Erufosine simultaneously induces apoptosis and autophagy by modulating the Akt-mTOR signaling pathway in oral squamous cell carcinoma

Cancer Letters

Volumn 319, Issue 1, 2012, Pages 39-48

  Kapoor, Vaishali ^a,b   Zaharieva, Maya M ^a   Das, Satya N ^b   Berger, Martin R ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

Alkylphosphocholine; Autophagy; Erufosine; MTOR signaling cascade; Oral squamous cell cancer

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 3; CASPASE 7; CISPLATIN; CYCLIN D1; ERUFOSINE; FLUOROURACIL; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN KINASE B; S6 KINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGY; CARCINOMA CELL; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; ORAL SQUAMOUS CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; SQUAMOUS CELL CARCINOMA;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; MOUTH NEOPLASMS; PHOSPHORIC ACID ESTERS; PROTO-ONCOGENE PROTEINS C-AKT; QUATERNARY AMMONIUM COMPOUNDS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

RAPTORES;

EID: 84858074187     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.12.032     Document Type: Article

References (44)

1. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA Cancer J. Clin. 2011, 61:69-90.
2. Saranath D. Epidemiology and Prevention of Head and Neck Cancer: a Global View. Contemporary Issues in Oral Cancer 2000, Oxford University Press.
3. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Murray T., et al. Cancer statistics. CA Cancer J. Clin. 2008, 58:71-96.
4. Kapoor V., Singh A.K., Dey S., Sharma S.C., Das S.N. Circulating cycloxygenase-2 in patients with tobacco-related intraoral squamous cell carcinoma and evaluation of its peptide inhibitors as potential antitumor agent. J. Cancer Res. Clin. Oncol. 2010, 136:1795-1804.
5. Molinolo A.A., Amornphimoltham P., Squarize C.H., Castilho R.M., Patel V., Gutkind J.S. Dysregulated molecular networks in head and neck carcinogenesis. Oral Oncol. 2009, 45:324-334.
6. Amornphimoltham P., Patel V., Sodhi A., Nikitakis N.G., Sauk J.J., Sausville E.A., et al. Mammalian target of rapamycin, a molecular target in squamous cell carcinomas of the head and neck. Cancer Res. 2005, 65:9953-9961.
7. Graff J.R., Konicek B.W., Carter J.H., Marcusson E.G. Targeting the eukaryotic translation initiation factor 4E for cancer therapy. Cancer Res. 2008, 68:631-634.
8. Mamane Y., Petroulakis E., LeBacquer O., Sonenberg N. mTOR, translation initiation and cancer. Oncogene 2006, 25:6416-6422.
9. Guertin D.A., Sabatini D.M. Defining the role of mTOR in cancer. Cancer Cell 2007, 12:9-22.
10. Eibl H., Engel J. Synthesis of hexadecylphosphocholine (miltefosine). Prog. Exp. Tumor Res. 1992, 34:1-5.
11. Zaharieva M.M., Konstantinov S.M., Pilicheva B., Karaivanova M., Berger M.R. Erufosine: a membrane targeting antineoplastic agent with signal transduction modulating effects. Ann. N. Y. Acad. Sci. 2007, 1095:182-192.
12. Berger M.R., Tsoneva I., Konstantinov S.M., Eibl H. Induction of apoptosis by erucylphospho-N, N, N-trimethylammonium is associated with changes in signal molecule expression and location. Ann. N. Y. Acad. Sci. 2003, 1010:307-310.
13. Fiegl M., Lindner L.H., Juergens M., Eibl H., Hiddemann W., Braess J. Erufosine, a novel alkylphosphocholine, in acute myeloid leukemia: single activity and combination with other antileukemic drugs. Cancer Chemother. Pharmacol. 2008, 62:321-329.
14. Konstantinov S.M., Topashka-Ancheva M., Benner A., Berger M.R. Alkylphosphocholines: effects on human leukemic cell lines and normal bone marrow cells. Int. J. Cancer 1998, 77:778-786.
15. Stekar J., Hilgard P., Klenner T. Opposite effect of miltefosine on the antineoplastic activity and haematological toxicity of cyclophosphamide. Eur. J. Cancer 1995, 31A:372-374.
16. Lucas L., Hernández-Alcoceba R., Penalva V., Lacal J.C. Modulation of phospholipase D by hexadecylphosphorylcholine: a putative novel mechanism for its antitumoral activity. Oncogene 2001, 20:1110-1117.
17. Arndt D., Zeisig R., Eue I., Sternberg B., Fichtner I. Antineoplastic activity of sterically stabilized alkylphosphocholine liposomes in human breast carcinomas. Breast Cancer Res. Treat. 1997, 43:237-246.
18. Grosman N., phospholipids Similar effects of ether PAF and lyso-PAF on the Ca(2+)-ATPase activity of rat brain synaptosomes and leukocyte membranes. Int. Immunopharmacol. 2001, 1:1321-1329.
19. Matzke A., Massing U., Krug H.F. Killing tumour cells by alkylphosphocholines: evidence for involvement of CD95. Eur. J. Cell Biol. 2001, 80:1-10.
20. Oberle C., Massing U., Krug H.F. On the mechanism of alkylphosphocholine (APC)-induced apoptosis in tumour cells. Biol. Chem. 2005, 386:237-245.
21. Ward P.D., Ouyang H., Thakker D.R. Role of phospholipase C-beta in the modulation of epithelial tight junction permeability. J. Pharmacol. Exp. Ther. 2003, 304:689-698.
22. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
23. Lundberg B.B. Ether lipids enhance the cytotoxic effect of teniposide and paclitaxel in liposomes against leukaemic cells in culture. Anticancer Drug Des. 1997, 12:503-513.
24. Georgieva M.C., Konstantinov S.M., Topashka-Ancheva M., Berger M.R. Combination effects of alkylphosphocholines and gemcitabine in malignant and normal hematopoietic cells. Cancer Lett. 2002, 182:163-174.
25. 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. 2001, 61:439-444.
26. Jendrossek V., Erdlenbruch B., Hunold A., Kugler W., Eibl H., Lakomek M. Erucylphosphocholine, a novel antineoplastic ether lipid, blocks growth and induces apoptosis in brain tumor cell lines in vitro. Int. J. Oncol. 1999, 14:15-22.
27. Konstantinov S.M., Eibl H., Berger M.R. Alkylphosphocholines induce apoptosis in HL-60 and U-937 leukemic cells. Cancer Chemother. Pharmacol. 1998, 41:210-216.
28. Kugler W., Veenman L., Shandalov Y., Leschiner S., Spanier I., Lakomek M., et al. Ligands of the mitochondrial 18kDa translocator protein attenuate apoptosis of human glioblastoma cells exposed to erucylphosphohomocholine. Cell. Oncol. 2008, 30:435-450.
29. van Blitterswijk W.J., Verheij M. Anticancer alkylphospholipids: mechanisms of action, cellular sensitivity and resistance, and clinical prospects. Curr. Pharm. Des. 2008, 14:2061-2074.
30. Jendrossek V., Hammersen K., Erdlenbruch B., Kugler W., Krügener R., Eibl H., et al. Structure-activity relationships of alkylphosphocholine derivatives: antineoplastic action on brain tumor cell lines in vitro. Cancer Chemother. Pharmacol. 2002, 50:71-79.
31. Konstantinov S.M., Eibl H., Berger M.R. BCR-ABL influences the antileukaemic efficacy of alkylphosphocholines. Brit. J. Haematol. 1999, 107:365-380.
32. Naumann U., Wischhusen J., Weit S., Rieger J., Wolburg H., Massing U., et al. Alkylphosphocholine-induced glioma cell death is BCL-X(L)-sensitive, caspase-independent and characterized by massive cytoplasmic vacuole formation. Cell Death Differ. 2004, 11:1326-1341.
33. 1-ATP(synth)ase and reactive oxygen species in apoptosis induction by the antineoplastic agent erucylphosphohomocholine in glioblastoma cell lines: a mechanism for induction of apoptosis via the 18kDa mitochondrial translocator protein. Apoptosis 2010, 15:753-768.
34. Rheinwald J.G., Beckett M.A. Tumorigenic keratinocyte lines requiring anchorage and fibroblast support cultures from human squamous cell carcinomas. Cancer Res. 1981, 41:1657-1663.
35. Martelli A.M., Papa V., Tazzari P.L., Ricci F., Evangelisti C., Chiarini F., et al. is cytotoxic to acute myelogenous leukemia cells through JNK- and PP2A-dependent mechanisms. Leukemia 2010, 24:687-698.
36. Jendrossek V., Müller I., Eibl H., Belka C. Intracellular mediators of erucylphosphocholine-induced apoptosis. Oncogene 2003, 22:2621-2631.
37. Kugler W., Buchholz F., Köhler F., Eibl H., Lakomek M., Erdlenbruch B. Downregulation of Apaf-1 and caspase-3 by RNA interference in human glioma cells: consequences for erucylphosphocholine-induced apoptosis. Apoptosis 2005, 10:1163-1174.
38. Lemeshko V.V., Kugler W. Synergistic inhibition of mitochondrial respiration by anticancer agent erucylphosphohomocholine and cyclosporin A. J. Biol. Chem. 2007, 282:37303-37307.
39. Morselli E., Galluzzi L., Kepp O., Vicencio J.-M., Criollo A., Maiuri M.C., et al. Anti- and pro-tumor functions of autophagy. Biochim. Biophys. Acta 2009, 1793:1524-1532.
40. Czerninski R., Amornphimoltham P., Patel V., Molinolo A.A., Gutkind J.S. Targeting mammalian target of rapamycin by rapamycin prevents tumor progression in an oral-specific chemical carcinogenesis model. Cancer Prevent. Res. 2009, 2:27.
41. Martelli A.M., Evangelisti C., Chiarini F., Grimaldi C., Manzoli L., McCubrey J.A. Targeting the PI3K/AKT/mTOR signaling network in acute myelogenous leukemia. Expert Opin. Invest. Drugs 2009, 18:1333-1349.
42. Yosifov D.Y., Todorov P.T., Zaharieva M.M., Georgiev K.D., Pilicheva B.A., Konstantinov S.M., et al. Erucylphospho-N, N, N-trimethylpropylammonium (erufosine) is a potential antimyeloma drug devoid of myelotoxicity. Cancer Chemother. Pharmacol. 2011, 67:13-25.
43. Kondapaka S.B., Singh S.S., Dasmahapatra G.P., Sausville E.A., Roy K.K. Perifosine, a novel alkylphospholipid, inhibits protein kinase B activation. Mol. Cancer Ther. 2003, 2:1093-1103.
44. Zhang C., Elkahloun A.G., Liao H., Delaney S., Saber B., Morrow B., et al. Expression signatures of the lipid-based Akt inhibitors phosphatidylinositol ether lipid analogues in NSCLC cells. Mol. Cancer Ther. 2011, 10:1137-1148.