Induction of autophagic cell death and radiosensitization by the pharmacological inhibition of nuclear factor-kappa B activation in human glioma cell lines: Laboratory investigation

Journal of Neurosurgery

Volumn 110, Issue 3, 2009, Pages 594-604

  Tsuboi, Yoshifumi ^a   Kurimoto, Masanori ^a   Nagai, Shoichi ^a   Hayakawa, Yumiko ^a   Kamiyama, Hironaga ^a   Hayashi, Nakamasa ^a   Kitajima, Isao ^a   Endo, Shunro ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

Author keywords

Autophagic cell death; Nuclear factor kappa B; Pitavastatin

Indexed keywords

3 METHYLADENINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PITAVASTATIN; 3-METHYLADENINE; ADENINE; DRUG DERIVATIVE; ENZYME INHIBITOR; QUINOLINE DERIVATIVE;

APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DAMAGE; CELL GROWTH; CELL NUCLEUS; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; ELECTRON MICROSCOPY; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IRRADIATION; NITROBLUE TETRAZOLIUM TEST; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RADIOSENSITIVITY; RADIOSENSITIZATION; STAINING; DRUG EFFECT; GLIOMA; PATHOLOGY; PHYSIOLOGY; RADIATION DOSE; TUMOR CELL LINE;

ADENINE; APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; ENZYME INHIBITORS; GLIOMA; HUMANS; IMMUNOBLOTTING; NF-KAPPA B; QUINOLINES; RADIATION TOLERANCE;

EID: 63849257538     PISSN: 00223085     EISSN: 19330693     Source Type: Journal    
DOI: 10.3171/2008.8.JNS17648     Document Type: Article

References (51)

1. Ahn KS, Sethi G, Aggarwal BB: Simvastatin potentiates TNFα- induced apoptosis through the down-regulation of NF-κB-dependent antiapoptotic gene products: role of IκBα kinase and TGFβ-activated kinase-1. J Immunol 178:2507-2516, 2007 (Pubitemid 46233452)
2. Avellino R, Romano S, Parasole R, Bisogni R, Lamberti A, Poggi V, et al: Rapamycin stimulates apoptosis of childhood acute lymphoblastic leukemia cells. Blood 106:1400-1406, 2005 (Pubitemid 41129607)
3. Baeuerle PA, Baichwal VR: NF-kappa B as a frequent target for immunosuppressive and anti-inflammatory molecules. Adv Immunol 65:111-137, 1997
4. Bellosta S, Ferri N, Bernini F, Paoletti R, Corsini A: Non-lipid- related effects of statins. Ann Med 32:164-176, 2000
5. Brach MA, Hass R, Sherman ML, Gunji H, Weichselbaum R, Kufe D: Ionizing radiation induces expression and binding activity of the nuclear factor κB. J Clin Invest 88:691-695, 1991
6. Bradbury CM, Markovina S, Wei SJ, Rene LM, Zoberi I, Horikoshi N, et al: Indomethacin-induced radiosensitization and inhibition of ionizing radiation-induced NF-kappaB activation in HeLa cells occur via a mechanism involving p38 MAP kinase. Cancer Res 61:7689-7696, 2001 (Pubitemid 32995067)
7. Campbell MJ, Esserman LJ, Zhou Y, Shoemaker M, Lobo M, Borman E, et al: Breast cancer growth prevention by statins. Cancer Res 66:8707-8714, 2006 (Pubitemid 44449187)
8. Campbell SL, Khosravi-Far R, Rossman KL, Clark GJ, Der CJ: Increasing complexity of Ras signaling. Reviews. Oncogene 17:1395-1413, 1998
9. Chendil D, Ranga RS, Meigooni D, Sathishkumar S, Ahmed MM: Curcumin confers radiosensitizing effect in prostate cancer cell line PC-3. Oncogene 23:1599-1607, 2004 (Pubitemid 38406523)
10. Conti A, Aguennouz M, Torre DL, Cardali S, Angileri FF, Buemi C, et al: Expression of the tumor necrosis factor receptor- associated factors 1 and 2 and regulation of the nuclear factor-κB antiapoptotic activity in human gliomas. J Neurosurg 103:873-881, 2005 (Pubitemid 43194582)
11. Daido S, Yamamoto A, Fujiwara K, Sawayaa R, Kondo S, Kondo Y: Inhibition of the DNA-dependent protein kinase catalytic subunit radiosensitizes malignant glioma cells by inducing autophagy. Cancer Res 65:4368-4375, 2005 (Pubitemid 40775676)
12. Denoyelle C, Vasse M, Korner M, Mishal Z, Ganne F, Vannier JP, et al: Cerivastatin, an inhibitor of HMG-CoA reductase, inhibits the signaling pathways involved in the invasiveness and metastatic properties of highly invasive breast cancer cell lines: an in vitro study. Carcinogenesis 22:1139-1148, 2001 (Pubitemid 32737327)
13. Djavaheri-Mergny M, Amelotti M, Mathieu J, Besancon F, Bauvy C, Souquere S, et al: NF-κB activation represses tumor necrosis factor-α-induced autophagy. J Biol Chem 281:30373-30382, 2006 (Pubitemid 44582093)
14. Djavaheri-Mergny M, Javelaud D, Wietzerbin J, Besancon F: NF-κB activation prevents apoptotic oxidative stress via an increase of both thioredoxin and MnSOD levels in TNFα- treated Ewing sarcoma cells. FEBS Lett 578:111-115, 2004 (Pubitemid 39576110)
15. Dritschilo A: Radiosensitivity and transcription factor NF-κB inhibition. Progress and pitfalls. J Natl Cancer Inst 91:1910-1911, 1999
16. Fabre C, Carvalho G, Tasdemir E, Braun T, Ades L, Grosjean J, et al: NF-kappa B inhibition sensitizes to starvation-induced cell death in high-risk myelodysplastic syndrome and acute myeloid leukemia. Oncogene 26:4071-4083, 2007 (Pubitemid 46920171)
17. Fritz G, Brachetti C, Kaina B: Lovastatin causes sensitization of HeLa cells to ionizing radiation-induced apoptosis by the abrogation of G2 blockage. Int J Radiat Biol 79:601-610, 2003 (Pubitemid 37297218)
18. Gray-Bablin J, Rao S, Keyomarsi K: Lovastatin induction of cyclin-dependent kinase inhibitors in human breast cells occurs in a cell cycle-independent fashion. Cancer Res 57:604-609, 1997 (Pubitemid 27085640)
19. Held KD: Radiation-induced apoptosis and its relationship to loss of clonogenic survival. Apoptosis 2:265-282, 1997
20. 1-to-S-phase transition. Mol Cell Biol 19:2690-2698, 1999
21. Hosoi H, Dilling MB, Shikata T, Liu LN, Shu L, Ashmun RA, et al: Rapamycin causes poorly reversible inhibition of mTOR and induces p53-independent apoptosis in human rhabdomyosarcoma cells. Cancer Res 59:886-894, 1999 (Pubitemid 29086744)
22. Ito H, Daido S, Kanzawa T, Kondo S, Kondo Y: Radiation-induced autophagy is associated with LC3 and its inhibition sensitizes malignant glioma cells. Int J Oncol 26:1401-1410, 2005
23. Iwamaru A, Kondo Y, Iwado E, Aoki H, Fujiwara K, Yokoyama T, et al: Silencing mammalian target of rapamycin signaling by small interfering RNA enhances rapamycin-induced autophagy in malignant glioma cells. Oncogene 26:1840-1851, 2007 (Pubitemid 46474638)
24. Kajinami K, Takekoshi N, Saito Y: Pitavastatin: Efficacy and safety profiles of a novel synthetic HMGCoA reductase inhibitor. Cardiovasc Drug Rev 21:199-215, 2003 (Pubitemid 37243525)
25. Kamata H, Honda S, Maeda S, Chang L, Hirata H, Karin M: Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120:649-661, 2005 (Pubitemid 40343077)
26. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S: Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ 11:448-457, 2004 (Pubitemid 38489422)
27. Kieran M, Blank V, Logeat F, Vandekerckhove J, Lottspeich F, Bail OL, et al: The DNA binding subunit of NF-κB is identical to factor KBF1 and homologous to the rel oncogene product. Cell 62:1007-1018, 1990 (Pubitemid 20269147)
28. Klionsky DJ, Emr SD: Autophagy as a regulated pathway of cellular degradation. Science 290:1717-1721, 2000
29. Kondo Y, Kanzawa T, Sawaya R, Kondo S: The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 5:726-734, 2005 (Pubitemid 41486365)
30. Lang FF, Yung WK, Raju U, Libunao F, Terry NH, Tofilon PJ: Enhancement of radiosensitivity of wild-type p53 human glioma cells by adenovirus-mediated delivery of the p53 gene. J Neurosurg 89:125-132, 1998 (Pubitemid 28285933)
31. Moretti L, Attia A, Kim KW, Lu B: Crosstalk between Bak/ Bax and mTOR signaling regulates radiationinduced autophagy. Autophagy 3:142-144, 2007 (Pubitemid 46449106)
32. Nagai S, Kurimoto M, Washiyama K, Hirashima Y, Kumanishi T, Endo S: Inhibition of cellular proliferation and induction of apoptosis by curcumin in human malignant astrocytoma cell lines. J Neurooncol 74:105-111, 2005 (Pubitemid 41478905)
33. Nagai S, Washiyama K, Kurimoto M, Takaku A, Endo S, Kumanishi T: Aberrant nuclear factor- kB activity and its participation in the growth of human malignant astrocytoma. J Neurosurg 96:909-917, 2002 (Pubitemid 34415406)
34. Noda T, Ohsumi Y: Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273:3963-3966, 1998 (Pubitemid 28103257)
35. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, et al: A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res 61:439-444, 2001 (Pubitemid 32128593)
36. Pahl HL: Activators and target genes of Rel/NF-κB transcription factors. Oncogene 18:6853-6866, 1999
37. Pich A, Ponti R, Valente G, Chiusa L, Geuna M, Novero D, et al: Mib-1, Ki67, and PCNA scores and DNA flow cytometry in intermediate grade malignant lymphomas. J Clin Pathol 47:18-22, 1994 (Pubitemid 24057742)
38. Price P, McMillan TJ: Use of the tetrazolium assay in measuring the response of human tumor cells to ionizing radiation. Cancer Res 50:1392-1396, 1990 (Pubitemid 20090446)
39. Rao S, Lowe M, Herliczek TW, Keyomarsi K: Lovastatin mediated G1 arrest in normal and tumor breast cells is through inhibition of CDK2 activity and redistribution of p21 and p27, independent of p53. Oncogene 17:2393-2402, 1998 (Pubitemid 28515393)
40. Rao S, Porter DC, Chen X, Herliczek T, Lowe M, Keyomarsi K: Lovastatin-mediated G1 arrest is through inhibition of the proteasome, independent of hydroxymethyl glutaryl-CoA reductase. Proc Natl Acad Sci U S A 96:7797-7802, 1999 (Pubitemid 29328361)
41. Russo SM, Tepper JE, Baldwin AS, Liu R, Adams J, Elliott P, et al: Enhancement of radiosensitivity by proteasome inhibition: implications for a role of NF-κB. Int J Radiat Oncol Biol Phys 50:183-193, 2001
42. Schwartz SA, Hernandez A, Evers M: The role of NF-κB/IκB proteins in cancer: implications for novel treatment strategies. Surg Oncol 8:143-153, 1999
43. Story MD, Voehringer DW, Malone CG, Hobbs ML, Meyn RE: Radiation-induced apoptosis in sensitive and resistant cells isolated from a mouse lymphoma. Int J Radiat Biol 66:659-668, 1994
44. Takeuchi H, Kondo Y, Fujiwara K, Kanzawa T, Aoki H, Mills GB, et al: Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Res 65:3336-3346, 2005 (Pubitemid 40524618)
45. Tsujimoto A, Takemura G, Mikami A, Aoyama T, Ohno T, Maruyama R, et al: A therapeutic dose of the lipophilic statin pitavastatin enhances oxidant-induced apoptosis in human vascular smooth muscle cells. J Cardiovasc Pharmacol 48:160-165, 2006
46. Wang J, Kitajima I: Pitavastatin inactivates NF-κB and decreased IL-6 production through Rho kinase pathway in MCF-7 cells. Oncol Rep 17:1149-1154, 2007
47. Wang J, Xu Zhenye, Kitajima I, Wang Z: Effects of different statins on endothelial nitric oxide synthase and AKT phosphorylation in endothelial cells. Int J Cardiol 15: [epub ahead of print], 2008
48. Xiao G: Autophagy and NF-kB: Fight for fate. Cytokine Growth Factor Rev 18:233-243, 2007
49. Yamamoto Y, Gaynor RB: Therapeutic potential of inhibition of the NF-κB pathway in the treatment of inflammation and cancer. J Clin Invest 107:135-142, 2001 (Pubitemid 32096826)
50. Yao KC, Komata T, Kondo Y, Kanzawa T, Kondo S, Germano IM: Molecular response of human glioblastoma multiforme cells to ionizing radiation: cell cycle arrest, modulation of the expression of cyclin-dependent kinase inhibitors, and autophagy. J Neurosurg 98:378-384, 2003 (Pubitemid 36151035)
51. Yount GL, Hass-Kogan DA, Vidair CA, Haas M, Dewey WC, Israel MA: Cell cycle synchrony unmasks the influence of p53 function on radiosensitivity of human glioblastoma cells. Cancer Res 56:500-506, 1996 (Pubitemid 26043646)