HDAC inhibition prevents NF-κB activation by suppressing proteasome activity: Down-regulation of proteasome subunit expression stabilizes IκBα

Biochemical Pharmacology

Volumn 70, Issue 3, 2005, Pages 394-406

  Place, Robert F ^a   Noonan, Emily J ^a   Giardina, Charles ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

1; 2; 5; Butyrate; Caco 2; HDAC; I B ; IL 1 ; NF B; Proteasome; TNF ; TSA

Indexed keywords

ANTINEOPLASTIC AGENT; BUTYRIC ACID; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MESSENGER RNA; PROTEASOME; PROTEIN SUBUNIT; TRICHOSTATIN A; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CANCER CELL CULTURE; CATALYSIS; CELL DIFFERENTIATION; CELL STRAIN CACO 2; COLON CANCER; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BUTYRATES; CACO-2 CELLS; DOWN-REGULATION; HISTONE DEACETYLASES; HT29 CELLS; HUMANS; HYDROXAMIC ACIDS; I-KAPPA B PROTEINS; NF-KAPPA B; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS;

EID: 21344464730     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2005.04.030     Document Type: Article

References (99)

1. W.G. Bennett, and J.J. Cerda Benefits of dietary fiber, Myth or medicine? Postgrad Med 99 2 1996 p. 153-6, 166-8, 171-2 [passim]
2. B.S. Reddy Role of dietary fiber in colon cancer: an overview Am J Med 106 1A 1999 16S 19S [discussion 50S-51S]
3. M.S. Inan The luminal short-chain fatty acid butyrate modulates NF-kappaB activity in a human colonic epithelial cell line Gastroenterology 118 4 2000 724 734
4. A. Toscani, D.R. Soprano, and K.J. Soprano Molecular analysis of sodium butyrate-induced growth arrest Oncogene Res 3 3 1988 223 238
5. R.D. Fusunyan Butyrate switches the pattern of chemokine secretion by intestinal epithelial cells through histone acetylation Mol Med 5 9 1999 631 640
6. W. Scheppach Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis Gastroenterology 103 1 1992 51 56
7. A. Hague Sodium butyrate induces apoptosis in human colonic tumour cell lines in a p53-independent pathway: implications for the possible role of dietary fibre in the prevention of large-bowel cancer Int J Cancer 55 3 1993 498 505
8. G.L. Thomas Enhanced apoptosis in transformed human lung fibroblasts after exposure to sodium butyrate In Vitr Cell Dev Biol Anim 32 8 1996 505 513
9. O.C. Velazquez, and J.L. Rombeau Butyrate potential role in colon cancer prevention and treatment Adv Exp Med Biol 427 1997 169 181
10. C.A. Hassig, J.K. Tong, and S.L. Schreiber Fiber-derived butyrate and the prevention of colon cancer Chem Biol 4 11 1997 783 789
11. A. Csordas Butyrate, aspirin and colorectal cancer Eur J Cancer Prev 5 4 1996 221 231
12. R.I. Breuer Rectal irrigation with short-chain fatty acids for distal ulcerative colitis. Preliminary report Dig Dis Sci 36 2 1991 185 187
13. O. Kanauchi Butyrate from bacterial fermentation of germinated barley foodstuff preserves intestinal barrier function in experimental colitis in the rat model J Gastroenterol Hepatol 14 9 1999 880 888
14. A. Wachtershauser, and J. Stein Rationale for the luminal provision of butyrate in intestinal diseases Eur J Nutr 39 4 2000 164 171
15. L.C. Boffa Suppression of histone deacetylation in vivo and in vitro by sodium butyrate J Biol Chem 253 10 1978 3364 3366
16. H. Kawai Overexpression of histone deacetylase HDAC1 modulates breast cancer progression by negative regulation of estrogen receptor alpha Int J Cancer 107 3 2003 353 358
17. J.H. Choi Expression profile of histone deacetylase 1 in gastric cancer tissues Jpn J Cancer Res 92 12 2001 1300 1304
18. K. Halkidou Upregulation and nuclear recruitment of HDAC1 in hormone refractory prostate cancer Prostate 59 2 2004 177 189
19. P. Zhu Induction of HDAC2 expression upon loss of APC in colorectal tumorigenesis Cancer Cell 5 5 2004 455 463
20. P. Atadja Molecular and cellular basis for the anti-proliferative effects of the HDAC inhibitor LAQ824 Novartis Found Symp 259 2004 249 266 [discussion 266-8, 285-8]
21. W.K. Kelly Phase I clinical trial of histone deacetylase inhibitor: suberoylanilide hydroxamic acid administered intravenously Clin Cancer Res 9 10 Pt 1 2003 3578 3588
22. R. Piekarz, and S. Bates A review of depsipeptide and other histone deacetylase inhibitors in clinical trials Curr Pharm Des 10 19 2004 2289 2298
23. J.M. Mariadason, G.A. Corner, and L.H. Augenlicht 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 16 2000 4561 4572
24. J. Boyes Regulation of activity of the transcription factor GATA-1 by acetylation Nature 396 6711 1998 594 598
25. W. Gu, and R.G. Roeder Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain Cell 90 4 1997 595 606
26. K. Nakano Butyrate activates the WAF1/Cip1 gene promoter through Sp1 sites in a p53-negative human colon cancer cell line J Biol Chem 272 35 1997 22199 22206
27. H. Braun Transcription factor Sp3 is regulated by acetylation Nucleic Acids Res 29 24 2001 4994 5000
28. J.P. Segain Butyrate inhibits inflammatory responses through NF-kappaB inhibition: implications for Crohn's disease Gut 47 3 2000 397 403
29. G.D. Wu High-level expression of I kappa B-beta in the surface epithelium of the colon: in vitro evidence for an immunomodulatory role J Leukoc Biol 66 6 1999 1049 1056
30. L. Yin, G. Laevsky, and C. Giardina Butyrate suppression of colonocyte NF-kappa B activation and cellular proteasome activity J Biol Chem 276 48 2001 44641 44646
31. H. Luhrs Butyrate inhibits NF-kappa B activation in lamina propria macrophages of patients with ulcerative colitis Scand J Gastroenterol 37 4 2002 458 466
32. F.R. Greten IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer Cell 118 3 2004 285 296
33. A.S. Baldwin Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights Annu Rev Immunol 14 1996 649 683
34. C. Maaser Colonic epithelial cells induce endothelial cell expression of ICAM-1 and VCAM-1 by a NF-kappa B-dependent mechanism Clin Exp Immunol 124 2 2001 208 213
35. S. Shishodia, and B.B. Aggarwal Nuclear factor-kappa B: a friend or a foe in cancer? Biochem Pharmacol 68 6 2004 1071 1080
36. P.A. Baeuerle I kappa B-NF-kappaB structures: at the interface of inflammation control Cell 95 6 1998 729 731
37. P.A. Baeuerle, and D. Baltimore I kappa B: a specific inhibitor of the NF-kappa B transcription factor Science 242 4878 1988 540 546
38. T.D. Gilmore, and P.J. Morin The I kappa B proteins: members of a multifunctional family Trends Genet 9 12 1993 427 433
39. F. Hirano Alternative splicing variants of I kappa B beta establish differential NF-kappa B signal responsiveness in human cells Mol Cell Biol 18 5 1998 2596 2607
40. S. Haskill Characterization of an immediate-early gene induced in adherent monocytes that encodes I kappa B-like activity Cell 65 7 1991 1281 1289
41. S. Yamazaki, T. Muta, and K. Takeshige A novel I kappa B protein, I kappa B-zeta, induced by proinflammatory stimuli, negatively regulates nuclear factor-kappa B in the nuclei J Biol Chem 276 29 2001 27657 27662
42. I.M. Verma Rel/NF-kappa B/I kappa B family: intimate tales of association and dissociation Genes Dev 9 22 1995 2723 2735
43. R.F. Place Cytokine stabilization of newly synthesized I(kappa)B-alpha Biochem Biophys Res Commun 283 4 2001 813 820
44. R.F. Place, D. Haspeslagh, and C. Giardina Induced stabilization of I kappa B-alpha can facilitate its re-synthesis and prevent sequential degradation J Cell Physiol 195 3 2003 470 478
45. K. Brown Mutual regulation of the transcriptional activator NF-kappa B and its inhibitor, I kappa B-alpha Proc Natl Acad Sci USA 90 6 1993 2532 2536
46. M.L. Scott The p65 subunit of NF-kappa B regulates I kappa B by two distinct mechanisms Genes Dev 7 7A 1993 1266 1276
47. S.C. Sun NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway Science 259 5103 1993 1912 1915
48. Z. Chen Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway Genes Dev 9 13 1995 1586 1597
49. A. Yaron Identification of the receptor component of the I kappa B alpha-ubiquitin ligase Nature 396 6711 1998 590 594
50. D.C. Scherer Signal-induced degradation of I kappa B alpha requires site-specific ubiquitination Proc Natl Acad Sci USA 92 24 1995 11259 11263
51. S. Miyamoto Tumor necrosis factor alpha-induced phosphorylation of I kappa B alpha is a signal for its degradation but not dissociation from NF-kappa B Proc Natl Acad Sci USA 91 26 1994 12740 12744
52. T.S. Finco, A.A. Beg, and A.S. Baldwin Jr. Inducible phosphorylation of I kappa B alpha is not sufficient for its dissociation from NF-kappa B and is inhibited by protease inhibitors Proc Natl Acad Sci USA 91 25 1994 11884 11888
53. L. Catley NVP-LAQ824 is a potent novel histone deacetylase inhibitor with significant activity against multiple myeloma Blood 102 7 2003 2615 2622
54. K.L. Rock Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules Cell 78 5 1994 761 771
55. E. Borenfreund, and O. Borrero In vitro cytotoxicity assays. Potential alternatives to the Draize ocular allergy test Cell Biol Toxicol 1 1 1984 55 65
56. Z. Qin, Y. Wang, and T.N. Chasea A caspase-3-like protease is involved in NF-kappaB activation induced by stimulation of N-methyl-d-aspartate receptors in rat striatum Brain Res Mol Brain Res 80 2 2000 111 122
57. F. Chen Calpain contributes to silica-induced I kappa B-alpha degradation and nuclear factor-kappa B activation Arch Biochem Biophys 342 2 1997 383 388
58. S. Miyamoto, B.J. Seufzer, and S.D. Shumway Novel I kappa B alpha proteolytic pathway in WEHI231 immature B cells Mol Cell Biol 18 1 1998 19 29
59. Y. Han Tumor necrosis factor-alpha-inducible I kappa B alpha proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-kappa B activation J Biol Chem 274 2 1999 787 794
60. Z.H. Nemeth Proteasome inhibitors induce inhibitory kappa B (I kappa B) kinase activation, I kappa B alpha degradation, and nuclear factor kappa B activation in HT-29 cells Mol Pharmacol 65 2 2004 342 349
61. C.Y. Ito, A.G. Kazantsev, and A.S. Baldwin Jr. Three NF-kappa B sites in the I kappa B-alpha promoter are required for induction of gene expression by TNF alpha Nucleic Acids Res 22 18 1994 3787 3792
62. C.S. Mitsiades Transcriptional signature of histone deacetylase inhibition in multiple myeloma: biological and clinical implications Proc Natl Acad Sci USA 101 2 2004 540 545
63. M.E. Figueiredo-Pereira, K.A. Berg, and S. Wilk A new inhibitor of the chymotrypsin-like activity of the multicatalytic proteinase complex (20S proteasome) induces accumulation of ubiquitin-protein conjugates in a neuronal cell J Neurochem 63 4 1994 1578 1581
64. A. Vinitsky Inhibition of the chymotrypsin-like activity of the pituitary multicatalytic proteinase complex Biochemistry 31 39 1992 9421 9428
65. Z. Li A single amino acid substitution in a proteasome subunit triggers aggregation of ubiquitinated proteins in stressed neuronal cells J Neurochem 90 1 2004 19 28
66. C. Wojcik, and G.N. DeMartino Analysis of Drosophila 26 S proteasome using RNA interference J Biol Chem 277 8 2002 6188 6197
67. M. Gaczynska, K.L. Rock, and A.L. Goldberg Gamma-interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes Nature 365 6443 1993 264 267
68. Y. Yang Proteasomes are regulated by interferon gamma: implications for antigen processing Proc Natl Acad Sci USA 89 11 1992 4928 4932
69. M. Groll A gated channel into the proteasome core particle Nat Struct Biol 7 11 2000 1062 1067
70. V.M. Richon Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation Proc Natl Acad Sci USA 97 18 2000 10014 10019
71. M.V. Blagosklonny Histone deacetylase inhibitors all induce p21 but differentially cause tubulin acetylation, mitotic arrest, and cytotoxicity Mol Cancer Ther 1 11 2002 937 941
72. F.M. Ruemmele Butyrate mediates Caco-2 cell apoptosis via up-regulation of pro-apoptotic BAK and inducing caspase-3 mediated cleavage of poly-(ADP-ribose) polymerase (PARP) Cell Death Differ 6 8 1999 729 735
73. J.A. McBain Apoptotic death in adenocarcinoma cell lines induced by butyrate and other histone deacetylase inhibitors Biochem Pharmacol 53 9 1997 1357 1368
74. I. Luque, and C. Gelinas Rel/NF-kappa B and I kappa B factors in oncogenesis Semin Cancer Biol 8 2 1997 103 111
75. T.D. Gilmore Rel/NF-kappa B/I kappa B proteins and cancer Oncogene 13 7 1996 1367 1378
76. M.F. Neurath Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice Nat Med 2 9 1996 998 1004
77. G. Rogler Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa Gastroenterology 115 2 1998 357 369
78. H. Luhrs Cytokine-activated degradation of inhibitory kappa B protein alpha is inhibited by the short-chain fatty acid butyrate Int J Colorectal Dis 16 4 2001 195 201
79. E. Adam Potentiation of tumor necrosis factor-induced NF-kappa B activation by deacetylase inhibitors is associated with a delayed cytoplasmic reappearance of I kappa B alpha Mol Cell Biol 23 17 2003 6200 6209
80. V.A. Soldatenkov Sodium butyrate induces apoptosis and accumulation of ubiquitinated proteins in human breast carcinoma cells Cell Death Differ 5 4 1998 307 312
81. P. Chen, and M. Hochstrasser Autocatalytic subunit processing couples active site formation in the 20S proteasome to completion of assembly Cell 86 6 1996 961 972
82. M. Gaczynska Proteasome subunits X and Y alter peptidase activities in opposite ways to the interferon-gamma-induced subunits LMP2 and LMP7 J Biol Chem 271 29 1996 17275 17280
83. N. Chondrogianni Central role of the proteasome in senescence and survival of human fibroblasts: induction of a senescence-like phenotype upon its inhibition and resistance to stress upon its activation J Biol Chem 278 30 2003 28026 28037
84. G. Mannhaupt Rpn4p acts as a transcription factor by binding to PACE, a nonamer box found upstream of 26S proteasomal and other genes in yeast FEBS Lett 450 1-2 1999 27 34
85. Y. Xie, and A. Varshavsky RPN4 is a ligand, substrate, and transcriptional regulator of the 26S proteasome: a negative feedback circuit Proc Natl Acad Sci USA 98 6 2001 3056 3061
86. S.M. Wyke, S.T. Russell, and M.J. Tisdale Induction of proteasome expression in skeletal muscle is attenuated by inhibitors of NF-kappa B activation Br J Cancer 91 9 2004 1742 1750
87. T. Grune, T. Reinheckel, and K.J. Davies Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome J Biol Chem 271 26 1996 15504 15509
88. N. Qureshi The proteasome as a lipopolysaccharide-binding protein in macrophages: differential effects of proteasome inhibition on lipopolysaccharide-induced signaling events J Immunol 171 3 2003 1515 1525
89. M.A. Kania The proteasome subunit, C2, contains an important site for binding of the PA28 (11S) activator Eur J Biochem 236 2 1996 510 516
90. F.G. Whitby Structural basis for the activation of 20S proteasomes by 11S regulators Nature 408 6808 2000 115 120
91. K.B. Hendil, S. Khan, and K. Tanaka Simultaneous binding of PA28 and PA700 activators to 20 S proteasomes Biochem J 332 Pt 3 1998 749 754
92. D.H. Lee, and A.L. Goldberg Proteasome inhibitors: valuable new tools for cell biologists Trends Cell Biol 8 10 1998 397 403
93. J. Adams, V.J. Palombella, and P.J. Elliott Proteasome inhibition: a new strategy in cancer treatment Invest New Drugs 18 2 2000 109 121
94. C.E. Denlinger Combined proteasome and histone deacetylase inhibition in non-small cell lung cancer J Thorac Cardiovasc Surg 127 4 2004 1078 1086
95. C. Yu The proteasome inhibitor bortezomib interacts synergistically with histone deacetylase inhibitors to induce apoptosis in Bcr/Abl+ cells sensitive and resistant to STI571 Blood 102 10 2003 3765 3774
96. X.Y. Pei, Y. Dai, and S. Grant Synergistic induction of oxidative injury and apoptosis in human multiple myeloma cells by the proteasome inhibitor bortezomib and histone deacetylase inhibitors Clin Cancer Res 10 11 2004 3839 3852
97. M. Rolfe, M.I. Chiu, and M. Pagano The ubiquitin-mediated proteolytic pathway as a therapeutic area J Mol Med 75 1 1997 5 17
98. A. Hershko Roles of ubiquitin-mediated proteolysis in cell cycle control Curr Opin Cell Biol 9 6 1997 788 799
99. P.A. Marks Histone deacetylase inhibitors: development as cancer therapy Novartis Found Symp 259 2004 269 281 [discussion 281-8]