Inhibition of NF-κB activation by the histone deacetylase inhibitor 4-Me2N-BAVAH induces an early G1 cell cycle arrest in primary hepatocytes

Cell Proliferation

Volumn 40, Issue 5, 2007, Pages 640-655

  Papeleu, P ^a   Wullaert, A ^b   Elaut, G ^a   Henkens, T ^a   Vinken, M ^a   Laus, G ^a   Tourwe D ^a   Beyaert, R ^b   Rogiers, V ^a   Vanhaecke, T ^a,c  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c FACULTY OF MEDICINE AND PHARMACY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

5 (4 DIMETHYLAMINOBENZOYL)AMINOVALERIC ACID HYDROXAMIDE; CASPASE 3; CYCLIN D1; EPIDERMAL GROWTH FACTOR; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BAX; PROTEIN BID; PROTEIN P21; TRICHOSTATIN A; UNCLASSIFIED DRUG; 5 (4 DIMETHYLAMINOBENZOYL) AMINOVALERIC ACID HYDROXAMATE; 5-(4-DIMETHYLAMINOBENZOYL)-AMINOVALERIC ACID HYDROXAMATE; CYCLIN D; CYCLINE; ENZYME INHIBITOR; HYDROXAMIC ACID; LUCIFERASE; VALERIC ACID DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DNA SYNTHESIS; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC TRANSCRIPTION; LIVER CELL; NONHUMAN; NORTHERN BLOTTING; RAT; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; GENETICS; METABOLISM; REPORTER GENE;

RATTUS;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CYCLINS; DOWN-REGULATION; ENZYME INHIBITORS; G1 PHASE; GENES, REPORTER; HEPATOCYTES; HISTONE DEACETYLASES; HYDROXAMIC ACIDS; LUCIFERASES; NF-KAPPA B; PENTANOIC ACIDS; RATS; TRANSCRIPTION, GENETIC;

EID: 34548686795     PISSN: 09607722     EISSN: 13652184     Source Type: Journal    
DOI: 10.1111/j.1365-2184.2007.00466.x     Document Type: Article

References (51)

1. Albrecht JH, Hansen LK (1999) Cyclin D1 promotes mitogen-independent cell cycle progression in hepatocytes. Cell Growth Differ. 10, 397 404.
2. Ashburner BP, Westerheide SD, Baldwin AS Jr. (2001) The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol. Cell. Biol. 21, 7065 7077.
3. Bailly-Maitre B, de Sousa G, Zucchini N, Gugenheim J, Boulukos KE, Rahmani R (2002) Spontaneous apoptosis in primary cultures of human and rat hepatocytes: molecular mechanisms and regulation by dexamethasone. Cell Death Differ. 9, 945 955.
4. Chiba T, Yokosuka O, Arai M, Tada M, Fukai K, Imazeki F, Kato M, Seki N, Saisho H (2004) Identification of genes up-regulated by histone deacetylase inhibition with cDNA microarray and exploration of epigenetic alterations on hepatoma cells. J. Hepatol. 41, 436 445.
5. Chou MM, Blenis J (1995) The 70 kDa S6 kinase: regulation of a kinase with multiple roles in mitogenic signalling. Curr. Opin. Cell Biol. 7, 806 814.
6. Cousens LS, Gallwitz D, Alberts BM (1979) Different accessibilities in chromatin to histone acetylase. J. Biol. Chem. 254, 1716 1723.
7. Coutant A, Rescan C, Gilot D, Loyer P, Guguen-Guillouzo C, Baffet G (2002) PI3K-FRAP/mTOR pathway is critical for hepatocyte proliferation whereas MEK/ERK supports both proliferation and survival. Hepatology 36, 1079 1088.
8. De Valck D, Heyninck K, Van Criekinge W, Contreras R, Beyaert R, Fiers W (1996) A20, an inhibitor of cell death, self-associates by its zinc finger domain. FEBS Lett. 384, 61 64.
9. Dunn JC, Tompkins RG, Yarmush ML (1991) Long-term in vitro function of adult hepatocytes in a collagen sandwich configuration. Biotechnol. Prog. 7, 237 245.
10. El Bakkouri K, Wullaert A, Haegman M, Heyninck K, Beyaert R (2005) Adenoviral gene transfer of the NF-kappa B inhibitory protein ABIN-1 decreases allergic airway inflammation in a murine asthma model. J. Biol. Chem. 280, 17938 17944.
11. Elaut G, Laus G, Alexandre E, Richert L, Bachellier P, Tourwé D, Rogiers V, Vanhaecke T (2007) A metabolic screening study of Trichostatin A (TSA) and TSA-like histone deacetylase inhibitors in rat and human primary hepatocyte cultures. J. Pharmacol. Exp. Ther. 321, 400 408.
12. Elaut G, Török G, Papeleu P, Vanhaecke T, Laus G, Tourwe D, Rogiers V (2004) Rat hepatocyte suspensions as a suitable in vitro model for studying the biotransformation of histone deacetylase inhibitors. Altern. Lab. Anim. 32, 105 112.
13. Elaut G, Török G, Vinken M, Laus G, Papeleu P, Tourwe D, Rogiers V (2002) Major phase I biotransformation pathways of Trichostatin A in rat hepatocytes and in rat and human liver microsomes. Drug Metab. Dispos. 30, 1320 1328.
14. Glaser KB, Staver MJ, Waring JF, Stender J, Ulrich RG, Davidsen SK (2003) Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. Mol. Cancer Ther. 2, 151 163.
15. Grempler R, Kienitz A, Werner T, Meyer M, Barthel A, Ailett F, Sutherland C, Walther R, Schmoll D (2004) Tumour necrosis factor alpha decreases glucose-6-phosphatase gene expression by activation of nuclear factor kappaB. Biochem. J. 382, 471 479.
16. Henkens T, Papeleu P, Elaut G, Vinken M, Rogiers V, Vanhaecke T (2007) Trichostatin A, a critical factor in maintaining the functional differentiation of primary cultured rat hepatocytes. Toxicol. Appl. Pharmacol. 218, 64 71.
17. Joyce D, Albanese C, Steer J, Fu M, Bouzahzah B, Pestell RG (2001) NF-kappaB and cell-cycle regulation: the cyclin connection. Cytokine Growth Factor Rev. 12, 73 90.
18. Jung M, Brosch G, Kolle D, Scherf H, Gerhauser C, Loidl P (1999) Amide analogues of trichostatin A as inhibitors of histone deacetylase and inducers of terminal cell differentiation. J. Med. Chem. 42, 4669 4679.
19. Kobayashi K, Tsukamoto I (2001) Prolonged Jun N-terminal kinase (JNK) activation and the upregulation of p53 and p21 (WAF1/CIP1) preceded apoptosis in hepatocytes after partial hepatectomy and cisplatin. Biochim. Biophys. Acta 1537, 79 88.
20. Koniaris LG, McKillop IH, Schwartz SI, Zimmers TA (2003) Liver regeneration. J. Am. Coll. Surg. 197, 634 659.
21. Kouzarides T (1999) Histone acetylases and deacetylases in cell proliferation. Curr. Opin. Genet. Dev. 9, 40 48.
22. Lagger G, Doetzlhofer A, Schuettengruber B, Haidweger E, Simboeck E, Tischler J, Chiocca S, Suske G, Rotheneder H, Wintersberger E, Seiser C (2003) The tumor suppressor p53 and histone deacetylase 1 are antagonistic regulators of the cyclin-dependent kinase inhibitor p21/WAF1/CIP1 gene. Mol. Cell. Biol. 23, 2669 2679.
23. 1. J. Biol. Chem. 271, 11484 11492.
24. Marks PA, Jiang X (2005) Histone deacetylase inhibitors in programmed cell death and cancer therapy. Cell Cycle 4, 549 551.
25. Marks P, Rifkind RA, Richon VM, Breslow R, Miller T, Kelly WK (2001) Histone deacetylases and cancer: causes and therapies. Nat. Rev. Cancer 1, 194 202.
26. Mayo MW, Denlinger CE, Broad RM, Yeung F, Reilly ET, Shi Y, Jones DR (2003) Ineffectiveness of histone deacetylase inhibitors to induce apoptosis involves the transcriptional activation of NF-kappa B through the Akt pathway. J. Biol. Chem. 278, 18980 18989.
27. Mitchell C, Gilgenkrantz H (2003) Transcriptional profiling of liver regeneration: new approaches to an old trick! J. Hepatol. 38, 847 849.
28. Moynagh PN (2005) The NF-kappaB pathway. J. Cell Sci. 118, 4589 4592.
29. Nelsen CJ, Rickheim DG, Timchenko NA, Stanley MW, Albrecht JH (2001) Transient expression of cyclin D1 is sufficient to promote hepatocyte replication and liver growth in vivo. Cancer Res. 61, 8564 8568.
30. Nelsen CJ, Rickheim DG, Tucker MM, Hansen LK, Albrecht JH (2003) Evidence that cyclin D1 mediates both growth and proliferation downstream of TOR in hepatocytes. J. Biol. Chem. 278, 3656 3663.
31. Papakyriakou P, Tzardi M, Valatas V, Kanavaros P, Karydi E, Notas G, Xidakis C, Kouroumalis E (2002) Apoptosis and apoptosis related proteins in chronic viral liver disease. Apoptosis 7, 133 141.
32. Papeleu P, Loyer P, Vanhaecke T, Henkens T, Elaut G, Guguen-Guillouzo C, Rogiers V (2004) Proliferation of epidermal growth factor-stimulated hepatocytes in a hormonally defined serum-free medium. Altern. Lab. Anim. 32, 57 64.
33. Papeleu P, Loyer P, Vanhaecke T, Elaut G, Geerts A, Guguen-Guillouzo C, Rogiers V (2003) Trichostatin A induces differential cell cycle arrests but does not induce differential cell cycle arrests but does not induce apoptosis in primary cultures of mitogen-stimulated rat hepatocytes. J. Hepatol. 39, 374 382.
34. Papeleu P, Vanhaecke T, Elaut G, Vinken M, Henkens T, Snykers S, Rogiers V (2005) Differential effects of histone deacetylase inhibitors in tumor and normal cells-what is the toxicological relevance? Crit. Rev. Toxicol. 35, 363 378.
35. Papeleu P, Vanhaecke T, Henkens T, Elaut G, Vinken M, Snykers S, Rogiers V (2006) Isolation of rat hepatocytes. In : Philips IR, Shephard EA, eds. Methods in Molecular Biology, pp. 229 237. Totowa, NJ : Humana Press.
36. Piekarz R, Bates S (2004) A review of depsipeptide and other histone deacetylase inhibitors in clinical trials. Curr. Pharm. Des. 10, 2289 2298.
37. Qiao L, McKinstry R, Gupta S, Gilfor D, Windle JJ, Hylemon PB, Grant S, Fisher PB, Dent P (2002) Cyclin kinase inhibitor p21 potentiates bile acid-induced apoptosis in hepatocytes that is dependent on p53. Hepatology 36, 39 48.
38. Rescan C, Coutant A, Talarmin H, Theret N, Glaise D, Guguen-Guillouzo C, Baffet G (2001) Mechanism in the sequential control of cell morphology and S phase entry by epidermal growth factor involves distinct MEK/ERK activations. Mol. Biol. Cell 12, 725 738.
39. Roff M, Thompson J, Rodriguez MS, Jacque JM, Baleux F, Arenzana-Seisdedos F, Hay RT (1996) Role of IkappaBalpha ubiquitination in signal-induced activation of NFkappaB in vivo. J. Biol. Chem. 271, 7844 7850.
40. Sambucetti LC, Fischer DD, Zabludoff S, Kwon PO, Chamberlin H, Trogani N, Xu H, Cohen D (1999) Histone deacetylase inhibition selectively alters the activity and expression of cell cycle proteins leading to specific chromatin acetylation and antiproliferative effects. J. Biol. Chem. 274, 34940 34947.
41. Sanderson L, Taylor GW, Aboagye EO, Alao JP, Latigo JR, Coombes RC, Vigushin DM (2004) Plasma pharmacokinetics and metabolism of the histone deacetylase inhibitor trichostatin A after intraperitoneal administration to mice. Drug Metab. Dispos. 32, 1132 1138.
42. Sanlioglu S, Williams CM, Samavati L, Butler NS, Wang G, McCray PB Jr., Ritchie TC, Hunninghake GW, Zandi E, Engelhardt JF (2001) Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-kappa B. J. Biol. Chem. 276, 30188 30198.
43. Sheahan S, Bellamy CO, Treanor L, Harrison DJ, Prost S (2004) Additive effect of p53, 21 and Rb deletion in triple knockout primary hepatocytes. Oncogene 23, 1489 1497.
44. Talarmin H, Rescan C, Cariou S, Glaise D, Zanninelli G, Bilodeau M, Loyer P, Guguen-Guillouzo C, Baffet G (1999) The mitogen-activated protein kinase kinase/extracellular signal-regulated kinase cascade activation is a key signalling pathway involved in the regulation of G (1) phase progression in proliferating hepatocytes. Mol. Cell. Biol. 19, 6003 6011.
45. Vanhaecke T, Papeleu P, Elaut G, Rogiers V (2004) Trichostatin A-like hydroxamate histone deacetylase inhibitors as therapeutic agents: toxicological point of view. Curr. Med. Chem. 11, 1629 1643.
46. Vinken M, Henkens T, Vanhaecke T, Papeleu P, Geerts A, Van Rossen E, Chipman JK, Meda P, Rogiers V (2006) Trichostatin A enhances gap junctional intercellular communication in primary cultures of adult rat hepatocytes. Toxicol. Sci. 91, 484 492.
47. Wharton W, Savell J, Cress WD, Seto E, Pledger WJ (2000) Inhibition of mitogenesis in Balb/c-3T3 cells by Trichostatin A. Multiple alterations in the induction and activation of cyclin-cyclin-dependent kinase complexes. J. Biol. Chem. 275, 33981 33987.
48. Workman JL, Kingston RE (1998) Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu. Rev. Biochem. 67, 545 579.
49. Wullaert A, Wielockx B, Van Huffel S, Bogaert V, De Geest B, Papeleu P, Schotte P, El Bakkouri K, Heyninck K, Libert C, Beyaert R (2005) Adenoviral gene transfer of ABIN-1 protects mice from TNF/galactosamine-induced acute liver failure and lethality. Hepatology 42, 381 389.
50. Yin L, Laevsky G, Giardina C (2001) Butyrate suppression of colonocyte NF-kappa B activation and cellular proteasome activity. J. Biol. Chem. 276, 44641 44646.
51. Yoshida M, Furumai R, Nishiyama M, Komatsu Y, Nishino N, Horinouchi S (2001) Histone deacetylase as a new target for cancer chemotherapy. Cancer Chemother. Pharmacol. 48 (Suppl. 1 S20 S26.