Triptolide inhibits Jak2 transcription and induces apoptosis in human myeloproliferative disorder cells bearing Jak2V617F through caspase-3-mediated cleavage of Mcl-1

Cancer Letters

Volumn 291, Issue 2, 2010, Pages 246-255

  Chen, Qi ^a   Lu, Zhongzheng ^a   Jin, Yanli ^a   Wu, Yongbin ^a   Pan, Jingxuan ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Apoptosis; Jak2; MPD; Triptolide; V617F mutation

Indexed keywords

CASPASE 3; JANUS KINASE 2; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; RNA POLYMERASE; SURVIVIN; TRIPTOLIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL DESTRUCTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; GENE MUTATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; MOUSE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; TUMOR; TUMOR REGRESSION;

AMINO ACID SUBSTITUTION; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; APOPTOSIS; CASPASE 3; CELL CYCLE; CELL LINE, TUMOR; CYCLOHEXIMIDE; DITERPENES; DNA PRIMERS; EPOXY COMPOUNDS; FLOW CYTOMETRY; HUMANS; JANUS KINASE 2; LEUKEMIA, ERYTHROBLASTIC, ACUTE; MYELOPROLIFERATIVE DISORDERS; PHENANTHRENES; PROTO-ONCOGENE PROTEINS C-BCL-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 77950025116     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2009.10.019     Document Type: Article

References (43)

1. Vainchenker W., Dusa A., and Constantinescu S.N. JAKs in pathology: role of Janus kinases in hematopoietic malignancies and immunodeficiencies. Semin. Cell Dev. Biol. 19 (2008) 385-393
2. Kralovics R., Passamonti F., Buser A.S., Teo S.S., Tiedt R., Passweg J.R., Tichelli A., Cazzola M., and Skoda R.C. A gain-of-function mutation of JAK2 in myeloproliferative disorders. New Engl. J. Med. 352 (2005) 1779-1790
3. Levine R.L., Wadleigh M., Cools J., Ebert B.L., Wernig G., Huntly B.J., Boggon T.J., Wlodarska I., Clark J.J., Moore S., Adelsperger J., Koo S., Lee J.C., Gabriel S., Mercher T., D'Andrea A., Frohling S., Dohner K., Marynen P., Vandenberghe P., Mesa R.A., Tefferi A., Griffin J.D., Eck M.J., Sellers W.R., Meyerson M., Golub T.R., Lee S.J., and Gilliland D.G. Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell 7 (2005) 387-397
4. Baxter E.J., Scott L.M., Campbell P.J., East C., Fourouclas N., Swanton S., Vassiliou G.S., Bench A.J., Boyd E.M., Curtin N., Scott M.A., Erber W.N., and Green A.R. Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet 365 (2005) 1054-1061
5. James C., Ugo V., Le Couedic J.P., Staerk J., Delhommeau F., Lacout C., Garcon L., Raslova H., Berger R., Bennaceur-Griscelli A., Villeval J.L., Constantinescu S.N., Casadevall N., and Vainchenker W. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 434 (2005) 1144-1148
6. Temerinac S., Klippel S., Strunck E., Roder S., Lubbert M., Lange W., Azemar M., Meinhardt G., Schaefer H.E., and Pahl H.L. Cloning of PRV-1, a novel member of the uPAR receptor superfamily, which is overexpressed in polycythemia rubra vera. Blood 95 (2000) 2569-2576
7. Parganas E., Wang D., Stravopodis D., Topham D.J., Marine J.C., Teglund S., Vanin E.F., Bodner S., Colamonici O.R., van Deursen J.M., Grosveld G., and Ihle J.N. Jak2 is essential for signaling through a variety of cytokine receptors. Cell 93 (1998) 385-395
8. Neubauer H., Cumano A., Muller M., Wu H., Huffstadt U., and Pfeffer K. Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell 93 (1998) 397-409
9. Ugo V., Marzac C., Teyssandier I., Larbret F., Lecluse Y., Debili N., Vainchenker W., and Casadevall N. Multiple signaling pathways are involved in erythropoietin-independent differentiation of erythroid progenitors in polycythemia vera. Exp. Hematol. 32 (2004) 179-187
10. Levine R.L., and Gilliland D.G. Myeloproliferative disorders. Blood 112 (2008) 2190-2198
11. Wernig G., Mercher T., Okabe R., Levine R.L., Lee B.H., and Gilliland D.G. Expression of Jak2V617F causes a polycythemia vera-like disease with associated myelofibrosis in a murine bone marrow transplant model. Blood 107 (2006) 4274-4281
12. Zhao R., Xing S., Li Z., Fu X., Li Q., Krantz S.B., and Zhao Z.J. Identification of an acquired JAK2 mutation in polycythemia vera. J. Biol. Chem. 280 (2005) 22788-22792
13. Lacout C., Pisani D.F., Tulliez M., Gachelin F.M., Vainchenker W., and Villeval J.L. JAK2V617F expression in murine hematopoietic cells leads to MPD mimicking human PV with secondary myelofibrosis. Blood 108 (2006) 1652-1660
14. Tiedt R., Hao-Shen H., Sobas M.A., Looser R., Dirnhofer S., Schwaller J., and Skoda R.C. Ratio of mutant JAK2-V617F to wild-type Jak2 determines the MPD phenotypes in transgenic mice. Blood 111 (2008) 3931-3940
15. Xing S., Wanting T.H., Zhao W., Ma J., Wang S., Xu X., Li Q., Fu X., Xu M., and Zhao Z.J. Transgenic expression of JAK2V617F causes myeloproliferative disorders in mice. Blood 111 (2008) 5109-5117
16. Dameshek W. Some speculations on the myeloproliferative syndromes. Blood 6 (1951) 372-375
17. Wernig G., Kharas M.G., Okabe R., Moore S.A., Leeman D.S., Cullen D.E., Gozo M., McDowell E.P., Levine R.L., Doukas J., Mak C.C., Noronha G., Martin M., Ko Y.D., Lee B.H., Soll R.M., Tefferi A., Hood J.D., and Gilliland D.G. Efficacy of TG101348, a selective JAK2 inhibitor, in treatment of a murine model of JAK2V617F-induced polycythemia vera. Cancer Cell 13 (2008) 311-320
18. Hexner E.O., Serdikoff C., Jan M., Swider C.R., Robinson C., Yang S., Angeles T., Emerson S.G., Carroll M., Ruggeri B., and Dobrzanski P. Lestaurtinib (CEP701) is a JAK2 inhibitor that suppresses JAK2/STAT5 signaling and the proliferation of primary erythroid cells from patients with myeloproliferative disorders. Blood 111 (2008) 5663-5671
19. Guerini V., Barbui V., Spinelli O., Salvi A., Dellacasa C., Carobbio A., Introna M., Barbui T., Golay J., and Rambaldi A. The histone deacetylase inhibitor ITF2357 selectively targets cells bearing mutated JAK2(V617F). Leukemia 22 (2008) 740-747
20. Shi J., Zhao Y., Ishii T., Hu W., Sozer S., Zhang W., Bruno E., Lindgren V., Xu M., and Hoffman R. Effects of chromatin-modifying agents on CD34+ cells from patients with idiopathic myelofibrosis. Cancer Res. 67 (2007) 6417-6424
21. Chen R., Gandhi V., and Plunkett W. A sequential blockade strategy for the design of combination therapies to overcome oncogene addiction in chronic myelogenous leukemia. Cancer Res. 66 (2006) 10959-10966
22. Jin Y., Chen Q., Shi X., Lu Z., Cheng C., Lai Y., Zheng Q., and Pan J. Activity of triptolide against human mast cells harboring the kinase domain mutant KIT. Cancer Sci. 100 (2009) 1335-1343
23. Shi X., Jin Y., Cheng C., Zhang H., Zou W., Zheng Q., Lu Z., Chen Q., Lai Y., and Pan J. Triptolide inhibits Bcr-Abl transcription and induces apoptosis in STI571-resistant chronic myelogenous leukemia cells harboring T315I mutation. Clin. Cancer Res. 15 (2009) 1686-1697
24. Jin Y., Chen Q., Lu Z., Chen B., and Pan J. Triptolide abrogates oncogene FIP1L1-PDGFRalpha addiction and induces apoptosis in hypereosinophilic syndrome. Cancer Sci. 100 (2009) 2210-2217
25. Pan J., Quintas-Cardama A., Manshouri T., Giles F.J., Lamb P., Tefferi A., Cortes J., Kantarjian H., and Verstovsek S. The novel tyrosine kinase inhibitor EXEL-0862 induces apoptosis in human FIP1L1-PDGFR-alpha-expressing cells through caspase-3-mediated cleavage of Mcl-1. Leukemia 21 (2007) 1395-1404
26. Pan J., Xu G., and Yeung S.C. Cytochrome c release is upstream to activation of caspase-9, caspase-8, and caspase-3, in the enhanced apoptosis of anaplastic thyroid cancer cells induced by manumycin and paclitaxel. J. Clin. Endocrinol. Metab. 86 (2001) 4731-4740
27. Pan [27] J., Quintas-Cardama A., Kantarjian H.M., Akin C., Manshouri T., Lamb P., Cortes J.E., Tefferi A., Giles F.J., and Verstovsek S. EXEL-0862, a novel tyrosine kinase inhibitor, induces apoptosis in vitro and ex vivo in human mast cells expressing the KIT D816V mutation. Blood 109 (2007) 315-322
28. Clohessy J.G., Zhuang J., and Brady H.J. Characterisation of Mcl-1 cleavage during apoptosis of haematopoietic cells. Br. J. Haematol. 125 (2004) 655-665
29. Michels J., O'Neill J.W., Dallman C.L., Mouzakiti A., Habens F., Brimmell M., Zhang K.Y., Craig R.W., Marcusson E.G., Johnson P.W., and Packham G. Mcl-1 is required for Akata6 B-lymphoma cell survival and is converted to a cell death molecule by efficient caspase-mediated cleavage. Oncogene 23 (2004) 4818-4827
30. Weinstein I.B., and Joe A. Oncogene addiction. Cancer Res. 68 (2008) 3077-3080
31. Corson T.W., and Crews C.M. Molecular understanding and modern application of traditional medicines: triumphs and trials. Cell 130 (2007) 769-774
32. Tao X.L., Sun Y., Dong Y., Xiao Y.L., Hu D.W., Shi Y.P., Zhu Q.L., Dai H., and Zhang N.Z. A prospective, controlled, double-blind, cross-over study of tripterygium wilfodii hook F in treatment of rheumatoid arthritis. Chin. Med. J. (Engl.) 102 (1989) 327-332
33. Jiang X. Clinical observations on the use of the Chinese herb Tripterygium wilfordii Hook for the treatment of nephrotic syndrome. Pediatr. Nephrol. 8 (1994) 343-344
34. Efferth T., Li P.C., Konkimalla V.S., and Kaina B. From traditional Chinese medicine to rational cancer therapy. Trends Mol. Med. 13 (2007) 353-361
35. Tao X., Schulze-Koops H., Ma L., Cai J., Mao Y., and Lipsky P.E. Effects of Tripterygium wilfordii hook F extracts on induction of cyclooxygenase 2 activity and prostaglandin E2 production. Arthritis Rheum. 41 (1998) 130-138
36. Fidler J.M., Li K., Chung C., Wei K., Ross J.A., Gao M., and Rosen G.D. PG490-88, a derivative of triptolide, causes tumor regression and sensitizes tumors to chemotherapy. Mol. Cancer Ther. 2 (2003) 855-862
37. Manshouri T., Quintas-Cardama A., Nussenzveig R.H., Gaikwad A., Estrov Z., Prchal J., Cortes J.E., Kantarjian H.M., and Verstovsek S. The JAK kinase inhibitor CP-690,550 suppresses the growth of human polycythemia vera cells carrying the JAK2V617F mutation. Cancer Sci. 99 (2008) 1265-1273
38. Carter B.Z., Mak D.H., Schober W.D., McQueen T., Harris D., Estrov Z., Evans R.L., and Andreeff M. Triptolide induces caspase-dependent cell death mediated via the mitochondrial pathway in leukemic cells. Blood 108 (2006) 630-637
39. Jiang X.H., Wong B.C., Lin M.C., Zhu G.H., Kung H.F., Jiang S.H., Yang D., and Lam S.K. Functional p53 is required for triptolide-induced apoptosis and AP-1 and nuclear factor-kappaB activation in gastric cancer cells. Oncogene 20 (2001) 8009-8018
40. Phillips P.A., Dudeja V., McCarroll J.A., Borja-Cacho D., Dawra R.K., Grizzle W.E., Vickers S.M., and Saluja A.K. Triptolide induces pancreatic cancer cell death via inhibition of heat shock protein 70. Cancer Res. 67 (2007) 9407-9416
41. Dasmahapatra G., Yerram N., Dai Y., Dent P., and Grant S. Synergistic interactions between vorinostat and sorafenib in chronic myelogenous leukemia cells involve Mcl-1 and p21CIP1 down-regulation. Clin. Cancer Res. 13 (2007) 4280-4290
42. Aichberger K.J., Mayerhofer M., Gleixner K.V., Krauth M.T., Gruze A., Pickl W.F., Wacheck V., Selzer E., Mullauer L., Agis H., Sillaber C., and Valent P. Identification of MCL1 as a novel target in neoplastic mast cells in systemic mastocytosis: inhibition of mast cell survival by MCL1 antisense oligonucleotides and synergism with PKC412. Blood 109 (2007) 3031-3041
43. Rahmani M., Davis E.M., Bauer C., Dent P., and Grant S. Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves down-regulation of Mcl-1 through inhibition of translation. J. Biol. Chem. 280 (2005) 35217-35227