Examination of the specificity of tumor cell derived exosomes with tumor cells in vitro

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 11, 2014, Pages 2954-2965

  Smyth, Tyson J ^a   Redzic, Jasmina S ^b   Graner, Michael W ^b   Anchordoquy, Thomas J ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Association; Exosomes; Liposomes; pH; Protein cleavage

Indexed keywords

CALNEXIN; CD63 ANTIGEN; CD9 ANTIGEN; CELL SURFACE PROTEIN; CHOLESTEROL; CYTOCHROME C; DRUG CARRIER; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; LIPOSOME; PHOSPHATIDYLCHOLINE; SPHINGOMYELIN;

ACIDIFICATION; ARTICLE; CELL ADHESION; CELL COMMUNICATION; CELL CONTACT; CELL SPECIFICITY; CELLULAR ASSOCIATION; CELLULAR DISTRIBUTION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; COMPARATIVE STUDY; CONTROLLED STUDY; EXOSOME; FAT CONTENT; IMMORTALIZED CELL LINE; INTERNALIZATION; LIPID COMPOSITION; MCF 7 CELL LINE; MOLECULAR DYNAMICS; PARTICLE SIZE; PH; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN FUNCTION; TUMOR CELL DERIVED EXOSOME; TUMOR CELL LINE; TUMOR MICROENVIRONMENT;

EID: 84908036925     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.07.026     Document Type: Article

References (73)

1. C. Théry, M. Ostrowski, and E. Segura Membrane vesicles as conveyors of immune responses Nat. Rev. Immunol. 9 2009 581 593
2. G. Camussi, M.C. Deregibus, S. Bruno, C. Grange, V. Fonsato, and C. Tetta Exosome/microvesicle-mediated epigenetic reprogramming of cells Am. J. Cancer Res. 1 2011 98 110
3. A. Lakkaraju, and E. Rodriguez-Boulan Itinerant exosomes: emerging roles in cell and tissue polarity Trends Cell Biol. 18 2008 199 209
4. E.N. Nolte-'t Hoen, S.I. Buschow, S.M. Anderton, W. Stoorvogel, and M.H. Wauben Activated T cells recruit exosomes secreted by dendritic cells via LFA-1 Blood 113 2009 1977 1981
5. E. Segura ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming Blood 106 2005 216 223 (Pubitemid 40967195)
6. S. Keller, A.-K. König, F. Marmé, S. Runz, S. Wolterink, D. Koensgen, A. Mustea, J. Sehouli, and P. Altevogt Systemic presence and tumor-growth promoting effect of ovarian carcinoma released exosomes Cancer Lett. 278 2009 73 81
7. M. Miyanishi, K. Tada, M. Koike, Y. Uchiyama, T. Kitamura, and S. Nagata Identification of Tim4 as a phosphatidylserine receptor Nature 450 2007 435 439 (Pubitemid 350126753)
8. A.E. Morelli Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells Blood 104 2004 3257 3266 (Pubitemid 39507144)
9. C. Escrevente, S. Keller, P. Altevogt, and J. Costa Interaction and uptake of exosomes by ovarian cancer cells BMC Cancer 11 2011 108
10. T. Tian, Y. Wang, H. Wang, Z. Zhu, and Z. Xiao Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy J. Cell. Biochem. 111 2010 488 496
11. D. Feng, W.-L. Zhao, Y.-Y. Ye, X.-C. Bai, R.-Q. Liu, L.-F. Chang, Q. Zhou, and S.-F. Sui Cellular Internalization of Exosomes Occurs Through Phagocytosis Traffic 11 2010 675 687
12. K. Al-Nedawi, B. Meehan, J. Micallef, V. Lhotak, L. May, A. Guha, and J. Rak Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells Nat. Cell Biol. 10 2008 619 624 (Pubitemid 351627382)
13. 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 Nat. Cell Biol. 9 2007 654 659 (Pubitemid 47214727)
14. J.M. Aliotta, M. Pereira, K.W. Johnson, N. de Paz, M.S. Dooner, N. Puente, C. Ayala, K. Brilliant, D. Berz, and D. Lee Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription Exp. Hematol. 38 2010 233 245
15. D.D. Taylor, and C. Gercel-Taylor MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer Gynecol. Oncol. 110 2008 13 21 (Pubitemid 351853251)
16. L. Alvarez-Erviti, Y. Seow, H. Yin, C. Betts, S. Lakhal, and M.J.A. Wood Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes Nat. Biotechnol. 29 2011 341 345
17. D. Sun, X. Zhuang, X. Xiang, Y. Liu, S. Zhang, C. Liu, S. Barnes, W. Grizzle, D. Miller, and H.-G. Zhang A Novel Nanoparticle Drug Delivery System: The Anti-inflammatory Activity of Curcumin Is Enhanced When Encapsulated in Exosomes Mol. Ther. 18 2010 1606 1614
18. I. Parolini, C. Federici, C. Raggi, L. Lugini, S. Palleschi, A. De Milito, C. Coscia, E. Iessi, M. Logozzi, A. Molinari, M. Colone, M. Tatti, M. Sargiacomo, and S. Fais Microenvironmental pH Is a Key Factor for Exosome Traffic in Tumor Cells J. Biol. Chem. 284 2009 34211 34222
19. P. Vaupel Tumor microenvironmental physiology and its implications for radiation oncology Semin. Radiat. Oncol. 14 2004 198 206 (Pubitemid 38903223)
20. B. Fevrier Cells release prions in association with exosomes Proc. Natl. Acad. Sci. 101 2004 9683 9688 (Pubitemid 38869296)
21. C. Thery, A. Regnault, J. Garin, J. Wolfers, L. Zitvogel, P. Ricciardi-Castagnoli, G. Raposo, and S. Amigorena Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73 J. Cell Biol. 147 1999 599 610 (Pubitemid 29523465)
22. W. Stillwell An introduction to biological membranes: from bilayers to rafts 2013 Elsevier/Academic Press London; Waltham, MA
23. W.S. Kamoun, S.S. Chae, D.A. Lacorre, J.A. Tyrrell, M. Mitre, M.A. Gillissen, D. Fukumura, R.K. Jain, and L.L. Munn Simultaneous measurement of RBC velocity, flux, hematocrit and shear rate in vascular networks Nat. Methods 7 2010 655 660
24. K. Trajkovic, C. Hsu, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, P. Schwille, B. Brugger, and M. Simons Ceramide Triggers Budding of Exosome Vesicles into Multivesicular Endosomes Science 319 2008 1244 1247 (Pubitemid 351323020)
25. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
26. M.P. Caby Exosomal-like vesicles are present in human blood plasma Int. Immunol. 17 2005 879 887
27. B. Février, and G. Raposo Exosomes: endosomal-derived vesicles shipping extracellular messages Curr. Opin. Cell Biol. 16 2004 415 421 (Pubitemid 38903148)
28. W. Stoorvogel, M.J. Kleijmeer, H.J. Geuze, and G. Raposo The biogenesis and functions of exosomes Traffic 3 2002 321 330 (Pubitemid 34461042)
29. R. Gastpar, M. Gehrmann, M.A. Bausero, A. Asea, C. Gross, J.A. Schroeder, and G. Multhoff Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells Cancer Res. 65 2005 5238 5247 (Pubitemid 40827334)
30. J.P. Mitchell, J. Court, M.D. Mason, Z. Tabi, and A. Clayton Increased exosome production from tumour cell cultures using the Integra CELLine Culture System J. Immunol. Methods 335 2008 98 105
31. J.-a. Cho, Y.-S. Lee, S.-H. Kim, J.-K. Ko, and C.-W. Kim MHC independent anti-tumor immune responses induced by Hsp70-enriched exosomes generate tumor regression in murine models Cancer Lett. 275 2009 256 265
32. R. Mears, R.A. Craven, S. Hanrahan, N. Totty, C. Upton, S.L. Young, P. Patel, P.J. Selby, and R.E. Banks Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry Proteomics 4 2004 4019 4031 (Pubitemid 39657475)
33. S. Mathivanan, and R.J. Simpson ExoCarta: A compendium of exosomal proteins and RNA Proteomics 9 2009 4997 5000
34. R. Safaei Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells Mol. Cancer Ther. 4 2005 1595 1604 (Pubitemid 41556443)
35. D. Fitzner, M. Schnaars, D. van Rossum, G. Krishnamoorthy, P. Dibaj, M. Bakhti, T. Regen, U.K. Hanisch, and M. Simons Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis J. Cell Sci. 124 2011 447 458
36. A. Montecalvo, W.J. Shufesky, D.B. Stolz, M.G. Sullivan, Z. Wang, S.J. Divito, G.D. Papworth, S.C. Watkins, P.D. Robbins, A.T. Larregina, and A.E. Morelli Exosomes as a short-range mechanism to spread alloantigen between dendritic cells during T cell allorecognition J. Immunol. 180 2008 3081 3090
37. H. Vallhov, C. Gutzeit, S.M. Johansson, N. Nagy, M. Paul, Q. Li, S. Friend, T.C. George, E. Klein, A. Scheynius, and S. Gabrielsson Exosomes Containing Glycoprotein 350 Released by EBV-Transformed B Cells Selectively Target B Cells through CD21 and Block EBV Infection In Vitro J. Immunol. 186 2010 73 82
38. C. Lässer, V. Seyed Alikhani, K. Ekström, M. Eldh, P. Torregrosa Paredes, A. Bossios, M. Sjöstrand, S. Gabrielsson, J. Lötvall, and H. Valadi Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages J. Transl. Med. 9 2011 9
39. C. Yang, and P.D. Robbins The Roles of Tumor-Derived Exosomes in Cancer Pathogenesis Clin. Dev. Immunol. 2011 2011 1 11
40. R. Wubbolts Proteomic and Biochemical Analyses of Human B Cell-derived Exosomes Potential Implications for their Function and Multiveesicular Body Formation J. Biol. Chem. 278 2003 10963 10972 (Pubitemid 36792644)
41. K. Laulagnier, C. Motta, S. Hamdi, S. Roy, F. Fauvelle, J.F. Pageaux, T. Kobayashi, J.P. Salles, B. Perret, C. Bonnerot, and M. Record Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization Biochem. J. 380 2004 161 171 (Pubitemid 38725741)
42. K. Laulagnier, H. Vincent-Schneider, S. Hamdi, C. Subra, D. Lankar, and M. Record Characterization of exosome subpopulations from RBL-2H3 cells using fluorescent lipids Blood Cell Mol. Dis. 35 2005 116 121 (Pubitemid 41267037)
43. C. Subra, K. Laulagnier, B. Perret, and M. Record Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies Biochimie 89 2007 205 212 (Pubitemid 46161956)
44. V.A. Fadok, D.L. Bratton, D.M. Rose, A. Pearson, R.A. Ezekewitz, and P.M. Henson A receptor for phosphatidylserine-specific clearance of apoptotic cells Nature 405 2000 85 90 (Pubitemid 30321820)
45. V.A. Fadok, A. de Cathelineau, D.L. Daleke, P.M. Henson, and D.L. Bratton Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts J. Biol. Chem. 276 2001 1071 1077 (Pubitemid 32096530)
46. R.J. Simpson, S.S. Jensen, and J.W.E. Lim Proteomic profiling of exosomes: Current perspectives Proteomics 8 2008 4083 4099
47. R. Schiffelers, Kooijmans, Vader, and D. van, S. van Exosome mimetics: a novel class of drug delivery systems Int. J. Nanomedicine 2012 1525
48. H. Eagle The effect of environmental pH on the growth of normal and malignant cells J. Cell. Physiol. 82 1973 1 8
49. L. Griffiths, G.U. Dachs, R. Bicknell, A.L. Harris, and I.J. Stratford The influence of oxygen tension and pH on the expression of platelet-derived endothelial cell growth factor/thymidine phosphorylase in human breast tumor cells grown in vitro and in vivo Cancer Res. 57 1997 570 572 (Pubitemid 27085632)
50. R. Martinez-Zaguilan, E.A. Seftor, R.E. Seftor, Y.W. Chu, R.J. Gillies, and M.J. Hendrix Acidic pH enhances the invasive behavior of human melanoma cells Clin. Exp. Metastasis 14 1996 176 186 (Pubitemid 26074280)
51. E. Segura, S. Amigorena, and C. Théry Mature dendritic cells secrete exosomes with strong ability to induce antigen-specific effector immune responses Blood Cell Mol. Dis. 35 2005 89 93 (Pubitemid 41267034)
52. S.M. van Dommelen, P. Vader, S. Lakhal, S.A.A. Kooijmans, W.W. van Solinge, M.J.A. Wood, and R.M. Schiffelers Microvesicles and exosomes: Opportunities for cell-derived membrane vesicles in drug delivery J. Control. Release 162 2 2012 635 644
53. S. Lakhal, and M.J.A. Wood Exosome nanotechnology: An emerging paradigm shift in drug delivery BioEssays 33 2011 737 741
54. D. Needham, and R.S. Nunn Elastic deformation and failure of lipid bilayer membranes containing cholesterol Biophys. J. 58 1990 997 1009 (Pubitemid 20307868)
55. T.J. McIntosh, S.A. Simon, D. Needham, and C.H. Huang Structure and cohesive properties of sphingomyelin/cholesterol bilayers Biochemistry 31 1992 2012 2020
56. T. Ishida, H. Harashima, and H. Kiwada Liposome clearance Biosci. Rep. 22 2002 197 224 (Pubitemid 35222732)
57. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572 (Pubitemid 27248754)
58. L. Xu, and T.J. Anchordoquy Effect of cholesterol nanodomains on the targeting of lipid-based gene delivery in cultured cells Mol. Pharm. 7 2010 1311 1317
59. L. Xu, M.F. Wempe, and T.J. Anchordoquy The effect of cholesterol domains on PEGylated liposomal gene delivery in vitro Ther. Deliv. 2 2011 451 460
60. L. Xu, J. Betker, H. Yin, and T.J. Anchordoquy Ligands located within a cholesterol domain enhance gene delivery to the target tissue J. Control. Release 160 2012 57 63
61. T.M. Allen, and A. Chonn Large unilamellar liposomes with low uptake into the reticuloendothelial system FEBS Lett. 223 1987 42 46
62. T.M. Allen, G.A. Austin, A. Chonn, L. Lin, and K.C. Lee Uptake of liposomes by cultured mouse bone marrow macrophages: influence of liposome composition and size Biochim. Biophys. Acta 1061 1991 56 64
63. M.E. Haque, T.J. McIntosh, and B.R. Lentz Influence of Lipid Composition on Physical Properties and PEG-Mediated Fusion of Curved and Uncurved Model Membrane Vesicles: "Nature's Own" Fusogenic Lipid Bilayer † Biochemistry 40 2001 4340 4348 (Pubitemid 32319580)
64. M.E. Hemler Targeting of tetraspanin proteins - potential benefits and strategies Nat. Rev. Drug Discov. 7 2008 747 758
65. I.D. Campbell, and M.J. Humphries Integrin Structure Activation, and Interactions Cold Spring Harb. Perspect. Biol. 3 2011 a004994
66. A. Clayton Adhesion and signaling by B cell-derived exosomes: the role of integrins FASEB J. 18 9 2004 977 979 (Pubitemid 39561497)
67. S. Rana, and M. Zöller Exosome target cell selection and the importance of exosomal tetraspanins: a hypothesis Biochem. Soc. Trans. 39 2011 559 562
68. S.K. Parks, J. Chiche, and J. Pouyssegur pH control mechanisms of tumor survival and growth J. Cell. Physiol. 226 2011 299 308
69. J.E. Park, H.S. Tan, A. Datta, R.C. Lai, H. Zhang, W. Meng, S.K. Lim, and S.K. Sze Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes Mol. Cell. Proteomics 9 2010 1085 1099
70. R.E. Moellering, K.C. Black, C. Krishnamurty, B.K. Baggett, P. Stafford, M. Rain, R.A. Gatenby, and R.J. Gillies Acid treatment of melanoma cells selects for invasive phenotypes Clin. Exp. Metastasis 25 2008 411 425
71. E.K. Rofstad Acidic Extracellular pH Promotes Experimental Metastasis of Human Melanoma Cells in Athymic Nude Mice Cancer Res. 66 2006 6699 6707 (Pubitemid 44085627)
72. S. Hao, Z. Ye, F. Li, Q. Meng, M. Qureshi, J. Yang, and J. Xiang Epigenetic transfer of metastatic activity by uptake of highly metastatic B16 melanoma cell-released exosomes Exp. Oncol. 28 2006 126 131 (Pubitemid 44140264)
73. A. Janowska-Wieczorek, M. Wysoczynski, J. Kijowski, L. Marquez-Curtis, B. Machalinski, J. Ratajczak, and M.Z. Ratajczak Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer Int. J. Cancer 113 2005 752 760 (Pubitemid 40101256)