Tumor exosomes induce tunneling nanotubes in lipid raft-enriched regions of human mesothelioma cells

Experimental Cell Research

Volumn 323, Issue 1, 2014, Pages 178-188

  Thayanithy, Venugopal ^a   Babatunde, Victor ^b   Dickson, Elizabeth L ^c   Wong, Phillip ^a   Oh, Sanghoon ^b   Ke, Xu ^b   Barlas, Afsar ^b   Fujisawa, Sho ^b   Romin, Yevgeniy ^b   Moreira, André L ^b   Downey, Robert J ^b   Steer, Clifford J ^c   Subramanian, Subbaya ^a   Manova Todorova, Katia ^b   Moore, Malcolm A S ^b   Lou, Emil ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Exosomes; Intercellular communication; Intercellular transfer; Lipid rafts; Mesothelioma; Tunneling nanotubes

Indexed keywords

CD63 ANTIGEN; CD81 ANTIGEN; CD9 ANTIGEN; HEAT SHOCK PROTEIN 70; NANOTUBE; TUNNELING NANOTUBE; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL COMMUNICATION; CELL COUNT; CELL ISOLATION; CELL TRANSPORT; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXOSOME; FLUORESCENCE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; LIPID RAFT; MESOTHELIOMA; MESOTHELIUM CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

EXOSOMES; INTERCELLULAR COMMUNICATION; INTERCELLULAR TRANSFER; LIPID RAFTS; MESOTHELIOMA; TUNNELING NANOTUBES;

BIOLOGICAL TRANSPORT; CELL COMMUNICATION; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; EXOSOMES; HUMANS; MEMBRANE MICRODOMAINS; MESOTHELIOMA; NANOTUBES; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84896491146     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.01.014     Document Type: Article

References (49)

1. Rustom A., Saffrich R., Markovic I., Walther P., Gerdes H.H. Nanotubular highways for intercellular organelle transport. Science 2004, 303:1007-1010.
2. Lou E., Fujisawa S., Morozov A., Barlas A., Romin Y., Dogan Y., Gholami S., Moreira A.L., Manova-Todorova K., Moore M.A. Tunneling nanotubes provide a unique conduit for intercellular transfer of cellular contents in human malignant pleural mesothelioma. PLoS One 2012, 7:e33093.
3. Lou E., Fujisawa S., Barlas A., Romin Y., Manova-Todorova K., Moore M.A.S., Subramanian S. Tunneling nanotubes: a new paradigm for studying intercellular communication and therapeutics in cancer. Commun. Integr. Biol. 2012, 5.
4. Wang Z.G., Liu S.L., Tian Z.Q., Zhang Z.L., Tang H.W., Pang D.W. Myosin-driven intercellular transportation of wheat germ agglutinin mediated by membrane nanotubes between human lung cancer cells. ACS Nano 2012, 6:10033-10041.
5. Watkins S.C., Salter R.D. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 2005, 23:309-318.
6. Hase K., Kimura S., Takatsu H., Ohmae M., Kawano S., Kitamura H., Ito M., Watarai H., Hazelett C.C., Yeaman C., Ohno H. M-sec promotes membrane nanotube formation by interacting with ral and the exocyst complex. Nat. Cell Biol. 2009, 11:1427-1432.
7. Eugenin E.A., Gaskill P.J., Berman J.W., (Tnt) Are Tunneling Nanotubes Induced by Hiv-infection of macrophages: a potential mechanism for intercellular Hiv trafficking. Cell. Immunol. 2009, 254:142-148.
8. Sowinski S., Jolly C., Berninghausen O., Purbhoo M.A., Chauveau A., Kohler K., Oddos S., Eissmann P., Brodsky F.M., Hopkins C., Onfelt B., Sattentau Q., Davis D.M. Membrane nanotubes physically connect T cells over long distances presenting a novel route for Hiv-1 transmission. Nat. Cell Biol. 2008, 10:211-219.
9. Ranzinger J., Rustom A., Abel M., Leyh J., Kihm L., Witkowski M., Scheurich P., Zeier M., Schwenger V. Nanotube action between human mesothelial cells reveals novel aspects of inflammatory responses. PLoS One 2011, 6:e29537.
10. Xu W., Santini P.A., Sullivan J.S., He B., Shan M., Ball S.C., Dyer W.B., Ketas T.J., Chadburn A., Cohen-Gould L., Knowles D.M., Chiu A., Sanders R.W., Chen K., Cerutti A. Hiv-1 evades virus-specific Igg2 and Iga responses by targeting systemic and intestinal B cells via long-range intercellular conduits. Nat. Immunol. 2009, 10:1008-1017.
11. Galkina S.I., Stadnichuk V.I., Molotkovsky J.G., Romanova J.M., Sud'ina G.F., Klein T. Microbial alkaloid staurosporine induces formation of nanometer-wide membrane tubular extensions (cytonemes, membrane tethers) in human neutrophils. Cell Adhes. Migr. 2010, 4:32-38.
12. Gousset K., Schiff E., Langevin C., Marijanovic Z., Caputo A., Browman D.T., Chenouard N., de Chaumont F., Martino A., Enninga J., Olivo-Marin J.C., Mannel D., Zurzolo C. Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 2009, 11:328-336.
13. Gurke S., Barroso J.F., Hodneland E., Bukoreshtliev N.V., Schlicker O., Gerdes H.H. Tunneling nanotube (Tnt)-like structures facilitate a constitutive, actomyosin-dependent exchange of endocytic organelles between normal rat kidney cells. Exp. Cell Res. 2008, 314:3669-3683.
14. Yasuda K., Park H.C., Ratliff B., Addabbo F., Hatzopoulos A.K., Chander P., Goligorsky M.S. Adriamycin nephropathy: a failure of endothelial progenitor cell-induced repair. Am. J. Pathol. 2010, 176:1685-1695.
15. Hegmans J.P., Bard M.P., Hemmes A., Luider T.M., Kleijmeer M.J., Prins J.B., Zitvogel L., Burgers S.A., Hoogsteden H.C., Lambrecht B.N. Proteomic analysis of exosomes secreted by human mesothelioma cells. Am. J. Pathol. 2004, 164:1807-1815.
16. Koumangoye R.B., Sakwe A.M., Goodwin J.S., Patel T., Ochieng J. Detachment of breast tumor cells induces rapid secretion of exosomes which subsequently mediate cellular adhesion and spreading. PLoS One 2011, 6:e24234.
17. Taner S.B., Onfelt B., Pirinen N.J., McCann F.E., Magee A.I., Davis D.M. Control of immune responses by trafficking cell surface proteins, vesicles and lipid rafts to and from the immunological synapse. Traffic 2004, 5:651-661.
18. Rudnicka D., Feldmann J., Porrot F., Wietgrefe S., Guadagnini S., Prevost M.C., Estaquier J., Haase A.T., Sol-Foulon N., Schwartz O. Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J. Virol. 2009, 83:6234-6246.
19. Gupta N., DeFranco A.L. Visualizing lipid raft dynamics and early signaling events during antigen receptor-mediated B-lymphocyte activation. Mol. Biol. Cell 2003, 14:432-444.
20. Mukerji J., Olivieri K.C., Misra V., Agopian K.A., Gabuzda D. Proteomic analysis of Hiv-1 Nef cellular binding partners reveals a role for exocyst complex proteins in mediating enhancement of intercellular nanotube formation. Retrovirology 2012, 9:33.
21. Calzolari A., Raggi C., Deaglio S., Sposi N.M., Stafsnes M., Fecchi K., Parolini I., Malavasi F., Peschle C., Sargiacomo M., Testa U. Tfr2 localizes in lipid raft domains and is released in exosomes to activate signal transduction along the mapk pathway. J. Cell Sci. 2006, 119:4486-4498.
22. Kabaso D., Lokar M., Kralj-Iglic V., Veranic P., Iglic A. Temperature and cholera toxin B are factors that influence formation of membrane nanotubes in Rt4 and T24 urothelial cancer cell lines. Int. J. Nanomed. 2011, 6:495-509.
23. Lokar M., Kabaso D., Resnik N., Sepcic K., Kralj-Iglic V., Veranic P., Zorec R., Iglic A. The role of cholesterol-sphingomyelin membrane nanodomains in the stability of intercellular membrane nanotubes. Int. J. Nanomed. 2012, 7:1891-1902.
24. Escrevente C., Keller S., Altevogt P., Costa J. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 2011, 11:108.
25. Bobrie A., Colombo M., Raposo G., Thery C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 2011, 12:1659-1668.
26. Chalmin F., Ladoire S., Mignot G., Vincent J., Bruchard M., Remy-Martin J.P., Boireau W., Rouleau A., Simon B., Lanneau D., De Thonel A., Multhoff G., Hamman A., Martin F., Chauffert B., Solary E., Zitvogel L., Garrido C., Ryffel B., Borg C., Apetoh L., Rebe C., Ghiringhelli F. Membrane-associated Hsp72 from tumor-derived exosomes mediates Stat3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J. Clin. Invest. 2010, 120:457-471.
27. Gatenby R.A., Gawlinski E.T., Reaction-Diffusion A. Model of cancer invasion. Cancer Res. 1996, 56:5745-5753.
28. Hood J.L., Pan H., Lanza G.M., Wickline S.A. Paracrine induction of endothelium by tumor exosomes. Lab. Invest. 2009, 89:1317-1328.
29. Mineo M., Garfield S.H., Taverna S., Flugy A., De Leo G., Alessandro R., Kohn E.C. Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion. Angiogenesis 2012, 15:33-45.
30. Kenny P.A., Lee G.Y., Bissell M.J. Targeting the tumor microenvironment. Front. Biosci. 2007, 12:3468-3474.
31. Kosaka N., Iguchi H., Yoshioka Y., Takeshita F., Matsuki Y., Ochiya T. Secretory mechanisms and intercellular transfer of micrornas in living cells. J. Biol. Chem. 2010, 285:17442-17452.
32. Luo S.S., Ishibashi O., Ishikawa G., Ishikawa T., Katayama A., Mishima T., Takizawa T., Shigihara T., Goto T., Izumi A., Ohkuchi A., Matsubara S., Takeshita T. Human villous trophoblasts express and secrete placenta-specific micrornas into maternal circulation via exosomes. Biol. Reprod. 2009, 81:717-729.
33. Michael A., Bajracharya S.D., Yuen P.S., Zhou H., Star R.A., Illei G.G., Alevizos I. Exosomes from human saliva as a source of microrna biomarkers. Oral Dis. 2010, 16:34-38.
34. Mittelbrunn M., Gutierrez-Vazquez C., Villarroya-Beltri C., Gonzalez S., Sanchez-Cabo F., Gonzalez M.A., Bernad A., Sanchez-Madrid F. Unidirectional transfer of microrna-loaded exosomes from T cells to antigen-presenting cells. Nat. Commun. 2011, 2:282.
35. Ohshima K., Inoue K., Fujiwara A., Hatakeyama K., Kanto K., Watanabe Y., Muramatsu K., Fukuda Y., Ogura S., Yamaguchi K., Mochizuki T. Let-7 microrna family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One 2010, 5:e13247.
36. Pegtel D.M., Cosmopoulos K., Thorley-Lawson D.A., van Eijndhoven M.A., Hopmans E.S., Lindenberg J.L., de Gruijl T.D., Wurdinger T., Middeldorp J.M. Functional delivery of viral mirnas via exosomes. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6328-6333.
37. Skog J., Wurdinger T., van Rijn S., Meijer D.H., Gainche L., Sena-Esteves M., Curry W.T., Carter B.S., Krichevsky A.M., Breakefield X.O. Glioblastoma microvesicles transport rna and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10:1470-1476.
38. Taylor D.D., Gercel-Taylor C. Microrna signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 2008, 110:13-21.
39. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mrnas and micrornas is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9:654-659.
40. Sharma S., Rasool H.I., Palanisamy V., Mathisen C., Schmidt M., Wong D.T., Gimzewski J.K. Structural-mechanical characterization of nanoparticle exosomes in human saliva, using correlative afm, fesem, and force spectroscopy. ACS Nano 2010, 4:1921-1926.
41. Chen T., Guo J., Yang M., Zhu X., Cao X. Chemokine-containing exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J. Immunol. 2011, 186:2219-2228.
42. Bukoreshtliev N.V., Wang X., Hodneland E., Gurke S., Barroso J.F., Gerdes H.H. Selective block of tunneling nanotube (Tnt) formation inhibits intercellular organelle transfer between Pc12 cells. FEBS Lett. 2009, 583:1481-1488.
43. Taverna S., Flugy A., Saieva L., Kohn E.C., Santoro A., Meraviglia S., De Leo G., Alessandro R. Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis. Int. J. Cancer 2012, 130:2033-2043.
44. Parolini I., Federici C., Raggi C., Lugini L., Palleschi S., De Milito A., Coscia C., Iessi E., Logozzi M., Molinari A., Colone M., Tatti M., Sargiacomo M., Fais S. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem. 2009, 284:34211-34222.
45. Martinez-Zaguilan R., Seftor E.A., Seftor R.E., Chu Y.W., Gillies R.J., Hendrix M.J. Acidic pH enhances the invasive behavior of human melanoma cells. Clin. Exp. Metastasis 1996, 14:176-186.
46. Tang K., Zhang Y., Zhang H., Xu P., Liu J., Ma J., Lv M., Li D., Katirai F., Shen G.X., Zhang G., Feng Z.H., Ye D., Huang B. Delivery of chemotherapeutic drugs in tumour cell-derived microparticles. Nat. Commun. 2012, 3:1282.
47. Fruhbeis C., Frohlich D., Kuo W.P., Amphornrat J., Thilemann S., Saab A.S., Kirchhoff F., Mobius W., Goebbels S., Nave K.A., Schneider A., Simons M., Klugmann M., Trotter J., Kramer-Albers E.M. Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol. 2013, 11:e1001604.
48. de Gassart A., Geminard C., Fevrier B., Raposo G., Vidal M. Lipid raft-associated protein sorting in exosomes. Blood 2003, 102:4336-4344.
49. Mincheva-Nilsson L., Baranov V. The role of placental exosomes in reproduction. Am. J. Reprod. Immunol. 2010, 63:520-533.