Inhibition of Histone Deacetylase 3 Causes Replication Stress in Cutaneous T Cell Lymphoma

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Wells, Christina E ^a   Bhaskara, Srividya ^b   Stengel, Kristy R ^a   Zhao, Yue ^a   Sirbu, Bianca ^a   Chagot, Benjamin ^a,c   Cortez, David ^a,d   Khabele, Dineo ^a,d,e   Chazin, Walter J ^a   Cooper, Andrew ^f   Jacques, Vincent ^f   Rusche, James ^f   Eischen, Christine M ^d,e   McGirt, Laura Y ^d,e   Hiebert, Scott W ^a,d  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c UNIVERSITÉ DE LORRAINE   (France)

^d VANDERBILT INGRAM CANCER CENTER   (United States)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^f REPLIGEN CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEXAROTENE; DNA; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; METHOTREXATE; RETINOIC ACID; RGFP 136; RGFP 233; RGFP 966; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL STRESS; CHROMATIN; CUTANEOUS T CELL LYMPHOMA; DNA ISOLATION; DNA REPLICATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; TUMOR CELL;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMATIN; DNA DAMAGE; DNA REPLICATION; DRUG SYNERGISM; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; LYMPHOMA, T-CELL, CUTANEOUS; S PHASE; STRESS, PHYSIOLOGICAL;

EID: 84880655164     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068915     Document Type: Article

References (50)

1. Lansigan F, Foss FM, (2010) Current and emerging treatment strategies for cutaneous T-cell lymphoma. Drugs 70: 273-286.
2. Wilcox RA, (2011) Cutaneous T-cell lymphoma: 2011 update on diagnosis, risk-stratification, and management. Am J Hematol 86: 928-948.
3. Li JY, Horwitz S, Moskowitz A, Myskowski PL, Pulitzer M, et al. (2012) Management of cutaneous T cell lymphoma: new and emerging targets and treatment options. Cancer Manag Res 4: 75-89.
4. Wollina U, (2012) Cutaneous T cell lymphoma: update on treatment. Int J Dermatol 51: 1019-1036.
5. Willemze R, Jaffe ES, Burg G, Cerroni L, Berti E, et al. (2005) WHO-EORTC classification for cutaneous lymphomas. Blood 105: 3768-3785.
6. Barneda-Zahonero B, Parra M, (2012) Histone deacetylases and cancer. Mol Oncol. 6: 579-89.
7. Cotto M, Cabanillas F, Tirado M, Garcia MV, Pacheco E, (2010) Epigenetic therapy of lymphoma using histone deacetylase inhibitors. Clin Transl Oncol 12: 401-409.
8. Melnick A, Licht JD, (2002) Histone deacetylases as therapeutic targets in hematologic malignancies. Curr Opin Hematol 9: 322-332.
9. Yoshida M, Furumai R, Nishiyama M, Komatsu Y, Nishino N, et al. (2001) Histone deacetylase as a new target for cancer chemotherapy. Cancer Chemother Pharmacol 48Suppl 1: S20-26.
10. Prince HM, Bishton MJ, Harrison SJ, (2009) Clinical studies of histone deacetylase inhibitors. Clin Cancer Res 15: 3958-3969.
11. Mann BS, Johnson JR, He K, Sridhara R, Abraham S, et al. (2007) Vorinostat for treatment of cutaneous manifestations of advanced primary cutaneous T-cell lymphoma. Clin Cancer Res 13: 2318-2322.
12. Mann BS, Johnson JR, Cohen MH, Justice R, Pazdur R, (2007) FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 12: 1247-1252.
13. Whittaker SJ, Demierre MF, Kim EJ, Rook AH, Lerner A, et al. (2010) Final results from a multicenter, international, pivotal study of romidepsin in refractory cutaneous T-cell lymphoma. J Clin Oncol 28: 4485-4491.
14. Gallinari P, Di Marco S, Jones P, Pallaoro M, Steinkuhler C, (2007) HDACs, histone deacetylation and gene transcription: from molecular biology to cancer therapeutics. Cell Res 17: 195-211.
15. Goodarzi AA, Noon AT, Jeggo PA, (2009) The impact of heterochromatin on DSB repair. Biochem Soc Trans 37: 569-576.
16. Bhaskara S, Knutson SK, Jiang G, Chandrasekharan MB, Wilson AJ, et al. (2010) Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell 18: 436-447.
17. Bhaskara S, Chyla BJ, Amann JM, Knutson SK, Cortez D, et al. (2008) Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell 30: 61-72.
18. Knutson SK, Chyla BJ, Amann JM, Bhaskara S, Huppert SS, et al. (2008) Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks. EMBO J 27: 1017-1028.
19. Insinga A, Monestiroli S, Ronzoni S, Gelmetti V, Marchesi F, et al. (2005) Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nat Med 11: 71-76.
20. Insinga A, Minucci S, Pelicci PG, (2005) Mechanisms of selective anticancer action of histone deacetylase inhibitors. Cell Cycle 4: 741-743.
21. Rosato RR, Almenara JA, Dai Y, Grant S, (2003) Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells. Mol Cancer Ther 2: 1273-1284.
22. Rosato RR, Grant S, (2005) Histone deacetylase inhibitors: insights into mechanisms of lethality. Expert Opin Ther Targets 9: 809-824.
23. Xu WS, Parmigiani RB, Marks PA, (2007) Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 26: 5541-5552.
24. Khan O, La Thangue NB, (2012) HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol Cell Biol 90: 85-94.
25. Taunton J, Hassig CA, Schreiber SL, (1996) A mammalian histone deacetylase related to the yeast transcriptional regulator Rpd3p. Science 272: 408-411.
26. Bernstein BE, Tong JK, Schreiber SL, (2000) Genomewide studies of histone deacetylase function in yeast. Proc Natl Acad Sci U S A 97: 13708-13713.
27. Emiliani S, Fischle W, Van Lint C, Al-Abed Y, Verdin E, (1998) Characterization of a human RPD3 ortholog, HDAC3. Proc Natl Acad Sci U S A 95: 2795-2800.
28. Grozinger CM, Hassig CA, Schreiber SL, (1999) Three proteins define a class of human histone deacetylases related to yeast Hda1p. Proc Natl Acad Sci U S A 96: 4868-4873.
29. Hagelkruys A, Sawicka A, Rennmayr M, Seiser C, (2011) The biology of HDAC in cancer: the nuclear and epigenetic components. Handb Exp Pharmacol 206: 13-37.
30. Yang WM, Tsai SC, Wen YD, Fejer G, Seto E, (2002) Functional domains of histone deacetylase-3. J Biol Chem 277: 9447-9454.
31. Yang WM, Yao YL, Sun JM, Davie JR, Seto E, (1997) Isolation and characterization of cDNAs corresponding to an additional member of the human histone deacetylase gene family. J Biol Chem 272: 28001-28007.
32. Malvaez M, McQuown SC, Rogge GA, Astarabadi M, Jacques V, et al. (2013) HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proc Natl Acad Sci U S A. 110: 2647-52.
33. Chou CJ, Herman D, Gottesfeld JM, (2008) Pimelic diphenylamide 106 is a slow, tight-binding inhibitor of class I histone deacetylases. J Biol Chem 283: 35402-35409.
34. Rai M, Soragni E, Chou CJ, Barnes G, Jones S, et al. (2010) Two new pimelic diphenylamide HDAC inhibitors induce sustained frataxin upregulation in cells from Friedreich's ataxia patients and in a mouse model. PLoS One 5: e8825.
35. Xu C, Soragni E, Chou CJ, Herman D, Plasterer HL, et al. (2009) Chemical probes identify a role for histone deacetylase 3 in Friedreich's ataxia gene silencing. Chem Biol 16: 980-989.
36. Sirbu BM, Couch FB, Cortez D, (2012) Monitoring the spatiotemporal dynamics of proteins at replication forks and in assembled chromatin using isolation of proteins on nascent DNA. Nat Protoc 7: 594-605.
37. Dorn ES, Chastain PD, 2nd, Hall JR, Cook JG (2009) Analysis of re-replication from deregulated origin licensing by DNA fiber spreading. Nucleic Acids Res 37: 60-69.
38. McQuown SC, Barrett RM, Matheos DP, Post RJ, Rogge GA, et al. (2011) HDAC3 is a critical negative regulator of long-term memory formation. J Neurosci 31: 764-774.
39. Yamaguchi T, Cubizolles F, Zhang Y, Reichert N, Kohler H, et al. (2010) Histone deacetylases 1 and 2 act in concert to promote the G1-to-S progression. Genes Dev 24: 455-469.
40. Drogaris P, Villeneuve V, Pomies C, Lee EH, Bourdeau V, et al. (2012) Histone deacetylase inhibitors globally enhance h3/h4 tail acetylation without affecting h3 lysine 56 acetylation. Sci Rep 2: 220.
41. Shen S, O'Brien T, Yap LM, Prince HM, McCormack CJ, (2012) The use of methotrexate in dermatology: a review. Australas J Dermatol 53: 1-18.
42. Zhang C, Duvic M, (2003) Retinoids: therapeutic applications and mechanisms of action in cutaneous T-cell lymphoma. Dermatol Ther 16: 322-330.
43. Abbott RA, Whittaker SJ, Morris SL, Russell-Jones R, Hung T, et al. (2009) Bexarotene therapy for mycosis fungoides and Sezary syndrome. Br J Dermatol 160: 1299-1307.
44. Fernandez-Capetillo O, Nussenzweig A, (2004) Linking histone deacetylation with the repair of DNA breaks. Proc Natl Acad Sci U S A 101: 1427-1428.
45. Sirbu BM, Couch FB, Feigerle JT, Bhaskara S, Hiebert SW, et al. (2011) Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev 25: 1320-1327.
46. Zhang Y, Iratni R, Erdjument-Bromage H, Tempst P, Reinberg D, (1997) Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 89: 357-364.
47. Ahmad A, Takami Y, Nakayama T, (2003) WD dipeptide motifs and LXXLL motif of chicken HIRA are necessary for transcription repression and the latter motif is essential for interaction with histone deacetylase-2 in vivo. Biochem Biophys Res Commun 312: 1266-1272.
48. Tyler JK, Bulger M, Kamakaka RT, Kobayashi R, Kadonaga JT, (1996) The p55 subunit of Drosophila chromatin assembly factor 1 is homologous to a histone deacetylase-associated protein. Mol Cell Biol 16: 6149-6159.
49. Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, et al. (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437: 1173-1178.
50. Conti C, Leo E, Eichler GS, Sordet O, Martin MM, et al. (2010) Inhibition of histone deacetylase in cancer cells slows down replication forks, activates dormant origins, and induces DNA damage. Cancer Res 70: 4470-4480.