Russian Journal of Bioorganic Chemistry

, Volume 44, Issue 2, pp 129–139 | Cite as

A Role of Vesicular Transduction of Intercellular Signals in Cancer Development

  • N. A. Logvina
  • V. O. Shender
  • G. P. Arapidi
  • T. D. Holina
Review Article


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.


transduction of intercellular signals exosomes extracellular vesicles cancers 



apoptotic bodies


an extracellular vesicle


multivesicular bodies


the disintegrin and metalloproteinase domain 10


the alpha serine/threonine-protein kinase


the B-cell lymphoma 2


the Bcl-2-like protein 11


the baculoviral inhibitor of apoptosis repeat-containing 5


the brain-specific homeobox protein homolog


the C-X-C chemokine receptor type 2


a cluster of differentiation


the EH domain-containing protein 1, where EH is the EPS15 homologue and EPS15 is the epidermal growth factor receptor substrate 15


the epidermal growth factor


the receptor of the epidermal growth factor


the endosomal sorting complex required for transport


the extracellular matrix metalloproteinase inducer


an epithelial cell adhesion molecule


the epidermal growth factor receptor kinase substrate 8-like protein 2


the ETS-related gene


erythroblast transformation-specific


extracellular signal–regulated kinases


glypican 1


the human epidermal growth factor receptor 2


heat shock proteins




the c-Jun N-terminal kinase


the L1 cell adhesion molecule


the mitogen-activated protein kinase


the major histocompatibility complex


a micro-RNA


the myosin light-chain kinase


the nuclear factor kappa-lightchain- enhancer of activated B cells


a prostate cancer antigen


the programmed cell death protein 4


phosphoinositide 3-kinase


phospholipase D


phosphatase and tensin homolog deleted on chromosome 10


the Ras-related protein in brain


the rat sarcoma


the ρ Greek letter


the rho-associated, coiled-coil-containing protein kinase 1




the transforming growth factor


the transmembrane serine protease 2


the tumor susceptibility gene 101


the tyrosinase-related protein 2


the vascular endothelial growth factor


the vacuolar protein sorting- associated protein 4


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Chargaff, E. and West, R., J. Biol. Chem., 1946, vol. 166, pp. 189–197.PubMedGoogle Scholar
  2. 2.
    Knox, K.W., Vesk, M., and Work, E., J. Bacteriol., 1966, vol. 92, pp. 1206–1217.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Soler, N., Marguet, E., Verbavatz, J.-M., and Forterre, P., Res. Microbiol., 2008, vol. 159, pp. 390–399.PubMedCrossRefGoogle Scholar
  4. 4.
    Kalra, H., Drummen, G.P.C., and Mathivanan, S., Int. J. Mol. Sci., 2016, vol. 17, p. 170.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Bobrie, A., Colombo, M., Raposo, G., and Thery, C., Traffic, 2011, vol. 12, pp. 1659–1668.PubMedCrossRefGoogle Scholar
  6. 6.
    Raposo, G. and Stoorvogel, W., J. Cell Biol., 2013, vol. 200, pp. 373–383.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    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.PubMedCrossRefGoogle Scholar
  8. 8.
    Pols, M.S. and Klumperman, J., Exp. Cell Res., 2009, vol. 315, pp. 1584–1592.PubMedCrossRefGoogle Scholar
  9. 9.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Stuffers, S., Sem, Wegner C., Stenmark, H., and Brech, A., Traffic, 2009, vol. 10, pp. 925–937.PubMedCrossRefGoogle Scholar
  11. 11.
    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.PubMedCrossRefGoogle Scholar
  12. 12.
    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.PubMedCrossRefGoogle Scholar
  13. 13.
    Bevers, E.M. and Williamson, P.L., FEBS Lett., 2010, vol. 584, pp. 2724–2730.PubMedCrossRefGoogle Scholar
  14. 14.
    Daleke, D.L., J. Lipid Res., 2003, vol. 44, pp. 233–242.PubMedCrossRefGoogle Scholar
  15. 15.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Lane, J.D., Allan, V.J., and Woodman, P.G., J. Cell Sci., 2005, vol. 118, pp. 4059–4071.PubMedCrossRefGoogle Scholar
  17. 17.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Sebbagh, M., Renvoize, C., Hamelin, J., Riche, N., Bertoglio, J., and Breard, J., Nat. Cell Biol., 2001, vol. 3, pp. 346–352.PubMedCrossRefGoogle Scholar
  19. 19.
    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.PubMedCrossRefGoogle Scholar
  20. 20.
    Suzuki, J., Denning, D.P., Imanishi, E., Horvitz, H.R., and Nagata, S., Science, 2013, vol. 341, pp. 403–406.PubMedCrossRefGoogle Scholar
  21. 21.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Mathivanan, S., Ji, H., and Simpson, R.J., J. Proteomics, 2010, vol. 73, pp. 1907–1920.PubMedCrossRefGoogle Scholar
  23. 23.
    Yakimchuk, K., Devices Methods Measurements, 2015, vol. 5, pp. 228–235.Google Scholar
  24. 24.
    Subra, C., Laulagnier, K., Perret, B., and Record, M., Biochimie, 2007, vol. 89, pp. 205–212.PubMedCrossRefGoogle Scholar
  25. 25.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Lydic, T.A., Townsend, S., Adda, C.G., Collins, C., Mathivanan, S., and Reid, G.E., Methods, 2015, vol. 87, pp. 83–95.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    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.PubMedCrossRefGoogle Scholar
  28. 28.
    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.PubMedCrossRefGoogle Scholar
  29. 29.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    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.PubMedCrossRefGoogle Scholar
  31. 31.
    Saunderson, S.C., Dunn, A.C., Crocker, P.R., and McLellan, A.D., Blood, 2014, vol. 123, pp. 208–216.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J.J., and Lotvall, J.O., Nat. Cell Biol., 2007, vol. 9, pp. 654–659.PubMedCrossRefGoogle Scholar
  34. 34.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Zhang, X., Yuan, X., Shi, H., Wu, L., Qian, H., and Xu, W., J. Hematol. Oncol., 2015, vol. 8, p. 83.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Howitt, J. and Hill, A.F., J. Biol Chem., 2016, vol. 291, p. 26589–26597.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    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.PubMedCrossRefGoogle Scholar
  42. 42.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    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.PubMedCrossRefGoogle Scholar
  45. 45.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    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.PubMedCrossRefGoogle Scholar
  48. 48.
    Turchinovich, A., Weiz, L., Langheinz, A., and Burwinkel, B., Nucleic Acids Res., 2011, vol. 39, pp. 7223–7233.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Gallo, A., Tandon, M., Alevizos, I., and Illei, G.G., PLoS One, 2012, vol. 7, e30679.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Yu, S., Cao, H., Shen, B., and Feng, J., Oncotarget, 2015, vol. 6, pp. 37151–37168.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Taylor, D.D. and Gercel-Taylor, C., Gynecol. Oncol., 2008, vol. 110, pp. 13–21.PubMedCrossRefGoogle Scholar
  52. 52.
    Rabinowits, G., Gercel-Taylor, C., Day, J.M., Taylor, D.D., and Kloecker, G.H., Clin. Lung Cancer, 2009, vol. 10, pp. 42–46.PubMedCrossRefGoogle Scholar
  53. 53.
    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.PubMedCrossRefGoogle Scholar
  54. 54.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    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.PubMedCrossRefGoogle Scholar
  56. 56.
    Tanaka, Y., Kamohara, H., Kinoshita, K., Kurashige, J., Ishimoto, T., Iwatsuki, M., Watanabe, M., and Baba, H., Cancer, 2013, vol. 119, pp. 1159–1167.PubMedCrossRefGoogle Scholar
  57. 57.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Corcoran, C., Friel, A.M., Duffy, M.J., Crown, J., and O’Driscoll, L., Clin. Chem., 2011, vol. 57, pp. 18–32.PubMedCrossRefGoogle Scholar
  59. 59.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Del Conde, I., Shrimpton, C.N., Thiagarajan, P., and Lopez, J.A., Blood, 2005, vol. 106, pp. 1604–1611.PubMedCrossRefGoogle Scholar
  61. 61.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Mezouar, S., Darbousset, R., Dignat-George, F., Panicot-Dubois, L., and Dubois, C., Int. J. Cancer, 2015, vol. 136, pp. 462–475.PubMedCrossRefGoogle Scholar
  63. 63.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Weerheim, A.M., Kolb, A.M., Sturk, A., and Nieuwland, R., Anal. Biochem., 2002, vol. 302, pp. 191–198.PubMedCrossRefGoogle Scholar
  69. 69.
    Losito, I., Patruno, R., Conte, E., Cataldi, T.R.I., Megli, F.M., and Palmisano, F., Anal. Chem., 2013, vol. 85, pp. 6405–6413.PubMedCrossRefGoogle Scholar
  70. 70.
    Mallat, Z., Hugel, B., Ohan, J., Leseche, G., Freyssinet, J.M., and Tedgui, A., Circulation, 1999, vol. 99, pp. 348–353.PubMedCrossRefGoogle Scholar
  71. 71.
    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.PubMedCrossRefGoogle Scholar
  72. 72.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Balkwill, F.R., Capasso, M., and Hagemann, T., J. Cell Sci., 2012, vol. 125, pp. 5591–5596.PubMedCrossRefGoogle Scholar
  75. 75.
    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.PubMedGoogle Scholar
  76. 76.
    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.CrossRefGoogle Scholar
  77. 77.
    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.PubMedCrossRefGoogle Scholar
  78. 78.
    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.PubMedCrossRefGoogle Scholar
  79. 79.
    Kogure, T., Lin, W.-L., Yan, I.K., Braconi, C., and Patel, T., Hepatology, 2011, vol. 54, pp. 1237–1248.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    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.PubMedCrossRefGoogle Scholar
  81. 81.
    Meehan, K. and Vella, L.J., Crit. Rev. Clin. Lab. Sci., 2016, vol. 53, pp. 121–131.PubMedCrossRefGoogle Scholar
  82. 82.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    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.PubMedCrossRefGoogle Scholar
  84. 84.
    Hood, J.L., San, R.S., and Wickline, S.A., Cancer Res., 2011, vol. 71, pp. 3792–3801.PubMedCrossRefGoogle Scholar
  85. 85.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    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.PubMedCrossRefGoogle Scholar
  87. 87.
    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.CrossRefGoogle Scholar
  88. 88.
    Ristorcelli, E., Beraud, E., Mathieu, S., Lombardo, D., and Verine, A., Int. J. Cancer, 2009, vol. 125, pp. 1016–1026.PubMedCrossRefGoogle Scholar
  89. 89.
    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.PubMedGoogle Scholar
  90. 90.
    Yang, L., Wu, X.-H., Wang, D., Luo, C.-L., and Chen, L.-X., Mol. Med. Rep., 2013, vol. 8, pp. 1272–1278.PubMedCrossRefGoogle Scholar
  91. 91.
    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.PubMedCrossRefGoogle Scholar
  92. 92.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    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.PubMedCrossRefGoogle Scholar
  94. 94.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    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.PubMedCrossRefGoogle Scholar
  96. 96.
    Shedden, K., Xie, X.T., Chandaroy, P., Chang, Y.T., and Rosania, G.R., Cancer Res., 2003, vol. 63, pp. 4331–4337.PubMedGoogle Scholar
  97. 97.
    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.PubMedCrossRefGoogle Scholar
  98. 98.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Xiao, X., Yu, S., Li, S., Wu, J., Ma, R., Cao, H., Zhu, Y., and Feng, J., PLoS One, 2014, vol. 9, e89534.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Corcoran, C., Rani, S., and O’Driscoll, L., Prostate, 2014, vol. 74, pp. 1320–1334.PubMedCrossRefGoogle Scholar
  102. 102.
    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.Google Scholar
  103. 103.
    Takahashi, K., Yan, I.K., Kogure, T., Haga, H., and Patel, T., FEBS Open Bio, 2014, vol. 4, pp. 458–467.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Hu, Y., Yan, C., Mu, L., Huang, K., Li, X., Tao, D., Wu, Y., and Qin, J., PLoS One, 2015, vol. 10, e0125625.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    King, H.W., Michael, M.Z., and Gleadle, J.M., BMC Cancer, 2012, vol. 12, p. 421.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Umezu, T., Tadokoro, H., Azuma, K., Yoshizawa, S., Ohyashiki, K., and Ohyashiki, J.H., Blood, 2014, vol. 124, pp. 3748–3757.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    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.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • N. A. Logvina
    • 1
  • V. O. Shender
    • 1
  • G. P. Arapidi
    • 1
  • T. D. Holina
    • 1
  1. 1.Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of SciencesMoscow GSP-7Russia

Personalised recommendations