Cancer Letters
Volume 241, Issue 1 , Pages 31-41 , 8 September 2006

Triptolide induces Bcl-2 cleavage and mitochondria dependent apoptosis in p53-deficient HL-60 cells

Received 9 July 2005 ,Accepted 4 October 2005.

References 

  1. Li FQ, Lu XZ, Liang XB, Zhou HF, Xue B, Liu XY, et al. Triptolide, a Chinese herbal extract, protects dopaminergic neurons from inflammation-mediated damage through inhibiton of microglial activation,. J. Neuroimmunol. 2004;148:24–31
  2. Qiu D, Kao PN. Immunosuppressive and anti-inflammatory mechanism of triptolide, the principal active diterpenoid from the Chinese medicinal herb tripterygium wilfordii hook. f. Drugs R.D. 2003;4:1–18
  3. Lue Y, Sinhahikim AP, Wang C, Leung A, Baravarian S, Reutrakul V, et al. Triptolide: a potential male contraceptive. J. Androl. 1998;19:479–486
  4. Matlin SA, Belenguer A, Stacey VE, Oian SZ, Xu Y, Zhang JW, et al. Male antifertility compounds from Tripterygium wilfordii Hook f. Contraception. 1993;47:387–400
  5. Shamon LA, Pezzuto JM, Graves JM, Mehta RR, Wangcharoentrakul S, Sangsuwan R, et al. Evaluation of the mutagenic, cytotoxic, and antitumor potential of triptolide, a highly oxygenated diterpene isolated from Tripterygium wilfordii. Cancer Lett. 1997;112:113–117
  6. Wei YS, Adachi I. Inhibitory effect of triptolide on colony formation of breast and stomach cancer cell lines. Acta Pharmacol. Sin. 1991;12:406–410
  7. Fidler JM, Li K, Chung C, Wei K, Ross JA, Gao M, et al. PG490-88, a derivative of triptolide, causes tumor regression and sensitizes tumors to chemotherapy. Mol. Cancer Ther. 2003;2:855–862
  8. Jiang XH, Wong BC, Lin MC, Zhu GH, Kung HF, Jiang SH, et al. Functional p53 is required for triptolide-induced apoptosis and AP-1 and nuclear factor-κB activation in gastric cancer cells. Oncogene. 2001;20:8009–8018
  9. Kiviharju TM, Lecane PS, Sellers RG, Peehl DM. Antiproliferative and proapoptotic activities of triptolide (PG490), a natural product entering clinical trials, on primary cultures of human prostatic epithelial cells. Clin. Cancer Res. 2002;8:2666–2674
  10. Chan EW, Cheng SC, Sin FW, Xie Y. Triptolide induced cytotoxic effects on human promyelocytic leukemia, T cell lymphoma and human hepatocellular carcinoma cell lines. Toxicol. Lett. 2001;122:81–87
  11. Lee KY, Chang WT, Oiu D, Kao PN, Rosen GD. PG490 (triptolide) cooperate with tumor necrosis factor-α to induce apoptosis in tumor cells. J. Biol. Chem. 1999;274:13451–13455
  12. Chang WT, Kang JJ, Lee KY, Wei K, Anderson E, Gotmare S, et al. Triptolide and chemotherapy cooperate in tumor cell apoptosis, a role for the p53 pathway. J. Biol. Chem. 2001;276:2221–2227
  13. El-Deiry WS. The role of p53 in chemosensitivity and radiosensitivity. Oncogene. 2000;22:7486–7495
  14. O'Connor PM, Jackman J, Bae I, Myers TG, Fan S, Mutoh M, et al. Characterization of the p53 tumor suppressor pathway in cell lines of the National Cancer Institute anticancer drug screen and correlations with the growth-inhibitory potency of 123 anticancer agents. Cancer Res. 1997;57:4285–4300
  15. Piovesan B, Pennell N, Berinstein NL. Human lymphoblastoid cell lines expressing mutant p53 exhibit decreased sensitivity to cisplatin-induced cytotoxicity. Oncogene. 1998;17:2339–2350
  16. Yamamoto M, Maehara Y, Oda S, Ichiyoshi Y, Kusumoto T, Sugimachi K. The p53 tumor suppressor gene in anticancer agent-induced apoptosis and chemosensitivity of human gastrointestinal cancer cell lines. Cancer Chemother. Pharmacol. 1999;43:43–49
  17. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature. 2000;408:307–310
  18. Takimoto R, El-Deiry WS. Wild-type p53 transactivates the KILLER/DR5 gene through an intronic sequence-specific DNA-binding site. Oncogene. 2000;19:1735–1743
  19. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, et al. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science. 2000;288:1053–1058
  20. Sax JK, Fei P, Murphy ME, Bernhard E, Korsmeyer SJ, El-Deiry WS. BID regulation by p53 contributes to chemosensitivity. Nat. Cell. Biol. 2002;4:842–849
  21. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ. Proapoptotic BAX and BAK: a requisite gateway to mitochondria dysfunction and death. Science. 2001;292:727–730
  22. El-Deiry WS. Regulation of p53 downstream genes. Semin. Cancer Biol. 1998;8:345–357
  23. Hermeking H, Lengauer C, Polyak K, He TC, Zhang L, Thiagalingam S, et al. 14-3-3 sigma is a p53-regulated inhibitor of G2/M progression. Mol. Cell. 1997;1:3–11
  24. Cory S, Adams JM. The Bcl-2 family: regulation of the cellular life-or-death switch. Nat. Rev. Cancer. 2002;2:647–656
  25. Dole M, Nunez G, Merchant AK, Maybaum J, Rode CK, Bloch CA, et al. Bcl-2 inhibits chemotherapy-induced apoptosis in neuroblastoma. Cancer Res. 1994;54:3253–3259
  26. Kamesaki S, Kamesaki H, Jorgensen TJ, Tanizawa A, Pommier Y, Cossman J. Bcl-2 protein inhibits etoposide-induced apoptosis through its effects on events subsequent to topoisomerase II-induced DNA strand breaks and their repair. Cancer Res. 1993;53:4251–4256
  27. Teixeira C, Reed JC, Pratt MA. Estrogen promotes chemotherapeutic drug resistance by a mechanism involving Bcl-2 proto-oncogene expression in human breast cancer cells. Cancer Res. 1995;55:3902–3907
  28. Jiang M, Milner J. Bcl-2 constitutively suppresses p53-dependent apoptosis in colorectal cancer cells. Genes Dev. 2003;17:832–837
  29. Cheng EH, Kirsh DG, Clem RJ, Ravi RR, Kastan MB, Bedi A, et al. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 1997;278:1966–1968
  30. Sato T, Hanada M, Bodrug S, Irie S, Iwama N, Boise LH, et al. Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system. Proc. Natl. Acad. Sci. USA. 1994;91:9238–9242
  31. Haldar S, Jena N, Croce CM. Inactivation of Bcl-2 by phosphorylation. Proc. Natl. Acad. Sci. USA. 1995;92:4507–4511
  32. Srivastava RK, Srivastava AR, Korsmeyer SJ, Nesterova M, Cho-Chung YS, Longo DL. Involvement of microtubules in the regulation of Bcl-2 phosphorylation and apoptosis through cyclic AMP-dependent protein kinases. Mol. Cell. Biol. 1998;18:3509–3517
  33. Kirsch DG, Doseff A, Chau BN, Lim DS, De Souza-Pinto NC, Hansford R, et al. Caspase-3-dependent cleavage of Bcl-2 promotes release of cytochrome c. J. Biol. Chem. 1999;274:21155–21161
  34. Kim YM, Kim TH, Seol DW, Talanian RV, Billiar TR. Nitric oxide suppression of apoptosis occurs in association with an inhibition of Bcl-2 cleavage and cytochrome c release. J. Biol. Chem. 1998;273:1437–1441
  35. Liang Y, Nylander KD, Yan C, Schor NF. Role of caspase 3-dependent Bcl-2 cleavage in potentiation of apoptosis by Bcl-2. Mol. Pharmacol. 2002;61:142–149
  36. Wada T, Penninger JM. Mitogen-activated protein kinases in apoptosis regulation. Oncogene. 2004;23:2838–2849
  37. Platanias LC. Map kinase signaling pathways and hematologic malignancies. Blood. 2003;101:4667–4679
  38. Dhanwada KR, Dickens M, Neades R, Davis R, Pelling JC. Differential effects of UV-B and UV-C components of solar radiation on MAP kinase signal transduction pathways in epidermal keratinocytes. Oncogene. 1995;11:1947–1953
  39. Porras A, Zuluaga S, Black E, Valladares A, Alvarez AM, Ambrosino C, et al. P38 alpha Mitogen-activated protein kinase sensitizes cells to apoptosis induced by different stimuli. Mol. Biol. Cell. 2004;15:922–933
  40. Price MA, Cruzalegui FH, Treisman R. The p38 and ERK MAP kinase pathways cooperate to activate ternary complex factors and c-fos transcription in response to UV light. EMBO J. 1996;15:6552–6563
  41. Frese S, Pirnia F, Miescher D, Krajewski S, Borner MM, Reed JC, et al. PG490-mediated sensitization of lung cancer cells to Apo-2L/TRAIL-induced apoptosis requires action of ERK2. Oncogene. 2003;22:5427–5435
  42. Zhang QH, Sheng HP, Loh TT. Bcl-2 protects HL-60 cells from apoptosis by stabilizing their intracellular calcium pools. Life Sci. 2001;68:2873–2883
  43. Budihardjo I, Oliver H, Lutter M, Luo X, Wang X. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell. Dev. Biol. 1999;15:269–290
  44. Gimonet D, Landais E, Bobichon H, Coninx P, Liautaud-Roger F. Induction of apoptosis by bleomycin in p53-null HL-60 leukemia cells. Int. J. Oncol. 2004;24:313–319
  45. Choi YJ, Kim TG, Kim YH, Lee SH, Kwon YK, Suh SI, et al. Immunosuppressant PG490 (triptolide) induces apoptosis through the activation of caspase-3 and down-regulation of XIAP in U937 cells. Biochem. Pharmacol. 2003;66:273–280
  46. O'Reilly LA, Huang DC, Strasser A. The cell death inhibitor Bcl-2 and its homologues influence control of cell cycle entry. EMBO J. 1996;15:6979–6990
  47. Gao G, Dou QP. G1 phase-dependent expression of Bcl-2 mRNA and protein correlates with chemoresistance of human cancer cells. Mol. Pharmacol. 2000;58:1001–1010
  48. Vairo S, Soos TJ, Upton TM, Zalvide J, DeCaprio JA, Ewen ME, et al. Bcl-2 retards cell cycle entry through p27(kip1), pRB, relative p130, and altered E2F regulation. Mol. Cell. Biol. 2000;20:4745–4753
  49. Marvel J, Perkins GR, Lopez-Rivas A, Collins MK. Growth factor starvation of Bcl-2 overexpressing murine bone marrow cells induced refractoriness of IL-3 stimulation of proliferation. Oncogene. 1994;9:1117–1122
  50. Liu Q, Chen T, Chen H, Zhang M, Li N, Lu Z, et al. Triptolide (PG-490) induces apoptosis of dendritic cells through sequential p38 MAP kinase phosphorylation and caspase 3 activation. Biochem. Biophys. Res. Commun. 2004;319:980–986
  51. Del Bello B, Valentini MA, Zunino F, Comporti M, Maellaro E. Cleavage of Bcl-2 in oxidant-and cisplatin-induced apoptosis of human melanoma cells. Oncogene. 2001;20:4591–4595
  52. Mahieux R, Pise-Masison C, Gessain A, Brady JN, Olivier R, Perret E, et al. Arsenic trioxide induces apoptosis in human T-cell leukemia virus type 1- and type 2-infected cells by a caspase-3-dependent mechanism involving Bcl-2 cleavage. Blood. 2001;98:3762–3769
  53. Fadeel B, Hassan Z, Hellstrom-Liderg E, Henter JI, Orrenius S, Zhivotovsky B. Cleavage of Bcl-2 is an early event in chemotherapy-induced apoptosis of human myeloid leukemia cells. Leukemia. 1999;13:719–728
  54. Chen Q, Gong B, Almasan A. Distinct stages of cytochrome c release from mitochondria: evidence for a feedback amplification loop linking caspase activation to mitochondrial dysfunction in genotoxic stress induced apoptosis. Cell Death Differ. 2000;7:227–233
  55. Prokop A, Wrasidlo W, Lode H, Herold R, Lang F, Henze G, et al. Induction of apoptosis by enediyne antibiotic calicheamicin thetaII proceeds through a caspase-mediated mitochondrial amplification loop in an entirely Bax-dependent manner. Oncogene. 2003;22:9107–9120
  56. Chen P, Li J, Barnes J, Kokkonen GC, Lee JC, Liu Y. Restraint of proinflammatory cytokine biosynthesis by mitogen-activated protein kinase phosphate-1 in lipopolysaccharide-stimulated macrophages,. J. Immunol. 2002;169:6408–6416

PII: S0304-3835(05)00874-8

doi: 10.1016/j.canlet.2005.10.001

Cancer Letters
Volume 241, Issue 1 , Pages 31-41 , 8 September 2006