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BioMed Research International
Volume 2015, Article ID 821613, 9 pages
http://dx.doi.org/10.1155/2015/821613
Review Article

Role of Extracellular Vesicles in Hematological Malignancies

1Dipartimento di Biopatologia e Biotecnologie Mediche, Università degli Studi di Palermo, Sezione di Biologia e Genetica, Via Divisi 83, 90133 Palermo, Italy
2Laboratorio di Ingegneria Tissutale-Piattaforme Innovative per l’Ingegneria Tessutale (PON01-00829), Istituto Ortopedico Rizzoli, 90133 Palermo, Italy
3Institute of Biomedicine and Molecular Immunology (IBIM), National Research Council of Italy, 90146 Palermo, Italy

Received 27 January 2015; Accepted 13 April 2015

Academic Editor: Martin Bornhaeuser

Copyright © 2015 Stefania Raimondo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Skog, T. Würdinger, S. van Rijn et al., “Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers,” Nature Cell Biology, vol. 10, no. 12, pp. 1470–1476, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Théry, M. Ostrowski, and E. Segura, “Membrane vesicles as conveyors of immune responses,” Nature Reviews Immunology, vol. 9, no. 8, pp. 581–593, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. H. F. G. Heijnen, A. E. Schiel, R. Fijnheer, H. J. Geuze, and J. J. Sixma, “Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and α-granules,” Blood, vol. 94, no. 11, pp. 3791–3799, 1999. View at Google Scholar · View at Scopus
  4. G. Raposo, H. W. Nijman, W. Stoorvogel et al., “B lymphocytes secrete antigen-presenting vesicles,” Journal of Experimental Medicine, vol. 183, no. 3, pp. 1161–1172, 1996. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Savina, C. M. Fader, M. T. Damiani, and M. I. Colombo, “Rab11 promotes docking and fusion of multivesicular bodies in a calcium-dependent manner,” Traffic, vol. 6, no. 2, pp. 131–143, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Ostrowski, N. B. Carmo, S. Krumeich et al., “Rab27a and Rab27b control different steps of the exosome secretion pathway,” Nature Cell Biology, vol. 12, supplement, pp. 19–30, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Hsu, Y. Morohashi, S.-I. Yoshimura et al., “Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C,” The Journal of Cell Biology, vol. 189, no. 2, pp. 223–232, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. M. F. Baietti, Z. Zhang, E. Mortier et al., “Syndecan-syntenin-ALIX regulates the biogenesis of exosomes,” Nature Cell Biology, vol. 14, no. 7, pp. 677–685, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Théry, M. Boussac, P. Véron et al., “Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles,” Journal of Immunology, vol. 166, no. 12, pp. 7309–7318, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Crescitelli, C. Lässer, T. G. Szabó et al., “Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes,” Journal of Extracellular Vesicles, vol. 2, 2013. View at Publisher · View at Google Scholar
  11. F. Andre, N. E. C. Schartz, M. Movassagh et al., “Malignant effusions and immunogenic tumour-derived exosomes,” The Lancet, vol. 360, no. 9329, pp. 295–305, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand, J. J. Lee, and J. O. Lötvall, “Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells,” Nature Cell Biology, vol. 9, no. 6, pp. 654–659, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Clayton, A. Turkes, S. Dewitt, R. Steadman, M. D. Mason, and M. B. Hallett, “Adhesion and signaling by B cell-derived exosomes: the role of integrins,” The FASEB Journal, vol. 18, no. 9, pp. 977–979, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. A. E. Morelli, A. T. Larregina, W. J. Shufesky et al., “Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells,” Blood, vol. 104, no. 10, pp. 3257–3266, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. K. Al-Nedawi, B. Meehan, J. Micallef et al., “Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells,” Nature Cell Biology, vol. 10, no. 5, pp. 619–624, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Zhang, D. Liu, X. Chen et al., “Secreted monocytic miR-150 enhances targeted endothelial cell migration,” Molecular Cell, vol. 39, no. 1, pp. 133–144, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Cocucci, G. Racchetti, and J. Meldolesi, “Shedding microvesicles: artefacts no more,” Trends in Cell Biology, vol. 19, no. 2, pp. 43–51, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. E. Pap, É. Pállinger, M. Pásztói, and A. Falus, “Highlights of a new type of intercellular communication: microvesicle-based information transfer,” Inflammation Research, vol. 58, no. 1, pp. 1–8, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Corrado, S. Raimondo, A. Chiesi, F. Ciccia, G. De Leo, and R. Alessandro, “Exosomes as intercellular signaling organelles involved in health and disease: basic science and clinical applications,” International Journal of Molecular Sciences, vol. 14, no. 3, pp. 5338–5366, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. M. A. Antonyak, B. Li, L. K. Boroughs et al., “Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 12, pp. 4852–4857, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Peinado, M. Alečković, S. Lavotshkin et al., “Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET,” Nature Medicine, vol. 18, no. 6, pp. 883–891, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Melo, H. Sugimoto, J. O’Connell et al., “Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis,” Cancer Cell, vol. 26, no. 5, pp. 707–721, 2014. View at Publisher · View at Google Scholar
  23. J. M. Brown and W. R. Wilson, “Exploiting tumour hypoxia in cancer treatment,” Nature Reviews Cancer, vol. 4, no. 6, pp. 437–447, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. S. M. Evans, K. D. Judy, I. Dunphy et al., “Hypoxia is important in the biology and aggression of human glial brain tumors,” Clinical Cancer Research, vol. 10, no. 24, pp. 8177–8184, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. L. S. Ziemer, C. J. Koch, A. Maity, D. P. Magarelli, A. M. Horan, and S. M. Evans, “Hypoxia and VEGF mRNA expression in human tumors,” Neoplasia, vol. 3, no. 6, pp. 500–508, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. A. B. Scandurro, C. W. Weldon, Y. G. Figueroa, J. Alam, and B. S. Beckman, “Gene microarray analysis reveals a novel hypoxia signal transduction pathway in human hepatocellular carcinoma cells,” International journal of oncology, vol. 19, no. 1, pp. 129–135, 2001. View at Google Scholar · View at Scopus
  27. H. W. King, M. Z. Michael, and J. M. Gleadle, “Hypoxic enhancement of exosome release by breast cancer cells,” BMC Cancer, vol. 12, article 421, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Salomon, J. Ryan, L. Sobrevia et al., “Exosomal signaling during hypoxia mediates microvascular endothelial cell migration and vasculogenesis,” PLoS ONE, vol. 8, no. 7, Article ID e68451, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Kucharzewska, H. C. Christianson, J. E. Welch et al., “Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 18, pp. 7312–7317, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. M. J. Bissell and W. C. Hines, “Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression,” Nature Medicine, vol. 17, no. 3, pp. 320–329, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. V. Muralidharan-Chari, J. W. Clancy, A. Sedgwick, and C. D'Souza-Schorey, “Microvesicles: mediators of extracellular communication during cancer progression,” Journal of Cell Science, vol. 123, no. 10, pp. 1603–1611, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. I. Nazarenko, S. Rana, A. Baumann et al., “Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation,” Cancer Research, vol. 70, no. 4, pp. 1668–1678, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. J. M. Aliotta, M. Pereira, K. W. Johnson et al., “Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription,” Experimental Hematology, vol. 38, no. 3, pp. 233–245, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Peinado, S. Lavotshkin, and D. Lyden, “The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts,” Seminars in Cancer Biology, vol. 21, no. 2, pp. 139–146, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Huan, N. Hornick, A. Skinner, N. Goloviznina, C. Roberts, and P. Kurre, “RNA trafficking by acute myelogenous leukemia exosomes,” Cancer Research, vol. 73, no. 2, pp. 918–929, 2013. View at Publisher · View at Google Scholar
  36. C. Corrado, S. Raimondo, L. Saieva, A. M. Flugy, G. de Leo, and R. Alessandro, “Exosome-mediated crosstalk between chronic myelogenous leukemia cells and human bone marrow stromal cells triggers an Interleukin 8-dependent survival of leukemia cells,” Cancer Letters, vol. 348, no. 1-2, pp. 71–76, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. A. K. Ghosh, C. R. Secreto, T. R. Knox, W. Ding, D. Mukhopadhyay, and N. E. Kay, “Circulating microvesicles in B-cell chronic lymphocytic leukemia can stimulate marrow stromal cells: implications for disease progression,” Blood, vol. 115, no. 9, pp. 1755–1764, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Cai, Y. Han, H. Ren et al., “Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells,” Journal of Molecular Cell Biology, vol. 5, no. 4, pp. 227–238, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Cai, G. Wu, X. Tan et al., “Transferred BCR/ABL DNA from K562 extracellular vesicles causes chronic myeloid leukemia in immunodeficient mice,” PLoS ONE, vol. 9, no. 8, Article ID e105200, 2014. View at Google Scholar
  40. K. E. de Visser, A. Eichten, and L. M. Coussens, “Paradoxical roles of the immune system during cancer development,” Nature Reviews Cancer, vol. 6, no. 1, pp. 24–37, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. A. S. Azmi, B. Bao, and F. H. Sarkar, “Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review,” Cancer and Metastasis Reviews, vol. 32, no. 3-4, pp. 623–642, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Hedlund, O. Nagaeva, D. Kargl, V. Baranov, and L. Mincheva-Nilsson, “Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells,” PLoS ONE, vol. 6, no. 2, Article ID e16899, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. H.-C. Zhang, X.-B. Liu, S. Huang et al., “Microvesicles derived from human umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo,” Stem Cells and Development, vol. 21, no. 18, pp. 3289–3297, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. A. M. Roccaro, A. Sacco, P. Maiso et al., “BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression,” The Journal of Clinical Investigation, vol. 123, no. 4, pp. 1542–1555, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. Y.-T. Ding, S. Kumar, and D.-C. Yu, “The role of endothelial progenitor cells in tumour vasculogenesis,” Pathobiology, vol. 75, no. 5, pp. 265–273, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. G. Taraboletti, S. D'Ascenzo, I. Giusti et al., “Bioavailability of VEGF in tumor-shed vesicles depends on vesicle burst induced by acidic pH 1,” Neoplasia, vol. 8, no. 2, pp. 96–103, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Trujillo, C. McGee, and C. R. Cogle, “Angiogenesis in acute myeloid leukemia and opportunities for novel therapies,” Journal of Oncology, vol. 2012, Article ID 128608, 9 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. N. Giuliani, P. Storti, M. Bolzoni, B. D. Palma, and S. Bonomini, “Angiogenesis and multiple myeloma,” Cancer Microenvironment, vol. 4, no. 3, pp. 325–337, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Letilovic, R. Vrhovac, S. Verstovsek, B. Jaksic, and A. Ferrajoli, “Role of angiogenesis in chronic lymphocytic leukemia,” Cancer, vol. 107, no. 5, pp. 925–934, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Marinaccio, B. Nico, E. Maiorano, G. Specchia, and D. Ribatti, “Insights in Hodgkin Lymphoma angiogenesis,” Leukemia Research, vol. 38, no. 8, pp. 857–861, 2014. View at Publisher · View at Google Scholar
  51. H. F. S. Negaard, N. Iversen, I. M. Bowitz-Lothe et al., “Increased bone marrow microvascular density in haematological malignancies is associated with differential regulation of angiogenic factors,” Leukemia, vol. 23, no. 1, pp. 162–169, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Taverna, A. Flugy, L. Saieva et al., “Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis,” International Journal of Cancer, vol. 130, no. 9, pp. 2033–2043, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Corrado, A. M. Flugy, S. Taverna et al., “Carboxyamidotriazole-orotate inhibits the growth of imatinib-resistant chronic myeloid leukaemia cells and modulates exosomes-stimulated angiogenesis,” PLoS ONE, vol. 7, no. 8, Article ID e42310, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Mineo, S. H. Garfield, S. Taverna et al., “Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion,” Angiogenesis, vol. 15, no. 1, pp. 33–45, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Wittmann and H.-M. Jäck, “Serum microRNAs as powerful cancer biomarkers,” Biochimica et Biophysica Acta—Reviews on Cancer, vol. 1806, no. 2, pp. 200–207, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Taverna, V. Amodeo, L. Saieva et al., “Exosomal shuttling of miR-126 in endothelial cells modulates adhesive and migratory abilities of chronic myelogenous leukemia cells,” Molecular Cancer, vol. 13, no. 1, article 169, 2014. View at Publisher · View at Google Scholar
  57. T. Umezu, K. Ohyashiki, M. Kuroda, and J. H. Ohyashiki, “Leukemia cell to endothelial cell communication via exosomal miRNAs,” Oncogene, vol. 32, no. 22, pp. 2747–2755, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. H. Tadokoro, T. Umezu, K. Ohyashiki, T. Hirano, and J. H. Ohyashiki, “Exosomes derived from hypoxic leukemia cells enhance tube formation in endothelial cells,” The Journal of Biological Chemistry, vol. 288, no. 48, pp. 34343–34351, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. J. E. Park, H. S. Tan, A. Datta et al., “Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes,” Molecular and Cellular Proteomics, vol. 9, no. 6, pp. 1085–1099, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Umezu, H. Tadokoro, K. Azuma, S. Yoshizawa, K. Ohyashiki, and J. H. Ohyashiki, “Exosomal miR-135b shed from hypoxic multiple myeloma cells enhances angiogenesis by targeting factor-inhibiting HIF-1,” Blood, vol. 124, no. 25, pp. 3748–3757, 2014. View at Publisher · View at Google Scholar
  61. Y. Liu, X.-J. Zhu, C. Zeng et al., “Microvesicles secreted from human multiple myeloma cells promote angiogenesis,” Acta Pharmacologica Sinica, vol. 35, no. 2, pp. 230–238, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. J. A. Tickner, A. J. Urquhart, S. A. Stephenson, D. J. Richard, and K. J. O'Byrne, “Functions and therapeutic roles of exosomes in cancer,” Frontiers in Oncology, vol. 4, article 127, 2014. View at Publisher · View at Google Scholar
  63. M. J. Szczepanski, M. Szajnik, A. Welsh, T. L. Whiteside, and M. Boyiadzis, “Blast-derived microvesicles in sera from patients with acute myeloid leukemia suppress natural killer cell function via membrane-associated transforming growth factor-beta1,” Haematologica, vol. 96, no. 9, pp. 1302–1309, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. F. F. van Doormaal, A. Kleinjan, M. Di Nisio, H. R. Büller, and R. Nieuwland, “Cell-derived microvesicles and cancer,” Netherlands Journal of Medicine, vol. 67, no. 7, pp. 266–273, 2009. View at Google Scholar · View at Scopus
  65. D. Zocco, P. Ferruzzi, F. Cappello, W. P. Kuo, and S. Fais, “Extracellular vesicles as shuttles of tumor biomarkers and anti-tumor drugs,” Frontiers in Oncology, vol. 4, article 267, 2014. View at Publisher · View at Google Scholar
  66. D. D. Taylor and C. Gercel-Taylor, “MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer,” Gynecologic Oncology, vol. 110, no. 1, pp. 13–21, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Logozzi, A. De Milito, L. Lugini et al., “High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients,” PLoS ONE, vol. 4, no. 4, Article ID e5219, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. B. K. Thakur, H. Zhang, A. Becker et al., “Double-stranded DNA in exosomes: a novel biomarker in cancer detection,” Cell Research, vol. 24, no. 6, pp. 766–769, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. K. Mizutani, R. Terazawa, K. Kameyama et al., “Isolation of prostate cancer-related exosomes,” Anticancer Research, vol. 34, no. 7, pp. 3419–3423, 2014. View at Google Scholar
  70. R. Cazzoli, F. Buttitta, M. di Nicola et al., “MicroRNAs derived from circulating exosomes as noninvasive biomarkers for screening and diagnosing lung cancer,” Journal of Thoracic Oncology, vol. 8, no. 9, pp. 1156–1162, 2013. View at Publisher · View at Google Scholar · View at Scopus
  71. C.-S. Hong, L. Muller, T. L. Whiteside, and M. Boyiadzis, “Plasma exosomes as markers of therapeutic response in patients with acute myeloid leukemia,” Frontiers in Immunology, vol. 5, article 160, 2014. View at Publisher · View at Google Scholar · View at Scopus
  72. P. Filipazzi, M. Bürdek, A. Villa, L. Rivoltini, and V. Huber, “Recent advances on the role of tumor exosomes in immunosuppression and disease progression,” Seminars in Cancer Biology, vol. 22, no. 4, pp. 342–349, 2012. View at Publisher · View at Google Scholar · View at Scopus
  73. A. V. Vlassov, S. Magdaleno, R. Setterquist, and R. Conrad, “Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials,” Biochimica et Biophysica Acta, vol. 1820, no. 7, pp. 940–948, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Ferrajoli, T. D. Shanafelt, C. Ivan et al., “Prognostic value of miR-155 in individuals with monoclonal B-cell lymphocytosis and patients with B chronic lymphocytic leukemia,” Blood, vol. 122, no. 11, pp. 1891–1899, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Khan, J. R. Aspe, M. G. Asumen et al., “Extracellular, cell-permeable survivin inhibits apoptosis while promoting proliferative and metastatic potential,” British Journal of Cancer, vol. 100, no. 7, pp. 1073–1086, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. D. Pilzer and Z. Fishelson, “Mortalin/GRP75 promotes release of membrane vesicles from immune attacked cells and protection from complement-mediated lysis,” International Immunology, vol. 17, no. 9, pp. 1239–1248, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. D. Pilzer, O. Gasser, O. Moskovich, J. A. Schifferli, and Z. Fishelson, “Emission of membrane vesicles: roles in complement resistance, immunity and cancer,” Springer Seminars in Immunopathology, vol. 27, no. 3, pp. 375–387, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. R. Safaei, B. J. Larson, T. C. Cheng et al., “Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells,” Molecular Cancer Therapeutics, vol. 4, no. 10, pp. 1595–1604, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. J. Yin, X. Yan, X. Yao et al., “Secretion of annexin A3 from ovarian cancer cells and its association with platinum resistance in ovarian cancer patients,” Journal of Cellular and Molecular Medicine, vol. 16, no. 2, pp. 337–348, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. J. Wang, A. Hendrix, S. Hernot et al., “Bone marrow stromal cell-derived exosomes as communicators in drug resistance in multiple myeloma cells,” Blood, vol. 124, no. 4, pp. 555–566, 2014. View at Publisher · View at Google Scholar
  81. T. Aung, B. Chapuy, D. Vogel et al., “Exosomal evasion of humoral immunotherapy in aggressive B-cell lymphoma modulated by ATP-binding cassette transporter A3,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 37, pp. 15336–15341, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. B. Chapuy, R. Koch, U. Radunski et al., “Intracellular ABC transporter A3 confers multidrug resistance in leukemia cells by lysosomal drug sequestration,” Leukemia, vol. 22, no. 8, pp. 1576–1586, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. B. Chapuy, M. Panse, U. Radunski et al., “ABC transporter A3 facilitates lysosomal sequestration of imatinib and modulates susceptibility of chronic myeloid leukemia cell lines to this drug,” Haematologica, vol. 94, no. 11, pp. 1528–1536, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. T. Efferth, J.-P. Gillet, A. Sauerbrey et al., “Expression profiling of ATP-binding cassette transporters in childhood T-cell acute lymphoblastic leukemia,” Molecular Cancer Therapeutics, vol. 5, no. 8, pp. 1986–1994, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. P. M. Jones and A. M. George, “The ABC transporter structure and mechanism: perspectives on recent research,” Cellular and Molecular Life Sciences, vol. 61, no. 6, pp. 682–699, 2004. View at Publisher · View at Google Scholar · View at Scopus
  86. C. H. Lee, “Reversing agents for ATP-binding cassette drug transporters,” Methods in Molecular Biology, vol. 596, pp. 325–340, 2010. View at Publisher · View at Google Scholar · View at Scopus