ABT-737 accelerates butyrate-induced death of HL-60 cells. Involvement of mitochondrial apoptosis pathway

General Physiology and Biophysics

Volumn 32, Issue 4, 2013, Pages 505-516

  Štefaniková, Andrea ^a   Kliková, Katarína ^a   Hatok, Jozef ^a   Račay, Peter ^a  

^a University Teaching Hospital in Martin   (Slovakia)

Author keywords

ABT 737; Bcl 2 family proteins; GRP78; HL 60; Sodium butyrate

Indexed keywords

4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BETA ACTIN; BIM PROTEIN; BUTYRIC ACID; GLUCOSE REGULATED PROTEIN 78; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1;

ADJUVANT THERAPY; APOPTOSIS; ARTICLE; CELL KINETICS; CELL STRAIN HL 60; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; ENDOPLASMIC RETICULUM STRESS; G2 PHASE CELL CYCLE CHECKPOINT; INCUBATION TIME; INTRACELLULAR SIGNALING; MITOCHONDRION;

APOPTOSIS; BIPHENYL COMPOUNDS; BUTYRIC ACID; CELL DEATH; DRUG SYNERGISM; HL-60 CELLS; HUMANS; KINETICS; MITOCHONDRIA; NITROPHENOLS; PIPERAZINES; SULFONAMIDES; TIME FACTORS;

EID: 84893712518     PISSN: 02315882     EISSN: 13384325     Source Type: Journal    
DOI: 10.4149/gpb_2013053     Document Type: Article

References (55)

1. Abrams S. L., Steelman L. S., Shelton J. G., Chappell W., Basecke J., Stivala F., Donia M., Nicoletti F., Libra M., Martelli A. M., McCubrey J. A. (2010): Enhancing therapeutic efficacy by targeting non-oncogene addicted cells with combinations of signal transduction inhibitors and chemotherapy. Cell Cycle 9, 1839-1846 http://dx.doi.org/10.4161/cc.9.9.11544
2. Bolden J. E., Peart M. J., Johnstone R. W. (2006): Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov. 5, 769-784 http://dx.doi.org/10.1038/nrd2133
3. Burgess A. J., Pavey S., Warrener R., Hunter L. J., Piva T. J., Musgrove E. A., Saunders N., Parsons P. G., Gabrielli B. G. (2001): Up-regulation of p21(WAF1/CIP1) by histone deacetylase inhibitors reduces their cytotoxicity. Mol. Pharmacol. 60, 828-837
4. Calabresse C., Venturini L., Ronco G., Villa P., Chomienne C., Belpomme D. (1993): Butyric acid and its monosaccharide ester induce apoptosis in the HL-60 cell line. Biochem. Biophys. Res. Commun. 195, 31-38 http://dx.doi.org/10. 1006/bbrc.1993.2005
5. Carew J. S., Giles F. J., Nawrocki S. T. (2008): Histone deacetylase inhibitors: mechanisms of cell death and promise in combination cancer therapy. Cancer Lett. 269, 7-17 http://dx.doi.org/10.1016/j.canlet.2008.03.037
6. Chauhan D., Velankar M., Brahmandam M., Hideshima T., Podar K., Richardson P., Schlossman R., Ghobrial I., Raje N., Munshi N., Anderson K. C. (2007): A novel Bcl-2/Bcl-X(L)/Bcl-w inhibitor ABT-737 as therapy in multiple myeloma. Oncogene 26, 2374-2380 http://dx.doi.org/10.1038/sj.onc.1210028
7. Chen S., Dai Y., Harada H., Dent P., Grant S. (2007): Mcl-1 downregulation potentiates ABT-737 lethality by cooperatively inducing Bak activation and Bax translocation. Cancer Res. 67, 782-791 http://dx.doi.org/10. 1158/0008-5472.CAN-06-3964
8. Chen S., Dai Y., Pei X. Y., Grant S. (2009): Bim upregulation by histone deacetylases inhibitors mediates interactions with the Bcl-2 antagonist ABT-737: evidence for distinct roles for Bcl-2, Bcl-xl, and Mcl-1. Mol. Cell Biol. 29, 6149-669 http://dx.doi.org/10.1128/MCB.01481-08
9. Dai Q. S., Liu W., Wang X. B., Lu N., Gong D. D., Kong L. Y., Guo Q. L. (2011): NCPMF-60 induces G2/M cell cycle arrest and apoptosis in human hepatocellular carcinoma HepG2 cells. Anticancer Drugs 22, 46-57 http://dx.doi.org/10.1097/CAD.0b013e3283405801
10. Del Gazo Moore V., Brown J. R., Certo M., Love T. M., Novina C. D., Letai A. (2007): Chronic lymphocytic leukemia requires BCL2 to sequester prodeath BIM, explaining sensitivity to BCL2 antagonist ABT-737. J. Clin. Investig. 117, 112-121 http://dx.doi.org/10.1172/JCI28281
11. Deng J., Carlson N., Takeyama K., Dal Cin P., Shipp M., Letai A. (2007): BH3 profiling identifies three distinct classes of apoptotic blocks to predict response to ABT-737 and conventional chemotherapeutic agents. Cancer Cell. 12, 171-185 http://dx.doi.org/10.1016/j.ccr.2007.07.001
12. Gorman A. M., Healy S. J., Jäger R., Samali A. (2012): Stress management at the ER: regulators of ER stress-induced apoptosis. Pharmacol Ther. 134, 306-316 http://dx.doi.org/10.1016/j.pharmthera.2012.02.003
13. Fauser J. K., Prisciandaro L. D., Cummins A. G., Howarth G. S. (2011): Fatty acids as potential adjunctive colorectal chemotherapeutic agents. Cancer Biol. Ther. 11, 724-731 http://dx.doi.org/10.4161/cbt.11.8.15281
14. Filippovich I., Sorokina N., Khanna K. K., Lavin M. F. (1994): Butyrate induced apoptosis in lymphoid cells preceded by transient over-expression of HSP70 mRNA. Biochem. Biophys. Res. Commun. 198, 257-265 http://dx.doi.org/10. 1006/bbrc.1994.1036
15. Jurečeková J., Hatok J., Štefániková A., Dobrota D., Račay P. (2011): Targeting of Bcl-2 family proteins for treatment of acute leukaemia. Gen. Physiol. Biophys. 30, S3-12 http://dx.doi.org/10.4149/gpb-2011-SI1-3
16. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., Yoshimori T. (2000): LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728 http://dx.doi.org/10.1093/emboj/19.21.5720
17. Kahali S., Sarcar B., Prabhu A., Seto E., Chinnaiyan P. (2012): Class I histone deacetylases localize to the endoplasmic reticulum and modulate the unfolded protein response. FASEB J. 26, 2437-2445 http://dx.doi.org/10.1096/fj. 11-193706
18. Konopleva M., Contractor R., Tsao T., Samudio I., Ruvolo P. P., Kitada S., Deng X., Zhai D., Shi X. Y., Sneed T., et al. (2006): Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell 10, 375-388 http://dx.doi.org/10.1016/j.ccr.2006.10.006
19. Kuroda J., Puthalakath H., Cragg M. S., Kelly P. N., Bouillet P., Huang D. C., Kimura S., Ottmann O. G., Druker B. J., Villunger A., Roberts A. W., Strasser A. (2006): Bim and Bad mediate imatinib-induced killing of Bcr/Abl leukemic cells, and resistance due to their loss is overcome by a BH3 mimetic. Proc. Natl. Acad. Sci. USA 103, 14907-14912 http://dx.doi.org/10.1073/pnas. 0606176103
20. Lin X., Morgan-Lappe S., Huang X., Li L., Zakula D. M., Vernetti L. A., Fesik S. W., Shen Y. (2007): 'Seed' analysis of off-target siRNAs reveals an essential role of Mcl-1 in resistance to the small-molecule Bcl-2/Bcl-xl inhibitor ABT-737. Oncogene 26, 3972-3979 http://dx.doi.org/10.1038/sj.onc. 1210166
21. Litvak D. A., Evers B. M., Hwang K. O., Hellmich M. R., Ko T. C., Townsend C. M. Jr. (1998): Butyrate-induced differentiation of Caco-2 cells is associated with apoptosis and early induction of p21Waf1/Cip1 and p27Kip1. Surgery 124, 161-199 http://dx.doi.org/10.1016/S0039-6060(98)70116-3
22. Lukas J., Lukas C., Bartek J. (2011): More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat. Cell Biol. 13, 1161-1169 http://dx.doi.org/10.1038/ncb2344
23. Luo B., Lee A. S. (2013): The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 32, 805-818 http://dx.doi.org/10.1038/onc.2012.130
24. Malik S. A., Orhon I., Morselli E., Criollo A., Shen S., Mari-o G., Ben Younes A., Bénit P., Rustin P., Maiuri M. C., Kroemer G. (2011): BH3 mimetics activate multiple pro-autophagic pathways. Oncogene 30, 3918-3929 http://dx.doi.org/10.1038/onc.2011.104
25. Marks P. A. (2010): Histone deacetylase inhibitors: a chemical genetics approach to understanding cellular functions. Biochim. Biophys. Acta 1799, 717-725 http://dx.doi.org/10.1016/j.bbagrm.2010.05.008
26. New M., Olzscha H., La Thangue N. B. (2012): HDAC inhibitor-based therapies: can we interpret the code? Mol. Oncol. 6, 637-656 http://dx.doi.org/10.1016/j.molonc.2012.09.003
27. Oltersdorf T., Elmore S. W., Shoemaker A. R., Armstrong R. C., Augeri D. J., Belli B. A., Bruncko M., Deckwerth T. L., Dinges J., Hajduk P. J., et al. (2005): An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435, 677-681 http://dx.doi.org/10.1038/nature03579
28. Pajak B., Orzechowski A., Gajkowska B. (2007): Molecular basis of sodium butyrate-dependent proapoptotic activity in cancer cells. Adv. Med. Sci. 52, 83-88
29. Peart M. J., Tainton K. M., Ruefli A. A., Dear A. E., Sedelies K. A., O'Reilly L. A., Waterhouse N. J., Trapani J. A., Johnstone R. W. (2003): Novel mechanisms of apoptosis induced by histone deacetylase. Cancer Res. 63, 4460-4471
30. Qiu L., Burgess A., Fairlie D. P., Leonard H., Parsons P. G., Gabrielli B. G. (2000): Histone deacetylase inhibitors trigger a G2 checkpoint in normal cells that is defective in tumor cells. Mol. Biol. Cell 11, 2069-2083 http://dx.doi.org/10.1091/mbc.11.6.2069
31. Reddy R. K., Mao C., Baumeister P., Austin R. C., Kaufman R. J., Lee A. S. (2003): Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J. Biol. Chem. 278, 20915-20924 http://dx.doi.org/10.1074/jbc.M212328200
32. Risberg K., Fodstad Ø., Andersson Y. (2011): Synergistic anticancer effects of the 9.2.27PE immunotoxin and ABT-737 in melanoma. PLoS One 6, e24012 http://dx.doi.org/10.1371/journal.pone.0024012
33. Rodriguez D., Rojas-Rivera D., Hetz C. (2011): Integrating stress signals at the endoplasmic reticulum: The BCL-2 protein family rheostat. Biochim. Biophys. Acta 1813, 564-574 http://dx.doi.org/10.1016/j.bbamcr.2010.11.012
34. Rosati E., Sabatini R., Rampino G., De Falco F., Di Ianni M., Falzetti F., Fettucciari K., Bartoli A., Screpanti I., Marconi P. (2010): Novel targets for endoplasmic reticulum stress-induced apoptosis in B-CLL. Blood 116, 2713-2723 http://dx.doi.org/10.1182/blood-2010-03-275628
35. Rosato R. R., Almenara J. A., Cartee L., Betts V., Chellappan S. P., Grant S. (2002): The cyclin-dependent kinase inhibitor flavopiridol disrupts sodium butyrate-induced p21WAF1/CIP1 expression and maturation while reciprocally potentiating apoptosis in human leukemia cells. Mol. Cancer Ther. 1, 253-266
36. Rosato R. R., Almenara J. A., 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
37. Ruefli A. A., Ausserlechner M. J., Bernhard D., Sutton V. R., Tainton K. M., Kofler R., Smyth M. J., Johnstone R. W. (2001): The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proc. Natl. Acad. Sci. USA 98, 10833-10838 http://dx.doi.org/10.1073/pnas.191208598
38. Shao Y., Gao Z, Marks P. A., Jiang X. (2004): Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc. Natl. Acad. Sci. USA 101, 18030-18035 http://dx.doi.org/10.1073/pnas.0408345102
39. Song J. H., Kandasamy K., Zemskova M., Lin Y. W., Kraft A. S. (2011): The BH3 mimetic ABT-737 induces cancer cell senescence. Cancer Res. 71, 506-515 http://dx.doi.org/10.1158/0008-5472.CAN-10-1977
40. Strait K. A., Warnick C. T., Ford C. D., Dabbas B., Hammond E. H., Ilstrup S. J. (2005): Histone deacetylase inhibitors induce G2-checkpoint arrest and apoptosis in cisplatinum-resistant ovarian cancer cells associated with overexpression of the Bcl-2-related protein Bad. Mol Cancer Ther. 4, 603-611 http://dx.doi.org/10.1158/1535-7163.MCT-04-0107
41. Taddei A., Roche D., Bickmore W. A. Almouzni G. (2005): The effects of histone deacetylase inhibitors on heterochroma tin: implications for anticancer therapy? EMBO Rep. 6, 520-524 http://dx.doi.org/10.1038/sj.embor.7400441
42. Tang Y., Chen Y., Jiang H., Nie D. (2011): Short-chain fatty acids induced autophagy serves as an adaptive strategy for retarding mitochondria-mediated apoptotic cell death. Cell Death Differ. 18, 602-618 http://dx.doi.org/10.1038/cdd.2010.117
43. Tanimura A., Yujiri T., Tanaka Y., Hatanaka M., Mitani N., Nakamura Y., Mori K., Tanizawa Y. (2009): The anti-apoptotic role of the unfolded protein response in Bcr-Abl-positive leukemia cells. Leuk. Res. 33, 924-928 http://dx.doi.org/10.1016/j.leukres.2009.01.027
44. Uckun F. M., Qazi S., Ozer Z., Garner A. L., Pitt J., Ma H., Janda K. D. (2011): Inducing apoptosis in chemotherapy-resistant B-lineage acute lymphoblastic leukaemia cells by targeting HSPA5, a master regulator of the anti-apoptotic unfolded protein response signalling network. Br. J. Haematol. 153, 741-752 http://dx.doi.org/10.1111/j.1365-2141.2011.08671.x
45. van Delft M. F., Wei A. H., Mason K. D., Vandenberg C. J., Chen L., Czabotar P. E., Willis S. N., Scott C. L., Day C. L., Cory S., Adams J. M., Roberts A. W., Huang D. C. (2006): The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 10, 389-399 http://dx.doi.org/10.1016/j.ccr.2006.08.027
46. Vaziri C., Stice L., Faller D. V. (1998): Butyrate-induced G1 arrest results from p21-independent disruption of retinoblastoma protein-mediated signals. Cell Growth Differ. 9, 465-474
47. Vogler M., Weber K., Dinsdale D., Schmitz I., Schulze-Osthoff K., Dyer M. J., Cohen G. M. (2009): Different forms of cell death induced by putative BCL2 inhibitors. Cell Death Differ. 16, 1030-1039 http://dx.doi.org/10.1038/cdd.2009. 48
48. Vrba J., Dolezel P., Ulrichova J. (2010): Neutrophilic differentiation modulates the apoptotic response of HL-60 cells to sodium butyrate and sodium valproate. Neoplasma 57, 438-448 http://dx.doi.org/10.4149/neo-2010-05-438
49. Wey S., Luo B., Lee A. S. (2012a): Acute Inducible Ablation of GRP78 Reveals Its Role in Hematopoietic Stem Cell Survival, Lymphogenesis and Regulation of Stress Signaling. PLoS One 7, e39047 http://dx.doi.org/10.1371/ journal.pone.0039047
50. Wey S., Luo B., Tseng C. C., Ni M., Zhou H., Fu Y., Bhojwani D., Carroll W. L., Lee A. S. (2012b): Inducible knockout of GRP78/BiP in the hematopoietic system suppresses Ptennull leukemogenesis and AKT oncogenic signaling. Blood 119, 817-825 http://dx.doi.org/10.1182/blood-2011-06-357384
51. Whitecross K. F., Alsop A. E., Cluse L. A., Wiegmans A., Banks K. M., Coomans C., Peart M. J., Newbold A., Lindemann R. K., Johnstone R. W. (2009): Defining the target specificity of ABT-737 and synergistic antitumor activities in combination with histone deacetylase inhibitors. Blood 113, 1982-1991 http://dx.doi.org/10.1182/blood-2008-05-156851
52. Xiao Y., Yang F. Q., Li S. P., Gao J. L., Hu G., Lao S. C., Conceição E. L, Fung K. P., Wangl Y. T., Lee S. M. (2007): Furanodiene induces G2/M cell cycle arrest and apoptosis through MAPK signaling and mitochondria-caspase pathway in human hepatocellular carcinoma cells. Cancer Biol. Ther. 6, 1044-1050 http://dx.doi.org/10.4161/cbt.6.7.4317
53. Yamaguchi T., Cubizolles F., Zhang Y., Reichert N., Kohler H., Seiser C., Matthias P. (2010) Histone deacetylases 1 and 2 act in concert to promote the G1-to-S progression. Genes Dev. 24, 455-469 http://dx.doi.org/10.1101/gad.552310
54. Zhang W., Konopleva M., Ruvolo V. R., McQueen T., Evans R. L., Bornmann W. G., McCubrey J., Cortes J., Andreeff M. (2008): Sorafenib induces apoptosis of AML cells via Bim-mediated activation of the intrinsic apoptotic pathway. Leukemia 22, 808-818 http://dx.doi.org/10.1038/sj.leu.2405098
55. Zimra Y., Wasserman L., Maron L., Shaklai M., Nudelman A., Rephaeli A. (1997): Butyric acid and pivaloyloxymethyl butyrate, AN-9, a novel butyric acid derivative, induce apoptosis in HL-60 cells. J. Cancer Res. Clin. Oncol. 123, 152-160