HDAC-mediated control of ERK- and PI3K-dependent TGF-β-induced extracellular matrix-regulating genes

Matrix Biology

Volumn 29, Issue 7, 2010, Pages 602-612

  Barter, Matt J ^a   Pybus, Leon ^a   Litherland, Gary J ^a   Rowan, Andrew D ^a   Clark, Ian M ^b   Edwards, Dylan R ^b   Cawston, Tim E ^a   Young, David A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

ADAM12; ERK; HDAC3; Histone deacetylases; PI3K; Signalling; TGF ; TIMP 1

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; A DISINTEGRIN AND METALLOPROTEINASE 12; ADAM PROTEIN; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; APICIDIN; HISTONE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PLASMINOGEN ACTIVATOR INHIBITOR 1; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD7 PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA; TRICHOSTATIN A; UNCLASSIFIED DRUG; VALPROIC ACID;

ACETYLATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; FIBROBLAST; GENE CONTROL; GENE EXPRESSION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ADAM PROTEINS; ANIMALS; ENZYME INHIBITORS; EXTRACELLULAR MATRIX; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; GENE EXPRESSION; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONES; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-RAF; RNA, SMALL INTERFERING; SERPIN E2; SIGNAL TRANSDUCTION; SMAD PROTEINS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TRANSCRIPTION FACTOR AP-1; TRANSFORMING GROWTH FACTOR BETA;

EID: 77957752356     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2010.05.002     Document Type: Article

References (47)

1. Bain J., Plater L., Elliott M., Shpiro N., Hastie C.J., McLauchlan H., Klevernic I., Arthur J.S., Alessi D.R., Cohen P. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 2007, 408:297-315.
2. Cao W., Bao C., Padalko E., Lowenstein C.J. Acetylation of mitogen-activated protein kinase phosphatase-1 inhibits Toll-like receptor signaling. J. Exp. Med. 2008, 205:1491-1503.
3. Chen L., Fischle W., Verdin E., Greene W.C. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 2001, 293:1653-1657.
4. Chen C.S., Weng S.C., Tseng P.H., Lin H.P., Chen C.S. Histone acetylation-independent effect of histone deacetylase inhibitors on Akt through the reshuffling of protein phosphatase 1 complexes. J. Biol. Chem. 2005, 280:38879-38887.
5. Cho H.J., Baek K.E., Saika S., Jeong M.J., Yoo J. Snail is required for transforming growth factor-beta-induced epithelial-mesenchymal transition by activating PI3 kinase/Akt signal pathway. Biochem. Biophys. Res. Commun. 2007, 353:337-343.
6. Clayton A.L., Hazzalin C.A., Mahadevan L.C. Enhanced histone acetylation and transcription: a dynamic perspective. Mol. Cell 2006, 23:289-296.
7. de Ruijter A.J., van Gennip A.H., Caron H.N., Kemp S., van Kuilenburg A.B. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J. 2003, 370:737-749.
8. Denker A.E., Nicoll S.B., Tuan R.S. Formation of cartilage-like spheroids by micromass cultures of murine C3H10T1/2 cells upon treatment with transforming growth factor-beta 1. Differentiation 1995, 59:25-34.
9. Dennler S., Itoh S., Vivien D., ten Dijke P., Huet S., Gauthier J.M. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. Embo J. 1998, 17:3091-3100.
10. Derynck R., Zhang Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003, 425:577-584.
11. Fecteau K.A., Mei J., Wang H.C. Differential modulation of signaling pathways and apoptosis of ras-transformed 10T1/2 cells by the depsipeptide FR901228. J. Pharmacol. Exp. Ther. 2002, 300:890-899.
12. Ghosh A.K., Mori Y., Dowling E., Varga J. Trichostatin A blocks TGF-beta-induced collagen gene expression in skin fibroblasts: involvement of Sp1. Biochem. Biophys. Res. Commun. 2007, 354:420-426.
13. Glenisson W., Castronovo V., Waltregny D. Histone deacetylase 4 is required for TGFbeta1-induced myofibroblastic differentiation. Biochim. Biophys. Acta 2007, 1773:1572-1582.
14. Glozak M.A., Sengupta N., Zhang X., Seto E. Acetylation and deacetylation of non-histone proteins. Gene 2005, 363:15-23.
15. Gottlicher M., Minucci S., Zhu P., Kramer O.H., Schimpf A., Giavara S., Sleeman J.P., Lo Coco F., Nervi C., Pelicci P.G., Heinzel T. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. Embo J. 2001, 20:6969-6978.
16. Gregoretti I.V., Lee Y.M., Goodson H.V. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J. Mol. Biol. 2004, 338:17-31.
17. Gurvich N., Tsygankova O.M., Meinkoth J.L., Klein P.S. Histone deacetylase is a target of valproic acid-mediated cellular differentiation. Cancer Res. 2004, 64:1079-1086.
18. Hazzalin C.A., Mahadevan L.C. Dynamic acetylation of all lysine 4-methylated histone H3 in the mouse nucleus: analysis at c-fos and c-jun. PLoS Biol. 2005, 3:e393.
19. Horowitz J.C., Lee D.Y., Waghray M., Keshamouni V.G., Thomas P.E., Zhang H., Cui Z., Thannickal V.J. Activation of the pro-survival phosphatidylinositol 3-kinase/AKT pathway by transforming growth factor-beta1 in mesenchymal cells is mediated by p38 MAPK-dependent induction of an autocrine growth factor. J. Biol. Chem. 2004, 279:1359-1367.
20. Khan N., Jeffers M., Kumar S., Hackett C., Boldog F., Khramtsov N., Qian X., Mills E., Berghs S.C., Carey N., Finn P.W., Collins L.S., Tumber A., Ritchie J.W., Jensen P.B., Lichenstein H.S., Sehested M. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J. 2008, 409:581-589.
21. Kobayashi Y., Ohtsuki M., Murakami T., Kobayashi T., Sutheesophon K., Kitayama H., Kano Y., Kusano E., Nakagawa H., Furukawa Y. Histone deacetylase inhibitor FK228 suppresses the Ras-MAP kinase signaling pathway by upregulating Rap1 and induces apoptosis in malignant melanoma. Oncogene 2006, 25:512-524.
22. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
23. Kuang P.P., Zhang X.H., Rich C.B., Foster J.A., Subramanian M., Goldstein R.H. Activation of elastin transcription by transforming growth factor-beta in human lung fibroblasts. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 292:L944-L952.
24. Kwak H.J., Park M.J., Cho H., Park C.M., Moon S.I., Lee H.C., Park I.C., Kim M.S., Rhee C.H., Hong S.I. Transforming growth factor-beta1 induces tissue inhibitor of metalloproteinase-1 expression via activation of extracellular signal-regulated kinase and Sp1 in human fibrosarcoma cells. Mol. Cancer Res. 2006, 4:209-220.
25. Le Pabic H., Bonnier D., Wewer U.M., Coutand A., Musso O., Baffet G., Clement B., Theret N. ADAM12 in human liver cancers: TGF-beta-regulated expression in stellate cells is associated with matrix remodeling. Hepatology 2003, 37:1056-1066.
26. Le Pabic H., L'Helgoualc'h A., Coutant A., Wewer U.M., Baffet G., Clement B., Theret N. Involvement of the serine/threonine p70S6 kinase in TGF-beta1-induced ADAM12 expression in cultured human hepatic stellate cells. J. Hepatol. 2005, 43:1038-1044.
27. Lee M.K., Pardoux C., Hall M.C., Lee P.S., Warburton D., Qing J., Smith S.M., Derynck R. TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. Embo J. 2007, 26:3957-3967.
28. Li B., Carey M., Workman J.L. The role of chromatin during transcription. Cell 2007, 128:707-719.
29. Lien S.C., Usami S., Chien S., Chiu J.J. Phosphatidylinositol 3-kinase/Akt pathway is involved in transforming growth factor-beta1-induced phenotypic modulation of 10T1/2 cells to smooth muscle cells. Cell. Signal. 2006, 18:1270-1278.
30. Litherland G.J., Dixon C., Lakey R.L., Robson T., Jones D., Young D.A., Cawston T.E., Rowan A.D. Synergistic collagenase expression and cartilage collagenolysis are phosphatidylinositol 3-kinase/Akt signaling-dependent. J. Biol. Chem. 2008, 283:14221-14229.
31. 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, 173:3979-3990.
32. Michaelis M., Suhan T., Michaelis U.R., Beek K., Rothweiler F., Tausch L., Werz O., Eikel D., Zornig M., Nau H., Fleming I., Doerr H.W., Cinatl J. Valproic acid induces extracellular signal-regulated kinase 1/2 activation and inhibits apoptosis in endothelial cells. Cell Death Differ. 2006, 13:446-453.
33. Rombouts K., Niki T., Greenwel P., Vandermonde A., Wielant A., Hellemans K., De Bleser P., Yoshida M., Schuppan D., Rojkind M., Geerts A. Trichostatin A, a histone deacetylase inhibitor, suppresses collagen synthesis and prevents TGF-beta(1)-induced fibrogenesis in skin fibroblasts. Exp. Cell Res. 2002, 278:184-197.
34. Shi Y., Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003, 113:685-700.
35. Togi S., Kamitani S., Kawakami S., Ikeda O., Muromoto R., Nanbo A., Matsuda T. HDAC3 influences phosphorylation of STAT3 at serine 727 by interacting with PP2A. Biochem. Biophys. Res. Commun. 2009, 379:616-620.
36. Tu A.W., Luo K. Acetylation of Smad2 by the co-activator p300 regulates activin and transforming growth factor beta response. J. Biol. Chem. 2007, 282:21187-21196.
37. Vannini A., Volpari C., Filocamo G., Casavola E.C., Brunetti M., Renzoni D., Chakravarty P., Paolini C., De Francesco R., Gallinari P., Steinkuhler C., Di Marco S. Crystal structure of a eukaryotic zinc-dependent histone deacetylase, human HDAC8, complexed with a hydroxamic acid inhibitor. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:15064-15069.
38. Verdin E., Dequiedt F., Kasler H.G. Class II histone deacetylases: versatile regulators. Trends Genet. 2003, 19:286-293.
39. Wang E.A., Israel D.I., Kelly S., Luxenberg D.P. Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells. Growth Factors 1993, 9:57-71.
40. Whitmarsh A.J., Shore P., Sharrocks A.D., Davis R.J. Integration of MAP kinase signal transduction pathways at the serum response element. Science 1995, 269:403-407.
41. Wrana J.L., Attisano L., Carcamo J., Zentella A., Doody J., Laiho M., Wang X.F., Massague J. TGF beta signals through a heteromeric protein kinase receptor complex. Cell 1992, 71:1003-1014.
42. Xu W.S., Parmigiani R.B., Marks P.A. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007, 26:5541-5552.
43. Yamaguchi K., Lantowski A., Dannenberg A.J., Subbaramaiah K. Histone deacetylase inhibitors suppress the induction of c-Jun and its target genes including COX-2. J. Biol. Chem. 2005, 280:32569-32577.
44. Yoshikawa M., Hishikawa K., Marumo T., Fujita T. Inhibition of histone deacetylase activity suppresses epithelial-to-mesenchymal transition induced by TGF-beta1 in human renal epithelial cells. J. Am. Soc. Nephrol. 2007, 18:58-65.
45. Young D.A., Billingham O., Sampieri C.L., Edwards D.R., Clark I.M. Differential effects of histone deacetylase inhibitors on phorbol ester- and TGF-beta1 induced murine tissue inhibitor of metalloproteinases-1 gene expression. Febs J. 2005, 272:1912-1926.
46. Yu X., Guo Z.S., Marcu M.G., Neckers L., Nguyen D.M., Chen G.A., Schrump D.S. Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J. Natl. Cancer Inst. 2002, 94:504-513.
47. Zhang S., Fei T., Zhang L., Zhang R., Chen F., Ning Y., Han Y., Feng X.H., Meng A., Chen Y.G. Smad7 antagonizes transforming growth factor beta signaling in the nucleus by interfering with functional Smad-DNA complex formation. Mol. Cell. Biol. 2007, 27:4488-4499.