A.W., and Crane-Robinson C. A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J. 7 (1988) 1395-1402
23. Pazin M.J., and Kadonaga J.T. What's up and down with histone deacetylation and transcription?. Cell 89 (1997) 325-328
24. Sterner D.E., and Berger S.L. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64 (2000) 435-459
25. Della Ragione F., Criniti V., Della Pietra V., Borriello A., Oliva A., Indaco S., Yamamoto T., and Zappia V. Genes modulated by histone acetylation as new effectors of butyrate activity. FEBS Lett. 499 (2001) 199-204
26. Mariadason J.M., Corner G.A., and Augenlicht L.H. Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, and curcumin and implications for chemoprevention of colon cancer. Cancer Res. 60 (2000) 4561-4572
27. Peart M.J., Smyth G.K., van Laar R.K., Bowtell D.D., Richon V.M., Marks P.A., Holloway A.J., and Johnstone R.W. Identification and functional significance of genes regulated by structurally different histone deacetylase inhibitors. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 3697-3702
28. Van Lint C., Emiliani S., and Verdin E. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expr. 5 (1996) 245-253
29. Esteller M. Epigenetics in cancer. N. Engl. J. Med. 358 (2008) 1148-1159
30. Marks P.A., and Breslow R. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat. Biotechnol. 25 (2007) 84-90
31. Roger T., Froidevaux C., Le Roy D., Reymond M.K., Chanson A.L., Mauri D., Burns K., Riederer B.M., Akira S., and Calandra T. Protection from lethal gram-negative bacterial sepsis by targeting Toll-like receptor 4. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 2348-2352
32. Bernhagen J., Mitchell R.A., Calandra T., Voelter W., Cerami A., and Bucala R. Purification, bioactivity, and secondary structure analysis of mouse and human macrophage migration inhibitory factor (MIF). Biochemistry 33 (1994) 14144-14155
33. Roger T., Froidevaux C., Martin C., and Calandra T. Macrophage migration inhibitory factor (MIF) regulates host responses to endotoxin through modulation of Toll-like receptor 4 (TLR4). J. Endotoxin Res. 9 (2003) 119-123
34. Delaloye J., Roger T., Steiner-Tardivel Q.G., Le Roy D., Knaup Reymond M., Akira S., Petrilli V., Gomez C.E., Perdiguero B., Tschopp J., Pantaleo G., Esteban M., and Calandra T. Innate immune sensing of Modified Vaccinia Virus Ankara (MVA) is mediated by TLR2-TLR6, MDA-5 and the NALP3 inflammasome. PLoS Pathogens 5 (2009) e1000480
35. Mulholland N.M., Soeth E., and Smith C.L. Inhibition of MMTV transcription by HDAC inhibitors occurs independent of changes in chromatin remodeling and increased histone acetylation. Oncogene 22 (2003) 4807-4818
36. Radstake T.R., Sweep F.C., Welsing P., Franke B., Vermeulen S.H., Geurts-Moespot A., Calandra T., Donn R., and van Riel P.L. Correlation of rheumatoid arthritis severity with the genetic functional variants and circulating levels of macrophage migration inhibitory factor. Arthritis Rheum. 52 (2005) 3020-3029
37. Patrone G., Puppo F., Cusano R., Scaranari M., Ceccherini I., Puliti A., and Ravazzolo R. Nuclear run-on assay using biotin labeling, magnetic bead capture and analysis by fluorescence-based RT-PCR. Biotechniques 29 (2000) 1012-1014 1016-1017
38. Roger T., Ding X., Chanson A.L., Renner P., and Calandra T. Regulation of constitutive and microbial pathogen-induced human macrophage migration inhibitory factor (MIF) gene expression. Eur. J. Immunol. 37 (2007) 3509-3521
39. Roger T., David J., Glauser M.P., and Calandra T. MIF regulates innate immune responses through modulation of Toll-like receptor 4. Nature 414 (2001) 920-924
40. Mitani Y., Oue N., Hamai Y., Aung P.P., Matsumura S., Nakayama H., Kamata N., and Yasui W. Histone H3 acetylation is associated with reduced p21(WAF1/CIP1) expression by gastric carcinoma. J. Pathol. 205 (2005) 65-73
41. Ryu H., Lee J., Olofsson B.A., Mwidau A., Dedeoglu A., Escudero M., Flemington E., Azizkhan-Clifford J., Ferrante R.J., and Ratan R.R. Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 4281-4286
42. Meyer-Siegler K.L., Bellino M.A., and Tannenbaum M. Macrophage migration inhibitory factor evaluation compared with prostate specific antigen as a biomarker in patients with prostate carcinoma. Cancer 94 (2002) 1449-1456
43. Shun C.T., Lin J.T., Huang S.P., Lin M.T., and Wu M.S. Expression of macrophage migration inhibitory factor is associated with enhanced angiogenesis and advanced stage in gastric carcinomas. World J. Gastroenterol. 11 (2005) 3767-3771
44. Smith C.L., and Hager G.L. Transcriptional regulation of mammalian genes in vivo. A tale of two templates. J. Biol. Chem. 272 (1997) 27493-27496
45. Camarero N., Nadal A., Barrero M.J., Haro D., and Marrero P.F. Histone deacetylase inhibitors stimulate mitochondrial HMG-CoA synthase gene expression via a promoter proximal Sp1 site. Nucleic Acids Res. 31 (2003) 1693-1703
46. Xiao H., Hasegawa T., and Isobe K. Both Sp1 and Sp3 are responsible for p21waf1 promoter activity induced by histone deacetylase inhibitor in NIH3T3 cells. J. Cell Biochem. 73 (1999) 291-302
47. Yokota T., Matsuzaki Y., Miyazawa K., Zindy F., Roussel M.F., and Sakai T. Histone deacetylase inhibitors activate INK4d gene through Sp1 site in its promoter. Oncogene 23 (2004) 5340-5349
48. Zelko I.N., and Folz R.J. Sp1 and Sp3 transcription factors mediate trichostatin A-induced and basal expression of extracellular superoxide dismutase. Free Radic. Biol. Med. 37 (2004) 1256-1271
49. Duan H., Heckman C.A., and Boxer L.M. Histone deacetylase inhibitors down-regulate bcl-2 expression and induce apoptosis in t(14;18) lymphomas. Mol. Cell. Biol. 25 (2005) 1608-1619
50. Huang W., Zhao S., Ammanamanchi S., Brattain M., Venkatasubbarao K., and Freeman J.W. Trichostatin A induces transforming growth factor beta type II receptor promoter activity and acetylation of Sp1 by recruitment of PCAF/p300 to a Sp1.NF-Y complex. J. Biol. Chem. 280 (2005) 10047-10054
51. Ferguson M., Henry P.A., and Currie R.A. Histone deacetylase inhibition is associated with transcriptional repression of the Hmga2 gene. Nucleic Acids Res. 31 (2003) 3123-3133
52. Reid G., Metivier R., Lin C.Y., Denger S., Ibberson D., Ivacevic T., Brand H., Benes V., Liu E.T., and Gannon F. Multiple mechanisms induce transcriptional silencing of a subset of genes, including oestrogen receptor alpha, in response to deacetylase inhibition by valproic acid and trichostatin A. Oncogene 24 (2005) 4894-4907
53. Chen C.S., Weng S.C., Tseng P.H., Lin H.P., and Chen C.S. Histone acetylation-independent effect of histone deacetylase inhibitors on Akt through the reshuffling of protein phosphatase 1 complexes. J. Biol. Chem. 280 (2005) 38879-38887
54. Chen J., Ghazawi F.M., Bakkar W., and Li Q. Valproic acid and butyrate induce apoptosis in human cancer cells through inhibition of gene expression of Akt/protein kinase B. Mol. Cancer 5 (2006) 71
55. Yu X.D., Wang S.Y., Chen G.A., Hou C.M., Zhao M., Hong J.A., Nguyen D.M., and Schrump D.S. Apoptosis induced by depsipeptide FK228 coincides with inhibition of survival signaling in lung cancer cells. Cancer J. 13 (2007) 105-113
56. Coussens L.M., and Werb Z. Inflammation and cancer. Nature 420 (2002) 860-867
57. Mantovani A., Allavena P., Sica A., and Balkwill F. Cancer-related inflammation. Nature 454 (2008) 436-444
58. Culp W.D., Tsagozis P., Burgio M., Russell P., Pisa P., and Garland D. Interference of macrophage migration inhibitory factor expression in a mouse melanoma inhibits tumor establishment by up-regulating thrombospondin-1. Mol. Cancer Res. 5 (2007) 1225-1231
59. Hagemann T., Robinson S.C., Thompson R.G., Charles K., Kulbe H., and Balkwill F.R. Ovarian cancer cell-derived migration inhibitory factor enhances tumor growth, progression, and angiogenesis. Mol. Cancer Ther. 6 (2007) 1993-2002
60. Ren Y., Chan H.M., Fan J., Xie Y., Chen Y.X., Li W., Jiang G.P., Liu Q., Meinhardt A., and Tam P.K. Inhibition of tumor growth and metastasis in vitro and in vivo by targeting macrophage migration inhibitory factor in human neuroblastoma. Oncogene 25 (2006) 3501-3508
61. Fingerle-Rowson G., Petrenko O., Metz C.N., Forsthuber T.G., Mitchell R., Huss R., Moll U., Muller W., and Bucala R. The p53-dependent effects of macrophage migration inhibitory factor revealed by gene targeting. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 9354-9359
62. Taylor III J.A., Kuchel G.A., Hegde P., Voznesensky O.S., Claffey K., Tsimikas J., Leng L., Bucala R., and Pilbeam C. Null mutation for macrophage migration inhibitory factor (MIF) is associated with less aggressive bladder cancer in mice. BMC Cancer 7 (2007) 135