Celastrol induces cell apoptosis and inhibits the expression of the AML1-ETO/C-KIT oncoprotein in t(8;21) leukemia

Molecules

Volumn 21, Issue 5, 2016, Pages

  Yu, Xianjun ^a,b   Ruan, Xuzhi ^a   Zhang, Jingxuan ^a   Zhao, Qun ^b  

^a HUBEI UNIVERSITY OF MEDICINE   (China)

^b Chinese Academy of Sciences   (China)

Author keywords

Apoptosis; C KIT; Celastrol; Mitochondrial dysfunction; T(8; 21) leukemia

Indexed keywords

ANTINEOPLASTIC AGENT; ONCOPROTEIN; RUNX1 PROTEIN, HUMAN; RUNX1T1 PROTEIN, HUMAN; STEM CELL FACTOR RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX1; TRIPTERINE; TRITERPENE;

APOPTOSIS; BIOSYNTHESIS; CELL PROLIFERATION; CHROMOSOME 21; CHROMOSOME 8; DOWN REGULATION; DRUG EFFECTS; GENE TRANSLOCATION; GENETICS; HUMAN; LEUKEMIA, MYELOID, ACUTE; METABOLISM; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMOSOMES, HUMAN, PAIR 21; CHROMOSOMES, HUMAN, PAIR 8; CORE BINDING FACTOR ALPHA 2 SUBUNIT; DOWN-REGULATION; HUMANS; LEUKEMIA, MYELOID, ACUTE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-KIT; TRANSCRIPTION FACTORS; TRANSLOCATION, GENETIC; TRITERPENES;

EID: 84973512749     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules21050574     Document Type: Article

References (37)

1. Estey, E.; Dohner, H. Acute myeloid leukaemia. Lancet 2006, 368, 1894-1907.
2. Kuhnl, A.; Valk, P.J.; Sanders, M.A.; Ivey, A.; Hills, R.K.; Mills, K.I.; Gale, R.E.; Kaiser, M.F.; Dillon, R.; Joannides, M.; et al. Down-regulation of the Wnt inhibitor CXXC5 predicts a better prognosis in acute myeloid leukemia. Blood 2015, 125, 2985-2994.
3. Kelly, L.M.; Gilliland, D.G. Genetics of myeloid leukemias. Annu. Rev. Genom. Hum. Genet. 2002, 3, 179-198.
4. Elagib, K.E.; Goldfarb, A.N. Oncogenic pathways of AML1-ETO in acute myeloid leukemia: Multifaceted manipulation of marrow maturation. Cancer Lett. 2007, 251, 179-186.
5. Peterson, L.F.; Zhang, D.E. The 8;21 translocation in leukemogenesis. Oncogene 2004, 23, 4255-4262.
6. Wang, Y.Y.; Zhou, G.B.; Yin, T.; Chen, B.; Shi, J.Y.; Liang, W.X.; Jin, X.L.; You, J.H.; Yang, G.; Shen, Z.X.; et al. AML1-ETO and C-KIT mutation/overexpression in t(8;21) leukemia: Implication in stepwise leukemogenesis and response to Gleevec. Proc. Natl. Acad. Sci. USA 2005, 102, 1104-1109.
7. Liu, S.; Wu, L.C.; Pang, J.; Santhanam, R.; Schwind, S.; Wu, Y.Z.; Hickey, C.J.; Yu, J.; Becker, H.; Maharry, K.; et al. Sp1/NFkappaB/HDAC/miR-29b regulatory network in KIT-driven myeloid leukemia. Cancer Cell 2010, 17, 333-347.
8. Zhen, T.; Wu, C.F.; Liu, P.; Wu, H.Y.; Zhou, G.B.; Lu, Y.; Liu, J.X.; Liang, Y.; Li, K.K.; Wang, Y.Y.; et al. Targeting of AML1-ETO in t(8;21) leukemia by oridonin generates a tumor suppressor-like protein. Sci. Transl Med. 2012, 4, 127ra38.
9. Fang, H.T.; Zhang, B.; Pan, X.F.; Gao, L.; Zhen, T.; Zhao, H.X.; Ma, L.; Xie, J.; Liu, Z.; Yu, X.J.; et al. Bortezomib interferes with C-KIT processing and transforms the t(8;21)-generated fusion proteins into tumor-suppressing fragments in leukemia cells. Proc. Natl. Acad. Sci. USA 2012, 109, 2521-2526.
10. Xia, J.; Chen, S.F.; Lv, Y.P.; Lu, L.N.; Hu, W.X.; Zhou, Y.L. ZGDHu-1 induces G(2)/M phase arrest and apoptosis in Kasumi-1 cells. Mol. Med. Rep. 2015, 11, 3398-3404.
11. Sawney, S.; Arora, R.; Aggarwal, K.K.; Saluja, D. Esculetin Downregulates the Expression of AML1-ETO and C-Kit in Kasumi-1 Cell Line by Decreasing Half-Life of mRNA. J. Oncol. 2015, 2015, 781473.
12. Liu, Z.; Ma, L.; Zhou, G.B. The main anticancer bullets of the Chinese medicinal herb, thunder god vine. Molecules 2011, 16, 5283-5297.
13. Wang, G.Z.; Liu, Y.Q.; Cheng, X.; Zhou, G.B. Celastrol induces proteasomal degradation of FANCD2 to sensitize lung cancer cells to DNA crosslinking agents. Cancer Sci. 2015, 106, 902-908.
14. Liu, Z.; Ma, L.; Wen, Z.S.; Hu, Z.; Wu, F.Q.; Li, W.; Liu, J.; Zhou, G.B. Cancerous inhibitor of PP2A is targeted by natural compound celastrol for degradation in non-small-cell lung cancer. Carcinogenesis 2014, 35, 905-914.
15. Shrivastava, S.; Jeengar, M.K.; Reddy, V.S.; Reddy, G.B.; Naidu, V.G. Anticancer effect of celastrol on human triple negative breast cancer: possible involvement of oxidative stress, mitochondrial dysfunction, apoptosis and PI3K/Akt pathways. Exp. Mol. Pathol. 2015, 98, 313-327.
16. Guo, J.; Huang, X.; Wang, H.; Yang, H. Celastrol Induces Autophagy by Targeting AR/miR-101 in Prostate Cancer Cells. PLoS ONE 2015, 10, e0140745.
17. Lee, J.H.; Won, Y.S.; Park, K.H.; Lee, M.K.; Tachibana, H.; Yamada, K.; Seo, K.I. Celastrol inhibits growth and induces apoptotic cell death in melanoma cells via the activation ROS-dependent mitochondrial pathway and the suppression of PI3K/AKT signaling. Apoptosis 2012, 17, 1275-1286.
18. Zhou, Y.X.; Huang, Y.L. Antiangiogenic effect of celastrol on the growth of human glioma: An in vitro and in vivo study. Chin. Med. J. 2009, 122, 1666-1673.
19. Nicholson, D.W. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ. 1999, 6, 1028-1042.
20. Hengartner, M.O. The biochemistry of apoptosis. Nature 2000, 407, 770-776.
21. Roy, M.J.; Vom, A.; Czabotar, P.E.; Lessene, G. Cell death and the mitochondria: therapeutic targeting of the BCL-2 family-driven pathway. Br. J. Pharmacol. 2014, 171, 1973-1987.
22. Orrenius, S.; Gogvadze, V.; Zhivotovsky, B. Mitochondrial oxidative stress: implications for cell death. Annu. Rev. Pharmacol. Toxicol. 2007, 47, 143-183.
23. Van Loo, G.; Saelens, X.; van Gurp, M.; MacFarlane, M.; Martin, S.J.; Vandenabeele, P. The role of mitochondrial factors in apoptosis: A Russian roulette with more than one bullet. Cell Death Differ. 2002, 9, 1031-1042.
24. Amann, J.M.; Nip, J.; Strom, D.K.; Lutterbach, B.; Harada, H.; Lenny, N.; Downing, J.R.; Meyers, S.; Hiebert, S.W. ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain. Mol. Cell Biol. 2001, 21, 6470-6483.
25. Hatlen, M.A.; Wang, L.; Nimer, S.D. AML1-ETO driven acute leukemia: Insights into pathogenesis and potential therapeutic approaches. Front. Med. 2012, 6, 248-262.
26. Spirin, P.V.; Lebedev, T.D.; Orlova, N.N.; Gornostaeva, A.S.; Prokofjeva, M.M.; Nikitenko, N.A.; Dmitriev, S.E.; Buzdin, A.A.; Borisov, N.M.; Aliper, A.M.; et al. Silencing AML1-ETO gene expression leads to simultaneous activation of both pro-apoptotic and proliferation signaling. Leukemia 2014, 28, 2222-2228.
27. Jiao, B.; Wu, C.F.; Liang, Y.; Chen, H.M.; Xiong, S.M.; Chen, B.; Shi, J.Y.; Wang, Y.Y.; Wang, J.H.; Chen, Y.; et al. AML1-ETO9a is correlated with C-KIT overexpression/mutations and indicates poor disease outcome in t(8;21) acute myeloid leukemia-M2. Leukemia 2009, 23, 1598-1604.
28. Hirota, S.; Isozaki, K.; Moriyama, Y.; Hashimoto, K.; Nishida, T.; Ishiguro, S.; Kawano, K.; Hanada, M.; Kurata, A.; Takeda, M.; et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998, 279, 577-580.
29. Schnittger, S.; Kohl, T.M.; Haferlach, T.; Kern, W.; Hiddemann, W.; Spiekermann, K.; Schoch, C. KIT-D816 mutations in AML1-ETO-positive AML are associated with impaired event-free and overall survival. Blood 2006, 107, 1791-1799.
30. Shimada, A.; Taki, T.; Tabuchi, K.; Tawa, A.; Horibe, K.; Tsuchida, M.; Hanada, R.; Tsukimoto, I.; Hayashi, Y. KIT mutations, and not FLT3 internal tandem duplication, are strongly associated with a poor prognosis in pediatric acute myeloid leukemia with t(8;21): A study of the Japanese Childhood AML Cooperative Study Group. Blood 2006, 107, 1806-1809.
31. Gao, X.; Lin, J.; Gao, L.; Deng, A.; Lu, X.; Li, Y.; Wang, L.; Yu, L. High expression of c-kit mRNA predicts unfavorable outcome in adult patients with t(8;21) acute myeloid leukemia. PLoS ONE 2015, 10, e0124241.
32. Yee, N.S.; Hsiau, C.W.; Serve, H.; Vosseller, K.; Besmer, P. Mechanism of down-regulation of c-kit receptor. Roles of receptor tyrosine kinase, phosphatidylinositol 3'-kinase, and protein kinase C. J. Biol. Chem. 1994, 269, 31991-31998.
33. Ueda, S.; Mizuki, M.; Ikeda, H.; Tsujimura, T.; Matsumura, I.; Nakano, K.; Daino, H.; Honda Zi, Z.; Sonoyama, J.; Shibayama, H.; et al. Critical roles of c-Kit tyrosine residues 567 and 719 in stem cell factor-induced chemotaxis: contribution of src family kinase and PI3-kinase on calcium mobilization and cell migration. Blood 2002, 99, 3342-3349.
34. Harir, N.; Boudot, C.; Friedbichler, K.; Sonneck, K.; Kondo, R.; Martin-Lanneree, S.; Kenner, L.; Kerenyi, M.; Yahiaoui, S.; Gouilleux-Gruart, V.; et al. Oncogenic Kit controls neoplastic mast cell growth through a Stat5/PI3-kinase signaling cascade. Blood 2008, 112, 2463-2473.
35. Zhou, G.S.; Hu, Z.; Fang, H.T.; Zhang, F.X.; Pan, X.F.; Chen, X.Q.; Hu, A.M.; Xu, L.; Zhou, G.B. Biologic activity of triptolide in t(8;21) acute myeloid leukemia cells. Leuk Res. 2011, 35, 214-218.
36. Yu, X.J.; Han, Q.B.; Wen, Z.S.; Ma, L.; Gao, J.; Zhou, G.B. Gambogenic acid induces G1 arrest via GSK3beta-dependent cyclin D1 degradation and triggers autophagy in lung cancer cells. Cancer Lett. 2012, 322, 185-194.
37. Wang, L.; Zhao, W.L.; Yan, J.S.; Liu, P.; Sun, H.P.; Zhou, G.B.; Weng, Z.Y.; Wu, W.L.; Weng, X.Q.; Sun, X.J.; et al. Eriocalyxin B induces apoptosis of t(8;21) leukemia cells through NF-kappaB and MAPK signaling pathways and triggers degradation of AML1-ETO oncoprotein in a caspase-3-dependent manner. Cell Death Differ. 2007, 14, 306-317.