Epigenetic repression of matrix metalloproteinases in myofibroblastic hepatic stellate cells through histone deacetylases 4: Implication in tissue fibrosis

American Journal of Pathology

Volumn 177, Issue 4, 2010, Pages 1915-1928

  Qin, Lan ^a   Han, Yuan Ping ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA ACTIN; COLLAGENASE 3; DESMIN; GELATINASE B; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HISTONE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1ALPHA; LAMIN A; LAMIN C; MATRIX METALLOPROTEINASE; PROTEIN C JUN; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL DIFFERENTIATION; CHROMATIN; CONTROLLED STUDY; EPIGENETICS; EXTRACELLULAR MATRIX; GENE REPRESSION; LIVER FIBROSIS; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STELLATE CELL;

EID: 77957331903     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100011     Document Type: Article

References (60)

1. Werb Z, Chin JR: Extracellular matrix remodeling during morphogenesis. Ann NY Acad Sci 1998, 857:110-118
2. Friedman SL: Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev 2008, 88:125-172
3. Alcolado R, Arthur MJ, Iredale JP: Pathogenesis of liver fibrosis. Clin Sci (Lond) 1997, 92:103-112
4. Bataller R, Brenner DA: Liver fibrosis. J Clin Invest 2005, 115:209-218
5. Reeves HL, Friedman SL: Activation of hepatic stellate cells-a key issue in liver fibrosis. Front Biosci 2002, 7:d808-d826
6. Geerts A: History, heterogeneity, developmental biology, and functions of quiescent hepatic stellate cells. Semin Liver Dis 2001, 21:311-335
7. Schuppan D, Ruehl M, Somasundaram R, Hahn EG: Matrix as a modulator of hepatic fibrogenesis. Semin Liver Dis 2001, 21:351-372
8. Yan C, Zhou L, Han YP: Contribution of hepatic stellate cells and matrix metalloproteinase 9 in acute liver failure. Liver Int 2008, 27:959-971
9. Yu Q, Stamenkovic I: Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 2000, 14:163-176
10. Reynaert H, Thompson MG, Thomas T, Geerts A: Hepatic stellate cells: role in microcirculation and pathophysiology of portal hypertension. Gut 2002, 50:571-581
11. Wells RG: The role of matrix stiffness in hepatic stellate cell activation and liver fibrosis. J Clin Gastroenterol 2005, 39:S158-S161
12. Kisseleva T, Brenner DA: Role of hepatic stellate cells in fibrogenesis and the reversal of fibrosis. J Gastroenterol Hepatol 2007, 22 Suppl 1:S73-S78
13. Rockey DC, Weisiger RA: Endothelin induced contractility of stellate cells from normal and cirrhotic rat liver: implications for regulation of portal pressure and resistance. Hepatology 1996, 24:233-240
14. Parsons CJ, Takashima M, Rippe RA: Molecular mechanisms of hepatic fibrogenesis. J Gastroenterol Hepatol 2007, 22 Suppl 1:S79-S84
15. Han YP, Zhou L, Wang J, Xiong S, Garner WL, French SW, Tsukamoto H: Essential role of matrix metalloproteinases in interleukin-1-induced myofibroblastic activation of hepatic stellate cell in collagen. J Biol Chem 2004, 279:4820-4828
16. Han YP, Tuan TL, Hughes M, Wu H, Garner WL: Transforming growth factor-beta - and tumor necrosis factor-alpha - mediated induction and proteolytic activation of MMP-9 in human skin. J Biol Chem 2001, 276:22341-22350
17. Zhou L, Yan C, Gieling RG, Kida Y, Garner W, Li W, Han YP: Tumor necrosis factor-alpha induced expression of matrix metalloproteinase-9 through p21-activated kinase-1. BMC Immunol 2009, 10:15
18. Wielockx B, Lannoy K, Shapiro SD, Itoh T, Itohara S, Vandekerckhove J, Libert C: Inhibition of matrix metalloproteinases blocks lethal hepatitis and apoptosis induced by tumor necrosis factor and allows safe antitumor therapy. Nat Med 2001, 7:1202-1208
19. Gum R, Lengyel E, Juarez J, Chen JH, Sato H, Seiki M, Boyd D: Stimulation of 92-kDa gelatinase B promoter activity by ras is mitogen-activated protein kinase kinase 1-independent and requires multiple transcription factor binding sites including closely spaced PEA3/ets and AP-1 sequences. J Biol Chem 1996, 271:10672-10680
20. Eberhardt W, Akool el S, Rebhan J, Frank S, Beck KF, Franzen R, Hamada FM, Pfeilschifter J: Inhibition of cytokine-induced matrix metalloproteinase 9 expression by peroxisome proliferator-activated receptor alpha agonists is indirect and due to a NO-mediated reduction of mRNA stability. J Biol Chem 2002, 277:33518-33528
21. Verdone L, Caserta M, Di Mauro E: Role of histone acetylation in the control of gene expression. Biochem Cell Biol 2005, 83:344-353
22. Clayton AL, Hazzalin CA, Mahadevan LC: Enhanced histone acetylation and transcription: a dynamic perspective. Mol Cell 2006, 23:289-296
23. O'Neill LP, Turner BM: Histone H4 acetylation distinguishes coding regions of the human genome from heterochromatin in a differentiation-dependent but transcription-independent manner. EMBO J 1995, 14:3946-3957
24. Ausio J, van Holde KE: Histone hyperacetylation: its effects on nucleosome conformation and stability. Biochemistry 1986, 25:1421-1428
25. Vermeulen M, Walter W, Le Guezennec X, Kim J, Edayathumangalam RS, Lasonder E, Luger K, Roeder RG, Logie C, Berger SL, Stunnenberg HG: A feed-forward repression mechanism anchors the Sin3/histone deacetylase and N-CoR/SMRT corepressors on chromatin. Mol Cell Biol 2006, 26:5226-5236
26. Kurdistani SK, Grunstein M: Histone acetylation and deacetylation in yeast. Nat Rev Mol Cell Biol 2003, 4:276-284
27. Hassig CA, Tong JK, Fleischer TC, Owa T, Grable PG, Ayer DE, Schreiber SL: A role for histone deacetylase activity in HDAC1-mediated transcriptional repression. Proc Natl Acad Sci USA 1998, 95:3519-3524
28. Yang XJ, Gregoire S: Class II histone deacetylases: from sequence to function, regulation, and clinical implication. Mol Cell Biol 2005, 25:2873-2884
29. Wolffe AP: Histone deacetylase: a regulator of transcription. Science 1996, 272:371-372
30. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB: Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 2003, 370:737-749
31. Friedman SL, Rockey DC, McGuire RF, Maher JJ, Boyles JK, Yamasaki G: Isolated hepatic lipocytes and Kupffer cells from normal human liver: morphological and functional characteristics in primary culture. Hepatology 1992, 15:234-243
32. Tsukamoto H, Cheng S, Blaner WS: Effects of dietary polyunsaturated fat on ethanol-induced Ito cell activation. Am J Physiol 1996, 270:G581-G586
33. Dahl JA, Collas P: A rapid micro chromatin immunoprecipitation assay (microChIP). Nat Protoc 2008, 3:1032-1045
34. Arthur MJ: Collagenases and liver fibrosis. J Hepatol 1995, 22:43-48
35. Han YP, Yan C, Zhou L, Qin L, Tsukamoto H: A matrix metalloproteinase-9 activation cascade by hepatic stellate cells in trans-differentiation in the three-dimensional extracellular matrix. J Biol Chem 2007, 282:12928-12939
36. Sato H, Kita M, Seiki M: v-Src activates the expression of 92-kDa type IV collagenase gene through the AP-1 site and the GT box homologous to retinoblastoma control elements. A mechanism regulating gene expression independent of that by inflammatory cytokines. J Biol Chem 1993, 268:23460-23468
37. Takahra T, Smart DE, Oakley F, Mann DA: Induction of myofibroblast MMP-9 transcription in three-dimensional collagen I gel cultures: regulation by NF-kappaB. AP-1 and Sp1. Int J Biochem Cell Biol 2004, 36:353-363
38. Tanimura S, Asato K, Fujishiro SH, Kohno M: Specific blockade of the ERK pathway inhibits the invasiveness of tumor cells: down-regulation of matrix metalloproteinase-3/-9/-14 and CD44. Biochem Biophys Res Commun 2003, 304:801-806
39. Raymond L, Eck S, Mollmark J, Hays E, Tomek I, Kantor S, Elliott S, Vincenti M: Interleukin-1 beta induction of matrix metalloproteinase-1 transcription in chondrocytes requires ERK-dependent activation of CCAAT enhancer-binding protein-beta. J Cell Physiol 2006, 207:683-688
40. Yan C, Boyd DD: Regulation of matrix metalloproteinase gene expression. J Cell Physiol 2007, 211:19-26
41. Nelson DE, Ihekwaba AE, Elliott M, Johnson JR, Gibney CA, Foreman BE, Nelson G, See V, Horton CA, Spiller DG, Edwards SW, McDowell HP, Unitt JF, Sullivan E, Grimley R, Benson N, Broomhead D, Kell DB, White MR: Oscillations in NF-kappaB signaling control the dynamics of gene expression. Science 2004, 306:704-708 (Pubitemid 39440922)
42. Komarnitsky P, Cho EJ, Buratowski S: Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev 2000, 14:2452-2460
43. Birkedal-Hansen H, Moore WG, Bodden MK, Windsor LJ, Birkedal-Hansen B, DeCarlo A, Engler JA: Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 1993, 4:197-250
44. Page-McCaw A, Ewald AJ, Werb Z: Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 2007, 8:221-233
45. Wysocki AB, Staiano-Coico L, Grinnell F: Wound fluid from chronic leg ulcers contains elevated levels of metalloproteinases MMP-2 and MMP-9. J Invest Dermatol 1993, 101:64-68
46. Friedman SL, Roll FJ, Boyles J, Bissell DM: Hepatic lipocytes: the principal collagen-producing cells of normal rat liver. Proc Natl Acad Sci USA 1985, 82:8681-8685
47. Arthur MJ, Friedman SL, Roll FJ, Bissell DM: Lipocytes from normal rat liver release a neutral metalloproteinase that degrades basement membrane (type IV) collagen. J Clin Invest 1989, 84:1076-1085
48. Mutskov V, Felsenfeld G: Silencing of transgene transcription precedes methylation of promoter DNA and histone H3 lysine 9. EMBO J 2004, 23:138-149
49. Hassig CA, Schreiber SL: Nuclear histone acetylases and deacetylases and transcriptional regulation: HATs off to HDACs. Curr Opin Chem Biol 1997, 1:300-308
50. Heinzel T, Lavinsky RM, Mullen TM, Soderstrom M, Laherty CD, Torchia J, Yang WM, Brard G, Ngo SD, Davie JR, Seto E, Eisenman RN, Rose DW, Glass CK, Rosenfeld MG: A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature 1997, 387:43-48
51. Razin A: CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J 1998, 17:4905-4908
52. El-Osta A, Wolffe AP: DNA methylation and histone deacetylation in the control of gene expression: basic biochemistry to human development and disease. Gene Expr 2000, 9:63-75
53. Mann J, Oakley F, Akiboye F, Elsharkawy A, Thorne AW, Mann DA: Regulation of myofibroblast transdifferentiation by DNA methylation and MeCP2: implications for wound healing and fibrogenesis. Cell Death Differ 2007, 14:275-285
54. Jin C, Li H, Murata T, Sun K, Horikoshi M, Chiu R, Yokoyama KK: JDP2, a repressor of AP-1, recruits a histone deacetylase 3 complex to inhibit the retinoic acid-induced differentiation of F9 cells. Mol Cell Biol 2002, 22:4815-4826
55. Gu W, Roeder RG: Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 1997, 90:595-606
56. Boyes J, Byfield P, Nakatani Y, Ogryzko V: Regulation of activity of the transcription factor GATA-1 by acetylation. Nature 1998, 396:594-598 (Pubitemid 28563723)
57. Chen LF, Mu Y, Greene WC: Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J 2002, 21:6539-6548
58. Knittel T, Mehde M, Kobold D, Saile B, Dinter C, Ramadori G: Expression patterns of matrix metalloproteinases and their inhibitors in parenchymal and non-parenchymal cells of rat liver: regulation by TNF-alpha and TGF-beta1. J Hepatol 1999, 30:48-60
59. Watanabe T, Niioka M, Ishikawa A, Hozawa S, Arai M, Maruyama K, Okada A, Okazaki I: Dynamic change of cells expressing MMP-2 mRNA and MT1-MMP mRNA in the recovery from liver fibrosis in the rat. J Hepatol 2001, 35:465-473
60. Iredale JP, Benyon RC, Arthur MJ, Ferris WF, Alcolado R, Winwood PJ, Clark N, Murphy G: Tissue inhibitor of metalloproteinase-1 messenger RNA expression is enhanced relative to interstitial collagenase messenger RNA in experimental liver injury and fibrosis. Hepatology 1996, 24:176-184