Drug uptake, lipid rafts, and vesicle trafficking modulate resistance to an anticancer lysophosphatidylcholine analogue in yeast

Journal of Biological Chemistry

Volumn 288, Issue 12, 2013, Pages 8405-8418

  Cuesta Marbán, Álvaro ^a   Botet, Javier ^a,b   Czyz, Ola ^c   Cacharro, Luis M ^a   Gajate, Consuelo ^a   Hornillos, Valentín ^d   Delgado, Javier ^d   Zhang, Hui ^a,g   Amat Guerri, Francisco ^d   Acuña, A Ulises ^e   McMaster, Christopher R ^f   Revuelta, José Luis ^b   Zaremberg, Vanina ^c   Mollinedo, Faustino ^a  

^a CSIC   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c UNIVERSITY OF CALGARY   (Canada)

^d INSTITUTO DE QUÍMICA ORGÁNICA GENERAL   (Spain)

^e INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^f DALHOUSIE UNIVERSITY   (Canada)

^g XIANGNAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELL MEMBRANES; CYTOTOXICITY; GENES; MOLECULAR BIOLOGY; PHOSPHOLIPIDS; PROTEINS;

CELL SURFACE PROTEINS; ENDOPLASMIC RETICULUM; ETHER PHOSPHOLIPIDS; LYSOPHOSPHATIDYL-CHOLINE; MECHANISM OF ACTION; RESISTANT MUTANTS; VESICLE TRAFFICKING; VESICULAR TRANSPORT;

YEAST;

AGP2 PROTEIN; DOC1 PROTEIN; EDELFOSINE; LEM3 PROTEIN; LYSOPHOSPHATIDYLCHOLINE; MILTEFOSINE; PERIFOSINE; PROTON PUMP; UNCLASSIFIED DRUG;

AGP2 GENE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL DEATH; CELL MEMBRANE; CELL MIGRATION; CELL TYPE; CELL VACUOLE; CYTOTOXICITY; DOC1 GENE; DRUG MECHANISM; DRUG STRUCTURE; DRUG UPTAKE; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; FUNGAL STRAIN; GENE; GENE DELETION; LEM3 GENE; LIPID RAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SACCHAROMYCES CEREVISIAE; TUMOR CELL; YEAST;

SACCHAROMYCES CEREVISIAE;

EID: 84875474914     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.425769     Document Type: Article

References (46)

1. Gajate, C., and Mollinedo, F. (2002) Biological activities, mechanisms of action, and biomedical prospect of the antitumor ether phospholipid ET- 18-OCH3 (edelfosine), a proapoptotic agent in tumor cells. Curr. Drug Metab. 3, 491-525 (Pubitemid 34987482)
2. Mollinedo, F., Gajate, C., Martín-Santamaría, S., and Gago, F. (2004) ET- 18-OCH3 (edelfosine): a selective antitumour lipid targeting apoptosis through intracellular activation of Fas/CD95 death receptor. Curr. Med. Chem. 11, 3163-3184 (Pubitemid 39539180)
3. Jendrossek, V., and Handrick, R. (2003) Membrane targeted anticancer drugs: potent inducers of apoptosis and putative radiosensitisers. Curr. Med. Chem. Anticancer Agents 3, 343-353 (Pubitemid 37045712)
4. Gajate, C., Del Canto-Jañez, E., Acuña, A. U., Amat-Guerri, F., Geijo, E., Santos-Beneit, A. M., Veldman, R. J., and Mollinedo, F. (2004) Intracellular triggering of Fas aggregation and recruitment of apoptotic molecules into Fas-enriched rafts in selective tumor cell apoptosis. J. Exp. Med. 200, 353-365 (Pubitemid 39031254)
5. Mollinedo, F., Fernández-Luna, J. L., Gajate, C., Martín-Martín, B., Benito, A., Martínez-Dalmau, R., and Modolell, M. (1997) Selective induction of apoptosis in cancer cells by the ether lipid ET-18-OCH3 (Edelfosine): molecular structure requirements, cellular uptake, and protection by Bcl-2 and Bcl-XL. Cancer Res. 57, 1320-1328 (Pubitemid 27152558)
6. Gajate, C., Fonteriz, R. I., Cabaner, C., Alvarez-Noves, G., Alvarez-Rodriguez, Y., Modolell, M., and Mollinedo, F. (2000) Intracellular triggering of Fas, independently of FasL, as a new mechanism of antitumor ether lipidinduced apoptosis. Int. J. Cancer 85, 674-682 (Pubitemid 30080481)
7. Gajate, C., and Mollinedo, F. (2007) Edelfosine and perifosine induce selective apoptosis in multiple myeloma by recruitment of death receptors and downstream signaling molecules into lipid rafts. Blood 109, 711-719 (Pubitemid 46105973)
8. Mollinedo, F., de la Iglesia-Vicente, J., Gajate, C., Estella-Hermoso de Mendoza, A., Villa-Pulgarin, J. A., Campanero, M. A., and Blanco-Prieto, M. J. (2010) Lipid raft-targeted therapy in multiple myeloma. Oncogene 29, 3748-3757
9. Mollinedo, F., de la Iglesia-Vicente, J., Gajate, C., Estella-Hermoso de Mendoza, A., Villa-Pulgarin, J. A., de Frias, M., Roué, G., Gil, J., Colomer, D., Campanero, M. A., and Blanco-Prieto, M. J. (2010) In vitro and in vivo selective antitumor activity of Edelfosine against mantle cell lymphoma and chronic lymphocytic leukemia involving lipid rafts. Clin. Cancer Res. 16, 2046-2054
10. Gajate, C., Matos-da-Silva, M., Dakir, el-H., Fonteriz, R. I., Alvarez, J., and Mollinedo, F. (2012) Antitumor alkyl-lysophospholipid analog edelfosine induces apoptosis in pancreatic cancer by targeting endoplasmic reticulum. Oncogene 31, 2627-2639
11. van der Luit, A. H., Budde, M., Ruurs, P., Verheij, M., and van Blitterswijk, W. J. (2002) Alkyl-lysophospholipid accumulates in lipid rafts and induces apoptosis via raft-dependent endocytosis and inhibition of phosphatidylcholine synthesis. J. Biol. Chem. 277, 39541-39547 (Pubitemid 35190932)
12. Gajate, C., Gonzalez-Camacho, F., and Mollinedo, F. (2009) Involvement of raft aggregates enriched in Fas/CD95 death-inducing signaling complex in the antileukemic action of edelfosine in Jurkat cells. PLoS ONE 4, e5044
13. Gajate, C., and Mollinedo, F. (2001) The antitumor ether lipid ET-18- OCH3 induces apoptosis through translocation and capping of Fas/ CD95 into membrane rafts in human leukemic cells. Blood 98, 3860 -3863
14. Nieto-Miguel, T., Fonteriz, R. I., Vay, L., Gajate, C., López-Hernández, S., and Mollinedo, F. (2007) Endoplasmic reticulum stress in the proapoptotic action of edelfosine in solid tumor cells. Cancer Res. 67, 10368-10378 (Pubitemid 350070812)
15. Nieto-Miguel, T., Gajate, C., and Mollinedo, F. (2006) Differential targets and subcellular localization of antitumor alkyl-lysophospholipid in leukemic versus solid tumor cells. J. Biol. Chem. 281, 14833-14840 (Pubitemid 43855188)
16. Mollinedo, F. (2007) Antitumour ether lipids: proapoptotic agents with multiple therapeutic indications. Expert Opin. Ther. Patents 17, 385- 405 (Pubitemid 46567158)
17. Zaremberg, V., Gajate, C., Cacharro, L. M., Mollinedo, F., and McMaster, C. R. (2005) Cytotoxicity of an anti-cancer lysophospholipid through selective modification of lipid raft composition. J. Biol. Chem. 280, 38047-38058 (Pubitemid 41642419)
18. Hanson, P. K., Malone, L., Birchmore, J. L., and Nichols, J. W. (2003) Lem3p is essential for the uptake and potency of alkylphosphocholine drugs, edelfosine and miltefosine. J. Biol. Chem. 278, 36041-36050 (Pubitemid 37139924)
19. Bjornsti, M. A. (2002) Cancer therapeutics in yeast. Cancer Cell 2, 267-273
20. Foury, F. (1997) Human genetic diseases: a cross-talk between man and yeast. Gene 195, 1-10 (Pubitemid 27336954)
21. Mager, W. H., and Winderickx, J. (2005) Yeast as a model for medical and medicinal research. Trends Pharmacol. Sci. 26, 265-273 (Pubitemid 40603075)
22. Niedenthal, R. K., Riles, L., Johnston, M., and Hegemann, J. H. (1996) Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast 12, 773-786 (Pubitemid 26202365)
23. Han, G. S., O'Hara, L., Carman, G. M., and Siniossoglou, S. (2008) An unconventional diacylglycerol kinase that regulates phospholipid synthesis and nuclear membrane growth. J. Biol. Chem. 283, 20433-20442
24. Balguerie, A., Bagnat, M., Bonneu, M., Aigle, M., and Breton, A. M. (2002) Rvs161p and sphingolipids are required for actin repolarization following salt stress. Eukaryot. Cell 1, 1021-1031 (Pubitemid 36557722)
25. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691 (Pubitemid 37314307)
26. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29 (Pubitemid 30257031)
27. Robinson, M. D., Grigull, J., Mohammad, N., and Hughes, T. R. (2002) FunSpec: a web-based cluster interpreter for yeast.BMCBioinformatics 3, 35
28. Cherry, J. M., Adler, C., Ball, C., Chervitz, S. A., Dwight, S. S., Hester, E. T., Jia, Y., Juvik, G., Roe, T., Schroeder, M., Weng, S., and Botstein, D. (1998) SGD: Saccharomyces Genome Database. Nucleic Acids Res. 26, 73-79 (Pubitemid 28295265)
29. Quesada, E., Delgado, J., Gajate, C., Mollinedo, F., Acuña, A. U., and Amat- Guerri, F. (2004) Fluorescent phenylpolyene analogues of the ether phospholipid edelfosine for the selective labeling of cancer cells. J. Med. Chem. 47, 5333-5335 (Pubitemid 39382782)
30. Mollinedo, F., Fernández, M., Hornillos, V., Delgado, J., Amat-Guerri, F., Acuña, A. U., Nieto-Miguel, T., Villa-Pulgarín, J. A., González-García, C., Ceña, V., and Gajate, C. (2011) Involvement of lipid rafts in the localization and dysfunction effect of the antitumor ether phospholipid edelfosine in mitochondria. Cell Death Dis. 2, e158
31. Pomorski, T., Lombardi, R., Riezman, H., Devaux, P. F., van Meer, G., and Holthuis, J. C. (2003) Drs2p-related P-type ATPases Dnf1p and Dnf2p are required for phospholipid translocation across the yeast plasma membrane and serve a role in endocytosis. Mol. Biol. Cell 14, 1240 -1254 (Pubitemid 36337466)
32. Riekhof, W. R., Wu, J., Gijón, M. A., Zarini, S., Murphy, R. C., and Voelker, D. R. (2007) Lysophosphatidylcholine metabolism in Saccharomyces cerevisiae: the role of P-type ATPases in transport and a broad specificity acyltransferase in acylation. J. Biol. Chem. 282, 36853-36861
33. Aouida, M., Pagé, N., Leduc, A., Peter, M., and Ramotar, D. (2004) A genome-wide screen in Saccharomyces cerevisiae reveals altered transport as a mechanism of resistance to the anticancer drug bleomycin. Cancer Res. 64, 1102-1109 (Pubitemid 38176916)
34. Aouida, M., Poulin, R., and Ramotar, D. (2010) The human carnitine transporter SLC22A16 mediates high affinity uptake of the anticancer polyamine analogue bleomycin-A5. J. Biol. Chem. 285, 6275-6284
35. Raths, S., Rohrer, J., Crausaz, F., and Riezman, H. (1993) end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J. Cell Biol. 120, 55-65 (Pubitemid 23014066)
36. Shi, Y., Stefan, C. J., Rue, S. M., Teis, D., and Emr, S. D. (2011) Two novel WD40 domain-containing proteins, Ere1 and Ere2, function in the retromer- mediated endosomal recycling pathway. Mol. Biol. Cell 22, 4093-4107
37. Seaman, M. N., McCaffery, J. M., and Emr, S. D. (1998) A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol. 142, 665-681 (Pubitemid 28381486)
38. Hettema, E. H., Lewis, M. J., Black, M. W., and Pelham, H. R. (2003) Retromer and the sorting nexins Snx4/41/42 mediate distinct retrieval pathways from yeast endosomes. EMBO J. 22, 548-557 (Pubitemid 36193599)
39. Rojas, R., van Vlijmen, T., Mardones, G. A., Prabhu, Y., Rojas, A. L., Mohammed, S., Heck, A. J., Raposo, G., van der Sluijs, P., and Bonifacino, J. S. (2008) Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 183, 513-526
40. Conibear, E., and Stevens, T. H. (2000) Vps52p, Vps53p, and Vps54p form a novel multisubunit complex required for protein sorting at the yeast late Golgi. Mol. Biol. Cell 11, 305-323 (Pubitemid 30075525)
41. Katzmann, D. J., Babst, M., and Emr, S. D. (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155 (Pubitemid 32772626)
42. Bagnat, M., Chang, A., and Simons, K. (2001) Plasma membrane proton ATPase Pma1p requires raft association for surface delivery in yeast. Mol. Biol. Cell 12, 4129-4138 (Pubitemid 34001097)
43. Busto, J. V., Del Canto-Jañez, E., Goñi, F. M., Mollinedo, F., and Alonso, A. (2008) Combination of the anti-tumour cell ether lipid edelfosine with sterols abolishes haemolytic side effects of the drug. J. Chem. Biol. 1, 89-94
44. Ausili, A., Torrecillas, A., Aranda, F. J., Mollinedo, F., Gajate, C., Corbalán- García, S., de Godos, A., and Gómez- Fernández, J. C. (2008) Edelfosine is incorporated into rafts and alters their organization. J. Phys. Chem. B 112, 11643-11654
45. Luo, Wj., and Chang, A. (1997) Novel genes involved in endosomal traffic in yeast revealed by suppression of a targeting-defective plasma membrane ATPase mutant. J. Cell Biol. 138, 731-746 (Pubitemid 27365038)
46. Czyz, O., Bitew, T., Cuesta-Marbán, A., McMaster, C. R., Mollinedo, F., and Zaremberg, V. (2013) Alteration of plasma membrane organization by an anticancer lysophosphatidylcholine analogue induces intracellular acidification and internalization of plasma membrane transporters in yeast. J. Biol. Chem. 288, 8419-8432