MRP- and BCL-2-mediated drug resistance in human SCLC: Effects of apoptotic sphingolipids in vitro

Lung Cancer

Volumn 66, Issue 1, 2009, Pages 48-57

  Khodadadian, M ^a   Leroux, M E ^a   Auzenne, E ^a   Ghosh, S C ^a   Farquhar, D ^a   Evans, R ^a   Spohn, W ^a   Zou, Y ^b   Klostergaard, J ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; Doxorubicin; Drug resistance; MRP; SCLC; Sphingolipids; Taxol; VP 16

Indexed keywords

CERAMIDE; COUMARIN; DOXORUBICIN; ETOPOSIDE; MULTIDRUG RESISTANCE PROTEIN; N,N DIMETHYLSPHINGOSINE; PACLITAXEL; PROTEIN BCL 2; SPHINGOLIPID; SPHINGOSINE;

APOPTOSIS; ARTICLE; CANCER CELL DESTRUCTION; CANCER RESISTANCE; CELL SURVIVAL; CHEMOSENSITIVITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG STRUCTURE; DRUG UPTAKE; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; LUNG SMALL CELL CANCER; PRIORITY JOURNAL;

APOPTOSIS; CELL LINE, TUMOR; CERAMIDES; DRUG RESISTANCE, NEOPLASM; HUMANS; LUNG NEOPLASMS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; SMALL CELL LUNG CARCINOMA; SPHINGOLIPIDS; SPHINGOSINE;

EID: 68949213189     PISSN: 01695002     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.lungcan.2009.01.006     Document Type: Article

References (60)

1. http://www.emedicine.com/radio/byname/Lung-Cancer--Small-Cell.htm.
2. Govindan R., Page N., Morgensztern D., Read W., Tierney R., Vlahiotis A., et al. Changing epidemiology of small-cell lung cancer in the United States over the last 30 years: analysis of the surveillance, epidemiologic, and end results database. J Clin Oncol 24 28 (2006) 4539-4544
3. Fischer B., and Arcaro A. Current status of clinical trials for small cell lung cancer. Rev Recent Clin Trials 3 January (1) (2008) 40-61 [Review]
4. Charpidou A., Hatzidarellis E.P., Alamara C., Dilana K., Pantazopoulos K., Kotteas E., et al. Pegylated liposomal doxorubicin HCL (Caelyx) in combination with sandostatin LAR as salvage therapy in patients with small-cell lung cancer. In Vivo 20 July-August (4) (2006) 553-557
5. Onoda S., Masuda N., Seto T., Eguchi K., Takiguchi Y., Isobe H., et al. Phase II trial of amrubicin for treatment of refractory or relapsed small-cell lung cancer: Thoracic Oncology Research Group Study 0301. J Clin Oncol 24 December (34) (2006) 5448-5453
6. O'Brien M., Eckardt J., and Ramlau R. Recent advances with topotecan in the treatment of lung cancer. Oncologist 12 October (10) (2007) 1194-1204 [Review]
7. Graziano S.L., Herndon II J.E., Socinski M.A., Wang X., Watson D., Vokes E., et al. Phase II trial of weekly dose-dense paclitaxel in extensive-stage small cell lung cancer: cancer and leukemia group B study 39901. J Thorac Oncol 3 February (2) (2008) 158-162
8. You B., Tranchand B., Girard P., Falandry C., Ribba B., Chabaud S., et al. Etoposide pharmacokinetics and survival in patients with small cell lung cancer: a multicentre study. Lung Cancer 62 November (2) (2008) 261-272
9. Mavroudis D., Veslemes M., Kouroussis Ch., Tzanakis N., Ferdoutsis E., Toumbis M., et al. Cisplatin-etoposide alternating with topotecan in patients with extensive stage small cell lung cancer (SCLC). A multicenter phase II study. Lung Cancer 38 October (1) (2002) 59-63
10. Shah C., Ready N., Perry M., Kirshner J., Gajra A., Neuman N., et al. A multi-center phase II study of weekly topotecan as second-line therapy for small cell lung cancer. Lung Cancer 57 July (1) (2007) 84-88
11. Sharom F.J. ABC multidrug transporters: structure, function and role in chemoresistance. Pharmacogenomics 9 January (1) (2008) 105-127 [Review]
12. Cole S.P.C., Bhardwaj G., and Gerlach J.H. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258 (1992) 1650-1654
13. Young L.C., Campling B.G., Voskoglou-Nomikos T., Cole S.P., Deeley R.G., and Gerlach J.H. Expression of multidrug resistance protein-related genes in lung cancer: correlation with drug response. Clin Cancer Res 5 March (3) (1999) 673-680
14. Young L.C., Campling B.G., Cole S.P., Deeley R.G., and Gerlach J.H. Multidrug resistance proteins MRP3, MRP1, and MRP2 in lung cancer: correlation of protein levels with drug response and messenger RNA levels. Clin Cancer Res 7 June (6) (2001) 1798-1804
15. Gandhi L., Harding M.W., Neubauer M., Langer C.J., Moore M., Ross H.J., et al. A phase II study of the safety and efficacy of the multidrug resistance inhibitor VX-710 combined with doxorubicin and vincristine in patients with recurrent small cell lung cancer. Cancer 109 March (5) (2007) 924-932
16. Scagliotti G.V., Novello S., and Selvaggi G. Multidrug resistance in non-small-cell lung cancer. Ann Oncol 10 Suppl 5 (1999) S83-S86
17. Tahir S.K., Yang X., Anderson M.G., Morgan-Lappe S.E., Sarthy A.V., Chen J., et al. Influence of Bcl-2 family members on the cellular response of small-cell lung cancer cell lines to ABT-737. Cancer Res 67 (2007) 1176-1183
18. Mortenson M.M., Schlieman M.G., Virudachalam S., Lara P.N., Gandara D.G., Davies A.M., et al. Reduction in BCL-2 levels by 26S proteasome inhibition with bortezomib is associated with induction of apoptosis in small cell lung cancer. Lung Cancer 49 (2005) 163-170
19. Cuvillier O. Downregulating sphingosine kinase-1 for cancer therapy. Expert Opin Ther Targets 12 August (8) (2008) 1009-1020
20. Pruett S.T., Bushnev A., Hagedorn K., Adiga M., Haynes C.A., Sullards M.C., et al. Thematic review series: sphingolipids. Biodiversity of sphingoid bases ("sphingosines") and related amino alcohols. J Lipid Res 49 August (8) (2008) 1621-1639 [Review]
21. Sweeney E.A., Sakakura C., Shirahama T., Masamune A., Ohta H., Hakomori S., et al. Sphingosine and its methylated derivative N,N-dimethylsphingosine (DMS) induce apoptosis in a variety of human cancer cell lines. Int J Cancer 66 May (3) (1996) 358-366
22. Endo K., Igarashi Y., Nisar M., Zhou Q.H., and Hakomori S. Cell membrane signaling as a target in cancer therapy: inhibitory effect of N,N-dimethyl and N,N,N-trimethyl sphingosine derivatives on in vitro and in vivo growth of human tumor cells in nude mice. Cancer Res 51 March (6) (1991) 1613-1618
23. Okoshi H., Hakomori S., Nisar M., Zhou Q.H., Kimura S., Tashiro K., et al. Cell membrane signaling as target in cancer therapy II: inhibitory effect of N,N,N-trimethylsphingosine on metastatic potential of murine B16 melanoma cell line through blocking of tumor cell-dependent platelet aggregation. Cancer Res 51 November (22) (1991) 6019-6024
24. Park Y.S., Hakomori S., Kawa S., Ruan F., and Igarashi Y. Liposomal N,N,N-trimethylsphingosine (TMS) as an inhibitor of B16 melanoma cell growth and metastasis with reduced toxicity and enhanced drug efficacy compared to free TMS: cell membrane signaling as a target in cancer therapy III. Cancer Res 54 April (8) (1994) 2213-2217
25. Shirahama T., Sweeney E.A., Sakakura C., Singhal A.K., Nishiyama K., Akiyama S., et al. In vitro and in vivo induction of apoptosis by sphingosine and N,N-dimethylsphingosine in human epidermoid carcinoma KB-3-1 and its multidrug-resistant cells. Clin Cancer Res 3 February (2) (1997) 257-264
26. Mandala S.M., Thornton R., Tu Z., Kurtz M.B., Nickels J., Broach J., et al. Sphingoid base 1-phosphate phosphatase: a key regulator of sphingolipid metabolism and stress response. Proc Natl Acad Sci USA 95 January (1) (1998) 150-155
27. Maceyka M., Payne S.G., Milstien S., and Spiegel S. Sphingosine kinase, sphingosine-1-phosphate, and apoptosis. Biochim Biophys Acta 1585 December (2-3) (2002) 193-201 [Review]
28. Ruckhäberle E., Rody A., Engels K., Gaetje R., von Minckwitz G., Schiffmann S., et al. Microarray analysis of altered sphingolipid metabolism reveals prognostic significance of sphingosine kinase 1 in breast cancer. Breast Cancer Res Treat 112 November (1) (2007) 41-52
29. Cuvillier O., Edsall L., and Spiegel. Involvement of sphingosine in mitochondria-dependent Fas-induced apoptosis of type II Jurkat T cells. J Biol Chem 275 21 (2000) 15691-15700
30. Cuvillier O., Nava V.E., Murthy S.K., Edsall L.C., Levade T., Milstien S., et al. Sphingosine generation, cytochrome c release, and activation of caspase-7 in doxorubicin-induced apoptosis of MCF7 breast adenocarcinoma cells. Cell Death Differ 8 February (2) (2001) 162-171
31. Cuvillier O., Pirianov G., Kleuser B., Vanek P.G., Coso O.A., Gutkind S., et al. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 381 June (6585) (1996) 800-803
32. Cuvillier O., Rosenthal D.S., Smulson M.E., and Spiegel S. Sphingosine 1-phosphate inhibits activation of caspases that cleave poly(ADP-ribose) polymerase and lamins during Fas-and ceramide-mediated apoptosis in Jurkat T lymphocytes. J Biol Chem 273 January (5) (1998) 2910-2916
33. Pyne S., and Pyne N.J. Sphingosine 1-phosphate signaling in mammalian cells. Biochem J 349 (2000) 385-402
34. Cuvillier O., and Levade T. Sphingosine 1-phosphate antagonizes apoptosis of human leukemia cells by inhibiting release of cytochrome c and Smac/DIABLO from mitochondria. Blood 9 (2001) 2828-2836
35. Edsall L.C., Cuvillier O., Twitty S., Spiegel S., and Milstien S. Sphingosine kinase expression regulates apoptosis and caspase activation in PC12 cells. J Neurochem 76 March (5) (2001) 1573-1584
36. Liu H., Chakravarty D., Maceyka M., Milstien S., and Spiegel S. Sphingosine kinases: a novel family of lipid kinases. Prog Nucl Acid Res Mol Biol 71 (2002) 493-511 [Review]
37. Nava V.E., Hobson J.P., Murthy S., Milstien S., and Spiegel S. Sphingosine kinase type 1 promotes estrogen-dependent tumorigenesis of breast cancer MCF-7 cells. Exp Cell Res 281 November (1) (2002) 115-127
38. Ancellin N., Colmont C., Su J., Li Q., Mittereder N., Chae S.S., et al. Extracellular export of sphingosine kinase-1 enzyme. Sphingosine 1-phosphate generation and the induction of angiogenic vascular maturation. J Biol Chem 277 February (8) (2002) 6667-6675
39. Edsall L.C., Van Brocklyn J.R., Cuvillier O., Kleuser B., and Spiegel S. N,N-Dimethylsphingosine is a potent competitive inhibitor of sphingosine kinase but not of protein kinase C: modulation of cellular levels of sphingosine 1-phosphate and ceramide. Biochemistry 37 September (37) (1998) 12892-12898
40. Doyle L.A., Ross D.D., Ordonez J.V., Yang W., Gao Y., Tong Y., et al. An etoposide-resistant small cell lung cancer cell subline overexpresses the multidrug resistance-associated protein (MRP) gene. Br J Cancer 72 September (3) (1995) 535-542
41. Perez-Soler R., Neamati N., Zou Y., Schneider E., Doyle L.A., Andreeff M., et al. Annamycin circumvents resistance mediated by the multidrug resistance-associated protein (MRP) in breast MCF-7 and small-cell lung UMCC-1 cancer cell lines selected for resistance to etoposide. Int J Cancer 71 March (1) (1997) 35-41
42. Mortenson M.M., Schlieman M.G., Virudachalam S., Lara P.N., Gandara D.G., Davies A.M., et al. Reduction in BCL-2 levels by 26S proteasome inhibition with bortezomib is associated with induction of apoptosis in small cell lung cancer. Lung Cancer 49 August (2) (2005) 163-170
43. Ben-Ezra J.M., Kornstein M.J., Grimes M.M., and Krystal G. Small cell carcinomas of the lung express the Bcl-2 protein. Am J Pathol 145 November (5) (1994) 1036-1040
44. Hipfner D.R., Gauldie S.D., Deeley R.G., and Cole S.P. Detection of the M(r) 190,000 multidrug resistance protein, MRP, with monoclonal antibodies. Cancer Res 54 November (22) (1994) 5788-5792
45. Slovak M.L., Ho J.P., Bhardwaj G., Kurz E.U., Deeley R.G., and Cole S.P. Localization of a novel multidrug resistance-associated gene in the HT1080/DR4 and H69AR human tumor cell lines. Cancer Res 53 July (14) (1993) 3221-3225
46. Ghosh S.C., Auzenne E., Farquhar D., and Klostergaard J. N,N-Dimethylsphingosine-coumarin: synthesis, chemical characterization, and biological evaluation. Bioconjug Chem 18 May-June (3) (2007) 731-735
47. Leroux M.E., Auzenne E., Evans R., Hail Jr. N., Spohn W., Ghosh S.C., et al. Sphingolipids and the sphingosine kinase inhibitor, SKI II, induce BCL-2-independent apoptosis in human prostatic adenocarcinoma cells. Prostate 67 November (15) (2007) 1699-1717
48. http://www.millipore.com/cellbiology/cb3/mttcellgrowth.
49. Bielawska A., Linardic C.M., and Hannun Y.A. Modulation of cell growth and differentiation by ceramide. FEBS Lett 307 (1992) 211-214
50. http://www.copewithcytokines.de/cope.cgi?key=TUNEL%20assay.
51. Jendiroba D.B., Klostergaard J., Keyhani A., Pagliaro L., and Freireich E.J. Effective cytotoxicity against human leukemias and chemotherapy-resistant leukemia cell lines by N-N-dimethylsphingosine. Leukemia Res 26 March (3) (2002) 301-310
52. Raggers R.J., van Helvoort A., Evers R., and van Meer G. The human multidrug resistance protein MRP1 translocates sphingolipid analogs across the plasma membrane. J Cell Sci 112 February (Pt 3) (1999) 415-422
53. Kok J.W., Veldman R.J., Klappe K., Koning H., Filipeanu C.M., and Müller M. Differential expression of sphingolipids in MRP1 overexpressing HT29 cells. Int J Cancer 87 July (2) (2000) 172-178
54. Narasaki F., Oka M., Fukuda M., Nakano R., Ikeda K., Takatani H., et al. A novel quinoline derivative, MS-209, overcomes drug resistance of human lung cancer cells expressing the multidrug resistance-associated protein (MRP) gene. Cancer Chemother Pharmacol 40 5 (1997) 425-432
55. Olson D.P., Scadden D.T., D'Aquila R.T., and De Pasquale M.P. The protease inhibitor ritonavir inhibits the functional activity of the multidrug resistance related-protein 1 (MRP-1). AIDS 16 September (13) (2002) 1743-1747
56. Tsurutani J., Soda H., Oka M., Suenaga M., Doi S., Nakamura Y., et al. Antiproliferative effects of the histone deacetylase inhibitor FR901228 on small-cell lung cancer lines and drug-resistant sublines. Int J Cancer 104 March (2) (2003) 238-242
57. Rudin C.M., Salgia R., Wang X., Hodgson L.D., Masters G.A., Green M., et al. Randomized phase II Study of carboplatin and etoposide with or without the bcl-2 antisense oligonucleotide oblimersen for extensive-stage small-cell lung cancer: CALGB 30103. J Clin Oncol 26 February (6) (2008) 870-876
58. French K.J., Schrecengost R.S., Lee B.D., Zhuang Y., Smith S.N., Eberly J.L., et al. Discovery and evaluation of inhibitors of human sphingosine kinase. Cancer Res 63 September (18) (2003) 5962-5969
59. Johnson K.R., Johnson K.Y., Crellin H.G., Ogretmen B., Boylan A.M., Harley R.A., et al. Immunohistochemical distribution of sphingosine kinase 1 in normal and tumor lung tissue. J Histochem Cytochem 53 September (9) (2005) 1159-1166
60. Auzenne E, Khodadadian M, Rivera B, Price RE, Zou Y, Klostergaard J. Targeting sphingosine kinase in vivo via liposomal-dimethyl-sphingosine: characterization of anti-tumor efficacy in human breast adenocarcinoma orthotopic xenograft models, in preparation.