The histone deacetylase inhibitor SAHA sensitizes acute myeloid leukemia cells to a combination of nucleoside analogs and the DNA-alkylating agent busulfan

Leukemia and Lymphoma

Volumn 55, Issue 7, 2014, Pages 1625-1634

  Song, Guiyun ^a   Valdez, Benigno C ^a   Li, Yang ^a   Dominguez, Jose R ^a   Corn, Paul ^a   Champlin, Richard E ^a   Andersson, Borje S ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

AML; DNA alkylator; Drug cytotoxicity; Nucleoside analog; SAHA

Indexed keywords

APOPTOSIS INDUCING FACTOR; ATM PROTEIN; BUSULFAN; CASPASE 3; CASPASE 8; CASPASE 9; CHECKPOINT KINASE 2; CLOFARABINE; CYTOCHROME C; FLUDARABINE; HISTONE DEACETYLASE; HISTONE H2AX; HISTONE H3; HISTONE H4; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; PROTEIN P53; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; VORINOSTAT; ADENINE NUCLEOTIDE; ALKYLATING AGENT; ARABINONUCLEOSIDE; DNA BINDING PROTEIN; DRUG COMBINATION; HISTONE; HISTONE DEACETYLASE INHIBITOR; NUCLEAR PROTEIN; P73 PROTEIN, HUMAN; TUMOR PROTEIN P73; TUMOR SUPPRESSOR PROTEIN; VIDARABINE;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; CELL CYCLE CHECKPOINT; CELL DEATH; CELL NUCLEUS; CELL PERMEABILIZATION; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOPLASM; CYTOSOL; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; DRUG POTENTIATION; ENZYME ACTIVATION; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; HUMAN TISSUE; LEUKEMIA CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; CELL MEMBRANE PERMEABILITY; DRUG COMBINATION; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; LEUKEMIA, MYELOID, ACUTE; METABOLISM; MITOCHONDRION; TUMOR CELL LINE;

ADENINE NUCLEOTIDES; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; ARABINONUCLEOSIDES; BUSULFAN; CELL LINE, TUMOR; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; DNA DAMAGE; DNA-BINDING PROTEINS; DRUG COMBINATIONS; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; HISTONE DEACETYLASE INHIBITORS; HISTONES; HUMANS; LEUKEMIA, MYELOID, ACUTE; MITOCHONDRIA; NUCLEAR PROTEINS; SIGNAL TRANSDUCTION; TUMOR PROTEIN P73; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS; VIDARABINE;

EID: 84903478359     PISSN: 10428194     EISSN: 10292403     Source Type: Journal    
DOI: 10.3109/10428194.2013.856007     Document Type: Article

References (63)

1. de Lima M, Couriel D, Thall P F, et al. Once-daily intravenousbusulfan and fl udarabine:clinical and pharmacokinetic results of amyeloablative, reduced-toxicity conditioning regimen for allogeneicstem cell transplantation in AML and MDS. Blood 2004 ; 104 : 857-864.
2. Russell JA, Tran HT, Quinlan D, et al. Once-daily intravenousbusulfan given with fl udarabine as conditioning for allogeneic stemcell transplantation: study of pharmacokinetics and early clinicaloutcomes. Biol Blood Marrow Transplant 2002 ; 8 : 468-476.
3. Russell J A, Savoie M L, Balogh A, et al. Allogeneic transplantationfor adult acute leukemia in fi rst and second remission with a novelregimen incorporating daily intravenous busulfan, fl udarabine, 400CGY total-body irradiation, and thymoglobulin. Biol Blood MarrowTransplant 2007 ; 13 : 814-821.
4. Andersson BS, de Lima M, Thall P F, et al. Once daily i.v. busulfanand fl udarabine (i.v. Bu-Flu) compares favorably with i.v. busulfan andcyclophosphamide (i.v. BuCy2) as pretransplant conditioning therapyin AML/MDS. Biol Blood Marrow Transplant 2008 ; 14 : 672-684.
5. Pidala J, Kim J, Anasetti C, et al. Pharmacokinetic targeting ofintravenous busulfan reduces conditioning regimen related toxicityfollowing allogeneic hematopoietic cell transplantation for acutemyelogenous leukemia. JHematol Oncol 2010; 3: 36-44.
6. Perkins J, Field T, Kim J, et al. Pharmacokinetic targeting ofi.v. BU with fl udarabine as conditioning before hematopoietic celltransplant: the Effect of fi rst-dose area under the concentration timecurve on transplant-related outcomes. Bone Marrow Transplantation2011 ; 46 : 1418-1425.
7. Chae YS, Sohn SK, Kim JG, et al. New myeloablativeconditioning regimen with fl udarabine and busulfan for allogeneicstem cell transplantation: comparison with BuCy2. Bone MarrowTransplantation 2007 ; 40 : 541-547.
8. Kantarjian HM, Gandhi V, Kozuch P, et al. Phase I clinicaland pharmacology study of clofarabine in patients with solid andhematologic cancers. J Clin Oncol 2003 ; 21 : 1167-1173.
9. Faderl S, Ferrajoli A, Wierda W, et al. Clofarabine combinationsas acute myeloid leukemia salvage therapy. Cancer 2008 ; 113 :2090-2096.
10. Jeha S, Razzouk B, Rytting M, et al. Phase II study of clofarabine inpediatric patients with refractory or relapsed acute myeloid leukemia.J Clin Oncol 2009 ; 27 : 4392-4397.
11. Kantarjian H M, Erba H P, Claxton D, et al. Phase II study ofclofarabine monotherapy in previously untreated older adults withacute myeloid leukemia and unfavorable prognostic factors. J Clin Oncol 2010 ; 28 : 549-555.
12. Valdez BC, Li Y, Murray D, et al. The synergistic cytotoxicity ofclofarabine, fl udarabine and busulfan in AML cells involves ATMpathway activation and chromatin remodeling. Biochem Pharmacol2011 ; 81 : 222-232.
13. Andersson BS, Valdez BC, de Lima M, et al. Clofarabine-fl udarabine with once daily i.v. busulfan as pretransplant conditioningtherapy for advanced myeloid leukemia and MDS. Biol Blood MarrowTransplant 2011 ; 17 : 893-900.
14. Ruefli AA, Bernhard D, Tainton KM, et al. Suberoylanilidehydroxamic acid (SAHA) overcomes multidrug resistance and inducescell death in P-glycoprotein-expressing cells. Int J Cancer 2002 ; 99 :292-298.
15. Mitsiades CS, Mitsiades NS, McMullan CJ, et al. Transcriptionalsignature of histone deacetylase inhibition in multiple myeloma:biological and clinical implications. Proc Natl Acad Sci USA 2004 ;101 : 540-545.
16. Shao Y, Gao Z, Marks PA, et al. Apoptotic and autophagic celldeath induced by histone deacetylase inhibitors. Proc Natl Acad SciUSA 2004 ; 101 : 18030-18035.
17. Yu C, Dasmahapatra G, Dent P, et al. Synergistic interactionsbetween MEK1/2 and histone deacetylase inhibitors in BCR/ABL human leukemia cells. Leukemia 2005; 19: 1579-1589.
18. Lindemann RK, Newbold A, Whitecross KF, et al. Analysis of theapoptotic and therapeutic activities of histone deacetylase inhibitorsby using a mouse model of B cell lymphoma. Proc Natl Acad Sci USA2007 ; 104 : 8071-8076.
19. Duvic M, Vu J. Vorinostat: a new oral histone deacetylase inhibitorapproved for cutaneous T-cell lymphoma. Expert Opin Investig Drugs2007 ; 16 : 1111-1120.
20. Marks P A, Breslow R. Dimethyl sulfoxide to vorinostat:developmentof this histone deacetylase inhibitor as an anticancer drug. NatBiotechnol 2007 ; 25 : 84-90.
21. Kelly W K, Marks P A. Drug insight: histone deacetylase inhibitorsdevelopmentof the new targeted anticancer agent suberoylanilidehydroxamic acid. Nat Clin Pract Oncol 2005 ; 2 : 150-157.
22. Ungerstedt JS, Sowa Y, Xu WS, et al. Role of thioredoxin in theresponse of normal and transformed cells to histone deacetylaseinhibitors. Proc Natl Acad Sci USA 2005 ; 102 : 673-678.
23. Duvic M, Vu J. Vorinostat in cutaneous T-cell lymphoma. DrugsToday (Barc) 2007 ; 43 : 585-599.
24. Lee JH, Choy ML, Ngo L, et al. Histone deacetylase inhibitorinduces DNA damage, which normal but not transformed cells canrepair. Proc Natl Acad Sci USA 2010 ; 107 : 14639-14644.
25. Andersson B S, Bergerheim U S, Collins V P, et al. KBM-3, an invitro model of human acute myelomonocytic leukemia. Exp Hematol1992 ; 20 : 361-367.
26. Valdez B C, Murray D, Ramdas L, et al. Altered gene expressionin busulfan-resistant human myeloid leukemia. Leuk Res 2008 ; 32 :1684-1697.
27. Drexler HG. The leukemia-lymphoma cell line factsbook.San Diego, CA: Academic Press ; 2001.
28. Quentmeier H, Martelli MP, Dirks WG, et al. Cell lineOCI/AML3 bears exon-12 NPM gene mutation-A and cytoplasmicexpression of nucleophosmin. Leukemia 2005 ; 19 : 1760-1767.
29. Carter BZ, Mak DH, Schober WD, et al. Triptolide sensitizesAML cells to TRAIL-induced apoptosis via decrease of XIAP andp53-mediated increase of DR5. Blood 2008 ; 111 : 3742-3750.
30. Kasugai S, Hasegawa N, Ogura H. Asimple i n vitro cytotoxicity testusing the MTT (3-(4, 5)-dimethylthiazol-2-yl)-2, 5-diphenyl tetrazoliumbromide) colorimetric assay: analysis of eugenol toxicity on dental pulpcells (RPC-C2A). Jpn J Pharmacol 1990; 52: 95-100.
31. Salvioli S, Ardizzoni A, Franceschi C, et al. JC-1, but notDiOC6(3) or rhodamine 123, is a reliable fluorescent probe toassess delta psi changes in intact cells: implications for studieson mitochondrial functionality during apoptosis. FEBS Lett1997 ; 411 : 77-82.
32. Schottelius A, Brennscheidt U, Ludwig W D, et al. Mechanisms ofp53 alteration in acute leukemias. Leukemia 1994; 8: 1673-1681.
33. Nakano Y, Naoe T, Kiyoi H, et al. Prognostic value of p53 genemutations and the product expression in de novo acute myeloidleukemia. Eur J Haematol 2000 ; 65 : 23-31.
34. Rogakou EP, Boon C, Redon C, et al. Megabase chromatindomains involved in DNA double-strand breaks in vivo. JCell Biol1999 ; 146 : 905-916.
35. Vayssiere JL, Petit PX, Risler Y, et al. Commitment to apoptosis isassociated with changes in mitochondrial biogenesis and activity incell lines conditionally immortalized with simian virus 40. Proc NatlAcad Sci USA 1994 ; 91 : 11752-11756.
36. Ankarcrona M, Dypbukt JM, Bonfoco E, et al. Glutamate-inducedneuronal death: a succession of necrosis or apoptosis depending onmitochondrial function. Neuron 1995 ; 15 : 961-973.
37. Marchenko N D, Zaika A, Moll U M. Death signal-inducedlocalization of p53 protein to mitochondria. Apotential role inapoptotic signaling. JBiol Chem 2000; 275: 16202-16212.
38. Mihara M, Erster S, Zaika A, et al. p53 has a direct apoptogenicrole at the mitochondria. Mol Cell 2003 ; 11 : 577-590.
39. Erster S, Mihara M, Kim R H, et al. In vivo mitochondrial p53translocation triggers a rapid fi rst wave of cell death in response toDNA damage that can precede p53 target gene activation. Mol Cell Biol2004 ; 24 : 6728-6741.
40. Levine AJ. p53, the cellular gatekeeper for growth and division.Cell 1997 ; 88 : 323-331.
41. Kojima K, Shimanuki M, Shikami M, et al. The dual PI3 kinase/mTOR inhibitor PI-103 prevents p53 induction by Mdm2 inhibitionbut enhances p53-mediated mitochondrial apoptosis in p53 wild-typeAML. Leukemia 2008; 22: 1728-1736.
42. Gudkov AV, Komarova EA. The role of p53 in determiningsensitivity to radiotherapy. Nat Rev Cancer 2003; 3: 117-129.
43. Irwin MS, Kondo K, Marin MC, et al. Chemosensitivity linked top73 function. Cancer Cell 2003 ; 3 : 403-410.
44. Ozaki T, Nakagawara A. p73, asophisticated p53 family memberin the cancer world. Cancer Sci 2005 ; 96 : 729-737.
45. Vayssade M, Haddada H, Faridoni-Laurens L, et al. P73functionally replaces p53 in adriamycin-treated, p53-defi cient breastcancer cells. Int J Cancer 2005 ; 116 : 860-869.
46. Nyman U, Sobczak-Pluta A, Vlachos P, et al. Full-length p73alpharepresses drug-induced apoptosis in small cell lung carcinoma cells.J Biol Chem 2005 ; 280 : 34159-34169.
47. Valdez BC, Murray D, Nieto Y, et al. Synergistic cytotoxicity ofthe DNA alkylating agent busulfan, nucleoside analogs and suberoylanilidehydroxamic acid in lymphoma cell lines. Leuk Lymphoma2012 ; 53 : 973-981.
48. Genini D, Adachi S, Chao Q, et al. Deoxyadenosine analogsinduce programmed cell death in chronic lymphocytic leukemia cellsby damaging the DNA and by directly aff ecting the mitochondria.Blood 2000 ; 96 : 3537-3543.
49. Shieh SY, Ikeda M, Taya Y, Prives C. DNA damage-inducedphosphorylation of p53 alleviates inhibition by MDM2. Cell 1997 ;91 : 325-334.
50. Evan G, Littlewood T. Amatter of life and cell death. Science1998 ; 281 : 1317-1322.
51. Genini D, Budihardjo I, Plunkett W, et al. Nucleotide requirementsfor the in vitro activation of the apoptosis protein-activating factor-1-mediated caspase pathway. JBiol Chem 2000 ; 275 : 29-34.
52. Bellosillo B, Villamor N, Lopez-Guillermo A, et al. Spontaneousand drug-induced apoptosis is mediated by conformational changesof Bax and Bak in B-cell chronic lymphocytic leukemia. Blood2002 ; 100 : 1810-1816.
53. Faria JR, Yamamoto M, Faria RM, et al. Fludarabine inducesapoptosis in chronic lymphocytic leukemia-the role of P53, Bcl-2, Bax, Mcl-1, and Bag-1 proteins. Braz J Med Biol Res 2006 ; 39 :327-333.
54. Richon VM, Webb Y, Merger R, et al. Second generationhybrid polar compounds are potent inducers of transformed celldiff erentiation. Proc Natl Acad Sci USA 1996 ; 93 : 5705-5708.
55. Richon VM, Garcia-Vargas J, Hardwick JS. Development ofvorinostat: current applications and future perspectives for cancertherapy. Cancer Lett 2009; 280: 201-210.
56. Frew AJ, Johnstone RW, Bolden JE. Enhancing the apoptoticand therapeutic effects of HDAC inhibitors. Cancer Lett 2009 ;280 : 125-133.
57. Schwartz YB, Pirrotta V. Polycomb silencing mechanisms andthe management of genomic programmes. Nat Rev Genet 2007 ; 8 :9-22.
58. Ke XS, Qu Y, Rostad K, et al. Genome-wide profi ling ofhistone h3 lysine 4 and lysine 27 trimethylation reveals anepigenetic signature in prostate carcinogenesis. PLoS One 2009 ;4 : e4687.
59. Vegliante MC, Royo C, Palomero J, et al. Epigenetic activation ofSOX11 in lymphoid neoplasms by histone modifi cations. PLoS One2011 ; 6 : e21382.
60. Abdel-Wahab O, Adli M, LaFave LM, et al. ASXL1 mutationspromote myeloid transformation through loss of PRC2-mediated generepression. Cancer Cell 2012 ; 22 : 180-193.
61. Jost CA, Marin MC, Kaelin WG, Jr. p73 is a simian [correctionof human] p53-related protein that can induce apoptosis. Nature1997 ; 389 : 191-194.
62. Hainaut P, Soussi T, Shomer B, et al. Database of p53 gene somaticmutations in human tumors and cell lines: updated compilation andfuture prospects. Nucleic Acids Res 1997 ; 25 : 151-157.
63. Soenen V, Preudhomme C, Roumier C, et al. 17p Deletion inacute myeloid leukemia and myelodysplastic syndrome. Analysisof breakpoints and deleted segments by fl uorescence in situ. Blood1998 ; 91 : 1008-1015.