Different modalities of intercellular membrane exchanges mediate cell-to-cell P-glycoprotein transfers in MCF-7 breast cancer cells

Journal of Biological Chemistry

Volumn 287, Issue 10, 2012, Pages 7374-7387

  Pasquier, Jennifer ^a,b   Galas, Ludovic ^b   Boulangé Lecomte, Céline ^a   Rioult, Damien ^a   Bultelle, Florence ^a   Magal, Pierre ^c   Webb, Glenn ^d   Le Foll, Frank ^a  

^a UNIVERSITÉ DU HAVRE   (France)

^b UNIVERSITY OF ROUEN   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; CONTROLLED DRUG DELIVERY; DISEASES; GLYCOPROTEINS; NANOTUBES;

CELLS INTERACTION; CHEMOTHERAPEUTIC DRUGS; DRUG EFFLUX PUMPS; EPIGENETIC MECHANISMS; INTERCELLULAR MEMBRANES; MCF-7 BREAST CANCER CELLS; MULTIDRUG RESISTANCE; SELECTION PRESSURES;

CELLS;

GLYCOPROTEIN P; NANOTUBE;

ARTICLE; BINDING AFFINITY; BINDING SITE; BREAST CANCER; CANCER CELL CULTURE; CELL DENSITY; CELL MEMBRANE TRANSPORT; CELL SUBPOPULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; INTERMETHOD COMPARISON; INTRACELLULAR TRANSPORT; MEMBRANE MICROPARTICLE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; WESTERN BLOTTING;

EID: 84857746017     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.312157     Document Type: Article

References (44)

1. Juliano, R. L., and Ling, V. (1976) A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta 455, 152-162
2. Pastan, I., and Gottesman, M. (1987) Multiple-drug resistance in human cancer. N. Engl. J. Med. 316, 1388-1393 (Pubitemid 17079683)
3. Ambudkar, S. V., Kimchi-Sarfaty, C., Sauna, Z. E., and Gottesman, M. M. (2003) P-glycoprotein. From genomics to mechanism. Oncogene 22, 7468-7485
4. Seelig, A., and Landwojtowicz, E. (2000) Structure-activity relationship of P-glycoprotein substrates and modifiers. Eur. J. Pharm. Sci. 12, 31-40
5. Rosenberg, M. F., Callaghan, R., Modok, S., Higgins, C. F., and Ford, R. C. (2005) Three-dimensional structure of P-glycoprotein. The transmembrane regions adopt an asymmetric configuration in the nucleotide-bound state. J. Biol. Chem. 280, 2857-2862 (Pubitemid 40189394)
6. Zhou, S. F. (2008) Structure, function, and regulation of P-glycoprotein and its clinical relevance in drug disposition. Xenobiotica 38, 802-832
7. Klimecki, W. T., Futscher, B. W., Grogan, T. M., and Dalton, W. S. (1994) P-glycoprotein expression and function in circulating blood cells from normal volunteers. Blood 83, 2451-2458 (Pubitemid 24135836)
8. Leslie, E. M., Deeley, R. G., and Cole, S. P. (2005) Multidrug resistance proteins. Role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 204, 216-237 (Pubitemid 40552845)
9. Mizutani, T., Masuda, M., Nakai, E., Furumiya, K., Togawa, H., Nakamura, Y., Kawai, Y., Nakahira, K., Shinkai, S., and Takahashi, K. (2008) Genuine functions of P-glycoprotein (ABCB1). Curr. Drug Metab. 9, 167-174 (Pubitemid 351461005)
10. Goldstein, L. J., Galski, H., Fojo, A., Willingham, M., Lai, S. L., Gazdar, A., Pirker, R., Green, A., Crist, W., and Brodeur, G. M. (1989) Expression of a multidrug resistance gene in human cancers. J. Natl. Cancer Inst. 81, 116-124 (Pubitemid 19031328)
11. Leighton, J. C., Jr., and Goldstein, L. J. (1995) P-glycoprotein in adult solid tumors. Expression and prognostic significance. Hematol. Oncol. Clin. North Am. 9, 251-273
12. Choi, C. H., Kim, H. S., Rha, H. S., Jeong, J. H., Park, Y. H., Min, Y. D., Kee, K. H., and Lim, D. Y. (1999) Drug concentration-dependent expression of multidrug resistance-associated protein and P-glycoprotein in the doxo-rubicin- resistant acute myelogenous leukemia sublines. Mol. Cells 9, 314-319
13. Nieth, C., and Lage, H. (2005) Induction of the ABC-transporters Mdr1/ P-gp (Abcb1), mrpl (Abcc1), and bcrp (Abcg2) during establishment of multidrug resistance after exposure to mitoxantrone. J. Chemother. 17, 215-223 (Pubitemid 40732883)
14. Meesungnoen, J., Jay-Gerin, J. P., and Mankhetkorn, S. (2002) Relation between MDR1 mRNA levels, resistance factor, and the efficiency of P-glycoprotein- mediated efflux of pirarubicin in multidrug-resistant K562 sublines. Can. J. Physiol. Pharmacol. 80, 1054-1063 (Pubitemid 36002662)
15. Riordan, J. R., Deuchars, K., Kartner, N., Alon, N., Trent, J., and Ling, V. (1985) Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature 316, 817-819 (Pubitemid 15003740)
16. Synold, T. W., Dussault, I., and Forman, B. M. (2001) The orphan nuclear receptor SXR coordinately regulates drug metabolism and efflux. Nat. Med. 7, 584-590 (Pubitemid 32448326)
17. Baker, E. K., Johnstone, R. W., Zalcberg, J. R., and El-Osta, A. (2005) Epigenetic changes to the MDR1 locus in response to chemotherapeutic drugs. Oncogene 24, 8061-8075 (Pubitemid 41746749)
18. Chekhun, V. F., Kulik, G. I., Yurchenko, O. V., Tryndyak, V. P., Todor, I. N., Luniv, L. S., Tregubova, N. A., Pryzimirska, T. V., Montgomery, B., Rusetskaya, N. V., and Pogribny, I. P. (2006) Role of DNA hypomethylation in the development of the resistance to doxorubicin in human MCF-7 breast adenocarcinoma cells. Cancer Lett. 231, 87-93 (Pubitemid 41779456)
19. Kovalchuk, O., Filkowski, J., Meservy, J., Ilnytskyy, Y., Tryndyak, V. P., Chekhun, V. F., and Pogribny, I. P. (2008) Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol. Cancer Ther. 7, 2152-2159
20. Reed, K., Hembruff, S. L., Laberge, M. L., Villeneuve, D. J., Côté, G. B., and Parissenti, A. M. (2008) Hypermethylation of the ABCB1 downstream gene promoter accompanies ABCB1 gene amplification and increased expression in docetaxel-resistant MCF-7 breast tumor cells. Epigenetics 3, 270-280
21. Fojo, T. (2007) Multiple paths to a drug resistance phenotype. Mutations, translocations, deletions, and amplification of coding genes or promoter regions, epigenetic changes, and microRNAs. Drug Resist. Updat. 10, 59-67
22. Callaghan, R., Crowley, E., Potter, S., and Kerr, I. D. (2008) P-glycoprotein. So many ways to turn it on. J. Clin. Pharmacol. 48, 365-378
23. Levchenko, A., Mehta, B. M., Niu, X., Kang, G., Villafania, L., Way, D., Polycarpe, D., Sadelain, M., and Larson, S. M. (2005) Intercellular transfer of P-glycoprotein mediates acquired multidrug resistance in tumor cells. Proc. Natl. Acad. Sci. U.S.A. 102, 1933-1938 (Pubitemid 40261990)
24. Rafii, A., Mirshahi, P., Poupot, M., Faussat, A. M., Simon, A., Ducros, E., Mery, E., Couderc, B., Lis, R., Capdet, J., Bergalet, J., Querleu, D., Dagonnet, F., Fournié, J. J., Marie, J. P., Pujade-Lauraine, E., Favre, G., Soria, J., and Mirshahi, M. (2008) Oncologic trogocytosis of an original stromal cells induces chemoresistance of ovarian tumors. PLoS One 3, e3894
25. Bebawy, M., Combes, V., Lee, E., Jaiswal, R., Gong, J., Bonhoure, A., and Grau, G. E. (2009) Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia 23, 1643-1649
26. Pasquier, J., Magal, P., Boulangé-Lecomte, C., Webb, G., and Le Foll, F. (2011) Consequences of cell-to-cell P-glycoprotein transfer on acquired multidrug resistance in breast cancer. A cell population dynamics model. Biol. Direct 6, 5
27. - channels in multidrug-resistant MCF7 cells. Biochem. Biophys. Res. Commun. 334, 1266-1278
28. Shedden, K., Xie, X. T., Chandaroy, P., Chang, Y. T., and Rosania, G. R. (2003) Expulsion of small molecules in vesicles shed by cancer cells. Association with gene expression and chemosensitivity profiles. Cancer Res. 63, 4331-4337 (Pubitemid 36950999)
29. Théry, C., Amigorena, S., Raposo, G., and Clayton, A. (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. 30, 3.22.1-3.22.29
30. Rustom, A., Saffrich, R., Markovic, I., Walther, P., and Gerdes, H. H. (2004) Nanotubular highways for intercellular organelle transport. Science 303, 1007-1010 (Pubitemid 38209703)
31. Gurke, S., Barroso, J. F., and Gerdes, H. H. (2008) The art of cellular communication. Tunneling nanotubes bridge the divide. Histochem Cell Biol. 129, 539-550
32. Gerdes, H. H., and Carvalho, R. N. (2008) Intercellular transfer mediated by tunneling nanotubes. Curr. Opin. Cell Biol. 20, 470-475
33. Oleinikov, V. A., Fleury, F., Ianoul, A., Zaitsev, S., and Nabiev, I. (2006) P-glycoprotein effect on the properties of its natural lipid environment probed by Raman spectroscopy and Langmuir-Blodgett technique. FEBS Lett. 580, 4953-4958 (Pubitemid 44286836)
34. Demeule, M., Brossard, M., and Béliveau, R. (1999) Cisplatin induces renal expression of P-glycoprotein and canalicular multispecific organic anion transporter. Am. J. Physiol. 277, F832-F840 (Pubitemid 30046057)
35. Geick, A., Eichelbaum, M., and Burk, O. (2001) Nuclear receptor response elements mediate induction of intestinal MDR1 by rifampin. J. Biol. Chem. 276, 14581-14587
36. Pajic, M., Bebawy, M., Hoskins, J. M., Roufogalis, B. D., and Rivory, L. P. (2004) Effect of short term morphine exposure on P-glycoprotein expression and activity in cancer cell lines. Oncol. Rep. 11, 1091-1095
37. Belli, J. A., Zhang, Y., and Fritz, P. (1990) Transfer of adriamycin resistance by fusion of Mr 170,000 P-glycoprotein to the plasma membrane of sensitive cells. Cancer Res. 50, 2191-2197 (Pubitemid 20115098)
38. Théry, C., Ostrowski, M., and Segura, E. (2009) Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581-593
39. Staubach, S., Razawi, H., and Hanisch, F. G. (2009) Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 9, 2820-2835
40. Simpson, R. J., Jensen, S. S., and Lim, J. W. (2008) Proteomic profiling of exosomes. Current perspectives. Proteomics 8, 4083-4099
41. Safaei, R., Larson, B. J., Cheng, T. C., Gibson, M. A., Otani, S., Naerdemann, W., and Howell, S. B. (2005) Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol. Cancer Ther. 4, 1595-1604 (Pubitemid 41556443)
42. Gottesman, M. M., Hrycyna, C. A., Schoenlein, P. V., Germann, U. A., and Pastan, I. (1995) Genetic analysis of the multidrug transporter. Annu. Rev. Genet. 29, 607-649 (Pubitemid 26005354)
43. Hawkins, B. T., Sykes, D. B., and Miller, D. S. (2010) Rapid, reversible modulation of blood-brain barrier P-glycoprotein transport activity by vascular endothelial growth factor. J. Neurosci. 30, 1417-1425
44. Hawkins, B. T., Rigor, R. R., and Miller, D. S. (2010) Rapid loss of bloodbrain barrier P-glycoprotein activity through transporter internalization demonstrated using a novel in situ proteolysis protection assay. J. Cereb. Blood Flow Metab. 30, 1593-1597