The NF (Nuclear factor)-κB inhibitor parthenolide interacts with histone deacetylase inhibitors to induce MKK7/JNK1-dependent apoptosis in human acute myeloid leukaemia cells

British Journal of Haematology

Volumn 151, Issue 1, 2010, Pages 70-83

  Dai, Yun ^a   Guzman, Monica L ^b   Chen, Shuang ^a   Wang, Li ^a   Yeung, Sin Kei ^a   Pei, Xin Yan ^a   Dent, Paul ^c   Jordan, Craig T ^d   Grant, Steven ^a,c  

^a Department of Medicine   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

acute myelogenous leukaemia (AML); histone deacetylase inhibitor; JNK; nuclear factor (NF) B; parthenolide

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; PANOBINOSTAT; PARTHENOLIDE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR RELA; VORINOSTAT; ANTINEOPLASTIC AGENT; HISTONE DEACETYLASE INHIBITOR; SESQUITERPENE;

ACUTE GRANULOCYTIC LEUKEMIA; APOPTOSIS; ARTICLE; BLAST CELL; COLONY FORMING UNIT; CONTROLLED STUDY; DRUG POTENTIATION; FLOW CYTOMETRY; FUSION GENE; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LETHALITY; LEUKEMIA CELL; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG SCREENING; ENZYME ACTIVATION; METABOLISM; PATHOLOGY; PROCEDURES; SIGNAL TRANSDUCTION; TUMOR CELL CULTURE;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; DRUG EVALUATION, PRECLINICAL; DRUG SYNERGISM; ENZYME ACTIVATION; HISTONE DEACETYLASE INHIBITORS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LEUKEMIA, MYELOID, ACUTE; NF-KAPPA B; SESQUITERPENES; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 77956844466     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2010.08319.x     Document Type: Article

References (54)

1. Barabe, F., Kennedy, J.A., Hope, K.J. Dick, J.E. (2007) Modeling the initiation and progression of human acute leukemia in mice. Science, 316, 600 604.
2. Baud, V. Karin, M. (2009) Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls Nature Reviews Drug Discovery, 8, 33 40.
3. Bolden, J.E., Peart, M.J. Johnstone, R.W. (2006) Anticancer activities of histone deacetylase inhibitors. Nature Reviews Drug Discovery, 5, 769 784.
4. Bueso-Ramos, C.E., Rocha, F.C., Shishodia, S., Medeiros, L.J., Kantarjian, H.M., Vadhan-Raj, S., Estrov, Z., Smith, T.L., Nguyen, M.H. Aggarwal, B.B. (2004) Expression of constitutively active nuclear-kappa B RelA transcription factor in blasts of acute myeloid leukemia. Human Pathology, 35, 246 253.
5. Chen, L.F., Fischle, W., Verdin, E. Greene, W.C. (2001) Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science, 293, 1653 1657.
6. Chen, L.F., Williams, S.A., Mu, Y., Nakano, H., Duerr, J.M., Buckbinder, L. Greene, W.C. (2005) NF-kappaB RelA phosphorylation regulates RelA acetylation. Molecular and Cellular Biology, 25, 7966 7975.
7. Cilloni, D., Messa, F., Rosso, V., Arruga, F., Defilippi, I., Carturan, S., Catalano, R., Pautasso, M., Panuzzo, C., Nicoli, P., Messa, E., Morotti, A., Iacobucci, I., Martinelli, G., Bracco, E. Saglio, G. (2008) Increase sensitivity to chemotherapeutical agents and cytoplasmatic interaction between NPM leukemic mutant and NF-kappaB in AML carrying NPM1 mutations. Leukemia, 22, 1234 1240.
8. Dai, Y., Rahmani, M., Dent, P. Grant, S. (2005a) Blockade of histone deacetylase inhibitor-induced RelA/p65 acetylation and NF-[kappa]B activation potentiates apoptosis in leukemia cells through a process mediated by oxidative damage, XIAP downregulation, and c-Jun N-terminal kinase 1 activation. Molecular and Cellular Biology, 25, 5429 5444.
9. Dai, Y., Rahmani, M., Pei, X.Y., Khanna, P., Han, S.I., Mitchell, C., Dent, P. Grant, S. (2005b) Farnesyltransferase inhibitors interact synergistically with the Chk1 inhibitor UCN-01 to induce apoptosis in human leukemia cells through interruption of both Akt and MEK/ERK pathways and activation of SEK1/JNK. Blood, 105, 1706 1716.
10. De Smaele, E., Zazzeroni, F., Papa, S., Nguyen, D.U., Jin, R., Jones, J., Cong, R. Franzoso, G. (2001) Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature, 414, 308 313.
11. Duan, J., Friedman, J., Nottingham, L., Chen, Z., Ara, G. Van Waes, C. (2007) Nuclear factor-kappaB p65 small interfering RNA or proteasome inhibitor bortezomib sensitizes head and neck squamous cell carcinomas to classic histone deacetylase inhibitors and novel histone deacetylase inhibitor PXD101. Molecular Cancer Therapeutics, 6, 37 50.
12. Frelin, C., Imbert, V., Griessinger, E., Peyron, A.C., Rochet, N., Philip, P., Dageville, C., Sirvent, A., Hummelsberger, M., Berard, E., Dreano, M., Sirvent, N. Peyron, J.F. (2005) Targeting NF-kappaB activation via pharmacologic inhibition of IKK2-induced apoptosis of human acute myeloid leukemia cells. Blood, 105, 804 811.
13. Garcia-Manero, G., Yang, H., Bueso-Ramos, C., Ferrajoli, A., Cortes, J., Wierda, W.G., Faderl, S., Koller, C., Morris, G., Rosner, G., Loboda, A., Fantin, V.R., Randolph, S.S., Hardwick, J.S., Reilly, J.F., Chen, C., Ricker, J.L., Secrist, J.P., Richon, V.M., Frankel, S.R. Kantarjian, H.M. (2008a) Phase 1 study of the histone deacetylase inhibitor vorinostat (suberoylanilide hydroxamic acid [SAHA]) in patients with advanced leukemias and myelodysplastic syndromes. Blood, 111, 1060 1066.
14. Garcia-Manero, G., Assouline, S., Cortes, J., Estrov, Z., Kantarjian, H., Yang, H., Newsome, W.M., Miller, Jr., W.H., Rousseau, C., Kalita, A., Bonfils, C., Dubay, M., Patterson, T.A., Li, Z., Besterman, J.M., Reid, G., Laille, E., Martell, R.E. Minden, M. (2008b) Phase 1 study of the oral isotype specific histone deacetylase inhibitor MGCD0103 in leukemia. Blood, 112, 981 989.
15. Garcia-Pineres, A.J., Castro, V., Mora, G., Schmidt, T.J., Strunck, E., Pahl, H.L. Merfort, I. (2001) Cysteine 38 in p65/NF-kappaB plays a crucial role in DNA binding inhibition by sesquiterpene lactones. The Journal of Biological Chemistry, 276, 39713 39720.
16. George, P., Bali, P., Annavarapu, S., Scuto, A., Fiskus, W., Guo, F., Sigua, C., Sondarva, G., Moscinski, L., Atadja, P. Bhalla, K. (2005) Combination of the histone deacetylase inhibitor LBH589 and the hsp90 inhibitor 17-AAG is highly active against human CML-BC cells and AML cells with activating mutation of FLT-3. Blood, 105, 1768 1776.
17. Giles, F., Fischer, T., Cortes, J., Garcia-Manero, G., Beck, J., Ravandi, F., Masson, E., Rae, P., Laird, G., Sharma, S., Kantarjian, H., Dugan, M., Albitar, M. Bhalla, K. (2006) A phase I study of intravenous LBH589, a novel cinnamic hydroxamic acid analogue histone deacetylase inhibitor, in patients with refractory hematologic malignancies. Clinical Cancer Research, 12, 4628 4635.
18. Gopal, Y.N., Arora, T.S. Van Dyke, M.W. (2007) Parthenolide specifically depletes histone deacetylase 1 protein and induces cell death through ataxia telangiectasia mutated. Chemistry & Biology, 14, 813 823.
19. Grant, S., Easley, C. Kirkpatrick, P. (2007) Vorinostat. Nature Reviews Drug Discovery, 6, 21 22.
20. Grosjean-Raillard, J., Ades, L., Boehrer, S., Tailler, M., Fabre, C., Braun, T., De Botton, S., Israel, A., Fenaux, P. Kroemer, G. (2008) Flt3 receptor inhibition reduces constitutive NFkappaB activation in high-risk myelodysplastic syndrome and acute myeloid leukemia. Apoptosis, 13, 1148 1161.
21. Guzman, M.L., Neering, S.J., Upchurch, D., Grimes, B., Howard, D.S., Rizzieri, D.A., Luger, S.M. Jordan, C.T. (2001) Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood, 98, 2301 2307.
22. Guzman, M.L., Swiderski, C.F., Howard, D.S., Grimes, B.A., Rossi, R.M., Szilvassy, S.J. Jordan, C.T. (2002) Preferential induction of apoptosis for primary human leukemic stem cells. Proceedings of the National Academy of Sciences of the United States of America, 99, 16220 16225.
23. Guzman, M.L., Rossi, R.M., Karnischky, L., Li, X., Peterson, D.R., Howard, D.S. Jordan, C.T. (2005) The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood, 105, 4163 4169.
24. Guzman, M.L., Rossi, R.M., Neelakantan, S., Li, X., Corbett, C.A., Hassane, D.C., Becker, M.W., Bennett, J.M., Sullivan, E., Lachowicz, J.L., Vaughan, A., Sweeney, C.J., Matthews, W., Carroll, M., Liesveld, J.L., Crooks, P.A. Jordan, C.T. (2007) An orally bioavailable parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood, 110, 4427 4435.
25. Hehner, S.P., Hofmann, T.G., Droge, W. Schmitz, M.L. (1999) The antiinflammatory sesquiterpene lactone parthenolide inhibits NF-kappa B by targeting the I kappa B kinase complex. Journal of Immunology, 163, 5617 5623.
26. Hewamana, S., Alghazal, S., Lin, T.T., Clement, M., Jenkins, C., Guzman, M.L., Jordan, C.T., Neelakantan, S., Crooks, P.A., Burnett, A.K., Pratt, G., Fegan, C., Rowntree, C., Brennan, P. Pepper, C. (2008a) The NF-kappaB subunit Rel A is associated with in vitro survival and clinical disease progression in chronic lymphocytic leukemia and represents a promising therapeutic target. Blood, 111, 4681 4689.
27. Hewamana, S., Lin, T.T., Jenkins, C., Burnett, A.K., Jordan, C.T., Fegan, C., Brennan, P., Rowntree, C. Pepper, C. (2008b) The novel nuclear factor-kappaB inhibitor LC-1 is equipotent in poor prognostic subsets of chronic lymphocytic leukemia and shows strong synergy with fludarabine. Clinical Cancer Research, 14, 8102 8111.
28. Jenkins, C., Hewamana, S., Gilkes, A., Neelakantan, S., Crooks, P., Mills, K., Pepper, C. Burnett, A. (2008) Nuclear factor-kappaB as a potential therapeutic target for the novel cytotoxic agent LC-1 in acute myeloid leukaemia. British Journal of Haematology, 143, 661 671.
29. Kamata, H., Honda, S., Maeda, S., Chang, L., Hirata, H. Karin, M. (2005) Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell, 120, 649 661.
30. Liu, Y., Denlinger, C.E., Rundall, B.K., Smith, P.W. Jones, D.R. (2006) Suberoylanilide hydroxamic acid induces Akt-mediated phosphorylation of p300, which promotes acetylation and transcriptional activation of RelA/p65. The Journal of Biological Chemistry., 281, 31359 31368.
31. Liu, Y., Adachi, M., Zhao, S., Hareyama, M., Koong, A.C., Luo, D., Rando, T.A., Imai, K. Shinomura, Y. (2009a) Preventing oxidative stress: a new role for XBP1. Cell Death and Differentiation, 16, 847 857.
32. Liu, Z., Liu, S., Xie, Z., Pavlovicz, R.E., Wu, J., Chen, P., Aimiuwu, J., Pang, J., Bhasin, D., Neviani, P., Fuchs, J.R., Plass, C., Li, P.K., Li, C., Huang, T.H., Wu, L.C., Rush, L., Wang, H., Perrotti, D., Marcucci, G. Chan, K.K. (2009b) Modulation of DNA methylation by a sesquiterpene lactone parthenolide. The Journal of Pharmacology and Experimental Therapeutics, 329, 505 514.
33. Lu, Z.G., Liu, H., Yamaguchi, T., Miki, Y. Yoshida, K. (2009) Protein kinase Cdelta activates RelA/p65 and nuclear factor-kappaB signaling in response to tumor necrosis factor-alpha. Cancer Research, 69, 5927 5935.
34. Marks, P.A. (2007) Discovery and development of SAHA as an anticancer agent. Oncogene, 26, 1351 1356.
35. Nakajima, A., Komazawa-Sakon, S., Takekawa, M., Sasazuki, T., Yeh, W.C., Yagita, H., Okumura, K. Nakano, H. (2006) An antiapoptotic protein, c-FLIPL, directly binds to MKK7 and inhibits the JNK pathway. EMBO Journal, 25, 5549 5559.
36. Nakshatri, H., Rice, S.E. Bhat-Nakshatri, P. (2004) Antitumor agent parthenolide reverses resistance of breast cancer cells to tumor necrosis factor-related apoptosis-inducing ligand through sustained activation of c-Jun N-terminal kinase. Oncogene, 23, 7330 7344.
37. Nimmanapalli, R., Fuino, L., Bali, P., Gasparetto, M., Glozak, M., Tao, J., Moscinski, L., Smith, C., Wu, J., Jove, R., Atadja, P. Bhalla, K. (2003) Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or -refractory chronic myelogenous leukemia-blast crisis cells. Cancer Research, 63, 5126 5135.
38. Papa, S., Zazzeroni, F., Bubici, C., Jayawardena, S., Alvarez, K., Matsuda, S., Nguyen, D.U., Pham, C.G., Nelsbach, A.H., Melis, T., De Smaele, E., Tang, W.J., D'Adamio, L. Franzoso, G. (2004) Gadd45 beta mediates the NF-kappa B suppression of JNK signalling by targeting MKK7/JNKK2. Nature Cell Biology, 6, 146 153.
39. Patel, N.M., Nozaki, S., Shortle, N.H., Bhat-Nakshatri, P., Newton, T.R., Rice, S., Gelfanov, V., Boswell, S.H., Goulet, Jr., R.J., Sledge, Jr., G.W. Nakshatri, H. (2000) Paclitaxel sensitivity of breast cancer cells with constitutively active NF-kappaB is enhanced by IkappaBalpha super-repressor and parthenolide. Oncogene, 19, 4159 4169.
40. Perkins, N.D. (2006) Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway. Oncogene, 25, 6717 6730.
41. Sobota, R., Szwed, M., Kasza, A., Bugno, M. Kordula, T. (2000) Parthenolide inhibits activation of signal transducers and activators of transcription (STATs) induced by cytokines of the IL-6 family. Biochemical and Biophysical Research Communications, 267, 329 333.
42. Suvannasankha, A., Crean, C.D., Shanmugam, R., Farag, S.S., Abonour, R., Boswell, H.S. Nakshatri, H. (2008) Antimyeloma effects of a sesquiterpene lactone parthenolide. Clinical Cancer Research, 14, 1814 1822.
43. Tang, G., Minemoto, Y., Dibling, B., Purcell, N.H., Li, Z., Karin, M. Lin, A. (2001) Inhibition of JNK activation through NF-kappaB target genes. Nature, 414, 313 317.
44. Tournier, C., Dong, C., Turner, T.K., Jones, S.N., Flavell, R.A. Davis, R.J. (2001) MKK7 is an essential component of the JNK signal transduction pathway activated by proinflammatory cytokines. Genes and Development, 15, 1419 1426.
45. Ungerstedt, J.S., Sowa, Y., Xu, W.S., Shao, Y., Dokmanovic, M., Perez, G., Ngo, L., Holmgren, A., Jiang, X. Marks, P.A. (2005) Role of thioredoxin in the response of normal and transformed cells to histone deacetylase inhibitors. Proceedings of the National Academy of Sciences of the United States of America, 102, 673 678.
46. Vivanco, I., Palaskas, N., Tran, C., Finn, S.P., Getz, G., Kennedy, N.J., Jiao, J., Rose, J., Xie, W., Loda, M., Golub, T., Mellinghoff, I.K., Davis, R.J., Wu, H. Sawyers, C.L. (2007) Identification of the JNK signaling pathway as a functional target of the tumor suppressor PTEN. Cancer Cell, 11, 555 569.
47. Vrana, J.A., Decker, R.H., Johnson, C.R., Wang, Z., Jarvis, W.D., Richon, V.M., Ehinger, M., Fisher, P.B. Grant, S. (1999) Induction of apoptosis in U937 human leukemia cells by suberoylanilide hydroxamic acid (SAHA) proceeds through pathways that are regulated by Bcl-2/Bcl-XL, c-Jun, and p21CIP1, but independent of p53. Oncogene, 18, 7016 7025.
48. Wang, X., Destrument, A. Tournier, C. (2007) Physiological roles of MKK4 and MKK7: insights from animal models. Biochimica et Biophysica Acta, 1773, 1349 1357.
49. Weston, C.R. Davis, R.J. (2002) The JNK signal transduction pathway. Current Opinion in Genetics & Development, 12, 14 21.
50. Yamamoto, K., Ichijo, H. Korsmeyer, S.J. (1999) BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Molecular and Cellular Biology, 19, 8469 8478.
51. Yang, G., Thompson, M.A., Brandt, S.J. Hiebert, S.W. (2007) Histone deacetylase inhibitors induce the degradation of the t(8;21) fusion oncoprotein. Oncogene, 26, 91 101.
52. Yao, Z., Xing, L. Boyce, B.F. (2009) NF-kappaB p100 limits TNF-induced bone resorption in mice by a TRAF3-dependent mechanism. The Journal of Clinical Investigation, 119, 3024 3034.
53. Zhang, S., Lin, Z.N., Yang, C.F., Shi, X., Ong, C.N. Shen, H.M. (2004) Suppressed NF-kappaB and sustained JNK activation contribute to the sensitization effect of parthenolide to TNF-alpha-induced apoptosis in human cancer cells. Carcinogenesis, 25, 2191 2199.
54. Zunino, S.J., Ducore, J.M. Storms, D.H. (2007) Parthenolide induces significant apoptosis and production of reactive oxygen species in high-risk pre-B leukemia cells. Cancer Letters, 254, 119 127.