The short chain cell-permeable ceramide (C6) restores cell apoptosis and perifosine sensitivity in cultured glioblastoma cells

Molecular Biology Reports

Volumn 40, Issue 10, 2013, Pages 5645-5655

  Qin, Li Sen ^a,b   Yu, Zheng Quan ^a   Zhang, Shi Ming ^a   Sun, Guan ^b   Zhu, Jian ^b   Xu, Jin ^b   Guo, Jun ^b   Fu, Lin Shan ^b  

^a THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^b Yan cheng Pavilion Lake District People's Hospital   (China)

Author keywords

Autophagy and apoptosis; Ceramide (C6); Glioblastoma; Perifosine

Indexed keywords

3 METHYLADENINE; AUTOPHAGY PROTEIN 5; CERAMIDE; MAMMALIAN TARGET OF RAPAMYCIN; PACLITAXEL; PERIFOSINE; PROTEIN KINASE B;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER INHIBITION; CELL LEVEL; CELL VIABILITY; CLONOGENESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SENSITIVITY; ENZYME ACTIVATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; RNA INTERFERENCE;

APOPTOSIS; AUTOPHAGY; BRAIN NEOPLASMS; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CELL SURVIVAL; CERAMIDES; GLIOBLASTOMA; HEK293 CELLS; HUMANS; PHOSPHORYLCHOLINE; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUMOR CELLS, CULTURED;

EID: 84892704308     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-013-2666-4     Document Type: Article

References (51)

1. Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, Lang FF, McCutcheon IE, Hassenbusch SJ, Holland E, Hess K, Michael C, Miller D, Sawaya R (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95(2):190-198. doi:10.3171/jns.2001.95.2.0190
2. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987-996
3. Van Meir EG, Hadjipanayis CG, Norden AD, Shu HK, Wen PY, Olson JJ (2010) Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J Clin 60(3):166-193. doi:10.3322/caac.2006960/3/166
4. Narita Y, Nagane M, Mishima K, Huang HJ, Furnari FB, Cavenee WK (2002) Mutant epidermal growth factor receptor signaling downregulates p27 through activation of the phosphatidylinositol 3-kinase/Akt pathway in glioblastomas. Cancer Res 62(22):6764-6769
5. Riemenschneider MJ, Betensky RA, Pasedag SM, Louis DN (2006) AKT activation in human glioblastomas enhances proliferation via TSC2 and S6 kinase signaling. Cancer Res 66(11):5618-5623
6. Gulati N, Karsy M, Albert L, Murali R, Jhanwar-Uniyal M (2009) Involvement of mTORC1 and mTORC2 in regulation of glioblastoma multiforme growth and motility. Int J Oncol 35(4):731-740
7. Almhanna K, Strosberg J, Malafa M (2011) Targeting AKT protein kinase in gastric cancer. Anticancer Res 31(12):4387-4392
8. Wu P, Hu YZ (2010) PI3 K/Akt/mTOR pathway inhibitors in cancer: a perspective on clinical progress. Curr Med Chem 17(35):4326-4341
9. Yap TA, Garrett MD, Walton MI, Raynaud F, de Bono JS, Workman P (2008) Targeting the PI3K-AKT-mTOR pathway: progress, pitfalls, and promises. Curr Opin Pharmacol 8(4):393-412. doi:10. 1016/j.coph.2008.08.004
10. Pitter KL, Galban CJ, Galban S, Tehrani OS, Li F, Charles N, Bradbury MS, Becher OJ, Chenevert TL, Rehemtulla A, Ross BD, Holland EC, Hambardzumyan D (2011) Perifosine and CCI 779 co-operate to induce cell death and decrease proliferation in PTEN-intact and PTEN-deficient PDGF-driven murine glioblastoma. PLoS ONE 6(1):e14545. doi:10.1371/journal.pone.0014545
11. Momota H, Nerio E, Holland EC (2005) Perifosine inhibits multiple signaling pathways in glial progenitors and cooperates with temozolomide to arrest cell proliferation in gliomas in vivo. Cancer Res 65(16):7429-7435. doi:65/16/7429
12. Clarke J, Butowski N, Chang S (2010) Recent advances in therapy for glioblastoma. Arch Neurol 67(3):279-283. doi:10. 1001/archneurol.2010.567/3/279
13. Hilgard P, Klenner T, Stekar J, Nossner G, Kutscher B, Engel J (1997) D-21266, a new heterocyclic alkylphospholipid with antitumour activity. Eur J Cancer 33(3):442-446
14. Vink SR, Schellens JH, van Blitterswijk WJ, Verheij M (2005) Tumor and normal tissue pharmacokinetics of perifosine, an oral anti-cancer alkylphospholipid. Investig New Drugs 23(4):279-286
15. Kondapaka SB, Singh SS, Dasmahapatra GP, Sausville EA, Roy KK (2003) Perifosine, a novel alkylphospholipid, inhibits protein kinase B activation. Mol Cancer Ther 2(11):1093-1103
16. Ruiter GA, Verheij M, Zerp SF, van Blitterswijk WJ (2001) Alkyl-lysophospholipids as anticancer agents and enhancers of radiation-induced apoptosis. Int J Radiat Oncol Biol Phys 49(2):415-419
17. Chiarini F, Del Sole M, Mongiorgi S, Gaboardi GC, Cappellini A, Mantovani I, Follo MY, McCubrey JA, Martelli AM (2008) The novel Akt inhibitor, perifosine, induces caspase-dependent apoptosis and downregulates P-glycoprotein expression in multidrug-resistant human T-Acute leukemia cells by a JNK-dependent mechanism. Leukemia 22(6):1106-1116
18. Hideshima T, Catley L, Yasui H, Ishitsuka K, Raje N, Mitsiades C, Podar K, Munshi NC, Chauhan D, Richardson PG, Anderson KC (2006) Perifosine, an oral bioactive novel alkylphospholipid, inhibits Akt and induces in vitro and in vivo cytotoxicity in human multiple myeloma cells. Blood 107(10):4053-4062
19. Li X, Luwor R, Lu Y, Liang K, Fan Z (2006) Enhancement of antitumor activity of the anti-EGF receptor monoclonal antibody cetuximab/C225 by perifosine in PTEN-deficient cancer cells. Oncogene 25(4):525-535
20. Fu L, Lin YD, Elrod HA, Yue P, Oh Y, Li B, Tao H, Chen GZ, Shin DM, Khuri FR, Sun SY (2010) c-Jun NH2-terminal kinasedependent upregulation of DR5 mediates cooperative induction of apoptosis by perifosine and TRAIL. Mol Cancer 9:315
21. Patel V, Lahusen T, Sy T, Sausville EA, Gutkind JS, Senderowicz AM (2002) Perifosine, a novel alkylphospholipid, induces p21(WAF1) expression in squamous carcinoma cells through a p53-independent pathway, leading to loss in cyclin-dependent kinase activity and cell cycle arrest. Cancer Res 62(5):1401-1409
22. Rahmani M, Reese E, Dai Y, Bauer C, Payne SG, Dent P, Spiegel S, Grant S (2005) Coadministration of histone deacetylase inhibitors and perifosine synergistically induces apoptosis in human leukemia cells through Akt and ERK1/2 inactivation and the generation of ceramide and reactive oxygen species. Cancer Res 65(6):2422-2432
23. Aarts M, Liu Y, Liu L, Besshoh S, Arundine M, Gurd JW, Wang YT, Salter MW, Tymianski M (2002) Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science 298(5594):846-850. doi:10.1126/science. 1072873
24. Ji C, Yang YL, Yang Z, Tu Y, Cheng L, Chen B, Xia JP, Sun WL, Su ZL, He L, Bi ZG (2012) Perifosine sensitizes UVB-induced apoptosis in skin cells: new implication of skin cancer prevention Cell Signal 24(9):1781-1789. doi:S0898-6568(12)00140-4
25. Chen MB, Wu XY, Tao GQ, Liu CY, Chen J, Wang LQ, Lu PH (2012) Perifosine sensitizes curcumin induced anti-colorectal cancer effects by targeting multiple signaling pathways both in vivo and in vitro. Int J Cancer 131:2487-2498. doi:10.1002/ijc. 27548
26. Sun H, Yu T, Li J (2011) Co-Administration of perifosine with paclitaxel synergistically induces apoptosis in ovarian cancer cells: more than just AKT inhibition. Cancer Lett 310(1):118-128. doi:10.1016/j.canlet.2011.06.010S0304- 3835(11)00346-6
27. Wu CH, Cao C, Kim JH, Hsu CH, Wanebo HJ, Bowen WD, Xu J, Marshall J (2012) Trojan-horse nanotube on-command intracellular drug delivery. Nano Lett 12(11):5475-5480. doi:10.1021/nl301865c 28. Zhu QY, Wang Z, Ji C, Cheng L, Yang YL, Ren J, Jin YH, Wang QJ, Gu XJ, Bi ZG, Hu G, Yang Y (2011) C6-ceramide synergistically potentiates the anti-tumor effects of histone deacetylase inhibitors via AKT dephosphorylation and alpha-tubulin hyperacetylation both in vitro and in vivo. Cell Death Dis 2:e117
28. van Lummel M, van Blitterswijk WJ, Vink SR, Veldman RJ, van der Valk MA, Schipper D, Dicheva BM, Eggermont AM, ten Hagen TL, Verheij M, Koning GA (2011) Enriching lipid nanovesicles with short-chain glucosylceramide improves doxorubicin delivery and efficacy in solid tumors. Faseb J 25(1):280-289
29. Tong Y, Liu YY, You LS, Qian WB (2012) Perifosine induces protective autophagy and upregulation of ATG5 in human chronic myelogenous leukemia cells in vitro. Acta Pharmacol Sin 33(4):542-550. doi:10.1038/aps.2011.192
30. Sabatini DM (2006) mTOR and cancer: insights into a complex relationship. Nat Rev Cancer 6(9):729-734. doi:nrc1974
31. Guertin DA, Sabatini DM (2007) Defining the role of mTOR in cancer. Cancer Cell 12(1):9-22. doi:S1535-6108(07)00151-1
32. Sun SY (2010) Enhancing perifosine's anticancer efficacy by preventing autophagy. Autophagy 6(1):184-185. doi:10816
33. Fu L, Kim YA, Wang X, Wu X, Yue P, Lonial S, Khuri FR, Sun SY (2009) Perifosine inhibits mammalian target of rapamycin signaling through facilitating degradation of major components in the mTOR axis and induces autophagy. Cancer Res 69(23):8967-8976. doi:10.1158/0008-5472.CAN-09-2190
34. Liu YQ, Cheng X, Guo LX, Mao C, Chen YJ, Liu HX, Xiao QC, Jiang S, Yao ZJ, Zhou GB (2012) Identification of an annonaceous acetogenin mimetic, AA005, as an AMPK activator and autophagy inducer in colon cancer cells. PLoS ONE 7(10):e47049. doi:10.1371/journal.pone.0047049
35. Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13(2):132-141. doi:ncb2152
36. Din FV, Valanciute A, Houde VP, Zibrova D, Green KA, Sakamoto K, Alessi DR, Dunlop MG (2012) Aspirin inhibits mTOR signaling, activates AMP-Activated protein kinase, and induces autophagy in colorectal cancer cells. Gastroenterology 142 :1504-1515, e1503
37. Tanida I, Ueno T, Kominami E (2004) Human light chain 3/MAP1LC3B is cleaved at its carboxyl-terminal Met121 to expose Gly120 for lipidation and targeting to autophagosomal membranes. J Biol Chem 279(46):47704-47710. doi:10.1074/jbc. M407016200
38. Mizushima N, Sugita H, Yoshimori T, Ohsumi Y (1998) A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J Biol Chem 273(51):33889-33892
39. Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, Klionsky DJ, Ohsumi M, Ohsumi Y (1998) A protein conjugation system essential for autophagy. Nature 395(6700):395-398. doi:10.1038/26506
40. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y (2000) A ubiquitin-like system mediates protein lipidation. Nature 408(6811):488-492. doi:10.1038/35044114
41. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 117(Pt 13):2805-2812. doi:10.1242/jcs. 01131
42. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402(6762):672-676. doi:10. 1038/45257
43. Obeid LM, Hannun YA (1995) Ceramide: a stress signal and mediator of growth suppression and apoptosis. J Cell Biochem 58(2):191-198. doi:10.1002/jcb.240580208
44. Hannun YA, Obeid LM (1995) Ceramide: an intracellular signal for apoptosis. Trends Biochem Sci 20(2):73-77. doi:S0968-0004
45. Ji C, Yang B, Yang YL, He SH, Miao DS, He L, Bi ZG (2010) Exogenous cell-permeable C6 ceramide sensitizes multiple cancer cell lines to doxorubicin-induced apoptosis by promoting AMPK activation and mTORC1 inhibition. Oncogene 29(50): 6557-6568
46. Gills JJ, Zhang C, Abu-Asab MS, Castillo SS, Marceau C, Lo-Piccolo J, Kozikowski AP, Tsokos M, Goldkorn T, Dennis PA (2012) Ceramide mediates nanovesicle shedding and cell death in response to phosphatidylinositol ether lipid analogs and perifosine. Cell Death Dis 3:e340. doi:10.1038/cddis.2012.72
47. Yao C, Wei JJ, Wang ZY, Ding HM, Li D, Yan SC, Yang YJ, Gu ZP (2012) Perifosine induces cell apoptosis in human osteosarcoma cells: new implication for osteosarcoma therapy? Cell Biochem Biophys 65(2):217-227. doi:10.1007/s12013-012-9423-5
48. Rami A (2009) Review: autophagy in neurodegeneration: firefighter and/or incendiarist? Neuropathol Appl Neurobiol 35(5):449-461. doi:NAN1034
49. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8(9):741-752. doi:nrm2239
50. Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Investig 115(10):2679-2688. doi:10.1172/JCI26390
51. Gozuacik D, Kimchi A (2004) Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23(16):2891-2906. doi:10.1038/sj.onc.1207521