Journal of Molecular and Cellular Cardiology
Volume 46, Issue 3 , Pages 292-299 , March 2009

HDAC2 deacetylates class II transactivator and suppresses its activity in macrophages and smooth muscle cells

  • Xiaocen Kong

      Affiliations

    • Atherosclerosis Research Center, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • Department of Pathophysiology, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • ,
  • Mingming Fang

      Affiliations

    • Atherosclerosis Research Center, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • Department of Pathophysiology, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • Jiangsu Provincial School of Continued Medical Education, Nanjing, Jiangsu 210029, China
    • ,
  • Ping Li

      Affiliations

    • Atherosclerosis Research Center, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • Department of Pathophysiology, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • ,
  • Fei Fang

      Affiliations

    • Atherosclerosis Research Center, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • Department of Pathophysiology, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • ,
  • Yong Xu

      Affiliations

    • Atherosclerosis Research Center, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • Department of Pathophysiology, Nanjing Medical University, Nanjing, Jiangsu 210029, China
    • Corresponding Author InformationCorresponding author. Atherosclerosis Research Center and Department of Pathophysiology, Nanjing Medical University, 140 Hanzhong Road, Nanjing, Jiangsu 210029, China. Tel.: +86 25 6862888; fax: +86 25 6862888.

Received 13 September 2008 ,Revised 24 October 2008 ,Accepted 28 October 2008.

References 

  1. Libby P. Inflammation in atherosclerosis. Nature. 2002 Dec 19–26;420(6917):868–874
  2. Katsuda S, Kaji T. Atherosclerosis and extracellular matrix. J. Atheroscler. Thromb. 2003;10(5):267–274
  3. Xu QB, Oberhuber G, Gruschwitz M, Wick G. Immunology of atherosclerosis: cellular composition and major histocompatibility complex class II antigen expression in aortic intima, fatty streaks, and atherosclerotic plaques in young and aged human specimens. Clin. Immunol. Immunopathol. 1990 Sep;56(3):344–359
  4. Gurfinkel E, Bozovich G. Chlamydia pneumoniae: inflammation and instability of the atherosclerotic plaque. Atherosclerosis. 1998 Oct;140(Suppl 1):S31–35
  5. McCullagh KG, Ehrhart LA. Enhanced synthesis and accumulation of collagen in cholesterol-aggravated pigeon atherosclerosis. Atherosclerosis. 1977 Mar;26(3):341–352
  6. McCullagh KG. Increased type I collagen in human atherosclerotic plaque. Atherosclerosis. 1983 Feb;46(2):247–248
  7. Hansson GK, Hellstrand M, Rymo L, Rubbia L, Gabbiani G. Interferon gamma inhibits both proliferation and expression of differentiation-specific alpha-smooth muscle actin in arterial smooth muscle cells. J. Exp. Med. 1989 Nov 1;170(5):1595–1608
  8. Amento EP, Ehsani N, Palmer H, Libby P. Cytokines and growth factors positively and negatively regulate interstitial collagen gene expression in human vascular smooth muscle cells. Arterioscler. Thromb. 1991 Sep-Oct;11(5):1223–1230
  9. Libby P, Sukhova G, Lee RT, Galis ZS. Cytokines regulate vascular functions related to stability of the atherosclerotic plaque. J. Cardiovasc. Pharmacol. 1995;25(Suppl 2):S9–12
  10. Kusaba K, Kai H, Koga M, Takayama N, Ikeda A, Yasukawa H, et al. Inhibition of intrinsic interferon-gamma function prevents neointima formation after balloon injury. Hypertension. 2007 Apr;49(4):909–915
  11. Zohlnhofer D, Richter T, Neumann F, Nuhrenberg T, Wessely R, Brandl R, et al. Transcriptome analysis reveals a role of interferon-gamma in human neointima formation. Mol. Cell. 2001 May;7(5):1059–1069
  12. Koga M, Kai H, Yasukawa H, Yamamoto T, Kawai Y, Kato S, et al. Inhibition of progression and stabilization of plaques by postnatal interferon-gamma function blocking in ApoE-knockout mice. Circ. Res. 2007 Aug 17;101(4):348–356
  13. Xu Y, McDonald J, Perloff E, Buttice G, Schreiber BM, Smith BD. Collagen and major histocompatibility class II expression in mesenchymal cells from CIITA hypomorphic mice. Mol. Immunol. 2007 Mar;44(7):1709–1721
  14. Buttice G, Miller J, Wang L, Smith BD. Interferon-gamma induces major histocompatibility class II transactivator (CIITA), which mediates collagen repression and major histocompatibility class II activation by human aortic smooth muscle cells. Circ. Res. 2006 Mar 3;98(4):472–479
  15. Huang L. Targeting histone deacetylases for the treatment of cancer and inflammatory diseases. J. Cell. Physiol. 2006 Dec;209(3):611–616
  16. Whetstine JR, Ceron J, Ladd B, Dufourcq P, Reinke V, Shi Y. Regulation of tissue-specific and extracellular matrix-related genes by a class I histone deacetylase. Mol. Cell. 2005 May 13;18(4):483–490
  17. Reith W, Mach B. The bare lymphocyte syndrome and the regulation of MHC expression. Annu. Rev. Immunol. 2001;19:331–373
  18. Sisk TJ, Gourley T, Roys S, Chang CH. MHC class II transactivator inhibits IL-4 gene transcription by competing with NF-AT to bind the coactivator CREB binding protein (CBP)/p300. J. Immunol. 2000 Sep 1;165(5):2511–2517
  19. Yee CS, Yao Y, Xu Q, McCarthy B, Sun-Lin D, Tone M, et al. Enhanced production of IL-10 by dendritic cells deficient in CIITA. J. Immunol. 2005 Feb 1;174(3):1222–1229
  20. Nozell S, Ma Z, Wilson C, Shah R, Benveniste EN. Class II major histocompatibility complex transactivator (CIITA) inhibits matrix metalloproteinase-9 gene expression. J. Biol. Chem. 2004 Sep 10;279(37):38577–38589
  21. Wong AW, Brickey WJ, Taxman DJ, van Deventer HW, Reed W, Gao JX, et al. CIITA-regulated plexin-A1 affects T-cell-dendritic cell interactions. Nat. Immunol. 2003 Sep;4(9):891–898
  22. Zhu XS, Ting JP. A 36-amino-acid region of CIITA is an effective inhibitor of CBP: novel mechanism of gamma interferon-mediated suppression of collagen alpha(2)(I) and other promoters. Mol. Cell. Biol. 2001 Oct;21(20):7078–7088
  23. Xu Y, Wang L, Buttice G, Sengupta PK, Smith BD. Major histocompatibility class II transactivator (CIITA) mediates repression of collagen (COL1A2) transcription by interferon gamma (IFN-gamma). J. Biol. Chem. 2004 Oct 1;279(40):41319–41332
  24. Spilianakis C, Papamatheakis J, Kretsovali A. Acetylation by PCAF enhances CIITA nuclear accumulation and transactivation of major histocompatibility complex class II genes. Mol. Cell. Biol. 2000 Nov;20(22):8489–8498
  25. Zika E, Greer SF, Zhu XS, Ting JP. Histone deacetylase 1/mSin3A disrupts gamma interferon-induced CIITA function and major histocompatibility complex class II enhanceosome formation. Mol. Cell. Biol. 2003 May;23(9):3091–3102
  26. Xu Y, Harton JA, Smith BD. CIITA mediates interferon-gamma repression of collagen transcription through phosphorylation-dependent interactions with co-repressor molecules. J. Biol. Chem. 2008 Jan 18;283(3):1243–1256
  27. Tsai SC, Seto E. Regulation of histone deacetylase 2 by protein kinase CK2. J. Biol. Chem. 2002 Aug 30;277(35):31826–31833
  28. Zhang X, Wharton W, Yuan Z, Tsai SC, Olashaw N, Seto E. Activation of the growth-differentiation factor 11 gene by the histone deacetylase (HDAC) inhibitor trichostatin A and repression by HDAC3. Mol. Cell. Biol. 2004 Jun;24(12):5106–5118
  29. Xu Y, Ravid K, Smith BD. Major histocompatibility Class II transactivator expression in smooth muscle cells from A2b adenosine receptor knock-out mice: cross-talk between the adenosine and interferon-{gamma} signaling. J. Biol. Chem. 2008 May 23;283(21):14213–14220
  30. Masternak K, Muhlethaler-Mottet A, Villard J, Zufferey M, Steimle V, Reith W. CIITA is a transcriptional coactivator that is recruited to MHC class II promoters by multiple synergistic interactions with an enhanceosome complex. Genes Dev. 2000 May 1;14(9):1156–1166
  31. Hansson GK, Libby P, Schonbeck U, Yan ZQ. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ. Res. 2002 Aug 23;91(4):281–291
  32. Barnes MJ, Farndale RW. Collagens and atherosclerosis. Exp. Gerontol. 1999 Jul;34(4):513–525
  33. Xu Y, Sengupta PK, Seto E, Smith BD. Regulatory factor for X-box family proteins differentially interact with histone deacetylases to repress collagen alpha2(I) gene (COL1A2) expression. J. Biol. Chem. 2006 Apr 7;281(14):9260–9270
  34. Glauben R, Batra A, Fedke I, Zeitz M, Lehr HA, Leoni F, et al. Histone hyperacetylation is associated with amelioration of experimental colitis in mice. J. Immunol. 2006 Apr 15;176(8):5015–5022
  35. Chung YL, Lee MY, Wang AJ, Yao LF. A therapeutic strategy uses histone deacetylase inhibitors to modulate the expression of genes involved in the pathogenesis of rheumatoid arthritis. Molec. Ther. 2003 Nov;8(5):707–717
  36. Choi JH, Nam KH, Kim J, Baek MW, Park JE, Park HY, et al. Trichostatin A exacerbates atherosclerosis in low density lipoprotein receptor-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2005 Nov;25(11):2404–2409
  37. Trivedi CM, Patel RC, Patel CV. Homeobox gene HOXA9 inhibits nuclear factor-kappa B dependent activation of endothelium. Atherosclerosis. 2007 Dec;195(2):e50–60
  38. Xu Y, Wang L, Buttice G, Sengupta PK, Smith BD. Interferon gamma repression of collagen (COL1A2) transcription is mediated by the RFX5 complex. J. Biol. Chem. 2003 Dec 5;278(49):49134–49144
  39. Morimoto Y, Toyota M, Satoh A, Murai M, Mita H, Suzuki H, et al. Inactivation of class II transactivator by DNA methylation and histone deacetylation associated with absence of HLA-DR induction by interferon-gamma in haematopoietic tumour cells. Br. J. Cancer. 2004 Feb 23;90(4):844–852
  40. Yao Y, Xu Q, Kwon MJ, Matta R, Liu Y, Hong SC, et al. ERK and p38 MAPK signaling pathways negatively regulate CIITA gene expression in dendritic cells and macrophages. J. Immunol. 2006 Jul 1;177(1):70–76
  41. Han Y, Zhou ZH, Ransohoff RM. TNF-alpha suppresses IFN-gamma-induced MHC class II expression in HT1080 cells by destabilizing class II trans-activator mRNA. J. Immunol. 1999 Aug 1;163(3):1435–1440
  42. Greer SF, Zika E, Conti B, Zhu XS, Ting JP. Enhancement of CIITA transcriptional function by ubiquitin. Nat. Immunol. 2003 Nov;4(11):1074–1082
  43. Tosi G, Jabrane-Ferrat N, Peterlin BM. Phosphorylation of CIITA directs its oligomerization, accumulation and increased activity on MHCII promoters. EMBO J. 2002 Oct 15;21(20):5467–5476
  44. Schnappauf F, Hake SB, Camacho Carvajal MM, Bontron S, Lisowska-Grospierre B, Steimle V. N-terminal destruction signals lead to rapid degradation of the major histocompatibility complex class II transactivator CIITA. Eur. J. Immunol. 2003 Aug;33(8):2337–2347
  45. Insinga A, Monestiroli S, Ronzoni S, Carbone R, Pearson M, Pruneri G, et al. Impairment of p53 acetylation, stability and function by an oncogenic transcription factor. EMBO J. 2004 Mar 10;23(5):1144–1154
  46. Harms KL, Chen X. Histone deacetylase 2 modulates p53 transcriptional activities through regulation of p53-DNA binding activity. Cancer Res. 2007 Apr 1;67(7):3145–3152
  47. Napoli C, Balestrieri ML, Sica V, Lerman LO, Crimi E, De Rosa G, et al. Beneficial effects of low doses of red wine consumption on perturbed shear stress-induced atherogenesis. Heart Vessels. 2008 Mar;23(2):124–133
  48. Li X, Zhang S, Blander G, Tse JG, Krieger M, Guarente L. SIRT1 deacetylates and positively regulates the nuclear receptor LXR. Mol. Cell. 2007 Oct 12;28(1):91–106
  49. van der Veer E, Ho C, O'Neil C, Barbosa N, Scott R, Cregan SP, et al. Extension of human cell lifespan by nicotinamide phosphoribosyltransferase. J. Biol. Chem. 2007 Apr 13;282(15):10841–10845

PII: S0022-2828(08)01397-7

doi: 10.1016/j.yjmcc.2008.10.023

Journal of Molecular and Cellular Cardiology
Volume 46, Issue 3 , Pages 292-299 , March 2009

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