Abstract
Export of biologically active compounds is essential for any living cell. Transport of bioactive molecules through a cellular membrane can be active, or passive, or vesicular. In the past decade, vesicular transduction of intercellular signals has attracted great interest in the scientific community. An extremely important role of the vesicle transduction has been established for almost all processes in a living body. Not only profiles of protein and RNA expression in a cell, but also its secretome change during various pathologies, including cancer development. The enhanced secretion of vesicles by transformed cells is one important factor in creating a special microenvironment that favors tumor progression. At present, a role of exosomes has been demonstrated for such important processes as an epithelial-mesenchymal transition, angiogenesis, metastatic niche formation, chemotherapeutic resistance, and interaction with the immune system. The special biological role of the extracellular vesicles and their basic differences depend on their molecular composition. Therefore, special protein and lipid markers are responsible for a vesicular targeted delivery with information due to the preferable interaction with cells of a definite type. The exosomes of cancer cells can facilitate apoptosis or growth of neighboring malignant cells depending on the exosome composition. These and other special features of the extracellular vesicles make studies of their composition and role especially interesting and attract significant attention from researchers. Despite the rapid progress in this field, there are still many unresolved problems, such as a search for specific markers which allow identification of different types of vesicles or vesicles secreted by distinct cells, as well as screening of vesicular markers of cancers and other diseases that are associated with disorders in a functioning immune system. This review is mainly focused on the role of intercellular vesicular transport of bioorganic molecules in cancer progression. We believe that a successful treatment of oncological diseases is impossible without an understanding of the intercellular communication of both cancer cells between each other and with other systems of an organism and with a concept of an active participation of the cell-secreted vesicles in this process.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- АBs:
-
apoptotic bodies
- EV:
-
an extracellular vesicle
- MVBs:
-
multivesicular bodies
- ADAM10:
-
the disintegrin and metalloproteinase domain 10
- AKT:
-
the alpha serine/threonine-protein kinase
- Bcl-2:
-
the B-cell lymphoma 2
- Bim:
-
the Bcl-2-like protein 11
- BIRC5:
-
the baculoviral inhibitor of apoptosis repeat-containing 5
- Bsx:
-
the brain-specific homeobox protein homolog
- CXCR2:
-
the C-X-C chemokine receptor type 2
- СD:
-
a cluster of differentiation
- EDH1:
-
the EH domain-containing protein 1, where EH is the EPS15 homologue and EPS15 is the epidermal growth factor receptor substrate 15
- EGF:
-
the epidermal growth factor
- EGFR:
-
the receptor of the epidermal growth factor
- ESCRT:
-
the endosomal sorting complex required for transport
- EMMPRIN:
-
the extracellular matrix metalloproteinase inducer
- EpCAM:
-
an epithelial cell adhesion molecule
- EPS8L:
-
the epidermal growth factor receptor kinase substrate 8-like protein 2
- ERG:
-
the ETS-related gene
- ETS:
-
erythroblast transformation-specific
- ERK:
-
extracellular signal–regulated kinases
- GPC1:
-
glypican 1
- HER-2:
-
the human epidermal growth factor receptor 2
- HSP:
-
heat shock proteins
- IL:
-
interleukin
- JNK:
-
the c-Jun N-terminal kinase
- L1CAM:
-
the L1 cell adhesion molecule
- MAPK:
-
the mitogen-activated protein kinase
- MHC:
-
the major histocompatibility complex
- miR:
-
a micro-RNA
- MLCK:
-
the myosin light-chain kinase
- NFκB:
-
the nuclear factor kappa-lightchain- enhancer of activated B cells
- PCA:
-
a prostate cancer antigen
- PDCD4:
-
the programmed cell death protein 4
- PI3:
-
phosphoinositide 3-kinase
- PLD:
-
phospholipase D
- PTEN:
-
phosphatase and tensin homolog deleted on chromosome 10
- Rab:
-
the Ras-related protein in brain
- Ras:
-
the rat sarcoma
- Rho:
-
the ρ Greek letter
- ROCK1:
-
the rho-associated, coiled-coil-containing protein kinase 1
- Src:
-
sarcoma
- TGF:
-
the transforming growth factor
- TMPRSS:
-
the transmembrane serine protease 2
- TSG101:
-
the tumor susceptibility gene 101
- TYRP-2:
-
the tyrosinase-related protein 2
- VEGF:
-
the vascular endothelial growth factor
- Vps4:
-
the vacuolar protein sorting- associated protein 4
References
Chargaff, E. and West, R., J. Biol. Chem., 1946, vol. 166, pp. 189–197.
Knox, K.W., Vesk, M., and Work, E., J. Bacteriol., 1966, vol. 92, pp. 1206–1217.
Soler, N., Marguet, E., Verbavatz, J.-M., and Forterre, P., Res. Microbiol., 2008, vol. 159, pp. 390–399.
Kalra, H., Drummen, G.P.C., and Mathivanan, S., Int. J. Mol. Sci., 2016, vol. 17, p. 170.
Bobrie, A., Colombo, M., Raposo, G., and Thery, C., Traffic, 2011, vol. 12, pp. 1659–1668.
Raposo, G. and Stoorvogel, W., J. Cell Biol., 2013, vol. 200, pp. 373–383.
Mathivanan, S., Lim, J.W.E., Tauro, B.J., Ji, H., Moritz, R.L., and Simpson, R.J., Mol. Cell Proteomics, 2010, vol. 9, pp. 197–208.
Pols, M.S. and Klumperman, J., Exp. Cell Res., 2009, vol. 315, pp. 1584–1592.
Perez-Hernandez, D., Gutierrez-Vazquez, C., Jorge, I., Lopez-Martin, S., Ursa, A., Sanchez-Madrid, F., Vazquez, J., and Yanez-Mo, M., J. Biol. Chem., 2013, vol. 288, pp. 11649–11661.
Stuffers, S., Sem, Wegner C., Stenmark, H., and Brech, A., Traffic, 2009, vol. 10, pp. 925–937.
Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brugger, B., and Simons, M., Science, 2008, vol. 319, pp. 1244–1247.
Ostrowski, M., Carmo, N.B., Krumeich, S., Fanget, I., Raposo, G., Savina, A., Moita, C.F., Schauer, K., Hume, A.N., Freitas, R.P., Goud, B., Benaroch, P., Hacohen, N., Fukuda, M., Desnos, C., Seabra, M.C., Darchen, F., Amigorena, S., Moita, L.F., and Thery, C., Nat. Cell Biol., 2010, vol. 12, pp. 19–30.
Bevers, E.M. and Williamson, P.L., FEBS Lett., 2010, vol. 584, pp. 2724–2730.
Daleke, D.L., J. Lipid Res., 2003, vol. 44, pp. 233–242.
Muralidharan-Chari, V., Clancy, J., Plou, C., Romao, M., Chavrier, P., Raposo, G., and D’Souza-Schorey, C., Curr. Biol., 2009, vol. 19, pp. 1875–1885.
Lane, J.D., Allan, V.J., and Woodman, P.G., J. Cell Sci., 2005, vol. 118, pp. 4059–4071.
Chang, J., Xie, M., Shah, V.R., Schneider, M.D., Entman, M.L., Wei, L., and Schwartz, R.J., Proc. Natl. Acad. Sci. U. S. A., 2006, vol. 103, pp. 14495–14500.
Sebbagh, M., Renvoize, C., Hamelin, J., Riche, N., Bertoglio, J., and Breard, J., Nat. Cell Biol., 2001, vol. 3, pp. 346–352.
Coleman, M.L., Sahai, E.A., Yeo, M., Bosch, M., Dewar, A., and Olson, M.F., Nat. Cell Biol., 2001, vol. 3, pp. 339–345.
Suzuki, J., Denning, D.P., Imanishi, E., Horvitz, H.R., and Nagata, S., Science, 2013, vol. 341, pp. 403–406.
Poon, I.K.H., Chiu, Y.-H., Armstrong, A.J., Kinchen, J.M., Juncadella, I.J., Bayliss, D.A., and Ravichandran, K.S., Nature, 2014, vol. 507, pp. 329–334.
Mathivanan, S., Ji, H., and Simpson, R.J., J. Proteomics, 2010, vol. 73, pp. 1907–1920.
Yakimchuk, K., Devices Methods Measurements, 2015, vol. 5, pp. 228–235.
Subra, C., Laulagnier, K., Perret, B., and Record, M., Biochimie, 2007, vol. 89, pp. 205–212.
Ciardiello, C., Cavallini, L., Spinelli, C., Yang, J., Reis-Sobreiro, M., De Candia, P., Minciacchi, V.R., and di Vizio, D., Int. J. Mol. Sci., 2016, vol. 17, p. 175.
Lydic, T.A., Townsend, S., Adda, C.G., Collins, C., Mathivanan, S., and Reid, G.E., Methods, 2015, vol. 87, pp. 83–95.
Wubbolts, R., Leckie, R.S., Veenhuizen, P.T.M., Schwarzmann, G., Mobius, W., Hoernschemeyer, J., Slot, J.-W., Geuze, H.J., and Stoorvogel, W., J. Biol. Chem., 2003, vol. 278, pp. 10963–10972.
Brouwers, J.F., Aalberts, M., Jansen, J.W.A., van Niel, G., Wauben, M.H., Stout, T.A.E., Helms, J.B., and Stoorvogel, W., Proteomics, 2013, vol. 13, pp. 1660–1666.
Laulagnier, K., Motta, C., Hamdi, S., Roy, S., Fauvelle, F., Pageaux, J.-F., Kobayashi, T., Salles, J.-P., Perret, B., Bonnerot, C., and Record, M., Biochem. J., 2004, vol. 380, pp. 161–171.
Matsuo, H., Chevallier, J., Mayran, N., Le Blanc, I., Ferguson, C., Faure, J., Blanc, N.S., Matile, S., Dubochet, J., Sadoul, R., Parton, R.G., Vilbois, F., and Gruenberg, J., Science, 2004, vol. 303, pp. 531–534.
Saunderson, S.C., Dunn, A.C., Crocker, P.R., and McLellan, A.D., Blood, 2014, vol. 123, pp. 208–216.
Batista, B.S., Eng, W.S., Pilobello, K.T., Hendricks-Munoz, K.D., and Mahal, L.K., J. Proteome Res., 2011, vol. 10, pp. 4624–4633.
Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J.J., and Lotvall, J.O., Nat. Cell Biol., 2007, vol. 9, pp. 654–659.
Thakur, B.K., Zhang, H., Becker, A., Matei, I., Huang, Y., Costa-Silva, B., Zheng, Y., Hoshino, A., Brazier, H., Xiang, J., Williams, C., Rodriguez-Barrueco, R., Silva, J.M., Zhang, W., Hearn, S., Elemento, O., Paknejad, N., Manova-Todorova, K., Welte, K., Bromberg, J., Peinado, H., and Lyden, D., Cell Res., 2014, vol. 24, pp. 766–769.
Zhang, X., Yuan, X., Shi, H., Wu, L., Qian, H., and Xu, W., J. Hematol. Oncol., 2015, vol. 8, p. 83.
Logozzi, M., Milito, A., Lugini, L., Borghi, M., Calabro, L., Spada, M., Perdicchio, M., Marino, M.L., Federici, C., Iessi, E., Brambilla, D., Venturi, G., Lozupone, F., Santinami, M., Huber, V., Maio, M., Rivoltini, L., and Fais, S., PLoS One, 2009, vol. 4, e5219.
Skog, J., Wurdinger, T., van Rijn, S., Meijer, D.H., Gainche, L., Sena-Esteves, M., Curry, W.T., Jr., Carter, B.S., Krichevsky, A.M., and Breakefield, X.O., Nat. Cell Biol., 2008, vol. 10, pp. 1470–1476.
Graner, M.W., Alzate, O., Dechkovskaia, A.M., Keene, J.D., Sampson, J.H., Mitchell, D.A., and Bigner, D.D., FASEB J., 2009, vol. 23, pp. 1541–1557.
Howitt, J. and Hill, A.F., J. Biol Chem., 2016, vol. 291, p. 26589–26597.
Peinado, H., Aleckovic, M., Lavotshkin, S., Matei, I., Costa-Silva, B., Moreno-Bueno, G., Hergueta-Redondo, M., Williams, C., Garcia-Santos, G., Ghajar, C., Nitadori-Hoshino, A., Hoffman, C., Badal, K., Garcia, B.A., Callahan, M.K., Yuan, J., Martins, V.R., Skog, J., Kaplan, R.N., Brady, M.S., Wolchok, J.D., Chapman, P.B., Kang, Y., Bromberg, J., and Lyden, D., Nat. Med., 2012, vol. 18, pp. 883–891.
Al-Nedawi, K., Meehan, B., Micallef, J., Lhotak, V., May, L., Guha, A., and Rak, J., Nat. Cell Biol., 2008, vol. 10, pp. 619–624.
Nilsson, J., Skog, J., Nordstrand, A., Baranov, V., Mincheva-Nilsson, L., Breakefield, X.O., and Widmark, A., Br. J. Cancer, 2009, vol. 100, pp. 1603–1607.
Li, J., Sherman-Baust, C.A., Tsai-Turton, M., Bristow, R.E., Roden, R.B., and Morin, P.J., BMC Cancer, 2009, vol. 9, p. 244.
Keller, S., Konig, A.-K., Marme, F., Runz, S., Wolterink, S., Koensgen, D., Mustea, A., Sehouli, J., and Altevogt, P., Cancer Lett., 2009, vol. 278, pp. 73–81.
Melo, S.A., Luecke, L.B., Kahlert, C., Fernandez, A.F., Gammon, S.T., Kaye, J., LeBleu, V.S., Mittendorf, E.A., Weitz, J., Rahbari, N., Reissfelder, C., Pilarsky, C., Fraga, M.F., Piwnica-Worms, D., and Kalluri, R., Nature, 2015, vol. 523, pp. 177–182.
Lin, S.-Y., Chang, C.-H., Wu, H.-C., Lin, C.-C., Chang, K.-P., Yang, C.-R., Huang, C.-P., Hsu, W.-H., Chang, C.-T., and Chen, C.-J., Sci Rep., 2016, vol. 6, p. 34446.
Chen, T.S., Lai, R.C., Lee, M.M., Choo, A.B.H., Lee, C.N., and Lim, S.K., Nucleic Acids Res., 2010, vol. 38, pp. 215–224.
Turchinovich, A., Weiz, L., Langheinz, A., and Burwinkel, B., Nucleic Acids Res., 2011, vol. 39, pp. 7223–7233.
Gallo, A., Tandon, M., Alevizos, I., and Illei, G.G., PLoS One, 2012, vol. 7, e30679.
Yu, S., Cao, H., Shen, B., and Feng, J., Oncotarget, 2015, vol. 6, pp. 37151–37168.
Taylor, D.D. and Gercel-Taylor, C., Gynecol. Oncol., 2008, vol. 110, pp. 13–21.
Rabinowits, G., Gercel-Taylor, C., Day, J.M., Taylor, D.D., and Kloecker, G.H., Clin. Lung Cancer, 2009, vol. 10, pp. 42–46.
Silva, J., Garcia, V., Zaballos, A., Provencio, M., Lombardia, L., Almonacid, L., Garcia, J.M., Dominguez, G., Pena, C., Diaz, R., Herrera, M., Varela, A., and Bonilla, F., Eur. Respir. J., 2011, vol. 37, pp. 617–623.
Mitchell, P.S., Parkin, R.K., Kroh, E.M., Fritz, B.R., Wyman, S.K., Pogosova-Agadjanyan, E.L., Peterson, A., Noteboom, J., O’Briant, K.C., Allen, A., Lin, D.W., Urban, N., Drescher, C.W., Knudsen, B.S., Stirewalt, D.L., Gentleman, R., Vessella, R.L., Nelson, P.S., Martin, D.B., and Tewari, M., Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, pp. 10513–10518.
Brase, J.C., Johannes, M., Schlomm, T., Falth, M., Haese, A., Steuber, T., Beissbarth, T., Kuner, R., and Sultmann, H., Int. J. Cancer, 2011, vol. 128, pp. 608–616.
Tanaka, Y., Kamohara, H., Kinoshita, K., Kurashige, J., Ishimoto, T., Iwatsuki, M., Watanabe, M., and Baba, H., Cancer, 2013, vol. 119, pp. 1159–1167.
Takeshita, N., Hoshino, I., Mori, M., Akutsu, Y., Hanari, N., Yoneyama, Y., Ikeda, N., Isozaki, Y., Maruyama, T., Akanuma, N., Komatsu, A., Jitsukawa, M., and Matsubara, H., Br. J. Cancer, 2013, vol. 108, pp. 644–652.
Corcoran, C., Friel, A.M., Duffy, M.J., Crown, J., and O’Driscoll, L., Clin. Chem., 2011, vol. 57, pp. 18–32.
Ohshima, K., Inoue, K., Fujiwara, A., Hatakeyama, K., Kanto, K., Watanabe, Y., Muramatsu, K., Fukuda, Y., Ogura, S.-I., Yamaguchi, K., and Mochizuki, T., PLoS One, 2010, vol. 5, p. e13247.
Del Conde, I., Shrimpton, C.N., Thiagarajan, P., and Lopez, J.A., Blood, 2005, vol. 106, pp. 1604–1611.
Falati, S., Liu, Q., Gross, P., Merrill-Skoloff, G., Chou, J., Vandendries, E., Celi, A., Croce, K., Furie, B.C., and Furie, B., J. Exp. Med., 2003, vol. 197, pp. 1585–1598.
Mezouar, S., Darbousset, R., Dignat-George, F., Panicot-Dubois, L., and Dubois, C., Int. J. Cancer, 2015, vol. 136, pp. 462–475.
Pluskota, E., Woody, N.M., Szpak, D., Ballantyne, C.M., Soloviev, D.A., Simon, D.I., and Plow, E.F., Blood, 2008, vol. 112, pp. 2327–2335.
Bernimoulin, M., Waters, E.K., Foy, M., Steele, B.M., Sullivan, M., Falet, H., Walsh, M.T., Barteneva, N., Geng, J.-G., Hartwig, J.H., Maguire, P.B., and Wagner, D.D., J. Thromb. Haemost., 2009, vol. 7, pp. 1019–1028.
Keerthikumar, S., Gangoda, L., Liem, M., Fonseka, P., Atukorala, I., Ozcitti, C., Mechler, A., Adda, C.G., Ang, C.-S., and Mathivanan, S., Oncotarget, 2015, vol. 6, pp. 15375–15396.
Minciacchi, V.R., You, S., Spinelli, C., Morley, S., Zandian, M., Aspuria, P.-J., Cavallini, L., Ciardiello, C., Reis Sobreiro, M., Morello, M., Kharmate, G., Jang, S.C., Kim, D.-K., Hosseini-Beheshti, E., Tomlinson Guns, E., Gleave, M., Gho, Y.S., Mathivanan, S., Yang, W., Freeman, M.R., and Di Vizio, D., Oncotarget, 2015, vol. 6, pp. 11327–11341.
Lunavat, T.R., Cheng, L., Kim, D.-K., Bhadury, J., Jang, S.C., Lasser, C., Sharples, R.A., Lopez, M.D., Nilsson, J., Gho, Y.S., Hill, A.F., and Lotvall, J., RNA Biol., 2015, vol. 12, pp. 810–823.
Weerheim, A.M., Kolb, A.M., Sturk, A., and Nieuwland, R., Anal. Biochem., 2002, vol. 302, pp. 191–198.
Losito, I., Patruno, R., Conte, E., Cataldi, T.R.I., Megli, F.M., and Palmisano, F., Anal. Chem., 2013, vol. 85, pp. 6405–6413.
Mallat, Z., Hugel, B., Ohan, J., Leseche, G., Freyssinet, J.M., and Tedgui, A., Circulation, 1999, vol. 99, pp. 348–353.
Turiak, L., Misjak, P., Szabo, T.G., Aradi, B., Paloczi, K., Ozohanics, O., Drahos, L., Kittel, A., Falus, A., Buzas, E.I., and Vekey, K., J. Proteomics, 2011, vol. 74, pp. 2025–2033.
Lleo, A., Zhang, W., McDonald, W.H., Seeley, E.H., Leung, P.S.C., Coppel, R.L., Ansari, A.A., Adams, D.H., Afford, S., Invernizzi, P., and Gershwin, M.E., Hepatology, 2014, vol. 60, pp. 1314–1323.
Atkin-Smith, G.K., Tixeira, R., Paone, S., Mathivanan, S., Collins, C., Liem, M., Goodall, K.J., Ravichandran, K.S., Hulett, M.D., and Poon, I.K.H., Nat. Commun., 2015, vol. 6, p. 7439.
Balkwill, F.R., Capasso, M., and Hagemann, T., J. Cell Sci., 2012, vol. 125, pp. 5591–5596.
Koga, K., Matsumoto, K., Akiyoshi, T., Kubo, M., Yamanaka, N., Tasaki, A., Nakashima, H., Nakamura, M., Kuroki, S., Tanaka, M., and Katano, M., Anticancer Res., 2005, vol. 25, pp. 3703–3707.
Demory, Beckler M., Higginbotham, J.N., Franklin, J.L., Ham, A.-J., Halvey, P.J., Imasuen, I.E., Whitwell, C., Li, M., Liebler, D.C., and Coffey, R.J., Mol. Cell Proteomics, 2013, vol. 12, pp. 343–355.
Soldevilla, B., Rodriguez, M., San, Millan C., Garcia, V., Fernandez-Perianez, R., Gil-Calderon, B., Martin, P., Garcia-Grande, A., Silva, J., Bonilla, F., and Dominguez, G., Hum. Mol. Genet., 2014, vol. 23, pp. 467–478.
Qu, J.-L., Qu, X.-J., Zhao, M.-F., Teng, Y.-E., Zhang, Y., Hou, K.-Z., Jiang, Y.-H., Yang, X.-H., and Liu, Y.-P., Dig. Liver Dis., 2009, vol. 41, pp. 875–880.
Kogure, T., Lin, W.-L., Yan, I.K., Braconi, C., and Patel, T., Hepatology, 2011, vol. 54, pp. 1237–1248.
Al-Nedawi, K., Meehan, B., Micallef, J., Lhotak, V., May, L., Guha, A., and Rak, J., Nat. Cell Biol., 2008, vol. 10, pp. 619–624.
Meehan, K. and Vella, L.J., Crit. Rev. Clin. Lab. Sci., 2016, vol. 53, pp. 121–131.
Hoshino, A., Costa-Silva, B., Shen, T.-L., Rodrigues, G., Hashimoto, A., Tesic, Mark M., Molina, H., Kohsaka, S., Di Giannatale, A., Ceder, S., Singh, S., Williams, C., Soplop, N., Uryu, K., Pharmer, L., King, T., Bojmar, L., Davies, A.E., Ararso, Y., Zhang, T., Zhang, H., Hernandez, J., Weiss, J.M., Dumont-Cole, V.D., Kramer, K., Wexler, L.H., Narendran, A., Schwartz, G.K., Healey, J.H., Sandstrom, P., Labori, K.J., Kure, E.H., Grandgenett, P.M., Hollingsworth, M.A., De Sousa, M., Kaur, S., Jain, M., Mallya, K., Batra, S.K., Jarnagin, W.R., Brady, M.S., Fodstad, O., Muller, V., Pantel, K., Minn, A.J., Bissell, M.J., Garcia, B.A., Kang, Y., Rajasekhar, V.K., Ghajar, C.M., Matei, I., Peinado, H., Bromberg, J., and Lyden, D., Nature, 2015, vol. 527, pp. 329–335.
Atay, S., Banskota, S., Crow, J., Sethi, G., Rink, L., and Godwin, A.K., Proc. Natl. Acad. Sci. U. S. A., 2014, vol. 111, pp. 711–716.
Hood, J.L., San, R.S., and Wickline, S.A., Cancer Res., 2011, vol. 71, pp. 3792–3801.
Costa-Silva, B., Aiello, N.M., Ocean, A.J., Singh, S., Zhang, H., Thakur, B.K., Becker, A., Hoshino, A., Mark, M.T., Molina, H., Xiang, J., Zhang, T., Theilen, T.-M., Garcia-Santos, G., Williams, C., Ararso, Y., Huang, Y., Rodrigues, G., Shen, T.-L., Labori, K.J., Lothe, I.M.B., Kure, E.H., Hernandez, J., Doussot, A., Ebbesen, S.H., Grandgenett, P.M., Hollingsworth, M.A., Jain, M., Mallya, K., Batra, S.K., Jarnagin, W.R., Schwartz, R.E., Matei, I., Peinado, H., Stanger, B.Z., Bromberg, J., and Lyden, D., Nat. Cell Biol., 2015, vol. 17, pp. 816–826.
Ostenfeld, M.S., Jeppesen, D.K., Laurberg, J.R., Boysen, A.T., Bramsen, J.B., Primdal-Bengtson, B., Hendrix, A., Lamy, P., Dagnaes-Hansen, F., Rasmussen, M.H., Bui, K.H., Fristrup, N., Christensen, E.I., Nordentoft, I., Morth, J.P., Jensen, J.B., Pedersen, J.S., Beck, M., Theodorescu, D., Borre, M., Howard, K.A., Dyrskjot, L., and Orntoft, T.F., Cancer Res., 2014, vol. 74, pp. 5758–5771.
Elmageed, Z.Y., Yang, Y., Thomas, R., Ranjan, M., Mondal, D., Moroz, K., Fang, Z., Rezk, B.M., Moparty, K., Sikka, S.C., Sartor, O., and Abdel-Mageed, A.B., Stem. Cells, 2014, vol. 32, pp. 983–997.
Ristorcelli, E., Beraud, E., Mathieu, S., Lombardo, D., and Verine, A., Int. J. Cancer, 2009, vol. 125, pp. 1016–1026.
Koga, K., Matsumoto, K., Akiyoshi, T., Kubo, M., Yamanaka, N., Tasaki, A., Nakashima, H., Nakamura, M., Kuroki, S., Tanaka, M., and Katano, M., Anticancer Res., 2005, vol. 25, pp. 3703–3707.
Yang, L., Wu, X.-H., Wang, D., Luo, C.-L., and Chen, L.-X., Mol. Med. Rep., 2013, vol. 8, pp. 1272–1278.
Cappellesso, R., Tinazzi, A., Giurici, T., Simonato, F., Guzzardo, V., Ventura, L., Crescenzi, M., Chiarelli, S., and Fassina, A., Cancer Cytopathol., 2014, vol. 122, pp. 685–693.
Kahlert, C., Melo, S.A., Protopopov, A., Tang, J., Seth, S., Koch, M., Zhang, J., Weitz, J., Chin, L., Futreal, A., and Kalluri, R., J. Biol. Chem., 2014, vol. 289, pp. 3869–3875.
Wang, J., Hendrix, A., Hernot, S., Lemaire, M., De Bruyne, E., van Valckenborgh, E., Lahoutte, T., de Wever, O., Vanderkerken, K., and Menu, E., Blood, 2014, vol. 124, pp. 555–566.
Federici, C., Petrucci, F., Caimi, S., Cesolini, A., Logozzi, M., Borghi, M., D’Ilio, S., Lugini, L., Violante, N., Azzarito, T., Majorani, C., Brambilla, D., and Fais, S., PLoS One, 2014, vol. 9, e88193.
Safaei, R., Larson, B.J., Cheng, T.C., Gibson, M.A., Otani, S., Naerdemann, W., and Howell, S.B., Mol. Cancer Ther., 2005, vol. 4, pp. 1595–1604.
Shedden, K., Xie, X.T., Chandaroy, P., Chang, Y.T., and Rosania, G.R., Cancer Res., 2003, vol. 63, pp. 4331–4337.
Ciravolo, V., Huber, V., Ghedini, G.C., Venturelli, E., Bianchi, F., Campiglio, M., Morelli, D., Villa, A., Della, Mina P., Menard, S., Filipazzi, P., Rivoltini, L., Tagliabue, E., and Pupa, S.M., J. Cell Physiol., 2012, vol. 227, pp. 658–667.
Aung, T., Chapuy, B., Vogel, D., Wenzel, D., Oppermann, M., Lahmann, M., Weinhage, T., Menck, K., Hupfeld, T., Koch, R., Trumper, L., and Wulf, G.G., Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, pp. 15336–15341.
Xiao, X., Yu, S., Li, S., Wu, J., Ma, R., Cao, H., Zhu, Y., and Feng, J., PLoS One, 2014, vol. 9, e89534.
Corcoran, C., Rani, S., O’Brien, K., O’Neill, A., Prencipe, M., Sheikh, R., Webb, G., McDermott, R., Watson, W., Crown, J., and O’Driscoll, L., PLoS One, 2012, vol. 7, e50999.
Corcoran, C., Rani, S., and O’Driscoll, L., Prostate, 2014, vol. 74, pp. 1320–1334.
Challagundla, K.B., Wise, P.M., Neviani, P., Chava, H., Murtadha, M., Xu, T., Kennedy, R., Ivan, C., Zhang, X., Vannini, I., Fanini, F., Amadori, D., Calin, G.A., Hadjidaniel, M., Shimada, H., Jong, A., Seeger, R.C., Asgharzadeh, S., Goldkorn, A., and Fabbri, M., J. Natl. Cancer Inst., 2015, vol. 107, djv135.
Takahashi, K., Yan, I.K., Kogure, T., Haga, H., and Patel, T., FEBS Open Bio, 2014, vol. 4, pp. 458–467.
Hu, Y., Yan, C., Mu, L., Huang, K., Li, X., Tao, D., Wu, Y., and Qin, J., PLoS One, 2015, vol. 10, e0125625.
King, H.W., Michael, M.Z., and Gleadle, J.M., BMC Cancer, 2012, vol. 12, p. 421.
Umezu, T., Tadokoro, H., Azuma, K., Yoshizawa, S., Ohyashiki, K., and Ohyashiki, J.H., Blood, 2014, vol. 124, pp. 3748–3757.
Svensson, K.J., Kucharzewska, P., Christianson, H.C., Skold, S., Lofstedt, T., Johansson, M.C., Morgelin, M., Bengzon, J., Ruf, W., and Belting, M., Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, pp. 13147–13152.
Kucharzewska, P., Christianson, H.C., Welch, J.E., Svensson, K.J., Fredlund, E., Ringnér, M., Mörgelin, M., Bourseau-Guilmain, E., Bengzon, J., and Belting, M., Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, pp. 7312–7317.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © N.A. Logvina, V.O. Shender, G.P. Arapidi, T.D. Holina, 2018, published in Bioorganicheskaya Khimiya, 2018, Vol. 44, No. 2, pp. 113–125.
Rights and permissions
About this article
Cite this article
Logvina, N.A., Shender, V.O., Arapidi, G.P. et al. A Role of Vesicular Transduction of Intercellular Signals in Cancer Development. Russ J Bioorg Chem 44, 129–139 (2018). https://doi.org/10.1134/S1068162018010120
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1068162018010120