Liposomal sphingomyelin influences the cellular lipid profile of human lymphoblastic leukemia cells without effect on P-glycoprotein activity

Molecular Pharmaceutics

Volumn 10, Issue 3, 2013, Pages 1020-1034

  Zembruski, Nadine C L ^a   Nguyen, Chi D L ^a   Theile, Dirk ^a   Ali, Ramadan M M ^a   Herzog, Melanie ^a   Hofhaus, Götz ^a   Heintz, Udo ^a   Burhenne, Jürgen ^a   Haefeli, Walter E ^a   Weiss, Johanna ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

lipid rafts; liposomes; multidrug resistance; P glycoprotein; SM

Indexed keywords

ABC TRANSPORTER; ABCC1 PROTEIN; ABCC10 PROTEIN; ABCC2 PROTEIN; ABCC3 PROTEIN; ABCC4 PROTEIN; ABCC6 PROTEIN; ALCOHOL; BREAST CANCER RESISTANCE PROTEIN; CALCEIN; CAMPTOTHECIN; DOXORUBICIN; LIPOSOME; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; RHODAMINE; SPHINGOMYELIN; UNCLASSIFIED DRUG; VINCRISTINE;

ARTICLE; CELL MEMBRANE; CHEMOSENSITIVITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DENSITY GRADIENT CENTRIFUGATION; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; LEUKEMIA CELL; LIPID RAFT; LIQUID CHROMATOGRAPHY; LYMPHATIC LEUKEMIA; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

EID: 84874589575     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300485j     Document Type: Article

References (63)

1. Slotte, J. P. Sphingomyelin-cholesterol interactions in biological and model membranes Chem. Phys. Lipids 1999, 102, 13-27
2. Simons, K.; Sampaio, J. L. Membrane organization and lipid rafts Cold Spring Harbor Perspect. Biol. 2011, 3, a004697
3. Ohvo-Rekila, H.; Ramstedt, B.; Leppimaki, P.; Slotte, J. P. Cholesterol interactions with phospholipids in membranes Prog. Lipid Res. 2002, 41, 66-97
4. Brown, D. A. Lipid rafts, detergent-resistant membranes, and raft targeting signals Physiology (Bethesda) 2006, 21, 430-9
5. Thiebaut, F.; Tsuruo, T.; Hamada, H.; Gottesman, M. M.; Pastan, I.; Willingham, M. C. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 7735-8
6. Lage, H. An overview of cancer multidrug resistance: a still unsolved problem Cell. Mol. Life Sci. 2008, 65, 3145-67
7. Dean, M.; Rzhetsky, A.; Allikmets, R. The human ATP-binding cassette (ABC) transporter superfamily Genome Res. 2001, 11, 1156-66
8. Szakacs, G.; Paterson, J. K.; Ludwig, J. A.; Booth-Genthe, C.; Gottesman, M. M. Targeting multidrug resistance in cancer Nat. Rev. Drug Discovery 2006, 5, 219-34
9. Orlowski, S.; Martin, S.; Escargueil, A. P-glycoprotein and 'lipid rafts': some ambiguous mutual relationships (floating on them, building them or meeting them by chance?) Cell. Mol. Life Sci. 2006, 63, 1038-59
10. Barakat, S.; Gayet, L.; Dayan, G.; Labialle, S.; Lazar, A.; Oleinikov, V.; Coleman, A. W.; Baggetto, L. G. Multidrug-resistant cancer cells contain two populations of P-glycoprotein with differently stimulated P-gp ATPase activities: evidence from atomic force microscopy and biochemical analysis Biochem. J. 2005, 388, 563-71
11. Doige, C. A.; Yu, X.; Sharom, F. J. The effects of lipids and detergents on ATPase-active P-glycoprotein Biochim. Biophys. Acta 1993, 1146, 65-72
12. Romsicki, Y.; Sharom, F. J. The ATPase and ATP-binding functions of P-glycoprotein-modulation by interaction with defined phospholipids Eur. J. Biochem. 1998, 256, 170-8
13. Meyer dos Santos, S.; Weber, C. C.; Franke, C.; Muller, W. E.; Eckert, G. P. Cholesterol: Coupling between membrane microenvironment and ABC transporter activity Biochem. Biophys. Res. Commun. 2007, 354, 216-21
14. Troost, J.; Albermann, N.; Emil Haefeli, W.; Weiss, J. Cholesterol modulates P-glycoprotein activity in human peripheral blood mononuclear cells Biochem. Biophys. Res. Commun. 2004, 316, 705-11
15. Modok, S.; Heyward, C.; Callaghan, R. P-glycoprotein retains function when reconstituted into a sphingolipid- and cholesterol-rich environment J. Lipid Res. 2004, 45, 1910-8
16. Gayet, L.; Dayan, G.; Barakat, S.; Labialle, S.; Michaud, M.; Cogne, S.; Mazane, A.; Coleman, A. W.; Rigal, D.; Baggetto, L. G. Control of P-glycoprotein activity by membrane cholesterol amounts and their relation to multidrug resistance in human CEM leukemia cells Biochemistry 2005, 44, 4499-509
17. Immordino, M. L.; Dosio, F.; Cattel, L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential Int. J. Nanomed. 2006, 1, 297-315
18. Webb, M. S.; Harasym, T. O.; Masin, D.; Bally, M. B.; Mayer, L. D. Sphingomyelin-cholesterol liposomes significantly enhance the pharmacokinetic and therapeutic properties of vincristine in murine and human tumour models Br. J. Cancer 1995, 72, 896-904
19. Boehlke, L.; Winter, J. N. Sphingomyelin/cholesterol liposomal vincristine: a new formulation for an old drug Expert Opin. Biol. Ther. 2006, 6, 409-15
20. Thomas, D. A.; Sarris, A. H.; Cortes, J.; Faderl, S.; O'Brien, S.; Giles, F. J.; Garcia-Manero, G.; Rodriguez, M. A.; Cabanillas, F.; Kantarjian, H. Phase II study of sphingosomal vincristine in patients with recurrent or refractory adult acute lymphocytic leukemia Cancer 2006, 106, 120-7
21. Sarris, A. H.; Hagemeister, F.; Romaguera, J.; Rodriguez, M. A.; McLaughlin, P.; Tsimberidou, A. M.; Medeiros, L. J.; Samuels, B.; Pate, O.; Oholendt, M.; Kantarjian, H.; Burge, C.; Cabanillas, F. Liposomal vincristine in relapsed non-Hodgkin's lymphomas: early results of an ongoing phase II trial Ann. Oncol. 2000, 11, 69-72
22. Thomas, D. A.; Kantarjian, H. M.; Stock, W.; Heffner, L. T.; Faderl, S.; Garcia-Manero, G.; Ferrajoli, A.; Wierda, W.; Pierce, S.; Lu, B.; Deitcher, S. R.; O'Brien, S. Phase 1 multicenter study of vincristine sulfate liposomes injection and dexamethasone in adults with relapsed or refractory acute lymphoblastic leukemia Cancer 2009, 115, 5490-8
23. Bedikian, A. Y.; Papadopoulos, N. E.; Kim, K. B.; Vardeleon, A.; Smith, T.; Lu, B.; Deitcher, S. R. A pilot study with vincristine sulfate liposome infusion in patients with metastatic melanoma Melanoma Res. 2008, 18, 400-4
24. Bedikian, A. Y.; Vardeleon, A.; Smith, T.; Campbell, S.; Namdari, R. Pharmacokinetics and urinary excretion of vincristine sulfate liposomes injection in metastatic melanoma patients J. Clin. Pharmacol. 2006, 46, 727-37
25. Troost, J.; Lindenmaier, H.; Haefeli, W. E.; Weiss, J. Modulation of cellular cholesterol alters P-glycoprotein activity in multidrug-resistant cells Mol. Pharmacol. 2004, 66, 1332-9
26. Dos Santos, N.; Mayer, L. D.; Abraham, S. A.; Gallagher, R. C.; Cox, K. A. K.; Tardi, P. G.; Bally, M. B. Improved retention of idarubicin after intravenous injection obtained for cholesterol-free liposomes Biochim. Biophys. Acta 2002, 1561, 188-201
27. Kimmig, A.; Gekeler, V.; Neumann, M.; Frese, G.; Handgretinger, R.; Kardos, G.; Diddens, H.; Niethammer, D. Susceptibility of multidrug-resistant human leukemia cell lines to human interleukin 2-activated killer cells Cancer Res. 1990, 50, 6793-9
28. Zembruski, N. C.; Büchel, G.; Jödicke, L.; Herzog, M.; Haefeli, W. E.; Weiss, J. Potential of novel antiretrovirals to modulate expression and function of drug transporters in vitro J. Antimicrob. Chemother. 2011, 66, 802-12
29. Theile, D.; Ketabi-Kiyanvash, N.; Herold-Mende, C.; Dyckhoff, G.; Efferth, T.; Bertholet, V.; Haefeli, W. E.; Weiss, J. Evaluation of drug transporters' significance for multidrug resistance in head and neck squamous cell carcinoma Head Neck 2011, 33, 959-68
30. Herzog, M.; Storch, C. H.; Gut, P.; Kotlyar, D.; Füllekrug, J.; Ehehalt, R.; Haefeli, W. E.; Weiss, J. Knockdown of caveolin-1 decreases activity of breast cancer resistance protein (BCRP/ABCG2) and increases chemotherapeutic sensitivity Naunyn Schmiedebergs Arch. Pharmacol. 2011, 383, 1-11
31. Szakács, G.; Annereau, J. P.; Lababidi, S.; Shankavaram, U.; Arciello, A.; Bussey, K. J.; Reinhold, W.; Guo, Y.; Kruh, G. D.; Reimers, M.; Weinstein, J. N.; Gottesman, M. M. Predicting drug sensitivity and resistance: profiling ABC transporter genes in cancer cells Cancer Cell 2004, 6, 129-37
32. Vandesompele, J.; De Preter, K.; Pattyn, F.; Poppe, B.; Van Roy, N.; De Paepe, A.; Speleman, F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3, RESEARCH0034.
33. Weiss, J.; Rose, J.; Storch, C. H.; Ketabi-Kiyanvash, N.; Sauer, A.; Haefeli, W. E.; Efferth, T. Modulation of human BCRP (ABCG2) activity by anti-HIV drugs J. Antimicrob. Chemother. 2007, 59, 238-45
34. Albermann, N.; Schmitz-Winnenthal, F. H.; Z'Graggen, K.; Volk, C.; Hoffmann, M. M.; Haefeli, W. E.; Weiss, J. Expression of the drug transporters MDR1/ABCB1, MRP1/ABCC1, MRP2/ABCC2, BCRP/ABCG2, and PXR in peripheral blood mononuclear cells and their relationship with the expression in intestine and liver Biochem. Pharmacol. 2005, 70, 949-58
35. Domazou, A. S.; Luisi, P. L. Size distribution of spontaneously formed liposomes by the alcohol injection method J. Liposome Res. 2002, 12, 205-220
36. Stano, P.; Bufali, S.; Pisano, C.; Bucci, F.; Barbarino, M.; Santaniello, M.; Carminati, P.; Luisi, P. L. Novel camptothecin analogue (gimatecan)-containing liposomes prepared by the ethanol injection method J. Liposome Res. 2004, 14, 87-109
37. Storch, C. H.; Ehehalt, R.; Haefeli, W. E.; Weiss, J. Localization of the human breast cancer resistance protein (BCRP/ABCG2) in lipid rafts/caveolae and modulation of its activity by cholesterol in vitro J. Pharmacol. Exp. Ther. 2007, 323, 257-64
38. Pieri, M.; Castiglia, L.; Basilicata, P.; Sannolo, N.; Acampora, A.; Miraglia, N. Biological monitoring of nurses exposed to doxorubicin and epirubicin by a validated liquid chromatography/fluorescence detection method Ann. Occup. Hyg. 2010, 54, 368-76
39. Guidance for Industry. Bioanalytical Method Validation. U.S. Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research (CDER), Center for Veterinary Medicine (CVM): Rockville, MD, 2001.
40. Zembruski, N. C.; Stache, V.; Haefeli, W. E.; Weiss, J. 7-Aminoactinomycin D for apoptosis staining in flow cytometry Anal. Biochem. 2012, 429, 79-81
41. Francis, G.; Kerem, Z.; Makkar, H. P.; Becker, K. The biological action of saponins in animal systems: a review Br. J. Nutr. 2002, 88, 587-605
42. Weiss, J.; Dormann, S. M.; Martin-Facklam, M.; Kerpen, C. J.; Ketabi-Kiyanvash, N.; Haefeli, W. E. Inhibition of P-glycoprotein by newer antidepressants J. Pharmacol. Exp. Ther. 2003, 305, 197-204
43. Fröhlich, M.; Albermann, N.; Sauer, A.; Walter-Sack, I.; Haefeli, W. E.; Weiss, J. In vitro and ex vivo evidence for modulation of P-glycoprotein activity by progestins Biochem. Pharmacol. 2004, 68, 2409-16
44. König, S. K.; Herzog, M.; Theile, D.; Zembruski, N.; Haefeli, W. E.; Weiss, J. Impact of drug transporters on cellular resistance towards saquinavir and darunavir J. Antimicrob. Chemother. 2010, 65, 2319-28
45. Weiss, J.; Weis, N.; Ketabi-Kiyanvash, N.; Storch, C. H.; Haefeli, W. E. Comparison of the induction of P-glycoprotein activity by nucleotide, nucleoside, and non-nucleoside reverse transcriptase inhibitors Eur. J. Pharmacol. 2008, 579, 104-9
46. Matyash, V.; Liebisch, G.; Kurzchalia, T. V.; Shevchenko, A.; Schwudke, D. Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics J. Lipid Res. 2008, 49, 1137-46
47. Retra, K.; Bleijerveld, O. B.; van Gestel, R. A.; Tielens, A. G.; van Hellemond, J. J.; Brouwers, J. F. A simple and universal method for the separation and identification of phospholipid molecular species Rapid Commun. Mass Spectrom. 2008, 22, 1853-62
48. Jesorka, A.; Orwar, O. Liposomes: technologies and analytical applications Annu. Rev. Anal. Chem. (Palo Alto, Calif.) 2008, 1, 801-32
49. Semple, S. C.; Leone, R.; Wang, J.; Leng, E. C.; Klimuk, S. K.; Eisenhardt, M. L.; Yuan, Z. N.; Edwards, K.; Maurer, N.; Hope, M. J.; Cullis, P. R.; Ahkong, Q. F. Optimization and characterization of a sphingomyelin/ cholesterol liposome formulation of vinorelbine with promising antitumor activity J. Pharm. Sci. 2005, 94, 1024-38
50. Johnston, M. J. W.; Semple, S. C.; Klimuk, S. K.; Ansell, S.; Maurer, N.; Cullis, P. R. Characterization of the drug retention and pharmacokinetic properties of liposomal nanoparticles containing dihydrosphingomyelin Biochim. Biophys. Acta 2007, 1768, 1121-7
51. Rainer, J.; Ploner, C.; Jesacher, S.; Ploner, A.; Eduardoff, M.; Mansha, M.; Wasim, M.; Panzer-Grumayer, R.; Trajanoski, Z.; Niederegger, H.; Kofler, R. Glucocorticoid-regulated microRNAs and mirtrons in acute lymphoblastic leukemia Leukemia 2009, 23, 746-52
52. Schmidt, S.; Irving, J. A.; Minto, L.; Matheson, E.; Nicholson, L.; Ploner, A.; Parson, W.; Kofler, A.; Amort, M.; Erdel, M.; Hall, A.; Kofler, R. Glucocorticoid resistance in two key models of acute lymphoblastic leukemia occurs at the level of the glucocorticoid receptor FASEB J. 2006, 20, 2600-2
53. Ploner, C.; Rainer, J.; Niederegger, H.; Eduardoff, M.; Villunger, A.; Geley, S.; Kofler, R. The BCL2 rheostat in glucocorticoid-induced apoptosis of acute lymphoblastic leukemia Leukemia 2008, 22, 370-7
54. Ramu, A.; Glaubiger, D.; Magrath, I. T.; Joshi, A. Plasma membrane lipid structural order in doxorubicin-sensitive and -resistant P388 cells Cancer Res. 1983, 43, 5533-7
55. Ramu, A.; Glaubiger, D.; Weintraub, H. Differences in lipid composition of doxorubicin-sensitive and -resistant P388 cells Cancer Treat. Rep. 1984, 68, 637-41
56. Modrak, D. E.; Gold, D. V.; Goldenberg, D. M. Sphingolipid targets in cancer therapy Mol. Cancer Ther. 2006, 5, 200-8
57. Bartke, N.; Hannun, Y. A. Bioactive sphingolipids: metabolism and function J. Lipid Res. 2009, 50 (Suppl.) S91-6
58. Osawa, Y.; Uchinami, H.; Bielawski, J.; Schwabe, R. F.; Hannun, Y. A.; Brenner, D. A. Roles for C16-ceramide and sphingosine 1-phosphate in regulating hepatocyte apoptosis in response to tumor necrosis factor-alpha J. Biol. Chem. 2005, 280, 27879-87
59. Michel, V.; Bakovic, M. Lipid rafts in health and disease Biol. Cell 2007, 99, 129-40
60. Simons, K.; Ehehalt, R. Cholesterol, lipid rafts, and disease J. Clin. Invest. 2002, 110, 597-603
61. Fuller, M. Sphingolipids: the nexus between Gaucher disease and insulin resistance Lipids Health Dis. 2010, 9, 113
62. EPAR-Product Information; Caelyx 2 mg/mL concentrate for solution for infusion; available from http://www.ema.europa.eu. Last updated 29.06.2012.
63. Rodriguez, M. A.; Pytlik, R.; Kozak, T.; Chhanabhai, M.; Gascoyne, R.; Lu, B.; Deitcher, S. R.; Winter, J. N. Vincristine sulfate liposomes injection (Marqibo) in heavily pretreated patients with refractory aggressive non-Hodgkin lymphoma: report of the pivotal phase 2 study Cancer 2009, 115, 3475-82