A Novel cyano derivative of 11-Keto-β-Boswellic acid causes apoptotic death by disrupting PI3K/AKT/Hsp-90 cascade, mitochondrial integrity, and other cell survival signaling events in HL-60 cells

Molecular Carcinogenesis

Volumn 51, Issue 9, 2012, Pages 679-695

  Khan, Sheema ^a   Kaur, Rajbir ^a   Shah, Bhahwal A ^a   Malik, Fayaz ^a   Kumar, Ajay ^a   Bhushan, Shashi ^a   Jain, S K ^b   Taneja, Subhash C ^a   Singh, Jaswant ^a  

^a CSIR INDIAN INSTITUTE OF INTEGRATIVE MEDICINE   (India)

^b HAMDARD UNIVERSITY   (India)

Author keywords

Apoptosis; Caspases; Cytotoxicity; NF B; PBMC

Indexed keywords

11 OXO BETA BOSWELLIC ACID; ANTINEOPLASTIC AGENT; APOPTOSIS INDUCING FACTOR; BUTYL 2 CYANO 3,11 DIOXOURS 1,12 DIEN 24 OATE; CASPASE 3; CASPASE 9; CYTOCHROME C; HEAT SHOCK PROTEIN 90; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BID; PROTEIN KINASE B; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SMALL INTERFERING RNA; SURVIVIN; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOSOL; DRUG CYTOTOXICITY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; IC 50; INTRACELLULAR SIGNALING; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; UPREGULATION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CASPASES; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; FIBROBLASTS; FLOW CYTOMETRY; GINGIVA; HL-60 CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LEUKOCYTES, MONONUCLEAR; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASE; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRITERPENES;

EID: 84864039094     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20821     Document Type: Article

References (52)

1. Fisher DE. Apoptosis in cancer therapy: Crossing the threshold. Cell 1994; 78: 539-542.
2. Bruckheimer EM, Kyprianou N. Apoptosis in prostate carcinogenesis. A growth regulator and a therapeutic target. Cell Tissue Res 2000; 301: 153-162.
3. Baer MR, George SL, Dodge RK, et al. Phase 3 study of the multidrug resistance modulator PSC-833 in previously untreated patients 60 years of age and older with acute myeloid leukemia: Cancer and Leukemia Group B Study 9720. Blood 2002; 100: 1224-1232.
4. Beran M, Estey E, O'Brien S, et al. Topotecan and cytarabine is an active combination regimen in myelodysplastic syndromes and chronic myelomonocytic leukemia. J Clin Oncol 1999; 17: 2819-2830.
5. Schimmer AD, Hedley DW, Penn LZ, Minden MD. Receptor- and mitochondrial mediated apoptosis in acute leukemia: A translational view. Blood 2001; 98: 3541-3553.
6. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2002; 2: 489-501.
7. Clark AS, West K, Streicher S, Dennis PA. Constitutive and inducible Akt activity promotes resistance to chemotherapy, trastuzumab, or tamoxifen in breast cancer cells. Mol Cancer Ther 2002; 1: 707-717.
8. Datta SR, Dudek H, Tao X, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997; 91: 231-241.
9. Mohsin SK, Weiss HL, Gutierrez MC, et al. Neoadjuvant trastuzumab induces apoptosis in primary breast cancers. J Clin Oncol 2005; 23: 2460-2468.
10. Sawyers CL. Rational therapeutic intervention in cancer: Kinases as drug targets. Curr Opin Genet Dev 2002; 12: 111-115.
11. Altieri DC. Validating survivin as a cancer therapeutic target. Nat Rev Cancer 2003; 3: 46-54.
12. Salvesen GS, Duckett CS. IAP proteins: Blocking the road to death's door. Nat Rev Mol Cell Biol 2002; 3: 401-410.
13. Ibrado AM, Huang Y, Fang G, Liu L, Bhalla K. Overexpression of Bcl-2 or Bcl-xL inhibits Ara-C-induced CPP32/Yama protease activity and apoptosis of human acute myelogenous leukemia HL-60 cells. Cancer Res 1996; 56: 4743-4748.
14. Cory S, Adams JM. The Bcl2 family: Regulators of the cellular life-or-death switch. Nat Rev Cancer 2002; 2: 647-656.
15. Daniel PT, Schulze OK, Belka C, Güner D. Guardians of cell death: The Bcl-2 family proteins. Essays Biochem 2003; 39: 73-88.
16. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004; 305: 626-629.
17. Martinou JC, Green DR. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2001; 2: 63-67.
18. Van Loo G, Saelens X, Van Gurp M, et al. The role of mitochondrial factors in apoptosis: A Russian roulette with more than one bullet. Cell Death Differ 2002; 9: 1031-1042.
19. Shah BA, Qazi GN, Taneja SC. Boswellic acids: A group of medicinally important compounds. Nat Prod Rep 2009; 26: 72-89.
20. Shashi B, Kumar A, Malik F, et al. A triterpenediol from Boswellia serrata induces apoptosis through both the intrinsic and extrinsic apoptotic pathways in human leukemia HL-60 cells. Apoptosis 2007; 12: 1911-1926.
21. Singh S, Khajuria A, Taneja SC, Khajuria RK, Singh J, Qazi GN. Boswellic acids and glucosamine show synergistic effect in preclinical anti-inflammatory study in rats. Bioorg Med Chem Lett 2007; 17: 3706-3711.
22. Khanna D, Sethi G, Ahn KS, et al. Natural products as a gold mine for arthritis treatment. Curr Opin Pharmacol 2007; 7: 344-351.
23. Gupta I, Parihar A, Malhotra P, et al. Effects of Boswellia serrata gum resin in patients with ulcerative colitis. Eur J Med Res 1997; 2: 37-43.
24. Gupta I, Parihar A, Malhotra P, et al. Effects of gum resin of Boswellia serrata in patients with chronic colitis. Planta Med 2001; 67: 391-395.
25. Gupta A, Gupta V, Parihar A, et al. Effects of Boswellia serrata gum resin in patients with bronchial asthma: Results of a double-blind, placebo-controlled, 6-week clinical study. Eur J Med Res 1998; 3: 511-514.
26. Safayhi H, Mack T, Ammon HP. Protection by boswellic acids against galactosamine/endotoxin-induced hepatitis in mice. Biochem Pharmacol 1991; 41: 1536-1537.
27. Glaser T, Winter S, Groscurth P, et al. Boswellic acids and malignant glioma: Induction of apoptosis but no modulation of drug sensitivity. Br J Cancer 1999; 80: 756-765.
28. Liu JJ, Nilsson A, Oredsson S, Badmaev V, Zhao WZ, Duan RD. Boswellic acids trigger apoptosis via a pathway dependent on caspase-8 activation but independent on Fas/Fas ligand interaction in colon cancer HT-29 cells. Carcinogenesis 2002; 7: 2087-2093.
29. Jing Y, Nakajo S, Xia L, et al. Boswellic acid acetate induces differentiation and apoptosis in leukemia cell lines. Leukemia Res 1999; 23: 43-50.
30. Hoernlein RF, Orlikowsky TH, Zehrer C, et al. Acetyl-11-keto-β-boswellic acid induces apoptosis in HL-60 and CCRF-CEM cells and inhibits topoisomerase I. JPET 1999; 288: 613-619.
31. Syrovets T, Buchele B, Gedig E, Slupsky JR, Simmet T. Acetyl-boswellic acids are novel catalytic inhibitors of human topoisomerases I and IIα. Mol Pharmacol 2000; 58: 71-81.
32. Shah BA, Kumar A, Gupta P, et al. Cytotoxic and apoptotic activities of novel amino analogues of boswellic acids. Bioorg Med Chem Lett 2007; 17: 6411-6416.
33. Fulda S, Friesen C, Los M, et al. Betulinic acid triggers CD95 (APO-1/Fas)- and p53-independent apoptosis via activation of caspases in neuroectodermal tumors. Cancer Res 1997; 57: 4956-4964.
34. Nigam M, Ranjan V, Srivastava S, Sharma R, Balapure AK. Centchroman induces G0/G1 arrest and caspase-dependent apoptosis involving mitochondrial membrane depolarization in MCF-7 and MDA MB-231 human breast cancer cells. Life Sci 2008; 82: 577-590.
35. English D, Andersen BR. Single-step separation of red blood cells, granulocytes and mononuclear leukocyte on discontinuous density gradient of Ficoll-Hypaque. J Immunol Method 1974; 5: 249-252.
36. Bhushan S, Singh J, Rao MJ, Saxena AK, Qazi GN. A novel lignan composition from Cedrus deodara induces apoptosis and early nitric oxide generation in human leukemia Molt-4 and HL-60 cells. Nitric Oxide 2006; 14: 72-88.
37. Kumar A, Malik F, Bhushan S, et al. An essential oil and its major constituent isointermedeol induce apoptosis by increased expression of mitochondrial cytochrome c and apical death receptors in human leukaemia HL-60 cells. Chem Biol Interact 2007; 171: 332-347.
38. Yu Z, Li W. Induction of apoptosis by puerarin in colon cancer HT-29 cells. Cancer Lett 2006; 238: 53-60.
39. Vermes I, Haanen C, Steffen-Nakken H, Reutellingsperger C. A novel assay for apoptosis, flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled AnnexinV. J Immunol Method 1995; 184: 39-51.
40. Malik F, Kumar A, Bhushan S, et al. Reactive oxygen species generation and mitochondrial dysfunction in the apoptotic cell death of human myeloid leukemia HL-60 cells by a dietary compound withaferin A with concomitant protection by N-acetyl cysteine. Apoptosis 2007; 12: 2115-2133.
41. Sakahira H, Enari M, Nagata S. Functional differences of two forms of the inhibitor of caspase-activated DNase, ICAD-L, and ICAD-S. J Biol Chem 1999; 274: 15740-15744.
42. Yingchang M, Thomas SD, Xiaohua X, Casson LK, Miller DM, Bates PJ. Apoptosis in leukemia cell is accompanied by alterations in the level and localization of nucleolin. J Biol Chem 2003; 278: 8572-8579.
43. Esposti MD. The roles of Bid. Apoptosis 2002; 7: 433-440.
44. Gallego MA, Ballot C, Kluza J, et al. Overcoming chemoresistance of non-small cell lung carcinoma through restoration of an AIF-dependent apoptotic pathway. Oncogene 2008; 27: 1981-1999.
45. Fulda S, Scaffidi C, Susin SA, et al. Activation of mitochondria and release of mitochondrial apoptogenic factors by betulinic acid. J Biol Chem 1998; 273: 33942-33948.
46. Kennedy SG, Kandel ES, Cross TK, Hay N. Akt/protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria. Mol Cell Biol 1999; 19: 5800-5810.
47. Antonsson B, Montessuit S, Sanchez B, Martinou JC. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J Biol Chem 2001; 276: 11615-11623.
48. Schneider C, Sepp-Lorenzino L, Nimmesgern E. Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc Natl Acad Sci USA 1996; 93: 14536-14541.
49. Wu GS, El-Deiry WS. Apoptotic death of tumor cells correlates with chemosensitivity, independent of p53 or bcl-2. Clin Cancer Res 1996; 2: 623-633.
50. Ferrarini M, Heltai S, Zocchi MR, Rugarli C. Unusual expression and localization of heat-shock proteins in human tumor cells. Int J Cancer 1992; 51: 613-619.
51. Kroemer G, Zamzami N, Susin SA. Mitochondrial control of apoptosis. Immunol Today 1997; 18: 44-51.
52. Susin SA, Zamzami N, Castedo M, et al. The central executioner of apoptosis: Multiple connections between protease activation and mitochondria in Fas/APO-1/CD95- and ceramide-induced apoptosis. J Exp Med 1997; 186: 25-37.