Alteration of plasma membrane organization by an anticancer lysophosphatidylcholine analogue induces intracellular acidification and internalization of plasma membrane transporters in yeast

Journal of Biological Chemistry

Volumn 288, Issue 12, 2013, Pages 8419-8432

  Czyz, Ola ^a   Bitew, Teshager ^a   Cuesta Marbán, Alvaro ^b   McMaster, Christopher R ^c   Mollinedo, Faustino ^b   Zaremberg, Vanina ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b CSIC   (Spain)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIFICATION; CELL DEATH; CELL PROLIFERATION; YEAST;

CELLULAR MEMBRANES; CYTOTOXIC EFFECTS; ENDOPLASMIC RETICULUM; LATERAL SEGREGATION; LYSOPHOSPHATIDYL-CHOLINE; MODE OF ACTION; PH HOMEOSTASIS; SELECTIVE MODIFICATION;

CELL MEMBRANES;

CARRIER PROTEIN; EDELFOSINE; LYSOPHOSPHATIDYLCHOLINE; PROTON PUMP; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ACIDIFICATION; ARTICLE; CELL GROWTH; CELL MEMBRANE; CELL PH; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG RESISTANCE; DRUG SELECTIVITY; DRUG TARGETING; ENDOPLASMIC RETICULUM; INTERNALIZATION; LIPID RAFT; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; UBIQUITINATION;

SACCHAROMYCES CEREVISIAE;

EID: 84875442887     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.425744     Document Type: Article

References (69)

1. Simons, K., and Gerl, M. J. (2010) Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 11, 688-699
2. Simons, K., and Toomre, D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39
3. Simons, K., and Sampaio, J. L. (2011) Cold Spring Harbor Perspect. Biol. 3, 1-17
4. 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
5. Wright, M. M., Howe, A. G., and Zaremberg, V. (2004) Cell membranes and apoptosis: role of cardiolipin, phosphatidylcholine, and anticancer lipid analogues. Biochem. Cell Biol. 82, 18-26 (Pubitemid 38580871)
6. 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)
7. Bitew, T., Sveen, C. E., Heyne, B., and Zaremberg, V. (2010) Vitamin E prevents lipid raft modifications induced by an anti-cancer lysophospholipid and abolishes a Yap1-mediated stress response in yeast. J. Biol. Chem. 285, 25731-25742
8. Gajate, C., and Mollinedo, F. (2001) The antitumor ether lipid ET-18- OCH(3) induces apoptosis through translocation and capping of Fas/ CD95 into membrane rafts in human leukemic cells. Blood 98, 3860-3863
9. 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)
10. 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)
11. 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)
12. 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
13. Boggs, K. P., Rock, C. O., and Jackowski, S. (1995) Lysophosphatidylcholine and 1-O-octadecyl-2-O-methyl-rac-glycero-3- phosphocholine inhibit the CDP-choline pathway of phosphatidylcholine synthesis at the CTP:phosphocholine cytidylyltransferase step. J. Biol. Chem. 270, 7757-7764
14. Boggs, K. P., Rock, C. O., and Jackowski, S. (1995) Lysophosphatidylcholine attenuates the cytotoxic effects of the antineoplastic phospholipid 1-O-octadecyl-2-O-methyl-rac-glycero-3-phosphocholine. J. Biol. Chem. 270, 11612-11618
15. 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-X(L). Cancer Res. 57, 1320-1328 (Pubitemid 27152558)
16. 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)
17. Gajate, C., and Mollinedo, F. (2002) Biological activities, mechanisms of action, and biomedical prospect of the antitumor ether phospholipid ET- 18-OCH(3) (edelfosine), a proapoptotic agent in tumor cells. Curr. Drug Metab. 3, 491-525 (Pubitemid 34987482)
18. 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)
19. 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)
20. Pomorski, T., Holthuis, J. C., Herrmann, A., and van Meer, G. (2004) Tracking down lipid flippases and their biological functions. J. Cell Sci. 117, 805-813 (Pubitemid 38386939)
21. Chen, R., Brady, E., and McIntyre, T. M. (2011) Human TMEM30a promotes uptake of antitumor and bioactive choline phospholipids into mammalian cells. J. Immunol. 186, 3215-3225
22. Winzeler, E. A., Shoemaker, D. D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J. D., Bussey, H., Chu, A. M., Connelly, C., Davis, K., Dietrich, F., Dow, S. W., El Bakkoury, M., Foury, F., Friend, S. H., Gentalen, E., Giaever, G., Hegemann, J. H., Jones, T., Laub, M., Liao, H., Liebundguth, N., Lockhart, D. J., Lucau-Danila, A., Lussier, M., M'Rabet, N., Menard, P., Mittmann, M., Pai, C., Rebischung, C., Revuelta, J. L., Riles, L., Roberts, C. J., Ross-MacDonald, P., Scherens, B., Snyder, M., Sookhai-Mahadeo, S., Storms, R. K., Véronneau, S., Voet, M., Volckaert, G., Ward, T. R., Wysocki, R., Yen, G. S., Yu, K., Zimmermann, K., Philippsen, P., Johnston, M., and Davis, R. W. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906 (Pubitemid 29381993)
23. Giaever, G., Chu, A. M., Ni, L., Connelly, C., Riles, L., Véronneau, S., Dow, S., Lucau-Danila, A., Anderson, K., André, B., Arkin, A. P., Astromoff, A., El-Bakkoury, M., Bangham, R., Benito, R., Brachat, S., Campanaro, S., Curtiss, M., Davis, K., Deutschbauer, A., Entian, K. D., Flaherty, P., Foury, F., Garfinkel, D. J., Gerstein, M., Gotte, D., Güldener, U., Hegemann, J. H., Hempel, S., Herman, Z., Jaramillo, D. F., Kelly, D. E., Kelly, S. L., Kötter, P., LaBonte, D., Lamb, D. C., Lan, N., Liang, H., Liao, H., Liu, L., Luo, C., Lussier, M., Mao, R., Menard, P., Ooi, S. L., Revuelta, J. L., Roberts, C. J., Rose, M., Ross-Macdonald, P., Scherens, B., Schimmack, G., Shafer, B., Shoemaker, D. D., Sookhai-Mahadeo, S., Storms, R. K., Strathern, J. N., Valle, G., Voet, M., Volckaert, G., Wang, C. Y., Ward, T. R., Wilhelmy, J., Winzeler, E. A., Yang, Y. H., Yen, G., Youngman, E., Yu, K. X., Bussey, H., Boeke, J. D., Snyder, M., Philippsen, P., Davis, R. W., and Johnston, M. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387-391 (Pubitemid 34826834)
24. Fyrst, H., Oskouian, B., Kuypers, F. A., and Saba, J. D. (1999) The PLB2 gene of Saccharomyces cerevisiae confers resistance to lysophosphatidylcholine and encodes a phospholipase B/lysophospholipase. Biochemistry 38, 5864-5871
25. Zaremberg, V., and McMaster, C. R. (2002) Differential partitioning of lipids metabolized by separate yeast glycerol-3-phosphate acyltransferases reveals that phospholipase D generation of phosphatidic acid mediates sensitivity to choline-containing lysolipids and drugs. J. Biol. Chem. 277, 39035-39044 (Pubitemid 35154770)
26. Fairn, G. D., and McMaster, C. R. (2005) Studying phospholipid metabolism using yeast systematic and chemical genetics. Methods 36, 102-108 (Pubitemid 40726142)
27. Breitkreutz, B. J., Stark, C., and Tyers, M. (2003) Osprey: a network visualization system. Genome Biol. 4, R22
28. Robinson, M. D., Grigull, J., Mohammad, N., and Hughes, T. R. (2002) FunSpec: a web-based cluster interpreter for yeast. BMC Bioinformatics 3, 35
29. Orij, R., Postmus, J., Ter Beek, A., Brul, S., and Smits, G. J. (2009) In vivo measurement of cytosolic and mitochondrial pH using a pH-sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiology 155, 268-278
30. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275
31. Graham, L. A., Hill, K. J., and Stevens, T. H. (1998) Assembly of the yeast vacuolar H-ATPase occurs in the endoplasmic reticulum and requires a Vma12p/Vma22p assembly complex. J. Cell Biol. 142, 39-49
32. Martínez-Muñoz, G. A., and Kane, P. (2008) Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast. J. Biol. Chem. 283, 20309-20319
33. Yenush, L., Merchan, S., Holmes, J., and Serrano, R. (2005) pH-responsive, posttranslational regulation of the Trk1 potassium transporter by the type 1-related Ppz1 phosphatase. Mol. Cell. Biol. 25, 8683-8692 (Pubitemid 41369186)
34. Young, B. P., Shin, J. J., Orij, R., Chao, J. T., Li, S. C., Guan, X. L., Khong, A., Jan, E., Wenk, M. R., Prinz, W. A., Smits, G. J., and Loewen, C. J. (2010) Phosphatidic acid is a pH biosensor that links membrane biogenesis to metabolism. Science 329, 1085-1088
35. Zhang, J., Vemuri, G., and Nielsen, J. (2010) Systems biology of energy homeostasis in yeast. Curr. Opin. Microbiol. 13, 382-388
36. Portillo, F., Mulet, J. M., and Serrano, R. (2005) A role for the non-phosphorylated form of yeast Snf1: tolerance to toxic cations and activation of potassium transport. FEBS Lett. 579, 512-516 (Pubitemid 40092436)
37. Ariño, J., Ramos, J., and Sychrová, H. (2010) Alkali metal cation transport and homeostasis in yeasts. Microbiol. Mol. Biol. Rev. 74, 95-120
38. Casamayor, A., Serrano, R., Platara, M., Casado, C., Ruiz, A., and Ariño, J. (2012) The role of the Snf1 kinase in the adaptive response of Saccharomyces cerevisiae to alkaline pH stress. Biochem. J. 444, 39-49
39. Schuldiner, M., Collins, S. R., Thompson, N. J., Denic, V., Bhamidipati, A., Punna, T., Ihmels, J., Andrews, B., Boone, C., Greenblatt, J. F., Weissman, J. S., and Krogan, N. J. (2005) Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123, 507-519 (Pubitemid 41546679)
40. Orij, R., Brul, S., and Smits, G. J. (2011) Intracellular pH is a tightly controlled signal in yeast. Biochim. Biophys. Acta 1810, 933-944
41. Orij, R., Urbanus, M. L., Vizeacoumar, F. J., Giaever, G., Boone, C., Nislow, C., Brul, S., and Smits, G. J. (2012) Genome-wide analysis of intracellular pH reveals quantitative control of cell division rate by pH(c) in Saccharomyces cerevisiae. Genome Biol. 13, R80
42. Carmelo, V., Bogaerts, P., and Sá-Correia, I. (1996) Activity of plasma membrane H-ATPase and expression of PMA1 and PMA2 genes in Saccharomyces cerevisiae cells grown at optimal and low pH. Arch. Microbiol. 166, 315-320
43. 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)
44. Pizzirusso, M., and Chang, A. (2004) Ubiquitin-mediated targeting of a mutant plasma membrane ATPase, Pma1-7, to the endosomal/vacuolar system in yeast. Mol. Biol. Cell 15, 2401-2409 (Pubitemid 38580655)
45. Spira, F., Mueller, N. S., Beck, G., von Olshausen, P., Beig, J., and Wedlich- Söldner, R. (2012) Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat. Cell Biol. 14, 640-648
46. Ziółkowska, N. E., Christiano, R., and Walther, T. C. (2012) Organized living: formation mechanisms and functions of plasma membrane domains in yeast. Trends Cell Biol. 22, 151-158
47. Malínská, K., Malínský, J., Opekarová, M., and Tanner, W. (2003) Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol. Biol. Cell 14, 4427-4436 (Pubitemid 37444645)
48. Olivera-Couto, A., and Aguilar, P. S. (2012) Eisosomes and plasma membrane organization. Mol. Genet. Genomics 287, 607-620
49. Bagnat, M., Keränen, S., Shevchenko, A., Shevchenko, A., and Simons, K. (2000) Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. U.S.A. 97, 3254-3259 (Pubitemid 30183288)
50. Lauwers, E., and André, B. (2006) Association of yeast transporters with detergent-resistant membranes correlates with their cell-surface location. Traffic 7, 1045-1059
51. Surma, M. A., Klose, C., and Simons, K. (2012) Lipid-dependent protein sorting at the trans-Golgi network. Biochim. Biophys. Acta 1821, 1059-1067
52. Marchal, C., Haguenauer-Tsapis, R., and Urban-Grimal, D. (1998) A PEST-like sequence mediates phosphorylation and efficient ubiquitination of yeast uracil permease. Mol. Cell. Biol. 18, 314-321 (Pubitemid 28021042)
53. Stringer, D. K., and Piper, R. C. (2011) A single ubiquitin is sufficient for cargo protein entry into MVBs in the absence of ESCRT ubiquitination. J. Cell Biol. 192, 229-242
54. Huang, C., and Chang, A. (2011) pH-dependent cargo sorting from the Golgi. J. Biol. Chem. 286, 10058-10065
55. Brett, C. L., Kallay, L., Hua, Z., Green, R., Chyou, A., Zhang, Y., Graham, T. R., Donowitz, M., and Rao, R. (2011) Genome-wide analysis reveals the vacuolar pH-stat of Saccharomyces cerevisiae. PLoS One 6, e17619
56. Baumann, N. A., Sullivan, D. P., Ohvo-Rekilä, H., Simonot, C., Pottekat, A., Klaassen, Z., Beh, C. T., and Menon, A. K. (2005) Transport of newly synthesized sterol to the sterol-enriched plasma membrane occurs via nonvesicular equilibration. Biochemistry 44, 5816-5826 (Pubitemid 40525118)
57. Hac-Wydro, K., Dynarowicz-Łatka, P., Wydro, P., and Bak, K. (2011) Edelfosine disturbs the sphingomyelin-cholesterol model membrane system in a cholesterol-dependent way-the Langmuir monolayer study. Colloids Surf. B Biointerfaces 88, 635-640
58. Grossmann, G., Opekarová, M., Malinsky, J., Weig-Meckl, I., and Tanner, W. (2007) Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J. 26, 1-8 (Pubitemid 46094694)
59. Grossmann, G., Malinsky, J., Stahlschmidt, W., Loibl, M., Weig-Meckl, I., Frommer, W. B., Opekarová, M., and Tanner, W. (2008) Plasma membrane microdomains regulate turnover of transport proteins in yeast. J. Cell Biol. 183, 1075-1088
60. Blondel, M. O., Morvan, J., Dupré, S., Urban-Grimal, D., Haguenauer- Tsapis, R., and Volland, C. (2004) Direct sorting of the yeast uracil permease to the endosomal system is controlled by uracil binding and Rsp5pdependent ubiquitylation. Mol. Biol. Cell 15, 883-895 (Pubitemid 38146501)
61. Nikko, E., and Pelham, H. R. (2009) Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic 10, 1856-1867
62. Novoselova, T. V., Zahira, K., Rose, R. S., and Sullivan, J. A. (2012) Bul proteins, a nonredundant, antagonistic family of ubiquitin ligase regulatory proteins. Eukaryot. Cell 11, 463-470
63. Lauwers, E., Erpapazoglou, Z., Haguenauer-Tsapis, R., and André, B. (2010) The ubiquitin code of yeast permease trafficking. Trends Cell Biol. 20, 196-204
64. Kamińska, J., Tobiasz, A., Gniewosz, M., and Zoładek, T. (2000) The growth of mdp1/rsp5 mutants of Saccharomyces cerevisiae is affected by mutations in the ATP-binding domain of the plasma membrane H- ATPase. Gene 242, 133-140 (Pubitemid 30064498)
65. Vincent, O., Townley, R., Kuchin, S., and Carlson, M. (2001) Subcellular localization of the Snf1 kinase is regulated by specific - subunits and a novel glucose signaling mechanism. Genes Dev. 15, 1104-1114
66. Serrano, R., Bernal, D., Simón, E., and Ariño, J. (2004) Copper and iron are the limiting factors for growth of the yeast Saccharomyces cerevisiae in an alkaline environment. J. Biol. Chem. 279, 19698-19704 (Pubitemid 38623407)
67. Zhang, Y. Q., Gamarra, S., Garcia-Effron, G., Park, S., Perlin, D. S., and Rao, R. (2010) Requirement for ergosterol in V-ATPase function underlies antifungal activity of azole drugs. Plos Pathog. 6, e1000939
68. Walther, T. C., Brickner, J. H., Aguilar, P. S., Bernales, S., Pantoja, C., and Walter, P. (2006) Eisosomes mark static sites of endocytosis. Nature 439, 998-1003 (Pubitemid 43292420)
69. Cuesta-Marbán, Á ., Botet, J., Czyz, O., Cacharro, L. M., Gajate, C., Hornillos, V., Delgado, J., Zhang, H., Amat-Guerri, F., Acuña, A. U., McMaster, C. R., Revuelta, J. L., Zaremberg, V., and Mollinedo, F. (2013) Drug uptake, lipid rafts, and vesicle trafficking modulate resistance to an anticancer lysophosphatidylcholine analogue in yeast. J. Biol. Chem. 288, 8405- 8418