Skip to main content
Log in

A Role of Vesicular Transduction of Intercellular Signals in Cancer Development

  • Review Article
  • Published:
Russian Journal of Bioorganic Chemistry Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

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

  1. Chargaff, E. and West, R., J. Biol. Chem., 1946, vol. 166, pp. 189–197.

    CAS  PubMed  Google Scholar 

  2. Knox, K.W., Vesk, M., and Work, E., J. Bacteriol., 1966, vol. 92, pp. 1206–1217.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Soler, N., Marguet, E., Verbavatz, J.-M., and Forterre, P., Res. Microbiol., 2008, vol. 159, pp. 390–399.

    Article  CAS  PubMed  Google Scholar 

  4. Kalra, H., Drummen, G.P.C., and Mathivanan, S., Int. J. Mol. Sci., 2016, vol. 17, p. 170.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Bobrie, A., Colombo, M., Raposo, G., and Thery, C., Traffic, 2011, vol. 12, pp. 1659–1668.

    Article  CAS  PubMed  Google Scholar 

  6. Raposo, G. and Stoorvogel, W., J. Cell Biol., 2013, vol. 200, pp. 373–383.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  8. Pols, M.S. and Klumperman, J., Exp. Cell Res., 2009, vol. 315, pp. 1584–1592.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Stuffers, S., Sem, Wegner C., Stenmark, H., and Brech, A., Traffic, 2009, vol. 10, pp. 925–937.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  13. Bevers, E.M. and Williamson, P.L., FEBS Lett., 2010, vol. 584, pp. 2724–2730.

    Article  CAS  PubMed  Google Scholar 

  14. Daleke, D.L., J. Lipid Res., 2003, vol. 44, pp. 233–242.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lane, J.D., Allan, V.J., and Woodman, P.G., J. Cell Sci., 2005, vol. 118, pp. 4059–4071.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sebbagh, M., Renvoize, C., Hamelin, J., Riche, N., Bertoglio, J., and Breard, J., Nat. Cell Biol., 2001, vol. 3, pp. 346–352.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  20. Suzuki, J., Denning, D.P., Imanishi, E., Horvitz, H.R., and Nagata, S., Science, 2013, vol. 341, pp. 403–406.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Mathivanan, S., Ji, H., and Simpson, R.J., J. Proteomics, 2010, vol. 73, pp. 1907–1920.

    Article  CAS  PubMed  Google Scholar 

  23. Yakimchuk, K., Devices Methods Measurements, 2015, vol. 5, pp. 228–235.

    Google Scholar 

  24. Subra, C., Laulagnier, K., Perret, B., and Record, M., Biochimie, 2007, vol. 89, pp. 205–212.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Lydic, T.A., Townsend, S., Adda, C.G., Collins, C., Mathivanan, S., and Reid, G.E., Methods, 2015, vol. 87, pp. 83–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  31. Saunderson, S.C., Dunn, A.C., Crocker, P.R., and McLellan, A.D., Blood, 2014, vol. 123, pp. 208–216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zhang, X., Yuan, X., Shi, H., Wu, L., Qian, H., and Xu, W., J. Hematol. Oncol., 2015, vol. 8, p. 83.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Howitt, J. and Hill, A.F., J. Biol Chem., 2016, vol. 291, p. 26589–26597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  48. Turchinovich, A., Weiz, L., Langheinz, A., and Burwinkel, B., Nucleic Acids Res., 2011, vol. 39, pp. 7223–7233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Gallo, A., Tandon, M., Alevizos, I., and Illei, G.G., PLoS One, 2012, vol. 7, e30679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Yu, S., Cao, H., Shen, B., and Feng, J., Oncotarget, 2015, vol. 6, pp. 37151–37168.

    PubMed  PubMed Central  Google Scholar 

  51. Taylor, D.D. and Gercel-Taylor, C., Gynecol. Oncol., 2008, vol. 110, pp. 13–21.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Corcoran, C., Friel, A.M., Duffy, M.J., Crown, J., and O’Driscoll, L., Clin. Chem., 2011, vol. 57, pp. 18–32.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Del Conde, I., Shrimpton, C.N., Thiagarajan, P., and Lopez, J.A., Blood, 2005, vol. 106, pp. 1604–1611.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Mezouar, S., Darbousset, R., Dignat-George, F., Panicot-Dubois, L., and Dubois, C., Int. J. Cancer, 2015, vol. 136, pp. 462–475.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Weerheim, A.M., Kolb, A.M., Sturk, A., and Nieuwland, R., Anal. Biochem., 2002, vol. 302, pp. 191–198.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  70. Mallat, Z., Hugel, B., Ohan, J., Leseche, G., Freyssinet, J.M., and Tedgui, A., Circulation, 1999, vol. 99, pp. 348–353.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Balkwill, F.R., Capasso, M., and Hagemann, T., J. Cell Sci., 2012, vol. 125, pp. 5591–5596.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  79. Kogure, T., Lin, W.-L., Yan, I.K., Braconi, C., and Patel, T., Hepatology, 2011, vol. 54, pp. 1237–1248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  81. Meehan, K. and Vella, L.J., Crit. Rev. Clin. Lab. Sci., 2016, vol. 53, pp. 121–131.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  84. Hood, J.L., San, R.S., and Wickline, S.A., Cancer Res., 2011, vol. 71, pp. 3792–3801.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  88. Ristorcelli, E., Beraud, E., Mathieu, S., Lombardo, D., and Verine, A., Int. J. Cancer, 2009, vol. 125, pp. 1016–1026.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  90. Yang, L., Wu, X.-H., Wang, D., Luo, C.-L., and Chen, L.-X., Mol. Med. Rep., 2013, vol. 8, pp. 1272–1278.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  96. Shedden, K., Xie, X.T., Chandaroy, P., Chang, Y.T., and Rosania, G.R., Cancer Res., 2003, vol. 63, pp. 4331–4337.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Xiao, X., Yu, S., Li, S., Wu, J., Ma, R., Cao, H., Zhu, Y., and Feng, J., PLoS One, 2014, vol. 9, e89534.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Corcoran, C., Rani, S., and O’Driscoll, L., Prostate, 2014, vol. 74, pp. 1320–1334.

    Article  CAS  PubMed  Google Scholar 

  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. Takahashi, K., Yan, I.K., Kogure, T., Haga, H., and Patel, T., FEBS Open Bio, 2014, vol. 4, pp. 458–467.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Hu, Y., Yan, C., Mu, L., Huang, K., Li, X., Tao, D., Wu, Y., and Qin, J., PLoS One, 2015, vol. 10, e0125625.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. King, H.W., Michael, M.Z., and Gleadle, J.M., BMC Cancer, 2012, vol. 12, p. 421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Umezu, T., Tadokoro, H., Azuma, K., Yoshizawa, S., Ohyashiki, K., and Ohyashiki, J.H., Blood, 2014, vol. 124, pp. 3748–3757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. A. Logvina.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1068162018010120

Keywords

Navigation