Parthenolide induces caspase-independent and AIF-mediated cell death in human osteosarcoma and melanoma cells

Journal of Cellular Physiology

Volumn 228, Issue 5, 2013, Pages 952-967

  D'Anneo, Antonella ^a   Carlisi, Daniela ^a   Lauricella, Marianna ^a   Emanuele, Sonia ^a   Di Fiore, Riccardo ^a   Vento, Renza ^a   Tesoriere, Giovanni ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOPTOSIS INDUCING FACTOR; CALCIUM ION; CASPASE; CYCLOSPORIN A; GLUTATHIONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N ACETYLCYSTEINYLASPARAGINYLPROLYLARGINYLGLYCYLASPARTYL(O METHYLTYROSYL)ARGINYLCYSTEINAMIDE CYCLIC 1,9 DISULFIDE; PARTHENOLIDE; PROPIDIUM IODIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STRESS ACTIVATED PROTEIN KINASE 1; THIOL GROUP;

ARTICLE; CELL DEATH; CELL VIABILITY; CHROMATIN CONDENSATION; CYTOTOXICITY; DNA FRAGMENTATION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; MELANOMA; MITOCHONDRIAL MEMBRANE POTENTIAL; OSTEOSARCOMA; PRIORITY JOURNAL;

AMINO ACID CHLOROMETHYL KETONES; APOPTOSIS INDUCING FACTOR; CASPASE INHIBITORS; CASPASES; CELL DEATH; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE SIGNALING SYSTEM; MELANOMA; NADPH OXIDASE; NF-KAPPA B; OSTEOSARCOMA; REACTIVE OXYGEN SPECIES; SESQUITERPENES;

EID: 84873877188     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24131     Document Type: Article

References (65)

1. Allan LA, Morrice N, Brady S, Magee G, Pathak S, Clarke PR. 2003. Inhibition of caspase-9 through phosphorylation at Thr125 by ERK MAPK. Nat Cell Biol 5:647-654.
2. Arnoult D, Parone P, Martinou JC, Antonsson B, Estaquier J, Ameisen JC. 2002. Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J Cell Biol 159:923-929.
3. Artus C, Boujrad H, Bouharrour A, Brunelle MN, Hoos S, Yuste VJ, Lenormand P, Rousselle JC, Namane A, England P, Lorenzo HK, Susin SA. 2010. AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX. EMBO J 29:1585-1599.
4. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD. 2005. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434:658-662.
5. Baritaud M, Boujrad H, Lorenzo HK, Krantic S, Susin SA. 2010. The missing link in AIF-mediated caspase independent programmed necrosis. Cell Cycle 9:3166-3173.
6. Batandier C, Guigas B, Detaille D, El-Mir MY, Fontaine E, Rigoulet M, Leverve XM. 2006. The ROS production induced by a reverse-electron flux at respiratory-chain complex 1 is hampered by metformin. J Bioenerg Biomembr 38:33-42.
7. Bours V, Bentires-Alj M, Hellin AC, Viatour P, Robe P, Delhalle S, Benoit V, Merville MP. 2000. Nuclear factor-kB, cancer and apoptosis. Biochem Pharmacol 60:1085-1089.
8. Cao C, Healey S, Amaral A, Lee-Couture A, Wan S, Kouttab N, Chu W, Wan Y. 2007. ATP-sensitive potassium channel: A novel target for protection against UV-induced human skin cell damage. J Cell Physiol 212:252-263.
9. Carlisi D, Vassallo B, Lauricella M, Emanuele S, D'Anneo A, Di Leonardo E, Di Fazio P, Vento R, Tesoriere G. 2008. Histone deacetylase inhibitors induce in human hepatoma HepG2 cells acetylation of p53 and histones in correlation with apoptotic effects. Int J Oncol 32:177-184.
10. Carlisi D, D'Anneo A, Angileri L, Lauricella M, Emanuele S, Santulli A, Vento R, Tesoriere G. 2011. Parthenolide sensitizes hepatocellular carcinoma cells to TRAIL by inducing the expression of death receptors through inhibition of STAT3 activation. J Cell Physiol 226:1632-1641.
11. Chernyak BV, Bernardi P. 1996. The mitochondrial permeability transition pore is modulated by oxidative agents through both pyridine nucleotides and glutathione at two separate sites. Eur J Biochem 238:623-630.
12. Costantini P, Chernyak BV, Petronilli V, Bernardi P. 1996. Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J Biol Chem 271:6746-6751.
13. Crompton M. 1999. The mitochondrial permeability transition pore and its role in cell death. Biochem J 341:233-249.
14. Czyz M, Lesiak-Mieczkowska K, Koprowska K, Szulawska-Mroczek A, Wozniak M. 2010. Cell context-dependent activities of parthenolide in primary and metastatic melanoma cells. Br J Pharmacol 160:1144-1157.
15. Dawson VL, Dawson TM. 2004. Deadly conversation: Nuclear-mitochondrial cross-talk. J Bioenerg Biomembr 36:287-294.
16. phox phosphorylation in human neutrophils. J Immunol 165:5238-5244.
17. Garcia-Rivas G De J, Carvajal K, Correa F, Zazueta C. 2006. RU360, a specific mitochondrial calcium uptake inhibitor, improves cardiac post-ischemic functional recovery in rats in vivo. Br J Parmacol 149:829-837.
18. Giuliano M, Lauricella M, Calvaruso G, Carabillò M, Emanuele S, Vento R, Tesoriere G. 1999. The apoptotic effects and synergistic interaction of sodium butyrate and MG132 in human retinoblastoma Y79 cells. Cancer Res 59:5586-5595.
19. Golstein P, Kroemer G. 2007. Cell death by necrosis: Towards a molecular definition. Trends Biochem Sci 32:37-43.
20. Guzman ML, Rossi RM, Neelakantan S, Li X, Corbett CA, Hassane DC, Becker MW, Bennett JM, Sullivan E, Lachowicz JL, Vaughan A, Sweeney CJ, Matthews W, Carroll M, Liesveld JL, Crooks PA, Jordan CT. 2007. An orally bioavailable parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood 110:4427-4435.
21. Halestrap AP, Kerr PM, Javadov S, Woodfield KY. 1998. Elucidating the molecular mechanism of the permeability transition pore and its role in reperfusion injury of the heart. Biochim Biophys Acta 1366:79-94.
22. Hampton MB, Orrenius S. 1998. Redox regulation of apoptotic cell death. Biofactors 8:1-5.
23. Hong SJ, Dawson TM, Dawson VL. 2004. Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling. Trends Pharmacol Sci 25:259-264.
24. Javadov S, Karmazyn M, Escobales N. 2009. Mitochondrial permeability transition pore opening as a promising therapeutic target in cardiac diseases. J Pharmacol Exp Ther 330:670-678.
25. Jin Z, El-Deiry WS. 2005. Overview of cell death signaling pathways. Cancer Biol Ther 4:139-163.
26. Keinan N, Tyomkin D, Shoshan-Barmatz V. 2010. Oligomerization of the mitochondrial protein voltage-dependent anion channel is coupled to the induction of apoptosis. Mol Cell Biol 30:5698-5709.
27. Kelly KJ, Sandoval RM, Dunn KW, Molitoris BA, Dagher P. 2003. A novel method to determine specificity and sensitivity of the TUNEL reaction in the quantitation of apoptosis. Am J Physiol Cell Physiol 284:1309-1318.
28. Kim JH, Liu L, Lee SO, Kim YT, You KR, Kim DG. 2005. Susceptibility of cholangiocarcinoma cells to parthenolide-induced apoptosis. Cancer Res 65:6312-6320.
29. Kurdi M, Booz GW. 2007. Evidence that IL-6-type cytokine signalling in cardiomyocytes is inhibited by oxidative stress: Parthenolide targets JAK1 activation by generating ROS. J Cell Physiol 212:424-431.
30. Kurdi M, Bowers MC, Dado J, Booz GW. 2007. Parthenolide induces a distinct pattern of oxidative stress in cardiac myocytes. Free Radic Biol Med 42:474-481.
31. Kwok BH, Koh B, Ndubuisi MI, Elofsson M, Crews CM. 2001. The anti-inflammatory natural product parthenolide from the medicinal herb Feverfew directly binds to and inhibits IκB kinase. Chem Biol 8:759-766.
32. - channels in adherent Ehrlich Lettré and NIH3T3 cells. Am J Physiol Cell Physiol 297:C198-C206.
33. Liu JW, Cai MX, Xin Y, Wu QS, Ma J, Yang P, Xie HY, Huang DS. 2010. Parthenolide induces proliferation inhibition and apoptosis of pancreatic cancer cells in vitro. Exp Clin Cancer Res 10:108-115.
34. McStay GP, Clarke SJ, Halestrap AP. 2002. Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore. Biochem J 367:541-548.
35. Moon EJ, Sonveaux P, Porporato PE, Danhier P, Gallez B, Batinic-Haberle I, Nien YC, Schroeder T, Dewhirst MW. 2010. NADPH oxidase-mediated reactive oxygen species production activates hypoxia-inducible factor-1 (HIF-1) via the ERK pathway after hyperthermia treatment. Proc Natl Acad Sci 107:20477-20482.
36. Nakshatri H, Rice SE, 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. 2+ is required for the activation of mitochondrial calpain to release AIF during cell death. Cell Death Differ 15:1857-1864.
38. Olivier S, Robe P, Bours V. 2006. Can NF-kB be a target for novel and efficient anti-cancer agents? Biochem Pharmacol 72:1054-1068.
39. Otera H, Ohsakaya S, Nagaura Z, Ishihara N, Mihara K. 2005. Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO J 24:1375-1386.
40. Pardo J, Pérez-Galán P, Gamen S, Marzo I, Monleón I, Kaspar AA, Susín SA, Kroemer G, Krensky AM, Naval J, Anel A. 2001. A role of the mitochondrial apoptosis-inducing factor in granulysin-induced apoptosis. J Immunol 167:1222-1229.
41. Pareek A, Suthar M, Rathore GS, Bansal V. 2011. Feverfew (Tanacetum parthenium L.): A systematic review. Pharmacogn Rev 5:103-110.
42. Petronilli V, Costantini P, Scorrano L, Colonna R, Passamonti S, Bernardi P. 1994. The voltage sensor of the mitochondrial permeability transition pore is tuned by the oxidation-reduction state of vicinal thiols. Increase of the gating potential by oxidants and its reversal by reducing agents. J Biol Chem 269:16638-16642.
43. Polster BM, Basañez G, Etxebarria A, Hardwick JM, Nicholls DG. 2005. Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J Biol Chem 280:6447-6454.
44. Ravi R, Bedi A. 2004. NF-kappaB in cancer-A friend turned foe. Drug Resist Updat 7:53-67.
45. Reubold TF, Eschenburg S. 2012. A molecular view on signal transduction by the apoptosome. Cell Signal 24:1420-1425.
46. Samali A, Nordgren H, Zhivotovsky B, Peterson E, Orrenius S. 1999. A comparative study of apoptosis and necrosis in HepG2 cells: Oxidant-induced caspase inactivation leads to necrosis. Biochem Biophys Res Commun 255:6-11.
47. Satoh T, Nakatsuka D, Watanabe Y, Nagata I, Kikuchi H, Namura S. 2000. Neuroprotection by MAPK/ERK kinase inhibition with U0126 against oxidative stress in a mouse neuronal cell line and rat primary cultured cortical neurons. Neurosci Lett 288:163-166.
48. Scharstuhl A, Mutsaers HA, Pennings SW, Russel FG, Wagener FA. 2009. Involvement of VDAC, Bax and Ceramides in the efflux of AIF from mitochondria during curcumin-induced apoptosis. Plos One 4:e6688.
49. Sevrioukova IF. 2011. Apoptosis-inducing factor: Structure, function, and redox regulation. Antioxid Redox Signal 14:2545-2579.
50. Shanmugam R, Kusumanchi P, Cheng L, Crooks P, Neelakantan S, Matthews W, Nakshatri H, Sweeney CJ. 2010. A water-soluble parthenolide analogue suppresses in vivo prostate cancer growth by targeting NF-kB and generating reactive oxygen species. Prostate 70:1074-1086.
51. Shanmugam R, Kusumanchi P, Appaiah H, Cheng L, Crooks P, Neelakantan S, Peat T, Klaunig J, Matthews W, Nakshatri H, Sweeney CJ. 2011. A water soluble parthenolide analog suppresses in vivo tumor growth of two tobacco-associated cancers, lung and bladder cancer, by targeting NF-kB and generating reactive oxygen species. Int J Cancer 128:2481-2494.
52. Shen HM, Liu ZG. 2006. JNK signaling pathway is a key modulator in cell death mediated by reactive oxygen and nitrogen species. Free Radical Biol Med 40:928-939.
53. Shoshan-Barmatz V, Keinan N, Abu-Hamad S, Tyomkin D, Aram L. 2010. Apoptosis is regulated by the VDAC1 N-terminal region and by VDAC oligomerization: Release of cytochrome c, AIF and Smac/Diablo. Biochim Biophys Acta 1797:1291-1291.
54. Song H, Cha MJ, Song BW, Kim IK, Chang W, Lim S, Choi EJ, Ham O, Lee SY, Chung N, Jang Y, Hwang KC. 2010. Reactive oxygen species inhibit adhesion of mesenchymal stem cells implanted into ischemic myocardium via interference of focal adhesion complex. Stem Cells 28:555-563.
55. Steele AJ, Jones DT, Ganeshaguru K, Duke VM, Yogashangary BC, North JM, Lowdell MW, Kottaridis PD, Mehta AB, Prentice AG, Hoffbrand AV, Wickremasinghe RG. 2006. The sesquiterpene lactone parthenolide induces selective apoptosis of B-chronic lymphocytic leukemia cells in vitro. Leukemia 20:1073-1079.
56. Sumner H, Salan U, Knight DW, Hoult JR. 1992. Inhibition of 5-lipoxygenase and cyclo-oxygenase in leukocytes by feverfew. Involvement of sesquiterpene lactones and other components. Biochem Pharmacol 43:2313-2320.
57. Sun Y, St Clair DK, Xu Y, Crooks PA, St Clair WH. 2010. A NADPH oxidase-dependent redox signaling pathway mediates the selective radiosensitization effect of parthenolide in prostate cancer cells. Cancer Res 70:2880-2890.
58. Susin SA, Daugas E, Ravagnan L, Samejima K, Zamzami N, Loeffler M, Costantini P, Ferri KF, Irinopoulou T, Prévost MC, Brothers G, Mak TW, Penninger J, Earnshaw WC, Kroemer G. 2000. Two distinct pathways leading to nuclear apoptosis. J Exp Med 192:571-580.
59. Tait SW, Green DR. 2008. Caspase-independent cell death: Leaving the set without the final cut. Oncogene 27:6452-6461.
60. Wang H, Joseph JA. 1999. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 27:612-616.
61. Wang W, Adachi M, Kawamura R, Sakamoto H, Hayashi T, Ishida T, Imai K, Shinomura Y. 2006. Parthenolide-induced apoptosis in multiple myeloma cells involves reactive oxygen species generation and cell sensitivity depends on catalase activity. Apoptosis 11:2225-2235.
62. Wen J, You KR, Lee SY, Song CH, Kim DG. 2002. Oxidative stress-mediated apoptosis. The anticancer effect of the sesquiterpene lactone parthenolide. J Biol Chem 277:38954-38964.
63. Wu F, Tyml K, Wilson JX. 2008. iNOS expression requires NADPH oxidase-dependent redox signaling in microvascular endothelial cells. J Cell Physiol 117:207-214.
64. Zhang S, Ong CN, Shen HM. 2004. Critical roles of intracellular thiols and calcium in parthenolide-induced apoptosis in human colorectal cancer cells. Cancer Lett 208:143-153.
65. Zunino SJ, Ducore JM, Storms DH. 2007. Parthenolide induces significant apoptosis and production of reactive oxygen species in high-risk pre-B leukemia cells. Cancer Lett 254:119-127.