EXTRACELLULAR VESICLES: CLASSIFICATION, FUNCTIONS AND CLINICAL RELEVANCE A. V. Oberemko, A. G. Popandopulo

Details: Hits: 550

ISSN 2410-7751 (Print)
ISSN 2410-776X (Online)

6 2014

"Biotechnologia Acta" v. 7, no 6, 2014
https://doi.org/10.15407/biotech7.06.102
Р. 102-108, Bibliography 56, English
Universal Decimal classification: 576.314.63.004.15:005]:617-089.844

EXTRACELLULAR VESICLES: CLASSIFICATION, FUNCTIONS AND CLINICAL RELEVANCE

A. V. Oberemko, A. G. Popandopulo

Government Institution «Institute of Urgent and Recovery Surgery named after Gusak of
Ukrainian National Academy of Medical Sciences», Donetsk

This review presents a generalized definition of vesicles as bilayer extracellular organelles of all celular forms of life: not only eu-, but also prokaryotic. The structure and composition of extracellular vesicles, history of research, nomenclature, their impact on life processes in health and disease are discussed. Moreover, vesicles may be useful as clinical instruments for biomarkers, and they are promising as biotechnological drug. However, many questions in this area are still unresolved and need to be addressed in the future.

The most interesting from the point of view of practical health care represents a direction to study the effect of exosomes and microvesicles in the development and progression of a particular disease, the possibility of adjusting the pathological process by means of extracellular vesicles of a particular type, acting as an active ingredient. Relevant is the further elucidation of the role and importance of exosomes to the surrounding cells, tissues and organs at the molecular level, the prospects for the use of non-cellular vesicles as biomarkers of disease.

Key words: exosomes, microvesicles.

References

1. Schwechheimer C., Kuehn M. J. Synthetic effect between envelope stress and lack of outer membrane vesicle production in Escherichia coli. J. Bacteriol. 2013, 195 (18), 4161–4173. doi: 10.1128/JB.02192-12.

2. Witwer K. W., Buz?s E. I., Bemis L. T., Bora A., L?sser C., L?tvall J., Nolte-’t Hoen E. N., Piper M. G., Sivaraman S., Skog J., Th?ry C., Wauben M. H., Hochberg F. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J. Extracell. Vesicles. 2013, V. 2, P. 20360. doi: 10.3402/jev.v2i0.20360.

3. Van der Pol E., B?ing A. N., Harrison P., Sturk A., Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol. Rev. 2012, V. 64, P. 676–705. doi: 10.1124/pr.112.005983.

4. Chargaff E., West R. The biological significance of the thromboplastic protein of blood. J. Biol. Chem. 1946, V. 166, P. 189–197.

5. Wolf P. The nature and significance of platelet products in human plasma. British J. Haematology. 1967, 13 (3), 269–288.
http://dx.doi.org/10.1111/j.1365-2141.1967.tb08741.x

6. L?tvall J., Rajendran L., Gho Y. S., Thery C., Wauben M., Raposo G., Sj?strand M., Taylor D., Telemo E., Breakefield X. O. The launch of Journal of Extracellular Vesicles (JEV), the official journal of the International Society for Extracellular Vesicles — about microvesicles, exosomes, ectosomes and other extracellular vesicles. Extracell. Vesicles. 2012, V. 1, P. 18514. doi: 10.3402/jev.v1i0.18514.

7. Crawford N. The presence of contractile proteins in platelet microparticles isolated from human and animal platelet-free plasma. British J. Haematology. 1971, 21(1), 53–69.
http://dx.doi.org/10.1111/j.1365-2141.1971.tb03416.x

8. Davis J. S., Lie J. T. Extracellular glomerular microparticles in nephrotic syndrome of heroin users. Arch Pathol. 1975, 99(5), 278–282.

9. Johnstone R. M, Adam M., Hammond J. R., Orr L., Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. boil. chem. 1987, 262(19), 9412–9420.

10. Johnstone R. M., Bianchini A., Teng K. Reticulocyte maturation and exosome release: transferrin receptor containing exosomes shows multiple plasma membrane functions. Blood. 1989, V. 74, P. 1844–1851.

11. Johnstone R. M., Mathew A., Mason A. B., Teng K. Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins. J. Cell Physiol. 1991, 147(1), 27–36.
http://dx.doi.org/10.1002/jcp.1041470105

12. Harding C. V., Heuser J. E., Stahl P. D. Exosomes: looking back three decades and into the future. J. Cell Biol. 2013, 200(4), 367–371. doi: 10.1083/jcb.201212113.

13. Morel O., Jesel L., Freyssinet J. M., Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb. Vasc. Biol. 2011, 31(1), 15–26. doi: 10.1161/ATVBAHA.109.200956.

14. Baryshnikov A. Ju., Shishkin Ju. V. Immunological problems of apoptosis. Moscow: Jeditorial URSS. 2002, 320 p.

15. Sohel M. M., Hoelker M., Noferesti S. S., Salilew-Wondim D., Tholen E., Looft C., Rings F., Uddin M. J., Spencer T. E., Schellander K., Tesfaye D. Exosomal and non-exosomal transport of extracellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS One. 2013, 8(11), 78505. doi: 10.1371/journal.pone.0078505.

16. Christianson H. C., Svensson K. J., van Kuppevelt T. H., Li J. P., Belting M. Cancer cell exosomes depend on cell-surface heparin sulfate proteoglycans for their internalization and functional activity. PNAS. 2013, 110 (43), 17380–17385. doi: 10.1073/pnas.1304266110.

17. Christianson H. C., Belting M. Heparan sulfate proteoglycan as a cell-surface endocytosis receptor. Matrix Biol. 2014, V. 35, P. 51–55. doi: 10.1016/j.matbio. 2013.10.004.

18. Johnstone R. M. Cleavage of the transferrin receptor by human granulocytes: differential proteolysis of the exosome-bound TFR. J. Cell Physiol. 1996, 168(2), 333–345.
http://dx.doi.org/10.1002/(SICI)1097-4652(199608)168:2<333::AID-JCP12>3.0.CO;2-4

19. Huang X., Yuan T., Tschannen M., Sun Z., Jacob H., Du M., Liang M., Dittmar R. L., Liu Y., Liang M., Kohli M., Thibodeau S. N., Boardman L., Wang L. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics. 2013, V. 14, P. 319. doi: 10.1186/1471-2164-14-319.

20. Guescini M., Guidolin D., Vallorani L., Casadei L., Gioacchini A. M., Tibollo P., Battistelli M., Falcieri E., Battistin L., Agnati L. F., Stocchi V. C2C12 myoblasts release microvesicles containing mtDNA and proteins involved in signal transduction. Exp. Cell Res. 2010, 316(12), 1977–1984. doi: 10.1016/j.yexcr.2010.04.006.

21. Kahlert C., Melo S. A., Protopopov A., Tang J., Seth S., Koch M., Zhang J., Weitz J., Chin L., Futreal A., Kalluri R. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J. Biol. Chem. 2014, 289(7), 3869–3875. doi: 10.1074/jbc.C 113.532267.

22. 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., Lyden D. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 2014, 24(6), 766–769. doi: 10.1038/cr.2014.44.

23. Forterre A., Jalabert A., Chikh K., Pesenti S., Euthine V., Granjon A., Errazuriz E., Lefai E., Vidal H., Rome S. Myotube-derived exosomal miRNAs downregulate Sirtuin1 in myoblasts during muscle cell differentiation. Cell Cycle. 2014, 13(1), 78–89. doi: 10.4161/cc.26808.

24. Raposo G., Nijman H. W., Stoorvogel W., Liejendekker R., Harding C. V., Melief C. J., Geuze H. J. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 1996, 183(3), 1161–1172.
http://dx.doi.org/10.1084/jem.183.3.1161

25. Luketic L., Delanghe J., Sobol P. T., Yang P., Frotten E., Mossman K. L., Gauldie J., Bramson J., Wan Y. Antigen presentation by exosomes released from peptide-pulsed dendritic cells is not suppressed by the presence of active CTL. J. Immunol. 2007, 11(8), 5024–5032.
http://dx.doi.org/10.4049/jimmunol.179.8.5024

26. Reinhardt T. A., Lippolis J. D., Nonnecke B. J., Sacco R. E. Bovine milk exosome proteome. J. Proteomics. 2012, 75(5), 1486–1492. doi: 10.1016/j.jprot.2011.11.017.

27. Gupta A., Pulliam L. Exosomes as mediators of neuroinflammation. J. Neuroinflammation. 2014, V. 11, P. 68. doi: 10.1186/1742-2094-11-68.

28. Mathew A., Bell A., Johnstone R. M. Hsp-70 is closely associated with the transferrin receptor in exosomes from maturing reticulocytes. Biochem. J. 1995, 308(3), 823–830.

29. Liu A. M., Xu Z., Shek F. H., Wong K. F., Lee N. P., Poon R. T., Chen J., Luk J. M. miR-122 targets pyruvate kinase M2 and affects metabolism of hepatocellular carcinoma. PLoS One. 2014, 9(1), e86872. doi: 10.1371/journal.pone.0086872.

30. Hulsmans M., Holvoent P. MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease. Cardiovascular Research. 2013, V. 100, P. 7–18. doi: 10.1093/cvr/cvt161.

31. Ismail N., Wang Y., Dakhlallah D., Moldovan L., Agarwal K., Batte K., Shah P., Wisler J., Eubank T. D., Tridandapani S., Paulaitis M. E., Piper M. G., Marsh C. B. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood. 2013, 121(6), 984–995. doi: 10.1182/blood-2011-08-374793.

32. Kshirsagar S. K., Alam S. M., Jasti S., Hodes H., Nauser T., Gilliam M., Billstrand C., Hunt J. S., Petroff M. G. Immunomodulatory molecules are released from the first trimester and term placenta via exosomes. Placenta. 2012, 33(12), 982–990. doi: 10.1016/j.placenta.2012.10.005.

33. Melnik B. C., John S. M., Schmitz G. Milk: an exosomal microRNA transmitter promoting thymic regulatory T cell maturation preventing the development of atopy? J. Transl. Med. 2014, V. 12, P. 43. doi: 10.1186/1479-5876-12-43.

34. Zhang L., Hou D., Chen X., Li D., Zhu L., Zhang Y., Li J., Bian Z., Liang X., Cai X., Yin Y., Wang C., Zhang T., Zhu D., Zhang D., Xu J., Chen Q., Ba Y., Liu J., Wang Q., Chen J., Wang J., Wang M., Zhang Q., Zhang J., Zen K., Zhang C. Y. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res. 2012, 22(1), 107–126. doi: 10.1038/cr.2011.158.

35. Smythies J., Edelstein L. Telocytes, exosomes, gap junctions and the cytoskeleton: the makings of a primitive nervous system? Front Cell Neurosci. 2014, V. 7, P. 278. doi: 10.3389/fncel.2013.00278.

36. Gu J., Qian H., Shen L., Zhang X., Zhu W., Huang L., Yan Y., Mao F., Zhao C., Shi Y., Xu W. Gastric cancer exosomes trigger differentiation of umbilical cord derived mesenchymal stem cells to carcinoma-associated fibroblasts through TGF-?/Smad pathway. PLoS ONE. 2012, 7(12), e52465. doi: 10.1371/journal.pone.0052465.

37. Whiteside T. L. Immune modulation of T-cell and NK (natural killer) cell activities by TEXs (tumour-derived exosomes). Biochem. Soc. Trans. 2013, 41(1), 245–251. doi: 10.1042/BST20120265.

38. Dutta S., Warshall C., Bandyopadhyay C., Dutta D., Chandran B. Interactions between Exosomes from Breast Cancer Cells and Primary Mammary Epithelial Cells Leads to Generation of Reactive Oxygen Species Which Induce DNA Damage Response, Stabilization of p53 and Autophagy in Epithelial Cells. PLoS One. 2014, 9 (5), e97580. doi: 10.1371/journal.pone.0097580.

39. Cosset F. L., Dreux M. HCV transmission by hepatic exosomes establishes a productive infection. J. Hepatol. 2014, 60 (3), 674–675. doi: 10.1016/j.jhep.2013.10.015.

40. Arenaccio C., Chiozzini C., Columba-Cabezas S., Manfredi F., Federico M. Cell activation and HIV-1 replication in unstimulated CD4+ T-lymphocytes ingesting exosomes from cells expressing defective HIV-1. Retrovirology. 2014, 11(1), 46.

41. Bang C., Batkai S., Dangwal S., Gupta S. K., Foinquinos A., Holzmann A., Just A., Remke J., Zimmer K., Zeug A., Ponimaskin E., Schmiedl A., Yin X., Mayr M., Halder R., Fischer A., Engelhardt S., Wei Y., Schober A., Fiedler J., Thum T. Cardiac fibroblast-derived microRNA passenger strand-enriched exosomes mediate cardiomyocyte hypertrophy. J. Clin. Invest. 2014, 124(5), 2136–2146. doi: 10.1172/JCI70577.

42. Li T., Yan Y., Wang B., Qian H., Zhang X., Shen L., Wang M., Zhou Y., Zhu W., Li W., Xu W. Exosomes derived from human umbilical cord mesenchymal stem cells alleviate liver fibrosis. Stem Cells Dev. 2013, 22(6), 845–854. doi: 10.1089/scd.2012.0395.

43. Dorronsoro A., Robbins P. Regenerating the injured kidney with human umbilical cord mesenchymal stem cell-derived exosomes. Stem Cell Research Therapy. 2013, V. 4, P. 39.

44. Ekstr?m K., Omar O., Gran?li C., Wang X., Vazirisani F., Thomsen P. Monocyte exosomes stimulate the osteogenic gene expression of mesenchymal stem cells. PLoS ONE. 2013, 8(9), e75227. doi: 10.1371/journal.pone.0075227.

45. Gross J. C., Chaudhary V., Bartscherer K., Boutros M. Active Wnt proteins are secreted on exosomes. Nat. Cell Biol. 2012, 14(10), 1036–1045. doi: 10.1038/ncb2574.

46. Lee J. K., Park S. R., Jung B. K., Jeon Y. K., Lee Y. S., Kim M. K., Kim Y. G., Jang J. Y., Kim C. W. Exosomes derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells. PLoS One. 2013, 8(12), e84256. doi: 10.1371/journal.pone.0084256.

47. Van Balkom B. W., de Jong O. G., Smits M., Brummelman J., den Ouden K., de Bree P. M., van Eijndhoven M. A., Pegtel D. M., Stoorvogel W., W?rdinger T., Verhaar M. C. Endothelial cells require miR-214 to secrete exosomes that suppress senescence and induce angiogenesis in human and mouse endothelial cells. Blood. 2013, V. 121, P. 3997–4006. doi: 10.1182/blood-2013-02-478925.

48. McDonald M. K., Tian Y., Qureshi R. A., Gormley M., Ertel A., Gao R., Aradillas Lopez E., Alexander G. M., Sacan A., Fortina P., Ajit S. K. Functional significance of macrophage-derived exosomes in inflammation and pain. Pain. 2014, 155(8), 1381–1396. doi: 10.1016/j.pain.2014.04.029.

49. Bottero D., Gaillard M. E., Errea A., Moreno G., Zurita E., Pianciola L., Rumbo M., Hozbor D. Outer membrane vesicles derived from Bordetella parapertussis as an acellular vaccine against Bordetella parapertussis and Bordetella pertussis infection. Vaccine. 2013, 31(45), 5262–5268. doi: 10.1016/j.vaccine.2013.08.059.

50. Jiang Y. J., Bikle D. D. LncRNA: a new player in 1?, 25(OH)(2) vitamin D(3) /VDR protection against skin cancer formation. Exp. Dermatol. 2014, 23(3), 147–150. doi: 10.1111/exd.12341.

51. Cheng L., Sharples R. A., Scicluna B. J., Hill A. F. Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood. J. Extracell. Vesicles. 2014, V. 3, P. 23743. doi: 10.3402/jev.v3.23743.

52. Marimpietri D., Petretto A., Raffaghello L., Pezzolo A., Gagliani C., Tacchetti C., Mauri P., Melioli G., Pistoia V. Proteome profiling of neuroblastoma-derived exosomes reveal the expression of proteins potentially involved in tumor progression. PLoS ONE. 2013, 8(9), e75054. doi: 10.1371/journal.pone.0075054.

53. S?enz-Cuesta M., Osorio-Querejeta I., Otaegui D. Extracellular vesicles in multiple sclerosis: what are they telling us? Front Cell Neurosci. 2014, V. 8, P. 100. doi: 10.3389/fncel.2014.00100.

54. Khalyfa A., Gozal D. Exosomal miRNAs as potential biomarkers of cardiovascular risk in children. J. Transl. Med. 2014, 12(1), 162. doi: 10.1186/1479-5876-12-162.

55. Rodr?guez-Su?rez E., Gonzalez E., Hughes C., Conde-Vancells J., Rudella A., Royo F., Palomo L., Elortza F., Lu S. C., Mato J. M., Vissers J. P., Falc?n-P?rez J. M. Quantitative proteomic analysis of hepatocyte-secreted extracellular vesicles reveals candidate markers for liver toxicity. J. Proteomics. 2014, V. 103, P. 227–240. doi: 10.1016/j.jprot.2014.04.008.

56. Johnstone R. M. Revisiting the road to the discovery of exosomes. Blood Cells Mol. Dis. 2005, 34(3), 214–219
http://dx.doi.org/10.1016/j.bcmd.2005.03.002